Cited by 420DNA Repair MechanismsFungal and yeast genetics researchBacterial Genetics and Biotechnology

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Global response of Saccharomyces cerevisiae to an alkylating agent

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Jelinsky, Scott A., Samson, Leona D.·1999·Proceedings of the National Academy of Sciences

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Abstract

DNA chip technology enables simultaneous examination of how ≈6,200 Saccharomyces cerevisiae gene transcript levels, representing the entire genome, respond to environmental change. By using chips bearing oligonucleotide arrays, we show that, after exposure to the alkylating agent methyl methanesulfonate, ≈325 gene transcript levels are increased and ≈76 are decreased. Of the 21 genes that already were known to be induced by a DNA-damaging agent, 18 can be scored as inducible in this data set, and surprisingly, most of the newly identified inducible genes are induced even more strongly than these 18. We examined 42 responsive and 8 nonresponsive ORFs by conventional Northern blotting, and 48 of these 50 ORFs responded as they did by DNA chip analysis, with magnitudes displaying a correlation coefficient of 0.79. Responsive genes fall into several expected and many unexpected categories. Evidence for the induction of a program to eliminate and replace alkylated proteins is presented.

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Multiprotein bridging factor 1 is required for robust activation of the integrated stress response on collided ribosomes
Kim, K. Q., Li, J. J., Urs, A. N. N., Pacheco, M., Lasehinde, V., Denk, T., Těšina, P., Tomomatsu, S., Matsuo, Y., McDonald, E., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.10.029 · Cited by 23
Systems based mapping demonstrates that recovery from alkylation damage requires DNA repair, RNA processing, and translation associated networks
Rooney, J. P., George, A. D., Patil, A., Begley, U., Bessette, E. E., Zappala, M. R., Huang, X., Conklin, D. S., Cunningham, R. P., & Begley, T. J. (2008) · Genomics · doi:10.1016/j.ygeno.2008.09.001 · Cited by 20
Specific transcriptional responses induced by 8-methoxypsoralen and UVA in yeast
Dardalhon, M., Lin, W., Nicolas, A. G., & Averbeck, D. (2007) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2007.00270.x · Cited by 20
“The genes that were up- or down-regulated after 8-MOP/ UVA exposure (see supplementary Table 1) were compared to those affected by other genotoxic agents (Jelinsky & Samson, 1999; Jelinsky et al., 2000; Gasch et al., 2001; Keller-Seitz et al., 2004; Mercier et al., 2004, 2005; Caba et al., 2005).”
Result
A Role for Checkpoint Kinase-Dependent Rad26 Phosphorylation in Transcription-Coupled DNA Repair in Saccharomyces cerevisiae
Taschner, M., Harreman, M., Teng, Y., Gill, H., Anindya, R., Maslen, S. L., Skehel, J. M., Waters, R., & Svejstrup, J. Q. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00822-09 · Cited by 19
“Indeed, approximately 5% of the yeast genome is upregulated in response to various DNA-damaging agents (15, 23, 24).”
Background
Increased genome instability is not accompanied by sensitivity to DNA damaging agents in aged yeast cells
Novarina, D., Mouton, S. N., Janssens, G. E., Rempel, I. L., Veenhoff, L. M., & Chang, M. (2017) · DNA repair · doi:10.1016/j.dnarep.2017.03.005 · Cited by 20
Modulation of the yeast protein interactome in response to DNA damage
Rochette, S., Gagnon‐Arsenault, I., Diss, G., & Landry, C. R. (2013) · Journal of Proteomics · doi:10.1016/j.jprot.2013.11.007 · Cited by 19
Transcriptional Effects of the Potent Enediyne Anti-Cancer Agent Calicheamicin γ1I
Watanabe, C. M. H., Supeková, Ľ., & Schultz, P. G. (2002) · Chemistry & Biology · doi:10.1016/s1074-5521(02)00103-5 · Cited by 19
Isolation and analysis of differentially expressed genes in Penicillium glabrum subjected to thermal stress
Névarez, L., Vasseur, V., Dréan, G. L., Tanguy, A., Guisle, I., Houlgatte, R., & Barbier, G. (2008) · Microbiology · doi:10.1099/mic.0.2008/021386-0 · Cited by 19
“For example, in Sac. cerevisiae mRNAs have been reported to represent an important part of total mRNAs; repression of these genes may therefore allow energy to be dedicated to increased expression of genes involved in the protective response (Jelinsky & Samson, 1999).”
Background
Ecotoxicological studies on the pejerrey (Odontesthes bonariensis, Pisces atherinopsidae).
Carriquiriborde, P., & Ronco, A. E. (2006) · PubMed · Cited by 19
Regulation of Saccharomyces cerevisiae DNA polymerase η transcript and protein
Pabla, R., Rozario, D., & Siede, W. (2007) · Radiation and Environmental Biophysics · doi:10.1007/s00411-007-0132-1 · Cited by 19
“A recent study on global changes in yeast protein expression following MMS treatment [45] found many examples of proteins showing no signiWcant change in abundance ( 46 ].”
Background
PROSPECT improves cis-acting regulatory element prediction by integrating expression profile data with consensus pattern searches
