Skin coat color-dependent risks and risk factors of squamous cell carcinoma and deafness of domestic cats inferred via RNA-seq data

The ribonucleic acid-sequencing (RNA-seq) data of skin cells from domestic cats with brown, orange, and white coats were analyzed using a public database to investigate the relationship between coat color-related gene expression and squamous cell carcinoma risk, as well as the mechanism of deafness in white cats. We found that the ratio of the expression level of genes suppressing squamous cell carcinoma to that of genes promoting squamous cell carcinoma was significantly lower than the theoretical estimation in skin cells with orange coats in white-spotted cat. We also found frequent production of KIT lacking the first exon (d1KIT) in skin cells with white coats, and d1KIT production exhibited a significant negative correlation with the expression of SOX10, which is essential for melanocyte formation and adjustment of hearing function. Additionally, the production of d1KIT was expected to be due to the insulating activity of the feline endogenous retrovirus 1 (FERV1) LTR in the 1st intron of KIT and its CTCF binding sequence repeat. These results are expected to contribute to basic veterinary research to understand the relationship between cat skin coat and disease risk, as well as the underlying mechanism.

[1]  T. Obayashi,et al.  COXPRESdb v8: an animal gene coexpression database navigating from a global view to detailed investigations , 2022, Nucleic Acids Res..

[2]  F. Muller,et al.  An Optimized Bioassay for Screening Combined Anticoronaviral Compounds for Efficacy against Feline Infectious Peritonitis Virus with Pharmacokinetic Analyses of GS-441524, Remdesivir, and Molnupiravir in Cats , 2022, Viruses.

[3]  J. Requicha,et al.  Feline Oral Squamous Cell Carcinoma: A Critical Review of Etiologic Factors , 2022, Veterinary sciences.

[4]  J. D. dos Reis,et al.  Developing a Feline Immunodeficiency Virus Subtype B Vaccine Prototype Using a Recombinant MVA Vector , 2022, Vaccines.

[5]  J. Pedraza-Chaverri,et al.  Pathological Similarities in the Development of Papillomavirus-Associated Cancer in Humans, Dogs, and Cats , 2022, Animals : an open access journal from MDPI.

[6]  S. Brandt,et al.  Investigation of multiple Felis catus papillomavirus types (-1/-2/-3/-4/-5/-6) DNAs in feline oral squamous cell carcinoma: a multicentric study , 2022, The Journal of veterinary medical science.

[7]  A. McCann,et al.  Comparative gene expression study highlights molecular similarities between triple negative breast cancer tumours and feline mammary carcinomas , 2022, Veterinary and comparative oncology.

[8]  Eun Jung Kwon,et al.  Identification of differentially expressed genes and pathways for risk stratification in HPV-associated cancers governing different anatomical sites. , 2022, Frontiers in bioscience.

[9]  James E. Allen,et al.  Ensembl 2022 , 2021, Nucleic Acids Res..

[10]  M. Krockenberger,et al.  Do papillomaviruses cause feline cutaneous squamous cell carcinoma? , 2021, Veterinary Evidence.

[11]  Wei Sun,et al.  Sox10 Gene is Required for the Survival of Saccular and Utricular Hair Cells , 2021 .

[12]  K. Uchida,et al.  Full-genome characterization of a novel Felis catus papillomavirus 4 subtype identified in a cutaneous squamous cell carcinoma of a domestic cat , 2021, Virus Genes.

[13]  E. Kyrodimos,et al.  C-Fos Digital Expression Analysis in Human PapillomavirusRelated Oral Squamous Cell Carcinoma , 2021 .

[14]  L. Lyons,et al.  Mining the 99 Lives Cat Genome Sequencing Consortium database implicates genes and variants for the Ticked locus in domestic cats (Felis catus) , 2021, Animal genetics.

[15]  D. Gunn-Moore,et al.  Cognitive Dysfunction in Cats: Update on Neuropathological and Behavioural Changes Plus Clinical Management. , 2021, The Veterinary record.

[16]  S. O’Brien,et al.  Ultracontinuous Single Haplotype Genome Assemblies for the Domestic Cat (Felis catus) and Asian Leopard Cat (Prionailurus bengalensis) , 2020, The Journal of heredity.

[17]  C. Quinn,et al.  "Exosomes as Biomarkers of Human and Feline Mammary Tumours; A Comparative Medicine Approach to Unravelling the Aggressiveness of TNBC". , 2020, Biochimica et biophysica acta. Reviews on cancer.

[18]  C. Badoual,et al.  HPV Detection in Head and Neck Squamous Cell Carcinomas: What Is the Issue? , 2020, Frontiers in Oncology.

[19]  R. Hofmann-Lehmann,et al.  Feline leukaemia virus infection: A practical approach to diagnosis , 2020, Journal of feline medicine and surgery.

[20]  L. Poncelet,et al.  The acoustically evoked short latency negative response (ASNR) in a unilaterally deaf cat with histologically-confirmed cochleosaccular degeneration , 2020, BMC Veterinary Research.

[21]  M. Shi,et al.  Identification of a Novel Papillomavirus Associated with Squamous Cell Carcinoma in a Domestic Cat , 2019, Viruses.

[22]  J. van Dijk,et al.  Prevalence of congenital sensorineural deafness in a population of client‐owned purebred kittens in the United Kingdom , 2019, Journal of veterinary internal medicine.

[23]  J. Vilo,et al.  g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update) , 2019, Nucleic Acids Res..

[24]  R. Malik,et al.  Diagnosing feline immunodeficiency virus (FIV) and feline leukaemia virus (FeLV) infection: an update for clinicians. , 2019, Australian veterinary journal.

[25]  N. Pedersen,et al.  Efficacy and safety of the nucleoside analog GS-441524 for treatment of cats with naturally occurring feline infectious peritonitis , 2019, Journal of feline medicine and surgery.

[26]  Steven J. M. Jones,et al.  CancerMine: a literature-mined resource for drivers, oncogenes and tumor suppressors in cancer , 2018, Nature Methods.

[27]  N. Husain,et al.  Human papillomavirus associated head and neck squamous cell carcinoma: Controversies and new concepts. , 2017, Journal of oral biology and craniofacial research.

[28]  J. Munday,et al.  Papillomaviruses in dogs and cats. , 2017, Veterinary journal.

[29]  G. M. Strain Hearing disorders in cats: Classification, pathology and diagnosis , 2017, Journal of feline medicine and surgery.

[30]  K. Yamamura,et al.  Impact of feline AIM on the susceptibility of cats to renal disease , 2016, Scientific Reports.

[31]  L. Pacini,et al.  Transforming properties of Felis catus papillomavirus type 2 E6 and E7 putative oncogenes in vitro and their transcriptional activity in feline squamous cell carcinoma in vivo. , 2016, Virology.

[32]  E. Nora,et al.  CTCF and Cohesin in Genome Folding and Transcriptional Gene Regulation. , 2016, Annual review of genomics and human genetics.

[33]  F. Adega,et al.  Cat Mammary Tumors: Genetic Models for the Human Counterpart , 2016, Veterinary sciences.

[34]  K. Dittmer,et al.  Frequent detection of transcriptionally active Felis catus papillomavirus 2 in feline cutaneous squamous cell carcinomas. , 2016, The Journal of general virology.

[35]  F. Millanta,et al.  Correlation Between Cyclo-oxygenase-2 and Vascular Endothelial Growth Factor Expression in Canine and Feline Squamous Cell Carcinomas. , 2016, Journal of comparative pathology.

[36]  Yusuke Suzuki,et al.  Apoptosis inhibitor of macrophage protein enhances intraluminal debris clearance and ameliorates acute kidney injury in mice , 2016, Nature Medicine.

[37]  T. Tokuda,et al.  The domestic cat as a natural animal model of Alzheimer’s disease , 2015, Acta neuropathologica communications.

[38]  G. M. Strain The Genetics of Deafness in Domestic Animals , 2015, Front. Vet. Sci..

[39]  Rachael Thomas,et al.  Cytogenomics of Feline Cancers: Advances and Opportunities , 2015, Veterinary sciences.

[40]  C. Cannon Cats, Cancer and Comparative Oncology , 2015, Veterinary sciences.

[41]  S. Lomber,et al.  Deaf white cats , 2015, Current Biology.

[42]  B. Cardazzo,et al.  Triple-negative vimentin-positive heterogeneous feline mammary carcinomas as a potential comparative model for breast cancer , 2014, BMC Veterinary Research.

[43]  A. Schäffer,et al.  Endogenous Retrovirus Insertion in the KIT Oncogene Determines White and White spotting in Domestic Cats , 2014, G3: Genes, Genomes, Genetics.

[44]  Ying Yue,et al.  Human papillomavirus oncoproteins and apoptosis (Review) , 2013, Experimental and therapeutic medicine.

[45]  M. Kiupel,et al.  Feline mammary basal-like adenocarcinomas: a potential model for human triple-negative breast cancer (TNBC) with basal-like subtype , 2013, BMC Cancer.

[46]  Wei Shi,et al.  featureCounts: an efficient general purpose program for assigning sequence reads to genomic features , 2013, Bioinform..

[47]  Yan Cui,et al.  CTCFBSDB 2.0: a database for CTCF-binding sites and genome organization , 2012, Nucleic Acids Res..

[48]  J. Munday,et al.  Loss of Retinoblastoma Protein, But Not p53, Is Associated With the Presence of Papillomaviral DNA in Feline Viral Plaques, Bowenoid In Situ Carcinomas, and Squamous Cell Carcinomas , 2012, Veterinary pathology.

[49]  J. Munday,et al.  Papillomaviral DNA and increased p16CDKN2A protein are frequently present within feline cutaneous squamous cell carcinomas in ultraviolet-protected skin. , 2011, Veterinary dermatology.

[50]  K. Newkirk,et al.  Detection of human papillomavirus DNA in feline premalignant and invasive squamous cell carcinoma. , 2011, Veterinary dermatology.

[51]  L. Marconato,et al.  Epidermal growth factor receptor expression is predictive of poor prognosis in feline cutaneous squamous cell carcinoma , 2010, Journal of feline medicine and surgery.

[52]  A. Schäffer,et al.  Defining and Mapping Mammalian Coat Pattern Genes: Multiple Genomic Regions Implicated in Domestic Cat Stripes and Spots , 2010, Genetics.

[53]  D. Mager,et al.  Endogenous retroviral LTRs as promoters for human genes: a critical assessment. , 2009, Gene.

[54]  J. Califano,et al.  Human Papillomavirus and Head and Neck Squamous Cell Carcinoma: Recent Evidence and Clinical Implications , 2009, Journal of dental research.

[55]  A. Schäffer,et al.  A Domestic cat X Chromosome Linkage Map and the Sex-Linked orange Locus: Mapping of orange, Multiple Origins and Epistasis Over nonagouti , 2009, Genetics.

[56]  M. Kiupel,et al.  Amplification of papillomaviral DNA sequences from a high proportion of feline cutaneous in situ and invasive squamous cell carcinomas using a nested polymerase chain reaction. , 2008, Veterinary dermatology.

[57]  H. Aburatani,et al.  Cohesin mediates transcriptional insulation by CCCTC-binding factor , 2008, Nature.

[58]  Stephan Sauer,et al.  Cohesins Functionally Associate with CTCF on Mammalian Chromosome Arms , 2008, Cell.

[59]  S. Heid,et al.  Does a pleiotropic gene explain deafness and blue irises in white cats? , 2007, Veterinary journal.

[60]  M. Thomson Squamous cell carcinoma of the nasal planum in cats and dogs. , 2007, Clinical techniques in small animal practice.

[61]  A. Schäffer,et al.  A homozygous single-base deletion in MLPH causes the dilute coat color phenotype in the domestic cat. , 2006, Genomics.

[62]  R. Grahn,et al.  Albinism in the domestic cat (Felis catus) is associated with a tyrosinase (TYR) mutation , 2006, Animal genetics.

[63]  Sandya Liyanarachchi,et al.  Genome-wide analysis of core promoter elements from conserved human and mouse orthologous pairs , 2006, BMC Bioinformatics.

[64]  S. O’Brien,et al.  Tyrosinase and tyrosinase related protein 1 alleles specify domestic cat coat color phenotypes of the albino and brown loci. , 2005, The Journal of heredity.

[65]  Thomas Werner,et al.  MatInspector and beyond: promoter analysis based on transcription factor binding sites , 2005, Bioinform..

[66]  L. Lyons,et al.  Chocolate coated cats: TYRP1 mutations for brown color in domestic cats , 2005, Mammalian Genome.

[67]  Naum I. Gershenzon,et al.  Synergy of human Pol II core promoter elements revealed by statistical sequence analysis , 2005, Bioinform..

[68]  Dixie L Mager,et al.  An endogenous retroviral long terminal repeat is the dominant promoter for human β1,3-galactosyltransferase 5 in the colon , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[69]  A. Moore,et al.  Environmental and lifestyle risk factors for oral squamous cell carcinoma in domestic cats. , 2003, Journal of veterinary internal medicine.

[70]  M. Churchill,et al.  A compilation of cellular transcription factor interactions with the HIV-1 LTR promoter. , 2000, Nucleic acids research.

[71]  T. Burke,et al.  The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila. , 1997, Genes & development.

[72]  T. Burke,et al.  Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-box-deficient promoters. , 1996, Genes & development.

[73]  B. Berkhout,et al.  Comparison of 5' and 3' long terminal repeat promoter function in human immunodeficiency virus , 1994, Journal of virology.

[74]  K. Helton,et al.  Multicentric Squamous Cell Carcinoma in situ Resembling Bowen's Disease in Cats , 1993, Veterinary pathology.

[75]  K. Brown,et al.  White fur, blue eyes, and deafness in the domestic cat. , 1971, The Journal of heredity.

[76]  R. E. Schneider,et al.  Sunlight exposure and risk of developing cutaneous and oral squamous cell carcinomas in white cats. , 1971, Journal of the National Cancer Institute.

[77]  J. Black,et al.  Xeroderma Pigmentosum , 2016, Head and Neck Pathology.

[78]  M. Menotti-Raymond,et al.  Feline deafness. , 2012, The Veterinary clinics of North America. Small animal practice.

[79]  G. M. Strain Aetiology, prevalence and diagnosis of deafness in dogs and cats. , 1996, The British veterinary journal.