Phenylbutyric acid suppresses protein accumulation-mediated ER stress in retrovirus-infected astrocytes and delays onset of paralysis in infected mice

Neurochemistry International

Volumn 57, Issue 7, 2010, Pages 738-748

  Kuang, Xianghong ^a   Hu, Wenhui ^b   Yan, Mingshan ^a   Wong, Paul K Y ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chemical chaperone; ER stress; MoMuLV ts1; Phenylbutyric acid; Unfolded protein response

Indexed keywords

ENVELOPE PROTEIN GPR 80; MESSENGER RNA; PHENYLBUTYRIC ACID; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN STEM; CELL DEATH; DISEASE SEVERITY; ENDOPLASMIC RETICULUM STRESS; IMMUNOFLUORESCENCE; MOLONEY LEUKEMIA ONCOVIRUS; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PARALYSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; REAL TIME POLYMERASE CHAIN REACTION; RETROVIRUS; RETROVIRUS INFECTION; RNA EXTRACTION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL LINE, TRANSFORMED; CELLS, CULTURED; ENDOPLASMIC RETICULUM; MICE; MOLONEY MURINE LEUKEMIA VIRUS; NIH 3T3 CELLS; OXIDATIVE STRESS; PARALYSIS; PHENYLBUTYRATES; RETROVIRIDAE; RETROVIRIDAE INFECTIONS; VIRAL PROTEINS;

MOLONEY MURINE LEUKEMIA VIRUS; MUS;

EID: 77958113231     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2010.08.010     Document Type: Article

References (84)

