Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

The Sensitive Genes in Response to Various Metal Ion Stresses in the Yeast Saccharomyces cerevisiae

Author(s): Keliang Lyu, Kailun Shi, Chengkun Liu, Zhiwen Lyu, Dongwu Liu and Xue Wang*

Volume 29, Issue 3, 2022

Published on: 28 March, 2022

Page: [231 - 241] Pages: 11

DOI: 10.2174/0929866529666220126102348

Price: $65

Abstract

Yeast Saccharomyces cerevisiae is a good eukaryotic model for studying the molecular mechanism of toxic metal ion stress. Numerous studies have been performed on the signal transduction induced by toxic metal ion stress. The physiological process of eukaryotic cells has been studied, and various stress factors have been elucidated by constructing a gene deletion library. The sensitivity and tolerance mechanism of yeast under metal ion stress has been widely studied. The sensitive genes induced by metal ion stress will provide a key foundation for studying the gene function of eukaryotic organisms. In addition, the functions of genes in response to metal ion stress mainly participate in regulating ion homeostasis, high glycerin pathway, vacuole protein separation pathway, cell wall integrity pathway, and cell autophagy. However, the interaction of these signal pathways and the detailed response mechanism need to be further studied. In addition, the technique of genomics and proteomics will help study the detailed molecular mechanism induced by toxic metal ion stress. Thus, the sensitive genes related to various signal pathways under toxic metal ion stress will be reviewed in the yeast S. cerevisiae.

Keywords: Yeast, toxic, metal ion, stress, signal pathway, functional gene.

