PI3Kδ regulates the magnitude of CD8+ T cell responses after challenge with Listeria monocytogenes

Journal of Immunology

Volumn 195, Issue 7, 2015, Pages 3206-3217

  Pearce, Verity Q ^a   Bouabe, Hicham ^a   MacQueen, Amy R ^a   Carbonaro, Valentina ^a   Okkenhaug, Klaus ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; GAMMA INTERFERON; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE DELTA; PROTEIN P110 DELTA; UNCLASSIFIED DRUG; CYTOKINE; GRANZYME; GZMB PROTEIN, MOUSE; PIK3CD PROTEIN, MOUSE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; HOST PATHOGEN INTERACTION; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE SUBPOPULATION; ADOPTIVE TRANSFER; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOSENESCENCE; METABOLISM; MICROBIOLOGY; PHOSPHORYLATION; TRANSGENIC MOUSE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; GRANZYMES; IMMUNOLOGIC MEMORY; IMMUNOSENESCENCE; INTERFERON-GAMMA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84942436988     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501227     Document Type: Article

References (64)

1. Williams, M. A., and M. J. Bevan. 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25: 171-192.
2. Harty, J. T., and V. P. Badovinac. 2008. Shaping and reshaping CD8+ T-cell memory. Nat. Rev. Immunol. 8: 107-119.
3. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
4. Okkenhaug, K. 2013. Rules of engagement: distinct functions for the four class I PI3K catalytic isoforms in immunity. Ann. N.Y. Acad. Sci. 1280: 24-26.
5. Okkenhaug, K. 2013. Signaling by the phosphoinositide 3-kinase family in immune cells. Annu. Rev. Immunol. 31: 675-704.
6. Soond, D. R., E. Bjørgo, K. Moltu, V. Q. Dale, D. T. Patton, K. M. Torgersen, F. Galleway, B. Twomey, J. Clark, J. S. Gaston, et al. 2010. PI3K p110d regulates T-cell cytokine production during primary and secondary immune responses in mice and humans. Blood 115: 2203-2213.
7. Finlay, D. K., E. Rosenzweig, L. V. Sinclair, C. Feijoo-Carnero, J. L. Hukelmann, J. Rolf, A. A. Panteleyev, K. Okkenhaug, and D. A. Cantrell. 2012. PDK1 regulation of mTOR and hypoxia-inducible factor 1 integrate metabolism and migration of CD8+ T cells. J. Exp. Med. 209: 2441-2453.
8. Macintyre, A. N., D. Finlay, G. Preston, L. V. Sinclair, C. M. Waugh, P. Tamas, C. Feijoo, K. Okkenhaug, and D. A. Cantrell. 2011. Protein kinase B controls transcriptional programs that direct cytotoxic T cell fate but is dispensable for T cell metabolism. Immunity 34: 224-236.
9. Sinclair, L. V., D. Finlay, C. Feijoo, G. H. Cornish, A. Gray, A. Ager, K. Okkenhaug, T. J. Hagenbeek, H. Spits, and D. A. Cantrell. 2008. Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat. Immunol. 9: 513-521.
10. Martin, A. L., M. D. Schwartz, S. C. Jameson, and Y. Shimizu. 2008. Selective regulation of CD8 effector T cell migration by the p110g isoform of phosphatidylinositol 3-kinase. J. Immunol. 180: 2081-2088.
11. Ladygina, N., S. Gottipati, K. Ngo, G. Castro, J. Y. Ma, H. Banie, T. S. Rao, and W. P. Fung-Leung. 2013. PI3Kg kinase activity is required for optimal T-cell activation and differentiation. Eur. J. Immunol. 43: 3183-3196.
12. Alcázar, I., M. Marqués, A. Kumar, E. Hirsch, M. Wymann, A. C. Carrera, and D. F. Barber. 2007. Phosphoinositide 3-kinase gamma participates in T cell receptor-induced T cell activation. J. Exp. Med. 204: 2977-2987.
13. Garcon, F., D. T. Patton, J. L. Emery, E. Hirsch, R. Rottapel, T. Sasaki, and K. Okkenhaug. 2008. CD28 provides T-cell costimulation and enhances PI3K activity at the immune synapse independently of its capacity to interact with the p85/p110 heterodimer. Blood 111: 1464-1471.
14. So, L., S. S. Yea, J. S. Oak, M. Lu, A. Manmadhan, Q. H. Ke, M. R. Janes, L. V. Kessler, J. M. Kucharski, L. S. Li, et al. 2013. Selective inhibition of phosphoinositide 3-kinase p110a preserves lymphocyte function. J. Biol. Chem. 288: 5718-5731.
15. Stephens, L., K. Anderson, D. Stokoe, H. Erdjument-Bromage, G. F. Painter, A. B. Holmes, P. R. Gaffney, C. B. Reese, F. McCormick, P. Tempst, et al. 1998. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphatedependent activation of protein kinase B. Science 279: 710-714.
16. Waugh, C., L. Sinclair, D. Finlay, J. R. Bayascas, and D. Cantrell. 2009. Phosphoinositide (3,4,5)-triphosphate binding to phosphoinositide-dependent kinase 1 regulates a protein kinase B/Akt signaling threshold that dictates T-cell migration, not proliferation. Mol. Cell. Biol. 29: 5952-5962.
17. Bayascas, J. R., S. Wullschleger, K. Sakamoto, J. M. García-Martínez, C. Clacher, D. Komander, D. M. van Aalten, K. M. Boini, F. Lang, C. Lipina, et al. 2008. Mutation of the PDK1 PH domain inhibits protein kinase B/Akt, leading to small size and insulin resistance. Mol. Cell. Biol. 28: 3258-3272.
18. Hedrick, S. M., R. Hess Michelini, A. L. Doedens, A. W. Goldrath, and E. L. Stone. 2012. FOXO transcription factors throughout T cell biology. Nat. Rev. Immunol. 12: 649-661.
19. Kerdiles, Y. M., D. R. Beisner, R. Tinoco, A. S. Dejean, D. H. Castrillon, R. A. DePinho, and S. M. Hedrick. 2009. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10: 176-184.
20. Fabre, S., F. Carrette, J. Chen, V. Lang, M. Semichon, C. Denoyelle, V. Lazar, N. Cagnard, A. Dubart-Kupperschmitt, M. Mangeney, et al. 2008. FOXO1 regulates L-selectin and a network of human T cell homing molecules downstream of phosphatidylinositol 3-kinase. J. Immunol. 181: 2980-2989.
21. Ouyang, W., O. Beckett, R. A. Flavell, and M. O. Li. 2009. An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity 30: 358-371.
22. Rao, R. R., Q. Li, M. R. Gubbels Bupp, and P. A. Shrikant. 2012. Transcription factor Foxo1 represses T-bet-mediated effector functions and promotes memory CD8+ T cell differentiation. Immunity 36: 374-387.
23. Araki, K., A. P. Turner, V. O. Shaffer, S. Gangappa, S. A. Keller, M. F. Bachmann, C. P. Larsen, and R. Ahmed. 2009. mTOR regulates memory CD8 T-cell differentiation. Nature 460: 108-112.
24. Rao, R. R., Q. Li, K. Odunsi, and P. A. Shrikant. 2010. The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity 32: 67-78.
25. Hamilton, K. S., B. Phong, C. Corey, J. Cheng, B. Gorentla, X. Zhong, S. Shiva, and L. P. Kane. 2014. T cell receptor-dependent activation of mTOR signaling in T cells is mediated by Carma1 and MALT1, but not Bcl10. Sci. Signal. 7: ra55.
26. Salmond, R. J., J. Emery, K. Okkenhaug, and R. Zamoyska. 2009. MAPK, phosphatidylinositol 3-kinase, and mammalian target of rapamycin pathways converge at the level of ribosomal protein S6 phosphorylation to control metabolic signaling in CD8 T cells. J. Immunol. 183: 7388-7397.
27. Okkenhaug, K., K. Ali, and B. Vanhaesebroeck. 2007. Antigen receptor signalling: a distinctive role for the p110d isoform of PI3K. Trends Immunol. 28: 80-87.
28. Okkenhaug, K., and D. A. Fruman. 2010. PI3Ks in lymphocyte signaling and development. Curr. Top. Microbiol. Immunol. 346: 57-85.
29. Fruman, D. A., and G. Bismuth. 2009. Fine tuning the immune response with PI3K. Immunol. Rev. 228: 253-272.
30. Putz, E. M., M. Prchal-Murphy, O. A. Simma, F. Forster, X. Koenig, H. Stockinger, R. P. Piekorz, M. Freissmuth, M. Müller, V. Sexl, and E. Zebedin-Brandl. 2012. PI3Kd is essential for tumor clearance mediated by cytotoxic T lymphocytes. PLoS One 7: e40852.
31. Ali, K., A. Bilancio, M. Thomas, W. Pearce, A. M. Gilfillan, C. Tkaczyk, N. Kuehn, A. Gray, J. Giddings, E. Peskett, et al. 2004. Essential role for the p110d phosphoinositide 3-kinase in the allergic response. Nature 431: 1007-1011.
32. Deane, J. A., M. G. Kharas, J. S. Oak, L. N. Stiles, J. Luo, T. I. Moore, H. Ji, C. Rommel, L. C. Cantley, T. E. Lane, and D. A. Fruman. 2007. T-cell function is partially maintained in the absence of class IA phosphoinositide 3-kinase signaling. Blood 109: 2894-2902.
33. Ali, K., D. R. Soond, R. Piñeiro, T. Hagemann,W. Pearce, E. L. Lim, H. Bouabe, C. L. Scudamore, T. Hancox, H. Maecker, et al. 2014. Inactivation of PI(3)K p110d breaks regulatory T-cell-mediated immune tolerance to cancer. Nature 510: 407-411.
34. Pamer, E. G. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4: 812-823.
35. Foulds, K. E., L. A. Zenewicz, D. J. Shedlock, J. Jiang, A. E. Troy, and H. Shen. 2002. Cutting edge: CD4 and CD8 T cells are intrinsically different in their proliferative responses. J. Immunol. 168: 1528-1532.
36. Pope, C., S. K. Kim, A. Marzo, D. Masopust, K. Williams, J. Jiang, H. Shen, and L. Lefrancois. 2001. Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166: 3402-3409.
37. Pearce, E. L., and H. Shen. 2007. Generation of CD8 T cell memory is regulated by IL-12. J. Immunol. 179: 2074-2081.
38. Patton, D. T., M. D. Wilson, W. C. Rowan, D. R. Soond, and K. Okkenhaug. 2011. The PI3K p110d regulates expression of CD38 on regulatory T cells. PLoS One 6: e17359.
39. Stetson, D. B., M. Mohrs, R. L. Reinhardt, J. L. Baron, Z. E. Wang, L. Gapin, M. Kronenberg, and R. M. Locksley. 2003. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198: 1069-1076.
40. Okkenhaug, K., A. Bilancio, G. Farjot, H. Priddle, S. Sancho, E. Peskett, W. Pearce, S. E. Meek, A. Salpekar, M. D. Waterfield, et al. 2002. Impaired B and T cell antigen receptor signaling in p110d PI 3-kinase mutant mice. Science 297: 1031-1034.
41. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198.
42. Mazo, I. B., M. Honczarenko, H. Leung, L. L. Cavanagh, R. Bonasio, W. Weninger, K. Engelke, L. Xia, R. P. McEver, P. A. Koni, et al. 2005. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity 22: 259-270.
43. Flurkey K., J. M. Currer, D. E. Harrison. 2007. The Mouse in Aging Research. In The Mouse in Biomedical Research, 2nd Ed. J. G. Fox, M. T. Davisson, F. W. Quimby, S. W. Barthold, C. E. Newcomer, and A. L. Smith, eds. American College Laboratory Animal Medicine (Elsevier), Burlington, MA, p. 637-672.
44. Badovinac, V. P., J. S. Haring, and J. T. Harty. 2007. Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8+ T cell response to infection. Immunity 26: 827-841.
45. Wong, P., and E. G. Pamer. 2003. Feedback regulation of pathogen-specific T cell priming. Immunity 18: 499-511.
46. Porter, B. B., and J. T. Harty. 2006. The onset of CD8+-T-cell contraction is influenced by the peak of Listeria monocytogenes infection and antigen display. Infect. Immun. 74: 1528-1536.
47. Seki, E., H. Tsutsui, N. M. Tsuji, N. Hayashi, K. Adachi, H. Nakano, S. Futatsugi-Yumikura, O. Takeuchi, K. Hoshino, S. Akira, et al. 2002. Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J. Immunol. 169: 3863-3868.
48. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11: 443-451.
49. Kurachi, M., J. Kurachi, F. Suenaga, T. Tsukui, J. Abe, S. Ueha, M. Tomura, K. Sugihara, S. Takamura, K. Kakimi, and K. Matsushima. 2011. Chemokine receptor CXCR3 facilitates CD8+ T cell differentiation into short-lived effector cells leading to memory degeneration. J. Exp. Med. 208: 1605-1620.
50. Feau, S., R. Arens, S. Togher, and S. P. Schoenberger. 2011. Autocrine IL-2 is required for secondary population expansion of CD8+ memory T cells. Nat. Immunol. 12: 908-913.
51. Marchingo, J. M., A. Kan, R. M. Sutherland, K. R. Duffy, C. J. Wellard, G. T. Belz, A. M. Lew, M. R. Dowling, S. Heinzel, and P. D. Hodgkin. 2014. T cell signaling. Antigen affinity, costimulation, and cytokine inputs sum linearly to amplify T cell expansion. Science 346: 1123-1127.
52. Soond, D. R., F. Garcon, D. T. Patton, J. Rolf, M. Turner, C. Scudamore, O. A. Garden, and K. Okkenhaug. 2012. Pten loss in CD4 T cells enhances their helper function but does not lead to autoimmunity or lymphoma. J. Immunol. 188: 5935-5943.
53. Rolf, J., S. E. Bell, D. Kovesdi, M. L. Janas, D. R. Soond, L. M. Webb, S. Santinelli, T. Saunders, B. Hebeis, N. Killeen, et al. 2010. Phosphoinositide 3-kinase activity in T cells regulates the magnitude of the germinal center reaction. J. Immunol. 185: 4042-4052.
54. Okkenhaug, K., D. T. Patton, A. Bilancio, F. Garcon, W. C. Rowan, and B. Vanhaesebroeck. 2006. The p110d isoform of phosphoinositide 3-kinase controls clonal expansion and differentiation of Th cells. J. Immunol. 177: 5122-5128.
55. Liu, D., T. Zhang, A. J. Marshall, K. Okkenhaug, B. Vanhaesebroeck, and J. E. Uzonna. 2009. The p110delta isoform of phosphatidylinositol 3-kinase controls susceptibility to Leishmania major by regulating expansion and tissue homing of regulatory T cells. J. Immunol. 183: 1921-1933.
56. Harrison, D. E., R. Strong, Z. D. Sharp, J. F. Nelson, C. M. Astle, K. Flurkey, N. L. Nadon, J. E. Wilkinson, K. Frenkel, C. S. Carter, et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460: 392-395.
57. Selman, C., S. Lingard, A. I. Choudhury, R. L. Batterham, M. Claret, M. Clements, F. Ramadani, K. Okkenhaug, E. Schuster, E. Blanc, et al. 2008. Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J. 22: 807-818.
58. Selman, C., J. M. Tullet, D. Wieser, E. Irvine, S. J. Lingard, A. I. Choudhury, M. Claret, H. Al-Qassab, D. Carmignac, F. Ramadani, et al. 2009. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326: 140-144.
59. Furman, R. R., J. P. Sharman, S. E. Coutre, B. D. Cheson, J. M. Pagel, P. Hillmen, J. C. Barrientos, A. D. Zelenetz, T. J. Kipps, I. Flinn, et al. 2014. Idelalisib and rituximab in relapsed chronic lymphocytic leukemia. N. Engl. J. Med. 370: 997-1007.
60. Gopal, A. K., B. S. Kahl, S. de Vos, N. D. Wagner-Johnston, S. J. Schuster, W. J. Jurczak, I. W. Flinn, C. R. Flowers, P. Martin, A. Viardot, et al. 2014. PI3Kd inhibition by idelalisib in patients with relapsed indolent lymphoma. N. Engl. J. Med. 370: 1008-1018.
61. Doisne, J. M., C. M. Hüber, K. Okkenhaug, and F. Colucci. 2015. Immunomodulation of selective naive T cell functions by p110d inactivation improves the outcome of mismatched cell transplantation. Cell Rep. 10: 702-710.
62. Brockstedt, D. G., M. A. Giedlin, M. L. Leong, K. S. Bahjat, Y. Gao, W. Luckett, W. Liu, D. N. Cook, D. A. Portnoy, and T. W. Dubensky, Jr. 2004. Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc. Natl. Acad. Sci. USA 101: 13832-13837.
63. Angulo, I., O. Vadas, F. Garcon, E. Banham-Hall, V. Plagnol, T. R. Leahy, H. Baxendale, T. Coulter, J. Curtis, C. Wu, et al. 2013. Phosphoinositide 3-kinase d gene mutation predisposes to respiratory infection and airway damage. Science 342: 866-871.
64. Lucas, C. L., H. S. Kuehn, F. Zhao, J. E. Niemela, E. K. Deenick, U. Palendira, D. T. Avery, L. Moens, J. L. Cannons, M. Biancalana, et al. 2014. Dominantactivating germline mutations in the gene encoding the PI(3)K catalytic subunit p110d result in T cell senescence and human immunodeficiency. Nat. Immunol. 15: 88-97.