Skip to main content

Growth and development of collagen fibrils in connective tissue

  • Chapter

Part of the book series: Electron Microscopy in Biology and Medicine ((EMBM,volume 3))

Abstract

The form and integrity of the animal body is largely dependent upon the composition and spatial arrangement of the structural composite known as connective tissue. Each member of this complex family of tissues contains the same building blocks — collagen, glycosaminoglycans, glycoproteins, elastic fibres, cellular constituents, water and minerals — but they are assembled in a multitude of different ways. Ultimately, the interactions of these components with one another bestow the appropriate mechanical attributes upon the tissue.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Parry DAD, Craig AS: The molecular structure of collagen. In: The Chemistry and Biology of Mineralized Connective Tissue. Veis A (ed), Amsterdam, Elsevier/North Holland, 1981, pp 63–67.

    Google Scholar 

  2. Fraser RDB, MacRae TP, Suzuki E: Chain conformation in the collagen molecule. J Mol Biol 129: 463–481, 1979.

    Article  PubMed  CAS  Google Scholar 

  3. Chapman JA, Hulmes DJS: Electron microscopy of the collagen fibril. In: Ultrastructure of the Connective Tissue Matrix. Ruggeri A, Motta PM (eds), The Hague, Martinus Nijhoff, 1984, pp. 1–33.

    Chapter  Google Scholar 

  4. Parry DAD, Craig AS: Quantitative electron microscope observations of the collagen fibrils in rat-tail tendon. Biopolymers 16: 1015–1031, 1977.

    Article  PubMed  CAS  Google Scholar 

  5. Parry DAD, Craig AS, Barnes GRG: Tendon and ligament from the horse: an ultrastructural study of collagen fibrils and elastic fibres as a function of age. Proc R Soc Lond [Biol] 203: 293–303, 1978.

    Article  CAS  Google Scholar 

  6. Eikenberry EF, Brodsky B, Parry DAD: Collagen fibril morphology in developing chick metatarsal tendon. I/1 X-ray diffraction studies. Int J Biol Macromol 4: 322–328, 1982.

    Article  CAS  Google Scholar 

  7. Eikenberry EF, Brodsky B, Craig AS, Parry DAD: Collagen fibril morphology in developing chick metatarsal tendon. II/2 Electron microscope studies. Int J Biol Macromol 4: 393–398, 1982.

    Article  CAS  Google Scholar 

  8. Craig AS, Parry DAD: Collagen fibrils of the vertebrate corneal stroma. J Ultrastruct Res 74: 232–239, 1981.

    Article  PubMed  CAS  Google Scholar 

  9. Jakus MA: The fine structure of human cornea. In: The Structure of the Eye. Smelser GK (ed), New York, Academic Press, 1961, pp 343–366.

    Google Scholar 

  10. Cox JL, Farrell RA, Hart RW, Langham ME: The transparency of the mammalian cornea: J Physiol 210: 601–616, 1970.

    PubMed  CAS  Google Scholar 

  11. Jackson SF: The morphogenesis of avian tendon. Proc R Soc Lond [Biol] 144: 556–572, 1956.

    Article  CAS  Google Scholar 

  12. Dyer RF, Enna CD: Ultrastructural features of adult human tendon. Cell Tissue Res 168: 247–259, 1976.

    Article  PubMed  CAS  Google Scholar 

  13. Schwarz W: Morphology and differentiation of the connective tissue fibres. In: Connective Tissue. Tunbridge RE, Keech M, Delafresnaye JF, Wood GC (eds), Oxford, Blackwell, 1957, pp 144–155.

    Google Scholar 

  14. Parry DAD, Craig AS: Collagen fibrils and elastic fibres in rat-tail tendon: an electron microscopic investigation. Biopolymers 17: 843–855, 1978.

    Article  PubMed  CAS  Google Scholar 

  15. Parry DAD, Craig AS, Barnes GRG: Fibrillar collagen in connective tissue. In: Fibrous Proteins: Scientific, Industrial and Medical Aspects. Parry DAD, Creamer LK (eds), London, Academic Press, 1980, 2, pp 77–88.

    Google Scholar 

  16. Craig AS, Parry DAD: Growth and development of collagen fibrils in immature tissues from rat and sheep. Proc R Soc Lond [Biol] 212: 85–92, 1981.

    Article  CAS  Google Scholar 

  17. Tajima S, Nagai Y: Distribution of macromolecular components in calf dermal connective tissue. Connect Tissue Res 7: 65–71, 1980.

    Article  PubMed  CAS  Google Scholar 

  18. Wainwright SA, Biggs WD, Currey JD, Gosline JM: Mechanical Design in Organisms. London, Edward Arnold, 1976.

    Google Scholar 

  19. Harkness RD: Mechanical properties of connective tisssue in relation to function. In: Fibrous Proteins: Scientific, Industrial and Medical Aspects. Parry DAD, Creamer LK (eds), London, Academic Press, 1979, 1, pp 207–230.

    Google Scholar 

  20. Wainwright SA, Vosbrugh F, Hebrank JH. Shark skin: function in locomotion. Science 202: 747–749, 1978.

    Article  PubMed  CAS  Google Scholar 

  21. Parry DAD, Barnes GRG, Craig AS: A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relationship between fibril size distribution and mechanical properties. Proc R Soc. Lond [Biol] 203: 305–321, 1978.

    Article  CAS  Google Scholar 

  22. Parry DAD, Barnes GRG, Craig AS: A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relationship between fibril size distribution and mechanical properties. Proc R Soc. Lond [Biol] 203: 305–321, 1978.

    Article  CAS  Google Scholar 

  23. Muir H, Bullough P, Maroudas A: The distribution of collagen in human articular cartilage with some of its physiological implications. J Bone Joint Surg 52: 554–563, 1970.

    CAS  Google Scholar 

  24. Aspden RM, Hukins DWL: Collagen organization in articular cartilage, determined by X-ray diffraction, and its relationship to tissue function. Proc R Soc Lond [Biol] 212: 299–304, 1981.

    Article  CAS  Google Scholar 

  25. Dahmen G: Polarizing and electronmicroscopic investigations of maturing and old human articular cartilage. In: Connective Tissue and Ageing. Vogel HG (ed), Amsterdam, Excerpta Medica, 1973, pp 109–113.

    Google Scholar 

  26. Maroudas A, Muir H: The distribution of collagen and glycosaminoglycans in human articular cartilage and the influence on hydraulic permeability. In: Chemistry and Molecular Biology of the Intercellular Matrix. Balazs EA (ed), London, Balazs EA (ed), 1970, 3, pp 1381–1401.

    Google Scholar 

  27. Happey F, Naylor A, Palframan J, Pearson CH, Render RM, Turner RL: Variations in the diameter of collagen fibrils, bound hexose and associated glycoproteins in the intervertebral disc. In: Connective Tissues, Biochemistry and Pathophysiology. Fricke R, Hartmann F (eds), New York, Springer-Verlag, 1974, pp 67–70.

    Chapter  Google Scholar 

  28. Dahmen G: Submikroskopische Untersuchungen an Wirbelbandscheiben. Z Rheumaforsch 22: 192–213, 1963.

    PubMed  CAS  Google Scholar 

  29. Berthet C, Hulmes DJS, Miller A, Timmins PA: Structure of collagen in cartilage of invertebral disk. Science 199: 547–549, 1978.

    Article  PubMed  CAS  Google Scholar 

  30. Szirmai JA: Structure of the invertebral disc. In: Chemistry and Molecular Biology of the Intercellular Matrix. Balazs EA (ed), London, Balazs EA (ed), 1970, 3, pp 1279–1308.

    Google Scholar 

  31. Glimcher M, Krane SM: The organization and structure of bone and the mechanism of calcification. In: Treatise on Collagen, Vol 2, Pt B. Gould BS (ed), London, Academic Press, 1968, pp 67–251.

    Google Scholar 

  32. White SW, Hulmes DJS, Miller A, Timmins PA: Collagen-mineral axial relationship in calcified turkey leg tendon by X-ray and neutron diffraction. Nature (Lond) 266: 421–425, 1977.

    Article  CAS  Google Scholar 

  33. Robinson RA, Watson ML: Crystal-collagen relationships in bone as observed in the electron microscope. III. Crystal and collagen morphology as a function of age. Ann NY Acad Sci 60: 596–628, 1955.

    Article  PubMed  CAS  Google Scholar 

  34. Jackson SF: The fine structure of developing bone in the embryonic fowl. Proc R Soc Lond [Biol] 146: 270–280, 1957.

    Article  Google Scholar 

  35. Weinstock M, Leblond CP: Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after [3H] proline administration. J Cell Biol 60: 92–127, 1974.

    Article  PubMed  CAS  Google Scholar 

  36. Watson ML, Avery JK: The development of the hamster lower incisor as observed by electron microscopy. Am J Anat 95: 109–161, 1954.

    Article  PubMed  CAS  Google Scholar 

  37. Ross R: The connective tissue fiber forming cell. In: Treatise on Collagen, Vol 2, Pt A. Gould BS (ed), London, Academic Press, 1968, pp 1–82.

    Google Scholar 

  38. Bellairs R, Harkness MLR, Harkness RD: The structure of the tape-turn of the eye of the sheep. Cell Tissue Res 157: 73–91, 1975.

    Article  PubMed  CAS  Google Scholar 

  39. Gross J, Matoltsy AG, Cohen C: Vitrosin: a member of the collagen class. J Biophys Biochem Cytol 1: 215–220, 1955.

    Article  PubMed  CAS  Google Scholar 

  40. Gross J, Sokal Z, Rougvie M: Structural and chemical studies on the connective tissue of marine sponges. J Histochem Cytochem 4: 227–246, 1956.

    Article  PubMed  CAS  Google Scholar 

  41. Cusack S, Miller A: Determination of the elastic constants of collagen by Brillouin light scattering. J Mol Biol 135: 39–51, 1979.

    Article  PubMed  CAS  Google Scholar 

  42. Vogel HG: Strain of rat skin at constant load (creep experiments): influence of age and desmotropic agents. Gerontology 23: 77–86, 1976.

    Article  Google Scholar 

  43. Vogel HG: Influence of maturation and age on mechanical and biochemical parameters of connective tissue of various organs in the rat. Connect Tissue Res 6: 161–166, 1978.

    Article  PubMed  CAS  Google Scholar 

  44. Light ND, Bailey AJ: Covalent crosslinks in collagen. Characterization and relationships to connective tissue disorders. In: Fibrous Proteins: Scientific, Industrial and Medical Aspects. Parry DAD, Creamer LK (eds), London, Creamer LK (eds), 1979, 1, pp 151–177.

    Google Scholar 

  45. Torp S, Arridge RGC, Armeniades CD, Baer E: Structure-property relationships in tendon as a function of age. In: Structure of Fibrous Biopolymers, Colston Papers No. 26. Atkins EDT, Keller A (eds), London, Butterworths, 1975, pp 197–221.

    Google Scholar 

  46. Vogel HG: Influence of maturation and aging on mechanical and biochemical parameters of rat bone. Gerontology 25: 16–23, 1979.

    Article  PubMed  CAS  Google Scholar 

  47. Flint MH, Gillard GC, Merrilees MJ: The effects of local physical environmental factors on connective tissue organization and glycosaminoglycan synthesis. In: Fibrous Proteins: Scientific, Industrial and Medical Aspects. Parry DAD, Creamer LK (eds), London, Creamer LK (eds), 1980, 2, pp 107–119.

    Google Scholar 

  48. Craig AS, Parry DAD: The sub-structure of collagen fibrils. In: The Chemistry and Biology of Mineralized Connective Tissue. Veis A (ed), Amsterdam, Elsevier/North Holland, 1981, pp 107–112.

    Google Scholar 

  49. Lillie JH, MacCallum DK, Scaletta LJ, Occhino JC: Collagen structure: evidence for a helical organization of the collagen fibril. J Ultrastruct Res 58: 134–143, 1977.

    Article  CAS  Google Scholar 

  50. Ruggeri A, Benazzo F, Reale E: Collagen fibrils with straight and helicoidal microfibrils: a freeze-fracture and thin-section study. J Ultrastruct Res 68: 101–108, 1979.

    Article  PubMed  CAS  Google Scholar 

  51. Bouteille M, Pease DC: The tridimensional structure of native col-lagenous fibrils, their proteinaceous filaments. J Ultrastruct Res 35: 314–338, 1971.

    Article  PubMed  CAS  Google Scholar 

  52. Knight DP, Hunt S: Fibril structure of collagen in egg capsule of dogfish. Nature (Lond) 249: 379–380, 1974.

    Article  CAS  Google Scholar 

  53. Hulmes DJS, Jesior JC, Miller A, Berthet-Colominas C, Wolff C: Electron microscopy shows periodic structure in collagen fibril cross sections. Proc Natl Acad Sci USA 78: 3567–3571, 1981.

    Article  PubMed  CAS  Google Scholar 

  54. Squire JM, Freundlich A: Direct observation of a transverse periodicity in collagen fibrils. Nature (Lond) 288: 410–413, 1980.

    Article  CAS  Google Scholar 

  55. Rayns DG: Collagen from frozen fractured glycerinated beef heart. J Ultrastruct Res 48: 59–66, 1974.

    Article  PubMed  CAS  Google Scholar 

  56. Reale E, Benazzo F, Ruggeri A: Differences in the microfibrillar arrangement of collagen fibrils. Distribution and possible significance. J. Submicro Cytol 13: 135–143, 1981.

    CAS  Google Scholar 

  57. Stolinski C, Breathnach AS: Freeze-fracture replication and surface sublimation of frozen collagen fibrils. J Cell Sci 23: 325–334, 1977.

    PubMed  CAS  Google Scholar 

  58. Reed R: Freeze-etched connective tissue. Int Rev Connect Tissue Res 6: 257–305, 1973.

    PubMed  CAS  Google Scholar 

  59. Breathnach AS: Application of the freeze-fracture technique to investigative dermatology. Br J Dermatol 88: 563–574, 1973.

    Article  PubMed  CAS  Google Scholar 

  60. Parry DAD, Craig AS: Electron microscope evidence for an 80Å unit in collagen fibrils. Nature (Lond) 282: 213–215, 1979.

    Article  CAS  Google Scholar 

  61. Parry DAD, Craig AS: An 80Å unit in collagen fibrils. In: Structural Aspects of Recognition and Assembly in Biological Macromolecules. Balaban M, Sussman JL, Traub W, Yonath A (eds), Boston, Yonath A (eds), 1981, 1, pp 377–386.

    Google Scholar 

  62. Doyle BB, Hukins DWL, Hulmes DJS, Miller A, Woodhead-Gallo-way J: Collagen polymorphism: its origins in the amino acid sequence. J Mol Biol 91: 79–99, 1975.

    Article  PubMed  CAS  Google Scholar 

  63. Doyle BB, Hulmes DJS, Miller A, Parry DAD, Piez KA, Woodhead-Galloway J: A D-period narrow filament in collagen. Proc R Soc Lond [Biol] 186: 67–74, 1974.

    Article  CAS  Google Scholar 

  64. Miller A, Wray JS: Molecular packing in collagen. Nature (Lond) 230: 437–439, 1971.

    Article  CAS  Google Scholar 

  65. Miller A, Parry DAD: Structure and packing of microfibrils in collagen. J Mol Biol 75: 441–447, 1973.

    Article  PubMed  CAS  Google Scholar 

  66. Fraser RDB, Miller A, Parry DAD: Packing of microfibrils in collagen. J Mol Biol 83: 281–283, 1974.

    Article  PubMed  CAS  Google Scholar 

  67. Miller A: Molecular packing in collagen fibrils. In: Biochemistry of collagen. Ramachandran GN, Reddi AH (eds), New York, Plenum Press, 1976, pp 85–136.

    Google Scholar 

  68. Brodsky B, Eikenberry EF: Characterization of fibrous forms of collagen. In: Methods in Enzymology ‘Structural and Contractile Proteins,’ Vol 82. Cunningham LW, Frederiksen DW (eds), New York, Academic Press, 1982, pp 127–174.

    Chapter  Google Scholar 

  69. Fraser RDB, MacRae TP: The crystalline structure of collagen fibrils in tendon. J Mol Biol 127: 129–133, 1979.

    Article  PubMed  CAS  Google Scholar 

  70. Fraser RDB, MacRae TP: Unit cell and molecular connectivity in tendon collagen. Int J Biol Macromol 3: 193–200, 1981.

    Article  CAS  Google Scholar 

  71. Hulmes DJS, Miller A: Quasi-hexagonal molecular packing in collagen fibrils. Nature (Lond) 282: 878–880, 1979.

    Article  CAS  Google Scholar 

  72. Smith JW: Molecular pattern in native collagen. Nature (Lond) 219: 157–158, 1968.

    Article  CAS  Google Scholar 

  73. Miller A, Tocchetti D: Calculated X-ray diffraction pattern from a quasi-hexagonal model for the molecular arrangement in collagen. Int J Biol Macromol 3: 9–18, 1981.

    Article  CAS  Google Scholar 

  74. Trus BL, Piez KA: Compressed microfibril models of the native collagen fibril. Nature (Lond) 286: 300–301, 1980.

    Article  CAS  Google Scholar 

  75. Piez KA, Trus BL: A new model for packing of type I collagen molecules in the native fibril. Biosci Rep 1: 801–810, 1981.

    Article  PubMed  CAS  Google Scholar 

  76. Brodsky B, Eikenberry EF, Cassidy K: An unusual collagen periodicity in skin. Biochim Biophys Acta 621: 162–166, 1980.

    PubMed  CAS  Google Scholar 

  77. Squire JM, Freundlich A: Molecular packing in collagen. Nature (Lond) 293: 240, 1981.

    Article  Google Scholar 

  78. Fraser RDB, MacRae TP, Suzuki E, Tulloch PA: Ordered assemblies in fibrous proteins. In: Structural aspects of recognition and assembly in biological macromolecules. Balaban M, Sussman JL, Traub W, Yonath A (eds), Boston, International Science Services, 1981, 1, pp 327–340.

    Google Scholar 

  79. Fjolstad M, Helle O: A hereditary dysplasia of collagen tissues in sheep. J Pathol 112: 183–188, 1974.

    Article  PubMed  CAS  Google Scholar 

  80. Cahill JI, Jones BR, Barnes GRG, Craig AS: A collagen dysplasia in a greyhound bitch. NZ Vet J 28: 203–204; 213, 1980.

    Google Scholar 

  81. Belton JC, Crise N, McLaughlin RF, Tueller EE: Ultrastructural alterations in collagen associated with microscopic foci of human emphysema. Hum Pathol 8: 669–677, 1977.

    Article  PubMed  CAS  Google Scholar 

  82. Menton DN, Hess RA: The ultrastructure of collagen in the dermis of tight-skin (Tsk) mutant mice. J Invest Dermatol 74: 139–147, 1980.

    Article  PubMed  CAS  Google Scholar 

  83. Uitto J, Santa Cruz DJ, Starcher BC, Whyte MP, Murphy WA: Biochemical and ultrastructural demonstration of elastin accumulation in the skin lesions of the Buschke-Ollendorff Syndrome. J Invest Dermatol 76: 284–287, 1981.

    Article  PubMed  CAS  Google Scholar 

  84. Vogel A, Holbrook KA, Steinmann B, Gitzelmann R, Byers PH: Abnormal collagen fibril structure in the gravis form (type I) of Ehlers-Danlos Syndrome. Lab Invest 40: 201–206, 1979.

    PubMed  CAS  Google Scholar 

  85. Dlugosz J, Gathercole LJ, Keller A: Cholesteric analogue packing of collagen fibrils in the cuvierian tubules of Holothuria forskali (Holo-thuroidea, Echinodermata). Micron 10: 81–87, 1979.

    Google Scholar 

  86. Bailey AJ, Gathercole LJ, Dlugosz J, Keller A, Voyle CA: Proposed resolution of the paradox of extensive cross-linking and low tensile strength of cuvierian tubule collagen from the sea cucumber Holothuria forskali. 4: 329–334, 1982.

    CAS  Google Scholar 

  87. Witschel H, Fine BS, Grutzner P, McTigue JW: Congenital hereditary stromal dystrophy of the cornea. Arch Opthalmol 96: 1043–1051, 1978.

    Article  CAS  Google Scholar 

  88. Jakus MA: Further observations on the fine structure of the cornea. Invest Opthalmol 1: 202–225, 1962.

    CAS  Google Scholar 

  89. Black CM, Gathercole LJ, Bailey AJ, Beighton P: The Ehlers-Danlos Syndrome: an analysis of the structure of the collagen fibres of the skin. Br J Dermatol 102: 85–96, 1980.

    Article  PubMed  CAS  Google Scholar 

  90. Holbrook KA, Byers PH; Ultrastructural characteristics of the skin in a form of the Ehlers-Danlos Syndrome type IV. Lab Invest 44: 342–350, 1981.

    PubMed  CAS  Google Scholar 

  91. Parry DAD, Flint MH, Gillard GC, Craig AS: A role for glycos-aminoglycans in the development of collagen fibrils. FEBS Lett 149: 1–7, 1982.

    Article  PubMed  CAS  Google Scholar 

  92. Henkel W, Glanville RW: Covalent crosslinking between molecules of Type I and Type III collagen. The involvement of N-terminal, nonheli-cal regions of the α1(I) and α1(III) chains in the formation of inter-molecular crosslinks. Eur J Biochem 122: 205–221, 1982.

    Article  PubMed  CAS  Google Scholar 

  93. Fraser RDB, MacRae TP, Miller A, Suzuki E: Molecular conformation and packing in collagen fibrils. J Mol Biol 167: 497–521, 1983.

    Article  PubMed  CAS  Google Scholar 

  94. Timpl R, Wiedemann H, van Delden V, Furthmayr H, Kuhn K: A network model for the organization of Type IV collagen molecules in basement membrane. Eur J Biochem 120: 203–211, 1981.

    Article  PubMed  CAS  Google Scholar 

  95. Timpl R, Wiedemann H, van Delden V, Furthmayr H, Kuhn K: A network model for the organization of Type IV collagen molecules in basement membrane. Eur J Biochem 120: 203–211, 1981.

    Article  PubMed  CAS  Google Scholar 

  96. Zambrano NZ, Montes GS, Shigihara KM, Sanchez EM, Junqueira LCU: Collagen arrangement in cartilages. Acta Anat 113: 26–38, 1983.

    Article  Google Scholar 

  97. Inouye H, Worthington CR: X-ray diffraction study of the cornea. Biophys J 41: 285a, 1983.

    Google Scholar 

  98. Sayers A: Koch MHJ, Whitburn SB, Meek KM, Elliott GF, Harmsen A: Synchrotron X-ray diffraction study of corneal stroma. J Mol Biol 160: 593–607, 1982.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1984 Martinus Nijhoff Publishers, Boston, The Hague, Dordrecht, Lancaster

About this chapter

Cite this chapter

Parry, D.A.D., Craig, A.S. (1984). Growth and development of collagen fibrils in connective tissue. In: Ruggeri, A., Motta, P.M. (eds) Ultrastructure of the Connective Tissue Matrix. Electron Microscopy in Biology and Medicine, vol 3. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2831-5_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-2831-5_2

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-9789-5

  • Online ISBN: 978-1-4613-2831-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics