Loss of SHIP-1 protein expression in high-risk myelodysplastic syndromes is associated with miR-210 and miR-155

Oncogene

Volumn 31, Issue 37, 2012, Pages 4085-4094

  Lee, D W ^a,d   Futami, M ^b,d   Carroll, M ^c   Feng, Y ^b   Wang, Z ^b   Fernandez, M ^a   Whichard, Z ^b   Chen, Y ^b   Kornblau, S ^a   Shpall, E J ^a   Bueso Ramos, C E ^a   Corey, S J ^b,d  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Akt; leukemia; SHIP 1

Indexed keywords

CD34 ANTIGEN; MICRORNA 155; MICRORNA 210; PHOSPHATASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SHIP 1 PHOSPHATASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; BONE MARROW CELL; CANCER GROWTH; CANCER INHIBITION; CANCER STEM CELL; CELL LEVEL; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOPENIA; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MYELODYSPLASTIC SYNDROME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

APOPTOSIS; BONE MARROW CELLS; CELL LINE, TUMOR; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICRORNAS; MYELODYSPLASTIC SYNDROMES; MYELOID CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 84866422595     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.579     Document Type: Article

References (45)

1. Aul C, Germing U, Gattermann N, Minning H. (1998). Increasing incidence of myelodysplastic syndromes: real or fictitious? Leuk Res 22: 93-100. (Pubitemid 28167552)
2. Cantley LC, Neel BG. (1999). New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinosi-tide 3-kinase/AKT pathway. Proc Natl Acad Sci USA 96: 4240-4245. (Pubitemid 29190320)
3. Corey SJ, Minden MD, Barber DL, Kantarjian H, Wang JC, Schimmer AD. (2007). Myelodysplastic syndromes: the complexity of stem-cell diseases. Nat Rev Cancer 7: 118-129. (Pubitemid 46164747)
4. Costinean S, Sandhu SK, Pedersen IM, Tili E, Trotta R, Perrotti D et al. (2009). Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of Emicro-MiR-155 transgenic mice. Blood 114: 1374-1382.
5. Dahia PL, Aguiar RC, Alberta J, Kum JB, Caron S, Sill H et al. (1999). PTEN is inversely correlated with the cell survival factor Akt/PKB and is inactivated via multiple mechanisms in haemato-logical malignancies. Hum Mol Genet 8: 185-193. (Pubitemid 29054260)
6. Damen JE, Liu L, Rosten P, Humphries RK, Jefferson AB, Majerus PW et al. (1996). The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphati-dylinositol 3,4,5-triphosphate 5-phosphatase. Proc Natl Acad Sci USA 93: 1689-1693.
7. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. (1998). Pten is essential for embryonic development and tumour suppression. Nat Genet 19: 348-355. (Pubitemid 28357906)
8. Di Cunto F, Topley G, Calautti E, Hsiao J, Ong L, Seth PK et al. (1998). Inhibitory function of p21Cip1/WAF1 in differentiation of primary mouse keratinocytes independent of cell cycle control. Science 280: 1069-1072. (Pubitemid 28234947)
9. Fenaux P. (2004). Myelodysplastic syndromes: from pathogenesis and prognosis to treatment. Semin Hematol 41: 6-12. (Pubitemid 38649813)
10. Follo MY, Mongiorgi S, Bosi C, Cappellini A, Finelli C, Chiarini F et al. (2007). The Akt/mammalian target of rapamycin signal transduction pathway is activated in high-risk myelodysplastic syndromes and influences cell survival and proliferation. Cancer Res 67: 4287-4294. (Pubitemid 46815076)
11. Geier SJ, Algate PA, Carlberg K, Flowers D, Friedman C, Trask B et al. (1997). The human SHIP gene is differentially expressed in cell lineages of the bone marrow and blood. Blood 89: 1876-1885. (Pubitemid 27132101)
12. Gilby DC, Goodeve AC, Winship PR, Valk PJ, Delwel R, Reilly JT. (2007). Gene structure, expression profiling and mutation analysis of the tumour suppressor SHIP1 in Caucasian acute myeloid leukaemia. Leukemia 21: 2390-2393. (Pubitemid 350011722)
13. Greenberg PL. (1998). Apoptosis and its role in the myelodysplastic syndromes: implications for disease natural history and treatment. Leuk Res 22: 1123-1136. (Pubitemid 29002986)
14. Greenberg PL, Young NS, Gattermann N. (2002). Myelodysplastic syndromes. Hematology (Am Soc Hematol Educ Program), 2002: 136-161.
15. Hazen AL, Smith MJ, Desponts C, Winter O, Moser K, Kerr WG. (2009). SHIP is required for a functional hematopoietic stem cell niche. Blood 113: 2924-2933.
16. Heaney ML, Golde DW. (1999). Myelodysplasia. N Engl J Med 340: 1649-1660. (Pubitemid 29249435)
17. Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM et al. (1998). Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 12: 1610-1620. (Pubitemid 28299513)
18. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK et al. (2009). Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 35: 856-867.
19. Kalesnikoff J, Sly LM, Hughes MR, Buchse T, Rauh MJ, Cao LP et al. (2003). The role of SHIP in cytokine-induced signaling. Rev Physiol Biochem Pharmacol 149: 87-103.
20. Krystal G. (2000). Lipid phosphatases in the immune system. Semin Immunol 12: 397-403.
21. Lakhanpal GK, Vecchiarelli-Federico LM, Li YJ, Cui JW, Bailey ML, Spaner DE et al. (2010). The inositol phosphatase SHIP-1 is negatively regulated by Fli-1 and its loss accelerates leukemogenesis. Blood 116: 428-436.
22. Luo JM, Liu ZL, Hao HL, Wang FX, Dong ZR, Ohno R. (2004). Mutation analysis of SHIP gene in acute leukemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi 12: 420-426.
23. Manning BD, Cantley LC. (2007). AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274. (Pubitemid 46962095)
24. Matsuda M, Morita Y, Hanamoto H, Tatsumi Y, Maeda Y, Kanamaru A. (2004). CD34+ progenitors from MDS patients are unresponsive to SDF-1, despite high levels of SDF-1 in bone marrow plasma. Leukemia 18: 1038-1040. (Pubitemid 38714636)
25. Melcher M, Unger B, Schmidt U, Rajantie IA, Alitalo K, Ellmeier W. (2008). Essential roles for the Tec family kinases Tec and Btk in M-CSF receptor signaling pathways that regulate macrophage survival. J Immunol 180: 8048-8056.
26. Moody JL, Xu L, Helgason CD, Jirik FR. (2004). Anemia, thrombocytopenia, leukocytosis, extramedullary hematopoiesis, and impaired progenitor function in Pten +-SHIP-/-mice: a novel model of myelodysplasia. Blood 103: 4503-4510. (Pubitemid 38745976)
27. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA et al. (2004). PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6: 117-127. (Pubitemid 39485684)
28. Nyakern M, Tazzari PL, Finelli C, Bosi C, Follo MY, Grafone T et al. (2006). Frequent elevation of Akt kinase phosphorylation in blood marrow and peripheral blood mononuclear cells from high-risk myelodysplastic syndrome patients. Leukemia 20: 230-238. (Pubitemid 43148660)
29. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D. (2009). Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA 106: 7113-7118.
30. Pedersen IM, Otero D, Kao E, Miletic AV, Hother C, Ralfkiaer E et al. (2009). Onco-miR-155 targets SHIP1 to promote TNFalpha-dependent growth of B cell lymphomas. EMBO Mol Med 1: 288-295.
31. Pons A, Nomdedeu B, Navarro A, Gaya A, Gel B, Diaz T et al. (2009). Hematopoiesis-related microRNA expression in myelodysplastic syndromes. Leuk Lymphoma 50: 1854-1859.
32. Robertson GP, Furnari FB, Miele ME, Glendening MJ, Welch DR, Fountain JW et al. (1998). In vitro loss of heterozygosity targets the PTEN/MMAC1 gene in melanoma. Proc Natl Acad Sci USA 95: 9418-9423. (Pubitemid 28506246)
33. Rosenfeld C, List A. (2000). A hypothesis for the pathogenesis of myelodysplastic syndromes: implications for new therapies. Leukemia 14: 2-8. (Pubitemid 30068366)
34. Ruifrok AC, Johnston DA. (2001). Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23: 291-299. (Pubitemid 32762920)
35. Ruschmann J, Ho V, Antignano F, Kuroda E, Lam V, Ibaraki M et al. (2010). Tyrosine phosphorylation of SHIP promotes its proteasomal degradation. Exp Hematol 38: 392-402, 402.e391.
36. Sato K, Mano H, Ariyama T, Inazawa J, Yazaki Y, Hirai H. (1994). Molecular cloning and analysis of the human Tec protein-tyrosine kinase. Leukemia 8: 1663-1672. (Pubitemid 24323782)
37. Sattler M, Verma S, Byrne CH, Shrikhande G, Winkler T, Algate PA et al. (1999). BCR/ABL directly inhibits expression of SHIP, an SH2-containing polyinositol-5-phosphatase involved in the regulation of hematopoiesis. Mol Cell Biol 19: 7473-7480. (Pubitemid 29493410)
38. Thompson JE, Conlon JP, Yang X, Sanchez PV, Carroll M. (2007). Enhanced growth of myelodysplastic colonies in hypoxic conditions. Exp Hematol 35: 21-31. (Pubitemid 46014366)
39. Tomlinson MG, Heath VL, Turck CW, Watson SP, Weiss A. (2004). SHIP family inositol phosphatases interact with and negatively regulate the Tec tyrosine kinase. J Biol Chem 279: 55089-55096. (Pubitemid 40066501)
40. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A et al. (2009). The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood 114: 937-951.
41. Ware MD, Rosten P, Damen JE, Liu L, Humphries RK, Krystal G. (1996). Cloning and characterization of human SHIP, the 145-kD inositol 5-phosphatase that associates with SHC after cytokine stimulation. Blood 88: 2833-2840. (Pubitemid 26357363)
42. Whichard ZL, Motter AE, Stein PJ, Corey SJ. (2011). Slowly produced MicroRNAs control protein levels. J Biol Chem 286: 4742-4748.
43. Worm J, Stenvang J, Petri A, Frederiksen KE, Obad S, Elmen J et al. (2009). Silencing of microRNA-155 in mice during inflammatory response leads to derepression of c/ebpa beta and down-regulation of G-CSF. Nucl Acids Res 37: 5784-5792.
44. Yamanaka Y, Tagawa H, Takahashi N, Watanabe A, Guo YM, Iwamoto K et al. (2009). Aberrant overexpression of micro RNAs activate AKT signaling via down-regulation of tumor suppressors in natural killer-cell lymphoma/leukemia. Blood 114: 3265-3275.
45. Zysman MA, Chapman WB, Bapat B. (2002). Considerations when analyzing the methylation status of PTEN tumor suppressor gene. Am J Pathol 160: 795-800. (Pubitemid 34224569)