CCR6- regulatory T cells blunt the restoration of gut Th17 cells along the CCR6-CCL20 axis in treated HIV-1-infected individuals

Mucosal Immunology

Volumn 9, Issue 5, 2016, Pages 1137-1150

  Loiseau, C ^a   Requena, M ^b   Mavigner, M ^c   Cazabat, M ^a,b   Carrere, N ^b,d   Suc, B ^b,d   Barange, K ^b   Alric, L ^b,d,e   Marchou, B ^b,d   Massip, P ^b,d   Izopet, J ^a,b,d   Delobel, P ^a,b,d  

^a INSERM   (France)

^b TOULOUSE UNIVERSITY HOSPITAL   (France)

^c EMORY UNIVERSITY   (United States)

^d UNIVERSITÉ PAUL SABATIER   (France)

^e Hôpital Purpan   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CHEMOKINE RECEPTOR CCR6; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CCL20 PROTEIN, HUMAN; CCR6 PROTEIN, HUMAN; CD4 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; IL10 PROTEIN, HUMAN;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL HOMING; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; MALE; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; SMALL INTESTINE; TH17 CELL; CASE CONTROL STUDY; CHEMOTAXIS; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; LYMPHOCYTE COUNT; MIDDLE AGED; PATHOLOGY; PHYSIOLOGICAL FEEDBACK; SIGNAL TRANSDUCTION; VIROLOGY;

ADULT; ANTI-HIV AGENTS; ANTIGENS, CD4; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CASE-CONTROL STUDIES; CHEMOKINE CCL20; CHEMOTAXIS; ENTEROCYTES; FEEDBACK, PHYSIOLOGICAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HIV INFECTIONS; HIV-1; HUMANS; INTERLEUKIN-10; INTERLEUKIN-17; INTESTINAL MUCOSA; INTESTINE, SMALL; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; RECEPTORS, CCR6; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84982282636     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.7     Document Type: Article

References (60)

1. Hooper, L.V., & Macpherson, A.J. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10, 159-169 (2010
2. Lim, S.G., et al. Loss of mucosal CD4 lymphocytes is an early feature of HIV infection. Clin. Exp. Immunol. 92, 448-454 (1993
3. Schneider, T., et al. Loss of CD4 T lymphocytes in patients infected with human immunodeficiency virus type 1 is more pronounced in the duodenal mucosa than in the peripheral blood. Berlin Diarrhea/Wasting Syndrome Study Group. Gut 37, 524-529 (1995
4. Guadalupe, M., et al. Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J. Virol. 77, 11708-11717 (2003
5. Brenchley, J.M., et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200, 749-759 (2004
6. Mehandru, S., et al. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200, 761-770 (2004
7. Raffatellu, M., et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14, 421-428 (2008
8. Brenchley, J.M., et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112, 2826-2835 (2008
9. Anton, P.A., et al. Enhanced levels of functional HIV-1 co-receptors on human mucosal T cells demonstrated using intestinal biopsy tissue. AIDS 14, 1761-1765 (2000
10. Poles, M.A., Elliott, J., Taing, P., Anton, P.A., & Chen, I.S. A preponderance of CCR5(+) CXCR4(+) mononuclear cells enhances gastrointestinal mucosal susceptibility to human immunodeficiency virus type 1 infection. J. Virol. 75, 8390-8399 (2001
11. Arthos, J., et al. HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 9, 301-309 (2008
12. Cicala, C., et al. The integrin alpha4beta7 forms a complex with cell-surface CD4 and defines a T-cell subset that is highly susceptible to infection by HIV-1. Proc. Natl. Acad. Sci. USA 106, 20877-20882 (2009
13. Brenchley, J.M. Mucosal immunity in human and simian immunodeficiency lentivirus infections. Mucosal Immunol. 6, 657-665 (2013
14. Brenchley, J.M., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12, 1365-1371 (2006
15. Sandler, N.G., et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J. Infect. Dis. 203, 780-790 (2011
16. Chege, D., et al. Sigmoid Th17 populations, the HIV latent reservoir, and microbial translocation in men on long-term antiretroviral therapy. AIDS 25, 741-749 (2011
17. Kim, C.J., et al. Mucosal Th17 cell function is altered during HIV infection and is an independent predictor of systemic immune activation. J. Immunol. 191, 2164-2173 (2013
18. Favre, D., et al. Critical loss of the balance between Th17 and Tregulatory cell populations in pathogenic SIV infection. PLoS Pathog. 5, e1000295 (2009
19. Schuetz, A., et al. Initiation of ART during early acute HIV infection preserves mucosal Th17 function and reverses HIV-related immune activation. PLoS Pathog. 10, e1004543 (2014
20. Kok, A., et al. Early initiation of combined antiretroviral therapy preserves immune function in the gut of HIV-infected patients. Mucosal Immunol. 8, 127-140 (2015
21. Mehandru, S., et al. Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection. PLoSMed. 3, e484 (2006
22. Mavigner, M., et al. Altered CD4+ T cell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J. Clin. Invest. 122, 62-69 (2012
23. Streeter, P.R., Berg, E.L., Rouse, B.T., Bargatze, R.F., & Butcher, E.C. A tissue-specific endothelial cell molecule involved in lymphocyte homing. Nature 331, 41-46 (1988
24. Kunkel, E.J., et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J. Exp. Med. 192, 761-768 (2000
25. Papadakis, K.A., et al. The role of thymus-expressed chemokine and its receptor CCR9 on lymphocytes in the regional specialization of the mucosal immune system. J. Immunol. 165, 5069-5076 (2000
26. Johansson-Lindbom, B., et al. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J. Exp. Med. 198, 963-969 (2003
27. Mora, J.R., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424, 88-93 (2003
28. Iwasaki, A., & Kelsall, B.L. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J. Exp. Med. 191, 1381-1394 (2000
29. Cook, D.N., et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12, 495-503 (2000
30. Annunziato, F., et al. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204, 1849-1861 (2007
31. Acosta-Rodriguez, E.V., et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8, 639-646 (2007
32. Yamazaki, T., et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J. Immunol. 181, 8391-8401 (2008
33. Esplugues, E., et al. Control of TH17 cells occurs in the small intestine. Nature 475, 514-518 (2011
34. Izadpanah, A., Dwinell, M.B., Eckmann, L., Varki, N.M., & Kagnoff, M.F. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G710-G719 (2001
35. Sierro, F., et al. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA 98, 13722-13727 (2001
36. Ivanov, I.I., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498 (2009
37. Cosmi, L., et al. Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor. J. Exp. Med. 205, 1903-1916 (2008
38. Kleinschek, M.A., et al. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J. Exp. Med. 206, 525-534 (2009
39. Seddiki, N., et al. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J. Exp. Med. 203, 1693-1700 (2006
40. Awane, M., Andres, P.G., Li, D.J., & Reinecker, H.C. NF-kappa B-inducing kinase is a commonmediator of IL-17-, TNF-alpha-, and IL-1 beta-induced chemokine promoter activation in intestinal epithelial cells. J. Immunol. 162, 5337-5344 (1999
41. Minegishi, Y., et al. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J. Exp. Med. 206, 1291-1301 (2009
42. Fontaine, J., Poudrier, J., & Roger, M. Short communication: persistence of high blood levels of the chemokines CCL2, CCL19, and CCL20 during the course of HIV infection. AIDS Res. Hum. Retroviruses 27, 655-657 (2011
43. Choi, Y.K., Fallert, B.A., Murphey-Corb, M.A., & Reinhart, T.A. Simian immunodeficiency virus dramatically alters expression of homeostatic chemokines and dendritic cell markers during infection in vivo. Blood 101, 1684-1691 (2003
44. Choi, Y.K., Whelton, K.M., Mlechick, B., Murphey-Corb, M.A., & Reinhart, T.A. Productive infection of dendritic cells by simian immunodeficiency virus in macaque intestinal tissues. J. Pathol. 201, 616-628 (2003
45. Gosselin, A., et al. Peripheral blood CCR4+CCR6+ and CXCR3+ CCR6+CD4+ T cells are highly permissive to HIV-1 infection. J. Immunol. 184, 1604-1616 (2010
46. Monteiro, P., et al. Memory CCR6+CD4+ T cells are preferential targets for productive HIV type 1 infection regardless of their expression of integrin beta7. J. Immunol. 186, 4618-4630 (2011
47. El Hed, A., et al. Susceptibility of human Th17 cells to human immunodeficiency virus and their perturbation during infection. J. Infect. Dis. 201, 843-854 (2010
48. Mowat, A.M., & Agace, W.W. Regional specialization within the intestinal immune system. Nat. Rev. Immunol. 14, 667-685 (2014
49. Koenen, H.J., et al. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112, 2340-2352 (2008
50. Beriou, G., et al. IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 113, 4240-4249 (2009
51. Voo, K.S., et al. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc. Natl. Acad. Sci. USA 106, 4793-4798 (2009
52. Duhen, T., Duhen, R., Lanzavecchia, A., Sallusto, F., & Campbell, D.J. Functionally distinct subsets of human FOXP3+ Treg cells that phenotypically mirror effector Th cells. Blood 119, 4430-4440 (2012
53. Ayyoub, M., et al. Humanmemory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t. Proc. Natl. Acad. Sci. USA 106, 8635-8640 (2009
54. Lindemann, M.J., Hu, Z., Benczik, M., Liu, K.D., & Gaffen, S.L. Differential regulation of the IL-17 receptor by gammac cytokines: inhibitory signaling by the phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 283, 14100-14108 (2008
55. Ortiz, A.M., et al. IL-21 and probiotic therapy improve Th17 frequencies, microbial translocation, and microbiome in ARV-treated, SIV-infected macaques. Mucosal Immunol.; advance online publication, 19 August 2015; doi: 10.1038/mi.2015.75 (2015
56. Micci, L., et al. Interleukin-21 combinedwith ARTreduces inflammation and viral reservoir in SIV-infected macaques. J. Clin. Invest. 125, 4497-4513 (2015
57. Harrington, L.E., et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6, 1123-1132 (2005
58. Park, H., et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 (2005
59. Delobel, P., et al. Naive T-cell depletion related to infection by X4 human immunodeficiency virus type 1 in poor immunological responders to highly active antiretroviral therapy. J. Virol. 80, 10229-10236 (2006
60. Mavigner, M., et al. HIV-1 residual viremia correlates with persistent T-cell activation in poor immunological responders to combination antiretroviral therapy. PLoS One 4, e7658 (2009