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Volume 98, Issue 2

Increased circulating microRNAs miR-342-3p and miR-21-5p in natural sheep prion disease Free

Abstract

Scrapie is a transmissible spongiform encephalopathy (TSE), or prion disease, of sheep and goats. As no simple diagnostic tests are yet available to detect TSEs , easily accessible biomarkers could facilitate the eradication of scrapie agents from the food chain. To this end, we analysed by quantitative reverse transcription PCR a selected set of candidate microRNAs (miRNAs) from circulating blood plasma of naturally infected, classical scrapie sheep that demonstrated clear scrapie symptoms and pathology. Significant scrapie-associated increase was repeatedly found for miR-342-3p and miR-21-5p. This is the first demonstration, to our knowledge, of circulating miRNA alterations in any animal suffering from TSE. Genome-wide expression studies are warranted to investigate the true depth of miRNA alterations in naturally occurring TSEs, especially in presymptomatic animals, as the presented study demonstrates the potential feasibility of miRNAs as circulating TSE biomarkers.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): biomarker , microRNA , neurodegeneration , prion disease , scrapie and transmissible spongiform encephalopathies
© 2017 The Authors
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2017-02-01
2024-04-24
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References

  1. Colby DW, Prusiner SB. Prions. Cold Spring Harb Perspect Biol 2011; 3:a006833 [View Article][PubMed]
     [Google Scholar]
  2. Cassard H, Torres JM, Lacroux C, Douet JY, Benestad SL et al. Evidence for zoonotic potential of ovine scrapie prions. Nat Commun 2014; 5:5821 [View Article][PubMed]
     [Google Scholar]
  3. Comoy EE, Mikol J, Luccantoni-Freire S, Correia E, Lescoutra-Etchegaray N et al. Transmission of scrapie prions to primate after an extended silent incubation period. Sci Rep 2015; 5:11573 [View Article][PubMed]
     [Google Scholar]
  4. EFSA Panel on Biological Hazards Scientific Opinion on the scrapie situation in the EU after 10 years of monitoring and control in sheep and goats. EFSA Journal 2014; 12:3781 [CrossRef]
     [Google Scholar]
  5. Kübler E, Oesch B, Raeber AJ. Diagnosis of prion diseases. Br Med Bull 2003; 66:267–279 [View Article][PubMed]
     [Google Scholar]
  6. Béringue V, Herzog L, Jaumain E, Reine F, Sibille P et al. Facilitated cross-species transmission of prions in extraneural tissue. Science 2012; 335:472–475 [View Article][PubMed]
     [Google Scholar]
  7. Andréoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J et al. Early accumulation of PrP(Sc) in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J Gen Virol 2000; 81:3115–3126 [View Article][PubMed]
     [Google Scholar]
  8. Schreuder BE, van Keulen LJ, Vromans ME, Langeveld JP, Smits MA. Tonsillar biopsy and PrPSc detection in the preclinical diagnosis of scrapie. Vet Rec 1998; 142:564–568 [View Article][PubMed]
     [Google Scholar]
  9. Andréoletti O, Orge L, Benestad SL, Beringue V, Litaise C et al. Atypical/Nor98 scrapie infectivity in sheep peripheral tissues. PLoS Pathog 2011; 7:e1001285 [View Article][PubMed]
     [Google Scholar]
  10. Hruska-Plochan M, Li B, Kyburz D, Krützfeld J, Landmesser U et al. New and emerging roles of small RNAs in neurodegeneration, muscle, cardiovascular and inflammatory diseases. Swiss Med Wkly 2015; 145:w14192 [View Article][PubMed]
     [Google Scholar]
  11. Hébert SS, De Strooper B. Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci 2009; 32:199–206 [View Article][PubMed]
     [Google Scholar]
  12. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105:10513–10518 [View Article][PubMed]
     [Google Scholar]
  13. Gibbings D, Leblanc P, Jay F, Pontier D, Michel F et al. Human prion protein binds Argonaute and promotes accumulation of microRNA effector complexes. Nat Struct Mol Biol 2012; 19:517–524 [View Article][PubMed]
     [Google Scholar]
  14. Saba R, Goodman CD, Huzarewich RL, Robertson C, Booth SA. A miRNA signature of prion induced neurodegeneration. PLoS One 2008; 3:e3652 [View Article][PubMed]
     [Google Scholar]
  15. Saba R, Gushue S, Huzarewich RL, Manguiat K, Medina S et al. MicroRNA 146a (miR-146a) is over-expressed during prion disease and modulates the innate immune response and the microglial activation state. PLoS One 2012; 7:e30832 [View Article][PubMed]
     [Google Scholar]
  16. Montag J, Hitt R, Opitz L, Schulz-Schaeffer WJ, Hunsmann G et al. Upregulation of miRNA hsa-miR-342-3p in experimental and idiopathic prion disease. Mol Neurodegener 2009; 4:36 [View Article][PubMed]
     [Google Scholar]
  17. Lukiw WJ, Dua P, Pogue AI, Eicken C, Hill JM. Upregulation of micro RNA-146a (miRNA-146a), a marker for inflammatory neurodegeneration, in sporadic Creutzfeldt–Jakob disease (sCJD) and Gerstmann–Straussler–Scheinker (GSS) syndrome. J Toxicol Environ Health A 2011; 74:1460–1468 [View Article][PubMed]
     [Google Scholar]
  18. Boese AS, Saba R, Campbell K, Majer A, Medina S et al. MicroRNA abundance is altered in synaptoneurosomes during prion disease. Mol Cell Neurosci 2016; 71:13–24 [View Article][PubMed]
     [Google Scholar]
  19. Majer A, Medina SJ, Niu Y, Abrenica B, Manguiat KJ et al. Early mechanisms of pathobiology are revealed by transcriptional temporal dynamics in hippocampal CA1 neurons of prion infected mice. PLoS Pathog 2012; 8:e1003002 [View Article][PubMed]
     [Google Scholar]
  20. Bellingham SA, Coleman BM, Hill AF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res 2012; 40:10937–10949 [View Article][PubMed]
     [Google Scholar]
  21. Acín C, Martín-Burriel I, Goldmann W, Lyahyai J, Monzón M et al. Prion protein gene polymorphisms in healthy and scrapie-affected Spanish sheep. J Gen Virol 2004; 85:2103–2110 [View Article][PubMed]
     [Google Scholar]
  22. Chim SS, Shing TK, Hung EC, Leung TY, Lau TK et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem 2008; 54:482–490 [View Article][PubMed]
     [Google Scholar]
  23. Houston F, Goldmann W, Foster J, González L, Jeffrey M et al. Comparative susceptibility of sheep of different origins, breeds and PRNP genotypes to challenge with bovine spongiform encephalopathy and scrapie. PLoS One 2015; 10:e0143251 [View Article][PubMed]
     [Google Scholar]
  24. Filali H, Martin-Burriel I, Harders F, Varona L, Lyahyai J et al. Gene expression profiling and association with prion-related lesions in the medulla oblongata of symptomatic natural scrapie animals. PLoS One 2011; 6:e19909 [View Article][PubMed]
     [Google Scholar]
  25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001; 25:402–408 [View Article][PubMed]
     [Google Scholar]
  26. Arsac JN, Baron T. Distinct transmissibility features of TSE sources derived from ruminant prion diseases by the oral route in a transgenic mouse model (TgOvPrP4) overexpressing the ovine prion protein. PLoS One 2014; 9:e96215 [View Article][PubMed]
     [Google Scholar]
  27. Langevin C, Andréoletti O, Le Dur A, Laude H, Béringue V. Marked influence of the route of infection on prion strain apparent phenotype in a scrapie transgenic mouse model. Neurobiol Dis 2011; 41:219–225 [View Article][PubMed]
     [Google Scholar]
  28. Saugstad JA. MicroRNAs as effectors of brain function with roles in ischemia and injury, neuroprotection, and neurodegeneration. J Cereb Blood Flow Metab 2010; 30:1564–1576 [View Article][PubMed]
     [Google Scholar]
  29. Sheedy FJ. Turning 21: induction of miR-21 as a key switch in the inflammatory response. Front Immunol 2015; 6:19 [View Article][PubMed]
     [Google Scholar]
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Increased circulating microRNAs miR-342-3p and miR-21-5p in natural sheep prion disease
J. Gen. Virol. 98, 305 (2017); https://doi.org/10.1099/jgv.0.000685
/content/journal/jgv/10.1099/jgv.0.000685
/content/journal/jgv/10.1099/jgv.0.000685
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