Crystal Structure of Escherichia coli Polynucleotide Phosphorylase Core Bound to RNase E, RNA and Manganese: Implications for Catalytic Mechanism and RNA Degradosome Assembly

Journal of Molecular Biology

Volumn 389, Issue 1, 2009, Pages 17-33

  Nurmohamed, Salima ^a   Vaidialingam, Bhamini ^a   Callaghan, Anastasia J ^b   Luisi, Ben F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

polynucleotide phosphorylase; protein protein interactions; RNA degradation; RNA degradosome; RNase E

Indexed keywords

MAGNESIUM; MANGANESE; PHENYLALANINE; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE E; RNA; TRANSITION ELEMENT;

ARTICLE; BACTERIUM IDENTIFICATION; BETA SHEET; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; EXOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RNA ANALYSIS; RNA BINDING; RNA CLEAVAGE; RNA DEGRADATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 67349257830     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.03.051     Document Type: Article

References (59)

1. Arraiano C.M., and Maquat L.E. Post-transcriptional control of gene expression: effectors of mRNA decay. Mol. Microbiol. 49 (2003) 267-276
2. Grunberg-Manago M. Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu. Rev. Genet. 33 (1999) 193-227
3. Wilusz C.J., and Wilusz J. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet. 20 (2004) 491-497
4. Deutscher M.P. Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucleic Acids Res. 34 (2006) 659-666
5. Grunberg-Manago M., Oritz P.J., and Ochoa S. Enzymatic synthesis of nucleic acidlike polynucleotides. Science 122 (1955) 907-910
6. Regnier P., Grunberg-Manago M., and Portier C. Nucleotide sequence of the pnp gene of Escherichia coli encoding polynucleotide phosphorylase. Homology of the primary structure of the protein with the RNA-binding domain of ribosomal protein S1. J. Biol. Chem. 262 (1987) 63-68
7. Jarrige A.C., Brechemier-Baey D., Mathy N., Duche O., and Portier C. Mutational analysis of polynucleotide phosphorylase from Escherichia coli. J. Mol. Biol. 321 (2002) 397-409
8. Lin-Chao S., Chiou N.T., and Schuster G. The PNPase, exosome and RNA helicases as the building components of evolutionarily-conserved RNA degradation machines. J. Biomed. Sci. 14 (2007) 523-532
9. Mohanty B.K., and Kushner S.R. Polynucleotide phosphorylase, RNase II and RNase E play different roles in the in vivo modulation of polyadenylation in Escherichia coli. Mol. Microbiol. 36 (2000) 982-994
10. Mohanty B.K., and Kushner S.R. Polynucleotide phosphorylase functions both as a 3′->5′ exonuclease and a poly(A) polymerase in Escherichia coli. Proc. Natl Acad. Sci. USA 97 (2000) 11966-11971
11. Slomovic S., and Schuster G. Stable PNPase RNAi silencing: Its effect on the processing and adenylation of human mitochondrial RNA. RNA 14 (2008) 310-323
12. Andrade J.M., and Arraiano C.M. PNPase is a key player in the regulation of small RNAs that control the expression of outer membrane proteins. RNA 14 (2008) 543-551
13. Clements M.O., Eriksson S., Thompson A., Lucchini S., Hinton J.C., Normark S., and Rhen M. Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enteric. Proc. Natl Acad. Sci. USA 99 (2002) 8784-8789
14. Ygberg S.E., Clements M.O., Rytkonen A., Thompson A., Holden D.W., Hinton J.C., and Rhen M. Polynucleotide phosphorylase negatively controls spv virulence gene expression in Salmonella enteric. Infect. Immun. 74 (2006) 1243-1254
15. Yang J., Jain C., and Schesser K. RNase E regulates the Yersinia type 3 secretion system. J. Bacteriol. 190 (2008) 3774-3778
16. Cheng Z.F., and Deutscher M.P. Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc. Natl Acad. Sci. USA 100 (2003) 6388-6393
17. Awano N., Inouye M., and Phadtare S. RNase activity of polynucleotide phosphorylase is critical at low temperature in Escherichia coli and is complemented by RNase II. J. Bacteriol. 190 (2008) 5924-5933
18. Matus-Ortega F.A.U., Regonesi M.E., Pina-Escobedo A.F., Tortora P.F., Deho G.F., and Garcia-Mena J. The KH and S1 domains of Escherichia coli polynucleotide phosphorylase are necessary for autoregulation and growth at low temperature. Biochim. Biophys. Acta 1769 (2007) 194-203
19. Symmons M.F., Jones G.H., and Luisi B.F. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure 8 (2000) 1215-1226
20. Buttner K., Wenig K., and Hopfner K.P. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol. Cell 20 (2005) 461-471
21. Harlow L.S., Kadziola A., Jensen K.F., and Larsen S. Crystal structure of the phosphorolytic exoribonuclease RNase PH from Bacillus subtilis and implications for its quaternary structure and tRNA binding. Protein Sci. 13 (2004) 668-677
22. Ishii R., Nureki O., and Yokoyama S. Crystal structure of the tRNA processing enzyme RNase PH from Aquifex aeolicus. J. Biol. Chem. 278 (2003) 32397-32404
23. Lorentzen E., and Conti E. Structural basis of 3′ end RNA recognition and exoribonucleolytic cleavage by an exosome RNase PH core. Mol. Cell 20 (2005) 473-481
24. Lorentzen E., Dziembowski A., Lindner D., Seraphin B., and Conti E. RNA channelling by the archaeal exosome. EMBO Rep. 8 (2007) 470-476
25. Liu Q., Greimann J.C., and Lima C.D. Erratum: Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 131 (2007) 188-189
