Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1998 Jun;74(6):3211–3216. doi: 10.1016/S0006-3495(98)78027-0

Fibrous long spacing collagen ultrastructure elucidated by atomic force microscopy.

M F Paige 1, J K Rainey 1, M C Goh 1
PMCID: PMC1299661  PMID: 9635774

Abstract

Fibrous long spacing collagen (FLS) fibrils are collagen fibrils in which the periodicity is clearly greater than the 67-nm periodicity of native collagen. FLS fibrils were formed in vitro by the addition of alpha1-acid glycoprotein to an acidified solution of monomeric collagen and were imaged with atomic force microscopy. The fibrils formed were typically approximately 150 nm in diameter and had a distinct banding pattern with a 250-nm periodicity. At higher resolution, the mature FLS fibrils showed ultrastructure, both on the bands and in the interband region, which appears as protofibrils aligned along the main fibril axis. The alignment of protofibrils produced grooves along the main fibril, which were 2 nm deep and 20 nm in width. Examination of the tips of FLS fibrils suggests that they grow via the merging of protofibrils to the tip, followed by the entanglement and, ultimately, the tight packing of protofibrils. A comparison is made with native collagen in terms of structure and mechanism of assembly.

Full Text

The Full Text of this article is available as a PDF (245.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baselt D. R., Revel J. P., Baldeschwieler J. D. Subfibrillar structure of type I collagen observed by atomic force microscopy. Biophys J. 1993 Dec;65(6):2644–2655. doi: 10.1016/S0006-3495(93)81329-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Binnig G, Quate CF, Gerber C. Atomic force microscope. Phys Rev Lett. 1986 Mar 3;56(9):930–933. doi: 10.1103/PhysRevLett.56.930. [DOI] [PubMed] [Google Scholar]
  3. CAUNA N., ROSS L. L. The fine structure of Meissner's touch corpuscles of human fingers. J Biophys Biochem Cytol. 1960 Oct;8:467–482. doi: 10.1083/jcb.8.2.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dingemans K. P., Teeling P. Long-spacing collagen and proteoglycans in pathologic tissues. Ultrastruct Pathol. 1994 Nov-Dec;18(6):539–547. doi: 10.3109/01913129409021896. [DOI] [PubMed] [Google Scholar]
  5. Franzblau C., Schmid K., Faris B., Beldekas J., Garvin P., Kagan H. M., Baum B. J. The interaction of collagen with alpha1-acid glycoprotein. Biochim Biophys Acta. 1976 Mar 18;427(1):302–314. doi: 10.1016/0005-2795(76)90306-8. [DOI] [PubMed] [Google Scholar]
  6. Gale M., Pollanen M. S., Markiewicz P., Goh M. C. Sequential assembly of collagen revealed by atomic force microscopy. Biophys J. 1995 May;68(5):2124–2128. doi: 10.1016/S0006-3495(95)80393-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gelman R. A., Williams B. R., Piez K. A. Collagen fibril formation. Evidence for a multistep process. J Biol Chem. 1979 Jan 10;254(1):180–186. [PubMed] [Google Scholar]
  8. Ghadially F. N., Mierau G. W. An unusual banded structure in Ewing's sarcoma. J Submicrosc Cytol. 1985 Oct;17(4):645–650. [PubMed] [Google Scholar]
  9. Gross J., Highberger J. H., Schmitt F. O. COLLAGEN STRUCTURES CONSIDERED AS STATES OF AGGREGATION OF A KINETIC UNIT. THE TROPOCOLLAGEN PARTICLE. Proc Natl Acad Sci U S A. 1954 Aug;40(8):679–688. doi: 10.1073/pnas.40.8.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. HIGHBERGER J. H., GROSS J., SCHMITT F. O. The interaction of mucoprotein with soluble collagen; an electron microscope study. Proc Natl Acad Sci U S A. 1951 May;37(5):286–291. doi: 10.1073/pnas.37.5.286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hansma H. G., Hoh J. H. Biomolecular imaging with the atomic force microscope. Annu Rev Biophys Biomol Struct. 1994;23:115–139. doi: 10.1146/annurev.bb.23.060194.000555. [DOI] [PubMed] [Google Scholar]
  12. Hansma H. G., Vesenka J., Siegerist C., Kelderman G., Morrett H., Sinsheimer R. L., Elings V., Bustamante C., Hansma P. K. Reproducible imaging and dissection of plasmid DNA under liquid with the atomic force microscope. Science. 1992 May 22;256(5060):1180–1184. doi: 10.1126/science.256.5060.1180. [DOI] [PubMed] [Google Scholar]
  13. Hashimoto K., Oyama H. Cross-banded filamentous aggregation in the human dermis. J Invest Dermatol. 1974 Feb;62(2):106–112. doi: 10.1111/1523-1747.ep12692245. [DOI] [PubMed] [Google Scholar]
  14. Holmes D. F., Chapman J. A., Prockop D. J., Kadler K. E. Growing tips of type I collagen fibrils formed in vitro are near-paraboloidal in shape, implying a reciprocal relationship between accretion and diameter. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9855–9859. doi: 10.1073/pnas.89.20.9855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. JAKUS M. A. Studies on the cornea. II. The fine structure of Descement's membrane. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):243–252. doi: 10.1083/jcb.2.4.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kadler K. E., Holmes D. F., Trotter J. A., Chapman J. A. Collagen fibril formation. Biochem J. 1996 May 15;316(Pt 1):1–11. doi: 10.1042/bj3160001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kajikawa K., Nakanishi I., Yamamura T. The effect of collagenase on the formation of fibrous long spacing collagen aggregates. Lab Invest. 1980 Nov;43(5):410–417. [PubMed] [Google Scholar]
  18. Kamiyama R. Fibrous long spacing-like fibers in the bone marrow of myloproliferative disorder. Virchows Arch B Cell Pathol Incl Mol Pathol. 1982;39(3):285–291. doi: 10.1007/BF02892855. [DOI] [PubMed] [Google Scholar]
  19. Kamiyama R., Shimamine T. Fibrous long spacing-like fibers in the bone marrow of primary myelofibrosis. J Electron Microsc (Tokyo) 1977;26(4):339–341. [PubMed] [Google Scholar]
  20. Kobayasi T., Asboe-Hansen G., Tsurufuji S. Filamentous aggregates of collagen. Ultrastructural evidence for collagen-fibril degradation in situ. Arch Dermatol Res. 1985;277(3):214–219. doi: 10.1007/BF00404319. [DOI] [PubMed] [Google Scholar]
  21. LUSE S. A. Electron microscopic studies of brain tumors. Neurology. 1960 Oct;10:881–905. doi: 10.1212/wnl.10.10.881. [DOI] [PubMed] [Google Scholar]
  22. Miki H., Unno K., Park P., Ohno T., Nakajima M. Morphogenesis and origin of fibrous long-spacing collagen fibers in collagenase-treated mouse skin tissues. Tissue Cell. 1993 Oct;25(5):669–680. doi: 10.1016/0040-8166(93)90049-q. [DOI] [PubMed] [Google Scholar]
  23. Morris C. J., Bradby G. V., Walton K. W. Fibrous long-spacing collagen in human atherosclerosis. Atherosclerosis. 1978 Nov;31(3):345–354. doi: 10.1016/0021-9150(78)90069-2. [DOI] [PubMed] [Google Scholar]
  24. Murray M. N., Hansma H. G., Bezanilla M., Sano T., Ogletree D. F., Kolbe W., Smith C. L., Cantor C. R., Spengler S., Hansma P. K. Atomic force microscopy of biochemically tagged DNA. Proc Natl Acad Sci U S A. 1993 May 1;90(9):3811–3814. doi: 10.1073/pnas.90.9.3811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. NAUMANN R. A., WOLFE D. E. A striated intercellular material in rat brain. Nature. 1963 May 18;198:701–703. doi: 10.1038/198701a0. [DOI] [PubMed] [Google Scholar]
  26. Nakanishi I., Masuda S., Kitamura T., Moriizumi T., Kajikawa K. Distribution of fibrous long-spacing fibers in normal and pathological lymph nodes. Acta Pathol Jpn. 1981 Sep;31(5):733–745. doi: 10.1111/j.1440-1827.1981.tb02799.x. [DOI] [PubMed] [Google Scholar]
  27. Park P., Ohno T. Ultrastructural study of long spacing collagen fibres and basal lamina in malignant schwannoma. Tissue Cell. 1985;17(5):699–707. doi: 10.1016/0040-8166(85)90005-9. [DOI] [PubMed] [Google Scholar]
  28. Revenko I., Sommer F., Minh D. T., Garrone R., Franc J. M. Atomic force microscopy study of the collagen fibre structure. Biol Cell. 1994;80(1):67–69. doi: 10.1016/0248-4900(94)90019-1. [DOI] [PubMed] [Google Scholar]
  29. Slavin R. E., Swedo J. L., Brandes D., Gonzalez-Vitale J. C., Osornio-Vargas A. Extrapulmonary silicosis: a clinical, morphologic, and ultrastructural study. Hum Pathol. 1985 Apr;16(4):393–412. doi: 10.1016/s0046-8177(85)80233-1. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES