The cerebrospinal fluid proteome in HIV infection: Change associated with disease severity

Clinical Proteomics

Volumn 9, Issue 1, 2012, Pages

  Angel, Thomas E ^a   Jacobs, Jon M ^a   Spudich, Serena S ^b,e   Gritsenko, Marina A ^a   Fuchs, Dietmar ^c   Liegler, Teri ^b   Zetterberg, Henrik ^d   Camp II, David G ^a   Price, Richard W ^b   Smith, Richard D ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amyloid; Cerebrospinal fluid; HIV; Pathway; Proteomics

Indexed keywords

ALPHA 2 MACROGLOBULIN; AMYLOID PRECURSOR PROTEIN; ANTIRETROVIRUS AGENT; APOLIPOPROTEIN E; AUTOTAXIN; BIOLOGICAL MARKER; BRAIN PROTEIN; CALSYNTENIN 1; CD59 ANTIGEN; CLUSTERIN; CONTACTIN 1; COPPER ZINC SUPEROXIDE DISMUTASE 1; COPPER ZINC SUPEROXIDE DISMUTASE 2; KALLIKREIN 6; NEOPTERIN; NERVE CELL ADHESION MOLECULE 1; NEUROFILAMENT LIGHT CHAIN PROTEIN; PROTEOME; PROTHROMBIN; UNCLASSIFIED DRUG; VIRUS RNA;

ADULT; ARTICLE; CEREBROSPINAL FLUID ANALYSIS; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOREGULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NERVE CELL PLASTICITY; NERVOUS SYSTEM INJURY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN DATABASE; SURVIVAL;

EID: 84865677957     PISSN: 15426416     EISSN: 15590275     Source Type: Journal    
DOI: 10.1186/1559-0275-9-3     Document Type: Article

References (95)

1. Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, Merlin TL, Young SA, Mills RG, Wachsman W, Wiley CA: Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 1992, 42:1736-1739.
2. Pilcher CD, Shugars DC, Fiscus SA, Miller WC, Menezes P, Giner J, Dean B, Robertson K, Hart CE, Lennox JL, et al: HIV in body fluids during primary HIV infection: implications for pathogenesis, treatment and public health. AIDS 2001, 15:837-845. (Pubitemid 32424387)
3. Ellis RJ, Hsia K, Spector SA, Nelson JA, Heaton RK, Wallace MR, Abramson I, Atkinson JH, Grant I, McCutchan JA: Cerebrospinal fluid human immunodeficiency virus type 1 RNA levels are elevated in neurocognitively impaired individuals with acquired immunodeficiency syndrome. HIV Neurobehavioral Research Center Group. Ann Neurol 1997, 42:679-688. (Pubitemid 27481539)
4. McArthur JC, McClernon DR, Cronin MF, Nance-Sproson TE, Saah AJ, St Clair M, Lanier ER: Relationship between human immunodeficiency virus-associated dementia and viral load in cerebrospinal fluid and brain. Ann Neurol 1997, 42:689-698. (Pubitemid 27481540)
5. Spudich SS, Nilsson AC, Lollo ND, Liegler TJ, Petropoulos CJ, Deeks SG, Paxinos EE, Price RW: Cerebrospinal fluid HIV infection and pleocytosis: Relation to systemic infection and antiretroviral treatment. BMC Infect Dis 2005, 5:98.
6. Spudich S, Lollo N, Liegler T, Deeks SG, Price RW: Treatment benefit on cerebrospinal fluid HIV-1 levels in the setting of systemic virological suppression and failure. J Infect Dis 2006, 194:1686-1696. (Pubitemid 44901999)
7. Navia BA, Jordan BD, Price RW: The AIDS dementia complex: I. Clinical features. Ann Neurol 1986, 19:517-524. (Pubitemid 16085185)
8. Navia BA, Cho ES, Petito CK, Price RW: The AIDS dementia complex: II. Neuropathology Ann Neurol 1986, 19:525-535.
9. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, et al: Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007, 69:1789-1799. (Pubitemid 350059308)
10. Gonzalez-Scarano F, Martin-Garcia J: The neuropathogenesis of AIDS. Nat Rev Immunol 2005, 5:69-81. (Pubitemid 40070332)
11. Kaul M: HIV-1 associated dementia: Update on pathological mechanisms and therapeutic approaches. Curr Opin Neurol 2009, 22:315-320.
12. D'Arminio Monforte A, Cinque P, Mocroft A, Goebel FD, Antunes F, Katlama C, Justesen US, Vella S, Kirk O, Lundgren J: Changing incidence of central nervous system diseases in the Euro SIDA cohort. Ann Neurol 2004, 55:320-328. (Pubitemid 38292033)
13. Lescure FX, Omland LH, Engsig FN, Roed C, Gerstoft J, Pialoux G, Kronborg G, Larsen CS, Obel N: Incidence and Impact on Mortality of Severe Neurocognitive Disorders in Persons With and Without HIV Infection: A Danish Nationwide Cohort Study. Clinical infectious diseases: An official publication of the Infectious Diseases Society of America 2011, 52:235-243.
14. Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, Wu J, McArthur JC, Collier AC, Evans SR, Ellis RJ: The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 2007, 21:1915-1921. (Pubitemid 47329768)
15. Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, et al: HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 2010, 75:2087-2096.
16. Smurzynski M, Wu K, Letendre S, Robertson K, Bosch RJ, Clifford DB, Evans S, Collier AC, Taylor M, Ellis R: Effects of central nervous system antiretroviral penetration on cognitive functioning in the ALLRT cohort. AIDS 2011, 25:357-365.
17. Deeks SG: HIV infection, inflammation, immunosenescence, and aging. Annual review of medicine 2011, 62:141-155.
18. Coisne C, Engelhardt B: Tight junctions in brain barriers during central nervous system inflammation. Antioxidants & redox signaling 2011, 15(5):1285-1303.
19. Engelhardt B, Sorokin L: The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction. Semin Immunopathol 2009, 31:497-511.
20. Harrington PR, Haas DW, Ritola K, Swanstrom R: Compartmentalized human immunodeficiency virus type 1 present in cerebrospinal fluid is produced by short-lived cells. J Virol 2005, 79:7959-7966. (Pubitemid 40853500)
21. Harrington PR, Schnell G, Letendre SL, Ritola K, Robertson K, Hall C, Burch CL, Jabara CB, Moore DT, Ellis RJ, et al: Crosssectional characterization of HIV-1 env compartmentalization in cerebrospinal fluid over the full disease course. AIDS 2009, 23:907-915.
22. Schnell G, Price RW, Swanstrom R, Spudich S: Compartmentalization and clonal amplification of HIV-1 variants in the cerebrospinal fluid during primary infection. J Virol 2010, 84:2395-2407.
23. Sinclair E, Ronquillo R, Lollo N, Deeks SG, Hunt P, Yiannoutsos CT, Spudich S, Price RW: Antiretroviral treatment effect on immune activation reduces cerebrospinal fluid HIV-1 infection. J Acquir Immune Defic Syndr 2008, 47:544-552. (Pubitemid 351442007)
24. Yilmaz A, Price RW, Spudich S, Fuchs D, Hagberg L, Gisslen M: Persistent intrathecal immune activation in HIV-1- infected individuals on antiretroviral therapy. J Acquir Immune Defic Syndr 2008, 47:168-173. (Pubitemid 351172183)
25. Hagberg L, Cinque P, Gisslen M, Brew BJ, Spudich S, Bestetti A, Price RW, Fuchs D: Cerebrospinal fluid neopterin: An informative biomarker of central nervous system immune activation in HIV-1 infection. AIDS Res Ther 2010, 7:15.
26. Abdulle S, Mellgren A, Brew BJ, Cinque P, Hagberg L, Price RW, Rosengren L, Gisslen M: CSF neurofilament protein (NFL) - A marker of active HIV-related neurodegeneration. J Neurol 2007, 254:1026-1032. (Pubitemid 47353414)
27. Gisslen M, Krut J, Andreasson U, Blennow K, Cinque P, Brew BJ, Spudich S, Hagberg L, Rosengren L, Price RW, Zetterberg H: Amyloid and tau cerebrospinal fluid biomarkers in HIV infection. BMC Neurol 2009, 9:63.
28. Mellgren A, Antinori A, Cinque P, Price RW, Eggers C, Hagberg L, Gisslen M: Cerebrospinal fluid HIV-1 infection usually responds well to antiretroviral treatment. Antivir Ther 2005, 10:701-707. (Pubitemid 41376848)
29. Canestri A, Lescure FX, Jaureguiberry S, Moulignier A, Amiel C, Marcelin AG, Peytavin G, Tubiana R, Pialoux G, Katlama C: Discordance between cerebral spinal fluid and plasma HIV replication in patients with neurological symptoms who are receiving suppressive antiretroviral therapy. Clin Infect Dis 2010, 50:773-778.
30. Eden A, Fuchs D, Hagberg L, Nilsson S, Spudich S, Svennerholm B, Price RW, Gisslen M: HIV-1 viral escape in cerebrospinal fluid of subjects on suppressive antiretroviral treatment. J Infect Dis 2010, 202:1819-1825.
31. Cinque P, Brew BJ, Gisslen M, Hagberg L, Price RW: Cerebrospinal fluid markers in central nervous system HIV infection and AIDS dementia complex. In Handbook of clinical neurology Edited by: Vinken PJ, Bruyn GW 2007, 85:261-300.
32. Gisslen M, Hagberg L, Rosengren L, Brew BJ, Cinque P, Spudich S, Price RW: Defining and evaluating HIV-related neurodegenerative disease and its treatment targets: A combinatorial approach to use of cerebrospinal fluid molecular biomarkers. J Neuroimmune Pharmacol 2007, 2:112-119.
33. Zimmer JS, Monroe ME, Qian WJ, Smith RD: Advances in proteomics data analysis and display using an accurate mass and time tag approach. Mass Spectrom Rev 2006, 25:450-482.
34. Fang Q, Strand A, Law W, Faca VM, Fitzgibbon MP, Hamel N, Houle B, Liu X, May DH, Poschmann G, et al: Brainspecific proteins decline in the cerebrospinal fluid of humans with Huntington disease. Molecular & cellular proteomics: MCP 2009, 8:451-466.
35. Rozek W, Ricardo-Dukelow M, Holloway S, Gendelman HE, Wojna V, Melendez LM, Ciborowski P: Cerebrospinal fluid proteomic profiling of HIV-1-infected patients with cognitive impairment. J Proteome Res 2007, 6:4189-4199. (Pubitemid 350158497)
36. Schutzer SE, Liu T, Natelson BH, Angel TE, Schepmoes AA, Purvine SO, Hixson KK, Lipton MS, Camp DG, Coyle PK, et al: Establishing the proteome of normal human cerebrospinal fluid. PLoS One 2010, 5:e10980.
37. Ekegren T, Hanrieder J, Bergquist J: Clinical perspectives of high-resolution mass spectrometry-based proteomics in neuroscience: exemplified in amyotrophic lateral sclerosis biomarker discovery research. J Mass Spectrom 2008, 43:559-571. (Pubitemid 351785680)
38. Maarouf CL, Andacht TM, Kokjohn TA, Castano EM, Sue LI, Beach TG, Roher AE: Proteomic analysis of Alzheimer's disease cerebrospinal fluid from neuropathologically diagnosed subjects. Curr Alzheimer Res 2009, 6:399-406.
39. Stoop MP, Dekker LJ, Titulaer MK, Lamers RJ, Burgers PC, Sillevis-Smitt PA, van Gool AJ, Luider TM, Hintzen RQ: Quantitative matrix-assisted laser desorption ionization-fourier transform ion cyclotron resonance (MALDI-FT-ICR) peptide profiling and identification of multiple-sclerosis-related proteins. J Proteome Res 2009, 8:1404-1414.
40. Constantinescu R, Andreasson U, Li S, Podust VN, Mattsson N, Anckarsater R, Anckarsater H, Rosengren L, Holmberg B, Blennow K, et al: Proteomic profiling of cerebrospinal fluid in parkinsonian disorders. Parkinsonism Relat Disord 2010, 16:545-549.
41. Schutzer SE, Angel TE, Liu T, Schepmoes AA, Clauss TR, Adkins JN, Camp DG, Holland BK, Bergquist J, Coyle PK, et al: Distinct cerebrospinal fluid proteomes differentiate post-treatment lyme disease from chronic fatigue syndrome. PLoS One 2011, 6:e17287.
42. Shaffer SA, Prior DC, Anderson GA, Udseth HR, Smith RD: An ion funnel interface for improved ion focusing and sensitivity using electrospray ionization mass spectrometry. Anal Chem 1998, 70:4111-4119. (Pubitemid 128484755)
43. Smith RD, Anderson GA, Lipton MS, Pasa-Tolic L, Shen Y, Conrads TP, Veenstra TD, Udseth HR: An accurate mass tag strategy for quantitative and high-throughput proteome measurements. Proteomics 2002, 2:513-523. (Pubitemid 34507341)
44. Wirleitner B, Schroecksnadel K, Winkler C, Fuchs D: Neopterin in HIV-1 infection. Mol Immunol 2005, 42:183-194. (Pubitemid 39361448)
45. Mellgren A, Price RW, Hagberg L, Rosengren L, Brew BJ, Gisslen M: Antiretroviral treatment reduces increased CSF neurofilament protein (NFL) in HIV-1 infection. Neurology 2007, 69:1536-1541. (Pubitemid 47537861)
46. Gunnarsson M, Malmestrom C, Axelsson M, Sundstrom P, Dahle C, Vrethem M, Olsson T, Piehl F, Norgren N, Rosengren L, et al: Axonal damage in relapsing multiple sclerosis is markedly reduced by natalizumab. Ann Neurol 2011, 69:83-89.
47. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, et al: GoMiner: A resource for biological interpretation of genomic and proteomic data. Genome Biol 2003, 4:R28.
48. Gisslen M, Hagberg L, Brew BJ, Cinque P, Price RW, Rosengren L: Elevated cerebrospinal fluid neurofilament light protein concentrations predict the development of AIDS dementia complex. J Infect Dis 2007, 195:1774-1778. (Pubitemid 46870250)
49. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R: APP processing and synaptic function. Neuron 2003, 37:925-937. (Pubitemid 36398299)
50. Nuutinen T, Suuronen T, Kauppinen A, Salminen A: Clusterin: A forgotten player in Alzheimer's disease. Brain Res Rev 2009, 61:89-104.
51. Hwang HJ, Quinn T, Zhang J: Identification of glycoproteins in human cerebrospinal fluid. Methods Mol Biol 2009, 566:263-276.
52. Surinova S, Schiess R, Huttenhain R, Cerciello F, Wollscheid B, Aebersold R: On the Development of Plasma Protein Biomarkers. J Proteome Res 2011, 10:5-16.
53. Farrah T, Deutsch EW, et al: A high-confidence human plasma proteome reference set with estimated concentrations in Peptide Atlas. Molecular & cellular proteomics: MCP 2011, 10(9):110-6353.
54. Rifai N, Gerszten RE: Biomarker discovery and validation. Clin Chem 2006, 52:1635-1637. (Pubitemid 44330692)
55. Schiess R, Wollscheid B, Aebersold R: Targeted proteomic strategy for clinical biomarker discovery. Molecular oncology 2009, 3:33-44.
56. Hossain M, Kaleta DT, Robinson EW, Liu T, Zhao R, Page JS, Kelly RT, Moore RJ, Tang K, Camp DG, et al: Enhanced sensitivity for selected reaction monitoring mass spectrometry-based targeted proteomics using a dual stage electrodynamic ion funnel interface. Molecular & cellular proteomics: MCP 2011, 10:M000062-MCP000201.
57. Tashima KT, Flanigan TP, Kurpewski J, Melanson SM, Skolnik PR: Discordant Human Immunodeficiency Virus Type 1 drug resistance mutations, including K103N, observed in cerebrospinal fluid and plasma. Clinical infectious diseases: An official publication of the Infectious Diseases Society of America 2002, 35:82-83. (Pubitemid 34666864)
58. Antinori A, Perno CF, Giancola ML, Forbici F, Ippolito G, Hoetelmans RM, Piscitelli SC: Efficacy of cerebrospinal fluid (CSF)-penetrating antiretroviral drugs against HIV in the neurological compartment: different patterns of phenotypic resistance in CSF and plasma. Clinical infectious diseases: An official publication of the Infectious Diseases Society of America 2005, 41:1787-1793. (Pubitemid 41759866)
59. Strain MC, Letendre S, Pillai SK, Russell T, Ignacio CC, Gunthard HF, Good B, Smith DM, Wolinsky SM, Furtado M, et al: Genetic composition of human immunodeficiency virus type 1 in cerebrospinal fluid and blood without treatment and during failing antiretroviral therapy. J Virol 2005, 79:1772-1788. (Pubitemid 40459123)
60. Spudich SS, Huang W, Nilsson AC, Petropoulos CJ, Liegler TJ, Whitcomb JM, Price RW: HIV-1 chemokine coreceptor utilization in paired cerebrospinal fluid and plasma samples: A survey of subjects with viremia. J Infect Dis 2005, 191:890-898. (Pubitemid 40349804)
61. Bergroth T, Ekici H, Gisslen M, Hagberg L, Sonnerborg A: Difference in drug resistance patterns between minor HIV-1 populations in cerebrospinal fluid and plasma. HIV medicine 2009, 10:111-115.
62. Schnell G, Spudich S, Harrington P, Price RW, Swanstrom R: Compartmentalized human immunodeficiency virus type 1 originates from long-lived cells in some subjects with HIV-1-associated dementia. PLoS Pathog 2009, 5:e1000395.
63. Staprans S, Marlowe N, Glidden D, Novakovic-Agopian T, Grant RM, Heyes M, Aweeka F, Deeks S, Price RW: Time course of cerebrospinal fluid responses to antiretroviral therapy: evidence for variable compartmentalization of infection. AIDS 1999, 13:1051-1061. (Pubitemid 29361395)
64. Ellis RJ, Gamst AC, Capparelli E, Spector SA, Hsia K, Wolfson T, Abramson I, Grant I, McCutchan JA: Cerebrospinal fluid HIV RNA originates from both local CNS and systemic sources. Neurology 2000, 54:927-936. (Pubitemid 30111354)
65. Rosengren LE, Karlsson JE, Sjogren M, Blennow K, Wallin A: Neurofilament protein levels in CSF are increased in dementia. Neurology 1999, 52:1090-1093. (Pubitemid 29161631)
66. Norgren N, Sundstrom P, Svenningsson A, Rosengren L, Stigbrand T, Gunnarsson M: Neurofilament and glial fibrillary acidic protein in multiple sclerosis. Neurology 2004, 63:1586-1590. (Pubitemid 39507573)
67. Rosen H, Karlsson JE, Rosengren L: CSF levels of neurofilament is a valuable predictor of long-term outcome after cardiac arrest. J Neurol Sci 2004, 221:19-24. (Pubitemid 38721286)
68. Haghighi S, Andersen O, Oden A, Rosengren L: Cerebrospinal fluid markers in MS patients and their healthy siblings. Acta Neurol Scand 2004, 109:97-99. (Pubitemid 38175047)
69. Petzold A, Thompson EJ, Keir G, Quinn N, Holmberg B, Dizdar N, Wenning GK, Rascol O, Tolosa E, Rosengren L: Longitudinal one-year study of levels and stoichiometry of neurofilament heavy and light chain concentrations in CSF in patients with multiple system atrophy. J Neurol Sci 2009, 279:76-79.
70. Constantinescu R, Holmberg B, Rosengren L, Corneliusson O, Johnels B, Zetterberg H: Light subunit of neurofilament triplet protein in the cerebrospinal fluid after subthalamic nucleus stimulation for Parkinson's disease. Acta Neurol Scand 2010.
71. Constantinescu R, Romer M, Oakes D, Rosengren L, Kieburtz K: Levels of the light subunit of neurofilament triplet protein in cerebrospinal fluid in Huntington's disease. Parkinsonism Relat Disord 2009, 15:245-248.
72. Constantinescu R, Zetterberg H, Holmberg B, Rosengren L: Levels of brain related proteins in cerebrospinal fluid: An aid in the differential diagnosis of parkinsonian disorders. Parkinsonism Relat Disord 2009, 15:205-212.
73. Michaels J, Price RW, Rosenblum MK: Microglia in the giant cell encephalitis of acquired immune deficiency syndrome: proliferation, infection and fusion. Acta neuropathologica 1988, 76:373-379.
74. Dickson DW, Lee SC, Mattiace LA, Yen SH, Brosnan C: Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 1993, 7:75-83.
75. Harroch S, Furtado GC, Brueck W, Rosenbluth J, Lafaille J, Chao M, Buxbaum JD, Schlessinger J: A critical role for the protein tyrosine phosphatase receptor type Z in functional recovery from demyelinating lesions. Nat Genet 2002, 32:411-414. (Pubitemid 35266117)
76. Lin MT, Beal MF: Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795. (Pubitemid 44622683)
77. Kemp K, Gray E, Mallam E, Scolding N, Wilkins A: Inflammatory Cytokine Induced Regulation of Superoxide Dismutase 3 Expression by Human Mesenchymal Stem Cells. Stem Cell Rev 2010.
78. Laspiur JP, Anderson ER, Ciborowski P, Wojna V, Rozek W, Duan F, Mayo R, Rodriguez E, Plaud-Valentin M, Rodriguez-Orengo J, et al: CSF proteomic fingerprints for HIV-associated cognitive impairment. J Neuroimmunol 2007, 192:157-170. (Pubitemid 350213110)
79. Mattsson N, Bremell D, Anckarsater R, Blennow K, Anckarsater H, Zetterberg H, Hagberg L: Neuroinflammation in Lyme neuroborreliosis affects amyloid metabolism. BMC Neurol 2010, 10:51.
80. Diamandis EP, Yousef GM, Petraki C, Soosaipillai AR: Human kallikrein 6 as a biomarker of alzheimer's disease. Clin Biochem 2000, 33:663-667. (Pubitemid 32146202)
81. Boutin JA, Ferry G: Autotaxin. Cellular and molecular life sciences: CMLS 2009, 66:3009-3021.
82. Pendyala G, Trauger SA, Kalisiak E, Ellis RJ, Siuzdak G, Fox HS: Cerebrospinal fluid proteomics reveals potential pathogenic changes in the brains of SIV-infected monkeys. J Proteome Res 2009, 8:2253-2260.
83. Wikoff WR, Pendyala G, Siuzdak G, Fox HS: Metabolomic analysis of the cerebrospinal fluid reveals changes in phospholipase expression in the CNS of SIV-infected macaques. J Clin Invest 2008, 118:2661-2669. (Pubitemid 351949793)
84. Probasco JC, Deeks SG, Lee E, Hoh R, Hunt PW, Liegler T, Price RW, Spudich SS: Cerebrospinal fluid in HIV-1 systemic viral controllers: Absence of HIV-1 RNA and intrathecal inflammation. AIDS 2010, 24:1001-1005.
85. Price RW, Sidtis JJ: Evaluation of the AIDS dementia complex in clinical trials. J Acquir Immune Defic Syndr 1990, 3(Suppl 2):S51-S60.
86. Price RW, Yiannoutsos CT, Clifford DB, Zaborski L, Tselis A, Sidtis JJ, Cohen B, Hall CD, Erice A, Henry K: Neurological outcomes in late HIV infection: Adverse impact of neurological impairment on survival and protective effect of antiviral therapy. AIDS Clinical Trial Group and Neurological AIDS Research Consortium study team. AIDS 1999, 13:1677-1685. (Pubitemid 30015715)
87. Liu T, Qian WJ, Gritsenko MA, Xiao W, Moldawer LL, Kaushal A, Monroe ME, Varnum SM, Moore RJ, Purvine SO, et al: High dynamic range characterization of the trauma patient plasma proteome. Molecular & cellular proteomics: MCP 2006, 5:1899-1913. (Pubitemid 44688198)
88. Livesay EA, Tang K, Taylor BK, Buschbach MA, Hopkins DF, LaMarche BL, Zhao R, Shen Y, Orton DJ, Moore RJ, et al: Fully automated four-column capillary LC-MS system for maximizing throughput in proteomic analyses. Anal Chem 2008, 80:294-302. (Pubitemid 351448434)
89. Mayampurath AM, Jaitly N, Purvine SO, Monroe ME, Auberry KJ, Adkins JN, Smith RD: Decon MSn: A software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra. Bioinformatics 2008, 24:1021-1023. (Pubitemid 351448041)
90. Elias JE, Gygi SP: Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 2007, 4:207-214. (Pubitemid 46358868)
91. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP: Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome. J Proteome Res 2003, 2:43-50. (Pubitemid 36207189)
92. Qian WJ, Liu T, Monroe ME, Strittmatter EF, Jacobs JM, Kangas LJ, Petritis K, Camp DG, Smith RD: Probability-based evaluation of peptide and protein identifications from tandem mass spectrometry and SEQUEST analysis: The human proteome. J Proteome Res 2005, 4:53-62. (Pubitemid 40352578)
93. Monroe ME, Tolic N, Jaitly N, Shaw JL, Adkins JN, Smith RD: VIPER: An advanced software package to support highthroughput LC-MS peptide identification. Bioinformatics 2007, 23:2021-2023. (Pubitemid 47299846)
94. Nesvizhskii AI, Keller A, Kolker E, Aebersold R: A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003, 75:4646-4658. (Pubitemid 37082259)
95. Polpitiya AD, Qian WJ, Jaitly N, Petyuk VA, Adkins JN, Camp DG, Anderson GA, Smith RD: DAnTE: A statistical tool for quantitative analysis of -omics data. Bioinformatics 2008, 24:1556-1558. (Pubitemid 351911716)