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. 1976 Mar 1;68(3):521–538. doi: 10.1083/jcb.68.3.521

Supramolecular structure of polymorphic collagen fibrils

PMCID: PMC2109652  PMID: 67116

Abstract

Reconstituted cartilage collagen fibrils with an oblique banding pattern or with two types of symmetrical patterns, and reconstituted rattail tendon fibrils with a third type of symmetrical pattern were examined by electron microscopy and found to consist of narrow subfibrils having native-type cross-striations. Analysis of the four types of patterns by a graphic method of specific band matching revealed the orientation and axial relation of individual subfibrils and their component molecules. In fibrils with an oblique pattern, subfibrils have the same orientation and a regular 100A axial displacement. Observations on staining characteristics, folded fibrils, and transverse sections of embedded fibrils suggest that the obliquely banded fibrils are ribbonlike or layered structures. In the three types of fibrils with a symmetrical pattern, adjacent subfibrils are oppositely oriented and aligned within a 119-A segment of the 670-A major period. Considered together, the observations suggest that interaction sites on the surface of subfibrils (and perhaps on the surface of native collagen fibrils) occur in various patterns that are manifested accouding to the nature of the environment during fibril formation, and that such patterns can be mapped on the surface of subfibrils by noting the arrangement of subfibrils in polymorphic forms.

