Astrocytes survive chronic infection and cytopathic effects of the ts1 mutant of the retrovirus moloney murine leukemia virus by upregulation of antioxidant defenses

Journal of Virology

Volumn 80, Issue 7, 2006, Pages 3273-3284

  Qiang, Wenan ^a,b,c   Kuang, Xianghong ^a,d   Liu, Jinrong ^a,e   Liu, Na ^a   Scofield, Virginia L ^a   Reid, Amy J ^a   Jiang, Yuhong ^a   Stoica, Gheorghe ^a,f   Lynn, William S ^a   Wong, Paul K Y ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b Searle 7 457 ^*  (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d SICHUAN UNIVERSITY   (China)

^e ABBOTT LABORATORIES   (United States)

^f TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CYSTEINE; CYSTINE; ENVELOPE PROTEIN; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL CYCLE; CELL IMMORTALIZATION; CELL SURVIVAL; CELL VIABILITY; CHRONIC DISEASE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; ENZYME ACTIVITY; MOLONEY LEUKEMIA ONCOVIRUS; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RETROVIRUS; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS MUTANT; WESTERN BLOTTING;

ANIMALS; ANTIOXIDANTS; ASTROCYTES; CELL LINE, TRANSFORMED; CELL SURVIVAL; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; CYTOPATHOGENIC EFFECT, VIRAL; LEUKEMIA, EXPERIMENTAL; MICE; MOLONEY MURINE LEUKEMIA VIRUS; MUTATION; RETROVIRIDAE INFECTIONS; SIMIAN VIRUS 40; TEMPERATURE; TUMOR VIRUS INFECTIONS; UP-REGULATION;

ANIMALIA; MOLONEY MURINE LEUKEMIA VIRUS;

EID: 33645235475     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.7.3273-3284.2006     Document Type: Article

References (49)

1. Bender, A. S., W. Reichelt, and M. D. Norenberg. 2000. Characterization of cystine uptake in cultured astrocytes. Neurochem Int. 37:269-276.
2. Brack-Werner, R. 1999. Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13:1-22.
3. Chauhan, A., J. Turchan, C. Pocernich, A. Bruce-Keller, S. Roth, D. A. Butterfield, E. O. Major, and A. Nath. 2003. Intracellular human immunodeficiency virus Tat expression in astrocytes promotes astrocyte survival but induces potent neurotoxicity at distant sites via axonal transport. J. Biol. Chem. 278:13512-13519.
4. Choe, W., G. Stoica, W. Lynn, and P. K. Y. Wong. 1998. Neurodegeneration induced by MoMuLV-ts1 and increased expression of Fas and TNF-alpha in the central nervous system. Brain Res. 779:1-8.
5. Dalton, T. P., M. Z. Dieter, Y. Yang, H. G. Shertzer, and D. W. Nebert. 2000. Knockout of the mouse glutamate cysteine ligase catalytic subunit (Gclc) gene: embryonic lethal when homozygous, and proposed model for moderate glutathione deficiency when heterozygous. Biochem. Biophys. Res. Commun. 279:324-329.
6. Dringen, R. 2000. Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62:649-671.
7. Dringen, R., and B. Hamprecht. 1997. Involvement of glutathione peroxidase and catalase in the disposal of exogenous hydrogen peroxide by cultured astroglial cells. Brain Res. 759:67-75.
8. Dringen, R., B. Hamprecht, and S. Broer. 1998. The peptide transporter PepT2 mediates the uptake of the glutathione precursor CysGly in astrogliarich primary cultures. J. Neurochem. 71:388-393.
9. Dringen, R., O. Kranich, and B. Hamprecht. 1997. The gamma-glutamyl transpeptidase inhibitor acivicin preserves glutathione released by astroglial cells in culture. Neurochem. Res. 22:727-733.
10. Gonzalez-Scarano, F., N. Nathanson, and P. K. Y. Wong. 1995. Retroviruses and the nervous system, p. 409-490. In J. Levy (ed.), The Retroviridae, vol. 4. Plenum Press, New York, N.Y.
11. +, and calcineurin-signaling from the endoplasmic reticulum. Mol. Cell 17:383-389.
12. Itoh, K., N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J. D. Engel, and M. Yamamoto. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13:76-86.
13. Jaiswal, A. K. 2000. Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radic. Biol. Med. 29:254-262.
14. 13a. Jiang, Y., V. L. Scofield, M. Yan, W. Qiang, N. Liu, A. J. Reid, W. S. Lynn, and P. K. Y. Wong, J. Virol., in press.
15. Jolicoeur, P., C. Hu, T. W. Mak, J. C. Martinou, and D. G. Kay. 2003. Protection against murine leukemia virus-induced spongiform myeloencephalopathy in mice overexpressing Bcl-2 but not in mice deficient for interleukin-6, inducible nitric oxide synthetase, ICE, Fas, Fas ligand, or TNF-R1 genes. J. Virol. 77:13161-13170.
16. Jones, D. P., Y. M. Go, C. L. Anderson, T. R. Ziegler, J. M. Kinkade, Jr., and W. G. Kirlin. 2004. Cysteine/cystine couple is a newly recognized node in the circuitry for biologic redox signaling and control. FASEB J. 18:1246-1248.
17. Kozutsumi, Y., M. Segal, K. Normington, M. J. Gething, and J. Sambrook. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332:462-464.
18. LeBel, C. P., S. F. Ali, M. McKee, and S. C. Bondy. 1990. Organometal-induced increases in oxygen reactive species: the potential of 2′,7′-dichlorofluorescin diacetate as an index of neurotoxic damage. Toxicol. Appl. Pharmacol. 104:17-24.
19. Lin, Y. C., C. W. Chow, P. H. Yuen, and P. K. Y. Wong. 1997. Establishment and characterization of conditionally immortalized astrocytes to study their interaction with ts1, a neuropathogenic mutant of Moloney murine leukemia virus. J. Neurovirol. 3:28-37.
20. Liu, N., X. Kuang, H. T. Kim, G. Stoica, W. Qiang, V. L. Scofield, and P. K. Y. Wong. 2004. Possible involvement of both endoplasmic reticulum- and mitochondria-dependent pathways in MoMuLV-ts1-induced apoptosis in astrocytes. J. Neurovirol. 10:189-198.
21. Liu, N., W. Qiang, X. Kuang, P. Thuillier, W. S. Lynn, and P. K. Y. Wong. 2002. The peroxisome proliferator phenylbutyric acid (PBA) protects astrocytes from ts1 MoMuLV-induced oxidative cell death. J. Neurovirol. 8:318-325.
22. Lu, S. C. 1998. Regulation of hepatic glutathione synthesis. Semin. Liver Dis. 18:331-343.
23. Lynn, W. S., and P. K. Y. Wong. 1995. Neuroimmunodegeneration: do neurons and T cells use common pathways for cell death? FASEB J. 9:1147-1156.
24. McClung, C. R. 1997. Regulation of catalases in Arabidopsis. Free Radic. Biol. Med. 23:489-496.
25. Misra, I., and O. W. Griffith. 1998. Expression and purification of human gamma-glutamylcysteine synthetase. Protein Expr. Purif. 13:268-276.
26. Mollace, V., H. S. Nottet, P. Clayette, M. C. Turco, C. Muscoli, D. Salvemini, and C. F. Perno. 2001. Oxidative stress and neuroAIDS: triggers, modulators and novel antioxidants. Trends Neurosci. 24:411-416.
27. Prestera, T., and P. Talalay. 1995. Electrophile and antioxidant regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. USA 92:8965-8969.
28. Qiang, W., J. M. Cahill, J. Liu, X. Kuang, N. Liu, V. L. Scofield, J. R. Voorhees, A. J. Reid, M. Yan, W. S. Lynn, and P. K. Y. Wong. 2004. Activation of transcription factor Nrf-2 and its downstream targets in response to Moloney murine leukemia virus ts1-induced thiol depletion and oxidative stress in astrocytes. J. Virol. 78:11926-11938.
29. Ranki, A., M. Nyberg, V. Ovod, M. Haltia, I. Elovaara, R. Raininko, H. Haapasalo, and K. Krohn. 1995. Abundant expression of HIV Nef and Rev proteins in brain astrocytes in vivo is associated with dementia. AIDS 9:1001-1008.
30. Reed, J. C. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
31. Roederer, M., S. W. Ela, F. J. Staal, and L. A. Herzenberg. 1992. N-Acetylcysteine: a new approach to anti-HIV therapy. AIDS Res. Hum. Retrovir. 8:209-217.
32. Saha, K., P. H. Yuen, and P. K. Y. Wong. 1994. Murine retrovirus-induced depletion of T cells is mediated through activation-induced death by apoptosis. J. Virol. 68:2735-2740.
33. Shih, A. Y., D. A. Johnson, G. Wong, A. D. Kraft, L. Jiang, H. Erb, J. A. Johnson, and T. H. Murphy. 2003. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J. Neurosci. 23:3394-3406.
34. 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.
35. Solis, W. A., T. P. Dalton, M. Z. Dieter, S. Freshwater, J. M. Harrer, L. He, H. G. Shertzer, and D. W. Nebert. 2002. Glutamate-cysteine ligase modifier subunit: mouse Gclm gene structure and regulation by agents that cause oxidative stress. Biochem. Pharmacol. 63:1739-1754.
36. Stoica, G., R. Barker, G. Wu, W. S. Lynn, and P. K. Y. Wong. 1998. Quantitative variation of free amino acids in the central nervous system of MoMuLV-ts1-infected mice. In Vivo 12:395-401.
37. Stoica, G., E. Floyd, O. Illanes, and P. K, Y. Wong. 1992. Temporal lymphoreticular changes caused by ts1, a paralytogenic mutant of Moloney murine leukemia virus TB. Lab. Investig. 66:427-436.
38. Stoica, G., O. Illanes, S. I. Tasca, and P. K. Y. Wong. 1993. Temporal central and peripheral nervous system changes induced by a paralytogenic mutant of Moloney murine leukemia virus TB. Lab. Investig. 69:724-735.
39. Stoica, G., S. I. Tasca, and P. K. Y. Wong. 2000. Motor neuronal loss and neurofilament-ubiquitin alteration in MoMuLV-ts1 encephalopathy. Acta Neuropathol. 99:238-244.
40. Szurek, P. F., P. H. Yuen, J. K. Ball, and P. K. Y. Wong. 1990. A Val-25-to-Ile substitution in the envelope precursor polyprotein, gPr80env is responsible for the temperature sensitivity, inefficient processing of gPr80env, and neurovirulence of ts1, a mutant of Moloney murine leukemia virus TB. J. Virol. 64:467-475.
41. Wong, P. K. Y., G. Prasad, J. Hansen, and P. H. Yuen. 1989. ts1, a mutant of Moloney murine leukemia virus-TB, causes both immunodeficiency and neurologic disorders in BALB/c mice. Virology 170:450-459.
42. Wong, P. K. Y., L. J. Russ, and J. A. McCarter. 1973. Rapid, selective procedure for isolation of spontaneous temperature-sensitive mutants of Moloney leukemia virus. Virology 51:424-431.
43. Wong, P. K. Y. 1990. Moloney murine leukemia virus temperature-sensitive mutants: a model for retrovirus-induced neurologic disorders. Curr. Top. Microbiol. Immunol. 160:29-60.
44. Wong, P. K. Y., W. S. Lynn, Y. C. Lin, W. Choe, and P. H. Yuen. 1998. ts1 MoMuLV: a murine model of neuroimmunodegeneration, p. 75-93. In P. K. Y. Wong and W. S. Lynn (ed.), Neuroimmunodegeneration. R. G. Landes, Austin, Tex.
45. Wong, P. K. Y., and P. H. Yuen. 1992. Molecular basis of neurologic disorders induced by a mutant, ts1, of Moloney murine leukemia virus, p. 161-197. In R. P. Roos (ed.), Molecular neurovirology: pathogenesis of viral CNS infection. Humana Press, Totowa, N.J.
46. Wu, G., P. K. Davis, N. E. Flynn, D. A. Knabe, and J. T. Davidson. 1997. Endogenous synthesis of arginine plays an important role in maintaining arginine homeostasis in postweaning growing pigs. J. Nutr. 127:2342-2349.
47. Yu, Y., C. A. Kamps, P. H. Yuen, and P. K. Y. Wong. 1991. Construction and characterization of expression systems for the env gene of ts1, a mutant of Moloney murine leukemia virus-TB. Virus Res. 19:83-92.
48. Yu, Y., and P. K. Y. Wong. 1992. Studies on compartmentation and turnover of murine retrovirus envelope proteins. Virology 188:477-485.
49. Yuen, P. H., M. M. Soong, M. S. Kissil, and P. K. K. Wong. 1984. Restriction of Moloney murine leukemia virus replication in Moloney murine sarcoma virus-infected cells. Virology 132:377-389.