Molecular Packing in Collagen Fibrils

  • A. Miller

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.”

Keywords

Collagen Fibril Molecular Packing Collagen Molecule Heuristic Model Molecular Arrangement 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bear, R. S., 1942, Long X-ray diffraction spacings of collagen, J. Am. Chem. Soc. 64:727.Google Scholar
  2. Bear, R. S., 1952, The structure of collagen fibrils, Adv. Protein Chem. 7: 69.Google Scholar
  3. Bear, R. S., 1956, The structure of collagen molecules and fibrils, J. Biophys. Biochem. Cytol. 2: 363.PubMedCrossRefGoogle Scholar
  4. Bear, R. S., and Morgan, R. S., 1957, in: Connective Tissue (R. E. Turnbridge, ed.), p. 321, Blackwell, Oxford.Google Scholar
  5. Boedetker, H., and Doty, P., 1956, The native and denatured states of soluble collagen,/ Am. Chem. Soc. 78: 4267.CrossRefGoogle Scholar
  6. Bouteille, M., and Pease, D. C., 1971, The tridimensional structure of native collagenous fibrils, their proteinaceous filaments, J. Ultrastruct. Res. 35: 314.PubMedCrossRefGoogle Scholar
  7. Bruns, R. R., and Gross, J., 1973, Biochemistry 12: 808.PubMedCrossRefGoogle Scholar
  8. Bruns, R. R., Trelstad, R. L., and Gross, J., 1973, Cartilage collagen: A staggered substructure in reconstituted fibrils, Science 181: 269.PubMedCrossRefGoogle Scholar
  9. Burge, R. E., 1965, Structure and Function of Connective and Skeletal Tissue (S. Fitton Jackson et al.,eds.), p. 2, Butterworth, London.Google Scholar
  10. 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.CrossRefGoogle Scholar
  11. Caspar, D. L. D., and Klug, A., 1962, Physical principles in the construction of regular viruses, Cold Spring Harbor Symp. Quant. Biol. 27: 1.PubMedCrossRefGoogle Scholar
  12. Chandross, R. J., and Bear, R. S., 1973, Improved profiles of electron density distribution along collagen fibrils, Biophys. J. 13: 1030.PubMedCrossRefGoogle Scholar
  13. Chapman, J. A., 1974, Connect. Tissue Res. 2: 137.PubMedCrossRefGoogle Scholar
  14. Chapman, J. A., and Hardcastle, 1974, Connect. Tissue Res. 2: 151–159.PubMedCrossRefGoogle Scholar
  15. Chapman, J. A., and Steven, F. S., 1966, in: Biochimie et Physiologie du Tissu Conjontif (P. Compte, ed.), p. 65, Lyon.Google Scholar
  16. 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
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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
  22. 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
  23. Ellis, D. O., and McGavin, S., 1970, The structure of collagen—an X-ray study, J. Ultrastruct. Res. 32: 191.PubMedCrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Fraser, R. D. B., and MacRae, T. P., 1961, The a-configuration of fibrous proteins, Nature 189: 572.CrossRefGoogle Scholar
  26. Fraser, R. D. B., MacRae, T. P., Rodgers, G. E., and Filshie, B. K., 1963, Lipids in keratinised tissue, J. Mol. Biol. 7: 90.PubMedCrossRefGoogle Scholar
  27. Fraser, R. D. B., Miller, A., and Parry, D. A. D., 1974, Packing of microfibrils in collagen, J. Mol. Biol. 83: 281.PubMedCrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Gross, J., and Schmitt, F. 0., 1948, Further progress in the electron microscopy of collagen. J. Am. Leather Chem. Assoc. 43: 658.Google Scholar
  30. 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.CrossRefGoogle Scholar
  31. Hall, C. E., 1956, Visualisation of individual macromolecules with the electron microscope, Proc. Natl. Acad. Sci. U.S.A. 42: 801.CrossRefGoogle Scholar