Graphical Abstract
[1]
Rakowska, R.; Sadowska, A.; Dybkowska, E.; Świderski, F. Spent yeast as natural source of functional food additives. Rocz. Panstw. Zakl. Hig., 2017, 68(2), 115-121.
[PMID: 28646828]
[2]
Gallone, B.; Steensels, J.; Prahl, T.; Soriaga, L.; Saels, V.; Herrera-Malaver, B.; Merlevede, A.; Roncoroni, M.; Voordeckers, K.; Miraglia, L.; Teiling, C.; Steffy, B.; Taylor, M.; Schwartz, A.; Richardson, T.; White, C.; Baele, G.; Maere, S.; Verstrepen, K.J. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell, 2016, 166(6), 1397-1410.e16.
[http://dx.doi.org/10.1016/j.cell.2016.08.020] [PMID: 27610566]
[3]
Feng, L.; Wang, J.; Ye, D.; Song, Y.; Qin, Y.; Liu, Y. Yeast population dynamics during spontaneous fermentation of icewine and selection of indigenous saccharomyces cerevisiae strains for the winemaking in Qilian, China. J. Sci. Food Agric., 2020, 100(15), 5385-5394.
[http://dx.doi.org/10.1002/jsfa.10588] [PMID: 32535908]
[4]
Eide, D.J.; Clark, S.; Nair, T.M.; Gehl, M.; Gribskov, M.; Guerinot, M.L.; Harper, J.F. Characterization of the yeast ionome: A genome-wide analysis of nutrient mineral and trace element homeostasis in Saccharomyces cerevisiae. Genome Biol., 2005, 6(9), R77.
[http://dx.doi.org/10.1186/gb-2005-6-9-r77] [PMID: 16168084]
[5]
Arita, A.; Zhou, X.; Ellen, T.P.; Liu, X.; Bai, J.; Rooney, J.P.; Kurtz, A.; Klein, C.B.; Dai, W.; Begley, T.J.; Costa, M. A genome-wide deletion mutant screen identifies pathways affected by nickel sulfate in Saccharomyces cerevisiae. BMC Genomics, 2009, 10, 524.
[http://dx.doi.org/10.1186/1471-2164-10-524] [PMID: 19917080]
[6]
Zhao, Y.; Du, J.; Zhao, G.; Jiang, L. Activation of calcineurin is mainly responsible for the calcium sensitivity of gene deletion mutations in the genome of budding yeast. Genomics, 2013, 101(1), 49-56.
[http://dx.doi.org/10.1016/j.ygeno.2012.09.005] [PMID: 23026396]
[7]
Jiang, L.; Cao, C.; Zhang, L.; Lin, W.; Xia, J.; Xu, H.; Zhang, Y. Cadmium-induced activation of high osmolarity glycerol pathway through its Sln1 branch is dependent on the MAP kinase kinase kinase Ssk2, but not its paralog Ssk22, in budding yeast. FEMS Yeast Res., 2014, 14(8), 1263-1272.
[http://dx.doi.org/10.1111/1567-1364.12220] [PMID: 25331360]
[8]
Duan, S.F.; Shi, J.Y.; Yin, Q.; Zhang, R.P.; Han, P.J.; Wang, Q.M.; Bai, F.Y. Reverse evolution of a classic gene network in yeast offers a competitive advantage. Curr. Biol., 2019, 29(7), 1126-1136.e5.
[http://dx.doi.org/10.1016/j.cub.2019.02.038] [PMID: 30905601]
[9]
Shen, L.; Li, Y.; Jiang, L.; Wang, X. Response of Saccharomyces cerevisiae to the stimulation of lipopolysaccharide. PLoS One, 2014, 9(8), e104428.
[http://dx.doi.org/10.1371/journal.pone.0104428] [PMID: 25105496]
[10]
Lu, Y.; Wang, J.; Zhao, Y.; Deng, Y. The effect of calcium signaling pathway on the expression of genes regulated by crz1 in saccharomyces cerevisiae. Chinese J. Cell Biol., 2018, 40, 29-38.
[11]
Zhao, Y.; Xu, H.; Zhang, Y.; Jiang, L. Regulation of ion homeostasis in Saccharomyces cerevisiae. Biotechnology, 2015, 25, 403-408.
[12]
Zhao, J.; Lin, W.; Ma, X.; Lu, Q.; Ma, X.; Bian, G.; Jiang, L. The protein kinase Hal5p is the high-copy suppressor of lithium-sensitive mutations of genes involved in the sporulation and meiosis as well as the ergosterol biosynthesis in saccharomyces cerevisiae. Genomics, 2010, 95(5), 290-298.
[http://dx.doi.org/10.1016/j.ygeno.2010.02.010] [PMID: 20206679]
[13]
Thorsen, M.; Perrone, G.G.; Kristiansson, E.; Traini, M.; Ye, T.; Dawes, I.W.; Nerman, O.; Tamás, M.J. Genetic basis of arsenite and cadmium tolerance in saccharomyces cerevisiae. BMC Genomics, 2009, 10, 105.
[http://dx.doi.org/10.1186/1471-2164-10-105] [PMID: 19284616]
[14]
Tun, N.M.; O’Doherty, P.J.; Chen, Z.H.; Wu, X.Y.; Bailey, T.D.; Kersaitis, C.; Wu, M.J. Identification of aluminium transport-related genes via genome-wide phenotypic screening of Saccharomyces cerevisiae. Metallomics, 2014, 6(8), 1558-1564.
[http://dx.doi.org/10.1039/C4MT00116H] [PMID: 24926745]
[15]
Johnson, A.J.; Veljanoski, F.; O’Doherty, P.J.; Zaman, M.S.; Petersingham, G.; Bailey, T.D.; Münch, G.; Kersaitis, C.; Wu, M.J. Molecular insight into arsenic toxicity via the genome-wide deletion mutant screening of Saccharomyces cerevisiae. Metallomics, 2016, 8(2), 228-235.
[http://dx.doi.org/10.1039/C5MT00261C] [PMID: 26688044]
[16]
Luo, C.; Cao, C.; Jiang, L. The endosomal sorting complex required for transport (ESCRT) is required for the sensitivity of yeast cells to nickel ions in Saccharomyces cerevisiae. FEMS Yeast Res., 2016, 16(3), 16.
[http://dx.doi.org/10.1093/femsyr/fow028] [PMID: 26994103]
[17]
Cui, J.; Kaandorp, J.A.; Sloot, P.M.; Lloyd, C.M.; Filatov, M.V. Calcium homeostasis and signaling in yeast cells and cardiac myocytes. FEMS Yeast Res., 2009, 9(8), 1137-1147.
[http://dx.doi.org/10.1111/j.1567-1364.2009.00552.x] [PMID: 19678847]
[18]
Zhao, Y.; Du, J.; Xiong, B.; Xu, H.; Jiang, L. ESCRT components regulate the expression of the ER/Golgi calcium pump gene PMR1 through the Rim101/Nrg1 pathway in budding yeast. J. Mol. Cell Biol., 2013, 5(5), 336-344.
[http://dx.doi.org/10.1093/jmcb/mjt025] [PMID: 23933635]
[19]
Araki, Y.; Wu, H.; Kitagaki, H.; Akao, T.; Takagi, H.; Shimoi, H. Ethanol stress stimulates the Ca2+-mediated calcineurin/Crz1 pathway in Saccharomyces cerevisiae. J. Biosci. Bioeng., 2009, 107(1), 1-6.
[http://dx.doi.org/10.1016/j.jbiosc.2008.09.005] [PMID: 19147100]
[20]
Castrejon, F.; Gomez, A.; Sanz, M.; Duran, A.; Roncero, C. The RIM101 pathway contributes to yeast cell wall assembly and its function becomes essential in the absence of mitogen-activated protein kinase Slt2p. Eukaryot. Cell, 2006, 5(3), 507-517.
[http://dx.doi.org/10.1128/EC.5.3.507-517.2006] [PMID: 16524906]
[21]
Zhao, Y.; Jiang, L. Calcium/Calcineurin signal transduction pathway in Saccharomyces cerevisiae. Chinese J. Cell Biol., 2013, 35, 87-96.
[22]
Colinet, A.S.; Sengottaiyan, P.; Deschamps, A.; Colsoul, M.L.; Thines, L.; Demaegd, D.; Duchêne, M.C.; Foulquier, F.; Hols, P.; Morsomme, P. Yeast Gdt1 is a Golgi-localized calcium transporter required for stress-induced calcium signaling and protein glycosylation. Sci. Rep., 2016, 6, 24282.
[http://dx.doi.org/10.1038/srep24282] [PMID: 27075443]
[23]
Hamel, L.P.; Nicole, M.C.; Duplessis, S.; Ellis, B.E. Mitogen-activated protein kinase signaling in plant-interacting fungi: Distinct messages from conserved messengers. Plant Cell, 2012, 24(4), 1327-1351.
[http://dx.doi.org/10.1105/tpc.112.096156] [PMID: 22517321]
[24]
Vázquez-Ibarra, A.; Rodríguez-Martínez, G.; Guerrero-Serrano, G.; Kawasaki, L.; Ongay-Larios, L.; Coria, R. Negative feedback-loop mechanisms regulating HOG- and pheromone-MAPK signaling in yeast. Curr. Genet., 2020, 66(5), 867-880.
[http://dx.doi.org/10.1007/s00294-020-01089-5] [PMID: 32564133]
[25]
Román, E.; Correia, I.; Prieto, D.; Alonso, R.; Pla, J. The HOG MAPK pathway in Candida albicans: More than an osmosensing pathway. Int. Microbiol., 2020, 23(1), 23-29.
[http://dx.doi.org/10.1007/s10123-019-00069-1] [PMID: 30875035]
[26]
Jiménez-Gutiérrez, E.; Alegría-Carrasco, E.; Sellers-Moya, Á.; Molina, M.; Martín, H. Not just the wall: the other ways to turn the yeast CWI pathway on. Int. Microbiol., 2020, 23(1), 107-119.
[http://dx.doi.org/10.1007/s10123-019-00092-2] [PMID: 31342212]
[27]
González-Rubio, G.; Fernández-Acero, T.; Martín, H.; Molina, M. Mitogen-Activated protein kinase phosphatases (MKPs) in fungal signaling: Conservation, function, and regulation. Int. J. Mol. Sci., 2019, 20(7), 20.
[http://dx.doi.org/10.3390/ijms20071709] [PMID: 30959830]
[28]
Levin, D.E. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 2005, 69(2), 262-291.
[http://dx.doi.org/10.1128/MMBR.69.2.262-291.2005] [PMID: 15944456]
[29]
Rodríguez-Peña, J.M.; García, R.; Nombela, C.; Arroyo, J. The high-osmolarity glycerol (HOG) and cell wall integrity (CWI) signalling pathways interplay: A yeast dialogue between MAPK routes. Yeast, 2010, 27(8), 495-502.
[http://dx.doi.org/10.1002/yea.1792] [PMID: 20641030]
[30]
Capaldi, A.P.; Kaplan, T.; Liu, Y.; Habib, N.; Regev, A.; Friedman, N.; O’Shea, E.K. Structure and function of a transcriptional network activated by the MAPK Hog1. Nat. Genet., 2008, 40(11), 1300-1306.
[http://dx.doi.org/10.1038/ng.235] [PMID: 18931682]
[31]
Takayama, T.; Yamamoto, K.; Saito, H.; Tatebayashi, K. Interaction between the transmembrane domains of Sho1 and Opy2 enhances the signaling efficiency of the Hog1 MAP kinase cascade in Saccharomyces cerevisiae. PLoS One, 2019, 14(1), e0211380.
[http://dx.doi.org/10.1371/journal.pone.0211380] [PMID: 30682143]
[32]
Hohmann, S. Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett., 2009, 583(24), 4025-4029.
[http://dx.doi.org/10.1016/j.febslet.2009.10.069] [PMID: 19878680]
[33]
Ruan, H.; Li, X.; Lan, P.; Jiang, L. High osmolarity glycerol MAP kinase signal transduction pathway. Chinese J. Cell Biol., 2006, 5, 651-655.
[34]
Wu, X.; Hu, S.; Qian, K. HOG-MAPK pathway in yeast. Chinese J. Cell Biol., 2005, 27, 247-252.
[35]
MacDiarmid, C.W.; Gaither, L.A.; Eide, D. Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J., 2000, 19(12), 2845-2855.
[http://dx.doi.org/10.1093/emboj/19.12.2845] [PMID: 10856230]
[36]
Rosenfeld, L.; Reddi, A.R.; Leung, E.; Aranda, K.; Jensen, L.T.; Culotta, V.C. The effect of phosphate accumulation on metal ion homeostasis in Saccharomyces cerevisiae. Eur. J. Biochem., 2010, 15(7), 1051-1062.
[http://dx.doi.org/10.1007/s00775-010-0664-8] [PMID: 20429018]
[37]
Nguyen, T.Q.; Dziuba, N.; Lindahl, P.A. Isolated Saccharomyces cerevisiae vacuoles contain low-molecular-mass transition-metal polyphosphate complexes. Metallomics, 2019, 11(7), 1298-1309.
[http://dx.doi.org/10.1039/C9MT00104B] [PMID: 31210222]
[38]
Zhou, X.; O’Shea, E.K. Integrated approaches reveal determinants of genome-wide binding and function of the transcription factor Pho4. Mol. Cell, 2011, 42(6), 826-836.
[http://dx.doi.org/10.1016/j.molcel.2011.05.025] [PMID: 21700227]
[39]
Tomar, P.; Sinha, H. Conservation of PHO pathway in ascomycetes and the role of Pho84. J. Biosci., 2014, 39(3), 525-536.
[http://dx.doi.org/10.1007/s12038-014-9435-y] [PMID: 24845516]
[40]
Mouillon, J.M.; Persson, B.L. New aspects on phosphate sensing and signalling in Saccharomyces cerevisiae. FEMS Yeast Res., 2006, 6(2), 171-176.
[http://dx.doi.org/10.1111/j.1567-1364.2006.00036.x] [PMID: 16487340]
[41]
Chen, S.; Mari, M.; Parashar, S.; Liu, D.; Cui, Y.; Reggiori, F.; Novick, P.J.; Ferro-Novick, S. Vps13 is required for the packaging of the ER into autophagosomes during ER-phagy. Proc. Natl. Acad. Sci. USA, 2020, 117(31), 18530-18539.