1. Achim C.L., Adame A., Dumaop W., Everall I.P., Masliah E. Increased accumulation of intraneuronal amyloid beta in HIV-infected patients. J.Neuroimmune. Pharmacol. 2009, 4:190-199.
2. An S.F., Scaravilli F. Early HIV-1 infection of the central nervous system. Arch. Anat. Cytol. Pathol. 1997, 45:94-105.
3. Antony J.M., Ellestad K.K., Hammond R., Imaizumi K., Mallet F., Warren K.G., Power C. The human endogenous retrovirus envelope glycoprotein, syncytin-1, regulates neuroinflammation and its receptor expression in multiple sclerosis: a role for endoplasmic reticulum chaperones in astrocytes. J. Immunol. 2007, 179:1210-1224.
4. Antony J.M., van Marle G., Opii W., et al. Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat. Neurosci. 2004, 7:1088-1095.
5. Balch W.E., Morimoto R.I., Dillin A., Kelly J.W. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
6. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2000, 2:326-332.
7. Bonapace G., Waheed A., Shah G.N., Sly W.S. Chemical chaperones protect from effects of apoptosis-inducing mutation in carbonic anhydrase IV identified in retinitis pigmentosa 17. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:12300-12305.
8. Boyce M., Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 2006, 13:363-373.
9. Castilla J., Hetz C., Soto C. Molecular mechanisms of neurotoxicity of pathological prion protein. Curr. Mol. Med. 2004, 4:397-403.
10. Cheynet V., Ruggieri A., Oriol G., Blond J.L., Boson B., Vachot L., Verrier B., Cosset F.L., Mallet F. Synthesis, assembly, and processing of the Env ERVWE1/syncytin human endogenous retroviral envelope. J. Virol. 2005, 79:5585-5593.
11. Choe W., Stoica G., Lynn W., Wong P.K. Neurodegeneration induced by MoMuLV-ts1 and increased expression of Fas and TNF-alpha in the central nervous system. Brain Res. 1998, 779:1-8.
12. Churchill M.J., Wesselingh S.L., Cowley D., Pardo C.A., McArthur J.C., Brew B.J., Gorry P.R. Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann. Neurol. 2009, 66:253-258.
13. Clark S., Duggan J., Chakraborty J. Tsl and LP-BM5: a comparison of two murine retrovirus models for HIV. Viral Immunol. 2001, 14:95-109.
14. Collins A.F., Pearson H.A., Giardina P., McDonagh K.T., Brusilow S.W., Dover G.J. Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: a clinical trial. Blood 1995, 85:43-49.
15. DuRose J.B., Scheuner D., Kaufman R.J., Rothblum L.I., Niwa M. Phosphorylation of eukaryotic translation initiation factor 2alpha coordinates rRNA transcription and translation inhibition during endoplasmic reticulum stress. Mol. Cell Biol. 2009, 29:4295-4307.
16. Esiri M.M., Biddolph S.C., Morris C.S. Prevalence of Alzheimer plaques in AIDS. J. Neurol. Neurosurg. Psychiatry 1998, 65:29-33.
17. Fraldi A., Zito E., Annunziata F., et al. Multistep, sequential control of the trafficking and function of the multiple sulfatase deficiency gene product, SUMF1 by PDI, ERGIC-53 and ERp44. Hum. Mol. Genet. 2008, 17:2610-2621.
18. Gonzalez-Scarano F., Nathanson N., Wong P.K.Y. Retroviruses and the nervous system. The Retroviridae 1995, vol.4:409-490. New York, Plenum Press.
19. Griffiths D.J. Endogenous retroviruses in the human genome sequence. Genome Biol. 2001, 2. REVIEWS1017.
20. Hashimoto M., Rockenstein E., Crews L., Masliah E. Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med. 2003, 4:21-36.
21. Haze K., Okada T., Yoshida H., Yanagi H., Yura T., Negishi M., Mori K. Identification of the G13 (cAMP-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response. Biochem. J. 2001, 355:19-28.
22. Haze K., Yoshida H., Yanagi H., Yura T., Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 1999, 10:3787-3799.
23. Hetz C.A., Soto C. Stressing out the ER: a role of the unfolded protein response in prion-related disorders. Curr. Mol. Med. 2006, 6:37-43.
24. Hoozemans J.J., Stieler J., van Haastert E.S., Veerhuis R., Rozemuller A.J., Baas F., Eikelenboom P., Arendt T., Scheper W. The unfolded protein response affects neuronal cell cycle protein expression: implications for Alzheimer's disease pathogenesis. Exp. Gerontol. 2006, 41:380-386.
25. Hotamisligil G.S. Endoplasmic reticulum stress and atherosclerosis. Nat. Med. 2010, 16:396-399.
26. Ilieva E.V., Ayala V., Jove M., et al. Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 2007, 130:3111-3123.
27. Inden M., Kitamura Y., Takeuchi H., et al. Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J. Neurochem. 2007, 101:1491-1504.
28. Jiang Y., Scofield V.L., Yan M., Qiang W., Liu N., Reid A.J., Lynn W.S., Wong P.K. Retrovirus-induced oxidative stress with neuroimmunodegeneration is suppressed by antioxidant treatment with a refined monosodium alpha-luminol (Galavit). J. Virol. 2006, 80:4557-4569.
29. Kanekura K., Suzuki H., Aiso S., Matsuoka M. ER stress and unfolded protein response in amyotrophic lateral sclerosis. Mol. Neurobiol. 2009, 39:81-89.
30. Kanki K., Kawamura T., Watanabe Y. Control of ER stress by a chemical chaperone counteracts apoptotic signals in IFN-gamma-treated murine hepatocytes. Apoptosis 2009, 14:309-319.
31. Kim H.T., Tasca S., Qiang W., Wong P.K., Stoica G. Induction of p53 accumulation by Moloney murine leukemia virus-ts1 infection in astrocytes via activation of extracellular signal-regulated kinases 1/2. Lab. Invest. 2002, 82:693-702.
32. Kim H.T., Waters K., Stoica G., Qiang W., Liu N., Scofield V.L., Wong P.K. Activation of endoplasmic reticulum stress signaling pathway is associated with neuronal degeneration in MoMuLV-ts1-induced spongiform encephalomyelopathy. Lab. Invest. 2004, 84:816-827.
33. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 2008, 7:1013-1030.
34. Kuang X., Scofield V.L., Yan M., Stoica G., Liu N., Wong P.K. Attenuation of oxidative stress, inflammation and apoptosis by minocycline prevents retrovirus-induced neurodegeneration in mice. Brain Res. 2009, 1286:174-184.
35. Kuang X., Yan M., Liu N., Scofield V.L., Qiang W., Cahill J., Lynn W.S., Wong P.K. Control of Atm-/- thymic lymphoma cell proliferation in vitro and in vivo by dexamethasone. Cancer Chemother. Pharmacol. 2005, 55:203-212.
36. Kubota K., Niinuma Y., Kaneko M., et al. Suppressive effects of 4-phenylbutyrate on the aggregation of Pael receptors and endoplasmic reticulum stress. J. Neurochem. 2006, 97:1259-1268.
37. Kurokawa M., Hideshima M., Ishii Y., Kyuwa S., Yoshikawa Y. Aortic ER stress in streptozotocin-induced diabetes mellitus in APA hamsters. Exp. Anim. 2009, 58:113-121.
38. Lander E.S., Linton L.M., Birren B., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
39. Lin Y.C., Chow C.W., Yuen P.H., Wong P.K. Establishment and characterization of conditionally immortalized astrocytes to study their interaction with ts1, a neuropathogenic mutant of Moloney murine leukemia virus. J. Neurovirol. 1997, 3:28-37.
40. Lindholm D., Wootz H., Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ. 2006, 13:385-392.
41. Lindl K.A., Akay C., Wang Y., White M.G., Jordan-Sciutto K.L. Expression of the endoplasmic reticulum stress response marker, BiP, in the central nervous system of HIV-positive individuals. Neuropathol. Appl. Neurobiol. 2007, 33:658-669.
42. Liu N., Kuang X., Kim H.T., Stoica G., Qiang W., Scofield V.L., Wong P.K. Possible involvement of both endoplasmic reticulum- and mitochondria-dependent pathways in MoMuLV-ts1-induced apoptosis in astrocytes. J. Neurovirol. 2004, 10:189-198.
43. Liu N., Qiang W., Kuang X., Thuillier P., Lynn W.S., Wong P.K. The peroxisome proliferator phenylbutyric acid (PBA) protects astrocytes from ts1 MoMuLV-induced oxidative cell death. J. Neurovirol. 2002, 8:318-325.
44. Liu N., Scofield V.L., Qiang W., Yan M., Kuang X., Wong P.K. Interaction between endoplasmic reticulum stress and caspase 8 activation in retrovirus MoMuLV-ts1-infected astrocytes. Virology 2006, 348:398-405.
45. Malhotra J.D., Kaufman R.J. The endoplasmic reticulum and the unfolded protein response. Semin. Cell Dev. Biol. 2007, 18:716-731.
46. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., Kaufman R.J. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18525-18530.
47. Martinez I.M., Chrispeels M.J. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 2003, 15:561-576.
48. Matus S., Lisbona F., Torres M., Leon C., Thielen P., Hetz C. The stress rheostat: an interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Curr. Mol. Med. 2008, 8:157-172.
49. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell Biol. 2001, 21:1249-1259.
50. Na K.S., Park B.C., Jang M., Cho S., Lee do H., Kang S., Lee C.K., Bae K.H., Park S.G. Protein disulfide isomerase is cleaved by caspase-3 and -7 during apoptosis. Mol. Cell 2007, 24:261-267.
51. Ni M., Lee A.S. ER chaperones in mammalian development and human diseases. FEBS Lett. 2007, 581:3641-3651.
52. Ono K., Ikemoto M., Kawarabayashi T., Ikeda M., Nishinakagawa T., Hosokawa M., Shoji M., Takahashi M., Nakashima M. A chemical chaperone, sodium 4-phenylbutyric acid, attenuates the pathogenic potency in human alpha-synuclein A30P+A53T transgenic mice. Parkinsonism Relat. Disord. 2009, 15:649-654.
53. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Gorgun C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
54. Portis J.L., Askovich P., Austin J., Gutierrez-Cotto Y., McAtee F.J. The degree of folding instability of the envelope protein of a neurovirulent murine retrovirus correlates with the severity of the neurological disease. J. Virol. 2009, 83:6079-6086.
55. Power C. Retroviral diseases of the nervous system: pathogenic host response or viral gene-mediated neurovirulence?. Trends Neurosci. 2001, 24:162-169.
56. Qiang W., Cahill J.M., Liu J., et al. 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. 2004, 78:11926-11938.
57. Qiang W., Kuang X., Liu J., et al. Astrocytes survive chronic infection and cytopathic effects of the ts1 mutant of the retrovirus Moloney murine leukemia virus by upregulation of antioxidant defenses. J. Virol. 2006, 80:3273-3284.
58. Reddy P.V., Lungu G., Kuang X., Stoica G., Wong P.K. Neuroprotective effects of the drug GVT (monosodium luminol) are mediated by the stabilization of Nrf2 in astrocytes. Neurochem. Int. 2010, 56:780-788.
59. Rempel H.C., Pulliam L. HIV-1 Tat inhibits neprilysin and elevates amyloid beta. AIDS 2005, 19:127-135.
60. Ricobaraza A., Cuadrado-Tejedor M., Perez-Mediavilla A., Frechilla D., Del Rio J., Garcia-Osta A. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 2009, 34:1721-1732.
61. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
62. Rubenstein R.C., Zeitlin P.L. A pilot clinical trial of oral sodium 4-phenylbutyrate (Buphenyl) in deltaF508-homozygous cystic fibrosis patients: partial restoration of nasal epithelial CFTR function. Am. J. Respir. Crit. Care Med. 1998, 157:484-490.
63. Santos C.X., Tanaka L.Y., Wosniak J., Laurindo F.R. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid. Redox Signal. 2009, 11:2409-2427.
64. Sawkar A.R., Cheng W.C., Beutler E., Wong C.H., Balch W.E., Kelly J.W. Chemical chaperones increase the cellular activity of N370S beta-glucosidase: a therapeutic strategy for Gaucher disease. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15428-15433.
65. Scheper W., Hoozemans J.J. Endoplasmic reticulum protein quality control in neurodegenerative disease: the good, the bad and the therapy. Curr. Med. Chem. 2009, 16:615-626.
66. Scofield V.L., Yan M., Kuang X., Kim S.J., Crunk D., Wong P.K. The drug monosodium luminol (GVT) preserves thymic epithelial cell cytoarchitecture and allows thymocyte survival in mice infected with the T cell-tropic, cytopathic retrovirus ts1. Immunol. Lett. 2009, 122:159-169.
67. Scofield V.L., Yan M., Kuang X., Kim S.J., Wong P.K. The drug monosodium luminol (GVT) preserves crypt-villus epithelial organization and allows survival of intestinal T cells in mice infected with the ts1 retrovirus. Immunol. Lett. 2009, 122:150-158.
68. Shikova E., Lin Y.C., Saha K., Brooks B.R., Wong P.K. Correlation of specific virus-astrocyte interactions and cytopathic effects induced by ts1, a neurovirulent mutant of Moloney murine leukemia virus. J. Virol. 1993, 67:1137-1147.
69. Stoica G., Tasca S.I., Wong P.K. Motor neuronal loss and neurofilament-ubiquitin alteration in MoMuLV-ts1 encephalopathy. Acta Neuropathol. 2000, 99:238-244.
70. Szurek P.F., Yuen P.H., Ball J.K., Wong P.K. 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. 1990, 64:467-475.
71. Tan J.M., Wong E.S., Lim K.L. Protein misfolding and aggregation in Parkinson's disease. Antioxid. Redox Signal. 2009, 11:2119-2134.
72. Todd D.J., Lee A.H., Glimcher L.H. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat. Rev. Immunol. 2008, 8:663-674.
73. Wang C.C., Tsou C.L. Protein disulfide isomerase is both an enzyme and a chaperone. FASEB J. 1993, 7:1515-1517.
74. Welch W.J., Brown C.R. Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1996, 1:109-115.
75. Winklhofer K.F., Tatzelt J., Haass C. The two faces of protein misfolding: gain- and loss-of-function in neurodegenerative diseases. EMBO J. 2008, 27:336-349.
76. Wise-Faberowski L., Aono M., Pearlstein R.D., Warner D.S. Apoptosis is not enhanced in primary mixed neuronal/glial cultures protected by isoflurane against N-methyl-d-aspartate excitotoxicity. Anesth. Analg. 2004, 99:1708-1714. (table of contents).
77. Wong P.K., Shikova E., Lin Y.C., Saha K., Szurek P.F., Stoica G., Madden R., Brooks B.R. Murine leukemia virus induced central nervous system diseases. Leukemia 1992, 6(Suppl. 3):161S-165S.
78. Yam G.H., Gaplovska-Kysela K., Zuber C., Roth J. Sodium 4-phenylbutyrate acts as a chemical chaperone on misfolded myocilin to rescue cells from endoplasmic reticulum stress and apoptosis. Invest. Ophthalmol. Vis. Sci. 2007, 48:1683-1690.
79. Yan M., Shen J., Person M.D., Kuang X., Lynn W.S., Atlas D., Wong P.K. Endoplasmic reticulum stress and unfolded protein response in Atm-deficient thymocytes and thymic lymphoma cells are attributable to oxidative stress. Neoplasia 2008, 10:160-167.
80. Yu Y., Kamps C.A., Yuen P.H., Wong P.K. Construction and characterization of expression systems for the env gene of ts1, a mutant of Moloney murine leukemia virus-TB. Virus Res. 1991, 19:83-92.
81. Yu Y.E., Choe W., Zhang W., Stoica G., Wong P.K. Development of pathological lesions in the central nervous system of transgenic mice expressing the env gene of ts1 Moloney murine leukemia virus in the absence of the viral gag and pol genes and viral replication. J. Neurovirol. 1997, 3:274-282.
82. Zhang K., Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454:455-462.
83. Zhang K., Kaufman R.J. Identification and characterization of endoplasmic reticulum stress-induced apoptosis in vivo. Methods Enzymol. 2008, 442:395-419.
84. Zhao X., Yoshimura F.K. Expression of murine leukemia virus envelope protein is sufficient for the induction of apoptosis. J. Virol. 2008, 82:2586-2589.