New possibilities of laboratory diagnostics of diseases associated with amyloid formation

Czech version

Authors: S. Galušková ¹; T. Moško ¹; P. Dušek ²; R. Matěj ³; K. Holada ¹
Authors‘ workplace: Ústav imunologie a mikrobiologie, 1. LF UK v Praze ¹; Neurologická klinika, 1. LF UK a VFN v Praze ²; Oddělení patologie a národní, referenční laboratoř TSE-CJN, Thomayerova nemocnice, Praha ³
Published in: Cesk Slov Neurol N 2021; 84/117(4): 334-340
Category: Review Article
doi: https://doi.org/10.48095/cccsnn2021334

Overview

Many neurodegenerative diseases are defined by the aggregation and accumulation of the specific pathological protein in the CNS, leading to irreversible and fatal changes of the tissues. However, due to high clinical and epidemiological heterogeneity, a definitive ante-mortem diagnosis is very difficult to perform. The definitive diagnosis is confirmed by neuropathological evaluation made only at autopsy. Hope for early and accurate laboratory diagnostics of these diseases within a patient’s life represents methods based on the detection of seeding activity of pathological proteins. An example is a highly specific and ultrasensitive new method called Real-Time Quaking-Induced Conversion (RT-QuIC) assay. Originally, RT-QuIC was developed for the diagnosis of prions showing 92–97% sensitivity and 100% specificity. In our laboratory, we were able to detect prions in 39 brain samples, corresponding 24 cerebrospinal fluid samples, and in 38 skin samples of patients with Creutzfeldt-Jakob disease using RT-QuIC. Lately, the use of the RT-QuIC method for detection of pathological protein a-synuclein, which accumulates during Parkinson’s disease or dementia with Lewy bodies, and tau protein which is characteristic for Alzheimer’s disease or corticobasal degeneration, was described. This review aims to elucidate the diagnosis of neurodegenerative diseases and its recent approaches using RT-QuIC.

Keywords:

brain tract – comparative anatomy – Nervous system – corticospinal tract – optic chiasm – evolution

Sources

1. Riek R, Eisenberg DS. The activities of amyloids from a structural perspective. Nature 2016; 539 (7628): 227–235. doi: 10.1038/nature20416.

2. Prusiner SB. The prion diseases. Brain pathology 1998; 8 (3): 499–513. doi: 10.1111/j.1750-3639.1998.tb00171.x.

3. Ascari LM, Rocha SC, Gonçalves PB et al. Challenges and advances in antemortem diagnosis of human transmissible spongiform encephalopathies. Front Bioeng Biotechnol 2020; 8: 1228. doi: 10.3389/fbioe.2020.585 896.

4. Monari L, Chen SG, Brown P et al. Fatal familial insomnia and familial Creutzfeldt-Jakob disease: different prion proteins determined by a DNA polymorphism. Proc Natl Acad Sci U S A 1994; 91 (7): 2839–2842. doi: https: //doi.org/10.1073/pnas.91.7.2839.

5. Kobayashi A, Teruya K, Matsuura Y et al. The influence of PRNP polymorphisms on human prion disease susceptibility: an update. Acta Neuropathol 2015; 130 (2): 159–170. doi: 10.1007/s00401-015-1447-7.

6. Bernardi L, Bruni AC. Mutations in prion protein gene: pathogenic mechanisms in C-Terminal vs. N-Terminal domain, a review. Int J Mol Sci 2019; 20 (14): 3606. doi: 10.3390/ijms20143606.

7. Kim MO, Takada LT, Wong K et al. Genetic PrP prion diseases. Cold Spring Harb Perspect Biol 2018; 10 (5): a033134. doi: 10.1101/cshperspect.a033134.

8. Gdovinová Z. Creutzfeldt-Jakobova choroba. Cesk Slov Neurol N 2013; 76/109 (2): 138–154.

9. Mancuso M, Siciliano G, Capellari S et al. Creutzfeldt-Jakob disease with E200K PRNP mutation: a case report and revision of the literature. Neurol Sci 2009; 30 (5): 417–420. doi: 10.1007/s10072-009-0118-7.

10. Rohan Z, Parobková E, Johanidesová S et al. Lidské prionové nemoci v České republice – 10 let zkušeností s diagnostikou. Cesk Slov Neurol N 2013; 76/109 (3): 300–306.

11. Collins S, McLean CA, Masters CL. Gerstmann-Sträussler-Scheinker syndrome, fatal familial insomnia, and kuru: a review ofthese less common human transmissible spongiform encephalopathies. J Clin Neurosci 2001; 8 (5): 387–397. doi: 10.1054/jocn.2001.0919.

12. Holada K, Simák J, Vostal JG. Transmission of BSE by blood transfusion. Lancet 2000; 356 (9243): 1772. doi: 10.1016/S0410-6736 (05) 71968-1.

13. Will RG. Acquired prion disease: iatrogenic CJD, variant CJD, kuru. Br Med Bull 2003; 66 (1): 255–265. doi: 10.1093/bmb/66.1.225.

14. Brown P, Brunk C, Budka H et al. WHO manual for surveillance of human transmissible spongiform encephalopathies, including variant Creutzfeldt-Jakob disease. World Health Organization 2003. [online]. Available form URL: https: //www.who.int/bloodproducts/TSE-manual2003.pdf.

15. CDC’s diagnostic criteria for Creutzfeldt-Jakob disease (CJD), 2018. [online]. Available from URL: https: //www.cdc.gov/prions/cjd/diagnostic-criteria.html.

16. Panigaj M, Glier H, Wildova M et al. Expression of prion protein in mouse erythroid progenitors and differentiating murine erythroleukemia cells. PLoS One 2011; 6 (9): e24599. doi: 10.1371/journal.pone.0024599.

17. Collins SJ, Sanchez-Juan P, Masters CL et al. Determinants of diagnostic investigation sensitivities across the clinical spectrum of sporadic Creutzfeldt-Jakob disease. Brain 2006; 129 (9): 2278–2287. doi: 10.1093/brain/aw 1159.

18. Orrú CD, Caughey B. Prion seeded conversion and amplification assays. Top Curr Chem 2011; 305: 121–133. doi: 10.1007/128_2011_184.

19. Colby DW, Zhang Q, Wang S et al. Prion detection by an amyloid seeding assay. Proc Natl Acad Sci U S A 2007; 104 (52): 20914–20919. doi: 10.1073/pnas.0710152105.

20. Castilla J, Saá P, Hetz C et al. In vitro generation of infectious scrapie prions. Cell 2005; 121 (2): 195–206. doi: 10.1016/j.cell.2005.02.011.

21. Kraus A, Saijo E, Metrick MA. Seeding selectivity and ultrasensitive detection of tau aggregate conformers of Alzheimer disease. Acta Neuropathol 2019; 137 (4): 585–598. doi: 10.1007/s00401-018-1947-3.

22. Orrú CD, Wilham JM, Vascellari S et al. New generation QuIC assay for prion seeding activity. Prion 2012; 6 (2): 147–152. doi: 10.4161/pri.19430.

23. Atarashi R, Satoh K, Sano K et al. Ultrasensitive human prion detection in cerebrospinal fluid by real-time quaking-induced conversion. Nat Med 2011; 17 (2): 175. doi: 10.1038/nm.2294.

24. Saijo E, Groveman BR, Kraus A et al. Ultrasensitive RT-QuIC seed amplification assays for disease-associated tau, a-synuclein, and prion aggregates. Methods Mol Biol 2019; 1873: 19–37. doi: 10.1007/978-1-4939-8820-4_2.

25. Candelise N, Baiardi S, Franceschini A et al. Toward an improved early diagnosis of neurodegenerative diseases: the emerging role of in vitro conversion assays for protein amyloids. Acta Neuropathol Commun 2020; 8 (1): 1–16. doi: 10.1186/s40478-020-009900-x.

26. Orrú CD, Groveman BR, Foutz A et al. Ring trial of 2nd generation RT-QuIC diagnostic tests for sporadic CJD. Ann Clin Transl Neurol 2020; 7 (11): 2262–2271. doi: 10.1002/acn3.51219.

27. Mammana A, Baiardi S, Rossi M et al. Detection of prions in skin punch biopsies of Creutzfeldt-Jakob disease patients. Ann Clin Transl Neurol 2020; 7 (4): 559–564. doi: 10.1002/acn3.51000.

28. Orrú CD, Bongianni M, Tonoli G et al. A test for Creutzfeldt-Jakob disease using nasal brushings. N Engl J Med 2014; 371 (6): 519–529. doi: 10.1056/NEJMoal315200.

29. Moško T, Galušková S, Matěj R et al. Detection of prions in brain homogenates and CSF samples using a second-generation RT-QuIC assay: a useful tool for retrospective analysis of archived samples. Pathogens 2021; 10 (6): 750. doi: 10.3390/pathogens10060750.

30. Orrú C, Hughson A, Groveman B et al. Factors that improve RT-QuIC detection of prion seeding activity. Viruses 2016; 8 (5): 140. doi: 10.3390/v8050140.

31. Zahn R, von Schroetter C, Wüthrich K. Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett 1997; 417 (3): 400–404. doi: 10.1016/S0014-5793 (97) 01330-6.

32. Orrù CD, Groveman BR, Hughson AG 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.

33. Orrú CD, Groveman BR, Raymond LD 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.

34. Nonno R, Di Bari MA, Cardone F et al. Efficient transmission and characterization of Creutzfeldt–Jakob disease strains in bank voles. PLoS Pathog 2006; 2 (2): e12. doi: 10.1371/journal.ppat.0020012.

35. Cheng K, Sloan A, Waitt B et al. Altered rPrP substrate structures and their influence on real-time quaking induced conversion reactions. Protein Expr Purif 2018; 143: 20–27. doi: 10.1016/j.pep.2017.10.007.

36. Erkkinen MG, Kim MO, Geschwind MD. Clinical neurology and epidemiology of the major neurodegenerative diseases. Cold Spring Harb Perspect Biol 2018; 10 (4): a033118. doi: 10.1101/cshperspect.a033118.

37. Adler CH, Beach TG, Hentz JG et al. Low clinical diagnostic accuracy of early vs advanced Parkinson disease: clinicopathologic study. Neurology 2014; 83 (5): 406–412. doi: 10.1212/WNL.0000000000000641.

38. Williams DR. Tauopathies: classification and clinical update on neurodegenerative diseases associated with microtubule-associated protein tau. Intern Med J 2006; 36 (10): 652–660. doi: 10.1111/j.1445-5994.2006.011 53.x.

39. Soto C, Pritzkow S. Protein misfolding, aggregation and conformational strains in neurodegenerative diseases. Nat Neurosci 2018; 21 (10): 1332–1340. doi: 10.1038/s41593-018-0235-9.

40. De Luca CMG, Elia AE, Portaleone SM et al. Efficient RT-QuIC seeding activity for a-synuclein in olfactory mucosa samples of patients with Parkin- son’s disease and multiple system atrophy. Transl Neurodegener 2019; 8 (1): 24. doi: 10.1186/s40035-019-01 64-x.

41. Fairfoul G, McGuire LI., Pal S et al. Alpha-synuclein RT-Qu IC in the CSF of patients with alpha-synucleinopathies. Ann Clin Transl Neurol 2016; 3 (10): 812–818. doi: 10.1002/acn3.338.

42. Garrido A, Fairfoul G, Tolosa ES et al. α-synuclein RT-QuIC in cerebrospinal fluid of LRRK2-linked Parkinson’s disease. Ann Clin Transl Neurol 2019; 6 (6): 1024–1032. doi: 10.1002/acn3.772.

43. Spillantini MG, Goedert M. Tau pathology and neurodegeneration. Lancet Neurol 2013; 12 (6): 609–622. doi: 10.1016/S1474-4422 (13) 70090-5.

44. Saijo E, Ghetti B, Zanusso G et al. Ultrasensitive and selective detection of 3-repeat tau seeding activity in Pick disease brain and cerebrospinal fluid. Acta Neuropathol 2017; 133 (5): 751–765. doi: 10.1007/s00401-017-1692-z.

45. Saijo E, Metrick MA, Koga S et al. 4-repeat tau seeds and templating subtypes as brain and CSF biomarkers of frontotemporal lobar degeneration. Acta Neuropathol 2020; 139 (1): 63–77. doi: 10.1007/s00401-019-02080-2.