Structure of the Low pH Conformation of Chandipura Virus G Reveals Important Features in the Evolution of the Vesiculovirus Glycoprotein

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-19

  Baquero, Eduard ^a   Albertini, Aurélie A ^a   Raux, Hélène ^a   Buonocore, Linda ^b   Rose, John K ^b   Bressanelli, Stéphane ^a   Gaudin, Yves ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHANDIPURA VIRUS GLYCOPROTEIN G; GREEN FLUORESCENT PROTEIN; PLECKSTRIN; UNCLASSIFIED DRUG; VESICULOVIRUS GLYCOPROTEIN G; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; BHK CELL LINE; CELL FUSION; CHANDIPURA VIRUS; CRYSTALLIZATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MEMBRANE FLOTATION ASSAY; NONHUMAN; OLIGOMERIZATION; PH; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; VESICULOVIRUS; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PROTEIN TERTIARY STRUCTURE; VIRUS NUCLEOCAPSID;

CHANDIPURA VIRUS; VESICULAR STOMATITIS VIRUS; VESICULOVIRUS;

EVOLUTION, MOLECULAR; HUMANS; HYDROGEN-ION CONCENTRATION; NUCLEOCAPSID; PROTEIN STRUCTURE, TERTIARY; VESICULOVIRUS; VIRAL FUSION PROTEINS;

EID: 84926456786     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004756     Document Type: Article

References (45)

1. Dhanda V, Rodrigues FM, Ghosh SN, (1970) Isolation of Chandipura virus from sandflies in Aurangabad. Indian J Med Res 58: 179–180. 5528233
2. Mavale MS, Fulmali PV, Geevarghese G, Arankalle VA, Ghodke YS, et al. (2006) Venereal transmission of Chandipura virus by Phlebotomus papatasi (Scopoli). Am J Trop Med Hyg 75: 1151–1152. 17172384
3. Sudeep AB, Bondre VP, Gurav YK, Gokhale MD, Sapkal GN, et al. (2014) Isolation of Chandipura virus (Vesiculovirus: Rhabdoviridae) from Sergentomyia species of sandflies from Nagpur, Maharashtra, India. Indian J Med Res 139: 769–772. 25027088
4. Menghani S, Chikhale R, Raval A, Wadibhasme P, Khedekar P, (2012) Chandipura Virus: an emerging tropical pathogen. Acta Trop 124: 1–14. doi: 10.1016/j.actatropica.2012.06.001 22721825
5. Cherian SS, Gunjikar RS, Banerjee A, Kumar S, Arankalle VA, (2012) Whole genomes of Chandipura virus isolates and comparative analysis with other rhabdoviruses. PLoS One 7: e30315. doi: 10.1371/journal.pone.0030315 22272333
6. Masters PS, Bhella RS, Butcher M, Patel B, Ghosh HP, et al. (1989) Structure and expression of the glycoprotein gene of Chandipura virus. Virology 171: 285–290. 2741347
7. Albertini AA, Baquero E, Ferlin A, Gaudin Y, (2012) Molecular and cellular aspects of rhabdovirus entry. Viruses 4: 117–139. doi: 10.3390/v4010117 22355455
8. Finkelshtein D, Werman A, Novick D, Barak S, Rubinstein M, (2013) LDL receptor and its family members serve as the cellular receptors for vesicular stomatitis virus. Proc Natl Acad Sci U S A 110: 7306–7311. doi: 10.1073/pnas.1214441110 23589850
9. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP, (2009) Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5: e1000394. doi: 10.1371/journal.ppat.1000394 19390604
10. Johannsdottir HK, Mancini R, Kartenbeck J, Amato L, Helenius A, (2009) Host cell factors and functions involved in vesicular stomatitis virus entry. J Virol 83: 440–453. doi: 10.1128/JVI.01864-08 18971266
11. Doms RW, Keller DS, Helenius A, Balch WE, (1987) Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J Cell Biol 105: 1957–1969. 2824524
12. Libersou S, Albertini AA, Ouldali M, Maury V, Maheu C, et al. (2010) Distinct structural rearrangements of the VSV glycoprotein drive membrane fusion. J Cell Biol 191: 199–210. doi: 10.1083/jcb.201006116 20921141
13. Durrer P, Gaudin Y, Ruigrok RW, Graf R, Brunner J, (1995) Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. J Biol Chem 270: 17575–17581. 7615563
14. Gaudin Y, Tuffereau C, Segretain D, Knossow M, Flamand A, (1991) Reversible conformational changes and fusion activity of rabies virus glycoprotein. J Virol 65: 4853–4859. 1870204
15. Albertini AA, Merigoux C, Libersou S, Madiona K, Bressanelli S, et al. (2012) Characterization of Monomeric Intermediates during VSV Glycoprotein Structural Transition. PLoS Pathog 8: e1002556. doi: 10.1371/journal.ppat.1002556 22383886
16. Roche S, Gaudin Y, (2002) Characterization of the equilibrium between the native and fusion-inactive conformation of rabies virus glycoprotein indicates that the fusion complex is made of several trimers. Virology 297: 128–135. 12083843
17. Carr CM, Chaudhry C, Kim PS, (1997) Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc Natl Acad Sci U S A 94: 14306–14313. 9405608
18. Gaudin Y, (2000) Reversibility in fusion protein conformational changes. The intriguing case of rhabdovirus-induced membrane fusion. Subcell Biochem 34: 379–408. 10808339
19. Roche S, Bressanelli S, Rey FA, Gaudin Y, (2006) Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313: 187–191. 16840692
20. Roche S, Rey FA, Gaudin Y, Bressanelli S, (2007) Structure of the prefusion form of the vesicular stomatitis virus glycoprotein g. Science 315: 843–848. 17289996
21. Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, et al. (2006) Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313: 217–220. 16840698
22. Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM, (2008) The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 15: 1024–1030. doi: 10.1038/nsmb.1484 18776902
23. Backovic M, Jardetzky TS, (2009) Class III viral membrane fusion proteins. Curr Opin Struct Biol 19: 189–196. doi: 10.1016/j.sbi.2009.02.012 19356922
24. Baquero E, Albertini AA, Vachette P, Lepault J, Bressanelli S, et al. (2013) Intermediate conformations during viral fusion glycoprotein structural transition. Curr Opin Virol 3: 143–150. doi: 10.1016/j.coviro.2013.03.006 23562213
25. Ferlin A, Raux H, Baquero E, Lepault J, Gaudin Y (2014) Characterization of pH sensitive molecular switches triggering the structural transition of VSV Glycoprotein from the post- toward the pre-fusion state. J Virol.
26. Baquero E, Buonocore L, Rose JK, Bressanelli S, Gaudin Y, et al. (2012) Crystallization and preliminary X-ray analysis of Chandipura virus glycoprotein G. Acta Crystallogr Sect F Struct Biol Cryst Commun 68: 1094–1097. doi: 10.1107/S1744309112030151 22949203
27. Pasdeloup D, Poisson N, Raux H, Gaudin Y, Ruigrok RW, et al. (2005) Nucleocytoplasmic shuttling of the rabies virus P protein requires a nuclear localization signal and a CRM1-dependent nuclear export signal. Virology 334: 284–293. 15780878
28. Desmezieres E, Maillard AP, Gaudin Y, Tordo N, Perrin P, (2003) Differential stability and fusion activity of Lyssavirus glycoprotein trimers. Virus Res 91: 181–187. 12573496
29. Rose NF, Roberts A, Buonocore L, Rose JK, (2000) Glycoprotein exchange vectors based on vesicular stomatitis virus allow effective boosting and generation of neutralizing antibodies to a primary isolate of human immunodeficiency virus type 1. J Virol 74: 10903–10910. 11069984
30. Chothia C, Lesk AM, (1986) The relation between the divergence of sequence and structure in proteins. EMBO J 5: 823–826. 3709526
31. Wood TC, Pearson WR, (1999) Evolution of protein sequences and structures. J Mol Biol 291: 977–995. 10452901
32. Benmansour A, Leblois H, Coulon P, Tuffereau C, Gaudin Y, et al. (1991) Antigenicity of rabies virus glycoprotein. J Virol 65: 4198–4203. 1712859
33. Kongsuwan K, Cybinski DH, Cooper J, Walker PJ, (1998) Location of neutralizing epitopes on the G protein of bovine ephemeral fever rhabdovirus. J Gen Virol 79 (Pt 11): 2573–2581. 9820132
34. Prehaud C, Coulon P, LaFay F, Thiers C, Flamand A, (1988) Antigenic site II of the rabies virus glycoprotein: structure and role in viral virulence. J Virol 62: 1–7. 2446011
35. Vandepol SB, Lefrancois L, Holland JJ, (1986) Sequences of the major antibody binding epitopes of the Indiana serotype of vesicular stomatitis virus. Virology 148: 312–325. 2417417
36. Olsson MHM, Soendergard CR, Rostkowski M, Jensen JH, (2011) PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa predictions. Journal of Chemical Theory and Computation 7: 525–537.
37. Marriott AC, (2005) Complete genome sequences of Chandipura and Isfahan vesiculoviruses. Arch Virol 150: 671–680. 15614433
38. Vasilakis N, Widen S, Travassos da Rosa AP, Wood TG, Walker PJ, et al. (2013) Malpais spring virus is a new species in the genus vesiculovirus. Virol J 10: 69. doi: 10.1186/1743-422X-10-69 23497016
39. DuBois RM, Vaney MC, Tortorici MA, Kurdi RA, Barba-Spaeth G, et al. (2013) Functional and evolutionary insight from the crystal structure of rubella virus protein E1. Nature 493: 552–556. doi: 10.1038/nature11741 23292515
40. Modis Y, (2014) Relating structure to evolution in class II viral membrane fusion proteins. Curr Opin Virol 5: 34–41. doi: 10.1016/j.coviro.2014.01.009 24525225
41. Kabsch W, (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125–132. doi: 10.1107/S0907444909047337 20124692
42. Vagin A, Teplyakov A, (2010) Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66: 22–25. doi: 10.1107/S0907444909042589 20057045
43. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213–221. doi: 10.1107/S0907444909052925 20124702
44. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486–501. doi: 10.1107/S0907444910007493 20383002
45. Terwilliger TC, Grosse-Kunstleve RW, Afonine PV, Moriarty NW, Adams PD, et al. (2008) Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias. Acta Crystallogr D Biol Crystallogr 64: 515–524. doi: 10.1107/S0907444908004319 18453687