Type I IFN - A blunt spear in fighting HIV-1 infection

Cytokine and Growth Factor Reviews

Volumn 26, Issue 2, 2015, Pages 143-158

  Acchioni, Chiara ^a   Marsili, Giulia ^a   Perrotti, Edvige ^a   Remoli, Anna Lisa ^a   Sgarbanti, Marco ^a   Battistini, Angela ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

HIV 1; HIV 1 immune activation; Innate immune sensing; Interferon Regulatory Factors; Type I interferon

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; INTERFERON; INTERFERON REGULATORY FACTOR; MEMBRANE PROTEIN; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; MX2 PROTEIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; PROTEIN SAMHD1; SCHLAFEN 11; TETHERIN; TRANSCRIPTION FACTOR; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; VIRAL INTERFERON REGULATORY FACTORS; VIRUS PROTEIN;

CYTOKINE RESPONSE; DISEASE COURSE; HOST; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE EVASION; IMMUNOMODULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; INTERFERON PRODUCTION; MOLECULAR RECOGNITION; NONHUMAN; PATHOGENESIS; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; VIRUS REPLICATION; BIOSYNTHESIS; COMPLICATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOGENICITY; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

DISEASE PROGRESSION; HIV INFECTIONS; HIV-1; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; INFLAMMATION; INTERFERON REGULATORY FACTORS; INTERFERON TYPE I; PATHOGEN-ASSOCIATED MOLECULAR PATTERN MOLECULES; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84926460347     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2014.10.004     Document Type: Review

References (172)

1. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005, 5:375-386.
2. Kalliolias G.D., Ivashkiv L.B. Overview of the biology of type I interferons. Arthrit Res Ther 2010, 12(Suppl. 1):S1.
3. Blasius A.L., Beutler B. Intracellular Toll-like receptors. Immunity 2010, 32:305-315.
4. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
5. Elinav E., Strowig T., Henao-Mejia J., Flavell R.A. Regulation of the antimicrobial response by NLR proteins. Immunity 2011, 34:665-679.
6. Sancho D., Reis e Sousa C. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 2012, 30:491-529.
7. Paludan S.R., Bowie A.G. Immune sensing of DNA. Immunity 2013, 38:870-880.
8. Wu J., Chen Z.J. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 2014, 32:461-488.
9. Xiao T.S., Fitzgerald K.A. The cGAS-STING pathway for DNA sensing. Mol Cell 2013, 51:135-139.
10. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006, 124:783-801.
11. Stetson D.B., Medzhitov R. Type I interferons in host defense. Immunity 2006, 25:373-381.
12. Samarajiwa S.A., Forster S., Auchettl K., Hertzog P.J. INTERFEROME: the database of interferon regulated genes. Nucleic Acids Res 2009, 37:D852-D857.
13. Eisele E., Siliciano R.F. Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity 2012, 37:377-388.
14. Battistini A., Sgarbanti M. HIV-1 latency: an update of molecular mechanisms and therapeutic strategies. Viruses 2014, 6:1715-1758.
15. Iwasaki A. A virological view of innate immune recognition. Annu Rev Microbiol 2012, 66:177-196.
16. Rustagi A., Gale M. Innate antiviral immune signaling, viral evasion and modulation by HIV-1. J Mol Biol 2014, 426:1161-1177.
17. Malim M.H., Bieniasz P.D. HIV restriction factors and mechanisms of evasion. Cold Spring Harb Perspect Med 2012, 2:a006940.
18. van Montfoort N., Olagnier D., Hiscott J. Unmasking immune sensing of retroviruses: interplay between innate sensors and host effectors. Cytok Growth Factor Rev 2014, 10.1016/j.cytogfr.2014.08.006.
19. Towers G.J., Noursadeghi M. Interactions between HIV-1 and the cell-autonomous innate immune system. Cell Host Microbe 2014, 16:10-18.
20. von Sydow M., Sonnerborg A., Gaines H., Strannegard O. Interferon-alpha and tumor necrosis factor-alpha in serum of patients in various stages of HIV-1 infection. AIDS Res Hum Retroviruses 1991, 7:375-380.
