Identification of gold nanoparticle-resistant mutants of Saccharomyces cerevisiae suggests a role for respiratory metabolism in mediating toxicity

Applied and Environmental Microbiology

Volumn 79, Issue 2, 2013, Pages 728-733

  Smith, Mark R ^a   Boenzli, Matthew G ^a   Hindagolla, Vihangi ^a   Ding, Jun ^a   Miller, John M ^b,c   Hutchison, James E ^b,c   Greenwood, Jeffrey A ^a   Abeliovich, Hagai ^d   Bakalinsky, Alan T ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b Safer Nanomaterials and Nanomanufacturing Initiative   (United States)

^c UNIVERSITY OF OREGON   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CORE DIAMETERS; DELETION MUTANTS; GENES ENCODING; GOLD NANOPARTICLES; POSITIVELY CHARGED;

GOLD; METAL NANOPARTICLES;

YEAST;

GOLD; NANOPARTICLE;

GENE EXPRESSION; GENOME; GROWTH; IDENTIFICATION METHOD; METABOLISM; MITOCHONDRION; MUTATION; PARTICULATE MATTER; PROTEIN; TOXICITY; YEAST;

ANTIFUNGAL RESISTANCE; ARTICLE; DRUG EFFECT; GENE DELETION; GENETICS; METABOLISM; MICROBIAL VIABILITY; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

DRUG RESISTANCE, FUNGAL; GENE DELETION; GOLD; METABOLIC NETWORKS AND PATHWAYS; MICROBIAL VIABILITY; NANOPARTICLES; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 84871913633     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01737-12     Document Type: Article

References (32)

