Role of inositol poly-phosphatases and their targets in T cell biology

Frontiers in Immunology

Volumn 4, Issue SEP, 2013, Pages

  Srivastava, Neetu ^a   Sudan, Raki ^a   Kerr, William Garrow ^a,b  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b SYRACUSE UNIVERSITY   (United States)

Author keywords

Adoptive T cell transfer; INPP4; PI3K; PTEN; SHIP1; SHIP2; T cells; T lymphocytes

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN DAPP1; ADAPTOR PROTEIN SKAPP HOM; ADAPTOR PROTEIN SKAPP55; ADAPTOR PROTEIN TAPP1; ADAPTOR PROTEIN TAPP2; BRUTON TYROSINE KINASE; INOSITOL 1, 3, 4, 5 TETRAKISPHOSPHATE; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3, 4 BISPHOSPHATE; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOLIPASE C GAMMA; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; SYNAPTOJANIN; UNCLASSIFIED DRUG;

APOPTOSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR IMMUNITY; EFFECTOR CELL; GENE TARGETING; HUMAN; IMMUNOREGULATION; INTRACELLULAR SIGNALING; LYMPHOCYTE MIGRATION; NONHUMAN; PHOSPHOINOSITIDE METABOLISM; PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; TH17 CELL;

EID: 84886015544     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00288     Document Type: Review

References (116)

1. Fayard E, Moncayo G, Hemmings BA, Hollander GA. Phosphatidylinositol 3-kinase signaling in thymocytes: the need for stringent control. Sci Signal (2010) 3:re5. doi:10.1126/scisignal.3135re5.
2. Huang YH, Sauer K. Lipid signaling in T-cell development and function. Cold Spring Harb Perspect Biol (2010) 2:a002428. doi:10.1101/cshperspect.a002428.
3. Okkenhaug K, Vanhaesebroeck B. PI3K in lymphocyte development, differentiation and activation. Nat Rev Immunol (2003) 3:317-30. doi:10.1038/nri1056.
4. So L, Fruman DA. PI3K signalling in B-and T-lymphocytes: new developments and therapeutic advances. Biochem J (2012) 442:465-81. doi:10.1042/BJ20112092.
5. Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol (2008) 9:99-111. doi:10.1038/nrm2328.
6. Fayard E, Xue G, Parcellier A, Bozulic L, Hemmings BA. Protein kinase B (PKB/Akt), a key mediator of the PI3K signaling pathway. Curr Top Microbiol Immunol (2010) 346:31-56. doi:10.1007/82_2010_58.
7. Fruman DA. Phosphoinositide 3-kinase and its targets in B-cell and T-cell signaling. Curr Opin Immunol (2004) 16:314-20. doi:10.1016/j.coi.2004.03.014.
8. Janas ML, Varano G, Gudmundsson K, Noda M, Nagasawa T, Turner M. Thymic development beyond beta-selection requires phosphatidylinositol 3-kinase activation by CXCR4. J Exp Med (2010) 207:247-61. doi:10.1084/jem.20091430.
9. Ji H, Rintelen F, Waltzinger C, Bertschy Meier D, Bilancio A, Pearce W, et al. Inactivation of PI3Kgamma and PI3Kdelta distorts T-cell development and causes multiple organ inflammation. Blood (2007) 110:2940-7. doi:10.1182/blood-2007-04-086751.
10. Shiroki F, Matsuda S, Doi T, Fujiwara M, Mochizuki Y, Kadowaki T, et al. The p85alpha regulatory subunit of class IA phosphoinositide 3-kinase regulates beta-selection in thymocyte development. J Immunol (2007) 178:1349-56.
11. Swat W, Montgrain V, Doggett TA, Douangpanya J, Puri K, Vermi W, et al. Essential role of PI3Kdelta and PI3Kgamma in thymocyte survival. Blood (2006) 107:2415-22. doi:10.1182/blood-2005-08-3300.
12. Webb LM, Vigorito E, Wymann MP, Hirsch E, Turner M. Cutting edge: T cell development requires the combined activities of the p110gamma and p110delta catalytic isoforms of phosphatidylinositol 3-kinase. J Immunol (2005) 175:2783-7.
13. Okkenhaug K, Patton DT, Bilancio A, Garcon F, Rowan WC, Vanhaesebroeck B. The p110delta isoform of phosphoinositide 3-kinase controls clonal expansion and differentiation of Th cells. J Immunol (2006) 177:5122-8.
14. Patton DT, Garden OA, Pearce WP, Clough LE, Monk CR, Leung E, et al. Cutting edge: the phosphoinositide 3-kinase p110 delta is critical for the function of CD4+CD25+Foxp3+ regulatory T cells. J Immunol (2006) 177:6598-602.
15. Patton DT, Wilson MD, Rowan WC, Soond DR, Okkenhaug K. The PI3K p110delta regulates expression of CD38 on regulatory T cells. PLoS One (2011) 6:e17359. doi:10.1371/journal.pone.0017359.
16. Deane JA, Kharas MG, Oak JS, Stiles LN, Luo J, Moore TI, et al. T-cell function is partially maintained in the absence of class IA phosphoinositide 3-kinase signaling. Blood (2007) 109:2894-902.
17. Oak JS, Deane JA, Kharas MG, Luo J, Lane TE, Cantley LC, et al. Sjogren's syndrome-like disease in mice with T cells lacking class 1A phosphoinositide-3-kinase. Proc Natl Acad Sci U S A (2006) 103:16882-7. doi:10.1073/pnas.0607984103.
18. Damen JE, Liu L, Rosten P, Humphries RK, Jefferson AB, Majerus PW, et al. 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 U S A (1996) 93:1689-93. doi:10.1073/pnas.93.4.1689.
19. Di Cristofano A, Pesce B, Cordon-Cardo C, PandolfiPP. Pten is essential for embryonic development and tumour suppression. Nat Genet (1998) 19:348-55. doi:10.1038/1235.
20. Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM, et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev (1998) 12:1610-20.
21. Suzuki A, Nakano T, Mak TW, Sasaki T. Portrait of PTEN: messages from mutant mice. Cancer Sci (2008) 99:209-13. doi:10.1111/j.1349-7006.2007.00670.x.
22. Suzuki A, Yamaguchi MT, Ohteki T, Sasaki T, Kaisho T, Kimura Y, et al. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity (2001) 14:523-34. doi:10.1016/S1074-7613(01)00134-0.
23. Kerr WG. Inhibitor and activator: dual functions for SHIP in immunity and cancer. Ann N Y Acad Sci (2011) 1217:1-17. doi:10.1111/j.1749-6632.2010.05869.x.
24. Hazen AL, Smith MJ, Desponts C, Winter O, Moser K, Kerr WG. SHIP is required for a functional hematopoietic stem cell niche. Blood (2009) 113:2924-33. doi:10.1182/blood-2008-02-138008.
25. Osborne MA, Zenner G, Lubinus M, Zhang X, Songyang Z, Cantley LC, et al. The inositol 5'-phosphatase SHIP binds to immunoreceptor signaling motifs and responds to high affinity IgE receptor aggregation. J Biol Chem (1996) 271:29271-8. doi:10.1074/jbc.271.46.29271.
26. Pesesse X, Backers K, Moreau C, Zhang J, Blero D, Paternotte N, et al. SHIP1/2 interaction with tyrosine phosphorylated peptides mimicking an immunoreceptor signalling motif. Adv Enzyme Regul (2006) 46:142-53. doi:10.1016/j.advenzreg.2006.01.013.
27. Dowler S, Currie RA, Campbell DG, Deak M, Kular G, Downes CP, et al. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem J (2000) 351:19-31. doi:10.1042/0264-6021:3510019.
28. Lemmon MA, Ferguson KM. Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J (2000) 350(Pt 1):1-18. doi:10.1042/0264-6021:3500001.
29. Kerr WG, Park MY, Maubert M, Engelman RW. SHIP deficiency causes Crohn's disease-like ileitis. Gut (2011) 60:177-88. doi:10.1136/gut.2009.202283.
30. Ghansah T, Paraiso KH, Highfill S, Desponts C, May S, McIntosh JK, et al. Expansion of myeloid suppressor cells in SHIP-deficient mice represses allogeneic T cell responses. J Immunol (2004) 173:7324-30.
31. Edmunds C, Parry RV, Burgess SJ, Reaves B, Ward SG. CD28 stimulates tyrosine phosphorylation, cellular redistribution and catalytic activity of the inositol lipid 5-phosphatase SHIP. Eur J Immunol (1999) 29:3507-15. doi:10.1002/(SICI)1521-4141(199911)29:11<3507::AID-IMMU3507>3.0.CO;2-9.
32. Dong S, Corre B, Foulon E, Dufour E, Veillette A, Acuto O, et al. 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 (2006) 203:2509-18. doi:10.1084/jem.20060650.
33. Waterman PM, Marschner S, Brandl E, Cambier JC. The inositol 5-phosphatase SHIP-1 and adaptors Dok-1 and 2 play central roles in CD4-mediated inhibitory signaling. Immunol Lett (2012) 143:122-30. doi:10.1016/j.imlet.2012.02.009.
34. Scharenberg AM, El-Hillal O, Fruman DA, Beitz LO, Li Z, Lin S, et al. 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 (1998) 17:1961-72. doi:10.1093/emboj/17.7.1961.
35. Tomlinson MG, Heath VL, Turck CW, Watson SP, Weiss A. SHIP family inositol phosphatases interact with and negatively regulate the Tec tyrosine kinase. J Biol Chem (2004) 279:55089-96. doi:10.1074/jbc. M408141200.
36. Kashiwada M, Cattoretti G, McKeag L, Rouse T, Showalter BM, Al-Alem U, et al. 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 (2006) 176:3958-65.
37. Tarasenko T, Kole HK, Chi AW, Mentink-Kane MM, Wynn TA, Bolland S. T cell-specific deletion of the inositol phosphatase SHIP reveals its role in regulating Th1/Th2 and cytotoxic responses. Proc Natl Acad Sci U S A (2007) 104:11382-7. doi:10.1073/pnas.0704853104.
38. Leung WH, Tarasenko T, Bolland S. Differential roles for the inositol phosphatase SHIP in the regulation of macrophages and lymphocytes. Immunol Res (2009) 43:243-51. doi:10.1007/s12026-008-8078-1.
39. Maxwell MJ, Duan M, Armes JE, Anderson GP, Tarlinton DM, Hibbs ML. Genetic segregation of inflammatory lung disease and autoimmune disease severity in SHIP-1-/-mice. J Immunol (2011) 186:7164-75. doi:10.4049/jimmunol.1004185.
40. Peng Q, Malhotra S, Torchia JA, Kerr WG, Coggeshall KM, Humphrey MB. TREM2-and DAP12-dependent activation of PI3K requires DAP10 and is inhibited by SHIP1. Sci Signal (2010) 3:ra38. doi:10.1126/scisignal.2000500.
41. Wahle JA, Paraiso KH, Kendig RD, Lawrence HR, Chen L, Wu J, et al. 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 (2007) 179:8009-15.
42. Fernandes S, Iyer S, Kerr WG. Role of SHIP1 in cancer and mucosal inflammation. Ann N Y Acad Sci (2013) 1280:6-10. doi:10.1111/nyas.12038.
43. Brooks R, Fuhler GM, Iyer S, Smith MJ, Park MY, Paraiso KH, et al. SHIP1 inhibition increases immunoregulatory capacity and triggers apoptosis of hematopoietic cancer cells. J Immunol (2010) 184:3582-9. doi:10.4049/jimmunol.0902844.
44. Collazo MM, Paraiso KH, Park MY, Hazen AL, Kerr WG. Lineage extrinsic and intrinsic control of immunoregulatory cell numbers by SHIP. Eur J Immunol (2012) 42:1785-95. doi:10.1002/eji.201142092.
45. Collazo MM, Wood D, Paraiso KH, Lund E, Engelman RW, Le CT, et al. SHIP limits immunoregulatory capacity in the T-cell compartment. Blood (2009) 113:2934-44. doi:10.1182/blood-2008-09-181164.
46. Paraiso KH, Ghansah T, Costello A, Engelman RW, Kerr WG. Induced SHIP deficiency expands myeloid regulatory cells and abrogates graft-versus-host disease. J Immunol (2007) 178:2893-900.
47. Locke NR, Patterson SJ, Hamilton MJ, Sly LM, Krystal G, Levings MK. SHIP regulates the reciprocal development of T regulatory and Th17 cells. J Immunol (2009) 183:975-83. doi:10.4049/jimmunol.0803749.
48. O'Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci U S A (2009) 106:7113-8. doi:10.1073/pnas.0902636106.
49. Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, MacIsaac KD, et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature (2007) 445:931-5. doi:10.1038/nature05478.
50. Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature (2007) 445:936-40. doi:10.1038/nature05563.
51. Di Cristofano A, Kotsi P, Peng YF, Cordon-Cardo C, Elkon KB, PandolfiPP. Impaired Fas response and autoimmunity in Pten± mice. Science (1999) 285:2122-5. doi:10.1126/science.285.5436.2122.
52. Hagenbeek TJ, Naspetti M, Malergue F, Garcon F, Nunes JA, Cleutjens KB, et al. The loss of PTEN allows TCR alphabeta lineage thymocytes to bypass IL-7 and Pre-TCR-mediated signaling. J Exp Med (2004) 200:883-94. doi:10.1084/jem.20040495.
53. Walsh PT, Buckler JL, Zhang J, Gelman AE, Dalton NM, Taylor DK, et al. PTEN inhibits IL-2 receptor-mediated expansion of CD4+ CD25+ Tregs. J Clin Invest (2006) 116:2521-31.
54. Soond DR, Garcon F, Patton DT, Rolf J, Turner M, Scudamore C, et al. Pten loss in CD4 T cells enhances their helper function but does not lead to autoimmunity or lymphoma. J Immunol (2012) 188:5935-43. doi:10.4049/jimmunol.1102116.
55. Afonso PV, Parent CA. PI3K and chemotaxis: a priming issue? Sci Signal (2011) 4:e22. doi:10.1126/scisignal.2002019.
56. Ward SG. Do phosphoinositide 3-kinases direct lymphocyte navigation? Trends Immunol (2004) 25:67-74. doi:10.1016/j.it.2003.12.003.
57. Nishio M, Watanabe K, Sasaki J, Taya C, Takasuga S, Iizuka R, et al. Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1. Nat Cell Biol (2007) 9:36-44. doi:10.1038/ncb1515.
58. Kim CH, Hangoc G, Cooper S, Helgason CD, Yew S, Humphries RK, et al. Altered responsiveness to chemokines due to targeted disruption of SHIP. J Clin Invest (1999) 104:1751-9. doi:10.1172/JCI7310.
59. Wain CM, Westwick J, Ward SG. Heterologous regulation of chemokine receptor signaling by the lipid phosphatase SHIP in lymphocytes. Cell Signal (2005) 17:1194-202. doi:10.1016/j.cellsig.2004.12.009.
60. Harris SJ, Parry RV, Foster JG, Blunt MD, Wang A, Marelli-Berg F, et al. Evidence that the lipid phosphatase SHIP-1 regulates T lymphocyte morphology and motility. J Immunol (2011) 186:4936-45. doi:10.4049/jimmunol.1002350.
61. Nijhara R, van Hennik PB, Gignac ML, Kruhlak MJ, Hordijk PL, Delon J, et al. Rac1 mediates collapse of microvilli on chemokine-activated T lymphocytes. J Immunol (2004) 173:4985-93.
62. Al-Alwan M, Hou S, Zhang TT, Makondo K, Marshall AJ. Bam32/DAPP1 promotes B cell adhesion and formation of polarized conjugates with T cells. J Immunol (2010) 184:6961-9. doi:10.4049/jimmunol.0904176.
63. Boer AK, Drayer AL, Vellenga E. Effects of overexpression of the SH2-containing inositol phosphatase SHIP on proliferation and apoptosis of erythroid AS-E2 cells. Leukemia (2001) 15:1750-7. doi:10.1038/sj.leu.2402261.
64. Brauweiler A, Tamir I, Dal Porto J, Benschop RJ, Helgason CD, Humphries RK, et al. Differential regulation of B cell development, activation, and death by the src homology 2 domain-containing 5' inositol phosphatase (SHIP). J Exp Med (2000) 191:1545-54. doi:10.1084/jem.191.9.1545.
65. Gardai S, Whitlock BB, Helgason C, Ambruso D, Fadok V, Bratton D, et al. Activation of SHIP by NADPH oxidase-stimulated Lyn leads to enhanced apoptosis in neutrophils. J Biol Chem (2002) 277:5236-46. doi:10.1074/jbc. M110005200.
66. Valderrama-Carvajal H, Cocolakis E, Lacerte A, Lee EH, Krystal G, Ali S, et al. Activin/TGF-beta induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat Cell Biol (2002) 4:963-9. doi:10.1038/ncb885.
67. Charlier E, Conde C, Zhang J, Deneubourg L, Di Valentin E, Rahmouni S, et al. SHIP-1 inhibits CD95/APO-1/Fas-induced apoptosis in primary T lymphocytes and T leukemic cells by promoting CD95 glycosylation independently of its phosphatase activity. Leukemia (2010) 24:821-32. doi:10.1038/leu.2010.9.
68. Gloire G, Charlier E, Rahmouni S, Volanti C, Chariot A, Erneux C, et al. Restoration of SHIP-1 activity in human leukemic cells modifies NF-kappaB activation pathway and cellular survival upon oxidative stress. Oncogene (2006) 25:5485-94. doi:10.1038/sj.onc.1209542.
69. Ono M, Okada H, Bolland S, Yanagi S, Kurosaki T, Ravetch JV. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell (1997) 90:293-301. doi:10.1016/S0092-8674(00)80337-2.
70. Pearse RN, Kawabe T, Bolland S, Guinamard R, Kurosaki T, Ravetch JV. SHIP recruitment attenuates Fc gamma RIIB-induced B cell apoptosis. Immunity (1999) 10:753-60. doi:10.1016/S1074-7613(00)80074-6.
71. Franke TF, Kaplan DR, Cantley LC, Toker A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate [see comments]. Science (1997) 275:665-8. doi:10.1126/science.275.5300.665.
72. Ma K, Cheung SM, Marshall AJ, Duronio V. 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 (2008) 20:684-94. doi:10.1016/j.cellsig.2007.12.004.
73. Fuhler GM, Brooks R, Toms B, Iyer S, Gengo EA, Park MY, et al. Therapeutic potential of SH2 domain-containing inositol-5'-phosphatase 1 (SHIP1) and SHIP2 inhibition in cancer. Mol Med (2012) 18:65-75. doi:10.2119/molmed.2011.00178.
74. Gewinner C, Wang ZC, Richardson A, Teruya-Feldstein J, Etemadmoghadam D, Bowtell D, et al. Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell (2009) 16:115-25. doi:10.1016/j.ccr.2009.06.006.
75. Ivetac I, Gurung R, Hakim S, Horan KA, Sheffield DA, Binge LC, et al. Regulation of PI(3)K/Akt signalling and cellular transformation by inositol polyphosphate 4-phosphatase-1. EMBO Rep (2009) 10:487-93. doi:10.1038/embor.2009.28.
76. Zhang TT, Li H, Cheung SM, Costantini JL, Hou S, Al-Alwan M, et al. Phosphoinositide 3-kinase-regulated adapters in lymphocyte activation. Immunol Rev (2009) 232:255-72. doi:10.1111/j.1600-065X.2009.00838.x.
77. Marshall AJ, Krahn AK, Ma K, Duronio V, Hou S. TAPP1 and TAPP2 are targets of phosphatidylinositol 3-kinase signaling in B cells: sustained plasma membrane recruitment triggered by the B-cell antigen receptor. Mol Cell Biol (2002) 22:5479-91. doi:10.1128/MCB.22.15.5479-5491.2002.
78. Kliche S, Breitling D, Togni M, Pusch R, Heuer K, Wang X, et al. The ADAP/SKAP55 signaling module regulates T-cell receptor-mediated integrin activation through plasma membrane targeting of Rap1. Mol Cell Biol (2006) 26:7130-44. doi:10.1128/MCB.00331-06.
79. Zhang TT, Al-Alwan M, Marshall AJ. The pleckstrin homology domain adaptor protein Bam32/DAPP1 is required for germinal center progression. J Immunol (2010) 184:164-72. doi:10.4049/jimmunol.0902505.
80. Rouquette-Jazdanian AK, Sommers CL, Kortum RL, Morrison DK, Samelson LE. LAT-independent Erk activation via Bam32-PLC-gamma1-Pak1 complexes: GTPase-independent Pak1 activation. Mol Cell (2012) 48:298-312. doi:10.1016/j.molcel.2012.08.011.
81. Sommers CL, Gurson JM, Surana R, Barda-Saad M, Lee J, Kishor A, et al. Bam32: a novel mediator of Erk activation in T cells. Int Immunol (2008) 20:811-8. doi:10.1093/intimm/dxn039.
82. Krahn AK, Ma K, Hou S, Duronio V, Marshall AJ. Two distinct waves of membrane-proximal B cell antigen receptor signaling differentially regulated by Src homology 2-containing inositol polyphosphate 5-phosphatase. J Immunol (2004) 172:331-9.
83. Wullschleger S, Wasserman DH, Gray A, Sakamoto K, Alessi DR. Role of TAPP1 and TAPP2 adaptor binding to PtdIns(3,4)P2 in regulating insulin sensitivity defined by knock-in analysis. Biochem J (2011) 434:265-74. doi:10.1042/BJ20102012.
84. Landego I, Jayachandran N, Wullschleger S, Zhang TT, Gibson IW, Miller A, et al. Interaction of TAPP adapter proteins with phosphatidylinositol (3,4)-bisphosphate regulates B-cell activation and autoantibody production. Eur J Immunol (2012) 42:2760-70. doi:10.1002/eji.201242371.
85. Kimber WA, Deak M, Prescott AR, Alessi DR. Interaction of the protein tyrosine phosphatase PTPL1 with the PtdIns(3,4)P2-binding adaptor protein TAPP1. Biochem J (2003) 376:525-35. doi:10.1042/BJ20031154.
86. Lioubin MN, Algate PA, Tsai S, Carlberg K, Aebersold A, Rohrschneider LR. p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev (1996) 10:1084-95. doi:10.1101/gad.10.9.1084.
87. Sauer K, Cooke MP. Regulation of immune cell development through soluble inositol-1,3,4,5-tetrakisphosphate. Nat Rev Immunol (2010) 10:257-71. doi:10.1038/nri2745.
88. Pouillon V, Hascakova-Bartova R, Pajak B, Adam E, Bex F, Dewaste V, et al. Inositol 1,3,4,5-tetrakisphosphate is essential for T lymphocyte development. Nat Immunol (2003) 4:1136-43. doi:10.1038/ni980.
89. Wen BG, Pletcher MT, Warashina M, Choe SH, Ziaee N, Wiltshire T, et al. Inositol (1,4,5) trisphosphate 3 kinase B controls positive selection of T cells and modulates Erk activity. Proc Natl Acad Sci U S A (2004) 101:5604-9. doi:10.1073/pnas.0306907101.
90. Huang YH, Grasis JA, Miller AT, Xu R, Soonthornvacharin S, Andreotti AH, et al. Positive regulation of Itk PH domain function by soluble IP4. Science (2007) 316:886-9. doi:10.1126/science.1138684.
91. Iyer S, Margulies BS, Kerr WG. Role of SHIP1 in bone biology. Ann N Y Acad Sci (2013) 1280:11-4. doi:10.1111/nyas.12091.
92. Muraille E, Pesesse X, Kuntz C, Erneux C. Distribution of the src-homology-2-domain-containing inositol 5-phosphatase SHIP-2 in both non-haemopoietic and haemopoietic cells and possible involvement of SHIP-2 in negative signalling of B-cells. Biochem J (1999) 342(Pt 3):697-705. doi:10.1042/0264-6021:3420697.
93. Wisniewski D, Strife A, Swendeman S, Erdjument-Bromage H, Geromanos S, Kavanaugh WM, et al. A novel SH2-containing phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase (SHIP2) is constitutively tyrosine phosphorylated and associated with src homologous and collagen gene (SHC) in chronic myelogenous leukemia progenitor cells. Blood (1999) 93:2707-20.
94. Nakatsu F, Perera RM, Lucast L, Zoncu R, Domin J, Gertler FB, et al. The inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics. J Cell Biol (2010) 190:307-15. doi:10.1083/jcb.201005018.
95. Ooms LM, Horan KA, Rahman P, Seaton G, Gurung R, Kethesparan DS, et al. The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem J (2009) 419:29-49. doi:10.1042/BJ20081673.
96. Bruyns C, Pesesse X, Moreau C, Blero D, Erneux C. The two SH2-domain-containing inositol 5-phosphatases SHIP1 and SHIP2 are coexpressed in human T lymphocytes. Biol Chem (1999) 380:969-74. doi:10.1515/BC.1999.120.
97. Attree O, Olivos IM, Okabe I, Bailey LC, Nelson DL, Lewis RA, et al. The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature (1992) 358:239-42. doi:10.1038/358239a0.
98. Janne PA, Suchy SF, Bernard D, MacDonald M, Crawley J, Grinberg A, et al. Functional overlap between murine Inpp5b and Ocrl1 may explain why deficiency of the murine ortholog for OCRL1 does not cause Lowe syndrome in mice. J Clin Invest (1998) 101:2042-53. doi:10.1172/JCI2414.
99. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science (1997) 275:1943-7. doi:10.1126/science.275.5308.1943.
100. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet (1997) 15:356-62. doi:10.1038/ng0497-356.
101. Hobert JA, Eng C. PTEN hamartoma tumor syndrome: an overview. Genet Med (2009) 11:687-94. doi:10.1097/GIM.0b013e3181ac9aea.
102. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem (1998) 273:13375-8. doi:10.1074/jbc.273.22.13375.
103. Tamura M, Gu J, Danen EH, Takino T, Miyamoto S, Yamada KM. PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem (1999) 274:20693-703. doi:10.1074/jbc.274.29.20693.
104. Buckler JL, Walsh PT, Porrett PM, Choi Y, Turka LA. Cutting edge: T cell requirement for CD28 costimulation is due to negative regulation of TCR signals by PTEN. J Immunol (2006) 177:4262-6.
105. Buckler JL, Liu X, Turka LA. Regulation of T-cell responses by PTEN. Immunol Rev (2008) 224:239-48. doi:10.1111/j.1600-065X.2008.00650.x.
106. Bensinger SJ, Walsh PT, Zhang J, Carroll M, Parsons R, Rathmell JC, et al. Distinct IL-2 receptor signaling pattern in CD4+CD25+ regulatory T cells. J Immunol (2004) 172:5287-96.
107. Guo H, Qiao G, Ying H, Li Z, Zhao Y, Liang Y, et al. E3 ubiquitin ligase Cbl-b regulates Pten via Nedd4 in T cells independently of its ubiquitin ligase activity. Cell Rep (2012) 1:472-82. doi:10.1016/j.celrep.2012.04.008.
108. Liu X, Karnell JL, Yin B, Zhang R, Zhang J, Li P, et al. Distinct roles for PTEN in prevention of T cell lymphoma and autoimmunity in mice. J Clin Invest (2010) 120:2497-507. doi:10.1172/JCI42382.
109. Locke FL, Zha YY, Zheng Y, Driessens G, Gajewski TF. Conditional deletion of PTEN in peripheral T cells augments TCR-mediated activation but does not abrogate CD28 dependency or prevent anergy induction. J Immunol (2013) 191:1677-85. doi:10.4049/jimmunol.1202018.
110. Li Y, Prasad A, Jia Y, Roy SG, Loison F, Mondal S, et al. Pretreatment with phosphatase and tensin homolog deleted on chromosome 10 (PTEN) inhibitor SF1670 augments the efficacy of granulocyte transfusion in a clinically relevant mouse model. Blood (2011) 117:6702-13. doi:10.1182/blood-2010-09-309864.
111. Rosivatz E, Matthews JG, McDonald NQ, Mulet X, Ho KK, Lossi N, et al. A small molecule inhibitor for phosphatase and tensin homologue deleted on chromosome 10 (PTEN). ACS Chem Biol (2006) 1:780-90. doi:10.1021/cb600352f.
112. Hakim S, Bertucci MC, Conduit SE, Vuong DL, Mitchell CA. Inositol polyphosphate phosphatases in human disease. Curr Top Microbiol Immunol (2012) 362:247-314. doi:10.1007/978-94-007-5025-8_12.
113. Agoulnik IU, Hodgson MC, Bowden WA, Ittmann MM. INPP4B: the new kid on the PI3K block. Oncotarget (2011) 2:321-8.
114. Fedele CG, Ooms LM, Ho M, Vieusseux J, O'Toole SA, Millar EK, et al. Inositol polyphosphate 4-phosphatase II regulates PI3K/Akt signaling and is lost in human basal-like breast cancers. Proc Natl Acad Sci U S A (2010) 107:22231-6. doi:10.1073/pnas.1015245107.
115. Sasaki J, Kofuji S, Itoh R, Momiyama T, Takayama K, Murakami H, et al. The PtdIns(3,4)P(2) phosphatase INPP4A is a suppressor of excitotoxic neuronal death. Nature (2010) 465:497-501. doi:10.1038/nature09023.
116. Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, et al. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell (2010) 142:296-308. doi:10.1016/j.cell.2010.06.003.