An S/T-Q cluster domain census unveils new putative targets under Tel1/Mec1 control

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Cheung, Hannah C ^a   San Lucas, F Anthony ^b   Hicks, Stephanie ^c   Chang, Kyle ^a   Bertuch, Alison A ^a   Ribes Zamora, Albert ^d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c Rice University   (United States)

^d UNIVERSITY OF ST THOMAS   (United States)

Author keywords

ATM; ATR; DNA damage response; Phosphorylation; Proteome; Tel1 Mec1

Indexed keywords

GLUTAMINE; PROTEIN KINASE; PROTEIN MEC1; PROTEIN TEL1; SERINE; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CYTOKINESIS; DNA DAMAGE; ENDOCYTOSIS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN TARGETING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; ST Q CLUSTER DOMAIN; TELOPHASE;

AMINO ACID MOTIFS; COMPUTATIONAL BIOLOGY; GLUTAMINE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE; THREONINE;

SACCHAROMYCES CEREVISIAE;

EID: 84869865644     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-664     Document Type: Article

References (87)

1. Putnam CD, Jaehnig EJ, Kolodner RD. Perspectives on the DNA damage and replication checkpoint responses in Saccharomyces cerevisiae. DNA Repair (Amst) 2009, 8:974-982.
2. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007, 28:739-745. 10.1016/j.molcel.2007.11.015, 18082599.
3. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004, 73:39-85. 10.1146/annurev.biochem.73.011303.073723, 15189136.
4. Traven A, Heierhorst J. SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays 2005, 27:397-407. 10.1002/bies.20204, 15770685.
5. Su TT. Cellular responses to DNA damage: one signal, multiple choices. Annu Rev Genet 2006, 40:187-208. 10.1146/annurev.genet.40.110405.090428, 16805666.
6. Goudsouzian LK, Tuzon CT, Zakian VA. S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol Cell 2006, 24:603-610. 10.1016/j.molcel.2006.10.005, 17188035.
7. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 2008, 7:1389-1396. 10.1074/mcp.M700468-MCP200, 2493382, 18407956.
8. Stokes MP, Rush J, Macneill J, Ren JM, Sprott K, Nardone J, Yang V, Beausoleil SA, Gygi SP, Livingstone M, et al. Profiling of UV-induced ATM/ATR signaling pathways. Proc Natl Acad Sci USA 2007, 104:19855-19860. 10.1073/pnas.0707579104, 2148387, 18077418.
9. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166. 10.1126/science.1140321, 17525332.
10. Lee H, Yuan C, Hammet A, Mahajan A, Chen ES, Wu MR, Su MI, Heierhorst J, Tsai MD. Diphosphothreonine-specific interaction between an SQ/TQ cluster and an FHA domain in the Rad53-Dun1 kinase cascade. Mol Cell 2008, 30:767-778. 10.1016/j.molcel.2008.05.013, 18570878.
11. Usui T, Foster SS, Petrini JH. Maintenance of the DNA-damage checkpoint requires DNA-damage-induced mediator protein oligomerization. Mol Cell 2009, 33:147-159. 10.1016/j.molcel.2008.12.022, 2995296, 19187758.
12. Smolka MB, Albuquerque CP, Chen SH, Zhou H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc Natl Acad Sci USA 2007, 104:10364-10369. 10.1073/pnas.0701622104, 1965519, 17563356.
13. Chen SH, Albuquerque CP, Liang J, Suhandynata RT, Zhou H. A proteome-wide analysis of kinase-substrate network in the DNA damage response. J Biol Chem 2010, 285:12803-12812. 10.1074/jbc.M110.106989, 2857137, 20190278.
14. Caydasi AK, Ibrahim B, Pereira G. Monitoring spindle orientation: Spindle position checkpoint in charge. Cell Div 2010, 5:28. 10.1186/1747-1028-5-28, 3004881, 21143992.
15. Moseley JB, Goode BL. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol Mol Biol Rev 2006, 70:605-645. 10.1128/MMBR.00013-06, 1594590, 16959963.
16. Peddibhotla S, Rosen JM. Chking and executing cell division to prevent genomic instability. Cell Cycle 2009, 8:2339-2342. 10.4161/cc.8.15.9169, 19571679.
17. Chabes A, Georgieva B, Domkin V, Zhao X, Rothstein R, Thelander L. Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 2003, 112:391-401. 10.1016/S0092-8674(03)00075-8, 12581528.
18. Huang M, Zhou Z, Elledge SJ. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 1998, 94:595-605. 10.1016/S0092-8674(00)81601-3, 9741624.
19. Miyamoto S. Nuclear initiated NF-kappaB signaling: NEMO and ATM take center stage. Cell Res 2011, 21:116-130. 10.1038/cr.2010.179, 3193401, 21187855.
20. Daniel JA, Keyes BE, Ng YP, Freeman CO, Burke DJ. Diverse functions of spindle assembly checkpoint genes in Saccharomyces cerevisiae. Genetics 2006, 172:53-65. 1456180, 16157669.
21. Kim EM, Burke DJ. DNA damage activates the SAC in an ATM/ATR-dependent manner, independently of the kinetochore. PLoS Genet 2008, 4:e1000015. 10.1371/journal.pgen.1000015, 2265443, 18454191.
22. Dotiwala F, Haase J, Arbel-Eden A, Bloom K, Haber JE. The yeast DNA damage checkpoint proteins control a cytoplasmic response to DNA damage. Proc Natl Acad Sci USA 2007, 104:11358-11363. 10.1073/pnas.0609636104, 1896138, 17586685.
23. Oricchio E, Saladino C, Iacovelli S, Soddu S, Cundari E. ATM is activated by default in mitosis, localizes at centrosomes and monitors mitotic spindle integrity. Cell Cycle 2006, 5:88-92. 10.4161/cc.5.1.2269, 16319535.
24. Krishnan R, Pangilinan F, Lee C, Spencer F. Saccharomyces cerevisiae BUB2 prevents mitotic exit in response to both spindle and kinetochore damage. Genetics 2000, 156:489-500. 1461296, 11014800.
25. Park SY, Cable AE, Blair J, Stockstill KE, Shannnon KB. Bub2 regulation of cytokinesis and septation in budding yeast. BMC Cell Biol 2009, 10:43. 10.1186/1471-2121-10-43, 2701927, 19490645.
26. Evangelista M, Zigmond S, Boone C. Formins: signaling effectors for assembly and polarization of actin filaments. J Cell Sci 2003, 116:2603-2611. 10.1242/jcs.00611, 12775772.
27. Oh Y, Bi E. Septin structure and function in yeast and beyond. Trends Cell Biol 2011, 21:141-148. 10.1016/j.tcb.2010.11.006, 3073566, 21177106.
28. Wang Y, Shirogane T, Liu D, Harper JW, Elledge SJ. Exit from exit: resetting the cell cycle through Amn1 inhibition of G protein signaling. Cell 2003, 112:697-709. 10.1016/S0092-8674(03)00121-1, 12628189.
29. Nelson B, Kurischko C, Horecka J, Mody M, Nair P, Pratt L, Zougman A, McBroom LD, Hughes TR, Boone C, et al. RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol Biol Cell 2003, 14:3782-3803. 10.1091/mbc.E03-01-0018, 196567, 12972564.
30. Roncero C, Sanchez Y. Cell separation and the maintenance of cell integrity during cytokinesis in yeast: the assembly of a septum. Yeast 2010, 27:521-530. 10.1002/yea.1779, 20641019.
31. Harvey SL, Kellogg DR. Conservation of mechanisms controlling entry into mitosis: budding yeast wee1 delays entry into mitosis and is required for cell size control. Curr Biol 2003, 13:264-275. 10.1016/S0960-9822(03)00049-6, 12593792.
32. Nash RS, Volpe T, Futcher B. Isolation and characterization of WHI3, a size-control gene of Saccharomyces cerevisiae. Genetics 2001, 157:1469-1480. 1461599, 11290704.
33. Wickliffe K, Williamson A, Jin L, Rape M. The multiple layers of ubiquitin-dependent cell cycle control. Chem Rev 2009, 109:1537-1548. 10.1021/cr800414e, 3206288, 19146381.
34. Jonkers W, Rep M. Lessons from fungal F-box proteins. Eukaryot Cell 2009, 8:677-695. 10.1128/EC.00386-08, 2681605, 19286981.
35. Ho MS, Tsai PI, Chien CT. F-box proteins: the key to protein degradation. J Biomed Sci 2006, 13:181-191. 10.1007/s11373-005-9058-2, 16463014.
36. Huen MS, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007, 131:901-914. 10.1016/j.cell.2007.09.041, 2149842, 18001825.
37. Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, Panier S, Mendez M, Wildenhain J, Thomson TM, et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007, 318:1637-1640. 10.1126/science.1150034, 2430610, 18006705.
38. van Attikum H, Gasser SM. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol 2009, 19:207-217. 10.1016/j.tcb.2009.03.001, 19342239.
39. Ghosh S, Saha T. Central role of ubiquitination in genome maintenance: DNA replication and damage repair. In: ISRN Mol Biol. vol. 2012, 2012:9.
40. Cortez D, Glick G, Elledge SJ. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci USA 2004, 101:10078-10083. 10.1073/pnas.0403410101, 454167, 15210935.
41. Gohler T, Sabbioneda S, Green CM, Lehmann AR. ATR-mediated phosphorylation of DNA polymerase eta is needed for efficient recovery from UV damage. J Cell Biol 2011, 192:219-227. 10.1083/jcb.201008076, 3172178, 21242293.
42. Friedel AM, Pike BL, Gasser SM. ATR/Mec1: coordinating fork stability and repair. Curr Opin Cell Biol 2009, 21:237-244. 10.1016/j.ceb.2009.01.017, 19230642.
43. Hegnauer AM, Hustedt N, Shimada K, Pike BL, Vogel M, Amsler P, Rubin SM, van Leeuwen F, Guenole A, van Attikum H, et al. An N-terminal acidic region of Sgs1 interacts with Rpa70 and recruits Rad53 kinase to stalled forks. EMBO J 2012, 31:3768-3783. 10.1038/emboj.2012.195, 22820947.
44. Lou H, Komata M, Katou Y, Guan Z, Reis CC, Budd M, Shirahige K, Campbell JL. Mrc1 and DNA polymerase epsilon function together in linking DNA replication and the S phase checkpoint. Mol Cell 2008, 32:106-117. 10.1016/j.molcel.2008.08.020, 2699584, 18851837.
45. Labib K. Making connections at DNA replication forks: Mrc1 takes the lead. Mol Cell 2008, 32:166-168. 10.1016/j.molcel.2008.10.005, 18951084.
46. Hanna JS, Kroll ES, Lundblad V, Spencer FA. Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion. Mol Cell Biol 2001, 21:3144-3158. 10.1128/MCB.21.9.3144-3158.2001, 86942, 11287619.
47. Tomimatsu N, Mukherjee B, Burma S. Distinct roles of ATR and DNA-PKcs in triggering DNA damage responses in ATM-deficient cells. EMBO Rep 2009, 10:629-635. 10.1038/embor.2009.60, 2711839, 19444312.
48. Hirano T. The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev 2002, 16:399-414. 10.1101/gad.955102, 11850403.
49. Wood AJ, Severson AF, Meyer BJ. Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 2010, 11:391-404. 3491780, 20442714.
50. Rouse J. Control of genome stability by SLX protein complexes. Biochem Soc Trans 2009, 37:495-510. 10.1042/BST0370495, 19442243.
51. Baroni E, Viscardi V, Cartagena-Lirola H, Lucchini G, Longhese MP. The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol Cell Biol 2004, 24:4151-4165. 10.1128/MCB.24.10.4151-4165.2004, 400471, 15121837.
52. Perry JJ, Cotner-Gohara E, Ellenberger T, Tainer JA. Structural dynamics in DNA damage signaling and repair. Curr Opin Struct Biol 2010, 20:283-294. 10.1016/j.sbi.2010.03.012, 2916978, 20439160.
53. Cline SD, Hanawalt PC. Who's on first in the cellular response to DNA damage?. Nat Rev Mol Cell Biol 2003, 4:361-372. 10.1038/nrm1101, 12728270.
54. Marini V, Krejci L. Srs2: the "Odd-Job Man" in DNA repair. DNA Repair (Amst) 2010, 9:268-275.
55. Iijima K, Ohara M, Seki R, Tauchi H. Dancing on damaged chromatin: functions of ATM and the RAD50/MRE11/NBS1 complex in cellular responses to DNA damage. J Radiat Res 2008, 49:451-464. 10.1269/jrr.08065, 18772547.
56. Paull TT. Making the best of the loose ends: Mre11/Rad50 complexes and Sae2 promote DNA double-strand break resection. DNA Repair (Amst) 2010, 9:1283-1291.
57. Mimitou EP, Symington LS. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 2008, 455:770-774. 10.1038/nature07312, 18806779.
58. Petukhova G, Van Komen S, Vergano S, Klein H, Sung P. Yeast Rad54 promotes Rad51-dependent homologous DNA pairing via ATP hydrolysis-driven change in DNA double helix conformation. J Biol Chem 1999, 274:29453-29462. 10.1074/jbc.274.41.29453, 10506208.
59. Williams GJ, Lees-Miller SP, Tainer JA. Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair (Amst) 2010, 9:1299-1306.
60. Gao H, Toro TB, Paschini M, Braunstein-Ballew B, Cervantes RB, Lundblad V. Telomerase recruitment in Saccharomyces cerevisiae is not dependent on Tel1-mediated phosphorylation of Cdc13. Genetics 2010, 186:1147-1159. 10.1534/genetics.110.122044, 2998300, 20837994.
61. Flott S, Alabert C, Toh GW, Toth R, Sugawara N, Campbell DG, Haber JE, Pasero P, Rouse J. Phosphorylation of Slx4 by Mec1 and Tel1 regulates the single-strand annealing mode of DNA repair in budding yeast. Mol Cell Biol 2007, 27:6433-6445. 10.1128/MCB.00135-07, 2099619, 17636031.
62. Rouse J. Esc4p, a new target of Mec1p (ATR), promotes resumption of DNA synthesis after DNA damage. EMBO J 2004, 23:1188-1197. 10.1038/sj.emboj.7600129, 380984, 14988729.
63. Jelinsky SA, Samson LD. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc Natl Acad Sci USA 1999, 96:1486-1491. 10.1073/pnas.96.4.1486, 15489, 9990050.
64. Fu Y, Pastushok L, Xiao W. DNA damage-induced gene expression in Saccharomyces cerevisiae. FEMS Microbiol Rev 2008, 32:908-926. 10.1111/j.1574-6976.2008.00126.x, 18616603.
65. Jordan A, Reichard P. Ribonucleotide reductases. Annu Rev Biochem 1998, 67:71-98. 10.1146/annurev.biochem.67.1.71, 9759483.
66. Rodriguez-Navarro S. Insights into SAGA function during gene expression. EMBO Rep 2009, 10:843-850. 10.1038/embor.2009.168, 2726681, 19609321.
67. Carballo JA, Johnson AL, Sedgwick SG, Cha RS. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 2008, 132:758-770. 10.1016/j.cell.2008.01.035, 18329363.
68. Cartagena-Lirola H, Guerini I, Viscardi V, Lucchini G, Longhese MP. Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis. Cell Cycle 2006, 5:1549-1559. 10.4161/cc.5.14.2916, 16861895.
69. Brito IL, Monje-Casas F, Amon A. The Lrs4-Csm1 monopolin complex associates with kinetochores during anaphase and is required for accurate chromosome segregation. Cell Cycle 2010, 9:3611-3618. 10.4161/cc.9.17.12885, 3047622, 20818155.
70. Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci USA 2005, 102:737-742. 10.1073/pnas.0406212102, 545532, 15640358.
71. Ghavidel A, Kislinger T, Pogoutse O, Sopko R, Jurisica I, Emili A. Impaired tRNA nuclear export links DNA damage and cell-cycle checkpoint. Cell 2007, 131:915-926. 10.1016/j.cell.2007.09.042, 18045534.
72. Titov AA, Blobel G. The karyopherin Kap122p/Pdr6p imports both subunits of the transcription factor IIA into the nucleus. J Cell Biol 1999, 147:235-246. 10.1083/jcb.147.2.235, 2174230, 10525531.
73. Strawn LA, Shen T, Wente SR. The GLFG regions of Nup116p and Nup100p serve as binding sites for both Kap95p and Mex67p at the nuclear pore complex. J Biol Chem 2001, 276:6445-6452. 10.1074/jbc.M008311200, 11104765.
74. Greiner M, Caesar S, Schlenstedt G. The histones H2A/H2B and H3/H4 are imported into the yeast nucleus by different mechanisms. Eur J Cell Biol 2004, 83:511-520. 10.1078/0171-9335-00418, 15679097.
75. Strambio-De-Castillia C, Niepel M, Rout MP. The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 2010, 11:490-501. 10.1038/nrm2928, 20571586.
76. Wente SR, Rout MP. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2010, 2:a000562. 10.1101/cshperspect.a000562, 2944363, 20630994.
77. Sabourin M, Zakian VA. ATM-like kinases and regulation of telomerase: lessons from yeast and mammals. Trends Cell Biol 2008, 18:337-346. 10.1016/j.tcb.2008.04.004, 2556866, 18502129.
78. Hector RE, Shtofman RL, Ray A, Chen BR, Nyun T, Berkner KL, Runge KW. Tel1p preferentially associates with short telomeres to stimulate their elongation. Mol Cell 2007, 27:851-858. 10.1016/j.molcel.2007.08.007, 17803948.
79. Tseng SF, Shen ZJ, Tsai HJ, Lin YH, Teng SC. Rapid Cdc13 turnover and telomere length homeostasis are controlled by Cdk1-mediated phosphorylation of Cdc13. Nucleic Acids Res 2009, 37:3602-3611. 10.1093/nar/gkp235, 2699520, 19359360.
80. Arneric M, Lingner J. Tel1 kinase and subtelomere-bound Tbf1 mediate preferential elongation of short telomeres by telomerase in yeast. EMBO Rep 2007, 8:1080-1085. 10.1038/sj.embor.7401082, 2247385, 17917674.
81. McGee JS, Phillips JA, Chan A, Sabourin M, Paeschke K, Zakian VA. Reduced Rif2 and lack of Mec1 target short telomeres for elongation rather than double-strand break repair. Nat Struct Mol Biol 2010, 17:1438-1445. 10.1038/nsmb.1947, 3058685, 21057524.
82. Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, Winderickx J. Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae. Curr Genet 2010, 56:1-32. 10.1007/s00294-009-0287-1, 20054690.
83. O'Rourke SM, Herskowitz I, O'Shea EK. Yeast go the whole HOG for the hyperosmotic response. Trends Genet 2002, 18:405-412. 10.1016/S0168-9525(02)02723-3, 12142009.
84. Clotet J, Posas F. Control of cell cycle in response to osmostress: lessons from yeast. Methods Enzymol 2007, 428:63-76.
85. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell 2006, 124:471-484. 10.1016/j.cell.2006.01.016, 16469695.
86. Girao H, Geli MI, Idrissi FZ. Actin in the endocytic pathway: from yeast to mammals. FEBS Lett 2008, 582:2112-2119. 10.1016/j.febslet.2008.04.011, 18420037.
87. Robin S. A compound Poisson model for word occurrences in DNA sequences. J R Stat Soc C-Appl 2002, 51:437-541.