  32. Hall, C. E., Jakus, M. A., and Schmitt, F. 0., 1942, Electron microscope observations of collagen, J. Am. Chem. Soc. 64: 1234.Google Scholar
  33. Haydon, G. B., 1968, On the interpretation of high resolution electron micrographs of macromolecules, J. Ultrastruct. Res. 25: 349.PubMedCrossRefGoogle Scholar
  34. Haydon, G. B., 1969, Electron phase and amplitude images of stained biological thin sections, J. Microsc. 89: 73.PubMedCrossRefGoogle Scholar
  35. 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
  36. 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.CrossRefGoogle Scholar
  37. 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
  38. Hosemann, R., and Nemetschek, T., 1973, Reaktions Abäufe zwischen Phosphorwolframsaure und Kollagen, Kolloid-Z.Z. Polym. 351: 53.CrossRefGoogle Scholar
  39. Hosemann, R., Dreissig, W., and Nemetschek, T., 1974, Schachtelhalmstructure of the octafibrils in collagen, J. Mol. Biol. 83: 275.PubMedCrossRefGoogle Scholar
  40. Hulmes, D. J. S., 1975, D.Phil. Thesis, Oxford University.Google Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. Kaesberg, P., and Shurman, M., 1953, Further evidence concerning the periodic structure in collagen, Biochem. Biophys. Acta 11:1.Google Scholar
  43. Kang, A. H., 1972, Studies on the location of intermolecular cross-links in collagen, Biochemistry 11:1828.Google Scholar
  44. 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.PubMedCrossRefGoogle Scholar
  45. Katz, E. P., and Li, S. T., 1973, The intermolecular space of reconstituted collagen fibrils, J. Mol. Biol. 73: 351.PubMedCrossRefGoogle Scholar
  46. Katz, E. P., and Li, S. T., 1974, Structure and function of bone collagen fibrils, J. Mol. Biol. 80: 1.CrossRefGoogle Scholar
  47. Knight, D. P., and Hunt, S., 1974, Fibril structure of collagen in egg capsule of dogfish, Nature (London) 249: 380.CrossRefGoogle Scholar
  48. Kuhn, K., 1969, The structure of collagen, Essays Biochem. 5: 59.PubMedGoogle Scholar
  49. Kuhn, K., and Zimmer, E., 1961, Eigenschaften des Tropocollagen-Moleküls und deren Bedeutung für die Fibrillenbildung, Z. Naturforsch. 16: 648.Google Scholar
  50. Kuhn, K., Fietzek, P., and Kuhn, J., 1966, The action of proteolytic enzymes on collagen Biochem. Z. 344:418.Google Scholar
  51. Kuhn, K., Kuhn, J., and Schuppler, G., 1964, Kollagenfibrillen mit anormalen Querstreifungsmuster, Naturwissenschaften 51: 337.CrossRefGoogle Scholar
  52. Levine, Y. K., and Wilkins, M. H. F., 1971, Structure of oriented lipid bilayers Nature (London) New Biol. 230:69.Google Scholar
  53. Macfarlane, E. F., 1971, Molecular packing structure of collagen, Search 2: 171.Google Scholar
  54. Miller, A., and Parry, D. A. D., 1973, Structure and packing of microfibrils in collagen, J. Mol. Biol. 75: 441.PubMedCrossRefGoogle Scholar
  55. 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
  56. Nemetschek, T., and Hosemann, R., 1973, A kink model of native collagen Kolloid-Z.Z. Polym. 251 :1044.Google Scholar
  57. Nemetschek, T., Grassmann, W., and Hofmann, U., 1955, Über die hochunterteilte Querstreifung des Kollagens, Z. Naturforsch B. 10: 61.Google Scholar
  58. North, A. C. T., Cowan, P. M., and Randall, J. T., 1954, Structural units in collagen fibrils, Nature 174: 1142.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. Olsen, B. R., 1963, Electron microscope studies on collagen. I: Native collagen fibrils. Z. Zellforsch. 59: 199;PubMedCrossRefGoogle Scholar
  61. Electron microscope studies on collagen. II: Mechanism of linear polymerization of tropocollagen molecules, 59:184.Google Scholar
