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Published in: Journal of Neuroinflammation 1/2014

Open Access 01-12-2014 | Research

Met-CCL5 represents an immunotherapy strategy to ameliorate rabies virus infection

Authors: Ying Huang, Shaozhuo Jiao, Xiaoyan Tao, Qing Tang, Wentao Jiao, Jun Xiao, Xiaoyan Xu, Yanbo Zhang, Guodong Liang, Hongyan Wang

Published in: Journal of Neuroinflammation | Issue 1/2014

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Abstract

Background

Infection of rabies virus (RABV) causes central nervous system (CNS) dysfunction and results in high mortality in human and animals. However, it is still unclear whether and how CNS inflammation and immune response contribute to RABV infection.

Methods

Suckling mice were intracerebrally infected with attenuated RABV aG and CTN strains, followed by examination of chemokine or cytokine production, inflammatory cell infiltration and neuron apoptosis in the brain. Furthermore, the suckling mice and adult mice that were intracerebrally infected with aG and the adult mice that were intramuscularly infected with street RABV HN10 were treated with CCL5 antagonist (Met-CCL5) daily beginning on day 2 postinfection. The survival rates and inflammation responses in the CNS of these mice were analyzed.

Results

Excessive CCL5 in the CNS was associated with CNS dysfunction, inflammation, and macrophage or lymphocyte infiltration after attenuated or street RABV infection. Administration of exogenous CCL5 induced excessive infiltration of immune cells into the CNS and enhanced inflammatory chemokine and cytokine production. Met-CCL5 treatment significantly prolonged survival time of the suckling mice inoculated with aG and adult mice infected with aG and HN10.

Conclusions

These results suggest that CCL5 in the CNS is a key regulator involved in inducing rabies encephalomyelitis. Furthermore, treatment with the CCL5 antagonist Met-CCL5 prolongs survival time of the mice infected with attenuated or street RABVs, which might represent a novel therapeutic strategy to ameliorate RABV infection.
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Literature
1.
go back to reference Rupprecht CE: Rhabdoviruses: Rabies Virus . In Medical Microbiology. Edited by Baron S. Galveston TX: The University of Texas Medical Branch at Galveston; 1996.. Rupprecht CE: Rhabdoviruses: Rabies Virus . In Medical Microbiology. Edited by Baron S. Galveston TX: The University of Texas Medical Branch at Galveston; 1996..
2.
go back to reference WHO expert consultation on rabies. World Health Organ Tech Rep Ser. 2005, 931: 1-88. back cover WHO expert consultation on rabies. World Health Organ Tech Rep Ser. 2005, 931: 1-88. back cover
3.
go back to reference Miyamoto K, Matsumoto S: Comparative studies between pathogenesis of street and fixed rabies infection. J Exp Med. 1967, 125: 447-456. 10.1084/jem.125.3.447.PubMedCentralCrossRefPubMed Miyamoto K, Matsumoto S: Comparative studies between pathogenesis of street and fixed rabies infection. J Exp Med. 1967, 125: 447-456. 10.1084/jem.125.3.447.PubMedCentralCrossRefPubMed
5.
go back to reference Baloul L, Lafon M: Apoptosis and rabies virus neuroinvasion. Biochimie. 2003, 85: 777-788. 10.1016/S0300-9084(03)00137-8.CrossRefPubMed Baloul L, Lafon M: Apoptosis and rabies virus neuroinvasion. Biochimie. 2003, 85: 777-788. 10.1016/S0300-9084(03)00137-8.CrossRefPubMed
6.
go back to reference Wang ZW, Sarmento L, Wang Y, Li XQ, Dhingra V, Tseggai T, Jiang B, Fu ZF: Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol. 2005, 79: 12554-12565. 10.1128/JVI.79.19.12554-12565.2005.PubMedCentralCrossRefPubMed Wang ZW, Sarmento L, Wang Y, Li XQ, Dhingra V, Tseggai T, Jiang B, Fu ZF: Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol. 2005, 79: 12554-12565. 10.1128/JVI.79.19.12554-12565.2005.PubMedCentralCrossRefPubMed
7.
go back to reference Benveniste EN: Cytokines: influence on glial cell gene expression and function. Chem Immunol. 1997, 69: 31-75. 10.1159/000058653.CrossRefPubMed Benveniste EN: Cytokines: influence on glial cell gene expression and function. Chem Immunol. 1997, 69: 31-75. 10.1159/000058653.CrossRefPubMed
8.
go back to reference Benveniste EN: Cytokine actions in the central nervous system. Cytokine Growth Factor Rev. 1998, 9: 259-275. 10.1016/S1359-6101(98)00015-X.CrossRefPubMed Benveniste EN: Cytokine actions in the central nervous system. Cytokine Growth Factor Rev. 1998, 9: 259-275. 10.1016/S1359-6101(98)00015-X.CrossRefPubMed
9.
go back to reference Glabinski AR, Ransohoff RM: Chemokines and chemokine receptors in CNS pathology. J Neurovirol. 1999, 5: 3-12. 10.3109/13550289909029740.CrossRefPubMed Glabinski AR, Ransohoff RM: Chemokines and chemokine receptors in CNS pathology. J Neurovirol. 1999, 5: 3-12. 10.3109/13550289909029740.CrossRefPubMed
10.
go back to reference Kuang Y, Lackay SN, Zhao L, Fu ZF: Role of chemokines in the enhancement of BBB permeability and inflammatory infiltration after rabies virus infection. Virus Res. 2009, 144: 18-26. 10.1016/j.virusres.2009.03.014.PubMedCentralCrossRefPubMed Kuang Y, Lackay SN, Zhao L, Fu ZF: Role of chemokines in the enhancement of BBB permeability and inflammatory infiltration after rabies virus infection. Virus Res. 2009, 144: 18-26. 10.1016/j.virusres.2009.03.014.PubMedCentralCrossRefPubMed
11.
go back to reference Zhao L, Toriumi H, Kuang Y, Chen H, Fu ZF: The roles of chemokines in rabies virus infection: overexpression may not always be beneficial. J Virol. 2009, 83: 11808-11818. 10.1128/JVI.01346-09.PubMedCentralCrossRefPubMed Zhao L, Toriumi H, Kuang Y, Chen H, Fu ZF: The roles of chemokines in rabies virus infection: overexpression may not always be beneficial. J Virol. 2009, 83: 11808-11818. 10.1128/JVI.01346-09.PubMedCentralCrossRefPubMed
12.
go back to reference Nakamichi K, Saiki M, Sawada M, Takayama-Ito M, Yamamuro Y, Morimoto K, Kurane I: Rabies virus-induced activation of mitogen-activated protein kinase and NF-kappaB signaling pathways regulates expression of CXC and CC chemokine ligands in microglia. J Virol. 2005, 79: 11801-11812. 10.1128/JVI.79.18.11801-11812.2005.PubMedCentralCrossRefPubMed Nakamichi K, Saiki M, Sawada M, Takayama-Ito M, Yamamuro Y, Morimoto K, Kurane I: Rabies virus-induced activation of mitogen-activated protein kinase and NF-kappaB signaling pathways regulates expression of CXC and CC chemokine ligands in microglia. J Virol. 2005, 79: 11801-11812. 10.1128/JVI.79.18.11801-11812.2005.PubMedCentralCrossRefPubMed
13.
go back to reference Lafon M: Immune evasion, a critical strategy for rabies virus. Dev Biol (Basel). 2008, 131: 413-419. Lafon M: Immune evasion, a critical strategy for rabies virus. Dev Biol (Basel). 2008, 131: 413-419.
14.
go back to reference Hemachudha T: Human rabies: clinical aspects, pathogenesis, and potential therapy. Curr Top Microbiol Immunol. 1994, 187: 121-143.PubMed Hemachudha T: Human rabies: clinical aspects, pathogenesis, and potential therapy. Curr Top Microbiol Immunol. 1994, 187: 121-143.PubMed
15.
go back to reference Wang H, Zhang G, Wen Y, Yang S, Xia X, Fu ZF: Intracerebral administration of recombinant rabies virus expressing GM-CSF prevents the development of rabies after infection with street virus. PLoS One. 2011, 6: e25414-10.1371/journal.pone.0025414.PubMedCentralCrossRefPubMed Wang H, Zhang G, Wen Y, Yang S, Xia X, Fu ZF: Intracerebral administration of recombinant rabies virus expressing GM-CSF prevents the development of rabies after infection with street virus. PLoS One. 2011, 6: e25414-10.1371/journal.pone.0025414.PubMedCentralCrossRefPubMed
16.
go back to reference Gnanadurai CW, Zhou M, He W, Leyson CM, Huang CT, Salyards G, Chen Z, He B, Yang Y, Hooper DC, Dietzchold B, Fu ZF: Presence of virus neutralizing antibodies in cerebral spinal fluid correlates with non-lethal rabies in dogs. PLoS Negl Trop Dis. 2013, 7: e2375-10.1371/journal.pntd.0002375.PubMedCentralCrossRefPubMed Gnanadurai CW, Zhou M, He W, Leyson CM, Huang CT, Salyards G, Chen Z, He B, Yang Y, Hooper DC, Dietzchold B, Fu ZF: Presence of virus neutralizing antibodies in cerebral spinal fluid correlates with non-lethal rabies in dogs. PLoS Negl Trop Dis. 2013, 7: e2375-10.1371/journal.pntd.0002375.PubMedCentralCrossRefPubMed
17.
go back to reference Johnson N, Mansfield KL, Hicks D, Nunez A, Healy DM, Brookes SM, McKimmie C, Fazakerley JK, Fooks AR: Inflammatory responses in the nervous system of mice infected with a street isolate of rabies virus. Dev Biol (Basel). 2008, 131: 65-72. Johnson N, Mansfield KL, Hicks D, Nunez A, Healy DM, Brookes SM, McKimmie C, Fazakerley JK, Fooks AR: Inflammatory responses in the nervous system of mice infected with a street isolate of rabies virus. Dev Biol (Basel). 2008, 131: 65-72.
18.
go back to reference Chai Q, He WQ, Zhou M, Lu H, Fu ZF: Enhancement of blood–brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol. 2014, 88: 4698-4710. 10.1128/JVI.03149-13.PubMedCentralCrossRefPubMed Chai Q, He WQ, Zhou M, Lu H, Fu ZF: Enhancement of blood–brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol. 2014, 88: 4698-4710. 10.1128/JVI.03149-13.PubMedCentralCrossRefPubMed
19.
go back to reference Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B: Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol. 1998, 72: 3711-3719.PubMedCentralPubMed Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B: Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol. 1998, 72: 3711-3719.PubMedCentralPubMed
20.
go back to reference Levy JA: The unexpected pleiotropic activities of RANTES. J Immunol. 2009, 182: 3945-3946. 10.4049/jimmunol.0990015.CrossRefPubMed Levy JA: The unexpected pleiotropic activities of RANTES. J Immunol. 2009, 182: 3945-3946. 10.4049/jimmunol.0990015.CrossRefPubMed
21.
go back to reference Appay V, Rowland-Jones SL: RANTES: a versatile and controversial chemokine. Trends Immunol. 2001, 22: 83-87. 10.1016/S1471-4906(00)01812-3.CrossRefPubMed Appay V, Rowland-Jones SL: RANTES: a versatile and controversial chemokine. Trends Immunol. 2001, 22: 83-87. 10.1016/S1471-4906(00)01812-3.CrossRefPubMed
22.
go back to reference Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, Kramp BK, Piccinini AM, Paludan SR, Kowalska MA, Kungl AJ, Hackeng TM, Mayo KH, Weber C: Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009, 15: 97-103. 10.1038/nm.1898.CrossRefPubMed Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, Kramp BK, Piccinini AM, Paludan SR, Kowalska MA, Kungl AJ, Hackeng TM, Mayo KH, Weber C: Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009, 15: 97-103. 10.1038/nm.1898.CrossRefPubMed
23.
