Cited by 147DNA Repair MechanismsFungal and yeast genetics researchBacterial Genetics and Biotechnology

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RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation

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de la Torre‐Ruiz, Maria‐Angeles, Green, Catherine M., Lowndes, Noel F.·1998·The EMBO Journal

DOI 10.1093/emboj/17.9.2687PMC PMC1170609

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Abstract

In budding yeast, RAD9 and RAD24/RAD17/MEC3 are believed to function upstream of MEC1 and RAD53 in signalling the presence of DNA damage. Deletion of any one of these genes reduces the normal G1/S and G2/M checkpoint delays after UV irradiation, whereas in rad9Delta-rad24Delta cells the G1/S checkpoint is undetectable, although there is a residual G2/M checkpoint. We have shown previously that RAD9 also controls the transcriptional induction of a DNA damage regulon (DDR). We now report that efficient DDR induction requires all the above-mentioned checkpoint genes. Residual induction of the DDR after UV irradiation observed in all single mutants is not detectable in rad9Delta-rad24Delta. We have examined the G2/M checkpoint and UV sensitivity of single mutants after overexpression of the checkpoint proteins. This analysis indicates that RAD9 and the RAD24 epistasis group can be placed onto two separate, additive branches that converge on MEC1 and RAD53. Furthermore, MEC3 appears to function downstream of RAD24/RAD17. The transcriptional response to DNA damage revealed unexpected and specific antagonism between RAD9 and RAD24. Further support for genetic interaction between RAD9 and RAD24 comes from study of the modification and activation of Rad53 after damage. Evidence for bypass of RAD53 function under some conditions is also presented.

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Lee, S. E., Pellicioli, A., Vaze, M. B., Sugawara, N., Malkova, A., Foiani, M., & Haber, J. E. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.23.8913-8923.2003 · Cited by 60
“These checkpoint proteins include Rad17p, Rad24p, Mec3p, and Ddc1p that appear to act as DNA damage sensors (19, 20, 28), as well as Rad9p, which may be both a sensor and a modulator of protein kinases (5, 12).”
Background
Robust G1 checkpoint arrest in budding yeast: dependence on DNA damage signaling and repair
Gerald, J. N. F., Benjamin, J. M., & Kron, S. J. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.8.1749 · Cited by 54
An Origin-Deficient Yeast Artificial Chromosome Triggers a Cell Cycle Checkpoint
van Brabant, A. J., Buchanan, C. D., Charboneau, E., Fangman, W. L., & Brewer, B. J. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00216-7 · Cited by 54
Defending genome integrity during S-phase: putative roles for RecQ helicases and topoisomerase III
Oakley, T. J., & Hickson, I. D. (2002) · DNA repair · doi:10.1016/s1568-7864(02)00002-2 · Cited by 54
Role of Dot1 in the Response to Alkylating DNA Damage in Saccharomyces cerevisiae: Regulation of DNA Damage Tolerance by the Error-Prone Polymerases Polζ/Rev1
Conde, F., & San-Segundo, P. A. (2008) · Genetics · doi:10.1534/genetics.108.089003 · Cited by 51
“Genetic studies of DNA damage checkpoint mutants have placed RAD9 and RAD24 in different epistasis groups (Lydall and Weinert 1995; de la Torre-Ruiz et al. 1998).”
Background
Maintenance of Double-Stranded Telomeric Repeats as the Critical Determinant for Cell Viability in Yeast Cells Lacking Ku
Gravel, S., & Wellinger, R. J. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.7.2182-2193.2002 · Cited by 50
“In Yku cells incubated at 37°C, checkpoint activation is dependent on the RAD9 gene product (5, 75), a factor that has emerged as a candidate DNA damage sensor (18, 28, 50).”
Background
Activation of the Checkpoint Kinase Rad53 by the Phosphatidyl Inositol Kinase-like Kinase Mec1
Ma, N. J.-L., Lee, S.-J., Duong, J., & Stern, D. F. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507508200 · Cited by 50
RAD53 Regulates DBF4 Independently of Checkpoint Function in Saccharomyces cerevisiae
Dohrmann, P. R., Oshiro, G., Tecklenburg, M., & Sclafani, R. A. (1999) · Genetics · doi:10.1093/genetics/151.3.965 · Cited by 50
Ctf18-RFC and DNA Pol ϵ form a stable leading strand polymerase/clamp loader complex required for normal and perturbed DNA replication
Stokes, K., Winczura, A., Song, B., De Piccoli, G., & Grabarczyk, D. B. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa541 · Cited by 48
“Direct detection of Pol ε stalling by Ctf18-RFC and Mrc1 would be consistent with the rapid kinetics of the replication checkpoint, compared to slower activation of the compensatory RAD24 and RAD9-mediated DNA damage checkpoint by the slow build-up of unreplicated gaps and overpriming (74) (Figure 8C).”
BackgroundMethodInfluential
Activation of Ty transposition by mutagens
Staleva, L., & Venkov, P. (2001) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(00)00165-2 · Cited by 46
Fission Yeast Rad17 Associates with Chromatin in Response to Aberrant Genomic Structures
Kai, M., Tanaka, H., & Wang, T. S. ‐. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.10.3289-3301.2001 · Cited by 46
“pombe Cds1 and Chk1 counterparts) for cell cycle arrest (14, 25, 49).”
Background
DNA Damage Checkpoints Are Involved in Postreplication Repair
Barbour, L., Ball, L. G., Zhang, K., & Xiao, W. (2006) · Genetics · doi:10.1534/genetics.106.056283 · Cited by 43
Mdt1, a Novel Rad53 FHA1 Domain-Interacting Protein, Modulates DNA Damage Tolerance and G2/M Cell Cycle Progression in Saccharomyces cerevisiae
Pike, B. L., Yongkiettrakul, S., Tsai, M., & Heierhorst, J. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.7.2779-2788.2004 · Cited by 44
Genetic Analysis of Saccharomyces cerevisiae H2A Serine 129 Mutant Suggests a Functional Relationship Between H2A and the Sister-Chromatid Cohesion Partners Csm3–Tof1 for the Repair of Topoisomerase I-Induced DNA Damage
Redon, C. E., Pilch, D. R., & Bonner, W. M. (2005) · Genetics · doi:10.1534/genetics.105.046128 · Cited by 41
Involvement of the PP2C-Like Phosphatase Ptc2p in the DNA Checkpoint Pathways of Saccharomyces cerevisiae
Marsolier‐Kergoat, M., Roussel, P., Leroy, C., & Mann, C. (2000) · Genetics · doi:10.1093/genetics/154.4.1523 · Cited by 39
The Saccharomyces cerevisiae DNA damage checkpoint is required for efficient repair of double strand breaks by non‐homologous end joining
de la Torre-Ruiz, M. Á., & Lowndes, N. F. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01180-7 · Cited by 38
Self-citation
Eco1 is important for DNA damage repair inS. cerevisiae
Lu, S., Goering, M., Gard, S., Xiong, B., McNairn, A. J., Jaspersen, S. L., & Gerton, J. L. (2010) · Cell Cycle · doi:10.4161/cc.9.16.12673 · Cited by 35
“A rad9∆ mutant serves as a control; Rad53 is not phosphorylated in this mutant and cells do not arrest.(38,39) We conclude that the checkpoint is appropriately activated in the mutants and the sensitivity to ionizing radiation is due to a downstream defect.”
Background
Phosphorylation of Rph1, a damage-responsive repressor of PHR1 in Saccharomyces cerevisiae, is dependent upon Rad53 kinase
Kim, E.-M. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.3.643 · Cited by 32
“Several recent reports have suggested that the DNA damage checkpoint is linked directly or indirectly to the DNA damagedependent transcriptional response and to the delay of cell cycle progression (20, 21 ,25,28,29).”
Background
Roles for Gcn5 in promoting nucleosome assembly and maintaining genome integrity
Burgess, R. J., & Zhang, Z. (2010) · Cell Cycle · doi:10.4161/cc.9.15.12498 · Cited by 35
The Signal from the Initiation of Meiotic Recombination to the First Division of Meiosis
Malone, R. E., Haring, S. J., Foreman, K. E., Pansegrau, M. L., Smith, S. M., Houdek, D. R., Carpp, L. N., Shah, B. D., & Lee, K. E. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.3.598-609.2004 · Cited by 32
“Although both RAD9 and RAD24 are needed for proper checkpoint activity in the DNA damage pathway in mitosis (8), the RAD9 gene does not play a role in the meiotic pachytene checkpoint (29).”
Background
Small Ubiquitin-related Modifier Ligase Activity of Mms21 Is Required for Maintenance of Chromosome Integrity during the Unperturbed Mitotic Cell Division Cycle in Saccharomyces cerevisiae
Rai, R., Varma, S. P. M. V., Shinde, N. S., Ghosh, S., Kumaran, S. P., Skariah, G., & Laloraya, S. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.157149 · Cited by 31
Novel DNA‐Damaging Tropolone Derivatives from Goupia glabra
Mesa‐Siverio, D., Estévez‐Braun, A., Ravelo, Á. G., Murguía, J. R., & Rodrı́guez-Afonso, A. (2003) · European Journal of Organic Chemistry · doi:10.1002/ejoc.200300284 · Cited by 31
DUN1 defines one branch downstream of RAD53 for transcription and DNA damage repair in Saccharomyces cerevisiae
de la Torre-Ruiz, M. Á., & Lowndes, N. F. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)02198-0 · Cited by 31
Self-citation
Transcriptional induction of repair genes during slowing of replication in irradiated Saccharomyces cerevisiae
MERCIER, G., Denis, Y., Marc, P., Picard, L., & Dutreix, M. (2001) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(01)00116-1 · Cited by 29
The budding yeast Rad9 checkpoint complex: chaperone proteins are required for its function
Gilbert, C. S., van den Bosch, M., Green, C., Vialard, J. E., Grenon, M., Erdjument‐Bromage, H., Tempst, P., & Lowndes, N. F. (2003) · EMBO Reports · doi:10.1038/sj.embor.embor935 · Cited by 28
“The rad9Δ strain has been described previously (de la Torre-Ruiz et al., 1998).”
BackgroundMethodSelf-citation
Human and mouse RAD17 genes: identification, localization, genomic structure and histological expression pattern in normal testis and seminoma
von Deimling, F., Scharf, J. M., Liehr, T., Rothe, M., Kelter, A.-R., Albers, P., Dietrich, W. F., Kunkel, L. M., Wernert, N., & Wirth, B. (1999) · Human Genetics · doi:10.1007/s004390051058 · Cited by 28
Colocalization of human Rad17 and PCNA in late S phase of the cell cycle upon replication block
Dahm, K., & Hübscher, U. (2002) · Oncogene · doi:10.1038/sj.onc.1205872 · Cited by 28
Zim17/Tim15 links mitochondrial iron–sulfur cluster biosynthesis to nuclear genome stability
de la Loza, M. D. C. D., Gallardo, M., García-Rubio, M. L., Izquierdo, A., Herrero, E., Aguilera, A., & Wellinger, R. E. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr193 · Cited by 26
Genetic evidence for a role of Saccharomyces cerevisiae Mph1 in recombinational DNA repair under replicative stress
Panico, E. R., Ede, C., Schildmann, M., Schürer, K. A., & Kramer, W. (2009) · Yeast · doi:10.1002/yea.1727 · Cited by 26
“Upstream of Rad53, Rad9 and two more protein complexes signal the presence of DNA damage and fully activate Rad53 (De la Torre-Ruiz et al., 1998; Sanchez et al., 1999; Rouse and Jackson, 2002).”
Background
A Ddc2-Rad53 Fusion Protein Can Bypass the Requirements forRAD9andMRC1in Rad53 Activation
Lee, S.-J., Duong, J., & Stern, D. F. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-07-0608 · Cited by 27
“In G1 and G2, Rad53p activation in response to DNA damage requires RAD9, but not MRC1 (Navas et al., 1996; Paulovich et al., 1997; de la Torre Ruiz et al., 1998; Sun et al., 1998; Vialard et al., 1998; Alcasabas et al., 2001).”
BackgroundInfluential
The DNA Damage Checkpoint and Human CancerPreprint
Schultz, L. B., Chehab, N. H., Malikzay, A., DiTullio, R. A., Stavridi, E. S., & Halazonetis, T. D. (2000) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2000.65.489 · Cited by 26
The Saccharomyces cerevisiae RAD9 cell cycle checkpoint gene is required for optimal repair of UV-induced pyrimidine dimers in both G1 and G2/M phases of the cell cycle
Al-Moghrabi, N. M. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.10.2020 · Cited by 24
“Since the RAD9 gene product is known to be essential for DNA damage-dependent transactivation of several NER proteins (17, 18 ), without itself being inducible (11,15), it is reasonable to assume that the DNA repair defect observed in the rad9∆ cells may be due to a failure in the up-regulation of the RAD9-controlled…”
Background
Double-strand breaks trigger MRX- and Mec1-dependent, but Tel1-independent, checkpoint activation
Grenon, M., Magill, C. P., Lowndes, N. F., & Jackson, S. P. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00076.x · Cited by 22
“Serum NLO5 was used to detect Rad9 (de la Torre-Ruiz et al., 1998; Vialard et al., 1998).”
BackgroundMethodSelf-citation
DNA Replication and Sister Chromatid Cohesion 1 (DSCC1) of the Replication Factor Complex CTF18-RFC is Critical for Colon Cancer Cell Growth
Kim, J., Cho, H. J., Park, S., Oh, B. M., Hwang, Y. S., Baek, K. E., Lee, Y., Kim, H. C., & Lee, H. G. (2019) · Journal of Cancer · doi:10.7150/jca.32339 · Cited by 20
“The prototypical member (Rfc1-RFC) is essential for all replication and repair processes, whereas Rad24-RFC is involved in the DNA-damage checkpoint response [8-10], and Elg1-RFC is involved in proliferating cell Ivyspring”
Background

Authors: de la Torre‐Ruiz, M., Green, C. M., & Lowndes, N. F.
Corresponding author: Lowndes, Noel F.
ORCID: Lowndes, Noel F.
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 1998-05-01
Volume: 17
Issue: 9
Pages: 2687-2698
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.1093/emboj/17.9.2687
PMC: PMC1170609
OpenAlex: W2110112613
Cited by: 147
References: 33
Citations by year: 2024: 5 · 2023: 1 · 2021: 1 · 2020: 2 · 2019: 1 · 2017: 1 · 2016: 1 · 2015: 1 · 2014: 2 · 2013: 3 · 2012: 2
FWCI: 6.06
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: The EMBO Journal (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Rad9, Rad24, Rad17, Mec1, Rad53, DNA damage checkpoint, G1/S checkpoint, G2/M checkpoint, DNA damage response, UV irradiation, epistasis, genetic interactions, Saccharomyces cerevisiae
MeSH terms: Mating Factor, Cell Cycle, DNA Damage, DNA-Binding Proteins, DNA, Fungal, Exodeoxyribonucleases, Fungal Proteins, Kinetics, Mitosis, Nuclear Proteins, Peptides, Phosphorylation, Saccharomyces cerevisiae, Ultraviolet Rays, Nocodazole, G1 Phase, G2 Phase, S Phase, Cell Cycle Proteins, Saccharomyces cerevisiae Proteins, Intracellular Signaling Peptides and Proteins

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RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation

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