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. 1981 Oct 1;91(1):281–286. doi: 10.1083/jcb.91.1.281

Type I collagen reduces the degradation of basal lamina proteoglycan by mammary epithelial cells

PMCID: PMC2111933  PMID: 7298723

Abstract

When mouse mammary epithelial cells are cultured on a plastic substratum, no basal lamina forms. When cultured on a type I collagen gel, the rate of glycosaminoglycan (GAG) synthesis is unchanged, but the rate of GAG degradation is markedly reduced and a GAG-rich, basal lamina-like structure accumulates. This effect of collagen was investigated by comparing the culture distribution, nature, and metabolic stability of the 35S-GAG-containing molecules produced by cells on plastic and collagen. During 48 h of labeling with 35SO4, cultures on collagen accumulate 1.4-fold more 35S-GAG per microgram of DNA. In these cultures, most of the extracellular 35S-GAG is immobilized with the lamina and collagen gel, whereas in cultures on plastic all extracellular 35S-GAG is soluble. On both substrata, the cells produce several heparan sulfate-rich 35S-proteoglycan fractions that are distinct by Sepharose CL-4B chromatography. The culture types contain similar amounts of each fraction, except that collagen cultures contain nearly four times more of a fraction that is found largely bound to the lamina and collagen gel. During a chase this proteoglycan fraction is stable in cultures on collagen, but is extensively degraded in cultures on plastic. Thus, collagen-induced formation of a basal lamina correlates with reduced degradation and enhanced accumulation of a specific heparan sulfate-rich proteoglycan fraction. Immobilization and stabilization of basal laminar proteoglycan(s) by interstitial collagen may be a physiological mechanism of basal lamina maintenance and assembly.

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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. Cohn R. H., Banerjee S. D., Bernfield M. R. Basal lamina of embryonic salivary epithelia. Nature of glycosaminoglycan and organization of extracellular materials. J Cell Biol. 1977 May;73(2):464–478. doi: 10.1083/jcb.73.2.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. David G., Bernfield M. R. Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: possible mechanism for basal lamina formation. Proc Natl Acad Sci U S A. 1979 Feb;76(2):786–790. doi: 10.1073/pnas.76.2.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Emerman J. T., Burwen S. J., Pitelka D. R. Substrate properties influencing ultrastructural differentiation of mammary epithelial cells in culture. Tissue Cell. 1979;11(1):109–119. doi: 10.1016/0040-8166(79)90011-9. [DOI] [PubMed] [Google Scholar]
  5. Emerman J. T., Pitelka D. R. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro. 1977 May;13(5):316–328. doi: 10.1007/BF02616178. [DOI] [PubMed] [Google Scholar]
  6. Foidart J. M., Bere E. W., Jr, Yaar M., Rennard S. I., Gullino M., Martin G. R., Katz S. I. Distribution and immunoelectron microscopic localization of laminin, a noncollagenous basement membrane glycoprotein. Lab Invest. 1980 Mar;42(3):336–342. [PubMed] [Google Scholar]
  7. Gordon J. R., Bernfield M. R. The basal lamina of the postnatal mammary epithelium contains glycosaminoglycans in a precise ultrastructural organization. Dev Biol. 1980 Jan;74(1):118–135. doi: 10.1016/0012-1606(80)90056-1. [DOI] [PubMed] [Google Scholar]
  8. Hassell J. R., Robey P. G., Barrach H. J., Wilczek J., Rennard S. I., Martin G. R. Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4494–4498. doi: 10.1073/pnas.77.8.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kanwar Y. S., Farquhar M. G. Presence of heparan sulfate in the glomerular basement membrane. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1303–1307. doi: 10.1073/pnas.76.3.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lindahl U., Hök M. Glycosaminoglycans and their binding to biological macromolecules. Annu Rev Biochem. 1978;47:385–417. doi: 10.1146/annurev.bi.47.070178.002125. [DOI] [PubMed] [Google Scholar]
  11. Linder E., Vaheri A., Ruoslahti E., Wartiovaara J. Distribution of fibroblast surface antigen in the developing chick embryo. J Exp Med. 1975 Jul 1;142(1):41–49. doi: 10.1084/jem.142.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mann P. R., Constable H. Induction of basal lamina formation in epidermal cell cultures in vitro. Br J Dermatol. 1977 Apr;96(4):421–426. doi: 10.1111/j.1365-2133.1977.tb07138.x. [DOI] [PubMed] [Google Scholar]
  13. Meier L., Hay E. D. Stimulation of corneal differentiation by interaction between cell surface and extracellular matrix. I. Morphometric analysis of transfilter "induction". J Cell Biol. 1975 Aug;66(2):275–291. doi: 10.1083/jcb.66.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Meier S., Hay E. D. Control of corneal differentiation by extracellular materials. Collagen as a promoter and stabilizer of epithelial stroma production. Dev Biol. 1974 Jun;38(2):249–270. doi: 10.1016/0012-1606(74)90005-0. [DOI] [PubMed] [Google Scholar]
  15. Owens R. B., Smith H. S., Hackett A. J. Epithelial cell cultures from normal glandular tissue of mice. J Natl Cancer Inst. 1974 Jul;53(1):261–269. doi: 10.1093/jnci/53.1.261. [DOI] [PubMed] [Google Scholar]
  16. Sakashita S., Engvall E., Ruoslahti E. Basement membrane glycoprotein laminin binds to heparin. FEBS Lett. 1980 Jul 28;116(2):243–246. doi: 10.1016/0014-5793(80)80654-5. [DOI] [PubMed] [Google Scholar]
  17. Timpl R., Rohde H., Robey P. G., Rennard S. I., Foidart J. M., Martin G. R. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed] [Google Scholar]
  18. Yamada K. M., Kennedy D. W., Kimata K., Pratt R. M. Characterization of fibronectin interactions with glycosaminoglycans and identification of active proteolytic fragments. J Biol Chem. 1980 Jul 10;255(13):6055–6063. [PubMed] [Google Scholar]

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