Abstract:
We investigated the influence of the quaternary ammonium salt (QAS) called IM (N-(dodecyloxycarboxymethyl)-N,N,N-trimethyl ammonium chloride) on yeast cells of the parental strain and the IM-resistant mutant (EO25 IMR) growth. The phenotype of this mutant was pleiotropic. The IMR mutant exhibited resistance to ethanol, osmotic shock and oxidative stress, as well as increased sensitivity to UV. Moreover, it was noted that mutant EO25 appears to have an increased resistance to clotrimazole, ketoconazole, fluconazole, nystatin and cycloheximide. It also tolerated growth in the presence of crystal violet, DTT and metals (selenium, tin, arsenic). It was shown that the presence of IM decreased ergosterol level in mutant plasma membrane and increased its unsaturation. These results indicate changes in the cell lipid composition. Western blot analysis showed the induction of Pma1 level by IM. RT-PCR revealed an increased PMA1 expression after IM treatment.
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References
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W and Lipman DJ 1997 Gapped BLAST and PSI_BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 3389–3402
Anthoni U, Christophersen C, Hougard L and Nielsen PH 1991 Quaternary ammonium compounds in the biosphere - an example of a versatile adaptive strategy. Comp. Biochem. Physiol. 99B 1–18
Badawi AM, Mohamed MA, Mohamed MZ and Khowdairy MM 2007 Surface and antitumor activity of some novel metal-based cationic surfactants. J. Cancer Res. Ther. 3 198–206
Bartosiewicz D and Krasowska A 2009 Inhibitors of ABC transporters and biophysical methods to study their activity. Z. Naturforsch. C. 64 454–458
Basso TS, Pungartnik C and Brendel M 2008 Low productivity of ribonucleotide reductase in Saccharomyces cerevisiae increases sensitivity to stannous chloride. Genet. Mol. Res. 7 1–6
Benito B, Moreno E and Lagunas R 1991 Half-life of the plasma membrane ATPase and its activating system in resting yeast cells. Biochim. Biophys. Acta. 1063 265–268
Bore E, Hebraud M, Chafsey I, Chambon C, Skjaeret C, Moen B, Moretro T, Langsrud O, et al. 2007 Adapted tolerance to benzalkonium chloride in Escherichia coli K-12 studied by transcriptome and proteome analyses. Microbiology. 153 935–946
Braoudaki M and Hilton AC 2005 Mechanisms of resistance in Salmonella enterica adapted to erythromycin benzalkonium chloride and triclosan. Int. J. Antimicrob. Agents. 25 31–37
de Freitas JM, Bravim F, Buss DS, Lemos EM, Fernandes AA and Fernandes PM 2012 Influence of cellular fatty acid composition on the response of Saccharomyces cerevisiae to hydrostatic pressure stress. FEMS Yeast Res. 12 871–878
Dinh TN, Nagahisa K, Hirasawa T, Furusawa C and Shimizu H 2008 Adaptation of Saccharomyces cerevisiae cells to high ethanol concentration and changes in fatty acid composition of membrane and cell size. PLoS ONE. 3, e2623. doi:10.1371/journal.pone.0002623
Dubnicková M, Rezanka T and Koscová H 2006 Adaptive changes in fatty acids of E. coli strains exposed to a quaternary ammonium salt and an amine oxide. Folia Microbiol. 51 371–374
Dufour JP and Goffeau A 1980 Molecular and kinetic properties of the purified plasma membrane ATPase of the yeast Schizosaccharomyces pombe. Eur. J. Biochem. 105 145–154
Fernandes AR and Sa-Correia I 2003 Transcription patterns of PMA1 and PMA2 genes and activity of plasma memmbrane H+-ATPase in Saccharomyces cerevisiae during diauxic growth and stationary phase. Yeast. 20 207–219
Ferreira ME, Colombo AL, Paulsen I, Ren Q, Wortman J, Huang J, Goldman MHS and Goldman GH 2005 The ergosterol biosynthesis pathway, transporter genes, and azole resistance in Aspergillus fumigatus. Med. Mycol. 43 S313–S319
Folch J, Lees M and Sloane Stanley GH 1957 A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226 497–509
Garcia-Arranz M, Maldonado AM, Mazon MJ and Portillo F 1994 Transcriptional control of yeast plasma membrane H+-ATPase by glucose. Cloning and characterization of a new gene involved in this regulation. J. Biol. Chem. 269 18076–18082
Giraud I, Rapp M, Maurizis JC and Madelmont JC 2002 Synthesis and in vitro evaluation of quaternary ammonium derivatives of chlorambucil and melphalan, anticancer drugs designed for the chemotherapy of chondrosarcoma. J. Med. Chem. 45 2116–2119
Grossman G, Opekarova M, Malinsky J, Weig-Meckl I and Tanner W 2007 Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 26 1–8
Guerin-Mechin L, Leveau J-Y and Dubois-Brissonnet F 2004 Resistance of spheroplasts and whole cells of Pseudomonas aeruginosa to bactericidal activity of various biocides: evidence of the membrane implication. Microbiol. Res. 159 51–57
Hegstad K, Langsrud S, Lunestad BT, Scheie AA, Sunde M and Yazdankhah SP 2010 Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb. Drug Resist. 16 91–104
Heredia RM, Boeris PS, Biasutti MA, López GA, Paulucci NS and Lucchesi GI 2014 Coordinated response of phospholipids and acyl components of membrane lipids in Pseudomonas putida A (ATCC 12633) under stress caused by cationic surfactants. Microbiology. 160 2618–2626
Ito E, Yip KW, Katz D, Fonesca SB, Hedley DW, Chow S, Xu GW, Wood TE, et al. 2009 Potential use of cetrimonium bromide as an apoptosis - promoting anticancer agent for head and neck cancer. Mol. Pharmacol. 76 969–983
Jacqout C, Julien R and Guilloton M 1997 The Saccharomyces cerevisiae MFS superfamily SGE1 gene confers resistance to cationic dyes. Yeast. 13 891–902
Kontoyiannis DP, Sagar N and Hirsch KD 1999 Overexpression of Erg11p by the regulatable GAL1 promoter confers fluconazole resistance in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 43 2798–2800
Lachowicz TM, Witkowska R and Obłąk E 1990 Amino acid auxotrophy increases sensitivity of Saccharomyces cerevisiae to a quaternary ammonium salt IM. Acta Microbiol. Pol. 39 157–162
Lachowicz TM, Obłąk E and Piątkowski J 1992 Auxotropy-stimulated sensitivity to quaternary ammonium salt and its relation to active transport in yeast. Bul. Pol. Acad. Sci. Biol. Sci. 40 173–182
Lachowicz TM, Piątkowski J and Witek S 1995 Quaternary ammonium salts and arginine are inhibitors of general amino acid permease in yeast. Pestic. Sci. 43 169–171
Lee C 2001 Structure, conformation and action of neuromuscular blocking drugs. Br. J. Anaesth. 87 755–769
Lei J, Zhao X, Ge X and Bai F 2007 Ethanol tolerance and the variation of plasma membrane composition of yeast floc populations with different size distribution. J. Biotechnol. 131 270–275
Machnicka B, Grochowalska R, Boniewska-Bernacka E, Słomińska L and Lachowicz TM 2004 Acid excreting mutants of yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 325 1030–1036
Malinska K, Malinsky J, Opekarova M and Tanner W 2003 Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell. 14 4427–4436
Massi L, Guittard F and Geribaldi S 2004 Quaternary bisammonium fluorosurfactants for antimicrobial devices. Progr. Colloid Polym. Sci. 126 190–193
Obłąk E and Krasowska A 2010 The influence of organic nitrogen compounds on melanoma, bacterial and fungal cells. Adv. Clin. Exp. Med. 19 65–75
Obłąk E, Ułaszewski S and Lachowicz TM 1988 Mutants of Saccharomyces cerevisiae resistant to a quaternary ammonium salt. Acta Microbiol. Pol. 37 261–269
Obłąk E, Ułaszewski S, Morawiecki A, Witek S, Witkowska R, Majcher K and Lachowicz TM 1989 Quaternary ammonium salt mutants in yeast Saccharomyces cerevisiae. Yeast. 5 273–278
Obłąk E, Lachowicz TM and Witek S 1996 DL- leucine transport in a Saccharomyces cerevisiae mutant resistant to quaternary ammonium salts. Folia Microbiol. 41 116–119
Obłąk E, Bącal J and Lachowicz TM 2000 A quaternary ammonium salt as an inhibitor of plasma membrane H+-ATPase in yeast Saccharomyces cerevisiae. Cell. Mol. Biol. Lett. 5 315–324
Obłąk E, Lachowicz TM, Łuczyński J and Witek S 2001 Comparative studies of biological activities of the lysosomotropic aminoesters and quaternary ammonium salts on yeast Saccharomyces cerevisiae. Cell. Mol. Biol. Lett. 6 871–880
Obłąk E, Lachowicz TM, Łuczyński J and Witek S 2002 Lysosomotropic N, N-dimethyl alpha-aminoacid n-alkylesters and their quaternary ammonium salts as plasma membrane and mitochondrial ATPases inhibitors. Cell. Mol. Biol. Lett. 7 1121–1129
Obłąk E, Adamski R and Lachowicz TM 2003 pH-dependent influence of a quaternary ammonium salt and an aminoester on the yeast Saccharomyces cerevisiae ultrastructure. Cell. Mol. Biol. Lett. 8 105–110
Obłąk E, Lachowicz TM, Łuczyński J and Witek S 2004 The aminoesters as inhibitors of plasma membrane H+-ATPase in the yeast Saccharomyces cerevisiae. Cell. Mol. Biol. Lett. 9 755–763
Obłąk E, Gamian A, Adamski R and Ułaszewski S 2010 The physiological and morphological phenotype of a yeast mutant resistant to the quaternary ammonium salt N-(dodecyloxycarboxymethyl)-N, N, N-trimethyl ammonium chloride. Cell. Mol. Biol. Lett. 15 215–233
Obłąk E, Piecuch A, Krasowska A and Łuczyński J 2013 Antifungal activity of gemini quaternary ammonium salts. Microbiol. Res. 168 630–638
Obłąk E, Piecuch A, Guz-Regner K and Dworniczek E 2014 Antibacterial activity of gemini quaternary ammonium salts. FEMS Microbiol. Lett. 350 190–198
Obłąk E, Piecuch A, Dworniczek E and Olejniczak T 2015 The influence of biodegradable gemini surfactants, N, N'-bis(1-decyloxy-1-oxopronan-2-yl)-N, N, N', N'-tetramethyl- propane-1,3-diammonium dibromide and N, N'-bis(1-dodecyloxy-1-oxopronan -2-yl) N, N, N', N'-tetramethylethane-1,2-diammonium dibromide, on fungal biofilm and adhesion. J. Oleo. Sci. 64 527–537
Panaretou B and Piper PW 1990 Plasma membrane ATPase action affects several stress tolerances of Saccharomyces cerevisiae and Schizosaccharomyces pombe as well as the extent and duration of the heat shock response. J. Gen. Microbiol. 136 1763–1770
Park SG, Cha MK, Jeong W and Kim IH 2000 Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J. Biol. Chem. 275 5723–5732
Paściak M, Ekiel I, Grzegorzewicz A, Mordarska H and Gamian A 2002 Structure of the major glycolipid from Rothia dentocariosa. Biochim. Biophys. Acta. 1594 199–205
Pico Y, Font G, Molto JC and Manes J 2000 Solid-phase extraction of quaternary ammonium herbicides. J. Chromatogr. A. 885 251–271
Piecuch A and Obłąk E 2014 Yeast ABC proteins involved in multidrug resistance. Cell. Mol. Biol. Lett. 19 1–22
Piecuch A, Obłąk E and Guz-Regner K 2016 Antibacterial activity of alanine-derived gemini quaternary ammonium compounds. J. Surfactant Deterg. 19 275–282
Portillo F 2000 Regulation of plasma membrane H+-ATPase in fungi and plants. Biochim. Biophys. Acta. 1469 31–42
Prince DL, Prince HN, Thraenhart O, Muchomore E, Bonder E and Pugh J 1993 Methodoological approaches to disinfection of human hepatitis B virus. J. Clin. Microbiol. 31 3296–3304
Resnick L, Varen K, Salahuddin SZ, Tondreau S and Markham PD 1986 Stability and inactivation of HTLV-III/LAV under clinical and laboratory environments. JAMA. 255 1887–1891
Riezman H, Hase T, van Loon AP, Grivell LA, Suda K and Schatz G 1983 Import of proteins into mitochondria: 70 kDa outermembrane proteins with the large carboxy terminal deletion is still transported to the outer membrane. EMBO J. 2 2161–2168
Rogers B, Decottignies A, Kołaczkowski M, Carvajal E, Balzi E and Goffeau A 2001 The pleiotropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 3 207–214
Rucka M, Oświęcimska M and Witek S 1983 New biocides for cooling water treatment. Quaternary ammonium salts derivatives of glycine esters. Part III. Environ. Prot. Eng. 9 25–31
Springthorpe VS and Satter SA 1990 Chemical disinfection of virus-contaminated surfaces. Crit. Rev. Environ. Control. 2 169–229
Thorsteinsson T, Masson M, Kristinsson KG, Hjalmarsdottir MA, Hilmarsson H and Loftsson T 2003 Soft antimicrobial agents: synthesis and activity of labile environmentally friendly long chain quaternary ammonium compounds. J. Med. Chem. 46 4173–4181
Turk M, Abramovic Z, Plemenitas A and Gunde-Cimerman N 2007 Salt stress and plasma membrane fluidity in selected extremophilic yeasts and yeast-like fungi. FEMS Yeast Res. 7 550–557
Ullah A, Orij R, Brul S and Smits GJ 2012 Quantitative analysis of the modes of growth inhibition by weak organic acids in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 78 8377–8387
Vali L, Davies SE, Lai LL, Dave J and Amyes SG 2008 Frequency of biocide resistance genes, antibiotic resistance and the effect of chlorhexidine exposure on clinical methicillin-resistant Staphylococcus aureus isolates. J. Antimicrob. Chemother. 61 524–532
White TC, Maar KA and Bowden RA 1998 Clinical, cellular and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev. 11 282–402
Witek S, Goffeau A, Nader J, Łuczyński J, Lachowicz TM, Kuta B and Obłąk E 1997 Lysosomotropic aminoesters act as H+-ATPase inhibitors in yeast. Folia Microbiol. 42 252–254
Wysocki R, Bobrowicz P and Ułaszewski S 1997 The Saccharomyces cerevisiae ACR3 gene encode a putative membrane protein involved in arsenite transport. J. Biol. Chem. 272 30061–30066
Xiao Y, Chen J, Fang M, Xing X, Wang H, Wang Y and Li F 2008 Antibacterial effects of three experimental quaternary ammonium salt (QAS) monomers on bacteria associated with oral infections. J. Oral Sci. 50 323–327
Zhou J, Zhou H, Du G, Liu L and Chen J 2010 Screening of thiamine-auxotrophic yeast for alpha-ketoglutaric acid overproduction. Lett. Appl. Microbiol. 51 264–271
Zhu XY, Wu JM and Jia ZS 2004 Superoxide anion radical scavenging ability of quaternary ammonium salt of chitosan. Chin. Chem. Lett. 15 808–810
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The work was supported by the Polish Ministry of Science and Higher Education grant No N N303 068 534.
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[Obłąk E, Piecuch A, Maciaszczyk-Dziubińska E and Wawrzycka D 2016 Quaternary ammonium salt N-(dodecyloxycarboxymethyl)-N,N,N-trimethyl ammonium chloride induced alterations in Saccharomyces cerevisiae physiology. J. Biosci.]
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Obłąk, E., Piecuch, A., Maciaszczyk-Dziubińska, E. et al. Quaternary ammonium salt N-(dodecyloxycarboxymethyl)-N,N,N-trimethyl ammonium chloride induced alterations in Saccharomyces cerevisiae physiology. J Biosci 41, 601–614 (2016). https://doi.org/10.1007/s12038-016-9644-7
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DOI: https://doi.org/10.1007/s12038-016-9644-7