Atypical/Nor98 Scrapie Infectivity in Sheep Peripheral Tissues
Atypical/Nor98 scrapie was first identified in 1998 in Norway. It is now considered as a worldwide disease of small ruminants and currently represents a significant part of the detected transmissible spongiform encephalopathies (TSE) cases in Europe. Atypical/Nor98 scrapie cases were reported in ARR/ARR sheep, which are highly resistant to BSE and other small ruminants TSE agents. The biology and pathogenesis of the Atypical/Nor98 scrapie agent in its natural host is still poorly understood. However, based on the absence of detectable abnormal PrP in peripheral tissues of affected individuals, human and animal exposure risk to this specific TSE agent has been considered low. In this study we demonstrate that infectivity can accumulate, even if no abnormal PrP is detectable, in lymphoid tissues, nerves, and muscles from natural and/or experimental Atypical/Nor98 scrapie cases. Evidence is provided that, in comparison to other TSE agents, samples containing Atypical/Nor98 scrapie infectivity could remain PrPSc negative. This feature will impact detection of Atypical/Nor98 scrapie cases in the field, and highlights the need to review current evaluations of the disease prevalence and potential transmissibility. Finally, an estimate is made of the infectivity loads accumulating in peripheral tissues in both Atypical/Nor98 and classical scrapie cases that currently enter the food chain. The results obtained indicate that dietary exposure risk to small ruminants TSE agents may be higher than commonly believed.
Vyšlo v časopise:
Atypical/Nor98 Scrapie Infectivity in Sheep Peripheral Tissues. PLoS Pathog 7(2): e32767. doi:10.1371/journal.ppat.1001285
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001285
Souhrn
Atypical/Nor98 scrapie was first identified in 1998 in Norway. It is now considered as a worldwide disease of small ruminants and currently represents a significant part of the detected transmissible spongiform encephalopathies (TSE) cases in Europe. Atypical/Nor98 scrapie cases were reported in ARR/ARR sheep, which are highly resistant to BSE and other small ruminants TSE agents. The biology and pathogenesis of the Atypical/Nor98 scrapie agent in its natural host is still poorly understood. However, based on the absence of detectable abnormal PrP in peripheral tissues of affected individuals, human and animal exposure risk to this specific TSE agent has been considered low. In this study we demonstrate that infectivity can accumulate, even if no abnormal PrP is detectable, in lymphoid tissues, nerves, and muscles from natural and/or experimental Atypical/Nor98 scrapie cases. Evidence is provided that, in comparison to other TSE agents, samples containing Atypical/Nor98 scrapie infectivity could remain PrPSc negative. This feature will impact detection of Atypical/Nor98 scrapie cases in the field, and highlights the need to review current evaluations of the disease prevalence and potential transmissibility. Finally, an estimate is made of the infectivity loads accumulating in peripheral tissues in both Atypical/Nor98 and classical scrapie cases that currently enter the food chain. The results obtained indicate that dietary exposure risk to small ruminants TSE agents may be higher than commonly believed.
Zdroje
1. McKinleyMP
BoltonDC
PrusinerSB
1983 A protease-resistant protein is a structural component of the scrapie prion. Cell 35 57 62
2. PrusinerSB
1982 Novel proteinaceous infectious particles cause scrapie. Science 216 136 144
3. CollingeJ
SidleKC
MeadsJ
IronsideJ
HillAF
1996 Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature 383 685 690
4. BruceME
WillRG
IronsideJW
McConnellI
DrummondD
1997 Transmissions to mice indicate that ‘new variant’ CJD is caused by the BSE agent. Nature 389 498 501
5. BenestadSL
SarradinP
ThuB
SchonheitJ
TranulisMA
2003 Cases of scrapie with unusual features in Norway and designation of a new type, Nor98. Vet Rec 153 202 208
6. BenestadSL
ArsacJN
GoldmannW
NoremarkM
2008 Atypical/Nor98 scrapie: properties of the agent, genetics, and epidemiology. Vet Res 39 19
7. Le DurA
BeringueV
AndreolettiO
ReineF
LaiTL
2005 A newly identified type of scrapie agent can naturally infect sheep with resistant PrP genotypes. Proc Natl Acad Sci U S A 102 16031 16036
8. SimmonsMM
KonoldT
SimmonsHA
SpencerYI
LockeyR
2007 Experimental transmission of atypical scrapie to sheep. BMC Vet Res 3 20
9. SimmonsMM
KonoldT
ThurstonL
BellworthySJ
ChaplinMJ
2010 The natural atypical scrapie phenotype is preserved on experimental transmission and sub-passage in PRNP homologous sheep. BMC Vet Res 6 14
10. FediaevskyA
TongueSC
NoremarkM
CalavasD
RuG
2008 A descriptive study of the prevalence of atypical and classical scrapie in sheep in 20 European countries. BMC Vet Res 4 19
11. ElsenJM
AmiguesY
SchelcherF
DucrocqV
AndreolettiO
1999 Genetic susceptibility and transmission factors in scrapie: detailed analysis of an epidemic in a closed flock of Romanov. Arch Virol 144 431 445
12. HunterN
GoldmannW
FosterJD
CairnsD
SmithG
1997 Natural scrapie and PrP genotype: case-control studies in British sheep. Vet Rec 141 137 140
13. JeffreyM
MartinS
ThomsonJR
DingwallWS
Begara-McGorumI
2001 Onset and distribution of tissue prp accumulation in scrapie-affected suffolk sheep as demonstrated by sequential necropsies and tonsillar biopsies. J Comp Pathol 125 48 57
14. ArsacJN
AndreolettiO
BilheudeJM
LacrouxC
BenestadSL
2007 Similar biochemical signatures and prion protein genotypes in atypical scrapie and Nor98 cases, France and Norway. Emerg Infect Dis 13 58 65
15. MorenoCR
Moazami-GoudarziK
LaurentP
CazeauG
AndreolettiO
2007 Which PrP haplotypes in a French sheep population are the most susceptible to atypical scrapie? Arch Virol 152 1229 1232
16. SaundersGC
CawthrawS
MountjoySJ
HopeJ
WindlO
2006 PrP genotypes of atypical scrapie cases in Great Britain. J Gen Virol 87 3141 3149
17. LuhkenG
BuschmannA
BrandtH
EidenM
GroschupMH
2007 Epidemiological and genetical differences between classical and atypical scrapie cases. Vet Res 38 65 80
18. LuhkenG
BuschmannA
GroschupMH
ErhardtG
2004 Prion protein allele A136 H154Q171 is associated with high susceptibility to scrapie in purebred and crossbred German Merinoland sheep. Arch Virol 149 1571 1580
19. BuschmannA
LuhkenG
SchultzJ
ErhardtG
GroschupMH
2004 Neuronal accumulation of abnormal prion protein in sheep carrying a scrapie-resistant genotype (PrPARR/ARR). J Gen Virol 85 2727 2733
20. NentwigA
OevermannA
HeimD
BotteronC
ZellwegerK
2007 Diversity in neuroanatomical distribution of abnormal prion protein in atypical scrapie. PLoS Pathog 3 e82
21. VidalE
TortosaR
CostaC
BenavidesJ
FrancinoO
2008 Lack of PrP(sc) immunostaining in intracranial ectopic lymphoid follicles in a sheep with concomitant non-suppurative encephalitis and Nor98-like atypical scrapie: a case report. Vet J 177 283 288
22. RaceR
RainesA
RaymondGJ
CaugheyB
ChesebroB
2001 Long-term subclinical carrier state precedes scrapie replication and adaptation in a resistant species: analogies to bovine spongiform encephalopathy and variant creutzfeldt-jakob disease in humans. J Virol 75 10106 10112
23. LasmezasCI
DeslysJP
RobainO
JaeglyA
BeringueV
1997 Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275 402 405
24. GriffithsPC
SpiropoulosJ
LockeyR
ToutAC
JayasenaD
2010 Characterisation of atypical scrapie cases from Great Britain in transgenic ovine PrP mice. J Gen Virol 91 2132 8
25. AndreolettiO
BerthonP
MarcD
SarradinP
GrosclaudeJ
2000 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 81 Pt 12 3115 3126
26. AndreolettiO
SimonS
LacrouxC
MorelN
TabouretG
2004 PrPSc accumulation in myocytes from sheep incubating natural scrapie. Nat Med 10 591 593
27. HadlowWJ
KennedyRC
RaceRE
1982 Natural infection of Suffolk sheep with scrapie virus. J Infect Dis 146 657 664
28. LacrouxC
CorbiereF
TabouretG
LuganS
CostesP
2007 Dynamics and genetics of PrPSc placental accumulation in sheep. J Gen Virol 88 1056 1061
29. DickinsonAG
FraserH
1969 Genetical control of the concentration of ME7 scrapie agent in mouse spleen. J Comp Pathol 79 363 366
30. DickinsonAG
MeikleVM
FraserH
1969 Genetical control of the concentration of ME7 scrapie agent in the brain of mice. J Comp Pathol 79 15 22
31. PrusinerSB
CochranSP
GrothDF
DowneyDE
BowmanKA
1982 Measurement of the scrapie agent using an incubation time interval assay. Ann Neurol 11 353 358
32. LacrouxC
SimonS
BenestadSL
MailletS
MatheyJ
2008 Prions in milk from ewes incubating natural scrapie. PLoS Pathog 4 e1000238
33. HeikenwalderM
FederauC
BoehmerL
SchwarzP
WagnerM
2007 Germinal center B cells are dispensable in prion transport and neuroinvasion. J Neuroimmunol 192 113 123
34. TixadorP
HerzogL
ReineF
JaumainE
ChapuisJ
2010 The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog 15 6 4 e1000859
35. van KeulenLJ
SchreuderBE
VromansME
LangeveldJP
SmitsMA
2000 Pathogenesis of natural scrapie in sheep. Arch Virol Suppl 16 57 71
36. van KeulenLJ
VromansME
DolstraCH
BossersA
van ZijderveldFG
2008 Pathogenesis of bovine spongiform encephalopathy in sheep. Arch Virol 153 445 453
37. van KeulenLJ
VromansME
van ZijderveldFG
2002 Early and late pathogenesis of natural scrapie infection in sheep. Apmis 110 23 32
38. FediaevskyA
MaurellaC
NoremarkM
IngravalleF
ThorgeirsdottirS
2010 The prevalence of atypical scrapie in sheep from positive flocks is not higher than in the general sheep population in 11 European countries. BMC Vet Res 6 9
39. FediaevskyA
MorignatE
DucrotC
CalavasD
2009 A case-control study on the origin of atypical scrapie in sheep, France. Emerg Infect Dis 15 710 718
40. BuschmannA
GroschupMH
2005 TSE eradication in small ruminants—quo vadis? Berl Munch Tierarztl Wochenschr 118 365 371
41. WellsGA
SpiropoulosJ
HawkinsSA
RyderSJ
2005 Pathogenesis of experimental bovine spongiform encephalopathy: preclinical infectivity in tonsil and observations on the distribution of lingual tonsil in slaughtered cattle. Vet Rec 156 401 407
42. WellsGA
2003 Pathogenesis of BSE. Vet Res Commun 27 Suppl 1 25 28
43. TerryLA
MarshS
RyderSJ
HawkinsSA
WellsGA
2003 Detection of disease-specific PrP in the distal ileum of cattle exposed orally to the agent of bovine spongiform encephalopathy. Vet Rec 152 387 392
44. AndreolettiO
BerthonP
LevavasseurE
MarcD
LantierF
2002 Phenotyping of protein-prion (PrPsc)-accumulating cells in lymphoid and neural tissues of naturally scrapie-affected sheep by double-labeling immunohistochemistry. J Histochem Cytochem 50 1357 1370
45. van KeulenLJ
SchreuderBE
MeloenRH
Mooij-HarkesG
VromansME
1996 Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J Clin Microbiol 34 1228 1231
46. HoffmannC
ZieglerU
BuschmannA
WeberA
KupferL
2007 Prions spread via the autonomic nervous system from the gut to the central nervous system in cattle incubating bovine spongiform encephalopathy. J Gen Virol 88 1048 1055
47. EspinosaJC
HervaME
AndreolettiO
PadillaD
LacrouxC
2009 Transgenic mice expressing porcine prion protein resistant to classical scrapie but susceptible to sheep bovine spongiform encephalopathy and atypical scrapie. Emerg Infect Dis 15 1214 1221
48. HunterN
FosterJD
GoldmannW
StearMJ
HopeJ
1996 Natural scrapie in a closed flock of Cheviot sheep occurs only in specific PrP genotypes. Arch Virol 141 809 824
49. MoumT
OlsakerI
HoppP
MoldalT
ValheimM
2005 Polymorphisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor98 cases. J Gen Virol 86 231 235
50. AndreolettiO
BerthonP
LevavasseurE
MarcD
LantierF
2002 Phenotyping of Protein-Prion (PrPsc)-accumulating Cells in Lymphoid and Neural Tissues of Naturally Scrapie-affected Sheep by Double-labeling Immunohistochemistry. J Histochem Cytochem 50 1357 1370
51. TabouretG
LacrouxC
LuganS
CorbiereF
WeisbeckerJL
2010 Relevancy of oral experimental challenge with classical scrapie in sheep. J Gen Virol 91 2139 44
52. Schulz-SchaefferWJ
TschokeS
KranefussN
DroseW
Hause-ReitnerD
2000 The paraffin-embedded tissue blot detects PrP(Sc) early in the incubation time in prion diseases. Am J Pathol 156 51 56
53. WemheuerWM
BenestadSL
WredeA
Schulze-SturmU
WemheuerWE
2009 Similarities between forms of sheep scrapie and Creutzfeldt-Jakob disease are encoded by distinct prion types. Am J Pathol 175 2566 2573
54. VilotteJL
SoulierS
EssalmaniR
StinnakreMG
VaimanD
2001 Markedly increased susceptibility to natural sheep scrapie of transgenic mice expressing ovine prp. J Virol 75 5977 5984
55. FraserH
DickinsonAG
1968 The sequential development of the brain lesion of scrapie in three strains of mice. J Comp Pathol 78 301 311
56. MarkusRA
FrankJ
GroshenS
AzenSP
1995 An alternative approach to the optimal design of an LD50 bioassay. Stat Med 14 841 852
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 2
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Genetic Mapping Identifies Novel Highly Protective Antigens for an Apicomplexan Parasite
- Type I Interferon Signaling Regulates Ly6C Monocytes and Neutrophils during Acute Viral Pneumonia in Mice
- Infections in Cells: Transcriptomic Characterization of a Novel Host-Symbiont Interaction
- The ESCRT-0 Component HRS is Required for HIV-1 Vpu-Mediated BST-2/Tetherin Down-Regulation