1887

Microbiology Society logo

Volume 158, Issue 5

Involvement of in survival of UV radiation in K-12 Free

Abstract

Polynucleotide phosphorylase (PNPase), a multifunctional protein, is a 3′→5′ exoribonuclease or exoDNase in the presence of inorganic phosphate (P), and extends a 3′-OH of RNA or ssDNA in the presence of ADP or dADP. In , PNPase is known to protect against HO- and mitomycin C-induced damage. Recent reports show that PNPase is required for repair of HO-induced double-strand breaks. Here we show that absence of PNPase makes cells sensitive to UV, indicating that PNPase has a role in survival of UV radiation damage. Analyses of various DNA repair pathways show that in the absence of nucleotide excision repair, survival of UV radiation depends critically on PNPase function. Consequently, , and strains show hypersensitivity to UV radiation. Whereas the mutation is non-epistatic to , and mutations with respect to the UV-sensitivity phenotype, it is epistatic to , and mutations, implicating it in the recombinational repair process.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.056309-0
2012-05-01
2022-05-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/5/1196.html?itemId=/content/journal/micro/10.1099/mic.0.056309-0&mimeType=html&fmt=ahah

References

  1. Arraiano C. M., Yancey S. D., Kushner S. R. ( 1988). Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J Bacteriol 170:4625–4633[PubMed]
     [Google Scholar]
  2. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K. A., Tomita M., Wanner B. L., Mori H. ( 2006). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: [View Article][PubMed]
     [Google Scholar]
  3. Beljanski M. ( 1996). De novo synthesis of DNA-like molecules by polynucleotide phosphorylase in vitro . J Mol Evol 42:493–499 [View Article][PubMed]
     [Google Scholar]
  4. Bermúdez-Cruz R. M., Ramírez F., Kameyama-Kawabe L., Montañez C. ( 2005). Conserved domains in polynucleotide phosphorylase among eubacteria. Biochimie 87:737–745 [View Article][PubMed]
     [Google Scholar]
  5. Bockrath R., Wolff L., Farr A., Crouch R. J. ( 1987). Amplified RNase H activity in Escherichia coli B/r increases sensitivity to ultraviolet radiation. Genetics 115:33–40[PubMed]
     [Google Scholar]
  6. Brégeon D., Sarasin A. ( 2005). Hypothetical role of RNA damage avoidance in preventing human disease. Mutat Res 577:293–302 [View Article][PubMed]
     [Google Scholar]
  7. Cardenas P. P., Carrasco B., Sanchez H., Deikus G., Bechhofer D. H., Alonso J. C. ( 2009). Bacillus subtilis polynucleotide phosphorylase 3′-to-5′ DNase activity is involved in DNA repair. Nucleic Acids Res 37:4157–4169[PubMed] [CrossRef]
     [Google Scholar]
  8. Cardenas P. P., Carzaniga T., Zangrossi S., Briani F., Garcia-Tirado E., Dehò G., Alonso J. C. ( 2011). Polynucleotide phosphorylase exonuclease and polymerase activities on single-stranded DNA ends are modulated by RecN, SsbA and RecA proteins. Nucleic Acids Res 39:9250–9261 [View Article][PubMed]
     [Google Scholar]
  9. Carpousis A. J. ( 2002). The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes. Biochem Soc Trans 30:150–155 [View Article][PubMed]
     [Google Scholar]
  10. Centore R. C., Sandler S. J. ( 2007). UvrD limits the number and intensities of RecA-green fluorescent protein structures in Escherichia coli K-12. J Bacteriol 189:2915–2920 [View Article][PubMed]
     [Google Scholar]
  11. Coburn G. A., Miao X., Briant D. J., Mackie G. A. ( 1999). Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3′ exonuclease and a DEAD-box RNA helicase. Genes Dev 13:2594–2603 [View Article][PubMed]
     [Google Scholar]
  12. Courcelle J., Donaldson J. R., Chow K. H., Courcelle C. T. ( 2003). DNA damage-induced replication fork regression and processing in Escherichia coli . Science 299:1064–1067 [View Article][PubMed]
     [Google Scholar]
  13. Courcelle C. T., Chow K. H., Casey A., Courcelle J. ( 2006). Nascent DNA processing by RecJ favors lesion repair over translesion synthesis at arrested replication forks in Escherichia coli . Proc Natl Acad Sci U S A 103:9154–9159 [View Article][PubMed]
     [Google Scholar]
  14. Cox M. M. ( 1998). A broadening view of recombinational DNA repair in bacteria. Genes Cells 3:65–78 [View Article][PubMed]
     [Google Scholar]
  15. Cox M. M. ( 2001). Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annu Rev Genet 35:53–82 [View Article][PubMed]
     [Google Scholar]
  16. Datsenko K. A., Wanner B. L. ( 2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645 [View Article][PubMed]
     [Google Scholar]
  17. Friedberg E. C., Walker G. C., Siede W., Wood R. D., Schultz R. A., Ellenberger T. ( 2006). DNA Repair and Mutagenesis, 2nd edn. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  18. Gillam S., Smith M. ( 1974). Enzymatic synthesis of deoxyribo-oligonucleotides of defined sequence. Properties of the enzyme. Nucleic Acids Res 1:1631–1648 [View Article][PubMed]
     [Google Scholar]
  19. Griffiths H. R., Mistry P., Herbert K. E., Lunec J. ( 1998). Molecular and cellular effects of ultraviolet light-induced genotoxicity. Crit Rev Clin Lab Sci 35:189–237 [View Article][PubMed]
     [Google Scholar]
  20. Grunberg-Manago M. ( 1999). Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet 33:193–227 [View Article][PubMed]
     [Google Scholar]
  21. Handa N., Morimatsu K., Lovett S. T., Kowalczykowski S. C. ( 2009). Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli . Genes Dev 23:1234–1245 [View Article][PubMed]
     [Google Scholar]
  22. Horst J. P., Wu T. H., Marinus M. G. ( 1999). Escherichia coli mutator genes. Trends Microbiol 7:29–36 [View Article][PubMed]
     [Google Scholar]
  23. Howard-Flanders P., Boyce R. P., Theriot L. ( 1966). Three loci in Escherichia coli K-12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics 53:1119–1136[PubMed]
     [Google Scholar]
  24. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. ( 1994). Biochemistry of homologous recombination in Escherichia coli . Microbiol Rev 58:401–465[PubMed]
     [Google Scholar]
  25. Kuzminov A. ( 1995). Collapse and repair of replication forks in Escherichia coli . Mol Microbiol 16:373–384 [View Article][PubMed]
     [Google Scholar]
  26. Le Masson M., Baharoglu Z., Michel B. ( 2008). ruvA and ruvB mutants specifically impaired for replication fork reversal. Mol Microbiol 70:537–548 [View Article][PubMed]
     [Google Scholar]
  27. Lea D. E., Coulson C. A. ( 1949). The distribution of the number of mutants in bacterial populations. J Genet 49:264–285 [View Article]
     [Google Scholar]
  28. Lestini R., Michel B. ( 2007). UvrD controls the access of recombination proteins to blocked replication forks. EMBO J 26:3804–3814 [View Article][PubMed]
     [Google Scholar]
  29. Li S., Waters R. ( 1998). Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination. J Bacteriol 180:3750–3756[PubMed]
     [Google Scholar]
  30. Lloyd R. G. ( 1991). Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12 depends on recG . J Bacteriol 173:5414–5418[PubMed]
     [Google Scholar]
  31. Lloyd R. G., Buckman C. ( 1991). Genetic analysis of the recG locus of Escherichia coli K-12 and of its role in recombination and DNA repair. J Bacteriol 173:1004–1011[PubMed]
     [Google Scholar]
  32. Lloyd R. G., Porton M. C., Buckman C. ( 1988). Effect of recF, recJ, recN, recO and ruv mutations on ultraviolet survival and genetic recombination in a recD strain of Escherichia coli K12. Mol Gen Genet 212:317–324 [View Article][PubMed]
     [Google Scholar]
  33. Lombardo M. J., Rosenberg S. M. ( 2000). radC102 of Escherichia coli is an allele of recG . J Bacteriol 182:6287–6291 [View Article][PubMed]
     [Google Scholar]
  34. Mahdi A. A., Lloyd R. G. ( 1989). Identification of the recR locus of Escherichia coli K-12 and analysis of its role in recombination and DNA repair. Mol Gen Genet 216:503–510 [View Article][PubMed]
     [Google Scholar]
  35. Mandal T. N., Mahdi A. A., Sharples G. J., Lloyd R. G. ( 1993). Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB, and ruvC mutations. J Bacteriol 175:4325–4334[PubMed]
     [Google Scholar]
  36. Matson S. W., Robertson A. B. ( 2006). The UvrD helicase and its modulation by the mismatch repair protein MutL. Nucleic Acids Res 34:4089–4097 [View Article][PubMed]
     [Google Scholar]
  37. Michel B., Boubakri H., Baharoglu Z., LeMasson M., Lestini R. ( 2007). Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst) 6:967–980 [View Article][PubMed]
     [Google Scholar]
  38. Miller J. H. ( 1992). A Short Course in Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  39. Mohanty B. K., Kushner S. R. ( 2000). Polynucleotide phosphorylase functions both as a 3′→5′ exonuclease and a poly(A) polymerase in Escherichia coli . Proc Natl Acad Sci U S A 97:11966–11971 [View Article][PubMed]
     [Google Scholar]
  40. Nierlich D. P., Murakawa G. J. ( 1996). The decay of bacterial messenger RNA. Prog Nucleic Acid Res Mol Biol 52:153–216 [View Article][PubMed]
     [Google Scholar]
  41. Perry K. L., Elledge S. J., Mitchell B. B., Marsh L., Walker G. C. ( 1985). umuDC and mucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc Natl Acad Sci U S A 82:4331–4335 [View Article][PubMed]
     [Google Scholar]
  42. Pham P., Seitz E. M., Saveliev S., Shen X., Woodgate R., Cox M. M., Goodman M. F. ( 2002). Two distinct modes of RecA action are required for DNA polymerase V-catalyzed translesion synthesis. Proc Natl Acad Sci U S A 99:11061–11066 [View Article][PubMed]
     [Google Scholar]
  43. Piazza F., Zappone M., Sana M., Briani F., Dehò G. ( 1996). Polynucleotide phosphorylase of Escherichia coli is required for the establishment of bacteriophage P4 immunity. J Bacteriol 178:5513–5521[PubMed]
     [Google Scholar]
  44. Py B., Causton H., Mudd E. A., Higgins C. F. ( 1994). A protein complex mediating mRNA degradation in Escherichia coli . Mol Microbiol 14:717–729 [View Article][PubMed]
     [Google Scholar]
  45. Register J. C. III, Griffith J. ( 1985). 10 nm RecA protein filaments formed in the presence of Mg2+ and ATPγS may contain RNA. Mol Gen Genet 199:415–420 [View Article][PubMed]
     [Google Scholar]
  46. Regonesi M. E., Briani F., Ghetta A., Zangrossi S., Ghisotti D., Tortora P., Dehò G. ( 2004). A mutation in polynucleotide phosphorylase from Escherichia coli impairing RNA binding and degradosome stability. Nucleic Acids Res 32:1006–1017 [View Article][PubMed]
     [Google Scholar]
  47. Setlow R. B., Swenson P. A., Carrier W. L. ( 1963). Thymine dimers and inhibition of DNA synthesis by ultraviolet irradiation of cells. Science 142:1464–1466 [View Article][PubMed]
     [Google Scholar]
  48. Sinha R. P., Häder D. P. ( 2002). UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236 [View Article][PubMed]
     [Google Scholar]
  49. Steinborn G. ( 1979). Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. II. Further evidence for a novel function in error-prone repair. Mol Gen Genet 175:203–208 [View Article][PubMed]
     [Google Scholar]
  50. Tseng Y. C., Hung J. L., Wang T. C. V. ( 1994). Involvement of RecF pathway recombination genes in postreplication repair in UV-irradiated Escherichia coli cells. Mutat Res 315:1–9[PubMed] [CrossRef]
     [Google Scholar]
  51. Umitsuki G., Wachi M., Takada A., Hikichi T., Nagai K. ( 2001). Involvement of RNase G in in vivo mRNA metabolism in Escherichia coli . Genes Cells 6:403–410 [View Article][PubMed]
     [Google Scholar]
  52. Viswanathan M., Lovett S. T. ( 1998). Single-strand DNA-specific exonucleases in Escherichia coli. Roles in repair and mutation avoidance. Genetics 149:7–16[PubMed]
     [Google Scholar]
  53. Viswanathan M., Lanjuin A., Lovett S. T. ( 1999). Identification of RNase T as a high-copy suppressor of the UV sensitivity associated with single-strand DNA exonuclease deficiency in Escherichia coli . Genetics 151:929–934[PubMed]
     [Google Scholar]
  54. Wang T. C., Smith K. C. ( 1983). Mechanisms for recF-dependent and recB-dependent pathways of postreplication repair in UV-irradiated Escherichia coli uvrB . J Bacteriol 156:1093–1098[PubMed]
     [Google Scholar]
  55. Wu J., Jiang Z., Liu M., Gong X., Wu S., Burns C. M., Li Z. ( 2009). Polynucleotide phosphorylase protects Escherichia coli against oxidative stress. Biochemistry 48:2012–2020 [View Article][PubMed]
     [Google Scholar]
  56. Zahradka D., Zahradka K., Petranović M., Dermić D., Brcić-Kostić K. ( 2002). The RuvABC resolvase is indispensable for recombinational repair in sbcB15 mutants of Escherichia coli . J Bacteriol 184:4141–4147 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.056309-0
Loading
Involvement of pnp in survival of UV radiation in Escherichia coli K-12
Microbiology 158, 1196 (2012); https://doi.org/10.1099/mic.0.056309-0
/content/journal/micro/10.1099/mic.0.056309-0
/content/journal/micro/10.1099/mic.0.056309-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error