Modulation of the immune response in the nervous system by rabies virus

Current Topics in Microbiology and Immunology

Volumn 289, Issue , 2005, Pages 239-258

  Lafon, M ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CYTOKINE; FAS ANTIGEN; FAS LIGAND; GAMMA INTERFERON; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ACUTE DISEASE; ANIMAL MODEL; ANTIBODY TITER; ANTIGEN EXPRESSION; APOPTOSIS; BRAIN INFECTION; CENTRAL NERVOUS SYSTEM INFECTION; CYTOTOXIC T LYMPHOCYTE; DISEASE TRANSMISSION; HISTOLOGY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RABIES; RABIES VIRUS; REVIEW; SALIVARY GLAND; SPINAL CORD; SPLEEN CELL; T LYMPHOCYTE; VIRUS INFECTION;

EID: 14144249711     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-27320-4_11     Document Type: Review

References (80)

1. Akaike T, Weihe E, Schaefer M, Fu ZF, Zheng YM, Vogel W, Schmidt H, Koprowski H, Dietzschold B (1995) Effect of neurotropic virus infection on neuronal and inducible nitric oxide synthase activity in rat brain. J Neurovirol 1:118-125
2. Alcami A, Koszinowski UH (2000) Viral mechanisms of immune evasion. Trends Microbiol 8:410-418
3. Anilionis A, Wunner WH, Curtis PJ (1981) Structure of the glycoprotein gene in rabies virus. Nature 294:275-278
4. Badley AD, McElhinny JA, Leibson PJ, Lynch DH, Alderson MR, Paya CV (1996) Upregulation of Fas ligand expression by human immunodeficiency virus in human macrophages mediates apoptosis of uninfected T lymphocytes. J Virol 70:199-206
5. Baloul L, Lafon M (2003) Apoptosis and rabies virus neuroinvasion. Biochimie 85:777-788
6. Baloul L, Camelo S, Lafon M (2004) Up-regulation of FasL in the CNS: a mechanism of immune evasion by rabies virus. Journal of Neurovirology (in press)
7. Bechmann I, Mor G, Nilsen J, Eliza M, Nitsch R, Naftolin F (1999) FasL (CD95L, Apo1L) is expressed in the normal rat and human brain: evidence for the existence of an immunological brain barrier. Glia 27:62-74
8. Binder GK, Griffin DE (2001) Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons. Science 293:303-306
9. Bonetti B, Pohl J, Gao YL, Raine CS (1997) Cell death during autoimmune demyelination: effector but not target cells are eliminated by apoptosis. J Immunol 159:5733-5741
10. Camelo S, Castellanos J, Lafage M, Lafon M (2001a) Rabies virus ocular disease: T-cell-dependent protection is under the control of signaling by the p55 tumor necrosis factor alpha receptor, p55TNFR. J Virol 75:3427-3434
11. Camelo S, Lafage M, Galelli A, Lafon M (2001b) Selective role for the p55 Kd TNF-alpha receptor in immune unresponsiveness induced by an acute viral encephalitis. J Neuroimmunol 113:95-108
12. Camelo S, Lafage M, Lafon M (2000) Absence of the p55 Kd TNF-alpha receptor promotes survival in rabies virus acute encephalitis. J Neurovirol 6:507-518
13. Chesler DA, Reiss CS (2002) The role of IFN-gamma in immune responses to viral infections of the central nervous system. Cytokine Growth Factor Rev 13:441-454
14. Chiou SH, Liu JH, Hsu WM, Chen SS, Chang SY, Juan LJ, Lin JC, Yang YT, Wong WW, Liu CY, Lin YS, Liu WT, Wu CW (2001) Up-regulation of Fas ligand expression by human cytomegalovirus immediate-early gene product 2: a novel mechanism in cytomegalovirus-induced apoptosis in human retina. J Immunol 167:4098-4103
15. Choi C, Park JY, Lee J, Lim JH, Shin EC, Ahn YS, Kim CH, Kim SJ, Kim JD, Choi IS, Choi IH (1999) Fas ligand and Fas are expressed constitutively in human astrocytes and the expression increases with IL-1, IL-6, TNF-alpha, or IFN-gamma. J Immunol 162:1889-1895
16. Cippitelli M, Fionda C, Di Bona D, Di Rosa F, Lupo A, Piccoli M, Frati L, Santoni A (2002) Negative regulation of CD95 ligand gene expression by vitamin D3 in T lymphocytes. J Immunol 168:1154-1166
