CD28 ligation in the absence of TCR stimulation up-regulates IL-17A and pro-inflammatory cytokines in relapsing-remitting multiple sclerosis T lymphocytes

Immunology Letters

Volumn 158, Issue 1-2, 2014, Pages 134-142

  Camperio, Cristina ^a   Muscolini, Michela ^a   Volpe, Elisabetta ^b   Di Mitri, Diletta ^b   Mechelli, Rosella ^c   Buscarinu, Maria C ^c   Ruggieri, Serena ^d   Piccolella, Enza ^a   Salvetti, Marco ^c   Gasperini, Claudio ^d   Battistini, Luca ^b   Tuosto, Loretta ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d SAN CAMILLO FORLANINI HOSPITAL   (Italy)

Author keywords

Costimulation: Multiple sclerosis; Inflammation: Th17 cells; PI3K

Indexed keywords

CD28 ANTIGEN; INTERLEUKIN 17; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; RNA; T LYMPHOCYTE RECEPTOR; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; AUTACOID; CD86 ANTIGEN; CD86 PROTEIN, HUMAN; CHROMONE DERIVATIVE; LYMPHOCYTE ANTIGEN RECEPTOR; MORPHOLINE DERIVATIVE;

ADULT; ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LYMPHOCYTE ACTIVATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA EXTRACTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; FEMALE; GENETICS; IMMUNOLOGY; L CELL LINE; MALE; METABOLISM; MIDDLE AGED; TRANSGENE;

ADULT; ANIMALS; ANTIGENS, CD28; ANTIGENS, CD86; CD4-POSITIVE T-LYMPHOCYTES; CHROMONES; FEMALE; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-6; INTERLEUKIN-8; L CELLS (CELL LINE); MALE; MICE; MIDDLE AGED; MORPHOLINES; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, ANTIGEN, T-CELL; TRANSGENES; UP-REGULATION;

EID: 84892637762     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2013.12.020     Document Type: Article

References (68)

1. Bielekova B., Sung M.H., Kadom N., Simon R., McFarland H., Martin R. Expansion and functional relevance of high-avidity myelin-specific CD4+ T cells in multiple sclerosis. J Immunol 2004, 172:3893-3904.
2. Bielekova B., Lincoln A., McFarland H., Martin R. Therapeutic potential of phosphodiesterase-4 and -3 inhibitors in Th1-mediated autoimmune diseases. J Immunol 2000, 164:1117-1124.
3. Batoulis H., Addicks K., Kuerten S. Emerging concepts in autoimmune encephalomyelitis beyond the CD4/T(H)1 paradigm. Ann Anat 2010, 192:179-193.
4. Stromnes I.M., Cerretti L.M., Liggitt D., Harris R.A., Goverman J.M. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat Med 2008, 14:337-342.
5. Frohman E.M., Racke M.K., Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N Engl J Med 2006, 354:942-955.
6. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005, 23:683-747.
7. Rudd CE, Taylor A, Schneider H. CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev 2009;229:12-26.
8. Perrin P.J., Scott D., Quigley L., Albert P.S., Feder O., Gray G.S., et al. Role of B7:CD28/CTLA-4 in the induction of chronic relapsing experimental allergic encephalomyelitis. J Immunol 1995, 154:1481-1490.
9. Racke M.K., Scott D.E., Quigley L., Gray G.S., Abe R., June C.H., et al. Distinct roles for B7-1 (CD-80) and B7-2 (CD-86) in the initiation of experimental allergic encephalomyelitis. J Clin Invest 1995, 96:2195-2203.
10. Windhagen A., Newcombe J., Dangond F., Strand C., Woodroofe M.N., Cuzner M.L., et al. Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J Exp Med 1995, 182:1985-1996.
11. Marinari B., Costanzo A., Marzano V., Piccolella E., Tuosto L. CD28 delivers a unique signal leading to the selective recruitment of RelA and p52 NF-kappaB subunits on IL-8 and Bcl-xL gene promoters. Proc Natl Acad Sci USA 2004, 101:6098-6103.
12. Tuosto L. NF-kappaB family of transcription factors: biochemical players of CD28 co-stimulation. Immunol Lett 2011, 135:1-9.
13. Saccani S., Pantano S., Natoli G. Two waves of nuclear factor κb recruitment to target promoters. J Exp Med 2001, 193:1351-1360.
14. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007, 8:942-949.
15. Manel N., Unutmaz D., Littman D.R. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008, 9:641-649.
16. Volpe E., Servant N., Zollinger R., Bogiatzi S.I., Hupe P., Barillot E., et al. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat Immunol 2008, 9:650-657.
17. Yang L., Anderson D.E., Baecher-Allan C., Hastings W.D., Bettelli E., Oukka M., et al. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008, 454:350-352.
18. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007, 8:967-974.
19. McDonald W.I., Compston A., Edan G., Goodkin D., Hartung H.P., Lublin F.D., et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 2001, 50:121-127.
20. Lublin F.D., Reingold S.C. Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology 1996, 46:907-911.
21. Civil A., Rensink I., Aarden L.A., Verwei C.L. Functional disparity of distinct CD28 response elements toward mitogenic responses. J Biol Chem 1999, 274:34369-34374.
22. Ouaaz F., Li M., Beg A.A. A critical role for the RelA subunit of nuclear factor kappaB in regulation of multiple immune-response genes and in Fas-induced cell death. J Exp Med 1999, 189:999-1004.
23. Acosta-Rodriguez E.V., Rivino L., Geginat J., Jarrossay D., Gattorno M., Lanzavecchia A., et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 2007, 8:639-646.
24. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007, 204:1849-1861.
25. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., et al. 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 2009, 10:514-523.
26. Pinto-Medel M.J., Garcia-Leon J.A., Oliver-Martos B., Lopez-Gomez C., Luque G., Arnaiz-Urrutia C., et al. The CD4+ T-cell subset lacking expression of the CD28 costimulatory molecule is expanded and shows a higher activation state in multiple sclerosis. J Neuroimmunol 2012, 243:1-11.
27. Jadidi-Niaragh F., Mirshafiey A. Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand J Immunol 2011, 74:1-13.
28. Jin W., Zhou X.F., Yu J., Cheng X., Sun S.C. Regulation of Th17 cell differentiation and EAE induction by MAP3K NIK. Blood 2009, 113:6603-6610.
29. Li L., Ruan Q., Hilliard B., Devirgiliis J., Karin M., Chen Y.H. Transcriptional regulation of the Th17 immune response by IKK(alpha). J Exp Med 2011, 208:787-796.
30. Muscolini M., Sajeva A., Caristi S., Tuosto L. A novel association between filamin A and NF-kappaB inducing kinase couples CD28 to inhibitor of NF-kappaB kinase alpha and NF-kappaB activation. Immunol Lett 2011, 36:203-212.
31. August A., Dupont B. CD28 of T lymphocytes associates with phosphatidylinositol 3-kinase. Int Immunol 1994, 6:769-774.
32. Pages F., Ragueneau M., Rottapel R., Truneh A., Nunes J., Imbert J., et al. Binding of phosphatidylinositol-3-OH kinase to CD28 is required for T-cell signalling. Nature 1994, 369:327-329.
33. Prasad K.V., Cai Y.C., Raab M., Duckworth B., Cantley L., Shoelson S.E., et al. T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc Natl Acad Sci U S A 1994, 91:2834-2838.
34. Ghigo A., Hirsch E. Isoform selective phosphoinositide 3-kinase gamma and delta inhibitors and their therapeutic potential. Recent Pat Inflamm Allergy Drug Discov 2008, 2:1-10.
35. O'Brien K., Gran B., Rostami A. T-cell based immunotherapy in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunology 2010, 2:99-115.
36. Hayden M.S., West A.P., Ghosh S. NF-kappaB and the immune response. Oncogene 2006, 25:6758-6780.
