Connective Tissue: Macromolecular Structure and Evolution

331 Pages·1975·7.807 MB·English

by  Professor Martin B. Mathews Ph. D. (auth.)

Molecular Biology
Biochemistry and Biophysics
19
Editors:
A. Kleinzeller, Philadelphia· G. F. Springer, Evanston
H. G. Wittmann, Berlin
Advisory Editors:
C. R. Cantor, New York· F. Cramer, Gottingen . F. Egami, Tokyo
M. Eigen, Gottingen . F. Gros, Paris· H. Gutfreund, Bristol
B. Hess, Dortmund· H. J ahrmiirker, Munich· R. W J eanloz, Boston
E. Katzir, Rehovot . B. Keil, Gif-sur-Yvette· M. Klingenberg, Munich
I. M. Klotz, Evanston· F. Lynen, M artinsried/ Munich
W T. J. Morgan, London· K. Muhlethaler, Zurich· S. Ochoa, New York
G. Palmer, Ann Arbor· I. Pecht, Rehovot . R. R. Porter, Oxford
W Reichardt, Tiibingen . H. Tuppy, Vienna
J. Waldenstrom, Malmo
Martin B. Mathews
Connective Tissue
Macromolecular Structure
and Evolution
With 31 Figures
Springer-Verlag Berlin· Heidelberg· New York 1975
Professor MARTIN B. MATHEWS, Ph. D.
The University of Chicago,
Department of Pediatrics,
5825 Maryland Avenue, Chicago, IL 60637/USA
ISBN-l3: 978-3-642-80906-4 e-ISBN-13: 978-3-642-80904-0
DOl: 10.1007/978-3-642-80904-0
This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned.
specifically those of translation. reprinting, re-use of illustrations, broadcasting, reproduction by photocopying
machine or similar means, and storage in data banks. Under § 54 of the German Copyright Law, where copies are
made for other than private use, a fee is payable to the publisher, the amount of the fee to be determined by agree-
ment with the publisher.© by Springer-Verlag Berlin Heidelberg 1975.
Softcover reprint of the hardcover 1st edition 1975
Library of congress cataloging in publication data. Mathews, Martin B. 1912-Connective tissue. (Molecular biology,
biochemistry, and biophysics; v. 19). Bibliography: p. Includes index. I. Connective tissues. I. Title. II. Series.
[DNLM: I. Connective tissue. 2. Macromolecular systems. W1M0195t no. 19/ QS532.C7 M429c] QMS63.M37.
596'.08'2. 74-28052.
The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific
statement, that such names are exempt from the relevant protective laws and regulations and therefore free for
general use.
Preface
This book deals primarily with the principal extracellular macromole
cules of animal connective tissues. It attempts to answer some general
questions about the biological organization of the tissues: What is
the nature of this organization at various dimensional levels? What
functions does the organization serve? How has it evolved?
I have given major emphasis to the structures and properties of the
macromolecular components of extracellular matrices from a wide range
of invertebrates and vertebrates. In doing so, however, I have treated
cursorily many important aspects of connective tissue biology that
appeared to be only indirectly relevant to the principal questions
asked. On the other hand, I have not hesitated to search for broad
biological principles outside the prevailing conceptual boundaries of
animal connective tissues and the lower molecular dimensional levels.
The numerous speculations presented will, I hope, stimulate the reader
to further thought and investigation.
Acknowledgements
My previously unpublished data that have been included in this volume
could not have been obtained without the generous gifts of specimens
and other assistance by a number of individuals and institutions. These
are Dr. G. BERENSON of Louisiana State University, Drs. W.P. BRAKER
and D. ZUMWALD of the Shedd Aquarium, Dr. S.H. CHUANG of the Univer
sity of Singapore, Dr. L.G. CLARK and Mr. U.M. VARELA-DIAZ of the
University of Pennsylvania, the Government of Nicaragua, Dr. E. CLARK
of Cape Haze Marine Laboratories, Mr. C.E. CUTRESS of the University
of Puerto Rico, Dr. DE FIEBRE of Wilson and Co., Dr. D. DOCKINS of
the Scripps Institute of Oceanography, Dr. J.H. HOWELL and Mr. T.
