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Identification and characterization of the genome of a papillomavirus from skin lesions of four-toed hedgehogs (Atelerix albiventris)

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Abstract

The present study describes the clinical and pathological characteristics of skin lesions in two four-toed hedgehogs (Atelerix albiventris). We performed inverse PCR to identify the genome of papillomavirus (PV) in the skin lesions and subsequently sequenced the full genome of the virus, which was tentatively named Atelerix albiventris papillomavirus 1 (AalbPV1). The overall sequences of the viral genomes of both four-toed hedgehogs were identical. This study first identified the presence of a novel PV in Japanese four-toed hedgehogs and provided genetic information about this virus.

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References

  1. Rector A, Van Ranst M (2013) Animal papillomaviruses. Virology 445:213–223. https://doi.org/10.1016/j.virol.2013.05.007

    Article  CAS  PubMed  Google Scholar 

  2. Lunardi M, Alfieri AA, Otonel RAA, de Alcântara BK, Rodrigues WB, de Miranda AB, Alfieri AF (2013) Genetic characterization of a novel bovine papillomavirus member of the Deltapapillomavirus genus. Vet Microbiol 162:207–213. https://doi.org/10.1016/j.vetmic.2012.08.030

    Article  CAS  PubMed  Google Scholar 

  3. Christensen ND, Cladel NM, Reed CA, Han R (2000) Rabbit oral papillomavirus complete genome sequence and immunity following genital infection. Virology 269:451–461. https://doi.org/10.1006/viro.2000.0237

    Article  CAS  PubMed  Google Scholar 

  4. Joh J, Jenson AB, Proctor M, Ingle A, Silva KA, Potter CS et al (2012) Molecular diagnosis of a laboratory mouse papillomavirus (MusPV). Exp Mol Pathol 93:416–421. https://doi.org/10.1016/j.yexmp.2012.07.001

    Article  CAS  PubMed  Google Scholar 

  5. Truchado DA, Moens MA, Callejas S, Pérez-Tris J, Benítez L (2018) Genomic characterization of the first oral avian papillomavirus in a colony of breeding canaries (Serinus canaria). Vet Res Commu 42:111–120

    Article  Google Scholar 

  6. De Villiers EM, 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 

  7. Clifford GM, Smith JS, Aguado T, Franceschi S (2003) Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br J Cancer 89:101–105. https://doi.org/10.1038/sj.bjc.6601024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Muñoz N, Bosch FX, De Sanjosé S, Herrero R, Castellsagué X, Shah KV et al (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348:518–527. https://doi.org/10.1056/NEJMoa021641

    Article  PubMed  Google Scholar 

  9. Matsukura T, Sugase M (2001) Relationships between 80 human papillomavirus genotypes and different grades of cervical intraepithelial neoplasia: association and causality. Virology 283:139–147. https://doi.org/10.1006/viro.2001.0865

    Article  CAS  PubMed  Google Scholar 

  10. Zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350. https://doi.org/10.1038/nrc798

    Article  CAS  PubMed  Google Scholar 

  11. Grce M, Mravak-Stipetić M (2014) Human papillomavirus–associated diseases. Clin Dermatol 32:253–258. https://doi.org/10.1016/j.clindermatol.2013.10.006

    Article  PubMed  Google Scholar 

  12. 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. https://doi.org/10.1111/tbed.122229

    Article  CAS  PubMed  Google Scholar 

  13. Munday JS, Fairley R, Lowery I (2020) Detection of Ovis aries papillomavirus type 2 DNA sequences in a sarcoid-like mass in the mouth of a pig. Vet Microbiol 248:108801. https://doi.org/10.1016/j.vetmic.2020.108801

    Article  CAS  PubMed  Google Scholar 

  14. Kadaja M, Silla T, Ustav E, Ustav M (2009) Papillomavirus DNA replication—from initiation to genomic instability. Virology 384:360–368. https://doi.org/10.1016/j.virol.2008.11.032

    Article  CAS  PubMed  Google Scholar 

  15. Rosty C, Sheffer M, Tsafrir D, Stransky N, Tsafrir I, Peter M et al (2005) Identification of a proliferation gene cluster associated with HPV E6/E7 expression level and viral DNA load in invasive cervical carcinoma. Oncogene 24:7094–7104. https://doi.org/10.1038/sj.onc.1208854

    Article  CAS  PubMed  Google Scholar 

  16. Zheng ZM, Baker CC (2006) Papillomavirus genome structure, expression, and post-transcriptional regulation. Front Biosci 11:2286–2302. https://doi.org/10.2741/1971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Finnen RL, Erickson KD, Chen XS, Garcea RL (2003) Interactions between papillomavirus L1 and L2 capsid proteins. J Virol 77:4818–4826. https://doi.org/10.1128/jvi.77.8.4818-4826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Villanueva R, Morales-Peza N, Castelán-Sánchez I, García-Villa E, Tapia R, Cid-Arregui A et al (2006) Heparin (GAG-hed) inhibits LCR activity of human papillomavirus type 18 by decreasing AP1 binding [GAG-hed]. BMC Cancer 6:218. https://doi.org/10.1186/1471-2407-6-218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sichero L, Sobrinho JS, Villa LL (2012) Identification of novel cellular transcription factors that regulate early promoters of human papillomavirus types 18 and 16. J Infect Dis 206:867–874. https://doi.org/10.1093/infdis/jis430

    Article  CAS  PubMed  Google Scholar 

  20. Okada K, Kondo H, Sumi A, Kagawa Y (2018) A retrospective study of disease incidence in African pygmy hedgehogs (Atelerix albiventris). J Vet Med Sci 80:1504–1510. https://doi.org/10.1292/jvms.18-0238

    Article  PubMed  PubMed Central  Google Scholar 

  21. Raymond JT, Garner MM (2001) Spontaneous tumours in captive African hedgehogs (Atelerix albiventris): a retrospective study. J Comp Pathol 124:128–133. https://doi.org/10.1053/jcpa.2000.0441

    Article  CAS  PubMed  Google Scholar 

  22. Okumura N, Koizumi I, Iwata Y, Yoneya S, Koba R, Kondo H, Shibuya H (2021) Cutaneous papilloma and multicentric squamous cell carcinoma in four-toed hedgehogs (Atelerix albiventris). J Vet Med Sci 83:1726–1729. https://doi.org/10.1292/jvms.21-0302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schulz E, Gottschling M, Bravo IG, Wittstatt U, Stockfleth E, Nindl I (2009) Genomic characterization of the first insectivoran papillomavirus reveals an unusually long, second non-coding region and indicates a close relationship to Betapapillomavirus. J Gen Virol 90:626–633. https://doi.org/10.1099/vir.0.008011-0

    Article  CAS  PubMed  Google Scholar 

  24. Zaugg N, Nespeca G, Hauser B, Ackermann M, Favrot C (2005) Detection of novel papillomaviruses in canine mucosal, cutaneous and in situ squamous cell carcinomas. Vet Dermatol 16:290–298. https://doi.org/10.1111/j.1365-3164.2005.00467.x

    Article  CAS  PubMed  Google Scholar 

  25. Tobler K, Lange C, Carlotti DN, Ackermann M, Favrot C (2008) Detection of a novel papillomavirus in pigmented plaques of four pugs. Vet Dermatol 19:21–25. https://doi.org/10.1111/j.1365-3164.2007.00640.x

    Article  CAS  PubMed  Google Scholar 

  26. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, Chishti AH et al (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275:73–77. https://doi.org/10.1126/science.275.5296.73

    Article  CAS  PubMed  Google Scholar 

  27. Ganti K, Broniarczyk J, Manoubi W, Massimi P, Mittal S, Pim D et al (2015) The human papillomavirus E6 PDZ binding motif: from life cycle to malignancy. Viruses 7:3530–3551. https://doi.org/10.3390/v7072785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Helt AM, Galloway DA (2001) Destabilization of the retinoblastoma tumor suppressor by human papillomavirus type 16 E7 is not sufficient to overcome cell cycle arrest in human keratinocytes. J Virol 75:6737–6747. https://doi.org/10.1128/JVI.75.15.6737-6747.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ma T, Zou N, Lin BY, Chow LT, Harper JW (1999) Interaction between cyclin-dependent kinases and human papillomavirus replication-initiation protein E1 is required for efficient viral replication. Proc Natl Acad Sci USA 96:382–387. https://doi.org/10.1073/pnas.96.2.382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Van Doorslaer K, Rector A, Jenson AB, Sundberg JP, Van Ranst M, Ghim SJ (2007) Complete genomic characterization of a murine papillomavirus isolated from papillomatous lesions of a European harvest mouse (Micromys minutus). J Gen Virol 88:1484–1488. https://doi.org/10.1099/vir.0.82615-0

    Article  CAS  PubMed  Google Scholar 

  31. Matys V, Fricke E, Geffers R, Gössling E, Haubrock M, Hehl R et al (2003) TRANSFAC®: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31:374–378. https://doi.org/10.1093/nar/gkg108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. García-Vallvé S, Iglesias-Rozas JR, Alonso A, Bravo IG (2006) Different papillomaviruses have different repertoires of transcription factor binding sites: convergence and divergence in the upstream regulatory region. BMC Evol Biol 6:20. https://doi.org/10.1186/1471-2148-6-20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by the Academic Frontier Project for Private Universities from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan.

Author information

Author notes

  1. Shigeru Fujita

    Present address: Division of Systems Virology, Department of Infectious Disease Control, International Research Center for Infectious Diseases, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan

Authors and Affiliations

  1. Faculty of Agriculture, Animal Medical Center, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo, 183-8509, Japan

    Yotaro Shimazaki

  2. Laboratory of Veterinary Microbiology, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa-shi, Kanagawa, 252-0880, Japan

    Shion Yoneya, Shigeru Fujita, Ryota Koba & Yukinobu Tohya

  3. IDEXX Laboratories, K.K., 5-8-18 Kajinocho, Koganei-shi, Tokyo, 184-8515, Japan

    Tomomi Nakashima

  4. Ecological Risk Assessment and Control Section Center for Environmental Biology and Ecosystem, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba-shi, Ibaraki, 305-8506, Japan

    Kei Nabeshima

  5. Banquet Animal Hospital, 1-3-23 Mishuku, Setagaya-ku, Tokyo, 154-0005, Japan

    Sumire Sudoh & Katsuki Matsubara

  6. Laboratory of Veterinary Pathology, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa-shi, Kanagawa, 252-0880, Japan

    Naka Okumura & Hirotaka Kondo

  7. Division of Animal Life Science, Institute of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu-shi, Tokyo, 183-8509, Japan

    Koji Nishifuji

Authors
  1. Yotaro Shimazaki
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Contributions

Conceived and designed the experiments, YS and RK; Sample collection, YS, SS, and KM; Performed the experiments, YS, SY, TN, and RK; Analyzed the data, YS, SY, SF, KN, TN, NO, HK, KN, and RK; Wrote original draft, KN and RK; Review and Editing, KN, HK, KN, and YT. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Ryota Koba.

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Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval

All experimental procedures involving animals were approved by the ethics committee of our institution.

Consent to participate

Written informed consent to animal owners in the study was obtained from individual animal owners before specimen collection.

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Edited by Takeshi Noda.

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Shimazaki, Y., Yoneya, S., Fujita, S. et al. Identification and characterization of the genome of a papillomavirus from skin lesions of four-toed hedgehogs (Atelerix albiventris). Virus Genes 59, 234–239 (2023). https://doi.org/10.1007/s11262-022-01965-x

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