PI3Kγ Drives Priming and Survival of Autoreactive CD4+ T Cells during Experimental Autoimmune Encephalomyelitis

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Comerford, Iain ^a   Litchfield, Wendel ^a   Kara, Ervin ^a   McColl, Shaun R ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

5 (6 QUINOXALINYLMETHYLENE) 2,4 THIAZOLIDINEDIONE; CD4 ANTIGEN; CD8 ANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PROTEIN P110; PROTEIN P110 GAMMA; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MIGRATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEMYELINATION; DENDRITIC CELL; ENZYME INHIBITION; FEMALE; GRANULOCYTE; IMMUNE RESPONSE; LEUKOCYTE COUNT; LYMPHOID ORGAN; MONONUCLEAR PHAGOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOPHYSIOLOGY; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH17 CELL; TREATMENT OUTCOME;

ADMINISTRATION, ORAL; ANIMALS; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CLASS IB PHOSPHATIDYLINOSITOL 3-KINASE; CROSS-PRIMING; CYTOKINES; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE DELETION; HUMANS; MICE; MICE, INBRED C57BL; PROTEIN KINASE INHIBITORS; QUINOXALINES; SIGNAL TRANSDUCTION; TH1 CELLS; TH17 CELLS; THIAZOLIDINEDIONES;

MUS;

EID: 84866401348     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045095     Document Type: Article

References (61)

1. Sospedra M, Martin R, (2005) Immunology of multiple sclerosis. Annu Rev Immunol 23: 683-747.
2. Baxter AG, (2007) The origin and application of experimental autoimmune encephalomyelitis. Nat Rev Immunol 7: 904-912.
3. Steinman L, Zamvil SS, (2005) Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol 26: 565-571.
4. Webb M, Tham CS, Lin FF, Lariosa-Willingham K, Yu N, et al. (2004) Sphingosine 1-phosphate receptor agonists attenuate relapsing-remitting experimental autoimmune encephalitis in SJL mice. J Neuroimmunol 153: 108-121.
5. Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, et al. (1992) Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature 356: 63-66.
6. Williams R, Berndt A, Miller S, Hon WC, Zhang X, (2009) Form and flexibility in phosphoinositide 3-kinases. Biochem Soc Trans 37: 615-626.
7. Haylock-Jacobs S, Comerford I, Bunting M, Kara E, Townley S, et al. (2011) PI3Kdelta drives the pathogenesis of experimental autoimmune encephalomyelitis by inhibiting effector T cell apoptosis and promoting Th17 differentiation. J Autoimmun 36: 278-287.
8. Bi L, Okabe I, Bernard DJ, Nussbaum RL, (2002) Early embryonic lethality in mice deficient in the p110beta catalytic subunit of PI 3-kinase. Mamm Genome 13: 169-172.
9. Bi L, Okabe I, Bernard DJ, Wynshaw-Boris A, Nussbaum RL, (1999) Proliferative defect and embryonic lethality in mice homozygous for a deletion in the p110alpha subunit of phosphoinositide 3-kinase. J Biol Chem 274: 10963-10968.
10. Hirsch E, Katanaev VL, Garlanda C, Azzolino O, Pirola L, et al. (2000) Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287: 1049-1053.
11. Okkenhaug K, Bilancio A, Farjot G, Priddle H, Sancho S, et al. (2002) Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 297: 1031-1034.
12. Vanhaesebroeck B, Welham MJ, Kotani K, Stein R, Warne PH, et al. (1997) P110delta, a novel phosphoinositide 3-kinase in leukocytes. Proc Natl Acad Sci U S A 94: 4330-4335.
13. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, et al. (2000) Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 287: 1040-1046.
14. Del Prete A, Vermi W, Dander E, Otero K, Barberis L, et al. (2004) Defective dendritic cell migration and activation of adaptive immunity in PI3Kgamma-deficient mice. EMBO J 23: 3505-3515.
15. Weiss-Haljiti C, Pasquali C, Ji H, Gillieron C, Chabert C, et al. (2004) Involvement of phosphoinositide 3-kinase gamma, Rac, and PAK signaling in chemokine-induced macrophage migration. J Biol Chem 279: 43273-43284.
16. Li Z, Jiang H, Xie W, Zhang Z, Smrcka AV, et al. (2000) Roles of PLC-beta2 and-beta3 and PI3Kgamma in chemoattractant-mediated signal transduction. Science 287: 1046-1049.
17. Hayer S, Pundt N, Peters MA, Wunrau C, Kuhnel I, et al. (2009) PI3Kgamma regulates cartilage damage in chronic inflammatory arthritis. FASEB J 23: 4288-4298.
18. Camps M, Ruckle T, Ji H, Ardissone V, Rintelen F, et al. (2005) Blockade of PI3Kgamma suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat Med 11: 936-943.
19. Barber DF, Bartolome A, Hernandez C, Flores JM, Redondo C, et al. (2005) PI3Kgamma inhibition blocks glomerulonephritis and extends lifespan in a mouse model of systemic lupus. Nat Med 11: 933-935.
20. Kobayashi N, Ueki K, Okazaki Y, Iwane A, Kubota N, et al. (2011) Blockade of class IB phosphoinositide-3 kinase ameliorates obesity-induced inflammation and insulin resistance. Proc Natl Acad Sci U S A 108: 5753-5758.
21. Takeda M, Ito W, Tanabe M, Ueki S, Kato H, et al. (2009) Allergic airway hyperresponsiveness, inflammation, and remodeling do not develop in phosphoinositide 3-kinase gamma-deficient mice. J Allergy Clin Immunol 123: 805-812.
22. Lim DH, Cho JY, Song DJ, Lee SY, Miller M, et al. (2009) PI3K gamma-deficient mice have reduced levels of allergen-induced eosinophilic inflammation and airway remodeling. Am J Physiol Lung Cell Mol Physiol 296: L210-219.
23. Rommel C, Camps M, Ji H, (2007) PI3K delta and PI3K gamma: partners in crime in inflammation in rheumatoid arthritis and beyond? Nat Rev Immunol 7: 191-201.
24. Ben-Nun A, Wekerle H, Cohen IR, (1981) The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis. Eur J Immunol 11: 195-199.
25. Alcazar I, Marques M, Kumar A, Hirsch E, Wymann M, et al. (2007) Phosphoinositide 3-kinase gamma participates in T cell receptor-induced T cell activation. J Exp Med 204: 2977-2987.
26. Goverman J, (2009) Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 9: 393-407.
27. de Vos AF, van Meurs M, Brok HP, Boven LA, Hintzen RQ, et al. (2002) Transfer of central nervous system autoantigens and presentation in secondary lymphoid organs. J Immunol 169: 5415-5423.
28. Barbi J, Cummings HE, Lu B, Oghumu S, Ruckle T, et al. (2008) PI3Kgamma (PI3Kgamma) is essential for efficient induction of CXCR3 on activated T cells. Blood 112: 3048-3051.
29. Liston A, Kohler RE, Townley S, Haylock-Jacobs S, Comerford I, et al. (2009) Inhibition of CCR6 function reduces the severity of experimental autoimmune encephalomyelitis via effects on the priming phase of the immune response. J Immunol 182: 3121-3130.
30. Kohler RE, Caon AC, Willenborg DO, Clark-Lewis I, McColl SR, (2003) A role for macrophage inflammatory protein-3 alpha/CC chemokine ligand 20 in immune priming during T cell-mediated inflammation of the central nervous system. J Immunol 170: 6298-6306.
31. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, et al. (2009) C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 10: 514-523.
32. Kohler RE, Comerford I, Townley S, Haylock-Jacobs S, Clark-Lewis I, et al. (2008) Antagonism of the chemokine receptors CXCR3 and CXCR4 reduces the pathology of experimental autoimmune encephalomyelitis. Brain Pathol 18: 504-516.
33. Sporici R, Issekutz TB, (2010) CXCR3 blockade inhibits T-cell migration into the CNS during EAE and prevents development of adoptively transferred, but not actively induced, disease. Eur J Immunol 40: 2751-2761.
34. Smith DF, Deem TL, Bruce AC, Reutershan J, Wu D, et al. (2006) Leukocyte phosphoinositide-3 kinase {gamma} is required for chemokine-induced, sustained adhesion under flow in vivo. J Leukoc Biol 80: 1491-1499.
35. Jones GE, Prigmore E, Calvez R, Hogan C, Dunn GA, et al. (2003) Requirement for PI 3-kinase gamma in macrophage migration to MCP-1 and CSF-1. Exp Cell Res 290: 120-131.
36. Thomas M, Edwards MJ, Sawicka E, Duggan N, Hirsch E, et al. (2009) Essential role of phosphoinositide 3-kinase gamma in eosinophil chemotaxis within acute pulmonary inflammation. Immunology 126: 413-422.
37. Reif K, Okkenhaug K, Sasaki T, Penninger JM, Vanhaesebroeck B, et al. (2004) Cutting edge: differential roles for phosphoinositide 3-kinases, p110gamma and p110delta, in lymphocyte chemotaxis and homing. J Immunol 173: 2236-2240.
38. Thomas MS, Mitchell JS, DeNucci CC, Martin AL, Shimizu Y, (2008) The p110gamma isoform of phosphatidylinositol 3-kinase regulates migration of effector CD4 T lymphocytes into peripheral inflammatory sites. J Leukoc Biol 84: 814-823.
39. Nombela-Arrieta C, Mempel TR, Soriano SF, Mazo I, Wymann MP, et al. (2007) A central role for DOCK2 during interstitial lymphocyte motility and sphingosine-1-phosphate-mediated egress. J Exp Med 204: 497-510.
40. Nombela-Arrieta C, Lacalle RA, Montoya MC, Kunisaki Y, Megias D, et al. (2004) Differential requirements for DOCK2 and phosphoinositide-3-kinase gamma during T and B lymphocyte homing. Immunity 21: 429-441.
41. Smit MJ, Verdijk P, van der Raaij-Helmer EM, Navis M, Hensbergen PJ, et al. (2003) CXCR3-mediated chemotaxis of human T cells is regulated by a Gi- and phospholipase C-dependent pathway and not via activation of MEK/p44/p42 MAPK nor Akt/PI-3 kinase. Blood 102: 1959-1965.
42. Gruen M, Rose C, Konig C, Gajda M, Wetzker R, et al. (2010) Loss of phosphoinositide 3-kinase gamma decreases migration and activation of phagocytes but not T cell activation in antigen-induced arthritis. BMC Musculoskelet Disord 11: 63.
43. Berod L, Heinemann C, Heink S, Escher A, Stadelmann C, et al. (2011) PI3Kgamma deficiency delays the onset of experimental autoimmune encephalomyelitis and ameliorates its clinical outcome. Eur J Immunol 41: 833-844.
44. Strainic MG, Liu J, Huang D, An F, Lalli PN, et al. (2008) Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 28: 425-435.
45. Gollmer K, Asperti-Boursin F, Tanaka Y, Okkenhaug K, Vanhaesebroeck B, et al. (2009) CCL21 mediates CD4+ T-cell costimulation via a DOCK2/Rac-dependent pathway. Blood 114: 580-588.
46. Molon B, Gri G, Bettella M, Gomez-Mouton C, Lanzavecchia A, et al. (2005) T cell costimulation by chemokine receptors. Nat Immunol 6: 465-471.
47. Nanki T, Lipsky PE, (2000) Cutting edge: stromal cell-derived factor-1 is a costimulator for CD4+ T cell activation. J Immunol 164: 5010-5014.
48. Akekawatchai C, Holland JD, Kochetkova M, Wallace JC, McColl SR, (2005) Transactivation of CXCR4 by the insulin-like growth factor-1 receptor (IGF-1R) in human MDA-MB-231 breast cancer epithelial cells. J Biol Chem 280: 39701-39708.
49. Kumar A, Humphreys TD, Kremer KN, Bramati PS, Bradfield L, et al. (2006) CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity 25: 213-224.
50. Rodrigues DH, Vilela MC, Barcelos LS, Pinho V, Teixeira MM, et al. (2010) Absence of PI3Kgamma leads to increased leukocyte apoptosis and diminished severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 222: 90-94.
51. Barber DF, Bartolome A, Hernandez C, Flores JM, Fernandez-Arias C, et al. (2006) Class IB-phosphatidylinositol 3-kinase (PI3K) deficiency ameliorates IA-PI3K-induced systemic lupus but not T cell invasion. J Immunol 176: 589-593.
52. Lim SY, Constantinescu CS, (2010) Current and future disease-modifying therapies in multiple sclerosis. Int J Clin Pract 64: 637-650.
53. Scott LJ, (2011) Fingolimod: a review of its use in the management of relapsing-remitting multiple sclerosis. CNS Drugs 25: 673-698.
54. Hawkins PT, Stephens LR, (2007) PI3Kgamma is a key regulator of inflammatory responses and cardiovascular homeostasis. Science 318: 64-66.
55. Ji H, Rintelen F, Waltzinger C, Bertschy Meier D, Bilancio A, et al. (2007) Inactivation of PI3Kgamma and PI3Kdelta distorts T-cell development and causes multiple organ inflammation. Blood 110: 2940-2947.
56. Swat W, Montgrain V, Doggett TA, Douangpanya J, Puri K, et al. (2006) Essential role of PI3Kdelta and PI3Kgamma in thymocyte survival. Blood 107: 2415-2422.
57. Webb LM, Vigorito E, Wymann MP, Hirsch E, Turner M, (2005) Cutting edge: T cell development requires the combined activities of the p110gamma and p110delta catalytic isoforms of phosphatidylinositol 3-kinase. Journal of Immunology 175: 2783-2787.
58. Rommel C, (2010) Taking PI3Kdelta and PI3Kgamma one step ahead: dual active PI3Kdelta/gamma inhibitors for the treatment of immune-mediated inflammatory diseases. Curr Top Microbiol Immunol 346: 279-299.
59. Williams O, Houseman BT, Kunkel EJ, Aizenstein B, Hoffman R, et al. (2010) Discovery of dual inhibitors of the immune cell PI3Ks p110delta and p110gamma: a prototype for new anti-inflammatory drugs. Chem Biol 17: 123-134.
60. Comerford I, Nibbs RJ, Litchfield W, Bunting M, Harata-Lee Y, et al. (2010) The atypical chemokine receptor CCX-CKR scavenges homeostatic chemokines in circulation and tissues and suppresses Th17 responses. Blood 116: 4130-4140.
61. Burman AC, Banovic T, Kuns RD, Clouston AD, Stanley AC, et al. (2007) IFNgamma differentially controls the development of idiopathic pneumonia syndrome and GVHD of the gastrointestinal tract. Blood 110: 1064-1072.