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FIN BUDS, LIMR BUDS, SIMII AR TYPES OF BUDS ? JACQUELINE G]~RAUDIE GI~RAUDIE J. 1995 - Fin buds, limb buds, similar types of buds ? [Bourgeons de nageoires, bourgeons de mem- bres, sont-ils de m~me type ?]. GEOBIOS, M.S. n ° 19 : 249-254. ABSTRACT Some aspects of the development of fin and limb buds using data available in the literature are presented in order to examine whether patterning mechanisms bear more similarities than differences. Modern comparative studies are done between teleost fin buds and amniote limb buds. Although those taxa are not phylogenetically related in order to explain the transition fm-limb, cytological data emphasize differences which are not so apparent at the level of gene expression. Such an approach points out to a conservation of mechanisms establishing patterning of appendages in spite of uncertainities in the function of the genes studied. KEY-WORDS : FIN BUDS, LIMB BUDS, CYTOLOGY,TEOLEOST, AMNIOTE. Rt~SUME L'article analyse quelques aspects du d6veloppement des bourgeons de nageoires et de membres ~ l'6chelle cytolo- gique et mol6culaire dans le but de d6gager similarit6s et divergences dans les m6canismes de morphogen6se. Les donn6es sont disponibles dans la litt6rature en ce qui concerne le d6veloppement des bourgeons de nageoires des t414ost6ens et des membres des amniotes. Bien qu'il n'y ait pas de relations phylog6n6tiques entre eux pour expliquer la transition nageoire-membre, les r6sultats de l'6tude cytologique montrent des diff6rences dans rorga- nisation des deux types de bourgeons d'appendices que les donn6es de biologie mol6culaire ne font pas apparaitre aussi clairement. Une telle approche met l'accent sur la conservation des m6canismes qui permettent la formation des appendices bien que l'on ne connaisse pas toujours la fonction exacte des g6nes 6tudi4s. MOTS-CLI~S : BOURGEONS DE NAGEOIRES, BOURGEONS DE MEMBRES, CYTOLOGIE, T]~Lt~OSTI~ENS, AMNIOTES. INTRODUCTION The concept of homology between paired fins and limbs is widely accepted. Biologists are left with the task of convincingly explaining the transition fin-limb and how the first appendages which can be described as limbs fond in some fossils emer- ged from paired fins (Vorobyeva 1992 ; Coates 1994 ; Hinchliffe 1994). Adaptative diversity then arose from modulations of the basic chiri- dium plan giving rise to wings, arms or legs with large variations in size and configuration among different vertebrates. In this paper, a comparative ontogenesis of fin and limb buds is presented : what are their com- mon features and pecularities ? What can we learn from gene expression during their respec- tive development which could help under- standing their filiation ? THE SKELETON OF APPENDAGES : FIN SKELETON VERSUS LIMB ENDOSKELETON What makes the originality of a fin versus a limb is its large dermal skeleton which protudes outside the body. It comprises a bony component, either constituted basically by camptotrichia pre- sent in the dipnoans or by lepidotrichia found in actinopterygians where they coexist with actino- trichia, a collagenous skeleton laying at their distal end. The endochondral component of a fin is reduced to the girdle and rows of radials whose complexi- ty and extension outside the body vary largely according to : (1) the type of fin observed in teleosts, it is more prominent in the case of the pectoral fins than in the pelvic ones ;

Fin buds; limb buds; similar types of buds?

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Page 1: Fin buds; limb buds; similar types of buds?

FIN BUDS, LIMR BUDS, SIMII AR TYPES OF BUDS ?

JACQUELINE G]~RAUDIE

GI~RAUDIE J. 1995 - Fin buds, limb buds, similar types of buds ? [Bourgeons de nageoires, bourgeons de mem- bres, sont-ils de m~me type ?]. GEOBIOS, M.S. n ° 19 : 249-254.

ABSTRACT

Some aspects of the development of fin and limb buds using data available in the literature are presented in order to examine whether patterning mechanisms bear more similarities than differences. Modern comparative studies are done between teleost fin buds and amniote limb buds. Although those taxa are not phylogenetically related in order to explain the transition fm-limb, cytological data emphasize differences which are not so apparent at the level of gene expression. Such an approach points out to a conservation of mechanisms establishing patterning of appendages in spite of uncertainities in the function of the genes studied.

KEY-WORDS : FIN BUDS, LIMB BUDS, CYTOLOGY, TEOLEOST, AMNIOTE.

Rt~SUME

L'article analyse quelques aspects du d6veloppement des bourgeons de nageoires et de membres ~ l'6chelle cytolo- gique et mol6culaire dans le but de d6gager similarit6s et divergences dans les m6canismes de morphogen6se. Les donn6es sont disponibles dans la litt6rature en ce qui concerne le d6veloppement des bourgeons de nageoires des t414ost6ens et des membres des amniotes. Bien qu'il n'y ait pas de relations phylog6n6tiques entre eux pour expliquer la transition nageoire-membre, les r6sultats de l'6tude cytologique montrent des diff6rences dans rorga- nisation des deux types de bourgeons d'appendices que les donn6es de biologie mol6culaire ne font pas apparaitre aussi clairement. Une telle approche met l'accent sur la conservation des m6canismes qui permettent la formation des appendices bien que l'on ne connaisse pas toujours la fonction exacte des g6nes 6tudi4s.

MOTS-CLI~S : BOURGEONS DE NAGEOIRES, BOURGEONS DE MEMBRES, CYTOLOGIE, T]~Lt~OSTI~ENS, AMNIOTES.

I N T R O D U C T I O N

The concept of homology be tween pa i red fins and limbs is wide ly accepted. Biologists are lef t wi th the t a sk of convincingly expla in ing the t r ans i t ion fin-limb a nd how the f irs t appendages which can be descr ibed as l imbs fond in some fossils emer- ged f rom pa i red fins (Vorobyeva 1992 ; Coates 1994 ; Hinchliffe 1994). Adapta t ive d ivers i ty t h e n arose f rom modula t ions of the basic chiri- d ium plan giving r ise to wings, a rms or legs wi th large va r i a t ions in size and conf igura t ion among different ve r tebra tes .

In this paper , a compara t ive ontogenesis of fin and l imb buds is p r e sen t ed : wha t are t he i r com- mon f ea tu re s and pecular i t ies ? Wha t can we lea rn f rom gene express ion dur ing the i r respec- t ive deve lopmen t which could help under - s t and ing t h e i r f i l iat ion ?

T H E S K E L E T O N O F A P P E N D A G E S : F I N S K E L E T O N V E R S U S L I M B E N D O S K E L E T O N

W h a t makes the or ig inal i ty of a fin ve rsus a l imb is its large dermal skele ton which pro tudes outs ide the body. I t comprises a bony component , e i the r cons t i tu ted basical ly by campto t r i ch ia pre- sent in the d ipnoans or by lepidotr ichia found in ac t inopterygians where t h ey coexist wi th actino- tr ichia, a collagenous skele ton laying at the i r distal end.

The endochondra l component of a fin is r educed to the girdle and rows of radia ls whose complexi- t y and extens ion outs ide the body v a ry la rge ly according to : (1) the type of fin observed in teleosts , it is more p rominen t in the case of the pectoral fins t h a n in the pelvic ones ;

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(2) the group of fish studied: in some sarcoptery- gians fins, endoskeletal elements bearing the der- mal skeleton protude from the body surface while on the contrary, endochondral bones make all the skeletal elements of a limb or chiridium, inclu- ding the girdle located deeply in the body. In this respect, it should be mentionned that the com- plexity of the muscular organization within a limb differs from the simple dorsal and ventral muscle masses found in a teleost paired fin. Would these pecularities b e reflected in their on- togeny ?

THE EPITHELIUM

In the distal marginal region of a growing appen- dage bud, the organization of the epithelial ecto- dermal (epidermis) allows the distinction between a teleost fin and an amniote limb bud. An elonga- ted apical fold described as the "pseudoapical ridge" (G~raudie & Francois 1973) is a fin bud feature while the pseudostratified thickened epi- dermis defines the apical ectodermal ridge (AER) extending from the anterior to the posterior re- gion of the limb bud.

THE S T R U C T U R E O F THE B U D S

The paired fin and limb buds are constituted by a core of mesenchymal cells covered by an epithe- lium of ectodermal origin.

THE MESENCHYME

It is admitted that somatopleural cells migrate from the lateral plate at the level of the paired appendage field where they accumulate and di- vide and constitute the limb bud. Successive mi- grations of somitic mesoderm cells adjacent to the prospective limb bud contribute to a functio- nal limb musculature (Chevallier 1979). A somitic origin has also been proposed for the fin muscula- ture (G~raudie & Francois 1973) confined to the base of the appendage, connected to the endoske- leton and the base of the lepidotrichia.

A somatopleural origin does not apply to the un- paired fin buds where cell lineages studies using intracellular injections of vital fluorescent dyes showed that neural crest cells, like in amphibian median fin fold (Bodenstein 1952), are present in the developing tail fin (Smith et al. 1994). In the absence of somatopleura in this region of the em- bryo, like in dorsal and anal fins, it is obvious that cells originate from another source and it is of interest to determine whether neural crest cells with a skeletogenic fate are present in the fins. Indeed, some teeth are present on the poste- rior surface of the pectoral fins of some Bra- chyopterygii (G~raudie 1988). If fish odontoblats originate like other ver tebra te odontoblasts from neural crest cells (Lumsden 1988), the question is raised concerning the participation of neural crest cells with a skeletal fate (bone-forming cells = scleroblasts) during any fin morphogenesis be- cause neural crest cells derivatives such as pig- ment cells or later Schwann cells are present in developing buds (G~raudie 1985).

It should be stated that the growing fin buds of the sarcopterygian fish lineage and developing anamniote limb buds lack a distinctive epidermal ridge. Interestingly, it is in this fish lineage that the possible transition between fin and limb is searched. As we have not yet any data on the molecular identity of the ectodermal cells in the- se groups which we could compare with data available for amniote limb buds, it is premature to propose a meaningful explanation for this mor- phological difference.

A thickening of the epidermis occurs in the te- leost pelvic fin bud (G~raudie & Franqois 1973) but prior to its folding. If it can be compared then to an apical ectodermal ridge such as described in the case of early pectoral fin morphogenesis (Bou- vet 1968 ; Wood 1982) and during amniote limb bud development, it has three distinctive featu- res: 1 - The thickening occurs through the elongation of the cells of the basal layer which becomes co- lumnar and keeps a direct contact with the basal lamina while a pseudostratified epithelium char- acterizes the apical epidermal ridge limb bud. Such is also reported during pectoral fin develo- pment and these differences raise the possibility, in the case of fin development, of variations in the cellular organization if not in the morphoge- netic mechanisms between pectoral and pelvic fin buds which do not develop synchronously on the larvae. Molecular studies should help interpre- ting these differences and recognize their relative importance. 2 - The thickening of the epidermis appears in the fin bud in an earlier stage of development than in a limb bud and covers a small population of mesenchymal cells. Would it function then like a limb AER and be involved in cell proliferation and in the setting of the identity of the endoske- letal elements of the fin reduced to its girdle and radials as indirectly proposed by Thorogood (1991) ? Or should we envision a modulation be- cause we deal with a fin bud in which specific dermal skeletal elements will differentiate in ad-

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dition to the endoskeleton and set according to a sophisticated pat tern not yet fully understood ? 3 - The epithelial thickening occurs t ransient ly in the fin bud. The next step of the teleost paired fin bud outgrowth is the creation of a subepider- real space approximately at the center of the thickened epithelium owing to a precise new pat- tern of proliferation in both components of the bud (G~raudie 1980). This fold should be conside- red a fin bud feature, at least a teleost one. In this context, it is assumed tha t the cells of the fold express new morphogenetetic properties to be explained now in terms of specific gene ex- pression. Indeed, in the subepidermal space of this elongating epidermal fold (the "pseudoapical ridge"), collagenous actinotrichia are to be laid and are a specific fish fin component, prominent in teleosts though discrete in dipnoans (G~raudie 1984).

The bony lepidotrichia differentiate at the epithe- lio-mesenchymal interface (G~raudie & Landis 1981) into a proximo-distal direction, in contrast to the actinotrichia first observed in the fin bud apex. Current work aim to establish relationships in terms of molecular signals between the actino- trichia, the lepidotrichia and their progenitor cells, their overlapping and their role for the dif- ferentiation of the chondroblasts of the girdle. The s tudy of early dipnoan fin bud morphogene- sis is equally necessary in order to unders tand a possible transit ion fin-limb in spite of the difficul- ty of gett ing embryos.

Consequently, there are indeed similar features between fin and limb buds in their initial stages of development but each one acquire early its identity possibly related to the development of the skeleton.

To explain limb morphogenesis, the existence of epithelio-mesenchymal interactions is well docu- mented through ablation and t ransplantat ion ex- periments of the AER which is directing bud outgrowth. With respect to the fin buds, similar interactions have not been described in such de- tails owing to some difficulties in fish embryos handling but molecular studies could eventually be a substi tute.

C O M P A R A T I V E H O M E O B O X - C O N T A I N I N G G E N E E X P R E S S I O N D U R I N G E A R L Y A P P E N D A G E D E V E L O P M E N T

Although our knowledge of fin bud molecular ge- netic is in infancy compared to amniote limb bud, it appears tha t cognate genes are expressed in

both types of appendage buds with eventually for some of them, a similar strinking spatio-temporal pattern. These results on vertebrate development in general s temmed from the fruit fly Drosophila developmental pionner studies (N~isslein-Volhard & Wieschaus 1980 ; see Alberts et al. 1994). They allowed the identification of classes of homeobox- containing genes permitting then the isolation of homologous (= cognates) genes in higher verte- brates, some of them being of interest during limb outgrowth and patterning. The homeobox consists of about 180 base pairs tha t encodes a domain of the homeoprotein (homeodomain) which can bind to regulatory regions of other ge- nes, and as such is considered to be a transcrip- tion factor. The fact tha t a single gene in Droso- phila may be found in multiple different copies in vertebrates is explained by duplications of an an- cestral gene and divergence (McGinnis & Krum- lauf 1992). Recently, diverse homeobox-contai- ning genes have been isolated in the teleost ze- brafish (Danio rerio), a lower ver tebrate with a good potential to s tudy various aspects of develo- pment (Kimmel 1989).

So far there are no data on homeobox-containing genes expressed in sarcopterygian fin buds and anamniote limb buds, groups of major importance for the transition fin-limb. Consequently, the comparison of genes expressed during teleost fin and amniote limb buds development will be re- ported having in mind that they do not represent taxa in which there is a direct filiation to explain the transition fin-limb but assuming that pat- terns of gene expression will apply to anamniote limb buds as well based on the concept of conser- vation during evolution.

Sequence comparisons between the homeodomain region of the proteins encoded by these diverse homeobox-containing genes have been extensively searched in database. The pat tern of expression of the genes transcribed is studied basically by in situ hybridization techniques which allow a direct visualization of the regions of the embryo where the gene is expressed. These territories have been compared between vertebrate appendages. The expression of some segmentation genes (pair- rule genes : even-skipped ; segment-polarity gene: engrailed and hedgehog) and some homeotic se- lector genes of the Bithorax complex are presen- ted when these genes are studied in fin and limb buds. In addition, the expression of other hox- containing genes is reported when a comparison is also possible in both types of appendages. It is obvious that few data are available but results already point out to an evolutionary conservation of some mechanisms of appendage patterning.

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Most of hox containing genes are only expressed during appendage development and are "turned off' in the adult unless amputat ion followed by regeneration elicits an induction of the re-expres- sion for a few of them, but this aspect will not be discussed here.

Even-skipped (eve) Drosophila vertebrate cognates Even-skipped gene in Drosophila belongs to the pair-rule class of genes a n d its expression is re- quired for the correct development of the meta- meres in the embryo. Its homologues have been again first cloned in mouse where at least two genes : evx-1 and evx-2 ( Bastian & Gruss 1990 ; Dush & Mart in 1992) are present in the genome. Recently cloned in the teleost, eve-1 (Joly et al. 1993) and eve-2 (Duboule unpublished) Eve-1 transcripts are present, in addition to other sites in the embryo, in the mesenchyme of the develo- ping pectoral fin bud (G~raudie unpubl, observ.) like evx-1 and 2 both expressed in the posterior distal mesenchyme of the developing mouse limb buds. This gene family provides a first example of conservation of gene expression in the same component of both types of buds but is their func- tion similar ?

Mouse Evx-2 gene is located in the most posterior par t of the hox d complex (hox d13) while Evx-1 is physically close to hox a13 (see below). The ex- pression of both genes present similar pat terns during limb development (Doll~ et al. 1994) sug- gesting similar regulations which will have to be studied during fin bud development having in mind this evolutionary link.

Engrai led (En) Drosophila vertebrate co- gnates In Drosophila engrailed gene belongs to the seg- ment polarity group. Teleost genome contains at least three distinct engrailed genes - engl, eng2 and eng3 (Ekker et al. 1992) compared to the two genes En-1 and En-2 isolated so far in mammals (Joyner & Mart in 1987) but known to be present in other vertebrates . In both types of bud appen- dages, expression is found in the ectodermal co- ver during a short t ime of development. In the fishes it is restricted, to the pectoral fin bud and to engl only, related more closely to En-1 than the two others. This similar spatio-temporal ex- pression of this gene provides an other example of conservation through out evolution although the function of this gene is uncertain and could be different during fin and limb bud ontogenesis: in fish, it is expressed in the ventral region of the bud while in the limb En expression is not so res- tricted.

H e d g e h o g (hh) Drosophila vertebrate co- gnates Recent data point out to the structural and func- tional conservation of this other segment polarity gene family whose gene product is a protein in- volved in cell-cell interactions. First isolated in Drosophila, several hh homologs have been found in vertebrates. One of them, sonic hh is expres- sed in the posterior mesoderm of the limb bud (Riddle et al. 1993) and in the same region of the pectoral fin buds (Krauss et al. 1993). This pre- cise region in chick limb bud is endowed with a polarizing activity clearly demonstrated through transplantat ion in the anterior mesoderm which induces there the formation of mirror-image digit duplications. This striking similar spatially res- tricted pat tern of gene expression is the first strong indication of a possible similar s t ra tegy to build up an appendage through the conservation of the mechanism of initial patterning.

Homeot ic selector genes (HOM / hox com- plexes) . The genes of the Hox a, b, c and d clusters found in vertebrate are the counterparts of the homeo- tic gene complexes (Antennapedia ANT-C and Bi- thorax BX-C ) found in Drosophila ; it has been proposed that both complexes are functionally re- lated (Wilkinson 1993). They arose probably by duplication of a single ancestral gene cluster (Doll~ & Duboule 1993). During this gene expan- sion, they retain probably some of their previous function in the patterning of the antero-posterior body axis in addition to novelties. One of the functions of these hox genes could be related di- rectly or not to the control of local growth which could interact with patterning, and in the case of appendage linked to their evolution (Duboule 1994).

In limb buds, extensive studies have shown a co- ordinate expression of these genes, their succes- sive activation leading to the notion of temporal colinearity related with the spatial colinearity ob- served in the developing organ (Duboule 1992). Some zebrafish cognate genes are being cloned in Duboule's laboratory and the pat tern of expres- sion of hox a and hox d genes should yield soon to interesting results, possibly shedding some light on the phylogenetic relationships between fin and limb. Will their pat tern be similar to the one established in limb buds ? Will divergence of expression give some information on the setting of the endoskeleton less prominent in fin than in limb and possible mechanisms of transit ion fin- limb ? Or shall we learn more about pat terns of proliferation in an appendage as a whole (Duboule 1994) ? As mentionned by Coates

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(1991), the doma i n of express ion of hox d genes in the pos t e r io r to d is ta l l imb bud m e s e n c h y m e seems to b e a r some signif icance wi th the bend ing of the pos t e r io r side of the l imb (post axial) as proposed b y Shub in & Alberch (1986). Will any p a t t e r n of hox express ion d o m a i n of evo lu t iona ry s ignif icance emerge f rom a te leos t fin b u d s t u d y ?

M u s c l e - s p e c i f i c - h o m e o b o x (Msh) Drosophila v e r t e b r a t e c o g n a t e s Fi r s t c loned and sequenced in the mouse (Rober t et al. 1989 ; Hill et al. 1989), t h e n in chicken (Coelho et al. 1991 ; Rober t et al. 1991) and iden- tified f ina l ly as M s x l (=Hox 7-1) a n d Msx-2 (=Hox 8) w i th the possible exis tence of a t h i rd gene (see Ho l l and 1991), cogna te genes h a v e been cloned in zebra f i sh whose genome con ta ins a t leas t five genes , Msx A, B, C, D and E (Ak imenko et al. in press) . W h a t is i n t e r e s t i ng is the t r an - s ient express ion of all the m s x genes except MsxE in t h e fin bud ec toderm, l ike for a m n i o t e l imb buds and the r e s t r i c t ed express ion of Msx 1 to the l imb bud m e s e n c h y m e which lead to the proposal , b a s e d on p a t t e r n s of gene express ion , of funct ional s imi la r i t i e s b e t w e e n : 1, l imb Msx2 and fin MsxA and D, and 2, l imb M s x l and f in Msx B a n d C (Akimenko et al. 1995). F u r t h e r s tud ies should clar ify the func- t ion of t h e s e genes du r i ng the ep i the l io -mesen- chymal i n t e r ac t ions t h e y p r o b a b l y m e d i a t e in ap- pendages d e v e l o p m e n t as well as in o the r develo- p ing o rgans , t he i r evo lu t iona ry re l a t ionsh ips and also the poss ib i l i ty of a func t iona l r edundancy .

D i s t a l - l e s s (Dll) Drosophila v e r t e b r a t e co- g n a t e s This gene is exp res sed in t he ec tode rm of the de- ve loping f ly leg w h e r e i t is r equ i r ed du r i ng mor- phogenes i s (Cohen 1990). I t s homotogue has been ident i f ied in the m o u s e as Dlx-1, Dlx-2 and Tes-1 bu t e x p r e s s e d m a i n l y in t he ne rvous sys t em, an ec tode rma l der iva t ive . T r a n s c r i p t s of the cognate gene cloned in zebra f i sh (Akimenko, unpub l i shed ) h a v e b e e n found in t he ec tode rm of the develo- p ing zeb ra f i sh fin buds and cu r r en t s tudies should b r ing the m u c h needed addi t iona l d a t a for a m e a n i n g f u l compar i son .

Molecu la r d a t a leave us w i th the i m p r e s s i o n of un i t y of cogna te gene express ion dur ing appen- dage deve lopmen t . Neve r the l e s s , the d iscovery of new m a r k e r s is n e c e s s a r y because t h e r e should be combina t ions of molecules un ique to fin buds because of the specific fin d e r m a l ske le ton compo- nents . W h a t genes a re specif ical ly exp re s sed in the fin fold which are not exp re s sed in the l imb apical r idge and r eve r se is the nex t ques t ion to be asked.

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J . G E R A U D I E Universitg Paris-Sud XI

Laboratoire de Biologie du D~veloppement des Poissons et URA 1134 du CNRS

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