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. 1990 Apr 1;110(4):1457–1468. doi: 10.1083/jcb.110.4.1457

The spatial organization of Descemet's membrane-associated type IV collagen in the avian cornea

PMCID: PMC2116101  PMID: 2182654

Abstract

The organization of type IV collagen in the unconventional basement membrane of the corneal endothelium (Descemet's membrane) was investigated in developing chicken embryos using anti-collagen mAbs. Both immunofluorescence histochemistry and immunoelectron microscopy were performed. In mature embryos (greater than 15 d of development), the type IV collagen of Descemet's membrane was present as an array of discrete aggregates of amorphous material at the interface between Descemet's membrane and the posterior corneal stroma. Immunoreactivity for type IV collagen was also observed in the posterior corneal stroma as irregular plaques of material with a morphology similar to that of the Descemet's membrane-associated aggregates. This arrangement of Descemet's membrane-associated type IV collagen developed from a subendothelial mat of type IV collagen-containing material. This mat, in which type IV collagen-specific immunoreactivity was always discontinuous, first appeared at the time a confluent endothelium was established, well before the onset of Descemet's membrane formation. Immunoelectron microscopy of mature corneas revealed that the characteristic nodal matrix of Descemet's membrane itself was unreactive for type IV collagen, but was penetrated at intervals by projections of type IV collagen-containing material. These projections frequently appeared to contact cell processes from the underlying corneal endothelium. This spatial arrangement of type IV collagen suggests that it serves to suture the corneal endothelium/Descemet's membrane to the dense interfacial matrix of the posterior stroma.

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Selected References

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  1. Benya P. D., Padilla S. R. Isolation and characterization of type VIII collagen synthesized by cultured rabbit corneal endothelial cells. A conventional structure replaces the interrupted-helix model. J Biol Chem. 1986 Mar 25;261(9):4160–4169. [PubMed] [Google Scholar]
  2. Birk D. E., Fitch J. M., Babiarz J. P., Linsenmayer T. F. Collagen type I and type V are present in the same fibril in the avian corneal stroma. J Cell Biol. 1988 Mar;106(3):999–1008. doi: 10.1083/jcb.106.3.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brauer P. R., Markwald R. R. Specific configurations of fibronectin-containing particles correlate with pathways taken by neural crest cells at two axial levels. Anat Rec. 1988 Sep;222(1):69–82. doi: 10.1002/ar.1092220111. [DOI] [PubMed] [Google Scholar]
  4. Carlson E. C., Waring G. O., 3rd Ultrastructural analyses of enzyme-treated microfibrils in rabbit corneal stroma. Invest Ophthalmol Vis Sci. 1988 Apr;29(4):578–585. [PubMed] [Google Scholar]
  5. Cintron C., Covington H. I., Kublin C. L. Morphogenesis of rabbit corneal endothelium. Curr Eye Res. 1988 Sep;7(9):913–929. doi: 10.3109/02713688808997248. [DOI] [PubMed] [Google Scholar]
  6. Cohen A. M., Hay E. D. Secretion of collagen by embryonic neuroepithelium at the time of spinal cord--somite interaction. Dev Biol. 1971 Dec;26(4):578–605. doi: 10.1016/0012-1606(71)90142-4. [DOI] [PubMed] [Google Scholar]
  7. Fitch J. M., Birk D. E., Mentzer A., Hasty K. A., Mainardi C., Linsenmayer T. F. Corneal collagen fibrils: dissection with specific collagenases and monoclonal antibodies. Invest Ophthalmol Vis Sci. 1988 Jul;29(7):1125–1136. [PubMed] [Google Scholar]
  8. Fitch J. M., Gibney E., Sanderson R. D., Mayne R., Linsenmayer T. F. Domain and basement membrane specificity of a monoclonal antibody against chicken type IV collagen. J Cell Biol. 1982 Nov;95(2 Pt 1):641–647. doi: 10.1083/jcb.95.2.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fitch J. M., Gross J., Mayne R., Johnson-Wint B., Linsenmayer T. F. Organization of collagen types I and V in the embryonic chicken cornea: monoclonal antibody studies. Proc Natl Acad Sci U S A. 1984 May;81(9):2791–2795. doi: 10.1073/pnas.81.9.2791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fitch J. M., Linsenmayer T. F. Monoclonal antibody analysis of ocular basement membranes during development. Dev Biol. 1983 Jan;95(1):137–153. doi: 10.1016/0012-1606(83)90013-1. [DOI] [PubMed] [Google Scholar]
  11. Fitch J. M., Mayne R., Linsenmayer T. F. Developmental acquisition of basement membrane heterogeneity: type IV collagen in the avian lens capsule. J Cell Biol. 1983 Sep;97(3):940–943. doi: 10.1083/jcb.97.3.940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fujikawa L. S., Foster C. S., Gipson I. K., Colvin R. B. Basement membrane components in healing rabbit corneal epithelial wounds: immunofluorescence and ultrastructural studies. J Cell Biol. 1984 Jan;98(1):128–138. doi: 10.1083/jcb.98.1.128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gospodarowicz D., Greenburg G., Foidart J. M., Savion N. The production and localization of laminin in cultured vascular and corneal endothelial cells. J Cell Physiol. 1981 May;107(2):171–183. doi: 10.1002/jcp.1041070203. [DOI] [PubMed] [Google Scholar]
  14. Grant D. S., Leblond C. P. Immunogold quantitation of laminin, type IV collagen, and heparan sulfate proteoglycan in a variety of basement membranes. J Histochem Cytochem. 1988 Mar;36(3):271–283. doi: 10.1177/36.3.2963856. [DOI] [PubMed] [Google Scholar]
  15. Hay E. D. Development of the vertebrate cornea. Int Rev Cytol. 1980;63:263–322. doi: 10.1016/s0074-7696(08)61760-x. [DOI] [PubMed] [Google Scholar]
  16. Heathcote J. G., Grant M. E. The molecular organization of basement membranes. Int Rev Connect Tissue Res. 1981;9:191–264. doi: 10.1016/b978-0-12-363709-3.50011-5. [DOI] [PubMed] [Google Scholar]
  17. Hendrix M. J., Hay E. D., von der Mark K., Linsenmayer T. F. Immunohistochemical localization of collagen types I and II in the developing chick cornea and tibia by electron microscopy. Invest Ophthalmol Vis Sci. 1982 Mar;22(3):359–375. [PubMed] [Google Scholar]
  18. Hessle H., Sakai L. Y., Hollister D. W., Burgeson R. E., Engvall E. Basement membrane diversity detected by monoclonal antibodies. Differentiation. 1984;26(1):49–54. doi: 10.1111/j.1432-0436.1984.tb01372.x. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Jaffe R., Bender B., Santamaria M., Chung A. E. Segmental staining of the murine nephron by monoclonal antibodies directed against the GP-2 subunit of laminin. Lab Invest. 1984 Jul;51(1):88–96. [PubMed] [Google Scholar]
  21. Kapoor R., Sakai L. Y., Funk S., Roux E., Bornstein P., Sage E. H. Type VIII collagen has a restricted distribution in specialized extracellular matrices. J Cell Biol. 1988 Aug;107(2):721–730. doi: 10.1083/jcb.107.2.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kay E. D., Cheung C. C., Jester J. V., Nimni M. E., Smith R. E. Type I collagen and fibronectin synthesis by retrocorneal fibrous membrane. Invest Ophthalmol Vis Sci. 1982 Feb;22(2):200–212. [PubMed] [Google Scholar]
  23. Kay E. P. Expression of types I and IV collagen genes in normal and in modulated corneal endothelial cells. Invest Ophthalmol Vis Sci. 1989 Feb;30(2):260–268. [PubMed] [Google Scholar]
  24. Kay E. P., Smith R. E., Nimni M. E. Type I collagen synthesis by corneal endothelial cells modulated by polymorphonuclear leukocytes. J Biol Chem. 1985 Apr 25;260(8):5139–5146. [PubMed] [Google Scholar]
  25. Kefalides N. A., Alper R., Clark C. C. Biochemistry and metabolism of basement membranes. Int Rev Cytol. 1979;61:167–228. doi: 10.1016/s0074-7696(08)61998-1. [DOI] [PubMed] [Google Scholar]
  26. Kefalides N. A., Cameron J. D., Tomichek E. A., Yanoff M. Biosynthesis of basement membrane collagen by rabbit corneal endothelium in vitro. J Biol Chem. 1976 Feb 10;251(3):730–733. [PubMed] [Google Scholar]
  27. Kurkinen M., Alitalo K., Vaheri A., Stenman S., Saxén L. Fibronectin in the development of embryonic chick eye. Dev Biol. 1979 Apr;69(2):589–600. doi: 10.1016/0012-1606(79)90313-0. [DOI] [PubMed] [Google Scholar]
  28. Labermeier U., Kenney M. C. The presence of EC collagen and type IV collagen in bovine Descemet's membranes. Biochem Biophys Res Commun. 1983 Oct 31;116(2):619–625. doi: 10.1016/0006-291x(83)90569-7. [DOI] [PubMed] [Google Scholar]
  29. Leivo I., Engvall E. Merosin, a protein specific for basement membranes of Schwann cells, striated muscle, and trophoblast, is expressed late in nerve and muscle development. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1544–1548. doi: 10.1073/pnas.85.5.1544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Linsenmayer T. F., Fitch J. M., Schmid T. M. Multiple-reaction cycling: a method for enhancement of the immunochemical signal of monoclonal antibodies. J Histochem Cytochem. 1988 Aug;36(8):1075–1078. doi: 10.1177/36.8.3292645. [DOI] [PubMed] [Google Scholar]
  31. Linsenmayer T. F., Fitch J. M., Schmid T. M., Zak N. B., Gibney E., Sanderson R. D., Mayne R. Monoclonal antibodies against chicken type V collagen: production, specificity, and use for immunocytochemical localization in embryonic cornea and other organs. J Cell Biol. 1983 Jan;96(1):124–132. doi: 10.1083/jcb.96.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Linsenmayer T. F., Gibney E., Fitch J. M. Embryonic avian cornea contains layers of collagen with greater than average stability. J Cell Biol. 1986 Oct;103(4):1587–1593. doi: 10.1083/jcb.103.4.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Low F. N. Interstitial bodies in the early chick embryo. Am J Anat. 1970 May;128(1):45–55. doi: 10.1002/aja.1001280105. [DOI] [PubMed] [Google Scholar]
  34. MacCallum D. K., Lillie J. H., Scaletta L. J., Occhino J. C., Frederick W. G., Ledbetter S. R. Bovine corneal endothelium in vitro. Elaboration and organization and of a basement membrane. Exp Cell Res. 1982 May;139(1):1–13. doi: 10.1016/0014-4827(82)90313-5. [DOI] [PubMed] [Google Scholar]
  35. Mayer B. W., Jr, Hay E. D., Hynes R. O. Immunocytochemical localization of fibronectin in embryonic chick trunk and area vasculosa. Dev Biol. 1981 Mar;82(2):267–286. doi: 10.1016/0012-1606(81)90451-6. [DOI] [PubMed] [Google Scholar]
  36. Mayer B. W., Jr, Packard D. S., Jr A study of the expansion of the chick area vasculosa. Dev Biol. 1978 Apr;63(2):335–351. doi: 10.1016/0012-1606(78)90138-0. [DOI] [PubMed] [Google Scholar]
  37. Mayne R., Sanderson R. D., Wiedemann H., Fitch J. M., Linsenmayer T. F. The use of monoclonal antibodies to fragments of chicken type IV collagen in structural and localization studies. J Biol Chem. 1983 May 10;258(9):5794–5797. [PubMed] [Google Scholar]
  38. McLean I. W., Nakane P. K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem. 1974 Dec;22(12):1077–1083. doi: 10.1177/22.12.1077. [DOI] [PubMed] [Google Scholar]
  39. Murphy C., Alvarado J., Juster R. Prenatal and postnatal growth of the human Descemet's membrane. Invest Ophthalmol Vis Sci. 1984 Dec;25(12):1402–1415. [PubMed] [Google Scholar]
  40. Pratt B. M., Madri J. A. Immunolocalization of type IV collagen and laminin in nonbasement membrane structures of murine corneal stroma. A light and electron microscopic study. Lab Invest. 1985 Jun;52(6):650–656. [PubMed] [Google Scholar]
  41. Sakai L. Y., Keene D. R., Engvall E. Fibrillin, a new 350-kD glycoprotein, is a component of extracellular microfibrils. J Cell Biol. 1986 Dec;103(6 Pt 1):2499–2509. doi: 10.1083/jcb.103.6.2499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sankey E. A., Bown F. E., Morton L. F., Scott D. M., Barnes M. J. Analysis of the collagen types synthesized by bovine corneal endothelial cells in culture. Biochem J. 1981 Sep 15;198(3):707–710. doi: 10.1042/bj1980707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sawada H., Furthmayr H., Konomi H., Nagai Y. Immunoelectronmicroscopic localization of extracellular matrix components produced by bovine corneal endothelial cells in vitro. Exp Cell Res. 1987 Jul;171(1):94–109. doi: 10.1016/0014-4827(87)90254-0. [DOI] [PubMed] [Google Scholar]
  44. Sawada H., Konomi H., Nagai Y. The basement membrane of bovine corneal endothelial cells in culture with beta-aminopropionitrile: biosynthesis of hexagonal lattices composed of a 160 nm dumbbell-shaped structure. Eur J Cell Biol. 1984 Nov;35(2):226–234. [PubMed] [Google Scholar]
  45. Sawada H. The fine structure of the bovine Descemet's membrane with special reference to biochemical nature. Cell Tissue Res. 1982;226(2):241–255. doi: 10.1007/BF00218356. [DOI] [PubMed] [Google Scholar]
  46. Scheinman J. I., Tsai C. Monoclonal antibody to type IV collagen with selective basement membrane localization. Lab Invest. 1984 Jan;50(1):101–112. [PubMed] [Google Scholar]
  47. Schittny J. C., Timpl R., Engel J. High resolution immunoelectron microscopic localization of functional domains of laminin, nidogen, and heparan sulfate proteoglycan in epithelial basement membrane of mouse cornea reveals different topological orientations. J Cell Biol. 1988 Oct;107(4):1599–1610. doi: 10.1083/jcb.107.4.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Schmid T. M., Linsenmayer T. F. Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues. J Cell Biol. 1985 Feb;100(2):598–605. doi: 10.1083/jcb.100.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Stanley J. R., Hawley-Nelson P., Yuspa S. H., Shevach E. M., Katz S. I. Characterization of bullous pemphigoid antigen: a unique basement membrane protein of stratified squamous epithelia. Cell. 1981 Jun;24(3):897–903. doi: 10.1016/0092-8674(81)90115-x. [DOI] [PubMed] [Google Scholar]
  50. Sundarraj N., Willson J. Monoclonal antibody to human basement membrane collagen type IV. Immunology. 1982 Sep;47(1):133–140. [PMC free article] [PubMed] [Google Scholar]
  51. Timpl R., Dziadek M. Structure, development, and molecular pathology of basement membranes. Int Rev Exp Pathol. 1986;29:1–112. [PubMed] [Google Scholar]
  52. Tokuyasu K. T. Immunochemistry on ultrathin frozen sections. Histochem J. 1980 Jul;12(4):381–403. doi: 10.1007/BF01011956. [DOI] [PubMed] [Google Scholar]
  53. Tseng S. C., Savion N., Gospodarowicz D., Stern R. Characterization of collagens synthesized by cultured bovine corneal endothelial cells. J Biol Chem. 1981 Apr 10;256(7):3361–3365. [PubMed] [Google Scholar]
  54. Vracko R. Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structure. Am J Pathol. 1974 Nov;77(2):314–346. [PMC free article] [PubMed] [Google Scholar]
  55. von der Mark H., von der Mark K., Gay S. Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. I. Preparation of collagen type I and type II specific antibodies and their application to early stages of the chick embryo. Dev Biol. 1976 Feb;48(2):237–249. doi: 10.1016/0012-1606(76)90088-9. [DOI] [PubMed] [Google Scholar]
  56. von der Mark K., von der Mark H., Timpl R., Trelstad R. L. Immunofluorescent localization of collagen types I, II, and III in the embryonic chick eye. Dev Biol. 1977 Aug;59(1):75–85. doi: 10.1016/0012-1606(77)90241-x. [DOI] [PubMed] [Google Scholar]

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