Crystal structure of the oligomeric form of Lassa virus matrix protein Z

Journal of Virology

Volumn 90, Issue 9, 2016, Pages 4556-4562

  Hastie, Kathryn M ^a   Zandonatti, Michelle ^a   Liu, Tong ^b,c   Li, Sheng ^b   Woods, Virgil L ^b   Saphire, Erica Ollmann ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c SEQUENOM INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; MATRIX PROTEIN; MATRIX PROTEIN Z; MONOMER; OLIGOMER; PROTEIN P72; UNCLASSIFIED DRUG; CARRIER PROTEIN; HYBRID PROTEIN; PROTEIN Z, LASSA VIRUS;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; DNA TEMPLATE; DODECAMERIC FORM; HYDROGEN BOND; HYDROPHOBICITY; ISOMERIZATION; LASSA VIRUS; LIFE CYCLE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SIZE EXCLUSION CHROMATOGRAPHY; VIRUS ASSEMBLY; VIRUS EXPRESSION; VIRUS ISOLATION; VIRUS MORPHOLOGY; VIRUS PURIFICATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; MASS SPECTROMETRY; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION;

CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; LASSA VIRUS; MASS SPECTROMETRY; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL MATRIX PROTEINS;

EID: 84964978322     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02896-15     Document Type: Article

References (30)

1. Capul AA, Perez M, Burke E, Kunz S, Buchmeier MJ, de la Torre JC. 2007. Arenavirus Z-glycoprotein association requires Z myristoylation but not functional RING or late domains. J Virol 81:9451-9460. http://dx.doi.org/10.1128/JVI.00499-07.
2. Perez M, Craven RC, de la Torre JC. 2003. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100:12978-12983. http://dx.doi.org/10.1073/pnas.2133782100.
3. Strecker T, Eichler R, Meulen J, Weissenhorn W, Dieter Klenk H, Garten W, Lenz O. 2003. Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 77: 10700-10705. http://dx.doi.org/10.1128/JVI.77.19.10700-10705.2003.
4. Salvato MS, Schweighofer KJ, Burns J, Shimomaye EM. 1992. Biochemical and immunological evidence that the 11 kDa zinc-binding protein of lymphocytic choriomeningitis virus is a structural component of the virus. Virus Res 22:185-198. http://dx.doi.org/10.1016/0168-1702(92)90050-J.
5. Salvato MS, Shimomaye EM. 1989. The completed sequence of lymphocytic choriomeningitis virus reveals a uniqueRNAstructure and a gene for a zinc finger protein. Virology 173:1-10. http://dx.doi.org/10.1016/0042-6822(89)90216-X.
6. Campbell Dwyer EJ, Lai H, MacDonald RC, Salvato MS, Borden KL. 2000. The lymphocytic choriomeningitis virus RING protein Z associates with eukaryotic initiation factor 4E and selectively represses translation in a RING-dependent manner. J Virol 74:3293-3300. http://dx.doi.org/10.1128/JVI.74.7.3293-3300.2000.
7. Kentsis A, Dwyer EC, Perez JM, Sharma M, Chen A, Pan ZQ, Borden KL. 2001. The RING domains of the promyelocytic leukemia proteinPML and the arenaviral protein Z repress translation by directly inhibiting translation initiation factor eIF4E. J Mol Biol 312:609-623. http://dx.doi.org/10.1006/jmbi.2001.5003.
8. Cornu TI, de la Torre JC. 2001. RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replica-tion of an LCMV S-segment minigenome. J Virol 75:9415-9426. http://dx.doi.org/10.1128/JVI.75.19.9415-9426.2001.
9. Xing J, Ly H, Liang Y. 2015. The Z proteins of pathogenic but not nonpathogenic arenaviruses inhibit RIG-I-like receptor-dependent interferon production. J Virol 89:2944-2955. http://dx.doi.org/10.1128/JVI.03349-14.
10. Kentsis A, Gordon RE, Borden KL. 2002. Self-assembly properties of a model RING domain. Proc Natl Acad Sci U S A 99:667-672. http://dx.doi.org/10.1073/pnas.012317299.
11. Borden KL, Campbell Dwyer EJ, Carlile GW, Djavani M, Salvato MS. 1998. Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins. J Virol 72:3819-3826.
12. Volpon L, Osborne MJ, Capul AA, de la Torre JC, Borden KLB. 2010. Structural characterization of the Z RING-eIF4E complex reveals a distinct mode of control for eIF4E. Proc Natl Acad Sci U S A 107:5441-5446. http://dx.doi.org/10.1073/pnas.0909877107.
13. Volpon L, Osborne MJ, Borden KL. 2008. NMR assignment of the arenaviral protein Z from Lassa fever virus. BiomolNMRAssign 2:81-84. http://dx.doi.org/10.1007/s12104-008-9090-z.
14. Pflugrath JW. 1999. The finer things in X-ray diffraction data collection. Acta Crystallogr D Biol Crystallogr 55:1718-1725. http://dx.doi.org/10.1107/S090744499900935X.
15. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Pythonbased system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221. http://dx.doi.org/10.1107/S0907444909052925.
16. Panjikar SP, Lamzin VV, Weiss MS, Tucker PA. 2009. On the combination of molecular replacement and single anomalous diffraction phasing for automated structure determination. Acta Crystallogr D Biol Crystallogr 65:1089-1097. http://dx.doi.org/10.1107/S0907444909029643.
17. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486-501. http://dx.doi.org/10.1107/S0907444910007493.
18. Li S, Tsalkova T, White MA, Mei FC, Liu T, Wang D, Woods VL, Jr, Cheng X. 2011. Mechanism of intracellular cAMP sensor Epac2 activation: cAMP-induced conformational changes identified by amide hydrogen/deuterium exchange mass spectrometry (DXMS). J Biol Chem 286: 17889-17897. http://dx.doi.org/10.1074/jbc.M111.224535.
19. Hsu S, Kim Y, Li S, Durrant ES, Pace RM, Woods VL, Jr, Gentry MS. 2009. Structural insights into glucan phosphatase dynamics using amide hydrogen-deuterium exchange mass spectrometry. Biochemistry 48: 9891-9902. http://dx.doi.org/10.1021/bi9008853.
20. Hamuro Y, Anand GS, Kim JS, Juliano C, Stranz DD, Taylor SS, Woods VL, Jr. 2004. Mapping intersubunit interactions of the regulatory subunit (RIalpha) in the type I holoenzyme of protein kinase A by amide hydrogen/deuterium exchange mass spectrometry (DXMS). J Mol Biol 340: 1185-1196. http://dx.doi.org/10.1016/j.jmb.2004.05.042.
21. Zhang Z, Smith DL. 1993. Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci 2:522-531.
22. Kentsis A, Gordon RE, Borden KL. 2002. Control of biochemical reactions through supramolecular RING domain self-assembly. Proc Natl Acad Sci U S A 99:15404-15409. http://dx.doi.org/10.1073/pnas.202608799.
23. Gomis-Ruth FX, Dessen A, Timmins J, Bracher A, Kolesnikowa L, Becker S, Klenk HD, Weissenhorn W. 2003. The matrix protein VP40 from Ebola virus octamerizes into pore-like structures with specific RNA binding properties. Structure 11:423-433. http://dx.doi.org/10.1016/S0969-2126(03)00050-9.
24. Neumann P, Lieber D, Meyer S, Dautel P, Kerth A, Kraus I, Garten W, Stubbs MT. 2009. Crystal structure of the Borna disease virus matrix protein (BDV-M) reveals ssRNA binding properties. Proc Natl Acad Sci U S A 106:3710-3715. http://dx.doi.org/10.1073/pnas.0808101106.
25. Kranzusch PJ, Whelan SP. 2011. Arenavirus Z protein controls viral RNA synthesis by locking a polymerase-promoter complex. Proc Natl Acad Sci U S A 108:19743-19748. http://dx.doi.org/10.1073/pnas.1112742108.
26. Bornholdt ZA, Noda T, Abelson DM, Halfmann P, Wood MR, Kawaoka Y, Saphire EO. 2013. Structural rearrangement of Ebola virus VP40 begets multiple functions in the virus life cycle. Cell 154:763-774. http://dx.doi.org/10.1016/j.cell.2013.07.015.
27. Capul AA, de la Torre JC, Buchmeier MJ. 2011. Conserved residues in Lassa fever virus Z protein modulate viral infectivity at the level of the ribonucleoprotein. J Virol 85:3172-3178. http://dx.doi.org/10.1128/JVI.02081-10.
28. Dessen A, Volchkov V, Dolnik O, Klenk HD, Weissenhorn W. 2000. Crystal structure of the matrix protein VP40 from Ebola virus. EMBO J 19:4228-4236. http://dx.doi.org/10.1093/emboj/19.16.4228.
29. Wen J, Arakawa T, Philo JS. 1996. Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Anal Biochem 240:155-166. http://dx.doi.org/10.1006/abio.1996.0345.
30. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad SciUSA98:10037-10041. http://dx.doi.org/10.1073/pnas.181342398.