In vitro changes in plasma membrane heparan sulfate proteoglycans and in perlecan expression participate in the regulation of fibroblast growth factor 2 mitogenic activity

Journal of Cellular Physiology

Volumn 166, Issue 1, 1996, Pages 170-187

  Guillonneau, Xavier ^a   Tassin, Jacqueline ^a   Berrou, Eliane ^b   Bryckaert, Marijke ^b   Courtois, Yves ^a   Mascarelli, Frédéric ^a  

^a BICHAT HOSPITAL   (France)

^b HÔPITAL LARIBOISIÈRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE; HEPARIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; PROTEOHEPARAN SULFATE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CATTLE; CELL PROLIFERATION; CELL SURFACE; EXTRACELLULAR MATRIX; GENE EXPRESSION; IMMUNOFLUORESCENCE; MITOGENESIS; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RECEPTOR AFFINITY; RECEPTOR DOWN REGULATION;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CATTLE; CELL DIVISION; CELL MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; EXTRACELLULAR MATRIX; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; HEPARITIN SULFATE; IMMUNOHISTOCHEMISTRY; IODINE RADIOISOTOPES; KINETICS; MEMBRANE PROTEINS; MITOGENS; MOLECULAR SEQUENCE DATA; PIGMENT EPITHELIUM OF EYE; PROTEOGLYCANS; RECEPTORS, GROWTH FACTOR; RNA, MESSENGER; SULFATES; SULFUR RADIOISOTOPES;

ANIMALIA; BOS TAURUS; TRIXIS;

EID: 0030027806     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199601)166:1<170::AID-JCP19>3.0.CO;2-J     Document Type: Article

References (64)

1. Adler, A.J., and Martin, K. (1983) Lysosomal enzymes in the interphotoreceptor matrix: Acid protease. Curr Eye Res., 2:359-366.
2. Aguirre, G.D., and Stramm, L.E. (1991) The RPE: A model system for disease expression and disease correction. In: Progress in Retinal Research. N.N. Osborne and G.J. Chader, eds. Pergamon Press, Oxford, Vol. 11, pp. 153-191.
3. Arruti, C. and Courtois, Y. (1978) Morphological changes and growth stimulation of bovine epithelial lens cells by a retinal extract in vitro. Exp. Cell. Res., 117-290.
4. Aviezer, D., Hecht, D., Sofran, M., Eisinger, M., David, G., and Yayon, A. (1994) Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis and angiogenesis. Cell, 79:1005-1013
5. Baird, A., Esch, F., Gospodarowicz, D., and Guillemin, R. (1985) Retina- and eye-derived endothelial cell growth factors: Partial molecular characterization and identity with acidic and basic fibroblast growth factors. Biochemistry, 24:7855-7865.
6. Barnstable, C.J., Blum, A.S., Devoto, S.H., Hicks, D., Morabito, M.A., Sparrow, J.R., and Treisman, J.E. (1988) Cell differentiation and pattern formation in the developing mammalian retina. Neurosci. Res., 8(suppl.):S27-S41.
7. Bashkin, P., Neufeld, G., Gitay-Goren, H., and Vlodavsky, I. (1992) Release of cell surface-associated basic fibroblast growth factor by glycosylphosphatidylinositol-specific phospholipase C.J. Cell. Physiol., 151:126-137.
8. Basu, P.K., Sarkar, P., Menon, I., Carre, F., and Persad, S. (1983) Bovine retinal pigment epithelial cells cultured in vitro: Growth characteristics, morphology, chromosomes, phagocytosis ability, tyrosine kinase activity, and effects of freezing. Exp. Eye Res. 36:671-683.
9. Bernfield, M., and Hooper, K.C. (1991) Possible regulation of FGF activity by Syndecan, an integral membrane heparan sulfate proteoglycan. Ann. N. Y. Acad. Sci., 638:182-184.
10. Bost, L.M., Aotaki-Keien, A.E., and Hjelmeland, L.M. (1992) Coexpression of FGFa and bFGF by the retinal pigment epithelium in vitro. Exp. Eye Res., 55:727-734.
11. Boulton, M. (1991) Ageing of the retinal pigment epithelium. In: Progress in Retinal Research. N.N. Osborne and G.J. Chader, Eds. Pergamon Press, Oxford, Vol. 11, pp. 125-151.
12. Braunagel, S.C., Organisciak, D.T., and Wang, H.M. (1988) Characterization of pigment epithelial cell plasma membranes from normal and dystrophic rats. Invest. Ophthalmol. Vis. Sci., 29:1066-1075.
13. Burgess, W.H., and Maciag, T. (1989) The heparin binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem., 58:575-606.
14. Busch, S.J., Martin, G.A., Barnhart, R.L., Mano, M., Cardin, A.D., and Jackson, R.L. (1992) Trans repressor activity of nuclear glycosaminoglycans on fos and Jun/AP1 oncoprotein-mediated transcription. J. Cell. Biol., 116:31-42.
15. Chirgwin, J.M., Preyzyla, A.E., McDonald, R.J., and Rutter, W.J. (1978) Isolation of biological active ribonucleic acid from sources enriched in ribonuclease. Biochemistry, 18:5294-5299.
16. Clark, V.M., and Hall, M.O. (1986) RPE cells surface proteins in normal and dystrophic rats. Invest. Ophthalmol. Vis. Sci., 27:136-145.
17. Courty, J., Loret, C., Moenner, M., Chevallier, B., Lagente, O., Courtois, Y., and Barritault, D. (1985) Bovine retina contains three growth factor activities with different affinity to heparin: Eye derived growth factor I, II, III. Biochimie, 67:265-269.
18. Faktorovich, E., Steinberg, R., Yasumara, D., Matthes, M., and LaVail, M. (1990) Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature, 347:83-86.
19. Givol, D., and Yayon, A. (1992) Complexity of FGF receptors: Genetic basis for structural diversity and functional specificity FASEB J., 6:3362-3369.
20. Gospodarowicz, D., and Cheng, J. (1986) Heparin protects basic and acidic FGF from inactivation. J. Cell. Physiol., 128:475-484.
21. Guimond, S., Maccarana, M., Olwin, B.B., Lindahl, U., and Rappraeger, A.C. (1993) Activating and inhibitory heparin sequences for FGF2 (basic FGF). Distinct requirements for FGF1, FGF2 and FGF4. J. Biol. Chem., 268:23906-23914.
22. Hageman, G.S., and Johnson, L.V. (1991) Structure, composition and function of the retinal interphotoreceptor matrix. In: Progress in Retinal Research. N.N. Osborne and G.J. Chader, eds. Pergamon Press, Oxford, Vol. 10, pp. 207-250.
23. Hageman, G.S., Kirchoff-Rempe, M.A., Lewis, G.P., Fisher, S.K., and Anderson, D.H. (1991) Sequestration of basic fibroblast growth factor in the primate retinal inter-photoreceptor matrix. Proc. Natl. Acad. Sci. U.S.A., 88:67606-67610.
24. Hewitt, A.T., and Newsome, D.A. (1988) Altered proteoglycans in cultured human retinitis pigmentosa retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci., 29:720-726.
25. Ishigooka, H., Kitaoka, T., Boutilier, B., Bost, M., Aotaki-Keen, E., Tablin, F., and Hjelmeland, M. (1993) Developmental expression of bFGF in the bovine retina. Invest. Ophthalmol. Vis. Sci., 34:2813-2823.
26. Jeanny, J.C., Fayein, N.A., Moenner, M., Chevallier, B., Barritault, D., and Courtois, Y. (1987) Specific fixation of bovine brain and retinal acidic and basic fibroblast growth factors to mouse embryonic eye basement membranes. Exp. Cell. Res., 171:63-75.
27. Kiefer, M.C., Stephans, J.C., Crawford, K., Okina, K., and Barr, P. (1990) Ligand affinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. Proc. Natl. Acad. Sci. 87:6985-6989.
28. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227:680-685.
29. Li, L., and Turner, J.E. (1988) Inherited retinal dystrophy in the RCS rat: Prevention of photoreceptor degeneration by pigment epithelial cell transplantation. Exp. Eye Res., 47:911-917.
30. Malecaze, F., Mascarelli, F., Bugra, K., Fuhrmann, G., Courtois, Y., and Hicks, D. (1993) Fibroblast growth factor receptor deficiency in dystrophic retinal pigmented epithelium. J. Cell. Physiol., 154:631-642.
31. Mascarelli, F., Raulais, D., and Courtois, Y. (1989) Fibroblast growth factor phosphorylation and receptors in rod outer segments. EMBO J., 8:2265-2272.
32. Mascarelli, F., Tassin, J., and Courtois, Y. (1991) Effects of FGFs on adult bovine Muller cells: Proliferation, binding and internalization. Growth Factors, 4:81-95.
33. Mascarelli, F., Fuhrmann, G., and Courtois, Y. (1993) aFGF binding to low and high affinity receptors induces both aFGF and aFGF receptors dimerization. Growth Factors, 8:211-233.
34. McKechnie, N.M., Boulton, M.E., Robey, H.C., Savage, F.J., and Grierson, I. (1988) The cytoskeletal elements of human retinal pigment epithelium: In vitro and in vivo. J. Cell. Sci., 91:303-312.
35. Meloche, S., Seuwen, K., Pages, G., and Pouyssegur, J. (1992) Biphasic and synergistic activation of p44 (ERK1) by growth factor: Correlation between late phase activation and mitogenicity. Mol. Endocrinol., 6:845-854.
36. Miyamoto, M., Naruo, K., Seko, C., Matsomoto, S., Kondo, T., and Kurokawa, T. (1993) Molecular cloning of a novel cytokine cDNA encoding the ninth member of the fibroblast growth factor family, which has a unique secretion property. Mol. Cell. Biol., 13:4251-4259.
37. Moscatelli, D. (1987) High and low affinity binding sites for basic fibroblast growth factor on cultured cells: Absence of a role for low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells. J. Cell. Physiol., 131:123-130.
38. Moscatelli, D. (1992) Basic fibroblast growth factor (bFGF) dissociates rapidly from heparan sulfates but slowly from receptors. Implications for mechanisms of release from pericellular matrix. J. Biol. Chem., 267:25803-25809.
39. Moscatelli, D., and Devesly, P. (1990) Turnover of functional basic fibroblast growth factor receptors on the surface of BHK and NIH 3T3 cells. Growth Factors, 3:25-33.
40. Naruo, K., Seko, C., Kuroshima, K., Matsutani, E., Sasada, R., Kondo, T., and Kurokawa, T. (1993) Novel secretory heparin-binding factors from human glioma cells (glia-activating factors) involved in glial cell growth. J. Biol. Chem., 268:2857-2864.
41. Newsome, D.A., Pfeffer, B.A., Hewitt, T.A., Robey, P.G., and Hassell, J.R. (1988) Detection of extracellular matrix molecules synthesized in vitro by monkey and human retinal pigment epithelium: Influence of donor age and multiple passages. Exp. Eye Res., 46:305-321.
42. Nurcombe, V., Ford, M.D., Wildshut, A., and Bartlett, P.F. (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science, 260:103-106.
43. Oliver, L., Raulais, D., and Vigny, M. (1992) Acidic fibroblast growth factor in developing normal and dystrophic (mdx) mouse muscles: Distribution in degenerating and regenerating mdx myofibres. Growth Factors, 7:97-107.
44. Ornitz, D., Yayon, A., Flanagan, G., Svahn, M., Levi, E., and Leder, P. (1992) Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol. Cell. Biol., 12:240-247.
45. Partanen, J., Vainakka, S., Korhonen, J., Armstrong, E., and Alitalo, K. (1992) Diverse receptors for fibroblast growth factor. Prog. Growth Factor Res., 4:69-83.
46. Pfeffer, B.A. (1991) Improved methodology for cell culture of human and monkey retinal pigment epithelium. In: Progress in Retinal Research. N.N. Osborne and G.J. Chader, eds. Pergamon Press, Oxford, Vol. 10, pp. 251-291.
47. Plouët, J., Olivie, M., Courtois, Y., and Barritault, D. (1984) A highly reliable and sensitive assay for the purification of cellular growth factors. J. Cell Mol. Biol., 30:105-110.
48. Plouet, J., Mascarelli, F., Lagente, O., Dorey, C., Lorans, G., Faure, P.P., and Courtois, Y. (1986) Eye-derived growth factor: A component of rod outer segment implicated in phototransduction. In: Retinal Signal Systems Degeneration and Transplants. E. Agardh and B. Ehinger, eds. Elsevier Science, New York, pp. 311-322.
49. Plouet, J., Mascarelli, F., Loret, M., Faure, J.P., and Courtois, Y. (1988) Regulation of eye derived growth factor binding to membranes by light ATP or GTP in photoreceptor outer segment. EMBO J., 7:373-376.
50. Rappraeger, A., and Yeaman, C. (1989) A quantitative solid-phase assay for identifying radiolabelled glycoaminoglycans in crude cell extracts. Anal. Biochem., 98:132-135.
51. Rappraeger, A.C., Krufka, A., and Olwin, B.B. (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science, 252:1705-1708.
52. Reiland, J., and Rappraeger, A.C. (1993) Heparan sulfate proteoglycan and FGF receptor target FGF2 to different intracellular destinations. J. Cell Sci., 105:1085-1093.
53. Rifkin, D., and Moscatelli, D. (1989) Recent developments in the biology of basic fibroblast growth factor. J. Cell Biol., 109:1-6.
54. Rusnati, M., Urbinati, C., and Presta, M. (1993) Internalization of basic fibroblast growth factor (bFGF) in cultured endothelial cells: Role of the low affinity heparin-like bFGF receptor. J. Cell. Physiol., 154:152-161.
55. Saksela, O., Moscatelli, D., Sommer, A., and Rifkin, D.B. (1988) Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell. Biol., 107:743-751.
56. Scatchard, G. (1949) The attraction of proteins for small molecules and ions. Ann. N. Y. Acad. Sci., 51:660-672.
57. Schweigerer, L., Malerstein, B., Neufeld, G., and Gospodarowicz, D. (1987) Basic fibroblast growth factor is synthesized in cultured retinal pigment epithelial cells Biochem. Biophys. Res. Comm., 143:934-960.
58. Spivak-Kroizman, T., Lemmon, M.A., Dikic, J.E., Ladbury, J.E., Pinchasi, D., Huang, J., Jaye, N., Crumley, G., Schleissinger, J. and Lax, I. (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation and cell proliferation. Cell, 79:1015-1024.
59. Sternfeld, M.D., Robertson, J.E., Shipley, G.D., Tsai, J., and Robertson, J.T. (1989) Cultured human retinal pigment epithelial cells express basic fibroblast growth factor and its receptor. Curr. Eye Res., 8:1029-1037.
60. Tanaka, A., Miyanoto, K., Minamino, N., Takeda, M., Sato, B., Matsuo, H., and Matsumoto, K. (1992) Cloning and characterization of an androgen-induced growth factor essential for the androgen-dependent growth of mouse mammary carcinoma cells Proc. Natl. Acad. Sci. U.S.A., 89:8928-8932.
61. Vigny, M., Oliver-Hartman, M P., Lavigne, M., Fayein, N.A., Jeanny, J.C., Laurent, M., and Courtois, Y. (1987) Specific binding to fibroblast growth factor to basement membrane-like structures and to purified heparan sulfate proteoglycan of the EHS tumor. J. Cell. Physiol., 137:321-328.
62. Vlodavsky, I., Arias, Y., Atzman, R., and Fuks, Z. (1982) Tumor cell attachment to the ocular endothelium and subsequent degradation of the subendothelial extracellular matrix. Exp. Cell Res., 140:149-159.
63. Yanagihita, M. (1992) Glycosylphosphoinositol anchored and core protein-internalized heparan sulfate proteoglycan in rat ovarian granulosa cell have distinct secretory, intracellular degratative pathways. J. Cell. Biochem., 267:9505-9511.
64. Yayon, A., Klagsbrun, M., Esko, J.D., Leder, P., and Ornitz, D.M. (1991) Cell surface heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell, 64:841-848.