26. Liu Q., Greimann J.C., and Lima C.D. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127 (2006) 1223-1237
27. Lorentzen E., Walter P., Fribourg S., Evguenieva-Hackenberg E., Klug G., and Conti E. The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat. Struct. Mol. Biol. 12 (2005) 575-581
28. Dziembowski A., Lorentzen E., Conti E., and Seraphin B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 14 (2007) 15-22
29. Shi Z., Yang W.Z., Lin-Chao S., Chak K.F., and Yuan H.S. Crystal structure of Escherichia coli PNPase: central channel residues are involved in processive RNA degradation. RNA 14 (2008) 2361-2371
30. Messias A.C., and Sattler M. Structural basis of single-stranded RNA recognition. Acc. Chem. Res. 37 (2004) 279-287
31. Stickney L.M., Hankins J.S., Miao X., and Mackie G.A. Function of the conserved S1 and KH domains in polynucleotide phosphorylase. J. Bacteriol. 187 (2005) 7214-7221
32. Briani F., Curti S., Rossi F., Carzaniga T., Mauri P., and Deho G. Polynucleotide phosphorylase hinders mRNA degradation upon ribosomal protein S1 overexpression in Escherichia coli. RNA 14 (2008) 2417-2429
33. Garcia-Mena J., Das A., Sanchez-Trujillo A., Portier C., and Montanez C. A novel mutation in the KH domain of polynucleotide phosphorylase affects autoregulation and mRNA decay in Escherichia coli. Mol. Microbiol. 33 (1999) 235-248
34. Jarrige A.C., Mathy N., and Portier C. PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J. 20 (2001) 6845-6855
35. Carzaniga T., Briani F., Zangrossi S., Merlino G., Marchi P., and Deho G. Autogenous regulation of Escherichia coli polynucleotide phosphorylase expression revisited. J. Bacteriol. 191 (2009) 1738-1748
36. Carpousis A.J. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 61 (2007) 71-87
37. Liou G.G., Jane W.N., Cohen S.N., Lin N.S., and Lin-Chao S. RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proc. Natl Acad. Sci. USA 98 (2001) 63-68
38. Py B., Higgins C.F., Krisch H.M., and Carpousis A.J. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381 (1996) 169-172
39. Callaghan A.J., Aurikko J.P., Ilag L.L., Grossmann J.G., Chandran V., Kuhnel K., et al. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J. Mol. Biol. 340 (2004) 965-979
40. Carpousis A.J., Van Houwe G., Ehretsmann C., and Krisch H.M. Copurification of E. coli RNase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76 (1994) 889-900
41. Chandran V., Poljak L., Vanzo N.F., Leroy A., Miguel R.N., Fernandez-Recio J., et al. Recognition and cooperation between the ATP-dependent RNA helicase RhlB and ribonuclease RNase E. J. Mol. Biol. 367 (2007) 113-132
42. Marcaida M.J., DePristo M.A., Chandran V., Carpousis A.J., and Luisi B.F. The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem. Sci. 31 (2006) 359-365
43. Chandran V., and Luisi B.F. Recognition of enolase in the Escherichia coli RNA degradosome. J. Mol. Biol. 358 (2006) 8-15
44. Khemici V., Poljak L., Luisi B.F., and Carpousis A.J. The RNase E of Escherichia coli is a membrane-binding protein. Mol. Microbiol. 70 (2008) 799-813
45. Vanzo N.F., Li Y.S., Py B., Blum E., Higgins C.F., Raynal L.C., et al. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 12 (1998) 2770-2781
46. Symmons M.F., Williams M.G., Luisi B.F., Jones G.H., and Carpousis A.J. Running rings around RNA: a superfamily of phosphate-dependent RNases. Trends Biochem. Sci. 27 (2002) 11-18
47. Briani F., Del Favero M., Capizzuto R., Consonni C., Zangrossi S., Greco C., et al. Genetic analysis of polynucleotide phosphorylase structure and functions. Biochimie 89 (2007) 145-157
48. Navarro M.V., Oliveira C.C., Zanchin N.I., and Guimaraes B.G. Insights into the mechanism of progressive RNA degradation by the archaeal exosome. J. Biol. Chem. 283 (2008) 14120-14131
49. Pawelek P.D., Croteau N., Ng-Thow-Hing C., Khursigara C.M., Moiseeva N., Allaire M., and Coulton J.W. Structure of TonB in complex with FhuA E. coli outer membrane receptor. Science 312 (2006) 1399-1402
50. Lee K., and Cohen S.N. A Streptomyces coelicolor functional orthologue of Escherichia coli RNase E shows shuffling of catalytic and PNPase-binding domains. Mol. Microbiol. 48 (2003) 349-360
51. Lorentzen E., Basquin J., and Conti E. Structural organization of the RNA-degrading exosome. Curr. Opin. Struct. Biol. 18 (2008) 709-713
52. Gao J., Lee K., Zhao M., Qiu J., Zhan X., Saxena A., et al. Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol. Microbiol. 61 (2006) 394-406
53. Worrall J.A., Górna M., Crump N.T., Phillips L.G., Tuck A.C., Price A.J., et al. Reconstitution and analysis of the multienzyme Escherichia coli RNA degradosome. J. Mol. Biol. 382 (2008) 870-883
54. Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41 (2005) 207-234
55. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
56. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., and Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 40 (2007) 658-674
57. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60 (2004) 2126-2132
58. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. D 53 (1997) 240-255
59. Gouet P.F., Robert X.F., and Courcelle E. ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31 (2003) 3320-3323