Structural insights into Acyl-coenzyme A binding domain containing 3 (ACBD3) protein hijacking by picornaviruses

. 2019 Dec ; 28 (12) : 2073-2079. [epub] 20191017

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31583778

Many picornaviruses hijack the Golgi resident Acyl-coenzyme A binding domain containing 3 (ACBD3) protein in order to recruit the phosphatidylinositol 4-kinase B (PI4KB) to viral replication organelles (ROs). PI4KB, once recruited and activated by ACBD3 protein, produces the lipid phosphatidylinositol 4-phosphate (PI4P), which is a key step in the biogenesis of viral ROs. To do so, picornaviruses use their small nonstructural protein 3A that binds the Golgi dynamics domain of the ACBD3 protein. Here, we present the analysis of the highly flexible ACBD3 proteins and the viral 3A protein in solution using small-angle X-ray scattering and computer simulations. Our analysis revealed that both the ACBD3 protein and the 3A:ACBD3 protein complex have an extended and flexible conformation in solution.

Zobrazit více v PubMed

Harak C, Lohmann V. Ultrastructure of the replication sites of positive‐strand RNA viruses. Virology. 2015;479:418–433. PubMed PMC

Altan‐Bonnet N, Balla T. Phosphatidylinositol 4‐kinases: Hostages harnessed to build panviral replication platforms. Trends Biochem Sci. 2012;37:293–302. PubMed PMC

Fujita K, Krishnakumar SS, Franco D, Paul AV, London E, Wimmer E. Membrane topography of the hydrophobic anchor sequence of poliovirus 3A and 3AB proteins and the functional effect of 3A/3AB membrane association upon RNA replication. Biochemistry. 2007;46:5185–5199. PubMed PMC

Greninger AL, Knudsen GM, Betegon M, Burlingame AL, Derisi JL. The 3A protein from multiple picornaviruses utilizes the golgi adaptor protein ACBD3 to recruit PI4KIIIbeta. J Virol. 2012;86:3605–3616. PubMed PMC

Sasaki J, Ishikawa K, Arita M, Taniguchi K. ACBD3‐mediated recruitment of PI4KB to picornavirus RNA replication sites. EMBO J. 2012;31:754–766. PubMed PMC

Fan J, Liu J, Culty M, Papadopoulos V. Acyl‐coenzyme a binding domain containing 3 (ACBD3; PAP7; GCP60): An emerging signaling molecule. Prog Lipid Res. 2010;49:218–234. PubMed PMC

Klima M, Toth DJ, Hexnerova R, et al. Structural insights and in vitro reconstitution of membrane targeting and activation of human PI4KB by the ACBD3 protein. Sci Rep. 2016;6:23641. PubMed PMC

Boura E, Nencka R. Phosphatidylinositol 4‐kinases: Function, structure. and inhibition Exp Cell Res. 2015;337:136–145. PubMed

Baumlova A, Chalupska D, Rozycki B, et al. The crystal structure of the phosphatidylinositol 4‐kinase IIalpha. EMBO Rep. 2014;15:1085–1092. PubMed PMC

Sbodio JI, Paul BD, Machamer CE, Snyder SH. Golgi protein ACBD3 mediates neurotoxicity associated with Huntington's disease. Cell Rep. 2013;4:890–897. PubMed PMC

Klima M, Chalupska D, Rozycki B, et al. Kobuviral non‐structural 3A proteins act as molecular harnesses to hijack the host ACBD3 protein. Structure. 2017;25:219–230. PubMed

Horova V, Lyoo H, Rozycki B, et al. Convergent evolution in the mechanisms of ACBD3 recruitment to picornavirus replication sites. PLoS Pathog. 2019;15:e1007962. PubMed PMC

Dorobantu CM, Albulescu L, Harak C, et al. Modulation of the host lipid landscape to promote RNA virus replication: The picornavirus encephalomyocarditis virus converges on the pathway used by hepatitis C virus. PLoS Pathog. 2015;11:e1005185. PubMed PMC

Hsu NY, Ilnytska O, Belov G, et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell. 2010;141:799–811. PubMed PMC

Dubankova A, Humpolickova J, Klima M, Boura E. Negative charge and membrane‐tethered viral 3B cooperate to recruit viral RNA dependent RNA polymerase 3D (pol). Sci Rep. 2017;7:17309. PubMed PMC

Rozycki B, Boura E. Large, dynamic, multi‐protein complexes: A challenge for structural biology. J Phys Condens Matter. 2014;26:463103. PubMed

Peti W, Page R, Boura E, Rozycki B. Structures of dynamic protein complexes: Hybrid techniques to study MAP kinase complexes and the ESCRT system. Methods Mol Biol. 2018;1688:375–389. PubMed PMC

Klima M, Baumlova A, Chalupska D, et al. The high‐resolution crystal structure of phosphatidylinositol 4‐kinase IIbeta and the crystal structure of phosphatidylinositol 4‐kinase IIalpha containing a nucleoside analogue provide a structural basis for isoform‐specific inhibitor design. Acta Crystallogr. 2015;D71:1555–1563. PubMed

Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. PRIMUS: A windows PC‐based system for small‐angle scattering data analysis. J Appl Cryst. 2003;36:1277–1282.

