1887

Abstract

Bovine spongiform encephalopathy (BSE) prion is more resistant to heat inactivation compared to other prions, but the effect of heat inactivation has been reported to differ depending on the BSE-contaminated tissue state or heating type. We aimed to evaluate the secure level of inactivation of original BSE transmissibility by dry-heating. Cattle tissues affected with BSE were subjected to dry-heat treatment for 20 min at various temperatures ranging from 150 to 1000 °C. To assess the inactivation effect, we conducted protein misfolding cyclic amplification (PMCA) and follicular dendritic cell (FDC) assays in transgenic mice expressing bovine prion protein genes. Under dry-heating at 600 °C or higher, BSE cattle tissues lost their transmissibility in transgenic mice. In contrast, transmissibility was detected in the cattle tissues treated at temperatures of 400 °C or lower through the FDC assay combined with PMCA. In this study, we confirmed that transmissibility was eliminated in BSE-affected cattle tissues by dry-heating at 600 °C or higher.

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2020-01-01
2024-05-08
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References

  1. Prusiner SB. Prions. Proc Natl Acad Sci USA 1998; 95:13363–13383 [View Article]
    [Google Scholar]
  2. Legname G, Baskakov IV, Nguyen H-OB, Riesner D, Cohen FE et al. Synthetic mammalian prions. Science 2004; 305:673–676 [View Article]
    [Google Scholar]
  3. Buschmann A, Groschup MH. Highly bovine spongiform encephalopathy-sensitive transgenic mice confirm the essential restriction of infectivity to the nervous system in clinically diseased cattle. J Infect Dis 2005; 192:934–942 [View Article]
    [Google Scholar]
  4. Balkema-Buschmann A, Eiden M, Hoffmann C, Kaatz M, Ziegler U et al. BSE infectivity in the absence of detectable PrPSc accumulation in the tongue and nasal mucosa of terminally diseased cattle. J Gen Virol 2011; 92:467–476 [View Article]
    [Google Scholar]
  5. Hoffmann C, Eiden M, Kaatz M, Keller M, Ziegler U et al. Bse infectivity in jejunum, ileum and ileocaecal junction of incubating cattle. Vet Res 2011; 42:21 [View Article]
    [Google Scholar]
  6. Franz M, Eiden M, Balkema-Buschmann A, Greenlee J, Schatzl H et al. Detection of PrPSc in peripheral tissues of clinically affected cattle after oral challenge with bovine spongiform encephalopathy. J Gen Virol 2012; 93:2740–2748 [View Article]
    [Google Scholar]
  7. Taylor DM, Fraser H, McConnell I, Brown DA, Brown KL et al. Decontamination studies with the agents of bovine spongiform encephalopathy and scrapie. Arch Virol 1994; 139:313–326 [View Article]
    [Google Scholar]
  8. Wilesmith JW, Ryan JB, Atkinson MJ. Bovine spongiform encephalopathy: epidemiological studies on the origin. Vet Rec 1991; 128:199–203 [View Article]
    [Google Scholar]
  9. Maluquer de Motes C, Espinosa JC, Esteban A, Calvo M, Girones R et al. Persistence of the bovine spongiform encephalopathy infectious agent in sewage. Environ Res 2012; 117:1–7 [View Article]
    [Google Scholar]
  10. Marín-Moreno A, Espinosa JC, Fernández-Borges N, Píquer J, Girones R et al. An assessment of the long-term persistence of prion infectivity in aquatic environments. Environ Res 2016; 151:587–594 [View Article]
    [Google Scholar]
  11. Jacobson KH, Lee S, McKenzie D, Benson CH, Pedersen JA. Transport of the pathogenic prion protein through landfill materials. Environ Sci Technol 2009; 43:2022–2028 [View Article]
    [Google Scholar]
  12. Jacobson KH, Lee S, Somerville RA, McKenzie D, Benson CH et al. Transport of the pathogenic prion protein through soils. J Environ Qual 2010; 39:1145–1152 [View Article]
    [Google Scholar]
  13. Somerville RA, Fernie K, Smith A, Bishop K, Maddison BC et al. Bse infectivity survives burial for five years with only limited spread. Arch Virol 2019; 164:1135–1145 [View Article]
    [Google Scholar]
  14. Brown P, Rau EH, Lemieux P, Johnson BK, Bacote AE et al. Infectivity studies of both ash and air emissions from simulated incineration of scrapie-contaminated tissues. Environ Sci Technol 2004; 38:6155–6160 [View Article]
    [Google Scholar]
  15. Taylor DM, McConnell I, Fernie K. The effect of dry heat on the ME7 strain of mouse-passaged scrapie agent. J Gen Virol 1996; 77:3161–3164 [View Article]
    [Google Scholar]
  16. Taylor DM, Fernie K, McConnell I, Steele PJ. Observations on thermostable subpopulations of the unconventional agents that cause transmissible degenerative encephalopathies. Vet Microbiol 1998; 64:33–38 [View Article]
    [Google Scholar]
  17. Taylor DM. Inactivation of prions by physical and chemical means. J Hosp Infect 1999; 43:S69–S76 [View Article]
    [Google Scholar]
  18. Somerville RA, Oberthür RC, Havekost U, MacDonald F, Taylor DM et al. Characterization of thermodynamic diversity between transmissible spongiform encephalopathy agent strains and its theoretical implications. J Biol Chem 2002; 277:11084–11089 [View Article]
    [Google Scholar]
  19. Somerville RA, Gentles N. Characterization of the effect of heat on agent strains of the transmissible spongiform encephalopathies. J Gen Virol 2011; 92:1738–1748 [View Article]
    [Google Scholar]
  20. Schreuder BE, Geertsma RE, van Keulen LJ, van Asten JA, Enthoven P et al. Studies on the efficacy of hyperbaric rendering procedures in inactivating bovine spongiform encephalopathy (BSE) and scrapie agents. Vet Rec 1998; 142:474–480 [View Article]
    [Google Scholar]
  21. Taylor DM, Fernie K, Steele PJ, McConnell I, Somerville RA. Thermostability of mouse-passaged BSE and scrapie is independent of host PrP genotype: implications for the nature of the causal agents. J Gen Virol 2002; 83:3199–3204 [View Article]
    [Google Scholar]
  22. Fernie K, Steele PJ, Taylor DM, Somerville RA. Comparative studies on the thermostability of five strains of transmissible-spongiform-encephalopathy agent. Biotechnol Appl Biochem 2007; 47:175 [View Article]
    [Google Scholar]
  23. Giles K, Glidden DV, Beckwith R, Seoanes R, Peretz D et al. Resistance of bovine spongiform encephalopathy (BSE) prions to inactivation. PLoS Pathog 2008; 4:e1000206 [View Article]
    [Google Scholar]
  24. Matsuura Y, Ishikawa Y, Bo X, Murayama Y, Yokoyama T et al. Quantitative analysis of wet-heat inactivation in bovine spongiform encephalopathy. Biochem Biophys Res Commun 2013; 432:86–91 [View Article]
    [Google Scholar]
  25. Yoshioka M, Matsuura Y, Okada H, Shimozaki N, Yamamura T et al. Rapid assessment of bovine spongiform encephalopathy prion inactivation by heat treatment in yellow grease produced in the industrial manufacturing process of meat and bone meals. BMC Vet Res 2013; 9:134 [View Article]
    [Google Scholar]
  26. Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 2001; 411:810–813 [View Article]
    [Google Scholar]
  27. Murayama Y, Yoshioka M, Masujin K, Okada H, Iwamaru Y et al. Sulfated dextrans enhance in vitro amplification of bovine spongiform encephalopathy PrPSc and enable ultrasensitive detection of bovine PrPSc . PLoS One 2010; 5:e13152–10 [View Article]
    [Google Scholar]
  28. Matsuura Y, Ishikawa Y, Somerville RA, Yokoyama T, Hagiwara Ken’ichi et al. A rapid bioassay for classical and L-type bovine spongiform encephalopathies. Open J Vet Med 2013; 03:79–85 [View Article]
    [Google Scholar]
  29. Murayama Y, Yoshioka M, Horii H, Takata M, Yokoyama T et al. Protein misfolding cyclic amplification as a rapid test for assessment of prion inactivation. Biochem Biophys Res Commun 2006; 348:758–762 [View Article]
    [Google Scholar]
  30. Shimizu Y, Kaku-Ushiki Y, Iwamaru Y, Muramoto T, Kitamoto T et al. A novel anti-prion protein monoclonal antibody and its single-chain fragment variable derivative with ability to inhibit abnormal prion protein accumulation in cultured cells. Microbiol Immunol 2010; 54:112–121 [View Article]
    [Google Scholar]
  31. Kitamoto T, Mohri S, Ironside JW, Miyoshi I, Tanaka T et al. Follicular dendritic cell of the knock-in mouse provides a new bioassay for human prions. Biochem Biophys Res Commun 2002; 294:280–286 [View Article]
    [Google Scholar]
  32. Imamura M, Tabeta N, Kato N, Matsuura Y, Iwamaru Y et al. Heparan sulfate and heparin promote faithful prion replication in Vitro by binding to normal and abnormal prion proteins in protein misfolding cyclic amplification. J Biol Chem 2016; 291:26478–26486 [View Article]
    [Google Scholar]
  33. Murayama Y, Yoshioka M, Okada H, Takata E, Masujin K et al. Subcritical water hydrolysis effectively reduces the in Vitro seeding activity of PrPSc but fails to inactivate the infectivity of bovine spongiform encephalopathy prions. PLoS One 2015; 10:e0144761 [View Article]
    [Google Scholar]
  34. Brown P, Rau EH, Johnson BK, Bacote AE, Gibbs CJ et al. New studies on the heat resistance of hamster-adapted scrapie agent: threshold survival after ashing at 600 degrees C suggests an inorganic template of replication. Proc Natl Acad Sci USA 2000; 97:3418–3421 [View Article]
    [Google Scholar]
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