Centromere, kinetochore, kinochore, kinetosome, kinosome

Centromere, kinetochore, kinochore, kinetosome,kinosome, kinetomere, kinomere, kinetocentre,kinocentre: history, etymology and intepretationEMILIO BATTAGLIA

Dipartimento di Scienze Botaniche, via L. Ghini 5, I - 56126 Pisa, fax ++39 050 551345

Dedicated to the memory of Prof. Charles Berger S. J. (1901-1966)

Abstract - From 1936 until today, the terminological couplet centromere and kinetochore, has been con-troversially discussed and defined. The author analyzes this couplet here, mainly from the historical and ety-mological points of view together with several synonyms or related terms such as kinocentre, kinomere,kinosome, etc.For the purpose of avoiding ambiguities and misinterpretations, many other terms, linguistically identicalto those mentioned above although differently definied, i. e. kinetocentre, kinetomere and kinetosome, havealso been commented upon. Further, to accomplish a largely comprehensive analysis of this terminologicalsystem, Tables 1-4 summarize a number of related cytological terms which are almost ignored by currentcyto-genetical literature. They, indeed, represent the key in order to ascertain the history and the first def-inition of most terms here analyzed.The author also emphasizes the linguistic difference between the prefixes kino- and kineto- in relation tothe compound terms which refer to chromosome movement and to mitosis, as they are currently describedfor the cells of higher eukaryotes.

Key words: Centromere, kinetocentre, kinocentre, kinetochore, kinochore, kinetomere, kinomere, kineto-some, kinaster, kinodomain, kinopole, kinotubule, kinosome, kinosomiole, kinocentrosoma, kinocentriole,kinocilium, akinocilium (stereocilium).

INTRODUCTION

During the past fifty years the amount of biochemical and ultrastructural research concerning chro-matin-chromosome organization has been increasing and an impressive number of different terms andexpressions have been introduced.

This terminology has been proposed by authors of different languages and in conditions of differ-ent cytological knowledge and different linguistic competence.

Very often terminological priority, right etymology and synonymy have been totally ignored.In many previous accounts (BATTAGLIA 1985-2000), I have repeatedly, pointed out the resulting

chaotic, and sometimes contradictory, state of affairs of the modern cytological terminology. In the pre-sent days, it is also very disappointing to find inaccuracy or incompleteness, even in technical lists specif-ically intended to define the main and (or) the most current cytogenetic terms.

Considering the above facts, the “Genome Glossary” published in the recent Human Genome issueof Science (vol. 291, 16 February 2001) and the “Genome speak” published in the correspondingGenome issue of Nature (vol. 409, 15 February 2001) prompted and encouraged the author toexpand the present paper which has been mainly confined to comments on the current chromosometerminological couplet centromere- kinetochore. This is a matter that the author originally discusseda long time ago (BATTAGLIA 1955) proposing the term kinochore as short for the usual kinetochore.From this point of view, it is worth mentioning that the choice of the prefix kino (comb. form kin-o)

CARYOLOGIA Vol. 56, no. 1: 1-21, 2003

belongs to the classic linguistic proposals and was introduced in Cytology by Eduard Strasburger asearly as 1892 (cf. STRASBURGER, 1892b, p. 60: Kinesiplasma, oder, was kürzer und zülassig, “Kino-plasma”).

Centromere and kinetochore where considered synonyms in all papers published from 1934 to 1981whilst later on these two terms have been jointly utilized for indicating distinct structural parts of the“spindle fiber attachment” of earlier cytologists.

RIEDER (1982) published a widely quoted review on the structure and terminology of the “chro-mosome primary constriction”. To eliminate the terminological ambiguity between centromere andkinetochore, he suggested, cf. RIEDER (1982, pp. 5-6) “that the term kinetochore be used as defined byRIS and WITT (1981) to note, at the ultrastructural level, the precise region on the chromosome thatbecomes attached to spindle MTs… and the centromere… in a less precise manner to note the regionon the chromosome (e. g., the primary constriction, pericentromeric heterochromatin, etc.), withwhich the kinetochore is associated”; (see also Chapter F.).

Today, this reinterpretation of the couplet centromere-kinetochore is widely quoted in biologicalbooks and dictionaries, see for instance

– JOHN (1990, p. 18):These structures, termed kinetochores,are only visible in ultra-thin electron microscopesections and are most commonly restricted to a localized site which appears in the lightmicroscope as a visible constriction in the condensed chromosome thread. This con-striction is known as the centromere. The terms kinetochore and centromere were initiallycoined as synonyms and are still used as such by some authors. There are, however, nowsound reasons for restricting the term kinetochore specifically to that region of thechromosome to which, at the ultrastructural level, spindle MTs become attached, whileretaining the term centromere for the region of the chromosome with which the kine-tochore is associated (RIEDER 1982).

– SINGER and BERG (1991, p. 691):Gross anatomy of centromeres - In mammals, centromeres have a complex trilaminar disk-like structure called a kinetochore. There is one kinetochore disk on each side, of thechromosome. During mitosis, the microtubules of the spindle fibers appear to attachdirectly to the dense outer layer of the kinetochore, where loops of chromatin fibers canbe seen.

– BRAY (1992, p. 226): “In most higher eukaryotes, the centromere is associated with a specialized structure, akinetochore…”

– LAWRENCE (1995. Henderson’s Dictionary of Biological Terms, p. 301):“Kinetochore, densely-staining fibrillar region within the centromere of a chromo-some.”

– DORLAND’s Illustrated Medical Dictionary (1994 and 2000):“Kinetochore, a proteinaceous structure beside the centromere and to which the spin-dle fibers are attached.”

Disregarding the terminology mentioned above, both the “Genome Glossary” (Science) and the“Genome speak” (Nature) ignore the term kinetochore and propose a rather questionable definitionof centromere, namely:

– “Genome Glossary” (Science, 2001 p. 1200):“Centromere. The difficult-to-sequence central region of a chromosome.”

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Aside from the rather personal choice of the adjective “difficult”, the centromere is not character-ized by a definite central location along the length of the chromosome. Since the prefix centre- conveysthe meaning “central place”, almost automatically here, the centromere became qualified as a “centralregion”.

– “Genome speak” (Nature, 2001 p. 815):“Centromere. Chromosomes contain a compact region known as a centromere, where sis-ter chromatids (the two exact copies of each chromosome that are formed after replication)are joined.”.

Here the adjective compact is rather questionably ascribed to a chromosome site traditionallycalled “the chromosome primary constriction”.

Further, the present analysis has necessarily been extended to the synonyms of the couplet “cen-tromere-kinetochore” recorded by cytological literature, namely kinosome, kinomere and kinocentre.The almost identical terms kinetosome, kinetomere and kinetocentre, already recorded by cytologicalliterature, have also been, necessarily, taken into critical analysis.

Lastly, many historical data and references have been quoted, or summarized, since they are wide-ly ignored and, at the same time, they also represent the key in order to establish the priority and thefirst definition of most terms commented upon here.

A. Centromer (1903) and centromere (1936)

Many terms belonging to classical cytology are linguistically referable to the nouns centre and cen-trum which were coined in the period 1876-1906, (cf. Tables 1-4).

Nearly all of them have been accepted and used widely by the scientific community.There are, however, two remarkable exceptions, i.e. Kinocentrum (ZIMMERMANN 1898), cinocen-

tro in BILANCIONI (1906) and centromere (WALDEYER 1903: “Centromer”). “Kinocentrum” hasbeen ignored by cytologists (see further Chapter H) whilst “Centromer” (1903) was first widely over-looked and later (1936) reproposed with a quite different meaning (DARLINGTON 1936a,b,c, “cen-tromere”).

As a matter of fact, WALDEYER was the first, in 1903 (1) to coin the triplet “Centromer, “Cytomer”and “Karyomer” to indicate different parts of the general morphology of the sperm.

