Skip to main content

Advertisement

SpringerLink
Log in

Canine papillomavirus type 16 associated to squamous cell carcinoma in a dog: virological and pathological findings

  • Veterinary Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Papillomaviruses (PVs) are circular double-stranded DNA virus belonging to Papillomaviridae family. During the infection cycle, PVs translate proteins that can influence cell growth and differentiation, leading to epidermal hyperplasia and papillomas (warts) or malignant neoplasms. Canis familiaris papillomaviruses (CPVs) have been associated with different lesions, such as oral and cutaneous papillomatosis, pigmented plaques, and squamous cell carcinomas (SCCs). Here, we report a clinical case of a mixed bred female dog with pigmented plaques induced by CPV16 (Chipapillomavirus 2) that progressed to in situ and invasive SCCs. Gross and histological findings were characterized, and the lesions were mainly observed in ventral abdominal region and medial face of the limbs. In situ hybridization (ISH) revealed strong nuclear hybridization signals in the neoplastic epithelial cells, as well as in the keratinocytes and koilocytes of the pigmented viral plaques. The full genome of the CPV16 recovered directly from the lesions was characterized, and the phylogenetic relationships were determined. The identification of oncoprotein genes (E5, E6, and E7) by high throughput sequencing (HTS) and their expected domains are suggestive of the malignant transformation by CPV16.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. de Villiers E-M, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324:17–27. https://doi.org/10.1016/j.virol.2004.03.033

    Article  CAS  PubMed  Google Scholar 

  2. Doorbar J (2005) The papillomavirus life cycle. J Clin Virol 32:7–15. https://doi.org/10.1016/j.jcv.2004.12.006

    Article  CAS  Google Scholar 

  3. Munday JS, Thomson NA, Luff JA (2017) Papillomaviruses in dogs and cats. Vet J 225:23–31. https://doi.org/10.1016/j.tvjl.2017.04.018

    Article  PubMed  Google Scholar 

  4. Munday JS, O’Connor KI, Smits B (2011) Development of multiple pigmented viral plaques and squamous cell carcinomas in a dog infected by a novel papillomavirus. Vet Dermatol 22:104–110. https://doi.org/10.1111/j.1365-3164.2010.00913.x

    Article  PubMed  Google Scholar 

  5. Luff J, Rowland P, Mader M, Orr C, Yuan H (2016) Two canine papillomaviruses associated with metastatic squamous cell carcinoma in two related Basenji dogs. Vet Pathol 53:1160–1163. https://doi.org/10.1177/0300985816630795

    Article  CAS  PubMed  Google Scholar 

  6. Van Doorslaer K, Tan Q, Xirasagar S et al (2013) The papillomavirus episteme: a central resource for papillomavirus sequence data and analysis. Nucleic Acids Res 41:D571–D578. https://doi.org/10.1093/nar/gks984

    Article  CAS  PubMed  Google Scholar 

  7. Boom R, Sol CJ, Salimans MM et al (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495–503. https://doi.org/10.1556/AMicr.58.2011.1.7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Forslund O, Antonsson A, Nordin P, Stenquist B, Göran Hansson B (1999) Abroad range of human papilomavírus 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 

  9. Ye J, McGinnis S, Madden TL (2006) BLAST: improvements for better sequence analysis. Nucleic Acids Res 34:W6–W9. https://doi.org/10.1093/nar/gkl164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Castilho JG, Brandão PE, Carnieli P et al (2007) Molecular analysis of the N gene of canine distemper virus in dogs in Brazil. Arq Bras Med Vet Zootec 59:654–659. https://doi.org/10.1590/S0102-09352007000300016

    Article  CAS  Google Scholar 

  11. Frisk AL, König M, Moritz A, Baumgärtner W (1999) Detection of canine distemper virus nucleoprotein RNA by reverse transcription-PCR using serum, whole blood, and cerebrospinal fluid from dogs with distemper. J Clin Microbiol 37:3634–3643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Silva FRC, Cibulski SP, Daudt C et al (2016) Novel bovine papillomavirus type discovered by rolling-circle amplification coupled with next-generation sequencing. PLoS One 11:e0162345. https://doi.org/10.1371/journal.pone.0162345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Dezen D, Rijsewijk FAM, Teixeira TF, Holz CL, Cibulski SP, Franco AC, Dellagostin OA, Roehe PM (2010) Multiply-primed rolling-circle amplification (MPRCA) of PCV2 genomes: applications on detection, sequencing and virus isolation. Res Vet Sci 88:436–440. https://doi.org/10.1016/j.rvsc.2009.10.006

    Article  CAS  PubMed  Google Scholar 

  14. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  18. Luff J, Mader M, Britton M, Fass J, Rowland P, Orr C, Schlegel R, Yuan H (2015) Complete genome sequence of canine papillomavirus type 16. Genome Announc 3:e00404–e00415. https://doi.org/10.1128/genomeA.00404-15

    Article  PubMed  PubMed Central  Google Scholar 

  19. Luff J, Mader M, Rowland P, Britton M, Fass J, Yuan H (2019) Viral genome integration of canine papillomavirus 16. Papillomavirus Res 7:88–96. https://doi.org/10.1016/j.pvr.2019.02.002

    Article  PubMed  PubMed Central  Google Scholar 

  20. Goldschmidt MH, Goldschmidt KH (2017) Epithelial and melanocytic tumors of the skin. In: Meuten D (ed) Tumors of domestic animals, 5th edn. Wiley Blackwell, Ames, Iowa, pp 88–141

    Google Scholar 

  21. Munday JS, Kiupel M (2010) Papillomavirus-associated cutaneous neoplasia in mammals. Vet Pathol 47:254–264

    Article  CAS  PubMed  Google Scholar 

  22. Goldschmidt MH, Kennedy JS, Kennedy DR, Yuan H, Holt DE, Casal ML, Traas AM, Mauldin EA, Moore PF, Henthorn PS, Hartnett BJ, Weinberg KI, Schlegel R, Felsburg PJ (2006) Severe papillomavirus infection progressing to metastatic squamous cell carcinoma in bone marrow-transplanted X-linked SCID dogs. J Virol 80:6621–6628. https://doi.org/10.1128/JVI.02571-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Daudt C, Da Silva FRC, Lunardi M et al (2018) Papillomaviruses in ruminants : An update. Transbound Emerg Dis 65:1381–1395. https://doi.org/10.1111/tbed.12868

    Article  CAS  PubMed  Google Scholar 

  24. Mantovani F, Banks L (2001) The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20:7874–7887. https://doi.org/10.1038/sj.onc.1204869

    Article  CAS  PubMed  Google Scholar 

  25. Münger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, Zacny VL (2001) Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20:7888–7898. https://doi.org/10.1038/sj.onc.1204860

    Article  PubMed  Google Scholar 

  26. Dahiya A, Gavin MR, Luo RX, Dean DC (2000) Role of the LXCXE binding site in Rb function. Mol Cell Biol 20:6799–6805. https://doi.org/10.1128/MCB.20.18.6799-6805.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Finance Code 001, and Propesq/UFRGS.

Author information

Authors and Affiliations

  1. Laboratório de Virologia, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, av. Bento Gonçalves, 9090, Porto Alegre, RS, Brazil

    Christian D. B. T. Alves, Matheus N. Weber, Lorena L. B. Guimarães, Samuel P. Cibulski, Renata F. Budaszewski, Mariana S. Silva & Cláudio W. Canal

  2. Setor de Patologia Veterinária - Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, av. Bento Gonçalves, 9090, Porto Alegre, RS, Brazil

    Lorena L. B. Guimarães, Ronaldo M. Bianchi, Claiton Ismael Schwertz, Cláudio J. M. Laisse & David Driemeier

  3. Laboratório de Biologia Celular e Molecular, Centro de Biotecnologia, Universidade Federal da Paraíba, R. Tab. Stanislau Eloy, 41-769, João Pessoa, Paraíba, Brazil

    Samuel P. Cibulski

  4. Laboratório de Virologia Geral e Parasitologia, Centro de Ciências Biológicas e da Natureza, Universidade Federal do Acre, Rodovia BR 364, Km 04, Rio Branco, AC, Brazil

    Flávio R. C. da Silva & Cíntia Daudt

  5. Laboratório de Biologia Molecular, Instituto de Pesquisas Veterinárias Desidério Finamor (IPVDF), Fundação Estadual de Pesquisa Agropecuária, Estrada Do Conde, 6000, Eldorado do Sul, RS, Brazil

    Fabiana Q. Mayer

  6. Hospital de Clínicas Veterinárias, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul, av. Bento Gonçalves, 9090, Porto Alegre, RS, Brazil

    Carine R. Stefanello & Daniel G. Gerardi

  7. Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Südufer 10, 17493, Greifswald, InselRiems, Germany

    Jens P. Teifke

Authors
  1. Christian D. B. T. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matheus N. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lorena L. B. Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Samuel P. Cibulski
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Flávio R. C. da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cíntia Daudt
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Renata F. Budaszewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mariana S. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fabiana Q. Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ronaldo M. Bianchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Claiton Ismael Schwertz
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Carine R. Stefanello
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Daniel G. Gerardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Cláudio J. M. Laisse
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. David Driemeier
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Jens P. Teifke
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Cláudio W. Canal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cláudio W. Canal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Fernando R. Spilki.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves, C.D.B.T., Weber, M.N., Guimarães, L.L.B. et al. Canine papillomavirus type 16 associated to squamous cell carcinoma in a dog: virological and pathological findings. Braz J Microbiol 51, 2087–2094 (2020). https://doi.org/10.1007/s42770-020-00310-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-020-00310-4

Keywords

Search

Navigation