DURKIN of the United States Fish and Wildlife Service, Dr. A.M. FISHER
of Connaught Laboratories, Dr. R.B. GRINOLS of the University of
Washington, Dr. R.E. HALL of Wisconsin State Department of Agriculture,
Dr. W.O. HARTMAN of Yale University, Dr. E. HERALD of Steinhardt Aquar
ium, Dr. K. LIEM of the Field Museum, Profs. J. MILLOT and J. ANTHONY
of the Museum National D'Histoire Naturelle (Paris), Dr. T. MOHSEN of
the University of Dakar, Dr. P. PERSON of the Veterans Administration,
Dr. T. THORSON of the University of Nebraska, and Dr. A. WILSON of
Brandeis University. Financial support was received from the Chicago
Heart Association and from the United States Public Health Service
on grant nos. AM-05996 and HD-04583.
I am greatly indebted to many friends who read portions of the manu
script and freely offered advice and criticism. Drs. J.A. CIFONELLI,
A. DORFMAN, P. PERSON, L. RODEN,and A. VEIS detected my errors, con
tributed their own ideas and suffered my eccentricities of style. They
have done wonders in protecting the reader against the limitations of
VI
my ignorance and in correcting mistakes but, of course, are not re
sponsible for any that remain or for the views expressed. Numerous
colleagues generously furnished copies of their manuscripts prior to
publication. I am also grateful to Drs. S. SUZUKI and T. YAMAGATA of
Nagoya University for invaluable analytical data. The quoted fragments
by ANAXAGORAS are from translations by WHEELWRIGHT (1966).
Chicago, November 1974 MARTIN B. MATHEWS
Contents
Chapter 1 Introduction .•.•.•.•.•..•...•.••......•.....•......
1. General Considerations •.•..•...•.... .....••.••.. 1
2. Methodology .•...•..•.•..•.......••.....•........ 3
Chapter 2 The Tissues ..•.......••.•....•....•.....••....•...• 7
1. Principles •......•......•..•.•...••.......•..•.. 7
2. Molecular Unity and Di versi ty ...•........••..•.. 7
3. Morpho logy ...•.•........•............•.•...•.... 1 3
Chapter 3 Collagen....... • • . . . . . . . . • . • . . . . . . . . . • . . . . . . . . • • . • • 15
1. Identification •......•.•.•...•............•..... 15
2. Chemical Structure ........•...•••....•.......... 16
a) Primary and Direct-Coded Structure ...•....... 16
b) Secondary and Non-Coded Structure .•..•.•..... 18
i) Cross-Links............................... 18
ii) Aldehydes .•.•••...•..•.••.....•...•....... 21
iii) Hydroxyl Groups •.••..•.......•....•••...•• 21
i v) Carbohydrate Groups •.......•.•••...•••...• 21
v) Other Functional Groups •.•..•...••...•..•. 24
3. Aggregate Forms .•........•..........•...•.•..... 25
4 .. Stability ...•.....••••.....•.....•.•.•...••...•. 25
5. Comparative Biochemistry........................ 28
6. Invertebrate Collagen ....•....••.•.•..•.•••..... 29
a) Porifera .........•....•.•....••.•••••.•..••.. 29
b) Coelenterata ....•............................ 30
c) Platyhelminthes •.•••..•....•.....•.•......... 33
d) Annelida ...•....••.•..•....•......•....•..... 33
e) Aschelminthes .........•..•••...••...••....... 37
f) Arthropoda .•.••............••................ 38
g) Mollusca ...••...•....•..•....•.•..•.......•.. 38
h) Brachiopoda .............•..•...•.••......•.•• 39
i) Echinodermata .•..•.•......•..............•... 40
7. Deuterostomia •.•.....••.•....•........••...••..• 41
8. Chordata Acrania Collagen ..•.....•.....•....•..• 42
a) Urochordata (Tunicata) ..•...•......•••..•..•. 42
b) Cephalochordata ........•....••.•..•.•...•..•. 42
9. Chordata Craniata (Vertebrate) Collagen •..••.... 42
a) Cyclos toma ta ....•.•.•.•..•..•..•.•.•••.....•• 43
b) Chondrichthyes (Cartilage Fish) ••...•.•...... 43
i) Dermal Collagen ..•••...•.•....•.•..••••... 43
ii) Elastoidin .•.....•.....••..•.•..•...•...•• 44
iii) Ovokeratin ...•..•......•.••.•.•..•.•.••..• 45
i v) Cornea .••..•••.•....••.•.........••.....•. 45
c) Osteichthyes (Bony Fish) •.....•.••...•.•.•... 45
d) Reptilia and Amphibia ••.....•.•......••..•... 46
e) Aves .....••.......•...............•.......•.. 46
VIII
