Role of phosphatidylinositol 3-kinase in friend spleen focus-forming virus-induced erythroid disease

Journal of Virology

Volumn 84, Issue 15, 2010, Pages 7675-7682

  Umehara, Daigo ^a   Watanabe, Shinya ^a   Ochi, Haruyo ^a   Anai, Yukari ^a   Ahmed, Nursarat ^b   Kannagi, Mari ^b   Hanson, Charlotte ^c   Ruscetti, Sandra ^c   Nishigaki, Kazuo ^a  

^a YAMAGUCHI UNIVERSITY   (Japan)

^b Graduate School ^*  (Japan)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL HYPERPLASIA; CELL PROLIFERATION; DRUG INHIBITION; ERYTHROID CELL; ERYTHROLEUKEMIA; ERYTHROPOIESIS; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLEEN; SPLEEN FOCUS FORMING VIRUS; VIRUS STRAIN;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE, TUMOR; LEUKEMIA, ERYTHROBLASTIC, ACUTE; MICE; MICE, INBRED BALB C; RECEPTOR PROTEIN-TYROSINE KINASES; SPLEEN FOCUS-FORMING VIRUSES;

FRIEND SPLEEN FOCUS-FORMING VIRUS; MUS; SPLEEN FOCUS-FORMING VIRUS;

EID: 77954471088     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00488-10     Document Type: Article

References (52)

1. Backer, J. M., M. G. Myers, Jr., S. E. Shoelson, D. J. Chin, X. J. Sun, M. Miralpeix, P. Hu, B. Margolis, E. Y. Skolnik, J. Schlessinger, and M. F. White. 1992. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:3469-3479.
2. Bouscary, D., F. Pene, Y. E. Claessens, O. Muller, S. Chrétien, M. Fontenay-Roupie, S. Gisselbrecht, P. Mayeux, and C. Lacombe. 2003. Critical role for PI 3-kinase in the control of erythropoietin-induced erythroid progenitor proliferation. Blood 101:3436-3443. (Pubitemid 36857926)
3. Cancer Genome Atlas Research Network. 2008. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061-1068.
4. Carpenter, C. L., K. R. Auger, M. Chanudhuri, M. Yoakim, B. Schaffhausen, S. Shoelson, and L. C. Cantley. 1993. Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268:9478-9483.
5. Finkelstein, L. D., P. A. Ney, Q. P. Liu, R. F. Paulson, and P. H. Correll. 2002. Sf-Stk kinase activity and the Grb2 binding site are required for Epo-independent growth of primary erythroblasts infected with Friend virus. Oncogene 21:3562-3570.
6. Fruman, D. A., F. Mauvais-Jarvis, D. A. Pollard, C. M. Yballe, D. Brazil, R. T. Bronson, C. R. Kahn, and L. C. Cantley. 2000. Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85 alpha. Nat. Genet. 26:379-382.
7. Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley. 1999. Impaired B-cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 283:393-397. (Pubitemid 129501102)
8. 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.
9. Hoatlin, M. E., F. E. Ferro, Jr., R. W. Geib, M. T. Fox, S. L. Kozak, and D. Kabat. 1995. Deletions in one domain of the Friend virus-encoded membrane glycoprotein overcome host range restrictions for erythroleukemia. J. Virol. 69:856-863.
10. Huddleston, H., B. Tan, F. C. Yang, H. White, M. J. Wenning, A. Orazi, M. C. Yoder, R. Kapur, and D. A. Ingram. 2003. Functional p85alpha gene is required for normal murine fetal erythropoiesis. Blood 102:142-145.
11. Iwama, A., K. Okano, T. Sudo, Y. Matsuda, and T. Suda. 1994. Molecular cloning of a novel receptor tyrosine kinase gene, STK, derived from enriched hematopoietic stem cells. Blood 83:3160-3169. (Pubitemid 24158460)
12. Iwama, A., N. Yamaguchi, and T. Suda. 1996. STK/RON receptor tyrosine kinase mediates both apoptotic and growth signals via the multifunctional docking site conserved among the HGF receptor family. EMBO J. 15:5866-5875. (Pubitemid 26375508)
13. Jaiswal, B. S., V. Janakiraman, N. M. Kljavin, S. Chaudhuri, H. M. Stern, W. Wang, Z. Kan, H. A. Dbouk, B. A. Peters, P. Waring, T. Dela Vega, D. M. Kenski, K. K. Bowman, M. Lorenzo, H. Li, J. Wu, Z. Modrusan, J. Stinson, M. Eby, P. Yue, J. S. Kaminker, F. J. de Sauvage, J. M. Backer, and S. Seshagiri. 2009. Somatic mutations in p85alpha promote tumorigenesis through class IA PI3K activation. Cancer Cell 16:463-474.
14. Jelacic, T. M., D. Thompson, C. Hanson, J. L. Cmarik, K. Nishigaki, and S. Ruscetti. 2008. The tyrosine kinase sf-Stk and its downstream signals are required for maintenance of Friend spleen focus-forming virus-induced fibroblast transformation. J. Virol. 82:419-427.
15. Katso, R., K. Okkenhaug, K. Ahmadi, S. White, J. Timms, and M. D. Waterfield. 2001. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17:615-675.
16. rr host resistance encodes a small glycoprotein that dimerizes, is processed to cell surfaces, and specifically activates erythropoietin receptors. J. Virol. 67:2611-2620.
17. Li, J., A. D. D'Andrea, H. F. Lodish, and D. Baltimore. 1990. Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature 343:762-764. (Pubitemid 120028609)
18. Lilly, F. 1970. Fv-2: identification and location of a second gene governing the spleen focus response to Friend leukemia virus in mice. J. Natl. Cancer Inst. 45:163-169.
19. Majumdar, M. K., C.-L. Cho, M. T. Fox, K. L. Eckner, S. Kozak, D. Kabat, and R. W. Geib. 1992. Mutations in the env gene of Friend spleen focusforming virus overcome Fv-2r-mediated resistance to Friend virus-induced erythroleukemia. J. Virol. 66:3652-3660.
20. Mayeux, P., I. Dusanter-Fourt, O. Muller, P. Mauduit, 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.
21. Miura, O., N. Nakamura, J. N. Ihle, and N. Aoki. 1994. Erythropoietindependent association of phosphatidylinositol 3-kinase with tyrosine-phosphorylated erythropoietin receptor. J. Biol. Chem. 269:614-620.
22. Moreau-Gachelin, F., D. Ray, M. Mattei, P. Tambourin, and A. Tavitian. 1989. The putative oncogene Spi-1: murine chromosomal localization and transcriptional activation in murine acute erythroleukemias. Oncogene 4:1449-1456.
23. Moreau-Gachelin, F., A. Tavitian, and P. Tambourin. 1988. Spi-1 is a putative oncogene in virally induced murine erythroleukemias. Nature 331:277-280.
24. 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.
25. Muszynski, K. W., D. Thompson, C. Hanson, R. Lyons, A. Spadaccini, and S. K. Ruscetti. 2000. Growth factor-independent proliferation of erythroid cells infected with Friend spleen focus-forming virus is protein kinase C dependent but does not require Ras-GTP. J. Virol. 74:8444-8451.
26. Nishida, K., and T. Hirano. 2003. The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci. 94:1029-1033.
27. Nishigaki, K., C. Hanson, T. Jelacic, D. Thompson, and S. Ruscetti. 2005. Friend spleen focus-forming virus transforms rodent fibroblasts in cooperation with a short form of the receptor tyrosine kinase Stk. Proc. Natl. Acad. Sci. U. S. A. 102:15488-15493.
28. Nishigaki, K., C. Hanson, T. Ohashi, A. Spadaccini, and S. Ruscetti. 2006. Erythroblast transformation by the Friend spleen focus-forming virus is associated with a block in erythropoietin-induced STAT1 phosphorylation and DNA binding and correlates with high expression of the hematopoietic phosphatase SHP-1. J. Virol. 80:5678-5685.
29. Nishigaki, K., C. Hanson, T. Ohashi, D. Thompson, K. Muszynski, and S. Ruscetti. 2000. 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. J. Virol. 74:3037-3045.
30. Nishigaki, K., C. Hanson, D. Thompson, T. Yugawa, and S. Ruscetti. 2005. Activation of the Jun N-terminal kinase pathway by Friend spleen focus-forming virus and its role in the growth and survival of Friend virus-induced erythroleukemia cells. J. Virol. 79:12752-12762.
31. Nishigaki, K., D. Thompson, C. Hanson, T. Yugawa, and S. Ruscetti. 2001. The envelope glycoprotein of Friend spleen focus-forming virus covalently interacts with and constitutively activates a truncated form of the receptor tyrosine kinase Stk. J. Virol. 75:7893-7903.
32. Ohashi, T., M. Masuda, and S. K. Ruscetti. 1995. Induction of sequencespecific DNA-binding factors by erythropoietin and the spleen focus-forming virus. Blood 85:1454-1462.
33. Otsu, M., I. Hiles, I. Gout, M. J. Fry, F. Ruiz-Larrea, G. Panayotou, A. Thompson, R. Dhand, J. Hsuan, N. Totty, A. D. Smith, S. J. Morgan, S. A. Courtneidge, P. J. Parker, and M. D. Waterfield. 1991. Characterization of two 85 kd proteins that associate with receptor tyrosine kinases, middle-T/ pp60c-src complexes, and PI3-kinase. Cell 65:91-104.
34. Parsons, D. W., S. Jones, X. Zhang, J. C. Lin, R. J. Leary, P. Angenendt, P. Mankoo, H. Carter, I. H. Siu, G. L. Gallia, A. Olivi, R. McLendon, B. A. Rasheed, S. Keir, T. Nikolskaya, Y. Nikolsky, D. A. Busam, H. Tekleab, L. A. Diaz, Jr., J. Hartigan, D. R. Smith, R. L. Strausberg, S. K. Marie, S. M. Shinjo, H. Yan, G. J. Riggins, D. D. Bigner, R. Karchin, N. Papadopoulos, G. Parmigiani, B. Vogelstein, V. E. Velculescu, and K. W. Kinzler. 2008. An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807-1812.
35. Paul, R., S. Schuetze, S. L. Kozak, and D. Kabat. 1989. A common site for immortalizing proviral integrations in Friend erythroleukemia: molecular cloning and characterization. J. Virol. 63:4958-4961. (Pubitemid 19257886)
36. Paul, R., S. Schuetze, S. L. Kozak, C. A. Kozak, and D. Kabat. 1991. The Sfpi-1 proviral integration site of Friend erythroleukemia encodes the etsrelated transcription factor Pu.1. J. Virol. 65:464-467.
37. 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.
38. Philp, A. J., I. G. Campbell, C. Leet, E. Vincan, S. P. Rockman, R. H. Whitehead, R. J. Thomas, and W. A. Phillips. 2001. The phosphatidylinositol 3′-kinase p85alpha gene is an oncogene in human ovarian and colon tumors. Cancer Res. 61:7426-7429.
39. Porayette, P., and R. F. Paulson. 2008. BMP4/Smad5 dependent stress erythropoiesis is required for the expansion of erythroid progenitors during fetal development. Dev. Biol. 317:24-35.
40. Richmond, T. D., M. Chohan, and D. L. Barber. 2005. Turning cells red: signal transduction mediated by erthropoietin. Trends Cell Biol. 15:146-155.
41. Rulli, K., T. Yugawa, C. Hanson, D. Thompson, S. Ruscetti, and K. Nishigaki. 2004. Ex vivo and in vivo biological effects of a truncated form of the receptor tyrosine kinase Stk when activated by interaction with the Friend spleen focus-forming virus envelope glycoprotein or by point mutation. J. Virol. 78:4573-4581.
42. Ruscetti, S. K. 1999. Deregulation of erythropoiesis by the Friend spleen focus-forming virus. Int. J. Biochem. Cell Biol. 31:1089-1109.
43. 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.
44. Subramanian, A., S. Hegde, P. Porayette, M. Yon. P. Hankey, and R. F. Paulson. 2008. Friend virus utilizes the BMP4-dependent stress erythropoiesis pathway to induce erythroleukemia. J. Virol. 82:382-393.
45. Suzuki, H., Y. Terauchi, M. Fujiwara, S. Aizawa, Y. Yazaki, T. Kadowaki, and S. Koyasu. 1999. Xid-like immunodeficiency in mice with disruption of the p85alpha subunit of phosphoinositide 3-kinase. Science 283:390-392.
46. Teal, H., S. Ni, J. Xu, L. Finkelstein, A. Cheng, R. Paulson, G. Feng, and P. Correll. 2006. Grb2-mediated recruitment of Gab2, but not Gab1, to Sf-Stk supports the expansion of Friend virus-infected erythroid progenitor cells. Oncogene 25:2433-2443.
47. Terauchi, Y., Y. Tsuji, S. Satoh, H. Minoura, K. Murakami, A. Okuno, K. Inukai, T. Asano, Y. Kaburagi, K. Ueki, H. Nakajima, T. Hanafusa, Y. Matsuzawa, H. Sekihara, Y. Yin, J. C. Barrett, H. Oda, T. Ishikawa, Y. Akanuma, I. Komuro, M. Suzuki, K. Yamamura, T. Kodama, H. Suzuki, K. Yamamura, T. Kodama, H. Suzuki, S. Koyasu, S. Aizawa, K. Tobe, Y. Fukui, Y. Yazaki, and T. Kadowaki. 1999. Increased insulin sensitivity and hypoglycaemia in mice lacking the p85 alpha subunit of phosphoinositide 3-kinase. Nat. Genet. 21:230-235.
48. Wolff, L., R. Koller, and S. Ruscetti. 1982. Monoclonal antibody to spleen focus-forming virus-encoded gp52 provides a probe for the amino-terminal region of retroviral envelope proteins that confers dual tropism and xenotropism. J. Virol. 43:472-481. (Pubitemid 12096319)
49. Wolff, L., and S. Ruscetti. 1985. Malignant transformation of erythroid cells in vivo by introduction of a nonreplicating retrovirus vector. Science 228:1549-1552.
50. Wolff, L., P. Tambourin, and S. Ruscetti. 1986. Induction of the autonomous stage of transformation in erythroid cells infected with SFFV: helper virus is not required. Virology 152:272-276.
51. Wood, L. D., D. W. Parsons, S. Jones, J. Lin, T. Sjöblom, R. J. Leary, D. Shen, S. M. Boca, T. Barber, J. Ptak, N. Silliman, S. Szabo, Z. Dezso, V. Ustyanksky, T. Nikolskaya, Y. Nikolsky, R. Karchin, P. A. Wilson, J. S. Kaminker, Z. Zhang, R. Croshaw, J. Willis, D. Dawson, M. Shipitsin, J. K. Willson, S. Sukumar, K. Polyak, B. H. Park, C. L. Pethiyagoda, P. V. Pant, D. G. Ballinger, A. B. Sparks, J. Hartigan, D. R. Smith, E. Suh, N. Papadopoulos, P. Buckhaults, S. D. Markowitz, G. Parmigiani, K. W. Kinzler, V. E. Velculescu, and B. Vogelstein. 2007. The genomic landscapes of human breast and colorectal cancers. Science 318:1108-1113.
52. Zhang, J., M. S. Randall, M. R. Loyd, W. Li, R. L. Schweers, D. A. Persons, J. E. Rehg, C. T. Noguchi, J. N. Ihle, and P. A. Ney. 2006. Role of erythropoietin receptor signaling in Friend virus-induced erythroblastosis and polycythemia. Blood 107:73-78.