The rotavirus nonstructural protein NSP5 coordinates a [2Fe-2S] iron-sulfur cluster that modulates interaction to RNA

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1074-1083

  Martin, Davy ^a   Charpilienne, Annie ^a   Parent, Aubérie ^a   Boussac, Alain ^b   D'Autreaux, Benoit ^a   Poupon, Joël ^c   Poncet, Didier ^a  

^a CNRS   (France)

^b SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^c HÔPITAL LARIBOISIÈRE   (France)

Author keywords

CXXC motif; Metalloprotein

Indexed keywords

ADENOSINE TRIPHOSPHATASE; IRON SULFUR PROTEIN; METALLOPROTEIN; NONSTRUCTURAL PROTEIN 2; NSP5 PROTEIN; PROTEIN VP1; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; IN VIVO STUDY; INTERACTIONS WITH RNA; LIGHT ABSORPTION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; ULTRAVIOLET RADIATION; VIRUS LIKE AGENT;

HUMANS; IRON; METALLOPROTEINS; POINT MUTATION; RNA, VIRAL; ROTAVIRUS; ROTAVIRUS INFECTIONS; SPECTROPHOTOMETRY, ULTRAVIOLET; SULFUR; VIRAL NONSTRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 84874644140     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-217182     Document Type: Article

References (47)

1. Parashar, U. D., Gibson, C. J., Bresse, J. S., and Glass, R. I. (2006) Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis. 12, 304-306
2. Berois, M., Sapin, C., Erk, I., Poncet, D., and Cohen, J. (2003) Rotavirus nonstructural protein NSP5 interacts with major core protein VP2. J. Virol. 77, 1757-1763 (Pubitemid 36109987)
3. Kattoura, M. D., Chen, X., and Patton, J. T. (1994) The rotavirus RNA-binding protein NS35 (NSP2) forms 10S multimers and interacts with the viral RNA polymerase. Virology 202, 803-813 (Pubitemid 24254894)
4. Silvestri, L. S., Taraporewala, Z. F., and Patton, J. T. (2004) Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78, 7763-7774 (Pubitemid 38915922)
5. Trask, S. D., McDonald, S. M., and Patton, J. T. (2012) Structural insights into the coupling of virion assembly and rotavirus replication. Nat. Rev. Microbiol. 10, 165-177
6. Campagna M, Eichwald C, Vascotto, F., and Burrone, O. R. (2005) RNA interference of rotavirus segment 11 mRNA reveals the essential role of NSP5 in the virus replicative cycle. J. Gen. Virol. 86, 1481-1487 (Pubitemid 40613267)
7. Lopez T, Rojas M, Ayala-Breton C, Lopez, S., and Arias, C. F. (2005) Reduced expression of the rotavirus NSP5 gene has a pleiotropic effect on virus replication. J. Gen. Virol. 86, 1609-1617 (Pubitemid 40766873)
8. Martin, D., Ouldali, M., Menetrey, J., and Poncet, D. (2011) Structural organisation of the rotavirus nonstructural protein NSP5. J. Mol. Biol. 413, 209-221
9. Gonzalez, S. A., and Burrone, O. R. (1991) Rotavirus NS26 is modified by addition of single O-linked residues of N-acetylglucosamine. Virology 182, 8-16
10. Welch, S. K., Crawford, S. E., and Estes, M. K. (1989) Rotavirus SA11 genome segment 11 protein is a nonstructural phosphoprotein. J. Virol. 63, 3974-3982 (Pubitemid 19205473)
11. Eichwald, C., Jacob, G., Muszynski, B., Allende, J. E., and Burrone, O. R. (2004) Uncoupling substrate and activation functions of rotavirus NSP5: phosphorylation of Ser-67 by casein kinase 1 is essential for hyperphosphorylation. Proc. Natl. Acad. Sci. U. S. A. 101, 16304-16309 (Pubitemid 39552840)
12. Eichwald, C., Vascotto, F., Fabbretti, E., and Burrone, O. R. (2002) Rotavirus NSP5: mapping phosphorylation sites and kinase activation and viroplasm localization domains. J. Virol. 76, 3461-3470 (Pubitemid 34224547)
13. Sen, A., Agresti, D., and Mackow, E. R. (2006) Hyperphosphorylation of the rotavirus NSP5 protein is independent of serine 67, NSP2, or the intrinsic insolubility of NSP5 and is regulated by cellular phosphatases. J. Virol. 80, 1807-1816 (Pubitemid 43228721)
14. Bar-Magen, T., Spencer, E., and Patton, J. T. (2007) An ATPase activity associated with the rotavirus phosphoprotein NSP5. Virology 369, 389-399 (Pubitemid 350103593)
15. Afrikanova, I., Fabbretti, E., Miozzo, M. C., and Burrone, O. R. (1998) Rotavirus NSP5 phosphorylation is up-regulated by interaction with NSP2. J. Gen. Virol. 79, 2679-2686 (Pubitemid 28497620)
16. Chnaiderman, J., Barro, M., and Spencer, E. (2002) NSP5 phosphorylation regulates the fate of viral mRNA in rotavirus infected cells. Arch. Virol. 147, 1899-1911 (Pubitemid 35218715)
17. Poncet, D., Lindenbaum, P., L'Haridon, R., and Cohen, J. (1997) In vivo and in vitro phosphorylation of rotavirus NSP5 correlates with its localization in viroplasms. J. Virol. 71, 34-41 (Pubitemid 26412262)
18. Vende, P., Taraporewala, Z. F., and Patton, J. T. (2002) RNAbinding activity of the rotavirus phosphoprotein NSP5 includes affinity for double-stranded RNA. J. Virol. 76, 5291-5299 (Pubitemid 34441734)
19. Arnoldi, F., Campagna, M., Eichwald, C., Desselberger, U., and Burrone, O. R. (2007) Interaction of rotavirus polymerase VP1 with nonstructural protein NSP5 is stronger than that with NSP2. J. Virol. 81, 2128-2137
20. McDonald, S. M., and Patton, J. T. (2011) Rotavirus VP2 core shell regions critical for viral polymerase activation. J. Virol. 85, 3095-3105
21. Torres-Vega, M. A., González, R. A., Duarte, M., Poncet, D., López, S., and Arias, C. F. (2000) The C-terminal domain of rotavirus NSP5 is essential for its multimerization, hyperphosphorylation and interaction with NSP6. J. Gen. Virol. 81, 821-830 (Pubitemid 30105513)
22. Fabbretti, E., Afrikanova, I., Vascotto, F., and Burrone, O. R. (1999) Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80, 333-339 (Pubitemid 29095192)
23. Sen, A., Sen, N., and Mackow, E. R. (2007) The formation of viroplasm-like structures by the rotavirus NSP5 protein is calcium regulated and directed by a C-terminal helical domain. J. Virol. 81, 11758-11767 (Pubitemid 47623808)
24. Martin, D., Duarte, M., Lepault, J., and Poncet, D. (2010) Sequestration of free tubulin molecules by the viral protein NSP2 induces microtubule depolymerization during rotavirus infection. J. Virol. 84, 2522-2532
25. Cowart, R. E., Singleton, F. L., and Hind, J. S. (1993) A comparison of bathophenanthrolinedisulfonic acid and ferrozine as chelators of iron(II) in reduction reactions. Anal. Biochem. 211, 151-155 (Pubitemid 23189343)
26. Beinert, H. (1983) Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable iron-sulfur proteins. Anal. Biochem. 131, 373-378
27. Buchholz, U. J., Finke, S., and Conzelmann, K. K. (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J. Virol. 73, 251-259 (Pubitemid 28565367)
28. Baaske., P., Wienken, C. J, Reineck, P., Duhr, S., and Braun, D. (2010) Optical thermophoresis for quantifying the buffer dependence of aptamer binding. Angew. Chem. Int. Ed. Engl. 49, 2238-2241
29. Duhr, S., and Braun, D. (2006) Why molecules move along a temperature gradient. Proc. Natl. Acad. Sci. U. S. A. 103, 19678-19682 (Pubitemid 46037491)
30. Jerabek-Willemsen, M., Wienken, C. J., Braun, D., Baaske, P., and Duhr, S. (2011) Molecular interaction studies using microscale thermophoresis. Assay Drug Dev. Technol. 9, 342-353
31. Zillner, K., Jerabek-Willemsen, M., Duhr, S., Braun, D., Längst, G., and Baaske, P. (2012) Microscale thermophoresis as a sensitive method to quantify protein: nucleic acid interactions in solution. Methods Mol. Biol. 815, 241-252
32. Coghlan, V. M., and Vickery, L. E. (1989) Expression of human ferredoxin and assembly of the [2Fe-2S] center in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 86, 835-839 (Pubitemid 19056251)
33. Xia, B., Cheng, H., Bandarian, V., Reed, G. H., and Markley, J. L. (1996) Human ferredoxin: overproduction in Escherichia coli, reconstitution in vitro, and spectroscopic studies of ironsulfur cluster ligand cysteine-to-serine mutants. Biochemistry 35, 9488-9495 (Pubitemid 26320055)
34. Picciocchi, A., Saguez, C., Boussac, A., Cassier-Chauvat, C., and Chauvat, F. (2007) CGFS-type monothiol glutaredoxins from the cyanobacterium Synechocystis PCC6803 and other evolutionary distant model organisms possess a glutathione-ligated [2Fe-2S] cluster. Biochemistry 46, 15018-15026 (Pubitemid 350308893)
35. Guigliarelli, B., and Bertrand, P. (1999) Application of EPR spectroscopy to the structural and functional study of iron-sulfur proteins. Adv. Inorg. Chem. 47, 421-497
36. Iwasaki, T., Samoilova, R. I., Kounosu, A., Ohmori, D., and Dikanov, S. A. (2009) Continuous-wave and pulsed EPR characterization of the [2Fe-2S](Cys)3(His)1 cluster in rat MitoNEET. J. Am. Chem. Soc. 131, 13659-13667
37. Drakesmith, H., and Prentice, A. (2008) Viral infection and iron metabolism. Nat. Rev. Microbiol. 6, 541-552 (Pubitemid 351863367)
38. Hirata, A., and Murakami, K. S. (2009) Archaeal RNA polymerase. Curr. Opin. Struct. Biol. 19, 724-731
39. Netz, D. J., Stith, C. M, Stümpfig, M., Köpf, G., Vogel, D., Genau, H. M, Stodola, J. L., Lill, R., Burgers, P. M., and Pierik. A. J. (2012) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat. Chem. Biol. 8, 125-132
40. White, M. F., and Dillingham, M. S. (2012) Iron-sulphur clusters in nucleic acid processing enzymes. Curr. Opin. Struct. Biol. 22, 94-100
41. Wu, Y., and Brosh, R. M., Jr. (2012) DNA helicase and helicasenuclease enzymes with a conserved iron-sulfur cluster. Nucleic Acids Res. 40(10), 4247-4260
42. Klinge, S., Hirst, J., Maman, J. D., Krude, T., and Pellegrini, L. (2007) An iron-sulfur domain of the eukaryotic primase is essential for RNA primer synthesis. Nat. Struct. Mol. Biol. 14, 875-877 (Pubitemid 47373835)
43. Taraporewala, Z. F., and Patton, J. T. (2001) Identification and characterization of the helix-destabilizing activity of rotavirus nonstructural protein NSP2. J. Virol. 75, 4519-4527 (Pubitemid 32381494)
44. Howell, M. L., Sanders-Loehr, J., Loehr, T. M., Roseman, N. A., Mathews, C. K., and Slabaugh, M. B. (1992) Cloning of the vaccinia virus ribonucleotide reductase small subunit gene. Characterization of the gene product expressed in Escherichia coli. J. Biol. Chem. 267, 1705-1711
45. Jordan, A., and Reichard, P. (1998) Ribonucleotide reductases. Annu. Rev. Biochem. 67, 71-98 (Pubitemid 28411124)
46. Potsch, S., Sahlin, M., Langelier, Y., Graslund, A., and Lassmann, G. (1995) Reduction of the tyrosyl radical and the iron center in protein R2 of ribonucleotide reductase from mouse, herpes simplex virus and E. coli by p-alkoxyphenols. FEBS Lett. 374, 95-99
47. Young, P., Andersson, J., Sahlin, M., and Sjoberg, B. M. (1996) Bacteriophage T4 anaerobic ribonucleotide reductase contains a stable glycyl radical at position 580. J. Biol. Chem. 271, 20770-20775 (Pubitemid 26281862)