Membrane Remodeling by the Double-Barrel Scaffolding Protein of Poxvirus

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In contrast to most enveloped viruses, poxviruses produce infectious particles that do not acquire their internal lipid membrane by budding through cellular compartments. Instead, poxvirus immature particles are generated from atypical crescent-shaped precursors whose architecture and composition remain contentious. Here we describe the 2.6 Å crystal structure of vaccinia virus D13, a key structural component of the outer scaffold of viral crescents. D13 folds into two jellyrolls decorated by a head domain of novel fold. It assembles into trimers that are homologous to the double-barrel capsid proteins of adenovirus and lipid-containing icosahedral viruses. We show that, when tethered onto artificial membranes, D13 forms a honeycomb lattice and assembly products structurally similar to the viral crescents and immature particles. The architecture of the D13 honeycomb lattice and the lipid-remodeling abilities of D13 support a model of assembly that exhibits similarities with the giant mimivirus. Overall, these findings establish that the first committed step of poxvirus morphogenesis utilizes an ancestral lipid-remodeling strategy common to icosahedral DNA viruses infecting all kingdoms of life. Furthermore, D13 is the target of rifampicin and its structure will aid the development of poxvirus assembly inhibitors.

Vyšlo v časopise: Membrane Remodeling by the Double-Barrel Scaffolding Protein of Poxvirus. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002239
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002239

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Zdroje

1. MooreZSSewardJFLaneJM 2006 Smallpox. Lancet 367 425 435 doi:10.1016/S0140-6736(06)68143-9

2. ConditRCMoussatcheNTraktmanP 2006 In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66 31 124 doi:10.1016/S0065-3527(06)66002-8

3. LaliberteJPMossB 2010 Lipid Membranes in Poxvirus Replication. Viruses 2 972 986 doi:10.3390/v2040972

4. CyrklaffMRiscoCFernándezJJJiménezMVEstebanM 2005 Cryo-electron tomography of vaccinia virus. Proc Natl Acad Sci U S A 102 2772 2777 doi:10.1073/pnas.0409825102

5. DalesSMosbachEH 1968 Vaccinia as a model for membrane biogenesis. Virology 35 564 583

6. ChichónFJRodríguezMJRiscoCFraile-RamosAFernándezJJ 2009 Membrane remodeling during vaccinia virus morphogenesis. Biol Cell 101 401 414 doi:10.1042/BC20080176

7. ChlandaPCarbajalMACyrklaffMGriffithsGKrijnse-LockerJ 2009 Membrane rupture generates single open membrane sheets during vaccinia virus assembly. Cell Host Microbe 6 81 90 doi:10.1016/j.chom.2009.05.021

8. HeuserJ 2005 Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic “honeycomb” surface coat. J of Cell Biol 169 269 283 doi:10.1083/jcb.200412169

9. SzajnerPWeisbergASLebowitzJHeuserJMossB 2005 External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J of Cell Biol 170 971 981 doi:10.1083/jcb.200504026

10. BishtHWeisbergASSzajnerPMossB 2009 Assembly and disassembly of the capsid-like external scaffold of immature virions during vaccinia virus morphogenesis. J Virol 83 9140 9150 doi:10.1128/JVI.00875-09

11. MossBRosenblumENKatzEGrimleyPM 1969 Rifampicin: a specific inhibitor of vaccinia virus assembly. Nature 224 1280 1284

12. HyunJ-KCoulibalyFTurnerAPBakerENMercerAA 2007 The structure of a putative scaffolding protein of immature poxvirus particles as determined by electron microscopy suggests similarity with capsid proteins of large icosahedral DNA viruses. J Virol 81 11075 11083 doi:10.1128/JVI.00594-07

13. NandhagopalNSimpsonAAGurnonJRYanXBakerTS 2002 The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc Natl Acad Sci U S A 99 14758 14763 doi:10.1073/pnas.232580699

14. IyerLMBalajiSKooninEVAravindL 2006 Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117 156 184 doi:10.1016/j.virusres.2006.01.009

15. BensonSDBamfordJKBamfordDHBurnettRM 1999 Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98 825 833

16. AbresciaNGAGrimesJMKiveläHMAssenbergRSuttonGC 2008 Insights into Virus Evolution and Membrane Biogenesis from the Structure of the Marine Lipid-Containing Bacteriophage PM2. Mol Cell 31 749 761 doi:10.1016/j.molcel.2008.06.026

17. KhayatRTangLLarsonETLawrenceCMYoungM 2005 Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc Natl Acad Sci U S A 102 18944 18949 doi:10.1073/pnas.0506383102

18. RobertsMMWhiteJLGrütterMGBurnettRM 1986 Three-dimensional structure of the adenovirus major coat protein hexon. Science 232 1148 1151

19. BamfordDHGrimesJMStuartDI 2005 What does structure tell us about virus evolution? Curr Opin Struct Biol 15 655 663 doi:10.1016/j.sbi.2005.10.012

20. BensonSDBamfordJKHBamfordDHBurnettRM 2004 Does common architecture reveal a viral lineage spanning all three domains of life? Mol Cell 16 673 685 doi:10.1016/j.molcel.2004.11.016

21. LepaultJPetitpasIErkINavazaJBigotD 2001 Structural polymorphism of the major capsid protein of rotavirus. EMBO J 20 1498 1507 doi:10.1093/emboj/20.7.1498

22. BahadurRPRodierFJaninJ 2007 A dissection of the protein-protein interfaces in icosahedral virus capsids. J Mol Biol 367 574 590 doi:10.1016/j.jmb.2006.12.054

23. CharityJCKatzEMossB 2007 Amino acid substitutions at multiple sites within the vaccinia virus D13 scaffold protein confer resistance to rifampicin. Virology 359 227 232 doi:10.1016/j.virol.2006.09.031

24. SodeikBGriffithsGEricssonMMossBDomsRW 1994 Assembly of vaccinia virus: effects of rifampin on the intracellular distribution of viral protein p65. J Virol 68 1103 1114

25. XiaoCKuznetsovYGSunSHafensteinSLKostyuchenkoVA 2009 Structural studies of the giant mimivirus. PLoS Biol 7 e92 doi:10.1371/journal.pbio.1000092

26. KabschW 2010 XDS. Acta Crystallogr D Biol Crystallogr 66 125 132 doi:10.1107/S0907444909047337

27. MinorWCymborowskiMOtwinowskiZChruszczM 2006 HKL-3000: the integration of data reduction and structure solution—from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62 859 866 doi:10.1107/S0907444906019949

28. WinnMDBallardCCCowtanKDDodsonEJEmsleyP 2011 Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67 235 242 doi:10.1107/S0907444910045749

29. SheldrickGM 2008 A short history of SHELX. Acta Crystallographica Section A: Foundations of Crystallography 64 112 122 doi:10.1107/S0108767307043930

30. VonrheinCBlancERoversiPBricogneG 2007 Automated structure solution with autoSHARP. Methods Mol Biol 364 215 230 doi:10.1385/1-59745-266-1 : 215

31. LangerGCohenSXLamzinVSPerrakisA 2008 Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3 1171 1179 doi:10.1038/nprot.2008.91

32. EmsleyPLohkampBScottWGCowtanK 2010 Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66 486 501 doi:10.1107/S0907444910007493

33. BlancERoversiPVonrheinCFlensburgCLeaSM 2004 Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60 2210 2221 doi:10.1107/S0907444904016427

34. ChenVBArendallWBHeaddJJKeedyDAImmorminoRM 2010 MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66 12 21 doi:10.1107/S0907444909042073

35. AdamsPDAfoninePVBunkócziGChenVBDavisIW 2010 PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66 213 221 doi:10.1107/S0907444909052925

36. WatanabeJAsakaYMinoKKanamuraS 1996 Preparation of liposomes that mimic the membrane of endoplasmic reticulum of rat hepatocytes. J Electron Microsc (Tokyo) 45 171 176

37. LévyDMosserGLambertOMoeckGSBaldD 1999 Two-dimensional crystallization on lipid layer: A successful approach for membrane proteins. J Struct Biol 127 44 52 doi:10.1006/jsbi.1999.4155

38. HeymannJBBelnapDM 2007 Bsoft: image processing and molecular modeling for electron microscopy. J Struct Biol 157 3 18 doi:10.1016/j.jsb.2006.06.006

39. CrowtherRAHendersonRSmithJM 1996 MRC image processing programs. J Struct Biol 116 9 16 doi:10.1006/jsbi.1996.0003

40. PettersenEFGoddardTDHuangCCCouchGSGreenblattDM 2004 UCSF Chimera—a visualization system for exploratory research and analysis. Journal Comput Chem 25 1605 1612 doi:10.1002/jcc.20084

41. KleywegtGJReadRJ 1997 Not your average density. Structure 5 1557 1569

42. WriggersWBirmannsS 2001 Using situs for flexible and rigid-body fitting of multiresolution single-molecule data. J Struct Biol 133 193 202 doi:10.1006/jsbi.2000.4350

43. KrissinelEHenrickK 2007 Inference of macromolecular assemblies from crystalline state. J Mol Biol 372 774 797 doi:10.1016/j.jmb.2007.05.022

44. KrissinelEHenrickK 2004 Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60 2256 2268 doi:10.1107/S0907444904026460

45. AshkenazyHErezEMartzEPupkoTBen-TalN 2010 ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38 W529 33 doi:10.1093/nar/gkq399