Skip to main content

Molecular Packing in Collagen Fibrils

  • Chapter
Biochemistry of Collagen

Abstract

In this chapter I will discuss the three-dimensional arrangement of collagen molecules in the fibrils of connective tissue. This is a problem of quite general significance since the nature of the molecular packing in similar systems such as the fibrils of muscles and other biological fibers is still unknown. Once the sequence and symmetry of the individual collagen molecules are known, it is natural to proceed to inquire how these molecules aggregate to form the functional units of connective tissue. As Crick (1966) recognized, “the superlattice of collagen is a neglected problem and it is time somebody took it up again.”

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bear, R. S., 1942, Long X-ray diffraction spacings of collagen, J. Am. Chem. Soc. 64:727.

    Google Scholar 

  • Bear, R. S., 1952, The structure of collagen fibrils, Adv. Protein Chem. 7: 69.

    Google Scholar 

  • Bear, R. S., 1956, The structure of collagen molecules and fibrils, J. Biophys. Biochem. Cytol. 2: 363.

    Article  PubMed  CAS  Google Scholar 

  • Bear, R. S., and Morgan, R. S., 1957, in: Connective Tissue (R. E. Turnbridge, ed.), p. 321, Blackwell, Oxford.

    Google Scholar 

  • Boedetker, H., and Doty, P., 1956, The native and denatured states of soluble collagen,/ Am. Chem. Soc. 78: 4267.

    Article  Google Scholar 

  • Bouteille, M., and Pease, D. C., 1971, The tridimensional structure of native collagenous fibrils, their proteinaceous filaments, J. Ultrastruct. Res. 35: 314.

    Article  PubMed  CAS  Google Scholar 

  • Bruns, R. R., and Gross, J., 1973, Biochemistry 12: 808.

    Article  PubMed  CAS  Google Scholar 

  • Bruns, R. R., Trelstad, R. L., and Gross, J., 1973, Cartilage collagen: A staggered substructure in reconstituted fibrils, Science 181: 269.

    Article  PubMed  CAS  Google Scholar 

  • Burge, R. E., 1965, Structure and Function of Connective and Skeletal Tissue (S. Fitton Jackson et al.,eds.), p. 2, Butterworth, London.

    Google Scholar 

  • Burge, R. E., and Randall, J. T., 1955, The equivalence of electron microscopic and X-ray observations on collagen fibres, Proc. R. Soc. A 233: 1.

    Article  CAS  Google Scholar 

  • Caspar, D. L. D., and Klug, A., 1962, Physical principles in the construction of regular viruses, Cold Spring Harbor Symp. Quant. Biol. 27: 1.

    Article  PubMed  CAS  Google Scholar 

  • Chandross, R. J., and Bear, R. S., 1973, Improved profiles of electron density distribution along collagen fibrils, Biophys. J. 13: 1030.

    Article  PubMed  CAS  Google Scholar 

  • Chapman, J. A., 1974, Connect. Tissue Res. 2: 137.

    Article  PubMed  CAS  Google Scholar 

  • Chapman, J. A., and Hardcastle, 1974, Connect. Tissue Res. 2: 151–159.

    Article  PubMed  CAS  Google Scholar 

  • Chapman, J. A., and Steven, F. S., 1966, in: Biochimie et Physiologie du Tissu Conjontif (P. Compte, ed.), p. 65, Lyon.

    Google Scholar 

  • Crick, F. H. C., 1966, in: Principles of Biomolecular Organisation ed. (G. E. W. Wolstenholm and M. O’Connor, eds.), pp. 131–132. Churchill, London.

    Google Scholar 

  • Diamant, J., Keller, A., Baer, E., Litt, M., and Arridge, R. G. C., 1972, Collagen; Ultrastructure and its relation to mechanical properties as a function of ageing, Proc. R. Soc. B 180: 293.

