Ribosomal protein S19-binding domain provides insights into hantavirus nucleocapsid protein-mediated translation initiation mechanism

Biochemical Journal

Volumn 464, Issue 1, 2014, Pages 109-121

  Ganaie, Safder S ^a   Haque, Absarul ^a   Cheng, Erdong ^a   Bonny, Tania S ^a   Salim, Nilshad N ^a   Mir, Mohammad A ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Haemorrhagic fever with renal syndrome; Hantavirus cardiopulmonary syndrome; Hantavirus nucleocapsid protein; Ribosomal protein S19; Viral translation control

Indexed keywords

GENOMIC RNA; MESSENGER RNA; NITROGEN; NUCLEOCAPSID PROTEIN; PROTEIN; PROTEIN S19; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; RIBOSOMAL PROTEIN S19;

ARTICLE; HANTAVIRUS; HANTAVIRUS INFECTION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RIBOSOME; RIBOSOME SUBUNIT; TRANSLATION INITIATION; WILD TYPE; AMINO ACID SEQUENCE; BINDING SITE; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RNA TRANSLATION;

HANTAVIRUS; SIN NOMBRE VIRUS;

AMINO ACID SEQUENCE; BINDING SITES; HANTAVIRUS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOCAPSID PROTEINS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RIBOSOMAL PROTEINS;

EID: 84908374907     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140449     Document Type: Article

References (36)

1. Klempa, B., Avsic-Zupanc, T., Clement, J., Dzagurova, T. K., Henttonen, H., Heyman, P., Jakab, F., Kruger, D. H., Maes, P., Papa, A. et al. (2013) Complex evolution and epidemiology of Dobrava-Belgrade hantavirus: definition of genotypes and their characteristics. Arch. Virol. 158, 521-529 CrossRef PubMed
2. Vaheri, A., Henttonen, H., Voutilainen, L., Mustonen, J., Sironen, T. and Vapalahti, O. (2013) Hantavirus infections in Europe and their impact on public health. Rev. Med. Virol. 23, 35-49 CrossRef PubMed
3. Schmaljohn, C. S. and Hooper, J. W. (2001) Bunyaviridae: the viruses and their replication. In Fields Virology, fourth edition (Knipe, D. M. and Howley, P. M., eds), pp. 1581-1602, Lippincott, Williams and Wilkins, Philadelphia
4. Hepojoki, J., Strandin, T., Lankinen, H. and Vaheri, A. (2012) Hantavirus structure - molecular interactions behind the scene. J. Gen. Virol. 93, 1631-1644 CrossRef PubMed
5. Battisti, A. J., Chu, Y. K., Chipman, P. R., Kaufmann, B., Jonsson, C. B. and Rossmann, M. G. (2011) Structural studies of hantaan virus. J. Virol. 85, 835-841 CrossRef PubMed
6. Alfadhli, A., Love, Z., Arvidson, B., Seeds, J., Willey, J. and Barklis, E. (2001) Hantavirus nucleocapsid protein oligomerization. J. Virol. 75, 2019-2023 CrossRef PubMed
7. Alfadhli, A., Steel, E., Finlay, L., Bachinger, H. P. and Barklis, E. (2002) Hantavirus nucleocapsid protein coiled-coil domains. J. Biol. Chem. 277, 27103-27108 CrossRef PubMed
8. Blakqori, G., Kochs, G., Haller, O. and Weber, F. (2003) Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J. Gen. Virol. 84, 1207-1214 CrossRef PubMed
9. Bridgen, A. and Elliott, R. M. (1996) Rescue of a segmented negative-strand RNA virus entirely from cloned complementary DNAs. Proc. Natl. Acad. Sci. U.S.A. 93, 15400-15404 CrossRef PubMed
10. Ikegami, T., Peters, C. J. and Makino, S. (2005) Rift valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. J. Virol. 79, 5606-5615 CrossRef PubMed
11. Kohl, A., Hart, T. J., Noonan, C., Royall, E., Roberts, L. O. and Elliott, R. M. (2004) A bunyamwera virus minireplicon system in mosquito cells. J. Virol. 78, 5679-5685 CrossRef PubMed
12. Mir, M. A., Brown, B., Hjelle, B., Duran, W. A. and Panganiban, A. T. (2006) Hantavirus N protein exhibits genus-specific recognition of the viral RNA panhandle. J. Virol. 80, 11283-11292 CrossRef PubMed
13. Mir, M. A., Duran, W. A., Hjelle, B. L., Ye, C. and Panganiban, A. T. (2008) Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc. Natl. Acad. Sci. U.S.A. 105, 19294-19299 CrossRef PubMed
14. Mir, M. A. and Panganiban, A. T. (2006) The bunyavirus nucleocapsid protein is an RNA chaperone: possible roles in viral RNA panhandle formation and genome replication. RNA 12, 272-282 CrossRef PubMed
15. Mir, M. A. and Panganiban, A. T. (2008) A protein that replaces the entire cellular eIF4F complex. EMBO J. 27, 3129-3139 CrossRef PubMed
16. Pinschewer, D. D., Perez, M. and de la Torre, J. C. (2003) Role of the virus nucleoprotein in the regulation of lymphocytic choriomeningitis virus transcription and RNA replication. J. Virol. 77, 3882-3887 CrossRef PubMed
17. Taylor, S. L., Frias-Staheli, N., Garcia-Sastre, A. and Schmaljohn, C. S. (2009) Hantaan virus nucleocapsid protein binds to importin α proteins and inhibits tumor necrosis factor α-induced activation of nuclear factor κB. J. Virol. 83, 1271-1279 CrossRef PubMed
18. Taylor, S. L., Krempel, R. L. and Schmaljohn, C. S. (2009) Inhibition of TNF-α-induced activation of NF-κB by hantavirus nucleocapsid proteins. Ann. N.Y. Acad. Sci. 1171 (Suppl. 1), E86-E93 CrossRef PubMed
19. Severson, W., Xu, X., Kuhn, M., Senutovitch, N., Thokala, M., Ferron, F., Longhi, S., Canard, B. and Jonsson, C. B. (2005) Essential amino acids of the hantaan virus N protein in its interaction with RNA. J. Virol. 79, 10032-10039 CrossRef PubMed
20. Mir, M. A. and Panganiban, A. T. (2010) The triplet repeats of the Sin Nombre hantavirus 5′ untranslated region are sufficient in cis for nucleocapsid-mediated translation initiation. J. Virol. 84, 8937-8944 CrossRef PubMed
21. Vera-Otarola, J., Soto-Rifo, R., Ricci, E. P., Ohlmann, T., Darlix, J. L. and Lopez-Lastra, M. (2010) The 3′ untranslated region of the Andes hantavirus small mRNA functionally replaces the poly(A) tail and stimulates cap-dependent translation initiation from the viral mRNA. J. Virol. 84, 10420-10424 CrossRef PubMed
22. Haque, A. and Mir, M. A. (2010) Interaction of hantavirus nucleocapsid protein with ribosomal protein S19. J. Virol. 84, 12450-12453 CrossRef PubMed
23. Cheng, E., Haque, A., Rimmer, M. A., Hussein, I. T., Sheema, S., Little, A. and Mir, M. A. (2011) Characterization of the interaction between hantavirus nucleocapsid protein (N) and ribosomal protein S19 (RPS19). J. Biol. Chem. 286, 11814-11824 CrossRef PubMed
24. Mir, M. A., Sheema, S., Haseeb, A. and Haque, A. (2010) Hantavirus nucleocapsid protein has distinct m7G cap- and RNA-binding sites. J. Biol. Chem. 285, 11357-11368 CrossRef PubMed
25. Mir, M. A. and Panganiban, A. T. (2005) The hantavirus nucleocapsid protein recognizes specific features of the viral RNA panhandle and is altered in conformation upon RNA binding. J. Virol. 79, 1824-1835 CrossRef PubMed
26. Hussein, I. T., Cheng, E., Ganaie, S. S., Werle, M. J., Sheema, S., Haque, A. and Mir, M. A. (2012) Autophagic clearance of Sin Nombre hantavirus glycoprotein Gn promotes virus replication in cells. J. Virol. 86, 7520-7529 CrossRef PubMed
27. Xu, X., Severson, W., Villegas, N., Schmaljohn, C. S. and Jonsson, C. B. (2002) The RNA-binding domain of the hantaan virus N protein maps to a central, conserved region. J. Virol. 76, 3301-3308 CrossRef PubMed
28. Cencic, R., Hall, D. R., Robert, F., Du, Y., Min, J., Li, L., Qui, M., Lewis, I., Kurtkaya, S., Dingledine, R. et al. (2011) Reversing chemoresistance by small molecule inhibition of the translation initiation complex eIF4F. Proc. Natl. Acad. Sci. U.S.A. 108, 1046-1051 CrossRef PubMed
29. Bougie, I. and Bisaillon, M. (2003) Initial binding of the broad spectrum antiviral nucleoside ribavirin to the hepatitis C virus RNA polymerase. J. Biol. Chem. 278, 52471-52478 CrossRef PubMed
30. Weisshart, K., Kuo, A. A., Painter, G. R., Wright, L. L., Furman, P. A. and Coen, D. M. (1993) Conformational changes induced in herpes simplex virus DNA polymerase upon DNA binding. Proc. Natl. Acad. Sci. U.S.A. 90, 1028-1032 CrossRef PubMed
31. Hussein, I. T. and Mir, M. A. (2013) How hantaviruses modulate cellular pathways for efficient replication? Front. Biosci. 5, 154-166
32. Brown, B. A. and Panganiban, A. T. (2010) Identification of a region of hantavirus nucleocapsid protein required for RNA chaperone activity. RNA Biol. 7, 830-837 CrossRef PubMed
33. Alminaite, A., Backstrom, V., Vaheri, A. and Plyusnin, A. (2008) Oligomerization of hantaviral nucleocapsid protein: charged residues in the N-terminal coiled-coil domain contribute to intermolecular interactions. J. Gen. Virol. 89, 2167-2174 CrossRef PubMed
34. Gale, Jr, M., Tan, S. L. and Katze, M. G. (2000) Translational control of viral gene expression in eukaryotes. Microbiol. Mol. Biol. Rev. 64, 239-280 CrossRef PubMed
35. Muranyi, W., Bahr, U., Zeier, M. and van der Woude, F. J. (2005) Hantavirus infection. J. Am. Soc. Nephrol. 16, 3669-3679 CrossRef PubMed
36. Cheng, E., Wang, Z. and Mir, M. A. (2014) Interaction between hantavirus nucleocapsid protein (N) and RNA dependent RNA polymerase (RdRp) mutant reveals the requirement of N-RdRp interaction for viral RNA synthesis. J. Virol. 88, 8706-8712 CrossRef PubMed