This terminological triplet was disregarded by Waldeyer’s contemporary cytologists, probably forthe following reasons:– the term “Karyomer” already coined by FOL (1896, p. 242: “Karyomere”) Fol gave to this term a very

different meaning”– the heterogeneity of the triplet, since “Cytomer” and “Karyomer” both refer to cell morphology,

whilst “Centromer” is only a positional term.As regards classic text-books, the term “Centromer” was quoted only by WILSON (1925) and limit-

ed to the Glossary, as follows:

Centromere (kentron, center; meros, part), that part of the sperm containingthe central bodies; especially the neck-region. See Karyomere, Cytomere

(WALDEYER 1903).

There has been a revival-reinterpretation of the term centromere in a remarkable series of kary-ological papers published by DARLINGTON and collaborators in the years 1936-1939.

DARLINGTON (1936 a,b,c) wrote: “the centromeres are chromomeres belonging to the centric con-striction”; “their spindle attachment chromomeres, or centromeres as I propose to call them…”;“A small body, presumably the centromere, may sometimes be seen at metaphase of mitosis and sec-ond anaphase of meiosis at the centric or attachment constriction…”.

CENTROMERE: HISTORY, ETYMOLOGY AND INTERPRETATION 3

DARLINGTON’s centromere (1936), quickly became an alternative to the equivalent kinetochore, aterm already coined two years earlier and recommended by SHARP in his well-known text-book (1934)(cf. chapter F).

B. The classic and the present chromosome mono-…polycentric terminologies.

As regards chromosome movement and cell division, the terms monocentric and dicentric have beenwidely adopted by many classic authors of the 19th century, for instance:

FLEMMING (1878), p. 372: “eine dicentrische Anordnung”; p. 378: “eine dicentrische Gruppirung”;p. 422: “nach monocentrisch-radialem Typus… in dicentrisch, radialem Typus”; (1881), p. 17: “dermonocentrisch Strahlung”.

VAN BENEDEN (1883), p. 476: “aux poles de la figure dicentrique”; p. 553: “centres polaires”; p. 563:“deux centres dynamiques”.

PFITZNER (1883), p. 627: “die (monocentrische) Sternform”; p. 628: “Die achromatische Figur istin der Kranzform monocentrisch… In der Sternform ordnet sie sich dicentrisch…”; p. 660: “Diekinetischen Centra der Segmente, also die Mitte des Fadenabschnitts…”; p. 688: “Fig. 19. Monocen-trische Achromatinfigur”; “Fig. 20. Dicentrische Achromatinfigur”.

STRASBURGER (1884b), p. 11: “in Fig. 4 die dicentrische Umordnung des urspriinglich monocen-trischen…”; p. 59: “die dicentrische Anordnung des Segmentschleifen”.

CARNOY (1885), p. 229:”cellule monocentre”; “cellule dicentre”.

In modern times the expression “centric constriction” and the adjectives mono-, di-, polycentric(etc.) where chosen by DARLINGTON (1936 b, d, e, 1937) to qualify chromosomes having one, two ormore centromeres. This is a linguistically questionable choice because monocentromeric… polycen-tromeric are the only regular adjectives referable to the number of centromeres.

Today, as regards this matter, the author favours, see next chapter I, a re-interpretation of the termkinetocentre to define the chromosome passive kinetic centre and consequently the choice of the seriesmono… polykinetocentric in the place of the current mono-polycentric system.

C. The classic cytological kinetic centre; centrum (centro-, centri-) and related kino-, kineto- com-pound terms (Tables 1-4)

The present terminological use of the couplet centromere and kinetochore cannot be adequatelycommented upon without a short documentation of the old cyto-genetic terminology coined before theend of the 19th century by some outstanding classic authors such as Van Beneden, Flemming, Fol,Strasburger, Heidenhain, Boveri, Waldeyer etc.

From this point of view, the elaboration of Tables 1-4 is the logical and useful complement to thepresent account.

For the sake of simplification Tables 1-4 are here presented without any further comment. TheseTables are a collection of terms that should not be ignored in a wide terminological analysis of that solengthily debated couplet centromere and kinetochore, together with their synonyms and other relat-ed terms. Most of the terms quoted here are obsolete and cannot be found in current cytological lit-erature; the author also thinks that this collection of terms will be a useful guide to avoid their re-coin-ing by unaware or linguistically unskilled authors. Lastly, as regards the references therein cited, the pagefirst recording the term or its definition, with very few exceptions due to their minor interest, has beenquoted in order to allow an easy control by readers.

As regards the linguistic difference between kino- and kineto-, see chapter I.

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Table 1 – The classic centrum (-tren) compound terms

Centrum des Eies FLEMMING 1881, p. 17: “das Centrum, Centra”Polcentren FLEMMING 1881, p. 31Keimcentrum (-centren) FLEMMING 1884, p. 64, 68Centrenquadrille FOL 1891b, p. 266Ovocentrum FOL 1891b, p. 268; BÜRGER 1892, p. 230Spermocentrum FOL 1891b, p. 269; BÜRGER 1892, p. 230; FICK 1905Astrocentrum (-centren) FOL 1891b, p. 272-273; FOL 1896, p. 259Sphärencentrum BÜRGER 1892, p. 227Attraktioncentrum BÜRGER 1892, p. 229Mikrocentrum HEIDENHAIN 1893, p. 58; HEIDENHAIN 1894, p. 456, BOVERI 1895, p. 66Cinocentro = Kinocentrum cf. Tab. 2Chemocentrum ZIMMERMANN 1898, p. 697Cytocentrum VAN BENEDEN cf. BOVERI 1901, pp. 183, 205; MEVES 1902a, p. 155

Table 2 – The kinetic center.

kinetisches Centrum, Centra, cf. PFITZNER 1883, p. 644:Combinationscentra

Diese kinetischen Centra des Zellleibes ergeben mit dem Centrum des Kernszwei “Combinationscentra”, wie ich sie bezeichnen will, die Pole nämlich.

Die Pole sind die neuen kinetischen Centra der Gesammtzelle und setzen sichals solche aus zwei Componenten zusammen: aus dem (anfangs noch einheitlichen)des Kerns und je einem der (bereits doppelten) des Zellleibs.

STRASBURGER 1892b, p. 51: “will ich mit Fol hier kinetisches Centrum brauchen…”; FISCHER 1899, p. 237

kinetischen Centren FOL 1891b, p. 267; HUMPHREY 1894 p. 116; centres cinétiques:GUIGNARD 1898; FISCHER 1899, p. 237; KOERNICKE 1903, p. 84

Centrokinetische Theorie FOL 1891b, p. 266; 267Kinocentrum ZIMMERMANN 1898, p. 697cinocentro BILANCIONI 1906, p. 122Kinetozentrum GRUNDMANN 1964, p. 140, 152 (1966, p. 132: kinetocentre)

Table 3 - Central-, centri-, centro- classic compound terms

Corpuscule central VAN BENEDEN and NEYT 1887, pp. 264, 275Centralkörper FLEMMING 1881, p. 17; BÜTSCHLI 1889Centralkörperchen FLEMMING 1881, p. 17; HEIDENHAIN 1891, MOORE 1893: “central bodies” p. 185Centrosoma BOVERI 1888, p. 752; BOVERI 1901, p. 206: Centrosoma = Centralkörperchen,

Doppelcentrosom, Triplencentrosom; Fol 1896, p. 264

Centralplasma BÜTSCHLI 1889Centrenquadrille FOL 1891b, p. 266Centrokinetische Theorie FOL 1891b, p. 266Centralspindel HERMANN 1891, p. 580; BOVERI 1901, p. 182Centralspindelkörperchen KOSTANECKI 1892, p. 207: “Centralspindel-Körperchen”; KOSTANECKI 1893, p. 255:

“Centralspindelkörperchen”

