Molecular Mechanisms of MmuPV1 E6 and E7 and Implications for Human Disease
Abstract
:1. Introduction
2. Oncogenic Activities of High-Risk HPVs
3. Biological Activities of E6 and E7 Proteins Encoded by Cutaneous HPVs
4. Animal Models for Studying Oncogenic Activities of PVs
4.1. Transgenic Animal Models
4.2. Natural Infection Models
4.3. MmuPV1 Infection-Based Mouse Model System: A New Era for PV Research
5. Biological Activities of the MmuPV1 E6 and E7 Proteins
5.1. Known Activities of the MmuPV1 E6 Protein
5.2. Known Activities of MmuPV1 E7
6. How do MmuPV1 E6 and E7 Relate to the HPV E6 and E7 Proteins?
6.1. Similarities between MmuPV1 and Cutaneous HPV E6 Proteins
6.2. Cellular Targets and Effectors of MmuPV1 E7—Insights for HPV Pathogenesis
7. Conclusions and Future Directions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- De Martel, C.; Ferlay, J.; Franceschi, S.; Vignat, J.; Bray, F.; Forman, D.; Plummer, M. Global burden of cancers attributable to infections in 2008: A review and synthetic analysis. Lancet Oncol. 2012, 13, 607–615. [Google Scholar] [CrossRef]
- Moore, P.S.; Chang, Y. Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat. Cancer 2010, 10, 878–889. [Google Scholar] [CrossRef] [PubMed]
- Egan, C.; Bayley, S.T.; Branton, P.E. Binding of the Rb1 protein to E1A products is required for adenovirus transformation. Oncogene 1989, 4, 383–388. [Google Scholar]
- DeCaprio, J.A.; Ludlow, J.W.; Figge, J.; Shew, J.Y.; Huang, C.M.; Lee, W.H.; Marsilio, E.; Paucha, E.; Livingston, D.M. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 1988, 54, 275–283. [Google Scholar] [CrossRef]
- O’Reilly, D.R. p53 and transformation by SV40. Biol. Cell 1986, 57, 187–196. [Google Scholar] [CrossRef] [PubMed]
- Dyson, N.; Howley, P.M.; Münger, K.; Harlow, E. The Human Papilloma Virus-16 E7 Oncoprotein Is Able to Bind to the Retinoblastoma Gene Product. Science 1989, 243, 934–937. [Google Scholar] [CrossRef]
- Huibregtse, J.M.; Scheffner, M.; Howley, P.M. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J. 1991, 10, 4129–4135. [Google Scholar] [CrossRef] [PubMed]
- Mathey-Prevot, B.; Baltimore, D. Specific transforming potential of oncogenes encoding protein-tyrosine kinases. EMBO J. 1985, 4, 1769–1774. [Google Scholar] [CrossRef]
- zur Hausen, H. Papillomaviruses in the causation of human cancers—A brief historical account. Virology 2009, 384, 260–265. [Google Scholar] [CrossRef]
- Forman, D.; de Martel, C.; Lacey, C.J.; Soerjomataram, I.; Lortet-Tieulent, J.; Bruni, L.; Vignat, J.; Ferlay, J.; Bray, F.; Plummer, M.; et al. Global Burden of Human Papillomavirus and Related Diseases. Vaccine 2012, 30, F12–F23. [Google Scholar] [CrossRef]
- Liu, L. Fields Virology, 6th Edition. Clin. Infect. Dis. 2014, 59, 613. [Google Scholar] [CrossRef]
- McBride, A.A. Human papillomaviruses: Diversity, infection and host interactions. Nat. Rev. Microbiol. 2021, 20, 95–108. [Google Scholar] [CrossRef] [PubMed]
- IARC. Biological Agents. 2007. Available online: https://monographs.iarc.who.int/wp-content/uploads/2018/06/mono100B-11.pdf (accessed on 1 September 2022).
- Howley, P.M.; Pfister, H.J. Beta genus papillomaviruses and skin cancer. Virology 2015, 479–480, 290–296. [Google Scholar] [CrossRef]
- Meyers, J.M.; Munger, K. The Viral Etiology of Skin Cancer. J. Investig. Dermatol. 2014, 134, E29–E32. [Google Scholar] [CrossRef] [PubMed]
- Rollison, D.E.; Viarisio, D.; Amorrortu, R.P.; Gheit, T.; Tommasino, M. An Emerging Issue in Oncogenic Virology: The Role of Beta Human Papillomavirus Types in the Development of Cutaneous Squamous Cell Carcinoma. J. Virol. 2019, 93, e01003-18. [Google Scholar] [CrossRef]
- Jablonska, S.; Majewski, S.; Obalek, S.; Orth, G. Cutaneous warts. Clin. Dermatol. 1997, 15, 309–319. [Google Scholar] [CrossRef]
- Jablonska, S.; Orth, G.; Obalek, S.; Croissant, O. Cutaneous warts clinical, histologic, and virologic correlations. Clin. Dermatol. 1985, 3, 71–82. [Google Scholar] [CrossRef]
- Tschandl, P.; Rosendahl, C.; Kittler, H. Cutaneous Human Papillomavirus Infection: Manifestations and Diagnosis. Curr. Probl. Dermatol. 2014, 45, 92–97. [Google Scholar] [CrossRef]
- Lebwohl, M.G.; Rosen, T.; Stockfleth, E. The role of human papillomavirus in common skin conditions: Current viewpoints and therapeutic options. Cutis 2010, 86, 1–12. [Google Scholar]
- Schaper, I.D.; Marcuzzi, G.P.; Weissenborn, S.J.; Kasper, H.U.; Dries, V.; Smyth, N.; Fuchs, P.; Pfister, H. Development of Skin Tumors in Mice Transgenic for Early Genes of Human Papillomavirus Type 8. Cancer Res. 2005, 65, 1394–1400. [Google Scholar] [CrossRef]
- Viarisio, D.; Müller-Decker, K.; Accardi, R.; Robitaille, A.; Dürst, M.; Beer, K.; Jansen, L.; Flechtenmacher, C.; Bozza, M.; Harbottle, R.; et al. Beta HPV38 oncoproteins act with a hit-and-run mechanism in ultraviolet radiation-induced skin carcinogenesis in mice. PLoS Pathog. 2018, 14, e1006783. [Google Scholar] [CrossRef] [PubMed]
- Viarisio, D.; Mueller-Decker, K.; Kloz, U.; Aengeneyndt, B.; Kopp-Schneider, A.; Gröne, H.-J.; Gheit, T.; Flechtenmacher, C.; Gissmann, L.; Tommasino, M. E6 and E7 from Beta Hpv38 Cooperate with Ultraviolet Light in the Development of Actinic Keratosis-Like Lesions and Squamous Cell Carcinoma in Mice. PLoS Pathog. 2011, 7, e1002125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Viarisio, D.; Decker, K.M.; Aengeneyndt, B.; Flechtenmacher, C.; Gissmann, L.; Tommasino, M. Human papillomavirus type 38 E6 and E7 act as tumour promoters during chemically induced skin carcinogenesis. J. Gen. Virol. 2013, 94, 749–752. [Google Scholar] [CrossRef] [PubMed]
- Iftner, T.; Bierfelder, S.; Csapo, Z.; Pfister, H. Involvement of human papillomavirus type 8 genes E6 and E7 in transformation and replication. J. Virol. 1988, 62, 3655–3661. [Google Scholar] [CrossRef] [PubMed]
- Nishikawa, T.; Yamashita, T.; Yamada, T.; Kobayashi, H.; Ohkawara, A.; Fujinaga, K.; Kei, K. Tumorigenic Transformation of Primary Rat Embryonal Fibroblasts by Human Papillomavirus Type 8 E7 Gene in Collaboration with the Activated H-ras Gene. Jpn. J. Cancer Res. 1991, 82, 1340–1343. [Google Scholar] [CrossRef]
- Schiffman, M.; Clifford, G.; Buonaguro, F.M. Classification of weakly carcinogenic human papillomavirus types: Addressing the limits of epidemiology at the borderline. Infect. Agents Cancer 2009, 4, 8. [Google Scholar] [CrossRef]
- Moody, C.A.; Laimins, L.A. Human papillomavirus oncoproteins: Pathways to transformation. Nat. Cancer 2010, 10, 550–560. [Google Scholar] [CrossRef]
- Mesri, E.A.; Feitelson, M.A.; Munger, K. Human Viral Oncogenesis: A Cancer Hallmarks Analysis. Cell Host Microbe 2014, 15, 266–282. [Google Scholar] [CrossRef]
- Yamashita, T.; Segawa, K.; Fujinaga, Y.; Nishikawa, T.; Fujinaga, K. Biological and biochemical activity of E7 genes of the cutaneous human papillomavirus type 5 and 8. Oncogene 1993, 8, 2433–2441. [Google Scholar]
- Romero-Medina, M.C.; Venuti, A.; Melita, G.; Robitaille, A.; Ceraolo, M.G.; Pacini, L.; Sirand, C.; Viarisio, D.; Taverniti, V.; Gupta, P.; et al. Human papillomavirus type 38 alters wild-type p53 activity to promote cell proliferation via the downregulation of integrin alpha 1 expression. PLoS Pathog. 2020, 16, e1008792. [Google Scholar] [CrossRef]
- Akgül, B.; Pfefferle, R.; Marcuzzi, G.P.; Zigrino, P.; Krieg, T.; Pfister, H.; Mauch, C. Expression of matrix metalloproteinase (MMP)-2, MMP-9, MMP-13, and MT1-MMP in skin tumors of human papillomavirus type 8 transgenic mice. Exp. Dermatol. 2006, 15, 35–42. [Google Scholar] [CrossRef] [PubMed]
- Hufbauer, M.; Lazić, D.; Akgül, B.; Brandsma, J.; Pfister, H.; Weissenborn, S. Enhanced human papillomavirus type 8 oncogene expression levels are crucial for skin tumorigenesis in transgenic mice. Virology 2010, 403, 128–136. [Google Scholar] [CrossRef] [PubMed]
- Marcuzzi, G.P.; Hufbauer, M.; Kasper, H.U.; Weißenborn, S.J.; Smola, S.; Pfister, H. Spontaneous tumour development in human papillomavirus type 8 E6 transgenic mice and rapid induction by UV-light exposure and wounding. J. Gen. Virol. 2009, 90, 2855–2864. [Google Scholar] [CrossRef] [PubMed]
- Dong, W.; Kloz, U.; Accardi, R.; Caldeira, S.; Tong, W.-M.; Wang, Z.-Q.; Jansen, L.; Dürst, M.; Sylla, B.S.; Gissmann, L.; et al. Skin Hyperproliferation and Susceptibility to Chemical Carcinogenesis in Transgenic Mice Expressing E6 and E7 of Human Papillomavirus Type 38. J. Virol. 2005, 79, 14899–14908. [Google Scholar] [CrossRef]
- Ingle, A.; Ghim, S.; Joh, J.; Chepkoech, I.; Jenson, A.B.; Sundberg, J.P. Novel Laboratory Mouse Papillomavirus (MusPV) Infection. Vet. Pathol. 2010, 48, 500–505. [Google Scholar] [CrossRef]
- Ilahi, N.E.; Bhatti, A. Impact of HPV E5 on viral life cycle via EGFR signaling. Microb. Pathog. 2020, 139, 103923. [Google Scholar] [CrossRef]
- Pim, D.; Collins, M.; Banks, L. Human papillomavirus type 16 E5 gene stimulates the transforming activity of the epidermal growth factor receptor. Oncogene 1992, 7, 27–32. [Google Scholar]
- Leechanachai, P.; Banks, L.; Moreau, F.; Matlashewski, G. The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus. Oncogene 1992, 7, 19–25. [Google Scholar]
- Straight, S.W.; Hinkle, P.M.; Jewers, R.J.; McCance, D.J. The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. J. Virol. 1993, 67, 4521–4532. [Google Scholar] [CrossRef]
- Crusius, K.; Auvinen, E.; Steuer, B.; Gaissert, H.; Alonso, A. The Human Papillomavirus Type 16 E5-Protein Modulates Ligand-Dependent Activation of the EGF Receptor Family in the Human Epithelial Cell Line HaCaT. Exp. Cell Res. 1998, 241, 76–83. [Google Scholar] [CrossRef]
- Tomakidi, P.; Cheng, H.; Kohl, A.; Komposch, G.; Alonso, A. Modulation of the epidermal growth factor receptor by the human papillomavirus type 16 E5 protein in raft cultures of human keratinocytes. Eur. J. Cell Biol. 2000, 79, 407–412. [Google Scholar] [CrossRef] [PubMed]
- Straight, S.W.; Herman, B.; McCance, D.J. The E5 oncoprotein of human papillomavirus type 16 inhibits the acidification of endosomes in human keratinocytes. J. Virol. 1995, 69, 3185–3192. [Google Scholar] [CrossRef] [PubMed]
- Münger, K.; Scheffner, M.; Huibregtse, J.M.; Howley, P. Interactions of HPV E6 and E7 oncoproteins with tumour suppressor gene products. Cancer Surv. 1992, 12, 197–217. [Google Scholar]
- Gewin, L.; Galloway, D.A. E Box-Dependent Activation of Telomerase by Human Papillomavirus Type 16 E6 Does Not Require Induction of c- myc. J. Virol. 2001, 75, 7198–7201. [Google Scholar] [CrossRef] [PubMed]
- Gewin, L.; Myers, H.; Kiyono, T.; Galloway, D.A. Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16 E6/E6-AP complex. Genes Dev. 2004, 18, 2269–2282. [Google Scholar] [CrossRef] [PubMed]
- Stöppler, H.; Hartmann, D.-P.; Sherman, L.; Schlegel, R. The Human Papillomavirus Type 16 E6 and E7 Oncoproteins Dissociate Cellular Telomerase Activity from the Maintenance of Telomere Length. J. Biol. Chem. 1997, 272, 13332–13337. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Veldman, T.; Horikawa, I.; Barrett, J.C.; Schlegel, R. Transcriptional Activation of the Telomerase hTERT Gene by Human Papillomavirus Type 16 E6 Oncoprotein. J. Virol. 2001, 75, 4467–4472. [Google Scholar] [CrossRef]
- Watanabe, S.; Kanda, T.; Yoshiike, K. Human papillomavirus type 16 transformation of primary human embryonic fibroblasts requires expression of open reading frames E6 and E7. J. Virol. 1989, 63, 965–969. [Google Scholar] [CrossRef]
- Münger, K.; Phelps, W.C.; Bubb, V.; Howley, P.M.; Schlegel, R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 1989, 63, 4417–4421. [Google Scholar] [CrossRef]
- Hawley-Nelson, P.; Vousden, K.; Hubbert, N.; Lowy, D.; Schiller, J. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 1989, 8, 3905–3910. [Google Scholar] [CrossRef]
- Hudson, J.B.; Bedell, M.A.; McCance, D.J.; Laiminis, L.A. Immortalization and altered differentiation of human keratinocytes in vitro by the E6 and E7 open reading frames of human papillomavirus type 18. J. Virol. 1990, 64, 519–526. [Google Scholar] [CrossRef] [PubMed]
- Sedman, S.A.; Barbosa, M.S.; Vass, W.C.; Hubbert, N.L.; Haas, J.A.; Lowy, D.R.; Schiller, J.T. The full-length E6 protein of human papillomavirus type 16 has transforming and trans-activating activities and cooperates with E7 to immortalize keratinocytes in culture. J. Virol. 1991, 65, 4860–4866. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, S.; Yoshiike, K. Transformation of Rat 3Y1 Cells by a Deletion DNA of Human Papillomavirus Type 16 Molecularly Cloned from Genomic DNA of a Cervical Carcinoma. J. Gen. Virol. 1988, 69, 1431–1435. [Google Scholar] [CrossRef] [PubMed]
- Kanda, T.; Watanabe, S.; Yoshiike, K. Immortalization of primary rat cells by human papillomavirus type 16 subgenomic DNA fragments controlled by the SV40 promoter. Virology 1988, 165, 321–325. [Google Scholar] [CrossRef]
- Chesters, P.M.; Vousden, K.H.; Edmonds, C.; McCance, D.J. Analysis of human papillomavirus type 16 open reading frame E7 immortalizing function in rat embryo fibroblast cells. J. Gen. Virol. 1990, 71, 449–453. [Google Scholar] [CrossRef]
- Barnes, W.; Woodworth, C.; Waggoner, S.; Stoler, M.; Jenson, A.; Delgado, G.; DiPaolo, J. Rapid dysplastic transformation of human genital cells by human papillomavirus type 18. Gynecol. Oncol. 1990, 38, 343–346. [Google Scholar] [CrossRef]
- Waggoner, S.; Woodworth, C.; Stoler, M.; Barnes, W.; Delgado, G.; DiPaolo, J. Human cervical cells immortalized in vitro with oncogenic human papillomavirus DNA differentiate dysplastically in Vivo. Gynecol. Oncol. 1990, 38, 407–412. [Google Scholar] [CrossRef]
- Blanton, R.A.; Perez-Reyes, N.; Merrick, D.T.; McDougall, J.K. Epithelial cells immortalized by human papillomaviruses have premalignant characteristics in organotypic culture. Am. J. Pathol. 1991, 138, 673–685. [Google Scholar]
- Park, N.-H.; Min, B.-M.; Li, S.-L.; Huang, M.Z.; Cherick, H.M.; Doniger, J. Immortalization of normal human oral keratinocytes with type 16 human papillomavirus. Carcinogenesis 1991, 12, 1627–1631. [Google Scholar] [CrossRef]
- Magaldi, T.G.; Almstead, L.L.; Bellone, S.; Prevatt, E.G.; Santin, A.D.; DiMaio, D. Primary human cervical carcinoma cells require human papillomavirus E6 and E7 expression for ongoing proliferation. Virology 2012, 422, 114–124. [Google Scholar] [CrossRef]
- Boyer, S.N.; Wazer, D.E.; Band, V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 1996, 56, 4620–4624. [Google Scholar] [PubMed]
- Jones, D.L.; Münger, K. Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol. 1997, 71, 2905–2912. [Google Scholar] [CrossRef]
- Heck, D.V.; Yee, C.L.; Howley, P.M.; Münger, K. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 1992, 89, 4442–4446. [Google Scholar] [CrossRef] [PubMed]
- Chellappan, S.; Kraus, V.B.; Kroger, B.; Munger, K.; Howley, P.M.; Phelps, W.C.; Nevins, J.R. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. USA 1992, 89, 4549–4553. [Google Scholar] [CrossRef]
- Werness, B.A.; Levine, A.J.; Howley, P.M. Association of Human Papillomavirus Types 16 and 18 E6 Proteins with p53. Science 1990, 248, 76–79. [Google Scholar] [CrossRef] [PubMed]
- Scheffner, M.; Werness, B.A.; Huibregtse, J.M.; Levine, A.J.; Howley, P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990, 63, 1129–1136. [Google Scholar] [CrossRef]
- Katzenellenbogen, R.A.; Egelkrout, E.M.; Vliet-Gregg, P.; Gewin, L.C.; Gafken, P.R.; Galloway, D.A. NFX1-123 and Poly(A) Binding Proteins Synergistically Augment Activation of Telomerase in Human Papillomavirus Type 16 E6-Expressing Cells. J. Virol. 2007, 81, 3786–3796. [Google Scholar] [CrossRef] [Green Version]
- Katzenellenbogen, R.A.; Vliet-Gregg, P.; Xu, M.; Galloway, D.A. NFX1-123 Increases hTERT Expression and Telomerase Activity Posttranscriptionally in Human Papillomavirus Type 16 E6 Keratinocytes. J. Virol. 2009, 83, 6446–6456. [Google Scholar] [CrossRef]
- Katzenellenbogen, R.A.; Vliet-Gregg, P.; Xu, M.; Galloway, D.A. Cytoplasmic Poly(A) Binding Proteins Regulate Telomerase Activity and Cell Growth in Human Papillomavirus Type 16 E6-Expressing Keratinocytes. J. Virol. 2010, 84, 12934–12944. [Google Scholar] [CrossRef]
- Miller, J.; Dakic, A.; Chen, R.; Palechor-Ceron, N.; Dai, Y.; Kallakury, B.; Schlegel, R.; Liu, X. HPV16 E7 Protein and hTERT Proteins Defective for Telomere Maintenance Cooperate to Immortalize Human Keratinocytes. PLoS Pathog. 2013, 9, e1003284. [Google Scholar] [CrossRef]
- Liu, X.; Roberts, J.; Dakic, A.; Zhang, Y.; Schlegel, R. HPV E7 contributes to the telomerase activity of immortalized and tumorigenic cells and augments E6-induced hTERT promoter function. Virology 2008, 375, 611–623. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Dakic, A.; Chen, R.; Disbrow, G.L.; Zhang, Y.; Dai, Y.; Schlegel, R. Cell-Restricted Immortalization by Human Papillomavirus Correlates with Telomerase Activation and Engagement of the hTERT Promoter by Myc. J. Virol. 2008, 82, 11568–11576. [Google Scholar] [CrossRef] [PubMed]
- White, E.A. Manipulation of Epithelial Differentiation by HPV Oncoproteins. Viruses 2019, 11, 369. [Google Scholar] [CrossRef] [PubMed]
- Melar-New, M.; Laimins, L.A. Human Papillomaviruses Modulate Expression of MicroRNA 203 upon Epithelial Differentiation to Control Levels of p63 Proteins. J. Virol. 2010, 84, 5212–5221. [Google Scholar] [CrossRef]
- White, E.A.; Münger, K.; Howley, P. High-Risk Human Papillomavirus E7 Proteins Target PTPN14 for Degradation. mBio 2016, 7, e01530-16. [Google Scholar] [CrossRef]
- Szalmás, A.; Tomaić, V.; Basukala, O.; Massimi, P.; Mittal, S.; Kónya, J.; Banks, L. The PTPN14 Tumor Suppressor Is a Degradation Target of Human Papillomavirus E7. J. Virol. 2017, 91, e00057-17. [Google Scholar] [CrossRef]
- Hatterschide, J.; Bohidar, A.E.; Grace, M.; Nulton, T.J.; Kim, H.W.; Windle, B.; Morgan, I.M.; Munger, K.; White, E.A. PTPN14 degradation by high-risk human papillomavirus E7 limits keratinocyte differentiation and contributes to HPV-mediated oncogenesis. Proc. Natl. Acad. Sci. USA 2019, 116, 7033–7042. [Google Scholar] [CrossRef] [Green Version]
- Hatterschide, J.; Castagnino, P.; Kim, H.W.; Sperry, S.M.; Montone, K.T.; Basu, D.; White, E.A. YAP1 activation by human papillomavirus E7 promotes basal cell identity in squamous epithelia. eLife 2022, 11, e75466. [Google Scholar] [CrossRef]
- Hatterschide, J.; Brantly, A.C.; Grace, M.; Munger, K.; White, E.A. A Conserved Amino Acid in the C Terminus of Human Papillomavirus E7 Mediates Binding to PTPN14 and Repression of Epithelial Differentiation. J. Virol. 2020, 94, e01024-20. [Google Scholar] [CrossRef]
- Nees, M.; Geoghegan, J.M.; Munson, P.; Prabhu, V.; Liu, Y.; Androphy, E.; Woodworth, C.D. Human papillomavirus type 16 E6 and E7 proteins inhibit differentiation-dependent expression of transforming growth factor-beta2 in cervical keratinocytes. Cancer Res. 2000, 60, 4289–4298. [Google Scholar]
- Lee, D.K.; Kim, B.-C.; Kim, I.Y.; Cho, E.-A.; Satterwhite, D.J.; Kim, S.-J. The Human Papilloma Virus E7 Oncoprotein Inhibits Transforming Growth Factor-β Signaling by Blocking Binding of the Smad Complex to Its Target Sequence. J. Biol. Chem. 2002, 277, 38557–38564. [Google Scholar] [CrossRef] [PubMed]
- Dotto, G.P. Notch tumor suppressor function. Oncogene 2008, 27, 5115–5123. [Google Scholar] [CrossRef] [PubMed]
- Strickland, S.W.; Brimer, N.; Lyons, C.; Pol, S.B.V. Human Papillomavirus E6 interaction with cellular PDZ domain proteins modulates YAP nuclear localization. Virology 2018, 516, 127–138. [Google Scholar] [CrossRef] [PubMed]
- Mehta, K.; Laimins, L. High-Risk Human Papillomaviruses and DNA Repair. Recent Results Cancer Res. 2020, 217, 141–155. [Google Scholar] [CrossRef]
- Cigno, I.L.; Calati, F.; Albertini, S.; Gariglio, M. Subversion of Host Innate Immunity by Human Papillomavirus Oncoproteins. Pathogens 2020, 9, 292. [Google Scholar] [CrossRef]
- Gusho, E.; Laimins, L.A. Human papillomaviruses sensitize cells to DNA damage induced apoptosis by targeting the innate immune sensor cGAS. PLoS Pathog. 2022, 18, e1010725. [Google Scholar] [CrossRef]
- Evans, M.; Borysiewicz, L.K.; Evans, A.S.; Rowe, M.; Jones, M.; Gileadi, U.; Cerundolo, V.; Man, S. Antigen Processing Defects in Cervical Carcinomas Limit the Presentation of a CTL Epitope from Human Papillomavirus 16 E6. J. Immunol. 2001, 167, 5420–5428. [Google Scholar] [CrossRef]
- Muench, P.; Probst, S.; Schuetz, J.; Leiprecht, N.; Busch, M.; Wesselborg, S.; Stubenrauch, F.; Iftner, T. Cutaneous Papillomavirus E6 Proteins Must Interact with p300 and Block p53-Mediated Apoptosis for Cellular Immortalization and Tumorigenesis. Cancer Res. 2010, 70, 6913–6924. [Google Scholar] [CrossRef] [Green Version]
- Hussain, I.; Fathallah, I.; Accardi, R.; Yue, J.; Saidj, D.; Shukla, R.; Hasan, U.; Gheit, T.; Niu, Y.; Tommasino, M.; et al. NF-κB Protects Human Papillomavirus Type 38 E6/E7-Immortalized Human Keratinocytes against Tumor Necrosis Factor Alpha and UV-Mediated Apoptosis. J. Virol. 2011, 85, 9013–9022. [Google Scholar] [CrossRef]
- Minoni, L.; Romero-Medina, M.C.; Venuti, A.; Sirand, C.; Robitaille, A.; Altamura, G.; Le Calvez-Kelm, F.; Viarisio, D.; Zanier, K.; Müller, M.; et al. Transforming Properties of Beta-3 Human Papillomavirus E6 and E7 Proteins. mSphere 2020, 5, e00398-20. [Google Scholar] [CrossRef]
- Dacus, D.; Riforgiate, E.; Wallace, N.A. β-HPV 8E6 combined with TERT expression promotes long-term proliferation and genome instability after cytokinesis failure. Virology 2020, 549, 32–38. [Google Scholar] [CrossRef] [PubMed]
- Rehm, T.M.; Straub, E.; Iftner, T.; Stubenrauch, F. Restriction of viral gene expression and replication prevents immortalization of human keratinocytes by a beta-human papillomavirus. Proc. Natl. Acad. Sci. USA 2022, 119, e2118930119. [Google Scholar] [CrossRef] [PubMed]
- Orth, G.; Jablonska, S.; Favre, M.; Croissant, O.; Jarzabek-Chorzelska, M.; Rzesa, G. Characterization of two types of human papillomaviruses in lesions of epidermodysplasia verruciformis. Proc. Natl. Acad. Sci. USA 1978, 75, 1537–1541. [Google Scholar] [CrossRef]
- Neale, R.E.; Weissenborn, S.; Abeni, D.; Bavinck, J.N.B.; Euvrard, S.; Feltkamp, M.C.; Green, A.C.; Harwood, C.; de Koning, M.; Naldi, L.; et al. Human Papillomavirus Load in Eyebrow Hair Follicles and Risk of Cutaneous Squamous Cell Carcinoma. Cancer Epidemiol. Biomark. Prev. 2013, 22, 719–727. [Google Scholar] [CrossRef] [PubMed]
- Chahoud, J.; Semaan, A.; Chen, Y.; Cao, M.; Rieber, A.G.; Rady, P.; Tyring, S.K. Association Between β-Genus Human Papillomavirus and Cutaneous Squamous Cell Carcinoma in Immunocompetent Individuals—A Meta-analysis. JAMA Dermatol. 2016, 152, 1354–1364. [Google Scholar] [CrossRef] [PubMed]
- Pass, F.; Reissig, M.; Shah, K.V.; Eisinger, M.; Orth, G. Identification of an Immunologically Distinct Papillomavirus From Lesions of Epidermodysplasia Verruciformis 2. JNCI J. Natl. Cancer Inst. 1977, 59, 1107–1112. [Google Scholar] [CrossRef]
- Meyers, J.M.; Uberoi, A.; Grace, M.; Lambert, P.F.; Munger, K. Cutaneous HPV8 and MmuPV1 E6 Proteins Target the NOTCH and TGF-β Tumor Suppressors to Inhibit Differentiation and Sustain Keratinocyte Proliferation. PLoS Pathog. 2017, 13, e1006171. [Google Scholar] [CrossRef]
- Brimer, N.; Lyons, C.; Wallberg, A.E.; Pol, S.B.V. Cutaneous papillomavirus E6 oncoproteins associate with MAML1 to repress transactivation and NOTCH signaling. Oncogene 2012, 31, 4639–4646. [Google Scholar] [CrossRef] [Green Version]
- Han, G.; Wang, X.-J. Roles of TGFβ signaling Smads in squamous cell carcinoma. Cell Biosci. 2011, 1, 41. [Google Scholar] [CrossRef]
- Tan, M.J.A.; White, E.A.; Sowa, M.E.; Harper, J.W.; Aster, J.C.; Howley, P.M. Cutaneous β-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling. Proc. Natl. Acad. Sci. USA 2012, 109, E1473–E1480. [Google Scholar] [CrossRef]
- Wang, N.J.; Sanborn, Z.; Arnett, K.L.; Bayston, L.J.; Liao, W.; Proby, C.M.; Leigh, I.M.; Collisson, E.A.; Gordon, P.B.; Jakkula, L.; et al. Loss-of-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 2011, 108, 17761–17766. [Google Scholar] [CrossRef] [PubMed]
- South, A.P.; Purdie, K.J.; Watt, S.A.; Haldenby, S.; Breems, N.Y.D.; Dimon, M.; Arron, S.T.; Kluk, M.J.; Aster, J.C.; McHugh, A.; et al. NOTCH1 Mutations Occur Early during Cutaneous Squamous Cell Carcinogenesis. J. Investig. Dermatol. 2014, 134, 2630–2638. [Google Scholar] [CrossRef] [PubMed]
- Brimer, N.; Drews, C.M.; Pol, S.B.V. Association of papillomavirus E6 proteins with either MAML1 or E6AP clusters E6 proteins by structure, function, and evolutionary relatedness. PLoS Pathog. 2017, 13, e1006781. [Google Scholar] [CrossRef] [PubMed]
- White, E.A.; Kramer, R.E.; Tan, M.J.A.; Hayes, S.D.; Harper, J.W.; Howley, P.M. Comprehensive Analysis of Host Cellular Interactions with Human Papillomavirus E6 Proteins Identifies New E6 Binding Partners and Reflects Viral Diversity. J. Virol. 2012, 86, 13174–13186. [Google Scholar] [CrossRef]
- Wallace, N.; Robinson, K.; Howie, H.L.; Galloway, D.A. β-HPV 5 and 8 E6 Disrupt Homology Dependent Double Strand Break Repair by Attenuating BRCA1 and BRCA2 Expression and Foci Formation. PLoS Pathog. 2015, 11, e1004687. [Google Scholar] [CrossRef]
- Wallace, N.A.; Robinson, K.; Howie, H.L.; Galloway, D.A. HPV 5 and 8 E6 Abrogate ATR Activity Resulting in Increased Persistence of UVB Induced DNA Damage. PLoS Pathog. 2012, 8, e1002807. [Google Scholar] [CrossRef]
- Dacus, D.; Wallace, N.A. Beta-Genus Human Papillomavirus 8 E6 Destabilizes the Host Genome by Promoting p300 Degradation. Viruses 2021, 13, 1662. [Google Scholar] [CrossRef]
- Hufbauer, M.; Cooke, J.; van der Horst, G.; Pfister, H.; Storey, A.; Akgül, B. Human papillomavirus mediated inhibition of DNA damage sensing and repair drives skin carcinogenesis. Mol. Cancer 2015, 14, 183. [Google Scholar] [CrossRef] [Green Version]
- White, E.A.; Walther, J.; Javanbakht, H.; Howley, P.M. Genus Beta Human Papillomavirus E6 Proteins Vary in Their Effects on the Transactivation of p53 Target Genes. J. Virol. 2014, 88, 8201–8212. [Google Scholar] [CrossRef]
- Grace, M.; Munger, K. Proteomic analysis of the gamma human papillomavirus type 197 E6 and E7 associated cellular proteins. Virology 2016, 500, 71–81. [Google Scholar] [CrossRef]
- Wang, J.; Zhou, D.; Prabhu, A.; Schlegel, R.; Yuan, H. The Canine Papillomavirus and Gamma HPV E7 Proteins Use an Alternative Domain to Bind and Destabilize the Retinoblastoma Protein. PLoS Pathog. 2010, 6, e1001089. [Google Scholar] [CrossRef] [PubMed]
- Lambert, P.F.; Pan, H.; Pitot, H.C.; Liem, A.; Jackson, M.; Griep, A.E. Epidermal cancer associated with expression of human papillomavirus type 16 E6 and E7 oncogenes in the skin of transgenic mice. Proc. Natl. Acad. Sci. USA 1993, 90, 5583–5587. [Google Scholar] [CrossRef] [PubMed]
- Griep, A.E.; Lambert, P.F. Role of Papillomavirus Oncogenes in Human Cervical Cancer: Transgenic Animal Studies. Proc. Soc. Exp. Biol. Med. 1994, 206, 24–34. [Google Scholar] [CrossRef] [PubMed]
- Shai, A.; Brake, T.; Somoza, C.; Lambert, P.F. The Human Papillomavirus E6 Oncogene Dysregulates the Cell Cycle and Contributes to Cervical Carcinogenesis through Two Independent Activities. Cancer Res. 2007, 67, 1626–1635. [Google Scholar] [CrossRef] [PubMed]
- Shai, A.; Pitot, H.C.; Lambert, P.F. E6-Associated Protein Is Required for Human Papillomavirus Type 16 E6 to Cause Cervical Cancer in Mice. Cancer Res. 2010, 70, 5064–5073. [Google Scholar] [CrossRef]
- Gulliver, G.A.; Herber, R.L.; Liem, A.; Lambert, P.F. Both conserved region 1 (CR1) and CR2 of the human papillomavirus type 16 E7 oncogene are required for induction of epidermal hyperplasia and tumor formation in transgenic mice. J. Virol. 1997, 71, 5905–5914. [Google Scholar] [CrossRef]
- Jones, D.; Thompson, D.; Münger, K. Destabilization of the RB Tumor Suppressor Protein and Stabilization of p53 Contribute to HPV Type 16 E7-Induced Apoptosis. Virology 1997, 239, 97–107. [Google Scholar] [CrossRef]
- Song, S.; Gulliver, G.A.; Lambert, P.F. Human papillomavirus type 16 E6 and E7 oncogenes abrogate radiation-induced DNA damage responses in vivo through p53-dependent and p53-independent pathways. Proc. Natl. Acad. Sci. USA 1998, 95, 2290–2295. [Google Scholar] [CrossRef] [Green Version]
- Balsitis, S.; Dick, F.; Dyson, N.; Lambert, P.F. Critical Roles for Non-pRb Targets of Human Papillomavirus Type 16 E7 in Cervical Carcinogenesis. Cancer Res. 2006, 66, 9393–9400. [Google Scholar] [CrossRef]
- Park, J.W.; Shin, M.-K.; Pitot, H.C.; Lambert, P.F. High Incidence of HPV-Associated Head and Neck Cancers in FA Deficient Mice Is Associated with E7’s Induction of DNA Damage through Its Inactivation of Pocket Proteins. PLoS ONE 2013, 8, e75056. [Google Scholar] [CrossRef]
- Park, J.W.; Shin, M.-K.; Lambert, P.F. High incidence of female reproductive tract cancers in FA-deficient HPV16-transgenic mice correlates with E7’s induction of DNA damage response, an activity mediated by E7’s inactivation of pocket proteins. Oncogene 2013, 33, 3383–3391. [Google Scholar] [CrossRef] [PubMed]
- Strati, K.; Lambert, P.F. Role of Rb-Dependent and Rb-Independent Functions of Papillomavirus E7 Oncogene in Head and Neck Cancer. Cancer Res. 2007, 67, 11585–11593. [Google Scholar] [CrossRef] [PubMed]
- Shin, M.-K.; Sage, J.; Lambert, P.F. Inactivating All Three Rb Family Pocket Proteins Is Insufficient to Initiate Cervical Cancer. Cancer Res. 2012, 72, 5418–5427. [Google Scholar] [CrossRef] [PubMed]
- Williams, S.M.G.; Disbrow, G.L.; Schlegel, R.; Lee, D.; Threadgill, D.W.; Lambert, P.F. Requirement of Epidermal Growth Factor Receptor for Hyperplasia Induced by E5, a High-Risk Human Papillomavirus Oncogene. Cancer Res. 2005, 65, 6534–6542. [Google Scholar] [CrossRef]
- Maufort, J.P.; Williams, S.M.G.; Pitot, H.C.; Lambert, P.F. Human Papillomavirus 16 E5 Oncogene Contributes to Two Stages of Skin Carcinogenesis. Cancer Res. 2007, 67, 6106–6112. [Google Scholar] [CrossRef] [PubMed]
- Strati, K.; Pitot, H.C.; Lambert, P.F. Identification of biomarkers that distinguish human papillomavirus (HPV)-positive versus HPV-negative head and neck cancers in a mouse model. Proc. Natl. Acad. Sci. USA 2006, 103, 14152–14157. [Google Scholar] [CrossRef]
- Stelzer, M.K.; Pitot, H.C.; Liem, A.; Schweizer, J.; Mahoney, C.; Lambert, P.F. A Mouse Model for Human Anal Cancer. Cancer Prev. Res. 2010, 3, 1534–1541. [Google Scholar] [CrossRef]
- Brake, T.; Lambert, P.F. Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc. Natl. Acad. Sci. USA 2005, 102, 2490–2495. [Google Scholar] [CrossRef] [Green Version]
- Nyman, P.E.; Buehler, D.; Lambert, P.F. Loss of Function of Canonical Notch Signaling Drives Head and Neck Carcinogenesis. Clin. Cancer Res. 2018, 24, 6308–6318. [Google Scholar] [CrossRef]
- Wei, T.; Choi, S.; Buehler, D.; Lee, D.; Ward-Shaw, E.; Anderson, R.; Lambert, P. Role of IQGAP1 in Papillomavirus-Associated Head and Neck Tumorigenesis. Cancers 2021, 13, 2276. [Google Scholar] [CrossRef]
- Shin, M.-K.; Payne, S.; Bilger, A.; Matkowskyj, K.A.; Carchman, E.; Meyer, D.S.; Bentires-Alj, M.; Deming, D.A.; Lambert, P.F. Activating Mutations in Pik3ca Contribute to Anal Carcinogenesis in the Presence or Absence of HPV-16 Oncogenes. Clin. Cancer Res. 2019, 25, 1889–1900. [Google Scholar] [CrossRef]
- Griep, A.E.; Herber, R.; Jeon, S.; Lohse, J.K.; Dubielzig, R.R.; Lambert, P.F. Tumorigenicity by human papillomavirus type 16 E6 and E7 in transgenic mice correlates with alterations in epithelial cell growth and differentiation. J. Virol. 1993, 67, 1373–1384. [Google Scholar] [CrossRef] [PubMed]
- Bergin, I.L.; Bell, J.D.; Chen, Z.; Zochowski, M.K.; Chai, D.; Schmidt, K.; Culmer, D.L.; Aronoff, D.; Patton, D.L.; Mwenda, J.M.; et al. Novel Genital Alphapapillomaviruses in Baboons (Papio hamadryas Anubis) With Cervical Dysplasia. Vet. Pathol. 2012, 50, 200–208. [Google Scholar] [CrossRef]
- Harari, A.; Wood, C.E.; Van Doorslaer, K.; Chen, Z.; Domaingue, M.C.; Elmore, D.; Koenig, P.; Wagner, J.D.; Jennings, R.N.; Burk, R.D. Condylomatous Genital Lesions in Cynomolgus Macaques from Mauritius. Toxicol. Pathol. 2012, 41, 893–901. [Google Scholar] [CrossRef] [PubMed]
- Kloster, B.E.; Manias, D.A.; Ostrow, R.S.; Shaver, M.; McPherson, S.W.; Rangen, S.; Uno, H.; Faras, A.J. Molecular cloning and characterization of the DNA of two papiilomaviruses from monkeys. Virology 1988, 166, 30–40. [Google Scholar] [CrossRef]
- Sostrow, R.; Labresh, K.V.; Faras, A.J. Characterization of the complete RhPV 1 genomic sequence and an integration locus from a metastatic tumor. Virology 1991, 181, 424–429. [Google Scholar] [CrossRef]
- O’Banion, K.; Sundberg, J.P.; Shima, A.L.; Reichmann, M. Venereal Papilloma and Papillomavirus in a Colobus Monkey (Colobus guereza). Intervirology 1987, 28, 232–237. [Google Scholar] [CrossRef]
- Stanley, M.; Moore, R.; Nicholls, P.; Santos, E.; Thomsen, L.; Parry, N.; Walcott, S.; Gough, G. Intra-epithelial vaccination with COPV L1 DNA by particle-mediated DNA delivery protects against mucosal challenge with infectious COPV in beagle dogs. Vaccine 2001, 19, 2783–2792. [Google Scholar] [CrossRef] [Green Version]
- Moore, R.A.; Nicholls, P.K.; Santos, E.B.; Gough, G.W.; Stanley, M.A. Absence of canine oral papillomavirus DNA following prophylactic L1 particle-mediated immunotherapeutic delivery vaccination. J. Gen. Virol. 2002, 83, 2299–2301. [Google Scholar] [CrossRef]
- Kuntsi-Vaattovaara, H.; Verstraete, F.J.M.; Newsome, J.T.; Yuan, H. Resolution of persistent oral papillomatosis in a dog after treatment with a recombinant canine oral papillomavirus vaccine. Vet. Comp. Oncol. 2003, 1, 57–63. [Google Scholar] [CrossRef]
- Johnston, K.B.; Monteiro, J.M.; Schultz, L.D.; Chen, L.; Wang, F.; Ausensi, V.A.; Dell, E.C.; Santos, E.B.; Moore, R.A.; Palker, T.J.; et al. Protection of beagle dogs from mucosal challenge with canine oral papillomavirus by immunization with recombinant adenoviruses expressing codon-optimized early genes. Virology 2005, 336, 208–218. [Google Scholar] [CrossRef] [PubMed]
- Christensen, N.D.; Kreider, J.W.; Kan, N.C.; Diangelo, S.L. The open reading frame L2 of cottontail rabbit papillomavirus contains antibody-inducing neutralizing epitopes. Virology 1991, 181, 572–579. [Google Scholar] [CrossRef]
- Lin, Y.-L.; Borenstein, L.A.; Selvakumar, R.; Ahmed, R.; Wettstein, F.O. Effective vaccination against papilloma development by immunization with L1 or L2 structural protein of cottontail rabbit papillomavirus. Virology 1992, 187, 612–619. [Google Scholar] [CrossRef]
- Lin, Y.L.; Borenstein, L.A.; Ahmed, R.; Wettstein, F.O. Cottontail rabbit papillomavirus L1 protein-based vaccines: Protection is achieved only with a full-length, nondenatured product. J. Virol. 1993, 67, 4154–4162. [Google Scholar] [CrossRef] [PubMed]
- Breitburd, F.; Kirnbauer, R.; Hubbert, N.L.; Nonnenmacher, B.; Trin-Dinh-Desmarquet, C.; Orth, G.; Schiller, J.T.; Lowy, D.R. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. J. Virol. 1995, 69, 3959–3963. [Google Scholar] [CrossRef]
- Olson, C. Cutaneous papillomatosis in cattle and other animals. Ann. N. Y. Acad. Sci. 1963, 108, 1042–1056. [Google Scholar] [CrossRef]
- Lancaster, W.D.; Olson, C.; Meinke, W. Quantitation of bovine papilloma viral DNA in viral-induced tumors. J. Virol. 1976, 17, 824–831. [Google Scholar] [CrossRef]
- Sarver, N.; Rabson, M.S.; Yang, Y.C.; Byrne, J.C.; Howley, P. Localization and analysis of bovine papillomavirus type 1 transforming functions. J. Virol. 1984, 52, 377–388. [Google Scholar] [CrossRef] [Green Version]
- Schiller, J.T.; Vass, W.C.; Lowy, D.R. Identification of a second transforming region in bovine papillomavirus DNA. Proc. Natl. Acad. Sci. USA 1984, 81, 7880–7884. [Google Scholar] [CrossRef]
- Yang, Y.C.; Okayama, H.; Howley, P.M. Bovine papillomavirus contains multiple transforming genes. Proc. Natl. Acad. Sci. USA 1985, 82, 1030–1034. [Google Scholar] [CrossRef]
- Howley, P.; Yang, Y.-C.; Spalholz, B.A.; Rabson, M.S. Papillomavirus Transforming Functions. Ciba Found Symp. 1986, 120, 39–52. [Google Scholar] [CrossRef] [PubMed]
- Schlegel, R.; Wade-Glass, M.; Rabson, M.S.; Yang, Y.-C. The E5 Transforming Gene of Bovine Papillomavirus Encodes a Small, Hydrophobic Polypeptide. Science 1986, 233, 464–467. [Google Scholar] [CrossRef] [PubMed]
- Lambert, P.F.; Howley, P.M. Bovine papillomavirus type 1 E1 replication-defective mutants are altered in their transcriptional regulation. J. Virol. 1988, 62, 4009–4015. [Google Scholar] [CrossRef]
- Neary, K.; DiMaio, D. Open reading frames E6 and E7 of bovine papillomavirus type 1 are both required for full transformation of mouse C127 cells. J. Virol. 1989, 63, 259–266. [Google Scholar] [CrossRef]
- Dostatni, N.; Lambert, P.F.; Sousa, R.; Ham, J.; Howley, P.M.; Yaniv, M. The functional BPV-1 E2 trans-activating protein can act as a repressor by preventing formation of the initiation complex. Genes Dev. 1991, 5, 1657–1671. [Google Scholar] [CrossRef] [PubMed]
- Jareborg, N.; Alderborn, A.; Burnett, S. Identification and genetic definition of a bovine papillomavirus type 1 E7 protein and absence of a low-copy-number phenotype exhibited by E5, E6, or E7 viral mutants. J. Virol. 1992, 66, 4957–4965. [Google Scholar] [CrossRef]
- Band, V.; De Caprio, J.A.; Delmolino, L.; Kulesa, V.; Sager, R. Loss of p53 protein in human papillomavirus type 16 E6-immortalized human mammary epithelial cells. J. Virol. 1991, 65, 6671–6676. [Google Scholar] [CrossRef] [PubMed]
- Zemlo, T.R.; Lohrbach, B.; Lambert, P.F. Role of transcriptional repressors in transformation by bovine papillomavirus type 1. J. Virol. 1994, 68, 6787–6793. [Google Scholar] [CrossRef] [Green Version]
- Pol, S.B.V.; Howley, P.M. Negative regulation of the bovine papillomavirus E5, E6, and E7 oncogenes by the viral E1 and E2 genes. J. Virol. 1995, 69, 395–402. [Google Scholar] [CrossRef]
- Dowhanick, J.J.; McBride, A.A.; Howley, P.M. Suppression of cellular proliferation by the papillomavirus E2 protein. J. Virol. 1995, 69, 7791–7799. [Google Scholar] [CrossRef]
- Rudolph, R.; Hundeiker, M. “Keratoakanthome” bei mastomys natalensis. Arch. Dermatol. Res. 1975, 254, 239–243. [Google Scholar] [CrossRef] [PubMed]
- Müller, H.; Gissmann, L. Mastomys natalensis Papilloma Virus (MnPV), the Causative Agent of Epithelial Proliferations: Characterization of the Virus Particle. J. Gen. Virol. 1978, 41, 315–323. [Google Scholar] [CrossRef] [PubMed]
- Hasche, D.; Rösl, F. Mastomys Species as Model Systems for Infectious Diseases. Viruses 2019, 11, 182. [Google Scholar] [CrossRef] [PubMed]
- Schäfer, K.; Neumann, J.; Waterboer, T.; Rösl, F. Serological markers for papillomavirus infection and skin tumour development in the rodent model Mastomys coucha. J. Gen. Virol. 2010, 92, 383–394. [Google Scholar] [CrossRef] [PubMed]
- Wayss, K.; Reyes-Mayes, D.; Volm, M. Chemical carcinogenesis by the two-stage protocol in the skin of Mastomys natalensis (Muridae) using topical initiation with 7,12-dimethylbenz(a)anthracene and topical promotion with 12-0-tetradecanoylphorbol-13-acetate. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 1981, 38, 13–21. [Google Scholar] [CrossRef]
- Helfrich, I.; Chen, M.; Schmidt, R.; Fürstenberger, G.; Kopp-Schneider, A.; Trick, D.; Gröne, H.-J.; Hausen, H.Z.; Rösl, F. Increased Incidence of Squamous Cell Carcinomas in Mastomys natalensis Papillomavirus E6 Transgenic Mice during Two-Stage Skin Carcinogenesis. J. Virol. 2004, 78, 4797–4805. [Google Scholar] [CrossRef]
- Defeo-Jones, D.; Vuocolo, G.A.; Haskell, K.M.; Hanobik, M.G.; Kiefer, D.M.; McAvoy, E.M.; Ivey-Hoyle, M.; Brandsma, J.L.; Oliff, A.; Jones, R.E. Papillomavirus E7 protein binding to the retinoblastoma protein is not required for viral induction of warts. J. Virol. 1993, 67, 716–725. [Google Scholar] [CrossRef]
- Ganzenmueller, T.; Matthaei, M.; Muench, P.; Scheible, M.; Iftner, A.; Hiller, T.; Leiprecht, N.; Probst, S.; Stubenrauch, F.; Iftner, T. The E7 protein of the cottontail rabbit papillomavirus immortalizes normal rabbit keratinocytes and reduces pRb levels, while E6 cooperates in immortalization but neither degrades p53 nor binds E6AP. Virology 2008, 372, 313–324. [Google Scholar] [CrossRef] [Green Version]
- Meyers, C.; Harry, J.; Lin, Y.L.; Wettstein, F.O. Identification of three transforming proteins encoded by cottontail rabbit papillomavirus. J. Virol. 1992, 66, 1655–1664. [Google Scholar] [CrossRef]
- Cladel, N.M.; Xu, J.; Peng, X.; Jiang, P.; Christensen, N.D.; Zheng, Z.-M.; Hu, J. Modeling HPV-Associated Disease and Cancer Using the Cottontail Rabbit Papillomavirus. Viruses 2022, 14, 1964. [Google Scholar] [CrossRef]
- Uberoi, A.; Yoshida, S.; Lambert, P.F. Development of an in vivo infection model to study Mouse papillomavirus-1 (MmuPV1). J. Virol. Methods 2018, 253, 11–17. [Google Scholar] [CrossRef] [PubMed]
- Uberoi, A.; Yoshida, S.; Frazer, I.; Pitot, H.C.; Lambert, P.F. Role of Ultraviolet Radiation in Papillomavirus-Induced Disease. PLoS Pathog. 2016, 12, e1005664. [Google Scholar] [CrossRef] [PubMed]
- Spurgeon, M.E.; Uberoi, A.; McGregor, S.M.; Wei, T.; Ward-Shaw, E.; Lambert, P.F. A Novel In Vivo Infection Model To Study Papillomavirus-Mediated Disease of the Female Reproductive Tract. mBio 2019, 10, e00180-19. [Google Scholar] [CrossRef]
- Spurgeon, M.E.; Lambert, P.F. Sexual transmission of murine papillomavirus (MmuPV1) in Mus musculus. eLife 2019, 8, e50056. [Google Scholar] [CrossRef]
- Blaine-Sauer, S.; Shin, M.-K.; Matkowskyj, K.A.; Ward-Shaw, E.; Lambert, P.F. A Novel Model for Papillomavirus-Mediated Anal Disease and Cancer Using the Mouse Papillomavirus. mBio 2021, 12, e0161121. [Google Scholar] [CrossRef] [PubMed]
- Wei, T.; Buehler, D.; Ward-Shaw, E.; Lambert, P.F. An Infection-Based Murine Model for Papillomavirus-Associated Head and Neck Cancer. mBio 2020, 11, e00908-20. [Google Scholar] [CrossRef]
- Bilger, A.; King, R.E.; Schroeder, J.P.; Piette, J.T.; Hinshaw, L.A.; Kurth, A.D.; Alramahi, R.W.; Barthel, M.V.; Ward-Shaw, E.T.; Buehler, D.; et al. A Mouse Model of Oropharyngeal Papillomavirus-Induced Neoplasia Using Novel Tools for Infection and Nasal Anesthesia. Viruses 2020, 12, 450. [Google Scholar] [CrossRef]
- King, R.E.; Bilger, A.; Rademacher, J.; Ward-Shaw, E.T.; Hu, R.; Lambert, P.F.; Thibeault, S.L. A Novel In Vivo Model of Laryngeal Papillomavirus-Associated Disease Using Mus musculus Papillomavirus. Viruses 2022, 14, 1000. [Google Scholar] [CrossRef]
- Cladel, N.M.; Budgeon, L.R.; Cooper, T.K.; Balogh, K.K.; Hu, J.; Christensen, N.D. Secondary Infections, Expanded Tissue Tropism, and Evidence for Malignant Potential in Immunocompromised Mice Infected with Mus musculus Papillomavirus 1 DNA and Virus. J. Virol. 2013, 87, 9391–9395. [Google Scholar] [CrossRef]
- Uberoi, A.; Lambert, P.F. Rodent Papillomaviruses. Viruses 2017, 9, 362. [Google Scholar] [CrossRef]
- Wei, T.; Grace, M.; Uberoi, A.; Romero-Masters, J.C.; Lee, D.; Lambert, P.F.; Munger, K. The Mus musculus Papillomavirus Type 1 E7 Protein Binds to the Retinoblastoma Tumor Suppressor: Implications for Viral Pathogenesis. mBio 2021, 12, e0227721. [Google Scholar] [CrossRef] [PubMed]
- Saunders-Wood, T.; Egawa, N.; Zheng, K.; Giaretta, A.; Griffin, H.M.; Doorbar, J. Role of E6 in Maintaining the Basal Cell Reservoir during Productive Papillomavirus Infection. J. Virol. 2022, 96, e0118121. [Google Scholar] [CrossRef] [PubMed]
- Rozenblatt-Rosen, O.; Deo, R.C.; Padi, M.; Adelmant, G.; Calderwood, M.; Rolland, T.; Grace, M.; Dricot, A.; Askenazi, M.; Tavares, M.; et al. Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature 2012, 487, 491–495. [Google Scholar] [CrossRef] [PubMed]
- Hubbert, N.L.; Sedman, S.A.; Schiller, J.T. Human papillomavirus type 16 E6 increases the degradation rate of p53 in human keratinocytes. J. Virol. 1992, 66, 6237–6241. [Google Scholar] [CrossRef] [PubMed]
- Pietenpol, J.A.; Stein, R.W.; Moran, E.; Yaciuk, P.; Schlegel, R.; Lyons, R.M.; Pittelkow, M.R.; Münger, K.; Howley, P.M.; Moses, H.L. TGF-β1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 1990, 61, 777–785. [Google Scholar] [CrossRef]
- Dick, F.A.; Goodrich, D.W.; Sage, J.; Dyson, N.J. Non-canonical functions of the RB protein in cancer. Nat. Cancer 2018, 18, 442–451. [Google Scholar] [CrossRef]
- Ishak, C.; Marshall, A.E.; Passos, D.; White, C.R.; Kim, S.J.; Cecchini, M.J.; Ferwati, S.; MacDonald, W.A.; Howlett, C.J.; Welch, I.D.; et al. An RB-EZH2 Complex Mediates Silencing of Repetitive DNA Sequences. Mol. Cell 2016, 64, 1074–1087. [Google Scholar] [CrossRef]
- Ishak, C.; Coschi, C.H.; Roes, M.V.; Dick, F.A. Disruption of CDK-resistant chromatin association by pRB causes DNA damage, mitotic errors, and reduces Condensin II recruitment. Cell Cycle 2017, 16, 1430–1439. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.J.; MacDonald, J.I.; Dick, F.A. Phosphorylation of the RB C-terminus regulates condensin II release from chromatin. J. Biol. Chem. 2021, 296, 100108. [Google Scholar] [CrossRef]
- Welch, P. A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell 1993, 75, 779–790. [Google Scholar] [CrossRef]
- Ji, P.; Jiang, H.; Rekhtman, K.; Bloom, J.; Ichetovkin, M.; Pagano, M.; Zhu, L. An Rb-Skp2-p27 Pathway Mediates Acute Cell Cycle Inhibition by Rb and Is Retained in a Partial-Penetrance Rb Mutant. Mol. Cell 2004, 16, 47–58. [Google Scholar] [CrossRef] [PubMed]
- Sanidas, I.; Lee, H.; Rumde, P.H.; Boulay, G.; Morris, R.; Golczer, G.; Stanzione, M.; Hajizadeh, S.; Zhong, J.; Ryan, M.B.; et al. Chromatin-bound RB targets promoters, enhancers, and CTCF-bound loci and is redistributed by cell-cycle progression. Mol. Cell 2022, 82, 3333–3349.e9. [Google Scholar] [CrossRef] [PubMed]
- Dick, F.A.; Dyson, N. pRB Contains an E2F1-Specific Binding Domain that Allows E2F1-Induced Apoptosis to Be Regulated Separately from Other E2F Activities. Mol. Cell 2003, 12, 639–649. [Google Scholar] [CrossRef]
- Coschi, C.H.; Ishak, C.A.; Gallo, D.; Marshall, A.; Talluri, S.; Wang, J.; Cecchini, M.J.; Martens, A.L.; Percy, V.; Welch, I.; et al. Haploinsufficiency of an RB–E2F1–Condensin II Complex Leads to Aberrant Replication and Aneuploidy. Cancer Discov. 2014, 4, 840–853. [Google Scholar] [CrossRef]
- Julian, L.M.; Palander, O.; Seifried, L.A.; Foster, J.E.G.; Dick, F.A. Characterization of an E2F1-specific binding domain in pRB and its implications for apoptotic regulation. Oncogene 2007, 27, 1572–1579. [Google Scholar] [CrossRef]
- Marshall, A.E.; Ishak, C.A.; Dick, F.A. An RB-Condensin II Complex Mediates Long-Range Chromosome Interactions and Influences Expression at Divergently Paired Genes. Mol. Cell. Biol. 2020, 40, e00452-19. [Google Scholar] [CrossRef]
- Münger, K.; Werness, B.; Dyson, N.; Phelps, W.; Harlow, E.; Howley, P. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 1989, 8, 4099–4105. [Google Scholar] [CrossRef]
- Jewers, R.J.; Hildebrandt, P.; Ludlow, J.W.; Kell, B.; McCance, D.J. Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. J. Virol. 1992, 66, 1329–1335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Romero-Masters, J.C.; Lambert, P.F.; Munger, K. Molecular Mechanisms of MmuPV1 E6 and E7 and Implications for Human Disease. Viruses 2022, 14, 2138. https://doi.org/10.3390/v14102138
Romero-Masters JC, Lambert PF, Munger K. Molecular Mechanisms of MmuPV1 E6 and E7 and Implications for Human Disease. Viruses. 2022; 14(10):2138. https://doi.org/10.3390/v14102138
Chicago/Turabian StyleRomero-Masters, James C., Paul F. Lambert, and Karl Munger. 2022. "Molecular Mechanisms of MmuPV1 E6 and E7 and Implications for Human Disease" Viruses 14, no. 10: 2138. https://doi.org/10.3390/v14102138
APA StyleRomero-Masters, J. C., Lambert, P. F., & Munger, K. (2022). Molecular Mechanisms of MmuPV1 E6 and E7 and Implications for Human Disease. Viruses, 14(10), 2138. https://doi.org/10.3390/v14102138