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Searching for reliable premortem protein biomarkers for prion diseases: progress and challenges to date

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Pages 267-280 | Published online: 09 Jan 2014

References

  • Gajdusek DC. Unconventional viruses and the origin and disappearance of kuru. Science 197(4307), 943–960 (1977).
  • Pan KM, Baldwin M, Nguyen J et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA 90(23), 10962–10966 (1993).
  • Aguzzi A, Polymenidou M. Mammalian prion biology: one century of evolving concepts. Cell 116(2), 313–327 (2004).
  • Chesebro B, Race R, Wehrly K et al. Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain. Nature 315(6017), 331–333 (1985).
  • Oesch B, Westaway D, Walchli M et al. A cellular gene encodes scrapie PrP 27–30 protein. Cell 40(4), 735–746 (1985).
  • Hsiao K, Baker HF, Crow TJ et al. Linkage of a prion protein missense variant to Gerstmann–Sträussler syndrome. Nature 338(6213), 342–345 (1989).
  • Goldfarb LG, Brown P, Little BW et al. A new (two-repeat) octapeptide coding insert mutation in Creutzfeldt–Jakob disease. Neurology 43(11), 2392–2394 (1993).
  • Mead S. Prion disease genetics. Eur. J. Hum. Genet. 14(3), 273–281 (2006).
  • Kovács GG, Trabattoni G, Hainfellner JA, Ironside JW, Knight RS, Budka H. Mutations of the prion protein gene phenotypic spectrum. J. Neurol. 249(11), 1567–1582 (2002).
  • Collinge J. Molecular neurology of prion disease. J. Neurol. Neurosurg. Psychiatr. 76(7), 906–919 (2005).
  • Kawasaki Y, Kawagoe K, Chen CJ, Teruya K, Sakasegawa Y, Doh-ura K. Orally administered amyloidophilic compound is effective in prolonging the incubation periods of animals cerebrally infected with prion diseases in a prion strain-dependent manner. J. Virol. 81(23), 12889–12898 (2007).
  • Webb S, Lekishvili T, Loeschner C et al. Mechanistic insights into the cure of prion disease by novel antiprion compounds. J Virol. 81(19), 10729–10741 (2007).
  • Hill AF, Desbruslais M, Joiner S et al. The same prion strain causes vCJD and BSE. Nature 389(6650), 448–450, 526 (1997).
  • Will RG, Ironside JW, Zeidler M et al. A new variant of Creutzfeldt–Jakob disease in the UK. Lancet 347(9006), 921–925 (1996).
  • Brown P, Brandel JP, Preece M, Preese M, Sato T. Iatrogenic Creutzfeldt–Jakob disease: the waning of an era. Neurology 67(3), 389–393 (2006).
  • Llewelyn CA, Hewitt PE, Knight RS et al. Possible transmission of variant Creutzfeldt–Jakob disease by blood transfusion. Lancet 363(9407), 417–421 (2004).
  • Bishop MT, Hart P, Aitchison L et al. Predicting susceptibility and incubation time of human-to-human transmission of vCJD. Lancet Neurol. 5(5), 393–398 (2006).
  • Fraser H. The pathology of a natural and experimental scrapie. Front. Biol. 44, 267–305 (1976).
  • Oesch B, Doherr M, Heim D et al. Application of Prionics Western blotting procedure to screen for BSE in cattle regularly slaughtered at Swiss abattoirs. Arch. Virol. Suppl. (16), 189–195 (2000).
  • Schaller O, Fatzer R, Stack M et al. Validation of a Western immunoblotting procedure for bovine PrP(Sc) detection and its use as a rapid surveillance method for the diagnosis of bovine spongiform encephalopathy (BSE). Acta Neuropathol. 98(5), 437–443 (1999).
  • Grassi J, Créminon C, Frobert Y et al. Specific determination of the proteinase K-resistant form of the prion protein using two-site immunometric assays. Application to the post-mortem diagnosis of BSE. Arch. Virol. Suppl. 16, 197–205 (2000).
  • Onisko B, Dynin I, Requena JR, Silva CJ, Erickson M, Carter JM. Mass spectrometric detection of attomole amounts of the prion protein by nanoLC/MS/MS. J. Am. Soc. Mass Spectrom. 18(6), 1070–1079 (2007).
  • Onisko BC, Silva CJ, Dynin I et al. Sensitive, preclinical detection of prions in brain by nanospray liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 21(24), 4023–4026 (2007).
  • Silva CJ, Onisko BC, Dynin I, Erickson ML, Requena JR, Carter JM. Utility of mass spectrometry in the diagnosis of prion diseases. Anal Chem 83, 1609–1615 (2011).
  • Ugnon-Café S, Dorey A, Bilheude JM et al. Rapid screening and confirmatory methods for biochemical diagnosis of human prion disease. J. Virol. Methods 175(2), 216–223 (2011).
  • Edgeworth JA, Farmer M, Sicilia A et al. Detection of prion infection in variant Creutzfeldt–Jakob disease: a blood-based assay. Lancet 377(9764), 487–493 (2011).
  • Edgeworth JA, Jackson GS, Clarke AR, Weissmann C, Collinge J. Highly sensitive, quantitative cell-based assay for prions adsorbed to solid surfaces. Proc. Natl Acad. Sci. USA 106(9), 3479–3483 (2009).
  • Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411(6839), 810–813 (2001).
  • Orrú CD, Caughey B. Prion seeded conversion and amplification assays. Top. Curr. Chem. 305, 121–133 (2011).
  • Haley NJ, Mathiason CK, Carver S, Telling GC, Zabel MD, Hoover EA. Sensitivity of protein misfolding cyclic amplification versus immunohistochemistry in ante-mortem detection of chronic wasting disease. J. Gen. Virol. 93(Pt 5), 1141–1150 (2012).
  • Marouga R, David S, Hawkins E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382(3), 669–678 (2005).
  • Bischoff R, Luider TM. Methodological advances in the discovery of protein and peptide disease markers. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 803(1), 27–40 (2004).
  • Tang N, Tornatore P, Weinberger SR. Current developments in SELDI affinity technology. Mass Spectrom. Rev. 23(1), 34–44 (2004).
  • Wolters DA, Washburn MP, Yates JR 3rd. An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 73(23), 5683–5690 (2001).
  • Wilm M, Shevchenko A, Houthaeve T et al. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379(6564), 466–469 (1996).
  • Schirle M, Heurtier MA, Kuster B. Profiling core proteomes of human cell lines by one-dimensional PAGE and liquid chromatography-tandem mass spectrometry. Mol. Cell Proteomics 2(12), 1297–1305 (2003).
  • Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17(10), 994–999 (1999).
  • Haqqani AS, Kelly JF, Stanimirovic DB. Quantitative protein profiling by mass spectrometry using isotope-coded affinity tags. Methods Mol. Biol. 439, 225–240 (2008).
  • Aggarwal K, Choe LH, Lee KH. Shotgun proteomics using the iTRAQ isobaric tags. Brief. Funct. Genomic. Proteomic. 5(2), 112–120 (2006).
  • D’Ascenzo M, Choe L, Lee KH. iTRAQPak: an R based analysis and visualization package for 8-plex isobaric protein expression data. Brief. Funct. Genomic. Proteomic. 7(2), 127–135 (2008).
  • Dayon L, Hainard A, Licker V et al. Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags. Anal. Chem. 80(8), 2921–2931 (2008).
  • Pendyala G, Trauger SA, Siuzdak G, Fox HS. 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(1), 352–358 (2010).
  • Hsich G, Kenney K, Gibbs CJ, Lee KH, Harrington MG. The 14-3-3 brain protein in cerebrospinal fluid as a marker for transmissible spongiform encephalopathies. N. Engl. J. Med. 335(13), 924–930 (1996).
  • Jesse S, Steinacker P, Cepek L et al. Glial fibrillary acidic protein and protein S-100B: different concentration pattern of glial proteins in cerebrospinal fluid of patients with Alzheimer’s disease and Creutzfeldt–Jakob disease. J. Alzheimers Dis. 17(3), 541–551 (2009).
  • Otto M, Wiltfang J, Cepek L et al. Tau protein and 14-3-3 protein in the differential diagnosis of Creutzfeldt–Jakob disease. Neurology 58(2), 192–197 (2002).
  • Sanchez-Juan P, Green A, Ladogana A et al. CSF tests in the differential diagnosis of Creutzfeldt–Jakob disease. Neurology 67(4), 637–643 (2006).
  • World Health Organization. Global surveillance, diagnosis and therapy of human transmissible spongiform encephalopathies: report from a WHO consultation. World Health Organization, Geneva, Switzerland (1998).
  • Saiz A, Graus F, Dalmau J, Pifarré A, Marin C, Tolosa E. Detection of 14-3-3 brain protein in the cerebrospinal fluid of patients with paraneoplastic neurological disorders. Ann. Neurol. 46(5), 774–777 (1999).
  • Bartosik-Psujek H, Archelos JJ. Tau protein and 14-3-3 are elevated in the cerebrospinal fluid of patients with multiple sclerosis and correlate with intrathecal synthesis of IgG. J. Neurol. 251(4), 414–420 (2004).
  • Piubelli C, Fiorini M, Zanusso G et al. Searching for markers of Creutzfeldt–Jakob disease in cerebrospinal fluid by two-dimensional mapping. Proteomics 6(Suppl. 1), S256–S261 (2006).
  • Brechlin P, Jahn O, Steinacker P et al. Cerebrospinal fluid-optimized two-dimensional difference gel electrophoresis (2-D DIGE) facilitates the differential diagnosis of Creutzfeldt–Jakob disease. Proteomics 8(20), 4357–4366 (2008).
  • Sanchez JC, Guillaume E, Lescuyer P et al. Cystatin C as a potential cerebrospinal fluid marker for the diagnosis of Creutzfeldt–Jakob disease. Proteomics 4(8), 2229–2233 (2004).
  • Qualtieri A, Urso E, Le Pera M et al. Thymosin β4 is differentially expressed in the cerebrospinal fluid of Creutzfeldt–Jakob disease patients: a MALDI-TOF MS protein profiling study. Proteomics Clin. Appl. 3, 574–583 (2009).
  • Herbst A, McIlwain S, Schmidt JJ, Aiken JM, Page CD, Li L. Prion disease diagnosis by proteomic profiling. J. Proteome Res. 8(2), 1030–1036 (2009).
  • Qualtieri A, Urso E, Le Pera M et al. Proteomic profiling of cerebrospinal fluid in Creutzfeldt–Jakob disease. Expert Rev. Proteomics 7(6), 907–917 (2010).
  • Guillaume E, Zimmermann C, Burkhard PR, Hochstrasser DF, Sanchez JC. A potential cerebrospinal fluid and plasmatic marker for the diagnosis of Creutzfeldt–Jakob disease. Proteomics 3(8), 1495–1499 (2003).
  • Matsui Y, Satoh K, Mutsukura K et al. Development of an ultra-rapid diagnostic method based on heart-type fatty acid binding protein levels in the CSF of CJD patients. Cell. Mol. Neurobiol. 30(7), 991–999 (2010).
  • Lee HP, Jun YC, Choi JK, Kim JI, Carp RI, Kim YS. Activation of mitogen-activated protein kinases in hamster brains infected with 263K scrapie agent. J. Neurochem. 95(2), 584–593 (2005).
  • Steinacker P, Klafki H, Lehnert S et al. ERK2 is increased in cerebrospinal fluid of Creutzfeldt–Jakob disease patients. J. Alzheimers Dis. 22(1), 119–128 (2010).
  • Singh A, Beveridge AJ, Singh N. Decreased CSF transferrin in sCJD: a potential pre-mortem diagnostic test for prion disorders. PLoS ONE 6(3), e16804 (2011).
  • Reiber H. Proteins in cerebrospinal fluid and blood: barriers, CSF flow rate and source-related dynamics. Restor Neurol Neurosci. 21(3–4), 79–96 (2003).
  • Hunter N, Foster J, Chong A et al. Transmission of prion diseases by blood transfusion. J. Gen. Virol. 83(Pt 11), 2897–2905 (2002).
  • Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol. Cell Proteomics 1(11), 845–867 (2002).
  • Björhall K, Miliotis T, Davidsson P. Comparison of different depletion strategies for improved resolution in proteomic analysis of human serum samples. Proteomics 5(1), 307–317 (2005).
  • Wei X, Herbst A, Ma D, Aiken J, Li L. A quantitative proteomic approach to prion disease biomarker research: delving into the glycoproteome. J. Proteome Res. 10(6), 2687–2702 (2011).
  • Roche S, Tiers L, Provansal M, Piva MT, Lehmann S. Interest of major serum protein removal for Surface-Enhanced Laser Desorption/Ionization–Time Of Flight (SELDI-TOF) proteomic blood profiling. Proteome Sci. 4, 20 (2006).
  • Sihlbom C, Kanmert I, Bahr H, Davidsson P. Evaluation of the combination of bead technology with SELDI-TOF-MS and 2-D DIGE for detection of plasma proteins. J. Proteome Res. 7(9), 4191–4198 (2008).
  • Batxelli-Molina I, Salvetat N, Andréoletti O et al. Ovine serum biomarkers of early and late phase scrapie. BMC Vet. Res. 6, 49 (2010).
  • Kariv-Inbal Z, Ben-Hur T, Grigoriadis NC, Engelstein R, Gabizon R. Urine from scrapie-infected hamsters comprises low levels of prion infectivity. Neurodegener. Dis. 3(3), 123–128 (2006).
  • Gregori L, Kovacs GG, Alexeeva I, Budka H, Rohwer RG. Excretion of transmissible spongiform encephalopathy infectivity in urine. Emerging Infect. Dis. 14(9), 1406–1412 (2008).
  • Murayama Y, Yoshioka M, Okada H, Takata M, Yokoyama T, Mohri S. Urinary excretion and blood level of prions in scrapie-infected hamsters. J. Gen. Virol. 88(Pt 10), 2890–2898 (2007).
  • Rubenstein R, Chang B, Gray P et al. Prion disease detection, PMCA kinetics, and IgG in urine from sheep naturally/experimentally infected with scrapie and deer with preclinical/clinical chronic wasting disease. J. Virol. 85(17), 9031–9038 (2011).
  • Kuwabara Y, Mine K, Katayama A, Inagawa T, Akira S, Takeshita T. Proteomic analyses of recombinant human follicle-stimulating hormone and urinary-derived gonadotropin preparations. J. Reprod. Med. 54(8), 459–466 (2009).
  • Van Dorsselaer A, Carapito C, Delalande F et al. Detection of prion protein in urine-derived injectable fertility products by a targeted proteomic approach. PLoS ONE 6(3), e17815 (2011).
  • Simon SL, Lamoureux L, Plews M et al. The identification of disease-induced biomarkers in the urine of BSE infected cattle. Proteome Sci. 6, 23 (2008).
  • Serban A, Legname G, Hansen K, Kovaleva N, Prusiner SB. Immunoglobulins in urine of hamsters with scrapie. J. Biol. Chem. 279(47), 48817–48820 (2004).
  • Sasaki K, Doh-ura K, Ironside JW, Iwaki T. Increased clusterin (apolipoprotein J) expression in human and mouse brains infected with transmissible spongiform encephalopathies. Acta Neuropathol. 103(3), 199–208 (2002).
  • Lamoureux L, Simon SL, Plews M et al. Analysis of clusterin glycoforms in the urine of BSE-infected Fleckvieh-Simmental cows. J. Toxicol. Environ. Health Part A 74(2-4), 138–145 (2011).
  • Plews M, Lamoureux L, Simon SL et al. Factors affecting the accuracy of urine-based biomarkers of BSE. Proteome Sci. 9(1), 6 (2011).
  • Wang J, Tung YC, Wang Y, Li XT, Iqbal K, Grundke-Iqbal I. Hyperphosphorylation and accumulation of neurofilament proteins in Alzheimer disease brain and in okadaic acid-treated SY5Y cells. FEBS Lett. 507(1), 81–87 (2001).
  • Liu F, Iqbal K, Grundke-Iqbal I, Hart GW, Gong CX. O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer’s disease. Proc. Natl Acad. Sci. USA 101(29), 10804–10809 (2004).
  • Keller JN, Hanni KB, Markesbery WR. Impaired proteasome function in Alzheimer’s disease. J. Neurochem. 75(1), 436–439 (2000).
  • Wei X, Li L. Comparative glycoproteomics: approaches and applications. Brief. Funct. Genomic. Proteomic. 8(2), 104–113 (2009).
  • Wei X, Li L. Mass spectrometry-based proteomics and peptidomics for biomarker discovery in neurodegenerative diseases. Int. J. Clin. Exp. Pathol. 2(2), 132–148 (2009).
  • Sáez-Valero J, Fodero LR, Sjögren M et al. Glycosylation of acetylcholinesterase and butyrylcholinesterase changes as a function of the duration of Alzheimer’s disease. J. Neurosci. Res. 72(4), 520–526 (2003).
  • Silveyra MX, Cuadrado-Corrales N, Marcos A et al. Altered glycosylation of acetylcholinesterase in Creutzfeldt–Jakob disease. J. Neurochem. 96(1), 97–104 (2006).
  • Rudd PM, Endo T, Colominas C et al. Glycosylation differences between the normal and pathogenic prion protein isoforms. Proc. Natl Acad. Sci. USA 96(23), 13044–13049 (1999).
  • Botella-López A, Burgaya F, Gavín R et al. Reelin expression and glycosylation patterns are altered in Alzheimer’s disease. Proc. Natl Acad. Sci. USA 103(14), 5573–5578 (2006).
  • Puchades M, Hansson SF, Nilsson CL, Andreasen N, Blennow K, Davidsson P. Proteomic studies of potential cerebrospinal fluid protein markers for Alzheimer’s disease. Brain Res. Mol. Brain Res. 118(1-2), 140–146 (2003).
  • Sihlbom C, Davidsson P, Nilsson CL. Prefractionation of cerebrospinal fluid to enhance glycoprotein concentration prior to structural determination with FT-ICR mass spectrometry. J. Proteome Res. 4(6), 2294–2301 (2005).
  • Zhang H, Li XJ, Martin DB, Aebersold R. Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 21(6), 660–666 (2003).
  • Mao X, Luo Y, Dai Z, Wang K, Du Y, Lin B. Integrated lectin affinity microfluidic chip for glycoform separation. Anal. Chem. 76(23), 6941–6947 (2004).
  • Xiong L, Andrews D, Regnier F. Comparative proteomics of glycoproteins based on lectin selection and isotope coding. J. Proteome Res. 2(6), 618–625 (2003).
  • Goldstein IJ, Hollerman CE, Smith EE. Protein–carbohydrate Interaction. II. Inhibition studies on the interaction of concanavalin A with polysaccharides. Biochemistry 4, 876–883 (1965).
  • Kamra A, Gupta MN. Crosslinked concanavalin A-O-(diethylaminoethyl)-cellulose–an affinity medium for concanavalin A-interacting glycoproteins. Anal. Biochem. 164(2), 405–410 (1987).
  • Nagata Y, Burger MM. Wheat germ agglutinin. Molecular characteristics and specificity for sugar binding. J. Biol. Chem. 249(10), 3116–3122 (1974).
  • Wang Y, Wu SL, Hancock WS. Approaches to the study of N-linked glycoproteins in human plasma using lectin affinity chromatography and nano-HPLC coupled to electrospray linear ion trap–Fourier transform mass spectrometry. Glycobiology 16(6), 514–523 (2006).
  • Yang Z, Hancock WS. Approach to the comprehensive analysis of glycoproteins isolated from human serum using a multi-lectin affinity column. J. Chromatogr. A 1053(1–2), 79–88 (2004).
  • Yang Z, Hancock WS, Chew TR, Bonilla L. A study of glycoproteins in human serum and plasma reference standards (HUPO) using multilectin affinity chromatography coupled with RPLC-MS/MS. Proteomics 5(13), 3353–3366 (2005).
  • Bernhard OK, Kapp EA, Simpson RJ. Enhanced analysis of the mouse plasma proteome using cysteine-containing tryptic glycopeptides. J. Proteome Res. 6(3), 987–995 (2007).
  • Mole JE, Beaulieu BL, Geheran CA, Carnazza JA, Anderson JK. Isolation and analysis of murine serum amyloid P component cDNA clones. J. Immunol. 141(10), 3642–3646 (1988).
  • Kalaria RN, Golde TE, Cohen ML, Younkin SG. Serum amyloid P in Alzheimer’s disease. Implications for dysfunction of the blood-brain barrier. Ann. NY Acad. Sci. 640, 145–148 (1991).
  • Akiyama H, Yamada T, Kawamata T, McGeer PL. Association of amyloid P component with complement proteins in neurologically diseased brain tissue. Brain Res. 548(1–2), 349–352 (1991).
  • Coria F, Castaño E, Prelli F et al. Isolation and characterization of amyloid P component from Alzheimer’s disease and other types of cerebral amyloidosis. Lab. Invest. 58(4), 454–458 (1988).
  • Addona TA, Abbatiello SE, Schilling B et al. Multi-site assessment of the precision and reproducibility of multiple reaction monitoring-based measurements of proteins in plasma. Nat. Biotechnol. 27(7), 633–641 (2009).
  • Kim K, Kim SJ, Yu HG et al. Verification of biomarkers for diabetic retinopathy by multiple reaction monitoring. J. Proteome Res. 9(2), 689–699 (2010).
  • Kuhn E, Wu J, Karl J, Liao H, Zolg W, Guild B. Quantification of C-reactive protein in the serum of patients with rheumatoid arthritis using multiple reaction monitoring mass spectrometry and 13C-labeled peptide standards. Proteomics 4(4), 1175–1186 (2004).
  • Kuzyk MA, Smith D, Yang J et al. Multiple reaction monitoring-based, multiplexed, absolute quantitation of 45 proteins in human plasma. Mol. Cell Proteomics 8(8), 1860–1877 (2009).
  • Anderson NL, Anderson NG, Haines LR, Hardie DB, Olafson RW, Pearson TW. Mass spectrometric quantitation of peptides and proteins using Stable Isotope Standards and Capture by Anti-Peptide Antibodies (SISCAPA). J. Proteome Res. 3(2), 235–244 (2004).
  • Satoh J, Onoue H, Arima K, Yamamura T. The 14-3-3 protein forms a molecular complex with heat shock protein Hsp60 and cellular prion protein. J. Neuropathol. Exp. Neurol. 64(10), 858–868 (2005).
  • Hayes SA, Dice JF. Roles of molecular chaperones in protein degradation. J. Cell Biol. 132(3), 255–258 (1996).
  • Booth S, Bowman C, Baumgartner R et al. Molecular classification of scrapie strains in mice using gene expression profiling. Biochem. Biophys. Res. Commun. 325(4), 1339–1345 (2004).
  • Diedrich JF, Carp RI, Haase AT. Increased expression of heat shock protein, transferrin, and 2-microglobulin in astrocytes during scrapie. Microb. Pathog. 15(1), 1–6 (1993).
  • Kenward N, Hope J, Landon M, Mayer RJ. Expression of polyubiquitin and heat-shock protein 70 genes increases in the later stages of disease progression in scrapie-infected mouse brain. J. Neurochem. 62(5), 1870–1877 (1994).
  • Tatzelt J, Voellmy R, Welch WJ. Abnormalities in stress proteins in prion diseases. Cell. Mol. Neurobiol. 18(6), 721–729 (1998).
  • Zafar S, von Ahsen N, Oellerich M et al. Proteomics approach to identify the interacting partners of cellular prion protein and characterization of Rab7a interaction in neuronal cells. J. Proteome Res. 10(7), 3123–3135 (2011).
  • Hwang D, Lee IY, Yoo H et al. A systems approach to prion disease. Mol. Syst. Biol. 5, 252 (2009).
  • Kim Y, Kim TK, Kim Y et al. Principal network analysis: identification of subnetworks representing major dynamics using gene expression data. Bioinformatics 27(3), 391–398 (2011).
  • Harrington MG, Merril CR, Asher DM, Gajdusek DC. Abnormal proteins in the cerebrospinal fluid of patients with Creutzfeldt–Jakob disease. N. Engl. J. Med. 315(5), 279–283 (1986).
  • Choe LH, Green A, Knight RS, Thompson EJ, Lee KH. Apolipoprotein E and other cerebrospinal fluid proteins differentiate ante mortem variant Creutzfeldt–Jakob disease from ante mortem sporadic Creutzfeldt–Jakob disease. Electrophoresis 23(14), 2242–2246 (2002).
  • Steinacker P, Rist W, Swiatek-de-Lange M et al. Ubiquitin as potential cerebrospinal fluid marker of Creutzfeldt–Jakob disease. Proteomics 10(1), 81–89 (2010).

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