[http://dx.doi.org/10.1073/pnas.2008923117] [PMID: 32690699]
[42]
Kingsbury, J.M.; Sen, N.D.; Maeda, T.; Heitman, J.; Cardenas, M.E. Endolysosomal membrane trafficking complexes drive nutrient-dependent TORC1 signaling to control cell growth in Saccharomyces cerevisiae. Genetics, 2014, 196(4), 1077-1089.
[http://dx.doi.org/10.1534/genetics.114.161646] [PMID: 24514902]
[43]
Hecht, K.A.; O’Donnell, A.F.; Brodsky, J.L. The proteolytic landscape of the yeast vacuole. Cell. Logist., 2014, 4(1), e28023.
[http://dx.doi.org/10.4161/cl.28023] [PMID: 24843828]
[44]
Dokudovskaya, S; Waharte, F; Schlessinger, A; Pieper, U; Devos, DP; Cristea, IM; Williams, R; Salamero, J; Chait, BT; Sali, A A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae. Mol Cell Proteomics, 2011, 006478.
[http://dx.doi.org/10.1074/mcp.M110.006478]
[45]
Huang, H.; Li, W.; Yang, D. ESCRT system: A multifunctional machine for protein trafficking and membrane scission. Chin. J. Biochem. Mol. Biol., 2013, 29, 99-109.
[46]
Shanks, S.G.; Carpp, L.N.; Struthers, M.S.; McCann, R.K.; Bryant, N.J. The Sec1/Munc18 protein Vps45 regulates cellular levels of its SNARE binding partners Tlg2 and Snc2 in saccharomyces cerevisiae. PLoS One, 2012, 7(11), e49628.
[http://dx.doi.org/10.1371/journal.pone.0049628] [PMID: 23166732]
[47]
Saha, N.; Dutta, S.; Datta, S.P.; Sarkar, S. The minimal ESCRT machinery of giardia lamblia has altered inter-subunit interactions within the ESCRT-II and ESCRT-III complexes. Eur. J. Cell Biol., 2018, 97(1), 44-62.
[http://dx.doi.org/10.1016/j.ejcb.2017.11.004] [PMID: 29224850]
[48]
Fayyadkazan, M.; Tate, J.J.; Vierendeels, F.; Cooper, T.G.; Dubois, E.; Georis, I. Components of Golgi-to-vacuole trafficking are required for nitrogen- and TORC1-responsive regulation of the yeast GATA factors. MicrobiologyOpen, 2014, 3(3), 271-287.
[http://dx.doi.org/10.1002/mbo3.168] [PMID: 24644271]
[49]
Feyder, S.; De Craene, J.O.; Bär, S.; Bertazzi, D.L.; Friant, S. Membrane trafficking in the yeast Saccharomyces cerevisiae model. Int. J. Mol. Sci., 2015, 16(1), 1509-1525.
[http://dx.doi.org/10.3390/ijms16011509] [PMID: 25584613]
[50]
Grosjean, N.; Gross, E.M.; Le Jean, M.; Blaudez, D. Global deletome profile of Saccharomyces cerevisiae exposed to the technology-critical element yttrium. Front. Microbiol., 2018, 9, 2005.
[http://dx.doi.org/10.3389/fmicb.2018.02005] [PMID: 30233513]
[51]
Serero, A.; Lopes, J.; Nicolas, A.; Boiteux, S. Yeast genes involved in cadmium tolerance: identification of DNA replication as a target of cadmium toxicity. DNA Repair (Amst.), 2008, 7(8), 1262-1275.
[http://dx.doi.org/10.1016/j.dnarep.2008.04.005] [PMID: 18514590]
[52]
Johnson, A.J.; Veljanoski, F.; O’Doherty, P.J.; Zaman, M.S.; Petersingham, G.; Bailey, T.D.; Münch, G.; Kersaitis, C.; Wu, M.J. Revelation of molecular basis for chromium toxicity by phenotypes of Saccharomyces cerevisiae gene deletion mutants. Metallomics, 2016, 8(5), 542-550.
[http://dx.doi.org/10.1039/C6MT00039H] [PMID: 27146641]
[53]
Ruotolo, R.; Marchini, G.; Ottonello, S. Membrane transporters and protein traffic networks differentially affecting metal tolerance: A genomic phenotyping study in yeast. Genome Biol., 2008, 9(4), R67.
[http://dx.doi.org/10.1186/gb-2008-9-4-r67] [PMID: 18394190]
[54]
Du, J.; Cao, C.; Jiang, L. Genome-scale genetic screen of lead ion-sensitive gene deletion mutations in Saccharomyces cerevisiae. Gene, 2015, 563(2), 155-159.
[http://dx.doi.org/10.1016/j.gene.2015.03.018] [PMID: 25773006]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy