MtSSB may sequester UNG1 at mitochondrial ssDNA and delay uracil processing until the dsDNA conformation is restored

DNA Repair

Volumn 11, Issue 1, 2012, Pages 82-91

  Wollen Steen, Kristian ^a   Doseth, Berit ^a   P Westbye, Marianne ^a   Akbari, Mansour ^a   Kang, Dongchon ^b   Falkenberg, Maria ^c   Slupphaug, Geir ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Base excision repair; Mitochondrial DNA replication; Mitochondrial single strand binding protein; Uracil DNA glycosylase

Indexed keywords

CYTOSINE DERIVATIVE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DOUBLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN; URACIL; URACIL DNA GLYCOSIDASE;

ARTICLE; CONTROLLED STUDY; DEMETHYLATION; DNA REPAIR; ENZYME ACTIVITY; HUMAN; MITOCHONDRION; NONHUMAN; OXIDATION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; BASE SEQUENCE; CARBOXYLIC ESTER HYDROLASES; CELL EXTRACTS; DNA; DNA DAMAGE; DNA GLYCOSYLASES; DNA METHYLATION; DNA, SINGLE-STRANDED; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, TERTIARY; URACIL;

EUKARYOTA;

EID: 84855344195     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2011.10.026     Document Type: Article

References (69)

1. Shapiro R. Damage to DNA caused by hydrolysis, Life Sciences. NATO Advanced Study Institute Series 1981, 13-18. Plenum Press, New York/London. E. Seeberg, K. Kleppe (Eds.).
2. Flores-Rozas H., Kolodner R.D. Links between replication, recombination and genome instability in eukaryotes. Trends Biochem. Sci. 2000, 25:196-200.
3. Garvik B., Carson M., Hartwell L. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell Biol. 1995, 15:6128-6138.
4. Broderick S., Rehmet K., Concannon C., Nasheuer H.P. Eukaryotic single-stranded DNA binding proteins: central factors in genome stability. Subcell. Biochem. 2010, 50:143-163.
5. Wold M.S. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 1997, 66:61-92.
6. Fanning E., Klimovich V., Nager A.R. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 2006, 34:4126-4137.
7. Nagelhus T.A., Haug T., Singh K.K., Keshav K.F., Skorpen F., Otterlei M., Bharati S., Lindmo T., Benichou S., Benarous R., Krokan H.E. A sequence in the N-terminal region of human uracil-DNA glycosylase with homology to XPA interacts with the C-terminal part of the 34-kDa subunit of replication protein A. J. Biol. Chem. 1997, 272:6561-6566.
8. Hagen L., Kavli B., Sousa M.M., Torseth K., Liabakk N.B., Sundheim O., Pena-Diaz J., Otterlei M., Horning O., Jensen O.N., Krokan H.E., Slupphaug G. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J. 2008, 27:51-61.
9. Otterlei M., Warbrick E., Nagelhus T.A., Haug T., Slupphaug G., Akbari M., Aas P.A., Steinsbekk K., Bakke O., Krokan H.E. Post-replicative base excision repair in replication foci. EMBO J. 1999, 18:3834-3844.
10. Lindahl T., Nyberg B. Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry 1974, 13:3405-3410.
11. Frederico L.A., Kunkel T.A., Shaw B.R. A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 1990, 29:2532-2537.
12. Kavli B., Sundheim O., Akbari M., Otterlei M., Nilsen H., Skorpen F., Aas P.A., Hagen L., Krokan H.E., Slupphaug G. hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup. J. Biol. Chem. 2002, 277:39926-39936.
13. Fan J., Matsumoto Y., Wilson D.M. Nucleotide sequence and DNA secondary structure, as well as replication protein A, modulate the single-stranded abasic endonuclease activity of APE1. J. Biol. Chem. 2006, 281:3889-3898.
14. Otterlei M., Kavli B., Standal R., Skjelbred C., Bharati S., Krokan H.E. Repair of chromosomal abasic sites in vivo involves at least three different repair pathways. EMBO J. 2000, 19:5542-5551.
15. Van Dyck E., Foury F., Stillman B., Brill S.J. A single-stranded DNA binding protein required for mitochondrial DNA replication in S. cerevisiae is homologous to E. coli SSB. EMBO J. 1992, 11:3421-3430.
16. Maier D., Farr C.L., Poeck B., Alahari A., Vogel M., Fischer S., Kaguni L.S., Schneuwly S. Mitochondrial single-stranded DNA-binding protein is required for mitochondrial DNA replication and development in Drosophila melanogaster. Mol. Biol. Cell 2001, 12:821-830.
17. Ruhanen H., Borrie S., Szabadkai G., Tyynismaa H., Jones A.W., Kang D., Taanman J.W., Yasukawa T. Mitochondrial single-stranded DNA binding protein is required for maintenance of mitochondrial DNA and 7S DNA but is not required for mitochondrial nucleoid organisation. Biochim. Biophys. Acta 2010, 1803:931-939.
18. Kumar N.V., Varshney U. Contrasting effects of single stranded DNA binding protein on the activity of uracil DNA glycosylase from Escherichia coli towards different DNA substrates. Nucleic Acids Res. 1997, 25:2336-2343.
19. Robberson D.L., Kasamatsu H., Vinograd J. Replication of mitochondrial DNA. Circular replicative intermediates in mouse L cells. Proc. Natl. Acad. Sci. U.S.A. 1972, 69:737-741.
20. Clayton D.A. Replication of animal mitochondrial DNA. Cell 1982, 28:693-705.
21. Fuste J.M., Wanrooij S., Jemt E., Granycome C.E., Cluett T.J., Shi Y., Atanassova N., Holt I.J., Gustafsson C.M., Falkenberg M. Mitochondrial RNA polymerase is needed for activation of the origin of light-strand DNA replication. Mol. Cell 2010, 37:67-78.
22. Van Tuyle G.C., Pavco P.A. Characterization of a rat liver mitochondrial DNA-protein complex. Replicative intermediates are protected against branch migrational loss. J. Biol. Chem. 1981, 256:12772-12779.
23. Mignotte B., Barat M., Mounolou J.C. Characterization of a mitochondrial protein binding to single-stranded DNA. Nucleic Acids Res. 1985, 13:1703-1716.
24. Liu P., Demple B. DNA repair in mammalian mitochondria: much more than we thought?. Environ. Mol. Mutagen. 2010, 51:417-426.
25. Handa P., Acharya N., Varshney U. Chimeras between single-stranded DNA-binding proteins from Escherichia coli and Mycobacterium tuberculosis reveal that their C-terminal domains interact with uracil DNA glycosylases. J. Biol. Chem. 2001, 276:16992-16997.
26. Bharati S., Krokan H.E., Kristiansen L., Otterlei M., Slupphaug G. Human mitochondrial uracil-DNA glycosylase preform (UNG1) is processed to two forms one of which is resistant to inhibition by AP sites. Nucleic Acids Res. 1998, 26:4953-4959.
27. Westbye M.P., Feyzi E., Aas P.A., Vagbo C.B., Talstad V.A., Kavli B., Hagen L., Sundheim O., Akbari M., Liabakk N.B., Slupphaug G., Otterlei M., Krokan H.E. Human AlkB homolog 1 is a mitochondrial protein that demethylates 3-methylcytosine in DNA and RNA. J. Biol. Chem. 2008, 283:25046-25056.
28. Muller T.A., Meek K., Hausinger R.P. Human AlkB homologue 1 (ABH1) exhibits DNA lyase activity at abasic sites. DNA Repair (Amst.) 2010, 9:58-65.
29. Takamatsu C., Umeda S., Ohsato T., Ohno T., Abe Y., Fukuoh A., Shinagawa H., Hamasaki N., Kang D. Regulation of mitochondrial D-loops by transcription factor A and single-stranded DNA-binding protein. EMBO Rep. 2002, 3:451-456.
30. Akbari M., Visnes T., Krokan H.E., Otterlei M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair (Amst.) 2008, 7:605-616.
31. Visnes T., Akbari M., Hagen L., Slupphaug G., Krokan H.E. The rate of base excision repair of uracil is controlled by the initiating glycosylase. DNA Repair (Amst.) 2008, 7:1869-1881.
32. Kavli B., Andersen S., Otterlei M., Liabakk N.B., Imai K., Fischer A., Durandy A., Krokan H.E., Slupphaug G. B cells from hyper-IgM patients carrying UNG mutations lack ability to remove uracil from ssDNA and have elevated genomic uracil. J. Exp. Med. 2005, 201:2011-2021.
33. Korhonen J.A., Gaspari M., Falkenberg M. TWINKLE Has 5'→3' DNA helicase activity and is specifically stimulated by mitochondrial single-stranded DNA-binding protein. J. Biol. Chem. 2003, 278:48627-48632.
34. Slupphaug G., Eftedal I., Kavli B., Bharati S., Helle N.M., Haug T., Levine D.W., Krokan H.E. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry 1995, 34:128-138.
35. Gilljam K.M., Feyzi E., Aas P.A., Sousa M.M., Muller R., Vagbo C.B., Catterall T.C., Liabakk N.B., Slupphaug G., Drablos F., Krokan H.E., Otterlei M. Identification of a novel, widespread, and functionally important PCNA-binding motif. J. Cell Biol. 2009, 186:645-654.
36. Sousa M.M., Krokan H.E., Slupphaug G. DNA-uracil and human pathology. Mol. Aspects Med. 2007, 28:276-306.
37. Wong T.S., Rajagopalan S., Townsley F.M., Freund S.M., Petrovich M., Loakes D., Fersht A.R. Physical and functional interactions between human mitochondrial single-stranded DNA-binding protein and tumour suppressor p53. Nucleic Acids Res. 2009, 37:568-581.
38. Curth U., Urbanke C., Greipel J., Gerberding H., Tiranti V., Zeviani M. Single-stranded-DNA-binding proteins from human mitochondria and Escherichia coli have analogous physicochemical properties. Eur. J. Biochem. 1994, 221:435-443.
39. Hu J., de Souza-Pinto N.C., Haraguchi K., Hogue B.A., Jaruga P., Greenberg M.M., Dizdaroglu M., Bohr V.A. Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes. J. Biol. Chem. 2005, 280:40544-40551.
40. Gredilla R., Garm C., Holm R., Bohr V.A., Stevnsner T. Differential age-related changes in mitochondrial DNA repair activities in mouse brain regions. Neurobiol. Aging 2010, 31:993-1002.
41. Hashiguchi K., Stuart J.A., de Souza-Pinto N.C., Bohr V.A. The C-terminal alphaO helix of human Ogg1 is essential for 8-oxoguanine DNA glycosylase activity: the mitochondrial beta-Ogg1 lacks this domain and does not have glycosylase activity. Nucleic Acids Res. 2004, 32:5596-5608.
42. Ikeda S., Kohmoto T., Tabata R., Seki Y. Differential intracellular localization of the human and mouse endonuclease III homologs and analysis of the sorting signals. DNA Repair (Amst.) 2002, 1:847-854.
43. Ohtsubo T., Nishioka K., Imaiso Y., Iwai S., Shimokawa H., Oda H., Fujiwara T., Nakabeppu Y. Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria. Nucleic Acids Res. 2000, 28:1355-1364.
44. Dou H., Mitra S., Hazra T.K. Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem. 2003, 278:49679-49684.
45. Talpaert-Borle M. Formation, detection and repair of AP sites. Mutat. Res. 1987, 181:45-56.
46. Bailly V., Verly W.G. AP endonucleases and AP lyases. Nucleic Acids Res. 1989, 17:3617-3618.
47. Wiedmer A., Wang P., Zhou J., Rennekamp A.J., Tiranti V., Zeviani M., Lieberman P.M. Epstein-Barr virus immediate-early protein Zta co-opts mitochondrial single-stranded DNA binding protein to promote viral and inhibit mitochondrial DNA replication. J. Virol. 2008, 82:4647-4655.
48. Ali S.I., Shin J.S., Bae S.H., Kim B., Choi B.S. Replication protein A 32 interacts through a similar binding interface with TIPIN, XPA, and UNG2. Int. J. Biochem. Cell Biol. 2010, 42:1210-1215.
49. Brown W.M., George M., Wilson A.C. Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:1967-1971.
50. Wang Y., Bogenhagen D.F. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J. Biol. Chem. 2006, 281:25791-25802.
51. Sanchez-Cespedes M., Parrella P., Nomoto S., Cohen D., Xiao Y., Esteller M., Jeronimo C., Jordan R.C., Nicol T., Koch W.M., Schoenberg M., Mazzarelli P., Fazio V.M., Sidransky D. Identification of a mononucleotide repeat as a major target for mitochondrial DNA alterations in human tumors. Cancer Res. 2001, 61:7015-7019.
52. Reyes A., Gissi C., Pesole G., Saccone C. Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol. Biol. Evol. 1998, 15:957-966.
53. Faith J.J., Pollock D.D. Likelihood analysis of asymmetrical mutation bias gradients in vertebrate mitochondrial genomes. Genetics 2003, 165:735-745.
54. Kamenisch Y., Fousteri M., Knoch J., von Thaler A.K., Fehrenbacher B., Kato H., Becker T., Dolle M.E., Kuiper R., Majora M., Schaller M., van der Horst G.T., van Steeg H., Rocken M., Rapaport D., Krutmann J., Mullenders L.H., Berneburg M. Proteins of nucleotide and base excision repair pathways interact in mitochondria to protect from loss of subcutaneous fat, a hallmark of aging. J. Exp. Med. 2010, 207:379-390.
55. Thommes P., Farr C.L., Marton R.F., Kaguni L.S., Cotterill S. Mitochondrial single-stranded DNA-binding protein from Drosophila embryos. Physical and biochemical characterization. J. Biol. Chem. 1995, 270:21137-21143.
56. Farr C.L., Wang Y., Kaguni L.S. Functional interactions of mitochondrial DNA polymerase and single-stranded DNA-binding protein. Template-primer DNA binding and initiation and elongation of DNA strand synthesis. J. Biol. Chem. 1999, 274:14779-14785.
57. Zhao X., Krishnamurthy N., Burrows C.J., David S.S. Mutation versus repair: NEIL1 removal of hydantoin lesions in single-stranded, bulge, bubble, and duplex DNA contexts. Biochemistry 2010, 49:1658-1666.
58. Mambo E., Gao X., Cohen Y., Guo Z., Talalay P., Sidransky D. Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1838-1843.
59. Arima Y., Nishigori C., Takeuchi T., Oka S., Morimoto K., Utani A., Miyachi Y. 4-Nitroquinoline 1-oxide forms 8-hydroxydeoxyguanosine in human fibroblasts through reactive oxygen species. Toxicol. Sci. 2006, 91:382-392.
60. Amon W., Farrell P.J. Reactivation of Epstein-Barr virus from latency. Rev. Med. Virol. 2005, 15:149-156.
61. Petosa C., Morand P., Baudin F., Moulin M., Artero J.B., Muller C.W. Structural basis of lytic cycle activation by the Epstein-Barr virus ZEBRA protein. Mol. Cell 2006, 21:565-572.
62. Schelcher C., Valencia S., Delecluse H.J., Hicks M., Sinclair A.J. Mutation of a single amino acid residue in the basic region of the Epstein-Barr virus (EBV) lytic cycle switch protein Zta (BZLF1) prevents reactivation of EBV from latency. J. Virol. 2005, 79:13822-13828.
63. Stuart J.A., Mayard S., Hashiguchi K., Souza-Pinto N.C., Bohr V.A. Localization of mitochondrial DNA base excision repair to an inner membrane-associated particulate fraction. Nucleic Acids Res. 2005, 33:3722-3732.
64. Fukuoh A., Kang D. Methods for assessing binding of mitochondrial transcription factor A (TFAM) to DNA. Methods Mol. Biol. 2009, 554:87-101.
65. Canugovi C., Maynard S., Bayne A.C., Sykora P., Tian J., de Souza-Pinto N.C., Croteau D.L., Bohr V.A. The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair (Amst.) 2010, 9:1080-1089.
66. Webster G., Genschel J., Curth U., Urbanke C., Kang C., Hilgenfeld R. A common core for binding single-stranded DNA: structural comparison of the single-stranded DNA-binding proteins (SSB) from E. coli and human mitochondria. FEBS Lett. 1997, 411:313-316.
67. Yang C., Curth U., Urbanke C., Kang C.H. Crystal structure of human mitochondrial single stranded DNA binding protein at 2.4 angstrom resolution. Nat. Struct. Biol. 1997, 4:153-157.
68. Raghunathan S., Kozlov A.G., Lohman T.M., Waksman G. Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol. 2000, 7:648-652.
69. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.