Skip to main content

Advertisement

SpringerLink
Log in

Oxidative Stress and the HIV-Infected Brain Proteome

  • INVITED REVIEW
  • Published:
Journal of Neuroimmune Pharmacology Aims and scope Submit manuscript

Abstract

Human immunodeficiency virus (HIV) is capable of infiltrating the brain and infecting brain cells. In the years following HIV infection, patients show signs of various levels of neurocognitive problems termed HIV-associated neurocognitive disorders (HAND). Although the introduction of highly active antiretroviral therapy (HAART) has reduced the incidence of HIV-dementia, which is the most severe form of HAND, the milder forms have become more prevalent today due to the increased life expectancy of infected individuals. Pre-HAART era markers such as HIV RNA level, CD4+ count, TNF-α, MCP-1 and M-CSF are not able to clearly distinguish mild from advanced HAND. One promising approach for new biomarker discovery is the identification and quantitation of proteins that are post-translationally modified by oxidative and nitrosative species. The occurrence of oxidative and nitrosative stress in HIV-infected brain, both through the early direct and indirect effects of viral proteins and through the later effect on mitochondrial integrity during apoptosis, is well-established. This review will focus on how the reactive species are produced in the brain after HIV infection, the specific oxidative and nitrosative species that are involved in the post-translational modification of the brain proteome, and the methods that are currently used for the detection of such modified proteins. This review also provides an overview of related research pertaining to oxidative stress-related HAND using cerebrospinal fluid and human brain tissue.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adamson DC, Dawson TM, Zink MC, Clements JE, Dawson VL (1996) Neurovirulent simian immunodeficiency virus infection induces neuronal, endothelial, and glial apoptosis. Mol Med 2:417–428

    PubMed  CAS  PubMed Central  Google Scholar 

  • Adamson DC, Kopnisky KL, Dawson TM, Dawson VL (1999) Mechanisms and structural determinants of HIV-1 coat protein, gp41-induced neurotoxicity. J Neurosci 19:64–71

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Alvarez B, Radi R (2003) Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25:295–311

    PubMed  CAS  Google Scholar 

  • Alvarez B, Ferrer-Sueta G, Freeman BA, Radi R (1999) Kinetics of peroxynitrite reaction with amino acids and human serum albumin. J Biol Chem 274:842–848

    PubMed  CAS  Google Scholar 

  • Angel TE, Jacobs JM, Spudich SS, Gritsenko MA, Fuchs D, Liegler T, Zetterberg H, Camp DG II, Price RW, Smith RD (2012) The cerebrospinal fluid proteome in HIV infection: change associated with disease severity. Clin Proteomics 9:3

    PubMed  PubMed Central  Google Scholar 

  • Antinori A et al (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799

    PubMed  CAS  Google Scholar 

  • Bagasra O, Lavi E, Bobroski L, Khalili K, Pestaner JP, Tawadros R, Pomerantz RJ (1996) Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS 10:573–585

    PubMed  CAS  Google Scholar 

  • Banerjee S, Liao L, Russo R, Nakamura T, McKercher SR, Okamoto S, Haun F, Nikzad R, Zaidi R, Holland E, Eroshkin A, Yates JR III, Lipton SA (2012) Isobaric tagging-based quantification by mass spectrometry of differentially regulated proteins in synaptosomes of HIV/gp120 transgenic mice: implications for HIV-associated neurodegeneration. Exp Neurol 236:298–306

    PubMed  CAS  PubMed Central  Google Scholar 

  • Batthyany C, Schopfer FJ, Baker PR, Duran R, Baker LM, Huang Y, Cervenansky C, Branchaud BP, Freeman BA (2006) Reversible post-translational modification of proteins by nitrated fatty acids in vivo. J Biol Chem 281:20450–20463

    PubMed  CAS  PubMed Central  Google Scholar 

  • Beasley A, Anderson C, McArthur J, Sacktor N, Nath A, Cotter R (2010) Characterization of nitrotyrosine-modified proteins in cerebrospinal fluid. Clin Proteomics 29–41

  • Bell JE (2004) An update on the neuropathology of HIV in the HAART era. Histopathology 45:549–559

    PubMed  CAS  Google Scholar 

  • Boven LA, Gomes L, Hery C, Gray F, Verhoef J, Portegies P, Tardieu M, Nottet HS (1999) Increased peroxynitrite activity in AIDS dementia complex: implications for the neuropathogenesis of HIV-1 infection. J Immunol 162:4319–4327

