The SNM1/Pso2 family of ICL repair nucleases: From yeast to man

Environmental and Molecular Mutagenesis

Volumn 51, Issue 6, 2010, Pages 635-645

  Cattell, Emma ^a   Sengerová, Blanka ^a   McHugh, Peter J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Homologous recombination; Interstrand crosslink; Nuclease; Nucleotide excision repair; SNM1, PSO2, metallo lactamase domain; Translesion synthesis

Indexed keywords

CHLORAMBUCIL; CISPLATIN; CYCLOPHOSPHAMIDE; FANCONI ANEMIA GROUP C PROTEIN; METALLO BETA LACTAMASE; MITOMYCIN C; NUCLEASE; OXALIPLATIN; PROTEIN MUTS; PSO2 PROTEIN; SNM1 PROTEIN; SNM1A PROTEIN; SNM1B PROTEIN; SNM1C PROTEIN; UNCLASSIFIED DRUG; DCLRE1A PROTEIN, MOUSE; DCLRE1B PROTEIN, HUMAN; DEOXYRIBONUCLEASE; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE;

DNA CROSS LINKING; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SACCHAROMYCES CEREVISIAE; ANIMAL; ARTICLE; METABOLISM; PHYSIOLOGY; SEQUENCE ALIGNMENT; YEAST;

MAMMALIA;

ANIMALS; DEOXYRIBONUCLEASES; DNA REPAIR; DNA REPAIR ENZYMES; ENDODEOXYRIBONUCLEASES; HUMANS; NUCLEAR PROTEINS; SEQUENCE ALIGNMENT; YEASTS;

EID: 77955874736     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20556     Document Type: Review

References (102)

1. Ahel I, Ahel D, Matsusaka T, Clark AJ, Pines J, Boulton SJ, West SC. 2008. Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451:81-85.
2. Akhter S, Legerski RJ. 2008. SNM1A acts downstream of ATM to promote the G1 cell cycle checkpoint. Biochem Biophys Res Commun 377:236-241.
3. Akhter S, Richie C, Deng J, Brey E, Zhang X, Patrick C, Behringer R, Legerski R. 2004. Deficiency in SNM1 abolishes an early mitotic checkpoint induced by spindle stress. Mol Cell Biol 24:10448-10455. (Pubitemid 39507881)
4. Ahkter S, Richie CT, Zhang N, Behringer RR, Zhu C, Legerski RJ. 2005. Snm1-deficient mice exhibit accelerated tumorigenesis and susceptibility to infection. Mol Cell Biol 25:10071-10078. (Pubitemid 41572752)
5. Anders M, Mattow J, Digweed M, Demuth I. 2009. Evidence for hSNM1B/Apollo functioning in the HSP70 mediated DNA damage response. Cell Cycle 8:1725-1732.
6. Anderson L, Henderson C, Adachi Y. 2001. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol Cell Biol 21:1719-1729. (Pubitemid 32156392)
7. Aravind L, Walker DR, Koonin EV. 1999. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res 27:1223-1242. (Pubitemid 29206430)
8. Bae JB, Mukhopadhyay SS, Liu L, Zhang N, Tan J, Akhter S, Liu X, Shen X, Li L, Legerski RJ. 2008. Snm1B/Apollo mediates replication fork collapse and S phase checkpoint activation in response to DNA interstrand cross-links. Oncogene 27:5045-5056.
9. Barber L, Ward T, Hartley J, McHugh P. 2005a. DNA interstrand cross-link repair in the Saccharomyces cerevisiae cell cycle: Overlapping roles for PSO2 (SNM1) with MutS factors and EXO1 during S phase. Mol Cell Biol 25:2297-2309. (Pubitemid 40354626)
10. Barber LJ, Ward TA, Hartley JA, McHugh PJ. 2005b. DNA interstrand cross-link repair in the Saccharomyces cerevisiae cell cycle: Overlapping roles for PSO2 (SNM1) with MutS factors and EXO1 during S phase. Mol Cell Biol 25:2297-2309.
11. Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, Conrad S, Goodarzi AA, Krempler A, Jeggo PA, Lobrich M. 2009. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. Embo J 28:3413-3427.
12. Brendel M, Bonatto D, Strauss M, Revers L, Pungartnik C, Saffi J, Henriques J. 2003. Role of PSO genes in repair of DNA damage of Saccharomyces cerevisiae. Mutat Res 544:179-193.
13. Bush K, Jacoby GA, Medeiros AA. 1995. A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrob Agents Chemother 39:1211-1233.
14. Callebaut I, Moshous D, Mornon J, de Villartay J. 2002a. Metallo-beta-lactamase fold within nucleic acids processing enzymes: The beta-CASP family. Nucleic Acids Res 30:3592-3601.
15. Callebaut I, Moshous D, Mornon JP, de Villartay JP. 2002b. Metallo-beta- lactamase fold within nucleic acids processing enzymes: The beta-CASP family. Nucleic Acids Res 30:3592-3601.
16. Carfi A, Pares S, Duee E, Galleni M, Duez C, Frere JM, Dideberg O. 1995. The 3-D structure of a zinc metallo-beta-lactamase from Bacillus cereus reveals a new type of protein fold. Embo J 14:4914-4921.
17. Cassier-Chauvat C, Moustacchi E. 1988. Allelism between pso1-1 and rev3-1 mutants and between pso2-1 and snm1 mutants in Saccharomyces cerevisiae. Curr Genet 13:37-40.
18. Cavazzana-Calvo M, Le Deist F, de Saint Basile G, Papadopoulo D, de Villartay JP, Fischer A. 1993. Increased radiosensitivity of granulocyte macrophage colony-forming units and skin fibroblasts in human autosomal recessive severe combined immunodeficiency. J Clin Invest 91:1214-1218.
19. Chai W, Du Q, Shay J, Wright W. 2006. Human telomeres have different overhang sizes at leading versus lagging strands. Molecular Cell 21:427-435.
20. Chen Y, Yang Y, van Overbeek M, Donigian JR, Baciu P, de Lange T, Lei M. 2008. A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science 319:1092-1096.
21. Daiyasu H, Osaka K, Ishino Y, Toh H. 2001. Expansion of the zinc metallo- hydrolase family of the beta-lactamase fold. FEBS Lett 503:1-6.
22. Darroudi F, Wiegant W, Meijers M, Friedl AA, van der Burg M, Fomina J, van Dongen JJ, van Gent DC, Zdzienicka MZ. 2007. Role of Artemis in DSB repair and guarding chromosomal stability following exposure to ionizing radiation at different stages of cell cycle. Mutat Res 615:111-124.
23. de la Sierra-Gallay IL, Pellegrini O, Condon C. 2005. Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z. Nature 433:657-661.
24. de la Sierra-Gallay IL, Zig L, Jamalli A, Putzer H. 2008. Structural insights into the dual activity of RNase J. Nat Struct Mol Biol 15:206-212.
25. de Silva I, McHugh P, Clingen P, Hartley J. 2000. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 20:7980-7990.
26. de Silva IU, McHugh PJ, Clingen PH, Hartley JA. 2002. Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Res 30:3848-3856.
27. de Villartay JP, Shimazaki N, Charbonnier JB, Fischer A, Mornon JP, Lieber MR, Callebaut I. 2009. A histidine in the beta-CASP domain of Artemis is critical for its full in vitro and in vivo functions. DNA Repair (Amst) 8:202-208.
28. Deckbar D, Birraux J, Krempler A, Tchouandong L, Beucher A, Walker S, Stiff T, Jeggo P, Löbrich M. 2007. Chromosome breakage after G2 checkpoint release. J Cell Biol 176:749-755.
29. Demuth I, Digweed M. 1998. Genomic organization of a potential human DNA-crosslink repair gene, KIAA0086. Mutat Res 409:11-16.
30. Demuth I, Digweed M, Concannon P. 2004. Human SNM1B is required for normal cellular response to both DNA interstrand crosslink-inducing agents and ionizing radiation. Oncogene 23:8611-8618.
31. Demuth I, Bradshaw PS, Lindner A, Anders M, Heinrich S, Kallenbach J, Schmelz K, Digweed M, Meyn MS, Concannon P. 2008. Endogenous hSNM1B/Apollo interacts with TRF2 and stimulates ATM in response to ionizing radiation. DNA Repair (Amst) 7:1192-1201.
32. Dronkert ML, Kanaar R. 2001. Repair of DNA interstrand cross-links. Mutat Res 486:217-247.
33. Dronkert M, de Wit J, Boeve M, Vasconcelos M, van Steeg H, Tan T, Hoeijmakers J, Kanaar R. 2000. Disruption of mouse SNM1 causes increased sensitivity to the DNA interstrand cross-linking agent mitomycin C. Mol Cell Biol 20:4553-4561.
34. Drouet J, Frit P, Delteil C, de Villartay JP, Salles B, Calsou P. 2006. Interplay between Ku, Artemis, and the DNA-dependent protein kinase catalytic subunit at DNA ends. J Biol Chem 281:27784-27793.
35. Dudas A, Vlasakova D, Dudasova Z, Gabcova D, Brozmanova J, Chovanec M. 2007. Further characterization of the role of Pso2 in the repair of DNA interstrand cross-link-associated double-strand breaks in Saccharomyces cerevisiae. Neoplasma 54:189-194.
36. Freibaum BD, Counter CM. 2006. hSnm1B is a novel telomere-associated protein. J Biol Chem 281:15033-15036.
37. Freibaum BD, Counter CM. 2008. The protein hSnm1B is stabilized when bound to the telomere-binding protein TRF2. J Biol Chem 283:23671-23676.
38. Garrity JD, Bennett B, Crowder MW. 2005. Direct evidence that the reaction intermediate of metallo-beta-lactamase L1 is metal bound. Biochemistry 44:1078-1087.
39. Geng L, Zhang X, Zheng S, Legerski RJ. 2007. Artemis links ATM to G2/M checkpoint recovery via regulation of Cdk1-cyclin B. Mol Cell Biol 27:2625-2635.
40. Goodarzi AA, Yu Y, Riballo E, Douglas P, Walker SA, Ye R, Harer C, Marchetti C, Morrice N, Jeggo PA, Lees-Miller SP. 2006. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. Embo J 25:3880-3889.
41. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T. 1999. Mammalian telomeres end in a large duplex loop. Cell 97:503-514.
42. Grossmann K, Ward A, Moses R. 2000. Saccharomyces cerevisiae lacking Snm1, Rev3 or Rad51 have a normal S-phase but arrest permanently in G2 after cisplatin treatment. Mutat Res 461:1-13.
43. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J, Kanaar R. 2006. The structure-specific endonuclease Mus81- Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 25:4921-4932.
44. Hazrati A, Ramis-Castelltort M, Sarkar S, Barber LJ, Schofield CJ, Hartley JA, McHugh PJ. 2008. Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Repair (Amst) 7:230-238.
45. Hazrati A, Ramis-Castelltort M, Sarkar S, Barber LJ, Schofield CJ, Hartley JA, McHugh PJ. 2008. Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Repair (Amst) 7:230-238.
46. Hejna J, Philip S, Ott J, Faulkner C, Moses R. 2007. The hSNM1 protein is a DNA 5′-exonuclease. Nucleic Acids Res 35:6115-6123.
47. Hemphill AW, Bruun D, Thrun L, Akkari Y, Torimaru Y, Hejna K, Jakobs PM, Hejna J, Jones S, Olson SB, Moses RE. 2008. Mammalian SNM1 is required for genome stability. Mol Genet Metab 94:38-45.
48. Henriques JA, Moustacchi E. 1980. Isolation and characterization of pso mutants sensitive to photo-addition of psoralen derivatives in Saccharomyces cerevisiae. Genetics 95:273-288.
49. Henriques J, Moustacchi E. 1981a. Interactions between mutations for sensitivity to psoralen photoaddition (pso) and to radiation (rad) in Saccharomyces cerevisiae. J Bacteriol 148:248-256.
50. Henriques JA, Moustacchi E. 1981b. Interactions between mutations for sensitivity to psoralen photoaddition (pso) and to radiation (rad) in Saccharomyces cerevisiae. J Bacteriol 148:248-256.
51. Henriques JA, Brozmanova J, Brendel M. 1997. Role of PSO genes in the repair of photoinduced interstrand cross-links and photooxidative damage in the DNA of the yeast Saccharomyces cerevisiae. J Photochem Photobiol B 39:185-196.
52. Ishiai M, Kimura M, Namikoshi K, Yamazoe M, Yamamoto K, Arakawa H, Agematsu K, Matsushita N, Takeda S, Buerstedde J, Takato M. 2004. DNA cross-link repair protein SNM1A interacts with PIAS1 in nuclear focus formation. Mol Cell Biol 24:10733-10741.
53. Ishii R, Minagawa A, Takaku H, Takagi M, Nashimoto M, Yokoyama S. 2005. Crystal structure of the tRNA 3′ processing endoribonuclease tRNase Z from Thermotoga maritima. J Biol Chem 280:14138-14144.
54. Ishikawa H, Nakagawa N, Kuramitsu S, Masui R. 2006. Crystal structure of TTHA0252 from Thermus thermophilus HB8, a RNA degradation protein of the metallo-beta-lactamase superfamily. J Biochem 140:535-542. (Pubitemid 44870918)
55. Jeggo P, O'Neill P. 2002. The Greek Goddess, Artemis, reveals the secrets of her cleavage. DNA Repair (Amst) 1:771-777.
56. Lam AF, Krogh BO, Symington LS. 2008. Unique and overlapping functions of the Exo1, Mre11 and Pso2 nucleases in DNA repair. DNA Repair (Amst) 7:655-662.
57. Lambert S, Mason S, Barber L, Hartley J, Pearce J, Carr A, McHugh P. 2003. Schizosaccharomyces pombe checkpoint response to DNA interstrand cross-links. Mol Cell Biol 23:4728-4737.
58. Laurencon A, Orme CM, Peters HK, Boulton CL, Vladar EK, Langley SA, Bakis EP, Harris DT, Harris NJ, Wayson SM, Hawley R, Burtis K. 2004. A large-scale screen for mutagen-sensitive loci in Drosophila. Genetics 167:217-231.
59. Lenain C, Bauwens S, Amiard S, Brunori M, Giraud-Panis MJ, Gilson E. 2006. The Apollo 5′ exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr Biol 16:1303-1310.
60. Li de la Sierra-Gallay I, Mathy N, Pellegrini O, Condon C. 2006. Structure of the ubiquitous 3′ processing enzyme RNase Z bound to transfer RNA. Nat Struct Mol Biol 13:376-377.
61. Li X, Moses R. 2003a. The beta-lactamase motif in Snm1 is required for repair of DNA double-strand breaks caused by interstrand crosslinks in S. cerevisiae. DNA Repair (Amst) 2:121-129.
62. Li X, Moses RE. 2003b. The beta-lactamase motif in Snm1 is required for repair of DNA double-strand breaks caused by interstrand crosslinks in S. cerevisiae. DNA Repair (Amst) 2:121-129.
63. Li X, Hejna J, Moses R. 2005a. The yeast Snm1 protein is a DNA 5′-exonuclease. DNA Repair (Amst) 4:163-170.
64. Li X, Hejna J, Moses RE. 2005b. The yeast Snm1 protein is a DNA 5′- exonuclease. DNA Repair (Amst) 4:163-70.
65. Liu B, Liao J, Rao X, Kushner SA, Chung CD, Chang DD, Shuai K. 1998. Inhibition of Stat1-mediated gene activation by PIAS1. Proc Natl Acad Sci USA 95:10626-10631.
66. Liu L, Akhter S, Bae JB, Mukhopadhyay SS, Richie CT, Liu X, Legerski R. 2009. SNM1B/Apollo interacts with astrin and is required for the prophase cell cycle checkpoint. Cell Cycle 8:628-638.
67. Ma Y, Pannicke U, Schwarz K, Lieber MR. 2002. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108:781-794.
68. Ma Y, Schwarz K, Lieber M. 2005. The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. DNA Repair (Amst) 4:845-851.
69. Magana-Schwencke N, Henriques JA, Chanet R, Moustacchi E. 1982. The fate of 8-methoxypsoralen photoinduced crosslinks in nuclear and mitochondrial yeast DNA: Comparison of wild-type and repair-deficient strains. Proc Natl Acad Sci USA 79:1722-1726.
70. Mandel CR, Kaneko S, Zhang H, Gebauer D, Vethantham V, Manley JL, Tong L. 2006. Polyadenylation factor CPSF-73 is the premRNA 3′-end-processing endonuclease. Nature 444:953-956.
71. Maser RS, Monsen KJ, Nelms BE, Petrini JH. 1997. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol Cell Biol 17:6087-6096.
72. McHugh PJ, Sones WR, Hartley JA. 2000. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol Cell Biol 20:3425-3433.
73. Meier B, Barber LJ, Liu Y, Shtessel L, Boulton SJ, Gartner A, Ahmed S. 2009. The MRT-1 nuclease is required for DNA crosslink repair and telomerase activity in vivo in Caenorhabditis elegans. Embo J 28:3549-3563.
74. Molinier J, Stamm M, Hohn B. 2004. SNM-dependent recombinational repair of oxidatively induced DNA damage in Arabidopsis thaliana. EMBO Rep 5:994-999.
75. 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 Villartag JP. 2001. Artemis, a novel DNA doublestrand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 105:177-186.
76. Muller S, Hoege C, Pyrowolakis G, Jentsch S. 2001. SUMO, ubiquitin's mysterious cousin. Nat Rev Mol Cell Biol 2:202-210.
77. Nelms BE, Maser RS, MacKay JF, Lagally MG, Petrini JH. 1998. In situ visualization of DNA double-strand break repair in human fibroblasts. Science 280:590-592.
78. Niedernhofer LJ, Lalai AS, Hoeijmakers JH. 2005. Fanconi anemia (cross)linked to DNA repair. Cell 123:1191-1198.
79. Niewolik D, Pannicke U, Lu H, Ma Y, Wang LC, Kulesza P, Zandi E, Lieber MR, Schwarz K. 2006. DNA-PKcs dependence of Artemis endonucleolytic activity, differences between hairpins and 5′ or 3′ overhangs. J Biol Chem 281:33900-33909.
80. Povirk LF, Zhou T, Zhou R, Cowan MJ, Yannone SM. 2007. Processing of 3′-phosphoglycolate-terminated DNA double strand breaks by Artemis nuclease. J Biol Chem 282:3547-3558.
81. 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, Löbrich M. 2004. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell 16:715-724.
82. Richie CT, Peterson C, Lu T, Hittelman WN, Carpenter PB, Legerski RJ. 2002. hSnm1 colocalizes and physically associates with 53BP1 before and after DNA damage. Mol Cell Biol 22:8635-8647.
83. Rooney S, Sekiguchi J, Zhu C, Cheng HL, Manis J, Whitlow S, DeVido J, Foy D, Chaudhuri J, Lombard D, et al. 2002. Leaky Scid phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Mol Cell 10:1379-1390.
84. Ruhland A, Haase E, Siede W, Brendel M. 1981a. Isolation of yeast mutants sensitive to the bifunctional alkylating agent nitrogen mustard. Mol Gen Genet 181:346-351.
85. Ruhland A, Kircher M, Wilborn F, Brendel M. 1981b. A yeast mutant specifically sensitive to bifunctional alkylation. Mutat Res 91:457-462.
86. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD. 2000. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 151:1381-1390.
87. Siede W, Brendel M. 1982. Interactions among genes controlling sensitivity to radiation (RAD) and to alkylation by nitrogen mustard (SNM) in yeast. Curr Genet 5:33-38.
88. Suresh Kumar G, Lipman R, Cummings J, Tomasz M. 1997. Mitomycin C-DNA adducts generated by DT-diaphorase. Revised mechanism of the enzymatic reductive activation of mitomycin C. Biochemistry 36:14128-14136.
89. Taniguchi T, D'Andrea AD. 2006. Molecular pathogenesis of Fanconi anemia: Recent progress. Blood 107:4223-4233.
90. Tomasz M, Lipman R, Chowdary D, Pawlak J, Verdine GL, Nakanishi K. 1987. Isolation and structure of a covalent cross-link adduct between mitomycin C, DNA. Science 235:1204-1208.
91. Tran PT, Erdeniz N, Symington LS, Liskay RM. 2004. EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst) 3:1549-1559.
92. Ullah JH, Walsh TR, Taylor IA, Emery DC, Verma CS, Gamblin SJ, Spencer J. 1998. The crystal structure of the L1 metallo-beta-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution. J Mol Biol 284:125-136.
93. van Overbeek M, de Lange T. 2006. Apollo, an Artemis-related nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr Biol 16:1295-1302.
94. Wang Z, Fast W, Valentine AM, Benkovic SJ. 1999. Metallo-beta-lactamase: Structure and mechanism. Curr Opin Chem Biol 3:614-622.
95. Wang J, Pluth J, Cooper P, Cowan M, Chen D, Yannone S. 2005a. Artemis deficiency confers a DNA double-strand break repair defect and Artemis phosphorylation status is altered by DNA damage and cell cycle progression. DNA Repair (Amst) 4:556-570.
96. Wang J, Pluth JM, Cooper PK, Cowan MJ, Chen DJ, Yannone SM. 2005b. Artemis deficiency confers a DNA double-strand break repair defect and Artemis phosphorylation status is altered by DNA damage and cell cycle progression. DNA Repair (Amst) 4:556-570.
97. Wang H, Zhang X, Geng L, Teng L, Legerski RJ. 2009. Artemis regulates cell cycle recovery from the S phase checkpoint by promoting degradation of cyclin E. J Biol Chem 284:18236-18243.
98. Wolter R, Siede W, Brendel M. 1996. Regulation of SNM1, an inducible Saccharomyces cerevisiae gene required for repair of DNA crosslinks. Mol Gen Genet 250:162-168.
99. Yu J, Marshall K, Yamaguchi M, Haber JE, Weil CF. 2004. Microhomology- dependent end joining and repair of transposon-induced DNA hairpins by host factors in Saccharomyces cerevisiae. Mol Cell Biol 24:1351-1364.
100. Zhang X, Richie C, Legerski R. 2002. Translation of hSNM1 is mediated by an internal ribosome entry site that upregulates expression during mitosis. DNA Repair (Amst) 1:379-390.
101. Zhang X, Succi J, Feng Z, Prithivirajsingh S, Story MD, Legerski RJ. 2004. Artemis is a phosphorylation target of ATM, ATR and is involved in the G2/M DNA damage checkpoint response. Mol Cell Biol 24:9207-9220.
102. Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y, Tomkinson AE, Gu L, Li GM. 2005. Reconstitution of 5′-directed human mismatch repair in a purified system. Cell 122:693-705.