Role of phosphoinositide 3-kinase signaling in autoimmunity

References

• Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001; 70: 535–602
   PubMed Web of Science ®Google Scholar
• Stephens LR, Eguinoa A, Erdjument-Bromage H, Lui M, Cooke F, Coadwell J, Smrcka AS, Thelen M, Cadwallader K, Tempst P, Hawkins PT. The G beta gamma sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 1997; 89: 105–114
   PubMed Web of Science ®Google Scholar
• Suire S, Coadwell J, Ferguson GJ, Davidson K, Hawkins P, Stephens L. p84, a new Gbetagamma-activated regulatory subunit of the type IB phosphoinositide 3-kinase p110gamma. Curr Biol 2005; 15: 566–570
   PubMed Web of Science ®Google Scholar
• Deane JA, Fruman DA. Phosphoinositide 3-kinase: Diverse roles in immune cell activation. Annu Rev Immunol 2004; 22: 563–598
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Fruman DA, Snapper SB, Yballe CM, Davidson L, Yu JY, Alt FW, Cantley LC. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85alpha. Science 1999; 283: 393–397
   PubMed Web of Science ®Google Scholar
• Okkenhaug K, Bilancio A, Farjot G, Priddle H, Sancho S, Peskett E, Pearce W, Meek SE, Salpekar A, Waterfield MD, Smith AJ, Vanhaesebroeck B. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 2002; 297: 1031–1034
   PubMed Web of Science ®Google Scholar
• Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, Wakeham A, Itie A, Bouchard D, Kozieradzki I, Joza N, Mak TW, Ohashi PS, Suzuki A, Penninger JM. Function of PI3Kgamma in thymocyte development. T cell activation, and neutrophil migration. Science 2000; 287: 1040–1046
   PubMed Web of Science ®Google Scholar
• Suzuki H, Terauchi Y, Fujiwara M, Aizawa S, Yazaki Y, Kadowaki T, Koyasu S. Xid-like immunodeficiency in mice with disruption of the p85alpha subunit of phosphoinositide 3-kinase. Science 1999; 283: 390–392
   PubMed Web of Science ®Google Scholar
• Deane JA, Kharas MG, Oak JS, Stiles LN, Luo J, Moore TI, Ji H, Rommel C, Cantley LC, Lane TE, Fruman DA. T cell function is partially maintained in the absence of class IA phosphoinositide 3-kinase signaling. Blood 2007; 109: 2894–2902
   PubMed Web of Science ®Google Scholar
• Nombela-Arrieta C, Lacalle RA, Montoya MC, Kunisaki Y, Megias D, Marques M, Carrera AC, Manes S, Fukui Y, Martinez AC, Stein JV. Differential requirements for DOCK2 and phosphoinositide-3-kinase gamma during T and B lymphocyte homing. Immunity 2004; 21: 429–441
   Google Scholar
• Reif K, Okkenhaug K, Sasaki T, Penninger JM, Vanhaesebroeck B, Cyster JG. Cutting edge: Differential roles for phosphoinositide 3-kinases, p110gamma and p110delta, in lymphocyte chemotaxis and homing. J Immunol 2004; 173: 2236–2240
   PubMed Web of Science ®Google Scholar
• Borlado LR, Redondo C, Alvarez B, Jimenez C, Criado LM, Flores J, Marcos MA, Martinez AC, Balomenos D, Carrera AC. Increased phosphoinositide 3-kinase activity induces a lymphoproliferative disorder and contributes to tumor generation in vivo. FASEB J 2000; 14: 895–903
   PubMed Web of Science ®Google Scholar
• Rodriguez-Borlado L, Barber DF, Hernandez C, Rodriguez-Marcos MA, Sanchez A, Hirsch E, Wymann M, Martinez AC, Carrera AC. Phosphatidylinositol 3-kinase regulates the CD4/CD8 T cell differentiation ratio. J Immunol 2003; 170: 4475–4482
   PubMedGoogle Scholar
• Parsons MJ, Jones RG, Tsao MS, Odermatt B, Ohashi PS, Woodgett JR. Expression of active protein kinase B in T cells perturbs both T and B cell homeostasis and promotes inflammation. J Immunol 2001; 167: 42–48
   PubMedGoogle Scholar
• Rathmell JC, Elstrom RL, Cinalli RM, Thompson CB. Activated Akt promotes increased resting T cell size, CD28-independent T cell growth, and development of autoimmunity and lymphoma. Eur J Immunol 2003; 33: 2223–2232
   PubMed Web of Science ®Google Scholar
• Jones RG, Elford AR, Parsons MJ, Wu L, Krawczyk CM, Yeh WC, Hakem R, Rottapel R, Woodgett JR, Ohashi PS. CD28-dependent activation of protein kinase B/Akt blocks Fas-mediated apoptosis by preventing death-inducing signaling complex assembly. J Exp Med 2002; 196: 335–348
   PubMed Web of Science ®Google Scholar
• Na SY, Patra A, Scheuring Y, Marx A, Tolaini M, Kioussis D, Hemmings BA, Hunig T, Bommhardt U. Constitutively active protein kinase B enhances Lck and Erk activities and influences thymocyte selection and activation. J Immunol 2003; 171: 1285–1296
   PubMedGoogle Scholar
• Jones RG, Parsons M, Bonnard M, Chan VS, Yeh WC, Woodgett JR, Ohashi PS. Protein kinase B regulates T lymphocyte survival, nuclear factor kappaB activation, and Bcl-X(L) levels in vivo. J Exp Med 2000; 191: 1721–1734
   PubMedGoogle Scholar
• Coffer PJ, Burgering BM. Forkhead-box transcription factors and their role in the immune system. Nat Rev Immunol 2004; 4: 889–899
   PubMed Web of Science ®Google Scholar
• Peng SL. Immune regulation by Foxo transcription factors. Autoimmunity 2007; 40(6)462–469
   PubMed Web of Science ®Google Scholar
• Yusuf I, Fruman DA. Regulation of quiescence in lymphocytes. Trends Immunol 2003; 24: 380–386
   PubMed Web of Science ®Google Scholar
• Lin L, Hron JD, Peng SL. Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 2004; 21: 203–213
   PubMed Web of Science ®Google Scholar
• Cantley LC, Neel BG. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci USA 1999; 96: 4240–4245
   PubMed Web of Science ®Google Scholar
• Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. Pten is essential for embryonic development and tumour suppression. Nat Genet 1998; 19: 348–355
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Suzuki A, Yamaguchi MT, Ohteki T, Sasaki T, Kaisho T, Kimura Y, Yoshida R, Wakeham A, Higuchi T, Fukumoto M, Tsubata T, Ohashi PS, Koyasu S, Penninger JM, Nakano T, Mak TW. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 2001; 14: 523–534
   PubMed Web of Science ®Google Scholar
• Rohrschneider LR, Fuller JF, Wolf I, Liu Y, Lucas DM. Structure, function, and biology of SHIP proteins. Genes Dev 2000; 14: 505–520
   PubMed Web of Science ®Google Scholar
• Brauweiler A, Tamir I, Dal Porto J, Benschop RJ, Helgason CD, Humphries RK, Freed JH, Cambier JC. 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: 1545–1554
   PubMed Web of Science ®Google Scholar
• Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM, Borowski A, Jirik F, Krystal G, Humphries RK. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 1998; 12: 1610–1620
   PubMed Web of Science ®Google Scholar
• Helgason CD, Kalberer CP, Damen JE, Chappel SM, Pineault N, Krystal G, Humphries RK. 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 2000; 191: 781–794
   PubMedGoogle Scholar
• Moody JL, Jirik FR. Compound heterozygosity for Pten and SHIP augments T-dependent humoral immune responses and cytokine production by CD(4+) T cells. Immunology 2004; 112: 404–412
   PubMedGoogle Scholar
• Moody JL, Pereira CG, Magil A, Fritzler MJ, Jirik FR. Loss of a single allele of SHIP exacerbates the immunopathology of Pten heterozygous mice. Genes Immun 2003; 4: 60–66
   PubMedGoogle Scholar
• Ye H, Arron JR, Lamothe B, Cirilli M, Kobayashi T, Shevde NK, Segal D, Dzivenu OK, Vologodskaia M, Yim M, Du K, Singh S, Pike JW, Darnay BG, Choi Y, Wu H. Distinct molecular mechanism for initiating TRAF6 signalling. Nature 2002; 418: 443–447
   PubMed Web of Science ®Google Scholar
• Chiffoleau E, Kobayashi T, Walsh MC, King CG, Walsh PT, Hancock WW, Choi Y, Turka LA. TNF receptor-associated factor 6 deficiency during hemopoiesis induces Th2-polarized inflammatory disease. J Immunol 2003; 171: 5751–5759
   PubMed Web of Science ®Google Scholar
• King CG, Kobayashi T, Cejas PJ, Kim T, Yoon K, Kim GK, Chiffoleau E, Hickman SP, Walsh PT, Turka LA, Choi Y. TRAF6 is a T cell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat Med 2006; 12: 1088–1092
   PubMed Web of Science ®Google Scholar
• Chiang YJ, Kole HK, Brown K, Naramura M, Fukuhara S, Hu RJ, Jang IK, Gutkind JS, Shevach E, Gu H. Cbl-b regulates the CD28 dependence of T-cell activation. Nature 2000; 403: 216–220
   PubMed Web of Science ®Google Scholar
• Bachmaier K, Krawczyk C, Kozieradzki I, Kong YY, Sasaki T, Oliveira-dos-Santos A, Mariathasan S, Bouchard D, Wakeham A, Itie A, Le J, Ohashi PS, Sarosi I, Nishina H, Lipkowitz S, Penninger JM. Negative regulation of lymphocyte activation and autoimmunity by the molecular adaptor Cbl-b. Nature 2000; 403: 211–216
   PubMed Web of Science ®Google Scholar
• Fang D, Liu YC. Proteolysis-independent regulation of PI3K by Cbl-b-mediated ubiquitination in T cells. Nat Immunol 2001; 2: 870–875
   PubMed Web of Science ®Google Scholar
• Wohlfert EA, Callahan MK, Clark RB. Resistance to CD4+CD25+ regulatory T cells and TGF-beta in Cbl-b − / − mice. J Immunol 2004; 173: 1059–1065
   PubMed Web of Science ®Google Scholar
• Wohlfert EA, Clark RB. “Vive la Resistance!”—the PI3K-Akt pathway can determine target sensitivity to regulatory T cell suppression. Trends Immunol 2007; 28: 154–160
   PubMed Web of Science ®Google Scholar
• Ruckle T, Schwarz MK, Rommel C. PI3Kgamma inhibition: Towards an “aspirin of the 21st century”?. Nat Rev Drug Discov 2006; 5: 903–918
   PubMed Web of Science ®Google Scholar
• Barber DF, Bartolome A, Hernandez C, Flores JM, Redondo C, Fernandez-Arias C, Camps M, Ruckle T, Schwarz MK, Rodriguez S, Martinez AC, Balomenos D, Rommel C, Carrera AC. PI3Kgamma inhibition blocks glomerulonephritis and extends lifespan in a mouse model of systemic lupus. Nat Med 2005; 11: 933–935
   PubMed Web of Science ®Google Scholar
• Hirsch E, Katanaev VL, Garlanda C, Azzolino O, Pirola L, Silengo L, Sozzani S, Mantovani A, Altruda F, Wymann MP. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 2000; 287: 1049–1053
   PubMed Web of Science ®Google Scholar
• Laffargue M, Calvez R, Finan P, Trifilieff A, Barbier M, Altruda F, Hirsch E, Wymann MP. Phosphoinositide 3-kinase gamma is an essential amplifier of mast cell function. Immunity 2002; 16: 441–451
   PubMed Web of Science ®Google Scholar
• Li Z, Jiang H, Xie W, Zhang Z, Smrcka AV, Wu D. Roles of PLC-beta2 and -beta3 and PI3Kgamma in chemoattractant-mediated signal transduction. Science 2000; 287: 1046–1049
   PubMed Web of Science ®Google Scholar
• Camps M, Ruckle T, Ji H, Ardissone V, Rintelen F, Shaw J, Ferrandi C, Chabert C, Gillieron C, Francon B, Martin T, Gretener D, Perrin D, Leroy D, Vitte PA, Hirsch E, Wymann MP, Cirillo R, Schwarz MK, Rommel C. Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med 2005; 11: 936–943
   PubMed Web of Science ®Google Scholar
• Barber DF, Bartolome A, Hernandez C, Flores JM, Fernandez-Arias C, Rodriguez-Borlado L, Hirsch E, Wymann M, Balomenos D, Carrera AC. Class IB-phosphatidylinositol 3-kinase (PI3K) deficiency ameliorates IA-PI3K-induced systemic lupus but not T cell invasion. J Immunol 2006; 176: 589–593
   PubMed Web of Science ®Google Scholar
• 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: 5122–5128
   PubMed Web of Science ®Google Scholar
• Patton DT, Garden OA, Pearce WP, Clough LE, Monk CR, Leung E, Rowan WC, Sancho S, Walker LS, Vanhaesebroeck B, Okkenhaug K. Cutting edge: The phosphoinositide 3-kinase p110 delta is critical for the function of CD4+CD25+Foxp3+ regulatory T cells. J Immunol 2006; 177: 6598–6602
   PubMed Web of Science ®Google Scholar
• Oak JS, Deane JA, Kharas MG, Luo J, Lane TE, Cantley LC, Fruman DA. Sjogren's syndrome-like disease in mice with T cells lacking class 1A phosphoinositide-3-kinase. Proc Natl Acad Sci USA 2006; 103: 16882–16887
   PubMed Web of Science ®Google Scholar
• Fox RI. Sjogren's syndrome. Lancet 2005; 366: 321–331
   PubMed Web of Science ®Google Scholar
• Parkin B, Chew JB, White VA, Garcia-Briones G, Chhanabhai M, Rootman J. Lymphocytic infiltration and enlargement of the lacrimal glands: A new subtype of primary Sjogren's syndrome?. Ophthalmology 2005; 112: 2040–2047
   PubMedGoogle Scholar
• Bertorello R, Cordone MP, Contini P, Rossi P, Indiveri F, Puppo F, Cordone G. Increased levels of interleukin-10 in saliva of Sjogren's syndrome patients. Correlation with disease activity. Clin Exp Med 2004; 4: 148–151
   PubMed Web of Science ®Google Scholar
• Brookes SM, Cohen SB, Price EJ, Webb LM, Feldmann M, Maini RN, Venables PJ. T cell clones from a Sjogren's syndrome salivary gland biopsy produce high levels of IL-10. Clin Exp Immunol 1996; 103: 268–272
   PubMed Web of Science ®Google Scholar
• Swat W, Montgrain V, Doggett TA, Douangpanya J, Puri K, Vermi W, Diacovo TG. Essential role of PI3Kdelta and PI3Kgamma in thymocyte survival. Blood 2006; 107: 2415–2422
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Foukas LC, Claret M, Pearce W, Okkenhaug K, Meek S, Peskett E, Sancho S, Smith AJ, Withers DJ, Vanhaesebroeck B. Critical role for the p110alpha phosphoinositide-3-OH kinase in growth and metabolic regulation. Nature 2006; 441: 366–370
   PubMed Web of Science ®Google Scholar
• Chen D, Mauvais-Jarvis F, Bluher M, Fisher SJ, Jozsi A, Goodyear LJ, Ueki K, Kahn CR. p50alpha/p55alpha phosphoinositide 3-kinase knockout mice exhibit enhanced insulin sensitivity. Mol Cell Biol 2004; 24: 320–329
   PubMedGoogle Scholar
• Fruman DA, Mauvais-Jarvis F, Pollard DA, Yballe CM, Brazil D, Bronson RT, Kahn CR, Cantley LC. Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85 alpha. Nat Genet 2000; 26: 379–382
   PubMed Web of Science ®Google Scholar
• Terauchi Y, Tsuji Y, Satoh S, Minoura H, Murakami K, Okuno A, Inukai K, Asano T, Kaburagi Y, Ueki K, Nakajima H, Hanafusa T, Matsuzawa Y, Sekihara H, Yin Y, Barrett JC, Oda H, Ishikawa T, Akanuma Y, Komuro I, Suzuki M, Yamamura K, Kodama T, Suzuki H, Yamamura K, Kodama T, Suzuki H, Koyasu S, Aizawa S, Tobe K, Fukui Y, Yazaki Y, Kadowaki T. Increased insulin sensitivity and hypoglycaemia in mice lacking the p85 alpha subunit of phosphoinositide 3-kinase. Nat Genet 1999; 21: 230–235
   PubMed Web of Science ®Google Scholar
• Ueki K, Yballe CM, Brachmann SM, Vicent D, Watt JM, Kahn CR, Cantley LC. Increased insulin sensitivity in mice lacking p85beta subunit of phosphoinositide 3-kinase. Proc Natl Acad Sci USA 2002; 99: 419–424
   PubMed Web of Science ®Google Scholar
• Taniguchi CM, Tran TT, Kondo T, Luo J, Ueki K, Cantley LC, Kahn CR. Phosphoinositide 3-kinase regulatory subunit p85alpha suppresses insulin action via positive regulation of PTEN. Proc Natl Acad Sci USA 2006; 103: 12093–12097
   PubMed Web of Science ®Google Scholar
• 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
   PubMedGoogle Scholar
• Raizis AM, Ferguson MM, Robinson BA, Atkinson CH, George PM. Identification of a novel PTEN mutation (L139X) in a patient with Cowden disease and Sjogren's syndrome. Mol Pathol 1998; 51: 339–341
   PubMedGoogle Scholar
• Zhang HG, Wang Y, Xie JF, Liang X, Liu D, Yang P, Hsu HC, Ray RB, Mountz JD. Regulation of tumor necrosis factor alpha-mediated apoptosis of rheumatoid arthritis synovial fibroblasts by the protein kinase Akt. Arthritis Rheum 2001; 44: 1555–1567
   PubMed Web of Science ®Google Scholar
• Bernards A, de la Monte SM. The ltk receptor tyrosine kinase is expressed in pre-B lymphocytes and cerebral neurons and uses a non-AUG translational initiator. EMBO J 1990; 9: 2279–2287
   PubMed Web of Science ®Google Scholar
• Ueno H, Honda H, Nakamoto T, Yamagata T, Sasaki K, Miyagawa K, Mitani K, Yazaki Y, Hirai H. The phosphatidylinositol 3′ kinase pathway is required for the survival signal of leukocyte tyrosine kinase. Oncogene 1997; 14: 3067–3072
   PubMed Web of Science ®Google Scholar
• Li N, Nakamura K, Jiang Y, Tsurui H, Matsuoka S, Abe M, Ohtsuji M, Nishimura H, Kato K, Kawai T, Atsumi T, Koike T, Shirai T, Ueno H, Hirose S. Gain-of-function polymorphism in mouse and human Ltk: Implications for the pathogenesis of systemic lupus erythematosus. Hum Mol Genet 2004; 13: 171–179
   PubMed Web of Science ®Google Scholar
• Bilancio A, Okkenhaug K, Camps M, Emery JL, Ruckle T, Rommel C, Vanhaesebroeck B. Key role of the p110delta isoform of PI3K in B-cell antigen and IL-4 receptor signaling: Comparative analysis of genetic and pharmacologic interference with p110delta function in B cells. Blood 2006; 107: 642–650
   PubMed Web of Science ®Google Scholar
• Wetzker R, Rommel C. Phosphoinositide 3-kinases as targets for therapeutic intervention. Curr Pharm Des 2004; 10: 1915–1922
   PubMedGoogle Scholar
• Wymann MP, Zvelebil M, Laffargue M. Phosphoinositide 3-kinase signalling–which way to target?. Trends Pharmacol Sci 2003; 24: 366–376
   PubMed Web of Science ®Google Scholar
• Doukas J, Wrasidlo W, Noronha G, Dneprovskaia E, Fine R, Weis S, Hood J, Demaria A, Soll R, Cheresh D. Phosphoinositide 3-kinase gamma/delta inhibition limits infarct size after myocardial ischemia/reperfusion injury. Proc Natl Acad Sci USA 2006; 103: 19866–19871
   PubMed Web of Science ®Google Scholar
• Ali K, Bilancio A, Thomas M, Pearce W, Gilfillan AM, Tkaczyk C, Kuehn N, Gray A, Giddings J, Peskett E, Fox R, Bruce I, Walker C, Sawyer C, Okkenhaug K, Finan P, Vanhaesebroeck B. Essential role for the p110delta phosphoinositide 3-kinase in the allergic response. Nature 2004; 431: 1007–1011
   PubMed Web of Science ®Google Scholar