Recruitment of PI4KIIIβ to coxsackievirus B3 replication organelles is independent of ACBD3, GBF1, and Arf1

Journal of Virology

Volumn 88, Issue 5, 2014, Pages 2725-2736

  Dorobantu, Cristina M ^a   van der Schaar, Hilde M ^a   Ford, Lauren A ^b   Strating, Jeroen R P M ^a   Ulferts, Rachel ^a   Fang, Ying ^c   Belov, George ^b   Van Kuppeveld, Frank J M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF MARYLAND   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR 1; PI4KIII BETA PROTEIN; PROTEIN ACBD3; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; COXSACKIE VIRUS B3; ENTEROVIRUS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA INTERFERENCE; VIRUS REPLICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADP-RIBOSYLATION FACTOR 1; ANIMALS; CELL LINE; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MEMBRANE PROTEINS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84896718477     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03650-13     Document Type: Article

References (42)

1. Nagy PD, Pogany J. 2012. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 10:137-149. http://dx.doi.org /10.1038/nrmicro2692.
2. Belov GA, van Kuppeveld FJM. 2012. (+)RNA viruses rewire cellular pathways to build replication organelles. Curr. Opin. Virol. 2:740-747. http://dx.doi.org/10.1016/j.coviro.2012.09.006.
3. Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363-374. http://dx .doi.org/10.1038/nrmicro1890.
4. Romero-Brey I, Merz A, Chiramel A, Lee J-Y, Chlanda P, Haselman U, Santarella-Mellwig R, Habermann A, Hoppe S, Kallis S, Walther P, Antony C, Krijnse-Locker J, Bartenschlager R. 2012. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 8:e1003056. http://dx.doi.org/10 .1371/journal.ppat.1003056.
5. Welsch S, Miller S, Romero-Brey I, Merz A, Bleck CKE, Walther P, Fuller SD, Antony C, Krijnse-Locker J, Bartenschlager R. 2009. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5:365-375. http://dx.doi.org /10.1016/j.chom.2009.03.007.
6. Gillespie LK, Hoenen A, Morgan G, Mackenzie JM. 2010. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 84:10438-10447. http://dx.doi.org /10.1128/JVI.00986-10.
7. Limpens RWAL, van der Schaar HM, Kumar D, Koster AJ, Snijder EJ, van Kuppeveld FJM, Bárcena M. 2011. The transformation of enterovirus replication structures: a three-dimensional study of single-and double-membrane compartments. mBio 2:e00166-11. http://dx.doi.org/10 .1128/mBio.00166-11.
8. Belov GA, Nair V, Hansen BT, Hoyt FH, Fischer ER, Ehrenfeld E. 2012. Complex dynamic development of poliovirus membranous replication complexes. J. Virol. 86:302-312. http://dx.doi.org/10.1128/JVI.05937-11.
9. Bienz K, Egger D, Pasamontes L. 1987. Association of polioviral proteins of the P2 genomic region with the viral replication complex and virusinduced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 160:220-226. http://dx .doi.org/10.1016/0042-6822(87)90063-8.
10. Hsu N-Y, Ilnytska O, Belov G, Santiana M, Chen Y-H, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJM, Altan-Bonnet N. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799-811. http://dx.doi.org/10.1016/j.cell.2010.03 .050.
11. van der Schaar HM, Leyssen P, Thibaut HJ, de Palma A, van der Linden L, Lanke KHW, Lacroix C, Verbeken E, Conrath K, MacLeod AM, Mitchell DR, Palmer NJ, van de Poël H, Andrews M, Neyts J, van Kuppeveld FJM. 2013. A novel, broad-spectrum inhibitor of enterovirus replication that targets host cell factor phosphatidylinositol 4-kinase IIIβ. Antimicrob. Agents Chemother. 57:4971-4981. http://dx.doi.org/10 .1128/AAC.01175-13.
