Type 3 innate lymphoid cell depletion is mediated by TLRs in lymphoid tissues of simian immunodeficiency virus-infected macaques

FASEB Journal

Volumn 29, Issue 12, 2015, Pages 5072-5080

  Xu, Huanbin ^a   Wang, Xiaolei ^a   Lackner, Andrew A ^a   Veazey, Ronald S ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

GALT; HIV; ILC; SIV

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CELL MARKER; INTERLEUKIN 17; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; THY 1 ANTIGEN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL LINEAGE; CELL LOSS; CONTROLLED STUDY; CYTOKINE PRODUCTION; IN VITRO STUDY; IN VIVO STUDY; INTESTINE; INTESTINE LYMPHATIC TISSUE; LYMPHOID CELL; LYMPHOID TISSUE; MACACA; MOUSE; MUCOSA CELL; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; TH17 CELL; TH22 CELL; TISSUE SECTION; TISSUE STRUCTURE; ANIMAL; INNATE IMMUNITY; LYMPHOCYTE DEPLETION; METABOLISM; PHYSIOLOGY;

ANIMALS; IMMUNITY, INNATE; LYMPHOCYTE DEPLETION; LYMPHOID TISSUE; MACACA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TOLL-LIKE RECEPTORS;

EID: 84958134391     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-276477     Document Type: Article

References (49)

1. Spits, H., and Di Santo, J. P. (2011) The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 12, 21-27
2. Xu, H., Wang, X., Liu, D. X., Moroney-Rasmussen, T., Lackner, A. A., and Veazey, R. S. (2012) IL-17-producing innate lymphoid cells are restricted to mucosal tissues and are depleted in SIV-infected macaques. Mucosal Immunol. 5, 658-669
3. Hepworth, M. R., and Sonnenberg, G. F. (2014) Regulation of the adaptive immune system by innate lymphoid cells. Curr. Opin. Immunol. 27, 75-82
4. Tait Wojno, E. D., and Artis, D. (2012) Innate lymphoid cells: balancing immunity, inflammation, and tissue repair in the intestine. Cell Host Microbe 12, 445-457
5. Cherrier, M., Ohnmacht, C., Cording, S., and Eberl, G. (2012) Development and function of intestinal innate lymphoid cells. Curr. Opin. Immunol. 24, 277-283
6. Sonnenberg, G. F., Monticelli, L. A., Alenghat, T., Fung, T. C., Hutnick, N. A., Kunisawa, J., Shibata, N., Grunberg, S., Sinha, R., Zahm, A. M., Tardif, M. R., Sathaliyawala, T., Kubota, M., Farber, D. L., Collman, R. G., Shaked, A., Fouser, L. A., Weiner, D. B., Tessier, P. A., Friedman, J. R., Kiyono, H., Bushman, F. D., Chang, K. M., and Artis, D. (2012) Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 336, 1321-1325
7. Hepworth, M. R., Monticelli, L. A., Fung, T. C., Ziegler, C. G., Grunberg, S., Sinha, R., Mantegazza, A. R., Ma, H. L., Crawford, A., Angelosanto, J. M., Wherry, E. J., Koni, P. A., Bushman, F. D., Elson, C. O., Eberl, G., Artis, D., and Sonnenberg, G. F. (2013) Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498, 113-117
8. Pearson, C., Uhlig, H. H., and Powrie, F. (2012) Lymphoid microenvironments and innate lymphoid cells in the gut. Trends Immunol. 33, 289-296
9. Hoyler, T., Klose, C. S., Souabni, A., Turqueti-Neves, A., Pfeifer, D., Rawlins, E. L., Voehringer, D., Busslinger, M., and Diefenbach, A. (2012) The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37, 634-648
10. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S., Locksley, R. M., McKenzie, A. N., Mebius, R. E., Powrie, F., and Vivier, E. (2013) Innate lymphoid cells - a proposal for uniform nomenclature. Nat. Rev. Immunol. 13, 145-149
11. Klose, C. S., Flach, M., Möhle, L., Rogell, L., Hoyler, T., Ebert, K., Fabiunke, C., Pfeifer, D., Sexl, V., Fonseca-Pereira, D., Domingues, R. G., Veiga-Fernandes, H., Arnold, S. J., Busslinger, M., Dunay, I. R., Tanriver, Y., and Diefenbach, A. (2014) Differentiation of type1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157, 340-356
12. Bernink, J. H., Peters, C. P., Munneke, M., te Velde, A. A., Meijer, S. L., Weijer, K., Hreggvidsdottir, H. S., Heinsbroek, S. E., Legrand, N., Buskens, C. J., Bemelman, W. A., Mjösberg, J. M., and Spits, H. (2013) Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14, 221-229
13. Fuchs, A., Vermi, W., Lee, J. S., Lonardi, S., Gilfillan, S., Newberry, R. D., Cella, M., and Colonna, M. (2013) Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells. Immunity 38, 769-781
14. Nussbaum, J. C., Van Dyken, S. J., von Moltke, J., Cheng, L. E., Mohapatra, A., Molofsky, A. B., Thornton, E. E., Krummel, M. F., Chawla, A., Liang, H. E., and Locksley, R. M. (2013) Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502, 245-248
15. Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., Bucks, C., Kane, C. M., Fallon, P. G., Pannell, R., Jolin, H. E., and McKenzie, A. N. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370
16. Mjösberg, J., Bernink, J., Golebski, K., Karrich, J. J., Peters, C. P., Blom, B., te Velde, A. A., Fokkens, W. J., van Drunen, C. M., and Spits, H. (2012) The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37, 649-659
17. Gladiator, A., Wangler, N., Trautwein-Weidner, K., and LeibundGut-Landmann, S. (2013) Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 190, 521-525
18. Van de Pavert, S. A., Ferreira, M., Domingues, R. G., Ribeiro, H., Molenaar, R., Moreira-Santos, L., Almeida, F. F., Ibiza, S., Barbosa, I., Goverse, G., Labão-Almeida, C., Godinho-Silva, C., Konijn, T., Schooneman, D., O'Toole, T., Mizee, M. R., Habani, Y., Haak, E., Santori, F. R., Littman, D. R., Schulte-Merker, S., Dzierzak, E., Simas, J. P., Mebius, R. E., and Veiga-Fernandes, H. (2014) Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508, 123-127
19. Magri, G., Miyajima, M., Bascones, S., Mortha, A., Puga, I., Cassis, L., Barra, C. M., Comerma, L., Chudnovskiy, A., Gentile, M., Llige, D., Cols, M., Serrano, S., Aróstegui, J. I., Juan, M., Yagüe, J., Merad, M., Fagarasan, S., and Cerutti, A. (2014) Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat. Immunol. 15, 354-364
20. Qiu, J., Guo, X., Chen, Z. M., He, L., Sonnenberg, G. F., Artis, D., Fu, Y. X., and Zhou, L. (2013) Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39, 386-399
21. Estes, J. D., Harris, L. D., Klatt, N. R., Tabb, B., Pittaluga, S., Paiardini, M., Barclay, G. R., Smedley, J., Pung, R., Oliveira, K. M., Hirsch, V. M., Silvestri, G., Douek, D. C., Miller, C. J., Haase, A. T., Lifson, J., and Brenchley, J. M. (2010) Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 6, e1001052
22. Brenchley, J. M., Price, D. A., Schacker, T. W., Asher, T. E., Silvestri, G., Rao, S., Kazzaz, Z., Bornstein, E., Lambotte, O., Altmann, D., Blazar, B. R., Rodriguez, B., Teixeira-Johnson, L., Landay, A., Martin, J. N., Hecht, F. M., Picker, L. J., Lederman, M. M., Deeks, S. G., and Douek, D. C. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12, 1365-1371
23. Webster, R. L., and Johnson, R. P. (2005) Delineation of multiple subpopulations of natural killer cells in rhesus macaques. Immunology 115, 206-214
24. Reeves, R. K., Gillis, J., Wong, F. E., Yu, Y., Connole, M., and Johnson, R. P. (2010) CD16- natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 115, 4439-4446
25. Spencer, S. P., Wilhelm, C., Yang, Q., Hall, J. A., Bouladoux, N., Boyd, A., Nutman, T. B., Urban, Jr., J. F., Wang, J., Ramalingam, T. R., Bhandoola, A., Wynn, T. A., and Belkaid, Y. (2014) Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 343, 432-437
26. Crellin, N. K., Trifari, S., Kaplan, C. D., Satoh-Takayama, N., Di Santo, J. P., and Spits, H. (2010) Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 33, 752-764
27. Sonnenberg, G. F., Fouser, L. A., and Artis, D. (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12, 383-390
28. Eberl, G., Marmon, S., Sunshine, M. J., Rennert, P. D., Choi, Y., and Littman, D. R. (2004) An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73
29. Tsuji, M., Suzuki, K., Kitamura, H., Maruya, M., Kinoshita, K., Ivanov, I. I., Itoh, K., Littman, D. R., and Fagarasan, S. (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29, 261-271
30. Sawa, S., Lochner, M., Satoh-Takayama, N., Dulauroy, S., Bérard, M., Kleinschek, M., Cua, D., Di Santo, J. P., and Eberl, G. (2011) RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 12, 320-326
31. Takatori, H., Kanno, Y., Watford, W. T., Tato, C. M., Weiss, G., Ivanov, I. I., Littman, D. R., and O'Shea, J. J. (2009) Lymphoid tissue inducerlike cells are an innate source of IL-17 and IL-22. J. Exp. Med. 206, 35-41
32. Sanos, S. L., Bui, V. L., Mortha, A., Oberle, K., Heners, C., Johner, C., and Diefenbach, A. (2009) RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 10, 83-91
33. Satoh-Takayama, N., Vosshenrich, C. A., Lesjean-Pottier, S., Sawa, S., Lochner, M., Rattis, F., Mention, J. J., Thiam, K., Cerf-Bensussan, N., Mandelboim, O., Eberl, G., and Di Santo, J. P. (2008) Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29, 958-970
34. Xu, H., Wang, X., Pahar, B., Moroney-Rasmussen, T., Alvarez, X., Lackner, A. A., and Veazey, R. S. (2010) Increased B7-H1 expression on dendritic cells correlates with programmed death 1 expression on T cells in simian immunodeficiency virus-infected macaques and may contribute to T cell dysfunction and disease progression. J. Immunol. 185, 7340-7348
35. Xu, H., Wang, X., Lackner, A. A., and Veazey, R. S. (2014) PD-1 (HIGH) follicular CD4 T helper cell subsets residing in lymph node germinal centers correlate with B cell maturation and IgG production in rhesus macaques. Front. Immunol. 5, 85
36. + group 3 ILCs and controls intestinal immunity and inflammation. Semin. Immunopathol. 35, 657-670
37. Kiss, E. A., Vonarbourg, C., Kopfmann, S., Hobeika, E., Finke, D., Esser, C., and Diefenbach, A. (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334, 1561-1565
38. Behnsen, J., and Raffatellu, M. (2013) Keeping the peace: aryl hydrocarbon receptor signaling modulates the mucosal microbiota. Immunity 39, 206-207
39. Zelante, T., Iannitti, R. G., Cunha, C., De Luca, A., Giovannini, G., Pieraccini, G., Zecchi, R., D'Angelo, C., Massi-Benedetti, C., Fallarino, F., Carvalho, A., Puccetti, P., and Romani, L. (2013) Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39, 372-385
40. Xu, H., Wang, X., and Veazey, R. S. (2014) Th17cells coordinate with Th22 cells in maintaining homeostasis of intestinal tissues and both are depleted in SIV-infected macaques. J. AIDS Clin. Res. 5, 302
41. Klatt, N. R., Estes, J. D., Sun, X., Ortiz, A. M., Barber, J. S., Harris, L. D., Cervasi, B., Yokomizo, L. K., Pan, L., Vinton, C. L., Tabb, B., Canary, L. A., Dang, Q., Hirsch, V. M., Alter, G., Belkaid, Y., Lifson, J. D., Silvestri, G., Milner, J. D., Paiardini, M., Haddad, E. K., and Brenchley, J. M. (2012) Loss of mucosal CD103+ DCs and IL-17+ and IL-22+ lymphocytes is associated with mucosal damage in SIV infection. Mucosal Immunol. 5, 646-657
42. Shin, J. Y., Hu, W., Naramura, M., and Park, C. Y. (2014) High c-Kit expression identifies hematopoietic stem cells with impaired self-renewal and megakaryocytic bias. J. Exp. Med. 211, 217-231
43. Pennock, J. L., and Grencis, R. K. (2004) In vivo exit of c-kit+/CD49d (hi)/beta7+ mucosal mast cell precursors from the bone marrow following infection with the intestinal nematode Trichinella spiralis. Blood 103, 2655-2660
44. Van de Pavert, S. A., and Mebius, R. E. (2010) New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10, 664-674
45. Withers, D. R., Gaspal, F. M., Mackley, E. C., Marriott, C. L., Ross, E. A., Desanti, G. E., Roberts, N. A., White, A. J., Flores-Langarica, A., McConnell, F. M., Anderson, G., and Lane, P. J. (2012) Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J. Immunol. 189, 2094-2098
46. Lane, P. J., McConnell, F. M., Withers, D., Gaspal, F., Saini, M., and Anderson, G. (2009) Lymphoid tissue inducer cells: bridges between the ancient innate and the modern adaptive immune systems. Mucosal Immunol. 2, 472-477
47. Scandella, E., Bolinger, B., Lattmann, E., Miller, S., Favre, S., Littman, D. R., Finke, D., Luther, S. A., Junt, T., and Ludewig, B. (2008) Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat. Immunol. 9, 667-675
48. Pickert, G., Neufert, C., Leppkes, M., Zheng, Y., Wittkopf, N., Warntjen, M., Lehr, H. A., Hirth, S., Weigmann, B., Wirtz, S., Ouyang, W., Neurath, M. F., and Becker, C. (2009) STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206, 1465-1472
49. Douek, D. (2007) HIV disease progression: immune activation, microbes, and a leaky gut. Top. HIV Med. 15, 114-117