Human papillomavirus species-specific interaction with the basement membrane-resident non-heparan sulfate receptor

Viruses

Volumn 6, Issue 12, 2014, Pages 4856-4879

  Richards, Kathleen F ^a   Mukherjee, Santanu ^a   Bienkowska Haba, Malgorzata ^a   Pang, Jia ^a   Sapp, Martin ^a  

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

Author keywords

Entry; Extracellular matrix; Heparan sulfate; HPV; Laminin 332; Receptor

Indexed keywords

GREEN FLUORESCENT PROTEIN; HEPARIN; KALININ; MARIMASTAT; MATRIX METALLOPROTEINASE; SMALL INTERFERING RNA; LAMININ; VIRUS RECEPTOR;

ADENOCARCINOMA; ARTICLE; BASEMENT MEMBRANE; CELL TRANSFER; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; IMMUNOFLUORESCENCE; NONHUMAN; PAPILLOMAVIRUS INFECTION; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RNA ISOLATION; SQUAMOUS CELL CARCINOMA; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; WESTERN BLOTTING; FEMALE; GENETICS; METABOLISM; SPECIES DIFFERENCE; VIROLOGY;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

BASEMENT MEMBRANE; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMAN PAPILLOMAVIRUS 18; HUMANS; LAMININ; PAPILLOMAVIRUS INFECTIONS; RECEPTORS, VIRUS; SPECIES SPECIFICITY;

EID: 84930935143     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v6124856     Document Type: Article

References (75)

1. 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, 70-79.
2. 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.
3. Bosch, F.X.; Burchell, A.N.; Schiffman, M.; Giuliano, A.R.; de Sanjose, S.; Bruni, L.; Tortolero-Luna, G.; Kjaer, S.K.; Munoz, N. Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 2008, 26 (Suppl. 10), K1-K16.
4. Zur Hausen, H. Human papillomavirus & cervical cancer. Indian J. Med. Res. 2009, 130, 209.
5. Smith, J.S.; Lindsay, L.; Hoots, B.; Keys, J.; Franceschi, S.; Winer, R.; Clifford, G.M. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: A meta-analysis update. Int. J. Cancer 2007, 121, 621-632.
6. Bosch, F.X.; Manos, M.M.; Munoz, N.; Sherman, M.; Jansen, A.M.; Peto, J.; Schiffman, M.H.; Moreno, V.; Kurman, R.; Shah, K.V. Prevalence of human papillomavirus in cervical cancer: A worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J. Natl. Cancer Inst. 1995, 87, 796-802.
7. Zur Hausen, H. Papillomaviruses in the causation of human cancers—A brief historical account. Virology 2009, 384, 260-265.
8. Syrjanen, S.; Lodi, G.; von Bultzingslowen, I.; Aliko, A.; Arduino, P.; Campisi, G.; Challacombe, S.; Ficarra, G.; Flaitz, C.; Zhou, H.M.; et al. Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: A systematic review. Oral. Dis. 2011, 17 (Suppl. 1), 58-72.
9. Cubie, H.A. Diseases associated with human papillomavirus infection. Virology 2013, 445, 21-34.
10. Baker, T.S.; Newcomb, W.W.; Olson, N.H.; Cowsert, L.M.; Olson, C.; Brown, J.C. Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophys. J. 1991, 60, 1445-1456.
11. 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, 557-567.
12. Modis, Y.; Trus, B.L.; Harrison, S.C. Atomic model of the papillomavirus capsid. EMBO J. 2002, 21, 4754-4762.
13. Li, M.; Beard, P.; Estes, P.A.; Lyon, M.K.; Garcea, R.L. Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J. Virol. 1998, 72, 2160-2167.
14. Sapp, M.; Fligge, C.; Petzak, I.; Harris, J.R.; Streeck, R.E. Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines. J. Virol. 1998, 72, 6186-6189.
15. 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, 5190-5197.
16. Zhao, K.N.; Sun, X.Y.; Frazer, I.H.; Zhou, J. DNA packaging by L1 and L2 capsid proteins of bovine papillomavirus type 1. Virology 1998, 243, 482-491.
17. Roden, R.B.; Day, P.M.; Bronzo, B.K.; Yutzy, W.H.T.; Yang, Y.; Lowy, D.R.; Schiller, J.T. Positively charged termini of the L2 minor capsid protein are necessary for papillomavirus infection. J. Virol. 2001, 75, 10493-10497.
18. Buck, C.B.; Pastrana, D.V.; Lowy, D.R.; Schiller, J.T. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 2004, 78, 751-757.
19. Buck, C.B.; Thompson, C.D.; Pang, Y.Y.; Lowy, D.R.; Schiller, J.T. Maturation of papillomavirus capsids. J. Virol. 2005, 79, 2839-2846.
20. Leder, C.; Kleinschmidt, J.A.; Wiethe, C.; Muller, M. Enhancement of capsid gene expression: Preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J. Virol. 2001, 75, 9201-9209.
21. 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, 6062-6072.
22. Kines, R.C.; Thompson, C.D.; Lowy, D.R.; Schiller, J.T.; Day, P.M. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc. Natl. Acad. Sci. USA 2009, 106, 20458-20463.
23. Schelhaas, M.; Shah, B.; Holzer, M.; Blattmann, P.; Kuhling, L.; Day, P.M.; Schiller, J.T.; Helenius, A. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog. 2012, 8, e1002657.
24. Giroglou, T.; Florin, L.; Schafer, F.; Streeck, R.E.; Sapp, M. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 2001, 75, 1565-1570.
25. Joyce, J.G.; Tung, J.S.; Przysiecki, C.T.; Cook, J.C.; Lehman, E.D.; Sands, J.A.; Jansen, K.U.; Keller, P.M. 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. 1999, 274, 5810-5822.
26. Dasgupta, J.; Bienkowska-Haba, M.; Ortega, M.E.; Patel, H.D.; Bodevin, S.; Spillmann, D.; Bishop, B.; Sapp, M.; Chen, X.S. Structural basis of oligosaccharide receptor recognition by human papillomavirus. J. Biol. Chem. 2011, 286, 2617-2624.
27. Knappe, M.; Bodevin, S.; Selinka, H.C.; Spillmann, D.; Streeck, R.E.; Chen, X.S.; Lindahl, U.; Sapp, M. Surface-exposed amino acid residues of HPV16 L1 protein mediating interaction with cell surface heparan sulfate. J. Biol. Chem. 2007, 282, 27913-27922.
28. Richards, K.F.; Bienkowska-Haba, M.; Dasgupta, J.; Chen, X.S.; Sapp, M. Multiple heparan sulfate binding site engagements are required for the infectious entry of human papillomavirus type 16. J. Virol. 2013, 87, 11426-11437.
29. Bienkowska-Haba, M.; Patel, H.D.; Sapp, M. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog. 2009, 5, e1000524.
30. Richards, R.M.; Lowy, D.R.; Schiller, J.T.; Day, P.M. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc. Natl. Acad. Sci. USA 2006, 103, 1522-1527.
31. Spoden, G.; Kuhling, L.; Cordes, N.; Frenzel, B.; Sapp, M.; Boller, K.; Florin, L.; Schelhaas, M. Human papillomavirus types 16, 18, and 31 share similar endocytic requirements for entry. J. Virol. 2013, 87, 7765-7773.
32. Scheffer, K.D.; Gawlitza, A.; Spoden, G.A.; Zhang, X.A.; Lambert, C.; Berditchevski, F.; Florin, L. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J. Virol 2013, 87, 3435-3446.
33. Abban, C.Y.; Meneses, P.I. Usage of heparan sulfate, integrins, and FAK in HPV16 infection. Virology 2010, 403, 1-16.
34. Yoon, C.S.; Kim, K.D.; Park, S.N.; Cheong, S.W. α6 integrin is the main receptor of human papillomavirus type 16 VLP. Biochem. Biophys. Res. Commun. 2001, 283, 668-673.
35. Evander, M.; Frazer, I.H.; Payne, E.; Qi, Y.M.; Hengst, K.; McMillan, N.A. Identification of the alpha6 integrin as a candidate receptor for papillomaviruses. J. Virol. 1997, 71, 2449-2456.
36. 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, e3313.
37. Woodham, A.W.; da Silva, D.M.; Skeate, J.G.; Raff, A.B.; Ambroso, M.R.; Brand, H.E.; Isas, J.M.; Langen, R.; Kast, W.M. The S100A10 subunit of the annexin A2 heterotetramer facilitates L2-mediated human papillomavirus infection. PLoS One 2012, 7, e43519.
38. Dziduszko, A.; Ozbun, M.A. Annexin A2 and S100A10 Regulate Human Papillomavirus Type 16 Entry and Intracellular Trafficking in Human Keratinocytes. J. Virol. 2013, 87, 7502-7515.
39. Surviladze, Z.; Dziduszko, A.; Ozbun, M.A. Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections. PLoS Pathog. 2012, 8, e1002519.
40. Bienkowska-Haba, M.; Williams, C.; Kim, S.M.; Garcea, R.L.; Sapp, M. Cyclophilins Facilitate Dissociation of the Human Papillomavirus Type 16 Capsid Protein L1 from the L2/DNA Complex following Virus Entry. J. Virol. 2012, 86, 9875-9887.
41. Day, P.M.; Thompson, C.D.; Schowalter, R.M.; Lowy, D.R.; Schiller, J.T. Identification of a role for the trans-Golgi network in human papillomavirus 16 pseudovirus infection. J. Virol. 2013, 87, 3862-3870.
42. Day, P.M.; Baker, C.C.; Lowy, D.R.; Schiller, J.T. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc. Natl. Acad. Sci. USA 2004, 101, 14252-14257.
43. Pyeon, D.; Pearce, S.M.; Lank, S.M.; Ahlquist, P.; Lambert, P.F. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog. 2009, 5, e1000318.
44. Lipovsky, A.; Popa, A.; Pimienta, G.; Wyler, M.; Bhan, A.; Kuruvilla, L.; Guie, M.A.; Poffenberger, A.C.; Nelson, C.D.; Atwood, W.J.; et al. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc. Natl. Acad. Sci. USA 2013, 110, 7452-7457.
45. Aydin, I.; Weber, S.; Snijder, B.; Samperio Ventayol, P.; Kuhbacher, A.; Becker, M.; Day, P.M.; Schiller, J.T.; Kann, M.; Pelkmans, L.; et al. Large Scale RNAi Reveals the Requirement of Nuclear Envelope Breakdown for Nuclear Import of Human Papillomaviruses. PLoS Pathog. 2014, 10, e1004162.
46. DiGiuseppe, S.; Bienkowska-Haba, M.; Hilbig, L.; Sapp, M. The nuclear retention signal of HPV16 L2 protein is essential for incoming viral genome to transverse the trans-Golgi network. Virology 2014, 458-459, 93-105.
47. Bulk, S.; Berkhof, J.; Bulkmans, N.W.; Zielinski, G.D.; Rozendaal, L.; van Kemenade, F.J.; Snijders, P.J.; Meijer, C.J. Preferential risk of HPV16 for squamous cell carcinoma and of HPV18 for adenocarcinoma of the cervix compared to women with normal cytology in The Netherlands. Br. J. Cancer 2006, 94, 171-175.
48. Lindahl, U.; Kusche-Gullberg, M.; Kjellen, L. Regulated diversity of heparan sulfate. J. Biol. Chem. 1998, 273, 24979-24982.
49. Johnson, K.M.; Kines, R.C.; Roberts, J.N.; Lowy, D.R.; Schiller, J.T.; Day, P.M. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J. Virol. 2009, 83, 2067-2074.
50. Shafti-Keramat, S.; Handisurya, A.; Kriehuber, E.; Meneguzzi, G.; Slupetzky, K.; Kirnbauer, R. Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J. Virol. 2003, 77, 13125-13135.
51. Culp, T.D.; Budgeon, L.R.; Marinkovich, M.P.; Meneguzzi, G.; Christensen, N.D. Keratinocyte-secreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells. J. Virol. 2006, 80, 8940-8950.
52. Selinka, H.C.; Florin, L.; Patel, H.D.; Freitag, K.; Schmidtke, M.; Makarov, V.A.; Sapp, M. Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus. J. Virol. 2007, 81, 10970-10980.
53. Cerqueira, C.; Liu, Y.; Kuhling, L.; Chai, W.; Hafezi, W.; van Kuppevelt, T.H.; Kuhn, J.E.; Feizi, T.; Schelhaas, M. Heparin increases the infectivity of Human Papillomavirus type 16 independent of cell surface proteoglycans and induces L1 epitope exposure. Cell. Microbiol. 2013, 15, 1818-1836.
54. Rommel, O.; Dillner, J.; Fligge, C.; Bergsdorf, C.; Wang, X.; Selinka, H.C.; Sapp, M. Heparan sulfate proteoglycans interact exclusively with conformationally intact HPV L1 assemblies: Basis for a virus-like particle ELISA. J. Med. Virol. 2005, 75, 114-121.
55. Volpers, C.; Sapp, M.; Snijders, P.J.; Walboomers, J.M.; Streeck, R.E. Conformational and linear epitopes on virus-like particles of human papillomavirus type 33 identified by monoclonal antibodies to the minor capsid protein L2. J. Gen. Virol. 1995, 76 (Pt. 11), 2661-2667.
56. Bergsdorf, C.; Beyer, C.; Umansky, V.; Werr, M.; Sapp, M. Highly efficient transport of carboxyfluorescein diacetate succinimidyl ester into COS7 cells using human papillomavirus-like particles. FEBS Lett. 2003, 536, 120-124.
57. Schmidtke, M.; Karger, A.; Meerbach, A.; Egerer, R.; Stelzner, A.; Makarov, V. Binding of a N,N'-bisheteryl derivative of dispirotripiperazine to heparan sulfate residues on the cell surface specifically prevents infection of viruses from different families. Virology 2003, 311, 134-143.
58. Schmidtke, M.; Riabova, O.; Dahse, H.M.; Stelzner, A.; Makarov, V. Synthesis, cytotoxicity and antiviral activity of N,N'-bis-5-nitropyrimidyl derivatives of dispirotripiperazine. Antiviral. Res. 2002, 55, 117-127.
59. Day, P.M.; Thompson, C.D.; Buck, C.B.; Pang, Y.Y.; Lowy, D.R.; Schiller, J.T. Neutralization of human papillomavirus with monoclonal antibodies reveals different mechanisms of inhibition. J. Virol. 2007, 81, 8784-8792.
60. Culp, T.D.; Budgeon, L.R.; Christensen, N.D. Human papillomaviruses bind a basal extracellular matrix component secreted by keratinocytes which is distinct from a membrane-associated receptor. Virology 2006, 347, 147-159.
61. Alexopoulou, A.N.; Multhaupt, H.A.; Couchman, J.R. Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell. Biol. 2007, 39, 505-528.
62. Elenius, K.; Vainio, S.; Laato, M.; Salmivirta, M.; Thesleff, I.; Jalkanen, M. Induced expression of syndecan in healing wounds. J. Cell. Biol. 1991, 114, 585-595.
63. Giannelli, G.; Falk-Marzillier, J.; Schiraldi, O.; Stetler-Stevenson, W.G.; Quaranta, V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997, 277, 225-228.
64. Koshikawa, N.; Giannelli, G.; Cirulli, V.; Miyazaki, K.; Quaranta, V. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J. Cell. Biol. 2000, 148, 615-624.
65. Amano, S.; Scott, I.C.; Takahara, K.; Koch, M.; Champliaud, M.F.; Gerecke, D.R.; Keene, D.R.; Hudson, D.L.; Nishiyama, T.; Lee, S.; et al. Bone morphogenetic protein 1 is an extracellular processing enzyme of the laminin 5 gamma 2 chain. J. Biol. Chem 2000, 275, 22728-22735.
66. Hao, J.L.; Nagano, T.; Nakamura, M.; Kumagai, N.; Mishima, H.; Nishida, T. Effect of galardin on collagen degradation by Pseudomonas aeruginosa. Exp. Eye Res. 1999, 69, 595-601.
67. Deng, Y.; Foley, E.M.; Gonzales, J.C.; Gordts, P.L.; Li, Y.; Esko, J.D. Shedding of syndecan-1 from human hepatocytes alters very low density lipoprotein clearance. Hepatology 2012, 55, 277-286.
68. Endo, K.; Takino, T.; Miyamori, H.; Kinsen, H.; Yoshizaki, T.; Furukawa, M.; Sato, H. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 2003, 278, 40764-40770.
69. Broutian, T.R.; Brendle, S.A.; Christensen, N.D. Differential binding patterns to host cells associated with particles of several human alphapapillomavirus types. J. Gen. Virol. 2010, 91, 531-540.
70. Walboomers, J.M.; Jacobs, M.V.; Manos, M.M.; Bosch, F.X.; Kummer, J.A.; Shah, K.V.; Snijders, P.J.; Peto, J.; Meijer, C.J.; Munoz, N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 1999, 189, 12-19.
71. Arends, M.J.; Buckley, C.H.; Wells, M. Aetiology, pathogenesis, and pathology of cervical neoplasia. J. Clin. Pathol. 1998, 51, 96-103.
72. McCluggage, W.G. New developments in endocervical glandular lesions. Histopathology 2013, 62, 138-160.
73. Castellsague, X.; Diaz, M.; de Sanjose, S.; Munoz, N.; Herrero, R.; Franceschi, S.; Peeling, R.W.; Ashley, R.; Smith, J.S.; Snijders, P.J.; et al. Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: Implications for screening and prevention. J. Natl. Cancer Inst. 2006, 98, 303-315.
74. Munoz, N.; Bosch, F.X.; de Sanjose, S.; Herrero, R.; Castellsague, 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, 518-527.
75. Handisurya, A.; Day, P.M.; Thompson, C.D.; Buck, C.B.; Kwak, K.; Roden, R.B.; Lowy, D.R.; Schiller, J.T. Murine skin and vaginal mucosa are similarly susceptible to infection by pseudovirions of different papillomavirus classifications and species. Virology 2012, 433, 385-394.