Innate immune sensing of retroviral infection via Toll-like receptor 7 occurs upon viral entry

Immunity

Volumn 35, Issue 1, 2011, Pages 135-145

  Kane, Melissa ^a   Case, Laure K ^a,b   Wang, Christine ^a   Yurkovetskiy, Leonid ^a   Dikiy, Stanislav ^a   Golovkina, Tatyana V ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 7; MYELOID DIFFERENTIATION FACTOR 88; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 7;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENDOSOME; FEMALE; HUMORAL IMMUNITY; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS INFECTION; VIRION; VIRUS ENTRY; VIRUS INACTIVATION; VIRUS RESISTANCE;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CELLS, CULTURED; DISEASE SUSCEPTIBILITY; ENDOSOMES; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERFERON TYPE I; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED STRAINS; MYELOID DIFFERENTIATION FACTOR 88; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7; VIRUS INTERNALIZATION;

EID: 79960466171     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.05.011     Document Type: Article

References (67)

1. Adachi O., Kawai T., Takeda K., Matsumoto M., Tsutsui H., Sakagami M., Nakanishi K., Akira S. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998, 9:143-150.
2. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
3. Ammann C.G., Messer R.J., Peterson K.E., Hasenkrug K.J. Lactate dehydrogenase-elevating virus induces systemic lymphocyte activation via TLR7-dependent IFNalpha responses by plasmacytoid dendritic cells. PLoS ONE 2009, 4:e6105.
4. Andreadis S., Lavery T., Davis H.E., Le Doux J.M., Yarmush M.L., Morgan J.R. Toward a more accurate quantitation of the activity of recombinant retroviruses: alternatives to titer and multiplicity of infection. J. Virol. 2000, 74:3431-3439.
5. Beignon A.S., McKenna K., Skoberne M., Manches O., DaSilva I., Kavanagh D.G., Larsson M., Gorelick R.J., Lifson J.D., Bhardwaj N. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J. Clin. Invest. 2005, 115:3265-3275.
6. Bender A., Bui L.K., Feldman M.A., Larsson M., Bhardwaj N. Inactivated influenza virus, when presented on dendritic cells, elicits human CD8+ cytolytic T cell responses. J. Exp. Med. 1995, 182:1663-1671.
7. Bhoj V.G., Sun Q., Bhoj E.J., Somers C., Chen X., Torres J.P., Mejias A., Gomez A.M., Jafri H., Ramilo O., Chen Z.J. MAVS and MyD88 are essential for innate immunity but not cytotoxic T lymphocyte response against respiratory syncytial virus. Proc. Natl. Acad. Sci. USA 2008, 105:14046-14051.
8. Boeke J.D., Stoye J.P. Retrotransposons, endogenous retroviruses, and the evolution. Retroviruses 1997, 343-436. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. J.M. Coffin, S.H. Hughes, H.E. Varmus (Eds.).
9. Bowerman B., Brown P.O., Bishop J.M., Varmus H.E. A nucleoprotein complex mediates the integration of retroviral DNA. Genes Dev. 1989, 3:469-478.
10. Browne E.P., Littman D.R. Myd88 is required for an antibody response to retroviral infection. PLoS Pathog. 2009, 5:e1000298.
11. Buggiano V., Goldman A., Nepomnaschy I., Bekinschtein P., Berguer P., Lombardi G., Deroche A., Francisco M.V., Piazzon I. Characterization of two infectious mouse mammary tumour viruses: Superantigenicity and tumorigenicity. Scand. J. Immunol. 1999, 49:269-277.
12. Case L.K., Purdy A., Golovkina T.V. Molecular and cellular basis of the retrovirus resistance in I/LnJ mice. J. Immunol. 2005, 175:7543-7549.
13. Case L.K., Petell L., Yurkovetskiy L., Purdy A., Savage K.J., Golovkina T.V. Replication of beta- and gammaretroviruses is restricted in I/LnJ mice via the same genetic mechanism. J. Virol. 2008, 82:1438-1447.
14. Chesebro B., Miyazawa M., Britt W.J. Host genetic control of spontaneous and induced immunity to Friend murine retrovirus infection. Annu. Rev. Immunol. 1990, 8:477-499.
15. Choi Y., Kappler J.W., Marrack P. A superantigen encoded in the open reading frame of the 3′ long terminal repeat of mouse mammary tumour virus. Nature 1991, 350:203-207.
16. Cloyd M.W., Hartley J.W., Rowe W.P. Lymphomagenicity of recombinant mink cell focus-inducing murine leukemia viruses. J. Exp. Med. 1980, 151:542-552.
17. Coffin J.M. Retroviridae and their replication. Virology 1990, 1437-1500. Raven Press, New York. B.N. Fields, D.M. Knipe (Eds.).
