Interaction of folate receptor with signaling molecules lyn and Gα(i-3) in detergent-resistant complexes from the ovary carcinoma cell line IGROV1

Journal of Cell Science

Volumn 113, Issue 2, 2000, Pages 349-357

  Miotti, Silvia ^a   Bagnoli, Marina ^a   Tomassetti, Antonella ^a   Colnaghi, Maria Ines ^a   Canevari, Silvana ^a  

^a Unit of Molecular Therapies   (Italy)

Author keywords

Folate receptor; GPI linked protein; Heterotrimeric G protein; p53 56 lyn; Triton insoluble domain

Indexed keywords

CAVEOLIN; FOLIC ACID; MESSENGER RNA; MONOCLONAL ANTIBODY; PHOSPHOLIPASE C; PROTEIN P53; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; TRITON X 100;

ARTICLE; CANCER CELL CULTURE; CARCINOMA CELL; CELL PROLIFERATION; IMMUNOPRECIPITATION; MODEL; PRIORITY JOURNAL;

CARRIER PROTEINS; CAVEOLIN 1; CAVEOLINS; DETERGENTS; FEMALE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HUMANS; MEMBRANE PROTEINS; OCTOXYNOL; OVARIAN NEOPLASMS; RECEPTORS, CELL SURFACE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOLUBILITY; SRC-FAMILY KINASES; TUMOR CELLS, CULTURED;

EID: 0033960584     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Alberti, S., Miotti, S., Fornaro, M., Mantovani, L., Walter, S., Canevari, S., Ménard, S. and Colnaghi, M. I. (1990). The Ca-MOv18 molecule, a cell-surface marker of human ovarian carcinomas, is anchored to the cell membrane by phosphatidylinositol. Biochem. Biophys. Res. Commun. 171, 1051-1055.
2. Anderson, R. G. W., Kamen, B. A., Rothberg, K. G. and Lacey, S. W. (1992). Potocytosis: Sequestration and transport of small molecules by caveolae. Science 255, 410-411.
3. Anderson, R. G. W. (1998). The caveolae membrane system. Annu. Rev. Biochem. 67, 199-225.
4. Antony, A. C. (1996). Folate receptors. Annu. Rev. Nutr. 16, 501-521.
5. Bottero, F., Tomassetti, A., Canevari, S., Miotti, S., Ménard, S. and Colnaghi, M. I. (1993). Gene transfection and expression of the ovarian carcinoma marker folate binding protein on NIH/3T3 cells increases cell growth in vitro and in vivo. Cancer Res. 53, 5791-5796.
6. Brown, D. A. and Rose, J. K. (1992). Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
7. Buj-Bello, A., Adu, J., Piñón, L. G. P., Horton, A., Thompson, J., Rosenthal, A., Chinchetru, M., Buchman, V. L. and Davies, A. M. (1997). Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature 387, 721-724.
8. Burkhardt, A. L., Brunswick, M., Bolen, J. B. and Mond, J. J. (1991). Anti-immunoglobulin stimulation of B lymphocytes activates src-related protein tyrosine kinases. Proc. Nat. Acad. Sci. USA 88, 7410-7414.
9. Campbell, M. A. and Sefton, B. M. (1992). Association between B-lymphocyte membrane immunoglobulin and multiple members of the src family of protein tyrosine kinases. Mol. Cell Biol. 12, 2315-2321.
10. Chang, W.-J., Ying, Y., Rothberg, K. G., Hooper, N. M., Turner, A. J., Gambliel, H. A., De Gunzburg, J., Mumby, S. M., Gilman, A. G. and Anderson, R. G. W. (1994). Purification and characterization of smooth muscle cell caveolae. J. Cell Biol. 126, 127-138.
11. ras GAP association with fyn. lyn. and yes in thrombin-activated platelets. J. Biol. Chem. 267, 5025-5028.
12. Coney, L. R., Tomassetti, A., Carayannopoulos, L., Frasca, V., Kamen, B. A., Colnaghi, M. I. and Zurawski, V. R., Jr (1991). Cloning of a tumor-associated antigen: MOv18 and MOv19 antibodies recognize a folate-binding protein. Cancer Res. 51, 6125-6132.
13. Coney, L. R., Mezzanzanica, D., Sanborn, D., Casalini, P., Colnaghi, M. I. and Zurawski, V. R., Jr (1994). Chimeric murine-human antibodies directed against folate binding receptor are efficient mediators of ovarian carcinoma cell killing. Cancer Res. 54, 2448-2455.
14. Corey, S., Eguinoa, A., Puyana-Theall, K., Bolen, J. B., Cantley, L., Mollinedo, F., Jackson, T. R., Hawkins, P. T. and Stephens, L. R. (1993). Granulocyte macrophage-colony stimulating factor stimulates both association and activation of phosphoinositide 3OH-kinase and src-related tyrosine kinase(s) in human myeloid derived cells. EMBO J. 12. 2681-2690.
15. Corey, S. J., Burkhardt, A. L., Bolen, J. B., Geahlen, R. L., Tkatch, L. S. and Tweardy, D. J. (1994). Granulocyte colony-stimulating factor receptor signaling involves the formation of a three-component complex with lyn and syk protein-tyrosine kinases. Proc. Nat. Acad. Sci. USA 91, 4683-4687.
16. lyn: a new signaling pathway in human endometrium and endomerial adenocarcinomas. J. Soc. Gynecol. Invest. 4, 103-109.
17. Couet, J., Sargiacomo, M. and Lisanti, M. P. (1997). Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem. 272, 30429-30438.
18. Doyle, D. D., Goings, G. E., Upshaw-Earley, J., Page, E., Ranscht, B. and Palfrey, H. C. (1998). T-cadherin is a major glycophosphoinositol-anchored protein associated with noncaveolar detergent-insoluble domains of the cardiac. J. Biol. Chem. 273, 6937-6943.
19. Dumler, I., Weis, A., Mayboroda, O. A., Maasch, C., Jerke, U., Haller, H. and Gulba, D. C. (1998). The Jak/Stat pathway and urokinase receptor signaling inhuman aortic vascular smooth muscle cells. J. Biol. Chem. 273, 315-321.
20. Engelman, J. A., Wykoff, C. C., Yasuhara, S., Song, K. S., Okamoto, T. and Lisanti, M. P. (1997). Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J. Biol. Chem. 272, 16374-16381.
21. Engelman, J. A., Lee, R. J., Karnezis, A., Bearss, D. J., Webster, M., Siegel, P., Muller, W. J., Windle, J. J., Pestell, R. G. and Lisanti, M. P. (1998). Reciprocal regulation of neu tyrosine kinase activity and caveolin-1 protein expression in vitro and in vivo - Implications for human breast cancer. J. Biol. Chem. 273, 20448-20455.
22. Fra, A. M., Williamson, E., Simons, K. and Parton, R. G. (1994). Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269, 30745-30748.
23. Friedrichson, T. and Kurzchalia, T. V. (1998). Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394, 802-805.
24. Garin-Chesa, P., Campbell, I., Saigo, P. E., Lewis, J. L., Jr, Old, L. J. and Rettig, W. J. (1993). Trophoblast and ovarian cancer antigen LK26: Sensitivity and specificity in immunopathology and molecular identification as a folate-binding protein. Am. J. Pathol. 142, 557-567.
25. Gorodinsky, A. and Harris, D. A. (1995). Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J. Cell Biol. 129, 619-627.
26. Hanada, K., Nishijima, M., Akamatsu, Y. and Pagano, R. E. (1995). Both sphingolipids and cholesterol participate in the detergent insolubility of alkaline phosphatase, a glycosylphosphatidylinositol-anchored protein, in mammalian membranes. J. Biol. Chem. 270, 6254-6260.
27. Hooper, N. M. and Turner, A. J. (1988). Ectoenzymes of the kidney microvillar membrane. Biochem. J. 250, 865-869.
28. Kamen, B. A., Smith, A. K. and Anderson, R. G. W. (1991). The folate receptor works in tandem with a probenecid-sensitive carrier in MA104 cells in vitro. J. Clin. Invest. 87, 1442-1449.
29. Klein, R. D., Sherman, D., Ho, W. H., Stone, D., Bennett, G. L., Moffat, B., Vandlen, R., Simmons, L., Gu, Q. M., Hongo, J. A., et al. (1997). A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature 387, 717-721.
30. Koleske, A. J., Baltimore, D. and Lisanti, M. P. (1995). Reduction of caveolin and caveolae in oncogenically transformed cells. Proc. Nat. Acad. Sci. USA 92, 1381-1385.
31. Koshelnick, Y., Ehart, M., Hufnagl, P., Heinrich, P. C. and Binder, B. R. (1997). Urokinase receptor is associated with the components of the JAK1/STAT1 signaling pathway and leads to activation of this pathway upon receptor clustering in the human kidney epithelial tumor cell line TCL-598. J. Biol. Chem. 272, 28563-28567.
32. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
33. Lee, S. W., Reimer, C. L., Oh, P., Campbell, D. B. and Schnitzer, J. E. (1998). Tumor cell growth inhibition by caveolin re-expression in human breast cancer cell. Oncogene 16, 1391-1397.
34. Li, S., Okamoto, T., Chun, M., Sargiacomo, M., Casanova, J. E., Hansen, S. H., Nishimoto, I. and Lisanti, M. P. (1995). Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J. Biol. Chem. 270, 15693-15701.
35. Li, S. W., Couet, J. and Lisanti, M. P. (1996). Src tyrosine kinases, Gα subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin - Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J. Biol. Chem. 271, 29182-29190.
36. Liu, J., Oh, P., Horner, T., Rogers, R. A. and Schnitzer, J. E. (1997). Organized endothelial cell surface signal transduction in caveolae distinct from glycosylphosphatidylinositol-anchored protein microdomains. J. Biol. Chem. 272, 7211-7222.
37. Maeda, M. and Firtel, R. A. (1997). Activation of the mitogen-activated protein kinase ERK2 by the chemoattractant folic acid in dictyostelium. J. Biol. Chem. 272, 23690-23695.
38. Mayor, S., Rothberg, K. G. and Maxfield, F. R. (1994). Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 264, 1948-1951.
39. Miotti, S., Canevari, S., Ménard, S., Mezzanzanica, D., Porro, G., Pupa, S. M., Regazzoni, M., Tagliabue, E. and Colnaghi, M. I. (1987). Characterization of human ovarian carcinoma-associated antigens defined by novel monoclonal antibodies with tumor-restricted specificity. Int. J. Cancer 39, 297-303.
40. Miotti, S., Facheris, P., Tomassetti, A., Bottero, F., Bottini, C., Ottone, F., Colnaghi, M. I., Bunni, M. A., Priest, D. G. and Canevari, S. (1995) Growth of ovary carcinoma cell lines at physiological folate concentration: effect on folate binding protein expression in vitro and in vivo. Int. J. Cancer 63, 395-401.
41. Miotti, S., Bagnoli, M., Ottone, F., Tomassetti, A., Colnaghi, M. I. and Canevari, S. (1997). Simultaneous activity of two different mechanisms of folate transport in ovarian carcinoma cell lines. J. Cell. Biochem. 65, 479-491.
42. Mirshahi, S. S., Lounes, K. C., Lu, H., Pujade-Lauraine, E., Mishal, Z., Bénard, J., Bernadou, A., Soria, C. and Soria, J. (1997). Defective cell migration in an ovarian cancer cell line is associated with impaired urokinase-induced tyrosine phosphorylation. FEBS Lett. 411, 322-326.
43. Neer, E. J. (1995). Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80, 249-257.
44. Okamoto, T., Schlehel, A., Scherer, P. E. and Lisanti, M. P. (1998). Caveolins, a family of scaffolding proteins for organizing 'preassempled signaling complexes' at the plasma membrane. J. Biol. Chem. 273, 5419-5422.
45. Park, S. and Sanchez, M. P. (1997). The Eek receptor, a member of the Eph family of tyrosine protein kinases, can be activated by three different Eph family ligands. Oncogene 14, 533-542.
46. Parkin, E. T., Turner, A. J. and Hooper, N. M. (1996). Isolation and characterization of two distinct low-density, Triton-insoluble, complexes from porcine lung membranes. Biochem. J. 319, 887-896.
47. Peles, E., Nativ, M., Lustig, M., Grumet, M., Schilling, J., Martinez, R., Plowman, G. D. and Schlessinger, J. (1997). Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J. 16, 978-988.
48. Robinson, P. J. (1991). Phosphatidylinositol membrane anchors and T-cell activation. Immunol. Today 12, 35-41.
49. Rothberg, K. G., Ying, Y.-S., Kamen, B. A. and Anderson, R. G. W. (1990). Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J. Cell Biol. 111, 2931-2938.
50. Rothberg, K. G., Heuser, E., Donzell, W. C., Ying, Y.-S., Glenney, J. R., Jr and Anderson, R. G. W. (1992). Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682.
51. Sargiacomo, M., Sudol, M., Tang, Z. and Lisanti, M. P. (1993). Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122, 789-807.
52. Schnitzer, J. E., McIntosh, D. P., Dvorak, A. M., Liu, J. and Oh, P. (1995). Separation of caveolae from associated microdomains of GPI-anchored proteins. Science 269, 1435-1439.
53. Schroeder, R. J., Ahmed, S. N., Zhu, Y. Z., London, E. and Brown, D. A. (1998). Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273, 1150-1157.
54. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
55. Smart, E. J., Ying, Y. S., Mineo, C. and Anderson, R. G. W. (1995). A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc. Nat. Acad. Sci. USA 92, 10104-10108.
56. Solomon, K. R., Rudd, C. E. and Finberg, R. W. (1996). The association between glycosylphosphatidylinositol-anchored proteins and heterotrimeric G protein α subunits in lymphocytes. Proc. Nat. Acad. Sci. USA 93, 6053-6058.
57. Solomon, K. R., Mallory, M. A., Hanify, K. A. and Finberg, R. W. (1998). The nature of membrane anchorage determines kinase associations and detergent solubility of CD4. Biochem. Biophys. Res. Commun. 242, 423-428.
58. Song, K. S., Li, S., Okamoto, T., Quilliam, L. A., Sargiacomo, M. and Lisanti, M. P. (1996). Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. J. Biol. Chem. 271, 9690-9697.
59. Stefanova, I., Horejsi, V., Ansotegui, I. J., Knapp, W. and Stockinger, H. (1991). GPI-anchored cell suface molecules complexes to protein tyrosine kinases. Science 254, 1016-1019.
60. Stulnig, T. M., Berger, M., Sigmund, T., Stockinger, H., Horejsi, V. and Waldhäusl, W. (1997). Signal transduction via glycosyl phosphatidylinositol-anchored proteins in T cells is inhibited by lowering cellular cholesterol. J. Biol. Chem. 272, 19242-19247.
61. fyn protein tyrosine kinase in T cells. J. Biol. Chem. 267, 12317-12322.
62. Tilbrook, P. A., Ingley, E., Williams, J. H., Hibbs, M. L. and Klinken, S. P. (1997). Lyn tyrosine kinase is essential for erythropoietin-induced differentiation of J2E erythroid cells. EMBO J. 16, 1610-1619.
63. Toffoli, G., Cernigoi, C., Russo, A., Gallo, A., Bagnoli, M. and Boiocchi, M. (1997). Overexpression of folate binding protein in ovarian cancers. Int. J. Cancer 74, 193-198.
64. Torigoe, T., Saragovi, H. U. and Reed, J. C. (1992). Interleukin 2 regulates the activity of the lyn protein-tyrosine kinase in a B-cell line. Proc. Nat. Acad. Sci. USA 89, 2674-2678.
65. Varma, R. and Mayor, S. (1998). GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798-801.
66. Wu, C. B., Butz, S., Ying, Y. S. and Anderson, R. G. W. (1997). Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J. Biol. Chem. 272, 3554-3559.
67. Yamamoto, T., Yamanashi, Y. and Toyoshima, K. (1993). Association of src-family kinase lyn with B-cell antigen receptor. Immunol. Rev. 132, 187-206.
68. Yamanashi, Y., Fukui, Y., Wongsasant, B., Kinoshita, Y., Ichimori, Y., Toyoshima, K. and Yamamoto, T. (1992). Activation of src-like protein-tyrosine kinase lyn and its association with phosphatidylinositol 3-kinase upon B-cell antigen receptor-mediated signaling. Proc. Nat. Acad. Sci. USA 89, 1118-1122.
69. Ying, Y.-S., Anderson, R. G. W. and Rothberg, K. G. (1992). Each caveola contains multiple glycosyl-phosphatidylinositol-anchored membrane proteins. Cold Spring Harbor Symposia on Quantitative Biology. LVII, 593-604.