1. Nel A, Xia T, Madler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science 311:622-627.
2. Shaw SY, Westley EC, Pittet MJ, Subramanian A, Schreiber SL, Weissleder R. 2008. Pertubational profiling of nanomaterial biologic activity.Proc. Natl. Acad. Sci. U. S. A. 105:7387-7392.
3. Lévy R, Shaheen U, Cesbron Y, Sée V. 2010. Gold nanoparticles delivery in mammalian live cells: a critical review. Nano Rev. 1:4889.
4. Ma X, Wu Y, Shubin J, Tian Y, Zhang X, Zhao Y, Yu L, Liang X-J. 2011.Gold nanoparticles induce autophagosome accumulat on through sizedependent nano uptake and lysosome impairment. ACS Nano 5:8629-8639.
5. Alkilany AM, Murphy CJ. 2010. Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J. Nanopart. Res. 12:2313-2333.
6. Murphy CJ, Gole AM, Stone JW, Sisco PN, Alkilany AM, Goldsmith EC, Baxter SC. 2008. Gold nanoparticles in biology: beyond toxicity to cellular imaging. Acc. Chem. Res. 41:1721-1730.
7. Evans MV, Turton HE, Grant CM, Dawes IW. 1998. Toxicity of linoleic acid hydroperoxide to Saccharomyces cerevisiae: involvement of a respiration-related process for maximal sensitivity and adaptive response. J. Bacteriol.180:483-490.
8. Harper S, Usenko C, Hutchison JE, Maddux BLS, Tanguay RL. 2008. In vivo biodistribution and toxicity depends on nanomaterial composition,size, surface functionalisation and route of exposure. J. Exp. Nanosci.3:195-206.
9. Pan Y, Leifert A, Ruau D, Neuss S, Bornemann J, Schmid G, Brandau W, Simon U, Jahnen-Dechent W. 2009. Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 5:2067-2076.
10. Truong L, Tilton SC, Zaikova T, Richman E, Waters KM, Hutchison JE, Tanguay RL. 20 January 2012. Surface functionalities of gold nanoparticlesimpact embryonic gene expression responses.. Nanotoxicology.[Epub ahead of print.] doi:10.3109/17435390.2011.648225.
11. Botstein D, Fink GR. 2011. Yeast: an experimental organism for 21st century biology. Genetics 189:695-704.
12. Chiron JP, Lamandé J, Moussa F, Trivin F, Céolin R. 2000. Effect of "micronized" C60 fullerene on the microbial growth in vitro. Ann. Pharm.Fr. 58:170-175.
13. Hadduck AN, Hindagolla V, Contreras A, Li Q, Bakalinsky AT. 2010. Does aqueous fullerene inhibit growth of Saccharomyces cerevisiae or Escherichia coli? Appl. Environ. Microbiol. 76:8239-8242.
14. Kasemets K, Ivask A, Dubourguier Kahru H-CA. 2009. Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae.Toxicol. In Vitro 23:1116-1122.
15. Maheshwari V, Fomenko DE, Singh G, Saraf RF. 2010. Ion mediated monolayer deposition of gold nanoparticles on microorganisms: discrimination by age. Langmuir 26:371-377.
16. Harper SL, Carriere JL, Miller JM, Hutchison JE, Maddux BLS, Tanguay RL. 2011. Systematic evaluation of nanomaterial toxicity: utility of standardized materials and rapid assays. ACS Nano 5:4688-4697.
17. Woehrle GH, Hutchison JE. 2005. Thiol-functionalized undecagold clusters by ligand exchange: synthesis, mechanism, and properties. Inorg. Chem. 44:6149-6158.
18. Kaeberlein M, Hu D, Kerr EO, Tsuchiya M, Westman EA, Dang N, Fields S, Kennedy BK. 2005. Increased life span due to calorie restriction in respiratory-deficient yeast. PLoS Genet. 1:e69. doi:10.1371/journal.pgen.0010069.
19. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, Mittmann M, Pai C, Rebischung C, Revuelta JL, Riles L, Roberts CJ, Ross-MacDonald P, Scherens B, Snyder M, Sookhai-Mahadeo S, Storms RK, Véronneau S, Voet M, Volckaert G, Ward TR, Wysocki R, Yen GS, Yu K, Zimmermann K, Philippsen Pohnston M, Davis RW. 1999. Functional characterization of the S.cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906.
20. Williamson DH, Fennell DJ. 1975. The use of fluorescent DNA-binding agent for detecting and separating yeast mitochondrial DNA, p 335-351.In Prescott DM (ed), Methods in cell biology, vol XII. Yeast cells. Academic Press, New York, NY.
21. Burke D, Dawson D, Stearns T. 2000. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Griffith J, Reggiori F. 2009. Ultrastructural analysis or nanogold-labeledendocytic compartments of yeast Saccharomyces cerevisiae using a cryosectioning procedure. J. Histochem. Cytochem. 57:801-809.
23. Prescianotto-Baschong C, Riezman H. 1998. Morphology of the yeast endocytic pathway. Mol. Biol. Cell 9:173-189.
24. Prescianotto-Baschong C, Riezman H. 2002. Ordering of compartments in the yeast endocytic pathway. Traffic 3:37-49.
25. Dimmer KS, Fritz S, Fuchs F, Messerschmitt M, Weinbach N, Neupert W, Westermann B. 2002. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13:847-853.
26. Merz S, Westermann B. 2009. Genome-wide deletion mutant analysis reveals genes required for respiratory growth, mitochondrial genome maintenance and mitochondrial protein synthesis in Saccharomyces cerevisiae. Genome Biol. 10:R95.
27. Thorpe GW, Fong CS, Alic N, Higgins VJ, Dawes IW. 2004. Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc. Natl. Acad. Sci.U. S. A. 101:6564-6569.
28. Tucker CL, Fields S. 2004. Quantitative genome-wide analysis of yeast deletion strain sensitivities to oxidative and chemical stress. Comp. Funct. Genomics 5:216-224.
29. Grant CM, MacIver FH, Dawes IW. 1997. Mitochondrial function is required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. FEBS Lett. 410:219-222.
30. Baev D, Rivetta A, Vylkova S, Sun JN, Zeng Slayman G-FCL, Edgerton M. 2004. The TRK1 potassium transporter is the critical effector for killing of Candida albicans by the cationic protein, histatin 5. J. Biol. Chem. 279:55060-55072.
31. Perrone GG, Grant CM, Dawes IW. 2005. Genetic and environmental factors influencing glutathione homoeostasis in Saccharomyces cerevisiae.Mol. Biol. Cell 16:218-230.
32. Myers AM, Pape LK, Tzagoloff A. 1985. Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 4:2087-2092.