Biology of Invertebrate and Lower Vertebrate Collagens

NATO ASI Series Advanced Science Institutes Series

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The series is published by an international board of publishers in conjunction with the NATO Scientific Affairs Division

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Series A: Life Sciences

Biology of Invertebrate and Lower Vertebrate Collagens

Edited by

A. Bairati University of Milan Milan, Italy

and

R. Garrone Claude Bernard University Lyon, France

Plenum Press New York and London Published in cooperation with NATO Scientific Affairs Division

Proceedings of a NATO Advanced Research Workshop on the Biology of Invertebrate and Lower Vertebrate Collagens, held June 24-28, 1984, at the Alessandro Volta Center for Scientific Culture, Villa Olmo, Como, Italy

Library of Congress Cataloging in Publication Data

NATO Advanced Research Workshop on the Biology of Invertebrate and Vertebrate Collagens (1984: Alessandro Volta Center for Scientific Culture) Biology of invertebrate and lower vertebrate collagens.

(NATO ASI series. Series A, Life sciences; v. 93) "Proceedings of a NATO Advanced Reserach Workshop on the Biology of In­

vertebrate and Lower Vertebrate Collagens, held, June 24-28, 1984, at the Alessandro Volta Center for Scientific Culture, Villa Olmo, Como, Italy"-T.p. ver­so.

Includes bibliographies and indexes. 1. Collagen-Congresses. 2. Invertebrates-Physiology-Congresses. 3.

Fishes-Physiology-Congresses. I. Bairati, A. II. Garrone, R. III. Title. IV. Series. QP552.C6N37 1985 591.19/245 85-16876 ISBN-\3: 978-1-4684-7638-5 e-ISBN-\3: 978-1-4684-7636-1 001: 10.1007/978-1-4684-7636-1

©1985 Plenum Press, New York A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 Softcover reprint of the hardcover 1 st edition 1985

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

PREFACE

Knowledge in the field of the biology of the extracellular matrix, and in particular of collagen, has made considerable progress over the last ten years, especially in mammals, birds and ln man with respect to very important applied medical aspects.

Basic knowledge in the animal kingdom overall has increased more slowly and haphazardly. We, therefore, considered it useful to organize a meeting specifically devoted to the study of the invertebrate and lower vertebrate collagens.

The NATO Scientific Division financed an Advanced Research Workshop aimed at bringing together experts qualified in collagen biology (with morphological, biochemical and genetic specialization) with researchers who are currently studying collagenous tissues of invertebrates and lower vertebrates. The Medical-Biology Committee of the CNR-Rome and the University of Milan also supplied interest and support for the organization of this Meeting.

The format of the workshop consisted in: 1) main lectures on the most recent aspects of collagen biology; 2) minireviews on the current knowledge of collagenous tissues in the various invertebrate phyla and in fish; 3) contributed papers on particular aspects of research in specific fields; 4) workshops on the methodology of studying collagen.

As we had intended, the Workshop gave a comprehensive overview of acquired knowledge and of the present state of research actlvlty. It permitted wide interdisciplinary discussion, enabling collabora­tions to be established and new research themes to be chosen.

This volume contains the text of all the contributions presented at the Meeting, including posters.

v

To have brought together in one volume basic knowledge, recent experimental results and new methodologies should make this book a useful tool for comparative analysis and for knowledge of the mech­anisms which have governed the evolution of the collagens in the animal world.

We most sincerely thank the organ~z~ng staff of the A. Volta Scientific Centre at Villa Olmo, where the workshop was held, all the collaborators of our laboratories for their valuable co-operation given during the preparation of this volume and particularly Miss M. Properzi for her much appreciated secretarial work.

A. Bairati R. Garrone

Milano, Gennaio 1985

WILLIAM THOMAS ASTBURY AND EMMANUEL FAURE-FREMIET

In his lecture, J. Gross quite rightly recalled the importance of the work of W. T. Astbury and E. Faure-Fremiet as regards our knowledge of fibrous proteins, and collagen in particular.'