f) Mammalia .................................... 49
10. Basement Membranes and Vitrosin ................ 52
11. Biosynthesis ................................... 54
a) Polypeptide Synthesis ....................... 54
b) Hydroxylation ............................... 55
c) Glycosylation ............................... 56
d) Aldehyde Formation .......................... 56
1 2. Immuno logy ..................................... 57
13. Evolution ...•.................................. 58
a) General Considerations ...................... 58
b) Variation in Thermal Stability.............. 58
i) Correlation with Composition ......... .... 58
ii) Correlation with Environmental Temperature 62
iii) Biological Significance .................. 63
c) Fossils ..................................... 65
d) Origins and Remote Ancestry................. 66
e) Molecular Phylogeny......................... 69
i) Amino Acid Composition ................... 72
ii) Amino Acid Sequence ...................... 76
iii) Secondary Chemical Structure ............. 77
14. Development and Aging .......................... 77
Chapter 4 Elastin......................... . . . . . . . . . . . . . . . . . . . 79
1. Identification ................................. 79
2. Primary Structure .............................. 79
3. Secondary Chemical Features .................... 81
a) Cross-Links ................................. 81
b) Aldehydes ...................•............... 82
c) Hydroxylation •.............................. 82
4. Fibril Organization ................... ......... 82
5. Comparative Biology............................ 84
Chapter 5 Structural Glycoproteins 86
1. Characterization ............................... 86
a) Def ini tion .................................. 86
b) Structure ................................... 87
c) Biosynthesis ................................ 88
d) Immunology .........•........................ 88
e) Biological Function ......................... 88
2. Invertebrate ............•...................... 88
3. Vertebrate ...........•.....•................... 89
a) Aorta ....................................... 89
b) Ligament and Tendon •........................ 89
c) Skin ...•.................................... 89
d) Cartilage ................................... 91
e) Bone, Enamel, and Dentin .................... 91
f) Cornea .........................•............ 91
g) Brain ....................................... 91
h) Other Sources ............................... 92
4. Conclusions ......................•............. 92
Chapter 6 Polyanionic Proteoglycans ..... .•.•......•........•. 93
1. Characterization as Parent Types ............... 94
a) Glycosaminoglycans .......................... 94
i) Hyaluronate .............................. 97
IX
ii) Chondroitin 4-Sulfate, Chondroitin 6-Sulfate 97
iii) Dermatan Sulfate (Chondroitin Sulfate B) .. 98
iv) Keratan Sulfate .••..•.•..••.....•.•...•... 99
v) Heparan Sulfate •.....••....•....•....•.•.. 99
vi) Heparin .••.•.•..•.....•••..•.••••.......•. 100
b) Proteoglycosaminoglycan of Cartilage and Noto-
chord .•....•.••....•.............••.••....... 100
i) Parent Type .••...•......••....•••.•.....•. 100
ii) Relationship to Skeletal Keratan Sulfate •. 103
iii) Aggregates •....•......••..••.............. 103
c) Other Proteoglycosaminoglycans •.............. 104
i) Skeletal Keratan Sulfate ..........•.••.... 104
ii) Corneal Keratan Sulfate .........•..•••.... 105
iii) Dermatan Sulfate ....•..••.••.•.........•.• 105
iv) Hyaluronate .••.......•..............•..... 105
v) Heparan Sulfate ..••................••..... 105
vi) Heparin ..•.......•.................••....• 105
2. Structure of the Linkage Region •.........•••.... 106
a) Proteoglycans of Chondroitin Sulfate Type ..•• 106
i) Vertebrates ...•....•...•..••.•........•••• 106
ii) Inverteb~ates ••....••••...••••............ 107
b) Proteoglycans of Other Types .•............... 108
i) Dermatan Sulfate ••.............•..•.••...• 108
ii) Corneal Keratan Sulfate ..................• 108
iii) Skeletal Keratan Sulfate ...••............. 108
iv) Hyaluronate ..••......................•.... 109
v) Heparin ........•...•........••.........•.• 109
vi) Heparan Sulfate ....•......•.........•••... 109
3. Comparative Macromolecular Structures of Proteo-
glycans •••...•.•..•...•.•....••......••......•.. 109
a) Cyclostomes .........•.......•.......••......• 110
b) Chondrichthyes ..........•....•.•............. 110
c) Osteichthyes ...•...•.••.........•....•••..•.. 111
d) Amphibia .......••...........................• 111
e) Reptiles .....•.••...•...............•••....•• 111
f) Birds ..........••.....•.........•.....••.•... 111
g) Mammals ...............................•...•.• 111
h) Invertebrates •.•.•.•••.....•••.....••.....••• 115
4. Biosynthesis •......••.....•••................... 115
a) Precursors .•..•...•...•.....•...•.••...•..•.. 116
i) Vertebrates ...............•.....•......... 116
ii) Invertebrates ......•.............•••...... 116
b) Assembly of Biosynthetic Units in Vertebrates 116
i) Chondroitin Sulfate Type ............•..... 117
ii) Dermatan Sulfate Type .•....•••.....•..•... 118
iii) Heparin and Heparan Sulfate Types •..•..•.. 118
iv) Keratan Sulfate Types .....•......•......•• 119
v) Hyaluronic Acid .•..•...............•••.... 119
c) Assembly of Biosynthetic Units in Inverte-
brates ....................................... '19
d) Regulation of Biosynthesis •..•.•••..•....•••• 119
5. Immunology ....•••...................••..•...•••. 120
6. Evolutionary Relationships ....•.••....•......... 122
a) Proteoglycans of Cartilage and Notochord •...• 122
i) Macromolecular Architecture ..•.•.••..•.... 122
ii) Polypeptide Structure ••••••••••••••••...•• 122
iii) Glycan Structure .•........•...........•••. 123
b) Other Proteoglycans •........••..•.......••..• 123
c) Perspectives ........•..•..•••.........•.•.•.. 123
x
Chapter 7 Polyanionic Glycans of Cartilage, Bone and Notochord 126
1. Biological Significance .•..•..•...•..•.•.•..•.•. 126
a) Carti lage and Bone .•••••••.•••...•••...••.••• 126
b) Notochord .•..•••••.•..••••...•.•.•.•.•....••. 128
c) Taxonomic Interpretation •..•.......•......... 128
2. Invertebrates .••.•...••••....•.•...•••.••.•...•. 129
a) Annelida ...•..•.•....•......•.......•.....•.. 132
b) Mollusca •..•••......•••........•............. 133
i) Gastropod Odontophore Cartilage ••.••...•.. 133
ii) Cephalopod Cartilage ...•.....•....•......• 135
c) Arthropoda ..........•........•.•.•.•...•..•.. 1 36
d) Evolution ••.....•.••••..•...•.....••......... 136
3. Lower Deuterostomia •.•...•...•.•.............•.. 138
4. Vertebrates..................................... 139
a) Cyclostomata ....•....•••.•••••.•...•...•.•..• 139
i) Hagfish................................... 140
ii) Lamprey •.•.•.•.......••.•.......•..•.•.... 140
b) Chondrichthyes •...••••.•...•.•..•••••.•.•••.• 141
i) Ratfish (Holocephali) .•......•.•.......... 141
ii) Sharks (Pleurotremata) of Marine Habitat .. 142
iii) Rays and Skates (Hypotremata) of Marine
Habitat •.•..••••••..••...••....•...••..... 142
iv) Marine Sharks of Fresh Water •.•..•.•..••.. 143
v) Rays of Freshwater Habitat ..•.•..•.•...•.. 144
vi) Conclusions •.••......•..•.•...••••••.•.... 145
c) Osteichthyes................................. 146
i) Actinopterygii ......•...........•..•...... 146
i i ) Di pno i •.....•.•.......•.•..........•••..•. 1 4 7
iii) Crossopterygii .....•..........•........... 147
d) Tetrapoda .....•.••..........................• 150
i) Amphibia •.•.•....................•...•.... 1 50
ii) Reptilia .•..•.••......•..........•........ 152
iii) Aves ••...••....••....•.•••..••••••.•••••.• 152
iv) Mammalia .•...•••.•.•..•.•...•............. 152
5. Calcified Cartilage, Bone and Teeth ..........•.. 152
6. Discussion ......•.....•..............••..•...... 154
Chapter 8 Polyanionic Glycans in Development and Aging of
Vertebrate Cartilage ....•....•.....•.•....•..•.•... 156
1. General Considerations .••...•.•..............•.. 156