  62. Piez, K. A., and Torchia, D., 1975, Nature 258: 87.PubMedCrossRefGoogle Scholar
  63. Pollard, H., Miller, A., and Cox, C., 1973, Synaptic vesicles: Structure of chromaffin granule membranes, J. Supramol. Struct. 1: 295.PubMedCrossRefGoogle Scholar
  64. Pomeroy, C. D., and Mitton, R. J., 1951, The real densities of chrome and vegetable-tanned leathers, J. Soc. Leather Trades Chem. 35: 360.Google Scholar
  65. Rayns, D. G., 1974, Collagen from frozen fractured glycerinated beef heart J. Ultrastruct. Res. 48:59.Google Scholar
  66. 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
  67. 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.PubMedCrossRefGoogle Scholar
  68. Schmitt, F. 0., 1956, Macromolecular interaction patterns in biological systems Proc. Am. Phil. Soc. 100:476.Google Scholar
  69. 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
  70. 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.CrossRefGoogle Scholar
  71. Segrest, J. P., and Cunningham, L. W., 1971, Molecular basis for fibrillar aggregation of tropocollagen, Nature (London), New Biol. 234: 26.Google Scholar
  72. Segrest, J. P., and Cunningham, L. W., 1973, Unit fibril models derived from the molecular topography of collagen, Biopolymers 12: 825.PubMedCrossRefGoogle Scholar
  73. Smith, J. W., 1968, Molecular pattern in native collagen, Nature 219: 157.PubMedCrossRefGoogle Scholar
  74. Smith, J. W., and Frame, J., 1969, Observations of the collagen and protein—polysaccaride complex of rabbit corneal stroma, J. Cell Sci. 4: 421.PubMedGoogle Scholar
  75. 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
  76. Thon, F., 1966a, Zur Defokussierungsabhängigkeit des Phasenkontrastes bei der elektronenmikroskopischen Abbildung, Z. Naturforsch. 21: 476.Google Scholar
  77. 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
  78. Tomlin, S. G., 1955, The structure of collagen fibres, Proc. Int. Wool Textile Res. Conf. B, p. 187, Melbourne, Australia.Google Scholar
  79. Tomlin, S. G., and Worthington, C. R., 1956, Low-angle X-ray diffraction patterns of collagen, Proc. R. Soc. A 235: 189.CrossRefGoogle Scholar
  80. 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.PubMedCrossRefGoogle Scholar
  81. 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
  82. Veis, A., and Yuan, L., 1975. Biopolymers 14: 895.CrossRefGoogle Scholar
  83. 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.PubMedCrossRefGoogle Scholar
  84. 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.PubMedCrossRefGoogle Scholar
  85. White, J. W., Miller, A., and Ibel, K., 1976, Neutron diffraction by collagen. J. Chem. Soc. Faraday Trans. II 72: 435.CrossRefGoogle Scholar
  86. Wolpers, C., 1943, Kollagenquerstreifung und Grundsubstanz. Klin. Wochenschr. 22: 624.Google Scholar
  87. Woodhead-Galloway, J., Hukins, D. W. L., and Wray, J. S., 1975, Biochem. Biophy.s. Res. ’ Comm. 64: 1237.CrossRefGoogle Scholar
  88. Wray, J. S., 1972, D. Phil. thesis, Oxford University.Google Scholar
  89. 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.PubMedCrossRefGoogle Scholar
  90. Zimmerman, B. K., Pikkarainen, J., Fietzek, P. P., and Kuhn, K., 1970, Cross-linkages in collagen, Eur. J. Biochem. 16: 217.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1976

Authors and Affiliations

  • A. Miller
    • 1
  1. 1.Laboratory of Molecular Biophysics, Zoology DepartmentOxford UniversityOxfordEngland

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