37. Lund B.T., Ashikian N., Ta H.Q., Chakryan Y., Manoukian K., Groshen S., et al. Increased CXCL8 (IL-8) expression in Multiple Sclerosis. J Neuroimmunol 2004, 155:161-171.
38. Malmestrom C., Andersson B.A., Haghighi S., Lycke J. I.L-6 and CCL2 levels in CSF are associated with the clinical course of MS: implications for their possible immunopathogenic roles. J Neuroimmunol 2006, 175:176-182.
39. Serada S., Fujimoto M., Mihara M., Koike N., Ohsugi Y., Nomura S., et al. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2008, 105:9041-9046.
40. Brucklacher-Waldert V., Stuerner K., Kolster M., Wolthausen J., Tolosa E. Phenotypical and functional characterization of T helper 17 cells in multiple sclerosis. Brain 2009, 132:3329-3341.
41. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., et al. A distinct lineage of CD4T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005, 6:1133-1141.
42. Annunziato F., Cosmi L., Liotta F., Maggi E., Romagnani S. Defining the human T helper 17 cell phenotype. Trends Immunol 2012, 33:505-512.
43. Pelletier M., Maggi L., Micheletti A., Lazzeri E., Tamassia N., Costantini C., et al. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 2010, 115:335-343.
44. Huppert J., Closhen D., Croxford A., White R., Kulig P., Pietrowski E., et al. Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J 2010, 24:1023-1034.
45. Tzartos J.S., Friese M.A., Craner M.J., Palace J., Newcombe J., Esiri M.M., et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 2008, 172:146-155.
46. Hedegaard C.J., Krakauer M., Bendtzen K., Lund H., Sellebjerg F., Nielsen C.H. T helper cell type 1 (Th1), Th2 and Th17 responses to myelin basic protein and disease activity in multiple sclerosis. Immunology 2008, 125:161-169.
47. Santarlasci V., Maggi L., Capone M., Querci V., Beltrame L., Cavalieri D., et al. Rarity of human T helper 17 cells is due to retinoic acid orphan receptor-dependent mechanisms that limit their expansion. Immunity 2012, 36:201-214.
48. Hong J., Li H., Chen M., Zang Y.C., Skinner S.M., Killian J.M., et al. Regulatory and pro-inflammatory phenotypes of myelin basic protein-autoreactive T cells in multiple sclerosis. Int Immunol 2009, 21:1329-1340.
49. Tzartos J.S., Craner M.J., Friese M.A., Jakobsen K.B., Newcombe J., Esiri M.M., et al. IL-21 and IL-21 receptor expression in lymphocytes and neurons in multiple sclerosis brain. Am J Pathol 2011, 178:794-802.
50. Fontenot J.D., Rudensky A.Y. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 2005, 6:331-337.
51. Ziegler S.F. FOXP3: of mice and men. Annu Rev Immunol 2006, 24:209-226.
52. Zozulya A.L., Wiendl H. The role of regulatory T cells in multiple sclerosis. Nat Clin Pract Neurol 2008, 4:384-398.
53. Dalla Libera D, Di Mitri D, Bergami A, Centonze D, Gasperini C, Grasso MG, et al. T regulatory cells are markers of disease activity in multiple sclerosis patients. PLoS One 2011; 6:e21386.
54. Camperio C., Caristi S., Fanelli G., Soligo M., Del Porto P., Piccolella E. Forkhead transcription factor FOXP3 upregulates CD25 expression through cooperation with RelA/NF-kappaB. PLoS One 2012, 7:e48303.
55. Scotta C., Soligo M., Camperio C., Piccolella E. FOXP3 induced by CD28/B7 interaction regulates CD25 and anergic phenotype in human CD4+CD25-T lymphocytes. J Immunol 2008, 181:1025-1033.
56. Soligo M., Camperio C., Caristi S., Scotta C., Porto P.D., Costanzo A., et al. CD28 costimulation regulates FOXP3 in a RelA/NF-kappaB-dependent mechanism. Eur J Immunol 2011, 41:503-513.
57. Lin C.H., Hunig T. Efficient expansion of regulatory T cells in vitro and in vivo with a CD28 superagonist. Eur J Immunol 2003, 33:626-638.
58. Waibler Z., Sender L.Y., Merten C., Hartig R., Kliche S., Gunzer M., et al. Signaling signatures and functional properties of anti-human CD28 superagonistic antibodies. PLoS One 2008, 3:e1708.
59. Suntharalingam G., Perry M.R., Ward S., Brett S.J., Castello-Cortes A., Brunner M.D., et al. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med 2006, 355:1018-1028.
60. Muscolini M., Camperio C., Capuano C., Caristi S., Piccolella E., Galandrini R., et al. Phosphatidylinositol 4-phosphate 5-kinases α activation critically contributes to CD28-dependent signaling responses. J Immunol 2013, 190:5279-5286.
61. Garcon F., Patton D.T., Emery J.L., Hirsch E., Rottapel R., Sasaki T., et al. 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 2008, 111:1464-1471.
62. Okkenhaug K., Patton D.T., Bilancio A., Garcon F., Rowan W.C., Vanhaesebroeck B. The p110delta isoform of phosphoinositide 3-kinase controls clonal expansion and differentiation of Th cells. J Immunol 2006, 177:5122-5128.
63. Sauer S., Bruno L., Hertweck A., Finlay D., Leleu M., Spivakov M., et al. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc Natl Acad Sci U S A 2008, 105:7797-7802.
64. Sinclair L.V., Finlay D., Feijoo C., Cornish G.H., Gray A., Ager A., et al. Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat Immunol 2008, 9:513-521.
65. Ghigo A., Damilano F., Braccini L., Hirsch E. PI3K inhibition in inflammation: toward tailored therapies for specific diseases. Bioessays 2010, 32:185-196.
66. Maira S.M., Pecchi S., Huang A., Burger M., Knapp M., Sterker D., et al. Identification and characterization of NVP-BKM120, an orally available pan-class I PI3-kinase inhibitor. Mol Cancer Ther 2012, 11:317-328.
67. Gasperini C., Ruggieri S. Development of oral agent in the treatment of multiple sclerosis: how the first available oral therapy, fingolimod will change therapeutic paradigm approach. Drug Des Devel Ther 2012, 6:175-186.
68. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 2009, 9:393-407.