Acritical role for SHP2 in STAT5 activation and growth factor-mediated proliferation, survival, and differentiation of human CD34+ cells

Blood

Volumn 118, Issue 6, 2011, Pages 1504-1515

  Li, Liang ^a   Modi, Hardik ^a   McDonald, Tinisha ^a   Rossi, John ^a   Yee, Jiing Kuan ^a   Bhatia, Ravi ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; GROWTH FACTOR; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; SHORT HAIRPIN RNA; STAT5 PROTEIN; HEMOPOIETIC GROWTH FACTOR; INTERLEUKIN 2 RECEPTOR GAMMA;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMING CELL; CONTROLLED STUDY; ERYTHROID PRECURSOR CELL; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; CELL TRANSPLANTATION; CYTOLOGY; DRUG EFFECT; FETUS BLOOD; GENETICS; HEMATOPOIETIC STEM CELL; METABOLISM; METHODOLOGY; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; RNA INTERFERENCE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; ANTIGENS, CD34; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPLANTATION; CELLS, CULTURED; FETAL BLOOD; HEMATOPOIETIC CELL GROWTH FACTORS; HEMATOPOIETIC STEM CELLS; HUMANS; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; RNA INTERFERENCE; STAT5 TRANSCRIPTION FACTOR; TRANSPLANTATION, HETEROLOGOUS;

EID: 80051646552     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-06-288910     Document Type: Article

References (50)

1. Neel BG, Gu H, Pao L. The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci. 2003;28(6):284-293. (Pubitemid 36776291)
2. Zhan Y, O'Rourke DM. SHP-2-dependent mitogen-activated protein kinase activation regulates EGFRvIII but not wild-type epidermal growth factor receptor phosphorylation and glioblastoma cell survival. Cancer Res. 2004;64(22):8292-8298. (Pubitemid 39491767)
3. Gadina M, Stancato LM, Bacon CM, Larner AC, O'Shea JJ. Involvement of SHP-2 in multiple aspects of IL-2 signaling: evidence for a positive regulatory role. J Immunol. 1998;160(10):4657-4661. (Pubitemid 28215296)
4. Saxton TM, Henkemeyer M, Gasca S, et al. Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J. 1997;16(9):2352-2364. (Pubitemid 27258636)
5. Qu CK, Shi ZQ, Shen R, Tsai FY, Orkin SH, Feng GS. Adeletion mutation in the SH2-N domain of Shp-2 severely suppresses hematopoietic cell development. Mol Cell Biol. 1997;17(9):5499-5507. (Pubitemid 27357646)
6. Zou GM, Chan RJ, Shelley WC, Yoder MC. Reduction of Shp-2 expression by small interfering RNA reduces murine embryonic stem cell-derived in vitro hematopoietic differentiation. Stem Cells. 2006;24(3):587-594. (Pubitemid 44464762)
7. Qu CK, Yu WM, Azzarelli B, Cooper S, Broxmeyer HE, Feng GS. Biased suppression of hematopoiesis and multiple developmental defects in chimeric mice containing Shp-2 mutant cells. Mol Cell Biol. 1998;18(10):6075-6082. (Pubitemid 28450558)
8. Qu CK, Nguyen S, Chen J, Feng GS. Requirement of Shp-2 tyrosine phosphatase in lymphoid and hematopoietic cell development. Blood. 2001;97(4):911-914. (Pubitemid 32154273)
9. Chan RJ, Li Y, Hass MN, et al. Shp-2 heterozygous hematopoietic stem cells have deficient repopulating ability due to diminished self-renewal. Exp Hematol. 2006;34(9):1230-1239.
10. Tartaglia M, Kalidas K, Shaw A, et al. PTPN11 mutations in Noonan syndrome: molecular spectrum, genotype-phenotype correlation, and phenotypic heterogeneity. Am J Hum Genet. 2002;70(6):1555-1563. (Pubitemid 34533902)
11. Tartaglia M, Niemeyer CM, Fragale A, et al. Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat Genet. 2003;34(2):148-150. (Pubitemid 36666923)
12. Schubbert S, Lieuw K, Rowe SL, et al. Functional analysis of leukemia-associated PTPN11 mutations in primary hematopoietic cells. Blood. 2005;106(1):311-317. (Pubitemid 40967207)
13. Chan RJ, Leedy MB, Munugalavadla V, et al. Human somatic PTPN11 mutations induce hematopoietic- cell hypersensitivity to granulocyte-macrophage colony-stimulating factor. Blood. 2005;105(9):3737-3742. (Pubitemid 40628224)
14. Yu WM, Daino H, Chen J, Bunting KD, Qu CK. Effects of a leukemia-associated gain-of-function mutation of SHP-2 phosphatase on interleukin-3 signaling. J Biol Chem. 2006;281(9):5426-5434. (Pubitemid 43847637)
15. Xu R, Yu Y, Zheng S, et al. Overexpression of Shp2 tyrosine phosphatase is implicated in leukemogenesis in adult human leukemia. Blood. 2005;106(9):3142-3149. (Pubitemid 41565912)
16. Miyakawa Y, Rojnuckarin P, Habib T, Kaushansky K. Thrombopoietin induces phosphoinositol 3-kinaseactivation through SHP2, Gab, and insulin receptor substrate proteins in BAF3 cells and primary murine megakaryocytes. J Biol Chem. 2001;276(4):2494-2502.
17. Lecoq-Lafon C, Verdier F, Fichelson S, et al. Erythropoietin induces the tyrosine phosphorylation of GAB1 and its association with SHC, SHP2, SHIP, and phosphatidylinositol 3-kinase. Blood. 1999;93(8):2578-2585. (Pubitemid 29181190)
18. Zhang S, Broxmeyer HE. Flt3 ligand induces tyrosine phosphorylation of gab1 and gab2 and their association with shp-2, grb2, and PI3 kinase. Biochem Biophys Res Commun. 2000;277(1):195-199.
19. Craddock BL, Welham MJ. Interleukin-3 induces association of the protein-tyrosine phosphatase SHP2 and phosphatidylinositol 3-kinase with a 100-kDa tyrosine-phosphorylated protein in hemopoietic cells. J Biol Chem. 1997;272(46):29281-29289. (Pubitemid 27498221)
20. Adachi M, Ishino M, Torigoe T, et al. Interleukin-2 induces tyrosine phosphorylation of SHP-2 through IL-2 receptor beta chain. Oncogene. 1997;14(13):1629-1633. (Pubitemid 27182848)
21. Ward AC, Smith L, de Koning JP, van Aesch Y, Touw IP. Multiple signals mediate proliferation, differentiation, and survival from the granulocyte colony-stimulating factor receptor in myeloid 32D cells. J Biol Chem. 1999;274(21):14956-14962.
22. Watanabe S, Itoh T, Arai K. Roles of JAK kinases in human GM-CSF receptor signal transduction. J Allergy Clin Immunol. 1996;98(6):S183-S191.
23. Jack GD, Zhang L, Friedman AD. M-CSF elevates c-Fos and phospho-C/EBPalpha(S21) via ERK whereas G-CSF stimulates SHP2 phosphorylation in marrow progenitors to contribute to myeloid lineage specification. Blood. 2009;114(10):2172-2180.
24. Castanotto D, Li H, Rossi JJ. Functional siRNA expression from transfected PCR products. RNA. 2002;8(11):1454-1460. (Pubitemid 35332968)
25. Mohi MG, Williams IR, Dearolf CR, et al. Prognostic, therapeutic, and mechanistic implications of a mouse model of leukemia evoked by Shp2 (PTPN11) mutations. Cancer Cell. 2005;7(2):179-191. (Pubitemid 40248343)
26. Chu S, Li L, Singh H, Bhatia R. BCR-tyrosine 177 plays an essential role in Ras and Akt activation and in human hematopoietic progenitor transformation in chronic myelogenous leukemia. Cancer Res. 2007;67(14):7045-7053. (Pubitemid 47105554)
27. Chu S, Holtz M, Gupta M, Bhatia R. BCR/ABL kinase inhibition by imatinib mesylate enhances MAP kinase activity in chronic myelogenous leukemia CD34+ cells. Blood. 2004;103(8):3167-3174. (Pubitemid 38451695)
28. Bhatia R, McGlave PB, Miller JS, Wissink S, Lin WN, Verfaillie CM. A clinically suitable ex vivo expansion culture system for LTC-IC and CFC using stroma-conditioned medium. Exp Hematol. 1997;25(9):980-991. (Pubitemid 27368290)
29. Bhatia R, McGlave PB, Dewald GW, Blazar BR, Verfaillie CM. Abnormal function of the bone marrow microenvironment in chronic myelogenous leukemia: role of malignant stromal macrophages. Blood. 1995;85(12):3636-3645.
30. Socolovsky M, Fallon AE, Wang S, Brugnara C, Lodish HF. Fetal anemia and apoptosis of red cell progenitors in Stat5a-/-5b-/- mice: a direct role for Stat5 in Bcl-X(L) induction. Cell. 1999;98(2):181-191.
31. Aichberger KJ, Mayerhofer M, Krauth MT, et al. Identification of mcl-1 as a BCR/ABL-dependent target in chronic myeloid leukemia (CML): evidence for cooperative antileukemic effects of imatinib and mcl-1 antisense oligonucleotides. Blood. 2005;105(8):3303-3311.
32. Qu CK. Role of the SHP-2 tyrosine phosphatase in cytokine-induced signaling and cellular response. Biochim Biophys Acta. 2002;1592(3):297-301.
33. Gu H, Pratt JC, Burakoff SJ, Neel BG. Cloning of p97/Gab2, the major SHP2-binding protein in hematopoietic cells, reveals a novel pathway for cytokine-induced gene activation. Mol Cell. 1998;2(6):729-740. (Pubitemid 128378981)
34. Xu D, Qu CK. Protein tyrosine phosphatases in the JAK/STAT pathway. Front Biosci. 2008;13: 4925-4932. (Pubitemid 351599646)
35. Chen Y, Wen R, Yang S, et al. Identification of Shp-2 as a Stat5A phosphatase. J Biol Chem. 2003;278(19):16520-16527. (Pubitemid 36799512)
36. Chen J, Yu WM, Bunting KD, Qu CK. A negative role of SHP-2 tyrosine phosphatase in growth factor-dependent hematopoietic cell survival. Oncogene. 2004;23(20):3659-3669. (Pubitemid 38658433)
37. Du Z, Shen Y, Yang W, Mecklenbrauker I, Neel BG, Ivashkiv LB. Inhibition of IFN-alpha signaling by a PKC- and protein tyrosine phosphatase SHP-2-dependent pathway. Proc Natl Acad Sci U S A. 2005;102(29):10267-10272. (Pubitemid 41023361)
38. Kim H, Baumann H. Dual signaling role of the protein tyrosine phosphatase SHP-2 in regulating expression of acute-phase plasma proteins by interleukin-6 cytokine receptors in hepatic cells. Mol Cell Biol. 1999;19(8):5326-5338. (Pubitemid 29339892)
39. Ali S, Nouhi Z, Chughtai N, Ali S. SHP-2 regulates SOCS-1-mediated Janus kinase-2 ubiquitination/ degradation downstream of the prolactin receptor. J Biol Chem. 2003;278(52):52021-52031. (Pubitemid 38035787)
40. Yu WM, Hawley TS, Hawley RG, Qu CK. Catalyticdependent and -independent roles of SHP-2 tyrosine phosphatase in interleukin-3 signaling. Oncogene. 2003;22(38):5995-6004. (Pubitemid 37175877)
41. Chan RJ, Johnson SA, Li Y, Yoder MC, Feng GS. A definitive role of Shp-2 tyrosine phosphatase in mediating embryonic stem cell differentiation and hematopoiesis. Blood. 2003;102(6):2074-2080. (Pubitemid 37122382)
42. Schmitz J, Weissenbach M, Haan S, Heinrich PC, Schaper F. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J Biol Chem. 2000;275(17):12848-12856. (Pubitemid 30241440)
43. Lehmann U, Schmitz J, Weissenbach M, et al. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J Biol Chem. 2003;278(1):661-671. (Pubitemid 36043620)
44. Zhang JG, Farley A, Nicholson SE, et al. The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc Natl Acad Sci U S A. 1999;96(5):2071-2076.
45. Boyle K, Zhang JG, Nicholson SE, et al. Deletion of the SOCS box of suppressor of cytokine signaling 3 (SOCS3) in embryonic stem cells reveals SOCS box-dependent regulation of JAK but not STAT phosphorylation. Cell Signal. 2009;21(3):394-404.
46. Opferman JT, Iwasaki H, Ong CC, et al. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science. 2005;307(5712):1101- 1104. (Pubitemid 40262114)
47. Opferman JT. Life and death during hematopoietic differentiation. Curr Opin Immunol. 2007;19(5):497-502. (Pubitemid 47464914)
48. Yoshimoto G, Miyamoto T, Jabbarzadeh-Tabrizi S, et al. FLT3-ITD up-regulates MCL-1 to promote survival of stem cells in acute myeloid leukemia via FLT3-ITD-specific STAT5 activation. Blood. 2009;114(24):5034-5043.
49. Schepers H, van Gosliga D, Wierenga AT, Eggen BJ, 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)
50. Chen L, Sung SS, Yip ML, et al. Discovery of a novel shp2 protein tyrosine phosphatase inhibitor. Mol Pharmacol. 2006;70(2):562-570. (Pubitemid 44092317)