18. Deeks S.G., Walker B.D. Human immunodeficiency virus controllers: Mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 2007, 27:406-416.
19. Diebold S.S., Kaisho T., Hemmi H., Akira S., Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303:1529-1531.
20. Dittmer U., He H., Messer R.J., Schimmer S., Olbrich A.R., Ohlen C., Greenberg P.D., Stromnes I.M., Iwashiro M., Sakaguchi S., et al. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity 2004, 20:293-303.
21. Edelmann K.H., Richardson-Burns S., Alexopoulou L., Tyler K.L., Flavell R.A., Oldstone M.B. Does Toll-like receptor 3 play a biological role in virus infections?. Virology 2004, 322:231-238.
22. Evans D.T., Desrosiers R.C. Immune evasion strategies of the primate lentiviruses. Immunol. Rev. 2001, 183:141-158.
23. Gerlach N., Schimmer S., Weiss S., Kalinke U., Dittmer U. Effects of type I interferons on Friend retrovirus infection. J. Virol. 2006, 80:3438-3444.
24. Golovkina T.V. A novel mechanism of resistance to mouse mammary tumor virus infection. J. Virol. 2000, 74:2752-2759.
25. Golovkina T.V., Chervonsky A., Prescott J.A., Janeway C.A., Ross S.R. The mouse mammary tumor virus envelope gene product is required for superantigen presentation to T cells. J. Exp. Med. 1994, 179:439-446.
26. Golovkina T.V., Dudley J.P., Jaffe A.B., Ross S.R. Mouse mammary tumor viruses with functional superantigen genes are selected during in vivo infection. Proc. Natl. Acad. Sci. USA 1995, 92:4828-4832.
27. Golovkina T.V., Piazzon I., Nepomnaschy I., Buggiano V., de Olano Vela M., Ross S.R. Generation of a tumorigenic milk-borne mouse mammary tumor virus by recombination between endogenous and exogenous viruses. J. Virol. 1997, 71:3895-3903.
28. Hardy A.W., Graham D.R., Shearer G.M., Herbeuval J.P. HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIV coreceptors by Toll-like receptor 7-induced IFN-alpha. Proc. Natl. Acad. Sci. USA 2007, 104:17453-17458.
29. Hasenkrug K.J., Valenzuela A., Letts V.A., Nishio J., Chesebro B., Frankel W.N. Chromosome mapping of Rfv3, a host resistance gene to Friend murine retrovirus. J. Virol. 1995, 69:2617-2620.
30. Heer A.K., Shamshiev A., Donda A., Uematsu S., Akira S., Kopf M., Marsland B.J. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J. Immunol. 2007, 178:2182-2191.
31. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., Horiuchi T., Tomizawa H., Takeda K., Akira S. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 2002, 3:196-200.
32. Hook L.M., Agafonova Y., Ross S.R., Turner S.J., Golovkina T.V. Genetics of mouse mammary tumor virus-induced mammary tumors: Linkage of tumor induction to the gag gene. J. Virol. 2000, 74:8876-8883.
33. Hook L.M., Jude B.A., Ter-Grigorov V.S., Hartley J.W., Morse H.C., Trainin Z., Toder V., Chervonsky A.V., Golovkina T.V. Characterization of a novel murine retrovirus mixture that facilitates hematopoiesis. J. Virol. 2002, 76:12112-12122.
34. Ichinohe T., Pang I.K., Iwasaki A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 2010, 11:404-410.
35. Iwasaki A., Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 2004, 5:987-995.
36. Johnson W.E., Desrosiers R.C. Viral persistence: HIV's strategies of immune system evasion. Annu. Rev. Med. 2002, 53:499-518.
37. Jude B.A., Pobezinskaya Y., Bishop J., Parke S., Medzhitov R.M., Chervonsky A.V., Golovkina T.V. Subversion of the innate immune system by a retrovirus. Nat. Immunol. 2003, 4:573-578.
38. Kane M., Case L.K., Golovkina T.V. Vital role for CD8+ cells in controlling retroviral infections. J. Virol. 2011, 85:3415-3423. Published online January 19, 2011.
39. Katen L.J., Januszeski M.M., Anderson W.F., Hasenkrug K.J., Evans L.H. Infectious entry by amphotropic as well as ecotropic murine leukemia viruses occurs through an endocytic pathway. J. Virol. 2001, 75:5018-5026.
40. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
41. Koyama S., Ishii K.J., Kumar H., Tanimoto T., Coban C., Uematsu S., Kawai T., Akira S. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J. Immunol. 2007, 179:4711-4720.
42. Lee H.K., Lund J.M., Ramanathan B., Mizushima N., Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007, 315:1398-1401.
43. Lund J.M., Alexopoulou L., Sato A., Karow M., Adams N.C., Gale N.W., Iwasaki A., Flavell R.A. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2004, 101:5598-5603.
44. MacDearmid C.C., Case L.K., Starling C.L., Golovkina T.V. Gradual elimination of retroviruses in YBR/Ei mice. J. Virol. 2006, 80:2206-2215.
45. Malim M.H., Emerman M. HIV-1 accessory proteins-Ensuring viral survival in a hostile environment. Cell Host Microbe 2008, 3:388-398.
46. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007, 449:819-826.
47. Medzhitov R., Janeway C.A. Innate immunity: The virtues of a nonclonal system of recognition. Cell 1997, 91:295-298.
48. Miyazawa M., Tsuji-Kawahara S., Kanari Y. Host genetic factors that control immune responses to retrovirus infections. Vaccine 2008, 26:2981-2996.
49. Müller U., Steinhoff U., Reis L.F., Hemmi S., Pavlovic J., Zinkernagel R.M., Aguet M. Functional role of type I and type II interferons in antiviral defense. Science 1994, 264:1918-1921.
50. Ogura H. XC cell fusion by murine leukemia viruses: Fusion from without. Med. Microbiol. Immunol. (Berl.) 1976, 162:175-181.
51. Pantaleo G., Fauci A.S. New concepts in the immunopathogenesis of HIV infection. Annu. Rev. Immunol. 1995, 13:487-512.
52. Piazzon I., Goldman A., Torello S., Nepomnaschy I., Deroche A., Dran G. Transmission of an Mls-1a-like superantigen to BALB/c mice by foster-nursing on F1 Mls-1bxa mothers. Sex-influenced onset of clonal deletion. J. Immunol. 1994, 153:1553-1562.
53. Purdy A., Case L., Duvall M., Overstrom-Coleman M., Monnier N., Chervonsky A., Golovkina T. Unique resistance of I/LnJ mice to a retrovirus is due to sustained interferon gamma-dependent production of virus-neutralizing antibodies. J. Exp. Med. 2003, 197:233-243.
54. Risser R., Horowitz J.M., McCubrey J. Endogenous mouse leukemia viruses. Annu. Rev. Genet. 1983, 17:85-121.
55. Rosenberg N., Jolicoeur P. Retroviral pathogenesis. Retroviruses 1997, 475-586. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. J.M. Coffin, S.H. Hughes, H.E. Varmus (Eds.).
56. Rowe W.P., Pugh W.E., Hartley J.W. Plaque assay techniques for murine leukemia viruses. Virology 1970, 42:1136-1139.
57. Santiago M.L., Montano M., Benitez R., Messer R.J., Yonemoto W., Chesebro B., Hasenkrug K.J., Greene W.C. Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection. Science 2008, 321:1343-1346.
58. Santiago M.L., Smith D.S., Barrett B.S., Montano M., Benitez R.L., Pelanda R., Hasenkrug K.J., Greene W.C. Persistent Friend virus replication and disease in Apobec3-deficient mice expressing functional B-cell-activating factor receptor. J. Virol. 2011, 85:189-199.
59. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., Nakaya T., Katsuki M., Noguchi S., Tanaka N., Taniguchi T. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13:539-548.
60. Schneider-Schaulies S., Dittmer U. Silencing T cells or T-cell silencing: Concepts in virus-induced immunosuppression. J. Gen. Virol. 2006, 87:1423-1438.
61. Shackleford G.M., Varmus H.E. Construction of a clonable, infectious, and tumorigenic mouse mammary tumor virus provirus and a derivative genetic vector. Proc. Natl. Acad. Sci. USA 1988, 85:9655-9659.
62. Stoye J.P., Moroni C., Coffin J.M. Virological events leading to spontaneous AKR thymomas. J. Virol. 1991, 65:1273-1285.
63. Super H.J., Hasenkrug K.J., Simmons S., Brooks D.M., Konzek R., Sarge K.D., Morimoto R.I., Jenkins N.A., Gilbert D.J., Copeland N.G., et al. Fine mapping of the friend retrovirus resistance gene, Rfv3, on mouse chromosome 15. J. Virol. 1999, 73:7848-7852.
64. Tsuji-Kawahara S., Chikaishi T., Takeda E., Kato M., Kinoshita S., Kajiwara E., Takamura S., Miyazawa M. Persistence of viremia and production of neutralizing antibodies differentially regulated by polymorphic APOBEC3 and BAFF-R loci in friend virus-infected mice. J. Virol. 2010, 84:6082-6095. Published online April 7, 2010.
65. Wang E., Obeng-Adjei N., Ying Q., Meertens L., Dragic T., Davey R.A., Ross S.R. Mouse mammary tumor virus uses mouse but not human transferrin receptor 1 to reach a low pH compartment and infect cells. Virology 2008, 381:230-240.
66. Wrona T., Dudley J.P. Major histocompatibility complex class II I-E-independent transmission of C3H mouse mammary tumor virus. J. Virol. 1996, 70:1246-1249.
67. Yamamoto K.R. Steroid receptor regulated transcription of specific genes and gene networks. Annu. Rev. Genet. 1985, 19:209-252.