Enhanced detection of prion infectivity from blood by preanalytical enrichment with peptoid-conjugated beads
Autoři:
Simone Hornemann aff001; Petra Schwarz aff001; Elisabeth J. Rushing aff001; Michael D. Connolly aff003; Ronald N. Zuckermann aff003; Alice Y. Yam aff002; Adriano Aguzzi aff001
Působiště autorů:
Institute of Neuropathology, University of Zurich, Zurich, Switzerland
aff001; Novartis Vaccines and Diagnostics Inc., Emeryville, California, United States of America
aff002; Biological Nanostructures Facility, The Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, California, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0216013
Souhrn
Prions cause transmissible infectious diseases in humans and animals and have been found to be transmissible by blood transfusion even in the presymptomatic stage. However, the concentration of prions in body fluids such as blood and urine is extremely low; therefore, direct diagnostic tests on such specimens often yield false-negative results. Quantitative preanalytical prion enrichment may significantly improve the sensitivity of prion assays by concentrating trace amounts of prions from large volumes of body fluids. Here, we show that beads conjugated to positively charged peptoids not only captured PrP aggregates from plasma of prion-infected hamsters, but also adsorbed prion infectivity in both the symptomatic and preclinical stages of the disease. Bead absorbed prion infectivity efficiently transmitted disease to transgenic indicator mice. We found that the readout of the peptoid-based misfolded protein assay (MPA) correlates closely with prion infectivity in vivo, thereby validating the MPA as a simple, quantitative, and sensitive surrogate indicator of the presence of prions. The reliable and sensitive detection of prions in plasma will enable a wide variety of applications in basic prion research and diagnostics.
Klíčová slova:
Biology and life sciences – Organisms – Eukaryota – Research and analysis methods – Animals – Anatomy – Medicine and health sciences – Physiology – Vertebrates – Amniotes – Mammals – Zoology – Infectious diseases – Body fluids – Blood – Blood plasma – Neurology – Rodents – Neurodegenerative diseases – Specimen preparation and treatment – Staining – Group-specific staining – Zoonoses – Hamsters – Animal diseases – Animal prion diseases – Prion diseases – Creutzfeldt-Jakob disease – Hematoxylin staining
Zdroje
1. Prusiner SB. Prions. Proc Natl Acad Sci U S A. 1998;95(23):13363–83. Epub 1998/11/13. doi: 10.1073/pnas.95.23.13363 9811807.
2. Weissmann C. The state of the prion. Nat Rev Microbiol. 2004;2(11):861–71. Epub 2004/10/21. doi: 10.1038/nrmicro1025 15494743.
3. Edgeworth JA, Gros N, Alden J, Joiner S, Wadsworth JD, Linehan J, et al. Spontaneous generation of mammalian prions. Proc Natl Acad Sci U S A. 2010;107(32):14402–6. Epub 2010/07/28. doi: 10.1073/pnas.1004036107 20660771.
4. Mastrianni JA. The genetics of prion diseases. Genet Med. 2010;12(4):187–95. Epub 2010/03/11. doi: 10.1097/GIM.0b013e3181cd7374 20216075.
5. Aguzzi A, Polymenidou M. Mammalian prion biology: one century of evolving concepts. Cell. 2004;116(2):313–27. Epub 2004/01/28. 14744440.
6. Weissmann C, Enari M, Klohn PC, Rossi D, Flechsig E. Transmission of prions. J Infect Dis. 2002;186 Suppl 2:S157–65. Epub 2002/11/09. doi: 10.1086/344575 12424692.
7. Haybaeck J, Heikenwalder M, Klevenz B, Schwarz P, Margalith I, Bridel C, et al. Aerosols transmit prions to immunocompetent and immunodeficient mice. PLoS Pathog. 2011;7(1):e1001257. doi: 10.1371/journal.ppat.1001257 21249178.
8. Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I, Collinge J, et al. The same prion strain causes vCJD and BSE. Nature. 1997;389(6650):448–50, 526. Epub 1997/10/23 22:27. doi: 10.1038/38925 9333232.
9. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, et al. Transmissions to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature. 1997;389(6650):498–501. Epub 1997/10/23 22:27. doi: 10.1038/39057 9333239.
10. Aguzzi A, Weissmann C. Spongiform encephalopathies: a suspicious signature. Nature. 1996;383(6602):666–7. Epub 1996/10/24. doi: 10.1038/383666a0 8878470.
11. Aguzzi A, Glatzel M. Prion infections, blood and transfusions. Nat Clin Pract Neurol. 2006;2(6):321–9. Epub 2006/08/26. doi: 10.1038/ncpneuro0214 16932576.
12. Llewelyn CA, Hewitt PE, Knight RS, Amar K, Cousens S, Mackenzie J, et al. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet. 2004;363(9407):417–21. 14962520.
13. Peden AH, Head MW, Ritchie DL, Bell JE, Ironside JW. Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet. 2004;364(9433):527–9. 15302196.
14. Houston F, Foster JD, Chong A, Hunter N, Bostock CJ. Transmission of BSE by blood transfusion in sheep. Lancet. 2000;356:999–1000. 11041403
15. Hunter N, Foster J, Chong A, McCutcheon S, Parnham D, Eaton S, et al. Transmission of prion diseases by blood transfusion. J Gen Virol. 2002;83(Pt 11):2897–905. 12388826.
16. Mathiason CK, Powers JG, Dahmes SJ, Osborn DA, Miller KV, Warren RJ, et al. Infectious prions in the saliva and blood of deer with chronic wasting disease. Science. 2006;314(5796):133–6. Epub 2006/10/07. doi: 10.1126/science.1132661 17023660.
17. Brown P, Rohwer RG, Dunstan BC, MacAuley C, Gajdusek DC, Drohan WN. The distribution of infectivity in blood components and plasma derivatives in experimental models of transmissible spongiform encephalopathy. Transfusion. 1998;38(9):810–6. 9738619.
18. Holada K, Vostal JG, Theisen PW, MacAuley C, Gregori L, Rohwer RG. Scrapie infectivity in hamster blood is not associated with platelets. Journal of virology. 2002;76(9):4649–50. doi: 10.1128/JVI.76.9.4649-4650.2002 11932431.
19. Douet JY, Zafar S, Perret-Liaudet A, Lacroux C, Lugan S, Aron N, et al. Detection of infectivity in blood of persons with variant and sporadic Creutzfeldt-Jakob disease. Emerg Infect Dis. 2014;20(1):114–7. Epub 2014/01/01. doi: 10.3201/eid2001.130353 24377668.
20. Brown P, Cervenakova L, McShane LM, Barber P, Rubenstein R, Drohan WN. Further studies of blood infectivity in an experimental model of transmissible spongiform encephalopathy, with an explanation of why blood components do not transmit Creutzfeldt-Jakob disease in humans. Transfusion. 1999;39(11–12):1169–78. Epub 1999/12/22. doi: 10.1046/j.1537-2995.1999.39111169.x 10604242.
21. Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature. 2001;411(6839):810–3. Epub 2001/07/19. doi: 10.1038/35081095 11459061.
22. Atarashi R, Moore RA, Sim VL, Hughson AG, Dorward DW, Onwubiko HA, et al. Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat Methods. 2007;4(8):645–50. 17643109.
23. Castilla J, Saa P, Soto C. Detection of prions in blood. Nat Med. 2005;11(9):982–5. Epub 2005/08/30. doi: 10.1038/nm1286 16127436.
24. Frontzek K, Pfammatter M, Sorce S, Senatore A, Schwarz P, Moos R, et al. Neurotoxic Antibodies against the Prion Protein Do Not Trigger Prion Replication. PLoS One. 2016;11(9):e0163601. doi: 10.1371/journal.pone.0163601 27684562.
25. McGuire LI, Poleggi A, Poggiolini I, Suardi S, Grznarova K, Shi S, et al. Cerebrospinal fluid real-time quaking-induced conversion is a robust and reliable test for sporadic creutzfeldt-jakob disease: An international study. Ann Neurol. 2016;80(1):160–5. doi: 10.1002/ana.24679 27130376.
26. Lau AL, Yam AY, Michelitsch MM, Wang X, Gao C, Goodson RJ, et al. Characterization of prion protein (PrP)-derived peptides that discriminate full-length PrPSc from PrPC. Proc Natl Acad Sci U S A. 2007;104(28):11551–6. Epub 2007/07/03. doi: 10.1073/pnas.0704260104 17601775.
27. Polymenidou M, Prokop S, Jung HH, Hewer E, Peretz D, Moos R, et al. Atypical Prion Protein Conformation in Familial Prion Disease with PRNP P105T Mutation. Brain Pathol. 2011;21(2):209–14. doi: 10.1111/j.1750-3639.2010.00439.x 20875062.
28. Kranich J, Krautler NJ, Falsig J, Ballmer B, Li S, Hutter G, et al. Engulfment of cerebral apoptotic bodies controls the course of prion disease in a mouse strain-dependent manner. J Exp Med. 2010;207(10):2271–81. Epub 2010/09/15. doi: 10.1084/jem.20092401 20837697.
29. Herrmann US, Schutz AK, Shirani H, Huang D, Saban D, Nuvolone M, et al. Structure-based drug design identifies polythiophenes as antiprion compounds. Sci Transl Med. 2015;7(299):299ra123. doi: 10.1126/scitranslmed.aab1923 26246168.
30. Yam AY, Wang X, Gao CM, Connolly MD, Zuckermann RN, Bleu T, et al. A universal method for detection of amyloidogenic misfolded proteins. Biochemistry. 2011;50(20):4322–9. doi: 10.1021/bi200215j 21539296.
31. Gao CM, Yam AY, Wang X, Magdangal E, Salisbury C, Peretz D, et al. Abeta40 oligomers identified as a potential biomarker for the diagnosis of Alzheimer’s disease. PLoS One. 2010;5(12):e15725. doi: 10.1371/journal.pone.0015725 21209907.
32. Simon RJ, Kania RS, Zuckermann RN, Huebner VD, Jewell DA, Banville S, et al. Peptoids: a modular approach to drug discovery. Proc Natl Acad Sci U S A. 1992;89(20):9367–71. Epub 1992/10/15. doi: 10.1073/pnas.89.20.9367 1409642.
33. Margalith I, Suter C, Ballmer B, Schwarz P, Tiberi C, Sonati T, et al. Polythiophenes Inhibit Prion Propagation by Stabilizing Prion Protein (PrP) Aggregates. J Biol Chem. 2012;287(23):18872–87. Epub 2012/04/12. doi: 10.1074/jbc.M112.355958 22493452.
34. Fischer M, Rulicke T, Raeber A, Sailer A, Moser M, Oesch B, et al. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 1996;15(6):1255–64. Epub 1996/03/15. 8635458.
35. Kimberlin RH, Walker CA. Pathogenesis of scrapie (strain 263K) in hamsters infected intracerebrally, intraperitoneally or intraocularly. J Gen Virol. 1986;67(Pt 2):255–63.
36. Laursen SE, Belknap JK. Intracerebroventricular injections in mice. Some methodological refinements. J Pharmacol Methods. 1986;16(4):355–7. Epub 1986/12/01. 3784576.
37. Saa P, Castilla J, Soto C. Presymptomatic detection of prions in blood. Science. 2006;313(5783):92–4. Epub 2006/07/11. doi: 10.1126/science.1129051 16825570.
38. Scott M, Foster D, Mirenda C, Serban D, Coufal F, Waelchli M, et al. Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell. 1989;59:847–57. 2574076
39. Zhu C, Schwarz P, Abakumova I, Aguzzi A. Unaltered Prion Pathogenesis in a Mouse Model of High-Fat Diet-Induced Insulin Resistance. PLoS One. 2015;10(12):e0144983. Epub 2015/12/15. doi: 10.1371/journal.pone.0144983 26658276.
40. Taraboulos A, Jendroska K, Serban D, Yang SL, DeArmond SJ, Prusiner SB. Regional mapping of prion proteins in brain. Proc Natl Acad Sci U S A. 1992;89(16):7620–4. doi: 10.1073/pnas.89.16.7620 1354357
41. Polymenidou M, Moos R, Scott M, Sigurdson C, Shi YZ, Yajima B, et al. The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS ONE. 2008;3(12):e3872. doi: 10.1371/journal.pone.0003872 19060956.
42. Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, Kobayashi Y, et al. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature. 1996;379(6563):339–43. doi: 10.1038/379339a0 8552188.
43. Menei P, Croue A, Daniel V, Pouplard-Barthelaix A, Benoit JP. Fate and biocompatibility of three types of microspheres implanted into the brain. J Biomed Mater Res. 1994;28(9):1079–85. Epub 1994/09/01. doi: 10.1002/jbm.820280913 7814435.
44. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. The American Journal of Hygiene. 1938;27:493–7.
45. Karber G. Beitrag zur kollektiven Behandlung Pharmakologische Reihen versuche. Arch Exp Pathol Pharmacol. 1931 (162):480–3.
46. Ramakrishnan MA. Determination of 50% endpoint titer using a simple formula. World J Virol. 2016;5(2):85–6. doi: 10.5501/wjv.v5.i2.85 27175354.
47. Prusiner SB, Cochran SP, Groth DF, Downey DE, Bowman KA, Martinez HM. Measurement of the scrapie agent using an incubation time interval assay. Ann Neurol. 1982;11(4):353–8. doi: 10.1002/ana.410110406 6808890.
48. Holada K, Simak J, Vostal JG. Transmission of BSE by blood transfusion. Lancet. 2000;356(9243):1772. 11095289
49. Adams RJ, Bray D. Rapid transport of foreign particles microinjected into crab axons. Nature. 1983;303(5919):718–20. 6190095.
50. Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med. 2015;212(7):991–9. doi: 10.1084/jem.20142290 26077718.
51. Raper D, Louveau A, Kipnis J. How Do Meningeal Lymphatic Vessels Drain the CNS? Trends Neurosci. 2016;39(9):581–6. doi: 10.1016/j.tins.2016.07.001 27460561.
52. Yakovleva O, Janiak A, McKenzie C, McShane L, Brown P, Cervenakova L. Effect of protease treatment on plasma infectivity in variant Creutzfeldt-Jakob disease mice. Transfusion. 2004;44(12):1700–5. Epub 2004/12/09. doi: 10.1111/j.0041-1132.2004.04198.x 15584983.
53. Zobeley E, Flechsig E, Cozzio A, Enari M, Weissmann C. Infectivity of scrapie prions bound to a stainless steel surface. Mol Med. 1999;5(4):240–3. 10448646.
54. Flechsig E, Hegyi I, Enari M, Schwarz P, Collinge J, Weissmann C. Transmission of scrapie by steel-surface-bound prions. Mol Med. 2001;7(10):679–84. Epub 2001/11/20. 11713367.
55. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, et al. Structural and functional features of central nervous system lymphatic vessels. Nature. 2015;523(7560):337–41. doi: 10.1038/nature14432 26030524.
56. Falsig J, Nilsson KP, Knowles TP, Aguzzi A. Chemical and biophysical insights into the propagation of prion strains. HFSP J. 2008;2(6):332–41. Epub 2009/05/14. doi: 10.2976/1.2990786 19436493.
57. Tixador P, Herzog L, Reine F, Jaumain E, Chapuis J, Le Dur A, et al. The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog. 2010;6(4):e1000859. Epub 2010/04/27. doi: 10.1371/journal.ppat.1000859 20419156.
58. Jucker M, Walker LC. Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol. 2011;70(4):532–40. Epub 2011/10/27. doi: 10.1002/ana.22615 22028219.
59. 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 U S A. 2009;106(9):3479–83. doi: 10.1073/pnas.0813342106 19204279.
60. Miller MB, Supattapone S. Superparamagnetic nanoparticle capture of prions for amplification. Journal of virology. 2011;85(6):2813–7. Epub 2011/01/14. doi: 10.1128/JVI.02451-10 21228242.
61. Orru CD, Wilham JM, Raymond LD, Kuhn F, Schroeder B, Raeber AJ, et al. Prion disease blood test using immunoprecipitation and improved quaking-induced conversion. MBio. 2011;2(3):e00078–11. doi: 10.1128/mBio.00078-11 21558432.
62. Bougard D, Brandel JP, Belondrade M, Beringue V, Segarra C, Fleury H, et al. Detection of prions in the plasma of presymptomatic and symptomatic patients with variant Creutzfeldt-Jakob disease. Sci Transl Med. 2016;8(370):370ra182. Epub 2016/12/23. doi: 10.1126/scitranslmed.aag1257 28003547.
63. Edgeworth JA, Farmer M, Sicilia A, Tavares P, Beck J, Campbell T, et al. Detection of prion infection in variant Creutzfeldt-Jakob disease: a blood-based assay. Lancet. 2011;377(9764):487–93. Epub 2011/02/08. doi: 10.1016/S0140-6736(10)62308-2 21295339.
64. Denkers ND, Henderson DM, Mathiason CK, Hoover EA. Enhanced prion detection in biological samples by magnetic particle extraction and real-time quaking-induced conversion. J Gen Virol. 2016;97(8):2023–9. Epub 2016/05/29. doi: 10.1099/jgv.0.000515 27233771.
65. Segarra C, Bougard D, Moudjou M, Laude H, Beringue V, Coste J. Plasminogen-based capture combined with amplification technology for the detection of PrP(TSE) in the pre-clinical phase of infection. PLoS One. 2013;8(7):e69632. Epub 2013/07/31. doi: 10.1371/journal.pone.0069632 23894513.
66. Hornshaw MP, McDermott JR, Candy JM, Lakey JH. Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides. Biochem Biophys Res Commun. 1995;214(3):993–9. Epub 1995/09/25. doi: 10.1006/bbrc.1995.2384 7575574.
67. Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R, et al. The cellular prion protein binds copper in vivo. Nature. 1997;390(6661):684–7. Epub 1997/12/31. doi: 10.1038/37783 9414160.
68. Luhr KM, Low P, Taraboulos A, Bergman T, Kristensson K. Prion adsorption to stainless steel is promoted by nickel and molybdenum. J Gen Virol. 2009;90(Pt 11):2821–8. Epub 2009/07/17. doi: 10.1099/vir.0.012302-0 19605588.
69. Fischer MB, Roeckl C, Parizek P, Schwarz HP, Aguzzi A. Binding of disease-associated prion protein to plasminogen. Nature. 2000;408(6811):479–83. Epub 2000/12/02. doi: 10.1038/35044100 11100730.
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania