Caveolin-1-dependent infectious entry of human papillomavirus type 31 in human keratinocytes proceeds to the endosomal pathway for pH-dependent uncoating

Journal of Virology

Volumn 82, Issue 19, 2008, Pages 9505-9512

  Smith, Jessica L ^a   Campos, Samuel K ^a   Wandinger Ness, Angela ^a   Ozbun, Michelle A ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; DEOXYRIBONUCLEASE; GUANOSINE TRIPHOSPHATASE;

ARTICLE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 31; KERATINOCYTE; LYSOSOME; MEMBRANE BINDING; NONHUMAN; PAPILLOMA VIRUS; PH; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME; VIRUS INFECTION;

CAVEOLIN 1; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; GENOME; GENOME, VIRAL; HUMANS; HYDROGEN-ION CONCENTRATION; KERATINOCYTES; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS;

DNA VIRUSES; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 31; MIRIDAE; PAPILLOMAVIRIDAE;

EID: 52649120857     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01014-08     Document Type: Article

References (41)

1. Barr, E., C. K. Gause, O. M. Bautista, R. A. Railkar, L. C. Lupinacci, R. P. Insinga, H. L. Sings, and R. M. Haupt. 2008. Impact of a prophylactic quadrivalent human papillomavirus (types 6, 11, 16, 18) L1 virus-like particle vaccine in a sexually active population of North American women. Am. J. Obstet. Gynecol. 198:261.e1-261.e11.
2. Bosch, F. X., X. Castellsagué, and S. de Sanjosé. 2008. HPV and cervical cancer: screening or vaccination? Br. J. Cancer 98:15-21.
3. Bosch, F. X., M. M. Manos, N. Muñoz, M. Sherman, A. M. Jansen, J. Peto, M. H. Schiffman, V. Moreno, R. Kurman, K. V. Shah, and I. S. Group. 1995. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. J. Natl. Cancer Inst. 87:796-802.
4. Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106:761-771.
5. Buck, C. B., C. D. Thompson, Y.-Y. S. Pang, D. R. Lowy, and J. T. Schiller. 2005. Maturation of papillomavirus capsids. J. Virol. 79:2839-2846.
6. Chandran, K., D. L. Farsetta, and M. L. Nibert. 2002. Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein μ1 mediates membrane disruption. J. Virol. 76:9920-9933.
7. Chen, W., Y. Feng, D. Chen, and A. Wandinger-Ness. 1998. Rab11 is required for trans-Golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol. Biol. Cell 9:3241-3257.
8. Chen, W., and A. Wandinger-Ness. 2001. Expression and functional analyses of Rab8 and Rab11a in exocytic transport from trans-Golgi network. Methods Enzymol. 329:165-175.
9. Colicelli, J. 2004. Human RAS superfamily proteins and related GTPases. Sci. STKE. 2004:re13.
10. Day, P. M., D. R. Lowy, and J. T. Schiller. 2003. Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307:1-11.
11. de Sanjosé, S., M. Diaz, X. Castellsagué, G. Clifford, L. Bruni, N. Muñoz, and F. X. Bosch. 2007. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect. Dis. 7:453-459.
12. Doms, R. W., and A. Helenius. 1986. Quaternary structure of influenza virus hemagglutinin after acid treatment. J. Virol. 60:833-839.
13. Feng, Y., B. Press, W. Chen, J. Zimmerman, and A. Wandinger-Ness. 2001. Expression and properties of Rab7 in endosome function. Methods Enzymol. 329:175-187.
14. Gillison, M. L., W. M. Koch, R. B. Capone, M. Spafford, W. H. Westra, L. Wu, M. L. Zahurak, R. W. Daniel, M. Viglione, D. E. Symer, K. V. Shah, and D. Sidransky. 2000. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J. Natl. Cancer Inst. 92:709-720.
15. Gruenberg, J., and F. G. van der Goot. 2006. Mechanisms of pathogen entry through the endosomal compartments. Nat. Rev. Mol. Cell. Biol. 7:495-504.
16. Kämper, N., P. M. Day, T. Nowak, H.-C. Selinka, L. Florin, J. Bolscher, L. Hilbig, J. T. Schiller, and M. Sapp. 2006. A membrane-destabilizing peptide in capsid protein L2 is required for egress of papillomavirus genomes from endosomes. J. Virol. 80:759-768.
17. Laniosz, V., K. A. Holthusen, and P. I. Meneses. 2008. Bovine papillomavirus type 1: from clathrin to caveolin. J. Virol. 82:6288-6298.
18. Li, M., P. Beard, P. A. Estes, M. K. Lyon, and R. L. Garcea. 1998. Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J. Virol. 72:2160-2167.
19. Ozbun, M. A. 2002. Human papillomavirus type 31b infection of human keratinocytes and the onset of early transcription. J. Virol. 76:11291-11300.
20. Ozbun, M. A. 2002. Infectious human papillomavirus type 31b: purification and infection of an immortalized human keratinocyte cell line. J. Gen. Virol. 83:2753-2763.
21. Patterson, N. A., J. L. Smith, and M. A. Ozbun. 2005. Human papillomavirus type 31b infection of human keratinocytes does not require heparan sulfate. J. Virol. 79:6838-6847.
22. Pelkmans, L., T. Bürli, M. Zerial, and A. Helenius. 2004. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118:767-780.
23. Pelkmans, L., and A. Helenius. 2002. Endocytosis via caveolae. Traffic 3:311-320.
24. Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
25. Pyeon, D., P. F. Lambert, and P. Ahlquist. 2005. Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation. Proc. Natl. Acad. Sci. USA 102:9311- 9316.
26. Querbes, W., B. A. O'Hara, G. Williams, and W. J. Atwood. 2006. Invasion of host cells by JC virus identifies a novel role for caveolae in endosomal sorting of noncaveolar ligands. J. Virol. 80:9402-9413.
27. Roberts, R. L., M. A. Barbieri, K. M. Pryse, M. Chua, J. H. Morisaki, and P. D. Stahl. 1999. Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112:3667-3675.
28. Roberts, R. L., M. A. Barbieri, J. Ullrich, and P. D. Stahl. 2000. Dynamics of rab5 activation in endocytosis and phagocytosis. J. Leukoc. Biol. 68:627-632.
29. Schelhaas, M., J. Malmström, L. Pelkmans, J. Haugstetter, L. Ellgaard, K. Grünewald, and A. Helenius. 2007. Simian virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131:516-529.
30. Schwartz, S. L., C. Cao, O. Pylypenko, A. Rak, and A. Wandinger-Ness. 2007. Rab GTPases at a glance. J. Cell Sci. 120:3905-3910.
31. Selinka, H.-C., T. Giroglou, and M. Sapp. 2002. Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299:279-287.
32. Sieczkarski, S. B., and G. R. Whittaker. 2005. Viral entry. Curr. Top. Microbiol. Immunol. 285:1-23.
33. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1:31-39.
34. Smith, J. L., S. K. Campos, and M. A. Ozbun. 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.
35. Stegmann, T., H. W. M. Morselt, J. Scholma, and J. Wilschut. 1987. Fusion of influenza virus in an intracellular acidic compartment measured by fluorescence dequenching. BBA Biomembr. 904:165-170.
36. Sturgis, E. M., and P. M. Cinciripini. 2007. Trends in head and neck cancer incidence in relation to smoking prevalence. Cancer 110:1429-1435.
37. Tsai, B. 2007. Penetration of nonenveloped viruses into the cytoplasm. Annu. Rev. Cell Dev. Biol. 23:23-43.
38. van der Bliek, A. M. 2005. A sixth sense for Rab5. Nat. Cell Biol. 7:548-550.
39. Wang, X., R. Kumar, J. Navarre, J. E. Casanova, and J. R. Goldenring. 2000. Regulation of vesicle trafficking in Madin-Darby canine kidney cells by Rab11a and Rab25. J. Biol. Chem. 275:29138-29146.
40. Wiethoff, C. M., H. Wodrich, L. Gerace, and G. R. Nemerow. 2005. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 79:1992-2000.
41. Zerial, M., and H. McBride. 2001. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2:107-117.