Concepts of papillomavirus entry into host cells

Current Opinion in Virology

Volumn 4, Issue , 2014, Pages 24-31

  Day, Patricia M ^a   Schelhaas, Mario ^b,c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c CiM ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA6 INTEGRIN; CD151 ANTIGEN; CYCLOPHILIN B; DYNEIN ADENOSINE TRIPHOSPHATASE; FOCAL ADHESION KINASE; GLYCOSAMINOGLYCAN; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; HEPARIN; KALININ; KARYOPHERIN; LIPOCORTIN 2; MAMMALIAN TARGET OF RAPAMYCIN; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; NOCODAZOLE; P21 ACTIVATED KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN TYROSINE KINASE; PROTEOHEPARAN SULFATE; RAB PROTEIN; RAS PROTEIN; SORTING NEXIN; SORTING NEXIN 17; TETRASPANIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; CONFORMATIONAL TRANSITION; DRUG INHIBITION; ENDOCYTOSIS; ENDOSOME; EXTRACELLULAR MATRIX; HOST CELL; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 33; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MICROTUBULE; MITOSIS; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TARGET CELL; TRANS GOLGI NETWORK; VIRION; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS LIKE AGENT; VIRUS STRAIN; X RAY CRYSTALLOGRAPHY;

ENDOCYTOSIS; HUMANS; PAPILLOMAVIRIDAE; VIRUS INTERNALIZATION;

EID: 84890544306     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2013.11.002     Document Type: Review

References (87)

1. J. Doorbar, W. Quint, L. Banks, I.G. Bravo, M. Stoler, T.R. Broker, and M.A. Stanley The biology and life-cycle of human papillomaviruses Vaccine 30 5 2012 F55 F70
2. T.S. Baker, W.W. Newcomb, N.H. Olson, L.M. Cowsert, C. Olson, and J.C. Brown Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction Biophys J 60 1991 1445 1456
3. C.B. Buck, N. Cheng, C.D. Thompson, D.R. Lowy, A.C. Steven, J.T. Schiller, and B.L. Trus Arrangement of L2 within the Papillomavirus capsid J Virol 82 2008 5190 5197
4. N.D. Christensen, N.M. Cladel, and C.A. Reed Postattachment neutralization of papillomaviruses by monoclonal and polyclonal antibodies Virology 207 1995 136 142
5. T.D. Culp, and N.D. Christensen Kinetics of in vitro adsorption and entry of papillomavirus virions Virology 319 2004 152 161
6. T. Giroglou, L. Florin, F. Schafer, R.E. Streeck, and M. Sapp Human papillomavirus infection requires cell surface heparan sulfate J Virol 75 2001 1565 1570
7. M. Schelhaas, B. Shah, M. Holzer, P. Blattmann, L. Kuhling, P.M. Day, J.T. Schiller, and A. Helenius Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis PLoS Pathog 8 2012 e1002657
8. J.L. Smith, S.K. Campos, and M.A. Ozbun Human papillomavirus type 31 uses a caveolin 1-mediated and dynamin 2-mediated entry pathway for infection of human keratinocytes J Virol 81 2007 9922 9931
9. R. Kirnbauer, J. Taub, H. Greenstone, R. Roden, M. Durst, L. Gissmann, D.R. Lowy, and J.T. Schiller Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles J Virol 67 1993 6929 6936
10. C.B. Buck, and C.D. Thompson Production of papillomavirus-based gene transfer vectors Curr Protoc Cell Biol 26 26 2007 21
11. C. Meyers, M.G. Frattini, J.B. Hudson, and L.A. Laimins Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation Science 257 1992 971 973
12. C.B. Buck, P.M. Day, and B.L. Trus The papillomavirus major capsid protein L1 Virology 445 2013 169 174
13. C.B. Buck, and B.L. Trus The papillomavirus virion: a machine built to hide molecular Achilles' heels Adv Exp Med Biol 726 2012 403 422
14. C. Cerqueira, and M. Schelhaas Principles of polyoma- and papillomavirus uncoating Med Microbiol Immunol 201 2012 427 436
15. L. Florin, M. Sapp, and G.A. Spoden Host-cell factors involved in papillomavirus entry Med Microbiol Immunol 201 2012 437 448
16. A.B. Raff, A.W. Woodham, L.M. Raff, J.G. Skeate, L. Yan, D.M. Da Silva, M. Schelhaas, and W.M. Kast The evolving field of human papillomavirus receptor research: a review of binding and entry J Virol 87 2013 6062 6070
17. M. Sapp, and M. Bienkowska-Haba Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus FEBS J 276 2009 7206 7210
18. M. Sapp, and P.M. Day Structure, attachment and entry of polyoma- and papillomaviruses Virology 384 2009 400 409
19. J.T. Schiller, P.M. Day, and R.C. Kines Current understanding of the mechanism of HPV infection Gynecol Oncol 118 2010 S12 S17
20. J.W. Wang, and R.B. Roden L2, the minor capsid protein of papillomavirus Virology 445 2013 175 186
21. J.G. Joyce, J.S. Tung, C.T. Przysiecki, J.C. Cook, E.D. Lehman, J.A. Sands, K.U. Jansen, and P.M. Keller 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 1999 5810 5820
22. C. Cerqueira, Y. Liu, L. Kuhling, W. Chai, W. Hafezi, T.H. van Kuppevelt, J.E. Kuhn, T. Feizi, and M. Schelhaas Heparin increases the infectivity of Human Papillomavirus Type 16 independent of cell surface proteoglycans and induces L1 epitope exposure Cell Microbiol 15 2013 1818 1836
23. T.D. Culp, L.R. Budgeon, and N.D. Christensen Human papillomaviruses bind a basal extracellular matrix component secreted by keratinocytes which is distinct from a membrane-associated receptor Virology 347 2006 147 159
24. T.D. Culp, L.R. Budgeon, M.P. Marinkovich, G. Meneguzzi, and N.D. Christensen 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 2006 8940 8950
25. H.C. Selinka, L. Florin, H.D. Patel, K. Freitag, M. Schmidtke, V.A. Makarov, and M. Sapp Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus J Virol 81 2007 10970 10980
26. J. Dasgupta, M. Bienkowska-Haba, M.E. Ortega, H.D. Patel, S. Bodevin, D. Spillmann, B. Bishop, M. Sapp, and X.S. Chen Structural basis of oligosaccharide receptor recognition by human papillomavirus J Biol Chem 286 2011 2617 2620
27. M. Knappe, S. Bodevin, H.C. Selinka, D. Spillmann, R.E. Streeck, X.S. Chen, U. Lindahl, and M. Sapp Surface-exposed amino acid residues of HPV16 L1 protein mediating interaction with cell surface heparan sulfate J Biol Chem 282 2007 27913 27922
28. S. Shafti-Keramat, A. Handisurya, E. Kriehuber, G. Meneguzzi, K. Slupetzky, and R. Kirnbauer Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses J Virol 77 2003 13125 13135
29. H.S. Huang, and P.F. Lambert Use of an in vivo animal model for assessing the role of integrin alpha(6)beta(4) and syndecan-1 in early steps in papillomavirus infection Virology 433 2012 395 400
30. R.M. Schowalter, D.V. Pastrana, and C.B. Buck Glycosaminoglycans and sialylated glycans sequentially facilitate Merkel cell polyomavirus infectious entry PLoS Pathog 7 2011 e1002161
31. H.C. Selinka, T. Giroglou, T. Nowak, N.D. Christensen, and M. Sapp Further evidence that papillomavirus capsids exist in two distinct conformations J Virol 77 2003 12961 12967
32. C.B. Buck, C.D. Thompson, J.N. Roberts, M. Muller, D.R. Lowy, and J.T. Schiller Carrageenan is a potent inhibitor of papillomavirus infection PLoS Pathog 2 2006 e69
33. L. Cruz, and C. Meyers Differential dependence on host cell glycosaminoglycans for infection of epithelial cells by high-risk HPV types PLOS ONE 8 2013 e68379
34. K.M. Johnson, R.C. Kines, J.N. Roberts, D.R. Lowy, J.T. Schiller, and P.M. Day Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus J Virol 83 2009 2067 2070
35. N.A. Patterson, J.L. Smith, and M.A. Ozbun Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate J Virol 79 2005 6838 6840
36. M. Bienkowska-Haba, H.D. Patel, and M. Sapp Target cell cyclophilins facilitate human papillomavirus type 16 infection PLoS Pathog 5 2009 e1000524
37. R.M. Richards, D.R. Lowy, J.T. Schiller, and P.M. Day Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection Proc Natl Acad Sci U S A 103 2006 1522 1527
38. R.C. Kines, C.D. Thompson, D.R. Lowy, J.T. Schiller, and P.M. Day The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding Proc Natl Acad Sci U S A 106 2009 20458 20463
39. P.M. Day, D.R. Lowy, and J.T. Schiller Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids J Virol 82 2008 12565 12568
40. A. Dziduszko, and M.A. Ozbun Annexin A2 and S100A10 regulate human papillomavirus type 16 entry and intracellular trafficking in human keratinocytes J Virol 87 2013 7502 7515
41. M. Evander, I.H. Frazer, E. Payne, Y.M. Qi, K. Hengst, and N.A. McMillan Identification of the alpha6 integrin as a candidate receptor for papillomaviruses J Virol 71 1997 2449 2456
42. N.A. McMillan, E. Payne, I.H. Frazer, and M. Evander Expression of the alpha6 integrin confers papillomavirus binding upon receptor-negative B-cells Virology 261 1999 271 279
43. K.D. Scheffer, A. Gawlitza, G.A. Spoden, X.A. Zhang, C. Lambert, F. Berditchevski, and L. Florin Tetraspanin CD151 mediates papillomavirus type 16 endocytosis J Virol 87 2013 3435 3446
44. G. Spoden, L. Kuhling, N. Cordes, B. Frenzel, M. Sapp, K. Boller, L. Florin, and M. Schelhaas Human papillomavirus types 16, 18, and 31 share similar endocytic requirements for entry J Virol 87 2013 7765 7773
45. A.W. Woodham, D.M. Da Silva, J.G. Skeate, A.B. Raff, M.R. Ambroso, H.E. Brand, J.M. Isas, R. Langen, and W.M. Kast The S100A10 subunit of the annexin A2 heterotetramer facilitates L2-mediated human papillomavirus infection PLOS ONE 7 2012 e43519
46. Z. Surviladze, A. Dziduszko, and M.A. Ozbun Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections PLoS Pathog 8 2012 e1002519
47. M. Schelhaas, H. Ewers, M.L. Rajamaki, P.M. Day, J.T. Schiller, and A. Helenius Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions PLoS Pathog 4 2008 e1000148
48. J.L. Smith, D.S. Lidke, and M.A. Ozbun Virus activated filopodia promote human papillomavirus type 31 uptake from the extracellular matrix Virology 381 2008 16 21
49. V. Vasioukhin, C. Bauer, M. Yin, and E. Fuchs Directed actin polymerization is the driving force for epithelial cell-cell adhesion Cell 100 2000 209 219
50. L. Bousarghin, A. Touze, P.Y. Sizaret, and P. Coursaget Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells J Virol 77 2003 3846 3850
51. P.M. Day, D.R. Lowy, and Schiller JT: Papillomaviruses infect cells via a clathrin-dependent pathway Virology 307 2003 1 11
52. V. Laniosz, S.A. Dabydeen, M.A. Havens, and P.I. Meneses Human papillomavirus type 16 infection of human keratinocytes requires clathrin and caveolin-1 and is brefeldin a sensitive J Virol 83 2009 8221 8232
53. V. Laniosz, K.A. Holthusen, and P.I. Meneses Bovine papillomavirus type 1: from clathrin to caveolin J Virol 82 2008 6288 6298
54. J.L. Smith, S.K. Campos, A. Wandinger-Ness, and M.A. Ozbun 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 2008 9505 9512
55. J. Mercer, M. Schelhaas, and A. Helenius Virus entry by endocytosis Annu Rev Biochem 79 2010 803 833
56. G. Spoden, K. Freitag, M. Husmann, K. Boller, M. Sapp, C. Lambert, and L. Florin Clathrin- and caveolin-independent entry of human papillomavirus type 16 - involvement of tetraspanin-enriched microdomains (TEMs) PLOS ONE 3 2008 e3313
57. H.C. Selinka, T. Giroglou, and M. Sapp Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions Virology 299 2002 279 287
58. C.Y. Abban, and P.I. Meneses Usage of heparan sulfate, integrins, and FAK in HPV16 infection Virology 403 2010 1 16
59. E. Payne, M.R. Bowles, A. Don, J.F. Hancock, and N.A. McMillan Human papillomavirus type 6b virus-like particles are able to activate the Ras-MAP kinase pathway and induce cell proliferation J Virol 75 2001 4150 4157
60. T. Fothergill, and N.A. McMillan Papillomavirus virus-like particles activate the PI3-kinase pathway via alpha-6 beta-4 integrin upon binding Virology 352 2006 319 328
61. Z. Surviladze, R.T. Sterk, S.A. DeHaro, and M.A. Ozbun Cellular entry of human papillomavirus type 16 involves activation of the phosphatidylinositol 3-kinase/Akt/mTOR pathway and inhibition of autophagy J Virol 87 2013 2508 2517
62. L.M. Griffin, L. Cicchini, and D. Pyeon Human papillomavirus infection is inhibited by host autophagy in primary human keratinocytes Virology 437 2013 12 19
63. H. Stenmark Rab GTPases as coordinators of vesicle traffic Nat Rev Mol Cell Biol 10 2009 513 525
64. P.M. Day, C.D. Thompson, R.M. Schowalter, D.R. Lowy, and J.T. Schiller Identification of a role for the trans-Golgi network in human papillomavirus 16 pseudovirus infection J Virol 87 2013 3862 3870
65. K. Quirin, B. Eschli, I. Scheu, L. Poort, J. Kartenbeck, and A. Helenius Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes Virology 378 2008 21 33
66. P.M. Day, C.C. Baker, D.R. Lowy, and J.T. Schiller Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression Proc Natl Acad Sci U S A 101 2004 14252 14257
67. M. Bienkowska-Haba, C. Williams, S.M. Kim, R.L. Garcea, and M. Sapp Cyclophilins facilitate dissociation of the HPV16 capsid protein L1 from the L2/DNA complex following virus entry J Virol 2012
68. A. Lipovsky, A. Popa, G. Pimienta, M. Wyler, A. Bhan, L. Kuruvilla, M.A. Guie, A.C. Poffenberger, C.D. Nelson, and W.J. Atwood Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus Proc Natl Acad Sci U S A 110 2013 7452 7457
69. J.S. Bonifacino, and J.H. Hurley Retromer Curr Opin Cell Biol 20 2008 427 436
70. M. Bergant, and L. Banks SNX17 facilitates infection with diverse papillomavirus types J Virol 87 2013 1270 1273
71. M. Bergant Marusic, M.A. Ozbun, S.K. Campos, M.P. Myers, and L. Banks Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17 Traffic 13 2012 455 467
72. R.T. Bottcher, C. Stremmel, A. Meves, H. Meyer, M. Widmaier, H.Y. Tseng, and R. Fassler Sorting nexin 17 prevents lysosomal degradation of beta1 integrins by binding to the beta1-integrin tail Nat Cell Biol 14 2012 584 592
73. J. Lee, C. Retamal, L. Cuitino, A. Caruano-Yzermans, J.E. Shin, P. van Kerkhof, M.P. Marzolo, and G. Bu Adaptor protein sorting nexin 17 regulates amyloid precursor protein trafficking and processing in the early endosomes J Biol Chem 283 2008 11501 11508
74. P. Farfan, J. Lee, J. Larios, P. Sotelo, G. Bu, and M.P. Marzolo A sorting nexin 17-binding domain within the LRP1 cytoplasmic tail mediates receptor recycling through the basolateral sorting endosome Traffic 14 2013 823 838
75. N. Kamper, P.M. Day, T. Nowak, H.C. Selinka, L. Florin, J. Bolscher, L. Hilbig, J.T. Schiller, and M. Sapp A membrane-destabilizing peptide in capsid protein L2 is required for egress of papillomavirus genomes from endosomes J Virol 80 2006 759 768
76. M.P. Bronnimann, J.A. Chapman, C.K. Park, and S.K. Campos A transmembrane domain and GxxxG motifs within L2 are essential for papillomavirus infection J Virol 87 2013 464 473
77. L. Florin, K.A. Becker, C. Lambert, T. Nowak, C. Sapp, D. Strand, R.E. Streeck, and M. Sapp Identification of a dynein interacting domain in the papillomavirus minor capsid protein l2 J Virol 80 2006 6691 6700
78. M.A. Schneider, G.A. Spoden, L. Florin, and C. Lambert Identification of the dynein light chains required for human papillomavirus infection Cell Microbiol 13 2011 32 46
79. M.S. Darshan, J. Lucchi, E. Harding, and J. Moroianu The l2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors J Virol 78 2004 12179 12188
80. S. Mamoor, Z. Onder, B. Karanam, K. Kwak, J. Bordeaux, L. Crosby, R.B. Roden, and J. Moroianu The high risk HPV16 L2 minor capsid protein has multiple transport signals that mediate its nucleocytoplasmic traffic Virology 422 2012 413 424
81. D. Pyeon, S.M. Pearce, S.M. Lank, P. Ahlquist, and P.F. Lambert Establishment of human papillomavirus infection requires cell cycle progression PLoS Pathog 5 2009 e1000318
82. R.D. Everett, P. Lomonte, T. Sternsdorf, R. van Driel, and A. Orr Cell cycle regulation of PML modification and ND10 composition J Cell Sci 112 Pt. 24 1999 4581 4588
83. P.M. Day, R.C. Kines, C.D. Thompson, S. Jagu, R.B. Roden, D.R. Lowy, and J.T. Schiller In vivo mechanisms of vaccine-induced protection against HPV infection Cell Host Microbe 8 2010 260 270
84. N.M. Cladel, L.R. Budgeon, T.K. Cooper, K.K. Balogh, J. Hu, and N.D. Christensen Secondary infections, expanded tissue tropism, and evidence for malignant potential in immunocompromised mice infected with mus musculus papillomavirus 1 DNA and virus J Virol 87 2013 9391 9395
85. A. Ingle, S. Ghim, J. Joh, I. Chepkoech, A. Bennett Jenson, and J.P. Sundberg Novel laboratory mouse papillomavirus (MusPV) infection Vet Pathol 48 2011 500 505
86. J. Joh, A.B. Jenson, W. King, M. Proctor, A. Ingle, J.P. Sundberg, and S.J. Ghim Genomic analysis of the first laboratory-mouse papillomavirus J Gen Virol 92 2011 692 698
87. E. Schulz, M. Gottschling, R.G. Ulrich, D. Richter, E. Stockfleth, and I. Nindl Isolation of three novel rat and mouse papillomaviruses and their genomic characterization PLOS ONE 7 2012 e47164