Erythroid cells rendered erythropoietin independent by infection with friend spleen focus-forming virus show constitutive activation of phosphatidylinositol 3-kinase and Akt kinase: Involvement of insulin receptor substrate-related adapter proteins

Journal of Virology

Volumn 74, Issue 7, 2000, Pages 3037-3045

  Nishigaki, Kazuo ^a   Hanson, Charlotte ^b   Ohashi, Takashi ^c   Thompson, Delores ^a   Muszynski, Karen ^b   Ruscetti, Sandra ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMING CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; ERYTHROID CELL; FRIEND LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION; VIRUS INDUCTION; VIRUS INFECTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ENZYME ACTIVATION; ERYTHROCYTES; ERYTHROPOIETIN; FRIEND MURINE LEUKEMIA VIRUS; ONCOGENE PROTEIN V-AKT; PHOSPHOPROTEINS; PHOSPHORYLATION; RECEPTORS, ERYTHROPOIETIN; RETROVIRIDAE PROTEINS, ONCOGENIC; TUMOR CELLS, CULTURED; TYROSINE;

EID: 0034057327     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.7.3037-3045.2000     Document Type: Article

References (70)

1. Akimoto, K., R. Takahashi, S. Moriya, N. Nishioka, J. Takayanagi, K. Kimura, Y. Fukui, S. Osada, K. Mizuno, S. Hirai, A. Kazlauskas, and S. Ohno. 1996. EGF or PDGF receptors activate atypical PKCX through phosphatidylinositol 3-kinase. EMBO J. 15:788-798.
2. Bao, H., S. M. Jacobs-Helber, A. E. Lawson, K. Penta, A. Wickrema, and S. T. Sawyer. 1999. Protein kinase B (c-Akt), phosphatidylinositol 3-kinase, and STAT5 are activated by erythropoietin (EPO) in HCD57 erythroid cells hut are constitutively active in an EPO-independent, apoptosis-resistant subclone (HCD57-SREI cells). Blood 93:3757-3773.
3. Barber, D. L., C. N. Corless, K. Xia, T. M. Roberts, and A. D. D'Andrea. 1997. Erythropoietin activates Raf1 by an She-independent pathway in CTLL-EPO-R cells. Blood 89:55-64.
4. Boudewijn, B. M., and P. J. Coffer. 1995. Protein kinase B (c-Akt) in phosphatidylinositol 3-OH kinase signal transduction. Nature 376:599-602.
5. Carroll, M. P., J. L. Spivak, M. McMahon, N. Weich, and U. F. Rapp. 1991. Erythropoietin induces Raf-1 activation and Raf-1 is required for erythropoietin-mediated proliferation. J. Biol. Chem. 266:14964-14969.
6. Chin, H., A. Arai, H. Wakao, R. Kamiyama, N. Miyasaka, and O. Miura. 1998. Lyn physically associates with the erythropoietin receptor and may play a role in activation of the Stat5 pathway. Blood 91:3734-3745.
7. Chung, S. W., L. Wolff, and S. Ruscetti. 1989. Transmembrane domain of the envelope gene of a polycythemia-inducing retrovirus determines erythropoietin-independent growth. Proc. Natl. Acad. Sci. USA 86:7957-7960.
8. Constanthinescu, S., X. Liu, W. Beyer, A. Fallon, S. Shekar, Y. I. Henis, S. O. Smith, and H. F. Lodish. 1999. Activation of the erythropoietin receptor by the gp55-P viral envelope protein is determined by a single amino acid in its transmembrane domain. EMBO J. 18:3334-3347.
9. Damen, J. E., L. Liu, R. L. Cutler, and G. Krystal. 1993. Erythropoietin stimulates the tyrosine phosphorylation of Shc and its association with Grb2 and a 145-Kd tyrosine phosphorylated protein. Blood 82:2296-2303.
10. Damen, J. E., A. L.-F. Mui, L. Puil, T. Pawson, and G. Krystal. 1993. Phosphatidylinositol 3-kinase associates, via its Src homology 2 domains, with the activated erythropoietin receptor. Blood 81:3204-3210.
11. Damen, J. E., H. Wakao, A. Miyajima, J. Krosl, R. K. Humphries, R. L. Cutler, and G. Krystal. 1995. Tyrosine 343 in the erythropoietin receptor positively regulates erythropoietin-induced cell proliferation and Stat5 activation. EMBO J. 14:5557-5568.
12. Damen, J. E., R. L. Cutler, H. Jiao, T. Yi, and G. Krystal. 1995. Phosphorylation of tyrosine 503 in the erythropoietin receptor (EpR) is essential for binding the P85 subunit of phosphatidylinositol (PI) 3-kinase and for EpR-associated PI 3-kinase activity. J. Biol. Chem. 270:23402-23408.
13. Damen, J. E., L. Liu, P. Rosten, R. K. Humphries, A. B. Jefferson, P. W. Majerus, and G. Krystal. 1996. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 93: 1689-1693.
14. Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241.
15. Del Peso, L., M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez. 1997. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689.
16. Devemy, E., C. Billat, and B. Haye. 1997. Activation of Raf-1 and mitogen-activated proteins kinases by erythropoietin and inositolphosphate-glycan in normal and erythroid progenitor cells: involvement of protein kinase C. Cell. Signal. 9:41-46.
17. Dusanter-Fourt, I. N. C., C. Lacombe, O. Muller, C. Billat, S. Fischer, and P. Mayeux. 1992. Erythropoietin induces the tyrosine phosphorylation of its own receptor in human erythropoietin-responsive cells. J. Biol. Chem. 267: 10670-10675.
18. Franke, T. F., S. I. Yang, T. O. Chan, K. Datta, A. Kazlauskas, D. K. Morrison, D. R. Kaplan, and P. N. Tsichlis. 1995. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
19. Franke, T. F., D. R. Kaplan, L. C. Cantley, and A. Toker. 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 275:665-668.
20. Gobert, S., F. Porteu, S. Pallu, O. Muller, M. Sabbah, I. Dusanler-Fourt, G. Courtois, C. Lacombe, S. Gisselbrecht, and P. Mayeux. 1995. Tyrosine phosphorylation of the erythropoietin receptor: role for differentiation and mitogenic signal transduction. Blood 86:598-606.
21. Gobert, S., S. Chretien, F. Gouilleux, O. Muller, C. Pallard, I. Dusanter-Fourt, B. Groner, C. Lacombe, S. Gisselbrecht, and P. Mayeux. 1996. Identification of tyrosine residues within the intracellular domain of the erythropoietin receptor crucial for STAT5 activation. EMBO J. 15:2434-2441.
22. Gouilleux, F., C. Pallard, I. Dusanter-Fourt, H. Wakao, L.-A. Haldosen, G. Norstedt, D. Levy, and B. Groner. 1995. Prolactin, growth hormone, erythropoietin and granulocyte-macrophage colony stimulating factor induce MGF-Stat5 DNA binding activity. EMBO J. 14:2005-2013.
23. Grammar, T. C., and J. Blenis. 1997. Evidence for MEK-independent pathways regulating the prolonged activation of the ERK-MAP kinases. Oncogene 14:1635-1642.
24. Hanazono, Y., S. Chiba, K. Sasaki, H. Mano, Y. Yazaki, and H. Hirai. 1993. Erythropoietin induces tyrosine phosphorylation and kinase activity of the c-fps/fes proto-oncogene product in human erythropoietin-responsive cells. Blood 81:3193-3196.
25. Haseyama, Y., K. Sawada, A. Oda, K. Koizumi, H. Takano, T. Tarumi, M. Nishio, M. Handa, Y. Ikeda, and T. Koike. 1999. Phosphatidylinositol 3-kinase is involved in the protection of primary cultured human erythroid precursor cells from apoptosis. Blood 94:1568-1577.
26. He, T. C., H. Zhuang, N. Jiang, M. D. Waterfield, and D. M. Wojchowski. 1993. Association of the p85 regulatory subunit of phosphatidylinositol 3-kinase with an essential erythropoietin receptor subdomain. Blood 82:3530-3538.
27. Jacobs-Helber, S. M., A. Wickrema, M. J. Birrer, and S. T. Sawyer. 1998. AP1 regulation of proliferation and initiation of apoptosis in erythropoietin-dependent erythroid cells. Mol. Cell. Biol. 18:3699-3707.
28. S6k. Cell. Signal. 9:175-179.
29. Kavanaugh, W., M. D. A. Pot, S. M. Chin, M. Deuter-Reinhard, A. B. Jefferson, F. A. Norris, F. R. Masiarz, L. S. Cousens, P. W. Majerus, and L. T. Williams. 1996. Multiple forms of an inositol polyphosphate-5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol. 6:438-445.
30. Klingmüller, U., S. Bergelson, J. G. Hsiao, and H. F. Lodish. 1996. Multiple tyrosine residues in the cytosolic domain of the erythropoietin receptor promote activation of STAT5. Proc. Natl. Acad. Sci. USA 93:8324-8328.
31. Klingmüller, U., H. Wu, J. G. Hsiao, A. Toker, B. C. Duckworth, L. C. Cantley, and H. F. Lodish. 1997. Identification of a novel pathway important for proliferation and differentiation of primary erythroid progenitors. Proc. Natl. Acad. Sci. USA 94:3016-3021.
32. Klippel, A., W. M. Kavanaugh, D. Pot, and L. T. Williams. 1997. A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17:338-344.
33. Kobayashi, M., S. Nagata, T. Iwasaki, K. Yanagihara, I. Saitoh, Y. Karouji, S. Ihara, and Y. Fukui. 1999. Dedifferentiation of adenocarcinomas by activation of phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 96: 4874-4879.
34. Kornmann, M., H. Maruyama, U. Bergmann, P. Tangvoranuntakul, H. G. Beger, M. F. White, and M. Korc. 1998. Enhanced expression of the insulin receptor substrate-2 docking protein in human pancreatic cancer. Cancer Res. 58:4250-4254.
35. Lecoq-Lafon, C., F. Verdier, S. Fichelson, S. Chretien, S. Gisselbrecht, C. Lacombe, and P. Mayeux. 1999. Erythropoietin induces the tyrosine phosphorylation of GAB1 and its association with SHC, SHP2 and phosphatidylinositol 3-kinase. Blood 93:2578-2585.
36. Li, D. M., and H. Sun. 1998. PTEN/MMAC1/TEP1 suppresses the tumorigenicity and induces G1 cell cycle arrest in human gliohlastoma cells. Proc. Natl. Acad. Sci. USA 95:15405-15411.
37. Machide, M., H. Mano, and K. Todokoro. 1995. Interleukin 3 and erythropoietin induce association of Vav with Tec kinase through Tec homology domain. Oncogene 11:619-625.
38. Mayeux, P., I. Dusanter-Fourt, O. Muller, P. Maudnit, M. Sabbah, B. Druker, W. Vainchenker, S. Fischer, C. Lacombe, and S. Gisselbrecht. 1993. Erythropoietin induces the association of phosphatidylinositol 3′-kinase with a tyrosine-phosphorylated complex containing the erythropoietin receptor. Eur. J. Biochem. 216:821-828.
39. Miura, O., A. D'Andrea, D. Kabat, and J. N. Ihle. 1991. Induction of tyrosine phosphorylation by the erythropoietin receptor correlates with mitogenesis. Mol. Cell. Biol. 11:4895-4902.
40. Miura, O., N. Nakamura, J. N. Ihle, and N. Aoki. 1994. Erythropoietin-dependent association of phosphatidylinositol 3-kinase with tyrosine-phosphorylated erythropoietin receptor. J. Biol. Chem. 269:614-620.
41. Miura, O., N. Nakamura, F. W. Quelle, B. A. Witthuhn, J. N. Ihle, and N. Aoki. 1994. Erythropoietin induces association of the JAK2 protein tyrosine kinase with the erythropoietin receptor in vivo. Blood 84:1501-1507.
42. Miura, Y., O. Miura, J. N. Ihle, and N. Aoki. 1994. Activation of the mitogen-activated protein kinase pathway by the erythropoietin receptor. J. Biol. Chem. 269:29962-29969.
43. s6k-dependent pathway. Cancer Res. 15:5239-5247.
44. Moriya, S., A. Kazlauskas, K. Akimoto, S.-I. Hirai, K. Mizuno, T. Takenawa, Y. Fukui, Y. Watanabe, S. Ozaki, and S. Ohno. 1996. Platelet-derived growth factor activates protein kinase Cε through redundant and independent signaling pathways involving phospholipase Cγ or phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 93:151-155.
45. Muszynski, K. W., T. Ohashi, C. Hanson, and S. K. Ruscetti. 1998. Both the polycythemia-and anemia-inducing strains of Friend spleen focus-forming virus induce constitutive activation of the Raf-1 mitogen-activated protein kinase signal transduction pathway. J. Virol. 72:919-925.
46. Nakanishi, H., K. A. Brewer, and J. H. Exton. 1993. Activation of the ζ enzyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 258:13-16.
47. Nishida, K., Y. Yoshida, M. Itoh, T. Fukada, T. Ohtani, T. Shirogane, T. Atsumi, M. Takahashi-Tezuka, K. Ishihara, M. Hibi, and T. Hirano. 1999. Gab-family adapter proteins act downstream of cytokine and growth factor receptors and T-and B-cell antigen receptors. Blood 93:1809-1816.
48. Ohashi, T., M. Masuda, and S. K. Ruscetti. 1995. Induction of sequence-specific DNA-binding factors by erythropoietin and the spleen focus-forming virus. Blood 85:1454-1462.
49. Penta, K., and S. T. Sawyer. 1995. Erythropoietin induces the tyrosine phosphorylation, nuclear translocation, and DNA binding of STAT1 and STAT5 in erythroid cells. J. Biol. Chem. 270:31282-31287.
50. Persons, D. A., R. F. Paulson, M. R. Loyd, M. T. Herley, S. M. Bodner, A. Bernstein, P. H. Correll, and P. A. Ney. 1999. Fv2 encodes a truncated form of the Stk receptor tyrosine kinase. Nat. Genet. 23:159-165.
51. Phillips, W. A., F. St. Clair, A. D. Munday, R. J. Thomas, and C. A. Mitchell. 1998. Increased levels of phosphatidylinositol 3-kinase activity in colorectal tumors. Cancer 1:41-47.
52. Quelle, F. W., D. Wang, T. Nosaka, W. E. Thierfelder, D. Stravopodis, Y. Weinstein, and J. N. Ihle. 1996. Erythropoietin induces the activation of STAT5 through association with specific tyrosines on the receptor that are not required for a mitogenic response. Mol. Cell. Biol. 16:1622-1631.
53. Ruscetti, S. K. 1999. Deregulation of erythropoiesis by the Friend spleen focus-forming virus. Int. J. Biochem. Cell Biol. 31:10-35.
54. Ruscetti, S. K., N. J. Janesch, A. Chakraborti, S. T. Sawyer, and W. D. Hankins. 1990. Friend spleen focus-forming virus induces factor independence in an erythropoietin-dependent erythroleukemia cell line. J. Virol. 64: 1057-1062.
55. Shayesteh, L., Y. Lu, W. L. Kuo, R. Baldocchi, T. Godfrey, C. Collins, D. Pinkel, B. Powell, G. B. Mills, and J. W. Gray. 1999. PIK3CA is implicated as an oncogene in ovarian cancer. Nat. Genet. 21:64-65.
56. 1 and Bc1-2. Blood 88:1576-1582.
57. Skorski, T., A. Bellacosa, M. Nieborowska-Skorska, M. Majewski, R. Martinez, J. K. Choi, R. Trotta, P. Wlodarski, D. Perrotti, T. O. Chan, M. A. Wasik, P. N. Tsichlis, and B. Calabretta. 1997. Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3k/Akt-dependent pathway. EMBO 16:6151-6161.
58. Takabashi-Tezuka, M., Y. Yoshida, T. Fukada, T. Ohlani, Y. Yamanaka, K. Nishida, K. Nakujima, M. Hibi, and T. Hirano. 1998. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol. Cell. Biol. 18:4109-4117.
59. Tauchi, T., G.-S. Feng, R. Shen, M. Hoatlin, G. C. Bagby, Jr., D. Kabat, L. Lu, and H. E. Broxmeyer. 1995. Involvement of SH2-containing phosphotyrosine phosphatase Syp in erythropoietin receptor signal transduction pathways. J. Biol. Chem. 270:5631-5635.
60. Tilbrook, P. A., E. Ingley, J. H. Williams, M. L. Hibbs, and S. P. Klinken. 1997. Lyn tyrosine kinase is essential for erythropoietin-induced differentiation of J2E erythroid cells. EMBO J. 16:1610-1619.
61. 3. J. Biol. Chem. 269:32358-32367.
62. GAP tyrosine phosphorylation in human erythroleukemia cells. J. Biol. Chem. 267:8293-8298.
63. Verdier, F., S. Chrétien, C. Billat, S. Gisselbrecht, C. Lacombe, and P. Mayeux. 1997. Erythropoietin induces the tyrosine phosphorylation of insulin receptor substrate-2. J. Biol. Chem. 272:26173-26178.
64. Vlahos, C. J., W. F. Matter, K. Y. Hui, and R. F. Brown. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269:5241-5248.
65. Wakao, H., N. Harada, T. Kitamura, A. L.-F. Mui, and A. Miyajima. 1995. Interleukin 2 and erythropoietin activate STAT5/MGF via distinct pathways. EMBO J. 11:2527-2535.
66. Watowich, S. S., D. J. Hilton, and H. F. Lodish. 1994. Activation and inhibition of erythropoietin receptor function: role of receptor dimerization. Mol. Cell. Biol. 14:3535-3549.
67. Wickrema, A., S. Uddin, A. Sharma, F. Chen, Y. Alsayed, S. Ahmad, S. T. Sawyer, G. Krystal, T. Yi, K. Nishada, M. Hibi, T. Hirano, and L. C. Platanias. 1999. Engagement of Gab1 and Gab2 in erythropoietin signaling. J. Biol. Chem. 274:24469-24474.
68. Witthuhn, B. A., F. W. Quelle, O. Silvennoinen, T. Yi, B. Tang, O. Miura, and J. N. Ihle. 1993. JAK2 associates with the erythropoietin receptor and is tyrosine phosphorylated and activated following stimulation with erythropoietin. Cell 74:227-236.
69. Wu, X., K. Senechal, M. S. Neshat, Y. E. Whang, and C. L. Sawyers. 1998. The PTEN/MMAC1 tumor suppressor phosphatase functions as a negative regulator of the phosphoinositide 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. USA 95:15587-15591.
70. Yamauchi, T., Y. Kaburagi, K. Ueki, Y. Tsuji, G. R. Stark, I. M. Kerr, T. Tsushima, Y. Akanuma, I. Komuro, K. Tobe, Y. Yazaki, and T. Kadowaki. 1998. Growth hormone and prolactin stimulate tyrosine phosphorylation of insulin receptor substrate-1, -2, and -3, their association with p85 phosphatidylinositol 3-kinase (PI 3-kinase), and concomitantly PI 3-kinase activation via JAK2 kinase. J. Biol. Chem. 273:15719-15726.