go back to reference Lane TE, Liu MT, Chen BP, Asensio VC, Samawi RM, Paoletti AD, Campbell IL, Kunkel SL, Fox HS, Buchmeier MJ: A central role for CD4(+) T cells and RANTES in virus-induced central nervous system inflammation and demyelination. J Virol. 2000, 74: 1415-1424. 10.1128/JVI.74.3.1415-1424.2000.PubMedCentralCrossRefPubMed Lane TE, Liu MT, Chen BP, Asensio VC, Samawi RM, Paoletti AD, Campbell IL, Kunkel SL, Fox HS, Buchmeier MJ: A central role for CD4(+) T cells and RANTES in virus-induced central nervous system inflammation and demyelination. J Virol. 2000, 74: 1415-1424. 10.1128/JVI.74.3.1415-1424.2000.PubMedCentralCrossRefPubMed
24.
go back to reference Wu L, Gerard NP, Wyatt R, Choe H, Parolin C, Ruffing N, Borsetti A, Cardoso AA, Desjardin E, Newman W, Gerard C, Sodroski J: CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature. 1996, 384: 179-183. 10.1038/384179a0.CrossRefPubMed Wu L, Gerard NP, Wyatt R, Choe H, Parolin C, Ruffing N, Borsetti A, Cardoso AA, Desjardin E, Newman W, Gerard C, Sodroski J: CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature. 1996, 384: 179-183. 10.1038/384179a0.CrossRefPubMed
25.
go back to reference Shahrara S, Proudfoot AE, Woods JM, Ruth JH, Amin MA, Park CC, Haas CS, Pope RM, Haines GK, Zha YY, Koch AE: Amelioration of rat adjuvant-induced arthritis by Met-RANTES. Arthritis Rheum. 2005, 52: 1907-1919. 10.1002/art.21033.PubMedCentralCrossRefPubMed Shahrara S, Proudfoot AE, Woods JM, Ruth JH, Amin MA, Park CC, Haas CS, Pope RM, Haines GK, Zha YY, Koch AE: Amelioration of rat adjuvant-induced arthritis by Met-RANTES. Arthritis Rheum. 2005, 52: 1907-1919. 10.1002/art.21033.PubMedCentralCrossRefPubMed
26.
go back to reference Khan IA, Thomas SY, Moretto MM, Lee FS, Islam SA, Combe C, Schwartzman JD, Luster AD: CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathog. 2006, 2: e49-10.1371/journal.ppat.0020049.PubMedCentralCrossRefPubMed Khan IA, Thomas SY, Moretto MM, Lee FS, Islam SA, Combe C, Schwartzman JD, Luster AD: CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathog. 2006, 2: e49-10.1371/journal.ppat.0020049.PubMedCentralCrossRefPubMed
27.
go back to reference Lim JK, Glass WG, McDermott DH, Murphy PM: CCR5: no longer a ‘good for nothing’ gene - chemokine control of West Nile virus infection. Trends Immunol. 2006, 27: 308-312. 10.1016/j.it.2006.05.007.CrossRefPubMed Lim JK, Glass WG, McDermott DH, Murphy PM: CCR5: no longer a ‘good for nothing’ gene - chemokine control of West Nile virus infection. Trends Immunol. 2006, 27: 308-312. 10.1016/j.it.2006.05.007.CrossRefPubMed
28.
go back to reference Kohlmeier JE, Miller SC, Smith J, Lu B, Gerard C, Cookenham T, Roberts AD, Woodland DL: The chemokine receptor CCR5 plays a key role in the early memory CD8+ T cell response to respiratory virus infections. Immunity. 2008, 29: 101-113. 10.1016/j.immuni.2008.05.011.PubMedCentralCrossRefPubMed Kohlmeier JE, Miller SC, Smith J, Lu B, Gerard C, Cookenham T, Roberts AD, Woodland DL: The chemokine receptor CCR5 plays a key role in the early memory CD8+ T cell response to respiratory virus infections. Immunity. 2008, 29: 101-113. 10.1016/j.immuni.2008.05.011.PubMedCentralCrossRefPubMed
29.
go back to reference Proudfoot AE, Buser R, Borlat F, Alouani S, Soler D, Offord RE, Schröder JM, Power CA, Wells TN: Amino-terminally modified RANTES analogues demonstrate differential effects on RANTES receptors. J Biol Chem. 1999, 274: 32478-32485. 10.1074/jbc.274.45.32478.CrossRefPubMed Proudfoot AE, Buser R, Borlat F, Alouani S, Soler D, Offord RE, Schröder JM, Power CA, Wells TN: Amino-terminally modified RANTES analogues demonstrate differential effects on RANTES receptors. J Biol Chem. 1999, 274: 32478-32485. 10.1074/jbc.274.45.32478.CrossRefPubMed
30.
go back to reference Matsui M, Weaver J, Proudfoot AE, Wujek JR, Wei T, Richer E, Trapp BD, Rao A, Ransohoff RM: Treatment of experimental autoimmune encephalomyelitis with the chemokine receptor antagonist Met-RANTES. J Neuroimmunol. 2002, 128: 16-22. 10.1016/S0165-5728(02)00121-2.CrossRefPubMed Matsui M, Weaver J, Proudfoot AE, Wujek JR, Wei T, Richer E, Trapp BD, Rao A, Ransohoff RM: Treatment of experimental autoimmune encephalomyelitis with the chemokine receptor antagonist Met-RANTES. J Neuroimmunol. 2002, 128: 16-22. 10.1016/S0165-5728(02)00121-2.CrossRefPubMed
31.
go back to reference Proudfoot AE: Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol. 2002, 2: 106-115. 10.1038/nri722.CrossRefPubMed Proudfoot AE: Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol. 2002, 2: 106-115. 10.1038/nri722.CrossRefPubMed
32.
go back to reference Lin F, Zeng F, Lu L, Lu X, Zen R, Yu Y, Chen N: The primary hamster kidney cell rabies vaccine: adaptation of viral strain, production of vaccine, and pre- and postexposure treatment. J Infect Dis. 1983, 147: 467-473. 10.1093/infdis/147.3.467.CrossRefPubMed Lin F, Zeng F, Lu L, Lu X, Zen R, Yu Y, Chen N: The primary hamster kidney cell rabies vaccine: adaptation of viral strain, production of vaccine, and pre- and postexposure treatment. J Infect Dis. 1983, 147: 467-473. 10.1093/infdis/147.3.467.CrossRefPubMed
33.
go back to reference Du J, Zhang Q, Tang Q, Li H, Tao X, Morimoto K, Nadin-Davis SA, Liang G: Characterization of human rabies virus vaccine strain in China. Virus Res. 2008, 135: 260-266. 10.1016/j.virusres.2008.04.002.CrossRefPubMed Du J, Zhang Q, Tang Q, Li H, Tao X, Morimoto K, Nadin-Davis SA, Liang G: Characterization of human rabies virus vaccine strain in China. Virus Res. 2008, 135: 260-266. 10.1016/j.virusres.2008.04.002.CrossRefPubMed
34.
go back to reference Ming P, Du J, Tang Q, Yan J, Nadin-Davis SA, Li H, Tao X, Huang Y, Hu R, Liang G: Molecular characterization of the complete genome of a street rabies virus isolated in China. Virus Res. 2009, 143: 6-14. 10.1016/j.virusres.2009.02.014.CrossRefPubMed Ming P, Du J, Tang Q, Yan J, Nadin-Davis SA, Li H, Tao X, Huang Y, Hu R, Liang G: Molecular characterization of the complete genome of a street rabies virus isolated in China. Virus Res. 2009, 143: 6-14. 10.1016/j.virusres.2009.02.014.CrossRefPubMed
35.
go back to reference Rowell JF, Griffin DE: The inflammatory response to nonfatal Sindbis virus infection of the nervous system is more severe in SJL than in BALB/c mice and is associated with low levels of IL-4 mRNA and high levels of IL-10-producing CD4+ T cells. J Immunol. 1999, 162: 1624-1632.PubMed Rowell JF, Griffin DE: The inflammatory response to nonfatal Sindbis virus infection of the nervous system is more severe in SJL than in BALB/c mice and is associated with low levels of IL-4 mRNA and high levels of IL-10-producing CD4+ T cells. J Immunol. 1999, 162: 1624-1632.PubMed
36.
go back to reference Jackson AC, Scott CA, Owen J, Weli SC, Rossiter JP: Therapy with minocycline aggravates experimental rabies in mice. J Virol. 2007, 81: 6248-6253. 10.1128/JVI.00323-07.PubMedCentralCrossRefPubMed Jackson AC, Scott CA, Owen J, Weli SC, Rossiter JP: Therapy with minocycline aggravates experimental rabies in mice. J Virol. 2007, 81: 6248-6253. 10.1128/JVI.00323-07.PubMedCentralCrossRefPubMed
37.
go back to reference Wang SW, Wu HH, Liu SC, Wang PC, Ou WC, Chou WY, Shen YS, Tang CH: CCL5 and CCR5 interaction promotes cell motility in human osteosarcoma. PLoS One. 2012, 7: e35101-10.1371/journal.pone.0035101.PubMedCentralCrossRefPubMed Wang SW, Wu HH, Liu SC, Wang PC, Ou WC, Chou WY, Shen YS, Tang CH: CCL5 and CCR5 interaction promotes cell motility in human osteosarcoma. PLoS One. 2012, 7: e35101-10.1371/journal.pone.0035101.PubMedCentralCrossRefPubMed
38.
go back to reference Vilela MC, Mansur DS, Lacerda-Queiroz N, Rodrigues DH, Lima GK, Arantes RM, Kroon EG, da Silva Campos MA, Teixeira MM, Teixeira AL: The chemokine CCL5 is essential for leukocyte recruitment in a model of severe Herpes simplex encephalitis. Ann N Y Acad Sci. 2009, 1153: 256-263. 10.1111/j.1749-6632.2008.03959.x.CrossRefPubMed Vilela MC, Mansur DS, Lacerda-Queiroz N, Rodrigues DH, Lima GK, Arantes RM, Kroon EG, da Silva Campos MA, Teixeira MM, Teixeira AL: The chemokine CCL5 is essential for leukocyte recruitment in a model of severe Herpes simplex encephalitis. Ann N Y Acad Sci. 2009, 1153: 256-263. 10.1111/j.1749-6632.2008.03959.x.CrossRefPubMed
39.
go back to reference Huang CY, Fong YC, Lee CY, Chen MY, Tsai HC, Hsu HC, Tang CH: CCL5 increases lung cancer migration via PI3K, Akt and NF-kappaB pathways. Biochem Pharmacol. 2009, 77: 794-803. 10.1016/j.bcp.2008.11.014.CrossRefPubMed Huang CY, Fong YC, Lee CY, Chen MY, Tsai HC, Hsu HC, Tang CH: CCL5 increases lung cancer migration via PI3K, Akt and NF-kappaB pathways. Biochem Pharmacol. 2009, 77: 794-803. 10.1016/j.bcp.2008.11.014.CrossRefPubMed
40.
go back to reference 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. 10.1126/science.1087262.CrossRefPubMed 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. 10.1126/science.1087262.CrossRefPubMed
41.
go back to reference Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of double-stranded RNA and activation of NF-kappa B by Toll-like receptor 3. Nature. 2001, 413: 732-738. 10.1038/35099560.CrossRefPubMed Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of double-stranded RNA and activation of NF-kappa B by Toll-like receptor 3. Nature. 2001, 413: 732-738. 10.1038/35099560.CrossRefPubMed
42.
go back to reference Prehaud C, Megret F, Lafage M, Lafon M: Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol. 2005, 79: 12893-12904. 10.1128/JVI.79.20.12893-12904.2005.PubMedCentralCrossRefPubMed Prehaud C, Megret F, Lafage M, Lafon M: Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol. 2005, 79: 12893-12904. 10.1128/JVI.79.20.12893-12904.2005.PubMedCentralCrossRefPubMed
43.
go back to reference Klein RS, Lin E, Zhang B, Luster AD, Tollett J, Samuel MA, Engle M, Diamond MS: Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol. 2005, 79: 11457-11466. 10.1128/JVI.79.17.11457-11466.2005.PubMedCentralCrossRefPubMed Klein RS, Lin E, Zhang B, Luster AD, Tollett J, Samuel MA, Engle M, Diamond MS: Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol. 2005, 79: 11457-11466. 10.1128/JVI.79.17.11457-11466.2005.PubMedCentralCrossRefPubMed
44.
go back to reference Aravalli RN, Hu S, Rowen TN, Palmquist JM, Lokensgard JR: Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J Immunol. 2005, 175: 4189-4193. 10.4049/jimmunol.175.7.4189.CrossRefPubMed Aravalli RN, Hu S, Rowen TN, Palmquist JM, Lokensgard JR: Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J Immunol. 2005, 175: 4189-4193. 10.4049/jimmunol.175.7.4189.CrossRefPubMed
45.
go back to reference Schall TJ, Bacon K, Toy KJ, Goeddel DV: Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature. 1990, 347: 669-671. 10.1038/347669a0.CrossRefPubMed Schall TJ, Bacon K, Toy KJ, Goeddel DV: Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature. 1990, 347: 669-671. 10.1038/347669a0.CrossRefPubMed
46.
go back to reference Grone HJ, Weber C, Weber KS, Gröne EF, Rabelink T, Klier CM, Wells TN, Proudfood AE, Schlöndorff D, Nelson PJ: Met-RANTES reduces vascular and tubular damage during acute renal transplant rejection: blocking monocyte arrest and recruitment. FASEB J. 1999, 13: 1371-1383.PubMed Grone HJ, Weber C, Weber KS, Gröne EF, Rabelink T, Klier CM, Wells TN, Proudfood AE, Schlöndorff D, Nelson PJ: Met-RANTES reduces vascular and tubular damage during acute renal transplant rejection: blocking monocyte arrest and recruitment. FASEB J. 1999, 13: 1371-1383.PubMed
47.
go back to reference Plater-Zyberk C, Hoogewerf AJ, Proudfoot AE, Power CA, Wells TN: Effect of a CC chemokine receptor antagonist on collagen induced arthritis in DBA/1 mice. Immunol Lett. 1997, 57: 117-120. 10.1016/S0165-2478(97)00075-8.CrossRefPubMed Plater-Zyberk C, Hoogewerf AJ, Proudfoot AE, Power CA, Wells TN: Effect of a CC chemokine receptor antagonist on collagen induced arthritis in DBA/1 mice. Immunol Lett. 1997, 57: 117-120. 10.1016/S0165-2478(97)00075-8.CrossRefPubMed
48.
go back to reference Ajuebor MN, Hogaboam CM, Kunkel SL, Proudfoot AE, Wallace JL: The chemokine RANTES is a crucial mediator of the progression from acute to chronic colitis in the rat. J Immunol. 2001, 166: 552-558. 10.4049/jimmunol.166.1.552.CrossRefPubMed Ajuebor MN, Hogaboam CM, Kunkel SL, Proudfoot AE, Wallace JL: The chemokine RANTES is a crucial mediator of the progression from acute to chronic colitis in the rat. J Immunol. 2001, 166: 552-558. 10.4049/jimmunol.166.1.552.CrossRefPubMed
49.
go back to reference Chvatchko Y, Proudfoot AE, Buser R, Juillard P, Alouani S, Kosco-Vilbois M, Coyle AJ, Nibbs RJ, Graham G, Offord RE, Wells TN: Inhibition of airway inflammation by amino-terminally modified RANTES/CC chemokine ligand 5 analogues is not mediated through CCR3. J Immunol. 2003, 171: 5498-5506. 10.4049/jimmunol.171.10.5498.CrossRefPubMed Chvatchko Y, Proudfoot AE, Buser R, Juillard P, Alouani S, Kosco-Vilbois M, Coyle AJ, Nibbs RJ, Graham G, Offord RE, Wells TN: Inhibition of airway inflammation by amino-terminally modified RANTES/CC chemokine ligand 5 analogues is not mediated through CCR3. J Immunol. 2003, 171: 5498-5506. 10.4049/jimmunol.171.10.5498.CrossRefPubMed
50.
go back to reference Berres ML, Koenen RR, Rueland A, Zaldivar MM, Heinrichs D, Sahin H, Schmitz P, Streetz KL, Berg T, Gassler N, Weiskirchen R, Proudfoot A, Weber C, Trautwein C, Wasmuth HE: Antagonism of the chemokine Ccl5 ameliorates experimental liver fibrosis in mice. J Clin Invest. 2010, 120: 4129-4140. 10.1172/JCI41732.PubMedCentralCrossRefPubMed Berres ML, Koenen RR, Rueland A, Zaldivar MM, Heinrichs D, Sahin H, Schmitz P, Streetz KL, Berg T, Gassler N, Weiskirchen R, Proudfoot A, Weber C, Trautwein C, Wasmuth HE: Antagonism of the chemokine Ccl5 ameliorates experimental liver fibrosis in mice. J Clin Invest. 2010, 120: 4129-4140. 10.1172/JCI41732.PubMedCentralCrossRefPubMed
51.
go back to reference Stock MK, Hammerich L, do O NT, Berres ML, Alsamman M, Heinrichs D, Nellen A, Trautwein C, Tacke F, Wasmuth HE, Sahin H: Met-CCL5 modifies monocyte subpopulations during liver fibrosis regression. Int J Clin Exp Pathol. 2013, 6: 678-685.PubMedCentralPubMed Stock MK, Hammerich L, do O NT, Berres ML, Alsamman M, Heinrichs D, Nellen A, Trautwein C, Tacke F, Wasmuth HE, Sahin H: Met-CCL5 modifies monocyte subpopulations during liver fibrosis regression. Int J Clin Exp Pathol. 2013, 6: 678-685.PubMedCentralPubMed
52.
go back to reference Prosniak M, Faber M, Hanlon CA, Rupprecht CE, Hooper DC, Dietzschold B: Development of a cocktail of recombinant-expressed human rabies virus-neutralizing monoclonal antibodies for postexposure prophylaxis of rabies. J Infect Dis. 2003, 188: 53-56. 10.1086/375247.CrossRefPubMed Prosniak M, Faber M, Hanlon CA, Rupprecht CE, Hooper DC, Dietzschold B: Development of a cocktail of recombinant-expressed human rabies virus-neutralizing monoclonal antibodies for postexposure prophylaxis of rabies. J Infect Dis. 2003, 188: 53-56. 10.1086/375247.CrossRefPubMed
53.
go back to reference de Kruif J, Bakker AB, Marissen WE, Kramer RA, Throsby M, Rupprecht CE, Goudsmit J: A human monoclonal antibody cocktail as a novel component of rabies postexposure prophylaxis. Annu Rev Med. 2007, 58: 359-368. 10.1146/annurev.med.58.061705.145053.CrossRefPubMed de Kruif J, Bakker AB, Marissen WE, Kramer RA, Throsby M, Rupprecht CE, Goudsmit J: A human monoclonal antibody cocktail as a novel component of rabies postexposure prophylaxis. Annu Rev Med. 2007, 58: 359-368. 10.1146/annurev.med.58.061705.145053.CrossRefPubMed
Metadata
Title
Met-CCL5 represents an immunotherapy strategy to ameliorate rabies virus infection
Authors
Ying Huang
Shaozhuo Jiao
Xiaoyan Tao
Qing Tang
Wentao Jiao
Jun Xiao
Xiaoyan Xu
Yanbo Zhang
Guodong Liang
Hongyan Wang
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2014
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-014-0146-y

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