17. Corriveau RA, Huh GS, Shatz CJ (1998) Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21:505-520
18. Dietzschold B, Wunner WH, Wiktor TJ, Lopes AD, Lafon M, Smith CL, Koprowski H (1983) Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proc Natl Acad Sci USA 80:70-74
19. Dockrell DH (2003) The multiple roles of Fas ligand in the pathogenesis of infectious diseases. Clin Microbiol Infect 9:766-779
20. Dockrell DH, Badley AD, Villacian JS, Heppelmann CJ, Algeciras A, Ziesmer S, Yagita H, Lynch DH, Roche PC, Leibson PJ, Paya CV (1998) The expression of Fas ligand by macrophages and its upregulation by human immunodeficiency virus infection. J Clin Invest 101:2394-2405
21. Etessami R, Conzelmann KK, Fadai-Ghotbi B, Natelson B, Tsiang H, Ceccaldi PE (2000) Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: an in vitro and in vivo study. J Gen Virol 81:2147-2153
22. Flugel A, Schwaiger FW, Neumann H, Medana I, Willem M, Wekerle H, Kreutzberg GW, Graeber MB (2000) Neuronal FasL induces cell death of encephalitogenic T lymphocytes. Brain Pathol 10:353-364
23. Galelli A, Baloul L, Lafon M (2000) Abortive rabies virus central nervous infection is controlled by T lymphocyte local recruitment and induction of apoptosis. J Neurovirol 6:359-372
24. Ghorpade A, Holler S, Borgmann K, Persidsky R, Wu L (2003) HIV-1 and IL-1 beta regulate Fas ligand expression in human astrocytes through the NF-kappa B pathway. J Neuroimmunol 141:141-149
25. Gillet JP, Derer P, Tsiang H (1986) Axonal transport of rabies virus in the central nervous system of the rat. J Neuropathol Exp Neurol 45:619-634
26. Giuliani F, Goodyer CG, Antel JP, Yong VW (2003) Vulnerability of human neurons to T cell-mediated cytotoxicity. J Immunol 171:368-379
27. Green DR, Ferguson TA (2001) The role of Fas ligand in immune privilege. Nat Rev Mol Cell Biol 2:917-924
28. Griffin DE (2003) Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol 3:493-502
29. Griffith TS, Brunner T, Fletcher SM, Green DR, Ferguson TA (1995) Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 270:1189-1192
30. Havert MB, Schofield B, Griffin DE, Irani DN (2000) Activation of divergent neuronal cell death pathways in different target cell populations during neuroadapted sindbis virus infection of mice. J Virol 74:5352-5356
31. Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B (1998) Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol 72:3711-3719
32. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290:2155-2159
33. Irwin DJ, Wunner WH, Ertl HC, Jackson AC (1999) Basis of rabies virus neurovirulence in mice: expression of major histocompatibility complex class I and class II mRNAs. J Neurovirol 5:485-494
34. Iwasaki Y, Gerhard W, Clark HF (1977) Role of host immune response in the development of either encephalitic or paralytic disease after experimental rabies infection in mice. Infect Immun 18:220-225
35. Joly E, Oldstone MB (1992) Neuronal cells are deficient in loading peptides onto MHC class I molecules. Neuron 8:1185-1190
36. Kelly RM, Strick PL (2000) Rabies as a transneuronal tracer of circuits in the central nervous system. J Neurosci Methods 103:63-71
37. + T cells and major histocompatibility complex class I expression in the central nervous system of mice infected with neurovirulent Sindbis virus. J Virol 74:6117-6125
38. Kohji T, Matsumoto Y (2000) Coexpression of Fas/FasL and Bax on brain and infiltrating T cells in the central nervous system is closely associated with apoptotic cell death during autoimmune encephalomyelitis. J Neuroimmunol 106:165-171
39. Komatsu T, Bi Z, Reiss CS (1996) Interferon-gamma induced type I nitric oxide synthase activity inhibits viral replication in neurons. J Neuroimmunol 68:101-108
40. Koprowski H, Zheng YM, Heber-Katz E, Fraser N, Rorke L, Fu ZF, Hanlon C, Dietzschold B (1993) In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc Natl Acad Sci USA 90:3024-3027
41. Kundig TM, Hengartner H, Zinkernagel RM (1993) T cell-dependent IFN-gamma exerts an antiviral effect in the central nervous system but not in peripheral solid organs. J Immunol 150:2316-2321
42. Lafon M (2004) Subversive neuroinvasive strategy of rabies virus. Archives of Virology S18:149-159
43. Lafon M, Edelman L, Bouvet JP, Lafage M, Montchatre E (1990) Human monoclonal antibodies specific for the rabies virus glycoprotein and N protein. J Gen Virol 71:1689-1696
44. Lafon M, Wiktor TJ, Macfarlan RI (1983) Antigenic sites on the CVS rabies virus glycoprotein: analysis with monoclonal antibodies. J Gen Virol 64:843-851
45. Lay S, Prehaud C, Dietzschold B, Lafon M (2003) Glycoprotein of nonpathogenic rabies viruses is a major inducer of apoptosis in human jurkat T cells. Ann NY Acad Sci 1010:577-581
46. Lee MO, Choi YH, Shin EC, Kang HJ, Kim YM, Jeong SY, Seong JK, Yu DY, Cho H, Park JH, Kim SJ (2002) Hepatitis B virus X protein induced expression of interleukin 18 (IL-18): a potential mechanism for liver injury caused by hepatitis B virus (HBV) infection. J Hepatol 37:380-386
47. Licon Luna RM, Lee E, Mullbacher A, Blanden RV, Langman R, Lobigs M (2002) Lack of both Fas ligand and perforin protects from flavivirus-mediated encephalitis in mice. J Virol 76:3202-3211
48. Li-Weber M, Krammer PH (2003) Function and regulation of the CD95 (APO-1/Fas) ligand in the immune system. Semin Immunol 15:145-157
49. Li-Weber M, Laur O, Dern K, Krammer PH (2000) T cell activation-induced and HIV tat-enhanced CD95(APO-1/Fas) ligand transcription involves NF-kappaB. Eur J Immunol 30:661-670
50. Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ, Olsen AL, Carter EE, Barber RD, Baban DF, Kingsman SM, Kingsman AJ, O'Malley K, Mitrophanous KA (2001) Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum Mol Genet 10:2109-2121
51. Medana I, Li Z, Flugel A, Tschopp J, Wekerle H, Neumann H (2001) Fas ligand (CD95L) protects neurons against perforin-mediated T lymphocyte cytotoxicity. J Immunol 167:674-681
52. + T lymphocytes is effected through the Fas/FasL, but not the perforin pathway. Eur J Immunol 30:3623-3633
53. Miller A, Morse HC, 3rd, Winkelstein J, Nathanson N (1978) The role of antibody in recovery from experimental rabies. I. Effect of depletion of B and T cells. J Immunol 121:321-326
54. Morimoto K, Foley HD, McGettigan JP, Schnell MJ, Dietzschold B (2000) Reinvestigation of the role of the rabies virus glycoprotein in viral pathogenesis using a reverse genetics approach. J Neurovirol 6:373-381
55. Morimoto K, Hooper DC, Carbaugh H, Fu ZF, Koprowski H, Dietzschold B (1998) Rabies virus quasispecies: implications for pathogenesis. Proc Natl Acad Sci USA 95:3152-3156
56. Morimoto K, Hooper DC, Spitsin S, Koprowski H, Dietzschold B (1999) Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J Virol 73:510-518
57. Pereira RA, Simmons A (1999) Cell surface expression of H2 antigens on primary sensory neurons in response to acute but not latent herpes simplex virus infection in vivo. J Virol 73:6484-6489
58. Pereira RA, Tscharke DC, Simmons A (1994) Upregulation of class I major histocompatibility complex gene expression in primary sensory neurons, satellite cells, and Schwann cells of mice in response to acute but not latent herpes simplex virus infection in vivo. J Exp Med 180:841-850
59. Poch O, Tordo N, Keith G (1988) Sequence of the 3386 3′ nucleotides of the genome of the AVO1 strain rabies virus: structural similarities in the protein regions involved in transcription. Biochimie 70:1019-1029
60. Prehaud C, Lay S, Dietzschold B, Lafon M (2003) Glycoprotein of nonpathogenic rabies viruses is a key determinant of human cell apoptosis. J Virol 77:10537-10547
61. Raftery MJ, Schwab M, Eibert SM, Samstag Y, Walczak H, Schonrich G (2001) Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 15:997-1009
62. Redwine JM, Buchmeier MJ, Evans CF (2001) In vivo expression of major histocompatibility complex molecules on oligodendrocytes and neurons during viral infection. Am J Pathol 159:1219-1224
63. Schlitt BP, Felrice M, Jelachich ML, Lipton HL (2003) Apoptotic cells, including macrophages, are prominent in Theiler's virus-induced inflammatory, demyelinating lesions. J Virol 77:4383-4388
64. Seabrook TJ, Hay JB (2001) Intracerebroventricular infusions of TNF-alpha preferentially recruit blood lymphocytes and induce a perivascular leukocyte infiltrate. J Neuroimmunol 113:81-88
65. Seif I, Coulon P, Rollin PE, Flamand A (1985) Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J Virol 53:926-934
66. Shin DH, Lee E, Kim HJ, Kim S, Cho SS, Chang KY, Lee WJ (2002) Fas ligand mRNA expression in the mouse central nervous system. J Neuroimmunol 123:50-57
67. Smith JS, McCelland CL, Reid FL, Baer GM (1982) Dual role of the immune response in street rabiesvirus infection of mice. Infect Immun 35:213-221
68. Suda T, Nagata S (1994) Purification and characterization of the Fas-ligand that induces apoptosis. J Exp Med 179:873-879
69. Sugamata M, Miyazawa M, Mori S, Spangrude GJ, Ewalt LC, Lodmell DL (1992) Paralysis of street rabies virus-infected mice is dependent on T lymphocytes. J Virol 66:1252-1260
70. Tanner JE, Alfieri C (1999) Epstein-Barr virus induces Fas (CD95) in T cells and Fas ligand in B cells leading to T-cell apoptosis. Blood 94:3439-3447
71. Thoulouze MI, Lafage M, Montano-Hirose JA, Lafon M (1997) Rabies virus infects mouse and human lymphocytes and induces apoptosis. J Virol 71:7372-7380
72. Thoulouze MI, Lafage M, Yuste VJ, Baloul L, Edelman L, Kroemer G, Israel N, Susin SA, Lafon M (2003a) High level of Bcl-2 counteracts apoptosis mediated by a live rabies virus vaccine strain and induces long-term infection. Virology 314:549-561
73. Thoulouze MI, Lafage M, Yuste VJ, Kroemer G, Susin SA, Israel N, Lafon M (2003b) Apoptosis inversely correlates with rabies virus neurotropism. Ann NY Acad Sci 1010:598-603
74. Tordo N, Poch O, Ermine A, Keith G, Rougeon F (1986) Walking along the rabies genome: is the large G-L intergenic region a remnant gene? Proc Natl Acad Sci USA 83:3914-3918
75. Ubol S, Hiriote W, Anuntagool N, Utaisincharoen P (2001) A radical form of nitric oxide suppresses RNA synthesis of rabies virus. Virus Res 81:125-132
76. Van Dam AM, Bauer J, Man AHWK, Marquette C, Tilders FJ, Berkenbosch F (1995) Appearance of inducible nitric oxide synthase in the rat central nervous system after rabies virus infection and during experimental allergic encephalomyelitis but not after peripheral administration of endotoxin. J Neurosci Res 40:251-260
77. Weiland F, Cox JH, Meyer S, Dahme E, Reddehase MJ (1992) Rabies virus neuritic paralysis: immunopathogenesis of nonfatal paralytic rabies. J Virol 66:5096-5099
78. Xiang ZQ, Knowles BB, McCarrick JW, Ertl HC (1995) Immune effector mechanisms required for protection to rabies virus. Virology 214:398-404
79. Xu XN, Screaton GR, Gotch FM, Dong T, Tan R, Almond N, Walker B, Stebbings R, Kent K, Nagata S, Stott JE, McMichael AJ (1997) Evasion of cytotoxic T lymphocyte (CTL) responses by nef-dependent induction of Fas ligand (CD95L) expression on simian immunodeficiency virus-infected cells. J Exp Med 186:7-16
80. + B lymphocytes susceptible to Fas/Fas ligand-mediated fratricide. J Immunol 168:3965-3973