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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Self-citation
Global protein expression profiling of budding yeast in response to DNA damage
Lee, M., Kim, B., Choi, H., Ryu, M., Kim, S., Kang, K. M., Cho, E., Youn, H., Huh, W., & Kim, S. (2007) · Yeast · doi:10.1002/yea.1446 · Cited by 55
“Transcriptional profiling studies (Birrell et al., 2002; Gasch et al., 2000, 2001; Hughes et al., 2000; Jelinsky et al., 2000; Jelinsky and Samson, 1999; Natarajan et al., 2001) and high-throughput phenotype analyses (Bennett et al., 2001; Birrell et al., 2002; Chang et al., 2002; Ross-Macdonald et…”
Influential
Drug‐induced alterations in gene expression of the asexual blood forms of Plasmodium falciparum
Gunasekera, A. M., Patankar, S., Schug, J., Eisen, G., & Wirth, D. F. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03787.x · Cited by 54
“For example, DNA chip methodology in Saccharomyces cerevisae demonstrated the modulation of over one-third of the yeast genome upon exposure to DNA-damaging agents (Jelinsky and Samson, 1999; Jelinsky et al ., 2000).”
BackgroundMethodResultInfluential
Proteasomes in the archaea from structure to function
Maupin-furlow, J. A. (2000) · Frontiers in bioscience · doi:10.2741/furlow · Cited by 54
“In addition, yeast genomic analysis using DNA chip technology reveals a 5 to 10 fold increase in mRNA transcripts of not only ubiquitin but also the Rpn1 (non-ATPase) and beta1 subunits of the 26S proteasome after exposure to a DNA-damaging agent (23).”
BackgroundMethod
Functions of the DNA damage response pathway target Ho endonuclease of yeast for degradation via the ubiquitin-26S proteasome system
Kaplun, L., Ivantsiv, Y., Kornitzer, D., & Raveh, D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.18.10077 · Cited by 53
Histone dosage regulates DNA damage sensitivity in a checkpoint-independent manner by the homologous recombination pathway
Liang, D., Burkhart, S. L., Singh, R. K., Kabbaj, M., & Gunjan, A. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks722 · Cited by 55
“Compared with the wild-type cells, the expression of 50 genes was significantly affected (expression changes of more than 2-fold) in the hht2-hhf2 deletion strain (Supplementary Figure S2 and Supplementary Table S1), none of which are known to be involved in the DDR (62).”
BackgroundInfluential
Role of Pex21p for Piggyback Import of Gpd1p and Pnc1p into Peroxisomes of Saccharomyces cerevisiae
Effelsberg, D., Cruz‐Zaragoza, L. D., Tonillo, J., Schliebs, W., & Erdmann, R. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.653451 · Cited by 52
“It also seems noteworthy that gene expression of Pex21p is up-regulated under DNA-damaging conditions (57).”
Background
FHA Domain-Mediated DNA Checkpoint Regulation of Rad53
Schwartz, M. F., Lee, S.-J., Duong, J., Eminaga, S., & Stern, D. F. (2003) · Cell Cycle · doi:10.4161/cc.2.4.457 · Cited by 52
Rad53 Checkpoint Kinase Phosphorylation Site Preference Identified in the Swi6 Protein of Saccharomyces cerevisiae
Sidorova, J. M., & Breeden, L. L. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.10.3405-3416.2003 · Cited by 51
The Yeast STM1 Gene Encodes a Purine Motif Triple Helical DNA-binding Protein
Nelson, L. D., Musso, M., & Dyke, M. W. V. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.8.5573 · Cited by 51
Budding Yeast CTDK-I Is Required for DNA Damage-Induced Transcription
Ostapenko, D., & Solomon, M. J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.2.274-283.2003 · Cited by 50
“For example, exposure of cells to genotoxic agents leads to induction of DNA repair and environmental stress response genes (12, 18).”
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Toxicology and Genetic Toxicology in the New Era of “Toxicogenomics”: Impact of “-omics” Technologies
Aardema, M. J., & MacGregor, J. T. (2003) · Springer eBooks · doi:10.1007/978-4-431-66999-9_22 · Cited by 49
A Network of Conserved Damage Survival Pathways Revealed by a Genomic RNAi Screen
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“Viability [14], gene transcription [15] and protein expression [16] were measured in these studies, all of which provided insights into the diverse nature of biological responses to alkylation damage.”
Background
SRC1: an intron‐containing yeast gene involved in sister chromatid segregation
Rodríguez‐Navarro, S., Igual, J. C., & Pérez-Ortín, J. E. (2001) · Yeast · doi:10.1002/yea.803 · Cited by 48
Candida albicans RFX2 Encodes a DNA Binding Protein Involved in DNA Damage Responses, Morphogenesis, and Virulence
Hao, B., Clancy, C. J., Cheng, S., Raman, S. B., Iczkowski, K. A., & Nguyen, M. H. (2009) · Eukaryotic Cell · doi:10.1128/ec.00246-08 · Cited by 47
PartsList: a web-based system for dynamically ranking protein folds based on disparate attributes, including whole-genome expression and interaction information
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“We report values for experiments from a number of different labs (41-44) and a single reference set that merges and scales all the expression sets together.”
Method
Transcriptional response to nitrosative stress in Saccharomyces cerevisiae
Horan, S., Bourges, I., & Meunier, B. (2006) · Yeast · doi:10.1002/yea.1372 · Cited by 49
The Impact of Genomics-Based Technologies on Drug Safety Evaluation
Waring, J. F., & Ulrich, R. G. (2000) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.40.1.335 · Cited by 47
Determination of genetic toxicity and potential carcinogenicity in vitro--challenges post the Seventh Amendment to the European Cosmetics Directive
Tweats, D. J., Scott, A. D., Westmoreland, C., & Carmichael, P. L. (2006) · Mutagenesis · doi:10.1093/mutage/gel052 · Cited by 45
“Exposure to the alkylating agent methylmethanesulphonate induced transcriptional changes in 20–30% of the yeast genome, only 8–10% of these belong to the stress category (30).”
Background
Transcriptional Response of Human Umbilical Vein Endothelial Cells to Low Doses of Ionizing Radiation
LANZA, V., Pretazzoli, V., Olivieri, G., Pascarella, G., Panconesi, A., & Negri, R. (2005) · Journal of Radiation Research · doi:10.1269/jrr.46.265 · Cited by 45
The “chip” as a specific genetic tool
Watson, S. J., Meng, F., Thompson, R. C., & Akil, H. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01080-5 · Cited by 45
“…models including yeast, T cells, tumor cell lines, and fibroblasts (Amundson et al 1999; DeRisi et al 1996; Heller et al 1997; Iyer et al 1999; Jelinsky and Samson 1999; Khan et al 1998, 1999; Lashkari et al 1997; Perou et al 1999; Schena et al 1995, 1996; Spellman et al 1998; Wang et al…”
Acetylation: A Novel Link between Double-Strand Break Repair and Autophagy
Shubassi, G., Robert, T., Vanoli, F., Minucci, S., & Foiani, M. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3172 · Cited by 44
“It is important to note that DNA-damaging agents also cause protein damage (21), which in turn may induce stress pathways such as autophagy as a survival mechanism to degrade damaged proteins or aggregates.”
Background
Gene transcription analysis of Saccharomyces cerevisiae exposed to neocarzinostatin protein– chromophore complex reveals evidence of DNA damage, a potential mechanism of resistance, and consequences of prolonged exposure
Schaus, S. E., Cavalieri, D., & Myers, A. G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191340698 · Cited by 43
The NIP7 protein is required for accurate pre-rRNA processing in human cells
Morello, L. G., Hesling, C., Coltri, P. P., Castilho, B. A., Rimokh, R., & Zanchin, N. I. T. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq758 · Cited by 44
“Saccharomyces cerevisiae NIP7 is part of the Ribi regulon (13,15) and its transcription levels were also shown to correlate with other Ribi regulon genes in response to stress caused by the alkylating agent methyl methanesulfonate (64).”
Background
A stable and sensitive genotoxic testing system based on DNA damage induced gene expression in Saccharomyces cerevisiae
Jia, X., Zhu, Y. B., & Xiao, W. (2002) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/s1383-5718(02)00129-8 · Cited by 42
Analyzing the dose-dependence of the Saccharomyces cerevisiae global transcriptional response to methyl methanesulfonate and ionizing radiation
Benton, M. G., Somasundaram, S., Glasner, J. D., & Palecek, S. P. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-305 · Cited by 43
“MMS induction of protein degradation has been observed in yeast and higher organisms [ 27 ,69] and may be related to the degradation of methylated proteins.”
BackgroundResultInfluential
Yeast Mutants As a Model System for Identification of Determinants of Chemosensitivity
Perego, P., Jimenez, G. S., Gatti, L., Howell, S. B., & Zunino, F. (2000) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01466-2 · Cited by 41
Genome-wide single-cell-level screen for protein abundance and localization changes in response to DNA damage in S. cerevisiae
Mazumder, A., Pesudo, L. Q., McRee, S. K., Bathe, M., & Samson, L. D. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt715 · Cited by 41
“In previous studies (20,21), no proteins met the cutoff set for downregulation, even though many genes are known to be transcriptionally repressed in response to MMS (6,7,9).”
