The papillomavirus virion: A machine built to hide molecular achilles' heels

Advances in Experimental Medicine and Biology

Volumn 726, Issue , 2012, Pages 403-422

  Buck, Christopher B ^a   Trus, Benes L ^b,c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CAPSID PROTEIN L1; CAPSID PROTEIN L2; HEPARAN SULFATE; UNCLASSIFIED DRUG; WART VIRUS VACCINE;

ARTICLE; CONFORMATIONAL TRANSITION; HUMAN; LIFE CYCLE; MATURATION; NONHUMAN; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PRIORITY JOURNAL; VERRUCA VULGARIS; VIRION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS LIFE CYCLE; VIRUS MATURATION; VIRUS MORPHOGENESIS;

ANIMALS; HUMANS; MODELS, MOLECULAR; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; PROTEIN CONFORMATION; VIRAL PROTEINS; VIRION;

DNA VIRUSES; HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE; VERTEBRATA;

EID: 84858271333     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-0980-9_18     Document Type: Article

References (113)

1. Alphs HH, Gambhira R, Karanam B, Roberts JN, Jagu S, Schiller JT et al (2008) Protection against heterologous human papillomavirus challenge by a synthetic lipopeptide vaccine containing a broadly cross-neutralizing epitope of L2. Proc Natl Acad Sci USA 105:5850-5855 (Pubitemid 351758461)
2. Bagiyan GA, Koroleva IK, Soroka NV, Ufi mstev AV (2003) Oxidation of thiol compounds by molecular oxygen in aqueous solutions. Russ Chem Bull 52:1135-1141
3. Baker TS, Cheng RH (1996) A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J Struct Biol 116:120-130
4. Belnap DM, Olson NH, Cladel NM, Newcomb WW, Brown JC, Kreider JW et al (1996) Conserved features in papillomavirus and polyomavirus capsids. J Mol Biol 259:249-263 (Pubitemid 26176029)
5. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen HZ, de Villiers EM (2010) Classifi cation of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70-79
6. Bienkowska-Haba M, Patel HD, Sapp M (2009) Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog 5:e1000524
7. Bordeaux J, Forte S, Harding E, Darshan MS, Klucevsek K, Moroianu J (2006) The l2 minor capsid protein of lowrisk human papillomavirus type 11 interacts with host nuclear import receptors and viral DNA. J Virol 80:8259-8262 (Pubitemid 44182325)
8. Boshart M, Gissmann L, Ikenberg H, Kleinheinz A, Scheurlen W, zur Hausen H (1984) A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J 3:1151-1157
9. 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 Virol 79:6723-6731 (Pubitemid 40677303)
10. Buck CB (2008) Defensins' offensive play: exploiting a viral Achilles' heel. Cell Host Microbe 3:3-4
11. Buck CB, Pastrana DV, Lowy DR, Schiller JT (2004) Efficient intracellular assembly of papillomaviral vectors. J Virol 78:751-757 (Pubitemid 38067597)
12. Buck CB, Pastrana DV, Lowy DR, Schiller JT (2005a) Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med 119:445-462
13. Buck CB, Thompson CD, Pang YY, Lowy DR, Schiller JT (2005b) Maturation of papillomavirus capsids. J Virol 79:2839-2846 (Pubitemid 40270562)
14. Buck CB, Day PM, Thompson CD, Lubkowski J, Lu W, Lowy DR et al (2006a) Human alpha-defensins block papillomavirus infection. Proc Natl Acad Sci USA 103:1516-1521 (Pubitemid 43191197)
15. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR, Schiller JT (2006b) Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2:e69
16. Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT et al (2008) Arrangement of L2 within the papillomavirus capsid. J Virol 82:5190-5197 (Pubitemid 351705228)
17. Burk RD, Chen Z, Van Doorslaer K (2009) Human papillomaviruses: genetic basis of carcinogenicity. Public Health Genomics 12:281-290
18. Campo MS, Roden RB (2010) Papillomavirus prophylactic vaccines: established successes, new approaches. J Virol 84:1214-1220
19. Campos SK, Ozbun MA (2009) Two highly conserved cysteine residues in HPV16 L2 form an intramolecular disulfi de bond and are critical for infectivity in human keratinocytes. PLoS One 4:e4463
20. 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 Cell 5:557-567
21. Christensen ND (2005) Cottontail rabbit papillomavirus (CRPV) model system to test antiviral and immunotherapeutic strategies. Antivir Chem Chemother 16:355-362 (Pubitemid 41746046)
22. Chromy LR, Pipas JM, Garcea RL (2003) Chaperone-mediated in vitro assembly of Polyomavirus capsids. Proc Natl Acad Sci USA 100:10477-10482 (Pubitemid 37071903)
23. Chung CH, Gillison ML (2009) Human papillomavirus in head and neck cancer: its role in pathogenesis and clinical implications. Clin Cancer Res 15:6758-6762
24. Ciuffo G (1907) Innesto positivo con fi ltrate di verruca vulgare. Giornale Italiano delle Malattie Veneree 48:12-17
25. Combita AL, Touze A, Bousarghin L, Sizaret PY, Munoz N, Coursaget P (2001) Gene transfer using human papillomavirus pseudovirions varies according to virus genotype and requires cell surface heparan sulfate. FEMS Microbiol Lett 204:183-188 (Pubitemid 33000054)
26. Conway MJ, Meyers C (2009) Replication and assembly of human papillomaviruses. J Dent Res 88:307-317
27. Conway MJ, Alam S, Christensen ND, Meyers C (2009a) Overlapping and independent structural roles for human papillomavirus type 16 L2 conserved cysteines. Virology 393:295-303
28. Conway MJ, Alam S, Ryndock EJ, Cruz L, Christensen ND, Roden RB et al (2009b) Tissue-spanning redox gradientdependent assembly of native human papillomavirus type 16 virions. J Virol 83:10515-10526
29. Culp TD, Budgeon LR, Christensen ND (2006) Human papillomaviruses bind a basal extracellular matrix component secreted by keratinocytes which is distinct from a membrane-associated receptor. Virology 347:147-159
30. Danos O, Engel LW, Chen EY, Yaniv M, Howley PM (1983) Comparative analysis of the human type 1a and bovine type 1 papillomavirus genomes. J Virol 46:557-566 (Pubitemid 13130028)
31. Day PM, Schiller JT (2009) The role of furin in papillomavirus infection. Future Microbiol 4:1255-1262
32. Day PM, Baker CC, Lowy DR, Schiller JT (2004) Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc Natl Acad Sci USA 101:14252-14257 (Pubitemid 39305061)
33. Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT (2008a) Mechanisms of human papillomavirus type 16 neutralization by l2 cross-neutralizing and l1 type-specifi c antibodies. J Virol 82:4638-4646 (Pubitemid 351563700)
34. Day PM, Lowy DR, Schiller JT (2008b) Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J Virol 82:12565-12568
35. Doorbar J (2005) The papillomavirus life cycle. J Clin Virol 32(Suppl 1):S7-S15 (Pubitemid 40332584)
36. Durst M, Gissmann L, Ikenberg H, zur Hausen H (1983) A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci USA 80:3812-3815 (Pubitemid 13063146)
37. Dvoretzky I, Shober R, Chattopadhyay SK, Lowy DR (1980) A quantitative in vitro focus assay for bovine papilloma virus. Virology 103:369-375 (Pubitemid 10119863)
38. Esko JD, Selleck SB (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71:435-471 (Pubitemid 34800227)
39. Esko JD, Kimata K, Lindahl U (2009) Proteoglycans and sulfated glycosaminoglycans. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR et al (eds) Essentials of glycobiology, 2nd edn. The Consortium of Glycobiology Editors
40. La Jolla Favre M, Breitburd F, Croissant O, Orth G (1975) Structural polypeptides of rabbit, bovine, and human papillomaviruses. J Virol 15:1239-1247
41. Fay A, Yutzy WH IV, 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 Virol 78:13447-13454 (Pubitemid 39612744)
42. Feltkamp MC, de Koning MN, Bavinck JN, Ter Schegget J (2008) Betapapillomaviruses: innocent bystanders or causes of skin cancer. J Clin Virol 43:353-360
43. Finch JT, Klug A (1965) The structure of viruses of the papilloma-polyoma type 3. Structure of rabbit papilloma virus, with an appendix on the topography of contrast in negative-staining for electron-microscopy. J Mol Biol 13:1-12
44. Florin L, Becker KA, Sapp C, Lambert C, Sirma H, Muller M et al (2004) Nuclear translocation of papillomavirus minor capsid protein L2 requires Hsc70. J Virol 78:5546-5553 (Pubitemid 38661641)
45. Florin L, Becker KA, Lambert C, Nowak T, Sapp C, Strand D et al (2006) Identification of a dynein interacting domain in the papillomavirus minor capsid protein l2. J Virol 80:6691-6696 (Pubitemid 43927472)
46. 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 Virol 81:13927-13931 (Pubitemid 350247886)
47. Gambhira R, Jagu S, Karanam B, Day PM, Roden R (2009) Role of L2 cysteines in papillomavirus infection and neutralization. Virol J 6:176
48. Gilbert J, Ou W, Silver J, Benjamin T (2006) Downregulation of protein disulfi de isomerase inhibits infection by the mouse polyomavirus. J Virol 80:10868-10870 (Pubitemid 44628933)
49. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M (2001) Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75:1565-1570 (Pubitemid 32094716)
50. Gissmann L, Pfi ster H, Zur Hausen H (1977) Human papilloma viruses (HPV): characterization of four different isolates. Virology 76:569-580 (Pubitemid 8078755)
51. Giuliano AR, Tortolero-Luna G, Ferrer E, Burchell AN, de Sanjose S, Kjaer SK et al (2008) Epidemiology of human papillomavirus infection in men, cancers other than cervical and benign conditions. Vaccine 26(Suppl 10): K17-K28
52. Groff DE, Lancaster WD (1986) Genetic analysis for the 3 ¢ early region transformation and replication functions of bovine papillomavirus type 1. Virology 150:221-230 (Pubitemid 16117738)
53. Hagensee ME, Olson NH, Baker TS, Galloway DA (1994) Three-dimensional structure of vaccinia virus-produced human papillomavirus type 1 capsids. J Virol 68:4503-4505 (Pubitemid 24183046)
54. Heymann JB, Cheng N, Newcomb WW, Trus BL, Brown JC, Steven AC (2003) Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy. Nat Struct Biol 10:334-341 (Pubitemid 36523267)
55. Horvath CA, Boulet GA, Renoux VM, Delvenne PO, Bogers JP (2010) Mechanisms of cell entry by human papillomaviruses: an overview. Virol J 7:11
56. Howley PM, Livingston DM (2009) Small DNA tumor viruses: large contributors to biomedical sciences. Virology 384:256-259
57. Ishii Y, Kondo K, Matsumoto T, Tanaka K, Shinkai-Ouchi F, Hagiwara K et al (2007) Thiol-reactive reagents inhibits intracellular traffi cking of human papillomavirus type 16 pseudovirions by binding to cysteine residues of major capsid protein L1. Virol J 4:110
58. Johnson KM, Kines RC, Roberts JN, Lowy DR, Schiller JT, Day PM (2009) Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J Virol 83:2067-2074
59. Joyce JG, Tung JS, Przysiecki CT, Cook JC, Lehman ED, Sands JA et al (1999) The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem 274:5810-5822 (Pubitemid 29109237)
60. Kämper N, Day PM, Nowak T, Selinka HC, Florin L, Bolscher J et al (2006) A membrane-destabilizing peptide in capsid protein L2 is required for egress of papillomavirus genomes from endosomes. J Virol 80:759-768 (Pubitemid 43062888)
61. Karanam B, Jagu S, Huh WK, Roden RB (2009) Developing vaccines against minor capsid antigen L2 to prevent papillomavirus infection. Immunol Cell Biol 87:287-299
62. Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM (2009) The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc Natl Acad Sci USA 106:20458-20463
63. Klug A, Finch JT (1965) Structure of viruses of the papilloma-polyoma type. I. Human wart virus. J Mol Biol 11:403-423
64. Klug A, Finch JT (1968) Structure of viruses of the papilloma-polyoma type. IV. Analysis of tilting experiments in the electron microscope. J Mol Biol 31:1-12
65. Knappe M, Bodevin S, Selinka HC, Spillmann D, Streeck RE, Chen XS et al (2007) Surface-exposed amino acid residues of HPV16 L1 protein mediating interaction with cell surface heparan sulfate. J Biol Chem 282:27913-27922 (Pubitemid 47529517)
66. Leder C, Kleinschmidt JA, Wiethe C, Muller M (2001) Enhancement of capsid gene expression: preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J Virol 75:9201-9209 (Pubitemid 32851924)
67. Li M, Beard P, Estes PA, Lyon MK, Garcea RL (1998) Intercapsomeric disulfi de bonds in papillomavirus assembly and disassembly. J Virol 72:2160-2167 (Pubitemid 28100772)
68. Lowy DR (2007) History of papillomavirus research. In: Garcea RL, DiMaio D (eds) The papillomaviruses. Springer, New York, NY, pp 13-28
69. Lowy DR, Solomon D, Hildesheim A, Schiller JT, Schiffman M (2008) Human papillomavirus infection and the primary and secondary prevention of cervical cancer. Cancer 113:1980-1993
70. Magnuson B, Rainey EK, Benjamin T, Baryshev M, Mkrtchian S, Tsai B (2005) ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol Cell 20:289-300 (Pubitemid 41484173)
71. McBride AA (2008) Replication and partitioning of papillomavirus genomes. Adv Virus Res 72:155-205
72. McCarthy MP, White WI, Palmer-Hill F, Koenig S, Suzich JA (1998) Quantitative disassembly and reassembly of human papillomavirus type 11 virus like particles in vitro. J Virol 72:32-41 (Pubitemid 28048810)
73. Meyers C, Frattini MG, Hudson JB, Laimins LA (1992) Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation. Science 257:971-973
74. Modis Y, Trus BL, Harrison SC (2002) Atomic model of the papillomavirus capsid. EMBO J 21:4754-4762
75. Nguyen EK, Nemerow GR, Smith JG (2010) Direct evidence from single-cell analysis that human {alpha}-defensins block adenovirus uncoating to neutralize infection. J Virol 84:4041-4049
76. Ogawa H, Taneda A, Kanaoka Y, Sekine T (1979) The histochemical distribution of protein bound sulfhydryl groups in human epidermis by the new staining method. J Histochem Cytochem 27:942-946 (Pubitemid 9196227)
77. Orth G (1986) Epidermodysplasia verruciformis: a model for understanding the oncogenicity of human papillomaviruses. Ciba Found Symp 120:157-174
78. Orth G, Favre M, Croissant O (1977) Characterization of a new type of human papillomavirus that causes skin warts. J Virol 24:108-120 (Pubitemid 8190844)
79. Orth G, Jablonska S, Favre M, Croissant O, Jarzabek-Chorzelska M, Rzesa G (1978) Characterization of two types of human papillomaviruses in lesions of epidermodysplasia verruciformis. Proc Natl Acad Sci USA 75:1537-1541 (Pubitemid 8301593)
80. Orth G, Jablonska S, Jarzabek-Chorzelska M, Obalek S, Rzesa G, Favre M et al (1979) Characteristics of the lesions and risk of malignant conversion associated with the type of human papillomavirus involved in epidermodysplasia verruciformis. Cancer Res 39:1074-1082 (Pubitemid 9135137)
81. Pastrana DV, Gambhira R, Buck CB, Pang YY, Thompson CD, Culp TD et al (2005) Cross-neutralization of cutaneous and mucosal papillomavirus types with anti-sera to the amino terminus of L2. Virology 337:365-372 (Pubitemid 40803480)
82. Pickard C, Louafi F, McGuire C, Lowings K, Kumar P, Cooper H et al (2009) The cutaneous biochemical redox barrier: a component of the innate immune defenses against sensitization by highly reactive environmental xenobiotics. J Immunol 183:7576-7584
83. Pyeon D, Lambert PF, Ahlquist P (2005) Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation. Proc Natl Acad Sci USA 102:9311-9316 (Pubitemid 40923560)
84. Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF (2009) Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 5:e1000318
85. 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 USA 103:1522-1527 (Pubitemid 43191198)
86. Rigoni-Stern D (1842) Fat ti statistici relativi alle malattie cancrose. Giornale Service Progr Pathol Terap Ser 2:507-517
87. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL et al (2007) Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 13:857-861 (Pubitemid 47038188)
88. Roden RB, Yutzy WH IV, Fallon R, Inglis S, Lowy DR, Schiller JT (2000) Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 270:254-257 (Pubitemid 30333671)
89. Rous P, Beard J (1935) The progression to carcinoma of virus induced rabbit papillomas (Shope). J Exp Med 62:523-545
90. Sapp M, Bienkowska-Haba M (2009) Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus. FEBS J 276:7206-7216
91. Sapp M, Fligge C, Petzak I, Harris JR, Streeck RE (1998) Papillomavirus assembly requires trimerization of the major capsid protein by disulfi des between two highly conserved cysteines. J Virol 72:6186-6189 (Pubitemid 28283413)
92. Schadlich L, Senger T, Gerlach B, Mucke N, Klein C, Bravo IG et al (2009) Analysis of modifi ed human papillomavirus type 16 L1 capsomeres: the ability to assemble into larger particles correlates with higher immunogenicity. J Virol 83:7690-7705
93. Schelhaas M, Malmstrom 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. Cell 131:516-529 (Pubitemid 350017762)
94. Schelhaas M, Ewers H, Rajamaki ML, Day PM, Schiller JT, Helenius A (2008) Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog 4:e1000148
95. Schiffman MH, Castle P (2003) Epidemiologic studies of a necessary causal risk factor: human papillomavirus infection and cervical neoplasia. J Natl Cancer Inst 95:E2
96. Schiller JT, Vass WC, Lowy DR (1984) Identification of a second transforming region in bovine papillomavrirus DNA. Proc Natl Acad Sci USA 81:7880-7884 (Pubitemid 15169165)
97. Schwartz S (2000) Regulation of human papillomavirus late gene expression. Ups J Med Sci 105:171-192
98. Schwarz E, Durst M, Demankowski C, Lattermann O, Zech R, Wolfsperger E et al (1983) DNA sequence and genome organization of genital human papillomavirus type 6b. EMBO J 2:2341-2348
99. Selinka HC, Giroglou T, Nowak T, Christensen ND, Sapp M (2003) Further evidence that papillomavirus capsids exist in two distinct conformations. J Virol 77:12961-12967 (Pubitemid 37494291)
100. Selinka HC, Florin L, Patel HD, Freitag K, Schmidtke M, Makarov VA et al (2007) Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus. J Virol 81:10970-10980 (Pubitemid 47536071)
101. Serra A (1924) Studi sul virus della verruca, del papilloma, del condiloma acuminato. Giornale Italiano delle Malattie Veneree e delle Pelle 65:1808-1814
102. Smith JG, Nemerow GR (2008) Mechanism of adenovirus neutralization by human alpha-defensins. Cell Host Microbe 3:11-19
103. Smith JL, Lidke DS, Ozbun MA (2008) Virus activated fi lopodia promote human papillomavirus type 31 uptake from the extracellular matrix. Virology 381:16-21
104. Syverton JT, Berry GP (1935) Carcinoma in the cottontail rabbit following spontaneous virus papilloma (Shope). Proc Soc Exp Biol Med 33:399-400
105. Touze A, Coursaget P (1998) In vitro gene transfer using human papillomavirus-like particles. Nucleic Acids Res 26:1317-1323 (Pubitemid 28291707)
106. 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 Biol 4:413-420 (Pubitemid 27190841)
107. Ullmann EV (1923) On the aetiology of the laryngeal papilloma. Acta Otolaryngol 5:317-334
108. Variot G (1894) Un cas d'incoluation experimentale des verrues de l'enfant a l'homme. J Clin Ther Infant 2:529-531
109. Wolf M, Garcea RL, Grigorieff N, Harrison SC (2010) Subunit interactions in bovine papillomavirus. Proc Natl Acad Sci USA 107:6298-6303
110. Yang YC, Okayama H, Howley PM (1985) Bovine papillomavirus contains multiple transforming genes. Proc Natl Acad Sci USA 82:1030-1034 (Pubitemid 15100488)
111. Zhao Q, Wu S, Manger W, Gadam S (2002) Process for making human papillomavirus virus-like particles with improved properties. Merck &, Inc.
112. Rahway, NJ Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I (1999) Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J Virol 73:4972-4982 (Pubitemid 29246758)
113. zur Hausen H (2009) Papillomaviruses in the causation of human cancers - a brief historical account. Virology 384:260-265