Proteopathic Seed Amplification Assays for Neurodegenerative Disorders

Overview

Journal Clin Lab Med

Specialty Pathology

Date 2020 Jul 29

PMID 32718498

Citations 12

Authors

Natalia do Carmo Ferreira

Byron Caughey

Affiliations

Soon will be listed here.

Abstract

The need for etiological biomarkers for neurodegenerative diseases involving protein aggregation has prompted development of ultrasensitive cellular and cell-free assays based on the prion-like seeding capacity of such aggregates. Among them, prion RT-QuIC assays allow accurate antemortem Creutzfeldt-Jakob disease diagnosis using cerebrospinal fluid and nasal brushings. Analogous assays for synucleinopathies (e.g., Parkinson disease and dementia with Lewy bodies) provide unprecedented diagnostic sensitivity using cerebrospinal fluid. Biosensor cell and tau RT-QuIC assays can detect and discriminate tau aggregates associated with multiple tauopathies (e.g., Alzheimer disease and frontotemporal degeneration). An expanding panel of seed amplification assays should improve diagnostics and therapeutics development.

Citing Articles

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References

Chiti F, Dobson C . Protein Misfolding, Amyloid Formation, and Human Disease: A Summary of Progress Over the Last Decade. Annu Rev Biochem. 2017; 86:27-68. DOI: 10.1146/annurev-biochem-061516-045115. View

Kraus A, Saijo E, Metrick 2nd M, Newell K, Sigurdson C, Zanusso G . Seeding selectivity and ultrasensitive detection of tau aggregate conformers of Alzheimer disease. Acta Neuropathol. 2018; 137(4):585-598. PMC: 6426988. DOI: 10.1007/s00401-018-1947-3. View

Moda F, Gambetti P, Notari S, Concha-Marambio L, Catania M, Park K . Prions in the urine of patients with variant Creutzfeldt-Jakob disease. N Engl J Med. 2014; 371(6):530-9. PMC: 4162740. DOI: 10.1056/NEJMoa1404401. View

Woerman A, Aoyagi A, Patel S, Kazmi S, Lobach I, Grinberg L . Tau prions from Alzheimer's disease and chronic traumatic encephalopathy patients propagate in cultured cells. Proc Natl Acad Sci U S A. 2016; 113(50):E8187-E8196. PMC: 5167200. DOI: 10.1073/pnas.1616344113. View

Gupta S, Jie S, Colby D . Protein misfolding detected early in pathogenesis of transgenic mouse model of Huntington disease using amyloid seeding assay. J Biol Chem. 2011; 287(13):9982-9989. PMC: 3323021. DOI: 10.1074/jbc.M111.305417. View

Candelise N, Schmitz M, Llorens F, Villar-Pique A, Cramm M, Thom T . Seeding variability of different alpha synuclein strains in synucleinopathies. Ann Neurol. 2019; 85(5):691-703. DOI: 10.1002/ana.25446. View

Kaufman S, Sanders D, Thomas T, Ruchinskas A, Vaquer-Alicea J, Sharma A . Tau Prion Strains Dictate Patterns of Cell Pathology, Progression Rate, and Regional Vulnerability In Vivo. Neuron. 2016; 92(4):796-812. PMC: 5392364. DOI: 10.1016/j.neuron.2016.09.055. View

Orru C, Wilham J, Hughson A, Raymond L, McNally K, Bossers A . Human variant Creutzfeldt-Jakob disease and sheep scrapie PrP(res) detection using seeded conversion of recombinant prion protein. Protein Eng Des Sel. 2009; 22(8):515-21. PMC: 2719501. DOI: 10.1093/protein/gzp031. View

Orru C, Soldau K, Cordano C, Llibre-Guerra J, Green A, Sanchez H . Prion Seeds Distribute throughout the Eyes of Sporadic Creutzfeldt-Jakob Disease Patients. mBio. 2018; 9(6). PMC: 6247090. DOI: 10.1128/mBio.02095-18. View

10.

Raymond G, Bossers A, Raymond L, ORourke K, McHolland L, Bryant 3rd P . Evidence of a molecular barrier limiting susceptibility of humans, cattle and sheep to chronic wasting disease. EMBO J. 2000; 19(17):4425-30. PMC: 302048. DOI: 10.1093/emboj/19.17.4425. View

11.

Powers E, Morimoto R, Dillin A, Kelly J, Balch W . Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem. 2009; 78:959-91. DOI: 10.1146/annurev.biochem.052308.114844. View

12.

Falcon B, Zhang W, Murzin A, Murshudov G, Garringer H, Vidal R . Structures of filaments from Pick's disease reveal a novel tau protein fold. Nature. 2018; 561(7721):137-140. PMC: 6204212. DOI: 10.1038/s41586-018-0454-y. View

13.

Castilla J, Saa P, Soto C . Detection of prions in blood. Nat Med. 2005; 11(9):982-5. DOI: 10.1038/nm1286. View

14.

Fitzpatrick A, Falcon B, He S, Murzin A, Murshudov G, Garringer H . Cryo-EM structures of tau filaments from Alzheimer's disease. Nature. 2017; 547(7662):185-190. PMC: 5552202. DOI: 10.1038/nature23002. View

15.

Kocisko D, Come J, Priola S, Chesebro B, Raymond G, Lansbury P . Cell-free formation of protease-resistant prion protein. Nature. 1994; 370(6489):471-4. DOI: 10.1038/370471a0. View

16.

Holmes B, Furman J, Mahan T, Yamasaki T, Mirbaha H, Eades W . Proteopathic tau seeding predicts tauopathy in vivo. Proc Natl Acad Sci U S A. 2014; 111(41):E4376-85. PMC: 4205609. DOI: 10.1073/pnas.1411649111. View

17.

Castilla J, Saa P, Hetz C, Soto C . In vitro generation of infectious scrapie prions. Cell. 2005; 121(2):195-206. DOI: 10.1016/j.cell.2005.02.011. View

18.

Wilham J, Orru C, Bessen R, Atarashi R, Sano K, Race B . Rapid end-point quantitation of prion seeding activity with sensitivity comparable to bioassays. PLoS Pathog. 2010; 6(12):e1001217. PMC: 2996325. DOI: 10.1371/journal.ppat.1001217. View

19.

Kocisko D, Priola S, Raymond G, Chesebro B, Lansbury Jr P, Caughey B . Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc Natl Acad Sci U S A. 1995; 92(9):3923-7. PMC: 42074. DOI: 10.1073/pnas.92.9.3923. View

20.

Meyer V, Dinkel P, Rickman Hager E, Margittai M . Amplification of Tau fibrils from minute quantities of seeds. Biochemistry. 2014; 53(36):5804-9. PMC: 4165214. DOI: 10.1021/bi501050g. View