Centrosphäre STRASBURGER 1892b, p. 58; 1893, p. 187Centrodesmose HEIDENHAIN 1894, p. 463Centriol(en) BOVERI 1895, p. 66Centriolum BOVERI 1901, p. 204: Centriolum diminutivbildung von “Centrum”; MEVES 1902 a,

p. 152Centroplast STRASBURGER 1897b, p. 388; GUIGNARD 1898, p. 204Centroplasma ERLANGER 1896a, b, BOVERI 1901, p. 204Centrodeutoplasma ERLANGER 1897a, p. 7Centrogranoplasma ERLANGER 1897c, p. 814Centralkapseln HEIDENHAIN 1900, p. 520Centralkorn BOVERI 1901, p. 204; p. 206,Centralkorn = CentriolCentronucleus BOVERI 1901, p. 183Centrotheca MEVES 1902b, p. 53Centromer WALDEYER 1903, p. 204; DARLINGTON 1936b, p. 249: “centromere”Centronema cf. SHARP 1934, p. 223Centroblepharoplast cf. SHARP 1934, p. 123Centrogene DARLINGTON 1939, p. 358


Table 4 - Kineto- and kino-terminologyKinetoterms Kinoterms

kinetoblast: cf. LAWRENCE 1995 kinoblast: cf. EICHHORN 1999kinetozentrum: GRUNDMANN 1964, pp. 140, 152 kinocentrum: ZIMMERMANN K.W. 1898, p. 697kinetocentre: GRUNDMANN 1966, p. 132 cinocentro: BILANCIONI 1906, p. 122kinetochore: J.A. MOORE in SHARP 1934, p. 116 kinochore: BATTAGLIA 1955, p. 179———————— kinochromatine: VAN CAMP 1924, p. 27———————— kinocilium: cf. STÖHR 1906: kinocilien and stereo cilien;

CAJAL 1926: kinocilios and estereo cilioskinetochromidien: SCHAXEL 1911, p. 588 ————————kinetocyst: cf. COLE 1998 ————————kinetodesma: cf. SINGLETON and SAINSBURY 1987 ————————kinetogene: cf. RIEGER and MICHAELIS 1958 ————————kinetogenesis: COPE 1884, 1887 ————————kinetomere (ana-,katakinetomere): MATHEWS 1924,pp. 26, 28 kinomere: SHARP 1943, p. 85; cited by HUSKINS 1944, p. 82

Kinetonema: MATSUURA 1941, p. 375 ————————kinetonucleus: WOODCOCK 1906, p. 182 ————————kinetoplasm: cf. HENDERSON and HENDERSON DICT. 1953 kinoplasma: STBASBUSGER 1892b, p. 60kinetoplasmid: cf. SIMPSON et al. 1989 (KtRNA),THOMAS et al. 2000 (KMP-11); ————————Kinetoplastida (Order) ———————————————— Kinorhyncha (Class)kinetoplastid: (KMP-11): cf.TOLSON et al. 1994; TRÜJILLO

et al. 1999; MCMANUS et al. 2001; RAMIREZ et al. 2002———————— kinoplasmasphäre: STRASBURGER 1897b, p. 381———————— kinoplasmasome: BAILEY 1919, p. 285kinetoplaste: ALEXEIEFF 1917, p. 512 kinoplastic: cf. ACADEMIC PRESS DICT. 1992kinetoplast: cf. LWOFF 1950; STEINERT 1960; kinoplast: cf. SCHELLMAN and HARVEY 1995K-DNA= kinetoplast DNA: cf. SIMPSON 1972, pp. 143-144k-DNA= kinetoplast DNA: cf. STUART and FEAGIN 1992dys-kinetoplastic: cf. TRAGER and RUDZINSKA 1964diskinetoplastie: cf. RIOU 1967pankinetoplastic: cf. VICKERMANN 1977akinetoplastic: cf. SIMPSON 1972, 1986———————— kinosphäre: BOVERI 1901, pp. 123, 157kinetospore:cf. LAWRENCE 1995 kinospore: KLEBS 1900, p. 87kinetosome: ALLEN 1912, p. 134 kinosome: HUSKINS cited by HUSKINS 1944, p. 82; see also

SHARP 1943, p. 85 and SCHRADER 1944, pp. 20-21cinétide, cinétie, cinétome, cinétodesme, cinétosome:CHATTON 1924; CHATTON and LWOFF 1935a, 1935b;(kinety, kinetodesma, kinetoplast, kinetosome inLWOFF 1949, 1950) ————————kinetium, kinetia, kinetodesmata: cf. LAWRENCE 1995

D. Kinoplasma (Strasburger 1892b), kinoplasmic bodies (Allen 1912) and kinoplasmasome (Bailey1919)

The term kinoplasma was introduced in Cytology by STRASBURGER (1892b)A few years later, Strasburger himself coined more similar terms such as kinoplasmafäden (-hulle,-

massen,-strahlungen) see STRASBURGER (1897a), kinoplasmasphäre (-mantel, -strahlen) see STRAS-BURGER (1897b), thus giving rise to a kinoterminology largely quoted and also expanded by the cytol-ogists of those years, cf. kinospore of KLEBS (1900), kinosphäre of BOVERI (1901) etc. (cf. Tab. 4).

An English interpretation “kinoplasmic bodies” can be found in a well-known paper by ALLEN

(1912). This author, describing the cell division of the antheridia of Polytrichum, speaks of a substancethat seems “to fall within Strasburger (1892) category of kinoplasma, aggregated into bodies of vari-ous forms, called kinoplasmic bodies”. Unexpectedly, Allen proposed to define these bodies as kine-tosomes, clearly avoiding the linguistically correct definition kinoplasmasomes (for details, and com-ments see Chapter E).

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However, the term kinoplasmasome was proposed just a few years later by BAILEY (1919). Thisauthor, investigating the spindle development and the formation of the cell-plate in the cambium ofPinus strobus, observed aggregations of kinoplasmic bodies that “may be called kinoplasmasomes”(2).

In further papers BAILEY (1920) distinguished a “kinoplasmasome stage” and defined the kino-plasmasomes as “rod-shaped masses of kinoplasma”.

As regards modern scientific literature the term kinoplasmasome is widely ignored and an entry“kinoplasmasomes, n.plu., phragmoplast fibres…” is recorded only by LAWRENCE (1995) Henderson’sDictionary of Biological Terms.

E. Kinetosome (Allen 1912, Simpson 1972), kinetosoma (Alexeieff 1917), kinosome (Huskins 1944,Sharp 1943), kinetonucleus (Woodcock 1906), kinétoplaste (Alexeieff 1917), kinetoplast andkinetic bodies (granules)

The expression kinetic bodies and the corresponding compound term kinetosome, together with theequivalent term kinosome have an identical meaning, that is of body (wide sense) characterized by apassive or active movement. Nevertheless, the meaning ascribed by scientific literature to these termsis controversial.

Kinetosome was coined by ALLEN (1912), as already mentioned in, Chapter D, Allen called those“bodies of various forms”, first as kinoplasmic bodies (ALLEN, op. cit. p.132) and secondly kinetosomes(ALLEN, op. cit., p.134):

There may even be an apparently continuous plate at one spindle pole, and at the othera group of smaller bodies (PL VII, Figs. 32,34,58; PI. VIII, Fig. 59); and all possibletransitions may be found from the condition of a compact plate to that of many distinctbodies It seems plain from.the appearances described that the plates and the groups ofsmaller bodies – which will be referred to as kinetosomes – are mutually equivalent,being merely different forms assumed by the same substance.

Since the expresssion kinoplasmic body corresponds to a the compound term kinoplasmasome(cf. Chapter D) there is the problem of inferring a reasonable explanation for Allen’s choice of such adeviating term as kinetosome (kinetic body) in place of the linguistically obvious kinoplasmasome (kino-plasmic body).

I believe that Allen, certainly aware of the terms kinetonucleus (WOODCOCK 1906) (3) and Kine-tochromidien (SCHAXEL 1911) (4) already present in cytological literature, coined kinetosome for thesake of terminological uniformity, in spite of its linguistic inaccuracy.

In this context, it is worth mentioning that a few years later ALEXEIEFF (1917) entirely unaware ofAllen’s kinetosome, coined “kinetoplaste (ou kinetosoma)” (5).

This terminology, enriched by the inclusion of kinoplasmasome (coined by BAILEY 1919, cf. Chap-ter D) was only partially recorded and variably evaluated by the main cytological text-books publishedfrom 1924 to 1944. In all cases the synonymy ‘kinetoplaste ou kinetosoma” of ALEXEIEFF (1917)escaped the attention of cytologists. I confine myself to a few instances, namely:

WILSON (1925) records only two entries: “kinetonucleus (WOODCOCK 1906)” and “kinetosome(ALLEN 1912)”;

SHARP (1934: Introduction to Cytology) records, only “kinetonucleus” and “kinetosome”, and at thesame time, recommends the new term “kinetochore” (cf. next Chapter F).

Equally worthy of mention are the terms kinomere and kinosome recorded by a further text-bookof SHARP (1943: Fundamentals of Cytology, 1st ed.), by an almost contemporary text-book of SCHRAD-ER (1944: Mitosis, 1st. ed.) and by HUSKINS (1944).

SHARP (1943), besides kinetochore, quotes kinomere and kinosome (6). SCHRADER (1944), besideskinetochore (and synonyms), also quotes “the spindle spherule or kinosome” (7), whilst HUSKINS (1944,p. 82) ascribes kinosome to himself and kinomere to SHARP (1943) (8).

The priority of kinomere will be discussed in Chapter G. Further, as regards a hypothetical pater-nity of Schrader concerning kinosome, I have ascertained the following data.


Schrader in his paper on Amphiuma (SCHRADER 1936, p. 489) wrote only: “that it is the commissuralcup and the spindle spherules that constitute the kinetochore “and once more the same expression canbe found in a review on the structure of the kinetochore (cf. SCHRADER 1939c, p. 231): “the tiny gran-ule which I have called spindle spherule because of its obvious relation to the half spindle fibers”.

As the term kinosome is not mentioned in any of the later papers published by Schrader in the years1940 and 1941 (cited by SCHRADER 1944) (7) (9) the term kinosome in the present paper will be record-ed as “kinosome, cf. HUSKINS 1944”.

As regards the quotation and definition of the term kinosome in modern scientific literature I havefound the following data:– kinosome is not cited in the scientific papers and reviews concerning the couplet “centromere and

kinetochore”;– an entry kinosome cannot be found in almost any of the biological dictionaries. There are only a few

exceptions, for instance KNIGHT (1948) quotes both kinosome and kinomere, whilst RIEGER andMICHAELIS (1958) only mention a “Kinosom (SCHRADER 1939)”. However this entry has beenremoved from the following editions of this Glossary, cf. RIEGER, MICHAELIS, GREEN (1968, 1991).As regards the modern quotation and definition of the term kinetosome, a well-known and appreci-

ated review on “The Kinetoplast of the Hemoflagellates” by SIMPSON (1972) deserves large quotation (10).Here kinetoplast and kinetosome are defined as follows:“K-DNA = Kinetoplast DNA . The mass of mitochondrial DNA that stains with Giemsa…” (11);“Kinetoplast. That portion of the mitochondrion of Kinetoplastidae containing the fibrous mass of

mitochondrial DNA”;“Kinetosome . The basal body of flagellum”.Clearly Simpson ignored or at least did not pay due attention to Allen’s priority as regards kinetosome.As regards the most recent biological literature, the term kinetosome is currently cited as the

“basal body”. I have found a double definition of kinetosome, only in LAWRENCE’s Dictionary (1995).Lastly, there is the question of the so-called kinetic bodies or kinetic granules.Although of minor interest, the expression “kinetic bodies”, which was very common in many old

cytological papers, deserves a short comment.First, the kinetosome of ALLEN (1912) is the compound term which linguistically corresponds to the

expression “kinetic body”.Second, overlooking both priority and linguistic relationship, several cytologists described the

occurrence of kinetic bodies at the spindle attachment region (12); for references see SHARP (1934pp. 116-117). DARLINGTON himself in 1934 described “attachment chromomeres” and “kinetic bod-ies” (13). An identical sentence, namely, “kinetic granules” was later chosen by other authors. As regardsthis matter, it is worth recalling that in the years 1949-1959, several authors, mainly plant cytologists,discussed the question to explain the differences in organization of the kinetochore at mitosis and meio-sis, in order to account for the so-called chromosome co-orientation and auto-orientation described byDARLINGTON and MATHER (1949, p. 407).

A paper by ÖSTERGREN (1951, p. 150), for instance, quotes:“During ordinary mitosis the kinetic granules (spindle spherules or what we may chose to call them)

are arranged on two opposite sides of the chromosome, but during the first meiotic division the wholekinetochore is arranged on one side of the chromosome body”.

The following deliberations, from LIMA-DE-FARIA (1958, p. 148) also document the terminologicaluncertainty as regards this matter, in those years:

.........Other workers such as Östergren (1951), who followed the mechanical interpre-tation of Darlington, tried to find differences between the mitotic and meiotic kineto-chore in order to account for co-orientation at first metaphase as opposed to the sup-posed auto-orientation at mitotic metaphase............................................At that time there was no criterion which accurately permitted delimitation of thekinetochore at first metaphase of meiosis. Thus, a confusion resulted between arms andkinetochore. The description of the kinetochore under several names “kinetic gran-ules,” “spindle spherules,” “kinetochore region,” and “kinetochore” was a way of avoid-ing this essential difficulty.

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The “kinetic terminology” quoted above, is recorded here, because it is widely disregarded or notdiscussed by most modern papers on chromosome structure and motion in both mitosis and meiosis.

F. Kinetochore (1934) or kinochore (1955) alternative to centromere and their terminological coex-istence

SHARP (1934) commenting on the chromosome region as the “variously called fiber-attachmentpoint, …primary constriction, kinetic constriction:”, inserted the following footnote (cf. SHARP 1934,p. 116): “The convenient term kinetochore (movement place) has been suggested to the author byJ.A. Moore. The use of this term is recommended”.

This is the beginning of a long terminological controversy which deserves a detailed comment.First, the right quotation of kinetochore “J. A. MOORE in SHARP (1934)” is usually overlooked with

very few exceptions (cf. e.g. WAGENITZ’s Wörterbuch 1996).Secondly, many years ago, I suggested “kinochore” in place of “kinetochore”, cf. BATTAGLIA (1955,

p. 179):

The relative merits of the terms centromere and kinetochore were discussed many yearsago by SCHRADER (1939a, 1939b) and MATHER (1939). From a strict etymologicalpoint of view the term kinochore should be equally correct and simpler than kinetochore.

Regrettably, kinochore escaped the attention of cytologists.Thirdly, just two years after the publication of Sharp’s text-book, DARLINGTON (1936 b, c, d, e) rede-

fined the centromere (cf. Chapter A) and this term almost immediately became an alternative or a sub-stitutive term in place of kinetochore.

As already cited in Chapter B, after the publication of DARLINGTON’s (1937) greatly appreciated“Recent Advances in Cytology”, the adjectives mono - polycentric became usual terms for almost allcytologists. However, the choice between centromere and kinetochore was hardly discussed in the year1939, cf. SCHRADER (1939 a, b) and MATHER (1939). Here, I wish to quote the following sentence fromMATHER (1939, p. 280):

FEW questions in cytological terminology can have caused more disagreement anddisorder than that of the name to be applied to the portion of the chromosome whichdetermines its movements on the spindle. The names given to this body have beenmany, and Dr. Schrader’s appeal for the general adoption of one term, with the aban-donment of all others, must be received sympathetically by cytologists and geneticists.

Most of the American and Japanese cytologists gave their preference to kinetochore and in this con-text it is worth recalling that MATSUURA (1941), describing a “kinetochore cycle” (Trillium, pollen grainmitosis) coined the term’’kinetonema” (14).

Also in those years, the kinetochore terminology was increased once more by the proposal of the terms“kinosome” and “kinomere” which receive detailed comment in Chapters E and G respectively.

In this context, and before taking into adequate consideration the modern use (or misuse), of thecouplet “centromere-kinetochore”, it seems to the author useful to anticipate some preliminary com-ments.

