1887

Chapter 26 : Theiler’s Virus Central Nervous System Infection

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Theiler’s Virus Central Nervous System Infection, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816698/9781555816032_Chap26-1.gif /docserver/preview/fulltext/10.1128/9781555816698/9781555816032_Chap26-2.gif

Abstract:

The genus is divided into two species: the species, which includes encephalomyocarditis virus (EMCV) and mengovirus, and the species, which includes Theiler’s murine encephalomyelitis virus (TMEV), Vilyuisk human encephalomyelitis virus (VHEV), and Saffold virus (SAFV). This chapter discusses members of the genus and distinctive characteristics of these viruses. It focuses on the pathogenesis of TMEV-induced disease because of the extensive investigations of this topic as well as the remarkable ability of this virus to establish lifelong infection of the central nervous system (CNS) and to produce an immune-mediated demyelinating disease. There are many features of cardioviruses, and especially TMEV, that make them attractive for pathogenesis studies, including the following: the unusual and rather unique characteristics of TMEV strains and TMEV-induced diseases (neurovirulent versus persistent strains, acute versus chronic disease, virus-induced versus immune-mediated pathology); the ability of some strains to persist in the host in the absence of latency or genome integration; the substantial knowledge concerning cardioviruses along with powerful tools for their study; the experimental model system of TMEV (and EMCV) infection in the mouse, which is the virus’ natural host. The recent identification of SAFV infection as a frequent one in humans has focused attention on whether this virus causes disease in humans. Furthermore, the identification of the human SAFV indicates that efforts investigating the involvement of cardioviruses as a cause of Vilyuisk encephalomyelitis should be renewed.

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1.
Figure 1.

Phylogenetic tree of the P1 capsid coding sequences of the genus. Three of the eight lineages of SAFV are shown. Note: sequences closest to SAFV isolates are those of TRV; VHEV is phylogenetically related to TMEV strains. (The figure was kindly provided by Nick Knowles.)

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2.
Figure 2.

Schematic representation of genomes of representative cardioviruses EMCV, SAFV, and TMEV. Features that differ from the prototypic poliovirus are outlined: structures of the 5′ and 3′ NCRs, CRE in the VP2 region, L, and protein 2A promoting a “ribosomal skip” and hence primary cleavage of the polyprotein at the NPG/P sequence of the 2A-2B boundary. Note that EMCV has a poly(C) tract in the 5′ NCR. TMEV (but not SAFV) encodes the L* protein from an ORF that overlaps the L, VP2, and VP4 coding regions.

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3.
Figure 3.

Alignment of predicted L protein sequences from EMCV (mengovirus), SAFV, TMEV (the neurovirulent GDVII strain), and TMEV (the persistent DA strain). The domains identified in the sequence are indicated. The boxed Y and T residues in the mengovirus sequence show putative phosphorylation sites.

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4.
Figure 4.

Trafficking and persistence of TMEV in the CNS. Cell-to-cell trafficking of the virus between neurons and oligoden-drocytes may represent a novel strategy to escape local CTL responses as well as neutralization by antibodies. (1) Infection of neuron; (2) slow replication in neurons and axonal transport; (3) noncytolytic passage from neuron to myelin; (4) trafficking through cytoplasmic channels within oligodendrocytes; (5) passage from myelin to neuron (which can be remote from the previously infected neuron); (6) some infected oligodendrocytes release viral particles; (7) infection of macrophages (with a constant infiltration of macrophages from peripheral monocytes). BBB, blood-brain barrier.