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Selected References

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  1. Anderson C. E., Parker J. Electron microscopy of the epiphyseal cartilage plate. A critical review of electron microscopy observations on enchondral ossification. Clin Orthop Relat Res. 1968 May-Jun;58:225–241. [PubMed] [Google Scholar]
  2. Balian G., Click E. M., Bornstein P. Structure of rat skin collagen 1-CB8. Amino acid sequence of the hydroxylamine-produced fragment HA1. Biochemistry. 1971 Nov 23;10(24):4470–4478. doi: 10.1021/bi00800a019. [DOI] [PubMed] [Google Scholar]
  3. Balian G., Click E. M., Hermodson M. A., Bornstein P. Structure of rat skin collagen alpha 1-CBB. Amino acid sequence of the hydroxyl amine-produced fragment HA2. Biochemistry. 1972 Sep 26;11(20):3798–3806. doi: 10.1021/bi00770a020. [DOI] [PubMed] [Google Scholar]
  4. Bard J. B., Chapman J. A. Polymorphism in collagen fibrils precipitated at low pH. Nature. 1968 Sep 21;219(5160):1279–1280. doi: 10.1038/2191279a0. [DOI] [PubMed] [Google Scholar]
  5. Bruns R. R., Gross J. Band pattern of the segment-long-spacing form of collagen. Its use in the analysis of primary structure. Biochemistry. 1973 Feb 27;12(5):808–815. doi: 10.1021/bi00729a004. [DOI] [PubMed] [Google Scholar]
  6. Bruns R. R., Gross J. High-resolution analysis of the modified quarter-stagger model of the collagen fibril. Biopolymers. 1974 May;13(5):931–941. doi: 10.1002/bip.1974.360130509. [DOI] [PubMed] [Google Scholar]
  7. Bruns R. R., Trelstad R. L., Gross J. Cartilage collagen: a staggered substructure in reconstituted fibrils. Science. 1973 Jul 20;181(4096):269–271. doi: 10.1126/science.181.4096.269. [DOI] [PubMed] [Google Scholar]
  8. Chapman J. A., Hardcastle R. A. The staining pattern of collagen fibrils. II. A comparison with patterns computer-generated from the amino acid sequence. Connect Tissue Res. 1974;2(2):151–159. doi: 10.3109/03008207409152100. [DOI] [PubMed] [Google Scholar]
  9. Chapman J. A. The staining pattern of collagen fibrils. I. An analysis of electron micrographs. Connect Tissue Res. 1974;2(2):137–150. doi: 10.3109/03008207409152099. [DOI] [PubMed] [Google Scholar]
  10. Doyle B. B., Hukins D. W., Hulmes D. J., Miller A., Rattew C. J., Woodhead-Galloway J. Origins and implications of the D stagger in collagen. Biochem Biophys Res Commun. 1974 Sep 23;60(2):858–864. doi: 10.1016/0006-291x(74)90320-9. [DOI] [PubMed] [Google Scholar]
  11. Doyle B. B., Hukins D. W., Hulmes D. J., Miller A., Woodhead-Galloway J. Collagen polymorphism: its origins in the amino acid sequence. J Mol Biol. 1975 Jan 5;91(1):79–99. doi: 10.1016/0022-2836(75)90373-3. [DOI] [PubMed] [Google Scholar]
  12. Doyle B. B., Hulmes D. J., Miller A., Parry A. D., Piez K. A., Woodhead-Galloway J. A D-periodic narrow filament in collagen. Proc R Soc Lond B Biol Sci. 1974 May 7;186(1082):67–74. doi: 10.1098/rspb.1974.0035. [DOI] [PubMed] [Google Scholar]
  13. Doyle B. B., Hulmes D. J., Miller A., Parry D. A., Piez K. A., Woodhead-Galloway J. Axially projected collagen structures. Proc R Soc Lond B Biol Sci. 1974 Aug 27;187(1086):37–46. doi: 10.1098/rspb.1974.0059. [DOI] [PubMed] [Google Scholar]
  14. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fietzek P. P., Kühn K. The vovalent structure of collagen: amino acid sequence of the N-terminal region of alpha 2-CB5 from rat skin collagen. FEBS Lett. 1973 Nov 1;36(3):289–291. doi: 10.1016/0014-5793(73)80393-x. [DOI] [PubMed] [Google Scholar]
  16. Fietzek P. P., Rexrodt F. W., Hopper K. E., Kühn K. The covalent structure of collagen. 2. The amino-acid sequence of alpha1-CB7 from calf-skin collagen. Eur J Biochem. 1973 Oct 5;38(2):396–400. doi: 10.1111/j.1432-1033.1973.tb03072.x. [DOI] [PubMed] [Google Scholar]
  17. Fietzek P. P., Rexrodt F. W., Wendt P., Stark M., Kühn K. The covalent structure of collagen. Amino-acid sequence of peptide 1-CB6-C2. Eur J Biochem. 1972 Oct 17;30(1):163–168. doi: 10.1111/j.1432-1033.1972.tb02083.x. [DOI] [PubMed] [Google Scholar]
  18. Fjolstad M., Helle O. A hereditary dysplasia of collagen tissues in sheep. J Pathol. 1974 Mar;112(3):183–188. doi: 10.1002/path.1711120309. [DOI] [PubMed] [Google Scholar]
  19. Fraser R. D., Miller A., Parry D. A. Letter: Packing of microfibrils in collagen. J Mol Biol. 1974 Feb 25;83(2):281–283. doi: 10.1016/0022-2836(74)90393-3. [DOI] [PubMed] [Google Scholar]
  20. GROSS J. The behavior of collagen units as a model in morphogenesis. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):261–274. doi: 10.1083/jcb.2.4.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ghosh S. K., Mitra H. P. Oblique banding pattern in collagen fibrils reconstituted in vitro after trypsin treatment. Biochim Biophys Acta. 1975 Oct 20;405(2):340–346. doi: 10.1016/0005-2795(75)90099-9. [DOI] [PubMed] [Google Scholar]
  22. Highberger J. H., Kang A. H., Gross J. Comparative studies on the amino acid sequence of the alpha 2-CB2 peptides from chick and rat skin collagens. Biochemistry. 1971 Feb 16;10(4):610–616. doi: 10.1021/bi00780a010. [DOI] [PubMed] [Google Scholar]
