Assembly of pericellular matrices by COS-7 cells transfected with CD44 lymphocyte-homing receptor genes (original) (raw)

Abstract

The capacity to assemble and retain a pericellular matrix is correlated with the expression of the cell surface binding sites specific for the extracellular matrix macromolecule hyaluronan. These binding proteins have been termed hyaluronan receptors. The lymphocyte-homing receptor CD44 may have identity with these hyaluronan receptors. To determine whether hyaluronan receptors function independently in this capacity for matrix assembly, mammalian cells were transfected with cDNA encoding the putative hyaluronan receptor CD44. After transfection with CD44 cDNA, COS cells gained the capacity to assemble hyaluronan-dependent pericellular matrices in the presence of exogenously added hyaluronan and proteoglycan. Thus, CD44 receptors do function as matrix-organizing, matrix-anchoring hyaluronan-binding proteins. In addition, the expression of CD44/hyaluronan receptors alone is sufficient to direct this matrix assembly. If matrix assembly is a function of cells in vivo that express hyaluronan receptors, this raises interesting possibilities for the role of the receptors in cell migration, when new extracellular matrix environments are encountered.

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Selected References

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  1. Aruffo A., Stamenkovic I., Melnick M., Underhill C. B., Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell. 1990 Jun 29;61(7):1303–1313. doi: 10.1016/0092-8674(90)90694-a. [DOI] [PubMed] [Google Scholar]
  2. Banerjee S. D., Toole B. P. Monoclonal antibody to chick embryo hyaluronan-binding protein: changes in distribution of binding protein during early brain development. Dev Biol. 1991 Jul;146(1):186–197. doi: 10.1016/0012-1606(91)90459-g. [DOI] [PubMed] [Google Scholar]
  3. Clarris B. J., Fraser J. R. On the pericellular zone of some mammalian cells in vitro. Exp Cell Res. 1968 Jan;49(1):181–193. doi: 10.1016/0014-4827(68)90530-2. [DOI] [PubMed] [Google Scholar]
  4. Clarris B. J., Fraser J. R., Rodda S. Effect of cell-bound hyaluronic acid on infectivity of Newcastle disease virus for human synovial cells in vitro. Ann Rheum Dis. 1974 May;33(3):240–242. doi: 10.1136/ard.33.3.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Culty M., Miyake K., Kincade P. W., Sikorski E., Butcher E. C., Underhill C., Silorski E. The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J Cell Biol. 1990 Dec;111(6 Pt 1):2765–2774. doi: 10.1083/jcb.111.6.2765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Goldstein L. A., Zhou D. F., Picker L. J., Minty C. N., Bargatze R. F., Ding J. F., Butcher E. C. A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins. Cell. 1989 Mar 24;56(6):1063–1072. doi: 10.1016/0092-8674(89)90639-9. [DOI] [PubMed] [Google Scholar]
  7. Günthert U., Hofmann M., Rudy W., Reber S., Zöller M., Haussmann I., Matzku S., Wenzel A., Ponta H., Herrlich P. A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell. 1991 Apr 5;65(1):13–24. doi: 10.1016/0092-8674(91)90403-l. [DOI] [PubMed] [Google Scholar]
  8. Hardwick C., Hoare K., Owens R., Hohn H. P., Hook M., Moore D., Cripps V., Austen L., Nance D. M., Turley E. A. Molecular cloning of a novel hyaluronan receptor that mediates tumor cell motility. J Cell Biol. 1992 Jun;117(6):1343–1350. doi: 10.1083/jcb.117.6.1343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Knudson C. B. Hyaluronan receptor-directed assembly of chondrocyte pericellular matrix. J Cell Biol. 1993 Feb;120(3):825–834. doi: 10.1083/jcb.120.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Knudson C. B., Toole B. P. Changes in the pericellular matrix during differentiation of limb bud mesoderm. Dev Biol. 1985 Dec;112(2):308–318. doi: 10.1016/0012-1606(85)90401-4. [DOI] [PubMed] [Google Scholar]
  11. Knudson C. B., Toole B. P. Hyaluronate-cell interactions during differentiation of chick embryo limb mesoderm. Dev Biol. 1987 Nov;124(1):82–90. doi: 10.1016/0012-1606(87)90462-3. [DOI] [PubMed] [Google Scholar]
  12. Knudson W., Biswas C., Li X. Q., Nemec R. E., Toole B. P. The role and regulation of tumour-associated hyaluronan. Ciba Found Symp. 1989;143:150-9; discussion 159-69, 281-5. doi: 10.1002/9780470513774.ch10. [DOI] [PubMed] [Google Scholar]
  13. Knudson W., Knudson C. B. Assembly of a chondrocyte-like pericellular matrix on non-chondrogenic cells. Role of the cell surface hyaluronan receptors in the assembly of a pericellular matrix. J Cell Sci. 1991 Jun;99(Pt 2):227–235. doi: 10.1242/jcs.99.2.227. [DOI] [PubMed] [Google Scholar]
  14. Laurent T. C., Fraser J. R. Hyaluronan. FASEB J. 1992 Apr;6(7):2397–2404. [PubMed] [Google Scholar]
  15. Lesley J., Schulte R., Hyman R. Binding of hyaluronic acid to lymphoid cell lines is inhibited by monoclonal antibodies against Pgp-1. Exp Cell Res. 1990 Apr;187(2):224–233. doi: 10.1016/0014-4827(90)90085-o. [DOI] [PubMed] [Google Scholar]
  16. McCarthy M. T., Toole B. P. Membrane-associated hyaluronate-binding activity of chondrosarcoma chondrocytes. J Cell Physiol. 1989 Oct;141(1):191–202. doi: 10.1002/jcp.1041410127. [DOI] [PubMed] [Google Scholar]
  17. Miyake K., Underhill C. B., Lesley J., Kincade P. W. Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition. J Exp Med. 1990 Jul 1;172(1):69–75. doi: 10.1084/jem.172.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nemec R. E., Toole B. P., Knudson W. The cell surface hyaluronate binding sites of invasive human bladder carcinoma cells. Biochem Biophys Res Commun. 1987 Nov 30;149(1):249–257. doi: 10.1016/0006-291x(87)91632-9. [DOI] [PubMed] [Google Scholar]
  19. Picker L. J., Nakache M., Butcher E. C. Monoclonal antibodies to human lymphocyte homing receptors define a novel class of adhesion molecules on diverse cell types. J Cell Biol. 1989 Aug;109(2):927–937. doi: 10.1083/jcb.109.2.927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Seed B. An LFA-3 cDNA encodes a phospholipid-linked membrane protein homologous to its receptor CD2. 1987 Oct 29-Nov 4Nature. 329(6142):840–842. doi: 10.1038/329840a0. [DOI] [PubMed] [Google Scholar]
  21. Seed B., Aruffo A. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc Natl Acad Sci U S A. 1987 May;84(10):3365–3369. doi: 10.1073/pnas.84.10.3365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stamenkovic I., Amiot M., Pesando J. M., Seed B. A lymphocyte molecule implicated in lymph node homing is a member of the cartilage link protein family. Cell. 1989 Mar 24;56(6):1057–1062. doi: 10.1016/0092-8674(89)90638-7. [DOI] [PubMed] [Google Scholar]
  23. Stamenkovic I., Aruffo A., Amiot M., Seed B. The hematopoietic and epithelial forms of CD44 are distinct polypeptides with different adhesion potentials for hyaluronate-bearing cells. EMBO J. 1991 Feb;10(2):343–348. doi: 10.1002/j.1460-2075.1991.tb07955.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sy M. S., Guo Y. J., Stamenkovic I. Distinct effects of two CD44 isoforms on tumor growth in vivo. J Exp Med. 1991 Oct 1;174(4):859–866. doi: 10.1084/jem.174.4.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Thomas L., Byers H. R., Vink J., Stamenkovic I. CD44H regulates tumor cell migration on hyaluronate-coated substrate. J Cell Biol. 1992 Aug;118(4):971–977. doi: 10.1083/jcb.118.4.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Toole B. P. Hyaluronan and its binding proteins, the hyaladherins. Curr Opin Cell Biol. 1990 Oct;2(5):839–844. doi: 10.1016/0955-0674(90)90081-o. [DOI] [PubMed] [Google Scholar]
  27. Toole B. P., Munaim S. I., Welles S., Knudson C. B. Hyaluronate-cell interactions and growth factor regulation of hyaluronate synthesis during limb development. Ciba Found Symp. 1989;143:138–285. doi: 10.1002/9780470513774.ch9. [DOI] [PubMed] [Google Scholar]
  28. Underhill C. B. The interaction of hyaluronate with the cell surface: the hyaluronate receptor and the core protein. Ciba Found Symp. 1989;143:87-99; discussion 100-6, 281-5. doi: 10.1002/9780470513774.ch6. [DOI] [PubMed] [Google Scholar]
  29. Yu Q., Banerjee S. D., Toole B. P. The role of hyaluronan-binding protein in assembly of pericellular matrices. Dev Dyn. 1992 Feb;193(2):145–151. doi: 10.1002/aja.1001930206. [DOI] [PubMed] [Google Scholar]