Identification of HIF2α as an important STAT5 target gene in human hematopoietic stem cells

Blood

Volumn 117, Issue 12, 2011, Pages 3320-3330

  Fatrai, Szabolcs ^a   Wierenga, Albertus T J ^a   Daenen, Simon M G J ^a   Vellenga, Edo ^a   Schuringa, Jan Jacob ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 2ALPHA; STAT5 PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; GLUCOSE; OXYGEN;

ARTICLE; CELL EXPANSION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE TARGETING; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; RNA INTERFERENCE; BIOLOGICAL MODEL; CELL CULTURE; CELL HYPOXIA; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; FEMALE; FETUS BLOOD; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MYELOID PROGENITOR CELL; NEWBORN; PHYSIOLOGY; PREGNANCY;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; FETAL BLOOD; GENE EXPRESSION REGULATION; GLUCOSE; HEMATOPOIETIC STEM CELLS; HUMANS; INFANT, NEWBORN; MODELS, BIOLOGICAL; MYELOID PROGENITOR CELLS; OXYGEN; PREGNANCY; STAT5 TRANSCRIPTION FACTOR;

EID: 79953116751     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-303669     Document Type: Article

References (46)

1. Bunting KD. STAT5 signaling in normal and pathologic hematopoiesis. Front Biosci. 2007;12: 2807-2820.
2. Paukku K, Silvennoinen O. STATs as critical mediators of signal transduction and transcription: lessons learned from STAT5. Cytokine Growth Factor Rev. 2004;15(6):435-455. (Pubitemid 39550454)
3. Schindler C, Darnell JE Jr. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu Rev Biochem. 1995;64:621-651.
4. Ihle JN. STATs: signal transducers and activators of transcription. Cell. 1996;84(3):331-334. (Pubitemid 26058558)
5. Bunting KD, Bradley HL, Hawley TS, Moriggl R, Sorrentino BP, Ihle JN. Reduced lymphomyeloid repopulating activity from adult bone marrow and fetal liver of mice lacking expression of STAT5. Blood. 2002;99(2):479-487. (Pubitemid 34533082)
6. Bradley HL, Hawley TS, Bunting KD. Cell intrinsic defects in cytokine responsiveness of STAT5-deficient hematopoietic stem cells. Blood. 2002; 100(12):3983-3989. (Pubitemid 35396864)
7. 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(8):2965-2972. (Pubitemid 38451668)
8. Snow JW, Abraham N, Ma MC, Abbey NW, Herndier B, Goldsmith MA. STAT5 promotes multilineage hematolymphoid development in vivo through effects on early hematopoietic progenitor cells. Blood. 2002;99(1):95-101.
9. Snow JW, Abraham N, Ma MC, Goldsmith MA. Bone marrow transplant completely rescues hematolymphoid defects in STAT5A/5B-deficient mice. Exp Hematol. 2003;31(12):1247-1252. (Pubitemid 37510030)
10. Liu G, Wang Z, Zhang Y, et al. STAT5 requires the N-domain to maintain hernatopoietic stem cell repopulating function and appropriate lymphoid-myeloid lineage output. Exp Hematol. 2007; 35(11):1684-1694. (Pubitemid 47633780)
11. Wang Z, Li G, Tse W, Bunting KD. Conditional deletion of STAT5 in adult mouse hematopoietic stem cells causes loss of quiescence and permits efficient nonablative stem cell replacement. Blood. 2009;113(20):4856-4865.
12. Schepers H, van Gosliga D, Wierenga ATJ, Eggen BJL, Schuringa JJ, Vellenga E. STAT5 is required for long-term maintenance of normal and leukemic human stem/progenitor cells. Blood. 2007;110(8):2880-2888. (Pubitemid 350006941)
13. Moriggl R, Sexl V, Kenner L, et al. Stat5 tetramer formation is associated with leukemogenesis. Cancer Cell. 2005;7(1):87-99. (Pubitemid 40126385)
14. 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(7):3871-3879. (Pubitemid 28287910)
15. Schwaller J, Parganas E, Wang D, et al. Stat5 is essential for the myelo- and lymphoproliferative disease induced by TEL/JAK2. Mol Cell. 2000; 6(3):693-704.
16. Kato Y, Iwama A, Tadokoro Y, et al. Selective activation of STAT5 unveils its role in stem cell self-renewal in normal and leukemic hematopoiesis. J Exp Med. 2005;202(1):169-179. (Pubitemid 41002919)
17. 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(5): 623-635. (Pubitemid 39258311)
18. Birkenkamp KU, Geugien M, Lemmink HH, Kruijer W, Vellenga E. Regulation of constitutive STAT5 phosphorylation in acute myeloid leukemia blasts. Leukemia. 2001;15(12):1923-1931. (Pubitemid 33115000)
19. Han L, Wierenga AT, Rozenveld-Geugien M, van de Lande K, Vellenga E, Schuringa JJ. Single-cell STAT5 signal transduction profiling in normal and leukemic stem and progenitor cell populations reveals highly distinct cytokine responses. PLoS ONE. 2009;4(11):e7989.
20. Spiekermann K, Pau M, Schwab R, Schmieja K, Franzrahe S, Hiddemann W. Constitutive activation of STAT3 and STAT5 is induced by leukemic fusion proteins with protein tyrosine kinase activity and is sufficient for transformation of hematopoietic precursor cells. Exp Hematol. 2002;30(3): 262-271. (Pubitemid 34203733)
21. Growney JD, Clark JJ, Adelsperger J, et al. Activation mutations of human c-KIT resistant to imatinib, mesylate are sensitive to the tyrosine kinase inhibitor PKC412. Blood. 2005;106(2):721-724. (Pubitemid 40981272)
22. Walters DK, Goss VL, Stoffregen EP, et al. Phosphoproteomic analysis of AML cell lines identifies leukemic oncogenes. Leuk Res. 2006;30(9): 1097-1104. (Pubitemid 44055977)
23. Hayakawa F, Towatari M, Kiyoi H, et al. Tandem-duplicated Flt3 constitutively activates STAT5 and MAP kinase and introduces autonomous cell growth in IL-3-dependent cell lines. Oncogene. 2000;19(5):624-631. (Pubitemid 30102913)
24. Wierenga AT, Vellenga E, Schuringa JJ. Down-regulation of GATA1 uncouples STAT5-induced erythroid differentiation from stem/progenitor cell proliferation. Blood. 2010;115(22):4367-4376.
25. Wierenga AT, Vellenga E, Schuringa JJ. Maximal STAT5-induced proliferation and self-renewal at intermediate STAT5 activity levels. Mol Cell Biol. 2008;28(21):6668-6680.
26. Hu YF, Smyth GK. Extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 2009;347(1-2):70-78.
27. Fatrai S, Schepers H, Tadema H, Vellenga E, Daenen SMGJ, Schuringa JJ. Mucin1 expression is enriched in the human stem cell fraction of cord blood and is upregulated in majority of the AML cases. Exp Hematol. 2008;36(10):1254-1265.
28. Franovic A, Holterman CE, Payette J, Lee S. Human cancers converge at the HIF-2alpha oncogenic axis. Proc Natl Acad Sci U S A. 2009; 106(50):21306-21311.
29. Heddleston JM, Li Z, Lathia JD, Bao S, Hjelmeland AB, Rich JN. Hypoxia inducible factors in cancer stem cells. Br J Cancer. 2010; 102(5):789-795.
30. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell. 2007;129(3):465-472. (Pubitemid 46660978)
31. Kaluz S, Kaluzova M, Stanbridge EJ. Regulation of gene expression by hypoxia: integration of the HIF-transduced hypoxic signal at the hypoxiaresponsive element. Clin Chim Acta. 2008;395(1-2):6-13.
32. Takubo K, Goda N, Yamada W, et al. Regulation of the HIF-1[alpha] level is essential for hematopoietic stem cells. Cell Stem Cell. 2010;7(3):391-402.
33. Simsek T, Kocabas F, Zheng J, et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell. 2010;7(3):380-390.
34. Chandel NS, McClintock DS, Feliciano CE, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275(33):25130- 25138.
35. Wofford JA, Wieman HL, Jacobs SR, Zhao Y, Rathmell JC. IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T-cell survival. Blood. 2008;111(4): 2101-2111. (Pubitemid 351451522)
36. Chen J, Kobayashi M, Darmanin S, et al. Hypoxia-mediated up-regulation of Pim-1 contributes to solid tumor formation. Am J Pathol. 2009;175(1):400-411.
37. Reiser-Erkan C, Erkan M, Pan Z, et al. Hypoxia-inducible proto-oncogene Pim-1 is a prognostic marker in pancreatic ductal adenocarcinoma. Cancer Biol Ther. 2008;7(9):1352-1359.
38. Franovic A, Gunaratnam L, Smith K, Robert I, Patten D, Lee S. Translational up-regulation of the EGFR by tumor hypoxia provides a nonmutational explanation for its overexpression in human cancer. Proc Natl Acad Sci U S A. 2007;104(32): 13092-13097. (Pubitemid 351737598)
39. Chen W, Kumar AR, Hudson WA, et al. Malignant transformation initiated by Mll-AF9: gene dosage and critical target cells. Cancer Cell. 2008;13(5): 432-440. (Pubitemid 351609442)
40. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 2003;17(24):3029-3035. (Pubitemid 38040767)
41. Krivtsov AV, Twomey D, Feng Z, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006; 442(7104):818-822. (Pubitemid 44258912)
42. Somervaille TC, Matheny CJ, Spencer GJ, et al. Hierarchical maintenance of MLL myeloid leukemia stem cells employs a transcriptional program shared with embryonic rather than adult stem cells. Cell Stem Cell. 2009;4(2):129-140.
43. Huntly BJ, Shigematsu H, Deguchi K, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6(6): 587-596. (Pubitemid 40017702)
44. Pérez-Caro M, Cobaleda C, Gonzalez-Herrero I, et al. Cancer induction by restriction of oncogene expression to the stem cell compartment. EMBO J. 2009;28(1):8-20.
45. Kimura A, Rieger MA, Simone JM, et al. The transcription factors STAT5A/B regulate GM-CSF-mediated granulopoiesis. Blood. 2009;114(21): 4721-4728.
46. WierengaAT, Schepers H, Moore MA, Vellenga E, Schuringa JJ. STAT5-induced self-renewal and impaired myelopoiesis of human hematopoietic stem/progenitor cells involves down-modulation of C/EBPalpha. Blood. 2006;107(11):4326-4333. (Pubitemid 43801357)