Structure, Genome, Infection Cycle and Clinical Manifestations Associated with Human Papillomavirus

Author(s): Srishti Vashisht, Harshita Mishra, Pawan K. Mishra, Adam Ekielski, Sushama Talegaonkar*

Journal Name: Current Pharmaceutical Biotechnology

Volume 20 , Issue 15 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


A small, non-enveloped, obligatory parasite, Human papillomavirus (HPV) is known to be the cause of a range of malignancies. These entail benign infections like genital warts as well as malignant, life-threatening conditions such as cervical cancer. Since a very high mortality rate is associated with HPV caused cancers (cervical cancer is a 2nd leading cause of death caused due to cancer among women globally), there is an escalating need to understand and search for ways to combat such medical conditions. Under the same light, the given article provides an insight into the world of this versatile pathogen. Distinct aspects related to HPV have been discussed here. Emphasis has been laid upon the composition, function and assembly of capsid proteins (structural studies) and various genetic elements and their gene products (genomic studies). The essence of the mechanism behind the development of persistent infection and modes responsible for the transmission of the infectious particles has been briefly covered. Finally, the review outlines various infections and diseases caused by HPV with a major focus on their clinical and histological manifestations.

Keywords: Human Papillomavirus (HPV), major and minor capsid proteins, genome, classification, infection cycle, malignancies, cancer.

Cubie, H.A. Diseases associated with human papillomavirus infection. Virology, 2013, 445(1-2), 21-34.
[] [PMID: 23932731]
Doorbar, J.; Egawa, N.; Griffin, H.; Kranjec, C.; Murakami, I. Human papillomavirus molecular biology and disease association. Rev. Med. Virol., 2015, 25(Suppl. 1), 2-23.
[] [PMID: 25752814]
Zheng, Z-M.; Baker, C.C. Papillomavirus genome structure, expression, and post-transcriptional regulation. Front. Biosci., 2006, 11, 2286-2302.
[] [PMID: 16720315]
Yanofsky, V.R.; Patel, R.V.; Goldenberg, G. Genital warts: A comprehensive review. J. Clin. Aesthet. Dermatol., 2012, 5(6), 25-36.
[PMID: 22768354]
Lowy, D.R.; Schiller, J.T. Reducing HPV-associated cancer globally. Cancer Prev. Res. (Phila.), 2012, 5(1), 18-23.
[] [PMID: 22219162]
de Martel, C.; Plummer, M.; Vignat, J.; Franceschi, S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int. J. Cancer, 2017, 141(4), 664-670.
[] [PMID: 28369882]
Torre, L.A.; Bray, F.; Siegel, R.L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin., 2015, 65(2), 87-108.
[] [PMID: 25651787]
Human Papillomaviruses, International Agency for Research on Cancer. 2007.
Graham, S.V. Human papillomavirus: Gene expression, regulation and prospects for novel diagnostic methods and antiviral therapies. Future Microbiol., 2010, 5(10), 1493-1506.
[] [PMID: 21073310]
Wang, J.W.; Roden, R.B. L2, the minor capsid protein of papillomavirus. Virology, 2013, 445(1-2), 175-186.
[] [PMID: 23689062]
Buck, C.B.; Day, P.M.; Trus, B.L. The papillomavirus major capsid protein L1. Virology, 2013, 445(1-2), 169-174.
[] [PMID: 23800545]
Raff, A.B.; Woodham, A.W.; Raff, L.M.; Skeate, J.G.; Yan, L.; Da Silva, D.M.; Schelhaas, M.; Kast, W.M. The evolving field of human papillomavirus receptor research: A review of binding and entry. J. Virol., 2013, 87(11), 6062-6072.
[] [PMID: 23536685]
Buck, C.B.; Trus, B.L. The papillomavirus virion: a machine built to hide molecular Achilles’ heels. Viral Mol. Mach; Springer, 2012, pp. 403-422.
Buck, C.B.; Cheng, N.; Thompson, C.D.; Lowy, D.R.; Steven, A.C.; Schiller, J.T.; Trus, B.L. Arrangement of L2 within the papillomavirus capsid. J. Virol., 2008, 82(11), 5190-5197.
[] [PMID: 18367526]
Okun, M.M.; Day, P.M.; Greenstone, H.L.; Booy, F.P.; Lowy, D.R.; Schiller, J.T.; Roden, R.B. L1 interaction domains of papillomavirus l2 necessary for viral genome encapsidation. J. Virol., 2001, 75(9), 4332-4342.
[] [PMID: 11287582]
Buck, C.B.; Thompson, C.D.; Pang, Y-Y.S.; Lowy, D.R.; Schiller, J.T. Maturation of papillomavirus capsids. J. Virol., 2005, 79(5), 2839-2846.
[] [PMID: 15709003]
Modis, Y.; Trus, B.L.; Harrison, S.C. Atomic model of the papillomavirus capsid. EMBO J., 2002, 21(18), 4754-4762.
[] [PMID: 12234916]
Chen, X.S.; Garcea, R.L.; Goldberg, I.; Casini, G.; Harrison, S.C. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell, 2000, 5(3), 557-567.
[] [PMID: 10882140]
Bissett, S.L.; Godi, A.; Beddows, S. The DE and FG loops of the HPV major capsid protein contribute to the epitopes of vaccine-induced cross-neutralising antibodies. Sci. Rep., 2016, 6, 39730.
[] [PMID: 28004837]
Fahey, L.M.; Raff, A.B.; Da Silva, D.M.; Kast, W.M. A major role for the minor capsid protein of human papillomavirus type 16 in immune escape. J. Immunol., 2009, 183(10), 6151-6156.
[] [PMID: 19864613]
Lowe, J.; Panda, D.; Rose, S.; Jensen, T.; Hughes, W.A.; Tso, F.Y.; Angeletti, P.C. Evolutionary and structural analyses of alpha-papillomavirus capsid proteins yield novel insights into L2 structure and interaction with L1. Virol. J., 2008, 5, 150.
[] [PMID: 19087355]
Mallon, R.G.; Wojciechowicz, D.; Defendi, V. DNA-binding activity of papillomavirus proteins. J. Virol., 1987, 61(5), 1655-1660.
[PMID: 3033292]
Finnen, R.L.; Erickson, K.D.; Chen, X.S.; Garcea, R.L. Interactions between papillomavirus L1 and L2 capsid proteins. J. Virol., 2003, 77(8), 4818-4826.
[] [PMID: 12663788]
Borgogna, C.; Zavattaro, E.; De Andrea, M.; Griffin, H.M.; Dell’Oste, V.; Azzimonti, B.; Landini, M.M.; Peh, W.L.; Pfister, H.; Doorbar, J.; Landolfo, S.; Gariglio, M. Characterization of beta papillomavirus E4 expression in tumours from Epidermodysplasia verruciformis patients and in experimental models. Virology, 2012, 423(2), 195-204.
[] [PMID: 22217391]
Auster, A.S.; Joshua-Tor, L. The DNA-binding domain of human papillomavirus type 18 E1. Crystal structure, dimerization, and DNA binding. J. Biol. Chem., 2004, 279(5), 3733-3742.
[] [PMID: 14593106]
Bergvall, M.; Melendy, T.; Archambault, J. The E1 proteins. Virology, 2013, 445(1-2), 35-56.
[] [PMID: 24029589]
Morin, G.; Fradet-Turcotte, A.; Di Lello, P.; Bergeron-Labrecque, F.; Omichinski, J.G.; Archambault, J. A conserved amphipathic helix in the N-terminal regulatory region of the papillomavirus E1 helicase is required for efficient viral DNA replication. J. Virol., 2011, 85(11), 5287-5300.
[] [PMID: 21450828]
Wilson, V.G.; West, M.; Woytek, K.; Rangasamy, D. Papillomavirus E1 proteins: form, function, and features. Virus Genes, 2002, 24(3), 275-290.
[] [PMID: 12086149]
Hughes, F.J.; Romanos, M.A. E1 protein of human papillomavirus is a DNA helicase/ATPase. Nucleic Acids Res., 1993, 21(25), 5817-5823.
[] [PMID: 8290339]
Enemark, E.J.; Joshua-Tor, L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature, 2006, 442(7100), 270-275.
[] [PMID: 16855583]
Giri, I.; Yaniv, M. Structural and mutational analysis of E2 trans-activating proteins of papillomaviruses reveals three distinct functional domains. EMBO J., 1988, 7(9), 2823-2829.
[] [PMID: 2846285]
Webster, K.; Parish, J.; Pandya, M.; Stern, P.L.; Clarke, A.R.; Gaston, K. The Human Papillomavirus (HPV) 16 E2 protein induces apoptosis in the absence of other HPV proteins and via a p53-dependent pathway. J. Biol. Chem., 2000, 275(1), 87-94.
[] [PMID: 10617590]
McBride, A.A. The papillomavirus E2 proteins. Virology, 2013, 445(1-2), 57-79.
[] [PMID: 23849793]
Dreer, M.; van de Poel, S.; Stubenrauch, F. Control of viral replication and transcription by the papillomavirus E8^E2 protein. Virus Res., 2017, 231, 96-102.
[] [PMID: 27825778]
Sanders, C.M.; Stenlund, A. Transcription factor-dependent loading of the E1 initiator reveals modular assembly of the papillomavirus origin melting complex. J. Biol. Chem., 2000, 275(5), 3522-3534.
[] [PMID: 10652347]
Egawa, N.; Nakahara, T.; Ohno, S.; Narisawa-Saito, M.; Yugawa, T.; Fujita, M.; Yamato, K.; Natori, Y.; Kiyono, T. The E1 protein of human papillomavirus type 16 is dispensable for maintenance replication of the viral genome. J. Virol., 2012, 86(6), 3276-3283.
[] [PMID: 22238312]
Võsa, L.; Sudakov, A.; Remm, M.; Ustav, M.; Kurg, R. Identification and analysis of papillomavirus E2 protein binding sites in the human genome. J. Virol., 2012, 86(1), 348-357.
[] [PMID: 22031941]
Doorbar, J. The E4 protein; structure, function and patterns of expression. Virology, 2013, 445(1-2), 80-98.
[] [PMID: 24016539]
Wang, X.; Meyers, C.; Wang, H-K.; Chow, L.T.; Zheng, Z-M. Construction of a full transcription map of human papillomavirus type 18 during productive viral infection. J. Virol., 2011, 85(16), 8080-8092.
[] [PMID: 21680515]
Venuti, A.; Paolini, F.; Nasir, L.; Corteggio, A.; Roperto, S.; Campo, M.S.; Borzacchiello, G. Papillomavirus E5: The smallest oncoprotein with many functions. Mol. Cancer, 2011, 10, 140.
[] [PMID: 22078316]
Müller, M.; Prescott, E.L.; Wasson, C.W.; Macdonald, A. Human papillomavirus E5 oncoprotein: Function and potential target for antiviral therapeutics. Future Virol., 2015, 10, 27-39.
DiMaio, D.; Petti, L.M. The E5 proteins. Virology, 2013, 445(1-2), 99-114.
[] [PMID: 23731971]
Campos-León, K.; Wijendra, K.; Siddiqa, A.; Pentland, I.; Feeney, K.M.; Knapman, A.; Davies, R.; Androphy, E.J.; Parish, J.L. Association of human papillomavirus 16 E2 with Rad50-interacting protein 1 enhances viral DNA replication. J. Virol., 2017, 91(5), e02305-e02316.
[] [PMID: 28031358]
de Freitas, A.C.; de Oliveira, T.H.A.; Barros, M.R.; Venuti, A. hrHPV E5 oncoprotein: immune evasion and related immunotherapies. J. Exp. Clin. Cancer Res., 2017, 36(1), 71.
[] [PMID: 28545552]
Genther Williams, S.M.; 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(15), 6534-6542.
[] [PMID: 16061632]
Howie, H.L.; Katzenellenbogen, R.A.; Galloway, D.A. Papillomavirus E6 proteins. Virology, 2009, 384(2), 324-334.
[] [PMID: 19081593]
Lowy, D.R.; Howley, P.M. Papillomaviruses. Fields Virol. In: Lippincott, 4th ed; Williams & Wilkins: Philadelphia, 2001; pp. 2231-2264.
Lipari, F.; McGibbon, G.A.; Wardrop, E.; Cordingley, M.G. Purification and biophysical characterization of a minimal functional domain and of an N-terminal Zn2+-binding fragment from the human papillomavirus type 16 E6 protein. Biochemistry, 2001, 40(5), 1196-1204.
[] [PMID: 11170444]
Pim, D.; Massimi, P.; Banks, L. Alternatively spliced HPV-18 E6* protein inhibits E6 mediated degradation of p53 and suppresses transformed cell growth. Oncogene, 1997, 15(3), 257-264.
[] [PMID: 9233760]
Filippova, M.; Johnson, M.M.; Bautista, M.; Filippov, V.; Fodor, N.; Tungteakkhun, S.S.; Williams, K.; Duerksen-Hughes, P.J. The large and small isoforms of human papillomavirus type 16 E6 bind to and differentially affect procaspase 8 stability and activity. J. Virol., 2007, 81(8), 4116-4129.
[] [PMID: 17267478]
Murray-Zmijewski, F.; Slee, E.A.; Lu, X. A complex barcode underlies the heterogeneous response of p53 to stress. Nat. Rev. Mol. Cell Biol., 2008, 9(9), 702-712.
[] [PMID: 18719709]
Ronco, L.V.; Karpova, A.Y.; Vidal, M.; Howley, P.M. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev., 1998, 12(13), 2061-2072.
[] [PMID: 9649509]
Hasan, U.A.; Bates, E.; Takeshita, F.; Biliato, A.; Accardi, R.; Bouvard, V.; Mansour, M.; Vincent, I.; Gissmann, L.; Iftner, T.; Sideri, M.; Stubenrauch, F.; Tommasino, M. TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16. J. Immunol., 2007, 178(5), 3186-3197.
[] [PMID: 17312167]
Kukimoto, I.; Aihara, S.; Yoshiike, K.; Kanda, T. Human papillomavirus oncoprotein E6 binds to the C-terminal region of human minichromosome maintenance 7 protein. Biochem. Biophys. Res. Commun., 1998, 249(1), 258-262.
[] [PMID: 9705868]
Roman, A.; Munger, K. The papillomavirus E7 proteins. Virology, 2013, 445(1-2), 138-168.
[] [PMID: 23731972]
McLaughlin-Drubin, M.E.; Bromberg-White, J.L.; Meyers, C. The role of the human papillomavirus type 18 E7 oncoprotein during the complete viral life cycle. Virology, 2005, 338(1), 61-68.
[] [PMID: 15921717]
Bodily, J.M.; Mehta, K.P.M.; Cruz, L.; Meyers, C.; Laimins, L.A. The E7 open reading frame acts in cis and in trans to mediate differentiation-dependent activities in the human papillomavirus type 16 life cycle. J. Virol., 2011, 85(17), 8852-8862.
[] [PMID: 21697473]
Cornet, I.; Gheit, T.; Franceschi, S.; Vignat, J.; Burk, R.D.; Sylla, B.S.; Tommasino, M.; Clifford, G.M. Human papillomavirus type 16 genetic variants: Phylogeny and classification based on E6 and LCR. J. Virol., 2012, 86(12), 6855-6861.
[] [PMID: 22491459]
Stünkel, W.; Bernard, H.U. The chromatin structure of the long control region of human papillomavirus type 16 represses viral oncoprotein expression. J. Virol., 1999, 73(3), 1918-1930.
[PMID: 9971771]
Smola-Hess, S.; Pahne, J.; Mauch, C.; Zigrino, P.; Smola, H.; Pfister, H.J. Expression of membrane type 1 matrix metalloproteinase in papillomavirus-positive cells: Role of the human papillomavirus (HPV) 16 and HPV8 E7 gene products. J. Gen. Virol., 2005, 86(Pt 5), 1291-1296.
[] [PMID: 15831939]
Sichero, L.; Sobrinho, J.S.; Villa, L.L. Identification of novel cellular transcription factors that regulate early promoters of human papillomavirus types 18 and 16. J. Infect. Dis., 2012, 206(6), 867-874.
[] [PMID: 22740717]
Bernard, H-U.; Burk, R.D.; Chen, Z.; van Doorslaer, K.; zur Hausen, H.; de Villiers, E-M. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology, 2010, 401(1), 70-79.
[] [PMID: 20206957]
de Villiers, E-M.; Fauquet, C.; Broker, T.R.; Bernard, H-U.; zur Hausen, H. Classification of papillomaviruses. Virology, 2004, 324(1), 17-27.
[] [PMID: 15183049]
Bzhalava, D.; Eklund, C.; Dillner, J. International standardization and classification of human papillomavirus types. Virology, 2015, 476, 341-344.
[] [PMID: 25577151]
Bzhalava, D.; Mühr, L.S.A.; Lagheden, C.; Ekström, J.; Forslund, O.; Dillner, J.; Hultin, E. Deep sequencing extends the diversity of human papillomaviruses in human skin. Sci. Rep., 2014, 4, 5807.
[] [PMID: 25055967]
Johansson, H.; Bzhalava, D.; Ekström, J.; Hultin, E.; Dillner, J.; Forslund, O. Metagenomic sequencing of “HPV-negative” condylomas detects novel putative HPV types. Virology, 2013, 440(1), 1-7.
[] [PMID: 23522725]
Burd, E.M. Human papillomavirus and cervical cancer. Clin. Microbiol. Rev., 2003, 16(1), 1-17.
[] [PMID: 12525422]
Muñoz, N.; Bosch, F.X.; de Sanjosé, S.; Herrero, R.; Castellsagué, X.; Shah, K.V.; Snijders, P.J.; Meijer, C.J. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med., 2003, 348(6), 518-527.
[] [PMID: 12571259]
Procop, G.W.; Pritt, B.S. Human papillomavirus, polyomavirus and parvovirus infections. Pathol Infect Dis E-Book Vol Ser Found Diagn Pathol. In: Elsevier Saunders, 1st ed; Philadelphia, 2014; p. 728.
Richards, K.F.; Mukherjee, S.; Bienkowska-Haba, M.; Pang, J.; Sapp, M. Human papillomavirus species-specific interaction with the basement membrane-resident non-heparan sulfate receptor. Viruses, 2014, 6(12), 4856-4879.
[] [PMID: 25490765]
Laniosz, V.; Holthusen, K.A.; Meneses, P.I. Bovine papillomavirus type 1: From clathrin to caveolin. J. Virol., 2008, 82(13), 6288-6298.
[] [PMID: 18417596]
Machado, F.S.; Rodriguez, N.E.; Adesse, D.; Garzoni, L.R.; Esper, L.; Lisanti, M.P. Recent developments in the interactions between caveolin and pathogens. Caveolins Caveolae In; Springer, 2012, pp. 65-82.
Smith, J.L.; Campos, S.K.; Ozbun, M.A. Human papillomavirus type 31 uses a caveolin 1- and dynamin 2-mediated entry pathway for infection of human keratinocytes. J. Virol., 2007, 81(18), 9922-9931.
[] [PMID: 17626097]
Spoden, G.; Freitag, K.; Husmann, M.; Boller, K.; Sapp, M.; Lambert, C.; Florin, L. Clathrin- and caveolin-independent entry of human papillomavirus type 16--involvement of tetraspanin-enriched microdomains (TEMs). PLoS One, 2008, 3(10) e3313
[] [PMID: 18836553]
Letian, T.; Tianyu, Z. Cellular receptor binding and entry of human papillomavirus. Virol. J., 2010, 7, 2.
[] [PMID: 20051141]
Doorbar, J.; Quint, W.; Banks, L.; Bravo, I.G.; Stoler, M.; Broker, T.R.; Stanley, M.A. The biology and life-cycle of human papillomaviruses. Vaccine, 2012, 30(Suppl. 5), F55-F70.
[] [PMID: 23199966]
Schiller, J.T.; Day, P.M.; Kines, R.C. Current understanding of the mechanism of HPV infection. Gynecol. Oncol., 2010, 118(1)(Suppl.), S12-S17.
[] [PMID: 20494219]
Senapati, R.; Senapati, N.N.; Dwibedi, B. Molecular mechanisms of HPV mediated neoplastic progression. Infect. Agent. Cancer, 2016, 11, 59.
[] [PMID: 27933097]
Horvath, C.A.; Boulet, G.A.; Renoux, V.M.; Delvenne, P.O.; Bogers, J-P.J. Mechanisms of cell entry by human papillomaviruses: an overview. Virol. J., 2010, 7, 11.
[] [PMID: 20089191]
Braaten, K.P.; Laufer, M.R. Human Papillomavirus (HPV), HPV-related disease, and the HPV vaccine. Rev. Obstet. Gynecol., 2008, 1(1), 2-10.
[PMID: 18701931]
Lee, S.M.; Park, J.S.; Norwitz, E.R.; Koo, J.N.; Oh, I.H.; Park, J.W.; Kim, S.M.; Kim, Y.H.; Park, C.W.; Song, Y.S. Risk of vertical transmission of human papillomavirus throughout pregnancy: A prospective study. PLoS One, 2013, 8(6) e66368
[] [PMID: 23785495]
Handisurya, A.; Schellenbacher, C.; Kirnbauer, R. Diseases caused by human papillomaviruses (HPV). J. Dtsch. Dermatol. Ges. J. Ger. Soc. Dermatol. JDDG., 2009, 7, 453-466.
Leto, Md.; Santos Júnior, G.F.; Porro, A.M.; Tomimori, J. Human papillomavirus infection: Etiopathogenesis, molecular biology and clinical manifestations. An. Bras. Dermatol., 2011, 86(2), 306-317.
[] [PMID: 21603814]
Ural, A.; Arslan, S.; Ersöz, Ş.; Değer, B. Verruca vulgaris of the tongue: A case report with a literature review. Bosn. J. Basic Med. Sci., 2014, 14(3), 136-138.
[] [PMID: 25172971]
Bruggink, S.C.; Gussekloo, J.; de Koning, M.N.C.; Feltkamp, M.C.W.; Bavinck, J.N.B.; Quint, W.G.V.; Assendelft, W.J.; Eekhof, J.A. HPV type in plantar warts influences natural course and treatment response: Secondary analysis of a randomised controlled trial. J. Clin. Virol., 2013, 57(3), 227-232.
[] [PMID: 23518443]
Egawa, K.; Honda, Y.; Inaba, Y.; Ono, T. Pigmented viral warts: A clinical and histopathological study including human papillomavirus typing. Br. J. Dermatol., 1998, 138(3), 381-389.
[] [PMID: 9580787]
Patidar, S. Combination treatment of periungual warts. J. Cutan. Aesthet. Surg., 2008, 1(1), 23-24.
[] [PMID: 20300336]
Riddel, C.; Rashid, R.; Thomas, V. Ungual and periungual human papillomavirus-associated squamous cell carcinoma: A review. J. Am. Acad. Dermatol., 2011, 64(6), 1147-1153.
[] [PMID: 21315482]
Neagu, T.P.; Ţigliş, M.; Botezatu, D.; Enache, V.; Cobilinschi, C.O.; Vâlcea-Precup, M.S. GrinŢescu, I.M. Clinical, histological and therapeutic features of Bowen’s disease. Rom. J. Morphol. Embryol., 2017, 58(1), 33-40.
[PMID: 28523295]
Morley, G.L.; Matthews, J.H.; Verpetinske, I.; Thom, G.A. A Comparative study examining the management of Bowen’s disease in the United Kingdom and Australia. Dermatol. Res. Pract., 2015, 2015 421460
[PMID: 26442118]
Emsen, I.M.; Kabalar, M.E. Epidermodysplasia verruciformis: An early and unusual presentation. Can. J. Plast. Surg., 2010, 18(1), 21-24.
[] [PMID: 21358870]
Sá, N.B.; Guerini, M.B.; Barbato, M.T.; Di Giunta, G.; Nunes, D.H. Epidermodysplasia verruciformis: Clinical presentation with varied forms of lesions. An. Bras. Dermatol., 2011, 86(4)(Suppl. 1), S57-S60.
[PMID: 22068772]
Chang, G.J.; Welton, M.L. Human papillomavirus, condylomata acuminata, and anal neoplasia. Clin. Colon Rectal Surg., 2004, 17(4), 221-230.
[] [PMID: 20011263]
Martin, J.M.; Molina, I.; Monteagudo, C.; Marti, N.; Lopez, V.; Jorda, E. Buschke-Lowenstein tumor. J. Dermatol. Case Rep., 2008, 2(4), 60-62.
[] [PMID: 21886716]
Agarwal, S.; Nirwal, G.K.; Singh, H. Buschke-Lowenstein tumour of glans penis. Int. J. Surg. Case Rep., 2014, 5(5), 215-218.
[] [PMID: 24705187]
Antônio, J.R.; Antônio, C.R.; Trídico, L.A.; Alves, F.T.; Rollemberg, I. Erythroplasia of Queyrat treated with topical 5-fluorouracil. An. Bras. Dermatol., 2016, 91(5)(Suppl. 1), 42-44.
[] [PMID: 28300890]
Léonard, B.; Kridelka, F.; Delbecque, K.; Goffin, F.; Demoulin, S.; Doyen, J.; Delvenne, P. A clinical and pathological overview of vulvar condyloma acuminatum, intraepithelial neoplasia, and squamous cell carcinoma. BioMed Res. Int., 2014, 2014 480573
[] [PMID: 24719870]
Orchard, M.; Roman, A.; Parvaiz, A.C. Anal intraepithelial neoplasia--is treatment better than observation? Int. J. Surg., 2013, 11(6), 438-441.
[] [PMID: 23643642]
Ratnavelu, N.; Patel, A.; Fisher, A.D.; Galaal, K.; Cross, P.; Naik, R. High-grade vaginal intraepithelial neoplasia: Can we be selective about who we treat? BJOG, 2013, 120(7), 887-893.
[] [PMID: 23551637]
Velazquez, E.F.; Chaux, A.; Cubilla, A.L. Histologic classification of penile intraepithelial neoplasia. Semin. Diagn. Pathol., 2012, 29(2), 96-102.
[] [PMID: 22641959]
Zreik, A.; Ismail, M.; Nigam, R. Penile intraepithelial neoplasia: Management and outcomes. Hum Androl., 2013, 3, 6-9.
Richart, R.M. Influence of diagnostic and therapeutic procedures on the distribution of cervical intraepithelial neoplasia. Cancer, 1966, 19(11), 1635-1638.
[<1635:AID-CNCR2820191130>3.0.CO;2-1] [PMID: 5925272]
Buckley, C.H.; Butler, E.B.; Fox, H. Cervical intraepithelial neoplasia. J. Clin. Pathol., 1982, 35(1), 1-13.
[] [PMID: 7037858]
Carifi, M.; Napolitano, D.; Morandi, M.; Dall’Olio, D. Recurrent respiratory papillomatosis: current and future perspectives. Ther. Clin. Risk Manag., 2015, 11, 731-738.
[] [PMID: 25999724]
Katsenos, S.; Becker, H.D. Recurrent respiratory papillomatosis: A rare chronic disease, difficult to treat, with potential to lung cancer transformation: apropos of two cases and a brief literature review. Case Rep. Oncol., 2011, 4(1), 162-171.
[] [PMID: 21526134]
Omland, T.; Lie, K.A.; Akre, H.; Sandlie, L.E.; Jebsen, P.; Sandvik, L.; Nymoen, D.A.; Bzhalava, D.; Dillner, J.; Brøndbo, K. Recurrent respiratory papillomatosis: HPV genotypes and risk of high-grade laryngeal neoplasia. PLoS One, 2014, 9(6) e99114
[] [PMID: 24918765]
Recurrent Respiratory Papillomatosis or Laryngeal Papillomatosis 2015. available at.
Al Juboori, A.M.; Afzal, Z.; Ahmed, N. Esophageal squamous cell papilloma: A not-so-rare cause of dysphagia. Gastroenterol. Hepatol. (N. Y.), 2015, 11(12), 815-816.
[PMID: 27134598]
D Kalogeropoulos, C.; M Moschos, M. Advances in diagnosis and treatment of HPV ocular surface infections. Med. Hypothesis Discov. Innov. Ophthalmol., 2015, 4(2), 31-35.
[PMID: 26060827]
Oguma, J.; Ozawa, S.; Kitagawa, Y.; Saikawa, Y.; Oyama, T.; Kitajima, M. Squamous: Clinicopathological study of 24 cases. Dig. Endosc., 16, 285-288.
Sasi, W.; Banerjee, D.; Mokbel, K.; Sharma, A.K. Bilateral florid papillomatosis of the nipple: An unusual indicator for metachronous breast cancer development-a case report. Case Rep. Oncol. Med., 2014, 2014 432609
Borborema-Santos, C.M.; Castro, M.M.; Santos, P.J.; Talhari, S.; Astolfi-Filho, S. Oral focal epithelial hyperplasia: Report of five cases. Braz. Dent. J., 2006, 17(1), 79-82.
[] [PMID: 16721472]
de Castro, L.A.; de Castro, J.G.L.; da Cruz, A.D.L.; Barbosa, B.H de S.; de Spindula-Filho, J.V.; Costa, M.B. Focal epithelial hyperplasia (Heck’s Disease) in a 57-Year-Old Brazilian Patient: A Case Report and Literature Review. J. Clin. Med. Res., 2016, 8(4), 346-350.
[] [PMID: 26985258]
Ozden, B.; Gunduz, K.; Gunhan, O.; Ozden, F.O. A Case Report of Focal Epithelial Hyperplasia (Heck’s disease) with PCR Detection of human papillomavirus. J. Maxillofac. Oral Surg., 2011, 10(4), 357-360.
[] [PMID: 23204755]
Sarabadani, J.; Heydari, S.; Mashreghi, A.; Poornazari, N. A Case report of multifocal epithelial hyperplasia (Heck’s Disease) treated with CO2 laser. J. Dent. Mater. Tech., 2017, 6, 138-141.
Cawson, R.A.; Odell, E.W. Cawson’s essentials of oral pathology and oral medicine. In: Churchill Livingstone; Edinburgh, New York, 2012.
Eze, J.N.; Emeka-Irem, E.N.; Edegbe, F.O. A six-year study of the clinical presentation of cervical cancer and the management challenges encountered at a state teaching hospital in southeast Nigeria. Clin. Med. Insights Oncol., 2013.
Finocchario-Kessler, S.; Wexler, C.; Maloba, M.; Mabachi, N.; Ndikum-Moffor, F.; Bukusi, E. Cervical cancer prevention and treatment research in Africa: A systematic review from a public health perspective. BMC Womens Health, 2016, 16, 29.
[] [PMID: 27259656]
Petignat, P.; Roy, M. Diagnosis and management of cervical cancer. BMJ, 2007, 335(7623), 765-768.
[] [PMID: 17932207]
Schiffman, M.; Wentzensen, N. Human papillomavirus infection and the multistage carcinogenesis of cervical cancer. Cancer Epidemiol. Biomarkers Prev., 2013, 22(4), 553-560.
Alkatout, I.; Schubert, M.; Garbrecht, N.; Weigel, M.T.; Jonat, W.; Mundhenke, C.; Günther, V. Vulvar cancer: Epidemiology, clinical presentation, and management options. Int. J. Womens Health, 2015, 7, 305-313.
[] [PMID: 25848321]
Sagdeo, A.; Gormley, R.H.; Abuabara, K.; Tyring, S.K.; Rady, P.; Elder, D.E.; Kovarik, C.L. The diagnostic challenge of vulvar squamous cell carcinoma: Clinical manifestations and unusual human papillomavirus types. J. Am. Acad. Dermatol., 2014, 70(3), 586-588.
[] [PMID: 24528909]
Sinno, A.K.; Saraiya, M.; Thompson, T.D.; Hernandez, B.Y.; Goodman, M.T.; Steinau, M.; Lynch, C.F.; Cozen, W.; Saber, M.S.; Peters, E.S.; Wilkinson, E.J.; Copeland, G.; Hopenhayn, C.; Watson, M.; Lyu, C.; Unger, E.R. Human papillomavirus genotype prevalence in invasive vaginal cancer from a registry-based population. Obstet. Gynecol., 2014, 123(4), 817-821.
[] [PMID: 24785610]
Woelber, L.; Trillsch, F.; Kock, L.; Grimm, D.; Petersen, C.; Choschzick, M.; Jaenicke, F.; Mahner, S. Management of patients with vulvar cancer: A perspective review according to tumour stage. Ther. Adv. Med. Oncol., 2013, 5(3), 183-192.
[] [PMID: 23634196]
Bansal, A.; Singh, M.P.; Rai, B. Human papillomavirus-associated cancers: A growing global problem. Int. J. Appl. Basic Med. Res., 2016, 6(2), 84-89.
[] [PMID: 27127735]
Gami, B.; Kubba, F.; Ziprin, P. Human papilloma virus and squamous cell carcinoma of the anus. Clin. Med. Insights Oncol., 2014, 8, 113-119.
[] [PMID: 25288893]
Pereira, A.C.C.; Lacerda, H.R.; Barros, R.C. Diagnostic methods for prevention of anal cancer and characteristics of anal lesions caused by HPV in men with HIV/AIDS. Braz. J. Infect. Dis., 2008, 12(4), 293-299.
[PMID: 19030728]
Shiels, M.S.; Kreimer, A.R.; Coghill, A.E.; Darragh, T.M.; Devesa, S.S. Anal cancer incidence in the United States, 1977-2011: Distinct patterns by histology and behavior. Cancer Epidemiol. Prev. Biomark., 2015, 24(10), 1548-1556.
[] [PMID: 26224796]
Clark, P.E.; Spiess, P.E.; Agarwal, N.; Biagioli, M.C.; Eisenberger, M.A.; Greenberg, R.E.; Herr, H.W.; Inman, B.A.; Kuban, D.A.; Kuzel, T.M.; Lele, S.M.; Michalski, J.; Pagliaro, L.; Pal, S.K.; Patterson, A.; Plimack, E.R.; Pohar, K.S.; Porter, M.P.; Richie, J.P.; Sexton, W.J.; Shipley, W.U.; Small, E.J.; Trump, D.L.; Wile, G.; Wilson, T.G.; Dwyer, M.; Ho, M. Penile cancer. J. Natl. Compr. Canc. Netw., 2013, 11(5), 594-615.
[] [PMID: 23667209]
Larke, N.L.; Thomas, S.L.; dos Santos Silva, I.; Weiss, H.A. Male circumcision and penile cancer: A systematic review and meta-analysis. Cancer Causes Control, 2011, 22(8), 1097-1110.
[] [PMID: 21695385]
Lau, Y.M.; Cheung, T.H.; Yeo, W.; Mo, F.; Yu, M.Y.; Lee, K.M. Prognostic implication of human papillomavirus types and species in cervical cancer patients undergoing primary treatment. PLoS One, 2015, 10(4) e0122557
[] [PMID: 25855986]
Viens, L.J.; Henley, S.J.; Watson, M.; Markowitz, L.E.; Thomas, C.C.; Thompson, T.D.; Razzaghi, H.; Saraiya, M. Human papillomavirus-associated cancers - United States, 2008-2012. MMWR Morb. Mortal. Wkly. Rep., 2016, 65(26), 661-666.
[] [PMID: 27387669]
Boscolo-Rizzo, P.; Del Mistro, A.; Bussu, F.; Lupato, V.; Baboci, L.; Almadori, G. New insights into human papillomavirus-associated head and neck squamous cell carcinoma. Acta Otorhinolaryngol Ital. Organo Uff Della Soc. Ital. Otorinolaringol. E Chir. Cerv-facc., 2013, 33, 77-87.
Galbiatti, A.L.S.; Padovani-Junior, J.A.; Maníglia, J.V.; Rodrigues, C.D.S.; Pavarino, É.C.; Goloni-Bertollo, E.M. Head and neck cancer: Causes, prevention and treatment. Rev. Bras. Otorrinolaringol., (Engl. Ed.), 2013, 79(2), 239-247.
[PMID: 23670332]
Ndiaye, C.; Alemany, L.; Diop, Y.; Ndiaye, N.; Diémé, M-J.; Tous, S.; Klaustermeier, J.E.; Alejo, M.; Castellsagué, X.; Bosch, F.X.; Trottier, H.; Sanjosé, S. The role of human papillomavirus in head and neck cancer in Senegal. Infect. Agent. Cancer, 2013, 8(1), 14.
[] [PMID: 23594504]
Nordfors, C.; Vlastos, A.; Du, J.; Ährlund-Richter, A.; Tertipis, N.; Grün, N.; Romanitan, M.; Haeggblom, L.; Roosaar, A.; Dahllöf, G.; Donà, M.G.; Benevolo, M.; Ramqvist, T.; Munck-Wikland, E.; Dalianis, T. Human papillomavirus prevalence is high in oral samples of patients with tonsillar and base of tongue cancer. Oral Oncol., 2014, 50(5), 491-497.
[] [PMID: 24613649]
Max Parkin, D.; Bray, F.; Ferlay, J.; Pisani, P. Global Cancer Statistics, 2002. CA: Cancer J. Clin, 2009.
Sobin, L.H.; Gospodarowicz, M.K.; Wittekind, C. NM Classification of Malignant Tumours, 7th ed; Chichester, West Sussex, UK; Hoboken, NJ: Wiley-Blackwell, 2010.
Cao, F.; Han, H.; Zhang, F.; Wang, B.; Ma, W.; Wang, Y. HPV infection in esophageal squamous cell carcinoma and its relationship to the prognosis of patients in Northern China. ScientificWorldJournal, 2014, 2014 804738
Liyanage, S.S.; Segelov, E.; Malik, A.; Garland, S.M.; Tabrizi, S.N.; Cummins, E.; Seale, H.; Rahman, B.; Moa, A.; Barbour, A.P.; Crowe, P.J.; MacIntyre, C.R. A case-control study of the role of human papillomavirus in oesophageal squamous cell carcinoma in Australia. J. Oncol, 2014, 2014 Article ID 236482. , 7.
Napier, K.J.; Scheerer, M.; Misra, S. Esophageal cancer: A Review of epidemiology, pathogenesis, staging workup and treatment modalities. World J. Gastrointest. Oncol., 2014, 6(5), 112-120.
[] [PMID: 24834141]
Syrjänen, K.J. HPV infections and lung cancer. J. Clin. Pathol., 2002, 55(12), 885-891.
[] [PMID: 12461047]
Kleinberg, L.; Kelly, R.; Yang, S.; Wang, J.S.; Forastiere, A.A. Cancer of the esophagus. Abeloff’s Clin Oncol In: Elsevier, 5th ed; Philadelphia, 2014.
Posner, M.C.; Minsky, B.; Ilson, D.H. Cancer of the esophagus. DeVita Hellman Rosenberg’s Cancer Princ. Pract. Oncol. In: Lippincott- Williams & Wilkins, 9th ed; Philadelphia, 2015.
Bae, J-M.; Kim, E.H. Human papillomavirus infection and risk of lung cancer in never-smokers and women: an ‘adaptive’ meta-analysis. Epidemiol. Health, 2015, 37 e2015052
Prabhu, P.R.; Jayalekshmi, D.; Pillai, M.R. Lung cancer and human papilloma viruses (HPVs): Examining the molecular evidence. J. Oncol. J. Oncol., 2012, 2012 750270
[] [PMID: 22363346]
van Boerdonk, R.A.; Daniels, J.M.; Bloemena, E.; Krijgsman, O.; Steenbergen, R.D.; Brakenhoff, R.H.; Grünberg, K.; Ylstra, B.; Meijer, C.J.; Smit, E.F.; Snijders, P.J.; Heideman, D.A. High-risk human papillomavirus-positive lung cancer: Molecular evidence for a pattern of pulmonary metastasis. J. Thorac. Oncol., 2013, 8(6), 711-718.
[] [PMID: 23571474]
Walter, F.M.; Rubin, G.; Bankhead, C.; Morris, H.C.; Hall, N.; Mills, K.; Dobson, C.; Rintoul, R.C.; Hamilton, W.; Emery, J. Symptoms and other factors associated with time to diagnosis and stage of lung cancer: A prospective cohort study. Br. J. Cancer, 2015, 112(Suppl. 1), S6-S13.
[] [PMID: 25734397]
Islam, S.; Dasgupta, H.; Roychowdhury, A.; Bhattacharya, R.; Mukherjee, N.; Roy, A.; Mandal, G.K.; Alam, N.; Biswas, J.; Mandal, S.; Roychoudhury, S.; Panda, C.K. Study of association and molecular analysis of human papillomavirus in breast cancer of Indian patients: Clinical and prognostic implication. PLoS One, 2017, 12(2) e0172760
[] [PMID: 28245287]
Kolodziej-Andrejuk, S.; Macielag, P.; Patyra, K.; Mandziuk, S.; Pachnia, D.; Mazurkiewicz, M. The presence of HPV DNA in breast cancer. J. Pre-Clin. Clin. Res., 2013, 7(2), 86-89.
Lawson, J.S.; Heng, B. Viruses and breast cancer. Cancers (Basel), 2010, 2(2), 752-772.
[] [PMID: 24281093]
Stratton, M.R.; Campbell, P.J.; Futreal, P.A. The cancer genome. Nature, 2009, 458(7239), 719-724.
[] [PMID: 19360079]
Arruebo, M.; Vilaboa, N.; Sáez-Gutierrez, B.; Lambea, J.; Tres, A.; Valladares, M.; González-Fernández, A. Assessment of the evolution of cancer treatment therapies. Cancers (Basel), 2011, 3(3), 3279-3330.
[] [PMID: 24212956]
Amani, H.; Ajami, M.; Nasseri Maleki, S.; Pazoki-Toroudi, H.; Daglia, M.; Tsetegho Sokeng, A.J.; Di Lorenzo, A.; Nabavi, S.F.; Devi, K.P.; Nabavi, S.M. Targeting signal transducers and activators of transcription (STAT) in human cancer by dietary polyphenolic antioxidants. Biochimie, 2017, 142, 63-79.
[] [PMID: 28807562]
Chan, C.W.H.; Law, B.M.H.; So, W.K.W.; Chow, K.M.; Waye, M.M.Y. 2017, Novel strategies on personalized medicine for breast cancer treatment: An update. Int. J. Mol. Sci., 2017, 18(11), 2423.
[PMID: 29140300]
Yang, F.; Zhang, T-T.; Li, S-S.; Song, P.; Zhang, K.; Guan, Q-Y.; Kang, B.; Xu, J.J.; Chen, H.Y. Endogenous microRNA-triggered and real-time monitored drug release via cascaded energy transfer payloads. Anal. Chem., 2017, 89(19), 10239-10247.
[] [PMID: 28884569]
Geiger, J.L.; Grandis, J.R.; Bauman, J.E. The STAT3 pathway as a therapeutic target in head and neck cancer: Barriers and innovations. Oral Oncol., 2016, 56, 84-92.
[] [PMID: 26733183]
Amani, H.; Habibey, R.; Shokri, F.; Hajmiresmail, S.J.; Akhavan, O.; Mashaghi, A.; Pazoki-Toroudi, H. Selenium nanoparticles for targeted stroke therapy through modulation of inflammatory and metabolic signaling. Sci. Rep., 2019, 9(1), 6044.
[] [PMID: 30988361]
Hassan, C.E.; Webster, T.J. The effect of red-allotrope selenium nanoparticles on head and neck squamous cell viability and growth. Int. J. Nanomedicine, 2016, 11, 3641-3654.
[] [PMID: 27536104]
Chen, Z.; Jing, Y.; Wen, Q.; Ding, X.; Wang, T.; Mu, X.; Chenzhang, Y.; Cao, M. E6 and E7 gene polymorphisms in human papillomavirus types-58 and 33 identified in Southwest China. PLoS One, 2017, 12(1) e0171140
[PMID: 28141822]
Harden, M.E.; Munger, K. Human papillomavirus 16 E6 and E7 oncoprotein expression alters microRNA expression in extracellular vesicles. Virology, 2017, 508, 63-69.
Cindy, C.; Eva-Katharina, P.; Jennifer, B.; Katharina, F.F.; Melissa, M.; Elizabeth, A.W.; Karl, M.; Peter, M.H.; Craig, M.; Michaela, U.G. The human papillomavirus E6 oncoprotein targets USP15 and TRIM25 to suppress RIG-I-mediated innate immune signaling. J. Virol., 2017.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Published on: 22 November, 2019
Page: [1260 - 1280]
Pages: 21
DOI: 10.2174/1389201020666190802115722
Price: $65

Article Metrics

PDF: 55
HTML: 12
PRC: 1