Repair of UV damage in bacteria

DNA Repair

Volumn 7, Issue 3, 2008, Pages 353-379

  Goosen, Nora ^a   Moolenaar, Geri F ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Archaea; Cryptochrome; Eubacteria; Evolution; Nucleotide excision repair; Photolyase; Pyrimidine dimer glycosylase; Spore photoproduct lyase; UV damage; UV damage endonuclease

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; CHO PROTEIN; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; DNA GLYCOSYLTRANSFERASE; ENDONUCLEASE; PROTEIN CRY1; PROTEIN CRY2; PYRIMIDINE; TRANSCRIPTION REPAIR COUPLING FACTOR; UNCLASSIFIED DRUG; UVRA PROTEIN; UVRB PROTEIN; UVRC PROTEIN;

ACIDOBACTERIA; ACTINOBACTERIA; ADAPTATION; AMINO ACID SEQUENCE; AQUIFICAE; ARCHAEBACTERIUM; BACILLUS SPHAERICUS; BACTERIUM; BACTEROIDETES; CARBOXY TERMINAL SEQUENCE; CHLAMYDIA; CHLOROBI; CHLOROFLEXI; CYANOBACTERIUM; DEINOCOCCUS; DNA DAMAGE; DNA REPAIR; DNA TRANSCRIPTION; EXCISION REPAIR; FIBROBACTERES; FIRMICUTES; FUSOBACTERIA; GENETIC CODE; HABITAT; HYDROPHOBICITY; LIGHT ABSORPTION; MICROCOCCUS LUTEUS; MOLECULAR WEIGHT; NONHUMAN; PHOTOREACTIVITY; PLANCTOMYCETE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEOBACTERIA; REVIEW; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; SPIROCHETE; THERMOTOGAE; THERMUS; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; BACTERIA; DNA DAMAGE; DNA REPAIR; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; ULTRAVIOLET RAYS;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 39049171187     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.09.002     Document Type: Review

References (95)

1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
2. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 (1994) 4673-4680
3. Sancar G.B. Enzymatic photoreactivation: 50 years and counting. Mutat. Res. 451 (2000) 25-37
4. Ahmad M., Jarillo J.A., Smirnova O., and Cashmore A.R. Cryptochrome blue-light photoreceptors of Arabidopsis implicated in phototropism. Nature 392 (1998) 720-723
5. Panda S., Hogenesch J.B., and Kay S.A. Circadian rhythms from flies to human. Nature 417 (1996) 329-335
6. Sancar A., Smith F.W., and Sancar G.B. Purification of Escherichia coli photolyase. J. Biol. Chem. 259 (1984) 6028-6032
7. Tamada T., Kitakodoro K., Higuchi Y., Inaka K., Yasui A., de Ruiter P.E., Eker A.P., and Miki K. Crystal structure of DNA photolyase from Anacystis nidulans. Nat. Struct. Biol. 4 (1997) 887-891
8. Park H.W., Kim S.T., Sancer A., and Deisenhofer J. Crystal structure of DNA photolyase from Escherichia coli. Science 268 (1995) 1866-1872
9. Komori H., Masui R., Kuramitsu S., Yokoyama S., Shibata T., Inoue Y., and Miki K. Crystal structure of thermostable DNA photolyase: pyrimidine dimer recognition mechanism. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 13560-13565
10. Mees A., Klar T., Gnau P., Hennecke U., Eker A.P.M., Carell T., and Essen L.O. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306 (2004) 1789-1793
11. Hitomi K., Okamoto K., Daiyasu H., Miyashita H., Iwai S., Toh H., Ishiura M., and Todo T. Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803. Nucleic Acids Res. 28 (2000) 2353-2362
12. Worthington E.N., Kavakli I.H., Berrocal-Tito G., Bondo B.E., and Sancar A. Purification and characterization of three members of the photolyase/cryptochrome family blue-light photoreceptors from Vibrio cholerae. J. Biol. Chem. 278 (2003) 39143-39154
13. Selby C.P., and Sancar A. A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 17696-17700