    PubMed  CAS  Google Scholar 

  • Brack-Werner R (1999) Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. AIDS 13:1–22

    PubMed  CAS  Google Scholar 

  • Bregere C, Rebrin I, Gallaher TK, Sohal RS (2010) Effects of age and calorie restriction on tryptophan nitration, protein content, and activity of succinyl-CoA:3-ketoacid CoA transferase in rat kidney mitochondria. Free Radic Biol Med 48:609–618

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bukrinsky MI, Nottet HS, Schmidtmayerova H, Dubrovsky L, Flanagan CR, Mullins ME, Lipton SA, Gendelman HE (1995) Regulation of nitric oxide synthase activity in human immunodeficiency virus type 1 (HIV-1)-infected monocytes: implications for HIV-associated neurological disease. J Exp Med 181:735–745

    PubMed  CAS  Google Scholar 

  • Burner U, Furtmuller PG, Kettle AJ, Koppenol WH, Obinger C (2000) Mechanism of reaction of myeloperoxidase with nitrite. J Biol Chem 275:20597–20601

    PubMed  CAS  Google Scholar 

  • Butterfield DA, Reed T, Sultana R (2011) Roles of 3-nitrotyrosine- and 4-hydroxynonenal-modified brain proteins in the progression and pathogenesis of alzheimer’s disease. Free Radic Res 45:59–72

    PubMed  CAS  Google Scholar 

  • Castagna A, Le Grazie C, Accordini A, Giulidori P, Cavalli G, Bottiglieri T, Lazzarin A (1995) Cerebrospinal fluid S-adenosylmethionine (SAMe) and glutathione concentrations in HIV infection: effect of parenteral treatment with SAMe. Neurology 45:1678–1683

    PubMed  CAS  Google Scholar 

  • Chang HC, Samaniego F, Nair BC, Buonaguro L, Ensoli B (1997) HIV-1 tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11:1421–1431

    PubMed  CAS  Google Scholar 

  • Charles RL, Schroder E, May G, Free P, Gaffney PR, Wait R, Begum S, Heads RJ, Eaton P (2007) Protein sulfenation as a redox sensor: proteomics studies using a novel biotinylated dimedone analogue. Mol Cell Proteomics 6:1473–1484

    PubMed  CAS  Google Scholar 

  • Chazotte-Aubert L, Hainaut P, Ohshima H (2000) Nitric oxide nitrates tyrosine residues of tumor-suppressor p53 protein in MCF-7 cells. Biochem Biophys Res Commun 267:609–613

    PubMed  CAS  Google Scholar 

  • Cherner M, Cysique L, Heaton RK, Marcotte TD, Ellis RJ, Masliah E, Grant I, HNRC Group (2007) Neuropathologic confirmation of definitional criteria for human immunodeficiency virus-associated neurocognitive disorders. J Neurovirol 13:23–28

    PubMed  Google Scholar 

  • Choi J, Liu RM, Kundu RK, Sangiorgi F, Wu W, Maxson R, Forman HJ (2000) Molecular mechanism of decreased glutathione content in human immunodeficiency virus type 1 tat-transgenic mice. J Biol Chem 275:3693–3698

    PubMed  CAS  Google Scholar 

  • Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, Gorry PR (2009) Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 66:253–258

    PubMed  Google Scholar 

  • Cooke MS, Evans MD, Dizdaroglu M, Lunec J (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17:1195–1214

    PubMed  CAS  Google Scholar 

  • Davies NW, Guillemin G, Brew BJ (2010) Tryptophan, neurodegeneration and HIV-associated neurocognitive disorder. Int J Tryptophan Res 3:121–140

    PubMed  CAS  PubMed Central  Google Scholar 

  • DeLeo FR, Quinn MT (1996) Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins. J Leukoc Biol 60:677–691

    PubMed  Google Scholar 

  • Ehrenshaft M, Silva SO, Perdivara I, Bilski P, Sik RH, Chignell CF, Tomer KB, Mason RP (2009) Immunological detection of N-formylkynurenine in oxidized proteins. Free Radic Biol Med 46:1260–1266

    PubMed  CAS  PubMed Central  Google Scholar 

  • Eleuteri E, Magno F, Gnemmi I, Carbone M, Colombo M, La Rocca G, Anzalone R, Tarro Genta F, Zummo G, Di Stefano A, Giannuzzi P (2009) Role of oxidative and nitrosative stress biomarkers in chronic heart failure. Front Biosci 14:2230–2237

    CAS  Google Scholar 

  • Forrester MT, Thompson JW, Foster MW, Nogueira L, Moseley MA, Stamler JS (2009) Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol 27:557–559

    PubMed  CAS  PubMed Central  Google Scholar 

  • Frankel AD, Chen L, Cotter RJ, Pabo CO (1988) Dimerization of the tat protein from human immunodeficiency virus: a cysteine-rich peptide mimics the normal metal-linked dimer interface. Proc Natl Acad Sci U S A 85:6297–6300

    PubMed  CAS  PubMed Central  Google Scholar 

  • Genis P, Jett M, Bernton EW, Boyle T, Gelbard HA, Dzenko K, Keane RW, Resnick L, Mizrachi Y, Volsky DJ, Epstein LG, Gendelman HE (1992) Cytokines and arachidonic metabolites produced during human immunodeficiency virus (HIV)-infected macrophage-astroglia interactions: implications for the neuropathogenesis of HIV disease. J Exp Med 176:1703–1718

    PubMed  CAS  Google Scholar 

  • Gras G, Chretien F, Vallat-Decouvelaere AV, Le Pavec G, Porcheray F, Bossuet C, Leone C, Mialocq P, Dereuddre-Bosquet N, Clayette P, Le Grand R, Creminon C, Dormont D, Rimaniol AC, Gray F (2003) Regulated expression of sodium-dependent glutamate transporters and synthetase: a neuroprotective role for activated microglia and macrophages in HIV infection? Brain Pathol 13:211–222

    PubMed  CAS  Google Scholar 

  • Hara MR, Cascio MB, Sawa A (2006) GAPDH as a sensor of NO stress. Biochim Biophys Acta 1762:502–509

    PubMed  CAS  Google Scholar 

  • Haughey NJ, Cutler RG, Tamara A, McArthur JC, Vargas DL, Pardo CA, Turchan J, Nath A, Mattson MP (2004) Perturbation of sphingolipid metabolism and ceramide production in HIV-dementia. Ann Neurol 55:257–267

    PubMed  CAS  Google Scholar 

  • Hegg CC, Hu S, Peterson PK, Thayer SA (2000) Beta-chemokines and human immunodeficiency virus type-1 proteins evoke intracellular calcium increases in human microglia. Neuroscience 98:191–199

    PubMed  CAS  Google Scholar 

  • Helland R, Fjellbirkeland A, Karlsen OA, Ve T, Lillehaug JR, Jensen HB (2008) An oxidized tryptophan facilitates copper binding in methylococcus capsulatus-secreted protein MopE. J Biol Chem 283:13897–13904

    PubMed  CAS  Google Scholar 

  • Herzenberg LA, De Rosa SC, Dubs JG, Roederer M, Anderson MT, Ela SW, Deresinski SC, Herzenberg LA (1997) Glutathione deficiency is associated with impaired survival in HIV disease. Proc Natl Acad Sci U S A 94:1967–1972

    PubMed  CAS  PubMed Central  Google Scholar 

  • Heyes MP, Jordan EK, Lee K, Saito K, Frank JA, Snoy PJ, Markey SP, Gravell M (1992a) Relationship of neurologic status in macaques infected with the simian immunodeficiency virus to cerebrospinal fluid quinolinic acid and kynurenic acid. Brain Res 570:237–250

    PubMed  CAS  Google Scholar 

  • Heyes MP, Brew BJ, Saito K, Quearry BJ, Price RW, Lee K, Bhalla RB, Der M, Markey SP (1992b) Inter-relationships between quinolinic acid, neuroactive kynurenines, neopterin and beta 2-microglobulin in cerebrospinal fluid and serum of HIV-1-infected patients. J Neuroimmunol 40:71–80

    PubMed  CAS  Google Scholar 

  • Holden CP, Haughey NJ, Nath A, Geiger JD (1999) Role of na+/H + exchangers, excitatory amino acid receptors and voltage-operated Ca2+ channels in human immunodeficiency virus type 1 gp120-mediated increases in intracellular Ca2+ in human neurons and astrocytes. Neuroscience 91:1369–1378

    PubMed  CAS  Google Scholar 

  • Hori K, Burd PR, Furuke K, Kutza J, Weih KA, Clouse KA (1999) Human immunodeficiency virus-1-infected macrophages induce inducible nitric oxide synthase and nitric oxide (NO) production in astrocytes: astrocytic NO as a possible mediator of neural damage in acquired immunodeficiency syndrome. Blood 93:1843–1850

    PubMed  CAS  Google Scholar 

  • Hu S, Ali H, Sheng WS, Ehrlich LC, Peterson PK, Chao CC (1999) Gp-41-mediated astrocyte inducible nitric oxide synthase mRNA expression: involvement of interleukin-1beta production by microglia. J Neurosci 19:6468–6474

    PubMed  CAS  Google Scholar 

  • Hunzinger C, Wozny W, Schwall GP, Poznanovic S, Stegmann W, Zengerling H, Schoepf R, Groebe K, Cahill MA, Osiewacz HD, Jagemann N, Bloch M, Dencher NA, Krause F, Schrattenholz A (2006) Comparative profiling of the mammalian mitochondrial proteome: multiple aconitase-2 isoforms including N-formylkynurenine modifications as part of a protein biomarker signature for reactive oxidative species. J Proteome Res 5:625–633

    PubMed  CAS  Google Scholar 

  • Ikeda K, Yukihiro Hiraoka B, Iwai H, Matsumoto T, Mineki R, Taka H, Takamori K, Ogawa H, Yamakura F (2007) Detection of 6-nitrotryptophan in proteins by western blot analysis and its application for peroxynitrite-treated PC12 cells. Nitric Oxide 16:18–28

    PubMed  CAS  Google Scholar 

  • Irie Y, Saeki M, Kamisaki Y, Martin E, Murad F (2003) Histone H1.2 is a substrate for denitrase, an activity that reduces nitrotyrosine immunoreactivity in proteins. Proc Natl Acad Sci U S A 100:5634–5639

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jaffrey SR, Snyder SH (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci STKE 2001:l1

    Google Scholar 

  • Jonsson TJ, Johnson LC, Lowther WT (2008) Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451:98–101

    PubMed  PubMed Central  Google Scholar 

  • Kamisaki Y, Wada K, Bian K, Balabanli B, Davis K, Martin E, Behbod F, Lee YC, Murad F (1998) An activity in rat tissues that modifies nitrotyrosine-containing proteins. Proc Natl Acad Sci U S A 95:11584–11589

    PubMed  CAS  PubMed Central  Google Scholar 

  • Koller H, Thiem K, Siebler M (1996) Tumour necrosis factor-alpha increases intracellular Ca2+ and induces a depolarization in cultured astroglial cells. Brain 119(Pt 6):2021–2027

    PubMed  Google Scholar 

  • Kuo WN, Kanadia RN, Shanbhag VP, Toro R (1999) Denitration of peroxynitrite-treated proteins by ‘protein nitratases’ from rat brain and heart. Mol Cell Biochem 201:11–16

    PubMed  CAS  Google Scholar 

  • Laspiur JP, Anderson ER, Ciborowski P, Wojna V, Rozek W, Duan F, Mayo R, Rodriguez E, Plaud-Valentin M, Rodriguez-Orengo J, Gendelman HE, Melendez LM (2007) CSF proteomic fingerprints for HIV-associated cognitive impairment. J Neuroimmunol 192:157–170

    PubMed  CAS  PubMed Central  Google Scholar 

  • Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, Strahler JR, Andrews PC, Jakob U (2008) Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci U S A 105:8197–8202

    PubMed  CAS  PubMed Central  Google Scholar 

  • Levine RL, Moskovitz J, Stadtman ER (2000) Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation. IUBMB Life 50:301–307

    PubMed  CAS  Google Scholar 

  • Li W, Malpica-Llanos TM, Gundry R, Cotter RJ, Sacktor N, McArthur J, Nath A (2008a) Nitrosative stress with HIV dementia causes decreased L-prostaglandin D synthase activity. Neurology 70:1753–1762

    PubMed  CAS  Google Scholar 

  • Li W, Huang Y, Reid R, Steiner J, Malpica-Llanos T, Darden TA, Shankar SK, Mahadevan A, Satishchandra P, Nath A (2008b) NMDA receptor activation by HIV-tat protein is clade dependent. J Neurosci 28:12190–12198

    PubMed  CAS  Google Scholar 

  • Liu X, Jana M, Dasgupta S, Koka S, He J, Wood C, Pahan K (2002) Human immunodeficiency virus type 1 (HIV-1) tat induces nitric-oxide synthase in human astroglia. J Biol Chem 277:39312–39319

    PubMed  CAS  PubMed Central  Google Scholar 

  • Madian AG, Regnier FE (2010a) Profiling carbonylated proteins in human plasma. J Proteome Res 9:1330–1343

    PubMed  CAS  Google Scholar 

  • Madian AG, Regnier FE (2010b) Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res 9:3766–3780

    PubMed  CAS  PubMed Central  Google Scholar 

  • Marcus JS, Karackattu SL, Fleegal MA, Sumners C (2003) Cytokine-stimulated inducible nitric oxide synthase expression in astroglia: Role of erk mitogen-activated protein kinase and NF-kappaB. Glia 41:152–160

    Google Scholar 

  • McArthur JC (2004) HIV dementia: an evolving disease. J Neuroimmunol 157:3–10

    PubMed  CAS  Google Scholar 

  • McArthur JC, Haughey N, Gartner S, Conant K, Pardo C, Nath A, Sacktor N (2003) Human immunodeficiency virus-associated dementia: an evolving disease. J Neurovirol 9:205–221

    PubMed  CAS  Google Scholar 

  • McArthur JC, McDermott MP, McClernon D, St Hillaire C, Conant K, Marder K, Schifitto G, Selnes OA, Sacktor N, Stern Y, Albert SM, Kieburtz K, deMarcaida JA, Cohen B, Epstein LG (2004) Attenuated central nervous system infection in advanced HIV/AIDS with combination antiretroviral therapy. Arch Neurol 61:1687–1696

    PubMed  Google Scholar 

  • McArthur JC, Brew BJ, Nath A (2005) Neurological complications of HIV infection. Lancet Neurol 4:543–555

    PubMed  Google Scholar 

  • McArthur JC, Steiner J, Sacktor N, Nath A (2010) Human immunodeficiency virus-associated neurocognitive disorders: mind the gap. Ann Neurol 67:699–714

    PubMed  CAS  Google Scholar 

  • Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER (2001) Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci U S A 98:12920–12925

    PubMed  CAS  PubMed Central  Google Scholar 

  • Murray MF (2010) Insights into therapy: tryptophan oxidation and HIV infection. Sci Transl Med 2:32ps23

    PubMed  Google Scholar 

  • Nagai R, Unno Y, Hayashi MC, Masuda S, Hayase F, Kinae N, Horiuchi S (2002) Peroxynitrite induces formation of N(epsilon)-(carboxymethyl) lysine by the cleavage of amadori product and generation of glucosone and glyoxal from glucose: novel pathways for protein modification by peroxynitrite. Diabetes 51:2833–2839

    PubMed  CAS  Google Scholar 

  • Nagy P, Lechte TP, Das AB, Winterbourn CC (2012) Conjugation of glutathione to oxidized tyrosine residues in peptides and proteins. J Biol Chem 287:26068–26076

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nakamura H, Masutani H, Yodoi J (2002) Redox imbalance and its control in HIV infection. Antioxid Redox Signal 4:455–464

    PubMed  CAS  Google Scholar 

  • Nath A, Conant K, Chen P, Scott C, Major EO (1999) Transient exposure to HIV-1 tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon. J Biol Chem 274:17098–17102

    PubMed  CAS  Google Scholar 

  • Nelson KJ, Klomsiri C, Codreanu SG, Soito L, Liebler DC, Rogers LC, Daniel LW, Poole LB (2010) Use of dimedone-based chemical probes for sulfenic acid detection methods to visualize and identify labeled proteins. Methods Enzymol 473:95–115

    PubMed  CAS  Google Scholar 

  • Nuriel T, Hansler A, Gross SS (2011) Protein nitrotryptophan: formation, significance and identification. J Proteomics 74:2300–2312

    PubMed  CAS  PubMed Central  Google Scholar 

  • Olivetta E, Pietraforte D, Schiavoni I, Minetti M, Federico M, Sanchez M (2005) HIV-1 nef regulates the release of superoxide anions from human macrophages. Biochem J 390:591–602

    PubMed  CAS  PubMed Central  Google Scholar 

  • Olivetta E, Mallozzi C, Ruggieri V, Pietraforte D, Federico M, Sanchez M (2009) HIV-1 nef induces p47(phox) phosphorylation leading to a rapid superoxide anion release from the U937 human monoblastic cell line. J Cell Biochem 106:812–822

    PubMed  CAS  Google Scholar 

  • Pacher P, Obrosova IG, Mabley JG, Szabo C (2005) Role of nitrosative stress and peroxynitrite in the pathogenesis of diabetic complications, emerging new therapeutical strategies. Curr Med Chem 12:267–275

    PubMed  CAS  PubMed Central  Google Scholar 

  • Paulsen CE, Carroll KS (2010) Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem Biol 5:47–62

    PubMed  CAS  Google Scholar 

  • Pendyala G, Trauger SA, Kalisiak E, Ellis RJ, Siuzdak G, Fox HS (2009) Cerebrospinal fluid proteomics reveals potential pathogenic changes in the brains of SIV-infected monkeys. J Proteome Res 8:2253–2260

    PubMed  CAS  PubMed Central  Google Scholar 

  • Perez A, Probert AW, Wang KK, Sharmeen L (2001) Evaluation of HIV-1 tat induced neurotoxicity in rat cortical cell culture. J Neurovirol 7:1–10

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Pocernich CB, Cardin AL, Racine CL, Lauderback CM, Butterfield DA (2001) Glutathione elevation and its protective role in acrolein-induced protein damage in synaptosomal membranes: relevance to brain lipid peroxidation in neurodegenerative disease. Neurochem Int 39:141–149

    PubMed  CAS  Google Scholar 

  • Polazzi E, Levi G, Minghetti L (1999) Human immunodeficiency virus type 1 tat protein stimulates inducible nitric oxide synthase expression and nitric oxide production in microglial cultures. J Neuropathol Exp Neurol 58:825–831

    PubMed  CAS  Google Scholar 

  • Poole LB, Zeng BB, Knaggs SA, Yakubu M, King SB (2005) Synthesis of chemical probes to map sulfenic acid modifications on proteins. Bioconjug Chem 16:1624–1628

    PubMed  CAS  Google Scholar 

  • Prakash A, Rezai T, Krastins B, Sarracino D, Athanas M, Russo P, Ross MM, Zhang H, Tian Y, Kulasingam V, Drabovich AP, Smith C, Batruch I, Liotta L, Petricoin E, Diamandis EP, Chan DW, Lopez MF (2010) Platform for establishing interlaboratory reproducibility of selected reaction monitoring-based mass spectrometry peptide assays. J Proteome Res 9:6678–6688

    PubMed  CAS  Google Scholar 

  • Prakash A et al (2012) Interlaboratory reproducibility of selective reaction monitoring assays using multiple upfront analyte enrichment strategies. J Proteome Res 11:3986–3995

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rebrin I, Bregere C, Kamzalov S, Gallaher TK, Sohal RS (2007) Nitration of tryptophan 372 in succinyl-CoA:3-ketoacid CoA transferase during aging in rat heart mitochondria. Biochemistry 46:10130–10144

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rozek W, Ricardo-Dukelow M, Holloway S, Gendelman HE, Wojna V, Melendez LM, Ciborowski P (2007) Cerebrospinal fluid proteomic profiling of HIV-1-infected patients with cognitive impairment. J Proteome Res 6:4189–4199

    PubMed  CAS  Google Scholar 

  • Sabri F, Tresoldi E, Di Stefano M, Polo S, Monaco MC, Verani A, Fiore JR, Lusso P, Major E, Chiodi F, Scarlatti G (1999) Nonproductive human immunodeficiency virus type 1 infection of human fetal astrocytes: independence from CD4 and major chemokine receptors. Virology 264:370–384

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Safinowski M, Wilhelm B, Reimer T, Weise A, Thome N, Hanel H, Forst T, Pfutzner A (2009) Determination of nitrotyrosine concentrations in plasma samples of diabetes mellitus patients by four different immunoassays leads to contradictive results and disqualifies the majority of the tests. Clin Chem Lab Med 47:483–488

    PubMed  CAS  Google Scholar 

  • Sala A, Nicolis S, Roncone R, Casella L, Monzani E (2004) Peroxidase catalyzed nitration of tryptophan derivatives. mechanism, products and comparison with chemical nitrating agents. Eur J Biochem 271:2841–2852

    PubMed  CAS  Google Scholar 

  • Sampson JB, Rosen H, Beckman JS (1996) Peroxynitrite-dependent tyrosine nitration catalyzed by superoxide dismutase, myeloperoxidase, and horseradish peroxidase. Methods Enzymol 269:210–218

    PubMed  CAS  Google Scholar 

  • Sardar AM, Reynolds GP (1995) Frontal cortex indoleamine-2,3-dioxygenase activity is increased in HIV-1-associated dementia. Neurosci Lett 187:9–12

    PubMed  CAS  Google Scholar 

  • Sardar AM, Bell JE, Reynolds GP (1995) Increased concentrations of the neurotoxin 3-hydroxykynurenine in the frontal cortex of HIV-1-positive patients. J Neurochem 64:932–935

    PubMed  CAS  Google Scholar 

  • Saurin AT, Neubert H, Brennan JP, Eaton P (2004) Widespread sulfenic acid formation in tissues in response to hydrogen peroxide. Proc Natl Acad Sci U S A 101:17982–17987

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sayre LM, Lin D, Yuan Q, Zhu X, Tang X (2006) Protein adducts generated from products of lipid oxidation: focus on HNE and one. Drug Metab Rev 38:651–675

    PubMed  CAS  Google Scholar 

  • Sethuraman M, McComb ME, Huang H, Huang S, Heibeck T, Costello CE, Cohen RA (2004) Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures. J Proteome Res 3:1228–1233

    PubMed  CAS  Google Scholar 

  • Simioni S, Cavassini M, Annoni JM, Rimbault Abraham A, Bourquin I, Schiffer V, Calmy A, Chave JP, Giacobini E, Hirschel B, Du Pasquier RA (2010) Cognitive dysfunction in HIV patients despite long-standing suppression of viremia. AIDS 24:1243–1250

    PubMed  Google Scholar 

  • Sinha V, Wijewickrama GT, Chandrasena RE, Xu H, Edirisinghe PD, Schiefer IT, Thatcher GR (2010) Proteomic and mass spectroscopic quantitation of protein S-nitrosation differentiates NO-donors. ACS Chem Biol 5:667–680

    PubMed  CAS  PubMed Central  Google Scholar 

  • Smallwood HS, Lourette NM, Boschek CB, Bigelow DJ, Smith RD, Pasa-Tolic L, Squier TC (2007) Identification of a denitrase activity against calmodulin in activated macrophages using high-field liquid chromatography–FTICR mass spectrometry. Biochemistry 46:10498–10505

    PubMed  CAS  Google Scholar 

  • Stark G (2005) Functional consequences of oxidative membrane damage. J Membr Biol 205:1–16

    PubMed  CAS  Google Scholar 

  • Starkov AA, Chinopoulos C, Fiskum G (2004) Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36:257–264

    PubMed  CAS  Google Scholar 

  • Steiner J, Haughey N, Li W, Venkatesan A, Anderson C, Reid R, Malpica T, Pocernich C, Butterfield DA, Nath A (2006) Oxidative stress and therapeutic approaches in HIV dementia. Antioxid Redox Signal 8:2089–2100

    PubMed  CAS  Google Scholar 

  • Sturgeon CM, Seth J (1996) Why do immunoassays for tumour markers give differing results?–a view from the UK national external quality assessment schemes. Eur J Clin Chem Clin Biochem 34:755–759

    PubMed  CAS  Google Scholar 

  • Sturgeon CM, Sprague SM, Metcalfe W (2011) Variation in parathyroid hormone immunoassay results–a critical governance issue in the management of chronic kidney disease. Nephrol Dial Transplant 26:3440–3445

    PubMed  CAS  PubMed Central  Google Scholar 

  • Torres-Munoz J, Stockton P, Tacoronte N, Roberts B, Maronpot RR, Petito CK (2001) Detection of HIV-1 gene sequences in hippocampal neurons isolated from postmortem AIDS brains by laser capture microdissection. J Neuropathol Exp Neurol 60:885–892

    PubMed  CAS  Google Scholar 

  • Tsikas D (2010) Measurement of nitrotyrosine in plasma by immunoassays is fraught with danger: commercial availability is no guarantee of analytical reliability. Clin Chem Lab Med 48:141–143, author reply 145–6

    PubMed  CAS  Google Scholar 

  • Tsikas D (2012) Analytical methods for 3-nitrotyrosine quantification in biological samples: the unique role of tandem mass spectrometry. Amino Acids 42:45–63

    PubMed  CAS  Google Scholar 

  • Tsikas D, Frolich JC (2004) Trouble with the analysis of nitrite, nitrate, S-nitrosothiols and 3-nitrotyrosine: freezing-induced artifacts? Nitric Oxide 11:209–213, author reply 214–5

    PubMed  CAS  Google Scholar 

  • Turchan J, Pocernich CB, Gairola C, Chauhan A, Schifitto G, Butterfield DA, Buch S, Narayan O, Sinai A, Geiger J, Berger JR, Elford H, Nath A (2003) Oxidative stress in HIV demented patients and protection ex vivo with novel antioxidants. Neurology 60:307–314

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tyor WR, Glass JD, Griffin JW, Becker PS, McArthur JC, Bezman L, Griffin DE (1992) Cytokine expression in the brain during the acquired immunodeficiency syndrome. Ann Neurol 31:349–360

    PubMed  CAS  Google Scholar 

  • Uda M, Kawasaki H, Shigenaga A, Baba T, Yamakura F (2012) Proteomic analysis of endogenous nitrotryptophan-containing proteins in rat hippocampus and cerebellum. Biosci Rep 32:521–530

    Google Scholar 

  • Velazquez I, Plaud M, Wojna V, Skolasky R, Laspiur JP, Melendez LM (2009) Antioxidant enzyme dysfunction in monocytes and CSF of hispanic women with HIV-associated cognitive impairment. J Neuroimmunol 206:106–111

    PubMed  CAS  PubMed Central  Google Scholar 

  • Vignais PV (2002) The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci 59:1428–1459

    PubMed  CAS  Google Scholar 

  • Westendorp MO, Shatrov VA, Schulze-Osthoff K, Frank R, Kraft M, Los M, Krammer PH, Droge W, Lehmann V (1995) HIV-1 tat potentiates TNF-induced NF-kappa B activation and cytotoxicity by altering the cellular redox state. EMBO J 14:546–554

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB (1986) Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci U S A 83:7089–7093

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yamakura F, Ikeda K (2006) Modification of tryptophan and tryptophan residues in proteins by reactive nitrogen species. Nitric Oxide 14:152–161

    Google Scholar 

  • Yamakura F, Matsumoto T, Taka H, Fujimura T, Murayama K (2003) 6-nitrotryptophan: A specific reaction product of tryptophan residue in human cu, zn-SOD treated with peroxynitrite. Adv Exp Med Biol 527:745–749

    Google Scholar 

  • Yamazaki I, Piette LH (1990) ESR spin-trapping studies on the reaction of Fe2+ ions with H2O2-reactive species in oxygen toxicity in biology. J Biol Chem 265:13589–13594

    PubMed  CAS  Google Scholar 

  • Zang L, Carlage T, Murphy D, Frenkel R, Bryngelson P, Madsen M, Lyubarskaya Y (2012) Residual metals cause variability in methionine oxidation measurements in protein pharmaceuticals using LC-UV/MS peptide mapping. J Chromatogr B Analyt Technol Biomed Life Sci 895–896:71–76

    PubMed  Google Scholar 

  • Zhang J, Li S, Zhang D, Wang H, Whorton AR, Xian M (2010a) Reductive ligation mediated one-step disulfide formation of S-nitrosothiols. Org Lett 12:4208–4211

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang X, Monroe ME, Chen B, Chin MH, Heibeck TH, Schepmoes AA, Yang F, Petritis BO, Camp DG II, Pounds JG, Jacobs JM, Smith DJ, Bigelow DJ, Smith RD, Qian WJ (2010b) Endogenous 3,4-dihydroxyphenylalanine and dopaquinone modifications on protein tyrosine: links to mitochondrially derived oxidative stress via hydroxyl radical. Mol Cell Proteomics 9:1199–1208

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhou L, Diefenbach E, Crossett B, Tran SL, Ng T, Rizos H, Rua R, Wang B, Kapur A, Gandhi K, Brew BJ, Saksena NK (2010) First evidence of overlaps between HIV-associated dementia (HAD) and non-viral neurodegenerative diseases: proteomic analysis of the frontal cortex from HIV + patients with and without dementia. Mol Neurodegener 5:27-1326-5-27

    Google Scholar 

Download references

Acknowledgments

RJC and LU were supported by grants R01NS039253 (Cotter R, PI) from the National Institute of Neurological Disorders and Stroke and P30MH075673 (McArthur J, PI) from the National Institute of Mental Health. AN is supported by intramural NIH funds.

Conflict of Interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA

    Lerna Uzasci & Robert Cotter

  2. Section of Infections of the Nervous System, NINDS, National Institutes of Health, Bethesda, MD, 20892, USA

    Avindra Nath

Authors
  1. Lerna Uzasci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Avindra Nath
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert Cotter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lerna Uzasci.

Additional information

Robert Cotter: deceased November 12, 2012

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uzasci, L., Nath, A. & Cotter, R. Oxidative Stress and the HIV-Infected Brain Proteome. J Neuroimmune Pharmacol 8, 1167–1180 (2013). https://doi.org/10.1007/s11481-013-9444-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11481-013-9444-x

Keywords

Search

Navigation