Thrombopoietin induces activation of the phosphatidylinositol-3' kinase pathway and formation of a complex containing p85(PI3K) and the protooncoprotein p120(CBL)

Journal of Cellular Physiology

Volumn 171, Issue 1, 1997, Pages 28-33

  Sattler, Martin ^a   Salgia, Ravi ^a   Durstin, Melissa A ^a   Prasad, Kanteti V ^a   Griffin, James D ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL KINASE; PROTEIN TYROSINE KINASE; THROMBOPOIETIN; WORTMANNIN;

ARTICLE; CELL GROWTH; CELL MATURATION; ENZYME ACTIVATION; IMMUNOPRECIPITATION; IN VITRO STUDY; MEGAKARYOCYTE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; B-LYMPHOCYTES; CELL LINE; MICE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CBL; SIGNAL TRANSDUCTION; THROMBOPOIETIN; UBIQUITIN-PROTEIN LIGASES;

EID: 0030887288     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199704)171:1<28::AID-JCP4>3.0.CO;2-J     Document Type: Article

References (49)

1. Andoniou, C.E., Thien, C., and Langdon, W.Y. (1994) Tumour induction by activated abl involves tyrosine phosphorylation of the product of the cbl oncogene. EMBO J., 13:4515-4523.
2. Bacon, C.M., Tortolani, P.J., Shimosaka, A., Rees, R.C., Longo, D.L., and Oshea, J.J. (1995) Thrombopoietin (TPO) induces tyrosine phosphorylation and activation of Stat5 and Stat3. FEBS Lett., 370:63-68.
3. Bartley, T.D., Bogenberger, J., Hunt, P., Li, Y.S., Lu, H.S., Martin, F., Chang, M.S., Samal, B., Nichol, J.L., Swift, S., Johnson, M.J., Hsu, R.Y., Parker, V.P., Suggs, S., Skrine, J.D., Merewether, L.A., Clogston, C., Hsu, E., Hokom, M.M., Hornkohl, A., Choi, E., Pangelinan, M., Sun, Y., Mar, V., McNinch, J., Simonet, L., Jacobsen, F., Xie, C., Shutter, J., Chute, H., Basu, R., Selander, L., Trollinger, D., Sieu, L., Padilla, D., Trail, G., Elliott, G., Izumi, R., Covey, T., Crouse, J., Garcia, A., Xu, W., Del Castillo, J., Biron, J., Cole, S., Hu, M.C.-T., Pacifici, R., Ponting, I., Saris, C., Wen, D., Yung, Y.P., Lin, H., and Bosselman, R.A. (1994) Identification and cloning of a megakaryocyte growth and development factor that is a ligand for the cytokine receptor mpl. Cell, 77:1117-1124.
4. Benit, L., Courtois, G., Charon, M., Varlet, P., Dusanterfourt, I., and Gisselbrecht, S. (1994) Characterization of mpl cytoplasmic domain sequences required for myeloproliferative leukemia virus pathogenicity. J. Virol., 68:5270-5274.
5. Berardi, A.C., Wang, A., Levine, J.D., Lopez, P., and Scadden, D.T. (1995) Functional isolation and characterization of human hematopoetic stem cells. Science, 267:104-108.
6. Blake, T.J., Shapiro, M., Morse, H.D., and Langdon, W.Y. (1991) The sequences of the human and mouse c-cbl proto-oncogenes show v-cbl was generated by a large truncation encompassing a proline-rich domain and a leucine zipper-like motif. Oncogene, 6:653-657.
7. Broudy, V.C., Lin, N.L., and Kaushansky, K. (1995) Thrombopoietin (c-Mpl ligand) acts synergistically with erythropoietin, stem cell factor, and interleukin-11 to enhance murine megakaryocyte colony growth and increases megakaryocyte ploidy in vitro. Blood, 85:1719-1726.
8. Cory, G., Lovering, R.C., Hinshelwood, S., MacCarthymorrogh, L., Levinsky, R.J., and Kinnon, C. (1995) The protein product of the c-cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of brutons tyrosine kinase. J. Exp. Med., 182:611-615.
9. Cross, M.J., Stewart, A., Hodgkin, M.N., Kerr, D.J., and Wakelam, M.J.O. (1995) Wortmannin and its structural analogue demethoxyviridin inhibit phospholipase A2 activity in Swiss 3T3 cells - Wortmannin is not a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem., 270:25352-25355.
10. Debili, N., Wendling, F., Cosman, D., Titeux, M., Florindo, C., Dusanter-Fourt, I., Schooley, K., Methia, N., Charon, M., Nador, R., Bettaieb, A., and Vainchenker, W. (1995) The Mpl receptor is expressed in the megakaryocytic lineage from late progenitors to platelets. Blood, 85:391-401.
11. de Sauvage, F.J., Hass, P.E., Spencer, S.D., Malloy, B.E., Gurney, A.L., Spencer, S.A., Darbonne, W.C., Henzel, W.J., Wong, S.C., Kuang, W.J., Oles, K.J., Hultgren, B., Solberg, L.A., Goeddel, D.V., and Eaton, D.L. (1994) Stimulation of megakaryocytopoiesis and thrombopoiesis by the c-Mpl ligand. Nature, 369:533-538.
12. Donovan, J.A., Wange, R.L., Langdon, W.Y., and Samelson, L.E. (1994) The protein product of the c-cbl protooncogene is the 120-kDa tyrosine-phosphorylated protein in Jurkat cells activated via the T cell antigen receptor. J. Biol. Chem., 269:22921-22924.
13. Drachman, J.G., Griffin, J.D., and Kaushansky, K. (1995) The c-Mpl ligand (thrombopoietin) stimulates tyrosine phosphorylation of Jak2, Shc, and c-Mpl. J. Biol. Chem., 270:4979-4982.
14. Fredrickson, T.N., Langdon, W.Y., Hoffman, P.M., Hartley, J.W., and Morse, H.D. (1984) Histologic and cell surface antigen studies of hematopoietic tumors induced by Cas-Br-M murine leukemia virus. J. Natl. Cancer Inst., 72:447-454.
15. Fukazawa, T., Reedquist, K.A., Trub, T., Soltoff, S., Panchamoorthy, G., Druker, B., Cantley, L., Shoelson, S.E., and Band, H. (1995) The SH3 domain-binding T cell tyrosyl phosphoprotein p120-demonstration of its identity with the c-cbl protooncogene product and in vivo complexes with fyn, grb2, and phosphatidylinositol 3-kinase. J. Biol. Chem., 270:19141-19150.
16. Galisteo, M.L., Dikic, I., Batzer, A.G., Langdon, W.Y., and Schlessinger, J. (1995) Tyrosine phosphorylation of the c-cbl proto-oncogene protein product and association with epidermal growth factor (EGF) receptor upon EGF stimulation. J. Biol. Chem., 270:20242-20245.
17. Gurney, A.L., Carvermoore, K., DeSauvage, F.J., and Moore, M.W. (1994) Thrombocytopenia in c-mpl-deficient mice. Science, 265: 1445-1447.
18. Kaushansky, K. (1994) The mpl ligand - molecular and cellular biology of the critical regulator of megakaryocyte development. Stem Cells, 12:91-97.
19. Kaushansky, K., Broudy, V.C., Grossmann, A., Humes, J., Lin, N., Ren, H.P., Bailey, M.C., Papayannopoulou, T., Forstrom, J.W., and Sprugel, K.H. (1995) Thrombopoietin expands erythroid progenitors, increases red cell production, and enhances erythroid recovery after myelosuppressive therapy. J. Clin. Invest., 96:1683-1687.
20. Kim, T.J., Kim, Y.T., and Pillai, S. (1995) Association of activated phosphatidylinositol 3-kinase with p120(cbl) in antigen receptor-ligated B cells. J. Biol. Chem., 270:27504-27509.
21. Kobayashi, M., Laver, J.H., Kato, T., Miyazaki, H., and Ogawa, M. (1995) Recombinant human thromobpoitin (mpl ligand) enhances proliferation of erythroid progenitors. Blood, 86:2494-2499.
22. Langdon, W.Y., Hartley, J.W., Klinken, S.P., Ruscetti, S.K., and Morse, H.D. (1989a) v-cbl, an oncogene from a dual-recombinant murine retrovirus that induces early B-lineage lymphomas. Proc. Natl. Acad. Sci. U.S.A., 86:1168-1172.
23. Langdon, W.Y., Hyland, C.D., Grumont, R.J., and Morse, H.D. (1989b) The c-cbl proto-oncogene is preferentially expressed in thymus and testis tissue and encodes a nuclear protein. J. Virol., 63:5420-5424.
24. Lok, S., Kaushansky, K., Holly, R.D., Kuijper, J.L., Loftonday, C.E., Oort, P.J., Grant, F.J., Heipel, M.D., Burkhead, S.K., Kramer, J.M., Bell, L.A., Sprecher, C.A., Blumberg, H., Johnson, R., Prunkard, D., Ching, A., Mathewes, S.L., Bailey, M.C., Forstrom, J.W., Buddle, M.M., Osborn, S.G., Evans, S.J., Sheppard, P.O., Presnell, S.R., Ohara, P.J., and Foster, D.C. (1994) Cloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivo. Nature, 369:565-568.
25. Marcilla, A., Riverolezcano, O.M., Agarwal, A., and Robbins, K.C. (1995) Identification of the major tyrosine kinase substrate in signaling complexes formed after engagement of Fc-gamma receptors. J. Biol. Chem., 270:9115-9120.
26. Matsuguchi, T., Salgia, R., Hallek, M., Eder, M., Druker, B., Ernst, T.J., and Griffin, J.D. (1994) She phosphorylation in myeloid cells is regulated by granulocyte macrophage colony-stimulating factor, interleukin-3, and steel factor and is constitutively increased by P210BCR/ABL. J. Biol. Chem., 269:5016-5021.
27. Meisner, H., and Czech, M.P. (1995) Coupling of the proto-oncogene product c-cbl to the epidermal growth factor receptor. J. Biol. Chem., 270:25332-25335.
28. Meisner, H., Conway, B.R., Hartley, D., and Czech, M.P. (1995) Interactions of cbl with grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol. Cell. Biol., 15:3571-3578.
29. Mignotte, V., Vigon, I., Decrevecoeur, E.B., Romeo, P.H., Lemarchandel, V., and Chretien, S. (1994) Structure and transcription of the human c-mpl gene (mpl). Genomics, 20:5-12.
30. Odai, H., Sasaki, K., Iwamatsu, A., Hanazono, Y., Tanaka, T., Mitani, K., Yazaki, Y., and Hirai, H. (1995) The proto-oncogene product c-cbl becomes tyrosine phosphorylated by stimulation with GM-CSF or EPO and constitutively binds to the SH3 domain of grb2/ash in human hematopoietic cells. J. Biol. Chem., 270:10800-10805.
31. Okada, T., Sakuma, L., Fukui, Y., Hazeki, O., and Ui, M. (1994) Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase. J. Biol. Chem., 269:3563-3567.
32. Pallard, C., Gouilleux, F., Benit, L., Cocault, L., Souvri, M., Levy, D., Groner, B., Gisselbrecht, S., and Dusanterfourt, I. (1995) Thrombopoietin activates a Stat5-like factor in hematopoietic cells. EMBO J., 14:2847-2856.
33. Prasad, K.V., Janssen, O., Kapeller, R., Raab, M., Cantley, L.C., and Rudd, C.E. (1993a) Src-homology 3 domain of protein kinase p59fyn mediates binding to phosphatidylinositol 3-kinase in T cells. Proc. Natl. Acad. Sci. U.S.A., 90:7366-7370.
34. Prasad, K.V., Kapeller, R., Janssen, O., Repke, H., Duke-Cohan, J.S., Cantley, L.C., and Rudd, C.E. (1993b) Phosphatidylinositol (PI) 3-kinase and PI 4-kinase binding to the CD4-p561ck complex: The p561ck SH3 domain binds to PI 3-kinase but not PI 4-kinase. Mol. Cell. Biol., 13:7708-7717.
35. Rameh, L.E., Chen, C.S., and Cantley, L.C. (1995) Phosphatidylinositol (3,4,5)P-3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell 83:821-830.
36. Rordorf-Nikolic, T., Van Horn, D.J., Chen, D., White, M.F., and Backer, J.M. (1995) Regulation of phosphatidylinositol 3′-kinase by tyrosyl phosphoproteins. Full activation requires occupancy of both SH2 domains in the 85-kDa regulatory subunit. J. Biol. Chem., 270:3662-3666.
37. Sattler, M., Durstin, M.A., Frank, D.A., Okuda, K., Kaushansky, K., Salgia, R., and Griffin, J.D. (1995) The thrombopoietin receptor c-Mpl activates Jak2 and Tyk2 tyrosine kinases. Exp. Hematol. 23:1040-1048.
38. Sattler, M., Salgia, R., Okuda, K., Uemura, N., Durstin, M.A., Pisick, E., Xu, G., Li, J.-L., Prasad, K.V., and Griffin, J.D. (1996) The proto-oncogene product p120CBL and the adaptor proteins CRKL and c-CRK link c-ABL, p190BCR/ABL and p210BCR/ABL to the phosphatidylinositol-3′ kinase pathway. Oncogene, 12:839-846.
39. Skoda, R.C., Seldin, D.C., Chiang, M.K., Peichel, C.L., Vogt, T.F., and Leder, P. (1993) Murine c-mpl: A member of the hematopoietic growth factor receptor superfamily that transduces a proliferative signal. EMBO J., 12:2645-2653.
40. Skorski, T., Kanakaraj, P., Nieborowska-Skorska, M., Ratajczak, M.Z., Wen, S.-C., Zon, G., Gewirtz, A.M., Perussia, B., and Calabretta, B. (1995) Phosphatidylinositol-3-kinase activity is regulated by BCR/ABL and is required for the growth of Philadelphia chromosome-positive cells. Blood, 86:726-736.
41. Sohma, Y., Akahori, H., Seki, N., Hori, T., Ogami, K., Kato, T., Shimada, Y., Kawamura, K., and Miyazaki, H. (1994) Molecular cloning and chromosomal localization of the human thrombopoietin gene. FEBS Lett., 353:57-61.
42. Souyri, M., Vigon, I., Penciolelli, J.F., Heard, J.M., Tambourin, P., and Wendling, F. (1990) A putative truncated cytokine receptor gene transduced by the myeloproliferative leukemia virus immortalizes hematopoietic progenitors. Cell, 63:1137-1147.
43. Tanaka, S., Neff, L., Baron, R., and Levy, J.B. (1995) Tyrosine phosphorylation and translocation of the c-cbl protein after activation of kinase signaling pathways. J. Biol. Chem., 270:14347-14351.
44. Vigon, I., Mornon, J.P., Cocault, L., Mitjavila, M.T., Tambourin, P., Gisselbrecht, S., and Souyri, M. (1992) Molecular cloning and characterization of MPL, the human homolog of the v-mpl oncogene: Identification of a member of the hematopoietic growth factor receptor superfamily. Proc. Natl. Acad. Sci. U.S.A., 89:5640-5644.
45. Vigon, I., Florindo, C., Fichelson, S., Guenet, J.L., Mattei, M.G., Souyri, M., Cosman, D., and Gisselbrecht, S. (1993) Characterization of the murine Mpl proto-oncogene, a member of the hematopoietic cytokine receptor family: Molecular cloning, chromosomal location and evidence for a function in cell growth. Oncogene, 8:2607-2615.
46. Wendling, F., Maraskovsky, E., Debili, N., Florindo, C., Teepe, M., Titeux, M., Methia, N., Bretongorius, J., Cosman, D., and Vainchenker, W. (1994) C-mpl ligand is a humoral regulator of megakaryocytopoiesis. Nature, 369:571-574.
47. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y., and Matsuda, Y. (1993) Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem., 268:25846-25856.
48. Yao, R.J., and Cooper, G.M. (1995) Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science, 267:2003-2006.
49. Yoon, C.H., Lee, J.H., Jongeward, G.D., and Sternberg, P.W. (1995) Similarity of sli-1, a regulator of vulval development in C-elegaus, to the mammalian proto-oncogene c-cbl. Science, 269:1102-1105.