Interaction of apurinic/apyrimidinic endonucleases Nfo and ExoA with the DNA integrity scanning protein DisA in the processing of oxidative DNA damage during Bacillus subtilis spore outgrowth

Journal of Bacteriology

Volumn 196, Issue 3, 2014, Pages 568-578

  Campos, Silvia S ^a   Ibarra Rodriguez, Juan R ^a   Barajas Ornelas, Rocío C ^a   Ramírez Guadiana, Fernando H ^a   Obregón Herrera, Armando ^a   Setlow, Peter ^b   Pedraza Reyes, Mario ^a  

^a UNIVERSITY OF GUANAJUATO   (Mexico)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; BACTERIAL PROTEIN; BETA GALACTOSIDASE; DISA PROTEIN; DNA; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; ENDONUCLEASE EXOA; ENDONUCLEASE NFO; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL SPORE; BACTERIAL STRAIN; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; FLUORESCENCE MICROSCOPY; GENE DISRUPTION; GENE EXPRESSION; GENE OVEREXPRESSION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SPORE GERMINATION; SPOROGENESIS; VEGETATIVE GROWTH; WILD TYPE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA DAMAGE; DNA, BACTERIAL; ENDONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; OXIDATIVE STRESS; SPORES, BACTERIAL;

EID: 84892379975     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01259-13     Document Type: Article

References (41)

1. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64:548-572. http://dx.doi.org/10.1128/MMBR.64.3.548-572.2000.
2. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101:514-525. http://dx.doi.org/10.1111/j.1365-2672.2005.02736.x.
3. Pedraza-Reyes M, Ramírez-Ramírez N, Vidales-Rodríguez LE, Robleto EA. 2012. Mechanisms of bacterial spores survival, p 73-84. In Abel-Santos E (ed), Bacterial spores: current research and applications. Caister Academic Press, Norfolk, United Kingdom.
4. Setlow P. 2007. I will survive: DNA protection in bacterial spores. Trends Microbiol. 15:172-180. http://dx.doi.org/10.1016/j.tim.2007.02.004.
5. Paidhungat M, Setlow P. 2001. Spore germination and outgrowth, p537-548. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and its relatives: from genes to cells. ASM Press, Washington, DC.
6. Setlow P. 2003. Spore germination. Curr. Opin. Microbiol. 6:550-556. http://dx.doi.org/10.1016/j.mib.2003.10.001.
7. Setlow P. 1988. Small, acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function and degradation. Annu. Rev. Microbiol. 42:319-338. http://dx.doi.org/10.1146/annurev.mi.42.100188.001535.
8. Ibarra JR, Orozco AD, Rojas JA, López K, Setlow P, Yasbin RE, Pedraza-Reyes M. 2008. Role of the Nfo and ExoA apurinic/apyrimidinic endonucleases in repair of DNA damage during outgrowth of Bacillus subtilis spores. J. Bacteriol. 190:2031-2038. http://dx.doi.org/10.1128/JB.01625-07.
9. Keijser JF, Ter Beek A, Rauwerda H, Schuren F, Montijn R, van der Spek H, Brul S. 2007. Analysis of temporal gene expression during Bacillus subtilis spore germination and outgrowth. J. Bacteriol. 189:3624-3634. http://dx.doi.org/10.1128/JB.01736-06.
10. Setlow B, Setlow P. 1996. Role of DNA repair in Bacillus subtilis spore resistance. J. Bacteriol. 178:3486-3495.
11. Burkholder WF, Kurtser I, Grossman AD. 2001. Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104:269-279. http://dx.doi.org/10.1016/S0092-8674(01)00211-2.
12. Veening JW, Murray H, Errington J. 2009. A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes Dev. 23:1959-1970. http://dx.doi.org/10.1101/gad.528209.
13. Bejerano-Sagie M, Oppenheimer-Shaanan Y, Berlatzky I, Rouvinski A, Meyerovich M, Ben-Yehuda S. 2006. A checkpoint protein that scans the chromosome for damage at the start of sporulation in Bacillus subtilis. Cell 125:679-690. http://dx.doi.org/10.1016/j.cell.2006.03.039.
14. Oppenheimer-Shaanan Y, Wexselblatt E, Katzhendler J, Yavin E, Ben-Yehuda S. 2011. c-di-AMP reportsDNAintegrity during sporulation in Bacillus subtilis. EMBO Rep. 12:594-601. http://dx.doi.org/10.1038/embor.2011.77.
15. Salas-Pacheco JM, Setlow B, Setlow P, Pedraza-Reyes M. 2005. Role of the Nfo (YqfS) and ExoA apurinic/apyrimidinic endonucleases in protecting Bacillus subtilis spores from DNA damage. J. Bacteriol. 187:7374-7381. http://dx.doi.org/10.1128/JB.187.21.7374-7381.2005.
16. Vagner V, Dervyn E, Ehrlich SD. 1998. A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144:3097-3104. http://dx.doi.org/10.1099/00221287-144-11-3097.
17. Kaltwasser M, Wiegert T, Schumann W. 2002. Construction and application of epitope- and green fluorescent protein-tagging integration vectors for Bacillus subtilis. Appl. Environ. Microbiol. 68:2624-2628. http://dx.doi.org/10.1128/AEM.68.5.2624-2628.2002.
18. Barraza-Salas M, Ibarra-Rodríguez JR, Mellado SJ, Salas-Pacheco JM, Setlow P, Pedraza-Reyes M. 2010. Effects of forespore-specific overexpression of apurinic/apyrimidinic endonuclease Nfo on the DNA-damage resistance properties of Bacillus subtilis spores. FEMS Microbiol. Lett. 302:159-165. http://dx.doi.org/10.1111/j.1574-6968.2009.01845.x.
19. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Nicholson WL, Setlow P. 1990. Sporulation, germination, and outgrowth, p 391-450. In Harwood CR, Cutting SM (ed), Molecular biological methods for Bacillus. John Wiley&Sons, Sussex, England.
21. Cutting SM, Vander Horn PB. 1990. Genetic analysis, p 27-74. In Harwood CR, Cutting SM (ed), Molecular biological methods for Bacillus. John Wiley&Sons, Sussex, England.
22. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
23. Boylan RJ, Mendelson NH, Brooks D, Young FE. 1972. Regulation of the bacterial cell wall: analysis of a mutant of Bacillus subtilis defective in biosynthesis of teichoic acid. J. Bacteriol. 110:281-290.
24. Ghosh S, Setlow P. 2009. Isolation and characterization of superdormant spores of Bacillus species. J. Bacteriol. 191:1787-1797. http://dx.doi.org/10.1128/JB.01668-08.
25. Schaeffer P, Millet J, Aubert JP. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. U. S. A. 54:704-711. http://dx.doi.org/10.1073/pnas.54.3.704.
26. Pedraza-Reyes M, Gutierrez-Corona F, Nicholson WL. 1994. Temporal regulation and forespore-specific expression of the spore photoproduct lyase gene by sigma-G RNA polymerase during Bacillus subtilis sporulation. J. Bacteriol. 176:3983-3991.
27. Mason JM, Hackett RH, Setlow P. 1988. Regulation of expression of genes coding for small, acid-soluble proteins of Bacillus subtilis spores: studies using lacZ gene fusions. J. Bacteriol. 170:239-244.
28. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T. 2006. DNA repair and mutagenesis 2nd ed. ASM PressWashington, DC
29. Barzilai A, Yamamoto K. 2004.DNAdamage responses to oxidative stress.DNA Repair 3:1109-1115. http://dx.doi.org/10.1016/j.dnarep.2004.03.002.
30. Cabrera-Martínez RM, Tovar-Rojo F, Vepachedu VR, Setlow P. 2003. Effects of overexpression of nutrient receptors on germination of spores of Bacillus subtilis. J. Bacteriol. 185:2457-2464. http://dx.doi.org/10.1128/JB.185.8.2457-2464.2003.
31. Paidhungat M, Setlow P. 2001. Localization of a germinant receptor protein (GerBA) to the inner membrane of Bacillus subtilis spores. J. Bacteriol. 183:3982-3990. http://dx.doi.org/10.1128/JB.183.13.3982-3990.2001.
32. Witte G, Hartung S, Büttner K, Hopfner KP. 2008. Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol. Cell 30:167-178. http://dx.doi.org/10.1016/j.molcel.2008.02.020.
33. Urtiz-Estrada N, Salas-Pacheco JM, Yasbin RE, Pedraza-Reyes M. 2003. Forespore-specific expression of Bacillus subtilis yqfS, which encodes type IV apurinic/apyrimidinic endonuclease, a component of the base excision repair pathway. J. Bacteriol. 185:340-348. http://dx.doi.org/10.1128/JB.185.1.340-348.2003.
34. Moeller R, Setlow P, Pedraza-Reyes M, Okayasu R, Reitz G, Nicholson WL. 2011. Role of the Nfo and ExoA apurinic/apyrimidinic endonucleases in radiation resistance and radiation-induced mutagenesis of Bacillus subtilis spores. J. Bacteriol. J. Bacteriol. 193:2875-2879. http://dx.doi.org/10.1128/JB.00134-11.
35. Hecker M, Pané-Farré J, Völker U. 2007. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 61:215-236. http://dx.doi.org/10.1146/annurev.micro.61.080706.093445.
36. Moeller R. 2008. Characterization of different types of radiation- and pressure-induced DNA damage in Bacillus subtilis spores and their global transcriptional response during spore germination. Ph.D. thesis. University of Carolo-Wilhelmina, Braunschweig, Germany.
37. Krüger E, Msadek T, Hecker M. 1996. Alternate promoters direct stressinduced transcription of the Bacillus subtilis clpC operon. Mol. Microbiol. 20:713-723. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02511.x.
38. M regulon and its contribution to cell envelope stress responses. Mol. Microbiol. 67:830-848. http://dx.doi.org/10.1111/j.1365-2958.2007.06090.x.
39. Fuangthong M, Herbig AF, Bsat N, Helmann JD. 2002. Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible. J. Bacteriol. 184:3276-3286. http://dx.doi.org/10.1128/JB.184.12.3276-3286.2002.
40. + and DNA repair-deficient strains. J. Bacteriol. 170:1467-1474.
41. Guillet M, Boiteux S. 2002. Endogenous DNA abasic sites cause cell death in the absence of Apn1, Apn2 and Rad1/Rad10 in Saccharomyces cerevisiae. EMBO J. 21:283-2841. http://dx.doi.org/10.1093/emboj/21.11.2833.