Collagen Fibrillogenesis: Intermediate Aggregates and Suprafibrillar Order

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1976 Nov 1

PMID 1069288

Citations 22

Authors

R L Trelstad

K Hayashi

J Gross

Affiliations

Soon will be listed here.

Abstract

Polymerization of collagen in vitro has been studied with the electron microscope at early time points of fibril assembly. We have found morphologically distinct stages of aggregation, which we suggest represent successive steps in fibril formation. Linear growth of the fibril appears to occur by the tandem addition of aggregates to each other and subsequently to the ends of a subfibril; lateral growth occurs by the entwining, like a rope, of these subfibrils. Fibrillogenesis is also accompanied by extensive development of suprafibrillar order in which various patterns of parallel, spiral, and orthogonal sets of fibrils were frequently observed.

Citing Articles

Engineered nanofibrillar collagen with tunable biophysical properties for myogenic, endothelial, and osteogenic cell guidance.

Tan Y, Habing K, Riesterer J, Stempinski E, Lewis S, Pfeifer C Acta Biomater. 2024; 186:95-107.

PMID: 39117115 PMC: 11407781. DOI: 10.1016/j.actbio.2024.08.002.

Human-scale tissues with patterned vascular networks by additive manufacturing of sacrificial sugar-protein composites.

Eltaher H, Abukunna F, Ruiz-Cantu L, Stone Z, Yang J, Dixon J Acta Biomater. 2020; 113:339-349.

PMID: 32553918 PMC: 7435351. DOI: 10.1016/j.actbio.2020.06.012.

Type-I collagen fibrils: From growth morphology to local order.

Charvolin J, Sadoc J Eur Phys J E Soft Matter. 2019; 42(4):49.

PMID: 31011856 DOI: 10.1140/epje/i2019-11812-1.

Structural and Functional Plasticity of Collagen Fibrils.

Zhao Z, Li F, Guo Q, Zhou Y, Miao Y, Li Y DNA Cell Biol. 2019; 38(4):367-373.

PMID: 30724579 PMC: 6477584. DOI: 10.1089/dna.2018.4494.

Remodeling by fibroblasts alters the rate-dependent mechanical properties of collagen.

Babaei B, Davarian A, Lee S, Pryse K, McConnaughey W, Elson E Acta Biomater. 2016; 37:28-37.

PMID: 27015891 PMC: 4890571. DOI: 10.1016/j.actbio.2016.03.034.

References

Wood G, KEECH M . The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J. 1960; 75:588-98. PMC: 1204515. DOI: 10.1042/bj0750588. View

Gross J . THERMAL DENATURATION OF COLLAGEN IN THE DISPERSED AND SOLID STATE. Science. 1964; 143(3609):960-1. DOI: 10.1126/science.143.3609.960. View

Gross J, Kirk D . The heat precipitation of collagen from neutral salt solutions: some rate-regulating factors. J Biol Chem. 1958; 233(2):355-60. View

Gross J . The behavior of collagen units as a model in morphogenesis. J Biophys Biochem Cytol. 1956; 2(4 Suppl):261-74. PMC: 2229734. DOI: 10.1083/jcb.2.4.261. View

Lapiere C, Nusgens B . Polymerization of procollagen in vitro. Biochim Biophys Acta. 1974; 342(2):237-46. DOI: 10.1016/0005-2795(74)90078-6. View

Weinstock M, Leblond C . Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after (3H)proline administration. J Cell Biol. 1974; 60(1):92-127. PMC: 2109148. DOI: 10.1083/jcb.60.1.92. View

Trelstad R, Hayashi K, Toole B . Epithelial collagens and glycosaminoglycans in the embryonic cornea. Macromolecular order and morphogenesis in the basement membrane. J Cell Biol. 1974; 62(3):815-30. PMC: 2109222. DOI: 10.1083/jcb.62.3.815. View

Bouligand Y . Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell. 1972; 4(2):189-217. DOI: 10.1016/s0040-8166(72)80042-9. View

BRUNS R, Gross J . Band pattern of the segment-long-spacing form of collagen. Its use in the analysis of primary structure. Biochemistry. 1973; 12(5):808-15. DOI: 10.1021/bi00729a004. View

10.

Trelstad R, Coulombre A . Morphogenesis of the collagenous stroma in the chick cornea. J Cell Biol. 1971; 50(3):840-58. PMC: 2108295. DOI: 10.1083/jcb.50.3.840. View

11.

Bornstein P . The biosynthesis of collagen. Annu Rev Biochem. 1974; 43(0):567-603. DOI: 10.1146/annurev.bi.43.070174.003031. View

12.

Hayashi T, Nagai Y . Effect of pH on the stability of collagen molecule in solution. J Biochem. 1973; 73(5):999-1006. DOI: 10.1093/oxfordjournals.jbchem.a130184. View

13.

Miller A, Parry D . Structure and packing of microfibrils in collagen. J Mol Biol. 1973; 75(2):441-7. DOI: 10.1016/0022-2836(73)90035-1. View

14.

Hulmes D, Miller A, Parry D, Piez K, Woodhead-Galloway J . Analysis of the primary structure of collagen for the origins of molecular packing. J Mol Biol. 1973; 79(1):137-48. DOI: 10.1016/0022-2836(73)90275-1. View

15.

Hayashi T, Nagai Y . Factors affecting the interactions of collagen molecules as observed by in vitro fibril formation. I. Effects of small molecules, especially saccharides. J Biochem. 1972; 72(3):749-58. DOI: 10.1093/oxfordjournals.jbchem.a129953. View

16.

Trelstad R, Kang A, Toole B, 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; 247(20):6469-73. View

17.

Obrink B . Non-aggregated tropocollagen at physiological pH and ionic strength. A chemical and physico-chemical characterization of tropocollagen isolated from the skin of lathyritic rats. Eur J Biochem. 1972; 25(3):563-72. DOI: 10.1111/j.1432-1033.1972.tb01729.x. View

18.

Martin G, Byers P, Piez K . Procollagen. Adv Enzymol Relat Areas Mol Biol. 1975; 42:167-91. DOI: 10.1002/9780470122877.ch3. View

19.

Fessler L, Morris N, FESSLER J . Procollagen: biological scission of amino and carboxyl extension peptides. Proc Natl Acad Sci U S A. 1975; 72(12):4905-9. PMC: 388841. DOI: 10.1073/pnas.72.12.4905. View

20.

DICK Y, Nordwig A . Effect of pH on the stability of the collagen fold. Arch Biochem Biophys. 1966; 117(2):466-8. DOI: 10.1016/0003-9861(66)90436-x. View