Friend retrovirus drives cytotoxic effectors through Toll-like receptor 3

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Gibbert, Kathrin ^a   Francois, Sandra ^a   Sigmund, Anna M ^a   Harper, Michael S ^b   Barrett, Bradley S ^b   Kirchning, Carsten J ^a   Lu, Mengji ^a   Santiago, Mario L ^b   Dittmer, Ulf ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Cytotoxic T cells; Dendritic cells; Friend Retrovirus; NK cells; Pathogen recognition; Toll like receptor 3

Indexed keywords

CD86 ANTIGEN; INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL COUNT; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; FRIEND LEUKEMIA VIRUS; GENE; GENE EXPRESSION; IFI44 GENE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID DENDRITIC CELL; NATURAL KILLER CELL; NONHUMAN; PKR GENE; PROTEIN EXPRESSION; RETROVIRUS INFECTION; VIRUS LOAD; WILD TYPE; ANIMAL; C57BL MOUSE; DEFICIENCY; EXPERIMENTAL LEUKEMIA; FRIEND MURINE LEUKEMIA VIRUS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; VIROLOGY; VIRUS INFECTION;

MUS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; FRIEND MURINE LEUKEMIA VIRUS; KILLER CELLS, NATURAL; LEUKEMIA, EXPERIMENTAL; MICE, INBRED C57BL; MICE, KNOCKOUT; RETROVIRIDAE INFECTIONS; TOLL-LIKE RECEPTOR 3; TUMOR VIRUS INFECTIONS; VIRAL LOAD;

EID: 84924142648     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0126-4     Document Type: Article

References (67)

1. Akira S, Takeda K: Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511.
2. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, Sun L, Chen ZJ: Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 2013, 341:903-906.
3. Sun L, Wu J, Du F, Chen X, Chen ZJ: Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339:786-791.
4. Cai X, Chiu YH, Chen ZJ: The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Molecular cell 2014, 54:289-296.
5. Randall RE, Goodbourn S: Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008, 89:1-47.
6. Gringhuis SI, van der Vlist M, van den Berg LM, den Dunnen J, Litjens M, Geijtenbeek TB: HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat Immunol 2010, 11:419-426.
7. Mogensen TH, Melchjorsen J, Larsen CS, Paludan SR: Innate immune recognition and activation during HIV infection. Retrovirology 2010, 7:54.
8. Beignon AS, McKenna K, Skoberne M, Manches O, DaSilva I, Kavanagh DG, Larsson M, Gorelick RJ, Lifson JD, Bhardwaj N: Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 2005, 115:3265-3275.
9. Lepelley A, Louis S, Sourisseau M, Law HK, Pothlichet J, Schilte C, Chaperot L, Plumas J, Randall RE, Si-Tahar M, Mammano F, Albert ML, Schwartz O: Innate sensing of HIV-infected cells. PLoS Pathog 2011, 7:e1001284.
10. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio-De-Castillia C, Mothes W, Pizzato M, Grutter MG, Luban J: TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365.
11. Browne EP, Littman DR: Myd88 is required for an antibody response to retroviral infection. PLoS pathogens 2009, 5:e1000298.
12. Kane M, Case LK, Wang C, Yurkovetskiy L, Dikiy S, Golovkina TV: Innate immune sensing of retroviral infection via Toll-like receptor 7 occurs upon viral entry. Immunity 2011, 35:135-145.
13. Gibbert K, Joedicke JJ, Meryk A, Trilling M, Francois S, Duppach J, Kraft A, Lang KS, Dittmer U: Interferon-alpha Subtype 11 Activates NK Cells and Enables Control of Retroviral Infection. PLoS pathogens 2012, 8:e1002868.
14. Littwitz E, Francois S, Dittmer U, Gibbert K: Distinct roles of NK cells in viral immunity during different phases of acute Friend retrovirus infection. Retrovirology 2013, 10:127.
15. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738.
16. Hajjar AM, Linial ML: Modification of retroviral RNA by double-stranded RNA adenosine deaminase. J Virol 1995, 69:5878-5882.
17. Tounekti N, Mougel M, Roy C, Marquet R, Darlix JL, Paoletti J, Ehresmann B, Ehresmann C: Effect of dimerization on the conformation of the encapsidation Psi domain of Moloney murine leukemia virus RNA. J Mol Biol 1992, 223:205-220.
18. Alford RL, Honda S, Lawrence CB, Belmont JW: RNA secondary structure analysis of the packaging signal for Moloney murine leukemia virus. Virology 1991, 183:611-619.
19. Kabat D: Molecular biology of Friend viral erythroleukemia. Curr Top Microbiol Immunol 1989, 148:1-42.
20. Hasenkrug KJ, Dittmer U: The role of CD4 and CD8 T cells in recovery and protection from retroviral infection: lessons from the Friend virus model. Virology 2000, 272:244-249.
21. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okabe M, Takeda K, Akira S: Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301:640-643.
22. Yoneyama M, Suhara W, Fukuhara Y, Fukuda M, Nishida E, Fujita T: Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J 1998, 17:1087-1095.
23. Doyle S, Vaidya S, O'Connell R, Dadgostar H, Dempsey P, Wu T, Rao G, Sun R, Haberland M, Modlin R, Cheng G: IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 2002, 17:251-263.
24. Barchet W, Wimmenauer V, Schlee M, Hartmann G: Accessing the therapeutic potential of immunostimulatory nucleic acids. Curr Opin Immunol 2008, 20:389-395.
25. Barbalat R, Ewald SE, Mouchess ML, Barton GM: Nucleic acid recognition by the innate immune system. Annu Rev Immunol 2011, 29:185-214.
26. Gerlach N, Schimmer S, Weiss S, Kalinke U, Dittmer U: Effects of Type I Interferons on Friend Retrovirus Infection (Erratum). J Virol 2007, 81:6160.
27. 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.
28. Zelinskyy G, Dietze KK, Husecken YP, Schimmer S, Nair S, Werner T, Gibbert K, Kershaw O, Gruber AD, Sparwasser T, Dittmer U: The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood 2009, 114:3199-3207.
29. Zelinskyy G, Kraft AR, Schimmer S, Arndt T, Dittmer U: Kinetics of CD8+ effector T cell responses and induced CD4+ regulatory T cell responses during Friend retrovirus infection. Eur J Immunol 2006, 36:2658-2670.
30. Browne EP: Toll-like receptor 7 inhibits early acute retroviral infection through rapid lymphocyte responses. J Virol 2013, 87:7357-7366.
31. Marques R, Antunes I, Eksmond U, Stoye J, Hasenkrug K, Kassiotis G: B lymphocyte activation by coinfection prevents immune control of friend virus infection. J Immunol 2008, 181:3432-3440.
32. Gururajan M, Jacob J, Pulendran B: Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets. PloS one 2007, 2:e863.
33. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, Klucking S, Barrat FJ, Coffman RL, Staprans SI, Feinberg MB: Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 2008, 14:1077-1087.
34. Lee H, Komano J, Saitoh Y, Yamaoka S, Kozaki T, Misawa T, Takahama M, Satoh T, Takeuchi O, Yamamoto N, Matsuura Y, Saitoh T, Akira S: Zinc-finger antiviral protein mediates retinoic acid inducible gene I-like receptor-independent antiviral response to murine leukemia virus. Proc Natl Acad Sci U S A 2013, 110:12379-12384.
35. Iwasaki A, Medzhitov R: Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004, 5:987-995.
36. Kawai T, Akira S: Antiviral signaling through pattern recognition receptors. J Biochem 2007, 141:137-145.
37. Akira S, Takeda K, Kaisho T: Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001, 2:675-680.
38. Iwasaki A, Pillai PS: Innate immunity to influenza virus infection. Nat Rev Immunol 2014, 14:315-328.
39. Koyama S, Ishii KJ, 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.
40. Heer AK, Shamshiev A, Donda A, Uematsu S, Akira S, Kopf M, Marsland BJ: TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J Immunol 2007, 178:2182-2191.
41. Xia J, Winkelmann ER, Gorder SR, Mason PW, Milligan GN: TLR3- and MyD88-dependent signaling differentially influences the development of West Nile virus-specific B cell responses in mice following immunization with RepliVAX WN, a single-cycle flavivirus vaccine candidate. J Virol 2013, 87:12090-12101.
42. Lazear HM, Pinto AK, Ramos HJ, Vick SC, Shrestha B, Suthar MS, Gale M Jr, Diamond MS: Pattern recognition receptor MDA5 modulates CD8+ T cell-dependent clearance of West Nile virus from the central nervous system. J Virol 2013, 87:11401-11415.
43. Errett JS, Suthar MS, McMillan A, Diamond MS, Gale M Jr: The essential, nonredundant roles of RIG-I and MDA5 in detecting and controlling West Nile virus infection. J Virol 2013, 87:11416-11425.
44. Suthar MS, Ma DY, Thomas S, Lund JM, Zhang N, Daffis S, Rudensky AY, Bevan MJ, Clark EA, Kaja MK, Diamond MS, Gale M Jr: IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog 2010, 6:e1000757.
45. Szretter KJ, Daffis S, Patel J, Suthar MS, Klein RS, Gale M Jr, Diamond MS: The innate immune adaptor molecule MyD88 restricts West Nile virus replication and spread in neurons of the central nervous system. J Virol 2010, 84:12125-12138.
46. Daffis S, Samuel MA, Suthar MS, Gale M Jr, Diamond MS: Toll-like receptor 3 has a protective role against West Nile virus infection. J Virol 2008, 82:10349-10358.
47. Jin YH, Kim SJ, So EY, Meng L, Colonna M, Kim BS: Melanoma differentiation-associated gene 5 is critical for protection against Theiler's virus-induced demyelinating disease. J Virol 2012, 86:1531-1543.
48. Jin YH, Kaneyama T, Kang MH, Kang HS, Koh CS, Kim BS: TLR3 signaling is either protective or pathogenic for the development of Theiler's virus-induced demyelinating disease depending on the time of viral infection. J Neuroinflammation 2011, 8:178.
49. Tabeta K, Georgel P, Janssen E, Du X, Hoebe K, Crozat K, Mudd S, Shamel L, Sovath S, Goode J, Alexopoulou L, Flavell RA, Beutler B: Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci U S A 2004, 101:3516-3521.
50. Moore MD, Hu WS: HIV-1 RNA dimerization: It takes two to tango. AIDS Rev 2009, 11:91-102.
51. Russell RS, Liang C, Wainberg MA: Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably? Retrovirology 2004, 1:23.
52. Greatorex J: The retroviral RNA dimer linkage: different structures may reflect different roles. Retrovirology 2004, 1:22.
53. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, Swanstrom R, Burch CL, Weeks KM: Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 2009, 460:711-716.
54. Tatematsu M, Nishikawa F, Seya T, Matsumoto M: Toll-like receptor 3 recognizes incomplete stem structures in single-stranded viral RNA. Nat Commun 2013, 4:1833.
55. Gibbert K, Dietze KK, Zelinskyy G, Lang KS, Barchet W, Kirschning CJ, Dittmer U: Polyinosinic-polycytidylic acid treatment of Friend retrovirus-infected mice improves functional properties of virus-specific T cells and prevents virus-induced disease. J Immunol 2010, 185:6179-6189.
56. Wang X, Chao W, Saini M, Potash MJ: A common path to innate immunity to HIV-1 induced by Toll-like receptor ligands in primary human macrophages. PLoS One 2011, 6:e24193.
57. Zhou Y, Wang X, Liu M, Hu Q, Song L, Ye L, Zhou D, Ho W: A critical function of toll-like receptor-3 in the induction of anti-human immunodeficiency virus activities in macrophages. Immunology 2010, 131:40-49.
58. Tsang J, Chain BM, Miller RF, Webb BL, Barclay W, Towers GJ, Katz DR, Noursadeghi M: HIV-1 infection of macrophages is dependent on evasion of innate immune cellular activation. AIDS 2009, 23:2255-2263.
59. Suh HS, Zhao ML, Choi N, Belbin TJ, Brosnan CF, Lee SC: TLR3 and TLR4 are innate antiviral immune receptors in human microglia: role of IRF3 in modulating antiviral and inflammatory response in the CNS. Virology 2009, 392:246-259.
60. Swaminathan G, Rossi F, Sierra LJ, Gupta A, Navas-Martin S, Martin-Garcia J: A role for microRNA-155 modulation in the anti-HIV-1 effects of Toll-like receptor 3 stimulation in macrophages. PLoS Pathog 2012, 8:e1002937.
61. Breckpot K, Escors D, Arce F, Lopes L, Karwacz K, Van Lint S, Keyaerts M, Collins M: HIV-1 lentiviral vector immunogenicity is mediated by Toll-like receptor 3 (TLR3) and TLR7. J Virol 2010, 84:5627-5636.
62. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D: mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004, 279:12542-12550.
63. Sironi M, Biasin M, Cagliani R, Forni D, De Luca M, Saulle I, Lo Caputo S, Mazzotta F, Macias J, Pineda JA, Caruz A, Clerici M: A common polymorphism in TLR3 confers natural resistance to HIV-1 infection. J Immunol 2012, 188:818-823.
64. 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.
65. Dittmer U, Brooks DM, Hasenkrug KJ: Characterization of a live-attenuated retroviral vaccine demonstrates protection via immune mechanisms. J Virol 1998, 72:6554-6558.
66. Smith DS, Guo K, Barrett BS, Heilman KJ, Evans LH, Hasenkrug KJ, Greene WC, Santiago ML: Noninfectious retrovirus particles drive the APOBEC3/Rfv3 dependent neutralizing antibody response. PLoS Pathog 2011, 7:e1002284.
67. Balkow S, Krux F, Loser K, Becker JU, Grabbe S, Dittmer U: Friend retrovirus infection of myeloid dendritic cells impairs maturation, prolongs contact to naive T cells, and favors expansion of regulatory T cells. Blood 2007, 110:3949-3958.