First, as a matter of fact, considerable confusion has been introduced into the literature of this con-troversy, by the rather different senses in which the word centromere has been used. To avoid this chaos,I believe that the term centromere should be exclusively utilized .to indicate a “central part”.

Secondly, as regards kinetochore, there is a very frequent abuse of the word region which corre-sponds to the suffix chore. In other words since “chore = region” the usual sentence “kinetochoreregion “is a very evident pleonasm (the same criticism is valid for the equally usual sentence “chro-mosome body”).

Furthermore, since “region” includes the meaning “wide space”, only sub-regions or districts or sitesshould be reasonably distinguished within a region; however this logical evaluation is widely overlooked.


Equally, since “mere” means “part”, the centromere should be evaluated or described or definedas a “part” of the kinetochore and not the contrary as often stated by some authors (see below).

Lastly, even the expression “centromere region” can be found!As regards the usage of the couplet “centromere-kinetochore” in recent times, and although the well-

known text-book of WHITE (1954) adopted centromere, both terms were usually considered synonymsin most papers published from 1950-1981.

Around the years 1965-1980, the kinetochore-centromere terminology became strongly influencedby the progress in electron microscopy and biochemical methodologies. Thus, e. g. the mammalianmetaphase chromosomes revealed a new structure ascribed to the “kinetochore region”, described asa trilaminar disk (cf. KRISHAN and BUCK 1965; JOKELAINEN 1967; etc. see review in RIS and WITT, 1981).

Once more, since some authors began to use the term kinetochore limiting it to the trilaminar diskwhile others used it for the outer dense layer, the use of this term again led to confusion (cf. ERICKSON

1979).The following year RIEDER (1982) published a widely quoted review on this matter and proposed

the terminological coexistence “kinetochore-centromere”, justified as follows (RIEDER 1982, pp. 5-6):

To eliminate this confusion, I suggest that the term kinetochore be used as defined by Risand Witt (1981) to note, at the ultrastructural level, the precise region on the chromo-some that becomes attached to spindle MTs. In mammalian cells this region differenti-ates into a trilaminar disk structure during mitosis and appears to contain unique com-ponents (see Section IV) not found in the adjacent heterochromatin or on the remain-der of the chromosome. However, unlike RIS and WITT (1981) I suggest that the termcentromere be used, as it is now often used by cytologists and geneticists, in a less pre-cise manner to note the region on the chromosome (e.g., the primay constriction, peri-centromeric heterochromatin, etc,) with which the kinetochore is associated.

The linguistic weakness of such a statement does not deserve further analysis.

The interpretative coexistence kinetochore-centromere, because it is cytologically based, was wide-ly accepted by the scientific community, although, sometimes, variably recorded; for instance GODWARD

(1985) writes: “The terms kinetochore and centromere will be discussed but kinetochore is used for thestructure seen with the electron microscope, centromere in a theoretical sense”.

No further terminological discussion is possible without considering the increased knowledge in thismatter, due to most modern methodologies. Many important data have been obtained as regards thechromosome kinetics (in both mitosis and meiosis), in animals and plants belonging to different sys-tematic orders. There are many hundreds of papers worthy of quotation and their cytological analysisis beyond the purpose of this account and the writer’s competence.

In any case, to have a basis for reaching terminological conclusions, I will confine myself to a shortcomment on a recent book by CHOO (1997), which clearly documents the current terminology in thisfield.

Choo’s book does not mention terms such as kinosome, kinomere, kinetonema, or the historical ref-erence “Centromer” of Waldeyer.

As regards the terminology adopted, it is enough to quote the explanation of the Fig. 4.1 of the book(CHOO 1997, p. 78):

Fig. 4.1 Structural domains of the human centromere-kinetochore complex. Theseinclude a centromere-pairing domain (as distinct from the sister chromatid arm-pairingdomains), a central domain consisting of densely packed heterochromatin, and a disc-shaped kinetochore domain. The kinetochore domain is made up of an outermostfibrous corona and a trilaminar structure composed of an electron-dense inner and out-er plate and an electron-lucent middle zone.

Here, we also find a non-coordinated use of the term domain which means “territory of control”or “field of action”. The use of “central domain” means that the other domains are “not central”.

10 BATTAGLIA

Finally, as several significant biochemical data have been achieved from 1996 onwards, I will limitmyself to quoting the very comprehensive review published by SULLIVAN, BLOWER and KARPEN (2001),because it documents, once more the present terminological disorder on this matter.

Here, the centromere is unevenly defined:– “the centromere is the site of spindle attachment”;– “… the centromere is the site of kinetochore formation, the proteinaceous structure …that is

responsible for their attachment to and movement along microtubules…”;– “The centromere is the genetic locus required for chromosome segregation…”.

In addition, these authors did not pay due attention to the etymological difference between “mere”and “chore” and consequently they write “ centromere-region”, op. cit. p.584-585: “In this review,weuse the term centromere to refer specifically to the chromatin (DNA and proteins) that is responsiblefor kinetochore formation, and the term “centromere region” in reference to the domains and functionspresent in the vicinity of a centromere (centric heterochromatin plus centromere,)”. In any case, foradditional data on the centromere-kinetochore problem, see e.g. PLUTA et al.(1995); DAWE (1998);SKIBBENS and HIETER (1998, review of the so-called chromosome, segregation machinery), MEGEE andKOSHLAND (1999); YAO et al. (2000); MARTINEZ-PEREZ, SHAW and MOORE (2001); MITCHISON andSALMON (2001); STACK and ANDERSON (2001); WITTMAN et al. (2001); BERNARD, MAURE and JAVERZAT

(2001); BERNARD et al. (2001); SULLIVAN., LEHANE and UHLMAM. (2001); SULLIVAN (2001); SHELBY,MONIER and SULLIVAN (2001); TADDEI et al. (2001); HENIKOFF, AHMAD and MALIK (2001); GARCIA-ORAD, VARGAS and VIG (2001); NONAKA et al. (2002).

G. Kinetomere (1924) and kinomere (1943)

Kinetomere, anakinetomere and katakinetomere, where coined by MATHEWS (in COWDRY 1924) anddefined as follows (cf. MATHEWS 1924 p. 26): “I propose that these two or more forms of molecules oratoms which differ in their energy content be called kinetomeres. The reactive, energy-rich ones willbe the anakinetomeres; the stable,unreactive, the katakinetomeres”. Indeed, these terms being ascribedto the molecules are so inadequate from the point of view of both etymology and physics, that todayany further comment is superfluous.

As regards biological dictionaries, I have found only a few times the entry “kinetomere”. Forinstance the HENDERSON and HENDERSON dictionary (1953, p. 237), rightly (priority) quotes “Kine-tomeres… molecules or atoms, reactive or stable, ana- and kata-kinetomeres”. By contrast, the Glos-sary of Genetics of RIEGER, MICHAELIS and GREEN (1968, p. 65) records: “The chromomeres localizedwithin the centromere region are called -centromeric chromomeres (ÖSTERGREN 1947) or kinetomeres(LIMA-DE-FARIA 1949)”.

The term kinetomere cannot be found in the Lima-de-Faria account, quoted above (i.e. LIMA-DE-FARIA 1949: 35: 77-85 and 422-444), or in other papers by this geneticist. Prof. Lima-de-Faria himselfnever adopted such a term (personal communication to the author).

As regards kinomere this term -is quoted by SHARP’s text-book (1943, p. 85) as follows:

An important feature of the chromosome is the specialised region at which its reactionswith the spindle mechanism seem to be largely centered. This region is called the kine-tochore. (Other terms in the literature are centromere, primary constriction and kinomere).

Kinomere is ascribed to Huskins by the well-known General Cytology of DE ROBERTIS, NOWINSKI

and SAEZ (1954, p. 218): “This clear region constitutes the centromere (Darlington), or kinetochore(Schrader), or kinomere (Huskins)…”.

In any case this question, at least apparently, is clarified by HUSKINS (1944, p. 82).As already quoted, cf. Chapter E, Huskins (8) ascribes to himself the paternity of kinosome and to

SHARP (1943) the priority of kinomere.Consequently, in the present paper the term kinomere will be quoted “kinomere, cf. SHARP (1943,

p. 85) and HUSKINS (1944, p. 82)”.


H. kinocentrum (Zimmermann 1898), cinocentro (Bilancioni 1906) and kinetozentrum (Grund-mann 1964; 1966: kinetocentre).

K.W. ZIMMERMANN (1898, p. 697) distinguished a motor of the cell, or Kinocentrum, as opposedto the nucleus or Chemocentrum:

Ich glaube aus alledem den Schluss ziehen zu dürfen, dass, ganz allgemein gesprochen,das Mikro-centrum das motorische Centrum, also das, “Kinocentrum” der Zelle sei(gegenüber dem Kern als „Chemocentrum”).Ob die an der Basis der Cilien der ächten Flimmerzellen dicht unter der Zelloberflächegelegenen längliehen Knötchen 1) mit dem das typische Kinocentrum darstellendenDiplosoma verwandt sind, woran beim Vergleich mit der “Centralgeissel” zu denken, sonahe liegt, oder nicht, liesse sich vielleicht durch entwicklungsgeschichtliche Unter-suchungen feststellen.

BILANCIONI (1906, pp. 122 and 926) translated kinocentrum into cinocentro (op. cit., p. 122), butascribed the term to A. ZIMMERMANN (op. cit., p. 926):

Cinocentro nome dato da ZIMMERMANN alla porzione centrale della sfera attrattiva,ordinar. occupata da uno o più centrosomi, considerati come centri dinamici, come pun-ti fissi su cui agiscono le forze meccaniche che producono la divisione cellulare.

As regards scientific literature, the term kinocentre is almost ignored and I have found an entry“kinocentrum: centrosome” only in DORLAND’s Medical Dictionary (2000).

The term “das Kinetozentrum” (pl. Kinetozentren) was coined by GRUNDMANN (1964, pp. 140, 152)The following sentence from GRUNDMANN (1964, p. 140) deserves quotation:

2. Die-KinetozentrenDieser Transport verläuft im groben in zwei Etappen: Zuerst gelangen die Chro-

mosomen nach Entwirrung des Prophaseknäuels in die Äquatorialebene der Metaphase,und dann wandern die Längshälften zu zwei einander im Regelfall genau -gegenüber-liegenden Polen. Diese Pole sind die Zentren der Chromosomen-bewegung, weswcgenwir sie Kinetozentren nennen. Sic bestimmen auch die Richtung der metaphasischenÄquatorialebene, die ja definitionsgemäß genau in der Mitte und senkrecht zur (gedacht-en) Verbindungslinie zwischen den beiden Polen liegt, also von der Position der Kine-tozentren abhängig ist. Umgekehrt definieren wir die Kinetozentren als diejenigenZellbestandteile, welche Richtung und Ausmaß der Chromosomenbewegung bestimmen.Sic sind in der typischen mitotischen Karyo-kinese zweimal vorhanden, also mit den“Mitosezentren” von MAZIA (1961 a) begrifflich identisch.

Kinetozentrum is translated as kinetocentre in GRUNDMANN (1966, p. 132) (15).The linguistic difference between kinetocentre and kinocentre will be discussed in chapter I.

I. The prefixes kino- (comb. form kin-o) and kineto- (comb. form kinet-o): a linguistic comment.

As a basic evaluation, not invalidated by the occurrence of a few exceptions, the linguistic differencebetween the combining forms kin-o and kinet-o and their corresponding couplet of prefixes kino- andkineto-, can be summarized as follows:kino- versus kineto- = transitive versus intransitive = active (causing) versus passive = motile versus mov-able.It is not superfluous to recall that kino- is a combining form which derives from the Greek, kãnàv,to set in motion (namely the stem kin- and the connecting vowel-o). Also kineto- is a combining formof the Greek kinhtêw, movable (kinet- and-o), cf. for instance the Greek-English Lexicon by LIDDELL

and SCOTT (1940).

12 BATTAGLIA

The linguistic difference mentioned above, has never been emphasized or clearly pointed out by sci-entific literature with the result that, today, the meaning ascribed to the two members of the kino- andkineto- couplet appears to be rather a matter of individual preference than a choice due to a proper lin-guisitic evaluation. I will limit myself to commenting briefly on the couplet kino- and kineto-plasm, asrecorded by some of the best known scientific dictionaries.

The HENDERSON and HENDERSON Dictionary (1953), does not record the combining forms kin-oand kinet-o and quotes the entries:

kinoplasm (kin’oplazm) n. [Gk. kinetoplasm (kinetoplazm) n. [Gkkinein; to move; plasma, mould.] kinein, to move; plasma, some-The substance of attraction-sphere, thing formed,], An iron-containingastral rays, and spindle-fibres; nucleo-protein forming a source ofarchiplasm; ergastoplasm. energy to Nissl granules.

The WEBSTER’s Dictionary (1986), by contrast, records the following combining forms:

cino- — see KIN- kine- — see KIN-

kin- or kine- or kino- or cin- or cino- comb form [Gk

kinema motion-more at CINEMATOGRAPH]:motion action <kinesthesia> <kinoplasm> <kineplasty>

kinet- or kineto- also cinet- or cineto-: comb form [Gkkinetos moving – more at KINETIC]: movement: motion<kinetogenic>

however only the term kinoplasm is cited namely:

kin·o·plasm \-plazem \ also- kin·o·plas·ma \-plazma n[ISV kin- + -plasm, -plasma; orig.- formed as G kinoplasma]:an active protoplasmic component held to form filaments andmobile-structures (as cilia, or spindle fibers) – opposed totrophoplasm

The Academic Press Dictionary (1992) records the following combining forms:

kine- or kin- a combining form meaning “movement,” as in kinematics, kinanesthesia,

kinet- a combining form meaning “movement,” as in kinetism.

kineto- a combining form meaning “movement,” as in kinetoplasm.

thus overlooking kino-.This is a rather unexpected choice because both members of the couplet kino-and kineto-plasm are

recorded, namely:

kinetoplasm Cell Biology, the highly contractile portion of a cell’s cytoplasm; generallyrefers to the chromatophilic substances of nerve tissue.

kinoplasm Cell Biology, a cellular component that is active in the formation of filamen-tous structures such as cilia and spindle fibers.

DORLAND’s Medical Dictionary (2000) records the following combining forms:

kinet(o)- [Gr. kinetos movable] a combining form denoting relationship to motion.

kin(o)- [Gr. kinein to move] see kine-.

kine- [Gr. kinein to move] a combining form denoting relationship to movement.See also words beginning cine-.


but, simplifying, quotes:

cino·plasm (sin’o-plaz- m) kinetoplasm.ki·ne·to·plasm (ki-ne’to-plaz” m) [kineto- + -plasm] the most highly contractile por-tion of the cytoplasm of a cell.

There is no doubt that the documentation mentioned above, shows the occurrence of a clear ter-minological disorder. I believe that this disorder may be greatly reduced by a general acceptance of thelinguistic difference which diversifies the two members of the kino- and kineto- couplet.

Let me mention a few examples .A spore motile by cilia should be qualified as a kinospore (KLEBS 1900) and not kinetospore. By con-

trast, the chromosome passive kinetic region should be called kinetochore (MOORE in SHARP 1934) andnot kinochore (BATTAGLIA 1955).

CONCLUSIONS

As a matter of discussion in a future panel on the terminological questions analyzed here from amainly linguistic point of view, the author wishes to put forward the following considerations.

It is useful to acknowledge the linguistic difference ascribable to the prefixes kino- and kineto-in coining compound terms referable to chromosome movement and cell division of higher eukary-otes. Consequently, the prefix kineto- should be chosen to indicate the occurrence of passive move-ment, ascertained or presumable. Necessarily, the prefix kino- should be utilized for all remainingcases, which are mainly cases of active movement or induction of movement.

Following this point of view, the author considers the term kinetochore as the right choice to indi-cate the classic chromosome primary constriction.

By contrast, he refuses the present use of the term centromere and proposes kinetocentre as analternative terminological solution. The acknowledgement of this last term makes it possible tosave the usual series” mono… polycentric chromosomes” by the simple change to “mono… polykine-tocentric chromosomes”. Still in this context, the old “attachment chromomeres” (DARLINGTON

1934) (13), or the “centromeric chromomeres”of ÖSTERGREN (1947) could be re-qualified as chro-mosome “kinetomeres”.

Further, in accordance with these considerations all instances referable to the occurrence of activemovement should be re-qualified by the choice of the prefix kino-. Thus, the current microtubulesshould be termed kinotubules, the aster as kinaster, the mitotic poles as kinopoles, and so on.

It is also not superfluous to recall that the already coined kinodomain (see, e.g. EARNSHAW and RAT-TNER 1989; EARNSHAW 1991; RATTNER 1991) should be qualified considering its own linguistic basis.

Furthermore I cannot fail to evaluate the lack of motion referable to the status non-motile versusmotile. In this case, I favour the choice of the classic a- (alpha privative), that is the choice of the pre-fix akino-.

Thus, for instance, the classical couplet kinocilium and stereocilium (cf. Tab. 4) could be re-qual-ified kinocilium and akinocilium.

A comprehensive discussion of the kino- and kineto- terminology cannot in any case overlook thepossible re-qualification or re-definition of two other terms proposed as synonyms of centromere,namely kinomere and kinosome.

Kinomere should be retained to indicate a “motile part”.As regards the re-use of kinosome, I would like to advance an analysis which at a first glance could

also be considered as provocative; namely the re-use of kinosoma(e) in place of centrosoma(e), cf.“Centrosoma” of Boveri, “Centralkörper” of classic German authors.

In the case of centrosoma, the prefix centro- has been chosen to indicate a body (soma) which insteadis not centrally located. Moreover, since it is a body that functions as the major microtubule – organiz-ing site (see reviews in MACK, JONGHUN and RATTNER, 2000; SHARP, ROGERS and SCHOLEY 2000, and bio-chemical data in STEVENSON et al. 2001; THEURKAUF 2001; LEE et al. 2001), the term kinosoma(e) seems

ee

14 BATTAGLIA

to me to be far more pertinent than the current centrosome(a), for defining this dynamic cellularorganelle. Thus, I also believe that kinosoma(e) (in the place of centrosoma) could be accepted as a reg-ular member of the homogenous family “kinopole, kinosphere, kinaster, kinotubule etc.”.

The renaming of centrosoma(e), almost automatically opens the problem of renaming Boveri’s oth-er term, centriole, cf.”Centriol(en)”: BOVERI 1895, p. 66; “Centriolum”: BOVERI 1901, p. 204; “Cen-triolum diminutivbildung von Centrum”: MEVES 1902a, p. 152.

As regards this question I am unable to find anything better than “kinosomiole”, that is the stemkinosom- + i (connecting vowel) + ole (from the Latin -olus, -ola, -olum, dim. suffix: “little one”).Kinosomiole has the merit of preserving a large analogy with the present centriole.

Last but not least, as I realize that the choice “kinosoma(e) in the place of centrosoma” may arouseperplexity, I would also like to propose a traditional respectful alternative, as follows:

Given that:– kinetocentre = movement-passive centre.– kinocentre = movement-active centre.the present centrosoma should be re-qualified as kinocentrosoma (kinocentr- o - soma) and almostautomatically centriole should become kinocentriole.

In conclusion, the author, believes that the present collection of terms and relative data togeth-er with the other critical analyses may well represent the basis for achieving a general agreement onthe so lengthily debated couplet “centromere and kinetochore” and related terminological problems.

(1) WALDEYER (1903) in HERTWIG (1906, p. 204):Man kann versucht sein, an jedem Spermium ein Karyomer, Centromer und Cytomer zu unterscheiden, wobei ich unter

Cytomer den protoplasmatischen Anteil verstanden wissen möchte. Der Kopf würde dann im wesentlichen dem Karyomer,der Hals als wesentliches Centrosomenstück, dem Centromer, der Rest dem Cytomer entsprechen.

(2) Cf. BAILEY (1919, p. 285):The formation of a cell-plate starting from one of these obliquely placed spindles is a very interesting phenomenon. The

spindle becomes greatly extended laterally by the addition of peripheral fibers and gradually assumes the curved form shownin (E). As more peripheral fibers are successively added the remains of. the central fibers disappear from about the cell-plate,leaving two separate aggregations of fibers which are connected by the first formed portion of the cell-plate (F). These aggre-gations of kinoplasmic fibers, which may be called kinoplasmasomes, have a very characteristic form and structure.

(3) Cf. WOODCOCK (1906, p. 182):The fertilisation spindle or definitive nucleus is to be regarded as representing the trophic portion, and it will be conve-

nient, therefore, to distinguish it as the tropho-nucleus. When reconstituted and in the resting condition this body possess-es, as the normal number, eight distinct chromatic aggregations or chromosomes (fig, 8 A, t.chr.).1 Close to either end of thespindle is another chromatic body (fig. 7, k, k’). These two masses also come from the micro-and megagamete respectively.They proceed to fuse, and the resulting body, which may be termed the. k i n e t o n u c 1 e u.s, passes into the now round-ed trophonucleus, where it takes up a central position. The kinetonucleus also possesses eight peripherally situated chro-mosomes (fig. 8 A, k.chr.), embedded

(4) Cf. SCHAXEL (1911, p. 588):Nucleolen der Strongylocentrotus-Ontogenesis). Gelegentlich der Emission findet die Beeinflussung des Cytoplasmas

durch das Chromatin statt, indem die Kinetochromidien (so nannte ich die hier behandelte Erscheinungsweise des extranu-clearen Chromatins den R. H e r t w i g schen Geschlechtschromidien [=Goldschmidts Sporetien] gegenüber) ins Plasma gelan-gen. Soll für einen Augen-blick in-Weismanns Terminologie gesprochen werden, so wären in den Kinetochromidien die deter-minierenden Biophoren enthalten zu denken, die zur Aktivierung der Zellproduktion die im Kern persistierenden Ide verlassen.Im Zelleib findet dann vom

(5) Cf. ALEXEIEFF (1917, p. 512):D’autre part, certaines observations que j’ai pu faire sur le kinetonucleus des Bodo montrent clairement que celui-ci n’est pas

un vrai noyau un plaste comparable à boaucoup d’égards au pyrénoyde des; Flagellés. La plus decisive de ces. observations est,lasuivant:le kinetonucleus presénte une METACHROMASIE tres nette avec le bleu de.toluidine; cet organite se colore, en effet,en rouge violacé foncé, tandis que le noyau et le protoplasma se colorent en bleu pale; on est ainsi amené a.contester la valour


nucleaire du kinetonucleus qui est en realité. un ORGANITE MITOCONDRIAL A FONCTION GLYCOPLASTIQUE. Cependant c’est là underivé nucleaire,en.quoi il ne differe du reste nullement des autres mitochondries, qui pour moi sont toujours d’origine nucle-aire. A la place du terme « kinetonucleus » qui consacre une opinion erronee, je propose celui de KINETOPLASTE (ou kine-tosoma)1;ce nom indique suffisamment qu’il s’agit ici d’un organite dont le role physiologique est au service des flagelles.

(6) Cf. SHARP (1943, p. 85):An important feature of the chromosome is the specialized region at which its reactions with the spindle mechanism seem

to be largely centered. This region is called the kinetochore. (Other terms in the literature are centromere, primary constriction,and kinomere.) The kine-tochore commonly appears as a relatively achromatic region. In certain large chromosomes it can beseen to be traversed by two slender strands which evidently represent the chromonemata. In some instances a minute body,the kinosome, has been made out at the middle of each strand.

(7) Cf. SCHRADER (1944, pp. 20-21):This kinetochore, though of considerable size, appears to be homogeneous and structureless, which may or may. not be

due to the acetocarmine method employed in the large volume of cytogenetic work in Zea. In certain Amphibia and especiallyAmphiuma, a second element – the spindle spherule or kinosome – appears in this commissural region.

