Intact Type I Interferon Production and IRF7 Function in Sooty Mangabeys

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Bosinger, Steven E ^a,b   Johnson, Zachary P ^a,b   Folkner, Kathryn A ^a   Patel, Nirav ^b   Hashempour, Tayebeh ^a   Jochems, Simon P ^a   del Rio Estrada, Perla M ^a   Paiardini, Mirko ^a   Lin, Rongtuan ^c   Vanderford, Thomas H ^a   Hiscott, John ^c,d   Silvestri, Guido ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d Vaccine and Gene Therapy Institute of Florida Port Saint Lucie   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; INTERFERON; INTERFERON REGULATORY FACTOR 7; CL097 COMPOUND; IMIDAZOLE DERIVATIVE; MESSENGER RNA; QUINOLINE DERIVATIVE; TOLL LIKE RECEPTOR 7;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ARTICLE; CERCOCEBUS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE SEQUENCE; HUMAN; HUMAN CELL; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; REAL TIME POLYMERASE CHAIN REACTION; RNA PURIFICATION; SEQUENCE ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TRANSACTIVATION; ACTIVE TRANSPORT; AGONISTS; ANIMAL; CELL NUCLEUS; CLINICAL TRIAL; DENDRITIC CELL; EXON; FEMALE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; MALE; MISSENSE MUTATION; MONONUCLEAR CELL; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SUBSTITUTION; ANIMALS; CELL NUCLEUS; CERCOCEBUS ATYS; DENDRITIC CELLS; DNA MUTATIONAL ANALYSIS; EXONS; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; IMIDAZOLES; INTERFERON REGULATORY FACTOR-7; INTERFERON-ALPHA; INTERFERON-BETA; LEUKOCYTES, MONONUCLEAR; MALE; MUTATION, MISSENSE; QUINOLINES; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TOLL-LIKE RECEPTOR 7;

EID: 84883365277     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003597     Document Type: Article

References (59)

1. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, et al. (2003) Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18: 441-452.
2. Kanki PJ, Alroy J, Essex M, (1985) Isolation of T-lymphotropic retrovirus related to HTLV-III/LAV from wild-caught African green monkeys. Science 230: 951-954.
3. Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G, (2012) Natural SIV hosts: showing AIDS the door. Science 335: 1188-1193.
4. Theofilopoulos AN, Baccala R, Beutler B, Kono DH, (2005) Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 23: 307-336.
5. Iwasaki A, (2012) Innate immune recognition of HIV-1. Immunity 37: 389-398.
6. Der SD, Zhou A, Williams BR, Silverman RH, (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 15623-15628.
7. Schoggins JW, Rice CM, (2011) Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1: 519-525.
8. Hyrcza MD, Kovacs C, Loutfy M, Halpenny R, Heisler L, et al. (2007) Distinct transcriptional profiles in ex vivo CD4+ and CD8+ T cells are established early in human immunodeficiency virus type 1 infection and are characterized by a chronic interferon response as well as extensive transcriptional changes in CD8+ T cells. J Virol 81: 3477-3486.
9. Bosinger SE, Hosiawa KA, Cameron MJ, Persad D, Ran L, et al. (2004) Gene expression profiling of host response in models of acute HIV infection. J Immunol 173: 6858-6863.
10. Bosinger SE, Li Q, Gordon SN, Klatt NR, Duan L, et al. (2009) Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 119: 3556-3572.
11. Rotger M, Dalmau J, Rauch A, McLaren P, Bosinger SE, et al. (2011) Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. J Clin Invest 121: 2391-2400.
12. Neumann A, Polis M, Rozenberg L, Jackson J, Reitano K, et al. (2007) Differential antiviral effect of PEG-interferon-alpha-2b on HIV and HCV in the treatment of HIV/HCV co-infected patients. AIDS 21: 1855-1865.
13. Pillai SK, Abdel-Mohsen M, Guatelli J, Skasko M, Monto A, et al. (2012) Role of retroviral restriction factors in the interferon-alpha-mediated suppression of HIV-1 in vivo. Proc Natl Acad Sci U S A 109: 3035-3040.
14. Vanderford TH, Slichter C, Rogers KA, Lawson BO, Obaede R, et al. (2012) Treatment of SIV-infected sooty mangabeys with a type-I IFN agonist results in decreased virus replication without inducing hyperimmune activation. Blood 119: 5750-5757.
15. von Sydow M, Sonnerborg A, Gaines H, Strannegard O, (1991) Interferon-alpha and tumor necrosis factor-alpha in serum of patients in various stages of HIV-1 infection. AIDS Res Hum Retroviruses 7: 375-380.
16. Herbeuval JP, Shearer GM, (2007) HIV-1 immunopathogenesis: how good interferon turns bad. Clin Immunol 123: 121-128.
17. Sedaghat AR, German J, Teslovich TM, Cofrancesco J Jr, Jie CC, et al. (2008) Chronic CD4+ T-cell activation and depletion in human immunodeficiency virus type 1 infection: type I interferon-mediated disruption of T-cell dynamics. J Virol 82: 1870-1883.
18. Fernandez S, Tanaskovic S, Helbig K, Rajasuriar R, Kramski M, et al. (2011) CD4+ T-cell deficiency in HIV patients responding to antiretroviral therapy is associated with increased expression of interferon-stimulated genes in CD4+ T cells. J Infect Dis 204: 1927-1935.
19. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, et al. (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14: 1077-1087.
20. Honda K, Taniguchi T, (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644-658.
21. Harris LD, Tabb B, Sodora DL, Paiardini M, Klatt NR, et al. (2010) Downregulation of robust acute type I interferon responses distinguishes nonpathogenic simian immunodeficiency virus (SIV) infection of natural hosts from pathogenic SIV infection of rhesus macaques. J Virol 84: 7886-7891.
22. Meythaler M, Martinot A, Wang Z, Pryputniewicz S, Kasheta M, et al. (2009) Differential CD4+ T-lymphocyte apoptosis and bystander T-cell activation in rhesus macaques and sooty mangabeys during acute simian immunodeficiency virus infection. J Virol 83: 572-583.
23. Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, et al. (2010) A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
24. Sumpter B, Dunham R, Gordon S, Engram J, Hennessy M, et al. (2007) Correlates of preserved CD4(+) T cell homeostasis during natural, nonpathogenic simian immunodeficiency virus infection of sooty mangabeys: implications for AIDS pathogenesis. J Immunol 178: 1680-1691.
25. Taaffe J, Chahroudi A, Engram J, Sumpter B, Meeker T, et al. (2010) A five-year longitudinal analysis of sooty mangabeys naturally infected with simian immunodeficiency virus reveals a slow but progressive decline in CD4+ T-cell count whose magnitude is not predicted by viral load or immune activation. J Virol 84: 5476-5484.
26. tenOever BR, Sharma S, Zou W, Sun Q, Grandvaux N, et al. (2004) Activation of TBK1 and IKKvarepsilon kinases by vesicular stomatitis virus infection and the role of viral ribonucleoprotein in the development of interferon antiviral immunity. J Virol 78: 10636-10649.
27. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, et al. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
28. Lin R, Mamane Y, Hiscott J, (2000) Multiple regulatory domains control IRF-7 activity in response to virus infection. J Biol Chem 275: 34320-34327.
29. Au WC, Moore PA, LaFleur DW, Tombal B, Pitha PM, (1998) Characterization of the interferon regulatory factor-7 and its potential role in the transcription activation of interferon A genes. J Biol Chem 273: 29210-29217.
30. Dai J, Megjugorac NJ, Amrute SB, Fitzgerald-Bocarsly P, (2004) Regulation of IFN regulatory factor-7 and IFN-alpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J Immunol 173: 1535-1548.
31. Paiardini M, Cervasi B, Reyes-Aviles E, Micci L, Ortiz AM, et al. (2011) Low levels of SIV infection in sooty mangabey central memory CD(4)(+) T cells are associated with limited CCR5 expression. Nat Med 17: 830-836.
32. Gordon SN, Klatt NR, Bosinger SE, Brenchley JM, Milush JM, et al. (2007) Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol 179: 3026-3034.
33. Estes JD, Gordon SN, Zeng M, Chahroudi AM, Dunham RM, et al. (2008) Early resolution of acute immune activation and induction of PD-1 in SIV-infected sooty mangabeys distinguishes nonpathogenic from pathogenic infection in rhesus macaques. J Immunol 180: 6798-6807.
34. Chang J, Lindsay RJ, Kulkarni S, Lifson JD, Carrington M, et al. (2011) Polymorphisms in interferon regulatory factor 7 reduce interferon-alpha responses of plasmacytoid dendritic cells to HIV-1. AIDS 25: 715-717.
35. Fu Q, Zhao J, Qian X, Wong JL, Kaufman KM, et al. (2011) Association of a functional IRF7 variant with systemic lupus erythematosus. Arthritis Rheum 63: 749-754.
36. Kawasaki A, Furukawa H, Kondo Y, Ito S, Hayashi T, et al. (2012) Association of PHRF1-IRF7 region polymorphism with clinical manifestations of systemic lupus erythematosus in a Japanese population. Lupus 21: 890-895.
37. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19-28.
38. Hoshino K, Sugiyama T, Matsumoto M, Tanaka T, Saito M, et al. (2006) IkappaB kinase-alpha is critical for interferon-alpha production induced by Toll-like receptors 7 and 9. Nature 440: 949-953.
39. Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, et al. (2004) Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 5: 1061-1068.
40. Zhao T, Yang L, Sun Q, Arguello M, Ballard DW, et al. (2007) The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat Immunol 8: 592-600.
41. Heikenwalder M, Polymenidou M, Junt T, Sigurdson C, Wagner H, et al. (2004) Lymphoid follicle destruction and immunosuppression after repeated CpG oligodeoxynucleotide administration. Nat Med 10: 187-192.
42. Taylor KE, Mossman KL, (2013) Recent advances in understanding viral evasion of type I interferon. Immunology 138: 190-197.
43. Litvak V, Ratushny AV, Lampano AE, Schmitz F, Huang AC, et al. (2012) A FOXO3-IRF7 gene regulatory circuit limits inflammatory sequelae of antiviral responses. Nature 490: 421-425.
44. Lee MS, Kim B, Oh GT, Kim YJ, (2013) OASL1 inhibits translation of the type I interferon-regulating transcription factor IRF7. Nat Immunol 14: 346-355.
45. O'Brien M, Manches O, Sabado RL, Baranda SJ, Wang Y, et al. (2011) Spatiotemporal trafficking of HIV in human plasmacytoid dendritic cells defines a persistently IFN-alpha-producing and partially matured phenotype. J Clin Invest 121: 1088-1101.
46. Lederer S, Favre D, Walters KA, Proll S, Kanwar B, et al. (2009) Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog 5: e1000296.
47. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, et al. (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119: 3544-3555.
48. Campillo-Gimenez L, Laforge M, Fay M, Brussel A, Cumont MC, et al. (2010) Nonpathogenesis of simian immunodeficiency virus infection is associated with reduced inflammation and recruitment of plasmacytoid dendritic cells to lymph nodes, not to lack of an interferon type I response, during the acute phase. J Virol 84: 1838-1846.
49. Mandl JN, Akondy R, Lawson B, Kozyr N, Staprans SI, et al. (2011) Distinctive TLR7 signaling, type I IFN production, and attenuated innate and adaptive immune responses to yellow fever virus in a primate reservoir host. J Immunol 186: 6406-6416.
50. Brenchley JM, Silvestri G, Douek DC, (2010) Nonprogressive and progressive primate immunodeficiency lentivirus infections. Immunity 32: 737-742.
51. Schindler M, Munch J, Kutsch O, Li H, Santiago ML, et al. (2006) Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125: 1055-1067.
52. Schindler M, Schmokel J, Specht A, Li H, Munch J, et al. (2008) Inefficient Nef-mediated downmodulation of CD3 and MHC-I correlates with loss of CD4+T cells in natural SIV infection. PLoS Pathog 4: e1000107.
53. Brenchley JM, Vinton C, Tabb B, Hao XP, Connick E, et al. (2012) Differential infection patterns of CD4+ T cells and lymphoid tissue viral burden distinguish progressive and nonprogressive lentiviral infections. Blood 120: 4172-4181.
54. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
55. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, et al. (2008) Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112: 2826-2835.
56. Beaumier CM, Harris LD, Goldstein S, Klatt NR, Whitted S, et al. (2009) CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat Med 15: 879-885.
57. Sundaravaradan V, Saleem R, Micci L, Gasper MA, Ortiz AM, et al. (2013) Multifunctional Double-negative T Cells in Sooty Mangabeys Mediate T-helper Functions Irrespective of SIV Infection. PLoS Pathog 9: e1003441.
58. Milush JM, Mir KD, Sundaravaradan V, Gordon SN, Engram J, et al. (2011) Lack of clinical AIDS in SIV-infected sooty mangabeys with significant CD4+ T cell loss is associated with double-negative T cells. J Clin Invest 121: 1102-1110.
59. Lamoreaux L, Roederer M, Koup R, (2006) Intracellular cytokine optimization and standard operating procedure. Nat Protoc 1: 1507-1516.