Abstract
Scrapie is a prion disease that affects the sheep and goats. It belongs to the group of transmissible spongiform encephalopathies (TSE). TSEs are characterized by the accumulation of the pathological form (\(\hbox {PrP}^{\mathrm{Sc}})\) of the cellular prion protein (\(\hbox {PrP}^{\mathrm{C}})\). The susceptibility of sheep to scrapie is influenced by polymorphisms in the PrP gene (PRNP). The aim of this study was to identify the genetic variability of sheep PRNP in Algerian sheep. Two-hundred and thirteen Algerian sheep from eight breeds (Ouled Djellal, Rembi, Hamra, Berbere, Barbarine, Sidaou, Taadmit and Tazegzawt) with no clinical manifestation of scrapie were analysed. Sequencing of the entire coding sequence of PRNP showed four main alleles (ARQ, ARR, AHQ and ARH) based on codons 136, 154 and 171 with different frequencies among the investigated breeds. Moreover, 14 additional nonsynonymous polymorphisms (Q101R, N103K, M112T, A116P, M137I, L141F, I142M, H143R, N146S, R151G, Y172D, N176K, H180Y and S240P) as well as two synonymous polymorphisms at codons 231 and 237 were found in the PRNP gene. Interestingly, the N103K, M137I and I142M polymorphisms were not described in sheep. The ARQ, ARR and ARH haplotypes were present in all breeds with a highest frequency of ARQ in Barbarine. The ARH was absent in Barbarine breed and the VRQ haplotype was absent in all Algerian breeds studied. The ARQ and ARR alleles were the most common with frequencies ranging from 30 to 65% and from 8 to 26%, respectively, in different breeds. These results represent the first study on PRNP variability in Algerian sheep and may serve as a basis for the development of breeding programmes to render national sheep breeds resistant to scrapie.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
19 September 2018
Figure 2 was printed incorrectly in the article.
References
Acín C., Martín-Burriel I., Goldmann W., Lyahyai J., Monzón M., Bolea R. et al. 2004 Prion protein gene polymorphisms in healthy and scrapie affected Spanish sheep. J. Gen. Virol. 85, 2103–2110.
Acutis P. L., Sbaiz L., Verburg F., Riina M. V., Ru G., Moda G. et al. 2004 Low frequency of the scrapie resistance associated allele and presence of lysine-171 allele of the prion protein gene in Italian Biellese ovine breed. J. Gen. Virol. 85, 3165–3172.
Alvarez L., Arranz J. J. and San Primitivo F. 2006 Identification of a new leucine haplotype (ALQ) at codon 154 in the ovine prion protein gene in Spanish sheep. J. Anim. Sci. 84, 259–265.
Alvarez L., Gutierrez-Gil B., Uzun M., Primitivo F. S. and Arranz J. J. 2011 Genetic variability in the prion protein gene in five indigenous Turkish sheep breeds. Small Rumin. Res. 99, 93–98.
Baylis M., Goldmann W., Houston F., Cairns D., Chong A., Ross A. et al. 2002a Scrapie epidemic in a fully PrP-genotyped sheep flock. J. Gen. Virol. 83, 2907–2914.
Baylis M., Houston F., Kao R. R., McLean A. R., Hunter N. and Gravenor M. B. 2002b BSE – a wolf in sheep’s clothing? Trends. Microbiol. 10, 563–570.
Billinis C., Psychas V., Leontides L., Spyrou V., Argyroudis S., Vlemmas I. et al. 2004 Prion protein gene polymorphisms in healthy and scrapie-affected sheep in Greece. J. Gen. Virol. 85, 547–554.
Bucalossi C., Cosseddu G., D’Agostino C., Di Bari M. A., Chiappini B., Conte M. et al. 2011 Assessment of the genetic susceptibility of sheep to scrapie by protein misfolding cyclic amplification and comparison with experimental scrapie transmission studies. J. Virol. 85, 8386–8392.
