Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1984 Dec 1;99(6):2099–2107. doi: 10.1083/jcb.99.6.2099

Cellular origin of fibronectin in interspecies hybrid kidneys

PMCID: PMC2113543  PMID: 6389571

Abstract

The cellular origin of fibronectin in the kidney was studied in three experimental models. Immunohistochemical techniques that use cross- reacting or species-specific antibodies against mouse or chicken fibronectin were employed. In the first model studied, initially avascular mouse kidneys cultured on avian chorioallantoic membranes differentiate into epithelial kidney tubules and become vascularized by chorioallantoic vessels. Subsequently, hybrid glomeruli composed of mouse podocytes and avian endothelial-mesangial cells form. In immunohistochemical studies, cross-reacting antibodies to fibronectin stained vascular walls, tubular basement membranes, interstitium, and glomeruli of mouse kidney grafts. The species-specific antibodies reacting only with mouse fibronectin stained interstitial areas and tubular basement membranes, but showed no reaction with hybrid glomeruli and avian vascular walls. In contrast, species-specific antibodies against chicken fibronectin stained both the interstitial areas and the vascular walls as well as the endothelial-mesangial areas of the hybrid glomeruli, but did not stain the mouse-derived epithelial structures of the kidneys. In the second model, embryonic kidneys cultured under avascular conditions in vitro develop glomerular tufts, which are devoid of endothelial cells. These explants showed fluorescence staining for fibronectin only in tubular basement membranes and in interstitium. The avascular, purely epithelial glomerular bodies remained unstained. Finally, in outgrowths of separated embryonic glomeruli, the cross-reacting fibronectin antibodies revealed two populations of cells: one devoid of fibronectin and another expressing fibronectin in strong fibrillar and granular patterns. These results favor the idea that the main endogenous cellular sources for fibronectin in the embryonic kidney are the interstitial and vascular cells. All experiments presented here suggest that fibronectin is not synthesized by glomerular epithelial cells in vivo.

Full Text

The Full Text of this article is available as a PDF (4.3 MB).

