Distinct malignant epithelial tumors associated with Felis catus papilloma virus type 3 and type 4 co-infection in a domestic cat

Hinata Abe; Nanami X Kato; Mika Tanabe; Taichi Shimabukuro; Saki Hashimoto; Takuya Hirai; Naoyuki Fuke; Saito, Akatsuki

doi:10.51094/jxiv.1905

##article.authors##

Hinata Abe Laboratory of Veterinary Pathology, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki
Nanami X Kato Laboratory of Veterinary Microbiology, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki
Mika Tanabe Veterinary Pathology Diagnostic Center
Taichi Shimabukuro Ryukyu Animal Medical Center
Saki Hashimoto Saki Animal Hospital
Takuya Hirai Laboratory of Veterinary Pathology, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki
Naoyuki Fuke Laboratory of Veterinary Pathology, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki
Saito, Akatsuki Laboratory of Veterinary Microbiology, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki

DOI:

https://doi.org/10.51094/jxiv.1905

キーワード:

Basosquamous cell carcinoma、 Bowenoid in situ carcinoma、 Co-infection、 Felis catus papillomavirus

抄録

A 12-year-8-month-old neutered male American Shorthair cat presented with multiple nail bed masses and an ulcerative lip lesion. PCR identified Felis catus papillomavirus type 3 (FcaPV3) in the nail masses and type 4 (FcaPV4) in the lip lesion. Histopathology revealed basosquamous cell carcinoma (BSCC) in the digits and Bowenoid in situ carcinoma (BISC) in the lip. Tumor cells showed strong p16 positivity and weak or negative pRb and p53 expression. In situ hybridization confirmed FcaPV3 and FcaPV4 E6 genes in digital and lip tumors, respectively. Over six months, viral sequencing showed 23 nucleotide changes in FcaPV3, suggesting viral evolution. This is the first report of distinct malignant epithelial tumors independently induced by FcaPV3 and FcaPV4 in a cat.

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The authors declare no conflict of interest.

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引用文献

Altamura, G., Cuccaro, B., Eleni, C., Strohmayer, C., Brandt, S. and Borzacchiello, G. 2022. Investigation of multiple Felis catus papillomavirus types (-1/-2/-3/-4/-5/-6) DNAs in feline oral squamous cell carcinoma: a multicentric study. J Vet Med Sci. 84: 881–884.

Boyer, S. N., Wazer, D. E. and Band, V. 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56: 4620–4624.

Carvalho, C. C. R., Batista, M. V. A., Silva, M. a. R., Balbino, V. Q. and Freitas, A. C. 2012. Detection of bovine papillomavirus types, co-infection and a putative new BPV11 subtype in cattle. Transbound Emerg Dis. 59: 441–447.

Cunningham, L. L., Pagano, G. M., Li, M., Tandon, R., Holm, S. W., White, D. K. and Lele, S. M. 2006. Overexpression of p16INK4 is a reliable marker of human papillomavirus-induced oral high-grade squamous dysplasia. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 102: 77–81.

Doorbar, J. 2005. The papillomavirus life cycle. J Clin Virol. 32 Suppl 1: S7-15.

Doorbar, J., Quint, W., Banks, L., Bravo, I. G., Stoler, M., Broker, T. R. and Stanley, M. A. 2012. The biology and life-cycle of human papillomaviruses. Vaccine. 30 Suppl 5: F55-70.

Dunowska, M., Munday, J. S., Laurie, R. E. and Hills, S. F. K. 2014. Genomic characterisation of Felis catus papillomavirus 4, a novel papillomavirus detected in the oral cavity of a domestic cat. Virus Genes. 48: 111–119.

Graham, S. V. 2017. The human papillomavirus replication cycle, and its links to cancer progression: a comprehensive review. Clin Sci (Lond). 131: 2201–2221.

Houghton, O. and McCluggage, W. G. 2009. The expression and diagnostic utility of p63 in the female genital tract. Adv Anat Pathol. 16: 316–321.

Ito, S., Chambers, J. K., Sumi, A., Yamashita-Kawanishi, N., Omachi, T., Haga, T., Nakayama, H. and Uchida, K. 2022. Involvement of Felis catus papillomavirus type 2 in the tumorigenesis of feline Merkel cell carcinoma. Vet Pathol. 59: 63–74.

Klaes, R., Friedrich, T., Spitkovsky, D., Ridder, R., Rudy, W., Petry, U., Dallenbach-Hellweg, G., Schmidt, D. and von Knebel Doeberitz, M. 2001. Overexpression of p16(INK4A) as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer. 92: 276–284.

Lange, C. E., Jennings, S. H., Diallo, A. and Lyons, J. 2019. Canine papillomavirus types 1 and 2 in classical papillomas: High abundance, different morphological associations and frequent co-infections. Vet J. 250: 1–5.

Mack, Z. E., Caserta, L. C., Renshaw, R. W., Nakagun, S., Gerdes, R. S., Diel, D. G., Childs-Sanford, S. E. and Peters-Kennedy, J. 2023. Histopathologic and molecular characterization of Erethizon dorsatum papillomavirus 1 and Erethizon dorsatum papillomavirus 2 infection in North American porcupines (Erethizon dorsatum). Vet Pathol. 60: 898–904.

Mazzei, M., Forzan, M., Carlucci, V., Anfossi, A. G., Alberti, A., Albanese, F., Binanti, D., Millanta, F., Baroncini, L., Pirone, A. and Abramo, F. 2018. A study of multiple Felis catus papillomavirus types (1, 2, 3, 4) in cat skin lesions in Italy by quantitative PCR. J Feline Med Surg. 20: 772–779.

McBride, A. A. 2013. The papillomavirus E2 proteins. Virology. 445: 57–79.

Medeiros-Fonseca, B., Faustino-Rocha, A. I., Medeiros, R., Oliveira, P. A. and Gil da Costa, R. M. 2023. Canine and feline papillomaviruses: an update. Front Vet Sci. 10: 1174673.

Munday, J. S. 2014. Bovine and human papillomaviruses: a comparative review. Vet Pathol. 51: 1063–1075.

Munday, J. S. 2014. Papillomaviruses in felids. Vet J. 199: 340–347.

Munday, J. S., French, A. and Thomson, N. 2017. Detection of DNA sequences from a novel papillomavirus in a feline basal cell carcinoma. Vet Dermatol. 28: 236-e60.

Munday, J. S. and Knight, C. G. 2024. Papillomaviruses and Papillomaviral Disease in Dogs and Cats: A Comprehensive Review. Pathogens. 13: 1057.

Munday, J. S. and Thomson, N. A. 2021. Papillomaviruses in Domestic Cats. Viruses. 13: 1664.

Munday, J. S., Thomson, N. A. and Luff, J. A. 2017. Papillomaviruses in dogs and cats. Vet J. 225: 23–31.

Oyervides-Muñoz, M. A., Pérez-Maya, A. A., Sánchez-Domínguez, C. N., Berlanga-Garza, A., Antonio-Macedo, M., Valdéz-Chapa, L. D., Cerda-Flores, R. M., Trevino, V., Barrera-Saldaña, H. A. and Garza-Rodríguez, M. L. 2020. Multiple HPV Infections and Viral Load Association in Persistent Cervical Lesions in Mexican Women. Viruses. 12: 380.

Ozbun, M. A. 2002. Human papillomavirus type 31b infection of human keratinocytes and the onset of early transcription. J Virol. 76: 11291–11300.

Parry, D., Bates, S., Mann, D. J. and Peters, G. 1995. Lack of cyclin D-Cdk complexes in Rb-negative cells correlates with high levels of p16INK4/MTS1 tumour suppressor gene product. EMBO J. 14: 503–511.

Santos, E. U. D., Silva, M. a. R., Pontes, N. E., Coutinho, L. C. A., Paiva, S. S. L., Castro, R. S. and Freitas, A. C. 2016. Detection of Different Bovine Papillomavirus Types and Co-infection in Bloodstream of Cattle. Transbound Emerg Dis. 63: e103-108.

Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J. and Howley, P. M. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell. 63: 1129–1136.

Schindler, S., Magalhães, R. A., Costa, E. L. F. and Brites, C. 2022. Genital Cytokines in HIV/Human Papillomavirus Co-Infection: A Systematic Review. AIDS Res Hum Retroviruses. 38: 683–691.

Steurer, S., Riemann, C., Büscheck, F., Luebke, A. M., Kluth, M., Hube-Magg, C., Hinsch, A., Höflmayer, D., Weidemann, S., Fraune, C., Möller, K., Menz, A., Fisch, M., Rink, M., Bernreuther, C., Lebok, P., Clauditz, T. S., Sauter, G., Uhlig, R., Wilczak, W., Dum, D., Simon, R., Minner, S., Burandt, E., Krech, R., Krech, T. and Marx, A. H. 2021. p63 expression in human tumors and normal tissues: a tissue microarray study on 10,200 tumors. Biomark Res. 9: 7.

Sumi, A., Chambers, J. K., Ito, S., Kojima, K., Omachi, T., Doi, M. and Uchida, K. 2024. Different expression patterns of p63 and p73 in Felis catus papillomavirus type 2-associated feline Merkel cell carcinomas and other epidermal carcinomas. J Vet Med Sci. 86: 39–48.

Vascellari, M., Mazzei, M., Zanardello, C., Melchiotti, E., Albanese, F., Forzan, M., Croce, M. F., Alberti, A. and Abramo, F. 2019. Felis catus Papillomavirus Types 1, 2, 3, 4, and 5 in Feline Bowenoid in Situ Carcinoma: An In Situ Hybridization Study. Vet Pathol. 56: 818–825.

Warren, C. J., Van Doorslaer, K., Pandey, A., Espinosa, J. M. and Pyeon, D. 2015. Role of the host restriction factor APOBEC3 on papillomavirus evolution. Virus Evol. 1: vev015.

Westra, W. H. 2014. Detection of human papillomavirus (HPV) in clinical samples: evolving methods and strategies for the accurate determination of HPV status of head and neck carcinomas. Oral Oncol. 50: 771–779.

Zhu, B., Xiao, Y., Yeager, M., Clifford, G., Wentzensen, N., Cullen, M., Boland, J. F., Bass, S., Steinberg, M. K., Raine-Bennett, T., Lee, D., Burk, R. D., Pinheiro, M., Song, L., Dean, M., Nelson, C. W., Burdett, L., Yu, K., Roberson, D., Lorey, T., Franceschi, S., Castle, P. E., Walker, J., Zuna, R., Schiffman, M. and Mirabello, L. 2020. Mutations in the HPV16 genome induced by APOBEC3 are associated with viral clearance. Nat Commun. 11: 886.