Influence of glutathione availability on cell damage induced by human immunodeficiency virus type 1 viral protein R

Virus Research

Volumn 213, Issue , 2016, Pages 116-123

  Monroy, Noemí ^a   Herrero, Laura ^a   Carrasco, Luis ^b   González, María Eugenia ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Heterologous expression; HIV 1; Oxidative stress; Phenotypic analysis; Therapeutic target; Vpr

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEHYDROASCORBIC ACID; GLUTATHIONE; VPR PROTEIN; VPR PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; BUDDING; CELL DAMAGE; CELL GROWTH; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; ENERGY; EUKARYOTIC CELL; FUNGUS CULTURE; FUNGUS GROWTH; HUMAN IMMUNODEFICIENCY VIRUS 1; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; WILD TYPE; YEAST; BUDDING YEAST; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; GLUTATHIONE; OXIDATIVE STRESS; SACCHAROMYCETALES; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84958787490     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2015.11.017     Document Type: Article

References (54)

1. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 1986, 59:284-291.
2. Alves-Rodrigues I., Galao R.P., Meyerhans A., Diez J. Saccharomyces cerevisiae: a useful model host to study fundamental biology of viral replication. Virus Res. 2006, 120:49-56.
3. Antal J., Pesti M. The dose-dependent H2O2 stress response promotes increased survival for Schizosaccharomyces pombe cells expressing HIV-1 Vpr. Folia Microbiol. (Praha) 2006, 51:406-412.
4. Baruchel S., Wainberg M.A. The role of oxidative stress in disease progression in individuals infected by the human immunodeficiency virus. J. Leukoc. Biol. 1992, 52:111-114.
5. Baudouin-Cornu P., Lagniel G., Kumar C., Huang M.E., Labarre J. Glutathione degradation is a key determinant of glutathione homeostasis. J. Biol. Chem. 2012, 287:4552-4561.
6. Bhaskar A., Munshi M., Khan S.Z., Fatima S., Arya R., Jameel S., Singh A. Measuring glutathione redox potential of HIV-1-infected macrophages. J. Biol. Chem. 2015, 290:1020-1038.
7. Burke D., Dawson D., Stearns T. Methods in Yeast Genetics. A Cold Spring Harbor Laboratory Course Manual 2000, Cold Spring Harbor Laboratory Press, New York.
8. Cesareni G., Murray J.A.H. Plasmid vectors carrying the replication origin of filamentous single-stranded phages. Genetic engineering Principles and methods 1987, 135-153. Plenum Press, New York. J.K. Setlow (Ed.).
9. Cohen E.A., Terwilliger E.F., Jalinoos Y., Proulx J., Sodroski J.G., Haseltine W.A. Identification of HIV-1 vpr product and function. J. Acquir. Immune Defic. Syndr. 1990, 3:11-18.
10. Connor R.I., Chen B.K., Choe S., Landau N.R. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 1995, 206:935-944.
11. De Rosa S.C., Zaretsky M.D., Dubs J.G., Roederer M., Anderson M., Green A., Mitra D., Watanabe N., Nakamura H., Tjioe I., Deresinski S.C., Moore W.A., Ela S.W., Parks D., Herzenberg L.A., Herzenberg L.A. N-acetylcysteine replenishes glutathione in HIV infection. Eur. J. Clin. Invest. 2000, 30:915-929.
12. Dedera D., Hu W., Vander H.N., Ratner L. Viral protein R of human immunodeficiency virus types 1 and 2 is dispensable for replication and cytopathogenicity in lymphoid cells. J. Virol. 1989, 63:3205-3208.
13. Ephrussi B. Action de l'acriflavine sur les levures. In: Unités biologiques douées de continuité génétique 1949, 165-180. CNRS, Paris.
14. Ferrucci A., Nonnemacher M.R., Cohen E.A., Wigdahl B. Extracellular human immunodeficiency virus type 1 viral protein R causes reductions in astrocytic ATP and glutathione levels compromising the antioxidant reservoir. Virus Res. 2012, 167:358-369.
15. Ferrucci A., Nonnemacher M.R., Wigdahl B. Extracellular HIV-1 viral protein R affects astrocytic glyceraldehyde 3-phosphate dehydrogenase activity and neuronal survival. J. Neurovirol. 2013, 19:239-253.
16. Goh W.C., Rogel M.E., Kinsey C.M., Michael S.F., Fultz P.N., Nowak M.A., Hahn B.H., Emerman M. HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo. Nat. Med. 1998, 4:65-71.
17. Goldring E.S., Grossman L.I., Krupnick D., Cryer D.R., Marmur J. The petite mutation in yeast. Loss of mitochondrial deoxyribonucleic acid during induction of petites with ethidium bromide. J. Mol. Biol. 1970, 52:323-335.
18. Gonzalez M.E. Vpu protein: the viroporin encoded by HIV-1. Viruses 2015, 7:4352-4368.
19. Gonzalez M.E., Carrasco L. Human immunodeficiency virus type 1 VPU protein affects Sindbis virus glycoprotein processing and enhances membrane permeabilization. Virology 2001, 279:201-209.
20. Grant C.M., MacIver F.H., Dawes I.W. Mitochondrial function is required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. FEBS Lett. 1997, 410:219-222.
21. Guenzel C.A., Herate C., Benichou S. HIV-1 Vpr-a still enigmatic multitasker. Front. Microbiol. 2014, 5:127.
22. Herrero L., Monroy N., Gonzalez M.E. HIV-1 Vpu protein mediates the transport of potassium in Saccharomyces cerevisiae. Biochemistry 2013, 52:171-177.
23. Jacotot E., Ferri K.F., El Hamel C., Brenner C., Druillennec S., Hoebeke J., Rustin P., Metivier D., Lenoir C., Geuskens M., Vieira H.L., Loeffler M., Belzacq A.S., Briand J.P., Zamzami N., Edelman L., Xie Z.H., Reed J.C., Roques B.P., Kroemer G. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J. Exp. Med. 2001, 193:509-519.
24. Jacotot E., Ravagnan L., Loeffler M., Ferri K.F., Vieira H.L., Zamzami N., Costantini P., Druillennec S., Hoebeke J., Briand J.P., Irinopoulou T., Daugas E., Susin S.A., Cointe D., Xie Z.H., Reed J.C., Roques B.P., Kroemer G. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 2000, 191:33-46.
25. Kim E.J., Park Y.G., Baik E.J., Jung S.J., Won R., Nahm T.S., Lee B.H. Dehydroascorbic acid prevents oxidative cell death through a glutathione pathway in primary astrocytes. J. Neurosci. Res. 2005, 79:670-679.
26. Kojer K., Bien M., Gangel H., Morgan B., Dick T.P., Riemer J. Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state. EMBO J. 2012, 31:3169-3182.
27. Levy D.N., Refaeli Y., MacGregor R.R., Weiner D.B. Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10873-10877.
28. Liu Z., Butow R.A. Mitochondrial retrograde signaling. Annu. Rev. Genet. 2006, 40:159-185.
29. Lu Y.L., Spearman P., Ratner L. Human immunodeficiency virus type 1 viral protein R localization in infected cells and virions. J. Virol. 1993, 67:6542-6550.
30. Macreadie I.G., Arunagiri C.K., Hewish D.R., White J.F., Azad A.A. Extracellular addition of a domain of HIV-1 Vpr containing the amino acid sequence motif H(S/F)RIG causes cell membrane permeabilization and death. Mol. Microbiol. 1996, 19:1185-1192.
31. Macreadie I.G., Castelli L.A., Hewish D.R., Kirkpatrick A., Ward A.C., Azad A.A. A domain of human immunodeficiency virus type 1 Vpr containing repeated H(S/F)RIG amino acid motifs causes cell growth arrest and structural defects. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:2770-2774.
32. Macreadie I.G., Thorburn D.R., Kirby D.M., Castelli L.A., de Rozario N.L., Azad A.A. HIV-1 protein Vpr causes gross mitochondrial dysfunction in the yeast Saccharomyces cerevisiae. FEBS Lett. 1997, 410:145-149.
33. Mehdi K., Penninckx M.J. An important role for glutathione and gamma-glutamyltranspeptidase in the supply of growth requirements during nitrogen starvation of the yeast Saccharomyces cerevisiae. Microbiology 1997, 143(Pt 6):1885-1889.
34. Mologni D., Citterio P., Menzaghi B., Zanone P.B., Riva C., Broggini V., Sinicco A., Milazzo L., Adorni F., Rusconi S., Galli M., Riva A. Vpr and HIV-1 disease progression: R77Q mutation is associated with long-term control of HIV-1 infection in different groups of patients. AIDS 2006, 20:567-574.
35. Muthumani K., Choo A.Y., Premkumar A., Hwang D.S., Thieu K.P., Desai B.M., Weiner D.B. Human immunodeficiency virus type 1 (HIV-1) Vpr-regulated cell death: insights into mechanism. Cell Death Differ. 2005, 12(Suppl. (1)):962-970.
36. Muthumani K., Hwang D.S., Desai B.M., Zhang D., Dayes N., Green D.R., Weiner D.B. HIV-1 Vpr induces apoptosis through caspase 9 in T cells and peripheral blood mononuclear cells. J. Biol. Chem. 2002, 277:37820-37831.
37. Nakamura H., Masutani H., Yodoi J. Redox imbalance and its control in HIV infection. Antioxid. Redox. Signal. 2002, 4:455-464.
38. Nguyen D., Hsu J.W., Jahoor F., Sekhar R.V. Effect of increasing glutathione with cysteine and glycine supplementation on mitochondrial fuel oxidation, insulin sensitivity, and body composition in older HIV-infected patients. J. Clin. Endocrinol. Metab. 2014, 99:169-177.
39. Ohlmeier S., Kastaniotis A.J., Hiltunen J.K., Bergmann U. The yeast mitochondrial proteome, a study of fermentative and respiratory growth. J. Biol. Chem. 2004, 279:3956-3979.
40. Pang X., Panee J. Roles of glutathione in antioxidant defense, inflammation, and neuron differentiation in the thalamus of HIV-1 transgenic rats. J. Neuroimmune. Pharmacol. 2014, 9:413-423.
41. Penninckx M.J. An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res 2002, 2:295-305.
42. Perl A., Banki K. Genetic and metabolic control of the mitochondrial transmembrane potential and reactive oxygen intermediate production in HIV disease. Antioxid. Redox. Signal. 2000, 2:551-573.
43. Porter K.M., Sutliff R.L. HIV-1, reactive oxygen species, and vascular complications. Free Radic. Biol. Med. 2012, 53:143-159.
44. Puskas F., Gergely P., Banki K., Perl A. Stimulation of the pentose phosphate pathway and glutathione levels by dehydroascorbate, the oxidized form of vitamin C. FASEB J. 2000, 14:1352-1361.
45. Rogel M.E., Wu L.I., Emerman M. The human immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection. J. Virol. 1995, 69:882-888.
46. Sambrook J., Rusell D.W. Molecular Cloning. A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
47. Staal F.J., Ela S.W., Roederer M., Anderson M.T., Herzenberg L.A., Herzenberg L.A. Glutathione deficiency and human immunodeficiency virus infection. Lancet 1992, 339:909-912.
48. Stromajer-Racz T., Gazdag Z., Belagyi J., Vagvolgyi C., Zhao R.Y., Pesti M. Oxidative stress induced by HIV-1 F34IVpr in Schizosaccharomyces pombe is one of its multiple functions. Exp. Mol. Pathol. 2010, 88:38-44.
49. Thomas B.J., Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell 1989, 56:619-630.
50. Vieira H.L., Haouzi D., El H.C., Jacotot E., Belzacq A.S., Brenner C., Kroemer G. Permeabilization of the mitochondrial inner membrane during apoptosis: impact of the adenine nucleotide translocator. Cell Death Differ. 2000, 7:1146-1154.
51. Wright R. Transmission electron microscopy of yeast. Microsc. Res. Tech. 2000, 51:496-510.
52. Zechmann B., Liou L.C., Koffler B.E., Horvat L., Tomasic A., Fulgosi H., Zhang Z. Subcellular distribution of glutathione and its dynamic changes under oxidative stress in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 2011, 11:631-642.
53. Zhao Y., Elder R.T. Yeast perspectives on HIV-1 VPR. Front. Biosci. 2000, 5:D905-D916.
54. Zhao Y., Yu M., Chen M., Elder R.T., Yamamoto A., Cao J. Pleiotropic effects of HIV-1 protein R (Vpr) on morphogenesis and cell survival in fission yeast and antagonism by pentoxifylline. Virology 1998, 246:266-276.