Curcio L., Sebastiani C., Ceccobelli S., Vaccari G., Pezzotti G., Lasagna E. et al. 2015 PRNP polymorphisms in four Italiansheep breeds. Livest Sci. 181, 38–42.
Dawson M., Moore R. C. and Bishop S. C. 2008 Progress and limits of PrP gene selection policy. Vet. Res. 39, 25.
De Silva U., Guo X., Kupfer D. M., Fernando S. C., Pillai A. T., Najar F. Z., So S. et al. 2003 Allelic variants of ovine prion protein gene (PRNP) in Oklahoma sheep. Cytogenet. Genome. Res. 102, 89–94.
EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards) 2014 Scientific opinion on the scrapie situation in the EU after 10 years of monitoring and control in sheep and goats. EFSA J. 12, 3781.
Goldmann W., Huntert N., Fosters J. D., Salbaum J. M., Beyreuther K. and Hopes J. 1990 Two alleles of a neural protein gene linked to scrapie in sheep. Proc. Natl. Acad. Sci. USA 87, 2476–2480.
Goldmann W. 2008 PrP genetics in ruminant transmissible spongiform encephalopathies. Vet. Res. 39, 30.
Goldmann W., Hunter N., Smith G., Foster J. and Hope J. 1994 PrP genotype and agent effects in scrapie: change in allelic interaction with different isolates of agent in sheep, a natural host of scrapie. J. Gen. Virol. 75, 989–995.
Goldmann W., Martin T., Foster J., Hughes S., Smith G., Hughes K. et al. 1996 Novel polymorphisms in the caprine PrP gene: a codon 142 mutation associated with scrapie incubation period. J. Gen. Virol. 77, 2885–2891.
Guan F., Pan L., Li J., Tang H., Zhu C. and Shi G. 2011 Polymorphisms of the prion protein gene and their effects on litter size and risk evaluation for scrapie in Chinese Hu sheep. Virus Genes 43, 147–152.
Harrington N. P., O’Rourke K. I., Feng Y., Rendulich J., Difruscio C. and Balachandran A. 2010 Prion genotypes of scrapie infected Canadian sheep 1998–2008. Can. J. Vet. Res. 74, 228–232.
Hunter N., Foster J. D., Goldmann W., Stear M. J., Hope J. and Bostock C. 1996 Natural scrapie in a closed flock of Cheviot sheep occurs only in specific PrP genotypes. Arch. Virol. 141, 809–824.
Hunter N., Goldmann W., Smith G. and Hope J. 1994 The association of a codon 136 PrP gene variant with the occurrence of natural scrapie. Arch. Virol. 137, 171–177.
Kalai S. M., Amara Y., Ameur Ameur A. and Gaouar S. B. S. 2017 Epidemiological study of Scrapie disease in local sheep population in Algeria. Gen. Biodiv. J. 26–29.
Karami M., Amirinia C., Kashan N. E. J, Amirmozafari N., Chamani M. and Banabazi M. H. 2011 Polymorphisms of the prion protein gene Arabi sheep breed in Iran. Afr. J. Biotechnol. 10, 15819–15822.
Kdidi S., Yahyaoui M. H., Conte M., Chiappini B., Zaccaria G., Bensassi M. et al. 2014 PRNP polymorphisms in Tunisian sheep breeds. Livest. Sci. 167, 100–103.
Kutzer T., Pfeiffer I. and Brenig B. 2002 Identification of new allelic variants in the ovine prion protein (PrP) gene. J. Anim. Breed. Genet. 119, 201–208.
Lan Z., Li J., Sun C., Liu Y., Zhao Y., Chi T. et al. 2014 Allelic variants of PRNP in 16 Chinese local sheep breeds. Arch. Virol. 159, 2141–2144.
Lan Z., Wang Z. L., Liu Y. and Zhang X. 2006 Prion protein gene (PRNP) polymorphisms in Xinjiang local sheep breeds in China. Arch. Virol. 151, 2095–2101.
MADR. 2013 Ministère de l’Agriculture, du Développement Rural et de la Pêche (2013).
Meydan H., Ozkan M. M., Yildiz M. A. and Goldmann W. 2013 Novel polymorphisms in ovine prion protein gene. Anim Genet. 44, 588–591.
Miller S. A., Dykes D. D. and Polesk H. F. 1988 A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16, 1215.
Moum T., Olsaker I., Hopp P., Moldal T., Valheim M., Moum T. et al. 2005 Polymorphisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor 98 cases. J. Gen. Virol. 86, 231–235.
Palmer M. S. V. and Collinge J. 1997 Prion diseases: an introduction. In Prion diseases (eds. J. Collinge and M. S. Palmer), pp. 1–17. Oxford University Press, New York.
Papasavva-Stylianou P., Windl O., Saunders G., Mavrikiou P., Toumazos P. and Kakoyiannis C. 2011 PrP gene polymorphisms in Cyprus goats and their association with resistance or susceptibility to natural scrapie. Vet. J. 187, 245–250.
Prusiner S. B. 1993 Prion encephalopathies of animals and humans. Dev. Biol. Stand. 80, 31–44.
Saunders G. C., Lantier S., Cawthraw S., Berthon P., Moore S. J., Arnold M. E. et al. 2009 Protective effect of the T112 PrP variant in sheep challenged with bovine spongiform encephalopathy. J. Gen. Virol. 90, 2569–2574.
Seabury C. M. and Derr J. N. 2003 Identification of a novel ovine PrP polymorphism and scrapie-resistant genotypes for St. Croix White and a related composite breed. Cytogenet. Genome. Res. 102, 85–88.
Serrano C., Martín-Burriel I., Lyahyai J., Monzón M., El Hamidi M., Acín C. et al. 2007 Polymorphisms of the PRNP gene in Moroccan sheep breeds. Vet Rec. 161, 524–525.
Traoré A., Royo L. J., Kaboré A., Pérez-Pardal L., Álvarez I., Fernández I. et al. 2012 Prion protein gene polymorphism in four West African sheep populations. Trop. Anim. Health Prod. 44, 1469–1472.
Ün C., Oztabak K., Ozdemir N., Akis I. and Mengi A. 2008 Genotyping of PrP gene in native Turkish sheep breeds. Small Rumin. Res. 74, 260–264.
Vaccari G., D’Agostino C., Nonno R., Rosone F., Conte M., Dibari M. A. et al. 2007 Prion protein alleles showing a protective effect on the susceptibility of sheep to scrapie and bovine spongiform encephalopathy. J. Virol. 81, 7306–7309.
Vaccari G., Scavia G., Sala M., Cosseddu G., Chiappini B., Conte M. et al. 2009a Protective effect of the AT137RQ and ARQK176 PrP allele against classical scrapie in Sarda breed sheep. Vet. Res. 40, 19–29.
Vaccari G., Panagiotidis C. H., Acin C., Peletto S., Barillet F., Acutis P. et al. 2009b State-of-the-art review of goat TSE in the European Union, with special emphasis on PRNP genetics and epidemiology. Vet. Res. 40, 48.
Windig J. J., Hoving R. A., Priem J., Bossers A., Van Keulen L. J. and Langeveld J. P. 2016 Variation in the prion protein sequence in Dutch goat breeds. J. Anim. Breed Genet. 133, 366–374.
Acknowledgements
The authors thank all the farmers and veterinarians who participated in the sampling. The extraction of DNA and sequencing analyses were conducted at Tlemcen University and Istituto Superiore di Sanità respectively. Especially, we would like to acknowledge and thank Alfredo Caggiano, and Consiglia Parisi for the technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Indrajit Nanda
Rights and permissions
About this article
Cite this article
Djaout, A., CHIAPPINI, B., GAOUAR, SBS. et al. Biodiversity and selection for scrapie resistance in sheep: genetic polymorphism in eight breeds of Algeria. J Genet 97, 453–461 (2018). https://doi.org/10.1007/s12041-018-0932-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12041-018-0932-x