Inhibition by cellular vacuolar atpase impairs human papillomavirus uncoating and infection

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 5, 2014, Pages 2905-2911

  MÜller, Konstantin H ^a   Spoden, Gilles A ^b   Scheffer, Konstanze D ^b   Brunnhöfer, Regina ^a   De Brabander, Jef K ^c,d   Maier, Martin E ^e   Florin, Luise ^b   Muller, Claude P ^a  

^a LABORATOIRE NATIONAL DE SANTÉ   (Luxembourg)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE INHIBITOR; ANTIVIRUS AGENT; ENZYME INHIBITOR; SALIPHENYLHALAMIDE; UNCLASSIFIED DRUG; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; VIRUS PROTEIN;

ACIDIFICATION; ARTICLE; CELL LINE; CELL VACUOLE; CELL VIABILITY; DRUG POTENCY; ENDOCYTOSIS; ENDOSOME; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; VIRUS INFECTION; WART VIRUS; ALPHAPAPILLOMAVIRUS; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DRUG EFFECTS; HELA CELL LINE; PATHOGENICITY;

ALPHAPAPILLOMAVIRUS; ANTIVIRAL AGENTS; CELL LINE; CELL SURVIVAL; ENDOCYTOSIS; HELA CELLS; HUMANS; VACUOLAR PROTON-TRANSLOCATING ATPASES; VIRAL PROTEINS;

EID: 84895173608     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02284-13     Document Type: Article

References (44)

1. Arbyn M, Castellsague X, de Sanjose S, Bruni L, Saraiya M, Bray F, Ferlay J. 2011. Worldwide burden of cervical cancer in 2008. Ann. Oncol. 22:2675-2686. http://dx.doi.org/10.1093/annonc/mdr015.
2. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, WHO International Agency for Research on Cancer. 2005. Carcinogenicity of human papillomaviruses. Lancet Oncol. 6:204. http://dx.doi.org/10.1016/S1470-2045(05) 70086-3.
3. zur Hausen H. 2009. Papillomaviruses in the causation of human cancers-A brief historical account. Virology 384:260-265. http://dx.doi.org/10.1016/j. virol.2008.11.046.
4. Greer CE, Wheeler CM, Ladner MB, Beutner K, Coyne MY, Liang H, Langenberg A, Yen TS, Ralston R. 1995. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J. Clin. Microbiol. 33:2058-2063.
5. Paavonen J, Jenkins D, Bosch FX, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter DL, Kitchener HC, Castellsague X, de Carvalho NS, Skinner SR, Harper DM, Hedrick JA, Jaisamrarn U, Limson GA, Dionne M, Quint W, Spiessens B, Peeters P, Struyf F, Wieting SL, Lehtinen MO, Dubin G, HPV PATRICIA study group. 2007. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 369:2161-2170. http://dx.doi.org/10.1016/S0140-6736(07)60946-5.
6. Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, Tang GW, Ferris DG, Steben M, Bryan J, Taddeo FJ, Railkar R, Esser MT, Sings HL, Nelson M, Boslego J, Sattler C, Barr E, Koutsky LA, Females United to Unilaterally Reduce Endo/Ectocervical Disease II. 2007. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N. Engl. J. Med. 356:1928-1943. http://dx.doi.org/10.1056/NEJMoa061760.
7. Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, Wheeler CM, Koutsky LA, Malm C, Lehtinen M, Skjeldestad FE, Olsson SE, Steinwall M, Brown DR, Kurman RJ, Ronnett BM, Stoler MH, Ferenczy A, Harper DM, Tamms GM, Yu J, Lupinacci L, Railkar R, Taddeo FJ, Jansen KU, Esser MT, Sings HL, Saah AJ, Barr E. 2005. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised doubleblind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol. 6:271-278. http://dx.doi.org/10.1016/S1470-2045(05)70101-7.
8. 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. http://dx.doi.org/10.1074/jbc.274.9.5810.
9. Giroglou T, Florin L, Schafer F, Streeck RE, Sapp M. 2001. Human papillomavirus infection requires cell surface heparan sulfate. J. Virol. 75:1565-1570. http://dx.doi.org/10.1128/JVI.75.3.1565-1570.2001.
10. Bienkowska-Haba M, Patel HD, Sapp M. 2009. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog. 5:e1000524. http://dx.doi.org/10.1371/journal.ppat.1000524.
11. Selinka HC, Giroglou T, Nowak T, Christensen ND, Sapp M. 2003. Further evidence that papillomavirus capsids exist in two distinct conformations. J. Virol. 77:12961-12967. http://dx.doi.org/10.1128/JVI.77.24.12961-12967.2003.
12. Selinka HC, Florin L, Patel HD, Freitag K, Schmidtke M, Makarov VA, Sapp M. 2007. Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus. J. Virol. 81:10970-10980. http://dx.doi.org/10.1128/JVI.00998- 07.
13. 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. http://dx.doi.org/10.1371/journal.pone.0003313.
14. 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. http://dx.doi.org/10.1371/ journal.ppat.1002519.
15. Scheffer KD, Gawlitza A, Spoden GA, Zhang XA, Lambert C, Berditchevski F, Florin L. 2013. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J. Virol. 87:3435-3446. http://dx.doi.org/10.1128/JVI.02906-12.
16. 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. http://dx.doi.org/10.1371/journal.ppat.1002657.
17. Spoden G, Kuhling L, Cordes N, Frenzel B, Sapp M, Boller K, Florin L, Schelhaas M. 2013. Human papillomaviruses type 16, 18, and 31 share similar endocytic requirements for entry. J. Virol. 87:7765-7773. http://dx.doi.org/10. 1128/JVI.00370-13.
18. Selinka HC, Giroglou T, Sapp M. 2002. Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299: 279-287. http://dx.doi.org/10.1006/viro.2001.1493.
19. Dabydeen SA, Meneses PI. 2009. The role of NH4Cl and cysteine proteases in human papillomavirus type 16 infection. Virol. J. 6:109. http://dx.doi.org/ 10.1186/1743-422X-6-109.
20. Smith JL, Campos SK, Wandinger-Ness A, Ozbun MA. 2008. Caveolin-1-dependent infectious entry of human papillomavirus type 31 in human keratinocytes proceeds to the endosomal pathway for pH-dependent uncoating. J. Virol. 82:9505-9512. http://dx.doi.org/10.1128/JVI.01014-08.
21. Bienkowska-Haba M, Williams C, Kim SM, Garcea RL, Sapp M. 2012. Cyclophilins facilitate dissociation of the human papillomavirus type 16 capsid protein L1 from the L2/DNA complex following virus entry. J. Virol. 86:9875-9887. http://dx.doi.org/10.1128/JVI.00980-12.
22. Day PM, Lowy DR, Schiller JT. 2003. Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307:1-11. http://dx.doi.org/10.1016/S0042- 6822(02)00143-5.
23. Müller KH, Kainov DE, El Bakkouri K, Saelens X, De Brabander JK, Kittel C, Samm E, Muller CP. 2011. The proton translocation domain of cellular vacuolar ATPase provides a target for the treatment of influenza A virus infections. Br. J. Pharmacol. 164:344-357. http://dx.doi.org/10.1111/j.1476- 5381.2011.01346.x.
24. Müller KH, Kakkola L, Nagaraj AS, Cheltsov AV, Anastasina M, Kainov DE. 2012. Emerging cellular targets for influenza antiviral agents. Trends Pharmacol. Sci. 33:89-99. http://dx.doi.org/10.1016/j.tips.2011.10.004.
25. Buck CB, Pastrana DV, Lowy DR, Schiller JT. 2004. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78:751-757. http://dx.doi.org/10. 1128/JVI.78.2.751-757.2004.
26. Schneider MA, Spoden GA, Florin L, Lambert C. 2011. Identification of the dynein light chains required for human papillomavirus infection. Cell. Microbiol. 13:32-46. http://dx.doi.org/10.1111/j.1462-5822.2010.01515.x.
27. Kondo K, Ishii Y, Ochi H, Matsumoto T, Yoshikawa H, Kanda T. 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. http://dx.doi.org/10.1016/j.virol.2006.08.037.
28. Leder C, Kleinschmidt JA, Wiethe C, Muller M. 2001. Enhancement of capsid gene expression: preparing the human papillomavirus type 16 major structural gene L1 for DNA vaccination purposes. J. Virol. 75:9201-9209. http://dx.doi.org/10.1128/JVI.75.19.9201-9209.2001.
29. Pastrana DV, Buck CB, Pang YY, Thompson CD, Castle PE, FitzGerald PC, Kruger Kjaer S, Lowy DR, Schiller JT. 2004. Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. Virology 321:205-216. http://dx.doi.org/10.1016/j.virol. 2003.12.027.
30. Pastrana DV, Gambhira R, Buck CB, Pang YY, Thompson CD, Culp TD, Christensen ND, Lowy DR, Schiller JT, Roden RB. 2005. Crossneutralization of cutaneous and mucosal Papillomavirus types with antisera to the amino terminus of L2. Virology 337:365-372. http://dx.doi.org/10.1016/j.virol.2005.04.011.
31. Mossadegh N, Gissmann L, Muller M, Zentgraf H, Alonso A, Tomakidi P. 2004. Codon optimization of the human papillomavirus 11 (HPV 11) L1 gene leads to increased gene expression and formation of virus-like particles in mammalian epithelial cells. Virology 326:57-66. http://dx.doi.org/10.1016/j.virol.2004.04. 050.
32. Lebreton S, Xie X-S, Ferguson D, De Brabander JK. 2004. Ring-closing metathesis: a powerful tool for the synthesis of simplified salicylihalamidebased V-ATPase inhibitors. Tetrahedron 60:9635-9647. http://dx.doi.org/10.1016/j.tet.2004.06.146.
33. Wu Y, Liao X, Wang R, Xie XS, De Brabander JK. 2002. Total synthesis and initial structure-function analysis of the potent V-ATPase inhibitors salicylihalamide A and related compounds. J. Am. Chem. Soc. 124:3245-3253. http://dx.doi.org/10.1021/ja0177713.
34. Lebreton S, Jaunbergs J, Roth MG, Ferguson DA, De Brabander JK. 2008. Evaluating the potential of vacuolar ATPase inhibitors as anticancer agents and multigram synthesis of the potent salicylihalamide analog saliphenylhalamide. Bioorg. Med. Chem. Lett. 18:5879-5883. http://dx.doi.org/10.1016/j.bmcl.2008.07. 003.
35. Xie XS, Padron D, Liao X, Wang J, Roth MG, De Brabander JK. 2004. SalicylihalamideAinhibits the V0 sector of the V-ATPase through a mechanism distinct from bafilomycin A1. J. Biol. Chem. 279:19755-19763. http://dx.doi.org/10.1074/jbc.M313796200.
36. Rommel O, Dillner J, Fligge C, Bergsdorf C, Wang X, Selinka HC, Sapp M. 2005. Heparan sulfate proteoglycans interact exclusively with conformationally intact HPV L1 assemblies: basis for a virus-like particle ELISA. J. Med. Virol. 75:114-121. http://dx.doi.org/10.1002/jmv.20245.
37. Scheffer KD, Popa-Wagner R, Florin L. 2013. Isolation and characterization of pathogen-bearing endosomes enable analysis of endosomal escape and identification of new cellular cofactors of infection. Methods Mol. Biol. 1064:101-113. http://dx.doi.org/10.1007/978-1-62703-601-6-7.
38. Campos SK, Chapman JA, Deymier MJ, Bronnimann MP, Ozbun MA. 2012. Opposing effects of bacitracin on human papillomavirus type 16 infection: enhancement of binding and entry and inhibition of endosomal penetration. J. Virol. 86:4169-4181. http://dx.doi.org/10.1128/JVI.05493-11.
39. Sapp M,Kraus U,Volpers C,Snijders PJ,Walboomers JM,Streeck RE. ,Analysis of type-restricted and cross-reactive epitopes on virus-like particles of human papillomavirus type 33 and in infected tissues using monoclonal antibodies to the major capsid protein. J. Gen. Virol. 75(Pt 12):3375-3383. http://dx.doi.org/10.1099/0022-1317-75-12-3375.
40. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR, Schiller JT. 2006. Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog. 2:e69. http://dx.doi.org/10.1371/journal.ppat.0020069.
41. Spoden GA, Besold K, Krauter S, Plachter B, Hanik N, Kilbinger AF, Lambert C, Florin L. 2012. Polyethylenimine is a strong inhibitor of human papillomavirus and cytomegalovirus infection. Antimicrob. Agents Chemother. 56:75-82. http://dx.doi.org/10.1128/AAC.05147-11.
42. Huang HS, Pyeon D, Pearce SM, Lank SM, Griffin LM, Ahlquist P, Lambert PF. 2012. Novel antivirals inhibit early steps in HPV infection. Antiviral Res. 93:280-287. http://dx.doi.org/10.1016/j.antiviral.2011.12.007.
43. Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A, Kuruvilla L, Guie MA, Poffenberger AC, Nelson CD, Atwood WJ, Dimaio D. 2013. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc. Natl. Acad. Sci. U. S. A. 110:7452-7457. http://dx.doi.org/10.1073/pnas. 1302164110.
44. De Brabander JK, Wu Y. May 2004. Synthetic salicylihalamides, apicularens and derivatives thereof. US patent 6,734,209.