During infection, Theiler's virions are cleaved by caspases and disassembled into pentamers

Journal of Virology

Volumn 90, Issue 7, 2016, Pages 3573-3583

  Arslan, Sevim Yildiz ^a,b   Son, Kyung No ^a   Lipton, Howard L ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ABBOTT LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CAPSID PROTEIN; CASPASE; CASPASE 3; CYSTEINE; PENTAMER; PEPTIDE FRAGMENT; POLYMER; POLYPROTEIN; PROTEIN VP0; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; PROTEINASE; SUCROSE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; BHK CELL LINE; CARDIOVIRUS INFECTION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE PRODUCT; IN VITRO STUDY; LIFE CYCLE STAGE; MACROPHAGE CULTURE; MOUSE; NECROPTOSIS; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTOMER; RNA REPLICATION; RNA TRANSLATION; STAINING; SUCROSE GRADIENT; THEILER MURINE ENCEPHALOMYELITIS VIRUS INFECTION; THEILER'S MURINE ENCEPHALOMYELITIS VIRUS; TRANSMISSION ELECTRON MICROSCOPY; VIRION; VIRUS ASSEMBLY; VIRUS ATTENUATION; VIRUS CAPSID; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS PURIFICATION; VIRUS UNCOATING; ANIMAL; CELL CULTURE; HAMSTER; MACROPHAGE; METABOLISM; PHYSIOLOGY; PROTEIN DEGRADATION; THEILOVIRUS; VIROLOGY; VIRUS LOAD;

ANIMALS; APOPTOSIS; CASPASES; CELLS, CULTURED; CRICETINAE; MACROPHAGES; MICE; PROTEOLYSIS; THEILOVIRUS; VIRAL LOAD; VIRION; VIRUS ASSEMBLY;

EID: 84960976582     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03035-15     Document Type: Article

References (38)

1. Lipton HL. 1975. Theiler's virus infection in mice: an unusual biphasic disease process leading to demyelination. Infect Immun 11:1147-1155.
2. Blakemore WF, Welsh CJ, Tonks P, Nash AA. 1988. Observations on demyelinating lesions induced by Theiler's virus in CBA mice. Acta Neuropathol 76:581-589. http://dx.doi.org/10.1007/BF00689596.
3. Gerety SJ, Rundell KM, Dal Canto MC, Miller SD. 1994. Class IIrestricted T cell responses in Theiler's murine encephalomyelitis virusinduced demyelinating disease. VI. Potentiation of demyelination with and characterization of an immunopathologic CD4+ T cell line specific for an immunodominant VP2 epitope. J Immunol 152:919-929.
4. Rodriguez M, Leibowitz JL, Lampert PW. 1983. Persistent infection of oligodendrocytes in Theiler's virus-induced demyelination. Ann Neurol 13:426-433. http://dx.doi.org/10.1002/ana.410130409.
5. Miller SD, Vanderlugt CL, Smith Begolka W, Pao W, Yauch RL, Neville KL, Katz-Levy Y, Carrizosa A, Kim BS. 1997. Persistent infection with Theiler's virus leads to myelin-specific autoimmunity via epitope spreading. Nat Med 3:1133-1136. http://dx.doi.org/10.1038/nm1097-1133.
6. Borrow P, Welsh CJ, Tonks P, Dean D, Blakemore WF, Nash AA. 1998. Investigation of the role of delayed-type-hypersensitivity responses to myelin in the pathogenesis of Theiler's virus-induced demyelinating disease. Immunology 93:478-484.
7. Olson JK, Eagar TN, Miller SD. 2002. Functional activation of myelinspecific T cells by virus-induced molecular mimicry. J Immunol 169: 2719-2726. http://dx.doi.org/10.4049/jimmunol.169.5.2719.
8. 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. http://dx.doi.org/10.1128/JVI.77.7.4383-4388.2003.
9. Jelachich ML, Brumlage C, Lipton HL. 1999. Differentiation of M1 myeloid precursor cells into macrophages results in binding and infection by Theiler's murine encephalomyelitis virus (TMEV) and apoptosis. J Virol 73:3227-3235.
10. Son K-N, Becker RP, Kallio P, Lipton HL. 2008. Theiler's virus-induced apoptosis in M1-D macrophages is Bax-mediated through the mitochondrial pathway, resulting in loss of infectious virus: a model for persistence in the mouse central nervous system. J Virol 82:4502-4510. http://dx.doi.org/10.1128/JVI.02349-07.
11. Arslan SY, Son K-N, Lipton HL. 2012. The anti-apoptotic Mcl-1 protein controls the type of cell death in Theiler's virus-infected BHK-21 cells. J Virol 86:1922-1929. http://dx.doi.org/10.1128/JVI.06516-11.
12. Son K-N, Pugazhenthi S, Lipton HL. 2009. Activation of tumor suppressor protein p53 is required for Theiler's murine encephalomyelitis virusinduced apoptosis in M1-D macrophages. J Virol 83:10770-10777. http://dx.doi.org/10.1128/JVI.01030-09.
13. Jelachich ML, Lipton HL. 1996. Theiler's murine encephalomyelitis virus kills restrictive but not permissive cells by apoptosis. J Virol 70:6856-6861.
14. Rozhon EJ, Kratochvil JD, Lipton HL. 1983. Analysis of genetic variation in Theiler's virus during persistent infection in the mouse central nervous system. Virology 128:16-32. http://dx.doi.org/10.1016/0042-6822(83)90315-X.
15. Hertzler S, Luo M, Lipton HL. 2000. Mutation of predicted virion pit residues alters binding of Theiler's murine encephalomyelitis virus to BHK-21 cells. J Virol 74:1994-2004. http://dx.doi.org/10.1128/JVI.74.4.1994-2004.2000.
16. Pritchard AE, Jensen K, Lipton HL. 1993. Assembly of Theiler's virus recombinants used in mapping determinants of neurovirulence. J Virol 67:3901-3907.
17. Rueckert RR, Fraenkel-Conrat H, Wagner RR. 1976. On the structure and morphogenesis of picornaviruses, p 131-213. In Fraenkel-Conrat H, Wagner RR (ed), Comprehensive virology. Plenum Press, New York, NY.
18. Luo M, He C, Toth KS, Zhang CX, Lipton HL. 1992. Three-dimensional structure of Theiler's murine encephalomyelitis virus (BeAn strain). Proc Natl Acad Sci U S A 89:2409-2413. http://dx.doi.org/10.1073/pnas.89.6.2409.
19. Stavrou S, Ghadge G, Roos RP. 2011. Apoptotic and antiapoptotic activity of L protein of Theiler's murine encephalomyelitis virus. J Virol 85:7177-7185. http://dx.doi.org/10.1128/JVI.00009-11.
20. Wee LJ, Tan TW, Ranganathan S. 2006. SVM-based prediction of caspase substrate cleavage sites. BMCBioinformatics 7:S14-S15. http://dx.doi.org/10.1186/1471-2105-7-S5-S14.
21. Wee LJ, Tan TW, Ranganathan S. 2007. CASVM: web server for SVMbased prediction of caspase substrates cleavage sites. Bioinformatics 23: 3241-3243. http://dx.doi.org/10.1093/bioinformatics/btm334.
22. Song C, Tan H, Shen H, Mahmood K, Boyd SE, Webb GI, Akutsu T, Whisstock JC. 2010. Cascleave: towards more accurate prediction of caspase substrate cleavage sites. Bioinformatics 26:752-760. http://dx.doi.org/10.1093/bioinformatics/btq043.
23. Luo M, Vriend G, Kamer G, Minor I, Arnold E, Rossmann MG, Boege U, Scraba DG, Duke GM, Palmenbergy AC. 1987. The atomic structure of Mengo virus at 3.0 A resolution. Science 235:182-191.
24. Krishnaswamy S, Rossmann NG. 1990. Structural refinement and analysis of Mengo virus. J Mol Biol 211:803-844. http://dx.doi.org/10.1016/0022-2836(90)90077-Y.
25. Best SM, Shelton JF, Pompey JM, Wolfinbarger JB, Bloom ME. 2003. Caspase cleavage of the nonstructural protein NS1 mediates replication of Aleutian mink disease parovirus. J Virol 77:5305-5312. http://dx.doi.org/10.1128/JVI.77.9.5305-5312.2003.
26. Al-Molawi N, Beardmore VA, Carter MJ, Kass GEN, Roberts LO. 2003. Caspase-mediated cleavage of the feline calcivirus capsid protein. J Gen Virol 84:1237-1244. http://dx.doi.org/10.1099/vir.0.18840-0.
27. Jelachich ML, Lipton HL. 1999. Restricted Theiler's murine encephalomyelitis virus infection in murine macrophages induced apoptosis 80: 1701-1705.
28. Jelachich ML, Reddi HV, Trottier M, Schlitt BP, Lipton HL. 2004. Susceptibility of peritoneal macrophages to infection by Theiler's virus. Virus Res 104:123-127. http://dx.doi.org/10.1016/j.virusres.2004.03.006.
29. Koromyslova AD, Hansman GS. 2015. Nanobody binding to a conserved epitope promotes norovirus particle disassembly. J Virol 89:2718-2730. http://dx.doi.org/10.1128/JVI.03176-14.
30. Crowder S, Kirkegaard K. 2005. Trans-dominant inhibition of RNA viral replicaiton can slow growth of drug-resistant viruses. Nat Genet 37:701-709. http://dx.doi.org/10.1038/ng1583.
31. Friedmann A, Lipton HL. 1980. Replication of GDVII and DA strains of Theiler's murine encephalomyelitis virus in BHK 21 cells: an electron microscopic study. Virology 101:389-398. http://dx.doi.org/10.1016/0042-6822(80)90452-3.
32. Zhirnov OP, Konakova TE, Garten W, Klenk HD. 1999. Caspasedependent N-terminal cleavage of influenza virus nucleocapsid protein in infected cells. J Virol 73:10158-10163.
33. Eleouet J-F, Slee EA, Saurini F, Castagne N, Poncet D, Garrido C, Solary E, Martin SJ. 2000. The viral nucleocapsid protein of transmissible gastroenteritis coronavirus (TGEV) is cleaved by caspase-6 and-7 during TGEV-induced apoptosis. J Virol 74:3975-3983. http://dx.doi.org/10.1128/JVI.74.9.3975-3983.2000.
34. Carter MJ. 1989. Feline calcivirus protein synthesis investigated by Western blotting. Arch Virol 108:69-79. http://dx.doi.org/10.1007/BF01313744.
35. Carter MJ, Cubitt WD. 1998. Caliciviruses: infection and immunity, p 399-402. In Delves PJ, Roitt IM (ed), Encyclopedia of immunology, 2nd ed. Academic Press, London, United Kingdom.
36. Hardy ME, White LJ, Ball JM, Estes MK. 1995. Specific proteolytic cleavage of recombinant Norwalk virus capsid protein. J Virol 69:1693-1698.
37. Cheng F, Chen AY, Best SM, Bloom ME, Pintel D, Olu J. 2010. The capsid proteins of Aleutian mink disease virus activate caspases and are specifically cleaved during infection. J Virol 84:2687-2696. http://dx.doi.org/10.1128/JVI.01917-09.
38. Richard A, Tulasne D. 2012. Caspase cleavage of viral proteins, another way for viruses to make the best of apoptosis. Cell Death Dis 2:e277.