1887

Abstract

Development of numerous advanced techniques in recent years have allowed detection of the pathological prion protein (PrP), the unique marker of transmissible spongiform encephalopathies (TSEs, or prion diseases), in the blood of animals and humans; however, an ante mortem screening test that can be used for the routine diagnosis of human prion diseases remains unavailable. A critical, analytical review of all the diagnostic assays developed to date will allow an evaluation of progress in this field and may facilitate the identification of the possible reasons for this delay. Thus, in this review, I provide a detailed overview of the techniques currently available for detecting PrP and other markers of the disease in blood, as well as an analysis of the significance, feasibility, reliability and application spectrum for these methods. I highlight that factors intrinsic and extrinsic to blood may interfere with the detection of PrP/prions, and that this is not yet taken into account in current tests. This may inspire researchers in this field to not only aspire to increase test sensitivity, but also to adopt other strategies in order to identify and overcome the limitations that hamper the development of a successful routine blood test for prion diseases.

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2015-03-01
2019-12-06
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References

  1. Abdel-Haq H.. ( 2012;). Recent developments in cell biology: role of glycosylation in prion diseases. . In Prions and Prion Diseases: New Developments, pp. 85–114. Edited by Verdier J.-M... New York:: Nova Science;. https://www.novapublishers.com/catalog/product_info.php?products_id=43852.
    [Google Scholar]
  2. Abdel-Haq H., Lu M., Cardone F., Liu Q. G., Puopolo M., Pocchiari M.. ( 2009;). Efficacy of phthalocyanine tetrasulfonate against mouse-adapted human prion strains. . Arch Virol 154:, 1005–1007. [CrossRef][PubMed]
    [Google Scholar]
  3. Amorfix Life Sciences Press Release ( 2008;). Amorfix vCJD assay achieves 100 % sensitivity and 100 % specificity on 1,000 fresh samples from UK blood donors. . http://www.amorfix.com/pdf_press/pr_2008/2008_10_17_AMF_vCJD_NIBSC_Fresh_Results.pdf.
  4. An S. S. A., Lim K. T., Oh H. J., Lee B. S., Zukic E., Ju Y. R., Yokoyama T., Kim S. Y., Welker E.. ( 2010;). Differentiating blood samples from scrapie infected and non-infected hamsters by detecting disease-associated prion proteins using Multimer Detection System. . Biochem Biophys Res Commun 392:, 505–509. [CrossRef][PubMed]
    [Google Scholar]
  5. Atarashi R., Wilham J. M., Christensen L., Hughson A. G., Moore R. A., Johnson L. M., Onwubiko H. A., Priola S. A., Caughey B.. ( 2008;). Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. . Nat Methods 5:, 211–212. [CrossRef][PubMed]
    [Google Scholar]
  6. Atarashi R., Satoh K., Sano K., Fuse T., Yamaguchi N., Ishibashi D., Matsubara T., Nakagaki T., Yamanaka H.. & other authors ( 2011;). Ultrasensitive human prion detection in cerebrospinal fluid by real-time quaking-induced conversion. . Nat Med 17:, 175–178. [CrossRef][PubMed]
    [Google Scholar]
  7. Bannach O., Birkmann E., Reinartz E., Jaeger K. E., Langeveld J. P., Rohwer R. G., Gregori L., Terry L. A., Willbold D., Riesner D.. ( 2012;). Detection of prion protein particles in blood plasma of scrapie infected sheep. . PLoS ONE 7:, e36620. [CrossRef][PubMed]
    [Google Scholar]
