Electron Microscopy Shows Periodic Structure in Collagen Fibril Cross Sections

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1981 Jun 1

PMID 6943556

Citations 31

Authors

D J Hulmes

J C Jesior

A Miller

C Berthet-Colominas

C Wolff

Affiliations

Soon will be listed here.

Abstract

X-ray diffraction was used to monitor the effects of electron microscope fixation, staining, and embedding procedures on the preservation of the three-dimensional crystalline order in collagen fibrils of rat tail tendon. A procedure is described in which the characteristic 3.8-nm lateral spacing is preserved, with increased contrast, in the diffraction pattern of the embedded fiber. This spacing is correlated with the separation between the tangentially oriented equally spaced lines of density observed in electron microscope ultrathin fibril cross sections of the same material. Optical diffraction of electron micrographs gives an objective measure of the periodicity and suggests that the fibril is composed of concentrically oriented crystalline domains. These observations, when combined with a recent interpretation of the native x-ray diffraction data [Hulmes, D. J. S. & Miller, A. (1979) Nature (London) 282, 878-880] suggest a tentative model for the three-dimensional structure of collagen fibrils.

Citing Articles

Peptidic "Molecular Beacon" for Collagen.

Yang J, Quan Y, Ouyang Y, Tan K, Weber R, Griffin R Biomacromolecules. 2024; 25(10):6773-6779.

PMID: 39225003 PMC: 11563731. DOI: 10.1021/acs.biomac.4c01000.

Extracellular matrix-derived materials for tissue engineering and regenerative medicine: A journey from isolation to characterization and application.

Noro J, Vilaca-Faria H, Reis R, Pirraco R Bioact Mater. 2024; 34:494-519.

PMID: 38298755 PMC: 10827697. DOI: 10.1016/j.bioactmat.2024.01.004.

Using sequence data to predict the self-assembly of supramolecular collagen structures.

Puszkarska A, Frenkel D, Colwell L, Duer M Biophys J. 2022; 121(16):3023-3033.

PMID: 35859421 PMC: 9463645. DOI: 10.1016/j.bpj.2022.07.019.

Glycation changes molecular organization and charge distribution in type I collagen fibrils.

Bansode S, Bashtanova U, Li R, Clark J, Muller K, Puszkarska A Sci Rep. 2020; 10(1):3397.

PMID: 32099005 PMC: 7042214. DOI: 10.1038/s41598-020-60250-9.

3D mapping of native extracellular matrix reveals cellular responses to the microenvironment.

Lansky Z, Mutsafi Y, Houben L, Ilani T, Armony G, Wolf S J Struct Biol X. 2020; 1:100002.

PMID: 32055794 PMC: 7001979. DOI: 10.1016/j.yjsbx.2018.100002.

References

Smith J, Frame J . Observations on the collagen and proteinpolysaccharide complex of rabbit cornea stroma. J Cell Sci. 1969; 4(2):421-36. DOI: 10.1242/jcs.4.2.421. View

TROMANS W, HORNE R, GRESHAM G, Bailey A . Electron microscope studies on the structure of collagen fibrils by negative staining. Z Zellforsch Mikrosk Anat. 1963; 58:798-802. DOI: 10.1007/BF00410661. View

BOUTEILLE M, PEASE D . The tridimensional structure of native collagenous fibrils, their proteinaceous filaments. J Ultrastruct Res. 1971; 35(3):314-38. DOI: 10.1016/s0022-5320(71)80161-2. View

REED R . Freeze-etched connective tissue. Int Rev Connect Tissue Res. 1973; 6:257-305. DOI: 10.1016/b978-0-12-363706-2.50012-x. View

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

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

DOYLE B, Hulmes D, Miller A, Parry A, Piez K, Woodhead-Galloway J . A D-periodic narrow filament in collagen. Proc R Soc Lond B Biol Sci. 1974; 186(1082):67-74. DOI: 10.1098/rspb.1974.0035. View

Rayns D . Collagen from frozen fractured glycerinated beef heart. J Ultrastruct Res. 1974; 48(1):59-66. DOI: 10.1016/s0022-5320(74)80044-4. View

Chapman J, Hardcastle R . The staining pattern of collagen fibrils. II. A comparison with patterns computer-generated from the amino acid sequence. Connect Tissue Res. 1974; 2(2):151-9. DOI: 10.3109/03008207409152100. View

10.

DOYLE B, Hulmes D, Miller A, Parry D, Piez K, Woodhead-Galloway J . Axially projected collagen structures. Proc R Soc Lond B Biol Sci. 1974; 187(1086):37-46. DOI: 10.1098/rspb.1974.0059. View

11.

Trelstad R, Hayashi K, Gross J . Collagen fibrillogenesis: intermediate aggregates and suprafibrillar order. Proc Natl Acad Sci U S A. 1976; 73(11):4027-31. PMC: 431312. DOI: 10.1073/pnas.73.11.4027. View

12.

Grynpas M . Three-dimensional packing of collagen in bone. Nature. 1977; 265(5592):381-2. DOI: 10.1038/265381a0. View

13.

Lillie J, MACCALLUM D, Scaletta L, Occhino J . Collagen structure: evidence for a helical organization of the collagen fibril. J Ultrastruct Res. 1977; (2):134-43. DOI: 10.1016/s0022-5320(77)90025-9. View

14.

BRUNS R . Supramolecular structure of polymorphic collagen fibrils. J Cell Biol. 1976; 68(3):521-38. PMC: 2109652. DOI: 10.1083/jcb.68.3.521. View

15.

Gillard G, Merrilees M, REILLY H, FLINT M . The proteoglycan content and the axial periodicity of collagen in tendon. Biochem J. 1977; 163(1):145-51. PMC: 1164670. DOI: 10.1042/bj1630145. View

16.

Hukins D . X-ray diffraction by collagen tape shows that type I collagen fibrils need not have a three-dimensional lattice. Biochem Biophys Res Commun. 1977; 77(1):335-9. DOI: 10.1016/s0006-291x(77)80201-5. View

17.

Stolinski C, Breathnach A . Freeze-fracture replication and surface sublimation of frozen collagen fibrils. J Cell Sci. 1977; 23:325-34. DOI: 10.1242/jcs.23.1.325. View

18.

Hukins D, Woodhead-Galloway J . Liquid-crystal model for the organization of molecules in collagen fibrils [proceedings]. Biochem Soc Trans. 1978; 6(1):238-9. DOI: 10.1042/bst0060238. View

19.

Brodsky B, Hukins D, Hulmes D, Miller A, White S, Woodhead-Galloway J . Low angle X-ray diffraction studies on stained rat tail tendons. Biochim Biophys Acta. 1978; 535(1):25-32. DOI: 10.1016/0005-2795(78)90029-6. View

20.

Gathercole L, Keller A . X-ray diffraction effects related to superstructure in rat tail tendon collagen. Biochim Biophys Acta. 1978; 535(2):253-71. DOI: 10.1016/0005-2795(78)90092-2. View