Yeast toxicogenomics: Genome-wide responses to chemical stresses with impact in environmental health, pharmacology, and biotechnology

Frontiers in Genetics

Volumn 3, Issue APR, 2012, Pages

  dos Santos, Sandra C ^a   Teixeira, Miguel Cacho ^a   Cabrito, Tânia R ^a   Sá Correia, Isabel ^a  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

Genome wide approaches; Molecular systems biology; Predictive toxicology; Response to stress; Toxicity mechanisms; Toxicogenomics; Yeast model

Indexed keywords

ANIMALIA; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84865480260     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00063     Document Type: Review

References (176)

1. Abbott, D. A., Zelle, R. M., Pronk, J. T., and Van Maris, A. J. (2009). Metabolic engineering of Saccha-romyces cerevisiae for production of carboxylic acids: current status and challenges. FEMS Yeast Res. 9, 1123-113
2. Abdulrehman, D., Monteiro, P. T., Teixeira, M. C., Mira, N. P., Lourenco, A. B., dos Santos, S. C., Cabrito, T. R., Francisco, A. P., Madeira, S. C., Aires, R. S., Oliveira, A. L., Sa-Correia, I., and Freitas, A. T. (2011). YEASTRACT: providing a programmatic access to curated transcriptional regulatory associations in Saccharomyces cerevisiae through a web services interface. Nucleic Acids Res. 39,D136-D14
3. Alenquer, M., Tenreiro, S., and Sá-Correia,I. (2006). Adaptive response to the antimalarial drug artesunate in yeast involves Pdr1p/Pdr3p-mediated transcriptional activation of the resistance determinants TPO1 and PDR5. FEMS Yeast Res. 6, 1130-113
4. Alexandre, H., Ansanay-Galeote, V., Dequin, S., and Blondin, B. (2001). Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Lett. 498, 98-10
5. Alkadi, H. O. (2007). Antimalarial drug toxicity: a review. Chemotherapy 53, 385-39
6. Aouida, M., Pagé, N., Leduc, A., Peter, M., and Ramotar, D. (2004). A genome-wide screen in Sac-charomyces cerevisiae reveals altered transport as a mechanism of resistance to the anticancer drug bleomycin. Cancer Res. 64, 1102-110
7. Auerbach, D., Arnoldo, A., Bogdan, B., and Fetchko, M. (2005). Drug discovery using yeast as a model system: a functional genomic and proteomic view. Curr. Proteomics 2, 1-1
8. Bach, S., Talarek, N., Andrieu, T., Vierfond, J. M., Mettey, Y., Galons, H., Dormont, D., Meijer, L., Cullin, C., and Blondel, M. (2003). Isolation of drugs active against mammalian prions using a yeast-based screening assay. Nat. Biotechnol. 21, 1075-108
9. Ballantyne, B. (2004). "Toxicology in fungicides," in Pesticide Toxicology and International Regulation, eds T. C. Marrs and B. Ballantyne (Chichester: John Wiley and Sons), 191- 30
10. Batova, M., Klobucnikova, V., Oblasova, Z., Gregan, J., Zahradnik, P., Hapala, I., Subik, J., and Schuller, C. (2010). Chemogenomic and transcriptome analysis identifies mode of action of the chemosensitizing agent CTBT(7-chlorotetrazolo[5,1-c]benzo[1,2,4]triazine). BMC Genomics 11, 15 doi:10.1186/1471-2164-11-153
11. Belpoggi, F., Soffritti, M., Guarino, M., Lambertini, L., Cevolani, D., and Maltoni, C. (2002). Results of long-term experimental studies on the carcinogenicity of ethylene-bis-dithiocarbamate (Mancozeb) in rats. Ann. N. Y Acad. Sci. 982, 123-13
12. Berkowitz, O., Jost, R., Pollmann, S., and Masle, J. (2008). Characterization of TCTP, the translationally controlled tumor protein, from Arabidopsis thaliana. Plant Cell 20, 3430-344
13. Bivi, N., Romanello, M., Harrison, R., Clarke, I., Hoyle, D. C., Moro, L., Ortolani, F., Bonetti, A., Quadri-foglio, F., Tell, G., and Delneri, D. (2009). Identification of secondary targets of N-containingbisphospho-nates in mammalian cells via parallel competition analysis of thebarcoded yeast deletion collection. Genome Biol. 10,R9
14. Blackburn,A. S.,andAvery,S.V. (2003). Genome-wide screening of Saccha-romyces cerevisiae to identify genes required for antibiotic insusceptibility of eukaryotes. Antimicrob. Agents Chemother. 47,676-68
15. Bleackley, M. R., Young, B. P., Loewen, C. J., and Macgillivray, R. T. (2011). High density array screeningto identify the genetic requirements for transition metal tolerance in Sac-charomyces cerevisiae. Metallomics 3, 195-20
16. Botstein, D., and Fink, G. R. (2011). Yeast: an experimental organism for 21st century biology. Genetics 189, 695-70
17. Bradberry, S. M., Proudfoot, A. T., and Vale, J. A. (2004). Poisoning due to chlorophenoxy herbicides. Toxicol. Rev. 23, 65-7
18. Bradberry, S. M., Watt, B. E., Proudfoot, A. T., and Vale, J. A. (2000). Mechanisms of toxicity, clinical features, and management of acute chlorophenoxy herbicide poisoning: a review. J. Toxicol. Clin. Toxicol. 38, 111-12
19. Cabrito, T. R., Teixeira, M. C., Duarte, A. A., Duque, P., and Sa-Correia, I. (2009). Heterologous expression of a Tpo1 homolog from Arabidopsis thaliana confers resistance to the herbicide 2,4-D and other chemical stresses in yeast. Appl. Microbiol. Biotechnol. 84, 927-93
20. Cabrito, T. R., Teixeira, M. C., Singh, A., Prasad, R., and Sa-Correia, I. (2011). The yeast ABC transporter Pdr18 (ORF YNR070w) controls plasma membrane sterol composition, playing a role in multidrug resistance. Biochem. J. 440,195-20
21. Calviello, G., Piccioni, E., Boninsegna, A., Tedesco, B., Maggiano, N., Serini, S., Wolf, F. I., and Palozza, P. (2006). DNA damage and apoptosis induction by the pesticide Mancozeb in rat cells: involvement of the oxidative mechanism. Toxicol. Appl. Pharmacol. 211,87-9
22. Chang, D. J., Lee, S. H., Lim, C. S., Jang, D. H., Lee, C. H., Lee, Y. D., and Kaang, B. K. (2004). Thiol oxidation-mediated cell death in Aplysia cultured sensory neurons. Brain Res. 1007, 71-7
23. Chen, B.-J., Causton, H. C., Mancenido, D., Goddard, N. L., Perlstein, E. O., and Pe'er, D. (2010). Harnessing gene expression to identify the genetic basis of drug resistance. Mol. Syst. Biol. 5, 1-1
24. Chen, Y., Feldman, D. E., Deng, C., Brown, J. A., De Giacomo, A. F., Gaw, A. F., Shi, G., Le, Q. T., Brown, J. M., and Koong, A. C. (2005). Identification of mitogen-activated protein kinase signaling pathways that confer resistance to endoplasmic reticulum stress in Saccharomyces cerevisiae. Mol. Cancer Res. 3, 669-67
25. Chondrogianni, N., Tzavelas, C., Pemberton, A. J., Nezis, I. P., Rivett, A. J., and Gonos, E. S. (2005). Overexpression of proteasome beta5 assembled subunit increases the amount of proteasome and confers ameliorated response to oxidative stress and higher survival rates. J. Biol. Chem. 280,11840-1185
26. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., Ding, H., Koh, J. L., Toufighi, K., Mostafavi, S., Prinz, J., St Onge, R. P., Vandersluis, B., Makhnevych, T., Vizeacoumar, F. J., Alizadeh, S., Bahr, S., Brost, R. L., Chen, Y., Cokol, M., Deshpande, R., Li, Z., Lin, Z. Y., Liang, W., Marback, M., Paw, J., San Luis, B. J., Shuteriqi, E., Tong, A. H., Van Dyk, N., Wallace, I. M., Whitney, J. A., Weirauch, M. T., Zhong, G., Zhu, H., Houry, W. A., Brudno, M., Ragibizadeh, S., Papp, B., Pal, C., Roth, F. P., Giaever, G., Nislow, C., Troyanskaya, O. G., Bussey, H., Bader, G. D., Gingras, A. C., Morris, Q. D., Kim, P. M., Kaiser, C. A., Myers, C. L., Andrews, B. J., and Boone, C. (2010). The genetic landscape of a cell. Science 327,425-43
27. Crespo, J. L., and Hall, M. N. (2002). Elucidating TOR signaling and rapamycin action: lessons from Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 66,579-59
28. Cumming, R. C., Dargusch, R., Fischer, W.H., and Schubert, D. (2007). Increase in expression levels and resistance to sulfhydryl oxidation of peroxiredoxin isoforms in amyloid beta-resistant nerve cells. J. Biol. Chem. 282, 30523-3053
29. Delling, U., Raymond, M., and Schurr, E. (1998). Identification of Saccharomyces cerevisiae genes conferring resistance to quinoline ring-containing antimalarial drugs. Antimicrob. Agents Chemother. 42, 1034-104
30. Devantier, R., Scheithauer, B., Villas-Boas, S. G., Pedersen, S., and Olsson, L. (2005). Metabolite profiling for analysis of yeast stress response during very high gravity ethanol fermentations. Biotechnol. Bioeng. 90, 703-71
31. Dias, P. J., Teixeira, M. C., Telo, J. P., and Sá-Correia, I. (2010). Insights into the mechanisms of toxicity and tolerance to the agricultural fungicide mancozeb in yeast, as suggested by a chemogenomic approach. OMICS 14,211-22
32. Ding, M. Z., Cheng, J. S., Xiao, W H., Qiao, B., and Yuan, Y. J. (2009). Comparative metabolomic analysis on industrial continuous and batch ethanol fermentation processes by GC-TOF-MS. Metabolomics 5, 229-23
33. Domico, L. M., Cooper, K. R., Bernard, L. P., and Zeevalk, G. D. (2007). Reactive oxygen species generation by the ethylene-bis-dithiocarbamate (EBDC) fungicide mancozeb and its contribution to neuronal toxicity in mesencephalic cells. Neurotoxicology 28, 1079-109
34. Doostzadeh, J., Davis, R. W., Giaever, G. N., Nislow, C., and Langston, J. W. (2007). Chemical genomic profiling for identifying intracellular targets of toxicants producing Parkinson's disease. Toxicol. Sci. 95, 182-18
35. + -ATPase function is an important target of this anticancer drug. OMICS 13, 185-19
36. dos Santos, S. C., and Sá-Correia, I. (2011). A genome-wide screen identifies yeast genes required for protection against or enhanced cytotoxicity of the antimalarial drug quinine. Mol. Genet. Genomics 286, 333-34
37. dos Santos, S. C., Tenreiro, S., Palma, M., Becker, J., and Sa-Correia, I. (2009). Transcriptomic profiling of the Saccharomyces cerevisiae response to quinine reveals a glucose limitation response attributable to drug-induced inhibition of glucose uptake. Antimicrob. Agents Chemother. 53, 5213-522
38. Emerson, L. R., Nau, M. E., Martin, R. K., Kyle, D. E., Vahey, M., and Wirth, D. F. (2002). Relationship between chloroquine toxicity and iron acquisition in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 46, 787-79
39. Endo, A., Nakamura, T., Ando, A., Tokuyasu, K., and Shima, J. (2008). Genome-wide screening of the genes required for tolerance to vanillin, which is a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. Biotechnol. Biofuels 1
40. Erasmus, D. J., Van Der Merwe, G. K., and Van Vuuren, H. J. (2003). Genome-wide expression analyses: metabolic adaptation of Saccharomyces cerevisiae to high sugar stress. FEMS Yeast Res. 3, 375-39
41. Ericson, E., Gebbia, M., Heisler, L. E., Wildenhain, J., Tyers, M., Giaever, G., and Nislow, C. (2008). Off-target effects of psychoactive drugs revealed by genome-wide assays in yeast. PLoS Genet. 4, e1000151. doi:10.1371/journal.pgen.1000151
42. Felder, T., Bogengruber, E., Tenreiro, S., Ellinger, A., Sá-Correia, I., and Briza, P. (2002). Dtrlp, a multidrug resistance transporter of the major facilitator superfamily, plays an essential role in spore wall maturation in Saccharomyces cerevisiae. Eukaryotic Cell 1,799-81
43. +-ATPase in Saccharomyces cerevisiae adaptation and resistance to the herbicide 2,4-dichlorophenoxyacetic acid. Biochem. Biophys. Res. Commun. 312,1317-132
44. Ferrari, G., Pastorelli, R., Buchi, F., Spinelli, E., Gozzini, A., Bosi, A., and Santini, V (2007). Comparative proteomic analysis of chronic myelogenous leukemia cells: inside the mechanism of imatinib resistance. J. Proteome Res. 6, 367-37
45. Fitch, C. D. (2004). Ferriprotopor-phyrin IX, phospholipids, and the antimalarial actions of quinoline drugs. LifeSci. 74, 1957-197
46. Foury, F. (1997). Human genetic diseases: a cross-talk between man and yeast. Gene 195,1-1
47. Fujita, K., Matsuyama, A., Kobayashi, Y., and Iwahashi, H. (2006). The genome-wide screening of yeast deletion mutants to identify the genes required for tolerance to ethanol and other alcohols. FEMS Yeast Res. 6,744-75
48. Gad, S. C. (1990). Recent developments in replacing, reducing, and refining animal use in toxicologic research and testing. Fundam. Appl. Toxicol. 15,8-1
49. Gammie, A. E., Erdeniz, N., Beaver, J., Devlin, B., Nanji, A., and Rose, M. D. (2007). Functional characterization of pathogenic human MSH2 missense mutations in Saccharomyces cerevisiae. Genetics 177, 707-72
50. Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Veronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., Andre, B., Ar kin, A. P., Astromoff, A., El-Bakkoury, M., Bangham, R., Benito, R., Brachat, S., Campanaro, S., Curtiss, M., Davis, K., Deutschbauer, A., Entian, K. D., Flaherty, P., Foury, F., Garfinkel, D. J., Gerstein, M., Gotte, D., Guldener, U., Hegemann, J. H., Hempel, S., Herman, Z., Jaramillo, D. F., Kelly, D. E., Kelly, S. L., Kotter, P., Labonte, D., Lamb, D. C., Lan, N., Liang, H., Liao, H., Liu, L., Luo, C., Lussier, M., Mao, R., Menard, P., Ooi, S. L., Revuelta, J. L., Roberts, C. J., Rose, M., Ross-Macdonald, P., Scherens, B., Schimmack, G., Shafer, B., Shoemaker, D. D., Sookhai-Mahadeo, S., Storms, R. K., Strathern, J. N., Valle, G., Voet, M.,Volckaert, G.,Wang, C. Y.,Ward, T. R., Wilhelmy, J., Winzeler, E. A., Yang, Y., Yen, G., Youngman, E., Yu, K., Bussey, H., Boeke, J. D., Snyder, M., Philippsen, P., Davis, R. W., and Johnston, M. (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418,387-39
51. Giaever, G., Flaherty, P., Kumm, J., Proctor, M., Nislow, C., Jaramillo, D. F., Chu, A. M., Jordan, M. I., Arkin, A. P., and Davis, R. W. (2004). Chemogenomic profiling: identifying the functional interactions of small molecules in yeast. Proc. Natl. Acad. Sci. U.S.A. 101, 793-79
52. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J. D., Jacq, C., Johnston, M., Louis, E. J., Mewes, H. W., Murakami, Y., Philippsen, P., Tettelin, H., and Oliver, S. G. (1996). Life with 6000 genes. Science 274, 546, 563-54
53. Gomase, V S., and Tagore, S. (2008). Toxicogenomics. Curr. Drug Metab. 9, 250-25
54. Gorsich, S. W., Dien, B. S., Nichols, N. N., Slininger, P. J., Liu, Z. L., and Skory, C. D. (2006). Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl. Microbiol Biotechnol. 71, 339-34
55. Guerreiro, N., Staedtler, F., Grenet, O., Kehren, J., and Chibout, S. D. (2003). Toxicogenomics in drug development. Toxicol. Pathol. 31, 471-47
56. Hamadeh, H. K., Amin, R. P., Paules, R. S., and Afshari, C. A. (2002). An overview of toxicogenomics. Curr. Issues Mol. Biol. 4, 45-5
57. Hammonds, T. R., Maxwell, A., and Jenkins, J. R. (1998). Use of a rapid throughput in vivo screen to investigate inhibitors of eukaryotic topoi-somerase II enzymes. Antimicrob. Agents Chemother. 42, 889-89
58. Hasunuma, T., Sanda, T., Yamada, R., Yoshimura, K., Ishii, J., and Kondo, A. (2011). Metabolic pathway engineering based on metabolomics confers acetic and formic acid tolerance to a recombinant xylose-fermenting strain of Saccharomyces cerevisiae. Microb. Cell Fact. 10
59. Heinicke, S., Livstone, M. S., Lu, C., Oughtred, R., Kang, F., Angiuoli, S. V., White, O., Botstein, D., and Dolinski, K. (2007). The Princeton protein orthology database (P-POD): a comparative genomics analysis tool for biologists. PLoS ONE 2, e766. doi:10.1371/journal.pone.0000766
60. Hellauer, K., Lesage, G., Sdicu, A.-M., and Turcotte, B. (2005). Largescale analysis of genes that alter sensitivity to the anticancer drug tirapazamine in Saccharomyces cerevisiae. Mol. Pharmacol. 68, 1365-137
61. Hillenmeyer, M. E., Fung, E., Wildenhain, J., Pierce, S. E., Hoon, S., Lee, W., Proctor, M., St Onge, R. P., Tyers, M., Koller, D., Altman, R. B., Davis, R. W., Nislow, C., and Giaever, G. (2008). The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320, 362-36
62. Hirasawa, T., Yoshikawa, K., Nakakura, Y., Nagahisa, K., Furusawa, C., Katakura, Y., Shimizu, H., and Shioya, S. (2007). Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J. Biotechnol. 131, 34-4
63. Hohmann,S., andMager,W. H. (1997). "Stress response mechanisms in the yeast Saccharomyces cerevisiae," in Yeast Stress Responses, eds S. Hohmann and W. H. Mager (Austin, TX: Molecular Biology Intelligence Unit, R.G. Landes Company), 1-5
64. Holland, S., Lodwig, E., Sideri, T., Reader, T., Clarke, I., Gkargkas, K., Hoyle, D. C., Delneri, D., Oliver, S. G., and Avery, S. V (2007). Application of the comprehensive set of heterozygous yeast deletion mutants to elucidate the molecular basis of cellular chromium toxicity. Genome Biol. 8, R26
65. Hoon, S., Smith, A. M., Wallace, I. M., Suresh, S., Miranda, M., Fung, E., Proctor, M., Shokat, K. M., Zhang, C., Davis, R. W., Giaever, G., St Onge, R. P., and Nislow, C. (2008a). An integrated platform of genomic assays reveals small-molecule bioactivities. Nat. Chem. Biol. 4,498-50
66. Hoon, S., St Onge, R. P., Giaever, G., and Nislow, C. (2008b). Yeast chemical genomics and drug discovery: an update. Trends Pharmacol. Sci. 29, 499-50
67. Huang, R.-Y., Eddy, M., Vujcic, M., and Kowalski, D. (2005). Genomewide screen identifies genes whose inactivation confer resistance to cisplatin in Saccharomyces cerevisiae. Cancer Res. 65, 5890-589
68. Hughes, T. R., Marton, M. J., Jones, A. R., Roberts, C. J., Stoughton, R., Armour, C. D., Bennett, H. A., Coffey, E., Dai, H., He, Y. D., Kidd, M. J., King, A. M., Meyer, M. R., Slade, D., Lum, P. Y., Stepaniants, S. B., Shoemaker, D. D., Gachotte, D., Chakraburtty, K., Simon, J., Bard, M., and Friend, S. H. (2000). Functional discovery via a compendium of expression profiles. Cell 102, 109-12
69. Ibrahim, M. A., Bond, G. G., Burke, T. A., Cole, P., Dost, F. N., Enter-line, P. E., Gough, M., Greenberg, R. S., Halperin, W. E., Mcconnell, E., Munro, I. C., Swenberg, J. A., Zahm, S. H., and Graham, J. D. (1991). Weight of the evidence on the human carcinogenicity of 2,4-D. Environ. Health Perspect. 96, 213-22
70. Ihara, Y., Nobukuni, K., Takata, H., and Hayabara, T. (2005). Oxidative stress and metal content in blood and cere-brospinal fluid of amyotrophic lateral sclerosis patients with and without a Cu, Zn-superoxide dismutase mutation. Neurol Res. 27,105-10
71. Ito, H., and Gray, W M. (2006). A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol. 142, 63-7
72. Jia, M. H., Larossa, R. A., Lee, J. M., Rafalski, A., Derose, E., Gonye, G., and Xue, Z. (2000). Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron methyl. Physiol. Genomics 3, 83-9
73. Jin, Y H., Dunlap, P. E., Mcbride, S. J., Al-Refai, H., Bushel, P. R., and Freedman, J. H. (2008). Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet. 4, e1000053. doi:10.1371/journal.pgen.1000053
74. Khozoie, C., Pleass, R. J.,and Avery, S. V. (2009). The antimalarial drug quinine disrupts Tat2p-mediated tryptophan transport and causes tryptophan starvation. J. Biol. Chem. 284, 17968-1797
75. Kitagawa, E., Momose, Y., and Iwahashi, H. (2003). Correlation of the structures of agricultural fungicides to gene expression in Saccharomyces cerevisiae upon exposure to toxic doses. Environ. Sci. Technol. 37, 2788-279
76. Kominsky, D. J., Klawitter, J., Brown, J. L., Boros, L. G., Melo, J. V., Eckhardt, S. G., and Serkova, N. J. (2009). Abnormalities in glucose uptake and metabolism in imatinib-resistant human BCR-ABL-positive cells. Clin. Cancer Res. 15,3442-345
77. Lamb, J., Crawford, E. D., Peck, D., Modell, J. W., Blat, I. C., Wrobel, M. J., Lerner, J., Brunet, J. P., Subramanian, A., Ross, K. N., Reich, M., Hieronymus, H., Wei, G., Armstrong, S. A., Haggarty, S. J., Clemons, P. A., Wei, R., Carr, S. A., Lander, E. S., and Golub, T. R. (2006). The connectivity map: using gene-expression signatures to connect small molecules, genes, and disease. Science 313, 1929-193
78. Landstetter, N., Glaser, W., Gregori, C., Seipelt, J., and Kuchler, K. (2010). Functional genomics of drug-induced ion homeostasis identifies a novel regulatory crosstalk of iron and zinc regulons in yeast. OMICS 14,651-66
79. Li, B. Z., Cheng, J. S., Qiao, B., and Yuan, Y. J. (2010). Genome-wide transcriptional analysis of Saccharomyces cerevisiae during industrial bioethanol fermentation. J. Ind. Microbiol Biotechnol. 37, 43-5
80. Li, W., Mo, W., Shen, D., Sun, L., Wang, J., Lu, S., Gitschier, J. M., and Zhou, B. (2005). Yeast model uncovers dual roles of mitochondria in action of artemisinin. PLoS Genet. 1, e36. doi:10.1371/journal.pgen.0010036
81. +- ATPase and cytosolic acidification in sensitivity to DNA-damaging agents such as cisplatin. Mol Pharmacol. 71, 416-42
82. Lourenço, A. B., Ascenso, J. R., and Sá-Correia, I. (2011). Metabolic insights into the yeast response to propionic acid based on high resolution 1H NMRspectroscopy. Metabolomics 7, 457-46
83. Lucau-Danila, A., Lelandais, G., Kozovska, Z., Tanty, V., Delaveau, T., Devaux, F., and Jacq, C. (2005). Early expression of yeast genes affected by chemical stress. Mol. Cell. Biol. 25, 1860-186
84. Lum, P. Y., Armour, C. D., Stepaniants, S. B., Cavet, G., Wolf, M. K., Butler, J. S., Hinshaw, J. C., Garnier, P., Prestwich, G. D., Leonardson, A., Garrett-Engele, P., Rush, C. M., Bard, M., Schimmack, G., Phillips, J. W., Roberts, C. J., and Shoemaker, D. D. (2004). Discovering modes of action for therapeutic compounds using a genome-wide screen of yeast heterozygotes. Cell 116, 121-13
85. Mager, W.H.,and Winderickx, J. (2005). Yeast as a model for medical and medicinal research. Trends Pharmacol. Sci. 26, 265-27
86. Marjanovic, J., Chalupska, D., Patenode, C., Coster, A., Arnold, E., Ye, A., Anesi, G., Lu, Y., Okun, I., Tkachenko, S., Haselkorn, R., and Gornicki, P. (2010). Recombinant yeast screen for new inhibitors of human acetyl-CoA carboxylase 2 identifies potential drugs to treat obesity. Proc. Natl. Acad. Sci. U.S.A. 107, 9093-909
87. Markovich, S., Yekutiel, A., Shalit, I., Shadkchan, Y., and Osherov, N. (2004). Genomic approach to identification of mutations affecting caspofungin susceptibility in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 48, 3871-387
88. Marks, V. D., Ho Sui, S. J., Erasmus, D., Van Der Merwe, G. K., Brumm, J., Wasserman, W. W., Bryan, J., and Van Vuuren, H. J. (2008). Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res. 8, 35-5
89. Maroni, M., Colosio, C., Ferioli, A., and Fait, A. (2000). Biological monitoring of pesticide exposure: a review. Toxicology 143,1-11
90. Martin, D., Brun, C., Remy, E., Mouren, P., Thieffry, D., and Jacq, B. (2004). GOToolBox: functional analysis of gene datasets based on Gene Ontology. Genome Biol. 5, R10
91. Marton, M. J., Derisi, J. L., Bennett, H. A., Iyer, V R., Meyer, M. R., Roberts, C. J., Stoughton, R., Burchard, J., Slade, D., Dai, H., Bassett, D. E. Jr., Hartwell, L. H., Brown, P. O., and Friend, S. H. (1998). Drug target validation and identification of secondary drug target effects usingDNA microarrays. Nat. Med. 4, 1293-130
92. Menacho-Marquez, M., and Murguia, J. R. (2007). Yeast on drugs: Saccharomyces cerevisiae as a tool for anti-cancer drug research. Clin. Transl. Oncol. 9,221-22
93. Mettetal, J. T., Muzzey, D., Gomez-Uribe, C., and Van Oudenaarden, A. (2008). The frequency dependence of osmo-adaptation in Saccharomyces cerevisiae. Science 319, 482-48
94. Mira, N. P., Becker, J. D., and Sa-Correia, I. (2010a). Genomic expression program involving the Haa1p-regulon in Saccharomyces cerevisiae response to acetic acid. OMICS 14, 587-60
95. Mira, N. P., Palma, M., Guerreiro, J. F., and Sa-Correia, I. (2010b). Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microb. Cell Fact. 9,7
96. Mira, N. P., Lourenço, A. B., Fernandes, A. R., Becker, J. D., and Sá-Correia, I. (2009). The RIM101 pathway has a role in Saccharomyces cerevisiae adaptive response and resistance to propionic acid and other weak acids. FEMS Yeast Res. 9,202-21
97. Miyamoto, M., Furuichi, Y., and Komiyama, T. (2011). Genome-wide screen of Saccharomyces cerevisiae for killer toxin HM-1 resistance. Yeast 28, 27-4
98. Mollapour, M., Fong, D., Balakrishnan, K., Harris, N., Thompson, S., Schuller, C., Kuchler, K., and Piper, P. W (2004). Screening the yeast deletant mutant collection for hyper-sensitivity and hyper-resistance to sorbate, a weak organic acid food preservative. Yeast 21, 927-94
99. Momose, Y., and Iwahashi, H. (2001). Bioassay of cadmium using a DNA microarray: genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium. Environ. Toxicol. Chem. 20, 2353-236
100. Monteiro, P. T., Dias, P. J., Ropers, D., Oliveira, A. L., Sá-Correia, I., Teixeira, M. C., and Freitas, A. T. (2011). Qualitative modeling and formal verification of the FLR1 gen mancozeb response in Saccharomyces cerevisiae. IET Syst. Biol. 5, 308-31
101. Morton, C. O., dos Santos, S. C., and Coote, P. (2007). An amphibian-derived, cationic, alpha-helical antimicrobial peptide kills yeast by caspase-independent but AIF-dependent programmed cell death. Mol. Microbiol. 65, 494-50
102. Murakami, T., Shibuya, I., Ise, T., Chen, Z. S., Akiyama, S., Nakagawa, M., Izumi, H., Nakamura, T., Matsuo, K., Yamada, Y., and Kohno, K. (2001). Elevated expression of vacuolar proton pump genes and cellular PH in cisplatin resistance. Int. J. Cancer 93, 869-87
103. Nicholson, J. K., Connelly, J., Lindon, J. C., and Holmes, E. (2002). Metabonomics: a platform for studying drug toxicity and gene function. Nat. Rev. DrugDiscov. 1,153-16
104. North, M., and Vulpe, C. D. (2010). Functional toxicogenomics: mechanism-centered toxicology. Int. I Mol. Sci. 11, 4796-481
105. Nowicki, M. O., Pawlowski, P., Fischer, T., Hess, G., Pawlowski, T., and Skorski, T. (2003). Chronic myelogenous leukemia molecular signature. Oncogene 22, 3952-396
106. Nunes, P. A., Tenreiro, S., and Sá-Correia, I. (2001). Resistance and adaptation to quinidine in Saccharomyces cerevisiae: role of QDR1 (YIL120w), encoding a plasma membrane transporter of the major facilitator superfamily required for multidrug resistance. Antimicrob. Agents Chemother. 45,1528-153
107. Outeiro, T. F., and Lindquist, S. (2003). Yeast cells provide insight into alpha -synuclein biology and pathobiology. Science 302,1772-177
108. Papaefthimiou, C., Cabral Mde, G., Mixailidou, C., Viegas, C. A., Sá-Correia, I., and Theophilidis, G. (2004). Comparison of two screening bioassays, based on the frog sciatic nerve and yeast cells, for the assessment of herbicide toxicity. Environ. Toxicol. Chem. 23, 1211-121
109. Parsons, A. B., Brost, R. L., Ding, H., Li, Z., Zhang, C., Sheikh, B., Brown, G. W., Kane, P. M., Hughes, T. R., andBoone, C. (2004). Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 22, 62-6
110. Parsons, A. B., Geyer, R., Hughes, T. R., and Boone, C. (2003). Yeast genomics and proteomics in drug discovery and target validation. Prog. Cell Cycle Res. 5,159-16
111. Parsons, A. B., Lopez, A., Givoni, I. E., Williams, D. E., Gray, C. A., Porter, J., Chua, G., Sopko, R., Brost, R. L., Ho, C. H., Wang, J., Ketela, T., Brenner, C., Brill, J. A., Fernandez, G. E., Lorenz, T. C., Payne, G. S., Ishihara, S., Ohya, Y., Andrews, B., Hughes, T. R., Frey, B. J., Graham, T. R., Andersen, R. J., and Boone, C. (2006). Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126,611-62
112. Parveen, M., Momose, Y., Kitagawa, E., Kurita, S., Kodama, O., and Iwahashi, H. (2003). Bioassay of pesticide Lindane using yeast-DNA microarrays technology. Chem-Bio Informatics J. 3,12-2
113. Pereira, F. B., Guimaraes, P. M., Gomes, D. G., Mira, N. P., Teixeira, M. C., Sa-Correia, I., and Domingues, L. (2011). Identification of candidate genes for yeast engineering to improve bioethanol production in very-high-gravity and lignocellu-losic biomass industrial fermentations. Biotechnol. Biofuels 4, 5
114. Perlstein, E. O., Ruderfer, D. M., Roberts, D. C., Schreiber, S. L., and Kruglyak, L. (2007). Geneticbasis of individual differences in the response to small-molecule drugs in yeast. Nat. Genet. 39,496-50
115. Pham, T. K., Chong, P. K., Gan, C. S., and Wright, P. C. (2006). Proteomic analysis of Saccharomyces cerevisiae under high gravity fermentation conditions. J. Proteome Res. 5,3411-341
116. Pocaly, M., Lagarde, V., Etienne, G., Dupouy, M., Lapaillerie, D., Claverol, S., Vilain, S., Bonneu, M., Turcq, B., Mahon, F.-X., and Pasquet, J.-M. (2008). Proteomic analysis of an imatinib-resistant K562 cell line highlights opposing roles of heat shock cognate 70 and heat shock 70 proteins in resistance. Proteomics 8, 2394-240
117. Quintás-Cardama, A., Kantarjian, H. M., and Cortes, J. E. (2009). Mechanisms of primary and secondary resistance to imatinib in chronic myeloid leukemia. Cancer Control 16,122-13
118. Ruderfer, D. M., Roberts, D. C., Schreiber, S. L., Perlstein, E. O., and Kruglyak, L. (2009). Using expression and genotype to predict drug response in yeast. PLoS ONE 4, e6907. doi:10.1371/journal.pone.0006907
119. Ruotolo, R., Marchini, G., and Ottonello, S. (2008). Membrane transporters and protein traffic networks differentially affecting metal tolerance: a genomic phenotyping study in yeast. Genome Biol. 9, R6
120. Sá-Correia, I., dos Santos, S. C., Teixeira, M. C., Cabrito, T. R., and Mira, N. P. (2009). Drug:H+ antiporters in chemical stress response in yeast. Trends Microbiol. 17,22-3
121. Sa-Correia, I., and Teixeira, M. C. (2010). 2D electrophoresis-based expression proteomics: a microbiologist's perspective. Expert Rev. Proteomics 7, 943-95
122. Saliba, K. J., Krishna, S., and Kirk, K. (2004). Inhibition of hexose transport and abrogation of pH homeostasis in the intraerythrocytic malaria parasite by an O-3-hexose derivative. FEBS Lett. 570, 93-9
123. Sanchez, C. P., Stein, W. D., and Lanzer, M. (2008). Dissecting the components of quinine accumulation in Plasmodium falciparum. Mol. Microbiol. 67, 1081-109
124. Santos, P. M., Simões, T., and Sá-Correia, I. (2009). Insights into yeast adaptive response to the agricultural fungicide mancozeb: a toxico-proteomics approach. Proteomics 9, 657-67
125. Schenk, P. W., Boersma, A. W., Brandsma, J. A., Den Dulk, H., Burger, H., Stoter, G., Brouwer, J., and Nooter, K. (2001). SKY1 is involved in cisplatin-induced cell kill in Saccharomyces cerevisiae, and inactivation of its human homo-logue, SRPK1, induces cisplatin resistance in a human ovarian carcinoma cell line. Cancer Res. 61, 6982-698
126. Schenk, P. W., Boersma, A. W. M., Brok, M., Burger, H., Stoter, G., and Nooter, K. (2002). Inactivation of the Saccharomyces cerevisiae SKY1 gene induces a specific modification of the yeast anticancer drug sensitivity profile accompanied by a mutator phenotype. Mol. Pharmacol. 61, 659-66
127. Scherens, B., and Goffeau, A. (2004). The uses of genome-wide yeast mutant collections. Genome Biol. 5, 22
128. Schüller, C., Mamnun, Y. M., Mollapour, M., Krapf, G., Schuster, M., Bauer, B. E., Piper, P. W., and Kuchler, K. (2004). Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 706-72
129. Schwartz, D. A., Freedman, J. H., and Linney, E. A. (2004). Environmental genomics: a key to understanding biology, pathophysiology and disease. Hum. Mol. Genet. 13, R217-R22
130. Sennoune, S. R., Bakunts, K., Martínez, G. M., Chua-Tuan, J. L., Kebir, Y., Attaya, M. N., and Martínez-Zaguilán, R. (2004). Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am. J. Physiol. Cell Physiol. 286, C1443-C145
131. Serero, A., Lopes, J., Nicolas, A., and Boiteux, S. (2008). Yeast genes involved in cadmium tolerance: identification of DNA replication as a target of cadmium toxicity. DNA Repair (Amst.) 7, 1262-127
132. Shaulian, E., and Karin, M. (2002). AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4,E131-E13
133. +-ATPase is involved in the adaptation of soybean to phosphorus starvation. J. Exp. Bot. 57, 1353-136
134. Simmons, P. T., and Portier, C. J. (2002). Toxicogenomics: the new frontier in risk analysis. Carcinogenesis 23, 903-90
135. Simões, T., Teixeira, M. C., Fernandes, A. R., and Sá-Correia, I. (2003). Adaptation of Saccharomyces cerevisiae to the herbicide 2,4-dichlorophenoxyacetic acid, mediated by Msn2p- and Msn4p-regulated genes: important role of SPI1. Appl. Environ. Microbiol. 69, 4019-402
136. Simon, J. A., and Bedalov, A. (2004). Yeast as a model system for anticancer drug discovery. Nat. Rev. Cancer 4, 481-49
137. Sletta, H., Klinkenberg, G., Winnberg, A., Kvitvang, H. F., Nilsen, M. B., Krokan, H. E., Otterlei, M., and Bruheim, P. (2011). A new high resolution screening method for study of phenotype stress responses of Saccharomyces cerevisiae mutants. J. Microbiol. Methods 87, 363-36
138. Smart, C. C., and Fleming, A. J. (1996). Hormonal and environmental regulation of a plant PDR5-like ABC transporter. J. Biol. Chem. 271, 19351-1935
139. Smith, A. M., Ammar, R., Nislow, C., and Giaever, G. (2010). A survey of yeast genomic assays for drug and target discovery. Pharmacol. Ther. 127, 156-16
140. Stanley, D., Chambers, P. J., Stanley, G. A., Borneman, A., and Fraser, S. (2010). Transcriptional changes associated with ethanol tolerance in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 88, 231-23
141. Steinmetz, L. M., Scharfe, C., Deutschbauer, A. M., Mokran-jac, D., Herman, Z. S., Jones, T., Chu, A. M., Giaever, G., Prokisch, H., Oefner, P. J., and Davis, R. W. (2002). Systematic screen for human disease genes in yeast. Nat. Genet. 31,400-40
142. Swen, J. J., Huizinga, T. W., Gelderblom, H., De Vries, E. G. E., Assendelft, W. J. J., Kirchheiner, J., and Guchelaar, H.-J. (2007). Translating pharma-cogenomics: challenges on the road to the clinic. PLoS Med. 4, e209. doi:10.1371/journal.pmed.0040209
143. Takumi, S., Kimura, H., Matsusaki, H., Kawazoe, S., Tominaga, N., and Arizono, K. (2010). DNA microarray analysis of genomic responses of yeast Saccharomyces cerevisiae to nickel chloride. J. Toxicol. Sci. 35, 125-12
144. Teixeira, M. C., Dias, P. J., Monteiro, P. T., Sala, A., Oliveira, A. L., Freitas, A. T., and Sá-Correia, I. (2010a). Refining current knowledge on the yeast FLR1 regulatory network by combined experimental and computational approaches. Mol. Biosyst. 6, 2471-248
145. Teixeira, M. C., Raposo, L. R., Palma, M., and Sa-Correia, I. (2010b). Identification of genes required for maximal tolerance to high-glucose concentrations, as those present in industrial alcoholic fermentation media, through a chemogenomics approach. OMICS 14,201-21
146. Teixeira, M. C., Duque, P., and Sá-Correia, I. (2007). Environmental genomics: mechanistic insights into toxicity of and resistance to the herbicide 2,4-D. Trends Biotechnol. 25, 363-37
147. Teixeira, M. C., Fernandes, A. R., Mira, N. P., Becker, J. D., and Sá-Correia, I. (2006a). Early transcriptional response of Saccharomyces cerevisiae to stress imposed by the herbicide 2,4-dichlorophenoxyacetic acid. FEMS Yeast Res. 6, 230-24
148. Teixeira, M. C., Monteiro, P., Jain, P., Tenreiro, S., Fernandes, A. R., Mira, N. P., Alenquer, M., Freitas, A. T., Oliveira, A. L., and Sá-Correia, I. (2006b). The YEAS-TRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res. 34, D446-D45
149. Teixeira, M. C., Mira, N. P., and Sa-Correia, I. (2011). A genome-wide perspective on the response and tolerance to food-relevant stresses in Saccharomyces cerevisiae. Curr. Opin. Biotechnol. 22, 150-15
150. Teixeira, M. C., Raposo, L. R., Mira, N. P., Lourenço, A. B., and Sá-Correia, I. (2009a). Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Appl. Environ. Microbiol. 75, 5761-577
151. Teixeira, M. C., Santos, P. M., Rodrigues, C., and Sa-Correia, I. (2009b). Teaching expression proteomics: from the wet-lab to the laptop. Biochem. Mol. Biol. Educ. 37, 279-28
152. Teixeira, M. C., and Sá-Correia, I. (2002). Saccharomyces cerevisiae resistance to chlorinated phenoxy-acetic acid herbicides involves Pdr1p-mediated transcriptional activation of TPO1 and PDR5 genes. Biochem. Biophys. Res. Commun. 292, 530-53