14. Brudler R., Hitomi K., Daiyasu H., Toh H., Kucho K., Ishiura M., Kanehisa M., Roberts V.A., Todo T., Tainer J.A., and Getzoff E.D. Identification of a new cryptochrome class: structure, function and evolution. Mol. Cell 11 (2003) 59-67
15. Huang Y., Baxter R., Smith B.S., Partch C.L., Colbert C.L., and Deisenhofer J. Crystal structure of cryptochrome 3 from Arabidopsis thaliana and its implications for photolyase activity. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 17701-17706
16. Todo T., Takemori H., Ryo H., Ihara M., Matsunaga T., Nikaido O., Sato K., and Nomura T. A new photoreacting enzyme that specifically repairs ultraviolet light-induced (6-4) photoproducts. Nature 361 (1993) 371-374
17. Setlow P. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49 (1995) 29-54
18. Fajardo-Cavazos P., Salazar C., and Nicholson W.L. Molecular cloning and characterization of the Bacillus subtilis spore photoproduct lyase (spl) gene, which is involved in repair of UV radiation-induced DNA damage during spore germination. J. Bacteriol. 175 (1993) 1735-1744
19. Rebeil R., and Nicholson W.L. The subunit structure and catalytic mechanism of the Bacillus subtilis DNA repair enzyme spore photoproduct lyase. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 9038-9043
20. Pieck J.C., Hennecke U., Pierik A.J., Friedel M.G., and Carell T. Characterization of a new thermophilic spore photoproduct lyase from Geobacillus stearothermophilus (SplG) with defined lesion containing DNA substrates. J. Biol. Chem. 281 (2006) 36317-36326
21. Friedberg E.C., and King J.J. Dark repair of ultraviolet-irradiated deoxyribonucleic acid by bacteriophage T4: purification and characterization of a dimer-specific phage-induced endonuclease. J. Bacteriol. 106 (1971) 500-507
22. Vassylyev D.G., Kashiwagi T., Mikami Y., Ariyoshi M., Iwai S., Ohtsuka E., and Morikawa K. Atomic model of a pyrimidine dimer excision repair enzyme complexed with a DNA substrate: structural basis for damaged DNA recognition. Cell 83 (1995) 773-782
23. Doi T., Recktenwald A., Karaki Y., Kikuchi M., Morikawa K., Ikehara M., Inaoka T., Hori N., and Ohtsuka E. Role of the basic amino acid cluster and Glu-23 in pyrimidine dimer glycosylase activity of T4 endonuclease V. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 9420-9424
24. Hori N., Doi T., Karaki Y., Kikuchi M., Ikehara M., and Ohtsuka E. Participation of glutamic acid 23 of T4 endonuclease V in the beta-elimination reaction of an abasic site in a synthetic duplex DNA. Nucleic Acids Res. 20 (1993) 4761-4764
25. Dodson M.L., Schrock R.D., and Lloyd R.S. Evidence for an imino intermediate in the T4 endonuclease V reaction. Biochemistry 32 (1993) 8284-8290
26. Golan G., Zharkov D.O., Grollman A.P., Dodson M.L., McCllogh A.K., Lloyd R.S., and Shoham G. Structure of T4 pyrimidine dimer glycosylase in a reduced imine covalent complex with abasic site-containing DNA. J. Mol. Biol. 362 (2006) 241-258
27. Stump D.G., and Lloyd R.S. Site-directed mutagenesis of the T4 endonuclease V gene: role of tyrosine-129 and -131 in pyrimidine dimer-specific binding. Biochemistry 27 (1988) 1839-1848
28. Ishida M., Kanamori Y., Hori N., Inaoka T., and Ohtska E. In vitro and in vivo activities of T4 endonuclease V mutants altered in the C-terminal aromatic region. Biochemistry 29 (1990) 3817-3821
29. Takagi Y., Sekiguchi M., Okubo S., Nakayama H., Shimada K., Yasuda S., Nishimoto T., and Yoshihara H. Nucleases specific for ultraviolet light-irradiated DNA and their possible role in dark repair. Cold Spring Harbor Symp. Quant. Biol. 33 (1968) 219-227
30. Riazuddin S., and Grossman L. Micrococcus luteus correndonucleases. I. Resolution and purification of two endonucleases specific for DNA containing pyrimidine dimmers. J. Biol. Chem. 252 (1977) 6280-6286
31. Carrier W.L., and Setlow R.B. Endonuclease from Micrococcus luteus which has activity toward ultraviolet-irradiated deoxyribonucleic acid: purification and properties. J. Bacteriol. 102 (1970) 178-186
32. Piersen C.E., Prince M.A., Augustine M.L., Dodson M.L., and Lloyd R.S. Purification and cloning of Micrococcus luteus ultraviolet endonuclease, an N-glycosylase/abasic lyase that proceeds via an imino enzyme-DNA intermediate. J. Biol. Chem. 270 (1995) 23475-23484
33. Shiota S., and Nakayama H. UV endonuclease of Micrococcus luteus, a cyclobutane pyrimidine dimer-DNA glycosylase/abasic lyase: cloning and characterization of the gene. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 593-598
34. Katcher H.L., and Wallace S.S. Characterization of the Escherichia coli X-ray endonuclease, endonuclease III. Biochemistry 22 (1983) 4071-4081
35. Thayer M.M., Ahern H., Xing D., Cunningham R.P., and Tainer J.A. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J. 14 (1995) 4108-4120
36. Nyaga S.G., and Lloyd R.S. Two glycosylase/abasic lyases from Neisseria mucosa that initiate DNA repair at sites of UV-induced photoproducts. J. Biol. Chem. 275 (2000) 23569-23576
37. Vasquez D.A., Nyaga S.G., and Lloyd R.S. Purification and characterization of a novel UV lesion-specific DNA glycosylase/AP lyase from Bacillus sphaericus. Mutat. Res. 459 (2000) 307-316
38. Wilson III D.M., Deutsch W.A., and Kelley M.R. Drosophila ribosomal protein S3 contains an activity that cleaves DNA at apurinic/apyrimidinic sites. J. Biol. Chem. 269 (1994) 25359-25364
39. Kim J., Chubatsu L.S., Admon A., Stahl J., Fellous R., and Linn S. Implication of mammalian ribosomal protein S3 in the processing of DNA damage. J. Biol. Chem. 270 (1995) 13620-13629
40. Jung S.-O., Lee J.Y., and Kim J. Yeast ribosomal protein S3 has an endonuclease activity on AP DNA. Mol. Cell 12 (2001) 84-90
41. Bruckner R.C., and Cox M.M. The histone-like H protein of Escherichia coli is ribosomal protein S3. Nucleic Acids Res. 17 (1989) 3145-3161
42. Bowman K.K., Sidik K., Smith C.A., Taylor J.S., Doetsch P.W., and Freyer G.A. A new ATP-independent DNA endonuclease from Schizosaccharomyces pombe that recognizes cyclobutane pyrimidine dimers and 6-4 photoproducts. Nucleic Acids Res. 22 (1994) 3026-3032
43. Takao M., Yonemasu R., Yamamoto K., and Yasui A. Characterization of a UV endonuclease gene from the fission yeast Schizosaccharomyces pombe and its bacterial homolog. Nucleic Acids Res. 7 (1996) 1267-1271
44. Avery A.M., Kaur B., Taylor J.S., Mello J.A., Essigmann J.M., and Doetsch P.W. Substrate specificity of ultraviolet DNA endonuclease (UVDE/Uve1p) from Schizosaccharomyces pombe. Nucleic Acids Res. 27 (1999) 2256-2264
45. Kanno S., Iwai S., Takao M., and Yasui A. Repair of apurinic/apyrimidinic sites by UV damage endonuclease; a repair protein for UV and oxidative damage. Nucleic Acids Res. 27 (1999) 3096-3103
46. Earl A.M., Rankin S.K., Kim K.P., Lamendola O.N., and Battista J.R. Genetic evidence that the uvsE gene product of Deinococcus radiodurans R1 is a UV damage endonuclease. J. Bacteriol. 184 (2002) 1003-1009
47. K. Paspaleva, E. Thomassen, N.S. Pannu, S. Iwai, G.F. Moolenaar, N. Goosen, J.P. Abrahams, Crystal structure of the DNA repair enzyme UV damage endonuclease, Structure 15 (2007).
