Inhibition of langerhans cell maturation by human papillomavirus type 16: A novel role for the annexin A2 heterotetramer in immune suppression

Journal of Immunology

Volumn 192, Issue 10, 2014, Pages 4748-4757

  Woodham, Andrew W ^a   Raff, Adam B ^a   Raff, Laura M ^a   Da Silva, Diane M ^a,b   Yan, Lisa ^a   Skeate, Joseph G ^a   Wong, Michael K ^a   Lin, Yvonne G ^a,b   Kast, W Martin ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD86 ANTIGEN; LIPOCORTIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; SMALL INTERFERING RNA;

ANTIGEN EXPRESSION; ARTICLE; BINDING AFFINITY; CELL MATURATION; CELLULAR IMMUNITY; CLINICAL TRIAL; CYTOKINE RELEASE; DOWN REGULATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOMODULATION; INTERNALIZATION; LANGERHANS CELL; MACROPHAGE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS MUTATION;

ANNEXIN A2; ANTIGENS, CD86; CAPSID PROTEINS; CYTOKINES; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNE TOLERANCE; LANGERHANS CELLS; MALE; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PEPTIDES; VIRUS INTERNALIZATION;

EID: 84901271916     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303190     Document Type: Article

References (84)

1. Arbyn, M., X. Castellsagué, S. de Sanjosé, L. Bruni, M. Saraiya, F. Bray, and J. Ferlay. 2011. Worldwide burden of cervical cancer in 2008. Ann. Oncol. 22: 2675-2686.
2. Haedicke, J., and T. Iftner. 2013. Human papillomaviruses and cancer. Radiother. Oncol. 108: 397-402.
3. Muñoz, N., F. X. Bosch, S. de Sanjosé, R. Herrero, X. Castellsagué, K. V. Shah, P. J. F. Snijders, and C. J. L. M. Meijer; International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. 2003. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348: 518-527.
4. Walboomers, J. M. M., M. V. Jacobs, M. M. Manos, F. X. Bosch, J. A. Kummer, K. V. Shah, P. J. F. Snijders, J. Peto, C. J. L. M. Meijer, and N. Muñoz. 1999. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189: 12-19.
5. zur Hausen, H. 1991. Human papillomaviruses in the pathogenesis of anogenital cancer. Virology 184: 9-13.
6. Bosch, F. X., M. M. Manos, N. Muñoz, M. Sherman, A. M. Jansen, J. Peto, M. H. Schiffman, V. Moreno, R. Kurman, and K. V. Shah; International Biological Study on Cervical Cancer (IBSCC) Study Group. 1995. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. J. Natl. Cancer Inst. 87: 796-802.
7. Stanley, M. A. P., M. R. Pett, and N. Coleman. 2007. HPV: from infection to cancer. Biochem. Soc. Trans. 35: 1456-1460.
8. Merad, M., F. Ginhoux, and M. Collin. 2008. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8: 935-947.
9. Modis, Y., B. L. Trus, and S. C. Harrison. 2002. Atomic model of the papillomavirus capsid. EMBO J. 21: 4754-4762.
10. Cumming, S. A., T. Cheun-Im, S. G. Milligan, and S. V. Graham. 2008. Human papillomavirus type 16 late gene expression is regulated by cellular RNA processing factors in response to epithelial differentiation. Biochem. Soc. Trans. 36: 522-524.
11. Parkin, D. M. 2006. The global health burden of infection-associated cancers in the year 2002. Int. J. Cancer 118: 3030-3044.
12. Kirnbauer, R., F. Booy, N. Cheng, D. R. Lowy, and J. T. Schiller. 1992. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl. Acad. Sci. USA 89: 12180-12184.
13. Buck, C. B., P. M. Day, and B. L. Trus. 2013. The papillomavirus major capsid protein L1. Virology 445: 169-174.
14. Buck, C. B., N. Cheng, C. D. Thompson, D. R. Lowy, A. C. Steven, J. T. Schiller, and B. L. Trus. 2008. Arrangement of L2 within the papillomavirus capsid. J. Virol. 82: 5190-5197.
15. Zhou, J. S., X. Y. Sun, K. Louis, and I. H. Frazer. 1994. Interaction of human papillomavirus (HPV) type 16 capsid proteins with HPV DNA requires an intact L2 N-terminal sequence. J. Virol. 68: 619-625.
16. Zhao, K. N., X. Y. Sun, I. H. Frazer, and J. Zhou. 1998. DNA packaging by L1 and L2 capsid proteins of bovine papillomavirus type 1. Virology 243: 482-491.
17. Giroglou, T., L. Florin, F. Schäfer, R. E. Streeck, and M. Sapp. 2001. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75: 1565-1570.
18. Evander, M. F., I. H. Frazer, E. Payne, Y. M. Qi, K. Hengst, and N. A. McMillan. 1997. Identification of the alpha6 integrin as a candidate receptor for papillomaviruses. J. Virol. 71: 2449-2456.
19. Bienkowska-Haba, M. P., H. D. Patel, and M. Sapp. 2009. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog. 5: e1000524.
20. Surviladze, Z., A. Dziduszko, and M. A. Ozbun. 2012. Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections. PLoS Pathog. 8: e1002519.
21. Spoden, G. F., K. Freitag, M. Husmann, K. Boller, M. Sapp, C. Lambert, and L. Florin. 2008. Clathrin- and caveolin-independent entry of human papillomavirus type 16: involvement of tetraspanin-enriched microdomains (TEMs). PLoS ONE 3: e3313.
22. Schelhaas, M., B. Shah, M. Holzer, P. Blattmann, L. Kuhling, P. M. Day, J. T. Schiller, and A. Helenius. 2012. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog. 8: e1002657.
23. Fausch, S. C., D. M. Da Silva, and W. M. Kast. 2003. Differential uptake and cross-presentation of human papillomavirus virus-like particles by dendritic cells and Langerhans cells. Cancer Res. 63: 3478-3482.
24. Wang, J. W., and R. B. Roden. 2013. L2, the minor capsid protein of papillomavirus. Virology 445: 175-186.
25. Kämper, N. D., 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.
26. Bronnimann, M. P., J. A. Chapman, C. K. Park, and S. K. Campos. 2013. A transmembrane domain and GxxxG motifs within L2 are essential for papillomavirus infection. J. Virol. 87: 464-473.
27. Bergant Marusic, M., M. A. Ozbun, S. K. Campos, M. P. Myers, and L. Banks. 2012. Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17. Traffic 13: 455-467.
28. Day, P. M., and J. T. Schiller. 2009. The role of furin in papillomavirus infection. Future Microbiol. 4: 1255-1262.
29. Yang, R., W. H. Yutzy, IV, R. P. Viscidi, and R. B. Roden. 2003. Interaction of L2 with b-actin directs intracellular transport of papillomavirus and infection. J. Biol. Chem. 278: 12546-12553.
30. Day, P. M., C. C. Baker, D. R. Lowy, and J. T. Schiller. 2004. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc. Natl. Acad. Sci. USA 101: 14252-14257.
31. Yang, R., P. M. Day, W. H. Yutzy, IV, K. Y. Lin, C. F. Hung, and R. B. Roden. 2003. Cell surface-binding motifs of L2 that facilitate papillomavirus infection. J. Virol. 77: 3531-3541.
32. Kawana, K., H. Yoshikawa, Y. Taketani, K. Yoshiike, and T. Kanda. 1999. Common neutralization epitope in minor capsid protein L2 of human papillomavirus types 16 and 6. J. Virol. 73: 6188-6190.
33. Gambhira, R., B. Karanam, S. Jagu, J. N. Roberts, C. B. Buck, I. Bossis, H. Alphs, T. Culp, N. D. Christensen, and R. B. Roden. 2007. A protective and broadly crossneutralizing epitope of human papillomavirus L2. J. Virol. 81: 13927-13931.
34. Slupetzky, K., R. Gambhira, T. D. Culp, S. Shafti-Keramat, C. Schellenbacher, N. D. Christensen, R. B. Roden, and R. Kirnbauer. 2007. A papillomavirus-like particle (VLP) vaccine displaying HPV16 L2 epitopes induces cross-neutralizing antibodies to HPV11. Vaccine 25: 2001-2010.