12. Godi A, Pertile P, Meyers R, Marra P, Di Tullio G, Iurisci C, Luini A, Corda D, De Matteis MA. 1999. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P2 on the Golgi complex. Nat. Cell Biol. 1:280-287. http://dx.doi.org/10.1038/12993.
13. Clayton EL, Minogue S, Waugh MG. 2013. Mammalian phosphatidylinositol 4-kinases as modulators of membrane trafficking and lipid signaling networks. Prog. Lipid Res. 52:294-304. http://dx.doi.org/10.1016/j .plipres.2013.04.002.
14. De Matteis MA, Wilson C, D'Angelo G. 2013. Phosphatidylinositol-4-phosphate: the Golgi and beyond. Bioessays 6:1-11. http://dx.doi.org/10 .1002/bies.201200180.
15. Donaldson JG, Honda A, Weigert R. 2005. Multiple activities for Arf1 at the Golgi complex. Biochim. Biophys. Acta 1744:364-373. http://dx.doi .org/10.1016/j.bbamcr.2005.03.001.
16. D'Souza-Schorey C, Chavrier P. 2006. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7:347-358. http://dx.doi.org /10.1038/nrm1910.
17. Presley JF, Ward TH, Pfeifer AC, Siggia ED, Phair RD, Lippincott-Schwartz J. 2002. Dissection of COPI and Arf1 dynamics in vivo and role in Golgi membrane transport. Nature 417:187-193. http://dx.doi.org/10 .1038/417187a.
18. Rabouille C, Klumperman J. 2005. Opinion: the maturing role of COPI vesicles in intra-Golgi transport. Nat. Rev. Mol. Cell Biol. 6:812-817. http: //dx.doi.org/10.1038/nrm1735.
19. Bonifacino JS, Lippincott-Schwartz J. 2003. Coat proteins: shaping membrane transport. Nat. Rev. Mol. Cell Biol. 4:409-414. http://dx.doi .org/10.1038/nrm1099.
20. Boehm M, Aguilar RC, Bonifacino JS. 2001. Functional and physical interactions of the adaptor protein complex AP-4 with ADP-ribosylation factors (ARFs). EMBO J. 20:6265-6276. http://dx.doi.org/10.1093/emboj /20.22.6265.
21. Ooi CE, Dell'Angelica EC, Bonifacino JS. 1998. ADP-ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol. 142:391-402. http://dx.doi.org/10.1083/jcb.142.2.391.
22. Belov GA, Feng Q, Nikovics K, Jackson CL, Ehrenfeld E. 2008. A critical role of a cellular membrane traffic protein in poliovirus RNA replication. PLoS Pathog. 4:e1000216. http://dx.doi.org/10.1371/journal.ppat.1000216.
23. Lanke KHW, van der Schaar HM, Belov GA, Feng Q, Duijsings D, Jackson CL, Ehrenfeld E, van Kuppeveld FJM. 2009. GBF1, a guanine nucleotide exchange factor for Arf, is crucial for coxsackievirus B3 RNA replication. J. Virol. 83:11940-11949. http://dx.doi.org/10.1128/JVI .01244-09.
24. Belov GA, Altan-Bonnet N, Kovtunovych G, Jackson CL, Lippincott-Schwartz J, Ehrenfeld E. 2007. Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 81:558-567. http://dx.doi.org/10.1128/JVI.01820-06.
25. Belov GA, Kovtunovych G, Jackson CL, Ehrenfeld E. 2010. Poliovirus replication requires the N-terminus but not the catalytic Sec7 domain of ArfGEF GBF1. Cell. Microbiol. 12:1463-1479. http://dx.doi.org/10.1111/j .1462-5822.2010.01482.x.
26. Wessels E, Duijsings D, Niu T-K, Neumann S, Oorschot VM, de Lange F, Lanke KHW, Klumperman J, Henke A, Jackson CL, Melchers WJG, van Kuppeveld FJM. 2006. A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1. Dev. Cell 11:191-201. http://dx.doi.org/10.1016/j.devcel.2006.06 .005.
27. Sasaki J, Ishikawa K, Arita M, Taniguchi K. 2012. ACBD3-mediated recruitment of PI4KB to picornavirus RNA replication sites. EMBO J. 31:754-766.
28. Greninger AL, Knudsen GM, Betegon M, Burlingame AL, Derisi JL. 2012. The 3A protein from multiple picornaviruses utilizes the Golgi adaptor protein ACBD3 to recruit PI4KIIIβ. J. Virol. 86:3605-3616. http: //dx.doi.org/10.1128/JVI.06778-11.
29. Sohda M, Misumi Y, Yamamoto A, Yano A, Nakamura N, Ikehara Y. 2001. Identification and characterization of a novel Golgi protein, GCP60, that interacts with the integral membrane protein giantin. J. Biol. Chem. 276:45298-45306. http://dx.doi.org/10.1074/jbc.M108961200.
