Skip to main content

Advertisement

Log in

The genetic diversity of bovine papillomaviruses (BPV) from different papillomatosis cases in dairy cows in Turkey

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Papillomaviruses (PVs) are epitheliotropic viruses that cause benign proliferative lesions in the skin (warts or papillomas) and mucous membranes of their natural hosts. In bovines specifically, 13 types of Bovine papillomaviruses (BPVs) are currently described in the literature, although the actual number may be greater than 20. BPV types are classified into four genera based on homology within the genomic regions of the L1 ORF, the most conserved sequence. This study conducted molecular typing of BPV in dairy cows with different papillomatosis cases and investigated the presence of co-infections across distinct BPV types in the same sample. After carrying out PCR using degenerate primers and type specific primers, 35 BPV suspected samples were detected as positive for BPV and these samples were used for typing using sequence analysis/PCR with type-specific primers. This analysis identified BPV-1, -2, -3, -4, -6, -7, -9 and -10, new putative types (BPV/BR/UEL6-like viruses) and the previously described putative type viruses (BAPV-6) in the 35 BPV-positive samples. In addition, co-infections across different BPV types were widely detected in the BPV-positive samples.  This study shows that PCR assays using degenerate primers to amplify partial fragments of the L1 gene followed by sequencing is useful for genotyping BPV. However, results need confirmation using type-specific primers in order to consider co-infections. In addition, this study identified a new putative type (in the same cluster as BPV/BR/UEL6-like viruses) and the previously described putative type viruses (BAPV-6) in teat papillomatosis of Turkish dairy cows. The study shows that it is essential to identify BPV types and their prevalence/distribution, and also to determine the clinical consequences of infection for the development of prophylactic and/or therapeutic procedures.

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

Access this article

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

Instant access to the full article PDF.

Picture 1
Picture 2
Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Altschul SF, Madden TL, Schäffer AA (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 17:3389–3402

    Article  Google Scholar 

  2. Antonsson A, Hansson BG (2002) Healthy skin of many animal species harbors papillomaviruses which are closely related to their human counterparts. J Virol 76:12537–12542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ataseven VS, Kanat Ö, Ergün Y (2016) Molecular identification of bovine papillomaviruses in dairy and beef cattle: First description of Xi- and Epsilonpapillomaviruses in Turkey. Turk J Vet Anim Sci. doi:10.3906/vet-1512-1564

    Google Scholar 

  4. Bastawecy IM (2012) Isolation of bovine herpesvirus-2 (BHV-2) from a case of pseudo-lumpy skin disease in Egypt. J Am Sci 8:2

    Google Scholar 

  5. Batista MV, Silva MA, Pontes NE, Reis MC, Corteggio A, Castro RS, Borzacchiello G, Balbino VQ, Freitas AC (2013) Molecular epidemiology of bovine papillomatosis and the identification of a putative new virus type in Brazilian cattle. Vet J 197:368–373

    Article  PubMed  Google Scholar 

  6. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, de Villiers EM (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bocaneti F, Altamura G, Corteggio A, Velescu E, Roperto F, Borzacchiello G (2016) Bovine papillomavirus: New insights into an old disease. Transbound Emerg Dis 63:14–23

    Article  CAS  PubMed  Google Scholar 

  8. Borzacchiello G, Roperto F (2008) Bovine papillomaviruses, papillomas and cancer in cattle. Vet Res 39:45

    Article  PubMed  Google Scholar 

  9. Campo MS (1987) Papillomas and cancer in cattle. Cancer Surv 6:39–54

    CAS  PubMed  Google Scholar 

  10. Campo MS (2006) Bovine Papillomavirus: old system, new lessons?. Caister Academic Press, England (Chapter 23)

    Google Scholar 

  11. Carvalho CCR, Batista MVA, Silva MAR, Balbino VQ, Freitas AC (2012) Detection of bovine papillomavirus types, co-infection and new BPV11 subtype in cattle. Transbound Emerg Dis 59:441–447

    Article  CAS  PubMed  Google Scholar 

  12. Claus MP, Lunardi M, Alfieri AF (2008) Identification of unreported putative new bovine papillomavirus types in Brazilian cattle herds. Vet Microbiol 132:396–401

    Article  CAS  PubMed  Google Scholar 

  13. Claus MP, Lunardi M, Alfieri AF (2009) Identification of the recently described new type of bovine papillomavirus (BPV-8) in a Brazilian beef cattle herd. Pesqui Vet Bras 29:25–28

    Article  Google Scholar 

  14. Claus MP, Vivian D, Lunardi M (2007) Phylogenetic analysis of bovine papillomavirus associated with skin warts in cattle herds from the state of Parana. Pesqui Vet Bras 27:314–318