21. Beignon A.S., McKenna K., Skoberne M., Manches O., DaSilva I., Kavanagh D.G., et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 2005, 115:3265-3275.
22. Fonteneau J.F., Larsson M., Beignon A.S., McKenna K., Dasilva I., Amara A., et al. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol 2004, 78:5223-5232.
23. Lepelley A., Louis S., Sourisseau M., Law H.K., Pothlichet J., Schilte C., et al. Innate sensing of HIV-infected cells. PLoS Pathog 2011, 7:e1001284.
24. Manches O., Frleta D., Bhardwaj N. Dendritic cells in progression and pathology of HIV infection. Trends Immunol 2014, 35:114-122.
25. Hrecka K., Hao C., Gierszewska M., Swanson S.K., Kesik-Brodacka M., Srivastava S., et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011, 474:658-661.
26. Laguette N., Sobhian B., Casartelli N., Ringeard M., Chable-Bessia C., Segeral E., et al. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 2011, 474:654-657.
27. Gao D., Wu J., Wu Y.T., Du F., Aroh C., Yan N., et al. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 2013, 341:903-906.
28. Li X.D., Wu J., Gao D., Wang H., Sun L., Chen Z.J. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013, 341:1390-1394.
29. Sun L., Wu J., Du F., Chen X., Chen Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339:786-791.
30. Puigdomenech I., Casartelli N., Porrot F., Schwartz O. SAMHD1 restricts HIV-1 cell-to-cell transmission and limits immune detection in monocyte-derived dendritic cells. J Virol 2013, 87:2846-2856.
31. Su B., Biedma M.E., Lederle A., Peressin M., Lambotin M., Proust A., et al. Dendritic cell-lymphocyte cross talk downregulates host restriction factor SAMHD1 and stimulates HIV-1 replication in dendritic cells. J Virol 2014, 88:5109-5121.
32. Granelli-Piperno A., Golebiowska A., Trumpfheller C., Siegal F.P., Steinman R.M. HIV-1-infected monocyte-derived dendritic cells do not undergo maturation but can elicit IL-10 production and T cell regulation. Proc Natl Acad Sci U S A 2004, 101:7669-7674.
33. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., et al. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
34. Gringhuis S.I., van der Vlist M., van den Berg L.M., den Dunnen J., Litjens M., Geijtenbeek T.B. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat Immunol 2010, 11:419-426.
35. Guo H., Gao J., Taxman D.J., Ting J.P., Su L. HIV-1 infection induces IL-1beta production via TLR8-dependent and NLRP3-inflammasome mechanisms in human monocytes. J Biol Chem 2014, 289:21716-21726.
36. Chattergoon M.A., Latanich R., Quinn J., Winter M.E., Buckheit R.W., Blankson J.N., et al. HIV and HCV activate the inflammasome in monocytes and macrophages via endosomal Toll-like receptors without induction of type 1 interferon. PLoS Pathog 2014, 10:e1004082.
37. Berg R.K., Melchjorsen J., Rintahaka J., Diget E., Soby S., Horan K.A., et al. Genomic HIV RNA induces innate immune responses through RIG-I-dependent sensing of secondary-structured RNA. PLoS ONE 2012, 7:e29291.
38. Solis M., Nakhaei P., Jalalirad M., Lacoste J., Douville R., Arguello M., et al. RIG-I-mediated antiviral signaling is inhibited in HIV-1 infection by a protease-mediated sequestration of RIG-I. J Virol 2011, 85:1224-1236.
39. Ryoo J., Choi J., Oh C., Kim S., Seo M., Kim S.Y., et al. The ribonuclease activity of SAMHD1 is required for HIV-1 restriction. Nat Med 2014, 20:936-941.
40. Jakobsen M.R., Bak R.O., Andersen A., Berg R.K., Jensen S.B., Tengchuan J., et al. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci U S A 2013, 110:E4571-E4580.
41. Yan N., Regalado-Magdos A.D., Stiggelbout B., Lee-Kirsch M.A., Lieberman J. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 2010, 11:1005-1013.
42. Pereira-Lopes S., Celhar T., Sans-Fons G., Serra M., Fairhurst A.M., Lloberas J., et al. The exonuclease Trex1 restrains macrophage proinflammatory activation. J Immunol 2013, 191:6128-6135.
43. Nissen S.K., Hojen J.F., Andersen K.L., Kofod-Olsen E., Berg R.K., Paludan S.R., et al. Innate DNA sensing is impaired in HIV patients and IFI16 expression correlates with chronic immune activation. Clin Exp Immunol 2014, 177:295-309.
44. Thompson M.R., Sharma S., Atianand M., Jensen S.B., Carpenter S., Knipe D.M., et al. Interferon Gamma Inducible protein (IFI)16 transcriptionally regulates type I interferons and other interferon stimulated genes and controls the interferon response to both DNA and RNA viruses. J Biol Chem 2014, 289:23568-23581.
45. Manel N., Hogstad B., Wang Y., Levy D.E., Unutmaz D., Littman D.R. A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 2010, 467:214-217.
46. Lahaye X., Satoh T., Gentili M., Cerboni S., Conrad C., Hurbain I., et al. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity 2013, 39:1132-1142.
47. Rasaiyaah J., Tan C.P., Fletcher A.J., Price A.J., Blondeau C., Hilditch L., et al. HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature 2013, 503:402-405.
48. Pertel T., Hausmann S., Morger D., Zuger S., Guerra J., Lascano J., et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365.
49. Zhao G., Ke D., Vu T., Ahn J., Shah V.B., Yang R., et al. Rhesus TRIM5alpha disrupts the HIV-1 capsid at the inter-hexamer interfaces. PLoS Pathog 2011, 7:e1002009.
50. Doehle B.P., Hladik F., McNevin J.P., McElrath M.J., Gale M. Human immunodeficiency virus type 1 mediates global disruption of innate antiviral signaling and immune defenses within infected cells. J Virol 2009, 83:10395-10405.
51. Okumura A., Alce T., Lubyova B., Ezelle H., Strebel K., Pitha P.M. HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 2008, 373:85-97.
52. Baldauf H.M., Pan X., Erikson E., Schmidt S., Daddacha W., Burggraf M., et al. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat Med 2012, 18:1682-1687.
53. Descours B., Cribier A., Chable-Bessia C., Ayinde D., Rice G., Crow Y., et al. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 2012, 9:87.
54. Doitsh G., Cavrois M., Lassen K.G., Zepeda O., Yang Z., Santiago M.L., et al. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 2010, 143:789-801.
55. Monroe K.M., Yang Z., Johnson J.R., Geng X., Doitsh G., Krogan N.J., et al. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 2014, 343:428-432.
56. Doitsh G., Galloway N.L., Geng X., Yang Z., Monroe K.M., Zepeda O., et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014, 505:509-514.
57. Honda K., Taniguchi T. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 2006, 6:644-658.
58. Marsili G., Remoli A.L., Sgarbanti M., Perrotti E., Fragale A., Battistini A. HIV-1, interferon and the interferon regulatory factor system: an interplay between induction, antiviral responses and viral evasion. Cytok Growth Factor Rev 2012, 23:255-270.
59. Remoli ALM G., Sgarbant M., Perrotti E., Fragale A., Orsatti R., Battistini A. HIV-1 targeting of IFN regulatory factors. Fut Virol 2011, 6:1397-1405.
60. Battistini A. Interferon regulatory factors in immune cell development and host response to infection 2012, Nova Science Publishers, Inc.
61. Battistini A. Interferon regulatory factors in hematopoietic cell differentiation and immune regulation. J Interf Cytok Res 2009, 29:765-779.
62. Taniguchi T., Ogasawara K., Takaoka A., Tanaka N. IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 2001, 19:623-655.
63. Savitsky D., Tamura T., Yanai H., Taniguchi T. Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunol Immunother: CII 2010, 59:489-510.
64. Doehle B.P., Chang K., Fleming L., McNevin J., Hladik F., McElrath M.J., et al. Vpu-deficient HIV strains stimulate innate immune signaling responses in target cells. J Virol 2012, 86:8499-8506.