Fujibuchi, W., Anderson, J. S. J., & Landsman, D. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.19.3988 · Cited by 19
“Furthermore, the selectivity ratios in searches for the ABF1 element plateau at a value of ∼2.0 at PEA levels ≤0.4.”
BackgroundInfluential
Genotype to phenotype: a technological challenge
Wilson, I. D., Barker, G., & Edwards, K. J. (2003) · Annals of Applied Biology · doi:10.1111/j.1744-7348.2003.tb00226.x · Cited by 19
Bayesian Estimation of Transcript Levels Using a General Model of Array Measurement Noise
Dror, R. O., Murnick, J. G., Rinaldi, N. J., Marinescu, V. D., Rifkin, R. M., & Young, R. A. (2003) · Journal of Computational Biology · doi:10.1089/10665270360688110 · Cited by 19
“…to simultaneously measure the expression levels of thousands of genes in a cell population, providing a potentially powerful tool in biology and medicine (Brown and Botstein, 1999; Holstege et al. , 1998; Hughes et al. , 2000; Jelinsky and Samson, 1999; Tanaka et al. , 2000; Wodicka et al. , 1997).”
The Protein Degradation Response of Saccharomyces cerevisiae to Classical DNA-Damaging Agents
Burgis, N. E., & Samson, L. D. (2007) · Chemical Research in Toxicology · doi:10.1021/tx700126e · Cited by 18
Self-citation
The DNA-damage signature in Saccharomyces cerevisiae is associated with single-strand breaks in DNA
Fry, R. C., DeMott, M. S., Cosgrove, J. P., Begley, T. J., Samson, L. D., & Dedon, P. C. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-313 · Cited by 18
“cerevisiae ~6000 genes respond upon exposure to MMS in a time-, agent- and dose-dependent manner [9,10].”
BackgroundMethodSelf-citation
Using Expression Information to Discover New Drug and Vaccine Targets in the Malaria Parasite Plasmodium Falciparum
Young, J. A., & Winzeler, E. A. (2005) · Pharmacogenomics · doi:10.1517/14622416.6.1.17 · Cited by 18
“In Saccharomyces cerevisae, DNA microarrays were used to assay genome-wide response to DNA-damaging agents [55].”
Method
Rpn4p is a positive and negative transcriptional regulator of the ubiquitin-proteasome system
Karpov, D. S., Osipov, S. A., Preobrazhenskaya, O. V., & Карпов, В. Л. (2008) · Molecular Biology · doi:10.1134/s0026893308030151 · Cited by 18
“According to our results, addition of MMS to the yeast growth medium increased the mRNA levels of the control gene (Fig.”
BackgroundInfluential
Proteomic analysis of cellular responses to low concentration N‐methyl‐N′‐nitro‐N‐nitrosoguanidine in human amnion FL cells
Jin, J., Yang, J. J., Gao, Z., & Yu, Y. (2004) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20001 · Cited by 18
“Although these methods can provide high-throughput information about differential gene expression [Amundson et al., 1999; Jelinsky and Samson, 1999], they cannot provide direct information of how proteins are regulated at the translational or posttranslational levels.”
Instability of Succinate Dehydrogenase in SDHD Polymorphism Connects Reactive Oxygen Species Production to Nuclear and Mitochondrial Genomic Mutations in Yeast
Chang, Y.-L., Hsieh, M., Chang, W., Wang, H., Lin, M., Wang, C., Lou, P., & Teng, S. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5966 · Cited by 17
“Since glucose-6-phosphate dehydrogenase is induced by MMS and Cd, we used Pgk1 as a loading control for these treatments (28, 69).”
Method
Transcriptional Networks in S. cerevisiae Linked to an Accumulation of Base Excision Repair Intermediates
Rusyn, I., Fry, R. C., Begley, T. J., Klapacz, J., Svensson, J. P., Ambrose, M., & Samson, L. D. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001252 · Cited by 17
“The expression patterns of the five yeast strains with modulated levels of BER were strikingly different from the expression patterns of yeast exposed to MMS (Fig.”
BackgroundInfluentialSelf-citation
Meta-Analysis of Published Transcriptional and Translational Fold Changes Reveals a Preferencefor Low-Fold Inductions
Wren, J. D., & Conway, T. (2006) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2006.10.15 · Cited by 17
“…such as cDNA libraries (Strausberg et al., 2000), Serial Analysis of Gene Expression (SAGE) (Velculescu et al., 1999), microarray hybridization (Jelinsky and Samson, 1999), and a combination of each (Kuznetsov et al., 2002), indicate that the distribution of gene expression and gene product…”
Genomics for Applied Microbiology
Nierman, W. C., & Nelson, K. E. (2002) · Advances in applied microbiology · doi:10.1016/s0065-2164(02)51007-8 · Cited by 17
ATM: Sounding the Double-strand Break AlarmPreprint
Shiloh, Y. (2000) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2000.65.527 · Cited by 17
The checkpoint transcriptional response: Make sure to turn it off once you are satisfied
Smolka, M. B., de Oliveira, F. M. B., Harris, M. R., & de Bruin, R. A. M. (2012) · Cell Cycle · doi:10.4161/cc.21197 · Cited by 14
“This became clear in the late 1990s with the use of high-throughput microarray technologies.(46) Genome-wide expression analysis in yeast has revealed that in response to replication stress induced by methyl methane sulphonate (MMS), ionizing radiation (IR), hydroxyurea (HU) and UV radiation, hundreds of genes are eit…”
Background
Proteome-wide remodeling of protein location and function by stress
Lee, K., Sung, M., Kim, J., Kim, K., Byun, J., Paik, H., Kim, B., Huh, W., & Ideker, T. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318881111 · Cited by 16
“Consistent with this notion, treatment of cells with MMS reduces the expression of proteins involved in the synthesis and assembly of ribosomes, including the DEAD box helicase Dbp3, the H/ACA box protein Nhp2, the late preribosomal RNA processing and particle assembly factors Nip7 and Nsr1 (nucleolin), and the C/D bo…”
Background
Profiles of gene expression changes in L5178Y mouse lymphoma cells treated with methyl methanesulfonate and sodium chloride
Seidel, S. D. (2004) · Mutagenesis · doi:10.1093/mutage/geh027 · Cited by 16
Secreted 3-Isopropylmalate Methyl Ester Signals Invasive Growth during Amino Acid Starvation in Saccharomyces cerevisiae
Dumlao, D. S., Hertz, N. T., & Clarke, S. G. (2007) · Biochemistry · doi:10.1021/bi7018157 · Cited by 16
“Interestingly, cells exposed to the DNA damaging agent methyl methanesulfonate results in a 24.5-fold induction of Tmt1 mRNA levels ( 32 ).”
BackgroundInfluential
Induction of Global Stress Response in Saccharomyces cerevisiae Cells Lacking Telomerase
Teng, S., Epstein, C. B., Tsai, Y.-L., Cheng, H.-W., Chen, H.-L., & Lin, J. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2002.6509 · Cited by 17
Cell Cycle Arrest Determines the Intensity of the Global Transcriptional Response ofSaccharomyces cerevisiaeto Ionizing Radiation
Sanctis, V. D., Bertozzi, C., Costanzo, G., Mauro, E. D., & Negri, R. (2001) · Radiation Research · doi:10.1667/0033-7587(2001)156[0379:ccadti]2.0.co;2 · Cited by 16
Quantification of N-(Deoxyguanosin-8-yl)-4-aminobiphenyl Adducts in Human Lymphoblastoid TK6 Cells Dosed with N-hydroxy-4-acetylaminobiphenyl and Their Relationship to Mutation, Toxicity, and Gene Expression Profiling
Ricicki, E. M., Luo, W., Fan, W., Zhao, L. P., Zarbl, H., & Vouros, P. (2006) · Analytical Chemistry · doi:10.1021/ac0607360 · Cited by 16
SVD Identifies Transcript Length Distribution Functions from DNA Microarray Data and Reveals Evolutionary Forces Globally Affecting GBM Metabolism
Bertagnolli, N. M., Drake, J. A., Tennessen, J. M., & Alter, O. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078913 · Cited by 15
“For example, using the SVD to identify the length distribution functions of the two mutually exclusive subsets of yeast transcripts that were detected as either overexpressed or underexpressed in response to the DNA damaging agent methyl methanesulfonate (MMS) [40], we find the equilibria of these subsets at the migra…”
MethodInfluential
7 Regulation of the yeast general amino acid control pathway in response to nutrient stress
Wek, R. C., Staschke, K. A., & Narasimhan, J. (2004) · Topics in current genetics · doi:10.1007/978-3-540-39898-1_8 · Cited by 15
“MMS induces DNA damage, and DNA microarray analysis indicates that this alkylating agent increases expression of genes involved in synthesis and repair of DNA and detoxification, and represses those functioning in the synthesis of nucleotides, RNA and ribosomes ( Jelinksy and Samson 1999 ).”
Background
Aspartate facilitates mitochondrial function, growth arrest and survival during doxorubicin exposure
Dornfeld, K. J., Madden, M., Skildum, A. J., & Wallace, K. B. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1087619 · Cited by 14
“cerevisiae examined transcriptional responses to a variety of adverse conditions, including DNA damaging agents.(15,16) Exposure to a wide variety of agents induced similar changes.”
Background
The amino-terminal tails of histones H2A and H3 coordinate efficient base excision repair, DNA damage signaling and postreplication repair in Saccharomyces cerevisiae
Meas, R., Smerdon, M. J., & Wyrick, J. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv372 · Cited by 15
“MAG1 is one of more than 300 genes that are induced after MMS exposure in budding yeast (53).”
Background
In UV‐irradiated Saccharomyces cerevisiae, overexpression of Swi2/Snf2 family member Rad26 increases transcription‐coupled repair and repair of the non‐transcribed strand
Bucheli, M. E., & Sweder, K. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04081.x · Cited by 14
The F-box protein, Ufo1, maintains genome stability by recruiting the yeast mating switch endonuclease, Ho, for rapid proteasome degradation.
Kaplun, L., Ivantsiv, Y., Bakhrat, A., Tzirkin, R., Baranes‐Bachar, K., Shabek, N., & Raveh, D. (2006) · PubMed · Cited by 14
Transcription Initiation of the Yeast IMD2 Gene Is Abolished in Response to Nutrient Limitation through a Sequence in Its Coding Region
Escobar‐Henriques, M., Collart, M. A., & Daignan‐Fornier, B. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.17.6279-6290.2003 · Cited by 14
“Indeed, challenging yeast cells with drugs impairing growth, such as the DNA-damaging agent methyl methanesulfonate or rapamycin, led to downregulation of the IMD2 mRNA (11, 13); sudden changes in temperature had a similar effect (9).”
Background

Authors: Jelinsky, S. A., & Samson, L. D.
Affiliations: Harvard University (US)
Corresponding author: Samson, Leona D.
ORCID: Jelinsky, Scott A.
Samson, Leona D.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 1999-02-16
Volume: 96
Issue: 4
Pages: 1486-1491
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.96.4.1486
PMC: PMC15489
OpenAlex: W2155675863
Cited by: 419
References: 36
Citations by year: 2026: 4 · 2025: 1 · 2024: 4 · 2023: 4 · 2022: 2 · 2021: 1 · 2020: 5 · 2019: 6 · 2018: 6 · 2017: 4 · 2016: 5 · 2015: 11 · 2014: 10 · 2013: 8 · 2012: 11
FWCI: 17.46
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5p01hg001323-03)
National Human Genome Research Institute (P01 HG 01323)
National Cancer Institute (CA-55042, CA09078, T32CA009078, R01CA055042)
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: Saccharomyces cerevisiae, methyl methanesulfonate, alkylating agents, DNA damage response, gene expression profiling, transcriptome, DNA repair genes
MeSH terms: Alkylating Agents, DNA Damage, Fungal Proteins, Genes, Fungal, Methyl Methanesulfonate, Saccharomyces cerevisiae, Transcription, Genetic, Open Reading Frames, Genome, Fungal

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Global response of Saccharomyces cerevisiae to an alkylating agent

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