48. Hosfield D.J., Guan Y., Haas B.J., Cunningham R.P., and Tainer J.A. Structure of the DNA repair enzyme endonuclease IV and its DNA complex: double-nucleotide flipping at abasic sites and three-metal-ion catalysis. Cell 98 (1999) 397-408
49. Pettijohn D.E., and Hanawalt P.C. Evidence for repair replication of ultraviolet damaged DNA in bacteria. J. Mol. Biol. 9 (1964) 395-410
50. van de Putte P., van Sluis C.A., van Dillewijn J., and Rorsch A. The location of genes controlling radiation sensitivity in Escherichia coli. Mutat. Res. 2 (1965) 97-110
51. Howard-Flanders P., Boyce R.P., and Theriot L. Three loci in Escherichia coli K12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics 53 (1966) 1119-1136
52. van Houten B., Croteau D.L., DellaVecchia M.J., Wang H., and Kisker C. 'Close-fitting sleeves': DNA damage recognition by the UvrABC nuclease system. Mutat. Res. 577 (2005) 92-117
53. Truglio J.J., Croteau D.L., van Houten B., and Kisker C. Prokaryotic nucleotide exsion repair, the UvrABC system. Chem. Rev. 106 (2006) 233-252
54. Croteau D.L., Stierum R.H., and Bohr V.A. Mitochondrial DNA repair pathways. Mutat. Res. 434 (1999) 137-148
55. Salerno V., Napoli A., White M.F., Rossi M., and Ciaramella M. Transcriptional response to DNA damage in the archeon Sulfolobus solfataricus. Nucleic Acids Res. 31 (2003) 6127-6138
56. Crowley D.J., Boubriak I., Berquist B.R., Clark M., Richard E., Sullivan L., DasSarma S., and McCready S. The uvrA, uvrB and uvrC genes are required for repair of ultraviolet light induced DNA photoproducts in Halobacterium sp. NRC-1. Saline Systems 13 (2006) 2-11
57. Ogrunc M., Becker D.F., Ragsdale S.W., and Sancar A. Nucleotide excision repair in the third kingdom. J. Bacteriol. 180 (1998) 5796-5798
58. Goosen N., and Moolenaar G.F. Role of ATP hydrolysis by UvrA and UvrB during nucleotide excision repair. Res. Microbiol. 152 (2001) 401-409
59. Wang J., Mueller K.L., and Grossman L. A mutational study of the C-terminal zinc-finger motif of the Escherichia coli UvrA protein. J. Biol. Chem. 269 (1994) 10771-10775
60. Croteau D.L., DellaVecchia M.J., Wang H., Bienstock R.J., Melton M.A., and Van Houten B. The C-terminal zinc finger of UvrA does not bind DNA directly but regulates damage-specific DNA binding J. Biol. Chem. 281 (2006) 26370-26381
61. Visse R., de Ruijter M., Ubbink M., Brandsma J.A., and van de Putte P. The first zinc-binding domain of UvrA is not essential for UvrABC-mediated DNA excision repair. Mutat. Res. 294 (1993) 263-274
62. Lomovskaya N., Hong S.K., Kim S.U., Fonstein L., Furuya K., and Hutchinson R.C. The Streptomyces peucetius drrC gene encodes a UvrA-like protein involved in daunorubicin resistance and production. J. Bacteriol. 178 (1996) 3235-3238
63. Ylihonko K., Tuikkanen J., Jussila S., Cong L., and Mantsala P. A gene cluster involved in nogalamycin biosynthesis from Streptomyces nogalater: sequence analysis and complementation of early-block mutations in the anthracycline pathway. Mol. Gen. Genet. 251 (1996) 113-120
64. Tanaka M., Narumi I., Funayama T., Kikuchi M., Watanabe H., Matsunaga T., Nikaido O., and Yamamoto K. Characterization of pathways dependent on the uvsE, uvrA1, or uvrA2 gene product for UV resistance in Deinococcus radiodurans. J. Bacteriol. 187 (2005) 3693-3697
65. Myles G.M., Hearst J.E., and Sancar A. Site-specific mutagenesis of conserved residues within Walker A and B sequences of Escherichia coli UvrA protein. Biochemistry 30 (1991) 3824-3834
66. Theis K., Chen P.J., Skorvaga M., Van Houten B., and Kisker C. Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair. EMBO J. 18 (1999) 6899-6907
67. Machius M., Henry L., Palnitkar M., and Deisenhofer J. Crystal structure of the DNA nucleotide excision repair protein UvrB from Thermus thermophilus. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 11717-11722
68. Nakagawa N., Sugahara M., Masui R., Kato F., Fukuyama K., and Kuramitsu S. Crystal structure of Thermus thermophilus HB8 UvrB protein, a key enzyme of nucleotide excision repair. J. Biochem. (Tokyo) 126 (1999) 986-990
69. Truglio J.J., Croteau D.L., Skorvaga M., DellaVecchia M.J., Theis K., Mandavilli B.S., Van Houten B., and Kisker C. Interactions between UvrA and UvrB: the role of UvrB's domain 2 in nucleotide excision repair. EMBO J. 23 (2004) 2498-2509
70. Malta E., Moolenaar G.F., and Goosen N. Dynamics of the UvrABC nucleotide excision repair proteins analyzed by fluorescence resonance energy transfer. Biochemistry 46 (2007) 9080-9088
71. Moolenaar G.F., Höglund L., and Goosen N. Clue to damage recognition by UvrB: residues in the β-hairpin structure prevent binding to non-damaged DNA. EMBO J. 20 (2001) 6140-6149
72. Skorvaga M., Theis K., Mandavilli B.S., Kisker C., and Van Houten B. The β-hairpin motif of UvrB is essential for DNA binding, damage processing and UvrC-mediated incisions. J. Biol. Chem. 277 (2002) 1553-1559
73. Malta E., Moolenaar G.F., and Goosen N. Base flipping in nucleotide excision repair. J. Biol. Chem. 281 (2006) 2184-2194
74. Waters T.R., Eryilmaz J., Geddes S., and Barrett T.E. Damage detection by the UvrABC pathway: crystal structure of UvrB bound to fluorescein-adducted DNA. FEBS Lett. 580 (2006) 6423-6427
75. Truglio J.J., Karakas E., Rhau B., Wang H., DellaVecchia M.J., van Houten B., and Kisker C. Structural basis for DNA recognition and processing by UvrB. Nat. Struct. Mol. Biol. 13 (2006) 360-364
76. Alexandrovich A., Sanderson M.R., Moolenaar G.F., Goosen N., and Lane A.N. NMR assignments and secondary structure of the UvrC binding domain of UvrB. FEBS Lett. 451 (1999) 181-185
77. Sohi M., Alexandrovich A., Moolenaar G.F., Visse R., Goosen N., Vernede X., Fontecilla-Camps J.C., Champness J., and Sanderson M.R. Crystal structure of Escherichia coli UvrB C-terminal domain and a model for UvrB-UvrC interaction. FEBS Lett. 465 (2000) 161-164
78. Moolenaar G.F., Franken K.L., van de Putte P., and Goosen N. Function of the homologous regions of the Escherichia coli DNA excision repair proteins UvrB and UvrC in stabilization of the UvrBC-DNA complex and in 3′-incision. Mutat. Res. 385 (1997) 195-203
79. Selby C.P., and Sancar A. Molecular mechanism of transcription-repair coupling. Science 260 (1993) 53-58
80. Deaconescu A.M., Savery N., and Darst S.A. The bacterial transcription repair coupling factor. Curr. Opin. Struct. Biol. 17 (2007) 96-102
81. Assenmacher N., Wenig K., Lammens A., and Hopfner K.P. Structural basis for transcription-coupled repair: the N-terminus of Mfd resembles UvrB with degenerate ATPase motifs. J. Mol. Biol. 355 (2006) 675-683
82. Deaconescu A.M., Chambers A.L., Smith A.J., Nickels B.E., Hochschild A., Savery N.J., and Darst S.A. Structural basis for bacterial transcription-coupled DNA repair. Cell 124 (2006) 507-520
83. Park J.S., Marr M.T., and Roberts J.W. E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109 (2002) 757-767
84. George D.L., and Witkin E.M. Slow excision repair in an mfd mutant of Escherichia coli B/r. Mol. Gen. Genet. 133 (1974) 283-291
85. Zalieckas J.M., Wray L.V.J., Ferson A.E., and Fisher S.H. Transcription-repair coupling factor is involved in carbon catabolite repression of the Bacillus subtilis hut and gnt operons. Mol. Microbiol. 27 (1998) 1031-1038
86. Zeng X., Galinier A., and Saxild H.H. Catabolite repression of dra-nupC-pdp operon expression in Bacillus subtilis. Mol. Microbiol. 146 (2000) 2901-2908
87. Truglio J.J., Rhau B., Croteau D.L., Wang L., Skorvaga M., Karakas E., DellaVecchia M.J., Wang H., Van Houten B., and Kisker C. Structural insights into the first incision reaction during nucleotide excision repair. EMBO J. 24 (2005) 885-894
88. Karakas E., Truglio J.J., Croteau D., Rhau B., Wang L., Van Houten B., and Kisker C. Structure of the C-terminal half of UvrC reveals an RNase H endonuclease domain with an Argonaute-like catalytic triad. EMBO J. 26 (2007) 613-622
89. Singh S., Folkers G.E., Bonvin A.M., Boelens R., Wechselberger R., Niztayev A., and Kaptein R. Solution structure and DNA-binding properties of the C-terminal domain of UvrC from E. coli. EMBO J. 21 (2002) 6257-6266
90. Verhoeven E.E., van Kesteren M., Turner J.J., van der Marel G.A., van Boom J.H., Moolenaar G.F., and Goosen N. The C-terminal region of Escherichia coli UvrC contributes to the flexibility of the UvrABC nucleotide excision repair system. Nucleic Acids Res. 30 (2002) 2492-2500
91. Lin J.J., and Sancar A. Active site of (A)BC excinuclease. I. Evidence for 5′ incision by UvrC through a catalytic site involving Asp399, Asp438, Asp466, and His538 residues. J. Biol. Chem. 267 (1992) 17688-17692
92. Moolenaar G.F., Moorman C., and Goosen N. Role of the Escherichia coli nucleotide excision repair proteins in DNA replication. J. Bacteriol. 182 (2000) 5706-5714
93. Moolenaar G.F., van Rossum-Fikkert S., van Kesteren M., and Goosen N. Cho, a second endonuclease involved in Escherichia coli nucleotide excision repair. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 1467-1472
94. Ryoji M., Katayama H., Fusamae H., Matsuda A., Sakai F., and Utano H. Repair of DNA damage in a mitochondrial lysate of Xenopus laevis oocytes. Nucleic Acids Res. 24 (1996) 4057-4062
95. Zinser E.R., Coe A., Johnson Z.I., Martiny A.C., Fuller N.J., Scanlan D.J., and Chisholm S.W. Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl. Environ. Microbiol. 72 (2006) 723-732