65. Hotter D., Kirchhoff F., Sauter D. HIV-1 Vpu does not degrade interferon regulatory factor 3. J Virol 2013, 87:7160-7165.
66. Sgarbanti M., Marsili G., Remoli A.L., Stellacci E., Mai A., Rotili D., et al. IkappaB kinase epsilon targets interferon regulatory factor 1 in activated T lymphocytes. Mol Cell Biol 2014, 34:1054-1065.
67. Chang J., Lindsay R.J., Kulkarni S., Lifson J.D., Carrington M., Altfeld M. Polymorphisms in interferon regulatory factor 7 reduce interferon-alpha responses of plasmacytoid dendritic cells to HIV-1. AIDS 2011, 25:715-717.
68. Harman A.N., Lai J., Turville S., Samarajiwa S., Gray L., Marsden V., et al. HIV infection of dendritic cells subverts the IFN induction pathway via IRF-1 and inhibits type 1 IFN production. Blood 2011, 118:298-308.
69. Sivro A., Su R.C., Plummer F.A., Ball T.B. HIV and interferon regulatory factor 1: a story of manipulation and control. AIDS Res Hum Retroviruses 2013, 29:1428-1433.
70. Sgarbanti M., Borsetti A., Moscufo N., Bellocchi M.C., Ridolfi B., Nappi F., et al. Modulation of human immunodeficiency virus 1 replication by interferon regulatory factors. J Exp Med 2002, 195:1359-1370.
71. Sgarbanti M., Remoli A.L., Marsili G., Ridolfi B., Borsetti A., Perrotti E., et al. IRF-1 is required for full NF-kappaB transcriptional activity at the human immunodeficiency virus type 1 long terminal repeat enhancer. J Virol 2008, 82:3632-3641.
72. el Kharroubi A., Martin M.A. cis-acting sequences located downstream of the human immunodeficiency virus type 1 promoter affect its chromatin structure and transcriptional activity. Mol Cell Biol 1996, 16:2958-2966.
73. Battistini A., Marsili G., Sgarbanti M., Ensoli B., Hiscott J. IRF regulation of HIV-1 long terminal repeat activity. J Interferon Cytok Res: Off J Int Soc Interferon Cytok Res 2002, 22:27-37.
74. Marsili G., Remoli A.L., Sgarbanti M., Battistini A. Role of acetylases and deacetylase inhibitors in IRF-1-mediated HIV-1 long terminal repeat transcription. Ann NY Acad Sci 2004, 1030:636-643.
75. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
76. Schoggins J.W., MacDuff D.A., Imanaka N., Gainey M.D., Shrestha B., Eitson J.L., et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 2014, 505:691-695.
77. Remoli A.L., Marsili G., Perrotti E., Gallerani E., Ilari R., Nappi F., et al. Intracellular HIV-1 Tat protein represses constitutive LMP2 transcription increasing proteasome activity by interfering with the binding of IRF-1 to STAT1. Biochem J 2006, 396:371-380.
78. Castaldello A., Sgarbanti M., Marsili G., Brocca-Cofano E., Remoli A.L., Caputo A., et al. Interferon regulatory factor-1 acts as a powerful adjuvant in tat DNA based vaccination. J Cell Physiol 2010, 224:702-709.
79. Cheng X., Ratner L. HIV-2 Vpx protein interacts with interferon regulatory factor 5 (IRF5) and inhibits its function. J Biol Chem 2014, 289:9146-9157.
80. Schoenemeyer A., Barnes B.J., Mancl M.E., Latz E., Goutagny N., Pitha P.M., et al. The interferon regulatory factor, IRF5, is a central mediator of Toll-like receptor 7 signaling. J Biol Chem 2005, 280:17005-17012.
81. Munier S., Delcroix-Genete D., Carthagena L., Gumez A., Hazan U. Characterization of two candidate genes, NCoA3 and IRF8, potentially involved in the control of HIV-1 latency. Retrovirology 2005, 2:73.
82. Strebel K. HIV accessory proteins versus host restriction factors. Curr Opin Virol 2013, 3:692-699.
83. Neil S., Bieniasz P. Human immunodeficiency virus, restriction factors, and interferon. J Interferon Cytok Res: Off J Int Soc Interferon Cytok Res 2009, 29:569-580.
