Mucosal Th17 cell function is altered during HIV infection and is an independent predictor of systemic immune activation

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2164-2173

  Kim, Connie J ^a   McKinnon, Lyle R ^a,b   Kovacs, Colin ^c   Kandel, Gabor ^a,d   Huibner, Sanja ^a   Chege, Duncan ^a   Shahabi, Kamnoosh ^a   Benko, Erika ^c   Loutfy, Mona ^a,c,e   Ostrowski, Mario ^a,d   Kaul, Rupert ^a,f  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF NAIROBI   (Kenya)

^c Maple Leaf Medical   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

^e WOMEN S COLLEGE HOSPITAL   (Canada)

^f UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CLINICAL FEATURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; FUNCTIONAL STATUS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE DEPLETION; MAJOR CLINICAL STUDY; MUCOSA CELL; PRIORITY JOURNAL; TH17 CELL;

ADULT; ANTI-RETROVIRAL AGENTS; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HUMANS; INTESTINAL MUCOSA; MALE; MIDDLE AGED; TH17 CELLS;

EID: 84883417251     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300829     Document Type: Article

References (45)

1. Hogg, R. S., B. Yip, K. J. Chan, E. Wood, K. J. Craib, M. V. O'Shaughnessy, and J. S. Montaner. 2001. Rates of disease progression by baseline CD4 cell count and viral load after initiating triple-drug therapy. JAMA 286: 2568-2577.
2. Kim, C. J., A. Nazli, O. L. Rojas, D. Chege, Z. Alidina, S. Huibner, S. Mujib, E. Benko, C. Kovacs, L. Y. Shin, et al. 2012. A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis. Mucosal Immunol. 5: 670-680.
3. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, D. Altmann, et al. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12: 1365-1371.
4. Estes, J. D., L. D. Harris, N. R. Klatt, B. Tabb, S. Pittaluga, M. Paiardini, G. R. Barclay, J. Smedley, R. Pung, K. M. Oliveira, et al. 2010. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 6: e1001052.
5. O'Connor, W., Jr., L. A. Zenewicz, and R. A. Flavell. 2010. The dual nature of T (H)17 cells: shifting the focus to function. Nat. Immunol. 11: 471-476.
6. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279.
7. Pelletier, M., L. Maggi, A. Micheletti, E. Lazzeri, N. Tamassia, C. Costantini, L. Cosmi, C. Lunardi, F. Annunziato, S. Romagnani, and M. A. Cassatella. 2010. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115: 335-343.
8. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517.
9. Chege, D., P. M. Sheth, T. Kain, C. J. Kim, C. Kovacs, M. Loutfy, R. Halpenny, G. Kandel, T. W. Chun, M. Ostrowski, and R. Kaul. 2011. Sigmoid Th17 populations, the HIV latent reservoir, and microbial translocation in men on longterm antiretroviral therapy. AIDS 25: 741-749.
10. Favre, D., J. Mold, P. W. Hunt, B. Kanwar, P. Loke, L. Seu, J. D. Barbour, M. M. Lowe, A. Jayawardene, F. Aweeka, et al. 2010. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci. Transl. Med. 2: 32ra36.
11. Brenchley, J. M., M. Paiardini, K. S. Knox, A. I. Asher, B. Cervasi, T. E. Asher, P. Scheinberg, D. A. Price, C. A. Hage, L. M. Kholi, et al. 2008. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112: 2826-2835.
12. da Silva, B., W. Singer, I. W. Fong, and C. A. Ottaway. 1999. In vivo cytokine and neuroendocrine responses to endotoxin in human immunodeficiency virusinfected subjects. J. Infect. Dis. 180: 106-115.
13. Sandler, N. G., and D. C. Douek. 2012. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat. Rev. Microbiol. 10: 655-666.
14. Giorgi, J. V., L. E. Hultin, J. A. McKeating, T. D. Johnson, B. Owens, L. P. Jacobson, R. Shih, J. Lewis, D. J. Wiley, J. P. Phair, et al. 1999. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179: 859-870.
15. Ancuta, P., A. Kamat, K. J. Kunstman, E. Y. Kim, P. Autissier, A. Wurcel, T. Zaman, D. Stone, M. Mefford, S. Morgello, et al. 2008. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS ONE 3: e2516.
16. Ross, A. C., N. Rizk, M. A. O'Riordan, V. Dogra, D. El-Bejjani, N. Storer, D. Harrill, M. Tungsiripat, J. Adell, and G. A. McComsey. 2009. Relationship between inflammatory markers, endothelial activation markers, and carotid intima-media thickness in HIV-infected patients receiving antiretroviral therapy. Clin. Infect. Dis. 49: 1119-1127.
17. Mehandru, S., M. A. Poles, K. Tenner-Racz, P. Jean-Pierre, V. Manuelli, P. Lopez, A. Shet, A. Low, H. Mohri, D. Boden, et al. 2006. Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoS Med. 3: e484.
18. McGeachy, M. J., and D. J. Cua. 2008. Th17 cell differentiation: the long and winding road. Immunity 28: 445-453.
19. Yang, L., D. E. Anderson, C. Baecher-Allan, W. D. Hastings, E. Bettelli, M. Oukka, V. K. Kuchroo, and D. A. Hafler. 2008. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 454: 350-352.
20. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8: 950-957.
21. McGeachy, M. J., K. S. Bak-Jensen, Y. Chen, C. M. Tato, W. Blumenschein, T. McClanahan, and D. J. Cua. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397.
22. Esplugues, E., S. Huber, N. Gagliani, A. E. Hauser, T. Town, Y. Y. Wan, W. O'Connor, Jr., A. Rongvaux, N. Van Rooijen, A. M. Haberman, et al. 2011. Control of TH17 cells occurs in the small intestine. Nature 475: 514-518.
23. Huber, S., N. Gagliani, E. Esplugues, W. O'Connor, Jr., F. J. Huber, A. Chaudhry, M. Kamanaka, Y. Kobayashi, C. J. Booth, A. Y. Rudensky, et al. 2011. Th17 cells express interleukin-10 receptor and are controlled by Foxp3(2) and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34: 554-565.
24. Steinman, L. 2010. Mixed results with modulation of TH-17 cells in human autoimmune diseases. Nat. Immunol. 11: 41-44.
25. Yen, D., J. Cheung, H. Scheerens, F. Poulet, T. McClanahan, B. McKenzie, M. A. Kleinschek, A. Owyang, J. Mattson, W. Blumenschein, et al. 2006. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116: 1310-1316.
26. Iwakura, Y., and H. Ishigame. 2006. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116: 1218-1222.
27. Curtis, M. M., and S. S. Way. 2009. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126: 177-185.
28. Zielinski, C. E., F. Mele, D. Aschenbrenner, D. Jarrossay, F. Ronchi, M. Gattorno, S. Monticelli, A. Lanzavecchia, and F. Sallusto. 2012. Pathogeninduced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484: 514-518.
29. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
30. Hersperger, A. R., F. Pereyra, M. Nason, K. Demers, P. Sheth, L. Y. Shin, C. M. Kovacs, B. Rodriguez, S. F. Sieg, L. Teixeira-Johnson, et al. 2010. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog. 6: e1000917.
31. Almeida, J. R., D. A. Price, L. Papagno, Z. A. Arkoub, D. Sauce, E. Bornstein, T. E. Asher, A. Samri, A. Schnuriger, I. Theodorou, et al. 2007. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204: 2473-2485.
32. Almeida, J. R., D. Sauce, D. A. Price, L. Papagno, S. Y. Shin, A. Moris, M. Larsen, G. Pancino, D. C. Douek, B. Autran, et al. 2009. Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113: 6351-6360.
33. Ferre, A. L., P. W. Hunt, J. W. Critchfield, D. H. Young, M. M. Morris, J. C. Garcia, R. B. Pollard, H. F. Yee, Jr., J. N. Martin, S. G. Deeks, and B. L. Shacklett. 2009. Mucosal immune responses to HIV-1 in elite controllers: a potential correlate of immune control. Blood 113: 3978-3989.
34. Ciccone, E. J., J. H. Greenwald, P. I. Lee, A. Biancotto, S. W. Read, M. A. Yao, J. N. Hodge, W. L. Thompson, S. B. Kovacs, C. L. Chairez, et al. 2011. CD4+ T cells, including Th17 and cycling subsets, are intact in the gut mucosa of HIV-1-infected long-term nonprogressors. J. Virol. 85: 5880-5888.
35. Guillot-Delost, M., S. Le Gouvello, M. Mesel-Lemoine, M. Cherai, C. Baillou, A. Simon, Y. Levy, L. Weiss, S. Louafi, N. Chaput, et al. 2012. Human CD90 identifies Th17/Tc17 T cell subsets that are depleted in HIV-infected patients. J. Immunol. 188: 981-991.
36. Nigam, P., S. Kwa, V. Velu, and R. R. Amara. 2011. Loss of IL-17-producing CD8 T cells during late chronic stage of pathogenic simian immunodeficiency virus infection. J. Immunol. 186: 745-753.
37. Raffatellu, M., R. L. Santos, D. E. Verhoeven, M. D. George, R. P. Wilson, S. E. Winter, I. Godinez, S. Sankaran, T. A. Paixao, M. A. Gordon, et al. 2008. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14: 421-428.
38. Sallusto, F., C. E. Zielinski, and A. Lanzavecchia. 2012. Human Th17 subsets. Eur. J. Immunol. 42: 2215-2220.
39. Edwards, B. H., A. Bansal, S. Sabbaj, J. Bakari, M. J. Mulligan, and P. A. Goepfert. 2002. Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J. Virol. 76: 2298-2305.
40. Betts, M. R., D. R. Ambrozak, D. C. Douek, S. Bonhoeffer, J. M. Brenchley, J. P. Casazza, R. A. Koup, and L. J. Picker. 2001. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75: 11983-11991.
41. Ostrowski, M. A., J. X. Gu, C. Kovacs, J. Freedman, M. A. Luscher, and K. S. MacDonald. 2001. Quantitative and qualitative assessment of human immunodeficiency virus type 1 (HIV-1)-specific CD4+ T cell immunity to gag in HIV-1-infected individuals with differential disease progression: reciprocal interferon-gamma and interleukin-10 responses. J. Infect. Dis. 184: 1268-1278.
42. Brockman, M. A., D. S. Kwon, D. P. Tighe, D. F. Pavlik, P. C. Rosato, J. Sela, F. Porichis, S. Le Gall, M. T. Waring, K. Moss, et al. 2009. IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virusspecific T cells. Blood 114: 346-356.
43. Biancotto, A., J. C. Grivel, S. J. Iglehart, C. Vanpouille, A. Lisco, S. F. Sieg, R. Debernardo, K. Garate, B. Rodriguez, L. B. Margolis, and M. M. Lederman. 2007. Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood 109: 4272-4279.
44. Nilsson, J., S. Kinloch-de-Loes, A. Granath, A. Sonnerborg, L. E. Goh, and J. Andersson. 2007. Early immune activation in gut-associated and peripheral lymphoid tissue during acute HIV infection. AIDS 21: 565-574.
45. Chun, T. W., D. C. Nickle, J. S. Justement, J. H. Meyers, G. Roby, C. W. Hallahan, S. Kottilil, S. Moir, J. M. Mican, J. I. Mullins, et al. 2008. Persistence of HIV in gut-associated lymphoid tissue despite long-term antiretroviral therapy. J. Infect. Dis. 197: 714-720.