Selected References

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

  1. Bernstein J., Cheng F., Roszka J. Glomerular differentiation in metanephric culture. Lab Invest. 1981 Aug;45(2):183–190. [PubMed] [Google Scholar]
  2. Courtoy P. J., Kanwar Y. S., Hynes R. O., Farquhar M. G. Fibronectin localization in the rat glomerulus. J Cell Biol. 1980 Dec;87(3 Pt 1):691–696. doi: 10.1083/jcb.87.3.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Courtoy P. J., Timpl R., Farquhar M. G. Comparative distribution of laminin, type IV collagen, and fibronectin in the rat glomerulus. J Histochem Cytochem. 1982 Sep;30(9):874–886. doi: 10.1177/30.9.7130672. [DOI] [PubMed] [Google Scholar]
  4. Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol. 1981 Oct;91(1):1–10. doi: 10.1083/jcb.91.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ekblom P., Sariola H., Karkinen-Jäskeläinen M., Saxén L. The origin of the glomerular endothelium. Cell Differ. 1982 Jan;11(1):35–39. doi: 10.1016/0045-6039(82)90014-8. [DOI] [PubMed] [Google Scholar]
  6. Foidart J. M., Foidart J. B., Mahieu P. R. Synthesis of collagen and fibronectin by glomerular cells in culture. Ren Physiol. 1980;3(1-6):183–192. doi: 10.1159/000172760. [DOI] [PubMed] [Google Scholar]
  7. GROBSTEIN C. Trans-filter induction of tubules in mouse metanephrogenic mesenchyme. Exp Cell Res. 1956 Apr;10(2):424–440. doi: 10.1016/0014-4827(56)90016-7. [DOI] [PubMed] [Google Scholar]
  8. Hayman E. G., Ruoslahti E. Distribution of fetal bovine serum fibronectin and endogenous rat cell fibronectin in extracellular matrix. J Cell Biol. 1979 Oct;83(1):255–259. doi: 10.1083/jcb.83.1.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hynes R. O., Yamada K. M. Fibronectins: multifunctional modular glycoproteins. J Cell Biol. 1982 Nov;95(2 Pt 1):369–377. doi: 10.1083/jcb.95.2.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Killen P. D., Striker G. E. Human glomerular visceral epithelial cells synthesize a basal lamina collagen in vitro. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3518–3522. doi: 10.1073/pnas.76.7.3518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kreisberg J. I., Karnovsky M. J. Glomerular cells in culture. Kidney Int. 1983 Mar;23(3):439–447. doi: 10.1038/ki.1983.40. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Madri J. A., Roll F. J., Furthmayr H., Foidart J. M. Ultrastructural localization of fibronectin and laminin in the basement membranes of the murine kidney. J Cell Biol. 1980 Aug;86(2):682–687. doi: 10.1083/jcb.86.2.682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Martinez-Hernandez A., Amenta P. S. The basement membrane in pathology. Lab Invest. 1983 Jun;48(6):656–677. [PubMed] [Google Scholar]
  15. Martinez-Hernandez A., Marsh C. A., Clark C. C., Macarak E. J., Brownell A. G. Fibronectin: its relationship to basement membranes. II. Ultrastructural studies in rat kidney. Coll Relat Res. 1981 Sep;1(5):405–418. doi: 10.1016/s0174-173x(81)80025-8. [DOI] [PubMed] [Google Scholar]
  16. Mosesson M. W., Chen A. B., Huseby R. M. The cold-insoluble globulin of human plasma: studies of its essential structural features. Biochim Biophys Acta. 1975 Apr 29;386(2):509–524. doi: 10.1016/0005-2795(75)90294-9. [DOI] [PubMed] [Google Scholar]
  17. Mosesson M. W., Umfleet R. A. The cold-insoluble globulin of human plasma. I. Purification, primary characterization, and relationship to fibrinogen and other cold-insoluble fraction components. J Biol Chem. 1970 Nov 10;245(21):5728–5736. [PubMed] [Google Scholar]
  18. Oh E., Pierschbacher M., Ruoslahti E. Deposition of plasma fibronectin in tissues. Proc Natl Acad Sci U S A. 1981 May;78(5):3218–3221. doi: 10.1073/pnas.78.5.3218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ruoslahti E., Engvall E., Hayman E. G. Fibronectin: current concepts of its structure and functions. Coll Relat Res. 1981;1(1):95–128. doi: 10.1016/s0174-173x(80)80011-2. [DOI] [PubMed] [Google Scholar]
  20. Sariola H., Ekblom P., Lehtonen E., Saxén L. Differentiation and vascularization of the metanephric kidney grafted on the chorioallantoic membrane. Dev Biol. 1983 Apr;96(2):427–435. doi: 10.1016/0012-1606(83)90180-x. [DOI] [PubMed] [Google Scholar]
  21. Sariola H., Timpl R., von der Mark K., Mayne R., Fitch J. M., Linsenmayer T. F., Ekblom P. Dual origin of glomerular basement membrane. Dev Biol. 1984 Jan;101(1):86–96. doi: 10.1016/0012-1606(84)90119-2. [DOI] [PubMed] [Google Scholar]
  22. Saxén L., Koskimies O., Lahti A., Miettinen H., Rapola J., Wartiovaara J. Differentiation of kidney mesenchyme in an experimental model system. Adv Morphog. 1968;7:251–293. doi: 10.1016/b978-1-4831-9954-2.50011-2. [DOI] [PubMed] [Google Scholar]
  23. Stenman S., Vaheri A. Distribution of a major connective tissue protein, fibronectin, in normal human tissues. J Exp Med. 1978 Apr 1;147(4):1054–1064. doi: 10.1084/jem.147.4.1054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Striker G. E., Killen P. D., Farin F. M. Human glomerular cells in vitro: isolation and characterization. Transplant Proc. 1980 Sep;12(3 Suppl 1):88–99. [PubMed] [Google Scholar]
  25. Thesleff I., Ekblom P., Kuusela P., Lehtonen E., Ruoslahti E. Exogenous fibronectin is not required for organogenesis in vitro. In Vitro. 1983 Dec;19(12):903–910. doi: 10.1007/BF02661711. [DOI] [PubMed] [Google Scholar]
  26. Vaheri A., Mosher D. F. High molecular weight, cell surface-associated glycoprotein (fibronectin) lost in malignant transformation. Biochim Biophys Acta. 1978 Sep 18;516(1):1–25. doi: 10.1016/0304-419x(78)90002-1. [DOI] [PubMed] [Google Scholar]
  27. Virtanen I., Ekblom P., Laurila P. Subcellular compartmentalization of saccharide moieties in cultured normal and malignant cells. J Cell Biol. 1980 May;85(2):429–434. doi: 10.1083/jcb.85.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vuento M., Vaheri A. Purification of fibronectin from human plasma by affinity chromatography under non-denaturing conditions. Biochem J. 1979 Nov 1;183(2):331–337. doi: 10.1042/bj1830331. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES