Establishment of human papillomavirus infection requires cell cycle progression

Pyeon, Dohun; Pearce, Shane M.; Lank, Simon M.; Ahlquist, Paul; Lambert, Paul F.

doi:10.1371/journal.ppat.1000318

Cited by 348Cervical Cancer and HPV ResearchVirus-based gene therapy researchCancer-related Molecular Pathways

Establishment of human papillomavirus infection requires cell cycle progression

Open access

Pyeon, Dohun, Pearce, Shane M., Lank, Simon M., Ahlquist, Paul, Lambert, Paul F.·2009·PLoS Pathogens

DOI 10.1371/journal.ppat.1000318PMC PMC2642596

Open this paper in CoChat — free account Open PDF

Abstract

Human papillomaviruses (HPVs) are DNA viruses associated with major human cancers. As such there is a strong interest in developing new means, such as vaccines and microbicides, to prevent HPV infections. Developing the latter requires a better understanding of the infectious life cycle of HPVs. The HPV infectious life cycle is closely linked to the differentiation state of the stratified epithelium it infects, with progeny virus only made in the terminally differentiating suprabasal compartment. It has long been recognized that HPV must first establish its infection within the basal layer of stratified epithelium, but why this is the case has not been understood. In part this restriction might reflect specificity of expression of entry receptors. However, this hypothesis could not fully explain the differentiation restriction of HPV infection, since many cell types can be infected with HPVs in monolayer cell culture. Here, we used chemical biology approaches to reveal that cell cycle progression through mitosis is critical for HPV infection. Using infectious HPV16 particles containing the intact viral genome, G1-synchronized human keratinocytes as hosts, and early viral gene expression as a readout for infection, we learned that the recipient cell must enter M phase (mitosis) for HPV infection to take place. Late M phase inhibitors had no effect on infection, whereas G1, S, G2, and early M phase cell cycle inhibitors efficiently prevented infection. We conclude that host cells need to pass through early prophase for successful onset of transcription of the HPV encapsidated genes. These findings provide one reason why HPVs initially establish infections in the basal compartment of stratified epithelia. Only this compartment of the epithelium contains cells progressing through the cell cycle, and therefore it is only in these cells that HPVs can establish their infection. By defining a major condition for cell susceptibility to HPV infection, these results also have potentially important implications for HPV control.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1371/journal.ppat.1000318

Cites

52 of 52 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Individual factors unique to mucosal surface such as epithelial surface integrity, mucosal secretions, and immune regulation likely play a role in HPV persistence and progression to cancer.
“Individual factors unique to the mucosal surface such as epithelial surface integrity, mucosal secretions, and immune regulation likely play a role in HPV persistence and progression to cancer (Pyeon et al., 2009; Schiffman et al., 2016).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Pyeon et al., 2009

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Primer3 on the WWW for General Users and for Biologist Programmers
Rozen, S., & Skaletsky, H. (2003) · Humana Press eBooks · doi:10.1385/1-59259-192-2:365 · Cited by 14,952 · see citing works
Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line.
Boukamp, P., Petrussevska, R. T., Breitkreutz, D., Hornung, J., Markham, A., & Fusenig, N. E. (1988) · The Journal of cell biology · doi:10.1083/jcb.106.3.761 · Cited by 4,170 · see citing works
Papillomaviruses and cancer: from basic studies to clinical application
Hausen, H. Z. (2002) · Nature reviews. Cancer · doi:10.1038/nrc798 · Cited by 4,031 · see citing works
Human papillomavirus and cervical cancer
Burd, E. M. (2003) · Clinical Microbiology Reviews · doi:10.1128/cmr.16.1.1-17.2003 · Cited by 2,420 · see citing works
Small Molecule Inhibitor of Mitotic Spindle Bipolarity Identified in a Phenotype-Based Screen
Mayer, T. U., Kapoor, T. M., Haggarty, S. J., King, R. W., Schreiber, S. L., & Mitchison, T. J. (1999) · Science · doi:10.1126/science.286.5441.971 · Cited by 1,732 · see citing works
Papillomavirus infections — a major cause of human cancers
Hausen, H. Z. (1996) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/0304-419x(96)00020-0 · Cited by 1,512 · see citing works
Cdk1 is sufficient to drive the mammalian cell cycle
Santamarı́a, D., Barrière, C., Cerqueira, A., Hunt, S. L., Tardy, C., Newton, K., Cáceres, J. F., Dubus, P. R., Malumbres, M., & Barbacid, M. (2007) · Nature · doi:10.1038/nature06046 · Cited by 1,096 · see citing works
Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies
Bernardi, R., & Pandolfi, P. P. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2277 · Cited by 876 · see citing works
Exploiting Chemical Libraries, Structure, and Genomics in the Search for Kinase Inhibitors
Gray, N. S., Wodicka, L. M., Thunnissen, A. M. W. H., Norman, T., Kwon, S., Espinoza, F. H., Morgan, D. O., Barnes, G., Leclerc, S., Meijer, L., et al. (1998) · Science · doi:10.1126/science.281.5376.533 · Cited by 808 · see citing works
Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus
Lewis, P. F., & Emerman, M. (1994) · Journal of Virology · doi:10.1128/jvi.68.1.510-516.1994 · Cited by 797 · see citing works
Viruses in Human Cancers
Hausen, H. Z. (1991) · Science · doi:10.1126/science.1659743 · Cited by 783 · see citing works
In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase
Peter, M., Nakagawa, J., Dorée, M., Labbé, J., & Nigg, E. A. (1990) · Cell · doi:10.1016/0092-8674(90)90471-p · Cited by 782 · see citing works
The Function of KGF in Morphogenesis of Epithelium and Reepithelialization of Wounds
Werner, S., Smola, H., Liao, X., Longaker, M. T., Krieg, T. M., HOFSCHNEIDER, P. H., & Williams, L. T. (1994) · Science · doi:10.1126/science.7973639 · Cited by 604 · see citing works
Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan
Roberts, J. N., Buck, C. B., Thompson, C. D., Kines, R. C., Bernardo, M., Choyke, P. L., Lowy, D. R., & Schiller, J. T. (2007) · Nature Medicine · doi:10.1038/nm1598 · Cited by 504 · see citing works
Efficient Intracellular Assembly of Papillomaviral Vectors
Buck, C. B., Pastrana, D. V., Lowy, D. R., & Schiller, J. T. (2003) · Journal of Virology · doi:10.1128/jvi.78.2.751-757.2004 · Cited by 489 · see citing works
Biosynthesis of Human Papillomavirus from a Continuous Cell Line Upon Epithelial Differentiation
Meyers, C., Frattini, M. G., Hudson, J. B., & Laimins, L. A. (1992) · Science · doi:10.1126/science.1323879 · Cited by 456 · see citing works
Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity
Hebner, C. M., & Laimins, L. A. (2005) · Reviews in Medical Virology · doi:10.1002/rmv.488 · Cited by 400 · see citing works
Microtubule-organizing centres: a re-evaluation
Lüders, J., & Stearns, T. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2100 · Cited by 397 · see citing works
Identification of the alpha6 integrin as a candidate receptor for papillomaviruses
Evander, M., Frazer, I. H., Payne, E., Qi, Y. M., Hengst, K., & McMillan, N. A. J. (1997) · Journal of Virology · doi:10.1128/jvi.71.3.2449-2456.1997 · Cited by 390 · see citing works
Cytoplasmic Dynein as a Facilitator of Nuclear Envelope Breakdown
Salina, D., Bodoor, K., Eckley, D. M., Schroer, T. A., Rattner, J. B., & Burke, B. E. (2002) · Cell · doi:10.1016/s0092-8674(01)00628-6 · Cited by 371 · see citing works
Pondering the Promyelocytic Leukemia Protein (PML) Puzzle: Possible Functions for PML Nuclear Bodies
Borden, K. L. B. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.15.5259-5269.2002 · Cited by 314 · see citing works
Human papillomavirus–associated head and neck squamous cell carcinoma: mounting evidence for an etiologic role for human papillomavirus in a subset of head and neck cancers
Gillison, M. L., & Shah, K. V. (2001) · Current Opinion in Oncology · doi:10.1097/00001622-200105000-00009 · Cited by 307 · see citing works
Synchronization of HeLa cell cultures by inhibition of DNA polymerase a with aphidicolin
Pedrali‐Noy, G., Spadari, S., Miller‐Faurès, A., Miller, A. O. A., Kruppa, J., & Koch, G. (1980) · Nucleic Acids Research · doi:10.1093/nar/8.2.377 · Cited by 290 · see citing works
Human papillomavirus life cycle: active and latent phases
Stubenrauch, F., & Laimins, L. A. (1999) · Seminars in Cancer Biology · doi:10.1006/scbi.1999.0141 · Cited by 273 · see citing works
Chemical genetics reveals the requirement for Polo-like kinase 1 activity in positioning RhoA and triggering cytokinesis in human cells
Burkard, M. E., Randall, C. L., Larochelle, S., Zhang, C., Shokat, K. M., Fisher, R. P., & Jallepalli, P. V. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701140104 · Cited by 252 · see citing works
Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression
Day, P. M., Baker, C. C., Lowy, D. R., & Schiller, J. T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404229101 · Cited by 246 · see citing works
A causal role for human papillomavirus in head and neck cancer
Gillison, M., & Lowy, D. (2004) · The Lancet · doi:10.1016/s0140-6736(04)16194-1 · Cited by 227 · see citing works
Inhibition of p34cdc2 kinase activity by etoposide or irradiation as a mechanism of G2 arrest in Chinese hamster ovary cells.
Lock, R. B., & Ross, W. E. (1990) · PubMed · Cited by 217 · see citing works
Viral Entry into the Nucleus
Whittaker, G. R., Kann, M., & Helenius, A. (2000) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.16.1.627 · Cited by 215 · see citing works
Exploitation of Nucleic Acid Packaging Signals To Generate a Novel Influenza Virus-Based Vector Stably Expressing Two Foreign Genes
Watanabe, T., Watanabe, S., Noda, T., Fujii, Y., & Kawaoka, Y. (2003) · Journal of Virology · doi:10.1128/jvi.77.19.10575-10583.2003 · Cited by 188 · see citing works
Production of human papillomavirus and modulation of the infectious program in epithelial raft cultures. OFF.Preprint
Dollard, S. C., Wilson, J. L., Demeter, L. M., Bonnez, W., Reichman, R. C., Broker, T. R., & Chow, L. T. (1992) · Genes & Development · doi:10.1101/gad.6.7.1131 · Cited by 186 · see citing works
Nuclear import and export of influenza virus nucleoprotein
Neumann, G., Castrucci, M. R., & Kawaoka, Y. (1997) · Journal of Virology · doi:10.1128/jvi.71.12.9690-9700.1997 · Cited by 184 · see citing works
Keratinocyte-Secreted Laminin 5 Can Function as a Transient Receptor for Human Papillomaviruses by Binding Virions and Transferring Them to Adjacent Cells
Culp, T. D., Budgeon, L. R., Marinkovich, M. P., Meneguzzi, G., & Christensen, N. D. (2006) · Journal of Virology · doi:10.1128/jvi.00724-06 · Cited by 176 · see citing works
Establishment of the Human Papillomavirus Type 16 (HPV-16) Life Cycle in an Immortalized Human Foreskin Keratinocyte Cell Line
Flores, E. R., Allen‐Hoffmann, B. L., Lee, D., Sattler, C. A., & Lambert, P. F. (1999) · Virology · doi:10.1006/viro.1999.9868 · Cited by 176 · see citing works
PML bodies: a meeting place for genomic loci?
Ching, R. W., Dellaire, G., Eskiw, C. H., & Bazett‐Jones, D. P. (2005) · Journal of Cell Science · doi:10.1242/jcs.01700 · Cited by 139 · see citing works
Clonal Selection for Transcriptionally Active Viral Oncogenes during Progression to Cancer
Tine, B. A. V., Kappes, J. C., Banerjee, N. S., Knops, J. F., Lai, L., Steenbergen, R. D. M., Meijer, C. J. L. M., Snijders, P. J. F., Chatis, P. A., Broker, T. R., et al. (2004) · Journal of Virology · doi:10.1128/jvi.78.20.11172-11186.2004 · Cited by 132 · see citing works
Delivering on the promise: HPV vaccines and cervical cancer
Schiller, J. T., & Davies, P. O. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro867 · Cited by 126 · see citing works
Identification of a Dynein Interacting Domain in the Papillomavirus Minor Capsid Protein L2
Florin, L., Becker, K. A., Lambert, C., Nowak, T., Sapp, C., Strand, D. J., Streeck, R. E., & Sapp, M. J. (2006) · Journal of Virology · doi:10.1128/jvi.00057-06 · Cited by 126 · see citing works
Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation
Pyeon, D., Lambert, P. F., & Ahlquist, P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504020102 · Cited by 121 · see citing works
Viruses in human cancers
Hausen, H. Z. (1999) · European Journal of Cancer · doi:10.1016/s0959-8049(99)00291-9 · Cited by 114 · see citing works
A Microtubule Interactome: Complexes with Roles in Cell Cycle and Mitosis
Hughes, J. R., Meireles, A. M., Fisher, K. H., García, Á. G., Antrobus, R., Wainman, A., Zitzmann, N., Deane, C. M., Ohkura, H., & Wakefield, J. G. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060098 · Cited by 107 · see citing works
Breaking and making of the nuclear envelope
Margalit, A., Vlcek, S., Gruenbaum, Y., & Foisner, R. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20433 · Cited by 105 · see citing works
Human papillomaviruses bind a basal extracellular matrix component secreted by keratinocytes which is distinct from a membrane-associated receptor
Culp, T. D., Budgeon, L. R., & Christensen, N. D. (2005) · Virology · doi:10.1016/j.virol.2005.11.025 · Cited by 101 · see citing works
Cell cycle dependence of foamy retrovirus infection
Bieniasz, P. D., Weiss, R. A., & McClure, M. O. (1995) · Journal of Virology · doi:10.1128/jvi.69.11.7295-7299.1995 · Cited by 94 · see citing works
Nuclear Import of Microinjected Influenza Virus Ribonucleoproteins
Kemler, I., Whittaker, G. R., & Helenius, A. (1994) · Virology · doi:10.1006/viro.1994.1432 · Cited by 71 · see citing works
Sequential PKC- and Cdc2-mediated phosphorylation events elicit zebrafish nuclear envelope disassembly
Collas, P. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.6.977 · Cited by 67 · see citing works
Protein kinases controlling the onset of mitosis
Ferrari, S. M. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5515-3 · Cited by 62 · see citing works
Papillomavirus virus-like particles activate the PI3-kinase pathway via alpha-6 beta-4 integrin upon binding
Fothergill, T., & McMillan, N. A. J. (2006) · Virology · doi:10.1016/j.virol.2006.05.002 · Cited by 56 · see citing works
The Positively Charged Termini of L2 Minor Capsid Protein Required for Bovine Papillomavirus Infection Function Separately in Nuclear Import and DNA Binding
Fay, A., Yutzy, W. H., Roden, R. B. S., & Moroianu, J. (2004) · Journal of Virology · doi:10.1128/jvi.78.24.13447-13454.2004 · Cited by 49 · see citing works
Microbicides for Prevention of Transmission of Sexually Transmitted Diseases
Howett, M. K., & Kuhl, J. (2005) · Current Pharmaceutical Design · doi:10.2174/138161205774580633 · Cited by 48 · see citing works
Human Papillomavirus Type 6b Virus-Like Particles Are Able To Activate the Ras-MAP Kinase Pathway and Induce Cell Proliferation
Payne, E., Bowles, M. R., Don, A. L. J., Hancock, J. F., & McMillan, N. A. J. (2001) · Journal of Virology · doi:10.1128/jvi.75.9.4150-4157.2001 · Cited by 34 · see citing works
Effect of 5-Fluorouracil on the Cell Growth and Cell Cycle Kinetics of a Mouse Ascites Tumor Growing in Vivo
Lewin, F., Skog, S., Tribukait, B., & Rjngborg, U. (1987) · Acta Oncologica · doi:10.3109/02841868709091751 · Cited by 15 · see citing works

Flagged first, then by citations

Sorted by citations

The Biology and Life-Cycle of Human Papillomaviruses
Doorbar, J., Quint, W. G. V., Banks, L., Bravo, I. G., Stoler, M. H., Tr, B., & Stanley, M. (2012) · Vaccine · doi:10.1016/j.vaccine.2012.06.083 · Cited by 1,554 · see citing works
Carcinogenic human papillomavirus infection
Schiffman, M., Doorbar, J., Wentzensen, N., de Sanjosé, S., Fakhry, C., Monk, B. J., Stanley, M. A., & Franceschi, S. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.86 · Cited by 999 · see citing works
Human papillomavirus molecular biology and disease association
Doorbar, J., Egawa, N., Griffin, H. M., Kranjec, C., & Murakami, I. (2015) · Reviews in Medical Virology · doi:10.1002/rmv.1822 · Cited by 957 · see citing works
Human Papillomaviruses; Epithelial Tropisms, and the Development of Neoplasia
Egawa, N., Egawa, K., Griffin, H. M., & Doorbar, J. (2015) · Viruses · doi:10.3390/v7072802 · Cited by 550 · see citing works
The human papillomavirus replication cycle, and its links to cancer progression: a comprehensive review
Graham, S. V. (2017) · Clinical Science · doi:10.1042/cs20160786 · Cited by 458 · see citing works
Human Papillomavirus in Head and Neck Cancer: Its Role in Pathogenesis and Clinical Implications
Chung, C. H., & Gillison, M. L. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0784 · Cited by 417 · see citing works
Human papillomaviruses: diversity, infection and host interactions
McBride, A. A. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00617-5 · Cited by 372 · see citing works
Opportunities and challenges for human papillomavirus vaccination in cancer
Roden, R. B. S., & Stern, P. L. (2018) · Nature reviews. Cancer · doi:10.1038/nrc.2018.13 · Cited by 334 · see citing works
Current understanding of the mechanism of HPV infection
Schiller, J. T., Day, P. M., & Kines, R. C. (2010) · Gynecologic Oncology · doi:10.1016/j.ygyno.2010.04.004 · Cited by 332 · see citing works
Mucosal and Cutaneous Human Papillomavirus Infections and Cancer Biology
Gheit, T. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00355 · Cited by 332 · see citing works
Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming
McLaughlin-Drubin, M. E., Crum, C. P., & Münger, K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009933108 · Cited by 325 · see citing works
The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding
Kines, R. C., Thompson, C. D., Lowy, D. R., Schiller, J. T., & Day, P. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908502106 · Cited by 292 · see citing works
L2, the minor capsid protein of papillomavirus
Wang, J. W., & Roden, R. B. S. (2013) · Virology · doi:10.1016/j.virol.2013.04.017 · Cited by 266 · see citing works
The role of the PI3K/Akt/mTOR signalling pathway in human cancers induced by infection with human papillomaviruses
Zhang, L., Wu, J., Ling, M. T., Zhao, L., & Zhao, K.-N. (2015) · Molecular Cancer · doi:10.1186/s12943-015-0361-x · Cited by 264 · see citing works
Human papillomavirus molecular biology
Harden, M. E., & Münger, K. (2016) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2016.07.002 · Cited by 262 · see citing works
The human papillomavirus oncoproteins: a review of the host pathways targeted on the road to transformation
Scarth, J. A., Patterson, M. R., Morgan, E. L., & Macdonald, A. (2021) · Journal of General Virology · doi:10.1099/jgv.0.001540 · Cited by 237 · see citing works
Cellular Entry of Human Papillomavirus Type 16 Involves Activation of the Phosphatidylinositol 3-Kinase/Akt/mTOR Pathway and Inhibition of Autophagy
Surviladze, Z., Sterk, R. T., DeHaro, S. A., & Ozbun, M. A. (2012) · Journal of Virology · doi:10.1128/jvi.02319-12 · Cited by 219 · see citing works
Evasion of host immune defenses by human papillomavirus
Westrich, J. A., Warren, C. J., & Pyeon, D. (2016) · Virus Research · doi:10.1016/j.virusres.2016.11.023 · Cited by 225 · see citing works
APOBEC3A Functions as a Restriction Factor of Human Papillomavirus
Warren, C. J., Xu, T., Guo, K., Griffin, L., Westrich, J. A., Lee, D., Lambert, P. F., Santiago, M. L., & Pyeon, D. (2014) · Journal of Virology · doi:10.1128/jvi.02383-14 · Cited by 186 · see citing works
Essential Roles for Soluble Virion-Associated Heparan Sulfonated Proteoglycans and Growth Factors in Human Papillomavirus Infections
Surviladze, Z., Dziduszko, A., & Ozbun, M. A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002519 · Cited by 183 · see citing works
Viral Infections, the Microbiome, and Probiotics
Harper, A., Vijayakumar, V., Ouwehand, A. C., ter Haar, J., Obis, D., Espadaler, J., Binda, S., Desiraju, S., & Day, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596166 · Cited by 177 · see citing works
Human papillomavirus and oropharynx cancer: Biology, detection and clinical implications
Allen, C. T., Lewis, J. S., El‐Mofty, S. K., Haughey, B. H., & Nussenbaum, B. A. (2010) · The Laryngoscope · doi:10.1002/lary.20936 · Cited by 175 · see citing works
Pathogenesis of human papillomavirus‐associated mucosal disease
Groves, I. J., & Coleman, N. (2014) · The Journal of Pathology · doi:10.1002/path.4496 · Cited by 163 · see citing works
Prophylactic and Therapeutic HPV Vaccines: Current Scenario and Perspectives
Mo, Y., Ma, J., Zhang, H., Shen, J., Chen, J., Hong, J., Xu, Y., & Qian, C. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.909223 · Cited by 163 · see citing works
Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus
Sapp, M. J., & Bienkowska‐Haba, M. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07400.x · Cited by 154 · see citing works
How viruses access the nucleus.
Cohen, S. S., Au, S., & Panté, N. (2011) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamcr.2010.12.009 · Cited by 143 · see citing works
Large Scale RNAi Reveals the Requirement of Nuclear Envelope Breakdown for Nuclear Import of Human Papillomaviruses
Aydin, I., Weber, S., Snijder, B., Ventayol, P. S., Kühbacher, A., Becker, M., Day, P. M., Schiller, J. T., Kann, M., Pelkmans, L., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004162 · Cited by 149 · see citing works
Identification of a Role for the trans -Golgi Network in Human Papillomavirus 16 Pseudovirus Infection
Day, P. M., Thompson, C. D., Schowalter, R. M., Lowy, D. R., & Schiller, J. T. (2013) · Journal of Virology · doi:10.1128/jvi.03222-12 · Cited by 145 · see citing works
Human Papillomavirus L2 Facilitates Viral Escape from Late Endosomes via Sorting Nexin 17
Bergant, M., Ozbun, M. A., Campos, S. K., Myers, M. P., & Banks, L. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01320.x · Cited by 141 · see citing works
Annexin A2 and S100A10 Regulate Human Papillomavirus Type 16 Entry and Intracellular Trafficking in Human Keratinocytes
Dziduszko, A., & Ozbun, M. A. (2013) · Journal of Virology · doi:10.1128/jvi.00519-13 · Cited by 138 · see citing works
Viral and Cellular Biomarkers in the Diagnosis of Cervical Intraepithelial Neoplasia and Cancer
Tornesello, M. L., Buonaguro, L., Rossi, P. G., & Buonaguro, F. M. (2013) · BioMed Research International · doi:10.1155/2013/519619 · Cited by 127 · see citing works
Mechanisms and strategies of papillomavirus replication
McBride, A. A. (2017) · Biological Chemistry · doi:10.1515/hsz-2017-0113 · Cited by 127 · see citing works
Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection
Popa, A., Zhang, W., Harrison, M. S., Goodner, K., Kazakov, T., Goodwin, E. C., Lipovsky, A. I., Burd, C. G., & DiMaio, D. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004699 · Cited by 121 · see citing works
Principles of Virus Uncoating: Cues and the Snooker Ball
Yamauchi, Y., & Greber, U. F. (2016) · Traffic · doi:10.1111/tra.12387 · Cited by 121 · see citing works
Suppression of Antitumor Immune Responses by Human Papillomavirus through Epigenetic Downregulation of CXCL14
Cicchini, L., Westrich, J. A., Xu, T., Vermeer, D. W., Berger, J., Clambey, E. T., Lee, D., Song, J. I., Lambert, P. F., Greer, R. O., et al. (2016) · mBio · doi:10.1128/mbio.00270-16 · Cited by 121 · see citing works
Molecular mechanisms of HPV mediated neoplastic progression
Senapati, R., Senapati, N. N., & Dwibedi, B. (2016) · Infectious Agents and Cancer · doi:10.1186/s13027-016-0107-4 · Cited by 121 · see citing works
Histology of cervical intraepithelial neoplasia and the role of biomarkers
Martin, C. M., & O’Leary, J. J. (2011) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2011.04.005 · Cited by 118 · see citing works
Cyclophilins Facilitate Dissociation of the Human Papillomavirus Type 16 Capsid Protein L1 from the L2/DNA Complex following Virus Entry
Bienkowska‐Haba, M., Williams, C., Kim, S. M., Garcea, R. L., & Sapp, M. J. (2012) · Journal of Virology · doi:10.1128/jvi.00980-12 · Cited by 116 · see citing works
Mechanisms by which HPV Induces a Replication Competent Environment in Differentiating Keratinocytes
Moody, C. A. (2017) · Viruses · doi:10.3390/v9090261 · Cited by 114 · see citing works
Oncogenic human papillomaviruses
McBride, A. A. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0273 · Cited by 112 · see citing works
Virus strategies for passing the nuclear envelope barrier
Kobiler, O., Drayman, N., Butin‐Israeli, V., & Oppenheim, A. (2012) · The Nucleus · doi:10.4161/nucl.21979 · Cited by 118 · see citing works
Nuclear entry of DNA viruses
Fay, N., & Panté, N. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00467 · Cited by 106 · see citing works
HPV entry into cells
Aksoy, P., Gottschalk, E. Y., & Meneses, P. I. (2016) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2016.09.004 · Cited by 103 · see citing works
HPV Infection: Immunological Aspects and Their Utility in Future Therapy
Deligeoroglou, E., Giannouli, A., Athanasopoulos, N., Karountzos, V., Vatopoulou, A., Dimopoulos, K., & Creatsas, G. (2013) · Infectious Diseases in Obstetrics and Gynecology · doi:10.1155/2013/540850 · Cited by 103 · see citing works
Concepts of papillomavirus entry into host cells
Day, P. M., & Schelhaas, M. (2013) · Current Opinion in Virology · doi:10.1016/j.coviro.2013.11.002 · Cited by 100 · see citing works
Incoming human papillomavirus type 16 genome resides in a vesicular compartment throughout mitosis
DiGiuseppe, S., Łuszczek, W., Keiffer, T. R., Bienkowska‐Haba, M., Guion, L. G. M., & Sapp, M. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600638113 · Cited by 97 · see citing works
Reduced p21WAF1/CIP1 via Alteration of p53-DDX3 Pathway Is Associated with Poor Relapse-Free Survival in Early-Stage Human Papillomavirus–Associated Lung Cancer
Wu, D., Liu, W.-S., Wang, J. C. K., Chen, C., Cheng, Y., & Lee, H. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2316 · Cited by 95 · see citing works
Vesicular Trafficking of Incoming Human Papillomavirus 16 to the Golgi Apparatus and Endoplasmic Reticulum Requires γ-Secretase Activity
Zhang, W., Kazakov, T., Popa, A., & DiMaio, D. (2014) · mBio · doi:10.1128/mbio.01777-14 · Cited by 93 · see citing works
Human papillomavirus infection is inhibited by host autophagy in primary human keratinocytes
Griffin, L., Cicchini, L., & Pyeon, D. (2013) · Virology · doi:10.1016/j.virol.2012.12.004 · Cited by 89 · see citing works
Cutaneous HPV8 and MmuPV1 E6 Proteins Target the NOTCH and TGF-β Tumor Suppressors to Inhibit Differentiation and Sustain Keratinocyte Proliferation
Meyers, J. M., Uberoi, A., Grace, M. R., Lambert, P. F., & Münger, K. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006171 · Cited by 85 · see citing works
RETRACTED ARTICLE: Molecular mechanisms in progression of HPV-associated cervical carcinogenesis
Gupta, S. M., & Mania‐Pramanik, J. (2019) · Journal of Biomedical Science · doi:10.1186/s12929-019-0520-2 · Cited by 88 · see citing works
Retracted
Biology of HPV Mediated Carcinogenesis and Tumor Progression
Cosper, P. F., Bradley, S. T., Luo, Q., & Kimple, R. J. (2021) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2021.02.006 · Cited by 83 · see citing works
Sp100 Provides Intrinsic Immunity against Human Papillomavirus Infection
Stepp, W. H., Meyers, J. M., & McBride, A. A. (2013) · mBio · doi:10.1128/mbio.00845-13 · Cited by 82 · see citing works
The Role of the DNA Damage Response throughout the Papillomavirus Life Cycle
McKinney, C. C., Hussmann, K., & McBride, A. A. (2015) · Viruses · doi:10.3390/v7052450 · Cited by 79 · see citing works
The Antiviral Restriction Factors IFITM1, 2 and 3 Do Not Inhibit Infection of Human Papillomavirus, Cytomegalovirus and Adenovirus
Warren, C. J., Griffin, L., Little, A. S., Huang, I., Farzan, M., & Pyeon, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096579 · Cited by 79 · see citing works
The role of furin in papillomavirus infection
Day, P. M., & Schiller, J. T. (2009) · Future Microbiology · doi:10.2217/fmb.09.86 · Cited by 77 · see citing works
Identification and Validation of Human Papillomavirus Encoded microRNAs
Qian, K., Pietilä, T., Rönty, M. J., Michon, F., Frilander, M. J., Ritari, J., Tarkkanen, J., Paulin, L. G., Auvinen, P., & Auvinen, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070202 · Cited by 76 · see citing works
Molecular mechanisms of human papillomavirus-related carcinogenesis in head and neck cancer
Faraji, F., Zaidi, M. A., Fakhry, C., & Gaykalova, D. A. (2017) · Microbes and Infection · doi:10.1016/j.micinf.2017.06.001 · Cited by 78 · see citing works
Entry Tropism of BK and Merkel Cell Polyomaviruses in Cell Culture
Schowalter, R. M., Reinhold, W. C., & Buck, C. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042181 · Cited by 75 · see citing works
Stratification of HPV-induced cervical pathology using the virally encoded molecular marker E4 in combination with p16 or MCM
Griffin, H. M., Soneji, Y., van Baars, R., Arora, R., Jenkins, D., van de Sandt, M. M., Wu, Z., Quint, W. G. V., Jach, R., Okoń, K., et al. (2015) · Modern Pathology · doi:10.1038/modpathol.2015.52 · Cited by 75 · see citing works
Topography of the Human Papillomavirus Minor Capsid Protein L2 during Vesicular Trafficking of Infectious Entry
DiGiuseppe, S., Keiffer, T. R., Bienkowska‐Haba, M., Łuszczek, W., Guion, L. G. M., Müller, M., & Sapp, M. J. (2015) · Journal of Virology · doi:10.1128/jvi.01588-15 · Cited by 72 · see citing works
Cruising the cellular highways: how human papillomavirus travels from the surface to the nucleus
DiGiuseppe, S., Bienkowska-Haba, M., Guion, L. G., & Sapp, M. (2017) · Virus Research · doi:10.1016/j.virusres.2016.10.015 · Cited by 67 · see citing works
Human Papillomavirus Episome Stability Is Reduced by Aphidicolin and Controlled by DNA Damage Response Pathways
Edwards, T. G., Helmus, M. J., Koeller, K. J., Bashkin, J. K., & Fisher, C. (2013) · Journal of Virology · doi:10.1128/jvi.03473-12 · Cited by 71 · see citing works
Epigenetic Regulation of the Human Papillomavirus Life Cycle
Mac, M., & Moody, C. A. (2020) · Pathogens · doi:10.3390/pathogens9060483 · Cited by 71 · see citing works
The Biology of Human Papillomaviruses
Nguyen, H. P., Ramirez‐Fort, M. K., & Rady, P. L. (2014) · Current problems in dermatology · doi:10.1159/000355959 · Cited by 70 · see citing works
Modulation of the DNA damage response during the life cycle of human papillomaviruses
Anacker, D. C., & Moody, C. A. (2016) · Virus Research · doi:10.1016/j.virusres.2016.11.006 · Cited by 70 · see citing works
Human Papillomavirus and the Stroma: Bidirectional Crosstalk during the Virus Life Cycle and Carcinogenesis
Spurgeon, M. E., & Lambert, P. F. (2017) · Viruses · doi:10.3390/v9080219 · Cited by 69 · see citing works
Epidemiology, Molecular Pathogenesis, Immuno-Pathogenesis, Immune Escape Mechanisms and Vaccine Evaluation for HPV-Associated Carcinogenesis
Jain, M., Yadav, D., Jarouliya, U., Chavda, V. K., Yadav, A. K., Chaurasia, B. K., & Song, M. (2023) · Pathogens · doi:10.3390/pathogens12121380 · Cited by 68 · see citing works
HPV-associated oropharyngeal cancer: in search of surrogate biomarkers for early lesions
Lim, Y. X., & D’Silva, N. J. (2024) · Oncogene · doi:10.1038/s41388-023-02927-9 · Cited by 68 · see citing works
A central region in the minor capsid protein of papillomaviruses facilitates viral genome tethering and membrane penetration for mitotic nuclear entry
Aydin, I., Villalonga-Planells, R., Greune, L., Bronnimann, M. P., Calton, C. M., Becker, M., Lai, K.-Y., Campos, S. K., Schmidt, M. A., & Schelhaas, M. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006308 · Cited by 67 · see citing works
Stem cells in squamous head and neck cancer
Albers, A. E., Chen, C., Köberle, B., Qian, X., Klußmann, J. P., Wollenberg, B., & Kaufmann, A. M. (2011) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2011.03.004 · Cited by 67 · see citing works
Microbiome factors in HPV-driven carcinogenesis and cancers
Lin, D., Kouzy, R., Jaoude, J. A., Noticewala, S. S., Medrano, A. Y. D., Klopp, A. H., Taniguchi, C. M., & Colbert, L. E. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008524 · Cited by 66 · see citing works
Special Issue about Head and Neck Cancers: HPV Positive Cancers
Economopoulou, P., Kotsantis, I., & Psyrri, A. K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093388 · Cited by 66 · see citing works
Human Papillomavirus Major Capsid Protein L1 Remains Associated with the Incoming Viral Genome throughout the Entry Process
DiGiuseppe, S., Bienkowska‐Haba, M., Guion, L. G. M., Keiffer, T. R., & Sapp, M. J. (2017) · Journal of Virology · doi:10.1128/jvi.00537-17 · Cited by 65 · see citing works
Heparin increases the infectivity of Human Papillomavirus Type 16 independent of cell surface proteoglycans and induces L1 epitope exposure
Cerqueira, C., Liu, Y., Kühling, L., Chai, W., Hafezi, W., Kuppevelt, T. H. V., Kühn, J., Feizi, T., & Schelhaas, M. (2013) · Cellular Microbiology · doi:10.1111/cmi.12150 · Cited by 64 · see citing works
Translocation of the papillomavirus L2/vDNA complex across the limiting membrane requires the onset of mitosis
Calton, C. M., Bronnimann, M. P., Manson, A. R., Li, S., Chapman, J. A., Suarez-Berumen, M., Williamson, T. R., Molugu, S. K., Bernal, R. A., & Campos, S. K. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006200 · Cited by 62 · see citing works
Infectious Entry of Merkel Cell Polyomavirus
Becker, M., Dominguez, M., Greune, L., Soria-Martínez, L., Pfleiderer, M. M., Schowalter, R. M., Buck, C. B., Blaum, B. S., Schmidt, M. A., & Schelhaas, M. (2019) · Journal of Virology · doi:10.1128/jvi.02004-18 · Cited by 59 · see citing works
Tetraspanins: Host Factors in Viral Infections
New, C. S., Lee, Z.-Y., Tan, K. S., Wong, A. H., Wang, D. Y., & Tran, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111609 · Cited by 58 · see citing works
The Interplay between Antiviral Signalling and Carcinogenesis in Human Papillomavirus Infections
Ferreira, A., Ramalho, A. C., Marques, M., & Ribeiro, D. (2020) · Cancers · doi:10.3390/cancers12030646 · Cited by 60 · see citing works
The nuclear retention signal of HPV16 L2 protein is essential for incoming viral genome to transverse the trans-Golgi network
DiGiuseppe, S., Bienkowska‐Haba, M., Hilbig, L., & Sapp, M. J. (2014) · Virology · doi:10.1016/j.virol.2014.04.024 · Cited by 57 · see citing works
Papillomavirus Infection Requires γ Secretase
Karanam, B., Peng, S., Li, T., Buck, C. B., Day, P. M., & Roden, R. B. S. (2010) · Journal of Virology · doi:10.1128/jvi.01081-10 · Cited by 57 · see citing works
Clinical relevance and implications of HPV-induced neoplasia in different anatomical locations
Prigge, E. S., Doeberitz, M. V. K., & Reuschenbach, M. (2016) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2016.06.005 · Cited by 58 · see citing works
Subcellular Trafficking of the Papillomavirus Genome during Initial Infection: The Remarkable Abilities of Minor Capsid Protein L2
Campos, S. K. (2017) · Viruses · doi:10.3390/v9120370 · Cited by 57 · see citing works
Alpha-Defensin HD5 Inhibits Furin Cleavage of Human Papillomavirus 16 L2 To Block Infection
Wiens, M. E., & Smith, J. G. (2014) · Journal of Virology · doi:10.1128/jvi.02901-14 · Cited by 56 · see citing works
Interaction of Human Tumor Viruses with Host Cell Surface Receptors and Cell Entry
Schäfer, G., Blumenthal, M. J., & Katz, A. A. (2015) · Viruses · doi:10.3390/v7052592 · Cited by 56 · see citing works
Biology and natural history of human papillomavirus infection
Fernandes, J. V., de Araújo, J. M. G., & Fernandes, T. A. A. D. M. (2013) · Open Access Journal of Clinical Trials · doi:10.2147/oajct.s37741 · Cited by 54 · see citing works
Hitchhiking on host chromatin: how papillomaviruses persist
McBride, A. A., Sakakibara, N., Stepp, W. H., & Jang, M. K. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.01.011 · Cited by 54 · see citing works
γ-Secretase promotes membrane insertion of the human papillomavirus L2 capsid protein during virus infection
Inoue, T., Zhang, P., Zhang, W., Goodner, K., Dupzyk, A., DiMaio, D., & Tsai, B. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201804171 · Cited by 54 · see citing works
Heterotetrameric annexin A2/S100A10 (A2t) is essential for oncogenic human papillomavirus trafficking and capsid disassembly, and protects virions from lysosomal degradation
Taylor, J. R., Fernandez, D. J., Thornton, S. M., Skeate, J. G., Lühen, K. P., Silva, D. M. D., Langen, R., & Kast, W. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-30051-2 · Cited by 53 · see citing works
The long and winding road: human papillomavirus entry and subcellular trafficking
Ozbun, M. A., & Campos, S. K. (2021) · Current Opinion in Virology · doi:10.1016/j.coviro.2021.07.010 · Cited by 52 · see citing works
DNA virus uncoating
Kilcher, S., & Mercer, J. (2015) · Virology · doi:10.1016/j.virol.2015.01.024 · Cited by 52 · see citing works
The full transcription map of mouse papillomavirus type 1 (MmuPV1) in mouse wart tissues
Xue, X., Majerčiak, V., Uberoi, A., Kim, B., Gotte, D., Chen, X., Cam, M., Lambert, P. F., & Zheng, Z. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006715 · Cited by 52 · see citing works
Impact of Replication Stress in Human Papillomavirus Pathogenesis
Moody, C. A. (2018) · Journal of Virology · doi:10.1128/jvi.01012-17 · Cited by 49 · see citing works
Human Papillomavirus Infections and Cancer Stem Cells of Tumors from the Uterine Cervix
Lopez, J. (2012) · The Open Virology Journal · doi:10.2174/1874357901206010232 · Cited by 51 · see citing works
Serial type‐specific human papillomavirus ( HPV ) load measurement allows differentiation between regressing cervical lesions and serial virion productive transient infections
Depuydt, C., Jonckheere, J., Berth, M., Salembier, G. M., Vereecken, A. J., & Bogers, J. (2015) · Cancer Medicine · doi:10.1002/cam4.473 · Cited by 49 · see citing works
Superinfection Exclusion between Two High-Risk Human Papillomavirus Types during a Coinfection
Biryukov, J., & Meyers, C. (2018) · Journal of Virology · doi:10.1128/jvi.01993-17 · Cited by 49 · see citing works
Virion Factors That Target Daxx To Overcome Intrinsic Immunity
Schreiner, S., & Wodrich, H. (2013) · Journal of Virology · doi:10.1128/jvi.00425-13 · Cited by 47 · see citing works
Furin Cleavage of L2 during Papillomavirus Infection: Minimal Dependence on Cyclophilins
Bronnimann, M. P., Calton, C. M., Chiquette, S. F., Li, S., Lu, M., Chapman, J. A., Bratton, K. N., Schlegel, A. M., & Campos, S. K. (2016) · Journal of Virology · doi:10.1128/jvi.00038-16 · Cited by 47 · see citing works
Extracellular Conformational Changes in the Capsid of Human Papillomaviruses Contribute to Asynchronous Uptake into Host Cells
Becker, M., Greune, L., Schmidt, M. A., & Schelhaas, M. (2018) · Journal of Virology · doi:10.1128/jvi.02106-17 · Cited by 46 · see citing works
YAP1 activation by human papillomavirus E7 promotes basal cell identity in squamous epithelia
Hatterschide, J., Castagnino, P. A., Kim, H. W., Sperry, S. M., Montone, K. T., Basu, D., & White, E. A. (2022) · eLife · doi:10.7554/elife.75466 · Cited by 46 · see citing works

PF: Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 2009
Pyeon, D., Pearce, S. M., Lank, S. M., Ahlquist, P., & Lambert, P. F. (2016)
Human Papilloma Virus-Infected Cells
Cruz‐Gregorio, A., & Aranda‐Rivera, A. K. (2023) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-031-40086-5_8 · Cited by 6 · see citing works
Pathogenesis of Human Papillomaviruses in Differentiating Epithelia
Longworth, M. S., & Laimins, L. A. (2004) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.68.2.362-372.2004 · Cited by 680 · see citing works
Human Keratinocyte Cultures in the Investigation of Early Steps of Human Papillomavirus Infection
Griffin, L., Cicchini, L., Xu, T., & Pyeon, D. (2013) · Methods in molecular biology · doi:10.1007/7651_2013_49 · Cited by 15 · see citing works
The Life Cycle of Human Papillomaviruses
Moody, C. A., & Laimins, L. A. (2008) · Springer eBooks · doi:10.1007/978-0-387-68945-6_4 · Cited by 3 · see citing works

Authors: Pyeon, D., Pearce, S. M., Lank, S. M., Ahlquist, P., & Lambert, P. F.
Affiliations: University of Wisconsin–Madison (US)
Howard Hughes Medical Institute (US)
Corresponding author: Ahlquist, Paul
Lambert, Paul F.
ORCID: Pyeon, Dohun
Pearce, Shane M.
Ahlquist, Paul
Lambert, Paul F.
Venue: PLoS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2009-02-27
Volume: 5
Issue: 2
Pages: e1000318
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.1000318
PMC: PMC2642596
OpenAlex: W2074766470
Cited by: 348
References: 52
Citations by year: 2026: 14 · 2025: 22 · 2024: 22 · 2023: 17 · 2022: 16 · 2021: 27 · 2020: 19 · 2019: 25 · 2018: 17 · 2017: 25 · 2016: 26 · 2015: 24 · 2014: 20 · 2013: 30 · 2012: 15
FWCI: 9.85
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Pathogens (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: Howard Hughes Medical Institute
University of Wisconsin-Madison
National Institutes of Health (CA022443)
National Cancer Institute (CA022443, P01CA022443)
National Institute of Allergy and Infectious Diseases (R33AI071947, AI071947, R21AI071947)
Topics: Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Keywords: human papillomavirus, HPV16, cell cycle progression, mitosis, stratified epithelium, keratinocytes, G1 phase, viral gene expression, microbicides, HPV vaccine, viral entry receptor
MeSH terms: Antiviral Agents, Cell Cycle, Cell Division, Cell Survival, Cells, Cultured, Etoposide, Humans, Orthomyxoviridae, Prophase, Transcription, Genetic, Virion, Keratinocytes, Gene Expression Regulation, Viral, Aphidicolin, Genome, Viral, Human papillomavirus 16

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Establishment of human papillomavirus infection requires cell cycle progression

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks