1887

Abstract

The presence of disease-associated prions in tissues and bodily fluids of chronic wasting disease (CWD)-infected cervids has received much investigation, yet little is known about mother-to-offspring transmission of CWD. Our previous work demonstrated that mother-to-offspring transmission is efficient in an experimental setting. To address the question of relevance in a naturally exposed free-ranging population, we assessed maternal and fetal tissues derived from 19 elk dam–calf pairs collected from free-ranging Rocky Mountain elk from north-central Colorado, a known CWD endemic region. Conventional immunohistochemistry identified three of 19 CWD-positive dams, whereas a more sensitive assay [serial protein misfolding cyclic amplification (sPMCA)] detected CWD prion seeding activity (PrP) in 15 of 19 dams. PrP distribution in tissues was widespread, and included the central nervous system (CNS), lymphoreticular system, and reproductive, secretory, excretory and adipose tissues. Interestingly, five of 15 sPMCA-positive dams showed no evidence of PrP in either CNS or lymphoreticular system, sites typically assessed in diagnosing CWD. Analysis of fetal tissues harvested from the 15 sPMCA-positive dams revealed PrP in 80 % of fetuses (12 of 15), regardless of gestational stage. These findings demonstrated that PrP is more abundant in peripheral tissues of CWD-exposed elk than current diagnostic methods suggest, and that transmission of prions from mother to offspring may contribute to the efficient transmission of CWD in naturally exposed cervid populations.

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2015-11-01
2024-12-08
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References

  1. Aguzzi A., Baumann F., Bremer J. 2008; The prion's elusive reason for being. Annu Rev Neurosci 31:439–477 [View Article][PubMed]
    [Google Scholar]
  2. Andréoletti O., Lacroux C., Chabert A., Monnereau L., Tabouret G., Lantier F., Berthon P., Eychenne F., Lafond-Benestad S., other authors. 2002; PrPSc accumulation in placentas of ewes exposed to natural scrapie: influence of foetal PrP genotype and effect on ewe-to-lamb transmission. J Gen Virol 83:2607–2616 [View Article][PubMed]
    [Google Scholar]
  3. Bencsik A., Debeer S., Petit T., Baron T. 2009; Possible case of maternal transmission of feline spongiform encephalopathy in a captive cheetah. PLoS One 4:e6929 [View Article][PubMed]
    [Google Scholar]
  4. Béringue V., Herzog L., Jaumain E., Reine F., Sibille P., Le Dur A., Vilotte J.L., Laude H. 2012; Facilitated cross-species transmission of prions in extraneural tissue. Science 335:472–475 [View Article][PubMed]
    [Google Scholar]
  5. Bishop M.T., Diack A.B., Ritchie D.L., Ironside J.W., Will R.G., Manson J.C. 2013; Prion infectivity in the spleen of a PRNP heterozygous individual with subclinical variant Creutzfeldt-Jakob disease. Brain 136:1139–1145 [View Article][PubMed]
    [Google Scholar]
  6. Brown P., Will R.G., Bradley R., Asher D.M., Detwiler L. 2001; Bovine spongiform encephalopathy and variant Creutzfeldt-Jakob disease: background, evolution, and current concerns. Emerg Infect Dis 7:6–16 [View Article][PubMed]
    [Google Scholar]
  7. Castilla J., Brun A., Díaz-San Segundo F., Salguero F.J., Gutiérrez-Adán A., Pintado B., Ramírez M.A., del Riego L., Torres J.M. 2005; Vertical transmission of bovine spongiform encephalopathy prions evaluated in a transgenic mouse model. J Virol 79:8665–8668 [View Article][PubMed]
    [Google Scholar]
  8. Di Gangi S., Bertin M., Noventa M., Cagnin A., Cosmi E., Gizzo S. 2015; Obstetric dilemma on the most appropriate management of Creutzfeldt–Jakob disease in pregnancy: seventh case presentation, literature review and new insight. J Matern Fetal Neonatal Med 28:254–261 [View Article][PubMed]
    [Google Scholar]
  9. Dulberger J., Hobbs N.T., Swanson H.M., Bishop C.J., Miller M.W. 2010; Estimating chronic wasting disease effects on mule deer recruitment and population growth. J Wildl Dis 46:1086–1095 [View Article][PubMed]
    [Google Scholar]
  10. Elder A.M., Henderson D.M., Nalls A.V., Wilham J.M., Caughey B.W., Hoover E.A., Kincaid A.E., Bartz J.C., Mathiason C.K. 2013; In vitro detection of prionemia in TSE-infected cervids and hamsters. PLoS One 8:e80203 [View Article][PubMed]
    [Google Scholar]
  11. Foster J.D., Goldmann W., Hunter N. 2013; Evidence in sheep for pre-natal transmission of scrapie to lambs from infected mothers. PLoS One 8:e79433 [View Article][PubMed]
    [Google Scholar]
  12. Gilch S., Chitoor N., Taguchi Y., Stuart M., Jewell J.E., Schätzl H.M. 2011; Chronic wasting disease. Top Curr Chem 305:51–77 [View Article][PubMed]
    [Google Scholar]
  13. Gill O.N., Spencer Y., Richard-Loendt A., Kelly C., Dabaghian R., Boyes L., Linehan J., Simmons M., Webb P., other authors. 2013; Prevalent abnormal prion protein in human appendixes after bovine spongiform encephalopathy epizootic: large scale survey. BMJ 347:f5675 [View Article][PubMed]
    [Google Scholar]
  14. Haley N.J., Mathiason C.K., Carver S., Telling G.C., Zabel M.D., Hoover E.A. 2012; Sensitivity of protein misfolding cyclic amplification versus immunohistochemistry in ante-mortem detection of chronic wasting disease. J Gen Virol 93:1141–1150 [View Article][PubMed]
    [Google Scholar]
  15. Hill A.F., Collinge J. 2003; Subclinical prion infection in humans and animals. Br Med Bull 66:161–170 [View Article][PubMed]
    [Google Scholar]
  16. Hill A.F., Desbruslais M., Joiner S., Sidle K.C., Gowland I., Collinge J., Doey L.J., Lantos P. 1997; The same prion strain causes vCJD and BSE. Nature 389:448–450, 526 [View Article][PubMed]
    [Google Scholar]
  17. Ironside J.W., Head M.W., Bell J.E., McCardle L., Will R.G. 2000; Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1–9 [View Article][PubMed]
    [Google Scholar]
  18. Joly D.O., Samuel M.D., Langenberg J.A., Rolley R.E., Keane D.P. 2009; Surveillance to detect chronic wasting disease in white-tailed deer in Wisconsin. J Wildl Dis 45:989–997 [View Article][PubMed]
    [Google Scholar]
  19. Lacroux C., Comoy E., Moudjou M., Perret-Liaudet A., Lugan S., Litaise C., Simmons H., Jas-Duval C., Lantier I., other authors. 2014; Preclinical detection of variant CJD and BSE prions in blood. PLoS Pathog 10:e1004202 [View Article][PubMed]
    [Google Scholar]
  20. Makzhami S., Passet B., Halliez S., Castille J., Moazami-Goudarzi K., Duchesne A., Vilotte M., Laude H., Mouillet-Richard S., other authors. 2014; The prion protein family: a view from the placenta. Front Cell Dev Biol 2:35 [View Article][PubMed]
    [Google Scholar]
  21. Mathiason C.K., Powers J.G., Dahmes S.J., Osborn D.A., Miller K.V., Warren R.J., Mason G.L., Hays S.A., Hayes-Klug J., other authors. 2006; Infectious prions in the saliva and blood of deer with chronic wasting disease. Science 314:133–136 [View Article][PubMed]
    [Google Scholar]
  22. Meyerett C., Michel B., Pulford B., Spraker T.R., Nichols T.A., Johnson T., Kurt T., Hoover E.A., Telling G.C., Zabel M.D. 2008; In vitro strain adaptation of CWD prions by serial protein misfolding cyclic amplification. Virology 382:267–276 [View Article][PubMed]
    [Google Scholar]
  23. Miller M.W., Williams E.S. 2004; Chronic wasting disease of cervids. Curr Top Microbiol Immunol 284:193–214[PubMed]
    [Google Scholar]
  24. Monello R.J., Powers J.G., Hobbs N.T., Spraker T.R., O'Rourke K.I., Wild M.A. 2013; Efficacy of antemortem rectal biopsies to diagnose and estimate prevalence of chronic wasting disease in free-ranging cow elk (Cervus elaphus nelsoni). J Wildl Dis 49:270–278 [View Article][PubMed]
    [Google Scholar]
  25. Monello R.J., Powers J.G., Hobbs N.T., Spraker T.R., Watry M.K., Wild M.A. 2014; Survival and population growth of a free-ranging elk population with a long history of exposure to chronic wasting disease. J Wildl Manage 78:214–223 [View Article]
    [Google Scholar]
  26. Nalls A.V., McNulty E., Powers J., Seelig D.M., Hoover C., Haley N.J., Hayes-Klug J., Anderson K., Stewart P., other authors. 2013; Mother to offspring transmission of chronic wasting disease in Reeves' muntjac deer. PLoS One 8:e71844 [View Article][PubMed]
    [Google Scholar]
  27. Nichols T.A., Pulford B., Wyckoff A.C., Meyerett C., Michel B., Gertig K., Hoover E.A., Jewell J.E., Telling G.C., Zabel M.D. 2009; Detection of protease-resistant cervid prion protein in water from a CWD-endemic area. Prion 3:171–183 [View Article][PubMed]
    [Google Scholar]
  28. Notari S., Moleres F.J., Hunter S.B., Belay E.D., Schonberger L.B., Cali I., Parchi P., Shieh W.J., Brown P., other authors. 2010; Multiorgan detection and characterization of protease-resistant prion protein in a case of variant CJD examined in the United States. PLoS One 5:e8765 [View Article][PubMed]
    [Google Scholar]
  29. Peralta O.A., Eyestone W.H. 2009; Quantitative and qualitative analysis of cellular prion protein (PrPC) expression in bovine somatic tissues. Prion 3:161–170 [View Article][PubMed]
    [Google Scholar]
  30. Peralta O.A., Huckle W.R., Eyestone W.H. 2012; Developmental expression of the cellular prion protein (PrPC) in bovine embryos. Mol Reprod Dev 79:488–498 [View Article][PubMed]
    [Google Scholar]
  31. Prusiner S.B. 1982; Novel proteinaceous infectious particles cause scrapie. Science 216:136–144 [View Article][PubMed]
    [Google Scholar]
  32. Race R., Jenny A., Sutton D. 1998; Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen, and lymph node: implications for transmission and antemortem diagnosis. J Infect Dis 178:949–953 [View Article][PubMed]
    [Google Scholar]
  33. Reed J., Muench H. 1938; A simple method of estimating fifty per cent end points. Am J Hygiene 27:493–497
    [Google Scholar]
  34. Saá P., Castilla J., Soto C. 2006; Ultra-efficient replication of infectious prions by automated protein misfolding cyclic amplification. J Biol Chem 281:35245–35252 [View Article][PubMed]
    [Google Scholar]
  35. Sakudo A., Onodera T. 2014; Prion protein (PrP) gene-knockout cell lines: insight into functions of the PrP. Front Cell Dev Biol 2:75[PubMed]
    [Google Scholar]
  36. Sargeant G.A., Weber D.C., Roddy D.E. 2011; Implications of chronic wasting disease, cougar predation, and reduced recruitment for elk management. J Wildl Manage 75:171–177 [View Article]
    [Google Scholar]
  37. Saunders S.E., Bartelt-Hunt S.L., Bartz J.C. 2012; Occurrence, transmission, and zoonotic potential of chronic wasting disease. Emerg Infect Dis 18:369–376 [View Article][PubMed]
    [Google Scholar]
  38. Sigurdson C.J., Aguzzi A. 2007; Chronic wasting disease. Biochim Biophys Acta 1772:610–618 [View Article][PubMed]
    [Google Scholar]
  39. Spiropoulos J., Hawkins S.A., Simmons M.M., Bellworthy S.J. 2014; Evidence of in utero transmission of classical scrapie in sheep. J Virol 88:4591–4594 [View Article][PubMed]
    [Google Scholar]
  40. Spraker T.R., VerCauteren K.C., Gidlewski T., Schneider D.A., Munger R., Balachandran A., O'Rourke K.I. 2009; Antemortem detection of PrPCWD in preclinical, ranch-raised Rocky Mountain elk (Cervus elaphus nelsoni) by biopsy of the rectal mucosa. J Vet Diagn Invest 21:15–24 [View Article][PubMed]
    [Google Scholar]
  41. Wells G.A., Wilesmith J.W., McGill I.S. 1991; Bovine spongiform encephalopathy: a neuropathological perspective. Brain Pathol 1:69–78 [View Article][PubMed]
    [Google Scholar]
  42. Williams E.S., Miller M.W. 2002; Chronic wasting disease in deer and elk in North America. Rev Sci Tech 21:305–316[PubMed]
    [Google Scholar]
  43. Wooding F.B., Morgan G., Adam C.L. 1997; Structure and function in the ruminant synepitheliochorial placenta: central role of the trophoblast binucleate cell in deer. Microsc Res Tech 38:88–99 [View Article][PubMed]
    [Google Scholar]
  44. Wyckoff A.C., Lockwood K.L., Meyerett-Reid C., Michel B.A., Bender H., VerCauteren K.C., Zabel M.D. 2013; Estimating prion adsorption capacity of soil by BioAssay of Subtracted Infectivity from Complex Solutions (BASICS). PLoS One 8:e58630 [View Article][PubMed]
    [Google Scholar]
  45. Wyckoff A.C., Galloway N., Meyerett-Reid C., Powers J., Spraker T., Monello R.J., Pulford B., Wild M., Antolin M., other authors. 2015; Prion amplification and hierarchical Bayesian modeling refine detection of prion infection. Sci Rep 5:8358 [View Article][PubMed]
    [Google Scholar]
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