30. Wessels E, Duijsings D, Lanke KHW, Melchers WJG, Jackson CL, van Kuppeveld FJM. 2007. Molecular determinants of the interaction between coxsackievirus protein 3A and guanine nucleotide exchange factor GBF1. J. Virol. 81:5238-5245. http://dx.doi.org/10.1128/JVI.02680-06.
31. Wessels E, Duijsings D, Notebaart RA, Melchers WJG, van Kuppeveld FJM, Melchers JG, van Kuppeveld FJM. 2005. A proline-rich region in the coxsackievirus 3A protein is required for the protein to inhibit endoplasmic reticulum-to-Golgi transport. J. Virol. 79:5163-5173. http://dx .doi.org/10.1128/JVI.79.8.5163-5173.2005.
32. van der Schaar HM, van der Linden L, Lanke KHW, Strating JRPM, Pürstinger G, de Vries E, de Haan CAM, Neyts J, van Kuppeveld FJM. 2012. Coxsackievirus mutants that can bypass host factor PI4KIIIβ and the need for high levels of PI4P lipids for replication. Cell Res. 22:1576-1592. http://dx.doi.org/10.1038/cr.2012.129.
33. Greninger AL, Knudsen GM, Betegon M, Burlingame AL, DeRisi JL. 2013. ACBD3 interaction with TBC1 domain 22 protein is differentially affected by enteroviral and kobuviral 3A protein binding. mBio 4(2): e00098-13. http://dx.doi.org/10.1128/mBio.00098-13.
34. Téoulé F, Brisac C, Pelletier I, Vidalain P-O, Jégouic Mirabelli SC, Bessaud M, Combelas N, Autret A, Tangy F, Delpeyroux F, Blondel B. 2013. The Golgi protein ACBD3, an interactor for poliovirus protein 3A, modulates poliovirus replication. J. Virol. 87:11031-11046. http://dx.doi .org/10.1128/JVI.00304-13.
35. Peyroche A, Antonny B, Robineau S, Acker J, Cherfils J, Jackson CL. 1999. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex. Mol. Cell 3:275-285. http://dx.doi.org/10.1016/S1097-2765(00)80455-4.
36. Pan H, Yu J, Zhang L, Carpenter A, Zhu H, Li L, Ma D, Yuan J. 2008. A novel small molecule regulator of guanine nucleotide exchange activity of the ADP-ribosylation factor and Golgi membrane trafficking. J. Biol. Chem. 283:31087-31096. http://dx.doi.org/10.1074/jbc.M806592200.
37. Van der Linden L, van der Schaar HM, Lanke KHW, Neyts J, van Kuppeveld FJM. 2010. Differential effects of the putative GBF1 inhibitors Golgicide A and AG1478 on enterovirus replication. J. Virol. 84:7535-7542. http://dx.doi.org/10.1128/JVI.02684-09.
38. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P, Kaderali L, Poenisch M, Blankenburg H, Hiet M-S, Longerich T, Diehl S, Ramirez F, Balla T, Rohr K, Kaul A, Bühler S, Pepperkok R, Lengauer T, Albrecht M, Eils R, Schirmacher P, Lohmann V, Bartenschlager R. 2011. Recruitment and activation of a lipid kinase by hepatitisCvirus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9:32-45. http://dx.doi.org/10.1016/j.chom.2010.12.002.
39. Martín-Acebes MA, Blázquez A-B, Jiménez de Oya N, Escribano-Romero E, Saiz J-C. 2011. West Nile virus replication requires fatty acid synthesis but is independent on phosphatidylinositol-4-phosphate lipids. PLoS One 6:e24970. http://dx.doi.org/10.1371/journal.pone.0024970.
40. Heaton NS, Perera R, Berger KL, Khadka S, Lacount DJ, Kuhn RJ, Randall G. 2010. Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. Proc. Natl. Acad. Sci. U. S. A. 107:17345-17350. http://dx.doi .org/10.1073/pnas.1010811107.
41. Nchoutmboube JA, Viktorova EG, Scott AJ, Ford LA, Pei Z, Watkins PA, Ernst RK, Belov GA. 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. http://dx.doi.org/10.1371/journal.ppat.1003401.
42. Shinoda Y, Fujita K, Saito S, Matsui H, Kanto Y, Nagaura Y, Fukunaga K, Tamura S, Kobayashi T. 2012. Acyl-CoA binding domain containing 3 (ACBD3) recruits the protein phosphatase PPM1L to ER-Golgi membrane contact sites. FEBS Lett. 586:3024-3029. http://dx.doi.org/10.1016 /j.febslet.2012.06.050.