Identification of Interferon-Stimulated Genes with Antiretroviral Activity

Cell Host and Microbe

Volumn 20, Issue 3, 2016, Pages 392-405

  Kane, Melissa ^a   Zang, Trinity M ^a,b   Rihn, Suzannah J ^c   Zhang, Fengwen ^a   Kueck, Tonya ^a   Alim, Mudathir ^a   Schoggins, John ^d   Rice, Charles M ^a   Wilson, Sam J ^c   Bieniasz, Paul D ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; TRIPARTITE MOTIF 56; UNCLASSIFIED DRUG; VIRAL PROTEIN; ANTIVIRUS AGENT; INTERFERON; UBIQUITIN PROTEIN LIGASE;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LIBRARY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; INTERFERON STIMULATED GENE; NONHUMAN; PRIORITY JOURNAL; RETROVIRIDAE; RHESUS MONKEY; VIRUS GENE; VIRUS INHIBITION; VIRUS REPLICATION; ANIMAL; GENETIC SCREENING; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIVIRAL AGENTS; GENE LIBRARY; GENETIC TESTING; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERONS; MACACA MULATTA; RETROVIRIDAE; UBIQUITIN-PROTEIN LIGASES; VIRUS REPLICATION;

EID: 84995603714     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.08.005     Document Type: Article

References (41)

1. Asmuth, D.M., Murphy, R.L., Rosenkranz, S.L., Lertora, J.J., Kottilil, S., Cramer, Y., Chan, E.S., Schooley, R.T., Rinaldo, C.R., Thielman, N., et al., AIDS Clinical Trials Group A5192 Team. Safety, tolerability, and mechanisms of antiretroviral activity of pegylated interferon Alfa-2a in HIV-1-monoinfected participants: a phase II clinical trial. J. Infect. Dis. 201 (2010), 1686–1696.
2. Bitzegeio, J., Sampias, M., Bieniasz, P.D., Hatziioannou, T., Adaptation to the interferon-induced antiviral state by human and simian immunodeficiency viruses. J. Virol. 87 (2013), 3549–3560.
3. Brenchley, J.M., Price, D.A., Schacker, T.W., Asher, T.E., Silvestri, G., Rao, S., Kazzaz, Z., Bornstein, E., Lambotte, O., Altmann, D., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12 (2006), 1365–1371.
4. Busnadiego, I., Kane, M., Rihn, S.J., Preugschas, H.F., Hughes, J., Blanco-Melo, D., Strouvelle, V.P., Zang, T.M., Willett, B.J., Boutell, C., et al. Host and viral determinants of Mx2 antiretroviral activity. J. Virol. 88 (2014), 7738–7752.
5. Cobbold, S.P., Adams, E., Farquhar, C.A., Nolan, K.F., Howie, D., Lui, K.O., Fairchild, P.J., Mellor, A.L., Ron, D., Waldmann, H., Infectious tolerance via the consumption of essential amino acids and mTOR signaling. Proc. Natl. Acad. Sci. USA 106 (2009), 12055–12060.
6. Dittmann, M., Hoffmann, H.H., Scull, M.A., Gilmore, R.H., Bell, K.L., Ciancanelli, M., Wilson, S.J., Crotta, S., Yu, Y., Flatley, B., et al. A serpin shapes the extracellular environment to prevent influenza A virus maturation. Cell 160 (2015), 631–643.
7. Doyle, T., Goujon, C., Malim, M.H., HIV-1 and interferons: who's interfering with whom?. Nat. Rev. Microbiol. 13 (2015), 403–413.
8. Estes, J.D., Li, Q., Reynolds, M.R., Wietgrefe, S., Duan, L., Schacker, T., Picker, L.J., Watkins, D.I., Lifson, J.D., Reilly, C., et al. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J. Infect. Dis. 193 (2006), 703–712.
9. Favre, D., Mold, J., Hunt, P.W., Kanwar, B., Loke, P., Seu, L., Barbour, J.D., Lowe, M.M., Jayawardene, A., Aweeka, F., et al. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci. Transl. Med., 2, 2010, 32ra36.
10. Fenton-May, A.E., Dibben, O., Emmerich, T., Ding, H., Pfafferott, K., Aasa-Chapman, M.M., Pellegrino, P., Williams, I., Cohen, M.S., Gao, F., et al. Relative resistance of HIV-1 founder viruses to control by interferon-alpha. Retrovirology, 10, 2013, 146.
11. Friberg, M., Jennings, R., Alsarraj, M., Dessureault, S., Cantor, A., Extermann, M., Mellor, A.L., Munn, D.H., Antonia, S.J., Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. International journal of cancer Journal international du cancer 101 (2002), 151–155.
12. Gack, M.U., Shin, Y.C., Joo, C.H., Urano, T., Liang, C., Sun, L., Takeuchi, O., Akira, S., Chen, Z., Inoue, S., Jung, J.U., TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446 (2007), 916–920.
13. Galão, R.P., Le Tortorec, A., Pickering, S., Kueck, T., Neil, S.J., Innate sensing of HIV-1 assembly by Tetherin induces NFκB-dependent proinflammatory responses. Cell Host Microbe 12 (2012), 633–644.
14. Goldstone, D.C., Ennis-Adeniran, V., Hedden, J.J., Groom, H.C., Rice, G.I., Christodoulou, E., Walker, P.A., Kelly, G., Haire, L.F., Yap, M.W., et al. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 480 (2011), 379–382.
15. Hammer, S.M., Gillis, J.M., Groopman, J.E., Rose, R.M., In vitro modification of human immunodeficiency virus infection by granulocyte-macrophage colony-stimulating factor and gamma interferon. Proc. Natl. Acad. Sci. USA 83 (1986), 8734–8738.
16. Hassanain, H.H., Chon, S.Y., Gupta, S.L., Differential regulation of human indoleamine 2,3-dioxygenase gene expression by interferons-gamma and -alpha. Analysis of the regulatory region of the gene and identification of an interferon-gamma-inducible DNA-binding factor. J. Biol. Chem. 268 (1993), 5077–5084.
17. Hatziioannou, T., Bieniasz, P.D., Antiretroviral restriction factors. Curr. Opin. Virol. 1 (2011), 526–532.
18. Hayaishi, O., Properties and function of indoleamine 2,3-dioxygenase. J. Biochem. 79 (1976), 13P–21P.
19. Kane, M., Yadav, S.S., Bitzegeio, J., Kutluay, S.B., Zang, T., Wilson, S.J., Schoggins, J.W., Rice, C.M., Yamashita, M., Hatziioannou, T., Bieniasz, P.D., MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502 (2013), 563–566.
