Mechanism of Poliovirus Resistance to Host Phosphatidylinositol-4 Kinase III β Inhibitor

ACS Infectious Diseases

Volumn 2, Issue 2, 2016, Pages 140-148

  Arita, Minetaro ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

enterovirus; inhibitor; PI4KB; poliovirus; resistance

Indexed keywords

AN 22A 6; CELL PROTEIN; OXYSTEROL BINDING PROTEIN; PHOSPHATIDYLINOSITOL 4 KINASE III BETA; PHOSPHATIDYLINOSITOL 4 KINASE III BETA INHIBITOR; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL KINASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN 2BC; PROTEIN 2C; PROTEIN 3A; PROTEIN 3AB; PROTEIN 3D; UNCLASSIFIED DRUG; VIRUS PROTEIN; ANTIVIRUS AGENT; PHOSPHATIDYLINOSITOL 4-KINASE IIIBETA, HUMAN; PHOSPHOTRANSFERASE; STEROID RECEPTOR; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; PHENOTYPE; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; VIRUS MUTATION; VIRUS REPLICATION; VIRUS RESISTANCE; ANTAGONISTS AND INHIBITORS; ANTIVIRAL RESISTANCE; BIOSYNTHESIS; DNA MUTATIONAL ANALYSIS; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; POLIOMYELITIS; VIROLOGY;

ANTIVIRAL AGENTS; DNA MUTATIONAL ANALYSIS; DRUG RESISTANCE, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POLIOMYELITIS; POLIOVIRUS; RECEPTORS, STEROID; RNA, VIRAL; VIRUS REPLICATION;

EID: 84969188132     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/acsinfecdis.5b00122     Document Type: Article

References (58)

1. Bodian, D. (1949) Histopathologic basis of clinical findings in poliomyelitis Am. J. Med. 6, 563-578 10.1016/0002-9343(49)90130-8
2. Couderc, T., Christodoulou, C., Kopecka, H., Marsden, S., Taffs, L. F., Crainic, R., and Horaud, F. (1989) Molecular pathogenesis of neural lesions induced by poliovirus type 1 J. Gen. Virol. 70, 2907-2918 10.1099/0022-1317-70-11-2907
3. Committee on Development of a Polio Antiviral and Its Potential Role in Global Poliomyelitis Eradication, NRC. ((2006) Exploring the Role of Antiviral Drugs in the Eradication of Polio: Workshop Report, National Academies Press, Washington, DC, USA.
4. Wikel, J. H., Paget, C. J., DeLong, D. C., Nelson, J. D., Wu, C. Y., Paschal, J. W., Dinner, A., Templeton, R. J., Chaney, M. O., Jones, N. D., and Chamberlin, J. W. (1980) Synthesis of syn and anti isomers of 6-[[(hydroxyimino)phenyl]methyl]-1-[(1-methylethyl)sulfonyl]-1H-benzimidaz ol-2-amine. Inhibitors of rhinovirus multiplication J. Med. Chem. 23, 368-372 10.1021/jm00178a004
5. Ishitsuka, H., Ohsawa, C., Ohiwa, T., Umeda, I., and Suhara, Y. (1982) Antipicornavirus flavone Ro 09-0179 Antimicrob. Agents Chemother. 22, 611-616 10.1128/AAC.22.4.611
6. Arita, M., Kojima, H., Nagano, T., Okabe, T., Wakita, T., and Shimizu, H. (2011) Phosphatidylinositol 4-kinase III beta is a target of enviroxime-like compounds for antipoliovirus activity J. Virol. 85, 2364-2372 10.1128/JVI.02249-10
7. Spickler, C., Lippens, J., Laberge, M. K., Desmeules, S., Bellavance, E., Garneau, M., Guo, T., Hucke, O., Leyssen, P., Neyts, J., Vaillancourt, F. H., Decor, A., O'Meara, J., Franti, M., and Gauthier, A. (2013) Phosphatidylinositol 4-kinase III beta is essential for replication of human rhinovirus and its inhibition causes a lethal phenotype in vivo Antimicrob. Agents Chemother. 57, 3358-3368 10.1128/AAC.00303-13
8. Arita, M., Kojima, H., Nagano, T., Okabe, T., Wakita, T., and Shimizu, H. (2013) Oxysterol-binding protein family I is the target of minor enviroxime-like compounds J. Virol. 87, 4252-4260 10.1128/JVI.03546-12
9. Fox, M. P., Otto, M. J., and McKinlay, M. A. (1986) Prevention of rhinovirus and poliovirus uncoating by WIN 51711, a new antiviral drug Antimicrob. Agents Chemother. 30, 110-116 10.1128/AAC.30.1.110
10. Molla, A., Hellen, C. U., and Wimmer, E. (1993) Inhibition of proteolytic activity of poliovirus and rhinovirus 2A proteinases by elastase-specific inhibitors J. Virology 67, 4688-4695
11. Caliguiri, L. A. and Tamm, I. (1968) Action of guanidine on the replication of poliovirus RNA Virology 35, 408-417 10.1016/0042-6822(68)90219-5
12. Shimizu, H., Agoh, M., Agoh, Y., Yoshida, H., Yoshii, K., Yoneyama, T., Hagiwara, A., and Miyamura, T. (2000) Mutations in the 2C region of poliovirus responsible for altered sensitivity to benzimidazole derivatives J. Virol. 74, 4146-4154 10.1128/JVI.74.9.4146-4154.2000
13. De Palma, A. M., Heggermont, W., Lanke, K., Coutard, B., Bergmann, M., Monforte, A. M., Canard, B., De Clercq, E., Chimirri, A., Purstinger, G., Rohayem, J., van Kuppeveld, F., and Neyts, J. (2008) The thiazolobenzimidazole TBZE-029 inhibits enterovirus replication by targeting a short region immediately downstream from motif C in the nonstructural protein 2C J. Virol. 82, 4720-4730 10.1128/JVI.01338-07
14. Ulferts, R., van der Linden, L., Thibaut, H. J., Lanke, K. H., Leyssen, P., Coutard, B., De Palma, A. M., Canard, B., Neyts, J., and van Kuppeveld, F. J. (2013) Selective serotonin reuptake inhibitor fluoxetine inhibits replication of human enteroviruses B and D by targeting viral protein 2C Antimicrob. Agents Chemother. 57, 1952-1956 10.1128/AAC.02084-12
15. Patick, A. K., Binford, S. L., Brothers, M. A., Jackson, R. L., Ford, C. E., Diem, M. D., Maldonado, F., Dragovich, P. S., Zhou, R., Prins, T. J., Fuhrman, S. A., Meador, J. W., Zalman, L. S., Matthews, D. A., and Worland, S. T. (1999) In vitro antiviral activity of AG7088, a potent inhibitor of human rhinovirus 3C protease Antimicrob. Agents Chemother. 43, 2444-2450
16. Furuta, Y., Takahashi, K., Fukuda, Y., Kuno, M., Kamiyama, T., Kozaki, K., Nomura, N., Egawa, H., Minami, S., Watanabe, Y., Narita, H., and Shiraki, K. (2002) In vitro and in vivo activities of anti-influenza virus compound T-705 Antimicrob. Agents Chemother. 46, 977-981 10.1128/AAC.46.4.977-981.2002
17. Hellen, C. U., Witherell, G. W., Schmid, M., Shin, S. H., Pestova, T. V., Gil, A., and Wimmer, E. (1993) A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein Proc. Natl. Acad. Sci. U. S. A. 90, 7642-7646 10.1073/pnas.90.16.7642
18. Wessels, E., Duijsings, D., Niu, T. K., Neumann, S., Oorschot, V. M., de Lange, F., Lanke, K. H., Klumperman, J., Henke, A., Jackson, C. L., Melchers, W. J., and van Kuppeveld, F. J. (2006) A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1 Dev. Cell 11, 191-201 10.1016/j.devcel.2006.06.005
19. Bedard, K. M., Daijogo, S., and Semler, B. L. (2007) A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation EMBO J. 26, 459-467 10.1038/sj.emboj.7601494
20. Arita, M., Wakita, T., and Shimizu, H. (2012) Valosin-containing protein (VCP/p97) is required for poliovirus replication and is involved in cellular protein secretion pathway in poliovirus infection J. Virol. 86, 5541-5553 10.1128/JVI.00114-12
21. Rozovics, J. M., Chase, A. J., Cathcart, A. L., Chou, W., Gershon, P. D., Palusa, S., Wilusz, J., and Semler, B. L. (2013) Picornavirus modification of a host mRNA decay protein mBio 3, e00431 10.1128/mBio.00431-12
22. Sasaki, J., Ishikawa, K., Arita, M., and Taniguchi, K. (2012) ACBD3-mediated recruitment of PI4KB to picornavirus RNA replication sites EMBO J. 31, 754-766 10.1038/emboj.2011.429
23. Virgen-Slane, R., Rozovics, J. M., Fitzgerald, K. D., Ngo, T., Chou, W., van der Heden van Noort, G. J., Filippov, D. V., Gershon, P. D., and Semler, B. L. (2012) An RNA virus hijacks an incognito function of a DNA repair enzyme Proc. Natl. Acad. Sci. U. S. A. 109, 14634-14639 10.1073/pnas.1208096109
24. Nchoutmboube, J. A., Viktorova, E. G., Scott, A. J., Ford, L. A., Pei, Z., Watkins, P. A., Ernst, R. K., and Belov, G. A. (2013) Increased long chain acyl-CoA synthetase activity and fatty acid import is linked to membrane synthesis for development of picornavirus replication organelles PLoS Pathog. 9, e1003401 10.1371/journal.ppat.1003401
25. Bordeleau, M. E., Mori, A., Oberer, M., Lindqvist, L., Chard, L. S., Higa, T., Belsham, G. J., Wagner, G., Tanaka, J., and Pelletier, J. (2006) Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A Nat. Chem. Biol. 2, 213-220 10.1038/nchembio776
26. Irurzun, A., Perez, L., and Carrasco, L. (1992) Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A Virology 191, 166-175 10.1016/0042-6822(92)90178-R
27. Maynell, L. A., Kirkegaard, K., and Klymkowsky, M. W. (1992) Inhibition of poliovirus RNA synthesis by brefeldin A J. Virol. 66, 1985-1994
28. Cuconati, A., Molla, A., and Wimmer, E. (1998) Brefeldin A inhibits cell-free, de novo synthesis of poliovirus J. Virol. 72, 6456-6464
29. Belov, G. A., Feng, Q., Nikovics, K., Jackson, C. L., and Ehrenfeld, E. (2008) A critical role of a cellular membrane traffic protein in poliovirus RNA replication PLoS Pathog. 4, e1000216 10.1371/journal.ppat.1000216
30. Arita, M. (2014) Phosphatidylinositol-4 kinase III beta and oxysterol-binding protein accumulate unesterified cholesterol on poliovirus-induced membrane structure Microbiol. Immunol. 58, 239-256 10.1111/1348-0421.12144
31. Arita, M., Wakita, T., and Shimizu, H. (2008) Characterization of pharmacologically active compounds that inhibit poliovirus and enterovirus 71 infectivity J. Gen. Virol. 89, 2518-2530 10.1099/vir.0.2008/002915-0
32. Arita, M., Takebe, Y., Wakita, T., and Shimizu, H. (2010) A bifunctional anti-enterovirus compound that inhibits replication and early stage of enterovirus 71 infection J. Gen. Virol. 91, 2734-2744 10.1099/vir.0.023374-0
33. Delang, L., Paeshuyse, J., and Neyts, J. (2012) The role of phosphatidylinositol 4-kinases and phosphatidylinositol 4-phosphate during viral replication Biochem. Pharmacol. 84, 1400-1408 10.1016/j.bcp.2012.07.034
34. Strating, J. R., van der Linden, L., Albulescu, L., Bigay, J., Arita, M., Delang, L., Leyssen, P., van der Schaar, H. M., Lanke, K. H., Thibaut, H. J., Ulferts, R., Drin, G., Schlinck, N., Wubbolts, R. W., Sever, N., Head, S. A., Liu, J. O., Beachy, P. A., De Matteis, M. A., Shair, M. D., Olkkonen, V. M., Neyts, J., and van Kuppeveld, F. J. (2015) Itraconazole inhibits enterovirus replication by targeting the oxysterol-binding protein Cell Rep. 10, 600-615 10.1016/j.celrep.2014.12.054
35. Arita, M., Philipov, S., and Galabov, A. S. (2015) Phosphatidylinositol 4-kinase III beta is the target of oxoglaucine and pachypodol (Ro 09-0179) for their anti-poliovirus activities, and is located at upstream of the target step of brefeldin A Microbiol. Immunol. 59, 338-347 10.1111/1348-0421.12261
36. Hsu, N. Y., Ilnytska, O., Belov, G., Santiana, M., Chen, Y. H., Takvorian, P. M., Pau, C., van der Schaar, H., Kaushik-Basu, N., Balla, T., Cameron, C. E., Ehrenfeld, E., van Kuppeveld, F. J., and Altan-Bonnet, N. (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication Cell 141, 799-811 10.1016/j.cell.2010.03.050
37. Galabov, A. S., Nikolaeva, L., and Philipov, S. (1995) Aporphinoid alkaloid glaucinone: a selective inhibitor of poliovirus replication Antiviral Res. 26, A347 10.1016/0166-3542(95)94930-Z
38. Arita, M., Wakita, T., and Shimizu, H. (2009) Cellular kinase inhibitors that suppress enterovirus replication have a conserved target in viral protein 3A similar to that of enviroxime J. Gen. Virol. 90, 1869-1879 10.1099/vir.0.012096-0
39. De Palma, A. M., Thibaut, H. J., van der Linden, L., Lanke, K., Heggermont, W., Ireland, S., Andrews, R., Arimilli, M., Altel, T., De Clercq, E., van Kuppeveld, F., and Neyts, J. (2009) Mutations in the non-structural protein 3A confer resistance to the novel enterovirus replication inhibitor TTP-8307 Antimicrob. Agents Chemother. 53, 1850-1857 10.1128/AAC.00934-08
40. MacLeod, A. M., Mitchell, D. R., Palmer, N. J., Van de Poel, H., Conrath, K., Andrews, M., Leyssen, P., and Neyts, J. (2013) Identification of a series of compounds with potent antiviral activity for the treatment of enterovirus infections ACS Med. Chem. Lett. 4, 585-589 10.1021/ml400095m
41. Heinz, B. A. and Vance, L. M. (1995) The antiviral compound enviroxime targets the 3A coding region of rhinovirus and poliovirus J. Virol. 69, 4189-4197
42. Ridgway, N. D. (2010) Oxysterol-binding proteins Subcell. Biochem. 51, 159-182 10.1007/978-90-481-8622-8-6
43. Mesmin, B., Bigay, J., Moser von Filseck, J., Lacas-Gervais, S., Drin, G., and Antonny, B. (2013) A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP Cell 155, 830-843 10.1016/j.cell.2013.09.056
44. Roulin, P. S., Lotzerich, M., Torta, F., Tanner, L. B., van Kuppeveld, F. J., Wenk, M. R., and Greber, U. F. (2014) Rhinovirus uses a phosphatidylinositol 4-phosphate/cholesterol counter-current for the formation of replication compartments at the ER-Golgi interface Cell Host Microbe 16, 677-690 10.1016/j.chom.2014.10.003
45. Rodriguez, P. L. and Carrasco, L. (1992) Gliotoxin: inhibitor of poliovirus RNA synthesis that blocks the viral RNA polymerase 3Dpol J. Virol. 66, 1971-1976
46. Suhy, D. A., Giddings, T. H., Jr., and Kirkegaard, K. (2000) Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles J. Virol. 74, 8953-8965 10.1128/JVI.74.19.8953-8965.2000
47. Rust, R. C., Landmann, L., Gosert, R., Tang, B. L., Hong, W., Hauri, H. P., Egger, D., and Bienz, K. (2001) Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex J. Virol. 75, 9808-9818 10.1128/JVI.75.20.9808-9818.2001
48. Jackson, W. T., Giddings, T. H., Jr., Taylor, M. P., Mulinyawe, S., Rabinovitch, M., Kopito, R. R., and Kirkegaard, K. (2005) Subversion of cellular autophagosomal machinery by RNA viruses PLoS Biol. 3, e156 10.1371/journal.pbio.0030156
49. McNamara, C. W., Lee, M. C., Lim, C. S., Lim, S. H., Roland, J., Nagle, A., Simon, O., Yeung, B. K., Chatterjee, A. K., McCormack, S. L., Manary, M. J., Zeeman, A. M., Dechering, K. J., Kumar, T. R., Henrich, P. P., Gagaring, K., Ibanez, M., Kato, N., Kuhen, K. L., Fischli, C., Rottmann, M., Plouffe, D. M., Bursulaya, B., Meister, S., Rameh, L., Trappe, J., Haasen, D., Timmerman, M., Sauerwein, R. W., Suwanarusk, R., Russell, B., Renia, L., Nosten, F., Tully, D. C., Kocken, C. H., Glynne, R. J., Bodenreider, C., Fidock, D. A., Diagana, T. T., and Winzeler, E. A. (2013) Targeting Plasmodium PI(4)K to eliminate malaria Nature 504, 248-253 10.1038/nature12782
50. Ford Siltz, L. A., Viktorova, E. G., Zhang, B., Kouiavskaia, D., Dragunsky, E., Chumakov, K., Isaacs, L., and Belov, G. A. (2014) New small-molecule inhibitors effectively blocking picornavirus replication J. Virol. 88, 11091-11107 10.1128/JVI.01877-14
51. Ilnytska, O., Santiana, M., Hsu, N. Y., Du, W. L., Chen, Y. H., Viktorova, E. G., Belov, G., Brinker, A., Storch, J., Moore, C., Dixon, J. L., and Altan-Bonnet, N. (2013) Enteroviruses harness the cellular endocytic machinery to remodel the host cell cholesterol landscape for effective viral replication Cell Host Microbe 14, 281-293 10.1016/j.chom.2013.08.002
52. van der Schaar, H. M., van der Linden, L., Lanke, K. H., Strating, J. R., Purstinger, G., de Vries, E., de Haan, C. A., Neyts, J., and van Kuppeveld, F. J. (2012) Coxsackievirus mutants that can bypass host factor PI4KIIIbeta and the need for high levels of PI4P lipids for replication Cell Res. 22, 1576-1592 10.1038/cr.2012.129
53. Crotty, S., Saleh, M. C., Gitlin, L., Beske, O., and Andino, R. (2004) The poliovirus replication machinery can escape inhibition by an antiviral drug that targets a host cell protein J. Virol. 78, 3378-3386 10.1128/JVI.78.7.3378-3386.2004
54. Belov, G. A., Kovtunovych, G., Jackson, C. L., and Ehrenfeld, E. (2010) Poliovirus replication requires the N-terminus but not the catalytic Sec7 domain of ArfGEF GBF1 Cell. Microbiol. 12, 1463-1479 10.1111/j.1462-5822.2010.01482.x
55. Teterina, N. L., Zhou, W. D., Cho, M. W., and Ehrenfeld, E. (1995) Inefficient complementation activity of poliovirus 2C and 3D proteins for rescue of lethal mutations J. Virol. 69, 4245-4254
56. Teterina, N. L., Rinaudo, M. S., and Ehrenfeld, E. (2003) Strand-specific RNA synthesis defects in a poliovirus with a mutation in protein 3A J. Virol. 77, 12679-12691 10.1128/JVI.77.23.12679-12691.2003
57. Arita, M., Nagata, N., Sata, T., Miyamura, T., and Shimizu, H. (2006) Quantitative analysis of poliomyelitis-like paralysis in mice induced by a poliovirus replicon J. Gen. Virol. 87, 3317-3327 10.1099/vir.0.82172-0
58. Andino, R., Rieckhof, G. E., Achacoso, P. L., and Baltimore, D. (1993) Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA EMBO J. 12, 3587-3598