W. Astbury and E. Faure-Fremiet must be considered the fathers of modern scientific research on collagen for having introduced and applied biophysical and ultrastructural methodologies to biological materials, for having established the major subject areas of compar­ison and evolution in the animal world, and for having gathered around them and instructed with their teachings many skillful researchers.

Following up on a suggestion made by J. Gross, we should like to briefly remember the lives and work of these men so that young researchers may be able to draw inspiration from them and go on to perpetuate their memory and emulate their spirit.

A. Bairati R. Garrone

William Thomas Astbury was born on February 25th, 1898 at Longton (Stoke-on-Trent, England) into a family of pottery-workers. He studied for a degree in physics at Cambridge where he attended courses in crystallography given by Prof. Hutchinson who, in 1921, introduced him to Prof. Sir William Bragg at University College London. With Bragg, Astbury worked also at the Davy-Faraday laboratory of the Royal Institution as part of a happy working community.

His pioneering nature and the attraction of new and unknown research fields led Astbury to accept an invitation to transfer to the University of Leeds in 1928 in the capacity of Professor of Physics with responsability for organizing a laboratory dedicated

to research in the field of the physics of textile fibres. In those days it must have seemed really strange for a scholar of crystallo­graphy to want to change the direction of his career towards the study of organic materials whose characteristics were considered to have practically nothing to do with the precise world of crystal­lography.

Astbury worked for 33 years in Leeds, obtaining important results in spite of the fact that for a long time the resources available to him were extremely limited (mainly grants from the Rockefeller Foun­dation), he had to construct his own apparatus and operate in a few rooms in an old building. After the Second War the applied importance of the results and the presence of a highly qualifed group of collab­orators prompted the transformation of the laboratory for the physics of textile fibres into the "Department of Biomolecular Structure" which, after Astbury's death in 1961, bec.ame the "Astbury Department of Biophysics".

W. T. Astbury's research activity can be schematically subdivided into several sectors: 1) Crystallography and experimental methodology research, 2) research on textile fibres (wool) and on fibrous pro­teins in general, 3) research on collagen, 4) research on nucleic acids, 5) ultrastructural research on various plant and animal tissues, 6) research of a biomedical type.

Here we are drawing attention to only some aspects of his extremely wide field of activity.

Faced with many technical problems depending on the nature of the biological materials, Astbury worked out some completely new methods and built new apparatus specially to obtain better diffracto­grams. As a result of this activity great biophysical research development began to take place in the field of the molecular structure of paracrystalline or crystallizable components in living material. This experimental technical ability was the result of his earlier collaboration with Sir W. Bragg in the crystallography field. As a physicist accustomed to the order and complexity of crystalline structures Astbury tirelessly sought the existence of general ordered rules in living material, analysing the form and structure of primary constituents and their functional modifications.

The results of his research carried out between 1928 and 1935 on the keratin of wool led to the definition of the secondary poly­peptide configurations a, S and crossed S.

Using biophysical investigation together with experimentation (physical and chemical treatments) Astbury pointed out the relation­ships between various molecular configurations, their modifications and the variable physical properties of the tissue.

ix

The extension of his studies to other proteins (myosin and fibrinogen) led to the concept being established of the existence of protein groups with different molecular structures and macromo­lecular configurations. He then compared the "collagen group" to the K-E-M-F group (keratin, epidermin, myosin, fibrinogen).

Astbury illustrated the diffractographic characteristics of collagen fibres hypothesizing a specific conformatio~ of aminoacid chains responsible for the peculiar distance of 2.8 A between adjacent aminoacids.

He, therefore, widely applied comparative analysis demonstrating the common biophysical characteristics of collagenic tissues belong­ing to different animal species: mammal tendons and cartilage, fish scales, swim-bladder walls, byssal threads of Bivalvia, the skate egg-capsule, sea cucumber filaments and Annelida cuticle. The studies of various animal tissues containing keratin (feathers and reptile scales) in addition to those of mammal hair and of collagens permitted Astbury to lay the foundations of modern comparative research: he outlined the idea that the differentiation of animal species might have a common denominator in the morphology of structural proteins, particularly fibrous ones, and that evolution could also be sought in the mutation of molecular and supramolecular configurations. Of equal importance were his intuitive ideas following the analysis of transformations observed in filamentous and globular proteins SUbjected to denaturation, tannation or crystallization. Astbury postulated the existence of hydrogen bridges between adjacent poly­peptide chains, and maintained that the configurations assumed by various proteins depended on the chemical nature of side chains underlining also the importance of the localization of the hydro­phobic elements.

His analysis of the transformations of the contractile proteins of various muscles and of fibrinogen in fibrin permitted Astbury to hypothesize the transformation of globular into fibrous proteins and the possibility of producing paracrystalline fibrous structures artificially.

~1oreover, Astbury guessed the importance of the application of biophysical and ultrastructural techniques in the industrial and biomedical applied fields. The methodologies introduced by Astbury were widely used in the manufacture of natural and synthethic yarns. The use of electron microscope allowed Astbury to check directly many of his architectural schemes deduced from diffractographic and polaroscopic analysis, also in relation to pathological modifications of collagenous tissues such as bone, joints and teeth.

Astbury's activity which began in the field of crystallography achieved its best results in the biological field where Astbury's genius showed itself in the way he exploited experimental results

x

in order to delineate with admirable intuition the general structural and functional characteristics of structural proteins at a molecular level and the general laws of evolutionary processes; moreover he proposed the notional and experimental bases for modern interdisci­plinary research in biology. In view of his work in interpreting and establishing important biological ideas Astbury can be considered to be the founder of Molecular Biology. With this in mind it is very instructive to reread some of his statements (Harvey Lecture, 1950): ••• "The name "molecular biology" seems to be passing now into fairly common use, and I am glad of that because, though it is un­likely I invented it first, I am fond of it and have long tried to propagate it. It implies not so much a technique as an approach, an approach from the viewpoint of the so-called basic sciences with the leading idea of searching below large-scale manifestations of classical biology for the corresponding molecular plan. It is concern­ed particularly with the forms of biological molecules, and with the evolution, exploitation and ramification of those forms in the ascent to higher and higher levels of organization. Molecular biology is predominantly three-dimensional and structural - which does not mean, however, that it is merely a refinement of morphology. It must of necessity inquire at the same time into genesis and function."

Astbury published two books and 127 papers both alone and in collaboration, thus not only spreading his experimental results but also general biological concepts and those which could be applied in the industrial field.

Here below are listed those of his works which are most closely connected with the subjects in this volume. Further information and particulars on the life and work of W.T. Astbury can be found in the memoirs of J. D. Bernal (Biogr. Mem. Royal Soc. 9, 1, 1963), from whom we have drawn great inspiration.

Books:

- 1933, "Fundamentals of fibre structure", Oxford University Press, London.

- 1940, "Textile fibres under the X-rays", Imperial Chemical In­dustries.

Papers:

- 1927, A simple radioactive method for the photographic measurement of the integrated intensity of X-ray spectra, Proc. Roy. Soc. A, ll5 :640.

1928, Photography and photometry in X-ray crystal analysis, Photo J., 68:500.

- 1931,-(With A. Street), The X-ray studies of the structure of hair, wool, and related fibres. I., General, Phil. Trans.A, 230:75.

xi

- 1932, (With T. C. Marwick and J. D. Bernal), X-ray analysis of the structure of the wall of Valonia ventricosa . I., Proc. Roy. Soc. B, 109:443. --

- 1932, (With T. C. Marwick), X-ray interpretation of the molecular structure of feather keratin, Nature, Lond., 130:309.

- 1933, (With W. R. Atkin), X-ray interpretation of the molecular structure of gelatin, Nature, Lond., 132:348.

