Tracking vaginal, anal and oral infection in a mouse papillomavirus infection model.

Noninvasive and practical techniques to longitudinally track viral infection are sought after in clinical practice. We report a proof-of-principle study to monitor the viral DNA copy number using a newly established mouse papillomavirus (MmuPV1) mucosal infection model. We hypothesized that viral presence could be identified and quantified by collecting lavage samples from cervicovaginal, anal and oral sites. Nude mice infected at these sites with infectious MmuPV1 were tracked for up to 23 weeks starting at 6 weeks post-infection. Viral DNA copy number was determined by SYBR Green Q-PCR analysis. In addition, we tracked viral DNA load through three complete oestrous cycles to pinpoint whether there was a correlation between the DNA load and the four stages of the oestrous cycle. Our results showed that high viral DNA copy number was reproducibly detected from both anal and cervicovaginal lavage samples. The infection and disease progression were further confirmed by histology, cytology, in situ hybridization, immunohistochemistry and transmission electron microscopy. Interestingly, the viral copy number fluctuated over the oestrous cycle, with the highest level at the oestrus stage, implying that multiple sampling might be necessary to provide a reliable diagnosis. Virus DNA was detected in oral lavage samples at a later time after infection. Lower viral DNA load was found in oral samples when compared with those in anal and vaginal tracts. To our knowledge, our study is the first in vivo study to sequentially monitor papillomavirus infection from mucosal anal, oral and vaginal tracts in a preclinical model.

[1]  S. Garland Faculty Opinions recommendation of HPV vaccines to prevent cervical cancer and genital warts: an update. , 2017 .

[2]  E. Stier,et al.  Prevalence of anal human papillomavirus infection and anal HPV-related disorders in women: a systematic review. , 2015, American journal of obstetrics and gynecology.

[3]  N. Christensen,et al.  A Novel Pre-Clinical Murine Model to Study the Life Cycle and Progression of Cervical and Anal Papillomavirus Infections , 2015, PloS one.

[4]  X. Cui,et al.  Simple regression for correcting ΔCt bias in RT-qPCR low-density array data normalization , 2015, BMC Genomics.

[5]  J. Palefsky,et al.  Human Papillomavirus in the HIV-Infected Host: Epidemiology and Pathogenesis in the Antiretroviral Era , 2015, Current HIV/AIDS Reports.

[6]  J. Sundberg,et al.  Immune Status, Strain Background, and Anatomic Site of Inoculation Affect Mouse Papillomavirus (MmuPV1) Induction of Exophytic Papillomas or Endophytic Trichoblastomas , 2014, PloS one.

[7]  H. Einarsdóttir,et al.  Anorectal Human Papillomavirus: Current Concepts , 2014, The Yale journal of biology and medicine.

[8]  Mardge H. Cohen,et al.  Long-term cumulative detection of human papillomavirus among HIV seropositive women , 2014, AIDS.

[9]  W. Liszewski,et al.  Anal Pap smears and anal cancer: what dermatologists should know. , 2014, Journal of the American Academy of Dermatology.

[10]  D. Flesch‐Janys,et al.  Feasibility and acceptance of cervicovaginal self-sampling within the German National Cohort (Pretest 2) , 2014, Bundesgesundheitsblatt - Gesundheitsforschung - Gesundheitsschutz.

[11]  B. Giraudeau,et al.  Vaginal self-sampling is a cost-effective way to increase participation in a cervical cancer screening programme: a randomised trial , 2014, British Journal of Cancer.

[12]  D. Lowy,et al.  Strain-Specific Properties and T Cells Regulate the Susceptibility to Papilloma Induction by Mus musculus Papillomavirus 1 , 2014, PLoS pathogens.

[13]  D. Hemingway,et al.  Cancers of the anal canal: diagnosis, treatment and future strategies. , 2014, Future oncology.

[14]  S. WellsJessica,et al.  An integrative review of guidelines for anal cancer screening in HIV-infected persons. , 2014 .

[15]  Xuezheng Sun,et al.  Worldwide incidence of cervical lesions: a systematic review , 2014, Epidemiology and Infection.

[16]  S. Kjaer,et al.  The prevalence of human papillomavirus in colorectal adenomas and adenocarcinomas: a systematic review and meta-analysis. , 2014, European journal of cancer.

[17]  N. Sathish,et al.  Human Papillomavirus (HPV)-associated Oral Cancers and Treatment Strategies , 2014, Journal of dental research.

[18]  H. Rees,et al.  HPV vaccines to prevent cervical cancer and genital warts: an update. , 2014, Vaccine.

[19]  O. Forslund,et al.  Characterization of Human Papillomavirus Type 154 and Tissue Tropism of Gammapapillomaviruses , 2014, PloS one.

[20]  D. Cummings,et al.  Menstrual cycle and detectable human papillomavirus in reproductive-age women: a time series study. , 2013, The Journal of infectious diseases.

[21]  D. Cummings,et al.  Characterizing the Temporal Dynamics of Human Papillomavirus DNA Detectability Using Short-Interval Sampling , 2013, Cancer Epidemiology, Biomarkers & Prevention.

[22]  O. Forslund,et al.  The nasal mucosa contains a large spectrum of human papillomavirus types from the Betapapillomavirus and Gammapapillomavirus genera. , 2013, The Journal of infectious diseases.

[23]  J. Doorbar Latent papillomavirus infections and their regulation. , 2013, Current opinion in virology.

[24]  N. Christensen,et al.  Secondary Infections, Expanded Tissue Tropism, and Evidence for Malignant Potential in Immunocompromised Mice Infected with Mus musculus Papillomavirus 1 DNA and Virus , 2013, Journal of Virology.

[25]  S. Whitehead,et al.  Cyclic changes in HIV shedding from the female genital tract during the menstrual cycle. , 2013, The Journal of infectious diseases.

[26]  C. Pérez,et al.  Human Papillomavirus Infection in Women in Puerto Rico: Agreement Between Physician-Collected and Self-Collected Anogenital Specimens , 2013, Journal of lower genital tract disease.

[27]  J. Sundberg,et al.  Molecular diagnosis of a laboratory mouse papillomavirus (MusPV). , 2012, Experimental and molecular pathology.

[28]  L. Villa,et al.  Cervical human papillomavirus detection is not affected by menstrual phase , 2012, Sexually Transmitted Infections.

[29]  Nicolas Valenzuela,et al.  Performing Vaginal Lavage, Crystal Violet Staining, and Vaginal Cytological Evaluation for Mouse Estrous Cycle Staging Identification , 2012, Journal of visualized experiments : JoVE.

[30]  M. Wiles,et al.  Mouse Estrous Cycle Identification Tool and Images , 2012, PloS one.

[31]  Deepak Mittal,et al.  New Approaches to Immunotherapy for HPV Associated Cancers , 2011, Cancers.

[32]  A. Kaufmann,et al.  Cervicovaginal Self-Sampling Is a Reliable Method for Determination of Prevalence of Human Papillomavirus Genotypes in Women Aged 20 to 30 Years , 2011, Journal of Clinical Microbiology.

[33]  J. Fortenberry,et al.  Reactions to Self-Sampling for Ano-Rectal Sexually Transmitted Infections Among Men Who Have Sex with Men: A Qualitative Study , 2011, Archives of sexual behavior.

[34]  D. Radice,et al.  Self-collected human papillomavirus testing acceptability: comparison of two self-sampling modalities. , 2011, Journal of women's health.

[35]  C. Kaushic,et al.  Increased prevalence of sexually transmitted viral infections in women: the role of female sex hormones in regulating susceptibility and immune responses. , 2011, Journal of reproductive immunology.

[36]  W. Quint,et al.  Effect of the Menstrual Cycle and Hormonal Contraceptives on Human Papillomavirus Detection in Young, Unscreened Women , 2010, Obstetrics and gynecology.

[37]  R. Roden,et al.  Papillomavirus Prophylactic Vaccines: Established Successes, New Approaches , 2009, Journal of Virology.

[38]  N. Christensen,et al.  Papillomavirus DNA complementation in vivo. , 2009, Virus research.

[39]  G. McFadden,et al.  Cytokine determinants of viral tropism , 2009, Nature Reviews Immunology.

[40]  C. Caligioni Assessing Reproductive Status/Stages in Mice , 2009, Current protocols in neuroscience.

[41]  A. Waxman Cervical cancer screening in the early post vaccine era. , 2008, Obstetrics and gynecology clinics of North America.

[42]  Mark R. Prausnitz,et al.  Effect of Microneedle Design on Pain in Human Volunteers , 2008, The Clinical journal of pain.

[43]  Mark R Prausnitz,et al.  Pocketed Microneedles for Drug Delivery to the Skin. , 2008, The Journal of physics and chemistry of solids.

[44]  N. Christensen,et al.  Wounding prior to challenge substantially improves infectivity of cottontail rabbit papillomavirus and allows for standardization of infection. , 2008, Journal of virological methods.

[45]  D. Stewart,et al.  Self-collected samples for testing of oncogenic human papillomavirus: a systematic review. , 2007, Journal of obstetrics and gynaecology Canada : JOGC = Journal d'obstetrique et gynecologie du Canada : JOGC.

[46]  P. Choyke,et al.  Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan , 2007, Nature Medicine.

[47]  N. Christensen,et al.  Impact of genetic changes to the CRPV genome and their application to the study of pathogenesis in vivo. , 2007, Virology.

[48]  R. Hogg,et al.  Illustrated Instructions for Self-Collection of Anorectal Swab Specimens and Their Adequacy for Cytological Examination , 2006, Sexually transmitted diseases.

[49]  R. Zanini,et al.  Vertical transmission of the human papillomavirus: a systematic quantitative review. , 2005, Cadernos de saude publica.

[50]  M. Ozbun,et al.  The Minor Capsid Protein L2 Contributes to Two Steps in the Human Papillomavirus Type 31 Life Cycle , 2005, Journal of Virology.

[51]  Andreas Krause,et al.  A standard curve based method for relative real time PCR data processing , 2005, BMC Bioinformatics.

[52]  A. Ashkar,et al.  Progesterone Increases Susceptibility and Decreases Immune Responses to Genital Herpes Infection , 2003, Journal of Virology.

[53]  Q. D. Walker,et al.  Vaginal lavage attenuates cocaine-stimulated activity and establishes place preference in rats , 2002, Pharmacology Biochemistry and Behavior.

[54]  M. Campo,et al.  Animal models of papillomavirus pathogenesis. , 2002, Virus research.

[55]  G W Gough,et al.  Regression of canine oral papillomas is associated with infiltration of CD4+ and CD8+ lymphocytes. , 2001, Virology.

[56]  B. Chohan,et al.  Cervical shedding of herpes simplex virus and cytomegalovirus throughout the menstrual cycle in women infected with human immunodeficiency virus type 1. , 2001, American journal of obstetrics and gynecology.

[57]  T. Carey,et al.  Mucosal swabs detect HPV in laryngeal papillomatosis patients but not family members. , 2000, International journal of pediatric otorhinolaryngology.

[58]  A. García-Sastre,et al.  The Role of Interferon in Influenza Virus Tissue Tropism , 1998, Journal of Virology.

[59]  K. Rosenthal,et al.  Effects of the estrous cycle on local humoral immune responses and protection of intranasally immunized female mice against herpes simplex virus type 2 infection in the genital tract. , 1996, Virology.

[60]  R. Wordinger,et al.  Effect of the estrous cycle on susceptibility of female mice to intravaginal inoculation of herpes simplex virus type 2 (HSV-2). , 1990, Antiviral research.

[61]  N. Schwartz,et al.  Grouped female mice: demonstration of pseudopregnancy. , 1977, Biology of reproduction.

[62]  J. Bogers,et al.  A real-time PCR approach based on SPF10 primers and the INNO-LiPA HPV genotyping extra assay for the detection and typing of human papillomavirus. , 2015, Methods in molecular biology.

[63]  G. Eslick,et al.  Prevalence and risk factors for oral human papillomavirus infection in 129 women screened for cervical HPV infection. , 2014, Oral oncology.

[64]  L. Dušek,et al.  The relationship between the cervical and anal HPV infection in women with cervical intraepithelial neoplasia. , 2014, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[65]  T. Thomas,et al.  An integrative review of guidelines for anal cancer screening in HIV-infected persons. , 2014, AIDS patient care and STDs.

[66]  P. Savelkoul,et al.  Comparison of subgingival bacterial sampling with oral lavage for detection and quantification of periodontal pathogens by real-time polymerase chain reaction. , 2007, Journal of periodontology.

[67]  S. Mocellin,et al.  Complementary techniques: validation of gene expression data by quantitative real time PCR. , 2007, Advances in experimental medicine and biology.

[68]  J. Brandsma The cottontail rabbit papillomavirus model of high-risk HPV-induced disease. , 2005, Methods in molecular medicine.

[69]  A. Taghian,et al.  The nude and SCID mice as a tumor model in experimental cancer biology , 1995 .

[70]  W. O'brien Viral determinants of cellular tropism. , 1992, Pathobiology (Basel).