Unique N-linked glycosylation of CasBrE env influences its stability, processing, and viral infectivity but not its neurotoxicity

Journal of Virology

Volumn 87, Issue 15, 2013, Pages 8372-8387

  Renszel, Krystal ^a,b,c   Traister, Russell ^a,d   Lynch, William ^a,b  

^a Northeast Ohio Medical University   (United States)

^b KENT STATE UNIVERSITY   (United States)

^c BANNER GOOD SAMARITAN MEDICAL CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN SPONGIOSIS; CELL FUSION; CONTROLLED STUDY; MOLECULAR PATHOLOGY; MOUSE; MURINE LEUKEMIA VIRUS; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; SEQUENCE ANALYSIS; VIRUS ASSEMBLY; VIRUS ENTRY; VIRUS IDENTIFICATION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TITRATION; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; CANAVAN DISEASE; DNA MUTATIONAL ANALYSIS; GENE PRODUCTS, ENV; GLYCOSYLATION; LEUKEMIA VIRUS, MURINE; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRULENCE; VIRUS REPLICATION;

EID: 84880590172     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00392-13     Document Type: Article

References (60)

1. Gardner MB. 1991. Retroviral leukemia and lower motor neuron disease in wild mice: natural history, pathogenesis, and genetic resistance. Adv. Neurol. 56:473-479.
2. Lynch WP, Czub S, McAtee FJ, Hayes SF, Portis JL. 1991. Murine retrovirus-induced spongiform encephalopathy: productive infection of microglia and cerebellar neurons in accelerated CNS disease. Neuron 7:365-379.
3. Nagra RM, Masliah E, Wiley CA. 1993. Synaptic and dendritic pathology in murine retroviral encephalitis. Exp. Neurol. 124:283-288.
4. Czub S, Lynch WP, Czub M, Portis JL. 1994. Kinetic analysis of spongiform neurodegenerative disease induced by a highly virulent murine retrovirus. Lab. Invest. 70:711-723.
5. Czub M, Czub S, McAtee FJ, Portis JL. 1991. Age-dependent resistance to murine retrovirus-induced spongiform neurodegeneration results from central nervous system-specific restriction of virus replication. J. Virol. 65:2539-2544.
6. Czub M, McAtee FJ, Portis JL. 1992. Murine retrovirus-induced spongiform encephalomyelopathy: host and viral factors which determine the length of the incubation period. J. Virol. 66:3298-3305.
7. Portis JL, Czub S, Garon CF, McAtee FJ. 1990. Neurodegenerative disease induced by the Wild Mouse ecotropic retrovirus is markedly accelerated by long terminal repeat and gag-pol sequences from nondefective Friend murine leukemia virus. J. Virol. 64:1648-1656.
8. Lynch WP, Portis JL. 1993. Murine retrovirus-induced spongiform encephalopathy: disease expression is dependent on postnatal development of the central nervous system. J. Virol. 67:2601-2610.
9. Li Y, Cardona SM, Traister RS, Lynch WP. 2011. Retrovirus-induced spongiform neurodegeneration is mediated by unique central nervous system viral targeting and expression of env alone. J. Virol. 85:2060-2078.
10. Sharpe AH, Hunter JJ, Chassler P, Jaenisch R. 1990. Role of abortive retroviral infection of neurons in spongiform CNS degeneration. Nature 346:181-183.
11. Gravel C, Kay DG, Jolicoeur P. 1993. Identification of the infected target cell type in spongiform myeloencephalopathy induced by the neurotropic Cas-Br-E murine leukemia virus. J. Virol. 67:6648-6658.
12. Kay DG, Gravel C, Robitaille Y, Jolicoeur P. 1991. Retrovirus-induced spongiform myeloencephalopathy in mice: regional distribution of infected target cells and neuronal loss occurring in the absence of viral expression in neurons. Proc. Natl. Acad. Sci. U. S. A. 88:1281-1285.
13. Baszler TV, Zachary JF. 1991. Murine retroviral neurovirulence correlates with an enhanced ability of virus to infect selectively, replicate in, and activate resident microglial cells. Am. J. Pathol. 138:655-671. (Erratum, 138:1058.)
14. Baszler TV, Zachary JF. 1990. Murine retroviral-induced spongiform neuronal degeneration parallels resident microglial cell infection: ultrastructural findings. Lab. Invest. 63:612-623.
15. Clase AC, Dimcheff DE, Favara C, Dorward D, McAtee FJ, Parrie LE, Ron D, Portis JL. 2006. Oligodendrocytes are a major target of the toxicity of spongiogenic murine retroviruses. Am. J. Pathol. 169:1026-1038.
16. Nagra RM, Burrola PG, Wiley CA. 1992. Development of spongiform encephalopathy in retroviral infected mice. Lab. Invest. 66:292-302.
17. Morey MK, Wiley CA. 1990. Immunohistochemical localization of neurotropic ecotropic murine leukemia virus in moribund mice. Virology 178:104-112.
18. Pitts OM, Powers JM, Bilello JA, Hoffman PM. 1987. Ultrastructural changes associated with retroviral replication in the central nervous system capillary endothelial cells. Lab. Invest. 56:401-409.
19. Lynch WP, Snyder EY, Qualtiere L, Portis JL, Sharpe AH. 1996. Late virus replication events in microglia are required for neurovirulent retrovirus-induced spongiform neurodegeneration: evidence from neural progenitor-derived chimeric mouse brains. J. Virol. 70:8896-8907.
20. Portis JL. 2001. Genetic determinants of neurovirulence of murine oncornaviruses. Adv. Virus Res. 56:3-38.
21. Lynch WP, Sharpe AH. 2000. Differential glycosylation of the Cas-Br-E env protein is associated with retrovirus-induced spongiform neurodegeneration. J. Virol. 74:1558-1565.
22. Battini J-L, Kayman SM, Pinter A, Heard JM, Danos O. 1994. Role of N-linked glycosylation in the activity of the Friend murine leukemia virus SU protein receptor binding domain. Virology 202:496-499.
23. Kayman SC, Kopelman R, Projan S, Kinney DM, Pinter A. 1991. Mutational analysis of N-linked glycosylation sites of Friend murine leukemia virus envelope protein. J. Virol. 65:5323-5332.
24. Askovic S, McAtee FJ, Favara C, Portis JL. 2000. Brain infection by neuroinvasive but avirulent murine oncornaviruses. J. Virol. 74:465-473.
25. Ryder EF, Snyder EY, Cepko CL. 1990. Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J. Neurobiol. 21:356-375.
26. Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartwieg E, Cepko CL. 1992. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 68:33-51.
27. Chesebro B, Britt W, Evans L, Wehrly K, Nishio J, Cloyd M. 1983. Characterization of monoclonal antibodies reactive with murine leukemia viruses: use in analysis of strains of Friend MCF and Friend ecotropic murine leukemia virus. Virology 127:134-148.
28. McAtee FJ, Portis JL. 1985. Monoclonal antibodies specific for wild mouse neurotropic retrovirus: detection of comparable levels of virus replication in mouse strains susceptible and resistant to paralytic disease. J. Virol. 56:1010-1022.
29. Lynch WP, Brown WJ, Spangrude GJ, Portis JL. 1994. Microglial infection by a neurovirulent murine retrovirus results in defective processing of envelope protein and intracellular budding of virus particles. J. Virol. 68: 3401-3409.
30. Lynch WP, Sharpe AH, Snyder EY. 1999. Neural stem cells as engraftable packaging lines can mediate gene delivery to microglia: evidence from studying retroviral env-related neurodegeneration. J. Virol. 73:6841-6851.
31. Jolicoeur P, Nicolaiew N, DesGroseillers L, Rassart E. 1983. Molecular cloning of infectious DNA from ecotropic neurotropic wild mouse retrovirus. J. Virol. 45:1159-1163.
32. Gavel Y, von Heijne G. 1990. Sequence differences between glycosylated and non glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 3:433-442.
33. Ferrarone J, Knoper RC, Li R, Kozak CA. 2012. Second site mutation in the virus envelope expands the host range of a cytopathic variant of Moloney murine leukemia virus. Virology 433:7-11.
34. Jung YT, Kozak CA. 2003. Generation of novel syncytium-inducing and host range variants of ecotropic Moloney murine leukemia virus in Mus spicilegus. J. Virol. 77:5065-5072.
35. Jung YT, Wu T, Kozak CA. 2004. Novel host range and cytopathic variant of ecotropic Friend murine leukemia virus. J. Virol. 78:12189-12197.
36. Murphy SL, Chung-Landers M, Honczarenko M, Gaulton GN. 2006. Linkage of reduced receptor affinity and superinfection to pathogenesis of TR1.3 murine leukemia virus. J. Virol. 80:4601-4609.
37. Murphy SL, Gaulton GN. 2007. TR1.3 viral pathogenesis and syncytium formation are linked to Env-Gag cooperation. J. Virol. 81:10777-10785.
38. Murphy SL, Honczarenko MJ, Dugger NV, Hoffman PM, Gaulton GN. 2004. Disparate regions of envelope protein regulate syncytium formation versus spongiform encephalopathy in neurological disease induced by murine leukemia virus TR. J. Virol. 78:8392-8399.
39. Aebi M, Bernasconi R, Clerc S, Molinari M. 2010. N-glycan structures: recognition and processing in the ER. Trends Biochem. Sci. 35:74-82.
40. Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73:1019-1049.
41. Chen R. 1982. Complete amino acid sequence and glycosylation sites of glycoprotein gp71A of Friend murine leukemia virus. Proc. Natl. Acad. Sci. U. S. A. 79:5788-5792.
42. Drickamer K, Taylor ME. 1998. Evolving views of protein glycosylation. Trends Biochem. Sci. 23:321-324.
43. Felkner RH, Roth MJ. 1992. Mutational analysis of the N-linked glycosylation sites of the SU envelope protein of Moloney murine leukemia virus. J. Virol. 66:4258-4264.
44. Polonoff E, Machida CA, Kabat D. 1982. Glycosylation and intracellular transport of membrane glycoproteins encoded by murine leukemia viruses. Inhibition by amino acid analogues and by tunicamycin. J. Biol. Chem. 257:14023-14028.
45. Pollakis G, Kang S, Kliphuis A, Chalaby MI, Goudsmit J, Paxton WA. 2001. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 276:13433-13441.
46. Dimcheff DE, Faasse MA, McAtee FJ, Portis JL. 2004. Endoplasmic reticulum (ER) stress induced by a neurovirulent mouse retrovirus is associated with prolonged BiP binding and retention of a viral protein in the ER. J. Biol. Chem. 279:33782-33790.
47. Kim HT, Waters K, Stoica G, Qiang W, Liu N, Scofield VL, Wong PK. 2004. Activation of endoplasmic reticulum stress signaling pathway is associated with neuronal degeneration in MoMuLV-ts1-induced spongiform encephalomyelopathy. Lab. Invest. 84:816-827.
48. Kuang X, Hu W, Yan M, Wong PK. 2010. Phenylbutyric acid suppresses protein accumulation-mediated ER stress in retrovirus-infected astrocytes and delays onset of paralysis in infected mice. Neurochem Int. 57: 738-748.
49. Liu N, Kuang X, Kim HT, Stoica G, Qiang W, Scofield VL, Wong PK. 2004. Possible involvement of both endoplasmic reticulum- and mitochondria-dependent pathways in MoMuLV-ts1-induced apoptosis in astrocytes. J. Neurovirol. 10:189-198.
50. Liu N, Scofield VL, Qiang W, Yan M, Kuang X, Wong PK. 2006. Interaction between endoplasmic reticulum stress and caspase 8 activation in retrovirus MoMuLV-ts1-infected astrocytes. Virology 348:398-405.
51. Portis JL, Askovich P, Austin J, Gutierrez-Cotto Y, McAtee FJ. 2009. The degree of folding instability of the envelope protein of a neurovirulent murine retrovirus correlates with the severity of the neurological disease. J. Virol. 83:6079-6086.
52. Fass D, Davey RA, Hamson CA, Kim PS, Cunningham JM, Berger JM.1997. Structure of a murine leukemia virus receptor-binding glycoprotein at 2.0 angstrom resolution. Nature 277:1662-1666.
53. Eiden MV, Farrell K, Warsowe J, Mahan LC, Wilson CA. 1993. Characterization of a naturally occurring ecotropic receptor that does not facilitate entry of all ecotropic murine retroviruses. J. Virol. 67:4056-4061.
54. Knoper RC, Ferrarone J, Yan Y, Lafont BA, Kozak CA. 2009. Removal of either N-glycan site from the envelope receptor binding domain of Moloney and Friend but not AKV mouse ecotropic gammaretroviruses alters receptor usage. Virology 391:232-239.
55. Zavorotinskaya T, Albritton LM. 1999. A hydrophobic patch in ecotropic murine leukemia virus envelope protein is the putative binding site for a critical tyrosine residue on the cellular receptor. J. Virol. 73:10164-10172.
56. Davey RA, Zou Y, Cunningham JM. 1999. Identification of a receptor binding pocket on the envelope protein of Friend murine leukemia virus. J. Virol. 73:3758-3763.
57. Melikyan GB, Markosyan RM, Brener SA, Rozenberg Y, Cohen FS. 2000. Role of the cytoplasmic tail of ecotropic Moloney murine leukemia virus Env protein in fusion pore formation. J. Virol. 74:447-455.
58. Ragheb JA, Anderson WF. 1994. pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J. Virol. 68:3220-3231.
59. Ragheb JA, Anderson WF. 1994. Uncoupled expression of Moloney murine leukemia virus envelope polypeptides SU and TM: a functional analysis of the role of TM domains in viral entry. J. Virol. 68:3207-3219.
60. Gardner MB, Henderson BE, Officer JE, Rongey RW, Parker JC, Oliver C, Estes JD, Huebner RJ. 1973. A spontaneous lower motor neuron disease apparently caused by indigenous type-C RNA virus in wild mice. J. Natl. Cancer Inst. 51:1243-1254.