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816698.ch26
1. Abed, Y., and, G. Boivin. 2008. New Saffold cardioviruses in 3 children, Canada. Emerg. Infect. Dis. 14:834846.
2. Abzug, M. J., and, R. W. Tyson. 2000. Picornavirus infection in early murine gestation: significance of maternal illness. Placenta 21:840846.
3. Abzug, M. J., and, R. W. Tyson. 2000. Protection of murine gestational tissues from picornavirus infection in the preim-plantation period. Placenta 21:422426.
4. Alley, J.,, S. Khasabov,, D. Simone,, A. Beitz,, M. Rodriguez, and, M. K. Njenga. 2003. More severe neurologic deficits in SJL/J male than female mice following Theiler’s virus-induced CNS demyelination. Exp. Neurol. 180:1424.
5. Al-Salleeh, F., and, T. M. Petro. 2007. TLR3 and TLR7 are involved in expression of IL-23 subunits while TLR3 but not TLR7 is involved in expression of IFN-beta by Theiler’s virus-infected RAW264.7 cells. Microbes Infect. 9:13841392.
6. Aminev, A. G.,, S. P. Amineva, and, A. C. Palmenberg. 2003. Encephalomyocarditis viral protein 2A localizes to nucleoli and inhibits cap-dependent mRNA translation. Virus Res. 95:4557.
7. Asakura, K.,, H. Murayama,, T. Himeda, and, Y. Ohara. 2007. Expression of L* protein of Theiler’s murine encephalomyelitis virus in the chronic phase of infection. J. Gen. Virol. 88:22682274.
8. Aubert, C.,, M. Chamorro, and, M. Brahic. 1987. Identification of Theiler’s virus infected cells in the central nervous system of the mouse during demyelinating disease. Microb. Pathog. 3:319326.
9. Azoulay, A.,, M. Brahic, and, J. F. Bureau. 1994. FVB mice transgenic for the H-2Db gene become resistant to persistent infection by Theiler’s virus. J. Virol. 68:40494052.
10. Azoulay-Cayla, A.,, S. Syan,, M. Brahic, and, J. F. Bureau. 2001. Roles of the H-2Db and H-Kb genes in resistance to persistent Theiler’s murine encephalomyelitis virus infection of the central nervous system. J. Gen. Virol. 82:10431047.
11. Baida, G.,, B. Popko,, R. L. Wollmann,, S. Stavrou,, W. Lin,, M. Tretiakova,, T. N. Krausz, and, R. P. Roos. 2008. A subgenomic segment of Theiler’s murine encephalomyelitis virus RNA causes demyelination. J. Virol. 82:58795886.
12. Bardina, M. V.,, P. V. Lidsky,, E. V. Sheval,, K. V. Fominykh,, F. J. van Kuppeveld,, V. Y. Polyakov, and, V. I. Agol. 2009. Mengovirus-induced rearrangement of the nuclear pore complex: hijacking cellular phosphorylation machinery. J. Virol. 83:31503161.
13. Bennett, J. L.,, A. Elhofy,, I. Charo,, S. D. Miller,, M. C. Dal Canto, and, W. J. Karpus. 2007. CCR2 regulates development of Theiler’s murine encephalomyelitis virus-induced demyelin-ating disease. Viral Immunol. 20:1933.
14. Bihl, F.,, C. Pena-Rossi,, J. L. Guenet,, M. Brahic, and, J. F. Bureau. 1997. The shiverer mutation affects the persistence of Theiler’s virus in the central nervous system. J. Virol. 71:50255030.
15. Blinkova, O.,, A. Kapoor,, J. Victoria,, M. Jones,, N. Wolfe,, A. Naeem,, S. Shaukat,, S. Sharif,, M. M. Alam,, M. Angez,, S. Zaidi, and, E. L. Delwart. 2009. Cardioviruses are genetically diverse and cause common enteric infections in South Asian children. J. Virol. 83:46314641.
16. Borson, N. D.,, C. Paul,, X. Lin,, W. K. Nevala,, M. A. Straus-bauch,, M. Rodriguez, and, P. J. Wettstein. 1997. Brain-infiltrating cytolytic T lymphocytes specific for Theiler’s virus recognize H2Db molecules complexed with a viral VP2 peptide lacking a consensus anchor residue. J. Virol. 71:52445250.
17. Brahic, M.,, J. F. Bureau, and, T. Michiels. 2005. The genetics of the persistent infection and demyelinating disease caused by Theiler’s virus. Annu. Rev. Microbiol. 59:279298.
18. Brahic, M.,, W. G. Stroop, and, J. R. Baringer. 1981. Theiler’s virus persists in glial cells during demyelinating disease. Cell 26:123128.
19. Calenoff, M. A.,, K. S. Faaberg, and, H. L. Lipton. 1990. Genomic regions of neurovirulence and attenuation in Theiler murine encephalomyelitis virus. Proc. Natl. Acad. Sci. USA 87:978982.
20. Chen, H. H.,, W. P. Kong, and, R. P. Roos. 1995. The leader peptide of Theiler’s murine encephalomyelitis virus is a zinc-binding protein. J. Virol. 69:80768078.
21. Chen, H. H.,, W. P. Kong,, L. Zhang,, P. L. Ward, and, R. P. Roos. 1995. A picornaviral protein synthesized out of frame with the polyprotein plays a key role in a virus- induced immune-mediated demyelinating disease. Nat. Med. 1:927931.
22. Chiu, C. Y.,, A. L. Greninger,, K. Kanada,, T. Kwok,, K. F. Fischer,, C. Runckel,, J. K. Louie,, C. A. Glaser,, S. Yagi,, D. P. Schnurr,, T. D. Haggerty,, J. Parsonnet,, D. Ganem, and, J. L. DeRisi. 2008. Identification of cardioviruses related to Theiler’s murine en-cephalomyelitis virus in human infections. Proc. Natl. Acad. Sci. USA 105:1412414129.
23. Coman, I.,, G. Barbin,, P. Charles,, B. Zalc, and, C. Lubetzki. 2005. Axonal signals in central nervous system myelination, demyelination and remyelination. J. Neurol. Sci. 233:6771.
24. Cornilescu, C. C.,, F. W. Porter,, K. Q. Zhao,, A. C. Palmenberg, and, J. L. Markley. 2008. NMR structure of the mengovirus Leader protein zinc-finger domain. FEBS Lett. 582:896900.
25. Croxford, J. L.,, J. K. Olson, and, S. D. Miller. 2002. Epitope spreading and molecular mimicry as triggers of autoimmunity in the Theiler’s virus-induced demyelinating disease model of multiple sclerosis. Autoimmun. Rev. 1:251260.
26. Dal Canto, M. C., and, H. L. Lipton. 1975. Primary demyelin-ation in Theiler’s virus infection. An ultrastructural study. Lab. Investig. 33:626637.
27. Deb, C., and, C. L. Howe. 2009. Functional characterization of mouse spinal cord infiltrating CD8+ lymphocytes. J. Neuroim-munol. 214:3342.
28. Deb, C.,, R. G. Lafrance-Corey,, L. Zoecklein,, L. Papke,, M. Rodriguez, and, C. L. Howe. 2009. Demyelinated axons and motor function are protected by genetic deletion of perforin in a mouse model of multiple sclerosis. J. Neuropathol. Exp. Neurol. 68:10371048.
29. Delhaye, S.,, S. Paul,, G. Blakqori,, M. Minet,, F. Weber,, P. Staeheli, and, T. Michiels. 2006. Neurons produce type I interferon during viral encephalitis. Proc. Natl. Acad. Sci. USA 103:78357840.
30. Delhaye, S.,, V. van Pesch, and, T. Michiels. 2004. The leader protein of Theiler’s virus interferes with nucleocytoplasmic trafficking of cellular proteins. J. Virol. 78:43574362.
31. Denis, P.,, H. D. Liebig,, N. Nowotny,, C. Billinis,, O. Papadopou-los,, R. S. O’Hara,, N. J. Knowles, and, F. Koenen. 2006. Genetic variability of encephalomyocarditis virus (EMCV) isolates. Vet. Microbiol. 113:112.
32. Dethlefs, S.,, N. Escriou,, M. Brahic,, S. van der Werf, and, E. L. Larsson-Sciard. 1997. Theiler’s virus and Mengo virus induce cross-reactive cytotoxic T lymphocytes restricted to the same immunodominant VP2 epitope in C57BL/6 mice. J. Virol. 71:53615365.
33. Donnelly, M. L.,, L. E. Hughes,, G. Luke,, H. Mendoza,, E. ten Dam,, D. Gani, and, M. D. Ryan. 2001. The ‘cleavage’ activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring ‘2A-like’ sequences. J. Gen. Virol. 82:10271041.
34. Donnelly, M. L.,, G. Luke,, A. Mehrotra,, X. Li,, L. E. Hughes,, D. Gani, and, M. D. Ryan. 2001. Analysis of the aphthovirus 2A/2B polyprotein ‘cleavage’ mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal ‘skip.’ J. Gen. Virol. 82:10131025.
35. Drescher, K. M.,, P. D. Murray,, C. S. David,, L. R. Pease, and, M. Rodriguez. 1999. CNS cell populations are protected from virus-induced pathology by distinct arms of the immune system. Brain Pathol. 9:2131.
36. Drexler, J. F.,, L. K. Luna,, A. Stocker,, P. S. Almeida,, T. C. Ri-beiro,, N. Petersen,, P. Herzog,, C. Pedroso,, H. I. Huppertz,, C. Ribeiro Hda, Jr.,, S. Baumgarte, and, C. Drosten. 2008. Circulation of 3 lineages of a novel Saffold cardiovirus in humans. Emerg. Infect. Dis. 14:13981405.
37. Duke, G. M.,, J. E. Osorio, and, A. C. Palmenberg. 1990. Attenuation of Mengo virus through genetic engineering of the 5′ noncoding poly(C) tract. Nature 343:474476.
38. Duque, H., and, A. C. Palmenberg. 2001. Phenotypic characterization of three phylogenetically conserved stem-loop motifs in the mengovirus 3′ untranslated region. J. Virol. 75:31113120.
39. Dvorak, C. M.,, D. J. Hall,, M. Hill,, M. Riddle,, A. Pranter,, J. Dillman,, M. Deibel, and, A. C. Palmenberg. 2001. Leader protein of encephalomyocarditis virus binds zinc, is phosphory-lated during viral infection, and affects the efficiency of genome translation. Virology 290:261271.
40. Fan, J.,, K. N. Son,, S. Y. Arslan,, Z. Liang, and, H. L. Lipton. 2009. Theiler’s murine encephalomyelitis virus leader protein is the only nonstructural protein tested that induces apoptosis when transfected into mammalian cells. J. Virol. 83:65466553.
41. Fiette, L.,, C. Aubert,, U. Muller,, S. Huang,, M. Aguet,, M. Brahic, and, J. F. Bureau. 1995. Theiler’s virus infection of 129Sv mice that lack the interferon alpha/beta or interferon gamma receptors. J. Exp. Med. 181:20692076.
42. Fu, J.,, M. Rodriguez, and, R. P. Roos. 1990. Strains from both Theiler’s virus subgroups encode a determinant for demyelination. J. Virol. 64:63456348.
43. Fuller, A.,, H. Yahikozawa,, E. Y. So,, M. Dal Canto,, C. S. Koh,, C. J. Welsh, and, B. S. Kim. 2007. Castration of male C57L/J mice increases susceptibility and estrogen treatment restores resistance to Theiler’s virus-induced demyelinating disease. J. Neurosci. Res. 85:871881.
44. Gerety, S. J.,, W. J. Karpus,, A. R. Cubbon,, R. G. Goswami,, M. K. Rundell,, J. D. Peterson, and, S. D. Miller. 1994. Class II-restricted T cell responses in Theiler’s murine encephalo-myelitis virus-induced demyelinating disease. V. Mapping of a dominant immunopathologic VP2 T cell epitope in susceptible SJL/J mice. J. Immunol. 152:908918.
45. Gerety, S. J.,, M. K. Rundell,, M. C. Dal Canto, and, S. D. Miller. 1994. Class II-restricted T cell responses in Theiler’s murine encephalomyelitis virus-induced demyelinating disease. VI. Potentiation of demyelination with and characterization of an immunopathologic CD4+ T cell line specific for an immuno-dominant VP2 epitope. J. Immunol. 152:919929.
46. Ghadge, G. D.,, L. Ma,, S. Sato,, J. Kim, and, R. P. Roos. 1998. A protein critical for a Theiler’s virus-induced immune system-mediated demyelinating disease has a cell type-specific anti-apoptotic effect and a key role in virus persistence. J. Virol. 72:86058612.
47. Gitlin, L.,, W. Barchet,, S. Gilfillan,, M. Cella,, B. Beutler,, R. A. Flavell,, M. S. Diamond, and, M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyri-bocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103:84598464.
48. Gomez, R. M.,, J. E. Rinehart,, R. Wollmann, and, R. P. Roos. 1996. Theiler’s murine encephalomyelitis virus-induced cardiac and skeletal muscle disease. J. Virol. 70:89268933.
49. Grant, R. A.,, D. J. Filman,, R. S. Fujinami,, J. P. Icenogle, and, J. M. Hogle. 1992. Three-dimensional structure of Theiler virus. Proc. Natl. Acad. Sci. USA 89:20612065.
50. Grobler, D. G.,, J. P. Raath,, L. E. Braack,, D. F. Keet,, G. H. Gerdes,, B. J. Barnard,, N. P. Kriek,, J. Jardine, and, R. Swane-poel. 1995. An outbreak of encephalomyocarditis-virus infection in free-ranging African elephants in the Kruger National Park. Onderstepoort J. Vet. Res. 62:97108.
51. Groppo, R., and, A. C. Palmenberg. 2007. Cardiovirus 2A protein associates with 40S but not 80S ribosome subunits during infection. J. Virol. 81:1306713074.
52. Hato, S. V.,, C. Ricour,, B. M. Schulte,, K. H. Lanke,, M. de Bruijni,, J. Zoll,, W. J. Melchers,, T. Michiels, and, F. J. van Kuppeveld. 2007. The mengovirus leader protein blocks interferon-alpha/beta gene transcription and inhibits activation of interferon regulatory factor 3. Cell. Microbiol. 9:29212930.
53. Hoffman, L. M.,, B. T. Fife,, W. S. Begolka,, S. D. Miller, and, W. J. Karpus. 1999. Central nervous system chemokine expression during Theiler’s virus-induced demyelinating disease. J. Neurovirol. 5:635642.
54. Hou, W.,, H. S. Kang, and, B. S. Kim. 2009. Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J. Exp. Med. 206:313328.
55. Howe, C. L.,, J. D. Adelson, and, M. Rodriguez. 2007. Absence of perforin expression confers axonal protection despite de-myelination. Neurobiol. Dis. 25:354359.
56. Howe, C. L.,, D. Ure,, J. D. Adelson,, R. LaFrance-Corey,, A. Johnson, and, M. Rodriguez. 2007. CD8+ T cells directed against a viral peptide contribute to loss of motor function by disrupting axonal transport in a viral model of fulminant demyelination. J. Neuroimmunol. 188:1321.
57. Inoue, A.,, C. S. Koh,, M. Yamazaki,, H. Yahikozawa,, M. Ichi-kawa,, H. Yagita, and, B. S. Kim. 1998. Suppressive effect on Theiler’s murine encephalomyelitis virus-induced demyelin-ating disease by the administration of anti-IL-12 antibody. J. Immunol. 161:55865593.
58. Jackson, R. J., and, A. Kaminski. 1995. Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA 1:9851000.
59. Jarousse, N.,, S. Syan,, C. Martinat, and, M. Brahic. 1998. The neurovirulence of the DA and GDVII strains of Theiler’s virus correlates with their ability to infect cultured neurons. J. Virol. 72:72137220.
60. Jin, Y. H.,, B. Kang, and, B. S. Kim. 2009. Theiler’s virus infection induces a predominant pathogenic CD4+ T cell response to RNA polymerase in susceptible SJL/J mice. J. Virol. 83:1098110992.
61. Jnaoui, K., and, T. Michiels. 1998. Adaptation of Theiler’s virus to L929 cells: mutations in the putative receptor binding site on the capsid map to neutralization sites and modulate viral persistence. Virology 244:397404.
62. Jnaoui, K., and, T. Michiels. 1999. Analysis of cellular mutants resistant to Theiler’s virus infection: differential infection of L929 cells by persistent and neurovirulent strains. J. Virol. 73:72487254.
63. Jnaoui, K.,, M. Minet, and, T. Michiels. 2002. Mutations that affect the tropism of DA and GDVII strains of Theiler’s virus in vitro influence sialic acid binding and pathogenicity. J. Virol. 76:81388147.
64. Johnson, A. J.,, M. K. Njenga,, M. J. Hansen,, S. T. Kuhns,, L. Chen,, M. Rodriguez, and, L. R. Pease. 1999. Prevalent class I-restricted T-cell response to the Theiler’s virus epitope Db:VP2121-130 in the absence of endogenous CD4 help, tumor necrosis factor alpha, gamma interferon, perforin, or co- stimulation through CD28. J. Virol. 73:37023708.
65. Jones, M. S.,, V. V. Lukashov,, R. D. Ganac, and, D. P. Schnurr. 2007. Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J. Clin. Microbiol. 45:21442150.
66. Kappel, C. A.,, R. W. Melvold, and, B. S. Kim. 1990. Influence of sex on susceptibility in the Theiler’s murine encephalomy-elitis virus model for multiple sclerosis. J. Neuroimmunol. 29:1519.
67. Karpus, W. J.,, K. J. Kennedy,, B. T. Fife,, J. L. Bennett,, M. C. Dal Canto,, S. L. Kunkel, and, N. W. Lukacs. 2006. Anti-CCL2 treatment inhibits Theiler’s murine encephalomyelitis virus-induced demyelinating disease. J. Neurovirol. 12:251261.
68. Kato, H.,, O. Takeuchi,, S. Sato,, M. Yoneyama,, M. Yamamoto,, K. Matsui,, S. Uematsu,, A. Jung,, T. Kawai,, K. J. Ishii,, O. Yama-guchi,, K. Otsu,, T. Tsujimura,, C. S. Koh,, C. Reis e Sousa,, Y. Matsuura,, T. Fujita, and, S. Akira. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101105.
69. Kim, B. S.,, J. P. Palma,, D. Kwon, and, A. C. Fuller. 2005. Innate immune response induced by Theiler’s murine encephalomy-elitis virus infection. Immunol. Res. 31:112.
70. Kim, B. S., and, J. P. Palna. 1999. Immune mechanisms of Theiler’s virus-induced demyelination. Exp. Mol. Med. 31:115121.
71. Knowles, N. J.,, N. D. Dickinson,, G. Wilsden,, E. Carra,, E. Broc-chi, and, F. De Simone. 1998. Molecular analysis of encepha-lomyocarditis viruses isolated from pigs and rodents in Italy. Virus Res. 57:5362.
72. Kong, W. P.,, G. D. Ghadge, and, R. P. Roos. 1994. Involvement of cardiovirus leader in host cell-restricted virus expression. Proc. Natl. Acad. Sci. USA 91:17961800.
73. Kong, W. P., and, R. P. Roos. 1991. Alternative translation initiation site in the DA strain of Theiler’s murine encephalomyelitis virus. J. Virol. 65:33953399.
74. Kumar, A. S.,, P. Kallio,, M. Luo, and, H. L. Lipton. 2003. Amino acid substitutions in VP2 residues contacting sialic acid in low-neurovirulence BeAn virus dramatically reduce viral binding and spread of infection. J. Virol. 77:27092716.
75. Levillayer, F.,, M. Mas,, F. Levi-Acobas,, M. Brahic, and, J. F. Bureau. 2007. Interleukin 22 is a candidate gene for Tmevp3, a locus controlling Theiler’s virus-induced neurological diseases. Genetics 176:18351844.
76. Liang, Z.,, A. S. Kumar,, M. S. Jones,, N. J. Knowles, and, H. L. Lipton. 2008. Phylogenetic analysis of the species Theilovirus: emerging murine and human pathogens. J. Virol. 82:1154511554.
77. Lidsky, P. V.,, S. Hato,, M. V. Bardina,, A. G. Aminev,, A. C. Palmenberg,, E. V. Sheval,, V. Y. Polyakov,, F. J. van Kuppeveld, and, V. I. Agol. 2006. Nucleocytoplasmic traffic disorder induced by cardioviruses. J. Virol. 80:27052717.
78. Lin, X.,, R. P. Roos,, L. R. Pease,, P. Wettstein, and, M. Rodriguez. 1999. A Theiler’s virus alternatively initiated protein inhibits the generation of H-2K-restricted virus-specific cytotoxicity. J. Immunol. 162:1724.
79. Lipton, H. L. 1978. Characterization of the TO strains of Theiler’s mouse encephalomyelitis viruses. Infect. Immun. 20:869872.
80. Lipton, H. L. 1975. Theiler’s virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect. Immun. 11:11471155.
81. Lipton, H. L.,, A. S. Kumar,, S. Hertzler, and, H. V. Reddi. 2006. Differential usage of carbohydrate co-receptors influences cellular tropism of Theiler’s murine encephalomyelitis virus infection of the central nervous system. Glycoconj. J. 23:3949.
82. Lipton, H. L.,, A. S. M. Kumar, and, S. Hertzler. 2007. Cardioviruses: encephalomyocarditis virus and Theiler’s murine en-cephalomyelitis virus, p. 311–323. In J. G. Fox et al. (ed.), The Mouse in Biomedical Research, 2nd ed. Elsevier, Amsterdam, The Netherlands.
83. Lipton, H. L., and, R. Melvold. 1984. Genetic analysis of susceptibility to Theiler’s virus-induced demyelinating disease in mice. J. Immunol. 132:18211825.
84. Lipton, H. L.,, G. Twaddle, and, M. L. Jelachich. 1995. The predominant virus antigen burden is present in macrophages in Theiler’s murine encephalomyelitis virus-induced demyelinating disease. J. Virol. 69:25252533.
85. Lobert, P. E.,, N. Escriou,, J. Ruelle, and, T. Michiels. 1999. A coding RNA sequence acts as a replication signal in cardioviruses. Proc. Natl. Acad. Sci. USA 96:1156011565.
86. Luke, G. A.,, P. de Felipe,, A. Lukashev,, S. E. Kallioinen,, E. A. Bruno, and, M. D. Ryan. 2008. Occurrence, function and evolutionary origins of ‘2A-like’ sequences in virus genomes. J. Gen. Virol. 89:10361042.
87. Luo, M.,, K. S. Toth,, L. Zhou,, A. Pritchard, and, H. L. Lipton. 1996. The structure of a highly virulent Theiler’s murine en-cephalomyelitis virus (GDVII) and implications for determinants of viral persistence. Virology 220:246250.
88. Lyman, M. A.,, H. G. Lee,, B. S. Kang,, H. K. Kang, and, B. S. Kim. 2002. Capsid-specific cytotoxic T lymphocytes recognize three distinct H-2Db-restricted regions of the BeAn strain of Theiler’s virus and exhibit different cytokine profiles. J. Virol. 76:31253134.
89. Lyman, M. A.,, J. Myoung,, M. Mohindru, and, B. S. Kim. 2004. Quantitative, not qualitative, differences in CD8+ T cell responses to Theiler’s murine encephalomyelitis virus between resistant C57BL/6 and susceptible SJL/J mice. Eur. J. Immunol. 34:27302739.
90. Marik, C.,, P. A. Felts,, J. Bauer,, H. Lassmann, and, K. J. Smith. 2007. Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity? Brain 130:28002815.
91. Martin, L. R.,, Z. C. Neal,, M. S. McBride, and, A. C. Palmenberg. 2000. Mengovirus and encephalomyocarditis virus poly(C) tract lengths can affect virus growth in murine cell culture. J. Virol. 74:30743081.
92. Martinat, C.,, N. Jarousse,, M. C. Prevost, and, M. Brahic. 1999. The GDVII strain of Theiler’s virus spreads via axonal transport. J. Virol. 73:60936098.
93. McAllister, A.,, F. Tangy,, C. Aubert, and, M. Brahic. 1990. Genetic mapping of the ability of Theiler’s virus to persist and demyelinate. J. Virol. 64:42524257.
94. McKnight, K. L., and, S. M. Lemon. 1998. The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication. RNA 4:15691584.
95. Mendez-Fernandez, Y. V.,, M. J. Hansen,, M. Rodriguez, and, L. R. Pease. 2005. Anatomical and cellular requirements for the activation and migration of virus-specific CD8+ T cells to the brain during Theiler’s virus infection. J. Virol. 79:30633070.
96. Michiels, T.,, V. Dejong,, R. Rodrigus, and, C. Shaw-Jackson. 1997. Protein 2A is not required for Theiler’s virus replication. J. Virol. 71:95499456.
97. Miller, S. D.,, C. L. Vanderlugt,, W. S. Begolka,, W. Pao,, R. L. Yauch,, K. L. Neville,, Y. Katz-Levy,, A. Carrizosa, and, B. S. Kim. 1997. Persistent infection with Theiler’s virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 3:11331136.
98. Mohindru, M.,, B. Kang, and, B. S. Kim. 2006. Initial capsid-specific CD4+ T cell responses protect against Theiler’s murine encephalomyelitisvirus-induced demyelinating disease. Eur. J. Immunol. 36:21062115.
99. Murray, P. D.,, K. Krivacic,, A. Chernosky,, T. Wei,, R. M. Ransohoff, and, M. Rodriguez. 2000. Biphasic and regionally-restricted chemokine expression in the central nervous system in the Theiler’s virus model of multiple sclerosis. J. Neurovirol. 6(Suppl. 1):S44S52.
100. Murray, P. D.,, D. B. McGavern,, X. Lin,, M. K. Njenga,, J. Leibowitz,, L. R. Pease, and, M. Rodriguez. 1998. Perforin-dependent neurologic injury in a viral model of multiple sclerosis. J. Neurosci. 18:73067314.
101. Nitayaphan, S.,, M. M. Toth, and, R. P. Roos. 1985. Localization of a neutralization site of Theiler’s murine encephalomyelitis viruses. J. Virol. 56:887895.
102. Njenga, M. K.,, K. Asakura,, S. F. Hunter,, P. Wettstein,, L. R. Pease, and, M. Rodriguez. 1997. The immune system preferentially clears Theiler’s virus from the gray matter of the central nervous system. J. Virol. 71:85928601.
103. Njenga, M. K.,, L. R. Pease,, P. Wettstein,, T. Mak, and, M. Rodriguez. 1997. Interferon alpha/beta mediates early virus-induced expression of H-2D and H-2K in the central nervous system. Lab. Investig. 77:7184.
104. Obuchi, M.,, Y. Ohara,, T. Takegami,, T. Murayama,, H. Takada, and, H. Iizuka. 1997. Theiler’s murine encephalo-myelitis virus subgroup strain-specific infection in a murine macrophage-like cell line. J. Virol. 71:729733.
105. Oleszak, E. L.,, J. R. Chang,, H. Friedman,, C. D. Katsetos, and, C. D. Platsoucas. 2004. Theiler’s virus infection: a model for multiple sclerosis. Clin. Microbiol. Rev. 17:174207.
106. Olson, J. K., and, S. D. Miller. 2009. The innate immune response affects the development of the autoimmune response in Theiler’s virus-induced demyelinating disease. J. Immunol. 182:57125722.
107. Ozden, S.,, C. Aubert,, D. Gonzalez-Dunia, and, M. Brahic. 1991. In situ analysis of proteolipid protein gene transcripts during persistent Theiler’s virus infection. J. Histochem. Cy-tochem. 39:13051309.
108. Paul, A. V.,, E. Rieder,, D. W. Kim,, J. H. van Boom, and, E. Wimmer. 2000. Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg. J. Virol. 74:1035910370.
109. Pavelko, K. D.,, C. L. Howe,, K. M. Drescher,, J. D. Gamez,, A. J. Johnson,, T. Wei,, R. M. Ransohoff, and, M. Rodriguez. 2003. Interleukin-6 protects anterior horn neurons from lethal virus-induced injury. J. Neurosci. 23:481492.
110. Pavelko, K. D.,, L. R. Pease,, C. S. David, and, M. Rodriguez. 2007. Genetic deletion of a single immunodominant T-cell response confers susceptibility to virus-induced demyelination. Brain Pathol. 17:184196.
111. Paya, C. V.,, A. K. Patick,, P. J. Leibson, and, M. Rodriguez. 1989. Role of natural killer cells as immune effectors in encephalitis and demyelination induced by Theiler’s virus. J. Immunol. 143:95102.
112. Pena-Rossi, C.,, E. Cash,, C. Aubert, and, A. Coutinho. 1991. Role of the humoral immune response in resistance to Theiler’s virus infection. J. Virol. 65:38953899.
113. Pena-Rossi, C.,, M. Delcroix,, I. Huitinga,, A. McAllister,, N. van Rooijen,, E. Claassen, and, M. Brahic. 1997. Role of macro-phages during Theiler’s virus infection. J. Virol. 71:33363340.
114. Pena-Rossi, C.,, A. McAllister,, M. Tanguy,, D. Kagi, and, M. Brahic. 1998. Theiler’s virus infection of perforin-deficient mice. J. Virol. 72:45154519.
115. Peterson, J. D.,, W. J. Karpus,, R. J. Clatch, and, S. D. Miller. 1993. Split tolerance of Th1 and Th2 cells in tolerance to Theiler’s murine encephalomyelitis virus. Eur. J. Immunol. 23:4655.
116. Pichlmair, A.,, O. Schulz,, C. P. Tan,, J. Rehwinkel,, H. Kato,, O. Takeuchi,, S. Akira,, M. Way,, G. Schiavo, and, E. S. C. Reis. 2009. Activation of MDA5 requires higher order RNA structures generated during virus infection. J. Virol. 83:1076110769.
117. Pilipenko, E. V.,, E. G. Viktorova,, S. T. Guest,, V. I. Agol, and, R. P. Roos. 2001. Cell-specific proteins regulate viral RNA translation and virus-induced disease. EMBO J. 20:68996908.
118. Porter, F. W.,, Y. A. Bochkov,, A. J. Albee,, C. Wiese, and, A. C. Palmenberg. 2006. A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport. Proc. Natl. Acad. Sci. USA 103:1241712422.
119. Porter, F. W., and, A. C. Palmenberg. 2009. Leader-induced phosphorylation of nucleoporins correlates with nuclear trafficking inhibition by cardioviruses. J. Virol. 83:19411951.
120. Ransohoff, R. M.,, T. Wei,, K. D. Pavelko,, J. C. Lee,, P. D. Murray, and, M. Rodriguez. 2002. Chemokine expression in the central nervous system of mice with a viral disease resembling multiple sclerosis: roles of CD4+ and CD8+ T cells and viral persistence. J. Virol. 76:22172224.
121. Reddacliff, L. A.,, P. D. Kirkland,, W. J. Hartley, and, R. L. Reece. 1997. Encephalomyocarditis virus infections in an Australian zoo. J. Zoo Wildl. Med. 28:153157.
122. Reddi, H. V., and, H. L. Lipton. 2002. Heparan sulfate mediates infection of high-neurovirulence Theiler’s viruses. J. Virol. 76:84008407.
123. Ricour, C.,, F. Borghese,, F. Sorgeloos,, S. V. Hato,, F. J. van Kup-peveld, and, T. Michiels. 2009. Random mutagenesis defines a domain of Theiler’s virus leader protein which is essential for antagonism of nucleocytoplasmic trafficking and of cytokine gene expression. J. Virol. 83:1122311232.
124. Ricour, C.,, S. Delhaye,, S. V. Hato,, T. D. Olenyik,, B. Michel,, F. J. van Kuppeveld,, K. E. Gustin, and, T. Michiels. 2009. Inhibition of mRNA export and dimerization of interferon regulatory factor 3 by Theiler’s virus leader protein. J. Gen. Virol. 90:177186.
125. Rodriguez, M.,, J. Leibowitz, and, C. S. David. 1986. Susceptibility to Theiler’s virus-induced demyelination. Mapping of the gene within the H-2D region. J. Exp. Med. 163:620631.
126. Rodriguez, M.,, J. L. Leibowitz, and, P. W. Lampert. 1983. Persistent infection of oligodendrocytes in Theiler’s virus-induced encephalomyelitis. Ann. Neurol. 13:426433.
127. Rodriguez, M.,, K. D. Pavelko,, M. K. Njenga,, W. C. Logan, and, P. J. Wettstein. 1996. The balance between persistent virus infection and immune cells determines demyelination. J. Immunol. 157:56995709.
128. Rodriguez, M.,, L. J. Zoecklein,, C. L. Howe,, K. D. Pavelko,, J. D. Gamez,, S. Nakane, and, L. M. Papke. 2003. Gamma interferon is critical for neuronal viral clearance and protection in a susceptible mouse strain following early intracranial Theiler’s murine encephalomyelitis virus infection. J. Virol. 77:1225212265.
129. Romanova, L. I.,, P. V. Lidsky,, M. S. Kolesnikova,, K. V. Fominykh,, A. P. Gmyl,, E. V. Sheval,, S. V. Hato,, F. J. van Kuppeveld, and, V. I. Agol. 2009. Antiapoptotic activity of the cardiovirus leader protein, a viral “security” protein. J. Virol. 83:72737284.
130. Roos, R. P. 2002. Pathogenesis of Theiler’s murine encephalomyelitis virus induces disease, p. 427–435. In B. L. Semler and, E. Wimmer (ed.), Molecular Biology of Picornaviruses. ASM Press, Washington, DC.
131. Roos, R. P.,, W. P. Kong, and, B. L. Semler. 1989. Polyprotein processing of Theiler’s murine encephalomyelitis virus. J. Virol. 63:53445353.
132. Roussarie, J. P.,, C. Ruffie, and, M. Brahic. 2007. The role of myelin in Theiler’s virus persistence in the central nervous system. PLoS Pathog. 3:e23.
133. Roussarie, J. P.,, C. Ruffie,, J. M. Edgar,, I. Griffiths, and, M. Brahic. 2007. Axon myelin transfer of a non-enveloped virus. PLoS One 2:e1331.
134. Rubio, N.,, F. Sanz-Rodriguez, and, H. L. Lipton. 2006. Theiler’s virus induces the MIP-2 chemokine (CXCL2) in astro. cytes from genetically susceptible but not from resistant mouse strains. Cell. Immunol. 239:3140.
135. Sato, S.,, L. Zhang,, J. Kim,, J. Jakob,, R. A. Grant,, R. Wollmann, and, R. P. Roos. 1996. A neutralization site of DA strain of Theiler’s murine encephalomyelitis virus important for disease phenotype. Virology 226:327337.
136. Shah, A. H., and, H. L. Lipton. 2002. Low-neurovirulence Theiler’s viruses use sialic acid moieties on N- linked oligo-saccharide structures for attachment. Virology 304:443450.
137. So, E. Y.,, M. H. Kang, and, B. S. Kim. 2006. Induction of che-mokine and cytokine genes in astrocytes following infection with Theiler’s murine encephalomyelitis virus is mediated by the Toll-like receptor 3. Glia 53:858867.
138. So, E. Y., and, B. S. Kim. 2009. Theiler’s virus infection induces TLR3-dependent upregulation of TLR2 critical for proinflammatory cytokine production. Glia 57:12161226.
139. Son, K. N.,, R. P. Becker,, P. Kallio, and, H. L. Lipton. 2008. Theiler’s virus-induced intrinsic apoptosis in M1-D mac-rophages is Bax mediated and restricts virus infectivity: a mechanism for persistence of a cytolytic virus. J. Virol. 82:45024510.
140. Stavrou, S.,, Z. Feng,, S. M. Lemon, and, R. P. Roos. 2010. Different strains of Theiler’s murine encephalomyelitis virus antagonize different sites in the type I interferon pathway. J. Virol. 84:91819189.
141. Steurbaut, S.,, E. Merckx,, B. Rombaut, and, R. Vrijsen. 2008. Modulation of viral replication in macrophages persistently infected with the DA strain of Theiler’s murine encephalomy-elitis virus. Virol. J. 5:89.
142. Theiler, M. 1933. Spontaneous encephalomyelitis of mice: a new virus disease. Science 80:122.
143. Theiler, M., and, S. Gard. 1940. Encephalomyelitis of mice. III. Epidemiology. J. Exp. Med. 72:7990.
144. Tompkins, S. M.,, K. G. Fuller, and, S. D. Miller. 2002. Theiler’s virus-mediated autoimmunity: local presentation of CNS antigens and epitope spreading. Ann. N. Y. Acad. Sci. 958:2638.
145. Trottier, M.,, B. P. Schlitt,, A. Y. Kung, and, H. L. Lipton. 2004. Transition from acute to persistent Theiler’s virus infection requires active viral replication that drives proinflamma-tory cytokine expression and chronic demyelinating disease. J. Virol. 78:1248012488.
146. Tsunoda, I.,, L. Q. Kuang,, M. Kobayashi-Warren, and, R. S. Fujinami. 2005. Central nervous system pathology caused by autoreactive CD8+ T-cell clones following virus infection. J. Virol. 79:1464014646.
147. Tsunoda, I.,, T. E. Lane,, J. Blackett, and, R. S. Fujinami. 2004. Distinct roles for IP-10/CXCL10 in three animal models, Theiler’s virus infection, EAE, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10. Mult. Scler. 10:2634.
148. Tsunoda, I.,, T. Tanaka, and, R. S. Fujinami. 2008. Regulatory role of CD1d in neurotropic virus infection. J. Virol. 82:1027910289.
149. Tsunoda, I.,, T. Tanaka,, M. Taniguchi, and, R. S. Fujinami. 2009. Contrasting roles for Va14+ natural killer T cells in a viral model for multiple sclerosis. J. Neurovirol. 15:9098.
150. Tsunoda, I.,, T. Tanaka,, E. J. Terry, and, R. S. Fujinami. 2007. Contrasting roles for axonal degeneration in an autoimmune versus viral model of multiple sclerosis: when can axonal injury be beneficial? Am. J. Pathol. 170:214226.
151. Turrin, N. P. 2008. Central nervous system Toll-like receptor expression in response to Theiler’s murine encephalomyelitis virus-induced demyelination disease in resistant and susceptible mouse strains. Virol. J. 5:154.
152. Ure, D. R.,, T. E. Lane,, M. T. Liu, and, M. Rodriguez. 2005. Neutralization of chemokines RANTES and MIG increases virus antigen expression and spinal cord pathology during Theiler’s virus infection. Int. Immunol. 17:569579.
153. van Eyll, O., and, T. Michiels. 2000. Influence of the Theiler’s virus L* protein on macrophage infection, viral persistence, and neurovirulence. J. Virol. 74:90719077.
154. van Eyll, O., and, T. Michiels. 2002. Non-AUG-initiated internal translation of the L* protein of Theiler’s virus and importance of this protein for viral persistence. J. Virol. 76:1066510673.
155. van Pesch, V.,, O. van Eyll, and, T. Michiels. 2001. The leader protein of Theiler’s virus inhibits immediate-early alpha/beta interferon production. J. Virol. 75:78117817.
156. Vigneau, S.,, P. S. Rohrlich,, M. Brahic, and, J. F. Bureau. 2003. tmevpg1, a candidate gene for the control of Theiler’s virus persistence, could be implicated in the regulation of gamma interferon. J. Virol. 77:56325638.
157. Weiner, H. L. 2009. The challenge of multiple sclerosis: how do we cure a chronic heterogeneous disease? Ann. Neurol. 65:239248.
158. Welsh, C. J.,, L. Bustamante,, M. Nayak,, T. H. Welsh,, D. D. Dean, and, M. W. Meagher. 2004. The effects of restraint stress on the neuropathogenesis of Theiler’s virus infection II: NK cell function and cytokine levels in acute disease. Brain Behav. Immun. 18:166174.
159. Welsh, C. J.,, A. J. Steelman,, W. Mi,, C. R. Young,, R. Storts,, T. H. Welsh, Jr., and, M. W. Meagher. 2009. Neuroimmune interactions in a model of multiple sclerosis. Ann. N. Y. Acad. Sci. 1153:209219.
160. Yahikozawa, H.,, A. Inoue,, C. S. Koh,, Y. K. Choe, and, B. S. Kim. 1997. Major linear antibody epitopes and capsid proteins differentially induce protective immunity against Theiler’s virus-induced demyelinating disease. J. Virol. 71:31053113.
161. Yoon, J. W., and, H. S. Jun. 2006. Viruses cause type 1 diabetes in animals. Ann. N. Y. Acad. Sci. 1079:138146.
162. Zhou, L.,, X. Lin,, T. J. Green,, H. L. Lipton, and, M. Luo. 1997. Role of sialyloligosaccharide binding in Theiler’s virus persistence. J. Virol. 71:97019712.
163. Zhou, L.,, Y. Luo,, Y. Wu,, J. Tsao, and, M. Luo. 2000. Sialylation of the host receptor may modulate entry of demy-elinating persistent Theiler’s virus. J. Virol. 74:14771485.
164. Zoll, J.,, S. Erkens Hulshof,, K. Lanke,, F. Verduyn Lunel,, W. J. Melchers,, E. Schoondermarkvan de Ven,, M. Roivainen,, J. M. Galama, and, F. J. van Kuppeveld. 2009. Saffold virus, a human Theiler’s-like cardiovirus, is ubiquitous and causes infection early in life. PLoS Pathog. 5:e1000416.
165. Zoll, J.,, J. M. Galama,, F. J. van Kuppeveld, and, W. J. Melchers. 1996. Mengovirus leader is involved in the inhibition of host cell protein synthesis. J. Virol. 70:49484952.
166. Zoll, J.,, W. J. Melchers,, J. M. Galama, and, F. J. van Kuppeveld. 2002. The mengovirus leader protein suppresses alpha/beta interferon production by inhibition of the iron/ferritin-mediated activation of NF-κB. J. Virol. 76:96649672.
167. Zoll, J.,, F. J. van Kuppeveld,, J. M. Galama, and, W. J. Melchers. 1998. Genetic analysis of mengovirus protein 2A: its function in polyprotein processing and virus reproduction. J. Gen. Virol. 79:1725.

Tables

Generic image for table
Table 1.

Functions of L, L*, and 2A nonstructural proteins of TMEV and EMCV

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26
Generic image for table
Table 2.

Effectors of the TMEV immune response and demyelination

Citation: Michiels T, Roos R. 2010. Theiler’s Virus Central Nervous System Infection, p 411-428. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch26

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error