Activating Mutations in Protein Tyrosine Phosphatase Ptpn11 (Shp2) Enhance Reactive Oxygen Species Production That Contributes to Myeloproliferative Disorder

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Xu, Dan ^a   Zheng, Hong ^a   Yu, Wen Mei ^a   Qu, Cheng Kui ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; PROTEIN TYROSINE PHOSPHATASE SHP 2; REACTIVE OXYGEN METABOLITE;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE TRANSFER; HEMATOPOIETIC STEM CELL; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; PROTEIN TYROSINE PHOSPHATASE SHP 2 GENE; REGULATOR GENE; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CYTOKINES; DISEASE MODELS, ANIMAL; HEMATOPOIETIC STEM CELLS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MUTATION; MYELOID CELLS; MYELOPROLIFERATIVE DISORDERS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84877593143     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063152     Document Type: Article

References (47)

1. Chan G, Kalaitzidis D, Neel BG, (2008) The tyrosine phosphatase Shp2 (PTPN11) in cancer. Cancer Metastasis Rev 27: 179-192.
2. Xu D, Qu CK, (2008) Protein tyrosine phosphatases in the JAK/STAT pathway. Front Biosci 13: 4925-4932.
3. Tonks NK, (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7: 833-846.
4. Eck MJ, Pluskey S, Trub T, Harrison SC, Shoelson SE, (1996) Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase SH-PTP2. Nature 379: 277-280.
5. Hof P, Pluskey S, Dhe-Paganon S, Eck MJ, Shoelson SE, (1998) Crystal structure of the tyrosine phosphatase SHP-2. Cell 92: 441-450.
6. Barford D, Neel BG, (1998) Revealing mechanisms for SH2 domain mediated regulation of the protein tyrosine phosphatase SHP-2. Structure 6: 249-254.
7. Bennett AM, Tang TL, Sugimoto S, Walsh CT, Neel BG, (1994) Protein-tyrosine-phosphatase SHPTP2 couples platelet-derived growth factor receptor beta to Ras. Proc Natl Acad Sci U S A 91: 7335-7339.
8. Li W, Nishimura R, Kashishian A, Batzer AG, Kim WJ, et al. (1994) A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol Cell Biol 14: 509-517.
9. Yu WM, Hawley TS, Hawley RG, Qu CK, (2003) Catalytic-dependent and-independent roles of SHP-2 tyrosine phosphatase in interleukin-3 signaling. Oncogene 22: 5995-6004.
10. Qu CK, Shi ZQ, Shen R, Tsai FY, Orkin SH, et al. (1997) A deletion mutation in the SH2-N domain of Shp-2 severely suppresses hematopoietic cell development. Mol Cell Biol 17: 5499-5507.
11. Qu CK, Yu WM, Azzarelli B, Cooper S, Broxmeyer HE, et al. (1998) Biased suppression of hematopoiesis and multiple developmental defects in chimeric mice containing Shp-2 mutant cells. Mol Cell Biol 18: 6075-6082.
12. Qu CK, Nguyen S, Chen J, Feng GS, (2001) Requirement of Shp-2 tyrosine phosphatase in lymphoid and hematopoietic cell development. Blood 97: 911-914.
13. Chan G, Cheung LS, Yang W, Milyavsky M, Sanders AD, et al. (2011) Essential role for Ptpn11 in survival of hematopoietic stem and progenitor cells. Blood 117: 4253-4261.
14. Zhu HH, Ji K, Alderson N, He Z, Li S, et al. (2011) Kit-Shp2-Kit signaling acts to maintain a functional hematopoietic stem and progenitor cell pool. Blood 117: 5350-5361.
15. Tartaglia M, Mehler EL, Goldberg R, Zampino G, Brunner HG, et al. (2001) Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 29: 465-468.
16. Tartaglia M, Niemeyer CM, Fragale A, Song X, Buechner J, et al. (2003) Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat Genet 34: 148-150.
17. Loh ML, Vattikuti S, Schubbert S, Reynolds MG, Carlson E, et al. (2004) Mutations in PTPN11 implicate the SHP-2 phosphatase in leukemogenesis. Blood 103: 2325-2331.
18. Tartaglia M, Martinelli S, Cazzaniga G, Cordeddu V, Iavarone I, et al. (2004) Genetic evidence for lineage-related and differentiation stage-related contribution of somatic PTPN11 mutations to leukemogenesis in childhood acute leukemia. Blood 104: 307-313.
19. Loh ML, Reynolds MG, Vattikuti S, Gerbing RB, Alonzo TA, et al. (2004) PTPN11 mutations in pediatric patients with acute myeloid leukemia: results from the Children's Cancer Group. Leukemia 18: 1831-1834.
20. Bentires-Alj M, Paez JG, David FS, Keilhack H, Halmos B, et al. (2004) Activating mutations of the noonan syndrome-associated SHP2/PTPN11 gene in human solid tumors and adult acute myelogenous leukemia. Cancer Res 64: 8816-8820.
21. Keilhack H, David FS, McGregor M, Cantley LC, Neel BG, (2005) Diverse biochemical properties of Shp2 mutants. Implications for disease phenotypes. J Biol Chem 280: 30984-30993.
22. Fragale A, Tartaglia M, Wu J, Gelb BD, (2004) Noonan syndrome-associated SHP2/PTPN11 mutants cause EGF-dependent prolonged GAB1 binding and sustained ERK2/MAPK1 activation. Hum Mutat 23: 267-277.
23. Araki T, Mohi MG, Ismat FA, Bronson RT, Williams IR, et al. (2004) Mouse model of Noonan syndrome reveals cell type- and gene dosage-dependent effects of Ptpn11 mutation. Nat Med 10: 849-857.
24. Yu WM, Daino H, Chen J, Bunting KD, Qu CK, (2006) Effects of a Leukemia-associated Gain-of-Function Mutation of SHP-2 Phosphatase on Interleukin-3 Signaling. J Biol Chem 281: 5426-5434.
25. Kontaridis MI, Swanson KD, David FS, Barford D, Neel BG, (2006) PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J Biol Chem 281: 6785-6792.
26. Mohi MG, Williams IR, Dearolf CR, Chan G, Kutok JL, et al. (2005) Prognostic, therapeutic, and mechanistic implications of a mouse model of leukemia evoked by Shp2 (PTPN11) mutations. Cancer Cell 7: 179-191.
27. Chan G, Kalaitzidis D, Usenko T, Kutok JL, Yang W, et al. (2009) Leukemogenic Ptpn11 causes fatal myeloproliferative disorder via cell-autonomous effects on multiple stages of hematopoiesis. Blood 113: 4414-4424.
28. Xu D, Wang S, Yu WM, Chan G, Araki T, et al. (2010) A germline gain-of-function mutation in Ptpn11 (Shp-2) phosphatase induces myeloproliferative disease by aberrant activation of hematopoietic stem cells. Blood 116: 3611-3621.
29. Xu D, Liu X, Yu WM, Meyerson HJ, Guo C, et al. (2011) Non-lineage/stage-restricted effects of a gain-of-function mutation in tyrosine phosphatase Ptpn11 (Shp2) on malignant transformation of hematopoietic cells. J Exp Med 208: 1977-1988.
30. Chughtai N, Schimchowitsch S, Lebrun JJ, Ali S, (2002) Prolactin induces SHP-2 association with Stat5, nuclear translocation, and binding to the beta-casein gene promoter in mammary cells. J Biol Chem 277: 31107-31114.
31. Wu TR, Hong YK, Wang XD, Ling MY, Dragoi AM, et al. (2002) SHP-2 is a dual-specificity phosphatase involved in Stat1 dephosphorylation at both tyrosine and serine residues in nuclei. J Biol Chem 22: 22.
32. Jakob S, Schroeder P, Lukosz M, Buchner N, Spyridopoulos I, et al. (2008) Nuclear protein tyrosine phosphatase Shp-2 is one important negative regulator of nuclear export of telomerase reverse transcriptase. J Biol Chem 283: 33155-33161.
33. Yuan L, Yu WM, Qu CK, (2003) DNA damage-induced G2/M checkpoint in SV40 large T antigen-immortalized embryonic fibroblast cells requires SHP-2 tyrosine phosphatase. J Biol Chem 278: 42812-42820.
34. Yuan L, Yu WM, Yuan Z, Haudenschild CC, Qu CK, (2003) Role of SHP-2 tyrosine phosphatase in the DNA damage-induced cell death response. J Biol Chem 278: 15208-15216.
35. Salvi M, Stringaro A, Brunati AM, Agostinelli E, Arancia G, et al. (2004) Tyrosine phosphatase activity in mitochondria: presence of Shp-2 phosphatase in mitochondria. Cell Mol Life Sci 61: 2393-2404.
36. Arachiche A, Augereau O, Decossas M, Pertuiset C, Gontier E, et al. (2008) Localization of PTP-1B, SHP-2, and Src exclusively in rat brain mitochondria and functional consequences. J Biol Chem 283: 24406-24411.
37. Araki T, Chan G, Newbigging S, Morikawa L, Bronson RT, et al. (2009) Noonan syndrome cardiac defects are caused by PTPN11 acting in endocardium to enhance endocardial-mesenchymal transformation. Proc Natl Acad Sci U S A 106: 4736-4741.
38. Shen J, Liu X, Yu WM, Liu J, Nibbelink MG, et al. (2011) A critical role of mitochondrial phosphatase Ptpmt1 in embryogenesis reveals a mitochondrial metabolic stress-induced differentiation checkpoint in embryonic stem cells. Mol Cell Biol 31: 4902-4916.
39. Birnbaum RA, O'Marcaigh A, Wardak Z, Zhang YY, Dranoff G, et al. (2000) Nf1 and Gmcsf interact in myeloid leukemogenesis. Mol Cell 5: 189-195.
40. Chan RJ, Leedy MB, Munugalavadla V, Voorhorst CS, Li Y, et al. (2005) Human somatic PTPN11 mutations induce hematopoietic-cell hypersensitivity to granulocyte-macrophage colony-stimulating factor. Blood 105: 3737-3742.
41. Agazie YM, Hayman MJ, (2003) Development of an efficient "substrate-trapping" mutant of Src homology phosphotyrosine phosphatase 2 and identification of the epidermal growth factor receptor, Gab1, and three other proteins as target substrates. J Biol Chem 278: 13952-13958.
42. Norddahl GL, Pronk CJ, Wahlestedt M, Sten G, Nygren JM, et al. (2011) Accumulating mitochondrial DNA mutations drive premature hematopoietic aging phenotypes distinct from physiological stem cell aging. Cell Stem Cell 8: 499-510.
43. Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, et al. (2010) The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7: 380-390.
44. Sattler M, Winkler T, Verma S, Byrne CH, Shrikhande G, et al. (1999) Hematopoietic growth factors signal through the formation of reactive oxygen species. Blood 93: 2928-2935.
45. Carcamo JM, Borquez-Ojeda O, Golde DW, (2002) Vitamin C inhibits granulocyte macrophage-colony-stimulating factor-induced signaling pathways. Blood 99: 3205-3212.
46. Lee I, Pecinova A, Pecina P, Neel BG, Araki T, et al. (2010) A suggested role for mitochondria in Noonan syndrome. Biochim Biophys Acta 1802: 275-283.
47. Gu H, Griffin JD, Neel BG, (1997) Characterization of two SHP-2-associated binding proteins and potential substrates in hematopoietic cells. J Biol Chem 272: 16421-16430.