Toll-like receptor 3 signaling inhibits simian immunodeficiency virus replication in macrophages from rhesus macaques

Antiviral Research

Volumn 112, Issue , 2014, Pages 103-112

  Sang, Ming ^a,c   Liu, Jin Biao ^a   Dai, Ming ^a,b   Wu, Jian Guo ^a   Ho, Wen Zhe ^a,b  

^a WUHAN UNIVERSITY   (China)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HUBEI UNIVERSITY OF MEDICINE   (China)

Author keywords

CC chemokine; Interferon; microRNA; Rhesus macaques; Simian immunodeficiency virus (SIV); Toll like receptor 3 (TLR3)

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; BETA CHEMOKINE; CHEMOKINE RECEPTOR CCR5; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MICRORNA 146A; MICRORNA 29A; MICRORNA 29B; MICRORNA 9; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; ANTIVIRUS AGENT;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; LYMPHOCYTE ACTIVATION; MACROPHAGE; NONHUMAN; PROTEIN EXPRESSION; RHESUS MONKEY; SIGNAL TRANSDUCTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TREATMENT OUTCOME; UPREGULATION; VIRUS REPLICATION; ANIMAL; CELL CULTURE; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY;

MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; ANTIVIRAL AGENTS; CELLS, CULTURED; MACACA MULATTA; MACROPHAGES; POLY I-C; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; TOLL-LIKE RECEPTOR 3; VIRUS REPLICATION;

EID: 84911139963     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2014.10.008     Document Type: Article

References (53)

1. Abel, K., Alegria-Hartman, M.J., Rothaeusler, K., Marthas, M., Miller, C.J., 2002. The relationship between simian immunodeficiency virus RNA levels and the mRNA levels of alpha/beta interferons (IFN-α/β) and IFN-α/β-inducible Mx in lymphoid tissues of rhesus macaques during acute and chronic infection. J. Virol. 76, 8433-8445.
2. Abrahams, V.M., Schaefer, T.M., Fahey, J.V., Visintin, I., Wright, J.A., Aldo, P.B., Romero, R., Wira, C.R., Mor, G., 2006. Expression and secretion of antiviral factors by trophoblast cells following stimulation by the TLR-3 agonist, poly (I:C). Hum. Reprod. 21, 2432-2439.
3. Akira, S., Takeda, K., 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511.
4. Akira, S., Uematsu, S., Takeuchi, O., 2006. Pathogen recognition and innate immunity. Cell 124, 783-801.
5. Alexopoulou, L., Holt, A.C., Medzhitov, R., Flavell, R.A., 2001. Recognition of double-stranded RNA and activation of NF-kappaB by toll-like receptor 3. Nature 413, 732-738.
6. Alsharifi, M., Mullbacher, A., Regner, M., 2008. Interferon type I responses in primary and secondary infections. Immunol. Cell Biol. 86, 239-245.
7. Aquaro, S., Caliò, R., Balzarini, J., Bellocchi, M.C., Garaci, E., Perno, C.F., 2002. Macrophages and HIV infection: therapeutical approaches toward this strategic virus reservoir. Antiviral Res. 55, 209-225.
8. Averett, D.R., Fletcher, S.P., Li, W., Webber, S.E., Appleman, J.R., 2007. The pharmacology of endosomal TLR agonists in viral disease. Biochem. Soc. Trans. 35, 1468-1472.
9. Baca-Regen, L., Heinzinger, N., Stevenson, M., Gendelman, H.E., 1994. Alpha interferon-induced antiretroviral activities: restriction of viral nucleic acid synthesis and progeny virion production in human immunodeficiency virus type 1-infected monocytes. J. Virol. 68, 7559-7565.
10. Baldauf, H.M., Pan, X., Erikson, E., Schmidt, S., Daddacha, W., Burggraf, M., Schenkova, K., Ambiel, I., Wabnitz, G., Gramberg, T., Panitz, S., Flory, E., Landau, N.R., Sertel, S., Rutsch, F., Lasitschka, F., Kim, B., Konig, R., Fackler, O.T., Keppler, O.T., 2012. SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells. Nat. Med. 18, 1682-1687.
11. Barber, S.A., Herbst, D.S., Bullock, B.T., Gama, L., Clements, J.E., 2004. Innate immune responses and control of acute simian immunodeficiency virus replication in the central nervous system. J. Neurovirol. 10 (Suppl. 1), 15-20.
12. Barr, S.D., Smiley, J.R., Bushman, F.D., 2008. The interferon response inhibits HIV particle production by induction of TRIM22. PLoS Pathog. 4, e1000007.
13. Black, L.R., Aiken, C., 2010. TRIM5alpha disrupts the structure of assembled HIV-1 capsid complexes in vitro. J. Virol. 84, 6564-6569.
14. Broering, R., Wu, J., Meng, Z., Hilgard, P., Lu, M., Trippler, M., Szczeponek, A., Gerken, G., Schlaak, J.F., 2008. Toll-like receptor-stimulated non-parenchymal liver cells can regulate hepatitis C virus replication. J. Hepatol. 48, 914-922.
15. Buitendijk, M., Eszterhas, S.K., Howell, A.L., 2014. Toll-like receptor agonists are potent inhibitors of human immunodeficiency virus-type 1 replication in peripheral blood mononuclear cells. AIDS Res. Hum. Retroviruses 30, 457-467.
16. Chattergoon, M.A., Latanich, R., Quinn, J., Winter, M.E., Buckheit 3rd, R.W., Blankson, J.N., Pardoll, D., Cox, A.L., 2014. HIV and HCV activate the inflammasome in monocytes and macrophages via endosomal toll-like receptors without induction of type 1 interferon. PLoS Pathog. 10, e1004082.
17. Daffis, S., Samuel, M.A., Suthar, M.S., Gale Jr., M., Diamond, M.S., 2008. Toll-like receptor 3 has a protective role against West Nile virus infection. J. Virol. 82, 10349-10358.
18. Deeks, S.G., Walker, B.D., 2007. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 27, 406-416.
19. Delneste, Y., Beauvillain, C., Jeannin, P., 2007. Innate immunity: structure and function of TLRs. Med. Sci. (Paris) 23, 67-73.
20. Gordon, S., Taylor, P.R., 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964.
21. Guo, C.J., Douglas, S.D., Gao, Z., Wolf, B.A., Grinspan, J., Lai, J.P., Riedel, E., Ho, W.Z., 2004. Interleukin-1beta upregulates functional expression of neurokinin-1 receptor (NK-1R) via NF-kappaB in astrocytes. Glia 48, 259-266.
22. Hill, C.M., Deng, H., Unutmaz, D., Kewalramani, V.N., Bastiani, L., Gorny, M.K., Zolla-Pazner, S., Littman, D.R., 1997. Envelope glycoproteins from human immunodeficiency virus types 1 and 2 and simian immunodeficiency virus can use human CCR5 as a coreceptor for viral entry and make direct CD4-dependent interactions with this chemokine receptor. J. Virol. 71, 6296-6304.
23. Honda, K., Yanai, H., Negishi, H., Asagiri, M., Sato, M., Mizutani, T., Shimada, N., Ohba, Y., Takaoka, A., Yoshida, N., Taniguchi, T., 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434, 772-777.
24. Hou, W., Wang, X., Ye, L., Zhou, L., Yang, Z.Q., Riedel, E., Ho, W.Z., 2009. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J. Virol. 83, 3834-3842.
25. Hrecka, K., Hao, C., Gierszewska, M., Swanson, S.K., Kesik-Brodacka, M., Srivastava, S., Florens, L., Washburn, M.P., Skowronski, J., 2011. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474, 658-661.
26. + T lymphocytes. Nat. Med. 13, 1241-1247.
27. Iwasaki, A., 2012. A virological view of innate immune recognition. Annu. Rev. Microbiol. 66, 177-196.
28. Janeway Jr., C.A., Medzhitov, R., 2002. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216.
29. Kabelitz, D., Medzhitov, R., 2007. Innate immunity - cross-talk with adaptive immunity through pattern recognition receptors and cytokines. Curr. Opin. Immunol. 19, 1-3.
30. Kadowaki, N., Ho, S., Antonenko, S., Malefyt, R.D., Kastelein, R.A., Bazan, F., Liu, Y.J., 2001. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194, 863-869.
31. Kanzler, H., Barrat, F.J., Hessel, E.M., Coffman, R.L., 2007. Therapeutic targeting of innate immunity with toll-like receptor agonists and antagonists. Nat. Med. 13, 552-559.
32. Koppensteiner, H., Brack-Werner, R., Schindler, M., 2012. Macrophages and their relevance in human immunodeficiency virus type I infection. Retrovirology 9, 82.
33. Kumar, A., 2007. The silent defense: micro-RNA directed defense against HIV-1 replication. Retrovirology 4, 26.
34. Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Segeral, E., Yatim, A., Emiliani, S., Schwartz, O., Benkirane, M., 2011. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474, 654-657.
35. Lau, Y.F., Tang, L.H., Ooi, E.E., 2009. A TLR3 ligand that exhibits potent inhibition of influenza virus replication and has strong adjuvant activity has the potential for dual applications in an influenza pandemic. Vaccine 27, 1354-1364.
36. Lecellier, C.H., Dunoyer, P., Arar, K., Lehmann-Che, J., Eyquem, S., Himber, C., Saib, A., Voinnet, O., 2005. A cellular microRNA mediates antiviral defense in human cells. Science 308, 557-560.
37. Liu, M.Q., Zhou, D.J., Wang, X., Zhou, W., Ye, L., Li, J.L., Wang, Y.Z., Ho, W.Z., 2012. IFN-k3 inhibits HIV infection of macrophages through the JAK-STAT pathway. PLoS One 7, e35902.
38. Neil, S.J., Zang, T., Bieniasz, P.D., 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430.
39. Proost, P., Schols, D., 2002. Role of chemokines in the HIV infection process. Verh. K. Acad. Geneeskd. Belg. 64, 403-420.
40. Riddick, N.E., Hermann, E.A., Loftin, L.M., Elliott, S.T., Wey, W.C., Cervasi, B., Taaffe, J., Engram, J.C., Li, B., Else, J.G., Li, Y., Hahn, B.H., Derdeyn, C.A., Sodora, D.L., Apetrei, C., Paiardini, M., Silvestri, G., Collman, R.G., 2010. A novel CCR5 mutation common in sooty mangabeys reveals SIVsmm infection of CCR5-null natural hosts and efficient alternative coreceptor use in vivo. PLoS Pathog. 6, e1001064.
41. Roberts, E.S., Zandonatti, M.A., Watry, D.D., Madden, L.J., Henriksen, S.J., Taffe, M.A., Fox, H.S., 2003. Induction of pathogenic sets of genes in macrophages and neurons in NeuroAIDS. Am. J. Pathol. 162, 2041-2057.
42. Ruiz, A., Lau, D., Mitchell, R.S., Hill, M.S., Schmitt, K., Guatelli, J.C., Stephens, E.B., 2010. BST-2 mediated restriction of simian-human immunodeficiency virus. Virology 406, 312-321.
43. Sanghavi, S.K., Reinhart, T.A., 2005. Increased expression of TLR3 in lymph nodes during simian immunodeficiency virus infection: implications for inflammation and immunodeficiency. J. Immunol. 175, 5314-5323.
44. Schmidt, K.N., Leung, B., Kwong, M., Zarember, K.A., Satyal, S., Navas, T.A., Wang, F., Godowski, P.J., 2004. APC-Independent activation of NK cells by the toll-like receptor 3 agonist double-stranded RNA. J. Immunol. 172, 138-143.
45. Sisk, J.M., Witwer, K.W., Tarwater, P.M., Clements, J.E., 2013. SIV replication is directly downregulated by four antiviral miRNAs. Retrovirology 10, 95.
46. Tabiasco, J., Devevre, E., Rufer, N., Salaun, B., Cerottini, J.C., Speiser, D., Romero, P., 2006. Human effector CD8(+) T lymphocytes express TLR3 as a functional coreceptor. J. Immunol. 177, 8708-8713.
47. Takeuchi, O., Akira, S., 2009. Innate immunity to virus infection. Immunol. Rev. 227, 75-86.
48. Trapp, S., Derby, N.R., Singer, R., Shaw, A., Williams, V.G., Turville, S.G., Bess Jr., J.W., Lifson, J.D., Robbiani, M., 2009. Double-stranded RNA analog poly (I:C) inhibits human immunodeficiency virus amplification in dendritic cells via type I interferon-mediated activation of APOBEC3G. J. Virol. 83, 884-895.
49. Wang, X., Ye, L., Hou, W., Zhou, Y., Wang, Y.J., Metzger, D.S., Ho, W.Z., 2009a. Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood 113, 671-674.
50. Wang, Y.J., Wang, X., Zhang, H., Zhou, L., Liu, S., Kolson, D.L., Song, L., Ye, L., Ho, W.Z., 2009b. Expression and regulation of antiviral protein APOBEC3G in human neuronal cells. J. Neuroimmunol. 206, 14-21.
51. Zhou, Y., Ye, L., Wan, Q., Zhou, L., Wang, X., Li, J., Hu, S., Zhou, D., Ho, W., 2009. Activation of toll-like receptors inhibits herpes simplex virus-1 infection of human neuronal cells. J. Neurosci. Res. 87, 2916-2925.
52. Zhou, Y., Wang, X., Liu, M., Hu, Q., Song, L., Ye, L., Zhou, D., Ho, W., 2010. A critical function of toll-like receptor-3 in the induction of anti-human immunodeficiency virus activities in macrophages. Immunology 131, 40-49.
53. Zhou, Y., Guo, M., Wang, X., Li, J., Wang, Y., Ye, L., Dai, M., Zhou, L., Persidsky, Y., Ho, W., 2013. TLR3 activation efficiency by high or low molecular mass poly I:C. Innate Immun. 19, 184-192.