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. 1987 Jul;84(14):4791–4795. doi: 10.1073/pnas.84.14.4791

Matrix-driven translocation: dependence on interaction of amino-terminal domain of fibronectin with heparin-like surface components of cells or particles.

S A Newman, D A Frenz, E Hasegawa, S K Akiyama
PMCID: PMC305191  PMID: 2440029

Abstract

During the process of matrix-driven translocation, certain types of cells or polystyrene latex beads are transported between compositionally different regions of a collagen matrix. Under appropriate conditions this translocation depends on an interaction between the cell or particle surface and fibronectin. We now show that this interaction takes place at a site located within the first 31 kDa of the amino-terminal end of the fibronectin molecule. Using defined fibronectin fragments and monoclonal antibodies directed against specific fibronectin domains, this site is established as both necessary and sufficient for the promotion of matrix-driven translocation. Competition experiments using heparin, heparan sulfate, and other sulfated polysaccharides show that this fibronectin site interacts with heparin-like cell or particle surface components in promoting matrix-driven translocation. Treatment of cells with heparinase renders them unresponsive to the translocational effect. An antibody directed against the amino-terminal domain of fibronectin completely inhibits matrix-driven translocation without interfering with heparin binding, suggesting that a post-binding conformational change in fibronectin may be required for promotion of the effect.

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Selected References

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

  1. Akiyama S. K., Hasegawa E., Hasegawa T., Yamada K. M. The interaction of fibronectin fragments with fibroblastic cells. J Biol Chem. 1985 Oct 25;260(24):13256–13260. [PubMed] [Google Scholar]
  2. Akiyama S. K., Yamada K. M. Comparisons of evolutionarily distinct fibronectins: evidence for the origin of plasma and fibroblast cellular fibronectins from a single gene. J Cell Biochem. 1985;27(2):97–107. doi: 10.1002/jcb.240270204. [DOI] [PubMed] [Google Scholar]
  3. Akiyama S. K., Yamada K. M. The interaction of plasma fibronectin with fibroblastic cells in suspension. J Biol Chem. 1985 Apr 10;260(7):4492–4500. [PubMed] [Google Scholar]
  4. Ankel E. G., Homandberg G., Tooney N. M., Lai C. S. Heparin modulates conformational states of plasma fibronectin: an electron spin resonance spin label approach. Arch Biochem Biophys. 1986 Jan;244(1):50–56. doi: 10.1016/0003-9861(86)90093-7. [DOI] [PubMed] [Google Scholar]
  5. Bronner-Fraser M. Distribution of latex beads and retinal pigment epithelial cells along the ventral neural crest pathway. Dev Biol. 1982 May;91(1):50–63. doi: 10.1016/0012-1606(82)90007-0. [DOI] [PubMed] [Google Scholar]
  6. Brown P. J., Juliano R. L. Selective inhibition of fibronectin-mediated cell adhesion by monoclonal antibodies to a cell-surface glycoprotein. Science. 1985 Jun 21;228(4706):1448–1451. doi: 10.1126/science.4012302. [DOI] [PubMed] [Google Scholar]
  7. Damsky C. H., Knudsen K. A., Bradley D., Buck C. A., Horwitz A. F. Distribution of the cell substratum attachment (CSAT) antigen on myogenic and fibroblastic cells in culture. J Cell Biol. 1985 May;100(5):1528–1539. doi: 10.1083/jcb.100.5.1528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dottavio-Martin D., Ravel J. M. Radiolabeling of proteins by reductive alkylation with [14C]formaldehyde and sodium cyanoborohydride. Anal Biochem. 1978 Jul 1;87(2):562–565. doi: 10.1016/0003-2697(78)90706-6. [DOI] [PubMed] [Google Scholar]
  9. Duband J. L., Rocher S., Chen W. T., Yamada K. M., Thiery J. P. Cell adhesion and migration in the early vertebrate embryo: location and possible role of the putative fibronectin receptor complex. J Cell Biol. 1986 Jan;102(1):160–178. doi: 10.1083/jcb.102.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fougnot C., Jozefonvicz J., Samama M., Bara L. New heparin-like insoluble materials: part I. Ann Biomed Eng. 1979;7(5-6):429–439. doi: 10.1007/BF02364219. [DOI] [PubMed] [Google Scholar]
  11. Fougnot C., Jozefowicz M., Rosenberg R. D. Catalysis of the generation of thrombin-antithrombin complex by insoluble anticoagulant polystyrene derivatives. Biomaterials. 1984 Mar;5(2):94–99. doi: 10.1016/0142-9612(84)90008-5. [DOI] [PubMed] [Google Scholar]
  12. Furth M. E., Davis L. J., Fleurdelys B., Scolnick E. M. Monoclonal antibodies to the p21 products of the transforming gene of Harvey murine sarcoma virus and of the cellular ras gene family. J Virol. 1982 Jul;43(1):294–304. doi: 10.1128/jvi.43.1.294-304.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hayashi M., Yamada K. M. Differences in domain structures between plasma and cellular fibronectins. J Biol Chem. 1981 Nov 10;256(21):11292–11300. [PubMed] [Google Scholar]
  14. Hayashi M., Yamada K. M. Divalent cation modulation of fibronectin binding to heparin and to DNA. J Biol Chem. 1982 May 10;257(9):5263–5267. [PubMed] [Google Scholar]
  15. Hayashi M., Yamada K. M. Domain structure of the carboxyl-terminal half of human plasma fibronectin. J Biol Chem. 1983 Mar 10;258(5):3332–3340. [PubMed] [Google Scholar]
  16. 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]
  17. Hynes R. Molecular biology of fibronectin. Annu Rev Cell Biol. 1985;1:67–90. doi: 10.1146/annurev.cb.01.110185.000435. [DOI] [PubMed] [Google Scholar]
  18. Jilek F., Hörmann H. Fibronectin (cold-insoluble globulin), VI. Influence of heparin and hyaluronic acid on the binding of native collagen. Hoppe Seylers Z Physiol Chem. 1979 Apr;360(4):597–603. doi: 10.1515/bchm2.1979.360.1.597. [DOI] [PubMed] [Google Scholar]
  19. Johansson S., Hök M. Heparin enhances the rate of binding of fibronectin to collagen. Biochem J. 1980 May 1;187(2):521–524. doi: 10.1042/bj1870521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kjellén L., Pettersson I., Hök M. Cell-surface heparan sulfate: an intercalated membrane proteoglycan. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5371–5375. doi: 10.1073/pnas.78.9.5371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kleinman H. K., Silbert J. E., Silbert C. K. Heparan sulfate of skin fibroblasts grown in culture. Connect Tissue Res. 1975;4(1):17–23. doi: 10.3109/03008207509152193. [DOI] [PubMed] [Google Scholar]
  22. Laterra J., Silbert J. E., Culp L. A. Cell surface heparan sulfate mediates some adhesive responses to glycosaminoglycan-binding matrices, including fibronectin. J Cell Biol. 1983 Jan;96(1):112–123. doi: 10.1083/jcb.96.1.112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marcum J. A., McKenney J. B., Rosenberg R. D. Acceleration of thrombin-antithrombin complex formation in rat hindquarters via heparinlike molecules bound to the endothelium. J Clin Invest. 1984 Aug;74(2):341–350. doi: 10.1172/JCI111429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McDonald J. A., Quade B. J., Broekelmann T. J., LaChance R., Forsman K., Hasegawa E., Akiyama S. Fibronectin's cell-adhesive domain and an amino-terminal matrix assembly domain participate in its assembly into fibroblast pericellular matrix. J Biol Chem. 1987 Mar 5;262(7):2957–2967. [PubMed] [Google Scholar]
  25. McKeown-Longo P. J., Mosher D. F. Binding of plasma fibronectin to cell layers of human skin fibroblasts. J Cell Biol. 1983 Aug;97(2):466–472. doi: 10.1083/jcb.97.2.466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McKeown-Longo P. J., Mosher D. F. Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the matrix-assembly receptor of fibroblasts. J Cell Biol. 1985 Feb;100(2):364–374. doi: 10.1083/jcb.100.2.364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miekka S. I., Ingham K. C., Menache D. Rapid methods for isolation of human plasma fibronectin. Thromb Res. 1982 Jul 1;27(1):1–14. doi: 10.1016/0049-3848(82)90272-9. [DOI] [PubMed] [Google Scholar]
  28. Moldover M. R., Cahn J. W. An interface phase transition: complete to partial wetting. Science. 1980 Mar 7;207(4435):1073–1075. doi: 10.1126/science.207.4435.1073. [DOI] [PubMed] [Google Scholar]
  29. Newman S. A., Frenz D. A., Tomasek J. J., Rabuzzi D. D. Matrix-driven translocation of cells and nonliving particles. Science. 1985 May 17;228(4701):885–889. doi: 10.1126/science.4001925. [DOI] [PubMed] [Google Scholar]
  30. Newman S. A., Pautou M. P., Kieny M. The distal boundary of myogenic primordia in chimeric avian limb buds and its relation to an accessible population of cartilage progenitor cells. Dev Biol. 1981 Jun;84(2):440–448. doi: 10.1016/0012-1606(81)90413-9. [DOI] [PubMed] [Google Scholar]
  31. Norling B., Glimelius B., Wasteson A. Heparan sulfate proteoglycan of cultured cells: demonstration of a lipid- and a matrix-associated form. Biochem Biophys Res Commun. 1981 Dec 31;103(4):1265–1272. doi: 10.1016/0006-291x(81)90259-x. [DOI] [PubMed] [Google Scholar]
  32. Oldberg A., Kjellén L., Hök M. Cell-surface heparan sulfate. Isolation and characterization of a proteoglycan from rat liver membranes. J Biol Chem. 1979 Sep 10;254(17):8505–8510. [PubMed] [Google Scholar]
  33. Pierschbacher M. D., Hayman E. G., Ruoslahti E. Location of the cell-attachment site in fibronectin with monoclonal antibodies and proteolytic fragments of the molecule. Cell. 1981 Oct;26(2 Pt 2):259–267. doi: 10.1016/0092-8674(81)90308-1. [DOI] [PubMed] [Google Scholar]
  34. Ruoslahti E., Engvall E. Complexing of fibronectin glycosaminoglycans and collagen. Biochim Biophys Acta. 1980 Aug 13;631(2):350–358. doi: 10.1016/0304-4165(80)90308-6. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Ruoslahti E., Pekkala A., Engvall E. Effect of dextran sulfate on fibronectin-collagen interaction. FEBS Lett. 1979 Nov 1;107(1):51–54. doi: 10.1016/0014-5793(79)80461-5. [DOI] [PubMed] [Google Scholar]
  37. Sekiguchi K., Fukuda M., Hakomori S. Domain structure of hamster plasma fibronectin. Isolation and characterization of four functionally distinct domains and their unequal distribution between two subunit polypeptides. J Biol Chem. 1981 Jun 25;256(12):6452–6462. [PubMed] [Google Scholar]
  38. Stone K. R., Smith R. E., Joklik W. K. Changes in membrane polypeptides that occur when chick embryo fibroblasts and NRK cells are transformed with avian sarcoma viruses. Virology. 1974 Mar;58(1):86–100. doi: 10.1016/0042-6822(74)90143-3. [DOI] [PubMed] [Google Scholar]
  39. Tomasek J. J., Hay E. D., Fujiwara K. Collagen modulates cell shape and cytoskeleton of embryonic corneal and fibroma fibroblasts: distribution of actin, alpha-actinin, and myosin. Dev Biol. 1982 Jul;92(1):107–122. doi: 10.1016/0012-1606(82)90155-5. [DOI] [PubMed] [Google Scholar]
  40. Torza S., Mason S. G. Coalescence of two immiscible liquid drops. Science. 1969 Feb 21;163(3869):813–814. doi: 10.1126/science.163.3869.813. [DOI] [PubMed] [Google Scholar]
  41. Yamada K. M. Cell surface interactions with extracellular materials. Annu Rev Biochem. 1983;52:761–799. doi: 10.1146/annurev.bi.52.070183.003553. [DOI] [PubMed] [Google Scholar]
  42. 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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