Stat5 activation enables erythropoiesis in the absence of EpoR and Jak2

Blood

Volumn 111, Issue 9, 2008, Pages 4511-4522

  Grebien, Florian ^a   Kerenyi, Marc A ^a   Kovacic, Boris ^b   Kolbe, Thomas ^c,d   Becker, Verena ^e   Dolznig, Helmut ^f   Pfeffer, Klaus ^g   Klingmüller, Ursula ^e   Müller, Mathias ^c   Beug, Hartmut ^b   Müllner, Ernst W ^a,f   Moriggl, Richard ^h  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^d UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

^g HEINRICH HEINE UNIVERSITY   (Germany)

^h LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN RECEPTOR; HYBRID PROTEIN; JANUS KINASE 2; MUTANT PROTEIN; STAT5 PROTEIN; STEM CELL FACTOR; TAMOXIFEN; CYTOKINE; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ERYTHROPOIESIS; FETUS DEVELOPMENT; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LIVER CELL; LIVER DEVELOPMENT; MOUSE; MYELOPOIESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; CELL CULTURE; METABOLISM; MOUSE MUTANT;

ANIMALS; CELLS, CULTURED; CYTOKINES; ERYTHROPOIESIS; JANUS KINASE 2; MICE; MICE, KNOCKOUT; MYELOPOIESIS; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTORS, ERYTHROPOIETIN; STAT5 TRANSCRIPTION FACTOR;

EID: 47149112573     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-07-102848     Document Type: Article

References (63)

1. Richmond TD, Chohan M, Barber DL. Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol. 2005;15:146-155.
2. Klingmuller U, Wu H, Hsiao JG, etal. 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.
3. Chen C, Sytkowski AJ. Erythropoietin regulation of Raf-1 and MEK: evidence for a Rasindependent mechanism. Blood. 2004;104:73-80.
4. von Lindern M. Parren-van Amelsvoort M. van Dijk T, et al. Protein kinase C alpha controls erythropoietin receptor signaling. J Biol Chem. 2000:275:34719-34727.
5. Tong Q. Chu X, Cheung JY, et al. Erythropoietinmodulated calcium influx through TRPC2 is mediated by phospholipase Cgammaand IP3R. Am J Physiol Cell Physiol. 2004;287:C1667-1678.
6. Cui Y Riedlinger G, Miyoshi K, et al. Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol Cell Biol. 2004:24:8037-8047.
7. Moriggl R, Gouilleux-Gruart V, Jahne R, et al. Deletion of the carboxyl-terminal trans activation domain of MGF-Stat5 results in sustained DNA binding and a dominant negative phenotype. Mol Cell Biol. 1996;16:5691-5700.
8. Teglund S, McKay C, Schuetz E, et al. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell. 1998;93:841-850.
9. Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pirn and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood. 2005;105:4477-4483.
10. Wilson A, Murphy MJ, Oskarsson T, et al. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 2004;18:2747-2763.
11. Tanaka M, Hirabayashi Y, Sekiguchi T. Inoue T. Katsuki M, Miyajima A. Targeted disruption of oncostatin M receptor results in altered hematopoiesis. Blood. 2003;102:3154-3162.
12. Wagner KU, Claudio E, Rucker EB 3rd, et al. Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development. 2000;127:494g-4958.
13. Starr R, Metcalf D. Elefanty AG, et al. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc Natl Acad Sci U S A. 1998;95:14395-14399.
14. Kozar K, Ciemerych MA, Rebel VI, etal. Mouse development and cell proliferation in the absence of D-cyclins. Cell. 2004;118:477-491.
15. Wu H, Liu X, Jaenisch R, Lodish HE Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 1995;83:59-67.
16. Neubauer H, Cumano A, Muller M, Wu H, Huffstadt U, Pfeffer K. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell. 1998;93:397-409.
17. Parganas E, Wang D, Stravopodis D, et al. Jak2 is essential for signaling through a variety of cytokine receptors. Cell. 1998;93:385-395.
18. Pelletier S, Gingras S, Funakoshi-Tago M, Howell S, Ihle JN. Two domains of the erythropoietin receptor are sufficient for Jak2 binding/activation and function. Mol Cell Biol. 2006;26:8527-8538.
19. -/- hematopoietic progenitors. Blood. 2001;98:2948-2957.
20. 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. 2006; 107:1888-1891.
21. -/- mice: a direct role for Stat5 in Bcl-X(L) induction. Cell. 1999;98:181-191.
22. -/- mice due to decreased survival of early erythroblasts. Blood. 2001;98:3261-3273.
23. Zang H, Sato K, Nakajima H, McKay C, Ney PA, Ihle JN. The distal region and receptor tyrosines of the Epo receptor are non-essential for in vivo erythropoiesis. EMBO J. 2001;20:3156-3166.
24. Menon MR Karur V, Bogacheva O, Bogachev O, Cuetara B, Wojchowski DM. Signals for stress erythropoiesis are integrated via an erythropoietin receptor-phosphotyrosine-343-Stat5 axis. J Clin Invest. 2006;116:683-694.
25. Onishi M, Nosaka T, Misawa K, et al. Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol Cell Biol. 1998;18:3871-3879.
26. Dolznig H, Kolbus A, Leberbauer C, et al. Expansion and differentiation of immature mouse and human hematopoietic progenitors. Methods Mol Med. 2005;105:323-344.
27. Moriggl R, Sexl V, Kenner L, et al. Stat5 tetramer formation is associated with leukemogenesis. Cancer Cell. 2005;7:87-99.
28. Kamogawa Y, Lee HJ, Johnston JA, McMahon M, O'Garra A, Arai N. A conditionally active form of STAT6 can mimic certain effects of IL-4. J Immunol. 1998;161:1074-1077.
29. Wang D, Moriggl R, Stravopodis D, et al. A small amphipathic alpha-helical region is required for transcriptional activities and proteasomedependent turnover of the tyrosine-phosphorylated Stat5. EMBO J. 2000;19:392-399.
30. Moriggl R, Berchtold S, Friedrich K, et al. Comparison of the transactivation domains of Stat5 and Stat6 in lymphoid cells and mammary epithelial cells. Mol Cell Biol. 1997;17:3663-3678.
31. John S, Vinkemeier U, Soldaini E, Darnell JE, Jr., Leonard WJ. The significance of tetramerization in promoter recruitment by Stat5. Mol Cell Biol. 1999;19:1910-1918.
32. Dolznig H. Boulme F, Stangl K, et al. Establishment of normal, terminally differentiating mouse erythroid progenitors: molecular characterization by cDNAarrays. Faseb J. 2001;15:1442-1444.
33. Littlewood TD, Hancock DC, Danielian PS, Parker MG, Evan Gl. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 1995;23:1686-1690.
34. Harir N, Pecquet C, Kerenyi M, et al. Constitutive activation of Stat5 promotes its cytoplasmic localization and association with PI3-kinase in myeloid leukemias. Blood. 2007;109:1678-1686.
35. Muta K, Krantz SB, Bondurant MC, Dai CH. Stem cell factor retards differentiation of normal human erythroid progenitor cells while stimulating proliferation. Blood. 1995;86:572-580.
36. Nocka K, Majumder S, Chabot B, et al. Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice-evidence for an impaired c-kit kinase in mutant mice. Genes Dev. 1989;3:816-826.
37. Zhao S, Zoller K, Masuko M, et al. JAK2, complemented by a second signal from c-kit or flt-3, triggers extensive self-renewal of primary multipotential hemopoietic cells. EMBO J. 2002;21:2159-2167.
38. Radosevic N, Winterstein D, Keller JR, Neubauer H, Pfeffer K, Linnekin D. JAK2 contributes to the intrinsic capacity of primary hematopoietic cells to respond to stem cell factor. Exp Hematol. 2004; 32:149-156.
39. Bowie MB, Kent DG, Copley MR, Eaves CJ. Steel factor responsiveness regulates the high selfrenewal phenotype of fetal hematopoietic stem cells. Blood. 2007;109:5043-5048.
40. Bryder D, Rossi DJ, Weissman IL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol. 2006:169:338-346.
41. Bradley HL, Couldrey C, Bunting KD. Hematopoietic-repopulating defects from STAT5-deficient bone marrow are not fully accounted for by loss of thrombopoietin responsiveness. Blood. 2004; 103:2965-2972.
42. Dolznig H, Grebien F, Deiner EM, et al. Erythroid progenitor renewal versus differentiation: genetic evidence for cell autonomous, essential functions of EpoR, Stat5 and the GR. Oncogene. 2006;25:2890-2900.
43. von Lindern M, Deiner EM, Dolznig H, et al. Leukemic transformation of normal murine erythroid progenitors: v-and c-ErbB act through signaling pathways activated by the EpoR and c-Kit in stress erythropoiesis. Oncogene. 2001;20:3651-3664.
44. Engblom D, Kornfeld JW, Schwake L, et al. Direct glucocorticoid receptor-StatS interaction in hepatocytes controls body size and maturation-related gene expression. Genes Dev. 2007;21:1157-1162.
45. Hoelbl A, Kovacic B, Kerenyi MA, et al. Clarifying the role of Stat5 in lymphoid development and Abelson-induced transformation. Blood. 2006; 107:4898-4906.
46. Murray PJ. The JAK-STAT signaling pathway: input and output integration. J Immunol. 2007; 178:2623-2629.
47. Dolznig H, Habermann B, Stangl K, et al. Apoptosis protection by the Epo target Bcl-X(L) allows factor-independent differentiation of primary erythroblasts. Curr Biol. 2002;12:1076-1085.
48. Garcon L, Rivat C, James C, et al. Constitutive activation of STAT5 and Bcl-xL overexpression can induce endogenous erythroid colony formation in human primary cells. Blood. 2006;108:1551-1554.
49. Fang J, Menon M, Kapelle W, et al. EPO modulation of cell cycle regulatory genes, and cell division, in primary bone marrow erythroblasts. Blood. 2007;110:2361-2370.
50. Sathyanarayana P, Menon MP, Bogacheva O, et al. Erythropoietin modulation of podocalyxin and a proposed erythroblast niche. Blood. 2007;110:509-518.
51. Schuringa JJ, Chung KY, Morrone G. Moore MA. Constitutive activation of STAT5A promotes human hematopoietic stem cell self-renewal and erythroid differentiation. J Exp Med. 2004;200:623-635.
52. Taylor DK, Walsh PT LaRosa DF, et al. Constitutive activation of STAT5 supersedes the requirement for cytokine and TGR engagement of GD4+ Tcells in steady-state homeostasis. J Immunol. 2006;177:2216-2223.
53. Huppertz C. Schwartz C. Becker W, Horn F, Heinrich PC, Joost HG. Comparison of the effects of insulin, PDGF, interleukin-6, and interferongamma on glucose transport in 3T3-L1 cells: lack of cross-talk between tyrosine kinase receptors and JAK/STAT pathways. Diabetologia. 1996;39:1432-1439.
54. Weiler SR, Mou S, DeBerry CS, et al. JAK2 is associated with the c-kit proto-oncogene product and is phosphorylated in response to stem cell factor. Blood. 1996;87:3688-3693.
55. Wu H, Klingmuller U, Besmer P, Lodish HF. Interaction of the erythropoietin and stem-cell-factor receptors. Nature. 1995;377:242-246.
56. Wu H, Klingmuller U, Acurio A, Hsiao JG, Lodish HF. Functional interaction of erythropoietin and stem cell factor receptors is essential for erythroid colony formation. Proc Natl Acad Sci U S A. 1997;94:1806-1810.
57. von Lindern M, Schmidt U, Beug H. Control of erythropoiesis by erythropoietin and stem cell factor: a novel role for Bruton's tyrosine kinase. Cell Cycle. 2004;3:876-879.
58. Wessely O, Bauer A, Quang CT, et al. A novel way to induce erythroid progenitor self renewal: cooperation of c-Kit with the erythropoietin receptor. Biol Chem. 1999;380:187-202.
59. Baxter EJ, Scott LM, Campbell PJ, et al. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 2005;365:1054-1061.
60. James C, Ugo V, Le Gouedic JP, et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 2005; 434:1144-1148.
61. 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.
62. 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.
63. Kaushansky K. On the molecular origins of the chronic myeloproliferative disorders: it all makes sense. Blood. 2005;105:4187-4190.