Identification of putative biomarkers for HIV-associated neurocognitive impairment in the CSF of HIV-infected patients under cART therapy determined by mass spectrometry

Journal of NeuroVirology

Volumn 20, Issue 5, 2014, Pages 457-465

  Bora, Adriana ^a,d   Mohien, Ceereena Ubaida ^a   Chaerkady, Raghothama ^b   Chang, Linda ^c   4th Moxley, Richard ^d   Sacktor, Ned ^d   Haughey, Norman ^d   McArthur, Justin C ^d   Cotter, Robert ^b   Nath, Avindra ^e   Graham, David R ^a  

^a Department of Molecular and Comparative Pathobiology Retrovirus Laboratory ^*  (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HAWAII   (United States)

^d UNIVERSITY OF HAWAII   (United States)

^e NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Biomarker; HIV; i TRAQ; Mass spectrometry; Proteomics

Indexed keywords

ALPHA N ACETYLGLUCOSAMINIDASE; APOLIPOPROTEIN E; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CADHERIN EGF LAG G TYPE RECEPTOR; CALDESMON; ENDOPLASMIN; FORMIN BINDING PROTEIN 1 LIKE ISOFORM 2; LAMIVUDINE; LEUKOCYTE ASSOCIATED IMMUNOGLOBULIN RECEPTOR 1; MEDIATOR OF RNA POLYMERASE II TRANSCRIPTION SUBUNIT 14; METALLOPROTEINASE INHIBITOR 2; MITOCHONDRIAL DAMAGE MEDIATOR BH3 INTERACTING DOMAIN DEATH AGONIST; MULTIMERIN 2 PROTEIN; NUCLEAR PROTEIN; OROSOMUCOID; PEROXIREDOXIN 2; PRORENIN RECEPTOR; PROTEINASE INHIBITOR; RUVB LIKE 2 PROTEIN; STAVUDINE; TRYPSIN; UNCLASSIFIED DRUG; ZIDOVUDINE; ANTIRETROVIRUS AGENT;

ADULT; ARTICLE; CEREBROSPINAL FLUID; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; MASS SPECTROMETRY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; AIDS DEMENTIA COMPLEX; LIQUID CHROMATOGRAPHY; MIDDLE AGED;

ADULT; AIDS DEMENTIA COMPLEX; ANTI-RETROVIRAL AGENTS; BIOMARKERS; CHROMATOGRAPHY, LIQUID; FEMALE; HUMANS; MALE; MASS SPECTROMETRY; MIDDLE AGED;

EID: 84910144160     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-014-0263-5     Document Type: Article

References (61)

1. Aggarwal A, Iemma TL, Shih I, Newsome TP, McAllery S et al (2012) Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog 8:e1002762
2. Alpert AJ, Andrews PC (1988) Cation-exchange chromatography of peptides on poly(2-sulfoethyl aspartamide)-silica. J Chromatogr 443:85–96
3. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA et al (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799
4. Atemezem A, Mbemba E, Vassy R, Slimani H, Saffar L, Gattegno L (2001) Human alpha1-acid glycoprotein binds to CCR5 expressed on the plasma membrane of human primary macrophages. Biochem J 356:121–128
5. Bantscheff M, Boesche M, Eberhard D, Matthieson T, Sweetman G, Kuster B (2008) Robust and sensitive iTRAQ quantification on an LTQ Orbitrap mass spectrometer. Mol Cell Proteomics 7:1702–1713
6. Boehm AM, Putz S, Altenhofer D, Sickmann A, Falk M (2007) Precise protein quantification based on peptide quantification using iTRAQ. BMC Bioinformatics 8:214
7. Boutin C, Goffinet AM, Tissir F (2012) Celsr1-3 cadherins in PCP and brain development. Curr Top Dev Biol 101:161–183
8. Chico L, Simoncini C, Lo Gerfo A, Rocchi A, Petrozzi L et al (2013) Oxidative stress and APO E polymorphisms in Alzheimer’s disease and in mild cognitive impairment. Free Radic Res 47:569–576
9. Choe LH, Aggarwal K, Franck Z, Lee KH (2005) A comparison of the consistency of proteome quantitation using two-dimensional electrophoresis and shotgun isobaric tagging in Escherichia coli cells. Electrophoresis 26:2437–2449
10. Cousin C, Bracquart D, Contrepas A, Corvol P, Muller L, Nguyen G (2009) Soluble form of the (pro)renin receptor generated by intracellular cleavage by furin is secreted in plasma. Hypertension 53:1077–1082
11. Gan CS, Chong PK, Pham TK, Wright PC (2007) Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res 6:821–827
12. Gautier VW, Gu L, O’Donoghue N, Pennington S, Sheehy N, Hall WW (2009) In vitro nuclear interactome of the HIV-1 Tat protein. Retrovirology 6:47
13. Hayward CP (1997) Multimerin: a bench-to-bedside chronology of a unique platelet and endothelial cell protein–from discovery to function to abnormalities in disease. Clin Invest Med 20:176–187
14. Heaton R. 2012a. Asymptomatic mild HIV-associated neurocognitive disorder increases risk for future symptomatic decline: a CHARTER longitudinal study. 19th CROI, 2012, Seattle. Oral abstract 81.
15. Heaton R. 2012b. Prevalence and predictors of neurocognitive decline over 18 to 42 Months: a CHARTER longitudinal study. 19th CROI, Seattle. Poster abstract 474.
16. Herbrich SM, Cole RN, West KP Jr, Schulze K, Yager JD et al (2013) Statistical inference from multiple iTRAQ experiments without using common reference standards. J Proteome Res 12:594–604
17. Hu J, Qian J, Borisov O, Pan S, Li Y et al (2006) Optimized proteomic analysis of a mouse model of cerebellar dysfunction using amine-specific isobaric tags. Proteomics 6:4321–4334
18. Huang X, Stone DK, Yu F, Zeng Y, Gendelman HE (2010) Functional proteomic analysis for regulatory T cell surveillance of the HIV-1-infected macrophage. J Proteome Res 9:6759–6773
19. Impens F, Timmerman E, Staes A, Moens K, Arien KK et al (2012) A catalogue of putative HIV-1 protease host cell substrates. Biol Chem 393:915–931
20. Jeimy SB, Tasneem S, Cramer EM, Hayward CP (2008) Multimerin 1. Platelets 19:83–95
21. Karim S, Hopkins S, Purandare N, Crowther J, Morris J, et al. 2013. Peripheral inflammatory markers in amnestic mild cognitive impairment. Int J Geriatr Psychiatry
22. Karp NA, Huber W, Sadowski PG, Charles PD, Hester SV, Lilley KS (2010) Addressing accuracy and precision issues in iTRAQ quantitation. Mol Cell Proteomics 9:1885–1897
23. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383–5392
24. Keshamouni VG, Michailidis G, Grasso CS, Anthwal S, Strahler JR et al (2006) Differential protein expression profiling by iTRAQ-2DLC-MS/MS of lung cancer cells undergoing epithelial-mesenchymal transition reveals a migratory/invasive phenotype. J Proteome Res 5:1143–1154
25. Kreipke CW, Morgan NC, Petrov T, Rafols JA (2006) Calponin and caldesmon cellular domains in reacting microvessels following traumatic brain injury. Microvasc Res 71:197–204
26. Lafrenie RM, Wahl LM, Epstein JS, Hewlett IK, Yamada KM, Dhawan S (1996a) HIV-1-Tat modulates the function of monocytes and alters their interactions with microvessel endothelial cells. A mechanism of HIV pathogenesis. J Immunol 156:1638–1645
27. Lafrenie RM, Wahl LM, Epstein JS, Hewlett IK, Yamada KM, Dhawan S (1996b) HIV-1-Tat protein promotes chemotaxis and invasive behavior by monocytes. J Immunol 157:974–977
28. Letendre S. 2012. A concise panel of biomarkers diagnoses and predicts neurocognitive status in HIV-infected individuals. 19th CROI, 2012, Seattle. Oral abstract 82.
29. Lin WT, Hung WN, Yian YH, Wu KP, Han CL et al (2006) Multi-Q: a fully automated tool for multiplexed protein quantitation. J Proteome Res 5:2328–2338
30. Lin CC, Chang CM, Liu CY, Huang TL (2013) Increased high-sensitivity C-reactive protein levels in Taiwanese schizophrenic patients. Asia Pac Psychiatry 5:E58–E63
31. Linde ME, Colquhoun DR, Ubaida Mohien C, Kole T, Aquino V, et al. 2013. The conserved set of host proteins incorporated into HIV-1 virions suggests a common egress pathway in multiple cell types. J Proteome Res
32. Liu Y, Jones M, Hingtgen CM, Bu G, Laribee N et al (2000) Uptake of HIV-1 tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat Med 6:1380–1387
33. Mahoney DW, Therneau TM, Heppelmann CJ, Higgins L, Benson LM et al (2011) Relative quantification: characterization of bias, variability and fold changes in mass spectrometry data from iTRAQ-labeled peptides. J Proteome Res 10:4325–4333
34. McArthur JC, McDermott MP, McClernon D, St Hillaire C, Conant K et al (2004) Attenuated central nervous system infection in advanced HIV/AIDS with combination antiretroviral therapy. Arch Neurol 61:1687–1696
35. Mohamed MA, Barker PB, Skolasky RL, Selnes OA, Moxley RT et al (2010) Brain metabolism and cognitive impairment in HIV infection: a 3-T magnetic resonance spectroscopy study. Magn Reson Imaging 28:1251–1257
36. Navare AT, Sova P, Purdy DE, Weiss JM, Wolf-Yadlin A et al (2012) Quantitative proteomic analysis of HIV-1 infected CD4+ T cells reveals an early host response in important biological pathways: protein synthesis, cell proliferation, and T-cell activation. Virology 429:37–46
37. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646–4658
38. Nie Z, Phenix BN, Lum JJ, Alam A, Lynch DH et al (2002) HIV-1 protease processes procaspase 8 to cause mitochondrial release of cytochrome c, caspase cleavage and nuclear fragmentation. Cell Death Differ 9:1172–1184
39. Ow SY, Salim M, Noirel J, Evans C, Rehman I, Wright PC (2009) iTRAQ underestimation in simple and complex mixtures: “the good, the bad and the ugly”. J Proteome Res 8:5347–5355
40. Park SE, Lee MJ, Yang MH, Ahn KY, Jang SI et al (2007) Expression profiles and pathway analysis in HEK 293 T cells overexpressing HIV-1 Tat and nucleocapsid using cDNA microarray. J Microbiol Biotechnol 17:154–161
41. Pendyala G, Trauger SA, Siuzdak G, Fox HS (2010) Quantitative plasma proteomic profiling identifies the vitamin E binding protein afamin as a potential pathogenic factor in SIV induced CNS disease. J Proteome Res 9:352–358
42. Pichler P, Kocher T, Holzmann J, Mazanek M, Taus T et al (2010) Peptide labeling with isobaric tags yields higher identification rates using iTRAQ 4-plex compared to TMT 6-plex and iTRAQ 8-plex on LTQ Orbitrap. Anal Chem 82:6549–6558
43. Pocernich CB, Sultana R, Hone E, Turchan J, Martins RN et al (2004) Effects of apolipoprotein E on the human immunodeficiency virus protein Tat in neuronal cultures and synaptosomes. J Neurosci Res 77:532–539
44. Pottiez G, Wiederin J, Fox HS, Ciborowski P (2012) Comparison of 4-plex to 8-plex iTRAQ quantitative measurements of proteins in human plasma samples. J Proteome Res 11:3774–3781
45. Price RW, Peterson J, Fuchs D, Angel TE, Zetterberg H et al (2013) Approach to cerebrospinal fluid (CSF) biomarker discovery and evaluation in HIV infection. Journal of neuroimmune pharmacology: the official journal of the Society on NeuroImmune Pharmacology 8:1147–1158
46. Rabehi L, Ferriere F, Saffar L, Gattegno L (1995) Alpha 1-acid glycoprotein binds human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein via N-linked glycans. Glycoconj J 12:7–16
47. Sadigh-Eteghad S, Talebi M, Farhoudi M (2012) Association of apolipoprotein E epsilon 4 allele with sporadic late onset Alzheimer’s disease. A meta-analysis Neurosciences (Riyadh) 17:321–326
48. Schouten J, Cinque P, Gisslen M, Reiss P, Portegies P (2011) HIV-1 infection and cognitive impairment in the cART era: a review. Aids 25:561–575
49. Shadforth IP, Dunkley TP, Lilley KS, Bessant C. 2005. i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics 6: 145
50. Shetty V, Jain P, Nickens Z, Sinnathamby G, Mehta A, Philip R (2011) Investigation of plasma biomarkers in HIV-1/HCV mono- and coinfected individuals by multiplex iTRAQ quantitative proteomics. Omics 15:705–717
51. Snyder A, Alsauskas ZC, Leventhal JS, Rosenstiel PE, Gong P et al (2010) HIV-1 viral protein r induces ERK and caspase-8-dependent apoptosis in renal tubular epithelial cells. Aids 24:1107–1119
52. Tharakan R, Edwards N, Graham DR (2010) Data maximization by multipass analysis of protein mass spectra. Proteomics 10:1160–1171
53. Toschi E, Barillari G, Sgadari C, Bacigalupo I, Cereseto A et al (2001) Activation of matrix-metalloproteinase-2 and membrane-type-1-matrix-metalloproteinase in endothelial cells and induction of vascular permeability in vivo by human immunodeficiency virus-1 Tat protein and basic fibroblast growth factor. Mol Biol Cell 12:2934–2946
54. Tun C, Guo W, Nguyen H, Yun B, Libby RT et al (2007) Activation of the extrinsic caspase pathway in cultured cortical neurons requires p53-mediated down-regulation of the X-linked inhibitor of apoptosis protein to induce apoptosis. J Neurochem 102:1206–1219
55. Turchan-Cholewo J, Liu Y, Gartner S, Reid R, Jie C et al (2006) Increased vulnerability of ApoE4 neurons to HIV proteins and opiates: protection by diosgenin and L-deprenyl. Neurobiol Dis 23:109–119
56. Tzoupis H, Leonis G, Megariotis G, Supuran CT, Mavromoustakos T, Papadopoulos MG (2012) Dual inhibitors for aspartic proteases HIV-1 PR and renin: advancements in AIDS-hypertension-diabetes linkage via molecular dynamics, inhibition assays, and binding free energy calculations. J Med Chem 55:5784–5796
57. Uzasci L, Nath A, Cotter R. 2013. Oxidative stress and the HIV-infected brain proteome. J Neuroimmune Pharmacol
58. Verghese PB, Castellano JM, Garai K, Wang Y, Jiang H et al (2013) ApoE influences amyloid-beta (Abeta) clearance despite minimal apoE/Abeta association in physiological conditions. Proc Natl Acad Sci U S A 110:E1807–E1816
59. Wang Y, Yang F, Gritsenko MA, Wang Y, Clauss T et al (2011) Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells. Proteomics 11:2019–2026
60. Wu WW, Wang G, Baek SJ, Shen RF (2006) Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J Proteome Res 5:651–658
61. Zieske LR (2006) A perspective on the use of iTRAQ reagent technology for protein complex and profiling studies. J Exp Bot 57:1501–1508