2. Lower Vertebrates .••..•..•.•.......•.......•.•.. 158
3. Amphibia .••.......•....••.••.•..•......•..••••.. 158
4. Birds •••....•.••.•..•••••.•.•.•...•...••.•.....• 159
5. Mammals ........•.•..•.••..•.•.....•......•.•.•.. 161
a) Rat ...........•........•.....•...•...••.•..•• 161
b) Hog .•.•.••.••...•...•.•...•••..•••.•••.•••.•• 1 62
c) Rabbit ...•..•..•......••...••••.............. 162
d) Ox ..........•.......•......•.....•.....••••.. 1 62
e) Man .•......••.........•••..•....•.•..•.•....• 1 64
i) Histochemical Studies ..•••.•.•.••.•••..... 164
ii) Chemical Studies ..•.........••...••.•..••. 164
6. Discussion .•.......••..•....•.......••...•.•...• 167
a) Functional Roles of Proteoglycans .......•.•.. 167
b) Embryonic Development and Maturation .....•... 167
c) Aging .•..•.••..•...•..•.•..•.••....•.......•. 169
XI
Chapter 9 Polyanionic Glycans of Other Tissues ...••...•.••.• 172
1. Introduction •.•..••.......•.•..••....•..•..••.. 172
2. Invertebrates •..•••.•....••.•.......••......••• 172
a) Protista ...•••••••...........••..•........•• 172
b) Porifera ..•..•.•••......•••...••.•.•..•.•..• 173
c) Coelenterata ..•.........••..•...•.•.••..•..• 174
d) Annelida ....•..••.....•.•.•....•.••.•....••• 175
e) Arthropoda .••.•...•••.•......•.••.......••.• 1 75
f) Mollusca ...........•........••.............. 176
i) Mucins .................•.•.....•...•••... 176
ii) Glycans of Shell and Mantle ..•••••....••. 177
iii) Mactin and Spisulan •••.....•••••......••. 177
iv) Glycans of Cephalopod Eye and Skin .....•. 178
g) Brachiopoda ......•.......•••.•......•••••... 180
h) Echinodermata .•••••.•.•••.•....••...•••...•. 181
3. Chordata Acrania •.•..••.••.......••••.......•.• 182
a) Urochordata (Tunicata) ........•••...•....••• 182
b) Cephalochordata .•.........••••.•............ 182
4. Chordata Craniata (Vertebrata) •••..•.•.•••••... 182
a) Skin •••..........•..•.....••••.....•.••••..• 183
i) Cyclostomes •••••..•••......•••••......•.. 183
ii) Chondrichthyes ..••.••.......••.••..•..••• 184
iii) Osteichthyes •..•••.......•...•.•.....••.. 184
iv) Amphibia •....•.......•••••..•.....•.••... 185
v) Aves ...•••.••••....••••....•.•••••••.•••. 187
vi) Mammalia................................. 188
b) Cornea ...•.•.•..•..••••........•....•....•.. 189
i) Chondrichthyes •.......•.•••...•••••••••.. 190
ii) Osteichthyes ...••.•••............•..•.... 190
iii) Reptilia •..•..••.•.••.................•.. 190
iv) Aves .......•.•......•••••.•..•.•.••.•..•• 190
v) Mammalia •••.••..•.•.•...••..•••.•.....•.. 191
c) Vitreous and Other Tissues of the Eye ...•... 192
i) Vitreous................................. 192
ii) Other Tissues of the Eye .............•... 192
d) Blood Vessels ..••.•.•.......•......•••••.•.. 193
i) Man •.•.•.....•..•.•...•••••......•••..... 195
ii) Other Vertebrates........................ 195
e) Intervertebral Disc ••••••••••••••••••••••••• 195
f) Eggs and their Matrices .••••.••.•..••...••.• 195
i) Teleosts •......••..•.•.•••••..••••••.••.. 195
ii) Amphibia .•.•...•.•.•..•..•....••••...•..• 196
iii) Birds •.••••..•.•••••..•.•••......•••••.•• 196
iv) Mammals •..•••.•.•.........•....•••.••.•.. 197
g) Neural Tissues •••••••........•..•..••••.•... 197
h) Electroreceptors and Electric Organs ••.••... 199
i) Electroreceptors ...•••.•...•...........•. 199
ii) Electric Organs •••••••..••.•••..........• 200
i) Cells that Store Glycosaminoglycans ••••.••.• 201
i) Leukocytes •••..••••........•...•••••••.•• 201
ii) Kurloff Cells .•..••••.............••••.•. 201
iii) Mast Cells ..........•••••...•••....•..•.. 201
j) Tumors .•••.•...••••.••....•..•...•.•••••.••• 202
k) Some Other Sources •..•••....••..•.••...••... 202
i) Body Fluids .......•.......•..•••••...••.• 202
ii) Kidney ••••••••.•.••....•......•••••.••••• 202
iii) Liver •.••••...•.•.•...•••••..••.••••••.•• 202
iv) Umbilical Chord (Human) ...•.•......•••.•. 203
v) Placenta •••••••••••....•.•.•..•.•.••••... 203
vi) Tendon ....•.............................. 203