Skip to main content
SpringerLink
Log in

Deletion / insertion polymorphisms of the prion protein gene (PRNP) in gayal (Bos frontalis)

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Resistance to fatal disease bovine spongiform encephalopathy (BSE), due to misfolded prion protein in cattle, is associated with a 23-bp indel polymorphism in the putative promoter and a 12-bp indel in intron 1 of the PRNP gene. Gayal (Bos frontalis) is an important semiwild bovid species and of great conservation concern, but till today these indel polymorphisms have not been evaluated in gayals. Therefore, we collected 225 samples of gayals and evaluated the genetic indel polymorphism in the two regions of this PRNP gene. The results revealed high allelic frequencies of insertions at these indel sites: 0.909 and 0.667 for, respectively, the 23 bp and 12 bp indels, both also with significant genotype frequencies (\(\chi ^{2}\): 9.81; 23 bp and \(\chi ^{2}\): 43.56; 12 bp). At the same time, the haplotype data showed indel polymorphisms with extremely low deletion (0.01) in both regions of the PRNP gene. We compared these data with those reported for healthy and BSE-affected cattle (Bos taurus) breeds from two European countries, Germany and Switzerland, and significant difference (\(P\,{<}\,0.001\)) was observed between BSE-affected as well as the healthy cattle. Further, our data were also extensively compared with previous reports on BSE and highly significant (\(P\,{<}\,0.001\)) outcomes were observed. This result suggested negligible genetic susceptibility to BSE in gayals. To the best of our knowledge, this study is the first comprehensive deciphering information about the PRNP indel polymorphisms of 23 bp and 12 bp in gayals, a semiwild species of China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Barrett J. C., Fry B., Maller J. and Daly M. J. 2005 Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265.

    Article  CAS  Google Scholar 

  • Brunelle B. W., Hamir A. N., Baron T., Biacabe A. G., Richt J. A. and Kunkle R. A. 2007 Polymorphisms of the prion gene promoter region that influence classical bovine spongiform encephalopathy susceptibility are not applicable to other transmissible spongiform encephalopathies in cattle. J. Anim. Sci. 85, 3142–3147.

    Article  CAS  Google Scholar 

  • Brunelle B. W., Kehrli M. E., Stabel J. R., Spurlock D. M., Hansen L. B. and Nicholson E. M. 2008 Allele, genotype, and haplotype data for bovine spongiform encephalopathy-resistance polymorphisms from healthy US Holstein cattle. J. Dairy Sci. 91, 338–342.

    Article  CAS  Google Scholar 

  • Clawson M. L., Heaton M. P., Keele J. W., Smith T. P., Harhay G. P. and Laegreid W. W. 2006 Prion gene haplotypes of U. S. cattle. BMC Genet. 7, 51–62.

    Article  Google Scholar 

  • Collinge J. and Clarke A. R. 2007 A general model of prion strains and their pathogenicity. Science 318, 930–936.

    Article  CAS  Google Scholar 

  • Czarnik U., Zabolewicz T., Strychalski J., Grzybowski G., Bogusz M. and Walawski K. 2007 Deletion/insertion polymorphism of the prion protein gene (PRNP) in Polish Holstein-Friesian cattle. J. Appl. Genet. 48, 69–71.

    Article  Google Scholar 

  • Czarnik U., Strychalski J., Zabolewicz T. and Pareek C. S. 2011 Populationwide investigation of two indel polymorphisms at the prion protein gene in Polish Holstein-Friesian cattle. Biochem. Genet. 49, 303–312.

    Article  CAS  Google Scholar 

  • Deng W. D., Wang L. P., Ma S. C., Jin B., He T. B., Yang Z. F. et al. 2007 Comparison of gayal (Bos frontalis) and Yunnan yellow cattle (Bos taurus): rumen function, digestibilities and nitrogen balance during feeding of pelleted lucerne (Medicago sativum). Asian-Aust. J. Anim. Sci. 20, 900–909.

    Article  CAS  Google Scholar 

  • Galvao C. E., Rosinha G. M., Sanches C. C., Elisei C., Araujo F. R. and Feijo G. L. 2012 Polymorphisms of intron 1 and the promoter region at the PRNP gene in BSE-free Caracu cattle. Biochem. Genet. 50, 657–669.

    Article  CAS  Google Scholar 

  • Ge C. R., Tian Y. B., Chen T. and Wu Y. 1996 Studies on the meat feature of gayal (Bos frontalis). Sci. Agric. Sin. 29, 75–78.

    Google Scholar 

  • Giasuddin M., Huque K. S. and Alam J. 2003 Reproductive potentials of gayal (Bos frontalis) under semi-intensive management. Asian-Aust. J. Anim. Sci. 16, 331–334.

    Google Scholar 

  • Gou X., Wang Y., Yang S. L, Deng W. D. and Mao H. M. 2010 Genetic diversity and origin of gayal and cattle in Yunnan revealed by mtDNA control region and SRY gene sequence variation. J. Anim. Breed. Genet. 127, 154–160.

    Article  CAS  Google Scholar 

  • Gurgul A., Czarnik U., Larska M., Polak M. P., Strychalski J. and Slota E. 2012 Polymorphism of the prion protein gene (PRNP) in Polish cattle affected by classical bovine spongiform encephalopathy. Mol. Biol. Rep. 39, 5211–5217.

    Article  CAS  Google Scholar 

  • Haase B., Doherr M. G., Seuberlich T., Drogemuller C., Dolf G. and Nicken P. 2007 PRNP promoter polymorphisms are associated with BSE susceptibility in Swiss and German cattle. BMC Genet. 16, 8–15.

    Google Scholar 

  • He Z. X., Qu K. X., Yuan X. P., San Y. H., Ma W. Z., Zhang J. C. et al. 2009 Appearance characteristics and major behavior of gayal (Bos frontalis) on the conservation ex situ in Phoenix mountain. J. Yunnan. Agric. Univ. 24, 225–230.

    Google Scholar 

  • Imran M., Mahmood S., Babar M. E., Hussain R., Yousaf M. Z. and Abid N. B. 2012 PRNP gene variation in Pakistani cattle and buffaloes. Gene 505, 180–185.

    Article  CAS  Google Scholar 

  • Jeong B. H., Lee Y. J., Kim N. H., Carp R. I. and Kim Y. S. 2006 Genotype distribution of the prion protein gene (PRNP) promoter polymorphisms in Korean cattle. Genome 49, 15394–15404.

    Article  Google Scholar 

  • Juling K., Schwarzenbacher H., Williams J. L. and Fries R. 2006 A major genetic component of BSE susceptibility. BMC Biol. 4, 33.

    Article  Google Scholar 

  • Kashkevich K., Humeny A., Ziegler U., Groschup M. H., Nicken P., Leeb T. et al. 2007 Functional relevance of DNA polymorphisms within the promoter region of the prion protein gene and their association to BSE infection. FASEB J. 21, 1547–1555.

  • Kerber A. R., Hepp D., Passos D. T. and de Azevedo Weimer T. 2008 Polymorphisms of two indels at the PRNP gene in three beef cattle herds. Biochem. Genet. 46, 1–7.

    Article  CAS  Google Scholar 

  • Kim Y., Kim J. B., Sohn H. and Lee C. 2009 A national survey on the allelic, genotypic, and haplotypic distribution of PRNP insertion and deletion polymorphisms in Korean cattle. J. Genet. 88, 99–103.

    Article  Google Scholar 

  • Mei C. G., Wang H. C., Zhu W. J., Wang H. B., Cheng G., Qu K. X. et al. 2016 Whole-genome sequencing of the endangered bovine species Gayal (Bos frontalis) provides new insights into its genetic features. Sci. Rep. 25, 19787.

    Article  Google Scholar 

  • Memon S., Wang L. P., Li G. Z., Liu X. Y., Deng W. D. and Xi D. M. 2018 Isolation and characterization of the major histocompatibility complex DQA1 and DQA2 genes in gayal (Bos frontalis). J. Genet. 97, 121–126.

    Article  CAS  Google Scholar 

  • Mohan M., Chandan R. and Prakash B. S. 2007 Development and validation of a highly sensitive economic enzymeimmuno-assay for prolactin determination in blood plasma of mithun (Bos frontalis) and its application during milk let down and cyclicity. Anim. Reprod. Sci. 99, 182–195.

    Article  Google Scholar 

  • Msalya G., Shimogiri T., Okamoto S., Kawabe K., Minezawa M. and Namikawa T. 2009 Gene and haplotype polymorphisms of the Prion gene (PRNP) in Japanese Brown, Japanese native and Holstein cattle. J. Anim. Sci. 80, 520–527.

    Article  CAS  Google Scholar 

  • Msalya G., Shimogiri T., Ohno S., Okamoto S., Kawabe K. and Minezawa M. 2011 Evaluation of PRNP expression based on genotypes and alleles of two indel loci in the medulla oblongata of Japanese Black and Japanese Brown cattle. PLoS One 6, e18787.

    Article  CAS  Google Scholar 

  • Muramutsu Y., Sakemi Y., Horiuchi M., Ogawa T., Suzuki K. and Kanameda M. 2008 Frequencies of PRNP gene polymorphisms in Vietnamese dairy cattle for potential association with BSE. Zoonoses Public Health. 55, 267–273.

    Article  Google Scholar 

  • Murdoch B. M., Clawson M. L., Yue S., Basu U., McKay S. and Settles M. 2010 PRNP haplotype associated with classical BSE incidence in European Holstein cattle. PLoS One 5, e12786.

    Article  Google Scholar 

  • Nakamitsu S., Miyazawa T., Horiuchi M., Onoe S., Ohoba Y. and Kitagawa H. 2006 Sequence variation of bovine prion protein gene in Japanese cattle (Holstein and Japanese Black). J. Vet Med. Sci. 68, 27–33.

    Article  CAS  Google Scholar 

  • Nei M. and Li W. H. 1979 Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76, 5269–5273.

    Article  CAS  Google Scholar 

  • Oztabak K., Ozkan E., Soysal I., Paya I. and Un C. 2009 Detection of prion gene promoter and intron 1 indel polymorphisms in Anatolian water buffalo (Bubalus bubalis). J. Anim. Breed. Genet. 126, 463–467.

    Article  CAS  Google Scholar 

  • Prusiner S. B., Scott M. R., DeArmond S. J. and Cohen F. E. 1998 Prion protein biology. Cell 93, 337–348.

    Article  CAS  Google Scholar 

  • Qin L. H., Zhao Y. M., Bao Y. H., Bai W. L., Chong J. and Zhang G. L. 2011 Polymorphism of the prion protein gene (PRNP) in two Chinese indigenous cattle breeds. Mol. Biol. Rep. 38, 4197–4204.

    Article  CAS  Google Scholar 

  • Qu K. X., He Z. X., Nie W. H., Zhang J. C., Jin X. D. and Yang G. R. 2012 Karyotype analysis of mithun (Bos frontalis) and mithun bull x Brahman cow hybrids. Genet. Mol. Res. 11, 131–140.

    Article  Google Scholar 

  • Sambrook J., Fritsch E. F. and Maniatis T. 1989 Molecular cloning: a laboratory manual, 2nd edition. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Sander P., Hamann H., Pfeiffer I., Wemheuer W., Brenig B. and Groschup M. H. 2004 Analysis of sequence variability of the bovine prion protein gene (PRNP) in German cattle breeds. Neurogenetics 5, 19–25.

    Article  CAS  Google Scholar 

  • Seabury C. M., Womack J. E., Piedrahita J. and Derr J. N. 2004 Comparative PRNP genotyping of U.S. cattle sires for potential association with BSE. Mamm. Genome 15, 828–833.

    Article  CAS  Google Scholar 

  • Shimogiri T., Msalya G., Myint S. L., Okamoto S., Kawabe K. and Tanaka K. 2010 Allele distributions and frequencies of the six prion protein gene (PRNP) polymorphisms in Asian native cattle, Japanese breeds, and mithun (Bos frontalis). Biochem. Genet. 48, 8293–8299.

    Article  Google Scholar 

  • Uchida L., Heriyanto A., Thongchai C., Hanh T. T., Horiuchi M. and Ishihara K. 2014 Genetic diversity in the prion protein gene (PRNP) of domestic cattle and water buffaloes in Vietnam, Indonesia and Thailand. J. Vet. Med. Sci. 76, 1001–1008.

    Article  CAS  Google Scholar 

  • Un C., Oztabak K., Ozdemir N., Tesfaye D., Mengi A. and Schellander K. 2008 Detection of bovine spongiform encephalopathy-related prion protein gene promoter polymorphisms in local Turkish cattle. Biochem. Genet. 46, 820–827.

    Article  CAS  Google Scholar 

  • Xi D. M., Liu Q., Guo J., Yu H. M., Yang Y. A., He Y. D. et al. 2011 Genetic variability of the coding region for the prion protein gene (PRNP) in gayal (Bos frontalis). Mol. Biol. Rep. 39, 2011–2020.

    Article  Google Scholar 

  • Xi D. M., Wu M., Fan Y. Y., Liu Q., Leng J., Gou X. et al. 2012 Polymorphisms of the insulin-like growth factor-binding protein 3 gene (IGFBP3) in gayal (Bos frontalis). Gene 497, 98–102.

    Article  CAS  Google Scholar 

  • Zhao H., Wang X. Y. and Zhang Y. P. 2009 The indel polymorphisms of the prion protein gene (PRNP) in Chinese yak. Anim. Genet. 40, 575–586.

    Article  CAS  Google Scholar 

  • Zhao H., Wang X. Y., Zou W. and Zhang Y. P. 2010 Prion protein gene (PRNP) polymorphisms in native Chinese cattle. Genome 53, 138–145.

    Article  CAS  Google Scholar 

  • Zhao H., Du Y., Chen S., Qing L., Wang X. and Huang J. 2015 The prion protein gene polymorphisms associated with bovine spongiform encephalopathy susceptibility differ significantly between cattle and buffalo. Infect. Genet. Evol. 36, 531–538.

    Article  CAS  Google Scholar 

  • Zhao K. D., Ou C. H., Huang Y. L. and He T. B. 2003 Rare animal germplasm resources in Yunnan Province: present situation and countermeasures of preservation and research on Dulong cattle (Bos frontalis). J. Yellow Cattle Sci. 29, 71–74.

    Google Scholar 

  • Zhu X. Y., Feng F. Y., Xue S. Y., Hou T. and Liu H. R. 2011 Bovine spongiform encephalopathy associated insertion/deletion polymorphisms of the prion protein gene in the four beef cattle breeds from North China. Genome 54, 805–811.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The current study was funded by the National Nature Science Foundation of China (grant nos 31460583 and 31101640) and the Yunnan Provincial Key Laboratory of Animal Nutrition and Feed (grant no. DYCX2015004). We thank the two anonymous reviewers for invaluable comments on the manuscript and also appreciate the help of staff (especially Zhijun He and Baqi Su) from the Gongshan County Agriculture, Science and Technology Bureau during sample collection.

Author information

Authors and Affiliations

  1. Yunnan Provincial Key Laboratory of Animal Nutrition and Feed Science, Faculty of Animal Science and Technology, Yunnan Agricultural University, Kunming, 650201, People’s Republic of China

    Sameeullah Memon, Guozhi Li, Heli Xiong, Liping Wang, Xiangying Liu, Mengya Yuan, Weidong Deng & Dongmei Xi

Authors
  1. Sameeullah Memon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guozhi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heli Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiangying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mengya Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Weidong Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dongmei Xi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dongmei Xi.

Additional information

Corresponding editor: Silvia Garagna

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Memon, S., Li, G., Xiong, H. et al. Deletion / insertion polymorphisms of the prion protein gene (PRNP) in gayal (Bos frontalis). J Genet 97, 1131–1138 (2018). https://doi.org/10.1007/s12041-018-1005-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-018-1005-x

Keywords

Search

Navigation