    Article  CAS  Google Scholar 

  • Doyle, B. B., Hulmes, D. J. S., Miller, A., Parry, D. A. D., Piez, K. A., and Woodhead Galloway, J., 1974a, A D-periodic narrow filament in collagen, Proc. R. Soc. B 186: 67.

    Article  CAS  Google Scholar 

  • Doyle, B. B., Hulmes, D. J. S., Miller, A., Parry, D. A. D., Piez, K. A., and Woodhead-Galloway, J., 19746, Axially projected collagen structures, Proc. R. Soc. B 187: 37.

    Google Scholar 

  • Doyle, B. B., Hukins, D. W. L., Hulmes, D. J. S., Miller, A., and Woodhead-Galloway, J., 1975a, Collagen polymorphism: Its origins in the amino-acid sequence, J. Mol. Biol 91: 79.

    Article  PubMed  CAS  Google Scholar 

  • Doyle, B. B., Hukins, D. W. L., Hulmes, D. J. S., Miller, A., Rattew, C. J., and WoodheadGalloway, J., 19756, Biochem. Biophys. Res. Comm. 60: 858.

    Google Scholar 

  • Doyle, B. B., Haas, J., Hulmes, D. J. S., Jenkins, G., Miller, A., Timmins, P., and White, J. W., 1976, Proc. Brookhaven Symposium (in press).

    Google Scholar 

  • Ellis, D. O., and McGavin, S., 1970, The structure of collagen—an X-ray study, J. Ultrastruct. Res. 32: 191.

    Article  PubMed  CAS  Google Scholar 

  • Ericson, L. G., and Tomlin, S. G., 1959, Further studies of low-angle X-ray diffraction patterns of collagen, Proc. R. Soc. A 252: 197.

    Article  CAS  Google Scholar 

  • Fraser, R. D. B., and MacRae, T. P., 1961, The a-configuration of fibrous proteins, Nature 189: 572.

    Article  CAS  Google Scholar 

  • Fraser, R. D. B., MacRae, T. P., Rodgers, G. E., and Filshie, B. K., 1963, Lipids in keratinised tissue, J. Mol. Biol. 7: 90.

    Article  PubMed  CAS  Google Scholar 

  • Fraser, R. D. B., Miller, A., and Parry, D. A. D., 1974, Packing of microfibrils in collagen, J. Mol. Biol. 83: 281.

    Article  PubMed  CAS  Google Scholar 

  • Fraser, R. D. B., Macrae, T. P., Miller, A., and Rowlands, R. J., 1976, Digital processing of fiber diffraction patterns. J. App. Cryst. 9: 81.

    Article  Google Scholar 

  • Gross, J., and Schmitt, F. 0., 1948, Further progress in the electron microscopy of collagen. J. Am. Leather Chem. Assoc. 43: 658.

    Google Scholar 

  • Gross, J., Highberger, J. H., and Schmidt, F. 0., 1954, Collagen structures considered as states of aggregation of a kinetic unit. The tropocollagen particle. Proc. Natl. Acad. Sci. U.S.A. 40: 679.

    Article  CAS  Google Scholar 

  • Hall, C. E., 1956, Visualisation of individual macromolecules with the electron microscope, Proc. Natl. Acad. Sci. U.S.A. 42: 801.

    Article  CAS  Google Scholar 

  • Hall, C. E., Jakus, M. A., and Schmitt, F. 0., 1942, Electron microscope observations of collagen, J. Am. Chem. Soc. 64: 1234.

    CAS  Google Scholar 

  • Haydon, G. B., 1968, On the interpretation of high resolution electron micrographs of macromolecules, J. Ultrastruct. Res. 25: 349.

    Article  PubMed  CAS  Google Scholar 

  • Haydon, G. B., 1969, Electron phase and amplitude images of stained biological thin sections, J. Microsc. 89: 73.

    Article  PubMed  CAS  Google Scholar 

  • Hodge, A. J., and Petruska, J. A., 1963, Recent studies with the electron microscope on ordered aggregates of the tropocollagen molecule, in: Aspects of Protein Structure ( G. N. Ramachandran, ed.), p. 289, Academic Press, London.

    Google Scholar 

  • Hodge, A. J., and Schmitt, F. 0., 1960, The charge profile of the tropocollagen macromolecule and packing arrangement in native type collagen fibrils, Proc. Natl. Acad. Sci. U.S.A. 46: 186.

    Article  CAS  Google Scholar 

  • Höhling, H. J., Ashton, B. A., and Köster, H. D., 1974, Cell Tissue Res. 148:11. Hosemann, R., 1973, Paracrystals in biopolymers and synthetic polypeptides, Endeavour 32: 99.

    Google Scholar 

  • Hosemann, R., and Nemetschek, T., 1973, Reaktions Abäufe zwischen Phosphorwolframsaure und Kollagen, Kolloid-Z.Z. Polym. 351: 53.

    Article  Google Scholar 

  • Hosemann, R., Dreissig, W., and Nemetschek, T., 1974, Schachtelhalmstructure of the octafibrils in collagen, J. Mol. Biol. 83: 275.

    Article  PubMed  CAS  Google Scholar 

  • Hulmes, D. J. S., 1975, D.Phil. Thesis, Oxford University.

    Google Scholar 

  • Hulmes, D. J. S., Miller, A., Parry, D. A. D., Piez, K. A., and Woodhead-Galloway, J., 1973, Analysis of the primary structure of collagen for the origins of molecular packing, J. Mol. Biol. 79: 137.

    Article  PubMed  CAS  Google Scholar 

  • Kaesberg, P., and Shurman, M., 1953, Further evidence concerning the periodic structure in collagen, Biochem. Biophys. Acta 11:1.

    Google Scholar 

  • Kang, A. H., 1972, Studies on the location of intermolecular cross-links in collagen, Biochemistry 11:1828.

    Google Scholar 

  • Katz, E. P., and Li, S. T., 1972, The molecular packing of collagen in mineralised and non-mineralised tissues, Biochem. Biophys. Res. Commun. 46: 1368.

    Article  PubMed  CAS  Google Scholar 

  • Katz, E. P., and Li, S. T., 1973, The intermolecular space of reconstituted collagen fibrils, J. Mol. Biol. 73: 351.

    Article  PubMed  CAS  Google Scholar 

  • Katz, E. P., and Li, S. T., 1974, Structure and function of bone collagen fibrils, J. Mol. Biol. 80: 1.

    Article  Google Scholar 

  • Knight, D. P., and Hunt, S., 1974, Fibril structure of collagen in egg capsule of dogfish, Nature (London) 249: 380.

    Article  Google Scholar 

  • Kuhn, K., 1969, The structure of collagen, Essays Biochem. 5: 59.

    PubMed  CAS  Google Scholar 

  • Kuhn, K., and Zimmer, E., 1961, Eigenschaften des Tropocollagen-Moleküls und deren Bedeutung für die Fibrillenbildung, Z. Naturforsch. 16: 648.

    Google Scholar 

  • Kuhn, K., Fietzek, P., and Kuhn, J., 1966, The action of proteolytic enzymes on collagen Biochem. Z. 344:418.

    Google Scholar 

  • Kuhn, K., Kuhn, J., and Schuppler, G., 1964, Kollagenfibrillen mit anormalen Querstreifungsmuster, Naturwissenschaften 51: 337.

    Article  Google Scholar 

  • Levine, Y. K., and Wilkins, M. H. F., 1971, Structure of oriented lipid bilayers Nature (London) New Biol. 230:69.

    Google Scholar 

  • Macfarlane, E. F., 1971, Molecular packing structure of collagen, Search 2: 171.

    Google Scholar 

  • Miller, A., and Parry, D. A. D., 1973, Structure and packing of microfibrils in collagen, J. Mol. Biol. 75: 441.

