RECQL4 localizes to mitochondria and preserves mitochondrial DNA integrity

Aging Cell

Volumn 11, Issue 3, 2012, Pages 456-466

  Croteau, Deborah L ^a   Rossi, Marie L ^a   Canugovi, Chandrika ^a   Tian, Jane ^a   Sykora, Peter ^a   Ramamoorthy, Mahesh ^a   Wang, Zhengming ^a,d   Singh, Dharmendra Kumar ^a   Akbari, Mansour ^b   Kasiviswanathan, Rajesh ^c   Copeland, William C ^c   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

MtDNA; RecQ helicase; Rothmund Thomson Syndrome

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; HELICASE; MITOCHONDRIAL DNA; RECQL4 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; BIOENERGY; CELL FRACTIONATION; CONTROLLED STUDY; DNA DAMAGE; DNA INTEGRATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MICROSCOPY; MITOCHONDRION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS;

AGE FACTORS; AGED, 80 AND OVER; ANIMALS; CELL FRACTIONATION; CELL LINE, TUMOR; DNA DAMAGE; DNA, MITOCHONDRIAL; GENOMIC INSTABILITY; HELA CELLS; HUMANS; MICE; MITOCHONDRIA; RECQ HELICASES;

EID: 84862782942     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2012.00803.x     Document Type: Article

References (41)

1. Bohr VA (2008) Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci. 33, 609-620.
2. Burks LM, Yin J, Plon SE (2007) Nuclear import and retention domains in the amino terminus of RECQL4. Gene, 391, 26-38.
3. Canugovi C, Maynard S, Bayne AC, Sykora P, Tian J, de Souza-Pinto NC, Croteau DL, Bohr VA (2010) The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair (Amst.) 9, 1080-1089.
4. Capp C, Wu J, Hsieh TS (2010) RecQ4: the second replicative helicase? Crit. Rev. Biochem. Mol. Biol. 45, 233-242.
5. Copeland WC (2008) Inherited mitochondrial diseases of DNA replication. Annu. Rev. Med. 59, 131-146.
6. Dietschy T, Shevelev I, Pena-Diaz J, Huhn D, Kuenzle S, Mak R, Miah MF, Hess D, Fey M, Hottiger MO, Janscak P, Stagljar I (2009) p300-mediated acetylation of the Rothmund-Thomson-syndrome gene product RECQL4 regulates its subcellular localization. J. Cell Sci. 122, 1258-1267.
7. Gelaw B, Ali S, Becker J (2004) Rothmund-Thomson syndrome, Klippel-Feil syndrome, and osteosarcoma. Skeletal Radiol. 33, 613-615.
8. Ghosh AK, Rossi ML, Singh DK, Dunn C, Ramamoorthy M, Croteau DL, Liu Y, Bohr VA (2012) RECQL4, the protein mutated in Rothmund-Thomson syndrome, functions in telomere maintenance. J. Biol. Chem. 287, 196-209.
9. Graziewicz MA, Longley MJ, Copeland WC (2006) DNA polymerase gamma in mitochondrial DNA replication and repair. Chem. Rev. 106, 383-405.
10. Hill BG, Dranka BP, Zou L, Chatham JC, Darley-Usmar VM (2009) Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal. Biochem. J. 424, 99-107.
11. Im JS, Ki SH, Farina A, Jung DS, Hurwitz J, Lee JK (2009) Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc. Natl. Acad. Sci. U.S.A. 106, 15628-15632.
12. Jiang Y, Liu X, Fang X, Wang X (2009) Proteomic analysis of mitochondria in Raji cells following exposure to radiation: implications for radiotherapy response. Protein Pept. Lett. 16, 1350-1359.
13. Jin W, Liu H, Zhang Y, Otta SK, Plon SE, Wang LL (2008) Sensitivity of RECQL4-deficient fibroblasts from Rothmund-Thomson syndrome patients to genotoxic agents. Hum. Genet. 123, 643-653.
14. Kang D, Hamasaki N (2005) Mitochondrial transcription factor A in the maintenance of mitochondrial DNA: overview of its multiple roles. Ann. N Y Acad. Sci. 1042, 101-108.
15. Kumata Y, Tada S, Yamanada Y, Tsuyama T, Kobayashi T, Dong YP, Ikegami K, Murofushi H, Seki M, Enomoto T (2007) Possible involvement of RecQL4 in the repair of double-strand DNA breaks in Xenopus egg extracts. Biochim. Biophys. Acta 1773, 556-564.
16. Larizza L, Roversi G, Volpi L (2010) Rothmund-Thomson syndrome. Orphanet. J. Rare Dis. 5, 2.
17. Lim SE, Longley MJ, Copeland WC (1999) The mitochondrial p55 accessory subunit of human DNA polymerase gamma enhances DNA binding, promotes processive DNA synthesis, and confers N-ethylmaleimide resistance. J. Biol. Chem. 274, 38197-38203.
18. Longley MJ, Prasad R, Srivastava DK, Wilson SH, Copeland WC (1998) Identification of 5′-deoxyribose phosphate lyase activity in human DNA polymerase gamma and its role in mitochondrial base excision repair in vitro. Proc. Natl. Acad. Sci. U.S.A. 95, 12244-12248.
19. Macris MA, Krejci L, Bussen W, Shimamoto A, Sung P (2006) Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair (Amst.) 5, 172-180.
20. Mambo E, Chatterjee A, Xing M, Tallini G, Haugen BR, Yeung SC, Sukumar S, Sidransky D (2005) Tumor-specific changes in mtDNA content in human cancer. Int. J. Cancer 116, 920-924.
21. Maynard S, de Souza-Pinto NC, Scheibye-Knudsen M, Bohr VA (2010) Mitochondrial base excision repair assays. Methods 51, 416-425.
22. Palau F, Espinos C (2006) Autosomal recessive cerebellar ataxias. Orphanet. J. Rare Dis. 1, 47.
23. Petkovic M, Dietschy T, Freire R, Jiao R, Stagljar I (2005) The human Rothmund-Thomson syndrome gene product, RECQL4, localizes to distinct nuclear foci that coincide with proteins involved in the maintenance of genome stability. J. Cell Sci. 118, 4261-4269.
24. Qian W, Van Houten B (2010) Alterations in bioenergetics due to changes in mitochondrial DNA copy number. Methods 51, 452-457.
25. Rossi ML, Ghosh AK, Kulikowicz T, Croteau DL, Bohr VA (2010) Conserved helicase domain of human RecQ4 is required for strand annealing-independent DNA unwinding. DNA Repair (Amst.) 9, 796-804.
26. Sahin E, Colla S, Liesa M, Moslehi J, Muller FL, Guo M, Cooper M, Kotton D, Fabian AJ, Walkey C, Maser RS, Tonon G, Foerster F, Xiong R, Wang YA, Shukla SA, Jaskelioff M, Martin ES, Heffernan TP, Protopopov A, Ivanova E, Mahoney JE, Kost-Alimova M, Perry SR, Bronson R, Liao R, Mulligan R, Shirihai OS, Chin L, DePinho RA (2011) Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 470, 359-365.
27. Sangrithi MN, Bernal JA, Madine M, Philpott A, Lee J, Dunphy WG, Venkitaraman AR (2005) Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 121, 887-898.
28. Santos JH, Mandavilli BS, Van Houten B (2002) Measuring oxidative mtDNA damage and repair using quantitative PCR. Methods Mol. Biol. 197, 159-176.
29. Santos JH, Meyer JN, Skorvaga M, Annab LA, Van Houten B (2004) Mitochondrial hTERT exacerbates free-radical-mediated mtDNA damage. Aging Cell 3, 399-411.
30. Schmidt O, Pfanner N, Meisinger C (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 11, 655-667.
31. Schurman SH, Hedayati M, Wang Z, Singh DK, Speina E, Zhang Y, Becker K, Macris M, Sung P, Wilson DM III, Croteau DL, Bohr VA (2009) Direct and indirect roles of RECQL4 in modulating base excision repair capacity. Hum. Mol. Genet. 18, 3470-3483.
32. Siitonen HA, Sotkasiira J, Biervliet M, Benmansour A, Capri Y, Cormier-Daire V, Crandall B, Hannula-Jouppi K, Hennekam R, Herzog D, Keymolen K, Lipsanen-Nyman M, Miny P, Plon SE, Riedl S, Sarkar A, Vargas FR, Verloes A, Wang LL, Kaariainen H, Kestila M (2009) The mutation spectrum in RECQL4 diseases. Eur. J. Hum. Genet. 17, 151-158.
33. Singh DK, Karmakar P, Aamann M, Schurman SH, May A, Croteau DL, Burks L, Plon SE, Bohr VA (2010) The involvement of human RECQL4 in DNA double-strand break repair. Aging Cell 9, 358-371.
34. Suzuki T, Kohno T, Ishimi Y (2009) DNA helicase activity in purified human RECQL4 protein. J. Biochem. 146, 327-335.
35. Szuhai K, Ouweland J, Dirks R, Lemaitre M, Truffert J, Janssen G, Tanke H, Holme E, Maassen J, Raap A (2001) Simultaneous A8344G heteroplasmy and mitochondrial DNA copy number quantification in myoclonus epilepsy and ragged-red fibers (MERRF) syndrome by a multiplex molecular beacon based real-time fluorescence PCR. Nucleic Acids Res. 29, E13.
36. Thangavel S, Mendoza-Maldonado R, Tissino E, Sidorova JM, Yin J, Wang W, Monnat RJ Jr, Falaschi A, Vindigni A (2010) Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol. Cell. Biol. 30, 1382-1396.
37. Werner SR, Prahalad AK, Yang J, Hock JM (2006) RECQL4-deficient cells are hypersensitive to oxidative stress/damage: insights for osteosarcoma prevalence and heterogeneity in Rothmund-Thomson syndrome. Biochem. Biophys. Res. Commun. 345, 403-409.
38. Woo LL, Futami K, Shimamoto A, Furuichi Y, Frank KM (2006) The Rothmund-Thomson gene product RECQL4 localizes to the nucleolus in response to oxidative stress. Exp. Cell Res. 312, 3443-3457.
39. Xu X, Liu Y (2009) Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J. 28, 568-577.
40. Xu X, Rochette PJ, Feyissa EA, Su TV, Liu Y (2009) MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J. 28, 3005-3014.
41. Yin J, Kwon YT, Varshavsky A, Wang W (2004) RECQL4, mutated in the Rothmund-Thomson and RAPADILINO syndromes, interacts with ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Hum. Mol. Genet. 13, 2421-2430.