Erythropoietin stimulates phosphorylation and activation of GATA-1 via the PI3-kinase/AKT signaling pathway

Blood

Volumn 107, Issue 3, 2006, Pages 907-915

  Zhao, Wei ^b   Kitidis, Claire ^b   Fleming, Mark D ^b   Lodish, Harvey F ^b   Ghaffari, Saghi ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR GATA 1;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROID PRECURSOR CELL; FETUS; FETUS LIVER; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 31544481433     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-06-2516     Document Type: Article

References (72)

1. Wu H, Liu X, Jaenisch R, Lodish HF. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 1995;83:59-67.
2. Lin CS, Lim SK, D'Agati V, Costantini F. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev. 1996;10:154-164.
3. Kieran MW, Perkins AC, Orkin SH, Zon LI. Thrombopoietin rescues in vitro erythroid colony formation from mouse embryos lacking the erythropoietin receptor. Proc Natl Acad Sci U S A. 1996;93:9126-9131.
4. Ghaffari S, Huang LJS, Zhang J, Lodish HF. Erythropoietin receptor signaling processes. In: Molineux G, Foote MA, Elliott SG, eds. Erythropoietins and Erythropoiesis. Basel, Switzerland: Birkhauser; 2003.
5. -/- erythroid progenitors and replaces EpoR in a synergistic interaction with c-kit. Blood. 1998;92:1491-1496.
6. Ghaffari S, Kitidis C, Fleming MD, Neubauer H, Pfeffer K, Lodish HF. Erythropoiesis in the absence of janus-kinase 2: BCR-ABL induces red cell formation in JAK2(-/-) hematopoietic progenitors. Blood. 2001;98:2948-2957.
7. Papayannopoulou T, Brice M, Blau CA. Kit ligand in synergy with interleukin-3 amplifies the erythropoietin-independent, globin-synthesizing progeny of normal human burst-forming units-erythroid in suspension cultures: physiologic implications. Blood. 1993;81:299-310.
8. Klingmuller U, Wu H, Hsiao JG, et al. Identification of a novel pathway important for proliferation and differentiation of primary erythroid progenitors. Proc Natl Acad Sci U S A. 1997;94:3016-3021.
9. Huddleston H, Tan B, Yang FC, et al. Functional p85alpha gene is required for normal murine fetal erythropoiesis. Blood. 2003;102:142-145.
10. Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood. 2005;105:4477-4483.
11. Cho H, Thorvaldsen JL, Chu Q, Feng F, Birnbaum MJ. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem. 2001;276:38349-38352.
12. Cho H, Mu J, Kim JK, et al. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science. 2001;292:1728-1731.
13. Chen WS, Xu PZ, Gottlob K, et al. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 2001;15:2203-2208.
14. Peng XD, Xu PZ, Chen ML, et al. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 2003;17:1352-1365.
15. Easton RM, Cho H, Roovers K, et al. Role for Akt3/Protein Kinase Bγ in attainment of normal brain size. Mol Cell Biol. 2005;25:1869-1878.
16. Brazil DP, Yang ZZ, Hemmings BA. Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci. 2004;29:233-242.
17. Haseyama Y, Sawada K, Oda A, et al. Phosphatidylinositol 3-kinase is involved in the protection of primary cultured human erythroid precursor cells from apoptosis. Blood. 1999;94:1568-1577.
18. Henry M, Lynch J, Eapen A, Quelle FW. DNA damage-induced cell-cycle arrest of hematopoietic cells is overridden. Blood. 2001;98:834-841.
19. Bao H, Jacobs-Helber SM, Lawson AE, Penta K, Wickrema A, Sawyer ST. Protein kinase B (c-Akt), phosphatidylinositol 3-kinase, and STAT5 are activated by erythropoietin (EPO) in HCD57 erythroid cells but are constitutively active in an EPO-independent, apoptosis-resistant subclone (HCD57-SREI cells). Blood. 1999;93:3757-3773.
20. Nishigaki K, Hanson C, Ohashi T, Thompson D, Muszynski K, Ruscetti S. 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. 2000;74:3037-3045.
21. Kashii Y, Uchida M, Kirito K, et al. A member of Forkhead family transcription factor, FKHRL1, is one of the downstream molecules of phosphatidylinositol 3-kinase-Akt activation pathway in erythropoietin signal transduction. Blood. 2000;96:941-949.
22. Bouscary D, Pene F, Claessens YE, et al. Critical role for PI 3-kinase in the control of erythropoietin-induced erythroid progenitor proliferation. Blood. 2003;101:3436-3443.
23. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002;21:3368-3376.
24. Fujiwara Y, Browne CP, Cunniff K, Goff SC, Orkin SH. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci U S A. 1996;93:12355-12358.
25. Weiss MJ, Keller G, Orkin SH. Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev. 1994;8:1184-1197.
26. Weiss MJ, Orkin SH. Transcription factor GATA-1 permits survival and maturation of erythroid precursors by preventing apoptosis. Proc Natl Acad Sci U S A. 1995;92:9623-9627.
27. Gregory T, Yu C, Ma A, Orkin SH, Blobel GA, Weiss MJ. GATA-1 and erythropoietin cooperate to promote erythroid cell survival by regulating bcl-xL expression. Blood. 1999;94:87-96.
28. Rylski M, Welch JJ, Chen YY, et al. GATA-1-mediated proliferation arrest during erythroid maturation. Mol Cell Biol. 2003;23:5031-5042.
29. Welch JJ, Watts JA, Vakoc CR, et al. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood. 2004;104:3136-3147.
30. Leonard M, Brice M, Engel JD, Papayannopoulou T. Dynamics of GATA transcription factor expression during erythroid differentiation. Blood. 1993;82:1071-1079.
31. Kapur R, Zhang L. A novel mechanism of cooperation between c-Kit and erythropoietin receptor. Stem cell factor induces the expression of Stat5 and erythropoietin receptor, resulting in efficient proliferation and survival by erythropoietin. J Biol Chem. 2001;276:1099-1106.
32. Ghaffari S, Wu H, Gerlach M, Han Y, Lodish HF, Daley GQ. BCR-ABL and v-SRC tyrosine kinase oncoproteins support normal erythroid development in erythropoietin receptor-deficient progenitor cells. Proc Natl Acad Sci U S A. 1999;96:13186-13190.
33. Brunet A, Bonni A, Zigmond MJ, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999;96:857-868.
34. Ghaffari S, Jagani Z, Kitidis C, Lodish HF, Khosravi-Far R. Cytokines and BCR-ABL mediate suppression of TRAIL-induced apoptosis through inhibition of forkhead FOXO3a transcription factor. Proc Natl Acad Sci U S A. 2003;100:6523-6528.
35. Alessi DR, Caudwell FB, Andjelkovic M, Hemmings BA, Cohen P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 1996;399:333-338.
36. Crossley M, Orkin SH. Phosphorylation of the erythroid transcription factor GATA-1. J Biol Chem. 1994;269:16589-16596.
37. Whyatt D, Lindeboom F, Karis A, et al. An intrinsic but cell-nonautonomous defect in GATA-1-overexpressing mouse erythroid cells. Nature. 2000;406:519-524.
38. Park J, Leong ML, Buse P, Maiyar AC, Firestone GL, Hemmings BA. Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI 3-kinase-stimulated signaling pathway. EMBO J. 1999;18:3024-3033.
39. Weiss MJ, Yu C, Orkin SH. Erythroid-cell-specific properties of transcription factor GATA-1 revealed by phenotypic rescue of a gene-targeted cell line. Mol Cell Biol. 1997;17:1642-1651.
40. Andjelkovic M, Alessi DR, Meier R, et al. Role of translocation in the activation and function of protein kinase B. J Biol Chem. 1997;272:31515-31524.
41. Meier R, Alessi DR, Cron P, Andjelkovic M, Hemmings BA. Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bbeta. J Biol Chem. 1997;272:30491-30497.
42. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for antiestrogen resistance. J Biol Chem. 2001;276:9817-9824.
43. Vojtek AB, Taylor J, DeRuiter SL, et al. Akt regulates basic helix-loop-helix transcription factor-coactivator complex formation and activity during neuronal differentiation. Mol Cell Biol. 2003;23:4417-4427.
44. Taxman DJ, Wojchowski DM. Erythropoietin-induced transcription at the murine beta maj-globin promoter. A central role for GATA-1. J Biol Chem. 1995;270:6619-6627.
45. Partington GA, Patient RK. Phosphorylation of GATA-1 increases its DNA-binding affinity and is correlated with induction of human K562 erythroleukaemia cells. Nucleic Acids Res. 1999;27:1168-1175.
46. Vannucchi AM, Bianchi L, Cellai C, et al. Accentuated response to phenylhydrazine and erythropoietin in mice genetically impaired for their GATA-1 expression (GATA-1(low) mice). Blood. 2001;97:3040-3050.
47. Papayannopoulou T, Abkowitz J, A. DA. Biology of erythropoiesis, erythroid differentiation, and maturation. In: Hoffman R, Benz EJ, Shattil SJ, et al, eds. Hematology, Basic Principles and Practice. New York, NY: Churchill Livingstone; 2000:202-219.
48. Zandstra PW, Conneally E, Petzer AL, Piret JM, Eaves CJ. Cytokine manipulation of primitive human hematopoietic cell self-renewal. Proc Natl Acad Sci U S A. 1997;94:4698-4703.
49. Zeng H, Masuko M, Jin L, Neff T, Otto KG, Blau CA. Receptor specificity in the self-renewal and differentiation of primary multipotential hemopoietic cells. Blood. 2001;98:328-334.
50. Omichinski JG, Clore GM, Schaad O, et al. NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science. 1993;261:438-446.
51. Briegel K, Bartunek P, Stengl G, et al. Regulation and function of transcription factor GATA-1 during red blood cell differentiation. Development. 1996;122:3839-3850.
52. Blobel GA, Nakajima T, Eckner R, Montminy M, Orkin SH. CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc Natl Acad Sci U S A. 1998;95:2061-2066.
53. Boyes J, Byfield P, Nakatani Y, Ogryzko V. Regulation of activity of the transcription factor GATA-1 by acetylation. Nature. 1998;396:594-598.
54. Hung HL, Lau J, Kim AY, Weiss MJ, Blobel GA. CREB-binding protein acetylates hematopoietic transcription factor GATA-1 at functionally important sites. Mol Cell Biol. 1999;19:3496-3505.
55. Du K, Montminy M. CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem. 1998;273:32377-32379.
56. Lambert PF, Kashanchi F, Radonovich MF, Shiekhattar R, Brady JN. Phosphorylation of p53 serine 15 increases interaction with CBP. J Biol Chem. 1998;273:33048-33053.
57. Gurbuxani S, Vyas P, Crispino JD. Recent insights into the mechanisms of myeloid leukemogenesis in Down syndrome. Blood. 2004;103:399-406.
58. Liu D, Yang X, Songyang Z. Identification of CISK, a new member of the SGK kinase family that promotes IL-3-dependent survival. Curr Biol. 2000;10:1233-1236.
59. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME. Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol Cell Biol. 2001;21:952-965.
60. Towatari M, Ciro M, Ottolenghi S, Tsuzuki S, Enver T. Involvement of mitogen-activated protein kinase in the cytokine-regulated phosphorylation of transcription factor GATA-1. Hematol J. 2004;5:262-272.
61. Spivak JL. Polycythemia vera: myths, mechanisms, and management. Blood. 2002;100:4272-4290.
62. James C, Ugo V, Le Couedic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005;434:1144-1148.
63. Baxter EJ, Scott LM, Campbell PJ, et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365:1054-1061.
64. Kralovics R, Passamonti F, Buser AS, et al. A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med. 2005;352:1779-1790.
65. Levine RL, Wadleigh M, Cools J, et al. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell. 2005;7:387-397.
66. Zhao R, Xing S, Li Z, et al. Identification of an acquired JAK2 mutation in polycythemia vera. J Biol Chem. 2005;280:22788-22792.
67. Ugo V, Marzac C, Teyssandier I, et al. Multiple signaling pathways are involved in erythropoietin-independent differentiation of erythroid progenitors in polycythemia vera. Exp Hematol. 2004;32:179-187.
68. Dai C, Chung IJ, Krantz SB. Increased erythropoiesis in polycythemia vera is associated with increased erythroid progenitor proliferation and increased phosphorylation of Akt/PKB. Exp Hematol. 2005;33:152-158.
69. Correa PN, Eskinazi D, Axelrad AA. Circulating erythroid progenitors in polycythemia vera are hypersensitive to insulin-like growth factor-1 in vitro: studies in an improved serum-free medium. Blood. 1994;83:99-112.
70. Mirza AM, Ezzat S, Axelrad AA. Insulin-like growth factor binding protein-1 is elevated in patients with polycythemia vera and stimulates erythroid burst formation in vitro. Blood. 1997;89:1862-1869.
71. Uddin S, Kottegoda S, Stigger D, Platanias LC, Wickrema A. Activation of the Akt/FKHRL1 pathway mediates the antiapoptotic effects of erythropoietin in primary human erythroid progenitors. Biochem Biophys Res Commun. 2000;275:16-19.
72. Ghaffari S, Kitidis C, Zhao W, et al. AKT induces erythroid cell maturation of JAK2-deficient fetal liver progenitor cells and is required for epo regulation of erythroid cell differentiation. Blood. Prepublished on October 27, 2005 as DOI 10.1182/blood-2005-06-2304.