- 1933, (With H. J. Woods), X-ray studies of the structure of hair, wool and related fibres. II. The molecular structure and elastic properties of hair keratin, Phil. Trans. A, 232:333.

- 1934, Aspects of growth, Cold Spring Harbor Symp., 2:15. - 1934, (With R. D. Preston), A mercury-sealed water-cooled rotating

X-ray target, Nature, Lond., 133:460. - 1935, (With S. Dickinson), a-S intramolecular transformation of

myosin, Nature Lond., 135:95. - 1935, (With W. A. Sisson), X-ray studies of the structure of hair,

wool and related fibres. III. The configuration of the keratin molecule and its orientation in the biological cell, Proc. Roy. Soc. A, 150:533.

- 1935, (With R. Lomax), An X-ray study of the hydration and dena­turation of proteins, J. Chem. Soc., 846

- 1936, Recent advances in the X-ray study of protein fibres, ~. Test. Inst., 33:778.

- 1936, X-ray studies of protein structure, Nature Lond., 137:803. - 1937, Relation between "fibrous" and "globular" proteins, Nature

Lond., 140:968. - 1937, (With R. D. Preston), The structure of the wall of the

green alga Valonia ventricosa, Proc. Roy. Soc. B, 122:76. - 1938, (With F. O. Bell), Some recent developments in the X-ray

study of proteins and related structures, Cold Spring Harbor Symp., 6:109.

- 1938, X-ray adventures among the proteins (4th Spiers Memorial Lecture, 1937), Trans. Faraday Soc., 34:377.

- 1938, (With F. n. Bell), X-ray study of thymonucleic acid, Nature Lond., 141:747.

- 1939, The molecular structure of the fibres of the collagen group, (1st Procter Memorial Lecture), J. Int. Soc. Leather Trades' Chemists, 24:69.

- 1940, (With R. G. Harrison and K. M. Rudall), An attempt at an X-ray analysis of embryonic processes, J. Expr. Zool., 85:339.

- 1940, (With F. O. Bell), Molecular structure of the collagen fibres, Nature Lond., 145:421.

- 1941, (With F. O. Bell), Nature of the intramolecular fold in a-keratin and a-myosin, Nature Lond., 147:696

- 1942, Textile fibres under the X-rays, Endeavour, 1:70. - 1943, (With K. Bailey and K. M. Rudall), Fibrinogen and fibrin

as members of the keratin-myosin group, Nature Lond., 151:716.

- 1945, Artificial protein fibres: their conception and preparation,

xii

Nature Lond., 155:501. - 1945, The forms of biological molecules. Essays on growth and

form, Oxford Univ. Press. - 1945, The structural properties of the cell, Biochem. J.,

39:1 VI. - 1946, Fibres and fabrics, old and new, Proc. Roy. Inst., 33:140. - 1946, Progress of X-ray analysis of organic and fibres structures,

Nature Lond., 157:121. - 1947, X-ray studies of nucleic acids, Symp. Soc. Exp. BioI.,

1:66. - 1949, The structure of biological tissues as revealed by X-ray

diffraction analysis and electron microscopy (Silvanus Thompson Memorial Lecture, 1948), Br. J. Radiol., 22:355.

- 1949, Structure of polyglycine, Nature LOnd., 163:722. - 1951, Adventures in molecular biology,(The Harvey Lecture, 1950),

Harvey Soc. Series, 46. - 1951, (With J. H. Kellgren, J. Ball, R. Reed, and E. Beighton),

Biophysical studies of rheumatoid connective tissue, Nature Lond., 168:493.

- 1952, (With R. E. Tunbridge, R. N. Tattersall, D. A. Hall, and R. Reed), The fibrous structure of normal and abnormal human skin, Clin. Sci., 11:315.

- 1953, The great adventure of fibre structure, (The Mather Lecture, 1952), J. Text. Inst., 44:81.