  8. Bannach O., Reinartz E., Henke F., Dreßen F., Oelschlegel A., Kaatz M., Groschup M. H., Willbold D., Riesner D., Birkmann E.. ( 2013;). Analysis of prion protein aggregates in blood and brain from pre-clinical and clinical BSE cases. . Vet Microbiol 166:, 102–108. [CrossRef][PubMed]
    [Google Scholar]
  9. Batxelli-Molina I., Salvetat N., Andréoletti O., Guerrier L., Vicat G., Molina F., Mourton-Gilles C.. ( 2010;). Ovine serum biomarkers of early and late phase scrapie. . BMC Vet Res 6:, 49. [CrossRef][PubMed]
    [Google Scholar]
  10. Bessen R. A., Marsh R. F.. ( 1994;). Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. . J Virol 68:, 7859–7868.[PubMed]
    [Google Scholar]
  11. Biasini E., Seegulam M. E., Patti B. N., Solforosi L., Medrano A. Z., Christensen H. M., Senatore A., Chiesa R., Williamson R. A., Harris D. A.. ( 2008;). Non-infectious aggregates of the prion protein react with several PrPSc-directed antibodies. . J Neurochem 105:, 2190–2204. [CrossRef][PubMed]
    [Google Scholar]
  12. Biasini E., Tapella L., Mantovani S., Stravalaci M., Gobbi M., Harris D. A., Chiesa R.. ( 2009;). Immunopurification of pathological prion protein aggregates. . PLoS ONE 4:, e7816. [CrossRef][PubMed]
    [Google Scholar]
  13. Bolton D. C., McKinley M. P., Prusiner S. B.. ( 1982;). Identification of a protein that purifies with the scrapie prion. . Science 218:, 1309–1311. [CrossRef][PubMed]
    [Google Scholar]
  14. Brown P.. ( 2001b;). Creutzfeldt-Jakob disease: blood infectivity and screening tests. . Semin Hematol 38: (Suppl 9), 2–6. [CrossRef][PubMed]
    [Google Scholar]
  15. Brown P., Rohwer R. G., Dunstan B. C., MacAuley C., Gajdusek D. C., Drohan W. N.. ( 1998;). The distribution of infectivity in blood components and plasma derivatives in experimental models of transmissible spongiform encephalopathy. . Transfusion 38:, 810–816. [CrossRef][PubMed]
    [Google Scholar]
  16. Brown P., Cervenáková L., Diringer H.. ( 2001a;). Blood infectivity and the prospects for a diagnostic screening test in Creutzfeldt-Jakob disease. . J Lab Clin Med 137:, 5–13. [CrossRef][PubMed]
    [Google Scholar]
  17. Castilla J., Saá P., Soto C.. ( 2005;). Detection of prions in blood. . Nat Med 11:, 982–985.[PubMed]
    [Google Scholar]
  18. Caughey B. W., Dong A., Bhat K. S., Ernst D., Hayes S. F., Caughey W. S.. ( 1991;). Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. . Biochemistry 30:, 7672–7680. [CrossRef][PubMed]
    [Google Scholar]
  19. Cervenakova L., Yakovleva O., McKenzie C., Kolchinsky S., McShane L., Drohan W. N., Brown P.. ( 2003;). Similar levels of infectivity in the blood of mice infected with human-derived vCJD and GSS strains of transmissible spongiform encephalopathy. . Transfusion 43:, 1687–1694. [CrossRef][PubMed]
    [Google Scholar]
  20. Chang B., Cheng X., Yin S., Pan T., Zhang H., Wong P., Kang S. C., Xiao F., Yan H.. & other authors ( 2007;). Test for detection of disease-associated prion aggregate in the blood of infected but asymptomatic animals. . Clin Vaccine Immunol 14:, 36–43. [CrossRef][PubMed]
    [Google Scholar]
  21. Choe L. H., Green A., Knight R. S., Thompson E. J., Lee K. H.. ( 2002;). Apolipoprotein E and other cerebrospinal fluid proteins differentiate ante mortem variant Creutzfeldt-Jakob disease from ante mortem sporadic Creutzfeldt-Jakob disease. . Electrophoresis 23:, 2242–2246. [CrossRef][PubMed]
    [Google Scholar]
  22. Chohan G., Llewelyn C., Mackenzie J., Cousens S., Kennedy A., Will R., Hewitt P.. ( 2010;). Variant Creutzfeldt-Jakob disease in a transfusion recipient: coincidence or cause?. Transfusion 50:, 1003–1006. [CrossRef][PubMed]
    [Google Scholar]
  23. Chung E., Prelli F., Dealler S., Lee W. S., Chang Y. T., Wisniewski T.. ( 2011;). Styryl-based and tricyclic compounds as potential anti-prion agents. . PLoS ONE 6:, e24844. [CrossRef][PubMed]
    [Google Scholar]
  24. Collinge J., Whitfield J., McKintosh E., Beck J., Mead S., Thomas D. J., Alpers M. P.. ( 2006;). Kuru in the 21st century–an acquired human prion disease with very long incubation periods. . Lancet 367:, 2068–2074. [CrossRef][PubMed]
    [Google Scholar]
  25. Debray H., Decout D., Strecker G., Spik G., Montreuil J.. ( 1981;). Specificity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. . Eur J Biochem 117:, 41–55. [CrossRef][PubMed]
    [Google Scholar]
  26. Diedrich J. F., Minnigan H., Carp R. I., Whitaker J. N., Race R., Frey W. II, Haase A. T.. ( 1991;). Neuropathological changes in scrapie and Alzheimer’s disease are associated with increased expression of apolipoprotein E and cathepsin D in astrocytes. . J Virol 65:, 4759–4768.[PubMed]
    [Google Scholar]
  27. Doh-ura K., Ishikawa K., Murakami-Kubo I., Sasaki K., Mohri S., Race R., Iwaki T.. ( 2004;). Treatment of transmissible spongiform encephalopathy by intraventricular drug infusion in animal models. . J Virol 78:, 4999–5006. [CrossRef][PubMed]
    [Google Scholar]
  28. Edgeworth J. A., Farmer M., Sicilia A., Tavares P., Beck J., Campbell T., Lowe J., Mead S., Rudge P.. & other authors ( 2011;). Detection of prion infection in variant Creutzfeldt-Jakob disease: a blood-based assay. . Lancet 377:, 487–493. [CrossRef][PubMed]
    [Google Scholar]
  29. Edwards J. C., Moore S. J., Hawthorn J. A., Neale M. H., Terry L. A.. ( 2010;). PrP(Sc) is associated with B cells in the blood of scrapie-infected sheep. . Virology 405:, 110–119. [CrossRef][PubMed]
    [Google Scholar]
  30. Elder A. M., Henderson D. M., Nalls A. V., Wilham J. M., Caughey B. W., Hoover E. A., Kincaid A. E., Bartz J. C., Mathiason C. K.. ( 2013;). In vitro detection of prionemia in TSE-infected cervids and hamsters. . PLoS ONE 8:, e80203. [CrossRef][PubMed]
    [Google Scholar]
  31. Ernoult E., Bourreau A., Gamelin E., Guette C.. ( 2010;). A proteomic approach for plasma biomarker discovery with iTRAQ labelling and OFFGEL fractionation. . J Biomed Biotechnol 2010:, 927917. [CrossRef][PubMed]
    [Google Scholar]
  32. European Commission DG Health and Consumer Directorate ( 2012;). Guideline for the CE marking of blood based in vitro diagnostic medical devices for vCJD based on detection of abnormal PrP. . http://ec.europa.eu/health/medical-devices/files/meddev/2_14_4_ol_en.pdf.
  33. Forloni G., Iussich S., Awan T., Colombo L., Angeretti N., Girola L., Bertani I., Poli G., Caramelli M.. & other authors ( 2002;). Tetracyclines affect prion infectivity. . Proc Natl Acad Sci U S A 99:, 10849–10854. [CrossRef][PubMed]
    [Google Scholar]
  34. Gabizon R. M., McKinley M. P., Prusiner S. B.. ( 1987;). Purified prion proteins and scrapie infectivity copartition into liposomes. . Proc Natl Acad Sci U S A 84:, 4017–4021. [CrossRef][PubMed]
    [Google Scholar]
  35. Gasset M., Baldwin M. A., Fletterick R. J., Prusiner S. B.. ( 1993;). Perturbation of the secondary structure of the scrapie prion protein under conditions that alter infectivity. . Proc Natl Acad Sci U S A 90:, 1–5. [CrossRef][PubMed]
    [Google Scholar]
  36. Gregori L., McCombie N., Palmer D., Birch P., Sowemimo-Coker S. O., Giulivi A., Rohwer R. G.. ( 2004;). Effectiveness of leucoreduction for removal of infectivity of transmissible spongiform encephalopathies from blood. . Lancet 364:, 529–531. [CrossRef][PubMed]
    [Google Scholar]
  37. Guillaume E., Zimmermann C., Burkhard P. R., Hochstrasser D. F., Sanchez J. C.. ( 2003;). A potential cerebrospinal fluid and plasmatic marker for the diagnosis of Creutzfeldt-Jakob disease. . Proteomics 3:, 1495–1499. [CrossRef][PubMed]
    [Google Scholar]
  38. Guntz P., Walter C., Schosseler P., Morel P., Coste J., Cazenave J.-P.. ( 2010;). Feasibility study of a screening assay that identifies the abnormal prion protein PrPTSE in plasma: initial results with 20 000 samples. . Transfusion 50:, 989–995. [CrossRef][PubMed]
    [Google Scholar]
  39. Herzog C., Salès N., Etchegaray N., Charbonnier A., Freire S., Dormont D., Deslys J. P., Lasmézas C. I.. ( 2004;). Tissue distribution of bovine spongiform encephalopathy agent in primates after intravenous or oral infection. . Lancet 363:, 422–428. [CrossRef][PubMed]
    [Google Scholar]
  40. Hewitt P. E., Llewelyn C. A., Mackenzie J., Will R. G.. ( 2006;). Creutzfeldt-Jakob disease and blood transfusion: results of the UK Transfusion Medicine Epidemiological Review study. . Vox Sang 91:, 221–230. [CrossRef][PubMed]
    [Google Scholar]
  41. Holada K., Vostal J. G., Theisen P. W., MacAuley C., Gregori L., Rohwer R. G.. ( 2002;). Scrapie infectivity in hamster blood is not associated with platelets. . J Virol 76:, 4649–4650. [CrossRef][PubMed]
    [Google Scholar]
  42. Honda H., Sasaki K., Minaki H., Masui K., Suzuki S. O., Doh-Ura K., Iwaki T.. ( 2012;). Protease-resistant PrP and PrP oligomers in the brain in human prion diseases after intraventricular pentosan polysulfate infusion. . Neuropathology 32:, 124–132. [CrossRef][PubMed]
    [Google Scholar]
  43. Houston F., Foster J. D., Chong A., Hunter N., Bostock C. J.. ( 2000;). Transmission of BSE by blood transfusion in sheep. . Lancet 356:, 999–1000. [CrossRef][PubMed]
    [Google Scholar]
  44. Hunter N., Foster J., Chong A., McCutcheon S., Parnham D., Eaton S., MacKenzie C., Houston F.. ( 2002;). Transmission of prion diseases by blood transfusion. . J Gen Virol 83:, 2897–2905.[PubMed]
    [Google Scholar]
  45. Jackson G. S., Burk-Rafel J., Edgeworth J. A., Sicilia A., Abdilahi S., Korteweg J., Mackey J., Thomas C., Wang G.. & other authors ( 2014;). Population screening for variant Creutzfeldt-Jakob disease using a novel blood test: diagnostic accuracy and feasibility study. . JAMA Neurol 71:, 421–428. [CrossRef][PubMed]
    [Google Scholar]
  46. Kocisko D. A., Lansbury P. T. Jr, Caughey B.. ( 1996;). Partial unfolding and refolding of scrapie-associated prion protein: evidence for a critical 16-kDa C-terminal domain. . Biochemistry 35:, 13434–13442. [CrossRef][PubMed]
    [Google Scholar]
  47. Kocisko D. A., Caughey B., Morrey J. D., Race R. E.. ( 2006a;). Enhanced antiscrapie effect using combination drug treatment. . Antimicrob Agents Chemother 50:, 3447–3449. [CrossRef][PubMed]
    [Google Scholar]
  48. Kocisko D. A., Vaillant A., Lee K. S., Arnold K. M., Bertholet N., Race R. E., Olsen E. A., Juteau J. M., Caughey B.. ( 2006b;). Potent antiscrapie activities of degenerate phosphorothioate oligonucleotides. . Antimicrob Agents Chemother 50:, 1034–1044. [CrossRef][PubMed]
    [Google Scholar]
  49. Korth C., Stierli B., Streit P., Moser M., Schaller O., Fischer R., Schulz-Schaeffer W., Kretzschmar H., Raeber A.. & other authors ( 1997;). Prion (PrPSc)-specific epitope defined by a monoclonal antibody. . Nature 390:, 74–77. [CrossRef][PubMed]
    [Google Scholar]
  50. Lacroux C., Vilette D., Fernández-Borges N., Litaise C., Lugan S., Morel N., Corbière F., Simon S., Simmons H.. & other authors ( 2012;). Prionemia and leukocyte-platelet-associated infectivity in sheep transmissible spongiform encephalopathy models. . J Virol 86:, 2056–2066. [CrossRef][PubMed]
    [Google Scholar]
  51. Lacroux C., Comoy E., Moudjou M., Perret-Liaudet A., Lugan S., Litaise C., Simmons H., Jas-Duval C., Lantier I.. & other authors ( 2014;). Preclinical detection of variant CJD and BSE prions in blood. . PLoS Pathog 10:, e1004202. [CrossRef][PubMed]
    [Google Scholar]
  52. Lourenco P. C., Schmerr M. J., MacGregor I., Will R. G., Ironside J. W., Head M. W.. ( 2006;). Application of an immunocapillary electrophoresis assay to the detection of abnormal prion protein in brain, spleen and blood specimens from patients with variant Creutzfeldt-Jakob disease. . J Gen Virol 87:, 3119–3124. [CrossRef][PubMed]
    [Google Scholar]
  53. Lukan A., Vranac T., Curin Šerbec V.. ( 2013;). TSE diagnostics: recent advances in immunoassaying prions. . Clin Dev Immunol 2013:, 360604. [CrossRef][PubMed]
    [Google Scholar]
  54. Madera M., Mechref Y., Klouckova I., Novotny M. V.. ( 2007;). High-sensitivity profiling of glycoproteins from human blood serum through multiple-lectin affinity chromatography and liquid chromatography/tandem mass spectrometry. . J Chromatogr B Analyt Technol Biomed Life Sci 845:, 121–137. [CrossRef][PubMed]
    [Google Scholar]
  55. Masters C. L., Richardson E. P. Jr. ( 1978;). Subacute spongiform encephalopathy (Creutzfeldt-Jakob disease). The nature and progression of spongiform change. . Brain 101:, 333–344. [CrossRef][PubMed]
    [Google Scholar]
  56. Minor P. D.. ( 2004;). Technical aspects of the development and validation of tests for variant Creutzfeldt-Jakob disease in blood transfusion. . Vox Sang 86:, 164–170. [CrossRef][PubMed]
    [Google Scholar]
  57. Murayama Y., Yoshioka M., Okada H., Takata M., Yokoyama T., Mohri S.. ( 2007;). Urinary excretion and blood level of prions in scrapie-infected hamsters. . J Gen Virol 88:, 2890–2898. [CrossRef][PubMed]
    [Google Scholar]
  58. Murman D. L.. ( 2012;). Early treatment of Parkinson’s disease: opportunities for managed care. . Am J Manag Care 18: (Suppl), S183–S188.[PubMed]
    [Google Scholar]
  59. Oesch B., Westaway D., Wälchli M., McKinley M. P., Kent S. B., Aebersold R., Barry R. A., Tempst P., Teplow D. B.. & other authors ( 1985;). A cellular gene encodes scrapie PrP 27-30 protein. . Cell 40:, 735–746. [CrossRef][PubMed]
    [Google Scholar]
  60. Orrú C. D., Wilham J. M., Hughson A. G., Raymond L. D., McNally K. L., Bossers A., Ligios C., Caughey B.. ( 2009;). Human variant Creutzfeldt-Jakob disease and sheep scrapie PrP(res) detection using seeded conversion of recombinant prion protein. . Protein Eng Des Sel 22:, 515–521. [CrossRef][PubMed]
    [Google Scholar]
  61. Orrú C. D., Wilham J. M., Raymond L. D., Kuhn F., Schroeder B., Raeber A. J., Caughey B.. ( 2011;). Prion disease blood test using immunoprecipitation and improved quaking-induced conversion. . MBio 2:, e00078-11. [CrossRef][PubMed]
    [Google Scholar]
  62. Pan K. M., Baldwin M., Nguyen J., Gasset M., Serban A., Groth D., Mehlhorn I., Huang Z., Fletterick R. J., Cohen F. E.. ( 1993;). Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. . Proc Natl Acad Sci U S A 90:, 10962–10966. [CrossRef][PubMed]
    [Google Scholar]
  63. Pan T., Li R., Wong B. S., Kang S. C., Ironside J., Sy M. S.. ( 2005a;). Novel antibody-lectin enzyme-linked immunosorbent assay that distinguishes prion proteins in sporadic and variant cases of Creutzfeldt-Jakob disease. . J Clin Microbiol 43:, 1118–1126. [CrossRef][PubMed]
    [Google Scholar]
  64. Pan T., Chang B., Wong P., Li C., Li R., Kang S. C., Robinson J. D., Thompsett A. R., Tein P.. & other authors ( 2005b;). An aggregation-specific enzyme-linked immunosorbent assay: detection of conformational differences between recombinant PrP protein dimers and PrP(Sc) aggregates. . J Virol 79:, 12355–12364. [CrossRef][PubMed]
    [Google Scholar]
  65. Pan T., Sethi J., Nelsen C., Rudolph A., Cervenakova L., Brown P., Orser C. S.. ( 2007;). Detection of misfolded prion protein in blood with conformationally sensitive peptides. . Transfusion 47:, 1418–1425. [CrossRef][PubMed]
    [Google Scholar]
  66. Prusiner S. B.. ( 1982;). Novel proteinaceous infectious particles cause scrapie. . Science 216:, 136–144. [CrossRef][PubMed]
    [Google Scholar]
  67. Prusiner S. B.. ( 1998;). Prions. . Proc Natl Acad Sci U S A 95:, 13363–13383. [CrossRef][PubMed]
    [Google Scholar]
  68. Relaño-Ginés A., Lehmann S., Bencsik A., Herva M. E., Torres J. M., Crozet C. A.. ( 2011;). Stem cell therapy extends incubation and survival time in prion-infected mice in a time window-dependant manner. . J Infect Dis 204:, 1038–1045. [CrossRef][PubMed]
    [Google Scholar]
  69. Rubenstein R., Chang B., Gray P., Piltch M., Bulgin M. S., Sorensen-Melson S., Miller M. W.. ( 2010;). A novel method for preclinical detection of PrPSc in blood. . J Gen Virol 91:, 1883–1892. [CrossRef][PubMed]
    [Google Scholar]
  70. Rudd P. M., Endo T., Colominas C., Groth D., Wheeler S. F., Harvey D. J., Wormald M. R., Serban H., Prusiner S. B.. & other authors ( 1999;). Glycosylation differences between the normal and pathogenic prion protein isoforms. . Proc Natl Acad Sci U S A 96:, 13044–13049. [CrossRef][PubMed]
    [Google Scholar]
  71. Ryou C., Titlow W. B., Mays C. E., Bae Y., Kim S.. ( 2011;). The suppression of prion propagation using poly-L-lysine by targeting plasminogen that stimulates prion protein conversion. . Biomaterials 32:, 3141–3149. [CrossRef][PubMed]
    [Google Scholar]
  72. Saá P., Castilla J., Soto C.. ( 2006;). Presymptomatic detection of prions in blood. . Science 313:, 92–94. [CrossRef][PubMed]
    [Google Scholar]
  73. Saborio G. P., Permanne B., Soto C.. ( 2001;). Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. . Nature 411:, 810–813. [CrossRef][PubMed]
    [Google Scholar]
  74. Sáez-Valero J., Fodero L. R., Sjögren M., Andreasen N., Amici S., Gallai V., Vanderstichele H., Vanmechelen E., Parnetti L.. & other authors ( 2003;). Glycosylation of acetylcholinesterase and butyrylcholinesterase changes as a function of the duration of Alzheimer’s disease. . J Neurosci Res 72:, 520–526. [CrossRef][PubMed]
    [Google Scholar]
  75. Segarra C., Bougard D., Moudjou M., Laude H., Béringue V., Coste J.. ( 2013;). Plasminogen-based capture combined with amplification technology for the detection of PrP(TSE) in the pre-clinical phase of infection. . PLoS ONE 8:, e69632. [CrossRef][PubMed]
    [Google Scholar]
  76. Sheinerman K. S., Umansky S. R.. ( 2013;). Circulating cell-free microRNA as biomarkers for screening, diagnosis and monitoring of neurodegenerative diseases and other neurologic pathologies. . Front Cell Neurosci 7:, 150. [CrossRef][PubMed]
    [Google Scholar]
  77. Silveyra M. X., Cuadrado-Corrales N., Marcos A., Barquero M. S., Rábano A., Calero M., Sáez-Valero J.. ( 2006;). Altered glycosylation of acetylcholinesterase in Creutzfeldt-Jakob disease. . J Neurochem 96:, 97–104. [CrossRef][PubMed]
    [Google Scholar]
  78. Sim V. L.. ( 2012;). Prion disease: chemotherapeutic strategies. . Infect Disord Drug Targets 12:, 144–160. [CrossRef][PubMed]
    [Google Scholar]
  79. Soto C.. ( 2004;). Diagnosing prion diseases: needs, challenges and hopes. . Nat Rev Microbiol 2:, 809–819. [CrossRef][PubMed]
    [Google Scholar]
  80. Talens S., Leebeek F. W., Demmers J. A., Rijken D. C.. ( 2012;). Identification of fibrin clot-bound plasma proteins. . PLoS ONE 7:, e41966. [CrossRef][PubMed]
    [Google Scholar]
  81. Tattum M. H., Jones S., Pal S., Collinge J., Jackson G. S.. ( 2010a;). Discrimination between prion-infected and normal blood samples by protein misfolding cyclic amplification. . Transfusion 50:, 996–1002. [CrossRef][PubMed]
    [Google Scholar]
  82. Tattum M. H., Jones S., Pal S., Khalili-Shirazi A., Collinge J., Jackson G. S.. ( 2010b;). A highly sensitive immunoassay for the detection of prion-infected material in whole human blood without the use of proteinase K. . Transfusion 50:, 2619–2627. [CrossRef][PubMed]
    [Google Scholar]
  83. Terry L. A., Howells L., Hawthorn J., Edwards J. C., Moore S. J., Bellworthy S. J., Simmons H., Lizano S., Estey L.. & other authors ( 2009;). Detection of PrPsc in blood from sheep infected with the scrapie and bovine spongiform encephalopathy agents. . J Virol 83:, 12552–12558. [CrossRef][PubMed]
    [Google Scholar]
  84. Thackray A. M., Klein M. A., Bujdoso R.. ( 2003;). Subclinical prion disease induced by oral inoculation. . J Virol 77:, 7991–7998. [CrossRef][PubMed]
    [Google Scholar]
  85. Thorne L., Terry L. A.. ( 2008;). In vitro amplification of PrPSc derived from the brain and blood of sheep infected with scrapie. . J Gen Virol 89:, 3177–3184. [CrossRef][PubMed]
    [Google Scholar]
  86. Triantaphyllidou I. E., Sklaviadis T., Vynios D. H.. ( 2006;). Detection, quantification, and glycotyping of prion protein in specifically activated enzyme-linked immunosorbent assay plates. . Anal Biochem 359:, 176–182. [CrossRef][PubMed]
    [Google Scholar]
  87. Trieschmann L., Navarrete Santos A., Kaschig K., Torkler S., Maas E., Schätzl H., Böhm G.. ( 2005;). Ultra-sensitive detection of prion protein fibrils by flow cytometry in blood from cattle affected with bovine spongiform encephalopathy. . BMC Biotechnol 5:, 26. [CrossRef][PubMed]
    [Google Scholar]
  88. Tsukui K., Takata M., Tadokoro K.. ( 2007;). A potential blood test for transmissible spongiform encephalopathies by detecting carbohydrate-dependent aggregates of PrPres-like proteins in scrapie-infected hamster plasma. . Microbiol Immunol 51:, 1221–1231. [CrossRef][PubMed]
    [Google Scholar]
  89. UK Health Protection Agency ( 2007;). Fourth case of transfusion-associated variant-CJD infection. . http://www.hpa.org.uk/hpr/archives/2007/news2007/news0307.htm#cjd [accessed Dec 24, 2010].
  90. Völkel D., Zimmermann K., Zerr I., Bodemer M., Lindner T., Turecek P. L., Poser S., Schwarz H. P.. ( 2001;). Immunochemical determination of cellular prion protein in plasma from healthy subjects and patients with sporadic CJD or other neurologic diseases. . Transfusion 41:, 441–448. [CrossRef][PubMed]
    [Google Scholar]
  91. Wei X., Herbst A., Ma D., Aiken J., Li L.. ( 2011;). A quantitative proteomic approach to prion disease biomarker research: delving into the glycoproteome. . J Proteome Res 10:, 2687–2702. [CrossRef][PubMed]
    [Google Scholar]
  92. Yakovleva O., Janiak A., McKenzie C., McShane L., Brown P., Cervenakova L.. ( 2004;). Effect of protease treatment on plasma infectivity in variant Creutzfeldt-Jakob disease mice. . Transfusion 44:, 1700–1705. [CrossRef][PubMed]
    [Google Scholar]
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