84. Desimmie B.A., Delviks-Frankenberrry K.A., Burdick R.C., Qi D., Izumi T., Pathak V.K. Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J Mol Biol 2014, 426:1220-1245.
85. Swiecki M., Omattage N.S., Brett T.J. BST-2/tetherin: structural biology, viral antagonism, and immunobiology of a potent host antiviral factor. Mol Immunol 2013, 54:132-139.
86. Sze A., Olagnier D., Lin R., van Grevenynghe J., Hiscott J. SAMHD1 host restriction factor: a link with innate immune sensing of retrovirus infection. J Mol Biol 2013, 425:4981-4994.
87. Rahm N., Telenti A. The role of tripartite motif family members in mediating susceptibility to HIV-1 infection. Curr Opin HIV AIDS 2012, 7:180-186.
88. Goujon C., Moncorge O., Bauby H., Doyle T., Ward C.C., Schaller T., et al. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 2013, 502:559-562.
89. Jakobsen M.R., Mogensen T.H., Paludan S.R. Caught in translation: innate restriction of HIV mRNA translation by a schlafen family protein. Cell Res 2013, 23:320-322.
90. Sheehy A.M., Gaddis N.C., Choi J.D., Malim M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650.
91. Sheehy A.M., Gaddis N.C., Malim M.H. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 2003, 9:1404-1407.
92. Mariani R., Chen D., Schrofelbauer B., Navarro F., Konig R., Bollman B., et al. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 2003, 114:21-31.
93. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
94. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., et al. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252.
95. Sauter D. Counteraction of the multifunctional restriction factor tetherin. Front Microbiol 2014, 5:163.
96. Perez-Caballero D., Zang T., Ebrahimi A., McNatt M.W., Gregory D.A., Johnson M.C., et al. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 2009, 139:499-511.
97. Cao W., Bover L., Cho M., Wen X., Hanabuchi S., Bao M., et al. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J Exp Med 2009, 206:1603-1614.
98. Strebel K., Klimkait T., Martin M.A. A novel gene of HIV-1, vpu, and its 16-kilodalton product. Science 1988, 241:1221-1223.
99. Jolly C., Booth N.J., Neil S.J. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J Virol 2010, 84:12185-12199.
100. Cohen E.A., Terwilliger E.F., Sodroski J.G., Haseltine W.A. Identification of a protein encoded by the vpu gene of HIV-1. Nature 1988, 334:532-534.
101. Theodore T.S., Englund G., Buckler-White A., Buckler C.E., Martin M.A., Peden K.W. Construction and characterization of a stable full-length macrophage-tropic HIV type 1 molecular clone that directs the production of high titers of progeny virions. AIDS Res Hum Retroviruses 1996, 12:191-194.
102. Giese S., Marsh M. Tetherin can restrict cell-free and cell-cell transmission of HIV from primary macrophages to T cells. PLoS Pathog 2014, 10:e1004189.
103. Goujon C., Arfi V., Pertel T., Luban J., Lienard J., Rigal D., et al. Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J Virol 2008, 82:12335-12345.
104. Goujon C., Riviere L., Jarrosson-Wuilleme L., Bernaud J., Rigal D., Darlix J.L., et al. SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 2007, 4:2.
105. Lahouassa H., Daddacha W., Hofmann H., Ayinde D., Logue E.C., Dragin L., et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 2012, 13:223-228.
106. White T.E., Brandariz-Nunez A., Valle-Casuso J.C., Amie S., Nguyen L.A., Kim B., et al. The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation. Cell Host Microbe 2013, 13:441-451.
107. Welbourn S., Dutta S.M., Semmes O.J., Strebel K. Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1. J Virol 2013, 87:11516-11524.
108. Cribier A., Descours B., Valadao A.L., Laguette N., Benkirane M. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep 2013, 3:1036-1043.
109. Rice G.I., Bond J., Asipu A., Brunette R.L., Manfield I.W., Carr I.M., et al. Mutations involved in Aicardi-Goutieres syndrome implicate SAMHD1 as regulator of the innate immune response. Nat Genet 2009, 41:829-832.
110. Crow Y.J., Rehwinkel J. Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum Mol Genet 2009, 18:R130-R136.
111. Crow Y.J., Hayward B.E., Parmar R., Robins P., Leitch A., Ali M., et al. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat Genet 2006, 38:917-920.
112. Laguette N., Bregnard C., Hue P., Basbous J., Yatim A., Larroque M., et al. Premature activation of the SLX4 complex by Vpr promotes G2/M arrest and escape from innate immune sensing. Cell 2014, 156:134-145.
113. Fletcher A.J., Towers G.J. Inhibition of retroviral replication by members of the TRIM protein family. Curr Top Microbiol Immunol 2013, 371:29-66.
114. Hatziioannou T., Princiotta M., Piatak M., Yuan F., Zhang F., Lifson J.D., et al. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 2006, 314:95.
115. Kutluay S.B., Perez-Caballero D., Bieniasz P.D. Fates of retroviral core components during unrestricted and TRIM5-restricted infection. PLoS Pathog 2013, 9:e1003214.
116. Kane M., Yadav S.S., Bitzegeio J., Kutluay S.B., Zang T., Wilson S.J., et al. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 2013, 502:563-566.
117. Liu Z., Pan Q., Ding S., Qian J., Xu F., Zhou J., et al. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 2013, 14:398-410.
118. Goujon C., Moncorge O., Bauby H., Doyle T., Barclay W.S., Malim M.H. Transfer of the amino-terminal nuclear envelope targeting domain of human MX2 converts MX1 into an HIV-1 resistance factor. J Virol 2014, 88:9017-9026.
119. Li M., Kao E., Gao X., Sandig H., Limmer K., Pavon-Eternod M., et al. Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature 2012, 491:125-128.
120. Moir S., Chun T.W., Fauci A.S. Pathogenic mechanisms of HIV disease. Annu Rev Pathol 2011, 6:223-248.
121. Deeks S.G., Tracy R., Douek D.C. Systemic effects of inflammation on health during chronic HIV infection. Immunity 2013, 39:633-645.
122. Hunt P.W. HIV and inflammation: mechanisms and consequences. Curr HIV/AIDS Rep 2012, 9:139-147.
123. Klatt N.R., Chomont N., Douek D.C., Deeks S.G. Immune activation and HIV persistence: implications for curative approaches to HIV infection. Immunol Rev 2013, 254:326-342.
124. Seddiki N., Brezar V., Draenert R. Cell exhaustion in HIV-1 infection: role of suppressor cells. Curr Opin HIV AIDS 2014, 9:452-458.
125. Sandler N.G., Douek D.C. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 2012, 10:655-666.
126. Benecke A., Gale M., Katze M.G. Dynamics of innate immunity are key to chronic immune activation in AIDS. Curr Opin HIV AIDS 2012, 7:79-85.
127. Boasso A., Type I. Interferon at the Interface of Antiviral Immunity and Immune Regulation: The Curious Case of HIV-1. Scientifica 2013, 2013:580968.
128. d'Ettorre G., Paiardini M., Ceccarelli G., Silvestri G., Vullo V. HIV-associated immune activation: from bench to bedside. AIDS Res Hum Retroviruses 2011, 27:355-364.
129. Bosinger S.E., Li Q., Gordon S.N., Klatt N.R., Duan L., Xu L., et al. Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 2009, 119:3556-3572.
130. Jacquelin B., Mayau V., Targat B., Liovat A.S., Kunkel D., Petitjean G., et al. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 2009, 119:3544-3555.
131. Jacquelin B., Petitjean G., Kunkel D., Liovat A.S., Jochems S.P., Rogers K.A., et al. Innate immune responses and rapid control of inflammation in African Green Monkeys treated or not with interferon-alpha during primary SIVagm infection. PLoS Pathog 2014, 10:e1004241.
132. Boasso A., Shearer G.M. Chronic innate immune activation as a cause of HIV-1 immunopathogenesis. Clin Immunol 2008, 126:235-242.
133. Rotger M., Dang K.K., Fellay J., Heinzen E.L., Feng S., Descombes P., et al. Genome-wide mRNA expression correlates of viral control in CD4+ T-cells from HIV-1-infected individuals. PLoS Pathog 2010, 6:e1000781.
134. Rotger M., Dalmau J., Rauch A., McLaren P., Bosinger S.E., Martinez R., et al. Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. J Clin Invest 2011, 121:2391-2400.
135. Haase A.T. Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu Rev Med 2011, 62:127-139.
136. Borrow P. Innate immunity in acute HIV-1 infection. Curr Opin HIV AIDS 2011, 6:353-363.
137. Lehmann C., Lafferty M., Garzino-Demo A., Jung N., Hartmann P., Fatkenheuer G., et al. Plasmacytoid dendritic cells accumulate and secrete interferon alpha in lymph nodes of HIV-1 patients. PLoS ONE 2010, 5:e11110.
138. Herbeuval J.P., Nilsson J., Boasso A., Hardy A.W., Kruhlak M.J., Anderson S.A., et al. Differential expression of IFN-alpha and TRAIL/DR5 in lymphoid tissue of progressor versus nonprogressor HIV-1-infected patients. Proc Natl Acad Sci U S A 2006, 103:7000-7005.
139. Lehmann C., Harper J.M., Taubert D., Hartmann P., Fatkenheuer G., Jung N., et al. Increased interferon alpha expression in circulating plasmacytoid dendritic cells of HIV-1-infected patients. J Acquir Immune Defic Syndr 2008, 48:522-530.
140. Zeng M., Smith A.J., Wietgrefe S.W., Southern P.J., Schacker T.W., Reilly C.S., et al. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J Clin Invest 2011, 121:998-1008.
141. Sandler N.G., Bosinger S.E., Estes J.D., Zhu R.T., Tharp G.K., Boritz E., et al. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 2014, 511:601-615.
142. O'Brien M., Manches O., Bhardwaj N. Plasmacytoid dendritic cells in HIV infection. Adv Exp Med Biol 2013, 762:71-107.
143. O'Brien M., Manches O., Sabado R.L., Baranda S.J., Wang Y., Marie I., et al. Spatiotemporal trafficking of HIV in human plasmacytoid dendritic cells defines a persistently IFN-alpha-producing and partially matured phenotype. J Clin Invest 2011, 121:1088-1101.
144. Nascimbeni M., Perie L., Chorro L., Diocou S., Kreitmann L., Louis S., et al. Plasmacytoid dendritic cells accumulate in spleens from chronically HIV-infected patients but barely participate in interferon-alpha expression. Blood 2009, 113:6112-6119.
145. Kader M., Smith A.P., Guiducci C., Wonderlich E.R., Normolle D., Watkins S.C., et al. Blocking TLR7- and TLR9-mediated IFN-alpha production by plasmacytoid dendritic cells does not diminish immune activation in early SIV infection. PLoS Pathog 2013, 9:e1003530.
146. Gougeon M.L., Piacentini M. New insights on the role of apoptosis and autophagy in HIV pathogenesis. Apoptosis: Int J Program Cell Death 2009, 14:501-508.
147. Herbeuval J.P., Shearer G.M. HIV-1 immunopathogenesis: how good interferon turns bad. Clin Immunol 2007, 123:121-128.
148. Dyrhol-Riise A.M., Stent G., Rosok B.I., Voltersvik P., Olofsson J., Asjo B. The Fas/FasL system and T cell apoptosis in HIV-1-infected lymphoid tissue during highly active antiretroviral therapy. Clin Immunol 2001, 101:169-179.
149. Cummins N.W., Badley A.D. Mechanisms of HIV-associated lymphocyte apoptosis: 2010. Cell Death Dis 2010, 1:e99.
150. Huang Y., Walstrom A., Zhang L., Zhao Y., Cui M., Ye L., et al. Type I interferons and interferon regulatory factors regulate TNF-related apoptosis-inducing ligand (TRAIL) in HIV-1-infected macrophages. PLoS ONE 2009, 4:e5397.
151. Herbeuval J.P., Grivel J.C., Boasso A., Hardy A.W., Chougnet C., Dolan M.J., et al. CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 2005, 106:3524-3531.
152. Zhang Z., Xu X., Lu J., Zhang S., Gu L., Fu J., et al. B and T lymphocyte attenuator down-regulation by HIV-1 depends on type I interferon and contributes to T-cell hyperactivation. J Infect Dis 2011, 203:1668-1678.
153. Riella L.V., Paterson A.M., Sharpe A.H., Chandraker A. Role of the PD-1 pathway in the immune response. Am J Transpl: Off J Am Soc Transpl Am Soc Transpl Surg 2012, 12:2575-2587.
154. Kulpa D.A., Lawani M., Cooper A., Peretz Y., Ahlers J., Sekaly R.P. PD-1 coinhibitory signals: the link between pathogenesis and protection. Semin Immunol 2013, 25:219-227.
155. Meier A., Bagchi A., Sidhu H.K., Alter G., Suscovich T.J., Kavanagh D.G., et al. Upregulation of PD-L1 on monocytes and dendritic cells by HIV-1 derived TLR ligands. AIDS 2008, 22:655-658.
156. Day C.L., Kaufmann D.E., Kiepiela P., Brown J.A., Moodley E.S., Reddy S., et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006, 443:350-354.
157. Trautmann L., Janbazian L., Chomont N., Said E.A., Gimmig S., Bessette B., et al. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med 2006, 12:1198-1202.
158. Porichis F., Kaufmann D.E. Role of PD-1 in HIV pathogenesis and as target for therapy. Curr HIV/AIDS Rep 2012, 9:81-90.
159. Demoulins T., Abdallah A., Kettaf N., Baron M.L., Gerarduzzi C., Gauchat D., et al. Reversible blockade of thymic output: an inherent part of TLR ligand-mediated immune response. J Immunol 2008, 181:6757-6769.
160. Tough D.F., Borrow P., Sprent J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 1996, 272:1947-1950.
161. Okoye A., Meier-Schellersheim M., Brenchley J.M., Hagen S.I., Walker J.M., Rohankhedkar M., et al. Progressive CD4+ central memory T cell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 2007, 204:2171-2185.
162. Sedaghat A.R., German J., Teslovich T.M., Cofrancesco J., Jie C.C., Talbot C.C., et al. 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 2008, 82:1870-1883.
163. Crawford A., Angelosanto J.M., Kao C., Doering T.A., Odorizzi P.M., Barnett B.E., et al. Molecular and transcriptional basis of CD4(+) T cell dysfunction during chronic infection. Immunity 2014, 40:289-302.
164. Manches O., Munn D., Fallahi A., Lifson J., Chaperot L., Plumas J., et al. HIV-activated human plasmacytoid DCs induce Tregs through an indoleamine 2,3-dioxygenase-dependent mechanism. J Clin Invest 2008, 118:3431-3439.
165. Munn D.H., Sharma M.D., Baban B., Harding H.P., Zhang Y., Ron D., et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 2005, 22:633-642.
166. Brenchley J.M., Paiardini M., Knox K.S., Asher A.I., Cervasi B., Asher T.E., et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008, 112:2826-2835.
167. Baban B., Chandler P.R., Sharma M.D., Pihkala J., Koni P.A., Munn D.H., et al. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 2009, 183:2475-2483.
168. Kanwar B., Favre D., McCune J.M. Th17 and regulatory T cells: implications for AIDS pathogenesis. Curr Opin HIV AIDS 2010, 5:151-157.
169. Stoddart C.A., Keir M.E., McCune J.M. IFN-alpha-induced upregulation of CCR5 leads to expanded HIV tropism in vivo. PLoS Pathog 2010, 6:e1000766.
170. Di Domizio J., Cao W. Fueling autoimmunity: type I interferon in autoimmune diseases. Exp Rev Clin Immunol 2013, 9:201-210.
171. Hall J.C., Rosen A. Type I interferons: crucial participants in disease amplification in autoimmunity. Nat Rev Rheumatol 2010, 6:40-49.
172. Whitney J.B., Hill A.L., Sanisetty S., Penaloza-MacMaster P., Liu J., Shetty M., et al. Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys. Nature 2014, 512:74-77.