- 1958, Fundamentals of collagen, Dent. Pract., 8:261. - 1958, Fine-structural studies of the collagen-apatite partnership,

Lect. on Sci. Basis of Med., 8:429. - 1959, (With E. Beighton and K. D. Parker), The cross-S configura­

tion in super-contracted proteins, Biochem. Biophys. Acta, 35:17.

- 1961, Molecular biology or ultrastructural biology?, Nature Lond., 190:1124.

- 1961, The structure of the fibres of the colla.gen groups and related matters twenty-one years after, (9th Procter Memorial Lecture, 1960), J. Soc. Leather Trades' Chemists, 45:186.

Emmanuel Faure-Fremiet was born on December 29th, 1883. He was the older son of the composer Gabriel Faure and he spent much of his youth with the sculptor Emmanuel Fremiet, who was his maternal grand­father. In 1928, he succeeded his father-in-law, Louis-Felix Henne­guy, at the chair of Embryogenie Comparee (which became in 1955 the Laboratoire d'Embryologie Experimental, of the college de France). Emmanuel Faure-Fremiet occupied this chair until his retirement in 1955, and until his death, on November 5th, 1971, he continued in active research at the college de France, as "Professeur Honoraire" and in the CNRS laboratories at Gif-sur-Yvette.

xiii

Faure-Fremiet was a great naturalist, who liked to study animals in their environment, to describe and to classify them. He spent much time in marine laboratories, specially at Concarneau and Roscoff. Faure-Fremiet contributed to four principal areas in biology: cytology, developmental biology, physico-chemistry of fibrous proteins and ciliate protozoology, being a pioneer in each of these fields. In the beginning of the c.entury, he was interested in protozoan biology, studying contractile fibres, describing the presence of mitochondria for the first time. Moreover he emphasized the importance of cilia as the basic elements of many structures, and he stressed the common properties of ciliate infraciliature recognizing the unity of this group of protozoa. In the 50's, when he first worked with electron microscope, his studies on ultrastruc­tural biology were,once more, a great contribution. Protozoology has owned much to Faure-Fremiet efforts since he was interested in several aspects of this fields: systematics, evolution, phylogeny, experimental morphogenesis and ecology. As a developmental biologist, Faure-Fremiet studied the basis of cell motility, the mechanisms of cell recognition (in particular from dissociated sponge cells) and worked on the chemical transformations occurring at the time of fecondation in Ascaris. Faure-Fremiet was not only an experimentator, but a theorist, who conceived original hypotheses in the field of systematic protozoology and protein chemistry.

In the field of collagen, with his collaborators, Faure-Fremiet has done pioneering work in several areas during the 30's: properties of soluble collagen, X-ray study of collagen, structure of elastoidin, structure of fish connective tissue, structure of the protein of the dog-fish eggcase. He was one of the first to point out the similar­ities between the tissues of sponges and connective tissue of verte­brates.

The researches of Faure-Fremiet have always dealt with the general problem of differentiation, and they have been supported by original ideas and new methods. He produced considerable litera­ture: over 500 publications, most of them dealing with protozoology. Some of his publications, as his book "La Cinetique du Developpement" which appeared in 1925, bringing up innovative hypothesis, have had an appreciable influence in the field of embryology.

Emmanuel Faure-Fremiet was active in many biological societies, in France and abroad, and was elected to membership of the Academie des Sciences and many other prestigious academies in the world.

In addition to be a leader of science, Emmanuel Faure-Fremiet was a talentuous painter and sculptor and he has leaved the image of a man of great humility and sensitivity.

A selection of the most cited articles dealing with fibrous proteins:

xiv

- 1933, Quelque proprietes du collagene soluble, C. R. Soc. BioI., 113:715.

- 1936, La structure des fibres d'elastoidine, Arch. Anat. Microsc., 32:249.

- 1937, Etude roentgenographique d'une proteine intracellulaire, C. R. Soc. BioI., 204:1901.

- 1937, (With G. Champetier), Etude roentgenographique de la struc­ture des fibres d'elastoidine, J. Chim. Phys., 34:197.

