T-cell function is partially maintained in the absence of class IA phosphoinositide 3-kinase signaling

Blood

Volumn 109, Issue 7, 2007, Pages 2894-2902

  Deane, Jonathan A ^a   Kharas, Michael G ^a   Oak, Jean S ^a   Stiles, Linda N ^a   Luo, Ji ^b,c   Moore, Travis I ^a   Ji, Hong ^d   Rommel, Christian ^d   Cantley, Lewis C ^b,c   Lane, Thomas E ^a   Fruman, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SERONO PHARMACEUTICAL RES INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE DELETION; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE;

EID: 33947595612     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-07-038620     Document Type: Article

References (63)

1. Deane JA, Fruman DA. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annu Rev Immunol. 2004;22:563-598.
2. Costello PS, Gallagher M, Cantrell DA. Sustained and dynamic inositol lipid metabolism inside and outside the immunological synapse. Nat Immunol. 2002;3:1082-1089.
3. Fabre S, Lang V, Harriague J, et al. Stable activation of phosphatidylinositol 3-kinase in the T cell immunological synapse stimulates Akt signaling to FoxO1 nuclear exclusion and cell growth control. J Immunol. 2005;174:4161-4171.
4. Harriague J, Bismuth G. Imaging antigen-induced PI3K activation in T cells. Nat Immunol. 2002;3:1090-1096.
5. Huppa JB, Gleimer M, Sumen C, Davis MM. Continuous T cell receptor signaling required for synapse maintenance and full effector potential. Nat Immunol. 2003;4:749-755.
6. Borlado LR, Redondo C, Alvarez B, et al. Increased phosphoinositide 3-kinase activity induces a lymphoproliferative disorder and contributes to tumor generation in vivo. FASEB J. 2000;14:895-903.
7. Di Cristofano A, Kotsi P, Peng YF, Cordon-Cardo C, Elkon KB, Pandolfi PP. Impaired Fas response and autoimmunity in Pten+/- mice. Science. 1999;285:2122-2125.
8. March ME, Ravichandran K. Regulation of the immune response by SHIP. Semin Immunol. 2002;14:37-47.
9. Suzuki A, Yamaguchi MT, Ohteki T, et al. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity. 2001;14:523-534.
10. Aagaard-Tillery KM, Jelinek DF. Phosphatidylinositol 3-kinase activation in normal human B lymphocytes. J Immunol. 1996;156:4543-4554.
11. Fruman DA, Snapper SB, Yballe CM, et al. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science. 1999;283:393-397.
12. Shi J, Cinek T, Truitt KE, Imboden JB. Wortmannin, a phosphatidylinositol 3-kinase inhibitor, blocks antigen- mediated, but not CD3 monoclonal antibody-induced, activation of murine CD4+ T cells. J Immunol. 1997;158:4688-4695.
13. Truitt KE, Shi J, Gibson S, Segal LG, Mills GB, Imboden JB. CD28 delivers costimulatory signals independently of its association with phosphatidylinositol 3-kinase. J Immunol. 1995;155:4702-4710.
14. Burr JS, Savage ND, Messah GE, et al. Cutting edge: distinct motifs within CD28 regulate T cell proliferation and induction of Bcl-XL. J Immunol. 2001;166:5331-5335.
15. Okkenhaug K, Wu L, Garza KM, et al. A point mutation in CD28 distinguishes proliferative signals from survival signals. Nat Immunol. 2001;2:325-332.
16. Sanchez-Lockhart M, Marin E, Graf B, et al. Cutting edge: CD28-mediated transcriptional and posttranscriptional regulation of IL-2 expression are controlled through different signaling pathways. J Immunol. 2004;173:7120-7124.
17. Fruman DA, Meyers RE, Cantley LC. Phosphoinositide kinases. Annu Rev Biochem. 1998;67:481-507.
18. Vanhaesebroeck B, Leevers SJ, Ahmadi K, et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001;70:535-602.
19. Brunn GJ, Williams J, Sabers C, Wiederrecht G, Lawrence JC Jr, Abraham RT. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 1996;15:5256-5267.
20. Withers DJ, Ouwens DM, Nave BT, et al. Expression, enzyme activity, and subcellular localization of mammalian target of rapamycin in insulin-responsive cells. Biochem Biophys Res Commun. 1997;241:704-709.
21. Vanhaesebroeck B, Ali K, Bilancio A, Geering B, Foukas LC. Signalling by PI3K isoforms: insights from gene-targeted mice. Trends Biochem Sci. 2005;30:194-204.
22. Fukao T, Yamada T, Tanabe M, et al. Selective loss of gastrointestinal mast cells and impaired immunity in PI3K-deficient mice. Nat Immunol. 2002;3:295-304.
23. Lu-Kuo JM, Fruman DA, Joyal DM, Cantley LC, Katz HR. Impaired kit- but not FcepsilonRI-initiated mast cell activation in the absence of phosphoinositide 3-kinase p85alpha gene products. J Biol Chem. 2000;275:6022-6029.
24. Suzuki H, Terauchi Y, Fujiwara M, et al. Xid-like immunodeficiency in mice with disruption of the p85alpha subunit of phosphoinositide 3-kinase. Science. 1999;283:390-392.
25. Deane JA, Trifilo MJ, Yballe CM, Choi S, Lane TE, Fruman DA. Enhanced T cell proliferation in mice lacking the p85beta subunit of phosphoinositide 3-kinase. J Immunol. 2004;172:6615-6625.
26. Fukao T, Tanabe M, Terauchi Y, et al. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat Immunol. 2002;3:875-881.
27. Bi L, Okabe I, Bernard DJ, Wynshaw-Boris A, Nussbaum RL. Proliferative defect and embryonic lethality in mice homozygous for a deletion in the p110alpha subunit of phosphoinositide 3-kinase. J Biol Chem. 1999;274:10963-10968.
28. Bi L, Okabe I, Bernard DJ, Nussbaum RL. Early embryonic lethality in mice deficient in the p110beta catalytic subunit of PI 3-kinase. Mamm Genome. 2002;13:169-172.
29. Okkenhaug K, Bilancio A, Farjot G, et al. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science. 2002;297:1031-1034.
30. Clayton E, Bardi G, Bell SE, et al. A crucial role for the p110delta subunit of phosphatidylinositol 3-kinase in B cell development and activation. J Exp Med. 2002;196:753-763.
31. Jou ST, Carpino N, Takahashi Y, et al. Essential, nonredundant role for the phosphoinositide 3-kinase p110delta in signaling by the B-cell receptor complex. Mol Cell Biol. 2002;22:8580-8591.
32. Luo J, McMullen JR, Sobkiw CL, et al. Class IA phosphoinositide 3-kinase regulates heart size and physiological cardiac hypertrophy. Mol Cell Biol. 2005;25:9491-9502.
33. Brachmann SM, Yballe CM, Innocenti M, et al. Role of phosphoinositide 3-kinase regulatory isoforms in development and actin rearrangement. Mol Cell Biol. 2005;25:2593-2606.
34. Orban PC, Chui D, Marth JD. Tissue- and site-specific DNA recombination in transgenic mice. Proc Natl Acad Sci U S A. 1992;89:6861-6865.
35. Lee PP, Fitzpatrick DR, Beard C, et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity. 2001;15:763-774.
36. Bergmann CC, Altman JD, Hinton D, Stohlman SA. Inverted immunodominance and impaired cytolytic function of CD8+ T cells during viral persistence in the central nervous system. J Immunol. 1999;163:3379-3387.
37. Glass WG, Lane TE. Functional analysis of the CC chemokine receptor 5 (CCR5) on virus-specific CD8+ T cells following coronavirus infection of the central nervous system. Virology. 2003;312:407-414.
38. Tkaczyk C, Beaven MA, Brachman SM, Metcalfe DD, Gilfillan AM. The phospholipase C gamma 1-dependent pathway of Fc epsilon RI-mediated mast cell activation is regulated independently of phosphatidylinositol 3-kinase. J Biol Chem. 2003;278:48474-48484.
39. Yu J, Zhang Y, McIlroy J, Rordorf-Nikolic T, Orr GA, Backer JM. Regulation of the p85/p110 phosphatidylinositol 3′-kinase: stabilization and inhibition of the p110alpha catalytic subunit by the p85 regulatory subunit. Mol Cell Biol. 1998;18:1379-1387.
40. Haring J, Perlman S. Mouse hepatitis virus. Curr Opin Microbiol. 2001;4:462-466.
41. Trifilo MJ, Lane TE. The CC chemokine ligand 3 regulates CD11c+CD11b+CD8alpha- dendritic cell maturation and activation following viral infection of the central nervous system: implications for a role in T cell activation. Virology. 2004;327:8-15.
42. Knight ZA, Gonzalez B, Feldman ME, et al. A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling. Cell. 2006;125:733-747.
43. Camps M, Ruckle T, Ji H, et al. Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med. 2005;11:936-943.
44. Condliffe AM, Davidson K, Anderson KE, et al. Sequential activation of class IB and class IA PI3Ks is important for the primed respiratory burst of human but not murine neutrophils. Blood. 2005;106:1432-1440.
45. Chamberlain MD, Berry TR, Pastor MC, Anderson DH. The p85alpha subunit of phosphatidylinositol 3′-kinase binds to and stimulates the GTPase activity of Rab proteins. J Biol Chem. 2004;279:48607-48614.
46. Kang H, Schneider H, Rudd CE. Phosphatidylinositol 3-kinase p85 adaptor function in T-cells. Co-stimulation and regulation of cytokine transcription independent of associated p110. J Biol Chem. 2002;277:912-921.
47. Xia X, Cheng A, Akinmade D, Hamburger AW. The N-terminal 24 amino acids of the p55 gamma regulatory subunit of phosphoinositide 3-kinase binds Rb and induces cell cycle arrest. Mol Cell Biol. 2003;23:1717-1725.
48. Rodriguez-Borlado L, Barber DF, Hernandez C, et al. Phosphatidylinositol 3-kinase regulates the CD4/CD8 T cell differentiation ratio. J Immunol. 2003;170:4475-4482.
49. 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;175:2783-2787.
50. Swat W, Montgrain V, Doggett TA, et al. Essential role of PI3Kdelta and PI3Kgamma in thymocyte survival. Blood. 2006;107:2415-2422.
51. Li CR, Berg LJ. Itk is not essential for CD28 signaling in naive T cells. J Immunol. 2005;174:4475-4479.
52. Kane LP, Andres PG, Howland KC, Abbas AK, Weiss A. Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-gamma but not TH2 cytokines. Nat Immunol. 2001;2:37-44.
53. Kane LP, Weiss A. The PI-3 kinase/Akt pathway and T cell activation: pleiotropic pathways downstream of PIP3. Immunol Rev. 2003;192:7-20.
54. Byfield MP, Murray JT, Backer JM. hVps34 is a nutrient-regulated lipid kinase required for activation of p70 S6 kinase. J Biol Chem. 2005;280:33076-33082.
55. Nobukuni T, Joaquin M, Roccio M, et al. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc Natl Acad Sci U S A. 2005;102:14238-14243.
56. Molon B, Gri G, Bettella M, et al. T cell costimulation by chemokine receptors. Nat Immunol. 2005;6:465-471.
57. Aagaard-Tillery KM, Jelinek DF. A role for phosphatidylinositol 3-kinase in generating T cell help for B cell growth and differentiation. J Immunol. 1996;157:2769-2778.
58. Wymann MP, Zvelebil M, Laffargue M. Phosphoinositide 3-kinase signalling - which way to target? Trends Pharmacol Sci. 2003;24:366-376.
59. Ali K, Bilancio A, Thomas M, et al. Essential role for the p110delta phosphoinositide 3-kinase in the allergic response. Nature. 2004;431:1007-1011.
60. Sujobert P, Bardet V, Cornillet-Lefebvre P, et al. Essential role for the p110delta isoform in phosphoinositide 3-kinase activation and cell proliferation in acute myeloid leukemia. Blood. 2005;106:1063-1066.
61. Oak JS, Deane JA, Kharas MG, 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;103:16882-16887.
62. Okkenhaug K, Patton DT, Bilancio A, et al. The p11Odelta isoform of phosphoinositide 3-kinase controls clonal expansion and differentiation of Th cells. J. Immunol. 2006;177:5122-5128.
63. + regulatory T cells. J. Immunol. 2006;177:6598-6602.