    Article  Google Scholar 

  15. Corteggio A, Altamura G, Roperto F, Borzacchiello G (2013) Bovine papillomavirus E5 and E7 oncoproteins in naturally occurring tumors: are two better than one? Infect Agents Cancer 8:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. de Villiers EM, Fauquet C, Broker TR, Bernard HU, Hausen H (2004) Classification of papillomaviruses. Virology 1:17–27

    Article  Google Scholar 

  17. Egyed J, Ballagi-Pordany A, Bartha A, Belak S (1996) Studies of in vivo distribution of bovine herpesvirus type 4 in the natural host. J Clin Microbiol 34:1091–1095

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Forslund O, Antonsson A, Nordin P (1999) A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol 80:2437–2443

    Article  CAS  PubMed  Google Scholar 

  19. Goltz M, Broll H, Mankertz A, Weıgelt W, Ludwıg H, Buhk HJ, Borchers K (1994) Glycoprotein B of bovine herpesvirus type 4: Its phylogenetic relationship to gB equivalents of the herpesviruses. Virus Genes 9:53–59

    Article  CAS  PubMed  Google Scholar 

  20. Grindatto A, Ferraro G, Varello K, Crescio M, Miceli I, Bozzetta E, Goria M, Nappi R (2015) Molecular and histological characterization of bovine papillomavirus in North 349 West Italy. Vet Microbiol 180:113–117

    Article  CAS  PubMed  Google Scholar 

  21. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  22. Hatama S, Ishihara R, Ueda Y, Kanno T, Uchida I (2011) Detection of a novel bovine papillomavirus type 11 (BPV-11) using xipapillomavirus consensus polymerase chain reaction primers. Arch Virol 156:1281–1285

    Article  CAS  PubMed  Google Scholar 

  23. Jarrett WF (1985) Bovine papillomaviruses. Clin Dermatol 3:8–19

    Article  CAS  PubMed  Google Scholar 

  24. Jarrett WFH, O’Neil BW, Gaukroger JM, Smith KT, Laird HM, Campo MS (1990) Studies on vaccination against papillomaviruses: the immunity after infection and vaccination with bovine papillomaviruses of different types. Vet Rec 126:473–475

    CAS  PubMed  Google Scholar 

  25. Kumar P, Nagarajan N, Saikumar G, Arya RS, Somvanshi R (2013) Detection of bovine papilloma viruses in wart-like lesions of upper gastrointestinal tract of cattle and buffaloes. Transbound Emerg Dis 63:56–67

    Google Scholar 

  26. Leishangthem GD, Somvanshi R, Tiwari AK (2008) Detection of bovine papillomaviruses in cutaneous warts/papillomas in cattle. Indian J Vet Pathol 32:15–20

    Google Scholar 

  27. Lindsey CL, Almeida ME, Vicari CF, Carvalho C, Yaguiu A, Freitas AC, Becak W, Stocco RC (2009) Bovine papillomavirus DNA in milk, blood, urine, semen, and spermatozoa of bovine papillomavirus-infected animals. Genet Mol Res 8:310–318

    Article  CAS  PubMed  Google Scholar 

  28. Lunardi M, de Alcantara BK, Otonel RA, Rodrigues WB, Alfieri AF, Alfieri AA (2013) Bovine papillomavirus type 13 DNA in equine sarcoids. J Clin Microbiol 51:2167–2171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lunardi M, Tozato CC, Alfieri AF, Alcantara BK, Vilas-Boas LA, Otonel RAA, Headley SA, Alfieri AA (2016) Genetic diversity of bovine papillomavirus types, including two putative new types, in teat warts from dairy cattle herds. Arch Virol 161:1569–1577

    Article  CAS  PubMed  Google Scholar 

  30. Maiolino PA, Ozkul A, Sepici-Dincel A, Roperto F, Yucel G, Russo V, Urraro C, Luca R, Riccardi MG, Martano M, Borzacchiello G, Esposito I, Roperto S (2013) Bovine papillomavirus type 2 infection and microscopic patterns of urothelial tumors of the urinary bladder in water buffaloes. Biomed Res Int 146:269–275

    Google Scholar 

  31. Maeda Y, Shibahara T, Wada Y, Kadota K, Kanno T, Uchida I, Hatama S (2007) An outbreak of teat papillomatosis in cattle caused by bovine papilloma virus (BPV) type 6 and unclassified BPVs. Vet Microbiol 121:242–248

    Article  PubMed  Google Scholar 

  32. Nasir L, Campo MS (2008) Bovine papillomaviruses: their role in the aetiology of cutaneous tumours of bovids and equids. Vet Dermatol 19:243–254

    Article  PubMed  Google Scholar 

  33. Ogawa T, Tomita Y, Okada M, Schinozaki K, Kubonoya H, Kaiho I, Shirisawa H (2004) Broad-spectrum detection of papillomaviruses in bovine teat papillomas and healthy teat skin. J Gen Virol 85:2191–2197

    Article  CAS  PubMed  Google Scholar 

  34. Pangty K, Singh S, Goswami R, Saikumar G, Somvanshi R (2010) Detection of BPV-1 and -2 and quantification of BPV-1 by real-time PCR in cutaneous warts in cattle and buffaloes. Transbound Emerg Dis 57:185–196

    Article  CAS  PubMed  Google Scholar 

  35. Rai GK, Saxena M, Singh V, Somvanshi R, Sharma B (2011) Identification of bovine papilloma virus 10 in teat warts of cattle by DNase-SISPA. Vet Microbiol 147:416–419

    Article  CAS  PubMed  Google Scholar 

  36. Roperto S, Russo V, Ozkul A, Corteggio A, Sepici-Dincel A, Catoi C, Esposito I, Riccardi MG, Urraro C, Luca R, Ceccarelli DM, Longo M, Roperto F (2013) Productive infection of bovine papillomavirus type 2 in the urothelial cells of naturally occurring urinary bladder tumors in cattle and water buffaloes. PLoS One 8:e62227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  38. Santos EUD, Silva MAR, Pontes NE, Coutinho LCA, Paiva SSL, Castro RS, Freitas AC (2016) Detection of different bovine papillomavirus types and co-infection in bloodstream of cattle. Transbound Emerg Dis 63:103–108

    Article  Google Scholar 

  39. Schmitt M, Fiedler V, Muller M (2010) Prevalence of BPV genotypes in a German cowshed determined by a novel multiplex BPV genotyping assay. J Virol Methods 170:67–72

    Article  CAS  PubMed  Google Scholar 

  40. Silva MS, Weiss M, Brum MCS, Anjos BL, Torres FD, Weiblen R, Flores EF (2010) Molecular identification of bovine papillomaviruses associated with cutaneous warts in southern Brazil. J Vet Diagn Invest 22:603–606

    Article  PubMed  Google Scholar 

  41. Silva MA, de Albuquerque BM, Pontes NE, Coutinho LC, Leitao MC, Reis MC, Castro RS, Freitas AC (2013) Detection and expression of bovine papillomavirus in blood of healthy and papillomatosis-affected cattle. Genet Mol Res 12:3150–3156

    CAS  PubMed  Google Scholar 

  42. Silvestre O, Borzacchiello G, Nava D, Iovane D, Russo V, Vecchio D, D’Ausilio F, Gault EA, Campo MS, Paciello O (2009) Bovine papillomavirus type 1 DNA and E5 oncoprotein expression in water buffalo fibropapillomas. Vet Pathol 46:636–641

    Article  CAS  PubMed  Google Scholar 

  43. Singh V, Somvanshi R, Tiwari AK (2009) Papillomatosis in Indian cattle: occurance and etiopathology. Indian J Vet Pathol 33:52–57

    Google Scholar 

  44. Tamura K, Dudley J, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Tan MT, Yıldırım Y, Sozmen M, Bılge Dagalp S, Yılmaz V, Kırmızıgul AH, Gokce E (2012) A histopathological, ımmunohistochemical and molecular study of cutaneous bovine papillomatosis. Kafkas Univ Vet Fak Derg 18:739–744

    Google Scholar 

  46. Van Engelenburg FAC, Maes RK, Van Oirschot JT, Rijsewijk FAM (1993) Development of a rapid and sensitive polymerase chain reaction assay for detection of bovine herpesvirus type 1 in bovine semen. J Clin Microbiol 31:3129–3135

    PubMed  PubMed Central  Google Scholar 

  47. Yaguiu A, Carvalho C, Freitas AC, Góes LGB, Dagli MLZ, Birgel EH Jr, Stocco dos Santos RC (2006) Papilomatosis in cattle: In situ detection of bovine papilomavirus DNA sequences in reproductives tissues. Braz J Morphol 23:525–529

    Google Scholar 

  48. Yaguiu A, Dagli ML, Birgel EH Jr, Alves Reis BC, Ferraz OP, Pituco EM, Freitas AC, Becak W, Stocco RC (2008) Simultaneous presence of bovine papillomavirus and bovine leukemia virus in different bovine tissues: in situ hybridization and cytogenetic analysis. Genet Mol Res 7:487–497

    Article  CAS  PubMed  Google Scholar 

  49. Zhu W, Dong J, Shimizu E, Hatama S, Kadota K, Goto Y, Haga T (2012) Characterization of novel bovine papillomavirus type 12 (BPV-12) causing epithelial papilloma. Arch Virol 157:85–91

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank to Vet.Ali Haciomeroglu for all helps.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seval Bilge Dagalp.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dagalp, S.B., Dogan, F., Farzanı, T.A. et al. The genetic diversity of bovine papillomaviruses (BPV) from different papillomatosis cases in dairy cows in Turkey. Arch Virol 162, 1507–1518 (2017). https://doi.org/10.1007/s00705-017-3258-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3258-8

Keywords

Navigation