Nucleic acid and protein factors involved in Escherichia coli polynucleotide phosphorylase function on RNA

Biochimie

Volumn 92, Issue 5, 2010, Pages 445-454

  Fernandez Ramirez F ^a,b   Bermudez Cruz R M ^a   Montanez C ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b HOSPITAL GENERAL DE MÉXICO   (Mexico)

Author keywords

Cold shock; Polynucleotide phosphorylase; Protein multimerization; RNA binding; RNA phosphorolysis

Indexed keywords

MUTANT PROTEIN; NUCLEIC ACID; OLIGONUCLEOTIDE; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RNA;

ARTICLE; AUTOREGULATION; BACTERIAL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ESCHERICHIA COLI; IN VITRO STUDY; MOLECULAR INTERACTION; NONHUMAN; POLYADENYLATION; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA BINDING; RNA DEGRADATION; RNA PROCESSING; TEMPERATURE;

BASE SEQUENCE; BLOTTING, NORTHERN; BLOTTING, WESTERN; DNA PRIMERS; ESCHERICHIA COLI; MOLECULAR WEIGHT; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RNA, BACTERIAL;

ESCHERICHIA COLI;

EID: 77951024620     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.01.004     Document Type: Article

References (52)

1. Coburn G., Mackie G.A. Degradation of mRNA in Escherichia coli: an old problem with some new twists. Prog. Nucleic Acid Res. Mol. Biol. 1999, 62:55-108.
2. Yehudai-Resheff S., Hirsh M., Schuster G. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell. Biol. 2001, 21:5408-5416.
3. Piwowarski J., Grzechnik P., Dziembowski A., Dmochowska A., Minczuk M., Stepien P. Human polynucleotide phosphorylase, hPNPase, is localized in mitochondria. J. Mol. Biol. 2003, 329:853-857.
4. Chou J., Singer M. Deoxyadenosine diphosphate as a substrate and inhibitor of polynucleotide phosphorylase of Micrococcus luteus. I. Deoxyadenosine diphosphate as a substrate for polymerization and the exchange reaction with inorganic 32 P. J. Biol. Chem. 1971, 246:7486-7496.
5. Godefroy T. Kinetics of polymerization and phosphorolysis reactions of Escherichia coli polynucleotide phosphorylase. Evidence for multiple binding of polynucleotide phosphorylase. Eur. J. Biochem. 1970, 14:222-231.
6. Thang M.N., Thang D.C., Leautey J. Séparation et identification de polynucléotide phosphorylase par électrophorése sur gel polyacrylamide. C. R. Acad. Sci. Paris 1967, 265:1823-1826.
7. Cardenas P.P., Carrasco B., Sanchez H., Deikus G., Bechhofer D.H., Alonso J.C. Bacillus subtilis polynucleotide phosphorylase 3′-to-5′ DNase activity is involved in DNA repair. Nucleic Acids Res. May 11, 2009, 1-13.
8. Donovan W., Kushner S. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:120-124.
9. Mohanty B.K., Kushner S.R. Polynucleotide phosphorylase functions both as a 3′ right-arrow 5′ exonuclease and a poly(A) polymerase in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11966-11971.
10. Liou G., Jane W., Cohen S.N., Lin N., 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. U.S.A. 2001, 98:63-68.
11. Taghbalout A., Rothfield L. RNaseE and RNA Helicase B play central roles in the cytoskeletal organization of the RNA degradosome. J. Biol. Chem. 2008, 283:13850-13855.
12. Valentine R., Thang M., Grunberg-Manago M. Electron microscopy of Escherichia coli polynucleotide phosphorylase molecules and polyribonucleotide formation. J. Mol. Biol. 1969, 39:389-391.
13. Soreq H., Littauer U. Purification and characterization of polynucleotide phosphorylase from Escherichia coli. Probe for the analysis of 3′ sequences of RNA. J. Biol. Chem. 1977, 252:6885-6888.
14. Sulewski M., Marchese-Ragona S.P., Johnson K.A., Benkovic S.J. Mechanism of polynucleotide phosphorylase. Biochemistry 1989, 28:5855-5864.
15. Symmons M.F., Jones G.H., Luisi B.F. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure 2000, 8:1215-1226.
16. Shi Z., Yang W., Lin-Chao S. Crystal structure of Escherichia coli PNPase: central channel residues are involved in processive RNA degradation. RNA 2008, 14:2361-2371.
17. Bycroft M., Hubbard T., Proctor M., Freund S., Murzin A. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 1997, 88:235-242.
18. Mattaj I. RNA recognition: a family matter? Review. Cell 1993, 73:837-840.
19. Régnier P., Grunberg-Manago M., 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. 1987, 262:63-68.
20. Bermúdez-Cruz R.M., García-Mena J., Montañez C. Polynucleotide phosphorylase binds to ssRNA with same affinity as to ssDNA. Biochimie 2002, 84:321-328.
21. Briani F., Del Favero M., Capizzuto R., Consonni C., Zangrossi S., Greco C., De Gioia L., Tortora P., Dehò G. Genetic analysis of polynucleotide phosphorylase structure and functions. Biochimie 2007, 89:145-157.
22. Chang S.A., Cozad M., Mackie G.A., Jones G.H. Kinetics of polynucleotide phosphorylase: comparison of enzymes from Streptomyces and Escherichia coli and effects of nucleoside diphosphates. J. Bacteriol. 2008, 190:98-106.
23. Jarrige A., Brechemier-Baey D., Mathy N., Duche O., Portier C. Mutational analysis of polynucleotide phosphorylase from Escherichia coli. J. Mol. Biol. 2002, 321:397-409.
24. Matus-Ortega M.E., Regonesi M.E., Piña-Escobedo A., Tortora P., Dehò G., García-Mena J. The KH and S1 domains of Escherichia coli polynucleotide phosphorylase are necessary for autoregulation and growth at low temperature. Biochim. Biophys. Acta 2007, 1769:194-203.
25. Regonesi M.E., Briani F., Ghetta A., Zangrossi S., Ghisotti D., Tortora P., Dehò G. A mutation in polynucleotide phosphorylase from Escherichia coli impairing RNA binding and degradosome stability. Nucleic Acids Res. 2004, 32:1006-1017.
26. Stickney L.M., Hankins J.S., Miao X., Mackie G.A. Function of the conserved S1 and KH domains in polynucleotide phosphorylase. J. Bacteriol. 2005, 187:7214-7221.
27. Jarrige A., Mathy N., Portier C. PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J. 2001, 20:6845-6855.
28. Carzaniga T., Briani F., Zangrossi S., Merlino G., Marchi P., Dehò G. Autogenous regulation of Escherichia coli polynucleotide phosphorylase expression revisited. J. Bacteriol. 2009, 191:1738-1748.
29. Briani F., Curti S., Rossi F., Carzaniga T., Mauri P., Dehò G. Polynucleotide phosphorylase hinders mRNA degradation upon ribosomal protein S1 overexpression in Escherichia coli. RNA 2008, 14:2417-2429.
30. García-Mena J., Das A., Sánchez-Trujillo A., Portier C., Montañez C. A novel mutation in the KH domain of polynucleotide phosphorylase affects autoregulation and mRNA decay in Escherichia coli. Mol. Microbiol. 1999, 33:235-248.
31. Sambrook J., Fritsch E., Maniatis T. Molecular Cloning: a Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, New York, pp. 1.25-1.28. second ed.
32. Hanrahan D. Techniques for transformation of E. coli. A Practical Approach 1985, vol. 1:109-135. I.R.L. Press, Oxford. D. Glover (Ed.).
33. Causton H., Py B., McLaren R., Higgins C. mRNA degradation in Escherichia coli: a novel factor which impedes the exoribonucleolytic activity of PNPase at stem-loop structures. Mol. Microbiol. 1994, 14:731-741.
34. Black D., Chan R., Min H., Wang J., Bell L. The electrophoretic mobility shift assay for RNA binding proteins. RNA: Protein Interactions - a Practical Approach 1998, 109-135. Oxford University Press, Oxford. C. Smith (Ed.).
35. Godefroy T., Cohn M., Grunberg-Manago M. Kinetics of polymerization and phosphorolysis reactions of E. coli polynucleotide phosphorylase. Role of oligonucleotides in polymerization. Eur. J. Biochem. 1970, 12:236-249.
36. Awano R., Inouye M., Phadtare S. RNase activity of polynucleotide phosphorylase is critical at low temperature in Escherichia coli and is complemented by Ribonuclease II. J. Bacteriol. 2008, 190:5924-5933.
37. Goverde R., Huis in't Velt J., Kusters J., Mooi F. The psychrotropic bacterium Yersinia enterocolitica requires expression of pnp, the gene for polynucleotide phosphorylase, for growth at low temperature (5 °C). Mol. Microbiol. 1998, 28:555-569.
38. Yamanaka K., Inouye M. Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J. Bacteriol. 2001, 183:2808-2816.
39. Zhou Z., Deutscher M. An essential function for the phosphate-dependent exoribonucleases RNase PH and polynucleotide phosphorylase. J. Bacteriol. 1997, 179:4391-4395.
40. Condon C. Maturation and degradation of RNA in bacteria. Curr. Opin. Microbiol. 2007, 10:271-278.
41. Mohanty B.K., Kushner S.R. Genomic analysis in Escherichia coli demonstrates differential roles for polynucleotide phosphorylase and RNAse II in mRNA abundance and decay. Mol. Microbiol. 2003, 50:645-658.
42. Robert-Le Meur M., Portier C. E.coli polynucleotide phosphorylase expression is autoregulated through an RNase III-dependent mechanism. EMBO J. 1992, 11:2633-2641.
43. Amblar M., Barbas A., Fialho A.M., Arraiano C.M. Characterization of the functional domains of Escherichia coli RNase II. J. Mol. Biol. 2006, 360:921-933.
44. Bouvet P., Matsumoto K., Wolffe A.P. Sequence-specific RNA recognition by the Xenopus Y-box proteins. An essential role for the cold shock domain. J. Biol. Chem. 1995, 270:28297-28303.
45. Jiang W., Hou Y., Inouye M. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 1997, 272:196-202.
46. Portnoy V., Palnizky G., Yehudai-Resheff S., Glaser F., Schuster G. Analysis of the human polynucleotide phosphorylase (PNPase) reveals differences in RNA binding and response to phosphate compared to its bacterial and chloroplast counterparts. RNA 2008, 14:1-13.
47. Kushner S.R. mRNA decay in Escherichia coli comes of age. J. Bacteriol. 2002, 184:4658-4665.
48. Fraz̃ao C., McVey C.E., Amblar M., Barbas A., Vonrhein C., Arraiano C.M., Carrondo M.A. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 2006, 443:110-114.
49. Tanabe H., Goldstein J., Yang M., Inouye M. Identification of the promoter region of the Escherichia coli major cold shock gene, cspA. J. Bacteriol. 1992, 174:3867-3873.
50. Neuhaus K., Rapposch S., Francis K.P., Scherer S. Restart of exponential growth of cold-shocked Yersinia enterocolitica occurs after down-regulation of cspA1/A2 mRNA. J. Bacteriol. 2000, 182:3285-3288.
51. Spickler C., Mackie G.A. Action of RNase II and polynucleotide phosphorylase against RNAs containing stem-loops of defined structure. J. Bacteriol. 2000, 182:2422-2427.
52. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.