Endoplasmic Reticulum Stress Is a Determinant of Retrovirus-Induced Spongiform Neurodegeneration

Journal of Virology

Volumn 77, Issue 23, 2003, Pages 12617-12629

  Dimcheff, Derek E ^a   Askovic, Srdjan ^a,b   Baker, Audrey H ^a   Johnson Fowler, Cedar ^a   Portis, John L ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b Myriad Proteomics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN SPONGIOSIS; CHOP GENE; CYTOPATHOLOGY; ENDOPLASMIC RETICULUM; GADD153 GENE; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; RETROVIRUS; UNINDEXED SEQUENCE; VIRUS ENVELOPE; VIRUS GENE; VIRUS VIRULENCE;

ANIMALS; BASE SEQUENCE; DNA PROBES; ENDOPLASMIC RETICULUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, VIRAL; MICE; NEURODEGENERATIVE DISEASES; NIH 3T3 CELLS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC;

EID: 0242492706     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.23.12617-12629.2003     Document Type: Article

References (61)

1. Albritton, L. M., L. Tseng, D. Scadden, and J. M. Cunningham. 1989. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659-666.
2. Andrews, J. M., and M. B. Gardner. 1974. Lower motor neuron degeneration associated with type C RNA virus infection in mice: neuropathological features. J. Neuropathol. Exp. Neurol. 33:285-307.
3. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, and G. Sherlock. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25:25-29.
4. Askovic, S., C. Favara, F. J. McAtee, and J. L. Portis. 2001. Increased expression of MIP-1α and MIP-1β mRNAs in the brain correlates spatially and temporally with the spongiform neurodegeneration induced by a murine oncornavirus. J. Virol. 75:2665-2674.
5. Askovic, S., F. J. McAtee, C. Favara, and J. L. Portis. 2000. Brain infection by neuroinvasive but avirulent murine oncornaviruses. J. Virol. 74:465-473.
6. Bitko, V., and S. Barik. 2001. An ondoplasmic reticulum-specific stress-activated caspase (caspase-12) is implicated in the apoptosis of A549 epithelial cells by respiratory syncytial virus. J. Cell. Biochem. 80:441-454.
7. Bolt, G., K. Berg, and M. Blixenkrone-Moller. 2002. Measles virus-induced modulation of host-cell gene expression. J. Gen. Virol. 83:1157-1165.
8. Brewer, J. W., L. M. Hendershot, C. J. Sherr, and J. A. Diehl. 1999. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc. Natl. Acad. Sci. USA 96:8505-8510.
9. Bush, K. T., A. L. Goldberg, and S. K. Nigam. 1997. Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J. Biol. Chem. 272:9086-9092.
10. Clement, K., N. Viguerie, M. Diehn, A. Alizadeh, P. Barbe, C. Thalamas, J. D. Storey, P. O. Brown, G. S. Barsh, and D. Langin. 2002. In vivo regulation of human skeletal muscle gene expression by thyroid hormone. Genome Res. 12:281-291.
11. Czub, S., W. P. Lynch, M. Czub, and J. L. Portis. 1994. Kinetic analysis of spongiform neurodegenerative disease induced by a highly virulent murine retrovirus. Lab. Investig. 70:711-723.
12. DesGroseillers, L., M. Barrette, and P. Jolicoeur. 1984. Physical mapping of the paralysis-inducing determinant of a wild mouse ecotropic neurotropic retrovirus. J. Virol. 52:356-363.
13. Gardner, M. B., B. E. Henderson, J. D. Estes, R. W. Rongey, J. Casagrande, M. Pike, and R. J. Huebner. 1976. The epidemiology and virology of C-type virus-associated hematological cancers and related diseases in wild mice. Cancer Res. 36:574-581.
14. Gardner, M. B., B. E. Henderson, J. E. Officer, R. W. Rongey, J. C. Parker, C. Oliver, J. D. Estes, and R. J. Huebner. 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.
15. Gething, M. J., and J. Sambrook. 1992. Protein folding in the cell. Nature 355:33-45.
16. Gunn, T. M., T. Inui, K. Kitada, S. Ito, K. Wakamatsu, L. He, D. M. Bouley, T. Serikawa, and G. S. Barsh. 2001. Molecular and phenotypic analysis of Attractin mutant mice. Genetics 158:1683-1695.
17. Hansen, R., S. Czub, E. Werder, J. Herold, G. Gosztonyi, H. Gelderblom, S. Schimmer, S. Mazgareanu, V. ter Meulen, and M. Czub. 2000. Abundant defective viral particles budding from microglia in the course of retroviral spongiform encephalopathy. J. Virol. 74:1775-1780.
18. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
19. Harding, H. P., Y. Zhang, H. Zeng, I. Novoa, P. D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, R. Paules, D. F. Stojdl, J. C. Bell, T. Hettmann, J. M. Leiden, and D. Ron. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress Mol. Cell 11:619-633.
20. Hashimoto, Y., C. Zhang, J. Kawauchi, I. Imoto, M. T. Adachi, J. Inazawa, T. Amagasa, T. Hai, and S. Kitajima. 2002. An alternatively spliced isoform of transcriptional repressor ATF3 and its induction by stress stimuli. Nucleic Acids Res. 30:2398-2406.
21. He, L., X. Y. Lu, A. F. Jolly, A. G. Eldridge, S. J. Watson, P. K. Jackson, G. S. Barsh, and T. M. Gunn. 2003. Spongiform degeneration in mahoganoid mutant mice. Science 299:710-712.
22. Imai, Y., M. Soda, H. Inoue, N. Hattori, Y. Mizuno, and R. Takahashi. 2001. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105:891-902.
23. Ivanova, L., S. Barmada, T. Kummer, and D. A. Harris. 2001. Mutant prion proteins are partially retained in the endoplasmic reticulum. J. Biol. Chem. 276:42409-42421.
24. Jin, T., Y. Gu, G. Zanusso, M. Sy, A. Kumar, M. Cohen, P. Gambetti, and N. Singh. 2000. The chaperone protein BiP binds to a mutant prion protein and mediates its degradation by the proteasome. J. Biol. Chem. 275:38699-38704.
25. Jordan, R., L. Wang, T. M. Graczyk, T. M. Block, and P. R. Romano. 2002. Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells. J. Virol. 76:9588-9599.
26. Kamps, C. A., Y. C. Lin, and P. K. Wong. 1991. Oligomerization and transport of the envelope protein of Moloney murine leukemia virus-TB and of ts1, a neurovirulent temperature-sensitive mutant of MoMuLV-TB. Virology 184:687-694.
27. Kaneko, M., M. Ishiguro, Y. Niinuma, M. Uesugi, and Y. Nomura. 2002. Human HRD1 protects against ER stress-induced apoptosis through ER-associated degradation. FEBS Lett. 532:147-152.
28. Katayama, T., K. Imaizumi, N. Sato, K. Miyoshi, T. Kudo, J. Hitomi, T. Morihara, T. Yoneda, F. Gomi, Y. Mori, Y. Nakano, J. Takeda, T. Tsuda, Y. Itoyama, O. Murayama, A. Takashima, P. George-Hyslop, M. Takeda, and M. Tohyama. 1999. Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat. Cell Biol. 1:479-485.
29. Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls, Genes Dev. 13:1211-1233.
30. Li, C., and W. W. Hung. 2001. Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol. 2:1-11.
31. Li, C., and W. H. Wong. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA 98:31-36.
32. Lindquist, J. A., O. N. Jensen, M. Mann, and G. J. Hammerling. 1998. ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J. 17:2186-2195.
33. Lynch, W. P., W. J. Brown, G. J. Spangrude, and J. L. Portis. 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.
34. Lynch, W. P., S. Czub, F. J. McAtee, S. F. Hayes, and J. L. Portis. 1991. Murine retrovirus-induced spongiform encephalopathy: productive infection of microglia and cerebellar neurons in accelerated CNS disease. Neuron 7:365-379.
35. Lynch, W. P., S. J. Robertson, and J. L. Portis. 1995. Induction of focal spongiform neurodegeneration in developmentally resistant mice by implantation of murine retrovirus-infected microglia. J. Virol. 69:1408-1419.
36. Lynch, W. P., and A. H. Sharpe. 2000. Differential glycosylation of the Cas-Br-E Env protein is associated with retrovirus-induced spongiform neurodegeneration. J. Virol. 74:1558-1565.
37. Lynch, W. P., E. Y. Snyder, L. Qualtiere, J. L. Portis, and A. H. Sharpe. 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.
38. Ma, J., R. Wollmann, and S. Lindquist. 2002. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 298:1781-1785.
39. McCullough, K. D., J. L. Martindale, L. O. Klotz, T. Y. Aw, and N. J. Holbrook. 2001. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21:1249-1259.
40. Melov, S., J. A. Schneider, B. J. Day, D. Hinerfeld, P. Coskun, S. S. Mirra, J. D. Crapo, and D. C. Wallace. 1998. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18:159-163.
41. Nishitoh, H., A. Matsuzawa, K. Tobiume, K. Saegusa, K. Takeda, K. Inoue, S. Hori, A. Kakizuka, and H. Ichijo. 2002. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16:1345-1355.
42. Pahl, H. L., and P. A. Baeuerle. 1997. The ER-overload response: activation of NF-kappa B. Trends Biochem. Sci. 22:63-67.
43. Portis, J. L. 2001. Genetic determinants of neurovirulence of murine oncornaviruses. Adv. Virus Res. 56:3-38.
44. Portis, J. L., S. Czub, C. F. Garon, and F. J. McAtee. 1990. Neurodegenerative disease induced by the wild mouse ecotrgpic retrovirus is markedly accelerated by long terminal repeat and gag-pol sequences from nondefective Friend murine leukemia virus. J. Virol. 64:1648-1656.
45. Ryu, E. J., H. P. Harding, J. M. Angelastro, O. V. Vitolo, D. Ron, and L. A. Greene. 2002. Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci. 22:10690-10698.
46. Scheuner, D., B. Song, E. McEwen, C. Liu, R. Laybutt, P. Gillespie, T. Saunders, S. Bonner-Weir, and R. J. Kaufman. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176.
47. Sheikh, M. S., E. Fernandez-Salas, M. Yu, A. Hussain, J. D. Dinman, S. W. Peltz, Y. Huang, and A. J. Fornace, Jr. 1999. Cloning and characterization of a human genotoxic and endoplasmic reticulum stress-inducible cDNA that encodes translation initiation factor 1(eIF1(A121/SUI1)). J. Biol. Chem. 274:16487-16493.
48. Shikova, E., Y.-C. Lin, K. Saha, B. R. Brooks, and P. K. Y. Wong. 1993. Correlation of specific virus-astrocyte interactions and cytopathic effects induced by ts1, a neurovirulent mutant of Moloney murine leukemia virus. J. Virol. 67:1137-1147.
49. Southwood, C. M., J. Garbern, W. Jiang, and A. Gow. 2002. The unfolded protein response modulates disease severity in Pelizaeus-Merzbacher disease. Neuron 36:585-596.
50. Su, H. L., C. L. Liao, and Y. L. Lin. 2002. Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response. J. Virol. 76:4162-4171.
51. Swanstrom, R., and J. W. Wills. 1997. Synthesis, assembly, and processing of viral proteins, p. 263-334. In J. M. Coffin, S. H. Hughes, and H. Varmus (ed.). Retroviruses. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
52. Swarz, J. R., B. R. Brooks, and R. T. Johnson. 1981. Spongiform polioencephalomyelopathy caused by a murine retrovirus. II. Ultrastructural localization of virus replication and spongiform changes in the central nervous system. Neuropathol. Appl. Neurobiol. 7:365-380.
53. env alters the neurovirulence of tsl, a mutant of Moloney murine leukemia virus TB. J. Virol. 64:5241-5249.
54. Tardif, K. D., K. Mori, and A. Siddiqui. 2002. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J. Virol. 76:7453-7459.
55. Terro, F., C. Czech, F. Esclaire, W. Elyaman, C. Yardin, M. C. Baclet, N. Touchet, G. Tremp, L. Pradier, and J. Hugon. 2002. Neurons overexpressing mutant presenilin-1 are more sensitive to apoptosis induced by endoplasmic reticulum-Golgi stress. J. Neurosci. Res. 69:530-539.
56. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98:5116-5121.
57. Urano, F., M. Calfon, T. Yoneda, C. Yun, M. Kiraly, S. G. Clark, and D. Ron. 2002. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J. Cell Biol. 158:639-646.
58. Wang, X. Z., B. Lawson, J. W. Brewer, H. Zinszner, A. Sanjay, L. J. Mi, R. Boorstein, G. Kreibich, L. M. Hendershot, and D. Ron. 1996. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16:4273-4280.
59. Werstuck, G. H., S. R. Lentz, S. Dayal, G. S. Hossain, S. K. Sood, Y. Y. Shi, J. Zhou, N. Maeda, S. K. Krisans, M. R. Malinow, and R. C. Austin. 2001. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J. Clin. Investig. 107: 1263-1273.
60. Wilt, S. G., N. V. Dugger, N. D. Hitt, and P. M. Hoffman. 2000. Evidence for oxidative damage in a murine leukemia virus-induced neurodegeneration. J. Neurosci. Res. 62:440-450.
61. Zinszner, H., M. Kuroda, X. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982-995.