Basic fibroblast growth factor (FGF-2) is addressed to caveolae after binding to the plasma membrane of BHK cells

European Journal of Cell Biology

Volumn 71, Issue 2, 1996, Pages 144-153

  Gleizes, Pierre Emmanuel ^a,b   Noaillac Depeyre, Jacqueline ^a   Dupont, Marie Ange ^a   Gas, Nicole ^a  

^a CNRS   (France)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basic fibroblast growth factor; Caveolae; Digoxigenin; Electron microscopy; Endocytosis

Indexed keywords

ANTIBODY; DIGOXIGENIN; GOLD; LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLINOSITOL; PHOSPHOLIPASE C; RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CELL STRAIN BHK; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ASSAY;

ANIMALIA;

EID: 0029862822     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Anderson, R. G.: Cavcolac: where incoming and outgoing messengers meet. Proc. Natl. Acad. Sci. USA 90, 10909-10913 (1993).
2. Anderson, R. G.: Plasmalemmal caveolae and GPI-anchored membrane proteins. Curr. Opin. Cell Biol. 5, 647-652 (1993).
3. Anderson, R. G. W., B. A. Kamen, K. G. Rothberg, S. W. Lacey: Potocytosis: sequestration and transport of small molecules by caveolae. Science 255, 410-411 (1992).
4. Bashkin, P., G. Neufeld, H. Gitay-Goren, I. Vlodavsky: Release of cell surface-associated basic fibroblast growth factor by glycosylphosphatidylinositol-specific phospholipase C. J. Cell. Physiol. 151, 126-137 (1992).
5. Basilico, C., D. Moscatelli: The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59, 115-165 (1992).
6. Bikfalvi, A., E. Dupuy, A. L. Inyang, N. Fayein, G. Leseche, Y. Courtois, G. Tobelem: Binding, internalization, and degradation of basic fibroblast growth factor in human microvascular endothelial cells. Exp. Cell Res. 181, 75-84 (1989).
7. Bouche, G., N. Gas, H. Prats, V. Baldin, J. P. Tauber, J. Teissie, F. Amalric: Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE undergoing G0 -G1 transition. Proc. Natl. Acad. Sci. USA 84, 6770-6774 (1987).
8. Brunner, G., J. Gabrilove, D. B. Rifkin, E. L. Wilson: Phospholipase C release of basic fibroblast growth factor from human bone marrow cultures as a biologically active complex with a phosphatidylinositol-anchored heparan sulfate proteoglycan. J. Cell Biol. 114, 1275-1283 (1991).
9. Cesarman, G. M., C. A. Guevara, K. A. Hajjar: An endothelial cell receptor for plasminogen/tissue plasminogen activator (t-PA): II. Annexin II-mediated enhancement of t-PA-dependent plasminogen activation. J. Biol. Chem. 269, 21198-21203 (1994).
10. Chang, W. J., Y. S. Ying, K. G. Rothberg, N. M. Hooper, A. J. Turner, H. A. Gambliel, J. De Gunzburg, S. M. Mumby, A. G. Gilman, R. G. Anderson: Purification and characterization of smooth muscle cell caveolae. J. Cell Biol. 126, 127-138 (1994).
11. Chun, M., U. K. Liyanage, M. P. Lisanti, H. F. Lodish: Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc. Natl. Acad. Sci. USA 91, 11728-11732 (1994).
12. Cisar, L. A., A. J. Hoogewerf, M. Cupp, C. A. Rapport, A. Bensadoun: Secretion and degradation of lipoprotein lipase in cultured adipocytes. J. Biol. Chem. 264, 1767-1774 (1989).
13. Dionne, C. A., G. Crumley, F. Bellot, J. M. Kaplow, G. Searfoss, M. Ruta, W. M. Burgess, M. Jaye, J. Schlessinger: Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J. 9, 2685-2692 (1990).
14. Flaumenhaft, R., D. B. Rifkin: The extracellular regulation of growth factor action. Mol. Biol. Cell 3, 1057-1065 (1992).
15. Frens: Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nature Phys. Sc. 241, 20-22 (1973).
16. Fujimoto, T.: Calcium pump of the plasma membrane is localized in caveolae. J. Cell Biol. 120, 1147-1157 (1993).
17. Fujimoto, T., S. Nakade, A. Miyawaki, K. Mikoshiba, K. Ogawa: Localization of inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae. J. Cell Biol. 119, 1507-1514 (1992).
18. Gannoun-Zaki, L., I. Pieri, J. Badet, M. Moenner, D. Barritault: Internalization of basic fibroblast growth factor by Chinese hamster lung fibroblast cells: involvement of several pathways. Exp. Cell Res. 197, 272-279 (1991).
19. Geoghegan, W. D., G. A. Ackerman: Adsorption of horseradish peroxidase, ovomucoid and anti-immunoglobulin to colloidal gold for the indirect detection of concanavalin A, wheat germ agglutinin and goat anti-human immunoglobulin G on cell surfaces at the electron microscopic level: a new method, theory and application. J. Histochem. Cytochem. 25, 1187-1200 (1977).
20. Ghitescu, L., A. Fixman, M. Simionescu, N. Simionescu: Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis. J. Cell Biol. 102, 1304-1311 (1986).
21. Gleizes, P. E., J. Noaillac-Depeyre, F. Amalric, N. Gas: Basic fibroblast growth factor (FGF-2) internalization through the heparan sulfate proteoglycans-mediated pathway: an ultrastructural approach. Eur. J. Cell Biol. 66, 47-59 (1995).
22. Gleizes, P. E., J. Noaillac-Depeyre, N. Gas: Labeling of basic fibroblast growth factor with digoxigenin: a nonradioactive probe for biochemical and cytological applications. Anal. Biochem. 219, 360-367 (1994).
23. Goldstein, J. L., M. S. Brown, R. G. Anderson, D. W. Russell, W. J. Schneider: Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1, 1-39 (1985).
24. Gospodarowicz, D., J. S. Moran, D. L. Braun, C. R. Birdwell: Clonal growth of bovine vascular endothelial cells: fibroblast growth factor as a survival agent. Proc. Natl. Acad. Sci. USA 73, 4120-4124 (1976).
25. Griffiths, G., R. Back, M. Marsh: A quantitative analysis of the endocytic pathway in baby hamster kidney cells. J. Cell Biol. 109, 2703-2720 (1989).
26. Iozzo, R. V.: Turnover of heparan sulfate proteoglycan in human colon carcinoma cells: a quantitative biochemical and autoradiographic study. J. Biol. Chem. 262, 1888-1900 (1987).
27. Keller, G. A., M. W. Siegel, I. W. Caras: Endocytosis of glycophospholipid-anchored and transmembrane forms of CD4 by different endocytic pathways. EMBO J. 11, 863-874 (1992).
28. Knutson, V. P.: Cellular trafficking and processing of the insulin receptor. FASEB J. 5, 2130-2138 (1991).
29. Lisanti, M. P., P. E. Scherer, J. Vidugiriene, Z. Tang, A. Hermanowski-Vosatka, Y. H. Tu, R. F. Cook, M. Sargiacomo: Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J. Cell Biol. 126, 111-126 (1994).
30. Mason, I. J.: The ins and outs of fibroblast growth factors. Cell 78, 1-20 (1994).
31. Milici, A. J., N. E. Watrous, H. Stukenbrok, G. E. Palade: Transcytosis of albumin in capillary endothelium. J. Cell Biol. 105, 2603-2612 (1987).
32. Moenner, M., L. Gannoun-Zaki, J. Badet, D. Barritault: Internalization and limited processing of basic fibroblast growth factor on Chinese hamster lung fibroblasts. Growth Factors 1, 115-123 (1989).
33. Mommaas-Kienhuis, A. M., L. H. Krijbolder, V. W. M. Van Hinsbergh, W. T. Daems, B. J. Vermeer: Visualization of binding and receptor-mediated uptake of low density lipoproteins by human endothelial cells. Eur. J. Cell Biol. 36, 201-208 (1985).
34. Montesano, R., J. Roth, A. Robert, L. Orci: Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296, 651-653 (1982).
35. Moscatelli, D.: High and low affinity binding sites for basic fibroblast growth factor on cultured cells: absence of a role for the low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells. J. Cell. Physiol. 131, 123-130 (1987).
36. Moscatelli, D.: Metabolism of receptor-bound and matrix-bound basic fibroblast growth factor by bovine capillary endothelial cells. J. Cell Biol. 107, 753-759 (1988).
37. Moscatelli, D., P. Devesly: Turnover of functional basic fibroblast growth factor receptors on the surface of BHK and NIH 3T3 cells. Growth Factors 3, 25-33 (1990).
38. Murphy-Ullrich, J. E., L. G. Westrick, J. D. Esko, D. F. Mosher: Altered metabolism of thrombospondin by Chinese hamster ovary cells defective in glycosaminoglycan synthesis. J. Biol. Chem. 263, 6400-6406 (1988).
39. Neufeld, G., D. Gospodarowicz: Basic and acidic fibroblast growth factors interact with the same cell surface receptors. J. Biol. Chem. 261, 5631-5637 (1986).
40. Okada, S. S., J. E. Tomaszewski, E. S. Barnathan: Migrating vascular smooth muscle cells polarize cell surface urokinase receptors after injury in vitro. Exp. Cell Res. 217, 180-187 (1995).
41. Parton, R. G., B. Joggerst, K. Simons: Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215 (1994).
42. Predescu, D., R. Horvat, S. Predescu, G. E. Palade: Transcytosis in the continuous endothelium of the myocardial microvasculature is inhibited by N-ethylmaleimide. Proc. Natl. Acad. Sci. USA 91, 3014-3018 (1994).
43. Quarto, N., F. Amalric: Heparan sulfate proteoglycans (HSPGs) as transducers of FGF-2 signalling. J. Cell Sci. 107, 3201-3212 (1994).
44. Raposo, G., I. Dunia, C. Delavier-Klutchko, S. Kaveri, A. D. Strosberg, E. L. Benedetti: Internalization of β-adrenergic receptor in A-431 cells involves non-coated vesicles. Eur. J. Cell Biol. 50, 340-352 (1989).
45. Rifkin, D. B., D. Moscatelli: Recent developments in the cell biology of basic fibroblast growth factor. J. Cell Biol. 109, 1-6 (1989).
46. Roghani, M., A. Mansukhani, P. Dell'Era, C. Basilico, D. B. Rifkin, D. Moscatelli: Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J. Biol. Chem. 269, 3976-3984 (1994).
47. Roghani, M., D. Moscatelli: Basic fibroblast growth factor is internalized through both receptor-mediated and heparan sulfate-mediated mechanisms. J. Biol. Chem. 267, 22156-22162 (1992).
48. Ron, D., R. Reich, M. Chedid, C. Lengel, O. E. Cohen, A. M. Chan, G. Neufeld, T. Miki, S. R. Tronick: Fibroblast growth factor receptor 4 is a high affinity receptor for both acidic and basic fibroblast growth factor but not for keratinocyte growth factor. J. Biol. Chem. 268, 5388-5394 (1993).
49. Sa, G., P. L. Fox: Basic fibroblast growth factor-stimulated endothelial cell movement is mediated by a pertussis toxin-sensitive pathway regulating phospholipase A2 activity. J. Biol. Chem. 269, 3219-3225 (1994).
50. Smith, E. P., L. Lu, S. D. Chernausek, D. J. Klein: Insulin-like growth factor-binding protein-3 (IGFBP-3) concentration in rat Sertoli cell-conditioned medium is regulated by a pathway involving association of IGFBP-3 with cell surface proteoglycans. Endocrinology 135, 359-364 (1994).
51. Sorokin, A., G. Carpenter: Interaction of activated EGF receptors with coated pit adaptins. Science 261, 612-615 (1993).
52. Sorokin, A., C. M. Waters: Endocytosis of growth factor receptors. BioEssays 15, 375-382 (1993).
53. Sorokin, A., M. Mohammadi, J. Huang, J. Schlessinger: Internalization of fibroblast growth factor receptor is inhibited by a point mutation at tyrosine 766. J. Biol. Chem. 269, 17056-17061 (1994).
54. Stahl, A., B. M. Mueller: The urokinase-type plasminogen activator receptor, a GPI-linked protein, is localized in caveolae. J. Cell Biol. 129, 335-344 (1995).
55. Stefanova, I., V. Horejsi, I. J. Ansotegui, W. Knapp, H. Stockinger: GPI anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254, 1016-1019 (1991).
56. Tran, D., J.-L. Carpentier, F. Sawano, P. Garden, L. Orci: Ligands internalized through coated or noncoated invaginations follow a common intracellular pathway. Proc. Natl. Acad. Sci. USA 84, 7957-7961 (1987).
57. Van Deurs, B., P. K. Holm, K. Sandvig, S. H. Hansen: Are caveolae involved in clathrin-independent endocytosis. Trends Cell Biol. 3, 249-251 (1993).
58. Vermeer, B. J., L. Havekes, M. C. Wijsman, J. J. Emeis: Immunoelectronmicroscopical investigations on the adsorptive endocytosis of low density lipoproteins by human fibroblasts. Exp. Cell Res. 129, 201-210 (1980).
59. Vlodavsky, I., F. Zvi, R. Ishai-Michaeli, P. Bashkin, E. Levi, G. Korner, R. Bar-Shavit, M. Klagsbrun: Extracellular matrix-resident basic fibroblast growth factor: implication for the control of angiogenesis. J. Cell. Biochem. 45, 167-176 (1991).
60. Yanagishita, M., V. C. Hascall: Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267, 9451-9454 (1992).
61. Yayon, A., M. Klagsbrun, J. D. Esko, P. Leder, D. M. Ornitz: Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848 (1991).
62. Ying, Y. S., R. G. W. Anderson, K. G. Rothberg: Each caveola contains multiple glycosyl-phosphatidylinositol-anchored membrane proteins. Cold Spring Harbor Symposium Quantitative Biology LVII, 593-604 (1992).
63. Zhan, X., C. Plourde, H. Xiaoguo, R. Friesel, T. Maciag: Association of fibroblast growth factor receptor-1 with c-Src correlates with association between c-Src and cortactin. J. Biol. Chem. 269, 20221-20224 (1994).