Kim YC, Hummer G. Coarse‐grained models for simulations of multiprotein complexes: Application to ubiquitin binding. J Mol Biol. 2008;375:1416–1433. PubMed PMC

Boura E, Rozycki B, Herrick DZ, et al. Solution structure of the ESCRT‐I complex by small‐angle X‐ray scattering, EPR and FRET spectroscopy. Proc Natl Acad Sci U S A. 2011;108:9437–9442. PubMed PMC

Boura E, Hurley JH. Structural basis for membrane targeting by the MVB12‐associated beta‐prism domain of the human ESCRT‐I MVB12 subunit. Proc Natl Acad Sci U S A. 2012;109:1901–1906. PubMed PMC

Rozycki B, Kim YC, Hummer G. SAXS ensemble refinement of ESCRT‐III CHMP3 conformational transitions. Structure. 2011;19:109–116. PubMed PMC

Leonard TA, Rozycki B, Saidi LF, Hummer G, Hurley JH. Crystal structure and allosteric activation of protein kinase C betaII. Cell. 2011;144:55–66. PubMed PMC

Francis DM, Rozycki B, Koveal D, Hummer G, Page R, Peti W. Structural basis of p38alpha regulation by hematopoietic tyrosine phosphatase. Nat Chem Biol. 2011;7:916–924. PubMed PMC

Francis DM, Rozycki B, Tortajada A, Hummer G, Peti W, Page R. Resting and active states of the ERK2:HePTP complex. J Am Chem Soc. 2011;133:17138–17141. PubMed PMC

Rozycki B, Cieplak M, Czjzek M. Large conformational fluctuations of the multi‐domain xylanase Z of clostridium thermocellum. J Struct Biol. 2015;191:68–75. PubMed

Rozycki B, Cazade PA, O'Mahony S, Thompson D, Cieplak M. The length but not the sequence of peptide linker modules exerts the primary influence on the conformations of protein domains in cellulosome multi‐enzyme complexes. Phys Chem Chem Phys. 2017;19:21414–21425. PubMed

Chalupska D, Eisenreichova A, Rozycki B, et al. Structural analysis of phosphatidylinositol 4‐kinase IIIbeta (PI4KB) ‐ 14‐3‐3 protein complex reveals internal flexibility and explains 14‐3‐3 mediated protection from degradation in vitro. J Struct Biol. 2017;200:36–44. PubMed

Chalupska D, Rozycki B, Humpolickova J, Faltova L, Klima M, Boura E. Phosphatidylinositol 4‐kinase IIIbeta (PI4KB) forms highly flexible heterocomplexes that include ACBD3, 14‐3‐3, and Rab11 proteins. Sci Rep. 2019;9:567. PubMed PMC

Steinkuhler J, Rozycki B, Alvey C, et al. Membrane fluctuations and acidosis regulate cooperative binding of ‘marker of self’ protein CD47 with the macrophage checkpoint receptor SIRPα. J Cell Sci. 2018;132(4):jcs216770. PubMed PMC

Suveges D, Gaspari Z, Toth G, Nyitray L. Charged single alpha‐helix: A versatile protein structural motif. Proteins. 2009;74:905–916. PubMed

Fiser A, Sali A. ModLoop: Automated modeling of loops in protein structures. Bioinformatics. 2003;19:2500–2501. PubMed

Boura E, Rozycki B, Chung HS, et al. Solution structure of the ESCRT‐I and ‐II supercomplex: Implications for membrane budding and scission. Structure. 2012;20:874–886. PubMed PMC

Greninger AL, Knudsen GM, Betegon M, Burlingame AL, DeRisi JL. ACBD3 interaction with TBC1 domain 22 protein is differentially affected by enteroviral and kobuviral 3A protein binding. MBio. 2013;4:e00098–13. PubMed PMC

Ishikawa‐Sasaki K, Sasaki J, Taniguchi K. A complex comprising phosphatidylinositol 4‐kinase IIIbeta, ACBD3, and Aichi virus proteins enhances phosphatidylinositol 4‐phosphate synthesis and is critical for formation of the viral replication complex. J Virol. 2014;88:6586–6598. PubMed PMC

Lei X, Xiao X, Zhang Z, et al. The Golgi protein ACBD3 facilitates enterovirus 71 replication by interacting with 3A. Sci Rep. 2017;7:44592. PubMed PMC

Lyoo H, van der Schaar HM, Dorobantu CM, Rabouw HH, Strating J, van Kuppeveld FJM. ACBD3 is an essential pan‐enterovirus host factor that mediates the interaction between viral 3A protein and cellular protein PI4KB. MBio. 2019;10:e02742–18. PubMed PMC

Mejdrova I, Chalupska D, Kogler M, et al. Highly selective phosphatidylinositol 4‐kinase IIIbeta inhibitors and structural insight into their mode of action. J Med Chem. 2015;58:3767–3793. PubMed

Mejdrova I, Chalupska D, Plackova P, et al. Rational design of novel highly potent and selective phosphatidylinositol 4‐kinase IIIbeta (PI4KB) inhibitors as broad‐spectrum antiviral agents and tools for chemical biology. J Med Chem. 2017;60:100–118. PubMed

Rutaganira FU, Fowler ML, McPhail JA, et al. Design and structural characterization of potent and selective inhibitors of phosphatidylinositol 4 kinase IIIbeta. J Med Chem. 2016;59:1830–1839. PubMed PMC

Humpolickova J, Mejdrova I, Matousova M, Nencka R, Boura E. Fluorescent inhibitors as tools to characterize enzymes: Case study of the lipid kinase phosphatidylinositol 4‐kinase IIIbeta (PI4KB). J Med Chem. 2017;60:119–127. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...