Regulation of Mutagenic DNA Polymerase V Activation in Space and Time

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Escherichia coli, and many other bacteria, respond to high levels of DNA damage with an inducible system called the SOS response. In this response, bacteria first try to restart replication using non-mutagenic DNA repair strategies. If that fails, replication can be restored using DNA polymerases that simply replicate over DNA lesions, a desperation strategy that results in mutations. DNA polymerase V (pol V) is responsible for most mutagenesis that accompanies the SOS response. Because of the risk inherent to elevated mutation levels, pol V activation is tightly constrained. This report introduces a new layer of regulation on pol V activation, with a novel spatial component. After synthesis, the UmuC subunit of pol V is sequestered transiently at the membrane. Release into the cytosol and final activation depends on the activity of RecA protein and the autocatalytic cleavage of UmuD to generate the UmuD' subunit of pol V. The resulting delay in activation represents an additional molecular mechanism that limits the amount of time that this sometimes necessary but potentially detrimental enzyme spends on the DNA.

Vyšlo v časopise: Regulation of Mutagenic DNA Polymerase V Activation in Space and Time. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005482
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005482

Souhrn

Zdroje

1. Kornberg A, Baker TA (1992) DNA Replication. New York: W. H. Freeman & Co.

2. Bloom LB, Chen X, Fygenson DK, Turner J, O'Donnell M, et al. (1997) Fidelity of Escherichia coli DNA polymerase III holoenzyme. The effects of beta, gamma complex processivity proteins and epsilon proofreading exonuclease on nucleotide misincorporation efficiencies. J Biol Chem 272: 27919–27930. 9346941

3. Borden A, O'Grady PI, Vandewiele D, Fernandez de Henestrosa AR, Lawrence CW, et al. (2002) Escherichia coli DNA Polymerase III Can Replicate Efficiently past a T-T cis-syn Cyclobutane Dimer if DNA Polymerase V and the 3' to 5' Exonuclease Proofreading Function Encoded by dnaQ Are Inactivated. J Bacteriol 184: 2674–2681. 11976296

4. Sommer S, Boudsocq F, Devoret R, Bailone A (1998) Specific RecA amino acid changes affect RecA-UmuD'C interaction. Mol Microbiol 28: 281–291. 9622353

5. Tang M, Shen X, Frank EG, O'Donnell M, Woodgate R, et al. (1999) UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc Natl Acad Sci U S A 96: 8919–8924. 10430871

6. Kato T, Shinoura Y (1977) Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol Gen Genet 156: 121–131. 340898

7. Corzett CH, Goodman MF, Finkel SE (2013) Competitive Fitness During Feast and Famine: How SOS DNA Polymerases Influence Physiology and Evolution in Escherichia coli. Genetics 194: 409–420. doi: 10.1534/genetics.113.151837 23589461

8. MacLean RC, Torres-Barcelo C, Moxon R (2013) Evaluating evolutionary models of stress-induced mutagenesis in bacteria. Nat Rev Genet 14: 221–227. doi: 10.1038/nrg3415 23400102

9. Fernandez De Henestrosa AR, Ogi T, Aoyagi S, Chafin D, Hayes JJ, et al. (2000) Identification of additional genes belonging to the LexA regulon in Escherichia coli. Mol Microbiol 35: 1560–1572. 10760155

10. Frank EG, Ennis DG, Gonzalez M, Levine AS, Woodgate R (1996) Regulation of SOS mutagenesis by proteolysis. Proc Natl Acad Sci U S A 93: 10291–10296. 8816793

11. Karata K, Vaisman A, Goodman MF, Woodgate R (2012) Simple and efficient purification of Escherichia coli DNA polymerase V: cofactor requirements for optimal activity and processivity in vitro. DNA Repair (Amst) 11: 431–440.

12. Nohmi T, Battista JR, Dodson LA, Walker GC (1988) RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc Natl Acad Sci U S A 85: 1816–1820. 3279418

13. Jiang Q, Karata K, Woodgate R, Cox MM, Goodman MF (2009) The active form of DNA polymerase V is UmuD'(2)C-RecA-ATP. Nature 460: 359–363. doi: 10.1038/nature08178 19606142

14. Erdem AL, Jaszczur M, Bertram JG, Woodgate R, Cox MM, et al. (2014) DNA polymerase V activity is autoregulated by a novel intrinsic DNA-dependent ATPase. Elife 3: e02384. doi: 10.7554/eLife.02384 24843026

15. Woodgate R, Ennis DG (1991) Levels of chromosomally encoded Umu proteins and requirements for in vivo UmuD cleavage. Mol Gen Genet 229: 10–16. 1654503

16. Frank EG, Gonzalez M, Ennis DG, Levine AS, Woodgate R (1996) In vivo stability of the Umu mutagenesis proteins: a major role for RecA. J Bacteriol 178: 3550–3556. 8655553

17. Witkin EM, McCall JO, Volkert MR, Wermundsen IE (1982) Constitutive expression of SOS functions and modulation of mutagenesis resulting from resolution of genetic instability at or near the recA locus of Escherichia coli. Mol Gen Genet 185: 43–50. 6211591

18. Vlasic I, Simatovic A, Brcic-Kostic K (2011) Genetic requirements for high constitutive SOS expression in recA730 mutants of Escherichia coli. J Bacteriol 193: 4643–4651. doi: 10.1128/JB.00368-11 21764927

19. Schlacher K, Cox MM, Woodgate R, Goodman MF (2006) RecA acts in trans to allow replication of damaged DNA by DNA polymerase V. Nature 442: 883–887. 16929290

20. Yeeles JT, Marians KJ (2011) The Escherichia coli replisome is inherently DNA damage tolerant. Science 334: 235–238. doi: 10.1126/science.1209111 21998391

21. Indiani C, Patel M, Goodman MF, O'Donnell ME (2013) RecA acts as a switch to regulate polymerase occupancy in a moving replication fork. Proc Natl Acad Sci U S A 110: 5410–5415. doi: 10.1073/pnas.1303301110 23509251

22. Reyes-Lamothe R, Sherratt DJ, Leake MC (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328: 498–501. doi: 10.1126/science.1185757 20413500

23. Elbaz Y, Schuldiner M (2011). Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci 36: 616–623. doi: 10.1016/j.tibs.2011.08.004 21958688

24. Fu MM, Holzbaur ELF (2014). Integrated regulation of motor-driven organelle transport by scaffolding proteins. Trends Cell Biol 24: 564–574. doi: 10.1016/j.tcb.2014.05.002 24953741

25. Kim YJ, Hernandez MLG, Balla T (2013). Inositol lipid regulation of lipid transfer in specialized membrane domains. Trends Cell Biol 23: 270–278. doi: 10.1016/j.tcb.2013.01.009 23489878

26. Langeberg LK, Scott JD (2015). Signalling scaffolds and local organization of cellular behaviour. Nature Rev Mol Cell Biol 16: 232–244.

27. Schuh AL, Audhya A (2014). The ESCRT machinery: From the plasma membrane to endosomes and back again. Crit Rev Biochem Mol Biol 49: 242–261. doi: 10.3109/10409238.2014.881777 24456136

28. Sweetlove LJ, Fernie AR (2013). The Spatial Organization of Metabolism Within the Plant Cell. Annu Rev Plant Biol, 64: 723–746. doi: 10.1146/annurev-arplant-050312-120233 23330793

29. Tutucci E, Stutz F (2011). Keeping mRNPs in check during assembly and nuclear export. Nature Rev Mol Cell Biol 12: 376–383.

30. Xu HX, Ren DJ (2015). Lysosomal Physiology. Annu Rev Physiol 77: 57–80. doi: 10.1146/annurev-physiol-021014-071649 25668017

31. Zattas D, Hochstrasser M (2015). Ubiquitin-dependent protein degradation at the yeast endoplasmic reticulum and nuclear envelope. Crit Rev Biochem Mol Biol 50: 1–17. doi: 10.3109/10409238.2014.959889 25231236

32. Chan YW, West SC (2014) Nat Commun 11: 4844.

33. Bruck I, Woodgate R, McEntee K, Goodman MF (1996) Purification of a soluble UmuD'C complex from Escherichia coli: Cooperative binding of UmuD'C to single-stranded DNA. Journal of Biological Chemistry 271: 10767–10774. 8631887

34. Garvey N, St John AC, Witkin EM (1985). Evidence for RecA protein association with the cell membrane and for changes in the levels of major outer membrane proteins in SOS-induced Escherichia coli cells. J Bacteriol 163: 870–876. 3897198

35. Frank EG, Hauser J, Levine AS, Woodgate R (1993). Targeting of the UmuD, UmuD', and MucA' mutagenesis proteins to DNA by RecA protein. Proc Natl Acad Sci U S A 90:8169–8173. 8367479

36. Frank EG, Cheng N, Do CC, Cerritelli ME, Bruck I, Goodman MF, Egelman EH, Woodgate R, Steven AC (2000). Visualization of two binding sites for the Escherichia coli UmuD'(2)C complex (DNA pol V) on RecA-ssDNA filaments. J Mol Biol 297: 585–597. 10731413

37. Gruber AJ, Erdem AL, Sabat G, Karata K, Jaszczur MM, Vo DD, Olsen TM, Woodgate R, Goodman MF, Cox MM (2015). A RecA protein surface required for activation of DNA polymerase V. PLoS Genet 11: e1005066. doi: 10.1371/journal.pgen.1005066 25811184

38. Langston LD, Indiani C, O'Donnell M (2009). Whither the replisome: emerging perspectives on the dynamic nature of the DNA replication machinery. Cell Cycle 8: 2686–2691. 19652539

39. Patel M, Jiang Q, Woodgate R, Cox MM, Goodman MF (2010). A new model for SOS-induced mutagenesis: how RecA protein activates DNA polymerase V. Crit Rev Biochem Mol Biol 45: 171–184. doi: 10.3109/10409238.2010.480968 20441441

40. Fijalkowska IJ, Dunn RL, Schaaper RM (1997) Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J Bacteriol 179: 7435–7445. 9393709

41. Fijalkowska IJ, Schaaper RM, Jonczyk P (2012) DNA replication fidelity in Escherichia coli: a multi-DNA polymerase affair. FEMS Microbiol Rev 36: 1105–1121. doi: 10.1111/j.1574-6976.2012.00338.x 22404288

42. Yeeles JT, Marians KJ (2013) Dynamics of leading-strand lesion skipping by the replisome. Mol Cell 52: 855–865. doi: 10.1016/j.molcel.2013.10.020 24268579

43. Ho C, Kulaeva OI, Levine AS, Woodgate R (1993). A rapid method for cloning mutagenic DNA repair genes: isolation of umu-complementing genes from multidrug resistance plasmids R391, R446b, and R471a. J Bacteriol 175: 5411–5419. 8366028

44. Mead S, Vaisman A, Valjavec-Gratian M, Karata K, Vandewiele D, et al. (2007) Characterization of polVR391: a Y-family polymerase encoded by rumA'B from the IncJ conjugative transposon, R391. Mol Microbiol 63: 797–810. 17302804

45. Miller JH (1992) A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Press.

46. Davis BD, Mingioli ES (1950) Mutants of Escherichia coli requiring methionine or vitamin B12. JBacteriol 60: 17–28.

47. Sedgwick SG, Bridges BA (1972) Evidence for indirect production of DNA strand scissions during mild heating of Escherichia coli. J Gen Microbiol 71: 191–193. 4556972

48. Gonzalez M, Frank EG, McDonald JP, Levine AS, Woodgate R (1998) Structural insights into the regulation of SOS mutagenesis. Acta Biochim Pol 45: 163–172. 9701508

49. McDonald JP, Frank EG, Levine AS, Woodgate R (1998) Intermolecular cleavage by UmuD-like mutagenesis proteins. Proc Natl Acad Sci U S A 95: 1478–1483. 9465040

50. Churchward G, Belin D, Nagamine Y (1984) A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors. Gene 31: 165–171. 6098521

51. Szekeres ES Jr., Woodgate R, Lawrence CW (1996) Substitution of mucAB or rumAB for umuDC alters the relative frequencies of the two classes of mutations induced by a site-specific T-T cyclobutane dimer and the efficiency of translesion DNA synthesis. J Bacteriol 178: 2559–2563. 8626322

52. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453–1462. 9278503

53. Huang LC, Wood EA, Cox MM (1997) Convenient and reversible site-specific targeting of exogenous DNA into a bacterial chromosome by use of the FLP recombinase: the FLIRT system. J Bacteriol 179: 6076–6083. 9324255

54. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675. 22930834

55. Tanner NA, van Oijen AM (2010) Visualizing DNA replication at the single-molecule level. Methods Enzymol 475: 259–278. doi: 10.1016/S0076-6879(10)75011-4 20627161

56. Biteen J.S., Thompson M.A., Tselentis N.K., Bowman G.R., Shapiro L., Moerner W.E. (2008). Super-resolution imaging in live Caulobacter crescentus cells using photoswitchable EYFP. Nat. Methods 5, 947–949. doi: 10.1038/nmeth.1258 18794860

57. Hedde PN, Fuchs J, Oswald F, Wiedenmann J, Nienhaus GU (2009) Online image analysis software for photoactivation localization microscopy. Nat Methods 6: 689–690. doi: 10.1038/nmeth1009-689 19789527

58. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C (2011) High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80: 612–627. doi: 10.1111/j.1365-2958.2011.07579.x 21414037

59. Watkins LP, Yang H (2005) Detection of intensity change points in time-resolved single-molecule measurements. J Phys Chem B 109: 617–628. 16851054

60. Yang H (2011) Change-Point Localization and Wavelet Spectral Analysis of Single-Molecule Time Series. Hoboken, NJ, USA: John Wiley & Sons, Inc.