153. Teixeira, M. C., Santos, P. M., Fernandes, A. R., and Sá-Correia, I. (2005). A proteome analysis of the yeast response to the herbicide 2,4-dichlorophenoxyacetic acid. Proteomics 5, 1889-190
154. Teixeira, M. C., Telo, J. P., Duarte, N. F., and Sá-Correia, I. (2004). The herbicide 2,4-dichlorophenoxyacetic acid induces the generation of free-radicals and associated oxidative stress responses in yeast. Biochem. Biophys. Res. Commun. 324, 1101-110
155. Tenreiro, S., Nunes, P. A., Viegas, C. A., Neves, M. S., Teixeira, M. C., Cabral, M. G., and Sá-Correia, I. (2002). AQR1 gene (ORFYNL065w) encodes a plasma membrane transporter of the major facilitator super-family that confers resistance to short-chain monocarboxylic acids and quinidine in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 292,741-74
156. Thorpe, G. W., Fong, C. S., Alic, N., Higgins, V. J., and Dawes, I. W. (2004). Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxi dative-stress-response genes. Proc. Natl Acad. Sci. U.S.A. 101,6564-656
157. Tribouillard, D., Bach, S., Gug, F., Desban, N., Beringue, V., Andrieu, T., Dormont, D., Galons, H., Laude, H., Vilette, D., and Blondel, M. (2006). Using budding yeast to screen for antiprion drugs. Biotechnol J. 1, 58-6
158. Tucker, C. L., and Fields, S. (2004). Quantitative genome-wide analysis of yeast deletion strain sensitivities to oxidative and chemical stress. Comp. Funct. Genomics 5,216-22
159. van Maris, A. J., Abbott, D. A., Bellis-simi, E., Van Den Brink, J., Kuyper, M., Luttik, M. A., Wisselink, H. W., Scheffers, W. A., Van Dijken, J. P., and Pronk, J. T. (2006). Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Antonie Van Leeuwenhoek 90, 391-41
160. van Voorst, F., Houghton-Larsen, J., Jonson, L., Kielland-Brandt, M. C., and Brandt, A. (2006). Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under ethanol stress. Yeast 23, 351-35
161. Vargas, R. C., Tenreiro, S., Teixeira, M. C., Fernandes, A. R., and Sá-Correia, I. (2004). Saccharomyces cerevisiae multidrug transporter Qdr2p (Yil121wp): localization and function as a quinidine resistance determinant. Antimicrob. Agents Chemother. 48, 2531-253
162. Volpe, G., Panuzzo, C., Ulisciani, S., and Cilloni, D. (2009). Imatinib resistance in CML. Cancer Lett. 274, 1-9
163. Wang, H. P., Long, X. H., Sun, Z. Z., Rigaud, O., Xu, Q. Z., Huang, Y. C., Sui, J. L., Bai, B., and Zhou, P. K. (2006a). Identification of differentially transcribed genes in human lymphoblastoid cells irradiated with 0.5 Gy of gamma-ray and the involvement of low dose radiation inducible CHD6 gene in cell proliferation and radiosensitivity. Int. J. Radiat.Biol. 82, 181-19
164. Wang, R. A., Zhang, H., Balasenthil, S., Medina, D., and Kumar, R. (2006b). PAK1 hyperactivation is sufficient for mammary gland tumor formation. Oncogene 25, 2931-293
165. Wang, L., and Weinshilboum, R. M. (2008). Pharmacogenomics: candidate gene identification, functional validation and mechanisms. Hum. Mol. Genet. 17, R174-R17
166. West, G. M., Tucker, C. L., Xu, T., Park, S. K., Han, X., Yates, J. R. III, and Fitzgerald, M. C. (2010). Quantitative proteomics approach for identifying proteindrug interactions in complex mixtures using protein stability measurements. Proc. Natl. Acad. Sci. U.S.A. 107, 9078-908
167. WHO. (2006). Guidelines for the Treatment of Malaria. Geneva: World Health Organization.
168. Willingham, S., Outeiro, T. F., Devit, M. J., Lindquist, S. L., and Muchowski, P. J. (2003). Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. Science 302,1769-177
169. Woodrow, C. J., Penny, J. I., and Krishna,S. (1999). Intraerythrocytic Plasmodium falciparum expresses a high affinity facilitative hexose transporter. J. Biol. Chem. 274, 7272-727
170. Wu, H. I., Brown, J. A., Dorie, M. J., Lazzeroni, L., and Brown, J. M. (2004). Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res. 64, 3940-394
171. Wuster, A., and Madan Babu, M. (2008). Chemogenomics and biotechnology. Trends Biotechnol. 26,252-25
172. Yasokawa, D., Murata, S., Kitagawa, E., Iwahashi, Y., Nakagawa, R., Hashido, T., and Iwahashi, H. (2008). Mechanisms of copper toxicity in Saccharomyces cerevisiae determined by microarray analysis. Environ. Toxicol. 23, 599-60
173. Yoshikawa, K., Tanaka, T., Furusawa, C., Nagahisa, K., Hirasawa, T., and Shimizu, H. (2009). Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res. 9, 32-4
174. Yuen, K. W Y, Warren, C. D., Chen, O., Kwok, T., Hieter, P., and Spencer, E A. (2007). Systematic genome instability screens in yeast and their potential relevance to cancer. Proc. Natl. Acad. Sci. U.S.A. 104, 3925-393
175. Zhang, L., Mchale, C. M., Rothman, N., Li, G., Ji,Z.,Vermeulen, R.,Hubbard, A. E., Ren, X., Shen, M., Rappaport, S. M., North, M., Skibola, C. F., Yin, S., Vulpe, C., Chanock, S. J., Smith, M. T., and Lan, Q. (2010). Systems biology of human benzene exposure. Chem. Biol. Interact. 184, 86-9
176. Zhou, Y., Shie, E S., Piccardo, P., Montine, T. J., and Zhang, J. (2004). Proteasomal inhibition induced by manganese ethylene-bisdithiocarbamate: relevance to Parkinson's disease. Neuroscience 128,281-29