Ebola virus VP35 interaction with dynein LC8 regulates viral RNA synthesis

Journal of Virology

Volumn 89, Issue 9, 2015, Pages 5148-5153

  Luthra, Priya ^a   Jordan, David S ^b   Leung, Daisy W ^b   Amarasinghe, Gaya K ^b   Basler, Christopher F ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CYTOPLASMIC DYNEIN; CYTOPLASMIC DYNEIN LIGHT CHAIN 8; DIMER; PROTEIN VP35; TETRAMER; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA; DYNLL1 PROTEIN, HUMAN; PROTEIN BINDING; VP35 PROTEIN, FILOVIRUS;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; EBOLA VIRUS; GENE MUTATION; GENE OVEREXPRESSION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA SYNTHESIS; VIRUS GENOME; VIRUS MUTANT; VIRUS REPLICATION; VIRUS TRANSCRIPTION; BIOSYNTHESIS; EBOLAVIRUS; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN ANALYSIS;

EBOLA VIRUS;

CYTOPLASMIC DYNEINS; DNA MUTATIONAL ANALYSIS; EBOLAVIRUS; HOST-PATHOGEN INTERACTIONS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RNA, VIRAL; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS REPLICATION;

EID: 84928556586     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03652-14     Document Type: Article

References (33)

1. Basler CF, Wang X, Mühlberger E, Volchkov V, Paragas J, Klenk HD, García-Sastre A, Palese P. 2000. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc Natl Acad Sci USA 97:12289-12294. http://dx.doi.org/10.1073/pnas.220398297.
2. Leung DW, Prins KC, Basler CF, Amarasinghe GK. 2010. Ebolavirus VP35 is a multifunctional virulence factor. Virulence 1:526-531. http://dx.doi.org/10.4161/viru.1.6.12984.
3. Leung DW, Ginder ND, Fulton DB, Nix J, Basler CF, Honzatko RB, Amarasinghe GK. 2009. Structure of the Ebola VP35 interferon inhibitory domain. Proc Natl Acad Sci USA 106:411-416. http://dx.doi.org/10.1073/pnas.0807854106.
4. Reid SP, Cardenas WB, Basler CF. 2005. Homo-oligomerization facilitates the interferon-antagonist activity of the ebolavirus VP35 protein. Virology 341:179-189. http://dx.doi.org/10.1016/j.virol.2005.06.044.
5. Basler CF, Mikulasova A, Martinez-Sobrido L, Paragas J, Mühlberger E, Bray M, Klenk HD, Palese P, Garcia-Sastre A. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J Virol 77:7945-7956. http://dx.doi.org/10.1128/JVI.77.14.7945-7956.2003.
6. Hartman AL, Towner JS, Nichol ST. 2004. A C-terminal basic amino acid motif of Zaire ebolavirus VP35 is essential for type I interferon antagonism and displays high identity with the RNA-binding domain of another interferon antagonist, the NS1 protein of influenza A virus. Virology 328:177-184. http://dx.doi.org/10.1016/j.virol.2004.07.006.
7. Cardenas WB, Loo YM, Gale M, Jr, Hartman AL, Kimberlin CR, Martinez-Sobrido L, Saphire EO, Basler CF. 2006. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J Virol 80:5168-5178. http://dx.doi.org/10.1128/JVI.02199-05.
8. Luthra P, Ramanan P, Mire CE, Weisend C, Tsuda Y, Yen B, Liu G, Leung DW, Geisbert TW, Ebihara H, Amarasinghe GK, Basler CF. 2013. Mutual antagonism between the Ebola virus VP35 protein and the RIG-I activator PACT determines infection outcome. Cell Host Microbe 14:74-84. http://dx.doi.org/10.1016/j.chom.2013.06.010.
9. Prins KC, Cardenas WB, Basler CF. 2009. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKKepsilon and TBK-1. J Virol 83:3069-3077. http://dx.doi.org/10.1128/JVI.01875-08.
10. Muhlberger E, Lötfering B, Klenk HD, Becker S. 1998. Three of the four nucleocapsid proteins of Marburg virus, NP, VP35, and L, are sufficient to mediate replication and transcription of Marburg virus-specific monocistronic minigenomes. J Virol 72:8756-8764.
11. Mühlberger E, Weik M, Volchkov VE, Klenk HD, Becker S. 1999. Comparison of the transcription and replication strategies of Marburg virus and Ebola virus by using artificial replication systems. J Virol 73: 2333-2342.
12. DiCarlo A, Moller P, Lander A, Kolesnikova L, Becker S. 2007. Nucleocapsid formation and RNA synthesis of Marburg virus is dependent on two coiled coil motifs in the nucleoprotein. Virol J 4:105. http://dx.doi.org/10.1186/1743-422X-4-105.
13. Becker S, Rinne C, Hofsass U, Klenk HD, Mühlberger E. 1998. Interactions of Marburg virus nucleocapsid proteins. Virology 249:406-417. http://dx.doi.org/10.1006/viro.1998.9328.
14. Groseth A, Charton JE, Sauerborn M, Feldmann F, Jones SM, Hoenen T, Feldmann H. 2009. The Ebola virus ribonucleoprotein complex: a novel VP30-L interaction identified. Virus Res 140:8-14. http://dx.doi.org/10.1016/j.virusres.2008.10.017.
15. Kubota T, Matsuoka M, Chang TH, Bray M, Jones S, Tashiro M, Kato A, Ozato K. 2009. Ebolavirus VP35 interacts with the cytoplasmic dynein light chain 8. J Virol 83:6952-6956. http://dx.doi.org/10.1128/JVI.00480-09.
16. King SM, Barbarese E, Dillman JF, III, Benashski SE, Do KT, Patel-King RS, Pfister KK. 1998. Cytoplasmic dynein contains a family of differentially expressed light chains. Biochemistry 37:15033-15041. http://dx.doi.org/10.1021/bi9810813.
17. Rodriguez-Crespo I, Yelamos B, Roncal F, Albar JP, Ortiz de Montellano PR, Gavilanes F. 2001. Identification of novel cellular proteins that bind to the LC8 dynein light chain using a pepscan technique. FEBS Lett 503:135-141. http://dx.doi.org/10.1016/S0014-5793(01)02718-1.
18. Martinez-Moreno M, Navarro-Lerida I, Roncal F, Albar JP, Alonso C, Gavilanes F, Rodriguez-Crespo I. 2003. Recognition of novel viral sequences that associate with the dynein light chain LC8 identified through a pepscan technique. FEBS Lett 544:262-267. http://dx.doi.org/10.1016/S0014-5793(03)00516-7.
19. Garcia-Mayoral MF, Rodriguez-Crespo I, Bruix M. 2011. Structural models of DYNLL1 with interacting partners: African swine fever virus protein p54 and postsynaptic scaffolding protein gephyrin. FEBS Lett 585: 53-57. http://dx.doi.org/10.1016/j.febslet.2010.11.027.
20. Lo KW, Naisbitt S, Fan JS, Sheng M, Zhang M. 2001. The 8-kDa dynein light chain binds to its targets via a conserved (K/R)XTQT motif. J Biol Chem 276:14059-14066. http://dx.doi.org/10.1074/jbc. M010320200.
21. Pichlmair A, Kandasamy K, Alvisi G, Mulhern O, Sacco R, Habjan M, Binder M, Stefanovic A, Eberle CA, Goncalves A, Burckstummer T, Muller AC, Fauster A, Holze C, Lindsten K, Goodbourn S, Kochs G, Weber F, Bartenschlager R, Bowie AG, Bennett KL, Colinge J, Superti-Furga G. 2012. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 487:486-490. http://dx.doi.org/10.1038/nature11289.
22. Benashski SE, Harrison A, Patel-King RS, King SM. 1997. Dimerization of the highly conserved light chain shared by dynein and myosin V J Biol Chem 272:20929-20935.
23. Wang W, Lo KW, Kan HM, Fan JS, Zhang M. 2003. Structure of the monomeric 8-kDa dynein light chain and mechanism of the domainswapped dimer assembly. J Biol Chem 278:41491-41499. http://dx.doi.org/10.1074/jbc. M307118200.
24. Hoenen T, Jung S, Herwig A, Groseth A, Becker S. 2010. Both matrix proteins of Ebola virus contribute to the regulation of viral genome replication and transcription. Virology 403:56-66. http://dx.doi.org/10.1016/j.virol.2010.04.002.
25. Tarbouriech N, Curran J, Ebel C, Ruigrok RW, Burmeister WP. 2000. On the domain structure and the polymerization state of the Sendai virus P protein. Virology 266:99-109. http://dx.doi.org/10.1006/viro.1999.0066.
26. Tarbouriech N, Curran J, Ruigrok RW, Burmeister WP. 2000. Tetrameric coiled coil domain of Sendai virus phosphoprotein. Nat Struct Biol 7:777-781. http://dx.doi.org/10.1038/79013.
27. Becker S, Mühlberger E. 1999. Co-and posttranslational modifications and functions of Marburg virus proteins. Curr Topics Microbiol Immunol 235:23-34.
28. Merino-Gracia J, Garcia-Mayoral MF, Rodriguez-Crespo I. 2011. The association of viral proteins with host cell dynein components during virus infection. FEBS J 278:2997-3011. http://dx.doi.org/10.1111/j.1742-4658.2011.08252.x.
29. Alonso C, Miskin J, Hernaez B, Fernandez-Zapatero P, Soto L, Canto C, Rodriguez-Crespo I, Dixon L, Escribano JM. 2001. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J Virol 75:9819-9827. http://dx.doi.org/10.1128/JVI.75.20.9819-9827.2001.
30. Douglas MW, Diefenbach RJ, Homa FL, Miranda-Saksena M, Rixon FJ, Vittone V, Byth K, Cunningham AL. 2004. Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport. J Biol Chem 279:28522-28530. http://dx.doi.org/10.1074/jbc. M311671200.
31. Schneider MA, Spoden GA, Florin L, Lambert C. 2011. Identification of the dynein light chains required for human papillomavirus infection. Cell Microbiol 13:32-46. http://dx.doi.org/10.1111/j.1462-5822.2010.01515.x.
32. Raux H, Flamand A, Blondel D. 2000. Interaction of the rabies virus P protein with the LC8 dynein light chain. J Virol 74:10212-10216. http://dx.doi.org/10.1128/JVI.74.21.10212-10216.2000.
33. Tan GS, Preuss MA, Williams JC, Schnell MJ. 2007. The dynein light chain 8 binding motif of rabies virus phosphoprotein promotes efficient viral transcription. Proc Natl Acad SciUS A 104:7229-7234. http://dx.doi.org/10.1073/pnas.0701397104.