Inhibition of nuclear factor erythroid 2-related factor 2 exacerbates HIV-1 gp120-induced oxidative and inflammatory response: Role in HIV associated neurocognitive disorder

Neurochemical Research

Volumn 37, Issue 8, 2012, Pages 1697-1706

  Reddy, Pichili Vijaya Bhaskar ^a   Agudelo, Marisela ^a   Atluri, Venkata S R ^a   Nair, Madhavan P ^a  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

HIV; Inflammation; NADPH oxidase; Nrf2; Oxidative stress

Indexed keywords

GELATINASE B; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NF E2; TUMOR NECROSIS FACTOR ALPHA;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ASTROCYTE; CELL FUNCTION; CHEMOLUMINESCENCE; CONTROLLED STUDY; ENZYME INHIBITION; GENE SILENCING; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN CELL; INFLAMMATION; MOLECULAR DYNAMICS; NEUROPATHOLOGY; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

AIDS DEMENTIA COMPLEX; ASTROCYTES; HIV ENVELOPE PROTEIN GP120; HUMANS; INFLAMMATION; MATRIX METALLOPROTEINASE 9; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84864374934     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-012-0779-0     Document Type: Article

References (65)

1. Ellis R, Langford D, Masliah E (2007) HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nat Rev Neurosci 8:33-44
2. Woods SP, Moore DJ, Weber E, Grant I (2009) Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol Rev 19:152-168
3. McArthur JC, Brew BJ (2010) HIV-associated neurocognitive disorders: is there a hidden epidemic? Aids 24:1367-1370
4. Nath A, Geiger J (1998) Neurobiological aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog Neurobiol 54:19-33
5. Yang Y, Yao H, Lu Y, Wang C, Buch S (2010) Cocaine potentiates astrocyte toxicity mediated by human immunodeficiency virus (HIV-1) protein gp120. PLoS ONE 5:e13427
6. Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C (2002) The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 202:13-23
7. Thompson KA, McArthur JC, Wesselingh SL (2001) Correlation between neurological progression and astrocyte apoptosis in HIV-associated dementia. Ann Neurol 49:745-752
8. Lipton SA (1992) Models of neuronal injury in AIDS: another role for the NMDA receptor? Trends Neurosci 15:75-79
9. Ushijima H, Nishio O, Klocking R, Perovic S, Muller WE (1995) Exposure to gp120 of HIV-1 induces an increased release of arachidonic acid in rat primary neuronal cell culture followed by NMDA receptor-mediated neurotoxicity. Eur J Neurosci 7: 1353-1359
10. Ilyin SE, Plata-Salaman CR (1997) HIV-1 gp120 modulates hypothalamic cytokine mRNAs in vivo: implications to cytokine feedback systems. Biochem Biophys Res Commun 231:514-518
11. Aksenov MY, Hasselrot U, Bansal AK, Wu G, Nath A, Anderson C, Mactutus CF, Booze RM (2001) Oxidative damage induced by the injection of HIV-1 Tat protein in the rat striatum. Neurosci Lett 305:5-8
12. Aksenov MY, Hasselrot U, Wu G, Nath A, Anderson C, Mactutus CF, Booze RM (2003) Temporal relationships between HIV-1 Tat-induced neuronal degeneration, OX-42 immunoreactivity, reactive astrocytosis, and protein oxidation in the rat striatum. Brain Res 987:1-9
13. Bansal AK, Mactutus CF, Nath A, Maragos W, Hauser KF, Booze RM (2000) Neurotoxicity of HIV-1 proteins gp120 and Tat in the rat striatum. Brain Res 879:42-49
14. Sacktor N, Haughey N, Cutler R, Tamara A, Turchan J, Pardo C, Vargas D, Nath A (2004) Novel markers of oxidative stress in actively progressive HIV dementia. J Neuroimmunol 157: 176-184
15. Betteridge DJ (2000) What is oxidative stress? Metabolism 49:3-8
16. Reddy NM, Kleeberger SR, Kensler TW, Yamamoto M, Hassoun PM, Reddy SP (2009) Disruption of Nrf2 impairs the resolution of hyperoxia-induced acute lung injury and inflammation in mice. J Immunol 182:7264-7271
17. Louboutin JP, Reyes BA, Agrawal L, Van Bockstaele EJ, Strayer DS (2010) HIV-1 gp120-induced neuroinflammation: relationship to neuron loss and protection by rSV40-delivered antioxidant enzymes. Exp Neurol 221:231-245
18. Ronaldson PT, Bendayan R (2008) HIV-1 viral envelope glycoprotein gp120 produces oxidative stress and regulates the functional expression of multidrug resistance protein-1 (Mrp1) in glial cells. J Neurochem 106:1298-1313
19. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179-194
20. Nath A (2002) Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J Infect Dis 186(Suppl 2):S193-S198
21. Pocernich CB, La Fontaine M, Butterfield DA (2000) In vivo glutathione elevation protects against hydroxyl free radical-induced protein oxidation in rat brain. Neurochem Int 36: 185-191
22. Pocernich CB, Poon HF, Boyd-Kimball D, Lynn BC, Nath A, Klein JB, Butterfield DA (2005) Proteomic analysis of oxidatively modified proteins induced by the mitochondrial toxin 3-nitropropionic acid in human astrocytes expressing the HIV protein tat. Brain Res Mol Brain Res 133:299-306
23. Viviani B, Corsini E, Binaglia M, Galli CL, Marinovich M (2001) Reactive oxygen species generated by glia are responsible for neuron death induced by human immunodeficiency virus-glycoprotein 120 in vitro. Neuroscience 107:51-58
24. Chauhan A, Turchan J, Pocernich C, Bruce-Keller A, Roth S, Butterfield DA, Major EO, Nath A (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
25. Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death Differ 12(Suppl 1):893-904
26. Turchan J, Pocernich CB, Gairola C, Chauhan A, Schifitto G, Butterfield DA, Buch S, Narayan O, Sinai A, Geiger J et al (2003) Oxidative stress in HIV demented patients and protection ex vivo with novel antioxidants. Neurology 60:307-314
27. Ma Q, Kinneer K, Bi Y, Chan JY, Kan YW (2004) Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. BiochemJ 377:205-213
28. Motohashi H, Yamamoto M (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10:549-557
29. Nguyen T, Sherratt PJ, Nioi P, Yang CS, Pickett CB (2005) Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J Biol Chem 280:32485-32492
30. Alfieri A, Srivastava S, Siow RC, Modo M, Fraser PA, Mann GE (2011) Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J Physiol 589:4125-4136
31. Chen G, Fang Q, Zhang J, Zhou D, Wang Z (2011) Role of the Nrf2-ARE pathway in early brain injury after experimental subarachnoid hemorrhage. J Neurosci Res 89:515-523
32. Guerrero-Beltran CE, Calderon-Oliver M, Pedraza-Chaverri J, Chirino YI (2010) Protective effect of sulforaphane against oxidative stress: recent advances. Exp Toxicol Pathol. doi:10.1016/j.etp.2010.11.005
33. Kuang X, Scofield VL, Yan M, Stoica G, Liu N, Wong PK (2009) Attenuation of oxidative stress, inflammation and apoptosis by minocycline prevents retrovirus-induced neurodegeneration in mice. Brain Res 1286:174-184
34. Rojo AI, Innamorato NG, Martin-Moreno AM, De Ceballos ML, Yamamoto M, Cuadrado A (2010) Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 58:588-598
35. Siebert A, Desai V, Chandrasekaran K, Fiskum G, Jafri MS (2009) Nrf2 activators provide neuroprotection against 6-hydroxydopamine toxicity in rat organotypic nigrostriatal cocultures. J Neurosci Res 87:1659-1669
36. Reddy PV, Gandhi N, Samikkannu T, Saiyed Z, Agudelo M, Yndart A, Khatavkar P, Nair MP (2011) HIV-1 gp120 induces antioxidant response element-mediated expression in primary astrocytes: Role in HIV associated neurocognitive disorder. Neurochem Int. doi:10.1016/j.neuint.2011.06.011
37. Zhang HS, Li HY, Zhou Y, Wu MR, Zhou HS (2009) Nrf2 is involved in inhibiting Tat-induced HIV-1 long terminal repeat transactivation. Free Radic Biol Med 47:261-268
38. Ikezu T (2009) The aging of human-immunodeficiency-virusassociated neurocognitive disorders. J Neuroimmune Pharmacol 4:161-162
39. Kanmogne GD, Schall K, Leibhart J, Knipe B, Gendelman HE, Persidsky Y (2007) HIV-1 gp120 compromises blood-brain barrier integrity and enhances monocyte migration across bloodbrain barrier: implication for viral neuropathogenesis. J Cereb Blood Flow Metab 27:123-134
40. Toborek M, Lee YW, Flora G, Pu H, Andras IE, Wylegala E, Hennig B, Nath A (2005) Mechanisms of the blood-brain barrier disruption in HIV-1 infection. Cell Mol Neurobiol 25:181-199
41. Mollace V, Nottet HS, Clayette P, Turco MC, Muscoli C, Salvemini D, Perno CF (2001) Oxidative stress and neuroAIDS: triggers, modulators and novel antioxidants. Trends Neurosci 24:411-416
42. Nicolini A, Ajmone-Cat MA, Bernardo A, Levi G, Minghetti L (2001) Human immunodeficiency virus type-1 Tat protein induces nuclear factor (NF)-kappaB activation and oxidative stress in microglial cultures by independent mechanisms. J Neurochem 79:713-716
43. Rappaport J, Joseph J, Croul S, Alexander G, Del Valle L, Amini S, Khalili K (1999) Molecular pathway involved in HIV-1-induced CNS pathology: role of viral regulatory protein. Tat J Leukoc Biol 65:458-465
44. Park J, Choi K, Jeong E, Kwon D, Benveniste EN, Choi C (2004) Reactive oxygen species mediate chloroquine-induced expression of chemokines by human astroglial cells. Glia 47:9-20
45. Song HY, Ju SM, Seo WY, Goh AR, Lee JK, Bae YS, Choi SY, Park J (2011) Nox2-based NADPH oxidase mediates HIV-1 Tatinduced up-regulation of VCAM-1/ICAM-1 and subsequent monocyte adhesion in human astrocytes. Free Radic Biol Med 50:576-584
46. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, Johnson JA, Murphy TH (2003) Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 23:3394-3406
47. Qiang W, Cahill JM, Liu J, Kuang X, Liu N, Scofield VL, Voorhees JR, Reid AJ, Yan M, Lynn WS, Wong PK (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
48. Abramov AY, Jacobson J, Wientjes F, Hothersall J, Canevari L, Duchen MR (2005) Expression and modulation of an NADPH oxidase in mammalian astrocytes. J Neurosci 25:9176-9184
49. Wu RF, Ma Z, Myers DP, Terada LS (2007) HIV-1 Tat activates dual Nox pathways leading to independent activation of ERK and JNK MAP kinases. J Biol Chem 282:37412-37419
50. Williams R, Yao H, Peng F, Yang Y, Bethel-Brown C, Buch S (2010) Cooperative induction of CXCL10 involves NADPH oxidase: Implications for HIV dementia. Glia 58:611-621
51. Turchan-Cholewo J, Dimayuga VM, Gupta S, Gorospe RM, Keller JN, Bruce-Keller AJ (2009) NADPH oxidase drives cytokine and neurotoxin release from microglia and macrophages in response to HIV-Tat. Antioxid Redox Signal 11:193-204
52. Kong X, Thimmulappa R, Kombairaju P, Biswal S (2010) NADPH oxidase-dependent reactive oxygen species mediate amplified TLR4 signaling and sepsis-induced mortality in Nrf2-deficient mice. J Immunol 185:569-577
53. Shah A, Kumar A (2010) HIV-1 gp120-mediated increases in IL-8 production in astrocytes are mediated through the NF-kappaB pathway and can be silenced by gp120-specific siRNA. J Neuroinflammation 7:96
54. Saha RN, Pahan K (2007) Differential regulation of Mn-superoxide dismutase in neurons and astroglia by HIV-1 gp120: implications for HIV-associated dementia. Free Radic Biol Med 42:1866-1878
55. Williams R, Dhillon NK, Hegde ST, Yao H, Peng F, Callen S, Chebloune Y, Davis RL, Buch SJ (2009) Proinflammatory cytokines and HIV-1 synergistically enhance CXCL10 expression in human astrocytes. Glia 57:734-743
56. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, Kensler TW, Biswal S (2006) Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 116:984-995
57. Surh YJ, Na HK (2008) NF-kappaB and Nrf2 as prime molecular targets for chemoprevention and cytoprotection with antiinflammatory and antioxidant phytochemicals. Genes Nutr 2: 313-317
58. Mao L, Wang H, Qiao L, Wang X (2011) Disruption of Nrf2 enhances the upregulation of nuclear factor-kappaB activity, tumor necrosis factor-alpha, and matrix metalloproteinase-9 after spinal cord injury in mice. Mediators Inflamm 2010:238321
59. Chen XL, Kunsch C (2004) Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr Pharm Des 10:879-891
60. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I et al (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313-322
61. Mori N, Sato H, Hayashibara T, Senba M, Geleziunas R, Wada A, Hirayama T, Yamamoto N (2003) Helicobacter pylori induces matrix metalloproteinase-9 through activation of nuclear factor kappaB. Gastroenterology 124:983-992
62. Ju SM, Song HY, Lee JA, Lee SJ, Choi SY, Park J (2009) Extracellular HIV-1 Tat up-regulates expression of matrix metalloproteinase-9 via a MAPK-NF-kappaB dependent pathway in human astrocytes. Exp Mol Med 41:86-93
63. Moi P, Chan K, Asunis I, Cao A, Kan YW (1994) Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci USA 91:9926-9930
64. Sporer B, Paul R, Koedel U, Grimm R, Wick M, Goebel FD, Pfister HW (1998) Presence of matrix metalloproteinase-9 activity in the cerebrospinal fluid of human immunodeficiency virus-infected patients. J Infect Dis 178:854-857
65. Bond M, Fabunmi RP, Baker AH, Newby AC (1998) Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEBS Lett 435:29-34