35. Kondo, K., Y. Ishii, H. Ochi, T. Matsumoto, H. Yoshikawa, and T. Kanda. 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.
36. Conway, M. J., L. Cruz, S. Alam, N. D. Christensen, and C. Meyers. 2011. Cross-neutralization potential of native human papillomavirus N-terminal L2 epitopes. PLoS ONE 6: e16405.
37. Kawana, Y., K. Kawana, H. Yoshikawa, Y. Taketani, K. Yoshiike, and T. Kanda. 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.
38. Woodham, A. W., 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. 2012. The S100A10 subunit of the annexin A2 heterotetramer facilitates L2-mediated human papillomavirus infection. PLoS ONE 7: e43519.
39. Dziduszko, A., and M. A. Ozbun. 2013. Annexin A2 and S100A10 regulate human papillomavirus type 16 entry and intracellular trafficking in human keratinocytes. J. Virol. 87: 7502-7515.
40. Fahey, L. M., A. B. Raff, D. M. Da Silva, and W. M. Kast. 2009. A major role for the minor capsid protein of human papillomavirus type 16 in immune escape. J. Immunol. 183: 6151-6156.
41. Yan, M., J. Peng, I. A. Jabbar, X. Liu, L. Filgueira, I. H. Frazer, and R. Thomas. 2004. Despite differences between dendritic cells and Langerhans cells in the mechanism of papillomavirus-like particle antigen uptake, both cells cross-prime T cells. Virology 324: 297-310.
42. Bousarghin, L., P. Hubert, E. Franzen, N. Jacobs, J. Boniver, and P. Delvenne. 2005. Human papillomavirus 16 virus-like particles use heparan sulfates to bind dendritic cells and colocalize with langerin in Langerhans cells. J. Gen. Virol. 86: 1297-1305.
43. Waisman, D. M. 1995. Annexin II tetramer: structure and function. Mol. Cell. Biochem. 149-150: 301-322.
44. Gerke, V., C. E. Creutz, and S. E. Moss. 2005. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6: 449-461.
45. Deora, A. B., G. Kreitzer, A. T. Jacovina, and K. A. Hajjar. 2004. An annexin 2 phosphorylation switch mediates p11-dependent translocation of annexin 2 to the cell surface. J. Biol. Chem. 279: 43411-43418.
46. Rescher, U., and V. Gerke. 2008. S100A10/p11: family, friends and functions. Pflugers Arch. 455: 575-582.
47. Rust, R., J. Kluiver, L. Visser, G. Harms, T. Blokzijl, W. Kamps, S. Poppema, and A. van den Berg. 2006. Gene expression analysis of dendritic/Langerhans cells and Langerhans cell histiocytosis. J. Pathol. 209: 474-483.
48. Fausch, S. C., D. M. Da Silva, M. P. Rudolf, and W. M. Kast. 2002. Human papillomavirus virus-like particles do not activate Langerhans cells: a possible immune escape mechanism used by human papillomaviruses. J. Immunol. 169: 3242-3249.
49. Fahey, L. M., A. B. Raff, D. M. Da Silva, and W. M. Kast. 2009. Reversal of human papillomavirus-specific T cell immune suppression through TLR agonist treatment of Langerhans cells exposed to human papillomavirus type 16. J. Immunol. 182: 2919-2928.
50. Dasgupta, J., M. Bienkowska-Haba, M. E. Ortega, H. D. Patel, S. Bodevin, D. Spillmann, B. Bishop, M. Sapp, and X. S. Chen. 2011. Structural basis of oligosaccharide receptor recognition by human papillomavirus. J. Biol. Chem. 286: 2617-2624.
51. Buck, C. B., and C. D. Thompson. 2007. Production of papillomavirus-based gene transfer vectors. Curr. Protoc. Cell Biol. Chapter 26: Unit 26.1.
52. Puisieux, A., J. Ji, and M. Ozturk. 1996. Annexin II up-regulates cellular levels of p11 protein by a post-translational mechanisms. Biochem. J. 313: 51-55.
53. He, K. L., A. B. Deora, H. Xiong, Q. Ling, B. B. Weksler, R. Niesvizky, and K. A. Hajjar. 2008. Endothelial cell annexin A2 regulates polyubiquitination and degradation of its binding partner S100A10/p11. J. Biol. Chem. 283: 19192-19200.
54. Renn, C. N., D. J. Sanchez, M. T. Ochoa, A. J. Legaspi, C. K. Oh, P. T. Liu, S. R. Krutzik, P. A. Sieling, G. Cheng, and R. L. Modlin. 2006. TLR activation of Langerhans cell-like dendritic cells triggers an antiviral immune response. J. Immunol. 177: 298-305.
55. Reddy, T. R., C. Li, P. M. Fischer, and L. V. Dekker. 2012. Three-dimensional pharmacophore design and biochemical screening identifies substituted 1,2,4- triazoles as inhibitors of the annexin A2-S100A10 protein interaction. Chem- MedChem 7: 1435-1446.
56. Ma, G., T. Greenwell-Wild, K. Lei, W. Jin, J. Swisher, N. Hardegen, C. T. Wild, and S. M. Wahl. 2004. Secretory leukocyte protease inhibitor binds to annexin II, a cofactor for macrophage HIV-1 infection. J. Exp. Med. 200: 1337-1346.
57. Kawamura, T., S. E. Kurtz, A. Blauvelt, and S. Shimada. 2005. The role of Langerhans cells in the sexual transmission of HIV. J. Dermatol. Sci. 40: 147-155.
58. de Jong, M. A., and T. B. Geijtenbeek. 2009. Human immunodeficiency virus-1 acquisition in genital mucosa: Langerhans cells as key-players. J. Intern. Med. 265: 18-28.
59. Drobni, P., N. Mistry, N. McMillan, and M. Evander. 2003. Carboxy-fluorescein diacetate, succinimidyl ester labeled papillomavirus virus-like particles fluoresce after internalization and interact with heparan sulfate for binding and entry. Virology 310: 163-172.
60. Swisher, J. F., N. Burton, S. M. Bacot, S. N. Vogel, and G. M. Feldman. 2010. Annexin A2 tetramer activates human and murine macrophages through TLR4. Blood 115: 549-558.
61. Stanley, M. A. 2012. Epithelial cell responses to infection with human papillomavirus. Clin. Microbiol. Rev. 25: 215-222.
62. Lenz, P., D. R. Lowy, and J. T. Schiller. 2005. Papillomavirus virus-like particles induce cytokines characteristic of innate immune responses in plasmacytoid dendritic cells. Eur. J. Immunol. 35: 1548-1556.
63. Lenz, P., P. M. Day, Y. Y. Pang, S. A. Frye, P. N. Jensen, D. R. Lowy, and J. T. Schiller. 2001. Papillomavirus-like particles induce acute activation of dendritic cells. J. Immunol. 166: 5346-5355.
64. Rudolf, M. P., S. C. Fausch, D. M. Da Silva, and W. M. Kast. 2001. Human dendritic cells are activated by chimeric human papillomavirus type-16 viruslike particles and induce epitope-specific human T cell responses in vitro. J. Immunol. 166: 5917-5924.
65. Da Silva, D. M., S. C. Fausch, J. S. Verbeek, and W. M. Kast. 2007. Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fcg receptors and contributes to acquisition of T cell immunity. J. Immunol. 178: 7587-7597.
66. Renoux, V. M., B. Bisig, I. Langers, E. Dortu, B. Clémenceau, M. Thiry, C. Deroanne, A. Colige, J. Boniver, P. Delvenne, and N. Jacobs. 2011. Human papillomavirus entry into NK cells requires CD16 expression and triggers cytotoxic activity and cytokine secretion. Eur. J. Immunol. 41: 3240-3252.
67. Raff, A. B., A. W. Woodham, L. M. Raff, J. G. Skeate, L. Yan, D. M. Da Silva, M. Schelhaas, and W. M. Kast. 2013. The evolving field of human papillomavirus receptor research: a review of binding and entry. J. Virol. 87: 6062-6072.
68. Mitra, S. K. S., and D. D. Schlaepfer. 2006. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18: 516-523.
69. Abban, C. Y., and P. I. Meneses. 2010. Usage of heparan sulfate, integrins, and FAK in HPV16 infection. Virology 403: 1-16.
70. Ling, K. D., R. L. Doughman, A. J. Firestone, M.W. Bunce, and R. A. Anderson. 2002. Type Ig phosphatidylinositol phosphate kinase targets and regulates focal adhesions. Nature 420: 89-93.
71. Di Paolo, G., L. Pellegrini, K. Letinic, G. Cestra, R. Zoncu, S. Voronov, S. Chang, J. Guo, M. R. Wenk, and P. De Camilli. 2002. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1g by the FERM domain of talin. Nature 420: 85-89.
72. van den Bout, I., and N. Divecha. 2009. PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J. Cell Sci. 122: 3837-3850.
73. Rescher, U. R., D. Ruhe, C. Ludwig, N. Zobiack, and V. Gerke. 2004. Annexin 2 is a phosphatidylinositol (4,5)-bisphosphate binding protein recruited to actin assembly sites at cellular membranes. J. Cell Sci. 117: 3473-3480.
74. Hayes, M. J., D. M. Shao, A. Grieve, T. Levine, M. Bailly, and S. E. Moss. 2009. Annexin A2 at the interface between F-actin and membranes enriched in phosphatidylinositol 4,5,-bisphosphate. Biochim. Biophys. Acta 1793: 1086-1095.
75. Schlaepfer, D. D., S. K. Miltra, and D. Ilic. 2004. Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim. Biophys. Acta 1692: 77-102.
76. Becker, T., K. Weber, and N. Johnsson. 1990. Protein-protein recognition via short amphiphilic helices; a mutational analysis of the binding site of annexin II for p11. EMBO J. 9: 4207-4213.
77. Réty, S., J. Sopkova, M. Renouard, D. Osterloh, V. Gerke, S. Tabaries, F. Russo- Marie, and A. Lewit-Bentley. 1999. The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nat. Struct. Biol. 6: 89-95.
78. Miyagi, J., T. Kinjo, K. Tsuhako, M. Higa, T. Iwamasa, Y. Kamada, and T. Hirayasu. 2001. Extremely high Langerhans cell infiltration contributes to the favourable prognosis of HPV-infected squamous cell carcinoma and adenocarcinoma of the lung. Histopathology 38: 355-367.
79. Muderspach, L., S. Wilczynski, L. Roman, L. Bade, J. Felix, L. A. Small, W. M. Kast, G. Fascio, V. Marty, and J. Weber. 2000. A phase I trial of a human papillomavirus (HPV) peptide vaccine for women with high-grade cervical and vulvar intraepithelial neoplasia who are HPV 16 positive. Clin. Cancer Res. 6: 3406-3416.
80. Wright, J. F., A. Kurosky, and S. Wasi. 1994. An endothelial cell-surface form of annexin II binds human cytomegalovirus. Biochem. Biophys. Res. Commun. 198: 983-989.
81. Malhotra, R., M. Ward, H. Bright, R. Priest, M. R. Foster, M. Hurle, E. Blair, and M. Bird. 2003. Isolation and characterisation of potential respiratory syncytial virus receptor(s) on epithelial cells. Microbes Infect. 5: 123-133.
82. Yang, S. L., Y. T. Chou, C. N. Wu, and M. S. Ho. 2011. Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J. Virol. 85: 11809-11820.
83. Buchbinder, S. P. 2011. HIV epidemiology and breakthroughs in prevention 30 years into the AIDS epidemic. Top. Antivir. Med. 19: 38-46.
84. Da Silva, D. M., C. A. Movius, A. B. Raff, H. E. Brand, J. G. Skeate, M. K. Wong, and W. M. Kast. 2014. Suppression of Langerhans cell activation is conserved amongst human papillomavirus a and b genotypes, but not a m genotype. Virology 452-453: 279-286.