Inhibitor and activator: Dual functions for SHIP in immunity and cancer

Annals of the New York Academy of Sciences

Volumn 1217, Issue 1, 2011, Pages 1-17

  Kerr, William G ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Antigen presentation; Cancer, Crohn's Disease, HSC; MIR cells; NK cells; Osteoblasts; S SHIP; SHIP

Indexed keywords

PHOSPHATASE; PROTEIN SHIP; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; BONE MARROW TRANSPLANTATION; CANCER CELL; ENZYME ACTIVITY; ENZYME SUBSTRATE; GRAFT REJECTION; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNITY; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 79251553448     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2010.05869.x     Document Type: Article

References (130)

1. Kavanaugh, W.M., D.A. Pot, S.M. Chin, et al 1996. Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol. 6: 438-445.
2. Damen, J.E., L. Liu, P. Rosten, et al 1996. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3, 4, 5-triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 93: 1689-1693.
3. Lioubin, M.N., P.A. Algate, S. Tsai, et al 1996. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10: 1084-1095.
4. Hawkins P.T., K.E. Anderson, K. Davidson, & L.R. Stephens 2006. Signalling through Class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34(Pt 5):647-662.
5. Xia, H.J. & G. Yang 2005. Inositol 1, 4, 5-trisphosphate 3-kinases: functions and regulations. Cell. Res. 15: 83-91.
6. Franke, T.F., D.R. Kaplan, L.C. Cantley & A. Toker 1997. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3, 4-bisphosphate [see comments]. Science 275: 665-668.
7. Scheid, M.P., M. Huber, J.E. Damen, et al 2002. Phosphatidylinositol (3, 4, 5)P3 is essential but not sufficient for protein kinase B (PKB) activation; phosphatidylinositol (3, 4)P2 is required for PKB phosphorylation at Ser-473: studies using cells from SH2-containing inositol-5-phosphatase knockout mice. J. Biol. Chem. 277: 9027-9035.
8. Ma, K., S.M. Cheung, A.J. Marshall & V. Duronio 2008. PI(3, 4, 5)P3 and PI(3, 4)P2 levels correlate with PKB/akt phosphorylation at Thr308 and Ser473, respectively; PI(3, 4)P2 levels determine PKB activity. Cell Signal. 20: 684-694.
9. Tiwari, S., H.P. Choi, T. Matsuzawa, et al 2009. Targeting of the GTPase Irgm1 to the phagosomal membrane via PtdIns(3, 4)P(2) and PtdIns(3, 4, 5)P(3) promotes immunity to mycobacteria. Nat. Immunol. 10: 907-917.
10. Brooks, R., G.M. Fuhler, S. Iyer, et al 2010. SHIP1 inhibition increases immunoregulatory capacity and triggers apoptosis of hematopoietic cancer cells. J. Immunol. 184: 3582-3589.
11. Scharenberg, A.M., O. El-Hillal, D.A. Fruman, et al 1998. Phosphatidylinositol-3, 4, 5-trisphosphate (PtdIns-3, 4, 5-P3)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO J. 17: 1961-1972.
12. Wahle, J.A., K.H. Paraiso, R.D. Kendig, et al 2007. Inappropriate recruitment and activity by the Src homology region 2 domain-containing phosphatase 1 (SHP1) is responsible for receptor dominance in the SHIP-deficient NK cell. J. Immunol. 179: 8009-8015.
13. Peng, Q., S. Malhotra, J.A. Torchia, et al TREM2- and DAP12-dependent activation of PI3K requires DAP10 and is inhibited by SHIP1. Sci. Signal. 3: ra38.
14. Ware, M.D., P. Rosten, J.E. Damen, et al 1996. Cloning and characterization of human SHIP, the 145-kD inositol 5-phosphatase that associates with SHC after cytokine stimulation. Blood 88: 2833-2840.
15. Kerr, W.G., M. Heller & L.A. Herzenberg 1996. Analysis of lipopolysaccharide-response genes in B-lineage cells demonstrates that they can have differentiation stage-restricted expression and contain SH2 domains. Proc. Natl. Acad. Sci. USA 93: 3947-3952.
16. Tu, Z., J.M. Ninos, Z. Ma, et al 2001. Embryonic and hematopoietic stem cells express a novel SH2-containing inositol 5'-phosphatase isoform that partners with the Grb2 adapter protein. Blood 98: 2028-2038.
17. Geier, S.J., P.A. Algate, K. Carlberg, et al 1997. The human SHIP gene is differentially expressed in cell lineages of the bone marrow and blood. Blood 89: 1876-1885.
18. Sly, L.M., M.J. Rauh, J. Kalesnikoff, et al 2004. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 21: 227-239.
19. Trotta, R., R. Parihar, J. Yu, et al 2005. Differential expression of SHIP1 in CD56bright and CD56dim NK cells provides a molecular basis for distinct functional responses to monokine costimulation. Blood 105: 3011-3018.
20. Valderrama-Carvajal, H., E. Cocolakis, A. Lacerte, et al 2002. Activin/TGF-beta induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat. Cell Biol. 4: 963-969.
21. Pan, H., E. Ding, M. Hu, et al SMAD4 is required for development of maximal endotoxin tolerance. J. Immunol. 184: 5502-5509.
22. O'Connell, R.M., A.A. Chaudhuri, D.S. Rao & D. Baltimore 2009. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. USA 106: 7113-7118.
23. Ruschmann, J., V. Ho, F. Antignano, et al Tyrosine phosphorylation of SHIP promotes its proteasomal degradation. Exp. Hematol. 38: 392-402, 402 e391.
24. Damen, J.E., L. Liu, M.D. Ware, et al 1998. Multiple forms of the SH2-containing inositol phosphatase, SHIP, are generated by C-terminal truncation. Blood 92: 1199-1205.
25. Damen, J.E., M.D. Ware, J. Kalesnikoff, et al 2001. SHIP's C-terminus is essential for its hydrolysis of PIP3 and inhibition of mast cell degranulation. Blood 97: 1343-1351.
26. Rohrschneider, L.R., J.M. Custodio, T.A. Anderson, et al 2005. The intron 5/6 promoter region of the ship1 gene regulates expression in stem/progenitor cells of the mouse embryo. Dev. Biol. 283: 503-521.
27. Phee, H., A. Jacob & K.M. Coggeshall 2000. Enzymatic activity of the Src homology 2 domain-containing inositol phosphatase is regulated by a plasma membrane location. J. Biol. Chem. 275: 19090-19097.
28. Miller, A.T., M. Sandberg, Y.H. Huang, et al 2007. Production of Ins(1, 3, 4, 5)P4 mediated by the kinase Itpkb inhibits store-operated calcium channels and regulates B cell selection and activation. Nat. Immunol. 8: 514-521.
29. Damen, J.E., L. Liu, H. Wakao, et al 1997. The role of erythropoietin receptor tyrosine phosphorylation in erythropoietin-induced proliferation. Leukemia 11: 423-425.
30. Huber, M., C.D. Helgason, J.E. Damen, et al 1998. The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation. Proc. Natl. Acad. Sci. USA 95: 11330-11335.
31. Verdier, F., S. Chretien, C. Billat, et al 1997. Erythropoietin induces the tyrosine phosphorylation of insulin receptor substrate-2. An alternate pathway for erythropoietin-induced phosphatidylinositol 3-kinase activation. J. Biol. Chem. 272: 26173-26178.
32. Zamorano, J. & A.D. Keegan 1998. Regulation of apoptosis by tyrosine-containing domains of IL-4R alpha: Y497 and Y713, but not the STAT6-docking tyrosines, signal protection from apoptosis. J. Immunol. 161: 859-867.
33. Zhang, S., C. Mantel & H.E. Broxmeyer 1999. Flt3 signaling involves tyrosyl-phosphorylation of SHP-2 and SHIP and their association with Grb2 and Shc in Baf3/Flt3 cells. J. Leuk. Biol. 65: 372-380.
34. Drachman, J.G. & K. Kaushansky 1997. Dissecting the thrombopoietin receptor: functional elements of the Mpl cytoplasmic domain. Proc. Natl. Acad. Sci. USA 94: 2350-2355.
35. Lemay, S., D. Davidson, S. Latour & A. Veillette 2000. Dok-3, a novel adapter molecule involved in the negative regulation of immunoreceptor signaling. Mol. Cell. Biol. 20: 2743-2754.
36. Robson, J.D., D. Davidson & A. Veillette 2004. Inhibition of the Jun N-terminal protein kinase pathway by SHIP-1, a lipid phosphatase that interacts with the adaptor molecule Dok-3. Mol. Cell. Biol. 24: 2332-2343.
37. Lamkin, T.D., S.F. Walk, L. Liu, et al 1997. Shc interaction with Src homology 2 domain containing inositol phosphatase (SHIP) in vivo requires the Shc-phosphotyrosine binding domain and two specific phosphotyrosines on SHIP. J. Biol. Chem. 272: 10396-10401.
38. Ono, M., S. Bolland, P. Tempst & J.V. Ravetch 1996. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature 383: 263-266.
39. Galandrini, R., I. Tassi, G. Mattia, et al 2002. SH2-containing inostiol phosphatase SHIP-1 transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells. Blood 100: 4581-4589.
40. Wang, J.W., J.M. Howson, T. Ghansah, et al 2002. Influence of SHIP on the NK repertoire and allogeneic bone marrow transplantation. Science 295: 2094-2097.
41. Eissmann, P., L. Beauchamp, J. Wooters, et al 2005. Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood 105: 4722-4729.
42. Abramson, J. & I. Pecht 2002. Clustering the mast cell function-associated antigen (MAFA) leads to tyrosine phosphorylation of p62Dok and SHIP and affects RBL-2H3 cell cycle. Immunol. Lett. 82: 23-28.
43. Gays, F., J.G. Aust, D.M. Reid, et al 2006. Ly49B is expressed on multiple subpopulations of myeloid cells. J. Immunol. 177: 5840-5851.
44. Rohrschneider, L.R., J.F. Fuller, I. Wolf, et al 2000. Structure, function, and biology of SHIP proteins. Genes Dev. 14: 505-520.
45. Krystal, G. 2000. Lipid phosphatases in the immune system [In Process Citation]. Semin. Immunol. 12: 397-403.
46. Tridandapani, S., T. Kelley, M. Pradhan, et al 1997. Recruitment and phosphorylation of SH2-containing inositol phosphatase and Shc to the B-cell Fc gamma immunoreceptor tyrosine-based inhibition motif peptide motif. Mol. Cell. Biol. 17: 4305-4311.
47. Newton, A.C. 1995. Protein kinase C. Seeing two domains. Curr. Biol. 5: 973-976.
48. Hurley, J.H. & T. Meyer 2001. Subcellular targeting by membrane lipids. Curr. Opin. Cell. Biol. 13: 146-152.
49. Ong, C.J., A. Ming-Lum, M. Nodwell, et al 2007. Small-molecule agonists of SHIP1 inhibit the phosphoinositide 3-kinase pathway in hematopoietic cells. Blood 110: 1942-1949.
50. Zhang, J., S.F. Walk, K.S. Ravichandran & J.C. Garrison 2009. Regulation of the Src homology 2 domain-containing inositol 5'-phosphatase (SHIP1) by the cyclic AMP-dependent protein kinase. J. Biol. Chem. 284: 20070-20078.
51. Liu, L., J.E. Damen, M. Ware, et al 1997. SHIP, a new player in cytokine-induced signalling. Leukemia 11: 181-184.
52. Huber, M., C.D. Helgason, J.E. Damen, et al 1999. The role of SHIP in growth factor induced signalling. Progr. Biophys. Mol. Biol. 71: 423-434.
53. Helgason, C.D., J. Antonchuk, C. Bodner & R.K. Humphries 2003. Homeostasis and regeneration of the hematopoietic stem cell pool is altered in SHIP-deficient mice. Blood 102: 3541-3547.
54. Desponts, C., A.L. Hazen, K.H. Paraiso & W.G. Kerr 2006. SHIP deficiency enhances HSC proliferation and survival but compromises homing and repopulation. Blood 107: 4338-4345.
55. Hazen, A.L., M.J. Smith, C. Desponts, et al 2009. SHIP is required for a functional hematopoietic stem cell niche. Blood 113: 2924-2933.
56. Zhu, J., R. Garrett, Y. Jung, et al 2007. Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood 109: 3706-3712.
57. Helgason, C.D., C.P. Kalberer, J.E. Damen, et al 2000. A dual role for Src homology 2 domain-containing inositol-5-phosphatase (SHIP) in immunity: aberrant development and enhanced function of b lymphocytes in ship -/- mice. J. Exp. Med. 191: 781-794.
58. Brauweiler, A., I. Tamir, J. Dal Porto, et al 2000. Differential regulation of B cell development, activation, and death by the src homology 2 domain-containing 5' inositol phosphatase (SHIP). J. Exp. Med. 191: 1545-1554.
59. Nakamura, K., T. Kouro, P.W. Kincade, et al 2004. Src homology 2-containing 5-inositol phosphatase (SHIP) suppresses an early stage of lymphoid cell development through elevated interleukin-6 production by myeloid cells in bone marrow. J. Exp. Med. 199: 243-254.
60. Maeda, K., H. Mehta, D.A. Drevets & K.M. Coggeshall IL-6 increases B-cell IgG production in a feed-forward proinflammatory mechanism to skew hematopoiesis and elevate myeloid production. Blood 115: 4699-4706.
61. Desponts, C., J.M. Ninos & W.G. Kerr 2006. s-SHIP associates with receptor complexes essential for pluripotent stem cell growth and survival. Stem Cells Dev. 15: 641-646.
62. Liu, Q., A.J. Oliveira-Dos-Santos, S. Mariathasan, et al 1998. The inositol polyphosphate 5-phosphatase ship is a crucial negative regulator of B cell antigen receptor signaling. J. Exp. Med. 188: 1333-1342.
63. Ono, M., H. Okada, S. Bolland, et al 1997. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 90: 293-301.
64. Marechal, Y., X. Pesesse, Y. Jia, et al 2007. Inositol 1, 3, 4, 5-tetrakisphosphate controls proapoptotic Bim gene expression and survival in B cells. Proc. Natl. Acad. Sci. USA 104: 13978-13983.
65. Marechal, Y., S. Queant, S. Polizzi, et al Inositol 1, 4, 5-trisphosphate 3-kinase B controls survival and prevents anergy in B cells. Immunobiology DOI: S0171-2985(10)00050-1 [pii].
66. Wahle, J.A., K.H. Paraiso, A.L. Costello, et al 2006. Cutting edge: dominance by an MHC-independent inhibitory receptor compromises NK killing of complex targets. J. Immunol. 176: 7165-7169.
67. Kerr, W.G. 2007. Acquisition and remodeling of the NK receptor repertoire. In Everything You Wanted to Know About NK Cells, But Were Afraid to Ask. L. Brossay, Ed. Research Signpost. Kerala, India.
68. Ghansah, T., K.H. Paraiso, S. Highfill, et al 2004. Expansion of myeloid suppressor cells in SHIP-deficient mice represses allogeneic T cell responses. J. Immunol. 173: 7324-7330.
69. Marti, F., C.W. Xu, A. Selvakumar, et al 1998. LCK-phosphorylated human killer cell-inhibitory receptors recruit and activate phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 95: 11810-11815.
70. Xu, R., J. Abramson, M. Fridkin & I. Pecht 2001. SH2 domain-containing inositol polyphosphate 5'-phosphatase is the main mediator of the inhibitory action of the mast cell function-associated antigen. J. Immunol. 167 6394-6402.
71. Abramson, J., R. Xu & I. Pecht 2002. An unusual inhibitory receptor-the mast cell function-associated antigen (MAFA). Mol. Immunol. 38: 1307-1313.
72. Fortenbery, N.R., K.H. Paraiso, M. Taniguchi, et al SHIP influences signals from CD48 and MHC class I ligands that regulate NK cell homeostasis, effector function, and repertoire formation. J. Immunol. 184: 5065-5074.
73. Kim, S., J. Poursine-Laurent, S.M. Truscott, et al 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436: 709-713.
74. Johansson, S., M. Johansson, E. Rosmaraki, et al 2005. Natural killer cell education in mice with single or multiple major histocompatibility complex class I molecules. J. Exp. Med. 201: 1145-1155.
75. Khoo, N.K., L. Fahlen & C.L. Sentman 1998. Modulation of Ly49A receptors on mature cells to changes in major histocompatibility complex class I molecules. Immunology 95: 126-131.
76. Paraiso, K.H., T. Ghansah, A. Costello, et al 2007. Induced SHIP deficiency expands myeloid regulatory cells and abrogates graft-versus-host disease. J. Immunol. 178: 2893-2900.
77. Neill, L., A.H. Tien, J. Rey-Ladino & C.D. Helgason 2007. SHIP-deficient mice provide insights into the regulation of dendritic cell development and function. Exp. Hematol. 35: 627-639.
78. Antignano, F., M. Ibaraki, C. Kim, et al SHIP is required for dendritic cell maturation. J. Immunol. 184: 2805-2813.
79. Shlomchik, W.D., M.S. Couzens, C.B. Tang, et al 1999. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285: 412-415.
80. Freeburn, R.W., K.L. Wright, S.J. Burgess, et al 2002. Evidence that SHIP-1 contributes to phosphatidylinositol 3, 4, 5-trisphosphate metabolism in T lymphocytes and can regulate novel phosphoinositide 3-kinase effectors. J. Immunol. 169: 5441-5450.
81. Tomlinson, M.G., V.L. Heath, C.W. Turck, et al 2004. SHIP family inositol phosphatases interact with and negatively regulate the Tec tyrosine kinase. J. Biol. Chem. 279: 55089-55096.
82. Tessmer, M.S., C. Fugere, F. Stevenaert, et al 2007. KLRG1 binds cadherins and preferentially associates with SHIP-1. Int. Immunol. 19: 391-400.
83. Dong, S., B. Corre, E. Foulon, et al 2006. T cell receptor for antigen induces linker for activation of T cell-dependent activation of a negative signaling complex involving Dok-2, SHIP-1, and Grb-2. J. Exp. Med. 203: 2509-2518.
84. Collazo, M.M., D. Wood, K.H. Paraiso, et al 2009. SHIP limits immunoregulatory capacity in the T-cell compartment. Blood 113: 2934-2944.
85. Locke, N.R., S.J. Patterson, M.J. Hamilton, et al 2009. SHIP regulates the reciprocal development of T regulatory and Th17 cells. J. Immunol. 183: 975-983.
86. Tarasenko, T., H.K. Kole, A.W. Chi, et al 2007. T cell-specific deletion of the inositol phosphatase SHIP reveals its role in regulating Th1/Th2 and cytotoxic responses. Proc. Natl. Acad. Sci. USA 104: 11382-11387.
87. Helgason, C.D., J.E. Damen, P. Rosten, et al 1998. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 12: 1610-1620.
88. Karlsson, M.C., R. Guinamard, S. Bolland, et al 2003. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J. Exp. Med. 198: 333-340.
89. Lo, T.C., L.M. Barnhill, Y. Kim, et al 2009. Inactivation of SHIP1 in T-cell acute lymphoblastic leukemia due to mutation and extensive alternative splicing. Leuk. Res. 33: 1562-1566.
90. Kashiwada, M., G. Cattoretti, L. McKeag, et al 2006. Downstream of tyrosine kinases-1 and Src homology 2-containing inositol 5'-phosphatase are required for regulation of CD4+CD25+ T cell development. J. Immunol. 176: 3958-3965.
91. Taylor, P.A., A. Panoskaltsis-Mortari, J.M. Swedin, et al 2004. L-Selectin(hi) but not the L-selectin(lo) CD4 + 25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood 104: 3804-3812.
92. Kerr, W.G., M.Y. Park, M. Maubert & R.W. Engelman SHIP deficiency causes Crohn's disease-like ileitis. Gut doi: PMID: 20940287.
93. Cox, D., B.M. Dale, M. Kashiwada, et al 2001. A regulatory role for Src homology 2 domain-containing inositol 5'-phosphatase (SHIP) in phagocytosis mediated by Fc gamma receptors and complement receptor 3 (alpha(M)beta(2); CD11b/CD18). J. Exp. Med. 193: 61-71.
94. Ganesan, L.P., T. Joshi, H. Fang, et al 2006. FcgammaR-induced production of superoxide and inflammatory cytokines is differentially regulated by SHIP through its influence on PI3K and/or Ras/Erk pathways. Blood 108: 718-725.
95. Kamen, L.A., J. Levinsohn, A. Cadwallader, et al 2008. SHIP-1 increases early oxidative burst and regulates phagosome maturation in macrophages. J. Immunol. 180: 7497-7505.
96. Takeshita, S., N. Namba, J.J. Zhao, et al 2002. SHIP-deficient mice are severely osteoporotic due to increased numbers of hyper-resorptive osteoclasts. Nat. Med. 8: 943-949.
97. Bronte, V., M. Wang, W.W. Overwijk, et al 1998. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J. Immunol. 161: 5313-5320.
98. Gabrilovich, D.I., V. Bronte, S.H. Chen, et al 2007. The terminology issue for myeloid-derived suppressor cells. Cancer Res. 67: 425; author reply 426.
99. Sakaguchi, S., N. Sakaguchi, M. Asano, et al 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
100. Thornton, A.M. & E.M. Shevach 1998. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188: 287-296.
101. Freud, A.G., B. Becknell, S. Roychowdhury, et al 2005. A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 22: 295-304.
102. Yanaba, K., J.D. Bouaziz, K.M. Haas, et al 2008. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28: 639-650.
103. Rauh, M.J., V. Ho, C. Pereira, et al 2005. SHIP represses the generation of alternatively activated macrophages. Immunity 23: 361-374.
104. Nishio, M., K. Watanabe, J. Sasaki, et al 2007. Control of cell polarity and motility by the PtdIns(3, 4, 5)P3 phosphatase SHIP1. Nat. Cell. Biol. 9: 36-44.
105. Kuroda, E., V. Ho, J. Ruschmann, et al 2009. SHIP represses the generation of IL-3-induced M2 macrophages by inhibiting IL-4 production from basophils. J. Immunol. 183: 3652-3660.
106. Haddon, D.J., F. Antignano, M.R. Hughes, et al 2009. SHIP1 is a repressor of mast cell hyperplasia, cytokine production, and allergic inflammation in vivo. J. Immunol. 183: 228-236.
107. Huber, M., C.D. Helgason, M.P. Scheid, et al 1998. Targeted disruption of SHIP leads to steel factor-induced degranulation of mast cells. EMBO J. 17: 7311-7319.
108. Oh, S.Y., T. Zheng, M.L. Bailey, et al 2007. Src homology 2 domain-containing inositol 5-phosphatase 1 deficiency leads to a spontaneous allergic inflammation in the murine lung. J. Allergy Clin. Immunol. 119: 123-131.
109. Sly, L.M., M.J. Hamilton, E. Kuroda, et al 2009. SHIP prevents lipopolysaccharide from triggering an antiviral response in mice. Blood 113: 2945-2954.
110. Moody, J.L., L. Xu, C.D. Helgason & F.R. Jirik 2004. Anemia, thrombocytopenia, leukocytosis, extramedullary hematopoiesis, and impaired progenitor function in Pten+/-SHIP-/- mice: a novel model of myelodysplasia. Blood 103: 4503-4510.
111. Perez, L.E., C. Desponts, N. Parquet & W.G. Kerr 2008. SH2-inositol phosphatase 1 negatively influences early megakaryocyte progenitors. PLoS One 3: e3565.
112. McMorran, B.J., V.M. Marshall, C. de Graaf, et al 2009. Platelets kill intraerythrocytic malarial parasites and mediate survival to infection. Science 323: 797-800.
113. Chari, R., S. Kim, S. Murugappan, et al 2009. Lyn, PKC-delta, SHIP-1 interactions regulate GPVI-mediated platelet-dense granule secretion. Blood 114: 3056-3063.
114. Hunter, M.G., A. Jacob, C. O'Donnell L, et al 2004. Loss of SHIP and CIS recruitment to the granulocyte colony-stimulating factor receptor contribute to hyperproliferative responses in severe congenital neutropenia/acute myelogenous leukemia. J. Immunol. 173: 5036-5045.
115. Luo, J.M., Z.L. Liu, H.L. Hao, et al 2004. Mutation analysis of SHIP gene in acute leukemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi 12: 420-426.
116. Fukuda, R., A. Hayashi, A. Utsunomiya, et al 2005. Alteration of phosphatidylinositol 3-kinase cascade in the multilobulated nuclear formation of adult T cell leukemia/lymphoma (ATLL). Proc. Natl. Acad. Sci. USA 102: 15213-15218.
117. Luo, J.M., H. Yoshida, S. Komura, et al 2003. Possible dominant-negative mutation of the SHIP gene in acute myeloid leukemia. Leukemia 17: 1-8.
118. Gilby, D.C., A.C. Goodeve, P.R. Winship, et al 2007. Gene structure, expression profiling and mutation analysis of the tumour suppressor SHIP1 in Caucasian acute myeloid leukaemia. Leukemia 21: 2390-2393.
119. Siegel, J., Y. Li & P. Whyte 1999. SHIP-mediated inhibition of K562 erythroid differentiation requires an intact catalytic domain and Shc binding site. Oncogene 18: 7135-7148.
120. Choi, Y., J. Zhang, C. Murga, et al 2002. PTEN, but not SHIP and SHIP2, suppresses the PI3K/Akt pathway and induces growth inhibition and apoptosis of myeloma cells. Oncogene 21: 5289-5300.
121. Wu, J., F. Meng, L.Y. Kong, et al 2008. Association between imatinib-resistant BCR-ABL mutation-negative leukemia and persistent activation of LYN kinase. J. Natl. Cancer Inst. 100: 926-939.
122. Dos Santos, C., C. Demur, V. Bardet, et al 2008. A critical role for Lyn in acute myeloid leukemia. Blood 111: 2269-2279.
123. Okamoto, M., F. Hayakawa, Y. Miyata, et al 2007. Lyn is an important component of the signal transduction pathway specific to FLT3/ITD and can be a therapeutic target in the treatment of AML with FLT3/ITD. Leukemia 21: 403-410.
124. Jain, S.K., M. Susa, M.L. Keeler, et al 1996. PI 3-kinase activation in BCR/abl-transformed hematopoietic cells does not require interaction of p85 SH2 domains with p210 BCR/abl. Blood 88: 1542-1550.
125. Gewinner, C., Z.C. Wang, A. Richardson, et al 2009. Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell 16: 115-125.
126. Ivetac, I., R. Gurung, S. Hakim, et al 2009. Regulation of PI(3)K/Akt signalling and cellular transformation by inositol polyphosphate 4-phosphatase-1. EMBO Rep. 10: 487-493.
127. Kennah, M., T.Y. Yau, M. Nodwell, et al 2009. Activation of SHIP via a small molecule agonist kills multiple myeloma cells. Exp. Hematol 37: 1274-1283.
128. Prasad, N.K., M. Tandon, S. Badve, et al 2008. Phosphoinositol phosphatase SHIP2 promotes cancer development and metastasis coupled with alterations in EGF receptor turnover. Carcinogenesis 29: 25-34.
129. Ruggeri, L., M. Capanni, E. Urbani, et al 2002. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295: 2097-2100.
130. Galandrini, R., I. Tassi, G. Mattia, et al 2002. SH2-containing inositol phosphatase (SHIP-1) transiently translocates to raft domains and modulates CD16-mediated cytotoxicity in human NK cells. Blood 100: 4581-4589.