Annexin A2 and S100A10 regulate human papillomavirus type 16 entry and intracellular trafficking in human keratinocytes

Journal of Virology

Volumn 87, Issue 13, 2013, Pages 7502-7515

  Dziduszko, Agnieszka ^a   Ozbun, Michelle A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; EPIDERMAL GROWTH FACTOR RECEPTOR; HEPARAN; LIPOCORTIN 2; LIPOCORTIN 2 ANTIBODY; PROTEIN ANTIBODY; PROTEIN S100A10; PROTEIN TYROSINE KINASE; PROTEOGLYCAN; REGULATOR PROTEIN; S100A10 ANTIBODY; UNCLASSIFIED DRUG;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; INTERNALIZATION; INTRACELLULAR TRANSPORT; KERATINOCYTE; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS PARTICLE;

ANNEXIN A2; CELL FRACTIONATION; ENZYME ACTIVATION; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KERATINOCYTES; LUCIFERASES; MICROSCOPY, ELECTRON, TRANSMISSION; PHOSPHORYLATION; PLASMIDS; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; S100 PROTEINS; SRC-FAMILY KINASES; VIRUS INTERNALIZATION;

EID: 84880357118     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00519-13     Document Type: Article

References (94)

1. Stanley M. 2010. Pathology and epidemiology of HPV infection in females. Gynecol. Oncol. 117:S5-S10.
2. Marklund L, Hammarstedt L. 2011. Impact of HPV in oropharyngeal cancer. J. Oncol. 2011:509036. doi:10.1155/2011/509036.
3. Joyce JG, Tung JS, 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.
4. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M. 2001. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75:1565-1570.
5. 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.
6. Cladel NM, Hu J, Balogh K, Mejia A, Christensen ND. 2008. Wounding prior to challenge substantially improves infectivity of cottontail rabbit papillomavirus and allows for standardization of infection. J. Virol. Methods 148:34-39.
7. Rous P, Beard JW. 1934. A virus-induced mammalian growth with the characters of a tumor (the Shope rabbit papilloma). I. The growth on implantation within favorable hosts. J. Exp. Med. 60:701-722.
8. Sapp M, Bienkowska-Haba M. 2009. Viral entry mechanisms: human papillomavirus and a long journey from extracellular matrix to the nucleus. FEBS J. 276:7206-7216.
9. Schiller JT, Day PM, Kines RC. 2010. Current understanding of the mechanism of HPV infection. Gynecol. Oncol. 118:S12-S17.
10. 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.
11. Evander M, Frazer IH, Payne E, Qi YM, Hengst K, McMillan NA. 1997. Identification of the alpha6 integrin as a candidate receptor for papillomaviruses. J. Virol. 71:2449-2456.
12. 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. doi:10.1371/journal.pone.0003313.
13. 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.
14. Sasaki T, Gohring W, Mann K, Brakebusch C, Yamada Y, Fassler R, Timpl R. 2001. Short arm region of laminin-5 gamma2 chain: structure, mechanism of processing and binding to heparin and proteins. J. Mol. Biol. 314:751-763.
15. Wang H, Leavitt L, Ramaswamy R, Rapraeger AC. 2010. Interaction of syndecan and alpha6beta4 integrin cytoplasmic domains: regulation of ErbB2-mediated integrin activation. J. Biol. Chem. 285:13569-13579.
16. Dowling J, Yu QC, Fuchs E. 1996. Beta4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J. Cell Biol. 134: 559-572.
17. Surviladze Z, Dziduszko A, Ozbun MA. 2012. Essential roles for soluble virion-associated heparan sulfonated proteoglycans and growth factors in human papillomavirus infections. PLoS Pathog. 8:e1002519. doi:10.1371 /journal.ppat.1002519.
18. Bishop JR, Schuksz M, Esko JD. 2007. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446:1030-1037.
19. Grove J, Marsh M. 2011. The cell biology of receptor-mediated virus entry. J. Cell Biol. 195:1071-1082.
20. Pelkmans L, Helenius A. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
21. Hindmarsh PL, Laimins LA. 2007. Mechanisms regulating expression of the HPV 31 L1 and L2 capsid proteins and pseudovirion entry. Virol. J. 4:19. doi:10.1186/1743-422X-4-19.
22. 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.
23. Day PM, Lowy DR, Schiller JT. 2003. Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307:1-11.
24. 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.
25. Schelhaas M, Shah B, Holzer M, Blattmann P, Kuhling L, Day PM, Schiller JT, Helenius A. 2012. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog. 8:e1002657. doi:10.1371/journal.ppat.1002657.
26. Gerke V, Moss SE. 2002. Annexins: from structure to function. Physiol. Rev. 82:331-371.
27. Hayes MJ, Rescher U, Gerke V, Moss SE. 2004. Annexin-actin interactions. Traffic 5:571-576.
28. Erikson E, Erikson RL. 1980. Identification of a cellular protein substrate phosphorylated by the avian sarcoma virus-transforming gene product. Cell 21:829-836.
29. Michener ML, Dawson WB, Creutz CE. 1986. Phosphorylation of a chromaffin granule-binding protein in stimulated chromaffin cells. J. Biol. Chem. 261:6548-6555.
30. Bellagamba C, Hubaishy I, Bjorge JD, Fitzpatrick SL, Fujita DJ, Waisman DM. 1997. Tyrosine phosphorylation of annexin II tetramer is stimulated by membrane binding. J. Biol. Chem. 272:3195-3199.
31. Deora AB, Kreitzer G, Jacovina AT, Hajjar KA. 2004. An annexin 2 phosphorylation switch mediates p11-dependent translocation of annexin 2 to the cell surface. J. Biol. Chem. 279:43411-43418.
32. Hubaishy I, Jones PG, Bjorge J, Bellagamba C, Fitzpatrick S, Fujita DJ, Waisman DM. 1995. Modulation of annexin II tetramer by tyrosine phosphorylation. Biochemistry 34:14527-14534.
33. Zheng L, Foley K, Huang L, Leubner A, Mo G, Olino K, Edil BH, Mizuma M, Sharma R, Le DT, Anders RA, Illei PB, Van Eyk JE, Maitra A, Laheru D, Jaffee EM. 2011. Tyrosine 23 phosphorylation-dependent cell-surface localization of annexin A2 is required for invasion and metastases of pancreatic cancer. PLoS One 6:e19390. doi:10.1371/journal.pone.0019390.
34. Morel E, Gruenberg J. 2009. Annexin A2 binding to endosomes and functions in endosomal transport are regulated by tyrosine 23 phosphorylation. J. Biol. Chem. 284:1604-1611.
35. Jost M, Zeuschner D, Seemann J, Weber K, Gerke V. 1997. Identification and characterization of a novel type of annexin-membrane interaction: Ca2Universal-GreekwithMathPi.-1.H1100 is not required for the association of annexin II with early endosomes. J. Cell Sci. 110:221-228.
36. Turpin E, Russo-Marie F, Dubois T, de Paillerets C, Alfsen A, Bomsel M. 1998. In adrenocortical tissue, annexins II and VI are attached to clathrin coated vesicles in a calcium-independent manner. Biochim. Biophys. Acta 1402:115-130.
37. Schnitzer JE, Liu J, Oh P. 1995. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J. Biol. Chem. 270:14399-14404.
38. Merrifield CJ, Rescher U, Almers W, Proust J, Gerke V, Sechi AS, Moss SE. 2001. Annexin 2 has an essential role in actin-based macropinocytic rocketing. Curr. Biol. 11:1136-1141.
39. Futter CE, White IJ. 2007. Annexins and endocytosis. Traffic 8:951-958.
40. Oliferenko S, Paiha K, Harder T, Gerke V, Schwarzler C, Schwarz H, Beug H, Gunthert U, Huber LA. 1999. Analysis of CD44-containing lipid rafts: Recruitment of annexin II and stabilization by the actin cytoskeleton. J. Cell Biol. 146:843-854.
41. Babiychuk EB, Draeger A. 2000. Annexins in cell membrane dynamics. Ca(2Universal-GreekwithMathPi.-1.H11001)-regulated association of lipid microdomains. J. Cell Biol. 150: 1113-1124.
42. Hayes MJ, Merrifield CJ, Shao D, Ayala-Sanmartin J, Schorey CD, Levine TP, Proust J, Curran J, Bailly M, Moss SE. 2004. Annexin 2 binding to phosphatidylinositol 4,5-bisphosphate on endocytic vesicles is regulated by the stress response pathway. J. Biol. Chem. 279:14157-14164.
43. Rescher U, Ruhe D, Ludwig C, Zobiack N, Gerke V. 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.
44. Creutz CE, Snyder SL. 2005. Interactions of annexins with the mu subunits of the clathrin assembly proteins. Biochemistry 44:13795-13806.
45. Grewal T, Enrich C. 2009. Annexins-modulators of EGF receptor signalling and trafficking. Cell. Signal. 21:847-858.
46. Morel E, Gruenberg J. 2007. The p11/S100A10 light chain of annexin A2 is dispensable for annexin A2 association to endosomes and functions in endosomal transport. PLoS One 2:e1118. doi:10.1371/journal.pone.0001118.
47. Madureira PA, O'Connell PA, Surette AP, Miller VA, Waisman DM. 2012. The biochemistry and regulation of S100A10: a multifunctional plasminogen receptor involved in oncogenesis. J. Biomed. Biotechnol. 2012:353687. doi:10.1155/2012/353687.
48. Puisieux A, Ji J, Ozturk M. 1996. Annexin II up-regulates cellular levels of p11 protein by a post-translational mechanisms. Biochem. J. 313:51-55.
49. Gonzalez-Reyes S, Garcia-Manso A, del Barrio G, Dalton KP, Gonzalez-Molleda L, Arrojo-Fernandez J, Nicieza I, Parra F. 2009. Role of annexin A2 in cellular entry of rabbit vesivirus. J. Gen. Virol. 90:2724-2730.
50. Derry MC, Sutherland MR, Restall CM, Waisman DM, Pryzdial EL. 2007. Annexin 2-mediated enhancement of cytomegalovirus infection op- poses inhibition by annexin 1 or annexin 5. J. Gen. Virol. 88:19-27.
51. Pietropaolo R, Compton T. 1999. Interference with annexin II has no effect on entry of human cytomegalovirus into fibroblast cells. J. Gen. Virol. 80:1807-1816.
52. Yang SL, Chou YT, Wu CN, Ho MS. 2011. Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J. Virol. 85: 11809-11820.
53. Ma G, Greenwell-Wild T, Lei K, Jin W, Swisher J, Hardegen N, Wild CT, Wahl SM. 2004. Secretory leukocyte protease inhibitor binds to annexin II, a cofactor for macrophage HIV-1 infection. J. Exp. Med. 200: 1337-1346.
54. Rai T, Mosoian A, Resh MD. 2010. Annexin 2 is not required for human immunodeficiency virus type 1 particle production but plays a cell type- dependent role in regulating infectivity. J. Virol. 84:9783-9792.
55. Ryzhova EV, Vos RM, Albright AV, Harrist AV, Harvey T, Gonzalez-Scarano F. 2006. Annexin 2: a novel human immunodeficiency virus type 1 Gag binding protein involved in replication in monocyte-derived macrophages. J. Virol. 80:2694-2704.
56. Dreier R, Schmid KW, Gerke V, Riehemann K. 1998. Differential expression of annexins I, II and IV in human tissues: an immunohistochemical study. Histochem. Cell Biol. 110:137-148.
57. Munz B, Gerke V, Gillitzer R, Werner S. 1997. Differential expression of the calpactin I subunits annexin II and p11 in cultured keratinocytes and during wound repair. J. Investig. Dermatol. 108:307-312.
58. Patchell BJ, Wojcik KR, Yang TL, White SR, Dorscheid DR. 2007. Glycosylation and annexin II cell surface translocation mediate airway epithelial wound repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 293: L354-L363.
59. Nakayama H, Fukuda S, Inoue H, Nishida-Fukuda H, Shirakata Y, Hashimoto K, Higashiyama S. 2012. Cell surface annexins regulate ADAM-mediated ectodomain shedding of proamphiregulin. Mol. Biol. Cell 23:1964-1975.
60. Woodham AW, Da Silva DM, Skeate JG, Raff AB, Ambroso MR, Brand HE, Isas JM, Langen R, Kast WM. 2012. The S100A10 subunit of the annexin A2 heterotetramer facilitates L2-mediated human papillomavirus infection. PLoS One 7:e43519. doi:10.1371/journal.pone.0043519.
61. Buck CB, Thompson CD, Pang YY, Lowy DR, Schiller JT. 2005. Maturation of papillomavirus capsids. J. Virol. 79:2839-2846.
62. Liu J, Rothermund CA, Ayala-Sanmartin J, Vishwanatha JK. 2003. Nuclear annexin II negatively regulates growth of LNCaP cells and substitution of ser 11 and 25 to glu prevents nucleo-cytoplasmic shuttling of annexin II. BMC Biochem. 4:10. doi:10.1186/1471-2091-4-10.
63. Buck CB, Pastrana DV, Lowy DR, Schiller JT. 2004. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78:751-757.
64. Ozbun MA. 2002. Human papillomavirus type 31b infection of human keratinocytes and the onset of early transcription. J. Virol. 76:11291-11300.
65. Ibragimova I, Ibanez de Caceres I, Hoffman AM, Potapova A, Dulaimi E, Al-Saleem T, Hudes GR, Ochs MF, Cairns P. 2010. Global reactivation of epigenetically silenced genes in prostate cancer. Cancer Prev. Res. (Phila) 3:1084-1092.
66. Liu JW, Shen JJ, Tanzillo-Swarts A, Bhatia B, Maldonado CM, Person MD, Lau SS, Tang DG. 2003. Annexin II expression is reduced or lost in prostate cancer cells and its re-expression inhibits prostate cancer cell migration. Oncogene 22:1475-1485.
67. Xie BX, Zhang H, Yu L, Wang J, Pang B, Wu RQ, Qian XL, Li SH, Shi QG, Wang LL, Zhou JG. 2010. The radiation response of androgenrefractory prostate cancer cell line C4-2 derived from androgen-sensitive cell line LNCaP. Asian J. Androl. 12:405-414.
68. Pyeon D, Lambert PF, Ahlquist P. 2005. Production of infectious human papillomavirus independently of viral replication and epithelial cell differentiation. Proc. Natl. Acad. Sci. U.S.A. 102:9311-9316.
69. Surviladze Z, Sterk RT, Deharo SA, Ozbun MA. 2013. Cellular entry of human papillomavirus type 16 involves activation of the phosphatidylinositol 3-kinase/Akt/mTOR pathway and inhibition of autophagy. J. Virol. 87:2508-2517.
70. Fried J, Perez AG, Clarkson BD. 1976. Flow cytofluorometric analysis of cell cycle distributions using propidium iodide. Properties of the method and mathematical analysis of the data. J. Cell Biol. 71:172-181.
71. Osherov N, Levitzki A. 1994. Epidermal-growth-factor-dependent activation of the src-family kinases. Eur. J. Biochem. 225:1047-1053.
72. Wilde A, Beattie EC, Lem L, Riethof DA, Liu SH, Mobley WC, Soriano P, Brodsky FM. 1999. EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell 96:677-687.
73. Pyeon D, Pearce SM, Lank SM, Ahlquist P, Lambert PF. 2009. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog. 5:e1000318. doi:10.1371/journal.ppat.1000318.
74. Shao C, Zhang F, Kemp MM, Linhardt RJ, Waisman DM, Head JF, Seaton BA. 2006. Crystallographic analysis of calcium-dependent heparin binding to annexin A2. J. Biol. Chem. 281:31689-31695.
75. Liu L, Tao JQ, Zimmerman UJ. 1997. Annexin II binds to the membrane of A549 cells in a calcium-dependent and calcium-independent manner. Cell. Signal. 9:299-304.
76. Falcone DJ, Borth W, Khan KM, Hajjar KA. 2001. Plasminogenmediated matrix invasion and degradation by macrophages is dependent on surface expression of annexin II. Blood 97:777-784.
77. Gniadecki R, Gajkowska B. 2003. Intracellular calcium pool emptying induces DNA synthesis in HaCaT keratinocytes. Exp. Dermatol. 12:453-459.
78. Chiang Y, Schneiderman MH, Vishwanatha JK. 1993. Annexin II expression is regulated during mammalian cell cycle. Cancer Res. 53:6017-6021.
79. Harder T, Gerke V. 1993. The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex. J. Cell Biol. 123:1119-1132.
80. Kassam G, Manro A, Braat CE, Louie P, Fitzpatrick SL, Waisman DM. 1997. Characterization of the heparin binding properties of annexin II tetramer. J. Biol. Chem. 272:15093-15100.
81. Greber UF. 2002. Signalling in viral entry. Cell. Mol. Life Sci. 59:608-626. 82. Grieve AG, Moss SE, Hayes MJ. 2012. Annexin A2 at the interface of actin and membrane dynamics: a focus on its roles in endocytosis and cell polarization. Int. J. Cell Biol. 2012:852430. doi:10.1155/2012/852430.
82. Grieve AG, Moss SE, Hayes MJ. 2012. Annexin A2 at the interface of actin and membrane dynamics: a focus on its roles in endocytosis and cell polarization. Int. J. Cell Biol. 2012:852430. doi:10.1155/2012/852430.
83. Fang YT, Lin CF, Wang CY, Anderson R, Lin YS. 2012. Interferongamma stimulates p11-dependent surface expression of annexin A2 in lung epithelial cells to enhance phagocytosis. J. Cell. Physiol. 227:2775-2787.
84. Zeuschner D, Stoorvogel W, Gerke V. 2001. Association of annexin 2 with recycling endosomes requires either calcium- or cholesterolstabilized membrane domains. Eur. J. Cell Biol. 80:499-507.
85. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP. 2009. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 5:e1000394. doi:10.1371/journal.ppat.1000394.
86. Kines RC, Thompson CD, Lowy DR, Schiller JT, Day PM. 2009. The initial steps leading to papillomavirus infection occur on the basement membrane prior to cell surface binding. Proc. Natl. Acad. Sci. U.S.A. 106:20458-20463.
87. Choi Y, Chung H, Jung H, Couchman JR, Oh ES. 2011. Syndecans as cell surface receptors: unique structure equates with functional diversity. Matrix Biol. 30:93-99.
88. Liu J, Thorp SC. 2002. Cell surface heparan sulfate and its roles in assisting viral infections. Med. Res. Rev. 22:1-25.
89. Wang X, Huong SM, Chiu ML, Raab-Traub N, Huang ES. 2003. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 424:456-461.
90. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S, Royer C, Fischer B, Zahid MN, Lavillette D, Fresquet J, Cosset FL, Rothenberg SM, Pietschmann T, Patel AH, Pessaux P, Doffoel M, Raffelsberger W, Poch O, McKeating JA, Brino L, Baumert TF. 2011. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat. Med. 17:589-595.
91. Nakano K, Kobayashi M, Nakamura K, Nakanishi T, Asano R, Kumagai I, Tahara H, Kuwano M, Cohen JB, Glorioso JC. 2011. Mechanism of HSV infection through soluble adapter-mediated virus bridging to the EGF receptor. Virology 413:12-18.
92. Kim JH, Jiang S, Elwell CA, Engel JN. 2011. Chlamydia trachomatis co-opts the FGF2 signaling pathway to enhance infection. PLoS Pathog. 7:e1002285. doi:10.1371/journal.ppat.1002285.
93. Nakano K, Asano R, Tsumoto K, Kwon H, Goins WF, Kumagai I, Cohen JB, Glorioso JC. 2005. Herpes simplex virus targeting to the EGF receptor by a gD-specific soluble bridging molecule. Mol. Ther. 11:617-626.
94. Harder T, Kellner R, Parton RG, Gruenberg J. 1997. Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8:533-545.