BackgroundInfluentialSelf-citation
Genome-wide transcriptional responses to sulfite in Saccharomyces cerevisiae
Park, H., & Hwang, Y.-S. (2008) · The Journal of Microbiology · doi:10.1007/s12275-008-0053-y · Cited by 41
Relationship between G+C content, ORF‐length and mRNA concentration in Saccharomyces cerevisiae
Marín, A., Gallardo, M., Kato, Y., Shirahige, K., Gutiérrez, G., Ohta, K., & Aguilera, A. (2003) · Yeast · doi:10.1002/yea.992 · Cited by 41
“Hybridization intensities were calculated by GENECHIP software from the fluorescence intensities of the probes of each gene, as described previously (Jelinsky and Samson, 1999).”
Method
Cross-Talk between Carbon Metabolism and the DNA Damage Response in S. cerevisiae
Simpson-Lavy, K. J., Bronstein, A. M., Kupiec, M., & Johnston, M. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.025 · Cited by 42
“…genes involved in respiration and increased expression of genes involved in fermentation (Caba et al., 2005, Fry et al., 2003, Gasch et al., 2001, Jelinsky and Samson, 1999, Lee et al., 2000, Shalem et al., 2008), and one of the effects of DNA damage in yeast is the reduction of respiration…”
Influential
Limitations of codon adaptation index and other coding DNA‐based features for prediction of protein expression in Saccharomyces cerevisiae
Friberg, M. T., von Rohr, P., & Gonnet, G. H. (2004) · Yeast · doi:10.1002/yea.1150 · Cited by 40
“(1998), Jelinsky and Samson (1999) and Velculescu et al .”
Background
Effect of Power-Frequency Magnetic Fields on Genome-Scale Gene Expression in Saccharomyces cerevisiae
Nakasono, S., Laramee, C. B., Saiki, H., & McLeod, K. J. (2003) · Radiation Research · doi:10.1667/rr3006 · Cited by 40
“Genome-scale screening methods such as 2D PAGE and cDNA microarray analyses are powerful methods for identifying global responses to various environmental perturbations, such as heat shock (18), different carbon sources (19, 20), UV radiation (21), mutagens (22), osmotic shock, radicals (20) and EMFs (18).”
Distribution Associated with Stochastic Processes of Gene Expression in a Single Eukaryotic Cell
Kuznetsov, V. A. (2001) · EURASIP Journal on Advances in Signal Processing · doi:10.1155/s1110865701000294 · Cited by 40
“Such statistical knowledge bears upon the fundamental biological problems of cell regulation, adaptation, and development.”
Background
Acute cyclophosphamide exposure has germ cell specific effects on the expression of stress response genes during rat spermatogenesis
Aguilar‐Mahecha, A., Hales, B. F., & Robaire, B. (2001) · Molecular Reproduction and Development · doi:10.1002/mrd.1092 · Cited by 39
Global effects of DNA replication and DNA replication origin activity on eukaryotic gene expression
Omberg, L., Meyerson, J. R., Kobayashi, K., Drury, L. S., Diffley, J. F. X., & Alter, O. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.70 · Cited by 39
“either the Cdc6 or Cdc45 conditions as previously described (Piatti et al, 1995; Tercero et al, 2000), and because we did not observe any significant enrichment in DNA damage-induced genes (Jelinsky and Samson, 1999) in the fourth through seventh combinations of expression patterns, in which the corresponding P-values…”
BackgroundInfluential
Transcriptional Response of Yeast to Aflatoxin B1: Recombinational Repair InvolvingRAD51andRAD1
Seitz, M. U. K., Certa, U., Sengstag, C., Würgler, F. E., Sun, M., & Fasullo, M. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-05-0375 · Cited by 38
“Five stress response genes, DDR48, PAI3, YML131W, YKL100C, and YNL116W, that are upregulated after MMS exposure (Jelinsky and Samson, 1999) and saline stress conditions (Posas et al.”
BackgroundMethodInfluential
Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
Gabunilas, J., & Chanfreau, G. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005999 · Cited by 38
“Earlier experiments have also shown that the transcript levels of many RPGs are repressed by exposure to methane methyl-sulfonate (MMS) [1], an alkylating agent that is thought to stall DNA replication fork movement.”
Background
Toxicogenomics using yeast DNA microarrays
Yasokawa, D., & Iwahashi, H. (2010) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2010.06.003 · Cited by 38

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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