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. 1974 Sep 1;62(3):815–830. doi: 10.1083/jcb.62.3.815

EPITHELIAL COLLAGENS AND GLYCOSAMINOGLYCANS IN THE EMBRYONIC CORNEA

Macromolecular Order and Morphogenesis in the Basement Membrane

Robert L Trelstad 1, Kimiko Hayashi 1, Bryan P Toole 1
PMCID: PMC2109222  PMID: 4136721

Abstract

The embryonic corneal epithelium synthesizes both collagen and chondroitin sulfate and excretes them across the basement membrane into the subepithelial space where they assemble into a spiraling orthogonal matrix of fibrils. The assembly of collagen into fibrils is first apparent at the outer face of the basement membrane in a region of ordered chondroitin sulfate molecules. Hyaluronate, another morphogenetically important corneal macromolecule, is produced at these early stages only by the inner endothelium. These correlated biosynthetic and ultrastructural data demonstrate discrete macromolecular products of the two corneal epithelia with differing morphogenetic properties and functions.

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Selected References

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  1. Bernfield M. R., Banerjee S. D., Cohn R. H. Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein (proteoglycan) at the epithelial surface. J Cell Biol. 1972 Mar;52(3):674–689. doi: 10.1083/jcb.52.3.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Conrad G. W. Collagen and mucopolysaccharide biosynthesis in the developing chick cornea. Dev Biol. 1970 Mar;21(3):292–317. doi: 10.1016/0012-1606(70)90126-0. [DOI] [PubMed] [Google Scholar]
  3. Coulombre A. J., Coulombre J. L. Corneal development. IV. Interruption of collagen excretion into the primary stroma of the cornea with L-azetidine-2-carboxylic acid. Dev Biol. 1972 May;28(1):183–190. doi: 10.1016/0012-1606(72)90136-4. [DOI] [PubMed] [Google Scholar]
  4. Dodson J. W., Hay E. D. Secretion of collagenous stroma by isolated epithelium grown in vitro. Exp Cell Res. 1971 Mar;65(1):215–220. doi: 10.1016/s0014-4827(71)80069-1. [DOI] [PubMed] [Google Scholar]
  5. Frank R. M. Etude autoradiographique de la dentinogenese en microscopie electronique a l'aide de la proline tritiee chez le chat. Arch Oral Biol. 1970 Jul;15(7):583–596. doi: 10.1016/0003-9969(70)90128-7. [DOI] [PubMed] [Google Scholar]
  6. GODMAN G. C., LANE N. ON THE SITE OF SULFATION IN THE CHONDROCYTE. J Cell Biol. 1964 Jun;21:353–366. doi: 10.1083/jcb.21.3.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Kefalides N. A. Isolation of a collagen from basement membranes containing three identical - chains. Biochem Biophys Res Commun. 1971 Oct 1;45(1):226–234. doi: 10.1016/0006-291x(71)90073-8. [DOI] [PubMed] [Google Scholar]
  9. Latta H. The glomerular cappillary wall. J Ultrastruct Res. 1970 Sep;32(5):526–544. doi: 10.1016/s0022-5320(70)80026-0. [DOI] [PubMed] [Google Scholar]
  10. Luft J. H. Ruthenium red and violet. II. Fine structural localization in animal tissues. Anat Rec. 1971 Nov;171(3):369–415. doi: 10.1002/ar.1091710303. [DOI] [PubMed] [Google Scholar]
  11. Meier S., Hay E. D. Synthesis of sulfated glycosaminoglycans by embryonic corneal epithelium. Dev Biol. 1973 Dec;35(2):318–331. doi: 10.1016/0012-1606(73)90027-4. [DOI] [PubMed] [Google Scholar]
  12. Myers D. B., Highton T. C., Rayns D. G. Acid mucopolysaccharides closely associated with collagen fibrils in normal human synovium. J Ultrastruct Res. 1969 Aug;28(3):203–213. doi: 10.1016/s0022-5320(69)90080-x. [DOI] [PubMed] [Google Scholar]
  13. REVEL J. P., HAY E. D. AN AUTORADIOGRAPHIC AND ELECTRON MICROSCOPIC STUDY OF COLLAGEN SYNTHESIS IN DIFFERENTIATING CARTILAGE. Z Zellforsch Mikrosk Anat. 1963 Oct 8;61:110–144. doi: 10.1007/BF00341524. [DOI] [PubMed] [Google Scholar]
  14. ROTH T. F., PORTER K. R. YOLK PROTEIN UPTAKE IN THE OOCYTE OF THE MOSQUITO AEDES AEGYPTI. L. J Cell Biol. 1964 Feb;20:313–332. doi: 10.1083/jcb.20.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Revel J. P., Karnovsky M. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol. 1967 Jun;33(3):C7–C12. doi: 10.1083/jcb.33.3.c7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Toole B. P., Gross J. The extracellular matrix of the regenerating newt limb: synthesis and removal of hyaluronate prior to differentiation. Dev Biol. 1971 May;25(1):57–77. doi: 10.1016/0012-1606(71)90019-4. [DOI] [PubMed] [Google Scholar]
  17. Toole B. P., Lowther D. A. The effect of chondroitin sulphate-protein on the formation of collagen fibrils in vitro. Biochem J. 1968 Oct;109(5):857–866. doi: 10.1042/bj1090857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Toole B. P., Trelstad R. L. Hyaluronate production and removal during corneal development in the chick. Dev Biol. 1971 Sep;26(1):28–35. doi: 10.1016/0012-1606(71)90104-7. [DOI] [PubMed] [Google Scholar]
  19. Trelstad R. L., Coulombre A. J. Morphogenesis of the collagenous stroma in the chick cornea. J Cell Biol. 1971 Sep;50(3):840–858. doi: 10.1083/jcb.50.3.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Trelstad R. L., Kang A. H., Cohen A. M., Hay E. D. Collagen synthesis in vitro by embryonic spinal cord epithelium. Science. 1973 Jan 19;179(4070):295–297. doi: 10.1126/science.179.4070.295. [DOI] [PubMed] [Google Scholar]
  21. Trelstad R. L., Kang A. H. Collagen heterogeneity in the avian eye: lens, vitreous body, cornea and sclera. Exp Eye Res. 1974 Apr;18(4):395–406. doi: 10.1016/0014-4835(74)90117-1. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Trelstad R. L. The Golgi apparatus in chick corneal epithelium: changes in intracellular position during development. J Cell Biol. 1970 Apr;45(1):34–42. doi: 10.1083/jcb.45.1.34. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Trelstad R. L. The developmental biology of vertebrate collagens. J Histochem Cytochem. 1973 Jun;21(6):521–528. doi: 10.1177/21.6.521. [DOI] [PubMed] [Google Scholar]
  25. WORTMAN B. Enzymic sulfation of corneal mucopolysaccharides by beef cornea epithelial extract. J Biol Chem. 1961 Apr;236:974–978. [PubMed] [Google Scholar]
  26. Weinstock M., Leblond C. P. Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after (3H)proline administration. J Cell Biol. 1974 Jan;60(1):92–127. doi: 10.1083/jcb.60.1.92. [DOI] [PMC free article] [PubMed] [Google Scholar]

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