- 1937, (With H. Garrault), Le tissu conjonctif aciculaire de la vessie natatoire, Arch. Anat. Microsc., 33:81.

- 1938, (With H. Garrault), Separation d'une prokeratine secretee par la glande nidamentaire de Raja batis L., Bull. Soc. Chim. BioI. Paris, 20:24.

- 1938, (With C. Baudovy), Sur l'ovokeratin des selaciens, Bull. Soc. Chim. BioI. Paris, 20:14.

- 1938, Etude roentgenographique des keratins secretees, C. R. Soc. BioI., 207:1133.

- 1938, Etude roentgenographique de quelques collagenes. J. Chim. Phys., 35:223.

- 1938, Structure du derme teliforme chez les Scombrides, Arch. Anat. Microsc., 34:219.

- 1938, Structure de la capsule ovulaire chez quelques selaciens, Arch. Anat. Microsc., 34:23.

- 1942, Etude roentgenographique de quelques corneines d'Anthozoaires, c. R. Soc. BioI., 215:94.

- 1944, (With H. Garrault), Proprietes physiques de l'Ascarocollagene, Bull. BioI., 78:206.

xv

CONTENTS

PART I: INTRODUCTION

Invertebrate Collagens in the Scheme of Things J. Gross

Collagen and Animal Phylogeny B. Baccetti

PART II: GENERAL DATA ON COLLAGEN BIOCHEMISTRY MOLECULAR ASSEMBLY AND INTERACTIONS

Collagen Families - Evolutionary Adaptations of Molecular and Macromolecular Structures to Physiological Functions • • • • • . • •

K. Kuhn and R. Timpl

The Different Types of Collagen Present in Cartilaginous Tissues . • . . .

S. Ricard-Blum and D. Herbage

Collagen Cross-Linking • M.L. Tanzer

Structure of Collagen Fibrils J. Galloway

Role of Collagenous and Non-Collagenous Components in Biological Calcification • • • • • • • •

E. Bonucci

Mediation of Cell Matrix Interactions by Collagen and Laminin Binding Cell Surface Proteins

J. Mollenhauer, U. Kunl, and K. von der Mark

29

49

53

65

73

83

95

xvii

Metazoan Mesenchyme Partitions the Extracellular Space during Matrix Morphogenesis • • • • •

D.E. Birk and R.L. Trelstad

Spatial Organization of Collagen Fibrils in Skeletal Tissues: Analogies with Liquid Crystals • • • • • • • • • • • •

Y. Bouligand and M.M. Giraud-Guille

Collagen Gene Structure • H. Boedtker and S. Aho

PART III: INVERTEBRATE AND LOWER VERTEBRATE COLLAGENS

PORIFERA

The Collagen of the Porifera R. Garrone

Sponge Gemmule Coats: Germanium Modification of a Collagenous Structure . . . • • • • • • •

T.L. Simpson, P.F. Langenbruch, and R. Garrone

Two Distinct Populations of Collagen Fibrils in a "Sclerosponge" • • • • • •.• • • •

J. Vacelet and R. Garrone

The Role of Sponge Collagens in the Diet of the Hawksbill Turtle (Eretmochelys imbricata)

A. Meylan

Colla&en of Coelenterates S. Franc

COELENTERATA

The Collagenous Component of Veretillum cynomorium (Cnidaria) ................ .

B. Senut and J.M. Franc

ACHELMINTHES

The Collagen of Aschelminthes • • • • • R. Ouazana

Ultrastructural Study of the Connective Tissues of Parascaris equorum • • . • • . • • • .

F. Cheli and L. Vitellaro-Zuccarello

xviii

103

115

135

157

177

183

191

197

211

217

237

ANNELIDA

The Collagens of the Annelida • L.W. Murray and M.L. Tanzer

The Interstitial Collagen of Lumbricus sp. (Annelida) ........... .

L. Vitellaro-Zuccarello, F. Cheli and G. Cetta

Long Pitch Helices in Invertebrate Collagens F. Gaill and Y. Bouligand

Similarity between Earthworm Cuticle Collagen and the Chemoattractant for Garter Snakes Solubilized from the Exterior Surface

243

259

267

of Earthworm.s . . . . . . . . . . . . . . . . . . . .. 275 D.~l. Kirschenbaum, P.T. Yao, N. Schulman,

and M. Halpern

The Collagen of the Mollusca A. Bairati

MOLLUSCA

The Role of Collagen in the Mechanical Design of Squid Mantle • • • • • • • • • • • •

R. Shacwick and J.M. Gosline

The Sclerotization of the Collagenous Byssal Threads of Mytilus edulis L. •••••

J.H. Waite

Ultrastructural and Biochemical Study on Collagen from the Neural Sheath of Sepia officinalis

S. De Biasi, F. Cheli and L. Vitellaro -Zuccarello

Comparative Ultrastructural Analysis on the Connective Tissue Organization of Neural Sheaths in Mollusca • • • • • • • • •

S. De Biasi, F. Cheli, and L. Vitellaro -Zuccarello

Quantitative Analysis on the Distribution of Collagen Fibril Diameters in the Neural Sheath of Sepia officinalis. • • • • •

G. Garino-Canina, S. De Biasi, and A. Bairati

277

299

305

309

317

325

xix

A Collagen Analogue System in Nucella lapillus (Prosobranchia, Stenoglossa) • • • • • • • • • • • • • • 331

L.J. Gathercole

Crosslinking and Chemical Characterization of Cephalopod Collagens • • • • • • • • • • • • • • • • 337

R.E. Shadwick

ARTHROPODA

The Collagen of the Arthropoda • • • • J. Francois

ECHINODERMATA

345

The Collagen of the Echinodermata A.J. Bailey

. • . . . • . • . • • 369

GRAPTOLITES

The Fine Structure of Graptolite Periderms D. Bates and N. Kirk

FISHES

389

The Interstitial Collagens of the Fishes • • • • • • • • • • • 397 S. Kimura

The Selachian Egg Case Collagen • • • • • • • • • • • • • • • 409 S. Hunt

Elas to idin •••••••••••••••••••••••• 435 J. Galloway

Comparative Fine Structure of the Actinotrichia (Elastoidin) in Developing Teleost and Dipnoi Fish Fins • • • • • • • • • • • • • • • • • • • • 451

J. Geraudie

Collagen and Mineralization in the Elasmoid Scales • • • • • • • • • ••• • • • • • • • • • • • 457

L. Zylberberg

The Deep Scleroblast of the Regenerating Teleost Scale: a Model of Cell Producing a Collagenic Plywood • • • • • • • • • • • • • • • • • • • • • • • • 465

J.Y. Sire

Nidamental Gland Secreting the Dog-Figh Egg-Shell •••••• 471 M. Rusaouen-Innocent

xx

PART IV: WORKSHOPS ON THE METHODOLOGICAL PROBLEMS IN THE ANALYSES OF INVERTEBRATE AND LOWER VERTEBRATE COLLAGENS

Methods of Extraction, Purification and Reprecipitation . • • • • • . • . . . • . . • . . • • • . 477

H.L. Tanzer

Collagen immunotyping . • • • . • • • . . • • • • • • • • • • • 487 J .A. Grimaud

The Banding Pattern of Collagen J.A. Chapman

• • . • • . . • . • • • • • • 515

Dielectric Spectroscopy in Collagen •••......••.. 539 M.F. Harmand, A. Lamure, N. Hitmi,

and G. Lacabanne

,/PART V: CONCLUSIONS

Evolution and Collagen M.B. Mathews

• • • • . • • . . • • 545

Concluding Remarks . • • • • • • . . • . • • • . . . . . . . . 561 J. Gross

Participants 565

Systematic Index 571

Subject Index • • • 575

xxi