  23. Hodge A. J., Schmitt F. O. THE CHARGE PROFILE OF THE TROPOCOLLAGEN MACROMOLECULE AND THE PACKING ARRANGEMENT IN NATIVE-TYPE COLLAGEN FIBRILS. Proc Natl Acad Sci U S A. 1960 Feb;46(2):186–197. doi: 10.1073/pnas.46.2.186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hosemann R., Dreissig W., Nemetschek T. Schachtelhalm-structure of the octafibrils in collagen. J Mol Biol. 1974 Feb 25;83(2):275–280. doi: 10.1016/0022-2836(74)90392-1. [DOI] [PubMed] [Google Scholar]
  25. Hulmes D. J., Miller A., Parry D. A., Piez K. A., Woodhead-Galloway J. Analysis of the primary structure of collagen for the origins of molecular packing. J Mol Biol. 1973 Sep 5;79(1):137–148. doi: 10.1016/0022-2836(73)90275-1. [DOI] [PubMed] [Google Scholar]
  26. Kang A. H., Gross J. Amino acid sequence of cyanogen bromide peptides from the amino-terminal region of chick skicollagen. Biochemistry. 1970 Feb 17;9(4):796–804. doi: 10.1021/bi00806a012. [DOI] [PubMed] [Google Scholar]
  27. Leibovich S. J., Weiss J. B. Electron microscope studies of the effects of endo- and exopeptidase digestion on tropocollagen. A novel concept of the role of terminal regions in fibrillogenesis. Biochim Biophys Acta. 1970 Sep 29;214(3):445–454. doi: 10.1016/0005-2795(70)90303-x. [DOI] [PubMed] [Google Scholar]
  28. Lenaers A., Ansay M., Nusgens B. V., Lapière C. M. Collagen made of extended -chains, procollagen, in genetically-defective dermatosparaxic calves. Eur J Biochem. 1971 Dec 10;23(3):533–543. doi: 10.1111/j.1432-1033.1971.tb01651.x. [DOI] [PubMed] [Google Scholar]
  29. Miller A., Parry D. A. Structure and packing of microfibrils in collagen. J Mol Biol. 1973 Apr 5;75(2):441–447. doi: 10.1016/0022-2836(73)90035-1. [DOI] [PubMed] [Google Scholar]
  30. Miller A., Wray J. S. Molecular packing in collagen. Nature. 1971 Apr 16;230(5294):437–439. doi: 10.1038/230437a0. [DOI] [PubMed] [Google Scholar]
  31. Nemetschek T. Zur Frage typischer Querstreifenmuster des Kollagens. Naturwissenschaften. 1965 Aug;52(16):478–479. doi: 10.1007/BF00626246. [DOI] [PubMed] [Google Scholar]
  32. O'Hara P. J., Read W. K., Romane W. M., Bridges C. H. A collagenous tissue dysplasia of calves. Lab Invest. 1970 Sep;23(3):307–314. [PubMed] [Google Scholar]
  33. Piez K. A., Miller A. The structure of collagen fibrils. J Supramol Struct. 1974;2(2-4):121–137. doi: 10.1002/jss.400020207. [DOI] [PubMed] [Google Scholar]
  34. RAMACHANDRAN G. N., KARTHA G. Structure of collagen. Nature. 1955 Sep 24;176(4482):593–595. doi: 10.1038/176593a0. [DOI] [PubMed] [Google Scholar]
  35. RICH A., CRICK F. H. The molecular structure of collagen. J Mol Biol. 1961 Oct;3:483–506. doi: 10.1016/s0022-2836(61)80016-8. [DOI] [PubMed] [Google Scholar]
  36. Schmitt F. O., Gross J., Highberger J. H. A New Particle Type in Certain Connective Tissue Extracts. Proc Natl Acad Sci U S A. 1953 Jun;39(6):459–470. doi: 10.1073/pnas.39.6.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smith J. W. Molecular pattern in native collagen. Nature. 1968 Jul 13;219(5150):157–158. doi: 10.1038/219157a0. [DOI] [PubMed] [Google Scholar]
  38. Stark M., Miller E. J., Kühn K. Comparative electron-microscope studies on the collagens extracted from cartilage, bone, and skin. Eur J Biochem. 1972 May;27(1):192–196. doi: 10.1111/j.1432-1033.1972.tb01825.x. [DOI] [PubMed] [Google Scholar]
  39. Trelstad R. L., Kang A. H., Igarashi S., Gross J. Isolation of two distinct collagens from chick cartilage. Biochemistry. 1970 Dec 8;9(25):4993–4998. doi: 10.1021/bi00827a025. [DOI] [PubMed] [Google Scholar]
  40. Trelstad R. L., Kang A. H., Toole B. P., Gross J. Collagen heterogeneity. High resolution separation of native ( 1(I) 2 2 and ( 1(II) 3 and their component chains. J Biol Chem. 1972 Oct 25;247(20):6469–6473. [PubMed] [Google Scholar]
  41. VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wendt P., von der Mark K., Rexrodt F., Kühn K. The covalent structure of collagen. The amino-acid sequence of the 112-residues. Amino-terminal part of peptide 1-CB6 from calf-skin collagen. Eur J Biochem. 1972 Oct 17;30(1):169–183. doi: 10.1111/j.1432-1033.1972.tb02084.x. [DOI] [PubMed] [Google Scholar]
  43. Yuan L., Veis A. The self-assembly of collagen molecules. Biopolymers. 1973 Jun;12(6):1437–1444. doi: 10.1002/bip.1973.360120618. [DOI] [PubMed] [Google Scholar]
  44. Zimmermann B. K., Timpl R., Kühn K. Intermolecular cross-links of collagen. Participation of the carboxy-terminal nonhelical region of the 1-chain. Eur J Biochem. 1973 Jun;35(2):216–221. doi: 10.1111/j.1432-1033.1973.tb02828.x. [DOI] [PubMed] [Google Scholar]
  45. von der Mark Klaus, Wendt Peter, Rexrodt Friedrich, Kühn Klaus. Direct evidence for a correlation between amino acid sequence and cross striation pattern of collagen. FEBS Lett. 1970 Nov 18;11(2):105–108. doi: 10.1016/0014-5793(70)80503-8. [DOI] [PubMed] [Google Scholar]

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