The immunosuppressive role of IL-32 in lymphatic tissue during HIV-1 infection

Journal of Immunology

Volumn 186, Issue 11, 2011, Pages 6576-6584

  Smith, Anthony J ^a   Toledo, Chad M ^a,c   Wietgrefe, Stephen W ^a   Duan, Lijie ^a   Schacker, Timothy W ^a   Reilly, Cavan S ^b   Haase, Ashley T ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IG LIKE TRANSCRIPT 4; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 32; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADULT; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; IMMUNE DEFICIENCY; IMMUNOREACTIVITY; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; LYMPHOID TISSUE; MACROPHAGE; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS REPLICATION;

ADULT; FEMALE; GENE EXPRESSION PROFILING; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; ILEUM; IN SITU HYBRIDIZATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERLEUKINS; LYMPH NODES; LYMPHOID TISSUE; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, IMMUNOLOGIC; RECTUM; RNA, VIRAL; TIME FACTORS; VIRUS REPLICATION;

EID: 79958022449     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100277     Document Type: Article

References (48)

1. Douek, D. C., M. Roederer, and R. A. Koup. 2009. Emerging concepts in the immunopathogenesis of AIDS. Annu. Rev. Med. 60: 471-484.
2. Appay, V., and D. Sauce. 2008. Immune activation and inflammation in HIV-1 infection: causes and consequences. J. Pathol. 214: 231-241. (Pubitemid 351160160)
3. Lori, F. 2008. Treating HIV/AIDS by reducing immune system activation: the paradox of immune deficiency and immune hyperactivation. Curr. Opin. HIV AIDS 3: 99-103.
4. Collins, F. M. 1978. Cellular antimicrobial immunity. CRC Crit. Rev. Microbiol. 7: 27-91.
5. Li, Q., T. Schacker, J. Carlis, G. Beilman, P. Nguyen, and A. T. Haase. 2004. Functional genomic analysis of the response of HIV-1-infected lymphatic tissue to antiretroviral therapy. J. Infect. Dis. 189: 572-582.
6. Li, Q., A. J. Smith, T. W. Schacker, J. V. Carlis, L. Duan, C. S. Reilly, and A. T. Haase. 2009. Microarray analysis of lymphatic tissue reveals stage-specific, gene expression signatures in HIV-1 infection. J. Immunol. 183: 1975-1982.
7. Smith, A. J., Q. Li, S. W. Wietgrefe, T. W. Schacker, C. S. Reilly, and A. T. Haase. 2010. Host genes associated with HIV-1 replication in lymphatic tissue. J. Immunol. 185: 5417-5424.
8. Dahl, C. A., R. P. Schall, H. L. He, and J. S. Cairns. 1992. Identification of a novel gene expressed in activated natural killer cells and T cells. J. Immunol. 148: 597-603.
9. Dinarello, C. A., and S. H. Kim. 2006. IL-32, a novel cytokine with a possible role in disease. Ann. Rheum. Dis. 65(Suppl 3): iii61-iii64.
10. Smith, A. J., T. W. Schacker, C. S. Reilly, and A. T. Haase. 2010. A role for syndecan-1 and claudin-2 in microbial translocation during HIV-1 infection. J. Acquir. Immune Defic. Syndr. 55: 306-315.
11. Zhang, Z., T. Schuler, M. Zupancic, S. Wietgrefe, K. A. Staskus, K. A. Reimann, T. A. Reinhart, M. Rogan, W. Cavert, C. J. Miller, et al. 1999. Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286: 1353-1357.
12. Kim, S. H., S. Y. Han, T. Azam, D. Y. Yoon, and C. A. Dinarello. 2005. Interleukin-32: a cytokine and inducer of TNFalpha. Immunity 22: 131-142.
13. Joosten, L. A., M. G. Netea, S. H. Kim, D. Y. Yoon, B. Oppers-Walgreen, T. R. Radstake, P. Barrera, F. A. van de Loo, C. A. Dinarello, and W. B. van den Berg. 2006. IL-32, a proinflammatory cytokine in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 103: 3298-3303.
14. Shoda, H., K. Fujio, Y. Yamaguchi, A. Okamoto, T. Sawada, Y. Kochi, and K. Yamamoto. 2006. Interactions between IL-32 and tumor necrosis factor alpha contribute to the exacerbation of immune-inflammatory diseases. Arthritis Res. Ther. 8: R166.
15. Shioya, M., A. Nishida, Y. Yagi, A. Ogawa, T. Tsujikawa, S. Kim-Mitsuyama, A. Takayanagi, N. Shimizu, Y. Fujiyama, and A. Andoh. 2007. Epithelial overexpression of interleukin-32α in inflammatory bowel disease. Clin. Exp. Immunol. 149: 480-486.
16. Felaco, P., M. L. Castellani, M. A. De Lutiis, M. Felaco, F. Pandolfi, V. Salini, D. De Amicis, J. Vecchiet, S. Tete, C. Ciampoli, et al. 2009. IL-32: a newly-discovered proinflammatory cytokine. J. Biol. Regul. Homeost. Agents 23: 141-147.
17. Kang, J. W., S. C. Choi, M. C. Cho, H. J. Kim, J. H. Kim, J. S. Lim, S. H. Kim, J. Y. Han, and D. Y. Yoon. 2009. A proinflammatory cytokine interleukin-32β promotes the production of an anti-inflammatory cytokine interleukin-10. Immunology 128(1 Suppl): e532-e540.
18. Choi, J. D., S. Y. Bae, J. W. Hong, T. Azam, C. A. Dinarello, E. Her, W. S. Choi, B. K. Kim, C. K. Lee, D. Y. Yoon, et al. 2009. Identification of the most active interleukin-32 isoform. Immunology 126: 535-542.
19. Mellor, A. L., and D. H. Munn. 2004. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4: 762-774.
20. Murray, M. F. 2003. Tryptophan depletion and HIV infection: a metabolic link to pathogenesis. Lancet Infect. Dis. 3: 644-652.
21. Munn, D. H., E. Shafizadeh, J. T. Attwood, I. Bondarev, A. Pashine, and A. L. Mellor. 1999. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189: 1363-1372.
22. Boasso, A., J. P. Herbeuval, A. W. Hardy, S. A. Anderson, M. J. Dolan, D. Fuchs, and G. M. Shearer. 2007. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. Blood 109: 3351-3359.
23. Fallarino, F., U. Grohmann, S. You, B. C. McGrath, D. R. Cavener, C. Vacca, C. Orabona, R. Bianchi, M. L. Belladonna, C. Volpi, et al. 2006. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J. Immunol. 176: 6752-6761. (Pubitemid 43787857)
24. Chen, W., X. Liang, A. J. Peterson, D. H. Munn, and B. R. Blazar. 2008. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J. Immunol. 181: 5396-5404.
25. Brenk, M., M. Scheler, S. Koch, J. Neumann, O. Takikawa, G. Häcker, T. Bieber, and D. von Bubnoff. 2009. Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4+CD25+ Foxp3+ T regulatory cells. J. Immunol. 183: 145-154.
26. Ravetch, J. V., and L. L. Lanier. 2000. Immune inhibitory receptors. Science 290: 84-89.
27. Potula, R., L. Poluektova, B. Knipe, J. Chrastil, D. Heilman, H. Dou, O. Takikawa, D. H. Munn, H. E. Gendelman, and Y. Persidsky. 2005. Inhibition of indoleamine 2,3-dioxygenase (IDO) enhances elimination of virus-infected macrophages in an animal model of HIV-1 encephalitis. Blood 106: 2382-2390. (Pubitemid 41510811)
28. Boasso, A., M. Vaccari, A. Hryniewicz, D. Fuchs, J. Nacsa, V. Cecchinato, J. Andersson, G. Franchini, G. M. Shearer, and C. Chougnet. 2007. Regulatory T-cell markers, indoleamine 2,3-dioxygenase, and virus levels in spleen and gut during progressive simian immunodeficiency virus infection. J. Virol. 81: 11593-11603. (Pubitemid 47623791)
29. Choi, J., S. Bae, J. Hong, S. Ryoo, H. Jhun, K. Hong, D. Yoon, S. Lee, E. Her, W. Choi, et al. 2010. Paradoxical effects of constitutive human IL-32γ in transgenic mice during experimental colitis. Proc. Natl. Acad. Sci. USA 107: 21082-21086.
30. Dimitriou, I. D., L. Clemenza, A. J. Scotter, G. Chen, F. M. Guerra, and R. Rottapel. 2008. Putting out the fire: coordinated suppression of the innate and adaptive immune systems by SOCS1 and SOCS3 proteins. Immunol. Rev. 224: 265-283.
31. Johnson,W. E., and R. C. Desrosiers. 2002. Viral persistence: HIV's strategies of immune system evasion. Annu. Rev. Med. 53: 499-518.
32. Alfano, M., A. Crotti, E. Vicenzi, and G. Poli. 2008. New players in cytokine control of HIV infection. Curr. HIV/AIDS Rep. 5: 27-32.
33. Nold, M. F., C. A. Nold-Petry, G. B. Pott, J. A. Zepp, M. T. Saavedra, S. H. Kim, and C. A. Dinarello. 2008. Endogenous IL-32 controls cytokine and HIV-1 production. J. Immunol. 181: 557-565.
34. Boasso, A., and G. M. Shearer. 2007. How does indoleamine 2,3-dioxygenase contribute to HIV-mediated immune dysregulation. Curr. Drug Metab. 8: 217-223.
35. Werner, E. R., D. Fuchs, A. Hausen, H. Jaeger, G. Reibnegger, G. Werner-Felmayer, M. P. Dierich, and H. Wachter. 1988. Tryptophan degradation in patients infected by human immunodeficiency virus. Biol. Chem. Hoppe Seyler 369: 337-340.
36. Fuchs, D., A. Forsman, L. Hagberg, M. Larsson, G. Norkrans, G. Reibnegger, E. R. Werner, and H. Wachter. 1990. Immune activation and decreased tryptophan in patients with HIV-1 infection. J. Interferon Res. 10: 599-603.
37. Gisslén, M., M. Larsson, G. Norkrans, D. Fuchs, H. Wachter, and L. Hagberg. 1994. Tryptophan concentrations increase in cerebrospinal fluid and blood after zidovudine treatment in patients with HIV type 1 infection. AIDS Res. Hum. Retroviruses 10: 947-951.
38. Huengsberg, M., J. B. Winer, M. Gompels, R. Round, J. Ross, and M. Shahmanesh. 1998. Serum kynurenine-to-tryptophan ratio increases with progressive disease in HIV-infected patients. Clin. Chem. 44: 858-862.
39. Boasso, A., A. W. Hardy, S. A. Anderson, M. J. Dolan, and G. M. Shearer. 2008. HIV-induced type I interferon and tryptophan catabolism drive T cell dysfunction despite phenotypic activation. PLoS ONE 3: e2961.
40. Chang, C. C., R. Ciubotariu, J. S. Manavalan, J. Yuan, A. I. Colovai, F. Piazza, S. Lederman, M. Colonna, R. Cortesini, R. Dalla-Favera, and N. Suciu-Foca. 2002. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat. Immunol. 3: 237-243.
41. Manavalan, J. S., P. C. Rossi, G. Vlad, F. Piazza, A. Yarilina, R. Cortesini, D. Mancini, and N. Suciu-Foca. 2003. High expression of ILT3 and ILT4 is a general feature of tolerogenic dendritic cells. Transpl. Immunol. 11: 245-258.
42. Gregori, S., D. Tomasoni, V. Pacciani, M. Scirpoli, M. Battaglia, C. F. Magnani, E. Hauben, and M. G. Roncarolo. 2010. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 116: 935-944.
43. Hryniewicz, A., A. Boasso, Y. Edghill-Smith, M. Vaccari, D. Fuchs, D. Venzon, J. Nacsa, M. R. Betts, W. P. Tsai, J. M. Heraud, et al. 2006. CTLA-4 blockade decreases TGF-b, IDO, and viral RNA expression in tissues of SIVmac251-infected macaques. Blood 108: 3834-3842. (Pubitemid 44864566)
44. Andersson, J., H. Behbahani, J. Lieberman, E. Connick, A. Landay, B. Patterson, A. Sönnerborg, K. Loré, S. Uccini, and T. E. Fehniger. 1999. Perforin is not coexpressed with granzyme A within cytotoxic granules in CD8 T lymphocytes present in lymphoid tissue during chronic HIV infection. AIDS 13: 1295-1303.
45. Zhang, D., P. Shankar, Z. Xu, B. Harnisch, G. Chen, C. Lange, S. J. Lee, H. Valdez, M. M. Lederman, and J. Lieberman. 2003. Most antiviral CD8 T cells during chronic viral infection do not express high levels of perforin and are not directly cytotoxic. Blood 101: 226-235. (Pubitemid 36025912)
46. Jiang, Y., E. Karita, D. Castor, and P. E. Jolly. 2005. Characterization of CD8+ T lymphocytes in chronic HIV-1 subtype A infection in Rwandan women. Cell. Mol. Biol. 51(Suppl): OL737-OL743.
47. Chae, J. I., J. H. Shim, K. S. Lee, Y. S. Cho, K. S. Lee, Y. Yoon, S. H. Kim, H. M. Chung, D. B. Koo, C. S. Park, et al. 2010. Downregulation of immune response by the human cytokines Interleukin-32α and β in cell-mediated rejection. Cell. Immunol. 264: 47-53.
48. Lieberman, J., N. Manjunath, and P. Shankar. 2002. Avoiding the kiss of death: how HIV and other chronic viruses survive. Curr. Opin. Immunol. 14: 478-486.