3 There is no point in keeping alive the many names that have been applied to the kinetochore. The following list of 27 termsdoes not attempt to give minor modifications, but shows quite adequately the length to which biological nomenclature may go:Achromatic region Guiding granule Polar granuleAchromite (Leitkorperchen) Proximal granuleAttachment body Insertion region (granule proximale)Attachment chromomere Insertion gap Separation regionAttachment constriction (Insertionslücke) (Trennstelle)Attachment locus Joint Spindle fiber attachmentAttachment point (Gelenk) Spindle fiber constrictionAttachment region Kinetic body Spindle fiber insertionCentric constriction Kinetic constriction Spindle fiber locusCentromere Kinetochore Traction coneCommissure Primary constriction.

(8) HUSKINS (1944, p. 82):Sharp has adopted the term kinosome, proposed -by the reviewer for the particle, but not his “kinomere” for the region

which, as a functional whole, is the usual concern of the geneticist.

(9) In last paper published by SCHRADER (1941d) only expressions such as “kinetochore region” and “kineto-chore-centriole hypothesis” can be found.

(10) Cf. SIMPSON (1972, p. 180: Terminology):Several groups of flagellated protozoa contain a unique mitochondrion which has an exceptionally large amount of DNA

localized in one region of the inner matrix. This DNA stains with ordinary basic dyes as a dark purple granule easily visiblein the light microscope (Fig. i). This darkly stained granule, which is always located at the base of the flagellum, was first not-ed by Ziernann (1898) in Trypanosoma rotatorium in the frog, and by Rabinowitsch – and Kempner (1899) in Trypanosomalewisi in the blood of the rat. The terminology of this granule has varied over the years in accordance with the current theo-ry as to its function. Thus we find the terms nucleolus (Rabinowitsch and Kempner, 1899), micronucleus (Plimmer and Brad-ford, 1899), blepharoplast (Wasielewski and Senn, 1900), centrosome (Laveran and Mesnil, 1900), kinetonudeus (Woodcock,1906), parabasalbody, kinetoplast (Alexeieff, 1917), and kinetoplast-mitochondrion (Pitelka, 1961).

Since we still do not understand the function of this large amount of mitochondrial DNA, and since studies with the elec-tron microscope have . revealed a much richer and more complex infrastructure than a mere “purple granule,” an appropriateuniversally acceptable terminology is difficult to obtain. The term kinetoplast has come into general usage in recent years(Miihlpfordt, 1964), but there is still confusion concerning the exact denotation. Some authors use the word to signify onlythe large DNA nucleoid structure present in the mitochondrion. Still others confuse the term kinetoplast with kinetosomewhich is actually another term for the basal body or centriole.

In this review we use the term kinetoplast to signify that portion of the mitochondrion containing the mitochondrial DNA,including the enclosing mitochondrial membranes. Kinetoplast DNA (K-DNA) indicates the DNA localized in the innermatrix of the mitochondrion that stains with basic dyes.

(11) The most recent papers quote “kinetoplast DNA (kDNA) see STUART and FEAGIN (1992).

(12) Cf. NAWASHIN (1932, p. 231):1. It is a well known fact that a chromosome can function both in mitosis and in meiosis only when it possesses the kinet-

ic constriction containing the kinetic body (DELAUNAY, 1930) or “Leitkorperchen” auctorum. (METZNER, 1894; S. NAVASHIN,1916; TRANKOVSKY, 1930), i. e. a. specially organized very small section where the spindle fibers are attached. Since each chro-mosome has only one kinetic body,

16 BATTAGLIA

(13) Cf. DARLINGTON (1934, pp. 237-238):Secondly we see that separation of these threads occurs following the separation of two bodies, the “attachment chro-

momeres” or, kinetic bodies, which appear to pull them to opposite poles.There is yet another empirical property which distinguishes, the chromosome behaviour at meiosis from that at mitosis.

The chromosomes do not divide at their spindle attachments. They behave as units in the anaphase movement. Further thismovement is seen in meiosis to be a continuation of a. repulsion between the kinetic bodies at the spindle attachments of thesame nature but of greater’degree than that between other parts of the chromosomes. There must be a localised charge onthe kinetic, bodies.

(14) Cf. MATSUURA (1941, p. 375):The writer infers from observations on the development of the kinetochore that the essential element persistent

throughout the kinetochore cycle is the fine thread, chromonemantic in structure but different in behavior (v. infra), whichmay be referred to as the kinetonema. At early stages of the division the kinetochore consists of the naked kinetonema; atmetaphase the latter is provided with a matrical substance.

(15) GRUNDMANN (1966, p. 132) describes his terminological preferences and interpretations as follows:This transportation .occurs roughly in three stages. First, after loosening of the prophase entanglement, the chromosomes

align themselves equatorially at metaphase, then the longitudinal halves move towards two poles, which are as a rule situat-ed at the exact opposite of each other,. These poles are the centres of the movement of the chromosomes and we call themtherefore kinetocentres. They determine also the orientation of the metaphase equatorial plane, which according to definitionlies exactly in the middle between both poles, vertical to the abstract line connecting them, thus dependent on the positionof the kinetocentres. Vice-versa, we define the kinetocentres as those cell components which determine direction and extentof the movement of the chromosomes. There are two kinetocentres in each typical mitotic karyokinesis, i.e., they are identi-cal with the “mitosis centres” of Mazia (1961a).

Acknowledgements - The author started the collection of .the.data presented in this article in the years1954 and 1955, when, as Fulbright Fellow, he worked at che Department of Biology, Fordham Univer-sity, New York, under the direction of the eminent Prof. Charles Berger S. J. It is only recently, that theauthor has had the opportunity of completing the collection and the elaboration of the data and com-piling the present note.

This work has been carried out in the “Dipartimento Scienze Botaniche-Universita di Pisa”. Theauthor wishes to thank Prof. Fabio Garbari, Director of the Department for the use of all Departmen-tal facilities.

The author also express sincere thanks and appreciation for their critical reading of the manuscript to:Prof. Canio G. Vosa, Linacre College, Univ. of Oxford, U.K.Prof. William F. Grant, Dept. Plant Sciences, McGill University, Quebec, Canada.Dr. Ronald Packham, Dip.Anglistica, Univ. Pisa.For careful bibliographical research, the author is greatly indebted to dr. Andrea Costa (Real Jardin

Botanico, CSIC, Madrid), Prof.sa Elettra Pepe D’Amato (Dip. Biologia Vegetale, Univ. La Sapienza,Roma), Dr. Giovanni Ferrara (Biblioteca Biologica, Univ. Milano), Direzione Biblioteca Stazione Zoo-logica A. Dohrn, Napoli), Regina Heroff (Europ. Mol. Biol. Lab.,Szilard Library, Heidelberg).

The author also duly acknowledges for suggestions, discussion or comments the following col-leagues:Prof. Johann Greilhuber, Institut f.Botanik Univ. Wien., Austria;

» Werner Greuter, Botan Museum, Berlin-Dahlem, Germany;» Gundolf Keil, Inst. f. Geschichte Medizin, Univ. Würzburg, Germany;» Imgard Müller, Medizinische Fakultät, Univ. Bochum, Germany;» Wilhelm Sauer, Institut f. Biologie I, Univ. Tübingen, Germany;» Manfred Schliwa, Inst. f. Cell. Biol., Univ. München, Germany;» Gerhard Wagenitz, A.v. Haller-Institut f. Pflanzenwiss, Univ. Göttingen, Germany;» Horace Freeland Judson, Dept. History, George Washington Univ. Washington, U.S.A.;» J.M. Herr Jr., Dept. Biology, Univ. South Carolina Columbia, U.S.A.;» Rudolf Schmid, Dept. Integrative Biology, Univ. of California, Berkeley, U.S.A.;» Veronica Hurst, Associate Editor, Oxford English Dictionary, Oxford, U.K.


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Received June 8, 2002; accepted June 28, 2002


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Centromere, kinetochore, kinochore, kinetosome, kinosome