DNA damage signaling and repair in Dictyostelium discoideum

Cell Cycle

Volumn 5, Issue 7, 2006, Pages 702-708

  Hsu, Duen Wei ^a   Gaudet, Pascale ^b   Hudson, Jessica J R ^a   Pears, Catherine J ^a   Lakin, Nicholas D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Dictyostelium; DNA damage signaling; DNA double strand breaks; DNA repair; DNA PK; Homologous recombination; Non homologous end joining

Indexed keywords

DNA; DOUBLE STRANDED DNA; GENOMIC DNA; SINGLE STRANDED DNA;

ATAXIA TELANGIECTASIA; AUTOPHOSPHORYLATION; CELL CYCLE S PHASE; DICTYOSTELIUM DISCOIDEUM; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DNA TEMPLATE; EUKARYOTE; GENETIC MODEL; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; MAMMAL CELL; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN PHOSPHORYLATION; REVIEW; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TERMINAL SEQUENCE; YEAST;

AMOEBA (GENUS); ATAXIA TELANGIECTASIA; DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 33645717034     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.7.2626     Document Type: Review

References (86)

1. Haber JE. Partners and pathways - Repairing a double-strand break. Trends Genet 2000; 16:259-64.
2. Jackson SP. Sensing and repairing DNA double-strand breaks. Carcinogenesis 2002; 23:687-96.
3. Lieber MR, Ma Y, Pannicke U, Schwarz K. Mechanism and regulation of human nonhomologous DNA end-joining. Nat Rev Mol Cell Biol 2003; 4:712-20.
4. Meek K, Gupta S, Ramsden DA, Lees-Miller SP. The DNA-dependent protein kinase: The director at the end. Immunol Rev 2004; 200:132-41.
5. Smith GCM, Jackson SP. The DNA-dependent protein kinase. Genes Dev 1999; 13:916-34.
6. Kienker LJ, Shin EK, Meek K. Both V(D)J recombination and radioresistance require DNA-PK kinase activity, though minimal levels suffice for V(D)J recombination. Nucleic Acids Res 2000; 28:2752-61.
7. Kurimasa A, Kumano S, Boubnov NV, Story MD, Tung CS, Peterson SR, Chen DJ. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol Cell Biol 1999; 19:3877-84.
8. Chan DW, Chen BP, Prithivirajsingh S, Kurimasa A, Story MD, Qin J, Chen DJ. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev 2002; 16:2333-8.
9. Ding Q, Reddy YV, Wang W, Woods T, Douglas P, Ramsden DA, Lees-Miller SP, Meek K. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol Cell Biol 2003; 23:5836-48.
10. Soubeyrand S, Pope L, Pakuts B, Hache RJ. Threonines 2638/2647 in DNA-PK are essential for cellular resistance to ionizing radiation. Cancer Res 2003; 63:1198-201.
11. Cui X, Yu Y, Gupta S, Cho YM, Lees-Miller SP, Meek K. Autophosphorylation of DNA-dependent protein kinase regulates DNA end processing and may also alter double-strand break repair pathway choice. Mol Cell Biol 2005; 25:10842-52.
12. Cary RB, Peterson SR, Wang JT, Bear DG, Bradbury EM, Chen DJ. DNA looping by Ku and the DNA-dependent protein kinase. Proc Natl Acad Sci USA 1997; 94:4267-72.
13. Ramsden DA, Gellert M. Ku protein stimulates DNA end joining by mammalian DNA ligases: A direct role for Ku in repair of DNA double-strand breaks. EMBO J 1998; 17:609-14.
14. DeFazio LG, Stansel RM, Griffith JD, Chu G. Synapsis of DNA ends by DNA-dependent protein kinase. EMBO J 2002; 21:3192-200.
15. Gao YJ, Sun Y, Frank KM, Dikkes P, Fujiwara Y, Seidl KJ, Sekiguchi JM, Rathbun GA, Swat W, Wang JY, Bronson RT, Malynn BA, Bryans M, Zhu CM, Chaudhuri J, Davidson L, Ferrini R, Stamato T, Orkin SH, Greenberg ME, Alt FW. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 1998; 95:891-902.
16. Grawunder U, Zimmer D, Fugmann S, Schwarz K, Lieber MR. DNA ligase IV is essential for V(D)J recombination and DNA double strand break repair in human precursor lymphocytes. Mol Cell 1998; 2:477-84.
17. Frank KM, Sekiguchi JM, Seidl KJ, Swat W, Rathbun GA, Cheng HL, Davidson L, Kangaloo L, Alt FW. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 1998; 396:173-7.
18. Chen L, Trujillo K, Sung P, Tomkinson AE. Interactions of the DNA ligase IV-XRCC4 complex with DNA ends and the DNA-dependent protein kinase. J Biol Chem 2000; 275:26196-205.
19. McElhinny SAN, Snowden CM, McCarville J, Ramsden DA. Ku recruits the XRCC4-ligase IV complex to DNA ends. Mol Cell Biol 2000; 20:2996-3003.
20. Moshous D, Callebaut I, de Chasseval R, Corneo B, Cavazzana-Calvo M, Le Deist F, Tezcan I, Sanal O, Bertrand Y, Philippe N, Fischer A, de Villartay J. Artemis, a novel dna double-strand break repair/v(d)j recombination protein, is mutated in human severe combined immune deficiency. Cell 2001; 105:177-86.
21. Ma Y, Pannicke U, Schwarz K, Lieber MR. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 2002; 108:781-94.
22. Riballo E, Kuhne M, Rief N, Doherty A, Smith GC, Recio MJ, Reis C, Dahm K, Fricke A, Krempler A, Parker AR, Jackson SP, Gennery A, Jeggo PA, Lobrich M. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell 2004; 16:715-24.
23. Chen L, Trujillo K, Ramos W, Sung P, Tomkinson AE. Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol Cell 2001; 8:1105-15.
24. Paull TT, Gellert M. A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proc Natl Acad Sci USA 2000; 97:6409-14.
25. D'Amours D, Jackson SP. The Mre11 complex: At the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002; 3:317-27.
26. Carney JP, Maser RS, Olivares H, Davis EM, LeBeau M, Yates JR, Hays L, Morgan WF, Petrini JHJ. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: Linkage of double strand break repair to the cellular DNA damage response. Cell 1998; 93:477-86.
27. Stewart GS, Maser RS, Stankovic T, Bressan DA, Kaplan MI, Jaspers NGJ, Raams A, Byrd PJ, Petrini JHJ, Taylor AMR. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 1999; 99:577-87.
28. Bender CF, Sikes ML, Sullivan R, Huye LE, Le Beau MM, Roth DB, Mirzoeva OK, Oltz EM, Petrini JH. Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev 2002; 16:2237-51.
29. Harfst E, Cooper S, Neubauer S, Distel L, Grawunder U. Normal V(D)J recombination in cells from patients with Nijmegen breakage syndrome. Mol Immunol 2000; 37:915-29.
30. Yeo TC, Xia D, Hassouneh S, Yang XO, Sabath DE, Sperling K, Gatti RA, Concannon P, Willerford DM. V(D)J rearrangement in Nijmegen breakage syndrome. Mol Immunol 2000; 37:1131-9.
31. Chappell C, Hanakahi LA, Karimi-Busheri F, Weinfeld M, West SC. Involvement of human polynucleotide kinase in double-strand break repair by nonhomologous end joining. EMBO J 2002; 21:2827-32.
32. Koch CA, Agyei R, Galicia S, Metalnikov P, O'Donnell P, Starostine A, Weinfeld M, Durocher D. Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV. Embo J 2004; 23:3874-85.
33. Nick McElhinny SA, Havener JM, Garcia-Diaz M, Juarez R, Bebenek K, Kee BL, Blanco L, Kunkel TA, Ramsden DA. A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining. Mol Cell 2005; 19:357-66.
34. Ma Y, Lu H, Tippin B, Goodman MF, Shimazaki N, Koiwai O, Hsieh CL, Schwarz K, Lieber MR. A biochemically defined system for mammalian nonhomologous DNA end joining. Mol Cell 2004; 16:701-13.
35. Lee JW, Blanco L, Zhou T, Garcia-Diaz M, Bebenek K, Kunkel TA, Wang Z, Povirk LF. Implication of DNA polymerase lambda in alignment-based gap filling for nonhomologous DNA end joining in human nuclear extracts. J Biol Chem 2004; 279:805-11.
36. Wilson TE, Lieber MR. Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J Biol Chem 1999; 274:23599-609.
37. Tseng HM, Tomkinson AE. A physical and functional interaction between yeast Pol4 and Dnl4-Lif1 links DNA synthesis and ligation in nonhomologous end joining. J Biol Chem 2002; 277:45630-7.
38. Mahajan KN, Nick McElhinny SA, Mitchell BS, Ramsden DA. Association of DNA polymerase mu (pol mu) with Ku and ligase IV: Role for pol mu in end-joining double-strand break repair. Mol Cell Biol 2002; 22:5194-202.
39. Strmecki L, Greene DM, Pears CJ. Developmental decisions in Dictyostelium discoideum. Dev Biol 2005; 284:25-36.
40. Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A. The genome of the social amoeba Dictyostelium discoideum. Nature 2005; 435:43-57.
41. Chisholm RL, Gaudet P, Just EM, Pilcher KE, Fey P, Merchant SN, Kibbe WA. dictyBase, the model organism database for Dictyostelium discoideum. Nucleic Acids Res 2006; 34:D423-7.
42. Bronner CE, Welker DL, Deering RA. Mutations affecting sensitivity of the cellular slime mold Dictyostelium discoideum to DNA-damaging agents. Mutat Res 1992; 274:187-200.
43. Deering RA, Guyer RB, Stevens L, Watson-Thais TE. Some repair-deficient mutants of Dictyostelium discoideum display enhanced susceptibilities to bleomycin. Antimicrob Agents Chemother 1996; 40:464-7.
44. Deering RA, Smith MS, Thompson BK, Adolf AC. Gamma-ray-resistant and -sensitive strains of slime mold (Dictyostelium discoideum). Radiat Res 1970; 43:711-28.
45. Freeland TM, Guyer RB, Ling AZ, Deering RA. Apurinic/apyrimidinic (AP) endonuclease from Dictyostelium discoideum: Cloning, nucleotide sequence and induction by sublethal levels of DNA damaging agents. Nucleic Acids Res 1996; 24:1950-3.
46. Lee SK, Yu SL, Alexander H, Alexander S. A mutation in repB, the dictyostelium homolog of the human xeroderma pigmentosum B gene, has increased sensitivity to UV-light but normal morphogenesis. Biochim Biophys Acta 1998; 1399:161-72.
47. Lee SK, Yu SL, Garcia MX, Alexander H, Alexander S. Differential developmental expression of the rep B and rep D xeroderma pigmentosum related DNA helicase genes from Dictyostelium discoideum. Nucleic Acids Res 1997; 25:2365-74.
48. Yu SL, Lee SK, Alexander H, Alexander S. Rapid changes of nucleotide excision repair gene expression following UV-irradiation and cisplatin treatment of Dictyostelium discoideum. Nucleic Acids Res 1998; 26:3397-403.
49. Block WD, Lees-Miller SP. Putative homologues of the DNA-dependent protein kinase catalytic subunit (DNA-PKcs) and other components of the nonhomologous end joining machinery in Dictyostelium discoideum. DNA Repair (Amst) 2005; 4:1061-5.
50. Hudson JJ, Hsu DW, Guo K, Zhukovskaya N, Liu PH, Williams JG, Pears CJ, Lakin ND. DNA-PKcs-dependent signaling of DNA damage in Dictyostelium discoideum. Curr Biol 2005; 15:1880-5.
51. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605-11.
52. Dronkert ML, Kanaar R. Repair of DNA interstrand cross-links. Mutat Res 2001; 486:217-47.
53. 1-phase cell-cycle arrest prior to terminal differentiation in Dictyostelium. Development 2004; 131:2619-30.
54. Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, YamaguchiIwai Y, Shinohara A, Takeda S. Homologous recombination and non homologous end joining pathways of DNA double strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 1998; 17:5497-508.
55. Ferreira MG, Cooper JP. Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle. Genes Dev 2004; 18:2249-54.
56. Karathanasis E, Wilson TE. Enhancement of Saccharomyces cerevisiae end-joining efficiency by cell growth stage but not by impairment of recombination. Genetics 2002; 161:1015-27.
57. Weijer CJ, Duschl G, David CN. A revision of the Dictyostelium discoideum cell cycle. J Cell Sci 1984; 70:111-31.
58. Katz KS, Ratner DI. Homologous recombination and the repair of double-strand breaks during cotransformation of Dictyostelium discoideum. Mol Cell Biol 1988; 8:2779-86.
59. Deering RA. Dictyostelium discoideum: A gamma-ray resistant organism. Science 1968; 162:1289-90.
60. Zhou BBS, Elledge SJ. The DNA damage response: Putting checkpoints in perspective. Nature 2000; 408:433-9.
61. Downs JA, Jackson SP. Cancer: Protective packaging for DNA. Nature 2003; 424:732-4.
62. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004; 64:2390-6.
63. Abraham RT. PI 3-kinase related kinases: 'Big' players in stress-induced signaling pathways. DNA Repair (Amst) 2004; 3:883-7.
64. Shechter D, Gautier J. ATM and ATR check in on origins: A dynamic model for origin selection and activation. Cell Cycle 2005; 4.
65. Wang H, Powell SN, Iliakis G, Wang Y. ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonhomologous end joining. Cancer Res 2004; 64:7139-43.
66. 2/M arrest after DNA damage. Cell 1998; 94:399-409.
67. Liang F, Jasin M. Ku80 deficient cells exhibit excess degradation of extrachromosomal DNA. J Biol Chem 1996; 271:14405-11.
68. Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003; 300:1542-8.
69. King J, Insall RH. Parasexual genetics of Dictyostelium gene disruptions: Identification of a ras pathway using diploids. BMC Genet 2003; 4:12.
70. Faix J, Kreppel L, Shaulsky G, Schleicher M, Kimmel AR. A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res 2004; 32:e143.
71. Dore AS, Drake AC, Brewerton SC, Blundell TL. Identification of DNA-PK in the arthropods. Evidence for the ancient ancestry of vertebrate nonhomologous end-joining. DNA Repair (Amst) 2004; 3:33-41.
72. Lieber MR, Ma Y, Pannicke U, Schwarz K. The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination. DNA Repair (Amst) 2004; 3:817-26.
73. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat Rev Cancer 2003; 3:155-68.
74. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM, Haber JE, Foiani M. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 2004; 431:1011-7.
75. Aylon Y, Liefshitz B, Kupiec M. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J 2004; 23:4868-75.
76. Ma Y, Pannicke U, Lu H, Niewolik D, Schwarz K, Lieber MR. The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J Biol Chem 2005; 280:33839-46.
77. Douglas P, Gupta S, Morrice N, Meek K, Lees-Miller SP. DNA-PK-dependent phosphorylation of Ku70/80 is not required for nonhomologous end joining. DNA Repair (Amst) 2005; 4:1006-18.
78. Chan DW, Ye RQ, Veillette CJ, Lees-Miller SP. DNA-Dependent protein kinase phosphorylation sites in Ku 70/80 heterodimer. Biochemistry 1999; 38:1819-28.
79. Yu Y, Wang W, Ding Q, Ye R, Chen D, Merkle D, Schriemer D, Meek K, Lees-Miller SP. DNA-PK phosphorylation sites in XRCC4 are not required for survival after radiation or for V(D)J recombination. DNA Repair (Amst) 2003; 2:1239-52.
80. Leber R, Wise TW, Mizuta R, Meek K. The XRCC4 gene product is a target for and interacts with the DNA-dependent protein kinase. J Biol Chem 1998; 273:1794-801.
81. Wang YG, Nnakwe C, Lane WS, Modesti M, Frank KM. Phosphorylation and regulation of DNA ligase IV stability by DNA-dependent protein kinase. J Biol Chem 2004; 279:37282-90.
82. Douglas P, Sapkota GP, Morrice N, Yu Y, Goodarzi AA, Merkle D, Meek K, Alessi DR, Lees-Miller SP. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem J 2002; 368:243-51.
83. Robinson DN, Spudich JA. Dynacortin, a genetic link between equatorial contractility and global shape control discovered by library complementation of a Dictyostelium discoideum cytokinesis mutant. J Cell Biol 2000; 150:823-38.
84. Souza GM, da Silva AM, Kuspa A. Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development 1999; 126:3263-74.
85. Hubscher U, Maga G, Spadari S. Eukaryotic DNA polymerases. Annu Rev Biochem 2002; 71:133-63.
86. Vance JR, Wilson TE. Uncoupling of 3′-phosphatase and 5′-kinase functions in budding yeast. Characterization of Saccharomyces cerevisiae DNA 3′-phosphatase (TPP1). J Biol Chem 2001; 276:15073-81.