Viral entry mechanisms: Human papillomavirus and a long journey from extracellular matrix to the nucleus

FEBS Journal

Volumn 276, Issue 24, 2009, Pages 7206-7216

  Sapp, Martin ^a   Bienkowska Haba, Malgorzata ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Attachment; Capsid protein; Conformational change; Endocytosis; Endosomal escape; Heparan sulfate; Papillomavirus; PML nuclear body; Receptor; Uncoating

Indexed keywords

CAPSID PROTEIN; CAPSID PROTEIN L1; CAPSID PROTEIN L2; CARRAGEENAN; CAVEOLIN 1; CHLORPROMAZINE; CLATHRIN HEAVY CHAIN; CYCLOPHILIN B; CYSTEINE; DYNAMIN; EPITOPE; F ACTIN; FURIN; GLUCOSAMINE; HEPARAN SULFATE; HEPARIN; HEPARIN LYASE; KALININ; LYSINE; MONOCLONAL ANTIBODY; MUTANT PROTEIN; NEUTRALIZING ANTIBODY; NOCODAZOLE; PEPTIDYLPROLYL ISOMERASE; PROTEIN INHIBITOR; PROTEOHEPARAN SULFATE; SMALL INTERFERING RNA; SYNDECAN 1; UNCLASSIFIED DRUG; URONIC ACID;

ACETYLATION; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; BASAL CELL; BASEMENT MEMBRANE; BINDING SITE; BOVINE PAPILLOMAVIRUS TYPE 1; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL ENERGY; CELL INVASION; CELL MIGRATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRAIN COS7; CELL SURFACE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CYTOMEGALOVIRUS; CYTOSKELETON; CYTOSOL; DISULFIDE BOND; DNA VIRUS; DOWN REGULATION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; EXTRACELLULAR MATRIX; GENE CONSTRUCT; GENE LOCATION; GENE OVEREXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC VARIABILITY; HELA CELL; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 31; HUMAN PAPILLOMAVIRUS TYPE 33; IN VITRO STUDY; INTERNALIZATION; KERATINOCYTE; KNOCKOUT GENE; MICROBIAL DIVERSITY; NONHUMAN; NUCLEAR IMPORT; PINOCYTOSIS; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; RECEPTOR BINDING; SHORT SURVEY; SULFATION; TARGET CELL; UPREGULATION; VIRION; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENE; VIRUS GENOME; VIRUS INFECTION; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSCRIPTION; VIRUS TRANSMISSION; WART VIRUS; WOUND HEALING;

ANIMALS; CAPSID PROTEINS; CELL NUCLEUS; ENDOCYTOSIS; ENDOSOMES; EXTRACELLULAR MATRIX; FEMALE; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PROTEIN CONFORMATION; VIRION; VIRUS INTERNALIZATION;

DNA VIRUSES; HUMAN PAPILLOMAVIRUS; MIRIDAE; PAPILLOMAVIRIDAE;

EID: 71949096137     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07400.x     Document Type: Short Survey

References (80)

1. 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.
2. Roden RB, Greenstone HL, Kirnbauer R, Booy FP, Jessie J, Lowy DR Schiller JT (1996) In vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. J Virol 70, 5875 5883.
3. Rossi JL, Gissmann L, Jansen K Muller M (2000) Assembly of human papillomavirus type 16 pseudovirions in Saccharomyces cerevisiae. Hum Gene Ther 11, 1165 1176.
4. Unckell F, Streeck RE Sapp M (1997) Generation and neutralization of pseudovirions of human papillomavirus type 33. J Virol 71, 2934 2939.
5. Leder C, Kleinschmidt JA, Wiethe C Müller 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.
6. 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.
7. Buck CB, Pastrana DV, Lowy DR Schiller JT (2004) Efficient intracellular assembly of papillomaviral vectors. J Virol 78, 751 757.
8. 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.
9. Wang HK, Duffy AA, Broker TR Chow LT (2009) Robust production and passaging of infectious HPV in squamous epithelium of primary human keratinocytes. Genes Dev 23, 181 194.
10. Day PM, Lowy DR Schiller JT (2008) Heparan sulfate-independent cell binding and infection with furin pre-cleaved papillomavirus capsids. J Virol 82, 12565 12568.
11. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, Lowy DR Schiller JT (2007) Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 13, 857 861.
12. 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 J 60, 1445 1456.
13. 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.
14. Modis Y, Trus BL Harrison SC (2002) Atomic model of the papillomavirus capsid. EMBO J 21, 4754 4762.
15. Carter JJ, Wipf GC, Benki SF, Christensen ND Galloway DA (2003) Identification of a Human Papillomavirus Type 16-Specific Epitope on the C-Terminal Arm of the Major Capsid Protein L1. J Virol 77, 11625 11632.
16. Ludmerer SW, Benincasa D, Mark GE Christensen ND (1997) A neutralizing epitope of human papillomavirus type 11 is principally described by a continuous set of residues which overlap a distinct linear, surface-exposed epitope. J Virol 71, 3834 3839.
17. Ludmerer SW, Benincasa D Mark GE III. (1996) Two amino acid residues confer type specificity to a neutralizing, conformationally dependent epitope on human papillomavirus type 11. J Virol 70, 4791 4794.
18. Roth SD, Sapp M, Streeck RE Selinka HC (2006) Characterization of neutralizing epitopes within the major capsid protein of human papillomavirus type 33. Virol J 3, 83.
19. White WI, Wilson SD, Palmer-Hill FJ, Woods RM, Ghim SJ, Hewitt LA, Goldman DM, Burke SJ, Jenson AB, Koenig S et al. (1999) Characterization of a major neutralizing epitope on human papillomavirus type 16 L1. J Virol 73, 4882 4886.
20. Bishop B, Dasgupta J, Klein M, Garcea RL, Christensen ND, Zhao R Chen XS (2007) Crystal structures of four types of human papillomavirus L1 capsid proteins: understanding the specificity of neutralizing monoclonal antibodies. J Biol Chem 282, 31803 31808.
21. Li M, Beard P, Estes PA, Lyon MK Garcea RL (1998) Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J Virol 72, 2160 2167.
22. 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 Virol 72, 6186 6189.
23. Buck CB, Thompson CD, Pang YYS, Lowy DR Schiller JT (2005) Maturation of papillomavirus capsids. J Virol 79, 2839 2846.
24. Fligge C, Schäfer F, Selinka HC, Sapp C Sapp M (2001) DNA-induced structural changes in the papillomavirus capsid. J Virol 75, 7727 7731.
25. Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT Trus BL (2008) Arrangement of L2 within the papillomavirus capsid. J Virol 82, 5190 5197.
26. Liu WJ, Gissmann L, Sun XY, Kanjanahaluethai A, Muller M, Doorbar J Zhou J (1997) Sequence close to the N-terminus of L2 protein is displayed on the surface of bovine papillomavirus type 1 virions. Virol 227, 474 483.
27. 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. Virology 358, 266 272.
28. Day PM, Gambhira R, Roden RB, Lowy DR Schiller JT (2008) Mechanisms of human papillomavirus type 16 neutralization by L2 cross-neutralizing and L1 type-specific antibodies. J Virol 82, 4638 4646.
29. Yang R, Day PM, Yutzy WH, Lin KY, Hung CF Roden RB (2003) Cell surface-binding motifs of L2 that facilitate papillomavirus infection. J Virol 77, 3531 3541.
30. Campos SK Ozbun MA (2009) Two highly conserved cysteine residues in HPV16 L2 form an intramolecular disulfide bond and are critical for infectivity in human keratinocytes. PLoS ONE 4, e4463.
31. Finnen RL, Erickson KD, Chen XS Garcea RL (2003) Interactions between papillomavirus L1 and L2 capsid proteins. J Virol 77, 4818 4826.
32. Okun MM, Day PM, Greenstone HL, Booy FP, Lowy DR, Schiller JT Roden RB (2001) L1 interaction domains of papillomavirus L2 necessary for viral genome encapsidation. J Virol 75, 4332 4342.
33. Sapp M, Volpers C, Müller M Streeck RE (1995) Organization of the major and minor capsid proteins in human papillomavirus type 33 virus-like particles. J Gen Virol 76, 2407 2412.
34. Giroglou T, Florin L, Schäfer F, Streeck RE Sapp M (2001) Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75, 1565 1570.
35. Joyce JG, Tung J-S, Przysiecki CT, Cook JC, Lehman ED, Sands JA, Jansen KU Keller PM (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.
36. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL Lose EJ (1992) Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 8, 365 393.
37. Fransson LA (2003) Glypicans. Int J Biochem Cell Biol 35, 125 129.
38. Selinka HC, Giroglou T, Nowak T, Christensen ND Sapp M (2003) Further evidence that papillomavirus particles exist in two distinct conformations. J Virol 77, 12961 12967.
39. Selinka HC, Florin L, Patel HD, Freitag K, Schmidtke M, Makarov VA Sapp M (2007) Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces non-infectious uptake of human papillomavirus. J Virol 81, 10970 10980.
40. Shafti-Keramat S, Handisurya A, Kriehuber E, Meneguzzi G, Slupetzky K Kirnbauer R (2003) Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J Virol 77, 13125 13135.
41. Elenius K, Vainio S, Laato M, Salmivirta M, Thesleff I Jalkanen M (1991) Induced expression of syndecan in healing wounds. J Cell Biol 114, 585 595.
42. Gallo RL, Ono M, Povsic T, Page C, Eriksson E, Klagsbrun M Bernfield M (1994) Syndecans, cell surface heparan sulfate proteoglycans, are induced by a proline-rich antimicrobial peptide from wounds. Proc Natl Acad Sci USA 91, 11035 11039.
43. Patterson NA, Smith JL Ozbun MA (2005) Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate. J Virol 79, 6838 6847.
44. 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.
45. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR Schiller JT (2006) Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2, e69.
46. 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.
47. Culp TD, Budgeon LR, Marinkovich MP, Meneguzzi G Christensen ND (2006) Keratinocyte-secreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells. J Virol 80, 8940 8950.
48. Knappe M, Bodevin S, Selinka HC, Spillmann D, Streeck RE, Chen XS, Lindahl U Sapp M (2007) Surface-exposed amino acid residues of HPV16 L1 protein mediating interaction with cell surface heparan sulfate. J Biol Chem 282, 27913 27922.
49. Day PM, Thompson CD, Buck CB, Pang YY, Lowy DR Schiller JT (2007) Neutralization of human papillomavirus with monoclonal antibodies reveals different mechanisms of inhibition. J Virol 81, 8784 8792.
50. Kawana Y, Kawana K, Yoshikawa H, Taketani Y, Yoshiike K Kanda T (2001) Human papillomavirus type 16 minor capsid protein L2 N-terminal region containing a common neutralization epitope binds to the cell surface and enters the cytoplasm. J Virol 75, 2331 2336.
51. Roden RB, Yutzy WH, 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.
52. 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.
53. Bienkowska-Haba M, Patel HD Sapp M (2009) Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog 5, e1000524.
54. Vanpouille C, Deligny A, Delehedde M, Denys A, Melchior A, Lienard X, Lyon M, Mazurier J, Fernig DG Allain F (2007) The heparin/heparan sulfate sequence that interacts with cyclophilin B contains a 3-O-sulfated N-unsubstituted glucosamine residue. J Biol Chem 282, 24416 24429.
55. 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 Virol 81, 9922 9931.
56. Christensen ND, Cladel NM Reed CA (1995) Postattachment neutralization of papillomaviruses by monoclonal and polyclonal antibodies. Virology 207, 136 142.
57. Culp TD Christensen ND (2004) Kinetics of in vitro adsorption and entry of papillomavirus virions. Virology 319, 152 161.
58. 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.
59. Smith JL, Lidke DS Ozbun MA (2008) Virus activated filopodia promote human papillomavirus type 31 uptake from the extracellular matrix. Virology 381, 16 21.
60. Spoden G, Freitag K, Husmann M, Boller K, Sapp M, Lambert C Florin L (2008) Clathrin- and caveolin-independent entry of human papillomavirus type 16 - involvement of tetraspanin-enriched microdomains (TEMs). PLoS ONE 3, e3313.
61. Day PM, Lowy DR Schiller JT (2003) Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307, 1 11.
62. Abban CY, Bradbury NA Meneses PI (2008) HPV16 and BPV1 infection can be blocked by the dynamin inhibitor dynasore. Am J Ther 15, 304 311.
63. Laniosz V, Holthusen KA Meneses PI (2008) Bovine papillomavirus type 1: from clathrin to caveolin. J Virol 82, 6288 6298.
64. Selinka HC, Giroglou T Sapp M (2002) Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299, 279 287.
65. Bousarghin L, Touze A, Sizaret PY Coursaget P (2003) Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol 77, 3846 3850.
66. Hindmarsh PL Laimins LA (2007) Mechanisms regulating expression of the HPV 31 L1 and L2 capsid proteins and pseudovirion entry. Virol J 4, 19.
67. Smith JL, Campos SK, Wandinger-Ness A Ozbun MA (2008) Caveolin-1 dependent infectious entry of human papillomavirus type 31 in human keratinocytes proceeds to the endosomal pathway for pH-dependent uncoating. J Virol 82, 9505 9512.
68. Bossis I, Roden RB, Gambhira R, Yang R, Tagaya M, Howley PM Meneses PI (2005) Interaction of tSNARE syntaxin 18 with the papillomavirus minor capsid protein mediates infection. J Virol 79, 6723 6731.
69. Laniosz V, Nguyen KC Meneses PI (2007) Bovine papillomavirus type 1 infection is mediated by SNARE syntaxin 18. J Virol 81, 7435 7448.
70. Kämper N, Day PM, Nowak T, Selinka HC, Florin L, Bolscher J, Hilbig L, Schiller JT Sapp M (2006) A membrane-destabilizing peptide in capsid protein L2 is required for egress of papillomavirus genomes from endosomes. J Virol 80, 759 768.
71. Rommel O, Dillner J, Fligge C, Bergsdorf C, Wang X, Selinka HC Sapp M (2005) Heparan sulfate proteoglycans interact exclusively with conformationally intact HPV L1 assemblies: basis for a virus-like particle ELISA. J Med Virol 75, 114 121.
72. 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.
73. Merle E, Rose RC, LeRoux L Moroianu J (1999) Nuclear import of HPV11 L1 capsid protein is mediated by karyopherin alpha2beta1 heterodimers. J Cell Biochem 74, 628 637.
74. Nelson LM, Rose RC, LeRoux L, Lane C, Bruya K Moroianu J (2000) Nuclear import and DNA binding of human papillomavirus type 45 L1 capsid protein. J Cell Biochem 79, 225 238.
75. Florin L, Becker KA, Lambert C, Nowak T, Sapp C, Strand D, Streeck RE Sapp M (2006) Identification of a dynein interacting domain in the papillomavirus minor capsid protein L2. J Virol 80, 6691 6696.
76. Becker KA, Florin L, Sapp C Sapp M (2003) Dissection of human papillomavirus type 33 L2 domains involved in nuclear domain (ND) 10 homing and reorganization. Virology 314, 161 167.
77. Darshan MS, Lucchi J, Harding E Moroianu J (2004) The L2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors. J Virol 78, 12179 12188.
78. Fay A, Yutzy WH, 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.
79. Sun XY, Frazer I, Muller M, Gissmann L Zhou J (1995) Sequences required for the nuclear targeting and accumulation of human papillomavirus type 6B L2 protein. Virology 213, 321 327.
80. Pyeon D, Pearce SM, Lank SM, Ahlquist P Lambert PF (2009) Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 5, e1000318.