Quaking-induced conversion of prion protein on a thermal mixer accelerates detection in brains infected with transmissible spongiform encephalopathy agents
Autoři:
Nadine Kaelber aff001; Cyrus Bett aff001; David M. Asher aff001; Luisa Gregori aff001
Působiště autorů:
Food and Drug Administration, Center for Biologics Evaluation and Research, Silver Spring, Maryland, United States of America
aff001
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225904
Souhrn
Detection of misfolded prion protein, PrPTSE, in biological samples is important to develop antemortem tests for transmissible spongiform encephalopathies (TSEs). The real-time quaking-induced conversion (RT-QuIC) assay detects PrPTSE but requires dedicated equipment and relatively long incubation times when applied to samples containing extremely low levels of PrPTSE. It was shown that a microplate shaker with heated top (Thermomixer-C) accelerated amplification of PrPTSE in brain suspensions of 263K scrapie and sporadic Creutzfeldt-Jakob disease (sCJD). We expanded the investigation to include TSE agents previously untested, including chronic wasting disease (CWD), macaque-adapted variant CJD (vCJD) and human vCJD, and we further characterized the assays conducted at 42°C and 55°C. PrPTSE from all brains containing the TSE agents were successfully amplified using a truncated hamster recombinant protein except for human vCJD which required truncated bank vole recombinant protein. We compared assays conducted at 42°C on Thermomixer-C, Thermomixer-R (without heated top) and on a fluorimeter used for RT-QuIC. QuIC on Thermomixer-R achieved in only 18 hours assay sensitivity similar to that of RT-QuIC read at 60 hours (or 48 hours with sCJD). QuIC on Thermomixer-C required 24 hours to complete and the endpoint titers of some TSEs were 10-fold lower than those obtained with RT-QuIC and Thermomixer-R. Conversely, at 55°C, the reactions with sCJD and CWD on Thermomixer-C achieved the same sensitivity as with RT-QuIC but in shorter times. Human vCJD samples tested at higher temperatures gave rise to high reactivity in wells containing normal control samples. Similarly, reactions on Thermomixer-R were unsuitable at 55°C. The main disadvantage of Thermomixers is that they cannot track formation of PrP fibrils in real time, a feature useful in some applications. The main advantages of Thermomixers are that they need shorter reaction times to detect PrPTSE, are easier to use, involve more robust equipment, and are relatively affordable. Improvements to QuIC using thermal mixers may help develop accessible antemortem TSE tests.
Klíčová slova:
Recombinant proteins – Reaction time – Hamsters – Animal prion diseases – Creutzfeldt-Jakob disease – Macaque – Chronic wasting disease – Scrapie
Zdroje
1. Will RG. Acquired prion disease: iatrogenic CJD, variant CJD, kuru. Br Med Bull. 2003;66: 255–265. doi: 10.1093/bmb/66.1.255 14522863
2. Kovacs GG, and Budka H. Prion diseases: from protein to cell pathology Am J Pathol. 2008;172: 555–565. doi: 10.2353/ajpath.2008.070442 18245809
3. Büeler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, et al. Mice devoid of PrP are resistant to scrapie. Cell. 1993;73: 1339–1347. doi: 10.1016/0092-8674(93)90360-3 8100741
4. Richt JA, Kasinathan P, Hamir AN, Castilla J, Sathiyaseelan T, Vargas F, et al. Production of cattle lacking prion protein. Nat Biotechnol. 2007;25: 132–138. doi: 10.1038/nbt1271 17195841
5. Brown P, Brandel JP, Sato T, Nakamura Y, MacKenzie J, Will RG, et al. Iatrogenic Creutzfeldt-Jakob disease, final assessment. Emerg Infect Dis. 2012;18: 901–907. doi: 10.3201/eid1806.120116 22607808
6. Bonda DJ, Manjila S, Mehndiratta P, Khan F, Miller BR, Onwuzulike K, et al. Human prion diseases: surgical lessons learned from iatrogenic prion transmission. Neurosurg Focus. 2016; 41(1):E10. doi: 10.3171/2016.5.FOCUS15126 27364252
7. Ae R, Hamaguchi T, Nakamura Y, Yamada M, Tsukamoto T, Mizusawa H, et al. Update: Dura mater graft-associated Creutzfeldt-Jakob Disease—Japan, 1975–2017. MMWR Morb Mortal Wkly Rep. 2018;67: 274–278. doi: 10.15585/mmwr.mm6709a3 29518068
8. Properzi F, and Pocchiari M. Identification of misfolded proteins in body fluids for the diagnosis of prion diseases. Int J Cell Biol. 2013; 839329. doi: 10.1155/2013/839329 24027585
9. Morales R, Duran-Aniotz C, Diaz-Espinoza R, Camacho MV, Soto C. Protein misfolding cyclic amplification of infectious prions. Nat Protoc. 2012;7: 1397–1409. doi: 10.1038/nprot.2012.067 22743831
10. Orrù CD, Groveman BR, Hughson AG, Manca M, Raymond LD, Raymond GJ, et al. RT-QuIC assays for prion disease detection and diagnostics. Methods Mol Biol. 2017;1658: 185–203. doi: 10.1007/978-1-4939-7244-9_14 28861791
11. Atarashi R, Satoh K, Sano K, Fuse T, Yamaguchi N, Ishibashi D. et al. Ultrasensitive human prion detection in cerebrospinal fluid by real-time quaking-induced conversion. Nat Med 2011;17: 175–178. doi: 10.1038/nm.2294 21278748
12. Wilham JM, Orrú CD, Bessen RA, Atarashi R, Sano K, Race B, et al. Rapid endpoint quantitation of prion seeding activity with sensitivity comparable to bioassays. PLoS Pathog. 20106; (12):e1001217.
13. Orrú CD, Bongianni M, Tonoli G, Ferrari S, Hughson AG, Groveman BR, et al. A test for Creutzfeldt-Jakob disease using nasal brushings. N Engl J Med. 2014;371: 519–29. doi: 10.1056/NEJMoa1315200 25099576
14. Bongianni M, Orrù C, Groveman BR, Sacchetto L, Fiorini M, Tonoli G, et al. Diagnosis of human prion disease using Real-Time Quaking-Induced Conversion testing of olfactory mucosa and cerebrospinal fluid samples. JAMA Neurol. 2017;74: 155–162. doi: 10.1001/jamaneurol.2016.4614 27942718
15. Davenport KA, Hoover CE, Denkers ND, Mathiason CK, Hoover EA. Modified PMCA overcomes RT-QuIC inhibitors in deer saliva to detect CWD prions. J Clin Microbiol. 2018; 56(1): e01243–17. doi: 10.1128/JCM.01243-17 29118163
16. Orrú CD, Hughson AG, Groveman BR, Campbell KJ, Anson KJ, Manca M, et al. Factors that improve RT-QuIC detection of prion seeding activity. Viruses. 2016; 8(5):140.
17. Orrú CD, Groveman BR, Hughson AG, Zanusso G, Coulthart MB, Caughey B. Rapid and sensitive RT-QuIC detection of human Creutzfeldt-Jakob disease using cerebrospinal fluid. MBio. 2015 Jan 20;6(1).
18. Franceschini A, Baiardi S, Hughson AG, McKenzie N, Moda F, Rossi M, et al. High diagnostic value of second generation CSF RT-QuIC across the wide spectrum of CJD prions. Sci Rep. 2017 Sep 6;7(1):10655. doi: 10.1038/s41598-017-10922-w 28878311
19. Favole A, Mazza M, Vallino Costassa E, D'Angelo A, Lombardi G, Marconi P, et al. Early and pre-clinical detection of prion seeding activity in cerebrospinal fluid of goats using Real-Time Quaking-Induced Conversion assay. Sci Rep. 2019 Apr 16;9(1):6173. doi: 10.1038/s41598-019-42449-7 30992522
20. Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, Johnson LM, et al. Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods. 2008;5: 211–212. doi: 10.1038/nmeth0308-211 18309304
21. Vendramelli R, Sloan A, Simon SLR, Godal D, Cheng K. ThermoMixer-Aided endpoint Quaking-Induced Conversion (EP-QuIC) permits faster sporadic Creutzfeldt-Jakob Disease (sCJD) identification than Real-Time Quaking-Induced Conversion (RT-QuIC). J Clin Microbiol. 2018; 56(7): e00423–18. doi: 10.1128/JCM.00423-18 29695523
22. Cooper JK, Ladhani K, Minor P. Comparison of candidate vCJD in vitro diagnostic assays using identical sample sets. Vox Sang. 2012;102: 100–109. doi: 10.1111/j.1423-0410.2011.01525.x 22126309
23. Minor P, Newham J, Jones N, Bergeron C, Gregori L, Asher D, et al. Standards for the assay of Creutzfeldt-Jakob disease specimens. J Gen Virol. 2004;85: 1777–1784. doi: 10.1099/vir.0.79959-0 15166463
24. McDowell KL, Nag N, Franco Z, Bu M, Piccardo P, Cervenak J, et al. Blood reference materials from macaques infected with variant Creutzfeldt-Jakob disease agent. Transfusion. 2015;55: 405–412. doi: 10.1111/trf.12841 25154296
25. Bett C, Piccardo P, Cervenak J, Torres JM, Asher DM, Gregori L. Both murine host and inoculum modulate expression of experimental variant Creutzfeldt-Jakob disease. J Gen Virol. 2018;99: 422–433.
26. Bett C, Grgac K, Lon D, Karfunkle M, Keire DA, Asher DM, et al. A heparin purification process removes spiked transmissible spongiform encephalopathy agent. AAPS J. 2017;19: 765–771. doi: 10.1208/s12248-017-0047-y 28116677
27. Dougherty RM. Animal virus titration techniques. In: Harris RJC, editor. Techniques in experimental virology. New York: Academic; 1964. p. 183–186. doi: 10.1016/0042-6822(64)90281-8
28. McNulty E, Nalls AV, Mellentine S, Hughes E, Pulscher L, Hoover EA, et al. Comparison of conventional, amplification and bio-assay detection methods for a chronic wasting disease inoculum pool. PLoS One. 2019 May 9;14(5):e0216621. doi: 10.1371/journal.pone.0216621 31071138
29. Orrú CD, Groveman BR, Raymond LD, Hughson AG, Nonno R, Zou W, et al. Bank vole prion protein as an apparently universal substrate for RT-QuIC-based detection and discrimination of prion strains. PLoS Pathog. 2015; 11(6):e1004983. doi: 10.1371/journal.ppat.1004983 26086786
30. Levavasseur E, Biacabe AG, Comoy E, Culeux A, Grznarova K, Privat N, et al. Detection and partial discrimination of atypical and classical bovine spongiform encephalopathies in cattle and primates using real-time quaking-induced conversion assay. PLoS One. 2017 Feb 23;12(2):e0172428. doi: 10.1371/journal.pone.0172428 28231300
31. Peden AH, McGuire LI, Appleford NE, Mallinson G, Wilham JM, Orrú CD, et al. Sensitive and specific detection of sporadic Creutzfeldt-Jakob disease brain prion protein using real-time quaking-induced conversion. J Gen Virol. 2012; 93:438–49. doi: 10.1099/vir.0.033365-0 22031526
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- 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
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts