Analysis of Deinococcus radiodurans's transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance

Genetics

Volumn 168, Issue 1, 2004, Pages 21-33

  Tanaka, Masashi ^a,d   Earl, Ashlee M ^a,e   Howell, Heather A ^b   Park, Mie Jung ^a,f   Eisen, Jonathan A ^b   Peterson, Scott N ^b,c   Battista, John R ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b J CRAIG VENTER INSTITUTE   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^d KAGOSHIMA UNIVERSITY   (Japan)

^e HARVARD MEDICAL SCHOOL   (United States)

^f PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOPROTEIN; GENE PRODUCT; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL STRAIN; DEINOCOCCUS RADIODURANS; DESICCATION; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; GENETIC CODE; GENETIC COMPLEMENTATION; GENETIC IDENTIFICATION; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RADIATION DOSE; RADIOSENSITIVITY; RECA GENE; TRANSCRIPTION INITIATION;

DEINOCOCCUS; DOSE-RESPONSE RELATIONSHIP, RADIATION; EPISTASIS, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RADIATION TOLERANCE; RADIATION, IONIZING; REC A RECOMBINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; WATER LOSS, INSENSIBLE;

BACTERIA (MICROORGANISMS); DEINOCOCCUS; DEINOCOCCUS RADIODURANS; POSIBACTERIA; TRIXIS;

EID: 5144234957     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.029249     Document Type: Article

References (45)

1. AGOSTINI, H. J., J. D. CARROLL and K. W. MINTON, 1996 Identification and characterization of uvrA, a DNA repair gene of Deinococcus radiodurans. J. Bacteriol. 178: 6759-6765.
2. ALMIRON, M., A. J. LINK, D. FURLONG and R. KOLTER, 1992 A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6: 2646-2654.
3. BADARINARAYANA, V., P. W. ESTEP, 3RD, J. SHENDURE, J. EDWARDS, S. TAVAZOIE et al., 2001 Selection analyses of insertional mutants using subgenic-resolution arrays. Nat. Biotechnol. 19:1060-1065.
4. BATTISTA, J. R., 1997 Against all odds: the survival strategies of Deinococcus radiodurans. Annu. Rev. Microbiol. 51: 203-224.
5. BATTISTA, J. R., 2000 Radiation resistance: the fragments that remain. Curr. Biol. 10: R204-R205.
6. BATTISTA, J. R., A. M. EARL and M. J. PARK, 1999 Why is Deinococcus radiodurans so resistant to ionizing radiation? Trends Microbiol. 7: 362-365.
7. DALY, M. J., and K. W. MINTON, 1995 Interchromosomal recombination in the extremely radioresistant bacterium Deinococcus radiodurans. J. Bacteriol. 177: 5495-5505.
8. DALY, M. J., and K. W. MINTON, 1996 An alternative pathway of recombination of chromosomal fragments precedes recA-dependent recombination in the radioresistant bacterium Deinococcus radiodurans. J. Bacteriol. 178: 4461-4471.
9. DEAN, C. J., P. FELDSCHREIBER and J. T. LETT, 1966 Repair of x-ray damage to the deoxyribonucleic acid in Micrococcus radiodurans. Nature 209: 49-52.
10. DEAN, C. J., M. G. ORMEROD, R. W. SERIANNI and P. ALEXANDER, 1969 DNA strand breakage in cells irradiated with X-rays. Nature 222: 1042-1044.
11. DOSE, K., A. BIEGER-DOSE, M. LABUSCH and M. GILL, 1992 Survival in extreme dryness and DNA-single strand breaks. Adv. Space Res. 12: 221-229.
12. EARL, A. M., M. M. MOHUNDRO, I. S. MIAN and J. R. BATTISTA, 2002 The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression. J. Bacteriol. 184: 6216-6224.
13. EDWARDS J. S., and J. R. BATTISTA, 2003 Using DNA microarray data to understand the ionizing radiation resistance of Deinococcus radiodurans. Trends Biotechnol. 21: 381-382.
14. EISEN, J. A., and P. C. HANAWALT, 1999 A phylogenomic study of DNA repair genes, proteins, and processes. Mutat. Res. 435: 171-213.
15. FUNAYAMA, T., I. NARUMI, M. KIKUCHI, S. KITAYAMA, H. WATANABE et al., 1999 Identification and disruption analysis of the recN gene in the extremely radioresistant bacterium Deinococcus radiodurans. Mutat. Res. 435: 151-161.
16. GAO, G., B. TIAN, L. LIU, D. SHENG, B. SHEN et al., 2003 Expression of Deinococcus radiodurans PprI enhances the radioresistance of Escherichia coli. DNA Repair 2: 1419-1427.
17. GUTMAN, P. D., P. FUCHS, L. OUYANG and K. W. MINTON, 1993 Identification, sequencing, and targeted mutagenesis of a DNA polymerase gene required for the extreme radioresistance of Deinococcus radiodurans. J. Bacteriol. 175: 3581-3590.
18. GUTMAN, P. D., J. D. CARROLL, C. I. MASTERS and K. W. MINTON, 1994 Sequencing, targeted mutagenesis and expression of a recA gene required for the extreme radioresistance of Deinococcus radiodurans. Gene 141: 31-37.
19. HARRIS, D. R., M. TANAKA, S. V. SAVELIEV, E. JOLIVET, A. M. EARL et al., 2004 Preserving genome integrity: the DdrA protein of Deinococcus radiodurans R1. PLOS Biol. 2 (in press).
20. HORTON, R. M., H. D. HUNT, S. N. HO J. K. PULLEN and L. R. PEASE, 1989 Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
21. HUA, Y., I. NARUMI, G. GAO, B. TIAN, K. SATOH et al., 2003 PprI: a general switch responsible for extreme radioresistance of Deinococcus radiodurans. Biochem. Biophys. Res. Commun. 306:354-360.
22. IYER, L. M., E. V. KOONIN and L. ARAVIND, 2002 Classification and evolutionary history of the single-strand annealing proteins, RecT, Redβ, ERF and RAD52. BMC Genomics 3: 8.
23. KITAYAMA, S., and A. MATSUYAMA, 1971 Double-strand scissions in DNA of gamma-irradiated Micrococcus radiodurans and their repair during postirradiation incubation. Agric. Biol. Chem. 35: 644-652.
24. KITAYAMA, S., M. KOHOROKU, A. TAKAGI and H. ITOH, 1997 Mutation of D. radiodurans in a gene homologous to ruvB of E. coli. Mutat. Res. 385: 151-157.
25. LEES-MILLER, S. P., and K. MEEK, 2003 Repair of DNA double strand breaks by non-homologous end joining. Biochimie 85: 1161-1173.
26. LETT, J. T., P. FELDSCHREIBER, J. G. LITTLE, K. STEELE and C. J. DEAN, 1967 The repair of x-ray damage to the deoxyribonucleic acid in Micrococcus radiodurans: a study of the excision process. Proc. R. Soc. Lond. Ser. B Biol. Sci. 167: 184-201.
27. LIPTON, M. S., L. PASA-TOLIC, G. A. ANDERSON, D. J. ANDERSON, D. L. AUBERRY et al., 2002 Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc. Natl. Acad. Sci. USA 99: 11049-11054.
28. LIU, Y., J. ZHOU, M. V. OMELCHENKO, A. S. BELIAEV, A. VENKATESWARAN et al., 2003 Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl. Acad. Sci. USA 100: 4191-4196.
29. MAKAROVA, K. S., L. ARAVIND, Y. I. WOLF, R. L. TATUSOV, K. W. MINTON et al., 2001 Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev. 65: 44-79.
30. MARTINEZ, A., and R. KOLTER, 1997 Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179: 5188-5194.
31. MATTIMORE, V., and J. R. BATTISTA, 1996 Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J. Bacteriol. 178: 633-637.
32. MATTIMORE, V., K. S. UDUPA, G. A. BERNE and J. R. BATTISTA, 1995 Genetic characterization of forty ionizing radiation-sensitive strains of Deinococcus radiodurans: linkage information from transformation. J. Bacteriol. 177: 5232-5237.
33. MENZEL, R., and M. GELLERT, 1983 Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell 34: 105-113.
34. MOSKOVITZ, J., M. A. RAHMAN, J. STRASSMAN, S. O. YANCEY, S. R. KUSHNER et al., 1995 Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J. Bacteriol. 177: 502-507.
35. NARUMI, I., 2003 Unlocking radiation resistance mechanisms: still a long way to go. Trends Microbiol. 11: 422-425.
36. NARUMI, I., K. SATOH, M. KIKUCHI, T. FUNAYAMA, S. KITAYAMA et al., 1999 Molecular analysis of the Deinococcus radiodurans recA locus and identification of a mutation site in a DNA repair-deficient mutant, rec30. Mutat. Res. 435: 233-243.
37. PETERSON, S., R. T. CLINE, H. TETTELIN, V. SHAROV and D. A. MORRISON, 2000 Gene expression analysis of the Streptococcus pneumoniae competence regulons by use of DNA microarrays. J. Bacteriol. 182: 6192-6202.
38. RUAN, B., H. NAKANO, M. TANAKA, J. A. MILLS, J. A. et al., 2004 Cysteinyl-tRNA(Cys) formation in Methanocaldococcus jannaschii: the mechanism is still unknown. J. Bacteriol. 186: 8-14.
39. SATOH, K., I. NARUMI, M. KIKUCHI, S. KITAYAMA, T. YANAGISAWA et al., 2002 Characterization of RecA424 and RecA670 proteins from Deinococcus radiodurans. J. Biochem. 131: 121-129.
40. TURNER, R. J., J. H. WEINER and D. E. TAYLOR, 1999 Tellurite-mediated thiol oxidation in Escherichia coli. Microbiology 145 (9): 2549-2557.
41. UDUPA, K. S., P. A. O'CAIN, V. MATTIMORE and J. R. BATTISTA, 1994 Novel ionizing radiation-sensitive mutants of Deinococcus radiodurans. J. Bacteriol. 176: 7439-7446.
42. VUKOVIC-NAGY, B., B. W. FOX and M. FOX, 1974 The release of a deoxyribonucleic acid fragment after x-irradiation of Micrococcus radiodurans. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 25: 329-337.
43. WARD, J. F., 1975 Molecular mechanisms of radiation-induced damage to nucleic acids. Adv. Radiat. Biol. 5: 181-239.
44. WHITE, O., J. A. EISEN, J. F. HEIDELBERG, E. K. HICKEY, J. D. PETERSON et al., 1999 Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286: 1571-1577.
45. WINZELER, E. A., D. D. SHOEMAKER, A. ASTROMOFF, H. LIANG, K. ANDERSON et al., 1999 Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.