Deregulated Ras signaling compromises DNA damage checkpoint recovery in S. cerevisiae

Cell Cycle

Volumn 9, Issue 16, 2010, Pages 3373-3383

  Wood, Matthew D ^a   Sanchez, Yolanda ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Anaphase promoting complex; Budding yeast; Camp dependent protein kinase; Dna damage checkpoint; Neurofibromatosis type 1; Ras signaling

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; DNA; NEUROFIBROMIN; PROTEIN KINASE; RAS PROTEIN;

ANAPHASE; ANIMAL CELL; ARTICLE; BUDDING; CELL CYCLE ARREST; CONTROLLED STUDY; CONVALESCENCE; DNA DAMAGE; GENE DELETION; HUMAN; METAPHASE; MITOSIS; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; YEAST;

SACCHAROMYCETALES;

EID: 77955720762     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.16.12713     Document Type: Article

References (47)

1. Elledge SJ. Cell cycle checkpoints: preventing an identity crisis. Science 1996; 274:1664-72.
2. Hartwell LH, Kastan MB. Cell cycle control and cancer. Science 1994; 266:1821-8.
3. Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 2000; 408:433-9.
4. Chen Y, Sanchez Y. Chk1 in the DNA damage response: conserved roles from yeasts to mammals. DNA Repair 2004; 3:1025-32.
5. Sanchez Y, Wong C, Thoma RS, Richman R, Wu Z, Piwnica-Worms H, et al. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 1997; 277:1497-501.
6. Agarwal R, Tang Z, Yu H, Cohen-Fix O. Two distinct pathways for inhibiting pds1 ubiquitination in response to DNA damage. J Biol Chem. 2003; 278:45027-33.
7. Sanchez Y, Bachant J, Wang H, Hu F, Liu D, Tetzlaff M, et al. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 1999; 286:1166-71.
8. Wang H, Liu D, Wang Y, Qin J, Elledge SJ. Pds1 phosphorylation in response to DNA damage is essential for its DNA damage checkpoint function. Genes Dev 2001; 15:1361-72.
9. Hu F, Wang Y, Liu D, Li Y, Qin J, Elledge SJ. Regulation of the Bub2/Bfa1 GAP complex by Cdc5 and cell cycle checkpoints. Cell 2001; 107:655-65.
10. Searle JS, Schollaert KL, Wilkins BJ, Sanchez Y. The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat Cell Biol 2004; 6:138-45.
11. Park JI, Grant CM, Dawes IW. The high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae is the major determinant of cAMP levels in stationary phase: involvement of different branches of the Ras-cyclic AMP pathway in stress responses. Biochem Biophys Res Commun 2005; 327:311-9.
12. Kataoka T, Powers S, Cameron S, Fasano O, Goldfarb M, Broach J, et al. Functional homology of mammalian and yeast RAS genes. Cell 1985; 40:19-26.
13. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, et al. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 1985; 40:27-36.
14. Tanaka K, Matsumoto K, Toh EA. IRA1, an inhibitory regulator of the RAS-cyclic AMP pathway in Saccharomyces cerevisiae. Mol Cell Biol. 1989; 9:757-68.
15. Tanaka K, Nakafuku M, Tamanoi F, Kaziro Y, Matsumoto K, Toh-e A. IRA2, a second gene of Saccharomyces cerevisiae that encodes a protein with a domain homologous to mammalian ras GTPase-activating protein. Mol Cell Biol1990; 10:4303-13.
16. Tanaka K, Nakafuku M, Satoh T, Marshall MS, Gibbs JB, Matsumoto K, et al. S. cerevisiae genes IRA1 and IRA2 encode proteins that may be functionally equivalent to mammalian ras GTPase activating protein. Cell 1990; 60:803-7.
17. Harashima T, Anderson S, Yates JR, 3rd, Heitman J. The kelch proteins Gpb1 and Gpb2 inhibit Ras activity via association with the yeast RasGAP neurofibromin homologs Ira1 and Ira2. Mol cell 2006; 22:819-30.
18. Clemenson C, Marsolier-Kergoat MC. DNA damage checkpoint inactivation: adaptation and recovery. DNA Repair 2009; 8:1101-9.
19. Bazzi M, Mantiero D, Trovesi C, Lucchini G, Longhese MP. Dephosphorylation of gamma H2A by Glc7/protein phosphatase 1 promotes recovery from inhibition of DNA replication. Mol Cell Biol 30:131-45.
20. Guillemain G, Ma E, Mauger S, Miron S, Thai R, Guerois R, et al. Mechanisms of checkpoint kinase Rad53 inactivation after a double-strand break in Saccharomyces cerevisiae. Mol Cell Biol 2007; 27:3378-89.
21. Leroy C, Lee SE, Vaze MB, Ochsenbien F, Guerois R, Haber JE, et al. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol cell 2003; 11:827-35.
22. Sandell LL, Zakian VA. Loss of a yeast telomere: arrest, recovery and chromosome loss. Cell 1993; 75:729-39.
23. Toczyski DP, Galgoczy DJ, Hartwell LH. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 1997; 90:1097-106.
24. 2/M arrest. Mol cell 2001; 7:293-300.
25. Vaze MB, Pellicioli A, Lee SE, Ira G, Liberi G, Arbel-Eden A, et al. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol cell 2002; 10:373-85.
26. Schwartz DC, Felberbaum R, Hochstrasser M. The Ulp2 SUMO protease is required for cell division following termination of the DNA damage checkpoint. Mol Cell Biol 2007; 27:6948-61.
27. Ballester R, Marchuk D, Boguski M, Saulino A, Letcher R, Wigler M, et al. The NF1 locus encodes a protein functionally related to mammalian GAP and yeast IRA proteins. Cell 1990; 63:851-9.
28. Buchberg AM, Cleveland LS, Jenkins NA, Copeland NG. Sequence homology shared by neurofibromatosis type-1 gene and IRA-1 and IRA-2 negative regulators of the RAS cyclic AMP pathway. Nature 1990; 347:291-4.
29. Carroll SL, Ratner N. How does the Schwann cell lineage form tumors in NF1? Glia 2008; 56:1590-605.
30. Kim HA, Ratner N, Roberts TM, Stiles CD. Schwann cell proliferative responses to cAMP and Nf1 are mediated by cyclin D1. J Neurosci 2001; 21:1110-6.
31. Sheela S, Riccardi VM, Ratner N. Angiogenic and invasive properties of neurofibroma Schwann cells. The J Cell Biol 1990; 111:645-53.
32. + current in Schwann cells: a protein kinase A-mediated mechanism. J Neurosci 2002; 22:9194-202.
33. Evans DG, Birch JM, Ramsden RT, Sharif S, Baser ME. Malignant transformation and new primary tumours after therapeutic radiation for benign disease: substantial risks in certain tumour prone syndromes. J Med Genet 2006; 43:289-94.
34. Sharif S, Ferner R, Birch JM, Gillespie JE, Gattamaneni HR, Baser ME, et al. Second primary tumors in neurofibromatosis 1 patients treated for optic glioma: substantial risks after radiotherapy. J Clin Oncol 2006; 24:2570-5.
35. Seshan A, Amon A. Ras and the Rho effector Cla4 collaborate to target and anchor Lte1 at the bud cortex. Cell Cycle 2005; 4:940-6.
36. Yoshida S, Ichihashi R, Toh-e A. Ras recruits mitotic exit regulator Lte1 to the bud cortex in budding yeast. J Cell Biol 2003; 161:889-97.
37. Hanway D, Chin JK, Xia G, Oshiro G, Winzeler EA, Romesberg FE. Previously uncharacterized genes in the UV- and MMS-induced DNA damage response in yeast. Proc Natl Acad Sci U S A 2002; 99:10605-10.
38. Schleker T, Shimada K, Sack R, Pike BL, Gasser SM. Cell cycle-dependent phosphorylation of Rad53 kinase by Cdc5 and Cdc28 modulates checkpoint adaptation. Cell Cycle 9:350-63.
39. Clemenson C, Marsolier-Kergoat MC. The spindle assembly checkpoint regulates the phosphorylation state of a subset of DNA checkpoint proteins in Saccharomyces cerevisiae. Mol Cell Biol 2006; 26:9149-61.
40. 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 U S A 2007; 104:11358-63.
41. Zaman S, Lippman SI, Zhao X, Broach JR. How Saccharomyces responds to nutrients. Annu Rev Genet 2008; 42:27-81.
42. Bolte M, Dieckhoff P, Krause C, Braus GH, Irniger S. Synergistic inhibition of APC/C by glucose and activated Ras proteins can be mediated by each of the Tpk1-3 proteins in Saccharomyces cerevisiae. Microbiology 2003; 149:1205-16.
43. Anghileri P, Branduardi P, Sternieri F, Monti P, Visintin R, Bevilacqua A, et al. Chromosome separation and exit from mitosis in budding yeast: dependence on growth revealed by cAMP-mediated inhibition. Exp Cell Res 1999; 250:510-23.
44. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW. The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev1999; 13:532-44.
45. Pinsky BA, Kung C, Shokat KM, Biggins S. The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol 2006; 8:78-83.
46. Li JM, Li Y, Elledge SJ. Genetic analysis of the kinetochore DASH complex reveals an antagonistic relationship with the ras/protein kinase A pathway and a novel subunit required for Ask1 association. Mol Cell Biol 2005; 25:767-78.
47. Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev 1994; 8:2401-15.