20. Liu, B., Li, N.L., Wang, J., Shi, P.Y., Wang, T., Miller, M.A., Li, K., Overlapping and distinct molecular determinants dictating the antiviral activities of TRIM56 against flaviviruses and coronavirus. J. Virol. 88 (2014), 13821–13835.
21. Liu, B., Li, N.L., Shen, Y., Bao, X., Fabrizio, T., Elbahesh, H., Webby, R.J., Li, K., The C-Terminal Tail of TRIM56 Dictates Antiviral Restriction of Influenza A and B Viruses by Impeding Viral RNA Synthesis. J. Virol. 90 (2016), 4369–4382.
22. Mao, R., Zhang, J., Jiang, D., Cai, D., Levy, J.M., Cuconati, A., Block, T.M., Guo, J.T., Guo, H., Indoleamine 2,3-dioxygenase mediates the antiviral effect of gamma interferon against hepatitis B virus in human hepatocyte-derived cells. J. Virol. 85 (2011), 1048–1057.
23. Munn, D.H., Zhou, M., Attwood, J.T., Bondarev, I., Conway, S.J., Marshall, B., Brown, C., Mellor, A.L., Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281 (1998), 1191–1193.
24. Munn, D.H., Sharma, M.D., Baban, B., Harding, H.P., Zhang, Y., Ron, D., Mellor, A.L., GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22 (2005), 633–642.
25. Murray, M.F., Tryptophan depletion and HIV infection: a metabolic link to pathogenesis. Lancet Infect. Dis. 3 (2003), 644–652.
26. Obojes, K., Andres, O., Kim, K.S., Däubener, W., Schneider-Schaulies, J., Indoleamine 2,3-dioxygenase mediates cell type-specific anti-measles virus activity of gamma interferon. J. Virol. 79 (2005), 7768–7776.
27. Opitz, C.A., Litzenburger, U.M., Sahm, F., Ott, M., Tritschler, I., Trump, S., Schumacher, T., Jestaedt, L., Schrenk, D., Weller, M., et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 478 (2011), 197–203.
28. Pauls, E., Ruiz, A., Riveira-Muñoz, E., Permanyer, M., Badia, R., Clotet, B., Keppler, O.T., Ballana, E., Este, J.A., p21 regulates the HIV-1 restriction factor SAMHD1. Proc. Natl. Acad. Sci. USA 111 (2014), E1322–E1324.
29. Pertel, T., Hausmann, S., Morger, D., Züger, S., Guerra, J., Lascano, J., Reinhard, C., Santoni, F.A., Uchil, P.D., Chatel, L., et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472 (2011), 361–365.
30. Pfefferkorn, E.R., Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. USA 81 (1984), 908–912.
31. Sakurai, K., Zou, J.P., Tschetter, J.R., Ward, J.M., Shearer, G.M., Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 129 (2002), 186–196.
32. Sandler, N.G., Bosinger, S.E., Estes, J.D., Zhu, R.T., Tharp, G.K., Boritz, E., Levin, D., Wijeyesinghe, S., Makamdop, K.N., del Prete, G.Q., et al. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 511 (2014), 601–605.
33. Schmidt, S.V., Schultze, J.L., New Insights into IDO Biology in Bacterial and Viral Infections. Front. Immunol., 5, 2014, 384.
34. Schoggins, J.W., Wilson, S.J., Panis, M., Murphy, M.Y., Jones, C.T., Bieniasz, P., Rice, C.M., A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472 (2011), 481–485.
35. Schoggins, J.W., MacDuff, D.A., Imanaka, N., Gainey, M.D., Shrestha, B., Eitson, J.L., Mar, K.B., Richardson, R.B., Ratushny, A.V., Litvak, V., et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505 (2014), 691–695.
36. Shen, Y., Li, N.L., Wang, J., Liu, B., Lester, S., Li, K., TRIM56 is an essential component of the TLR3 antiviral signaling pathway. J. Biol. Chem. 287 (2012), 36404–36413.
37. Stetson, D.B., Medzhitov, R., Type I interferons in host defense. Immunity 25 (2006), 373–381.
38. Tsuchida, T., Zou, J., Saitoh, T., Kumar, H., Abe, T., Matsuura, Y., Kawai, T., Akira, S., The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33 (2010), 765–776.
39. Uchil, P.D., Quinlan, B.D., Chan, W.T., Luna, J.M., Mothes, W., TRIM E3 ligases interfere with early and late stages of the retroviral life cycle. PLoS Pathog., 4, 2008, e16.
40. Wang, J., Liu, B., Wang, N., Lee, Y.M., Liu, C., Li, K., TRIM56 is a virus- and interferon-inducible E3 ubiquitin ligase that restricts pestivirus infection. J. Virol. 85 (2011), 3733–3745.
41. Wilson, S.J., Schoggins, J.W., Zang, T., Kutluay, S.B., Jouvenet, N., Alim, M.A., Bitzegeio, J., Rice, C.M., Bieniasz, P.D., Inhibition of HIV-1 particle assembly by 2′,3′-cyclic-nucleotide 3′-phosphodiesterase. Cell Host Microbe 12 (2012), 585–597.