Human papillomaviruses (HPVs) are small dsDNA tumor viruses, which are the etiologic agents of most cervical cancers and are associated with a growing percentage of oropharyngeal cancers. The HPV capsid is non-enveloped, having a T=7 icosahedral symmetry formed via the interaction among 72 pentamers of the major capsid protein, L1. The minor capsid protein L2 associates with L1 pentamers, although it is not known if each L1 pentamer contains a single L2 protein. The HPV life cycle strictly adheres to the host cell differentiation program, and as such, native HPV virions are only produced in vivo or in organotypic “raft” culture. Research producing synthetic papillomavirus particles—such as virus-like particles (VLPs), papillomavirus-based gene transfer vectors, known as pseudovirions (PsV), and papillomavirus genome-containing quasivirions (QV)—has bypassed the need for stratifying and differentiating host tissue in viral assembly and has allowed for the rapid analysis of HPV infectivity pathways, transmission, immunogenicity, and viral structure.
Get full access to this article
View all access options for this article.
References
1.
Anaya-Saavedra G, Ramirez-Amador V, Irigoyen-Camacho ME, Garcia-Cuellar CM, Guido-Jimenez M, Mendez-Martinez R, et al. -2008-. High association of human papillomavirus infection with oral cancer: a case-control study. Arch Med Res39:189–197.
2.
Androphy EJ, Hubbert NL, Schiller JT, Lowy DR -1987-. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J6:989–992.
3.
Baker TS, Drak J, Bina M -1989-. The capsid of small papova viruses contains 72 pentameric capsomeres: direct evidence from cryo-electron-microscopy of simian virus 40. Biophys J55:243–253.
4.
Baker TS, Newcomb WW, Olson NH, Cowsert LM, Olson C, Brown JC -1991-. Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophys J60:1445–1456.
5.
Banerjee NS, Genovese NJ, Noya F, Chien WM, Broker TR, Chow LT -2006-. Conditionally activated E7 proteins of high-risk and low-risk human papillomaviruses induce S phase in postmitotic, differentiated human keratinocytes. J Virol80:6517–6524.
6.
Barksdale SK, Baker CC -1993-. Differentiation-specific expression from the bovine papillomavirus type 1 P2443 and late promoters. J Virol67:5605–5616.
7.
Bastien N, McBride AA -2000-. Interaction of the papillomavirus E2 protein with mitotic chromosomes. Virology270:124–134.
8.
Bedell MA, Hudson JB, Golub TR, Turyk ME, Hosken M, Wilbanks GD, et al. -1991-. Amplification of human papillomavirus genomes in vitro is dependent on epithelial differentiation. J Virol65:2254–2260.
9.
Belnap DM, Olson NH, Cladel NM, Newcomb WW, Brown JC, Kreider JW, et al. -1996-. Conserved features in papillomavirus and polyomavirus capsids. J Mol Biol259:249–263.
10.
Bird G, O’Donnell M, Moroianu J, Garcea RL -2008-. A possible role for cellular karyopherins in regulating polyomavirus and papillomavirus capsid assembly. J Virol82:9848–9857.
11.
Bordeaux J, Forte S, Harding E, Darshan MS, Klucevsek K, Moroianu J -2006-. The l2 minor capsid protein of low-risk human papillomavirus type 11 interacts with host nuclear import receptors and viral DNA. J Virol80:8259–8262.
12.
Bossis I, Roden RB, Gambhira R, Yang R, Tagaya M, Howley PM, et al. -2005-. Interaction of tSNARE syntaxin 18 with the papillomavirus minor capsid protein mediates infection. J Virol79:6723–6731.
13.
Bousarghin L, Touze A, Sizaret PY, Coursaget P -2003-. Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol77:3846–3850.
14.
Breitburd F, Kirnbauer R, Hubbert NL, Nonnenmacher B, Trin-Dinh-Desmarquet C, Orth G, et al. -1995-. Immunization with viruslike particles from cottontail rabbit papillomavirus -CRPV- can protect against experimental CRPV infection. J Virol69:3959–3963.
15.
Brown DR, Kitchin D, Qadadri B, Neptune N, Batteiger T, Ermel A -2006-. The human papillomavirus type 11 E1--E4 protein is a transglutaminase 3 substrate and induces abnormalities of the cornified cell envelope. Virology345:290–298.
16.
Bryan JT, Brown DR -2000-. Association of the human papillomavirus type 11 E1--E4 protein with cornified cell envelopes derived from infected genital epithelium. Virology277:262–269.
17.
Buck CB, Pastrana DV, Lowy DR, Schiller JT -2004-. Efficient intracellular assembly of papillomaviral vectors. J Virol78-2-:751–7.
18.
Buck CB, Thompson CD, Pang YY, Lowy DR, Schiller JT -2005-. Maturation of papillomavirus capsids. J Virol79:2839–2846.
19.
Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR, Schiller JT -2006-. Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog2-7-:e69.
20.
Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT, et al. -2008-. Arrangement of L2 within the papillomavirus capsid. J Virol82:5190–5197.
21.
Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC -2000-. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol Cell5:557–567.
22.
Christensen ND, Cladel NM, Reed CA, Budgeon LR, Embers ME, Skulsky DM, et al. -2001-. Hybrid papillomavirus L1 molecules assemble into virus-like particles that reconstitute conformational epitopes and induce neutralizing antibodies to distinct HPV types. Virology291:324–334.
23.
Chromy LR, Pipas JM, Garcea RL -2003-. Chaperone-mediated in vitro assembly of Polyomavirus capsids. Proc Natl Acad Sci USA100:10477–10482.
24.
Chromy LR, Oltman A, Estes PA, Garcea RL -2006-. Chaperone-mediated in vitro disassembly of polyoma- and papillomaviruses. J Virol80: 5086–5091.
25.
Conger KL, Liu JS, Kuo SR, Chow LT, Wang TS -1999-. Human papillomavirus DNA replication. Interactions between the viral E1 protein and two subunits of human DNA polymerase alpha/primase. J Biol Chem274:2696–2705.
26.
Cripe TP, Haugen TH, Turk JP, Tabatabai F, Schmid PG 3rd, Durst M, et al. -1987-. Transcriptional regulation of the human papillomavirus-16 E6–E7 promoter by a keratinocyte-dependent enhancer, and by viral E2 trans-activator and repressor gene products: implications for cervical carcinogenesis. EMBO J6:3745–3753.
27.
Culp TD, Christensen ND -2004-. Kinetics of in vitro adsorption and entry of papillomavirus virions. Virology319:152–161.
28.
Cumming RC, Andon NL, Haynes PA, Park M, Fischer WH, Schubert D -2004-. Protein disulfide bond formation in the cytoplasm during oxidative stress. J Biol Chem279:21749–21758.
29.
D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, et al. -2007-. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med356:1944–1956.
30.
Day PM, Lowy DR, Schiller JT -2003-. Papillomaviruses infect cells via a clathrin-dependent pathway. Virology307:1–11.
31.
de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H -2004-. Classification of papillomaviruses. Virology324:17–27.
32.
Doorbar J -2005-. The papillomavirus life cycle. J Clin Virol32-Suppl 1-:S7–S15.
33.
Doorbar J, Gallimore PH -1987-. Identification of proteins encoded by the L1 and L2 open reading frames of human papillomavirus 1a. J Virol61:2793–2799.
34.
Doorbar J, Campbell D, Grand RJ, Gallimore PH -1986-. Identification of the human papilloma virus-1a E4 gene products. EMBO J5:355–362.
35.
Doorbar J, Foo C, Coleman N, Medcalf L, Hartley O, Prospero T, et al. -1997-. Characterization of events during the late stages of HPV16 infection in vivo using high-affinity synthetic Fabs to E4. Virology238:40–52.
36.
Dyson N, Howley PM, Munger K, Harlow E -1989-. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science243:934–937.
37.
Egawa K -2003-. Do human papillomaviruses target epidermal stem cells? Dermatology207:251–254.
38.
Embers ME, Budgeon LR, Culp TD, Reed CA, Pickel MD, Christensen ND -2004-. Differential antibody responses to a distinct region of human papillomavirus minor capsid proteins. Vaccine22:670–680.
39.
Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, et al. -2008-. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst100:261–269.
40.
Favre M -1975-. Structural polypeptides of rabbit, bovine, and human papillomaviruses. J Virol15:1239–1247.
41.
Favre M, Orth G, Croissant O, Yaniv M -1975-. Human papillomavirus DNA: physical map. Proc Natl Acad Sci USA72:4810–4814.
42.
Fay A, Yutzy WH 4th, Roden RB, Moroianu J -2004-. The positively charged termini of L2 minor capsid protein required for bovine papillomavirus infection function separately in nuclear import and DNA binding. J Virol78:13447–13454.
43.
Fehrmann F, Klumpp DJ, Laimins LA -2003-. Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J Virol77:2819–2831.
44.
Finnen RL, Erickson KD, Chen XS, Garcea RL -2003-. Interactions between papillomavirus L1 and L2 capsid proteins. J Virol77:4818–4826.
45.
Fligge C, Schafer F, Selinka HC, Sapp C, Sapp M -2001-. DNA-induced structural changes in the papillomavirus capsid. J Virol75:7727–7731.
46.
Flores ER, Lambert PF -1997-. Evidence for a switch in the mode of human papillomavirus type 16 DNA replication during the viral life cycle. J Virol71:7167–7179.
47.
Franquemont DW, Ward BE, Andersen WA, Crum CP -1989-. Prediction of ‘high-risk’ cervical papillomavirus infection by biopsy morphology. Am J Clin Pathol92:577–582.
48.
Gambhira R, Karanam B, Jagu S, Roberts JN, Buck CB, Bossis I, et al. -2007-. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J Virol81:13927–13931.
49.
Gillison ML -2004-. Human papillomavirus-associated head and neck cancer is a distinct epidemiologic, clinical, and molecular entity. Semin Oncol31:744–754.
50.
Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M -2001-. Human papillomavirus infection requires cell surface heparan sulfate. J Virol75:1565–1570.
51.
Gloss B, Bernard HU -1990-. The E6/E7 promoter of human papillomavirus type 16 is activated in the absence of E2 proteins by a sequence-aberrant Sp1 distal element. J Virol64:5577–5584.
52.
Grassmann K, Rapp B, Maschek H, Petry KU, Iftner T -1996-. Identification of a differentiation-inducible promoter in the E7 open reading frame of human papillomavirus type 16 -HPV-16- in raft cultures of a new cell line containing high copy numbers of episomal HPV-16 DNA. J Virol70:2339–2349.
53.
Gu W, Li M, Zhao WM, Fang NX, Bu S, Frazer IH, et al. -2004-. tRNASer-CGA- differentially regulates expression of wild-type and codon-modified papillomavirus L1 genes. Nucleic Acids Res32:4448–4461.
54.
Hagensee ME, Yaegashi N, Galloway DA -1993-. Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J Virol67:315–322.
55.
Hagensee ME, Olson NH, Baker TS, Galloway DA -1994-. Three-dimensional structure of vaccinia virus-produced human papillomavirus type 1 capsids. J Virol68:4503–4505.
56.
Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, et al. -2004-. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet364:1757–1765.
57.
Heino P, Zhou J, Lambert PF -2000-. Interaction of the papillomavirus transcription/replication factor, E2, and the viral capsid protein, L2. Virology276:304–314.
58.
Herrero R, Castellsague X, Pawlita M, Lissowska J, Kee F, Balaram P, et al. -2003-. Human papillomavirus and oral cancer: the International Agency for Research on Cancer multicenter study. J Natl Cancer Inst95:1772–1783.
59.
Hindmarsh PL, Laimins LA -2007-. Mechanisms regulating expression of the HPV 31 L1 and L2 capsid proteins and pseudovirion entry. Virol J4:19.
60.
Hirochika H, Broker TR, Chow LT -1987-. Enhancers and trans-acting E2 transcriptional factors of papillomaviruses. J Virol61:2599–2606.
61.
Holmgren SC, Patterson NA, Ozbun MA, Lambert PF -2005-. The minor capsid protein L2 contributes to two steps in the human papillomavirus type 31 life cycle. J Virol79:3938–3948.
62.
Hoshikawa T, Nakajima T, Uhara H, Gotoh M, Shimosato Y, Tsutsumi K, et al. -1990-. Detection of human papillomavirus DNA in laryngeal squamous cell carcinomas by polymerase chain reaction. Laryngoscope100:647–650.
63.
Hummel M, Hudson JB, Laimins LA -1992-. Differentiation-induced and constitutive transcription of human papillomavirus type 31b in cell lines containing viral episomes. J Virol66:6070–6080.
64.
IARC -2007-. Human papillomaviruses. In: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Geneva, Switzerland: WHO Press, pp. 45–177.
65.
Ishii Y, Kondo K, Matsumoto T, Tanaka K, Shinkai-Ouchi F, Hagiwara K, et al. -2007-. Thiol-reactive reagents inhibits [sic] intracellular trafficking of human papillomavirus type 16 pseudovirions by binding to cysteine residues of major capsid protein L1. Virol J4:110.
66.
Jao CC, Weidman MK, Perez AR, Gharakhanian E -1999-. Cys9, Cys104 and Cys207 of simian virus 40 Vp1 are essential for interpentamer disulfide-linkage and stabilization in cell-free lysates. J Gen Virol80-Pt 9-:2481–2489.
67.
Kanaya T, Kyo S, Laimins LA -1997-. The 5′ region of the human papillomavirus type 31 upstream regulatory region acts as an enhancer which augments viral early expression through the action of YY1. Virology237:159–169.
68.
Kaur P, Li A -2000-. Adhesive properties of human basal epidermal cells: an analysis of keratinocyte stem cells, transit amplifying cells, and postmitotic differentiating cells. J Invest Dermatol114:413–420.
69.
Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT -1992-. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA89:12180–12184.
70.
Kirnbauer R, Taub J, Greenstone H, Roden R, Durst M, Gissmann L, et al. -1993-. Efficient self-assembly of human papillomavirus type 16 L1 and L1–L2 into virus-like particles. J Virol67:6929–6936.
71.
Knight GL, Turnell AS, Roberts S -2006-. Role for Wee1 in inhibition of G2-to-M transition through the cooperation of distinct human papillomavirus type 1 E4 proteins. J Virol80:7416–7426.
72.
Kondo K, Ishii Y, Ochi H, Matsumoto T, Yoshikawa H, Kanda T -2007-. Neutralization of HPV16, 18, 31, and 58 pseudovirions with antisera induced by immunizing rabbits with synthetic peptides representing segments of the HPV16 minor capsid protein L2 surface region. Virology358:266–272.
73.
Koths K, Dressler D -1980-. The rolling circle.capsid complex as an intermediate in phi X DNA replication and viral assembly. J Biol Chem255:4328–4338.
74.
Kyo S, Tam A, Laimins LA -1995-. Transcriptional activity of human papillomavirus type 31b enhancer is regulated through synergistic interaction of AP1 with two novel cellular factors. Virology211:184–197.
75.
Laniosz V, Holthusen KA, Meneses PI -2008-. Bovine papillomavirus type 1: from clathrin to caveolin. J Virol82:6288–6298.
Lehman CW, Botchan MR -1998-. Segregation of viral plasmids depends on tethering to chromosomes and is regulated by phosphorylation. Proc Natl Acad Sci USA95:4338–4343.
78.
Longworth MS, Laimins LA -2004-. Pathogenesis of human papillomaviruses in differentiating epithelia. Microbiol Mol Biol Rev68: 362–372.
79.
Mach H, Volkin DB, Troutman RD, Wang B, Luo Z, Jansen KU, et al. -2006-. Disassembly and reassembly of yeast-derived recombinant human papillomavirus virus-like particles -HPV VLPs-. J Pharm Sci95:2195–2206.
80.
Madsen BS, Jensen HL, van den Brule AJ, Wohlfahrt J, Frisch M -2008-. Risk factors for invasive squamous cell carcinoma of the vulva and vagina—population-based case-control study in Denmark. Int J Cancer122:2827–2834.
81.
McLaughlin-Drubin ME, Meyers C -2004-. Evidence for the coexistence of two genital HPV types within the same host cell in vitro. Virology321:173–180.
82.
McLaughlin-Drubin ME, Meyers C -2005-. Propagation of infectious, high-risk HPV in organotypic “raft” culture. Methods Mol Med119:171–186.
83.
McLaughlin-Drubin ME, Wilson S, Mullikin B, Suzich J, Meyers C -2003-. Human papillomavirus type 45 propagation, infection, and neutralization. Virology312:1–7.
84.
McLaughlin-Drubin ME, Christensen ND, Meyers C -2004-. Propagation, infection, and neutralization of authentic HPV16 virus. Virology322:213–219.
85.
McPhillips MG, Oliveira JG, Spindler JE, Mitra R, McBride AA -2006-. Brd4 is required for e2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J Virol80:9530–9543.
86.
Mellin H, Friesland S, Lewensohn R, Dalianis T, Munck-Wikland E -2000-. Human papillomavirus -HPV- DNA in tonsillar cancer: clinical correlates, risk of relapse, and survival. Int J Cancer89:300–304.
87.
Meyers C, Frattini MG, Hudson JB, Laimins LA -1992-. Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation. Science257:971–973.
88.
Modis Y, Trus BL, Harrison SC -2002-. Atomic model of the papillomavirus capsid. EMBO J21:4754–4762.
89.
Mohr IJ, Clark R, Sun S, Androphy EJ, MacPherson P, Botchan MR -1990-. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science250:1694–1699.
90.
Mork J, Lie AK, Glattre E, Hallmans G, Jellum E, Koskela P, et al. -2001-. Human papillomavirus infection as a risk factor for squamous-cell carcinoma of the head and neck. N Engl J Med344:1125–1131.
91.
Morris JD, Crook T, Bandara LR, Davies R, LaThangue NB, Vousden KH -1993-. Human papillomavirus type 16 E7 regulates E2F and contributes to mitogenic signalling. Oncogene8:893–898.
92.
Morrison EA, Ho GY, Vermund SH, Goldberg GL, Kadish AS, Kelley KF, et al. -1991-. Human papillomavirus infection and other risk factors for cervical neoplasia: a case-control study. Int J Cancer49:6–13.
93.
Neary K, DiMaio D -1989-. Open reading frames E6 and E7 of bovine papillomavirus type 1 are both required for full transformation of mouse C127 cells. J Virol63:259–266.
94.
Niedobitek G, Pitteroff S, Herbst H, Shepherd P, Finn T, Anagnostopoulos I, et al. -1990-. Detection of human papillomavirus type 16 DNA in carcinomas of the palatine tonsil. J Clin Pathol43:918–921.
95.
Ostwald C, Muller P, Barten M, Rutsatz K, Sonnenburg M, Milde-Langosch K, et al. -1994-. Human papillomavirus DNA in oral squamous cell carcinomas and normal mucosa. J Oral Pathol Med23:220–225.
96.
Ozbun MA, Meyers C -1997-. Characterization of late gene transcripts expressed during vegetative replication of human papillomavirus type 31b. J Virol71:5161–5172.
97.
Ozbun MA, Meyers C -1998-. Temporal usage of multiple promoters during the life cycle of human papillomavirus type 31b. J Virol72:2715–2722.
98.
Ozbun MA, Meyers C -1999-. Two novel promoters in the upstream regulatory region of human papillomavirus type 31b are negatively regulated by epithelial differentiation. J Virol73:3505–3510.
99.
Pang YY, Schermer A, Yu J, Sun TT -1993-. Suprabasal change and subsequent formation of disulfide-stabilized homo- and heterodimers of keratins during esophageal epithelial differentiation. J Cell Sci104-Pt 3-:727–740.
100.
Parker JN, Zhao W, Askins KJ, Broker TR, Chow LT -1997-. Mutational analyses of differentiation-dependent human papillomavirus type 18 enhancer elements in epithelial raft cultures of neonatal foreskin keratinocytes. Cell Growth Differ8:751–762.
101.
Patterson NA, Smith JL, Ozbun MA -2005-. Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate. J Virol79:6838–6847.
102.
Phelps WC, Yee CL, Münger K, Howley PM -1988-. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell53:539–547.
103.
Pyeon D, Lambert PF, Ahlquist P -2005-. Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation. Proc Natl Acad Sci USA102:9311–9316.
104.
Querbes W, O’Hara BA, Williams G, Atwood WJ -2006-. Invasion of host cells by JC virus identifies a novel role for caveolae in endosomal sorting of noncaveolar ligands. J Virol80:9402–9413.
105.
Richards RM, Lowy DR, Schiller JT, Day PM -2006-. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc Natl Acad Sci USA103:1522–1527.
106.
Rolfe M, Beer-Romero P, Glass S, Eckstein J, Berdo I, Theodoras A, et al. -1995-. Reconstitution of p53-ubiquitinylation reactions from purified components: the role of human ubiquitin-conjugating enzyme UBC4 and E6-associated protein -E6AP-. Proc Natl Acad Sci USA92:3264–3268.
107.
Romanczuk H, Thierry F, Howley PM -1990-. Mutational analysis of cis elements involved in E2 modulation of human papillomavirus type 16 P97 and type 18 P105 promoters. J Virol64:2849–2859.
108.
Rose RC, Bonnez W, Reichman RC, Garcea RL -1993-. Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles. J Virol67:1936–1944.
109.
Rose RC, Reichman RC, Bonnez W -1994-. Human papillomavirus -HPV- type 11 recombinant virus-like particles induce the formation of neutralizing antibodies and detect HPV-specific antibodies in human sera. J Gen Virol75-Pt 8-:2075–2079.
110.
Sapp M, Fligge C, Petzak I, Harris JR, Streeck RE -1998-. Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines. J Virol72:6186–6189.
111.
Schelhaas M, Malmström J, Pelkmans L, Haugstetter J, Ellgaard L, Grunewald K, et al. -2007-. Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell131: 516–529.
112.
Shepherd CM, Borelli IA, Lander G, Natarajan P, Siddavanahalli V, Bajaj C, et al. -2006-. VIPERdb: a relational database for structural virology. Nucleic Acids Res34:386–389 -database issue-.
113.
Shindoh M, Chiba I, Yasuda M, Saito T, Funaoka K, Kohgo T, et al. -1995-. Detection of human papillomavirus DNA sequences in oral squamous cell carcinomas and their relation to p53 and proliferating cell nuclear antigen expression. Cancer76:1513–1521.
114.
Smith JL, Campos SK, Ozbun MA -2007-. Human papillomavirus type 31 uses a caveolin 1- and dynamin 2-mediated entry pathway for infection of human keratinocytes. J Virol81:9922–9931.
115.
Stehle T, Yan Y, Benjamin TL, Harrison SC -1994-. Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature369:160–163.
116.
Stehle T, Gamblin SJ, Yan Y, Harrison SC -1996-. The structure of simian virus 40 refined at 3.1 A resolution. Structure4:165–182.
117.
Swindle CS, Zou N, Van Tine BA, Shaw GM, Engler JA, Chow LT -1999-. Human papillomavirus DNA replication compartments in a transient DNA replication system. J Virol73:1001–1009.
118.
Trus BL, Roden RB, Greenstone HL, Vrhel M, Schiller JT, Booy FP -1997-. Novel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9 A resolution. Nat Struct Biol4:413–420.
119.
Venuti A, Manni V, Morello R, De Marco F, Marzetti F, Marcante ML -2000-. Physical state and expression of human papillomavirus in laryngeal carcinoma and surrounding normal mucosa. J Med Virol60:396–402.
120.
Vlazny DA, Kwong A, Frenkel N -1982-. Site-specific cleavage/packaging of herpes simplex virus DNA and the selective maturation of nucleocapsids containing full-length viral DNA. Proc Natl Acad Sci USA79:1423–1427.
121.
Volpers C, Schirmacher P, Streeck RE, Sapp M -1994-. Assembly of the major and the minor capsid protein of human papillomavirus type 33 into virus-like particles and tubular structures in insect cells. Virology200:504–512.
122.
White WI, Wilson SD, Palmer-Hill FJ, Woods RM, Ghim SJ, Hewitt LA, et al. -1999-. Characterization of a major neutralizing epitope on human papillomavirus type 16 L1. J Virol73:4882–4889.
123.
Yang R, Wheeler CM, Chen X, Uematsu S, Takeda K, Akira S, et al. -2005-. Papillomavirus capsid mutation to escape dendritic cell-dependent innate immunity in cervical cancer. J Virol79:6741–6750.
124.
Yoon CS, Kim KD, Park SN, Cheong SW -2001-. alpha-6- Integrin is the main receptor of human papillomavirus type 16 VLP. Biochem Biophys Res Commun283:668–673.
125.
You J, Croyle JL, Nishimura A, Ozato K, Howley PM -2004-. Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell117:349–360.
126.
Zhang W, Carmichael J, Ferguson J, Inglis S, Ashrafian H, Stanley M -1998-. Expression of human papillomavirus type 16 L1 protein in Escherichia coli: denaturation, renaturation, and self-assembly of virus-like particles in vitro. Virology243:423–431.
127.
Zheng ZM, Baker CC -2006-. Papillomavirus genome structure, expression, and post-transcriptional regulation. Front Biosci11:2286–2302.
128.
zur Hausen H -1996-. Papillomavirus infections—a major cause of human cancers. Biochim Biophys Acta1288:F55–F78.
