IL-17A expression in HIV-specific CD8 T cells is regulated by IL-4/IL-13 following HIV-1 prime-boost immunization

Journal of Interferon and Cytokine Research

Volumn 35, Issue 3, 2015, Pages 176-185

  Ravichandran, Jayashree ^a   Jackson, Ronald J ^a   Trivedi, Shubhanshi ^a   Ranasinghe, Charani ^a  

^a Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 17; INTERLEUKIN 23P19; INTERLEUKIN 4; INTERLEUKIN 6; MESSENGER RNA; STAT6 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; GAG PROTEIN; GAG PROTEIN P1, HUMAN IMMUNODEFICIENCY VIRUS; PEPTIDE FRAGMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNIZATION; LUNG; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; TRANSCRIPTION REGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; GENETICS; HIV INFECTIONS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; SECONDARY IMMUNIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MUS;

AIDS VACCINES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; FEMALE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; IMMUNIZATION, SECONDARY; INTERLEUKIN-13; INTERLEUKIN-17; INTERLEUKIN-4; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; STAT6 TRANSCRIPTION FACTOR;

EID: 84929172142     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2014.0078     Document Type: Article

References (54)

1. Campillo-Gimenez L, Cumont MC, Fay M, Kared H, Monceaux V, Diop O, Muller-Trutwin M, Hurtrel B, Levy Y, Zaunders J, Dy M, Leite-de-Moraes MC, Elbim C, Estaquier J. 2010. AIDS progression is associated with the emergence of IL-17-producing cells early after simian immunodeficiency virus infection. J Immunol 184(2):984-992.
2. Cecchinato V, Trindade CJ, Laurence A, Heraud JM, Brenchley JM, Ferrari MG, Zaffiri L, Tryniszewska E, Tsai WP, Vaccari M, Parks RW, Venzon D, Douek DC, O'Shea JJ, Franchini G. 2008. Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficiency virus-infected macaques. Mucosal Immunol 1(4):279-288.
3. Cooney LA, Towery K, Endres J, Fox DA. 2011. Sensitivity and resistance to regulation by IL-4 during Th17 maturation. J Immunol 187(9):4440-4450.
4. Cruz A, Khader SA, Torrado E, Fraga A, Pearl JE, Pedrosa J, Cooper AM, Castro AG. 2006. Cutting edge: IFN-gamma regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J Immunol 177(3):1416-1420.
5. de Mestre AM, Soe-Htwe T, Sutcliffe EL, Rao S, Pagler EB, Hornby JR, Hulett MD. 2007. Regulation of mouse Hepar-anase gene expression in T lymphocytes and tumor cells. Immunol Cell Biol 85(3):205-214.
6. DeLyria ES, Redline RW, Blanchard TG. 2009. Vaccination of mice against H pylori induces a strong Th-17 response and immunity that is neutrophil dependent. Gastroenterology 136(1):247-256.
7. Freches D, Korf H, Denis O, Havaux X, Huygen K, Romano M. 2013. Mice genetically inactivated in interleukin-17A receptor are defective in long-term control of Mycobacterium tuberculosis infection. Immunology 140(2):220-231.
8. Gao Z, Gao Y, Li Z, Chen Z, Lu D, Tsun A, Li B. 2012. Synergy between IL-6 and TGF-beta signaling promotes FOXP3 degradation. Int J Clin Exp Pathol 5(7):626-633.
9. Hamada H, Garcia-Hernandez MdeL, Reome JB, Misra SK, Strutt TM, McKinstry KK, Cooper AM, Swain SL, Dutton RW. 2009. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol 182(6):3469-3481.
10. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6(11):1123-1132.
11. He R, Kim HY, Yoon J, Oyoshi MK, MacGinnitie A, Goya S, Freyschmidt EJ, Bryce P, McKenzie AN, Umetsu DT, Oett-gen HC, Geha RS. 2009. Exaggerated IL-17 response to epicutaneous sensitization mediates airway inflammation in the absence of IL-4 and IL-13. J Allergy Clin Immunol 124(4):761-770 e1.
12. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH. 2006. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 177(11):7980-7989.
13. Hou W, Kang HS, Kim BS. 2009. Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J Exp Med 206(2):313-328.
14. Huber M, Heink S, Grothe H, Guralnik A, Reinhard K, Elflein K, Hunig T, Mittrucker HW, Brustle A, Kamradt T, Lohoff M. 2009. A Th17-like developmental process leads to CD8(+ ) Tc17 cells with reduced cytotoxic activity. Eur J Immunol 39(7):1716-1725.
15. Hwang ES. 2010. Transcriptional regulation of T helper 17 cell differentiation. Yonsei Med J 51(4):484-491.
16. Ivanov, II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17 + T helper cells. Cell 126(6):1121-1133.
17. Jackson RJ, Boyle DB, Ranasinghe C. 2014. Heterologous prime-boost regimens in DNA vaccination. In: Rinaldi M, Fioretti D, Iurescia S, eds. Methods in Molecular Biology. Springer.
18. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, Cilley GE, Shen F, Eaton SM, Gaffen SL, Swain SL, Locksley RM, Haynes L, Randall TD, Cooper AM. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4 + T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 8(4):369-377.
19. Korn T, Bettelli E, Oukka M, Kuchroo VK. 2009. IL-17 and Th17 Cells. Annu Rev Immunol 27:485-517.
20. Korn T, Mitsdoerffer M, Croxford AL, Awasthi A, Dardalhon VA, Galileos G, Vollmar P, Stritesky GL, Kaplan MH, Waisman A, Kuchroo VK, Oukka M. 2008. IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3 + regulatory T cells. Proc Natl Acad Sci U S A 105(47):18460-18465.
21. Korn T, Oukka M, Kuchroo V, Bettelli E. 2007. Th17 cells: effector T cells with inflammatory properties. Semin Immunol 19(6):362-371.
22. Lexberg MH, Taubner A, Förster A, Albrecht I, Richter A, Kamradt T, Radbruch A, Chang HD. 2008. Th memory for interleukin-17 expression is stable in vivo. Eur J Immunol 38(10):2654-2664.
23. Maloy KJ, Uhlig HH. 2013. ILC1 populations join the border patrol. Immunity 38(4):630-632.
24. McNeal MM, Basu M, Bean JA, Clements JD, Lycke NY, Ramne A, Lowenadler B, Choi AH, Ward RL. 2007. Intrarectal immunization of mice with VP6 and either LT(R192G) or CTA1-DD as adjuvant protects against fecal rotavirus shedding after EDIM challenge. Vaccine 25(33):6224-6231.
25. Newcomb DC, Boswell MG, Zhou W, Huckabee MM, Gole-niewska K, Sevin CM, Hershey GK, Kolls JK, Peebles RS, Jr. 2011. Human TH17 cells express a functional IL-13 receptor and IL-13 attenuates IL-17A production. J Allergy Clin Immunol 127(4):1006-1013.e1-e4.
26. Newcomb DC, Zhou W, Moore ML, Goleniewska K, Hershey GK, Kolls JK, Peebles RS, Jr. 2009. A functional IL-13 receptor is expressed on polarized murine CD4+ Th17 cells and IL-13 signaling attenuates Th17 cytokine production. J Immunol 182(9):5317-5321.
27. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6(11):1133-1141.
28. Pietrella D, Rachini A, Pines M, Pandey N, Mosci P, Bistoni F, d'Enfert C, Vecchiarelli A. 2011. Th17 cells and IL-17 in protective immunity to vaginal candidiasis. PLoS One 6(7):e22770.
29. Priebe GP, Walsh RL, Cederroth TA, Kamei A, Coutinho-Sledge YS, Goldberg JB, Pier GB. 2008. IL-17 is a critical component of vaccine-induced protection against lung infection by lipopolysaccharide-heterologous strains of Pseudomonas aeruginosa. J Immunol 181(7):4965-4975.
30. Ranasinghe C, Medveczky JC, Woltring D, Gao K, Thomson S, Coupar BE, Boyle DB, Ramsay AJ, Ramshaw IA. 2006. Evaluation of fowlpox-vaccinia virus prime-boost vaccine strategies for high-level mucosal and systemic immunity against HIV-1. Vaccine 24(31-32):5881-5895.
31. Ranasinghe C, Ramshaw IA. 2009. Immunisation route-dependent expression of IL-4/IL-13 can modulate HIV-specific CD8(+) CTL avidity. Eur J Immunol 39(7):1819-1830.
32. Ranasinghe C, Trivedi S, Stambas J, Jackson RJ. 2013. Unique IL-13Ralpha2-based HIV-1 vaccine strategy to enhance mucosal immunity, CD8(+) T-cell avidity and protective immunity. Mucosal Immunol 6(6):1068-1080.
33. Ranasinghe C, Turner SJ, McArthur C, Sutherland DB, Kim JH, Doherty PC, Ramshaw IA. 2007. Mucosal HIV-1 pox virus prime-boost immunization induces high-avidity CD8+ T cells with regime-dependent cytokine/granzyme B profiles. J Immunol 178(4):2370-2379.
34. Riol-Blanco L, Lazarevic V, Awasthi A, Mitsdoerffer M, Wilson BS, Croxford A, Waisman A, Kuchroo VK, Glimcher LH, Oukka M. 2010. IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J Immunol 184(4):1710-1720.
35. Salgado M, Rallon NI, Rodes B, Lopez M, Soriano V, Benito JM. 2011. Long-term non-progressors display a greater number of Th17 cells than HIV-infected typical progressors. Clin Immunol 139(2):110-114.
36. Smiley KL, McNeal MM, Basu M, Choi AH, Clements JD, Ward RL. 2007. Association of gamma interferon and interleukin-17 production in intestinal CD4 + T cells with protection against rotavirus shedding in mice intranasally immunized with VP6 and the adjuvant LT(R192G). J Virol 81(8):3740-3748.
37. Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 13(2):145-149.
38. Sutton CE, Mielke LA, Mills KH. 2012. IL-17-producing gammadelta T cells and innate lymphoid cells. Eur J Immunol 42(9):2221-2231.
39. Tabata Y, Chen W, Warrier MR, Gibson AM, Daines MO, Hershey GK. 2006. Allergy-driven alternative splicing of IL-13 receptor alpha2 yields distinct membrane and soluble forms. J Immunol 177(11):7905-7912.
40. Tabata Y, Khurana Hershey GK. 2007. IL-13 receptor isoforms: breaking through the complexity. Curr Allergy Asthma Rep 7(5):338-345.
41. Trivedi S, Jackson RJ, Ranasinghe C. 2014. Different HIV pox viral vector-based vaccines and adjuvants can induce unique antigen presenting cells that modulate CD8 T cell avidity. Virology 468-470C:479-489.
42. Van Dyken SJ, Mohapatra A, Nussbaum JC, Molofsky AB, Thornton EE, Ziegler SF, McKenzie AN, Krummel MF, Liang HE, Locksley RM. 2014. Chitin activates parallel immune modules that direct distinct inflammatory responses via innate lym-phoid type 2 and gammadelta T cells. Immunity 40(3):414-424.
43. VanCott JL, Prada AE, McNeal MM, Stone SC, Basu M, Huffer B, Jr., Smiley KL, Shao M, Bean JA, Clements JD, Choi AH, Ward RL. 2006. Mice develop effective but delayed protective immune responses when immunized as neonates either intra-nasally with nonliving VP6/LT(R192G) or orally with live rhesus rotavirus vaccine candidates. J Virol 80(10):4949-4961.
44. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24(2):179-189.
45. Wang X, Chan CC, Yang M, Deng J, Poon VK, Leung VH, Ko KH, Zhou J, Yuen KY, Zheng BJ, Lu L. 2011. A critical role of IL-17 in modulating the B-cell response during H5N1 influenza virus infection. Cell Mol Immunol 8(6):462-468.
46. Wang X, Seed B. 2003. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 31(24):154.
47. Wu Q, Martin RJ, Rino JG, Breed R, Torres RM, Chu HW. 2007. IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect 9(1):78-86.
48. Xi Y, Day SL, Jackson RJ, Ranasinghe C. 2012. Role of novel type I interferon epsilon in viral infection and mucosal immunity. Mucosal Immunol 5(6):610-622.
49. Xu H, Wang X, Liu DX, Moroney-Rasmussen T, Lackner AA, Veazey RS. 2012. IL-17-producing innate lymphoid cells are restricted to mucosal tissues and are depleted in SIV-infected macaques. Mucosal Immunol 2012(6):39.
50. Ye P, Garvey PB, Zhang P, Nelson S, Bagby G, Summer WR, Schwarzenberger P, Shellito JE, Kolls JK. 2001. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am J Respir Cell Mol Biol 25(3):335-340.
51. Yeh N, Glosson NL, Wang N, Guindon L, McKinley C, Ha-mada H, Li Q, Dutton RW, Shrikant P, Zhou B, Brutkiewicz RR, Blum JS, Kaplan MH. 2010. Tc17 cells are capable of mediating immunity to vaccinia virus by acquisition of a cytotoxic phenotype. J Immunol 185(4):2089-2098.
52. Yen HR, Harris TJ, Wada S, Grosso JF, Getnet D, Goldberg MV, Liang KL, Bruno TC, Pyle KJ, Chan SL, Anders RA, Trimble CL, Adler AJ, Lin TY, Pardoll DM, Huang CT, Drake CG. 2009. Tc17 CD8 T cells: functional plasticity and subset diversity. J Immunol 183(11):7161-7168.
53. Zhang Z, Clarke TB, Weiser JN. 2009. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest 119(7):1899-1909.
54. Zhou M, Yang B, Ma R, Wu C. 2008. Memory Th-17 cells specific for C. albicans are persistent in human peripheral blood. Immunol Lett 118(1):72-81.