    Article  PubMed  CAS  Google Scholar 

  • Miller, A., and Wray, J. S., 1971, Molecular packing in collagen Nature (London) 230:437. Millward, G. R., 1970, The substructure of a-keratin microfibrils J. Ultrastruct. Res. 31:349.

    Google Scholar 

  • Nemetschek, T., and Hosemann, R., 1973, A kink model of native collagen Kolloid-Z.Z. Polym. 251 :1044.

    Google Scholar 

  • Nemetschek, T., Grassmann, W., and Hofmann, U., 1955, Über die hochunterteilte Querstreifung des Kollagens, Z. Naturforsch B. 10: 61.

    Google Scholar 

  • North, A. C. T., Cowan, P. M., and Randall, J. T., 1954, Structural units in collagen fibrils, Nature 174: 1142.

    Article  PubMed  CAS  Google Scholar 

  • Okuyama, K., Tanaka, N., Ashida, T., Kakudo, M., Sakakibara, S., and Kishida, Y., 1972, An x-ray study of the synthetic polypeptide (Pro-Pro-Gly),o, J. Mol. Biol. 72: 571.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, B. R., 1963, Electron microscope studies on collagen. I: Native collagen fibrils. Z. Zellforsch. 59: 199;

    Article  PubMed  CAS  Google Scholar 

  • Electron microscope studies on collagen. II: Mechanism of linear polymerization of tropocollagen molecules, 59:184.

    Google Scholar 

  • Piez, K. A., and Torchia, D., 1975, Nature 258: 87.

    Article  PubMed  CAS  Google Scholar 

  • Pollard, H., Miller, A., and Cox, C., 1973, Synaptic vesicles: Structure of chromaffin granule membranes, J. Supramol. Struct. 1: 295.

    Article  PubMed  CAS  Google Scholar 

  • Pomeroy, C. D., and Mitton, R. J., 1951, The real densities of chrome and vegetable-tanned leathers, J. Soc. Leather Trades Chem. 35: 360.

    CAS  Google Scholar 

  • Rayns, D. G., 1974, Collagen from frozen fractured glycerinated beef heart J. Ultrastruct. Res. 48:59.

    Google Scholar 

  • Rougvie, M. A., and Bear, R. S., 1953, An X-ray diffraction investigation of swelling by collagen,/ Am. Leather Chem. Assoc. 48:735.

    Google Scholar 

  • Sakakibara, S., Kishida, Y., Okuyama, K., Tanaka, N., Ahsida, T., and Kakudo, M., 1972, Single crystals of (Pro-Pro-Gly),0, a synthetic polypeptide model of collagen, J. Mol. Biol. 65: 371.

    Article  PubMed  CAS  Google Scholar 

  • Schmitt, F. 0., 1956, Macromolecular interaction patterns in biological systems Proc. Am. Phil. Soc. 100:476.

    Google Scholar 

  • Schmitt, F. O., Gross, J., and Highberger, J. H., 1955, Tropocollagen and the properties of fibrous collagen, Exp. Cell. Res. (Suppl.) 3: 326.

    Google Scholar 

  • Schmitt, F. O., Hall, C. E., and Jakus, M. A., 1942, Electron microscope investigations of the structure of collagen, J. Cell. Comp. Physiol. 20: 11.

    Article  CAS  Google Scholar 

  • Segrest, J. P., and Cunningham, L. W., 1971, Molecular basis for fibrillar aggregation of tropocollagen, Nature (London), New Biol. 234: 26.

    CAS  Google Scholar 

  • Segrest, J. P., and Cunningham, L. W., 1973, Unit fibril models derived from the molecular topography of collagen, Biopolymers 12: 825.

    Article  PubMed  CAS  Google Scholar 

  • Smith, J. W., 1968, Molecular pattern in native collagen, Nature 219: 157.

    Article  PubMed  CAS  Google Scholar 

  • Smith, J. W., and Frame, J., 1969, Observations of the collagen and protein—polysaccaride complex of rabbit corneal stroma, J. Cell Sci. 4: 421.

    PubMed  CAS  Google Scholar 

  • Steven, F. S., 1970, Isolation and characterisation of polymeric collagen from complex connective tissue, in: Chemistry and Molecular Biology of the Intercellular Matrix ( E. A. Balazs, ed.), p. 43, Academic Press, New York.

    Google Scholar 

  • Thon, F., 1966a, Zur Defokussierungsabhängigkeit des Phasenkontrastes bei der elektronenmikroskopischen Abbildung, Z. Naturforsch. 21: 476.

    CAS  Google Scholar 

  • Thon, F., 19666, Imaging properties of the electron microscope near the theoretical limit of resolution, in: Electron Microscopy 1966 (R. Uycota, ed.), Vol. 1, p. 23, Maruzen, Tokyo.

    Google Scholar 

  • Tomlin, S. G., 1955, The structure of collagen fibres, Proc. Int. Wool Textile Res. Conf. B, p. 187, Melbourne, Australia.

    Google Scholar 

  • Tomlin, S. G., and Worthington, C. R., 1956, Low-angle X-ray diffraction patterns of collagen, Proc. R. Soc. A 235: 189.

    Article  CAS  Google Scholar 

  • Traub, W., and Yonath, A., 1966. Polymers of tripeptides as collagen models I. X-ray studies of poly(L-prolyl-glycyl-L-proline) and related polypeptides, J. Mol. Biol. 16: 404.

    Article  PubMed  CAS  Google Scholar 

  • Tromans, W. J., Home, R. W., Gresham, G. A., and Bailey, A. J., 1963, Electron microscope studies on the structure of collagen fibrils by negative staining, Z. Zellforsch. 58: 798.

    Google Scholar 

  • Veis, A., and Yuan, L., 1975. Biopolymers 14: 895.

    Article  CAS  Google Scholar 

  • Veis, A., Bhatnagar, R. S., Shuttleworth, C. A., and Mussell, S., 1970, The solubilization of mature, polymeric collagen fibrils by lyotropic relaxation, Biochim. Biophys. Acta. 200: 97.

    Article  PubMed  CAS  Google Scholar 

  • von der Mark, K., Wendt, P., Rexrodt, F., and Kuhn, K., 1970, Direct evidence for a correlation between amino-acid sequence and cross striation pattern of collagen, FEBS Lett. 11: 105.

    Article  PubMed  Google Scholar 

  • White, J. W., Miller, A., and Ibel, K., 1976, Neutron diffraction by collagen. J. Chem. Soc. Faraday Trans. II 72: 435.

    Article  CAS  Google Scholar 

  • Wolpers, C., 1943, Kollagenquerstreifung und Grundsubstanz. Klin. Wochenschr. 22: 624.

    Google Scholar 

  • Woodhead-Galloway, J., Hukins, D. W. L., and Wray, J. S., 1975, Biochem. Biophy.s. Res. ’ Comm. 64: 1237.

    Article  CAS  Google Scholar 

  • Wray, J. S., 1972, D. Phil. thesis, Oxford University.

    Google Scholar 

  • Yonath, A., and Traub, W., 1969, Polymers of tripeptides as collagen models IV. Structure analysis of poly(r. prolyl-glycyl-L-proline), J. Mol. Biol. 43: 461.

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman, B. K., Pikkarainen, J., Fietzek, P. P., and Kuhn, K., 1970, Cross-linkages in collagen, Eur. J. Biochem. 16: 217.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1976 Springer Science+Business Media New York

About this chapter

Cite this chapter

Miller, A. (1976). Molecular Packing in Collagen Fibrils. In: Ramachandran, G.N., Reddi, A.H. (eds) Biochemistry of Collagen. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-4602-0_3

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-4602-0_3

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-4604-4

  • Online ISBN: 978-1-4757-4602-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics