Characterization of goat prions demonstrates geographical variation of scrapie strains in Europe and reveals the composite nature of prion strains

Romolo Nonno, Alberto Marina Moreno, J.C. Espinosa, C. Fast, L.J.M. van Keulen, J. Spiropoulos, Isabelle Lantier, Olivier Andrèoletti, L. Pirisinu, M.A. Di Bari, Patricia Aguilar-Calvo, Theodoros Sklaviadis, P. Papasavva-Stylianou, Pier Luigi Acutis, C. Acin, A. Bossers, Jorge G. Jacobs, G. Vaccari, C. D'Agostino, B. Chiappini & 5 others F. Lantier, Martin H. Groschup, U. Agrimi, Juan Maria Torres, J.P.M. Langeveld

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Bovine Spongiform Encephalopathy (BSE) is the only animal prion which has been recognized as a zoonotic agent so far. The identification of BSE in two goats raised the need to reliably identify BSE in small ruminants. However, our understanding of scrapie strain diversity in small ruminants remains ill-defined, thus limiting the accuracy of BSE surveillance and spreading fear that BSE might lurk unrecognized in goats. We investigated prion strain diversity in a large panel of European goats by a novel experimental approach that, instead of assessing the neuropathological profile after serial transmissions in a single animal model, was based on the direct interaction of prion isolates with several recipient rodent models expressing small ruminants or heterologous prion proteins. The findings show that the biological properties of scrapie isolates display different patterns of geographical distribution in Europe and suggest that goat BSE could be reliably discriminated from a wide range of biologically and geographically diverse goat prion isolates. Finally, most field prion isolates showed composite strain features, with discrete strain components or sub-strains being present in different proportions in individual goats or tissues. This has important implications for understanding the nature and evolution of scrapie strains and their transmissibility to other species, including humans.
Original languageEnglish
Article number19
JournalScientific Reports
Volume10
Issue number1
DOIs
Publication statusPublished - 8 Jan 2020

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bovine spongiform encephalopathy
scrapie
prions
geographical variation
goats
small ruminants
strain differences
fearfulness
geographical distribution
rodents
animal models
monitoring
animals

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Nonno, Romolo ; Marina Moreno, Alberto ; Espinosa, J.C. ; Fast, C. ; van Keulen, L.J.M. ; Spiropoulos, J. ; Lantier, Isabelle ; Andrèoletti, Olivier ; Pirisinu, L. ; Di Bari, M.A. ; Aguilar-Calvo, Patricia ; Sklaviadis, Theodoros ; Papasavva-Stylianou, P. ; Acutis, Pier Luigi ; Acin, C. ; Bossers, A. ; Jacobs, Jorge G. ; Vaccari, G. ; D'Agostino, C. ; Chiappini, B. ; Lantier, F. ; Groschup, Martin H. ; Agrimi, U. ; Torres, Juan Maria ; Langeveld, J.P.M. / Characterization of goat prions demonstrates geographical variation of scrapie strains in Europe and reveals the composite nature of prion strains. In: Scientific Reports. 2020 ; Vol. 10, No. 1.
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title = "Characterization of goat prions demonstrates geographical variation of scrapie strains in Europe and reveals the composite nature of prion strains",
abstract = "Bovine Spongiform Encephalopathy (BSE) is the only animal prion which has been recognized as a zoonotic agent so far. The identification of BSE in two goats raised the need to reliably identify BSE in small ruminants. However, our understanding of scrapie strain diversity in small ruminants remains ill-defined, thus limiting the accuracy of BSE surveillance and spreading fear that BSE might lurk unrecognized in goats. We investigated prion strain diversity in a large panel of European goats by a novel experimental approach that, instead of assessing the neuropathological profile after serial transmissions in a single animal model, was based on the direct interaction of prion isolates with several recipient rodent models expressing small ruminants or heterologous prion proteins. The findings show that the biological properties of scrapie isolates display different patterns of geographical distribution in Europe and suggest that goat BSE could be reliably discriminated from a wide range of biologically and geographically diverse goat prion isolates. Finally, most field prion isolates showed composite strain features, with discrete strain components or sub-strains being present in different proportions in individual goats or tissues. This has important implications for understanding the nature and evolution of scrapie strains and their transmissibility to other species, including humans.",
author = "Romolo Nonno and {Marina Moreno}, Alberto and J.C. Espinosa and C. Fast and {van Keulen}, L.J.M. and J. Spiropoulos and Isabelle Lantier and Olivier Andr{\`e}oletti and L. Pirisinu and {Di Bari}, M.A. and Patricia Aguilar-Calvo and Theodoros Sklaviadis and P. Papasavva-Stylianou and Acutis, {Pier Luigi} and C. Acin and A. Bossers and Jacobs, {Jorge G.} and G. Vaccari and C. D'Agostino and B. Chiappini and F. Lantier and Groschup, {Martin H.} and U. Agrimi and Torres, {Juan Maria} and J.P.M. Langeveld",
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Nonno, R, Marina Moreno, A, Espinosa, JC, Fast, C, van Keulen, LJM, Spiropoulos, J, Lantier, I, Andrèoletti, O, Pirisinu, L, Di Bari, MA, Aguilar-Calvo, P, Sklaviadis, T, Papasavva-Stylianou, P, Acutis, PL, Acin, C, Bossers, A, Jacobs, JG, Vaccari, G, D'Agostino, C, Chiappini, B, Lantier, F, Groschup, MH, Agrimi, U, Torres, JM & Langeveld, JPM 2020, 'Characterization of goat prions demonstrates geographical variation of scrapie strains in Europe and reveals the composite nature of prion strains', Scientific Reports, vol. 10, no. 1, 19. https://doi.org/10.1038/s41598-019-57005-6

Characterization of goat prions demonstrates geographical variation of scrapie strains in Europe and reveals the composite nature of prion strains. / Nonno, Romolo; Marina Moreno, Alberto; Espinosa, J.C.; Fast, C.; van Keulen, L.J.M.; Spiropoulos, J.; Lantier, Isabelle; Andrèoletti, Olivier; Pirisinu, L.; Di Bari, M.A.; Aguilar-Calvo, Patricia; Sklaviadis, Theodoros; Papasavva-Stylianou, P.; Acutis, Pier Luigi; Acin, C.; Bossers, A.; Jacobs, Jorge G.; Vaccari, G.; D'Agostino, C.; Chiappini, B.; Lantier, F.; Groschup, Martin H.; Agrimi, U.; Torres, Juan Maria; Langeveld, J.P.M.

In: Scientific Reports, Vol. 10, No. 1, 19, 08.01.2020.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Characterization of goat prions demonstrates geographical variation of scrapie strains in Europe and reveals the composite nature of prion strains

AU - Nonno, Romolo

AU - Marina Moreno, Alberto

AU - Espinosa, J.C.

AU - Fast, C.

AU - van Keulen, L.J.M.

AU - Spiropoulos, J.

AU - Lantier, Isabelle

AU - Andrèoletti, Olivier

AU - Pirisinu, L.

AU - Di Bari, M.A.

AU - Aguilar-Calvo, Patricia

AU - Sklaviadis, Theodoros

AU - Papasavva-Stylianou, P.

AU - Acutis, Pier Luigi

AU - Acin, C.

AU - Bossers, A.

AU - Jacobs, Jorge G.

AU - Vaccari, G.

AU - D'Agostino, C.

AU - Chiappini, B.

AU - Lantier, F.

AU - Groschup, Martin H.

AU - Agrimi, U.

AU - Torres, Juan Maria

AU - Langeveld, J.P.M.

PY - 2020/1/8

Y1 - 2020/1/8

N2 - Bovine Spongiform Encephalopathy (BSE) is the only animal prion which has been recognized as a zoonotic agent so far. The identification of BSE in two goats raised the need to reliably identify BSE in small ruminants. However, our understanding of scrapie strain diversity in small ruminants remains ill-defined, thus limiting the accuracy of BSE surveillance and spreading fear that BSE might lurk unrecognized in goats. We investigated prion strain diversity in a large panel of European goats by a novel experimental approach that, instead of assessing the neuropathological profile after serial transmissions in a single animal model, was based on the direct interaction of prion isolates with several recipient rodent models expressing small ruminants or heterologous prion proteins. The findings show that the biological properties of scrapie isolates display different patterns of geographical distribution in Europe and suggest that goat BSE could be reliably discriminated from a wide range of biologically and geographically diverse goat prion isolates. Finally, most field prion isolates showed composite strain features, with discrete strain components or sub-strains being present in different proportions in individual goats or tissues. This has important implications for understanding the nature and evolution of scrapie strains and their transmissibility to other species, including humans.

AB - Bovine Spongiform Encephalopathy (BSE) is the only animal prion which has been recognized as a zoonotic agent so far. The identification of BSE in two goats raised the need to reliably identify BSE in small ruminants. However, our understanding of scrapie strain diversity in small ruminants remains ill-defined, thus limiting the accuracy of BSE surveillance and spreading fear that BSE might lurk unrecognized in goats. We investigated prion strain diversity in a large panel of European goats by a novel experimental approach that, instead of assessing the neuropathological profile after serial transmissions in a single animal model, was based on the direct interaction of prion isolates with several recipient rodent models expressing small ruminants or heterologous prion proteins. The findings show that the biological properties of scrapie isolates display different patterns of geographical distribution in Europe and suggest that goat BSE could be reliably discriminated from a wide range of biologically and geographically diverse goat prion isolates. Finally, most field prion isolates showed composite strain features, with discrete strain components or sub-strains being present in different proportions in individual goats or tissues. This has important implications for understanding the nature and evolution of scrapie strains and their transmissibility to other species, including humans.

U2 - 10.1038/s41598-019-57005-6

DO - 10.1038/s41598-019-57005-6

M3 - Article

VL - 10

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 19

ER -