Effects of mercury on dictyostelium discoideum: Proteomics reveals the molecular mechanisms of physiological adaptation and toxicity

Journal of Proteome Research

Volumn 9, Issue 6, 2010, Pages 2839-2854

  Marsano, Francesco ^a   Boatti, Lara ^a   Ranzato, Elia ^a   Cavaletto, Maria ^a   Magnelli, Valeria ^a   Dondero, Francesco ^a   Viarengo, Aldo ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Dictyostelium discoideum; mass spectrometry; mercury; oxidative stress response; protein carbonylation; proteomics

Indexed keywords

MERCURY; METAL ION; OXIDOREDUCTASE; TRANSFERASE;

ADAPTATION; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; CYTOTOXICITY; DETOXIFICATION; DICTYOSTELIUM DISCOIDEUM; DOSE RESPONSE; DOWN REGULATION; ELECTROPHORESIS; ENZYME ACTIVITY; MASS SPECTROMETRY; METAL BINDING; MORTALITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEOMICS; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; DICTYOSTELIUM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MASS SPECTROMETRY; MERCURY; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PROTEIN CARBONYLATION; PROTEOMICS; PROTOZOAN PROTEINS; REACTIVE OXYGEN SPECIES; STATISTICS, NONPARAMETRIC;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM;

EID: 77954599573     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr900914t     Document Type: Article

References (113)

1. Bonner, J. T. The Cellular Slime Molds, 2nd ed.; Princeton University Press: Princeton, NJ, 1967.
2. Kessin, R. H. Dictyostelium-Evolution, Cell Biology, and the Development of Multicellularity; Cambridge University Press: Cambridge, U.K., 2001.
3. Escalante, R.; Vicente, J. J. Dictyostelium discoideum: a model system for differentiation and patterning. Int. J. Dev. Biol. 2000, 44 (8), 819-835
4. Chubb, J. R.; Insall, R. H. Dictyostelium: an ideal organism for genetic dissection of Ras signalling networks. Biochim. Biophys. Acta 2001, 1525, 262-271.
5. Betapudi, V.; Shoebotham, K.; Egelhoff, T. T. Generation of double gene disruptions in Dictyostelium discoideum using a single antibiotic marker selection. Biotechniques 2004, 36, 106-112.
6. Eichinger, L.; Pachebat, J. A.; Glockner, G.; Rajandream, M. A.; Sucgang, R.; Berriman, M.; Song, J.; Olsen, R.; Szafranski, K.; Xu, Q.; Tunggal, B.; Kummerfeld, S.; Madera, M.; Konfortov, B. A.; Rivero, F.; Bankier, A. T.; Lehmann, R.; Hamlin, N.; Davies, R.; Gaudet, P.; Fey, P.; Pilcher, K.; Chen, G.; Saunders, D.; Sodergren, E.; Davis, P.; Kerhornou, A.; Nie, X.; Hall, N.; Anjard, C.; Hemphill, L.; Bason, N.; Farbrother, P.; Desany, B.; Just, E.; Morio, T.; Rost, R.; Churcher, C.; Cooper, J.; Haydock, S.; van Driessche, N.; Cronin, A.; Goodhead, I.; Muzny, D.; Mourier, T.; Pain, A.; Lu, M.; Harper, D.; Lindsay, R.; Hauser, H.; James, K.; Quiles, M.; Madan Babu, M.; Saito, T.; Buchrieser, C.; Wardroper, A.; Felder, M.; Thangavelu, M.; Johnson, D.; Knights, A.; Loulseged, H.; Mungall, K.; Oliver, K.; Price, C.; Quail, M. A.; Urushihara, H.; Hernandez, J.; Rabbinowitsch, E.; Steffen, D.; Sanders, M.Ma, J.; Kohara, Y.; Sharp, S.; Simmonds, M.; Spiegler, S.; Tivey, A.; Sugano, S.; White, B.; Walker, D.; Woodward, J.; Winckler, T.; Tanaka, Y.; Shaulsky, G.; Schleicher, M.; Weinstock, G.; Rosenthal, A.; Cox, E. C.; Chisholm, R. L.; Gibbs, R.; Loomis, W. F.; Platzer, M.; Kay, R. R.; Williams, J.; Dear, P. H.; Noegel, A. A.; Barrell, B.; Kuspa, A. The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435, 43-57. (Pubitemid 40655903)
7. Kreppel, L.; Fey, P.; Gaudet, P.; Just, E.; Kibbe, W. A.; Chisholm, R. L.; Kimmel, A. R. dictyBase: a new Dictyostelium discoideum genome database. Nucleic Acids Res. 2004, 1, 332-333.
8. Aubry, L.; Firtel, R. Integration of signaling networks that regulate Dictyostelium differentiation. Annu. Rev. Cell Dev. Biol. 1999, 15, 469-517.
9. Song, Y. H. Drosophila melanogaster: a Model for the Study of DNA Damage Checkpoint Response. Mol. Cells. 2005, 19 (2), 167-179.
10. Sychrova, H. Yeast as a Model Organism to Study Transport and Homeostasis of Alkali Metal Cations. Physiol. Res. 2004, 53 (1), 91-98.
11. Taminato, A.; Bagattini, R.; Gorjao, R.; Chen, G.; Kuspa, A.; Souza, G. M. Role for YakA, cAMP, and Protein Kinase A in Regulation of Stress Responses of Dictyostelium discoideum Cells. Mol. Biol. Cell 2002, 13, 2266-2275.
12. Burlando, B.; Evangelisti, V.; Dondero, F.; Pons, G.; Camakaris, J.; Viarengo, A. Occurrence of Cu-ATPase in Dictyostelium: Possible Role in Resistance to Copper. Biochem. Biophys. Res. Commun. 2002, 291 (3), 476-483.
13. He, Z. L.; Yang, X. E.; Stoffella, P. J. Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 2005, 19, 125-140.
14. Dondero, F.; Jonsson, H.; Rebelo, M.; Pesce, G.; Berti, E.; Pons, G.; Viarengo, A. Cellular responses to environmental contaminants in amoebic cells of the slime mould Dictyostelium discoideum. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2006, 143 (2), 150-157.
15. Fanous, A.; Weiss, W.; Gorg, A.; Jacob, F.; Parlar, H. A proteome analysis of the cadmium and mercury response in Corynebacterium glutamicum. Proteomics 2008, 8, 4976-4986.
16. Silvestre, F.; Dierick, J. F.; Dumont, V.; Dieu, M.; Raes, M.; Devos, P. Differential protein expression profiles in anterior gills of Eriocheir sinensis during acclimation to cadmium. Aquat. Toxicol. 2006, 76 (1), 46-58.
17. Sforzini, S.; Dagnino, A.; Torrielli, S.; Dondero, F.; Fenoglio, S.; Negri, A.; Boatti, L.; Viarengo, A. Use of highly sensitive sublethal stress responses in the social amoeba Dictyostelium discoideum for an assessment of freshwater quality. Sci. Total Environ. 2008, 395 (2-3), 101-108.
18. Gochfeld, M. Cases of mercury exposure, bioavailability, and absorption. Ecotox. Environ. Safe. 2003, 56 (1), 174-179.
19. Tchounwou, P. B.; Ayensu, W. K.; Ninashvili, N.; Sutton, D. Environmental exposure to mercury and its toxicopathologic implications for public health. Environ. Toxicol. 2003, 18 (3), 149-175.
20. Wang, Q.; Kim, D.; Dionysiou, D. D.; Sorial, G. A.; Timberlake, D. Sources and remediation for mercury contamination in aquatic systems-a literature review. Environ. Pollut. 2004, 131, 323-336.
21. Innanen, S. The ratio of anthropogenic to natural mercury release in Ontario: Three emission scenarios. Sci. Total Environ. 1998, 213, 25-32.
22. Bradshaw, R. A.; Burlingame, A. L. From proteins to proteomics. IUBMB Life 2005, 57 (4-5), 267-272.
23. Eichinger, L.; Rivero, F. Dictyostelium discoideum protocols; Humana Press Inc.: Totowa, NJ, 2006; pp 95-109.
24. Yan, J. X.; Tonella, L.; Sanchez, J. C.; Wilkins, M. R.; Packer, N. H.; Gooley, A. A.; Hochstrasser, D. F.; Williams, K. L. The Dictyostelium discoideum proteome-the SWISS-2DPAGE database of the multicellular aggregate (slug). Electrophoresis 1997, 18 (3-4), 491-497.
25. Alexander, S.; Srinivasan, S.; Alexander, H. Proteomics Opens Doors to the Mechanisms of Developmentally Regulated Secretion. Mol. Cell. Proteomics 2003, 2 (11), 1156-1163.
26. Shepard, J. L.; Olsson, B.; Tedengren, M.; Bradley, B. P. Protein expression signatures identified in Mytilus edulis exposed to PCBs, copper and salinity stress. Mar. Env. Res. 2000, 50 (1-5), 337-340.
27. Bradley, B. P.; Shrader, E. A.; Kimmel, D. G.; Meiller, J. C. Protein expression signatures: an application of proteomics. Mar. Env. Res. 2002, 54 (3-5), 373-377.
28. Merrick, B. A.; Bruno, M. E. Genomic and proteomic profiling for biomarkers and signature profiles of toxicity. Curr. Opin. Mol. Ther. 2004, 6, 600-607.
29. Apraiz, I.; Mi, J.; Cristobal, S. Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Mol. Cell. Proteomics 2006, 5 (7), 1274-1285
30. Mi, J.; Apraiz, I.; Cristobal, S. Peroxisomal proteomic approach for protein profiling in blue mussels (Mytilus edulis) exposed to crude oil. Biomarkers 2007, 12 (1), 47-60.
31. Hultberg, B.; Andersson, A.; Isaksson, A. Interaction of metals and thiols in cell damage and glutathione distribution: Potentiation of mercury toxicity by dithiotreitol. Toxicology 2001, 156, 93-100.
32. Ercal, N.; Gurer-Orhan, H.; Aykin-Burns, N. Toxic metal and oxidative stress part I: Mechanisms involved in metal induced oxidative damage. Curr. Top. Med. Chem. 2001, 1, 529-539.
33. Levine, R. L.; Williams, J. A.; Stadtman, E. R.; Shacter, E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994, 233, 346-357
34. Watts, D. J.; Ashworth, J. M. Growth of myxamoebae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem. J. 1970, 119 (2), 171-174.
35. Sussman, M. Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell. Biol. 1987, 28, 9-29.
36. Page, F. C. A new key to freshwater and soil gymnamoebae with instructions for culture; Freshwater Biological Association: Ambleside Cumbria, UK, 1988.
37. Han, Z.; Truong, Q. A.; Park, S.; Breslow, J. L. Two Hsp70 family members expressed in atherosclerotic lesions. Proc. Natl. Acad. Sci. USA 2003, 100, 1256-1261.
38. Isern, J.; Fraser, S. T.; He, Z.; Baron, M. H. The fetal liver is a niche for maturation of primitive erythroid cells. Proc. Natl. Acad. Sci. USA 2008, 105, 6662-6667.
39. Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9, 255-262.
40. Levine, R. L.; Williams, J. A.; Stadtman, E. R.; Shacter, E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994, 233, 346-357.
41. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20 (18), 3551-3567.
42. Shea, J.; Moran, T.; Dehn, P. F. A bioassay for metals utilizing a human cell line. Toxicol. In Vitro 2008, 22 (4), 1025-1031.
43. Wataha, J. C.; Lewis, J. B.; McCloud, V. V.; Shaw, M.; Omata, Y.; Lockwood, P. E.; Messer, R. L.; Hansen, J. M. Effect of mercury(II) on Nrf2, thioredoxin reductase-1 and thioredoxin-1 in human monocytes. Dent. Mater. 2008, 24 (6), 765-772.
44. Gonzalez, P.; Dominique, Y.; Massabuau, J. C.; Boudou, A.; Bourdineaud, J. P. Comparative effects of dietary methylmercury on gene expression in liver, skeletal muscle, and brain of the zebrafish (Danio rerio). Environ. Sci. Technol. 2005, 39 (11), 3972-3980.
45. Franzellitti, S.; Fabbri, E. Differential HSP70 gene expression in the Mediterranean mussel exposed to various stressors. Biochem. Biophys. Res. Commun. 2005, 336 (4), 1157-1163.
46. Franzellitti, S.; Fabbri, E. Cytoprotective responses in the Mediterranean mussel exposed to Hg2+ and CH3Hg+. Biochem. Biophys. Res. Commun. 2006, 351 (3)), 719-725
47. Helmcke, K. J.; Syversen, T.; Miller, D. M., 3rd; Aschner, M. Characterization of the effects of methylmercury on Caenorhabditis elegans. Toxicol. Appl. Pharmacol. 2009, 240, 265-272.
48. Jin, Y. H.; Dunlap, P. E.; McBride, S. J.; Al-Refai, H.; Bushel, P. R.; Freedman, J. H. Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet. 2008, 4 (4), e1000053.
49. Keyvanshokooh, S.; Vaziri, B.; Gharaei, A.; Mahboudi, F.; Esmaili-Sari, A.; Shahriari-Moghadam, M. Proteome modifications of juvenile beluga (Huso huso) brain as an effect of dietary methylmercury. Comp. Biochem. Physiol. D 2009, 4 (4), 243-248.
50. Quig, D. Cysteine metabolism and metal toxicity. Altern. Med. Rev. 1998, 3 (4), 262-270.
51. Stohs, S. J.; Bagchi, D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 1995, 18 (2), 321-336.
52. Zalups, R. K.; Lash, L. H. Interactions between glutathione and mercury in the kidney, liver and blood. In: Toxicology of Metals; Chang, L. W., Ed.; CRC Press: Boca Raton, FL, 1996; pp 145-163.
53. Kidd, P. Glutathione: Systemic protectant against oxidative and free radical damage. Altern. Med. Rev. 1997, 2, 155-176.
54. Stacey, N. H.; Kappus, H. Cellular toxicity and lipid peroxidation in response to mercury. Toxicol. Appl. Pharmacol. 1982, 63 (1), 29-35. (Pubitemid 12133337)
55. Costa, V.; Moradas-Ferreira, P. Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol. Aspects Med. 2001, 22 (4-5), 217-246.
56. Bossy-Wetzel, E.; Newmeyer, D. D.; Green, D. R. Mitochondrial cytochrome C release in apoptosis occurs upstream of DEVDspecific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 1998, 17 (1), 37-49.
57. Roisin-Bouffay, C.; Luciani, M. F.; Klein, G.; Levraud, J. P.; Adam, M.; Golstein, P. Developmental cell death in Dictyostelium does not require paracaspase. J. Biol. Chem. 2004, 279 (12), 11489-11494.
58. Hayes, J. D.; McLellan, L. I. Glutathione and glutathionedependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic. Res. 1999, 31 (4), 273-300.
59. Sheehan, D.; Meade, G.; Foley, V. M.; Dowd, C. A. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 2001, 360 (1), 1-16.
60. Salinas, A. E.; Wong, M. G. Glutathione S-transferases-a review. Curr. Med. Chem. 1999, 6 (4), 279-309.
61. Leiers, B.; Kampkotter, A.; Grevelding, C. G.; Link, C. D.; Johnson, T. E.; Henkle-Dührsen, K. A stress-responsive glutathione Stransferase confers resistance to oxidative stress in Caenorhabditis elegans. Free Radic. Biol. Med. 2003, 34 (11), 1405-1415.
62. Xie, C.; Lovell, M. A.; Xiong, S.; Kindy, M. S.; Guo, J.; Xie, J.; Amaranth, V.; Montine, T. J.; Markesbery, W. R. Expression of glutathione-S-transferase isozyme in the SY5Y neuroblastoma cell line increases resistance to oxidative stress. Free Radic. Biol. Med. 2001, 31 (1), 73-81.
63. Toba, G.; Aigaki, T. Disruption of the microsomal glutathione S-transferase-like gene reduces life span of Drosophila melanogaster. Gene 2000, 253 (2), 179-187.
64. Westwater, J.; McLaren, N. F.; Dormer, U. H.; Jamieson, J. The adaptive response of Saccharomyces cerevisiae to mercury exposure. Yeast 2002, 19, 233-239.
65. Hansen, J. M.; Zhang, H.; Jones, D. P. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic. Biol. Med. 2006, 40 (1), 138-145, Epub 2005 Oct 19.
66. Arabi, M.; Alaeddini, M. A. Metal-ion-mediated oxidative stress in the gill homogenate of rainbow trout (Oncorhynchus mykiss): antioxidant potential of manganese, selenium, and albumin. Biol. Trace Elem. Res. 2005, 108 (1-3), 155-168
67. Bando, I.; Sanchez Reus, M. I.; Andres, D.; Cascales, M. Endogenous antioxidant defence system in rat liver following mercury chloride oral intoxication. J. Biol. Mol. Toxicol. 2005, 19 (3), 154-161.
68. Shull, S.; Heintz, N. H.; Periasamy, M.; Manohar, M.; Janssen, Y. M.; Marsh, J. P.; Mossman, B. T. Differential regulation of antioxidant enzymes in response to oxidants. J. Biol. Chem. 1991, 266 (36), 24398-24403.
69. Powis, G.; Montfort, W. R. Properties and biological activities of thioredoxins. Annu. Rev. Pharmacol. Toxicol. 2001, 41, 261-295. (Pubitemid 32385890)
70. Yoshida, M.; Sendai, Y.; Sakuragi, N.; Hotta, Y. Analysis of a mod B mutant in Dictyostelium discoideum using mRNA differential display. Plant Cell Physiol. 2000, 41 (2), 239-243.
71. Marchi, B.; Burlando, B.; Moore, M. N.; Viarengo, A. Mercuryand copper-induced lysosomal membrane destabilisation depends on [Ca2+]i dependent phospholipase A2 activation. Aquat. Toxicol. 2004, 66, 197-204.
72. Burlando, B.; Marchi, B.; Panfoli, I.; Viarengo, A. Essential role of Ca2+-dependent phospholipase A2 in estradiol-induced lysosome activation. Am. J. Physiol. Cell Ph. 2002, 283, 1461-1468.
73. Tan, X. X.; Tang, C.; Castoldi, A. F.; Manzo, L.; Costa, L. G. Effects of inorganic and organic mercury on intracellular calcium levels in rat T lymphocytes. J. Toxicol. Environ. Health. 1993, 38 (2), 159-170.
74. Burlando, B.; Bonomo, M.; Fabbri, E.; Dondero, F.; Viarengo, A. Hg2+ signaling in trout hepatoma (RTH-149) cells: involvement of Ca2+-induced Ca2+ release. Cell Calcium 2003, 34 (3), 285-293.
75. Sirois, J. E.; Atchison, W. D. Effects of mercurials on ligand-and voltage-gated ion channels: a review. Neurotoxicology 1996, 17 (1), 63-84.
76. Ambudkar, I. S.; Smith, M. W.; Phelps, P. C.; Regec, A. L.; Trump, B. F. Extracellular Ca2+-dependent elevation in cytosolic Ca2+ potentiates HgCl2-induced renal proximal tubular cell damage. Toxicol. Ind. Health 1988, 4 (1), 107-123.
77. Reed, C. H. Diagnostic applications of cystatin C. Br. J. Biomed. Sci. 2000, 57 (4), 323-329.
78. El-Halawany, M. S.; Ohkouchi, S.; Shibata, H.; Hitomi, K.; Maki, M. Identification of cysteine protease inhibitors that belong to cystatin family 1 in the cellular slime mold Dictyostelium discoideum. Biol. Chem. 2004, 385, 547-550, DOI: 10.1515/BC.2004.065. (Pubitemid 38967784)
79. Ramagopal, S.; Ennis, H. L. Studies on ribosomal proteins in the cellular slime mold Dictyostelium discoideum. Resolution, nomenclature and molecular weights of proteins in the 40-S and 60-S ribosomal subunits. Eur. J. Biochem. 1980, 105 (2), 245-258.
80. Becker, B.; Holtgrefe, S.; Jung, S.; Wunrau, C.; Kandlbinder, A.; Baier, M.; Dietz, K. J.; Backhausen, J. E.; Scheibe, R. Influence of the photoperiod on redox regulation and stress responses in Arabidopsis thaliana, L. (Heynh.) plants under long-and shortday conditions. Planta 2006, 224, 380-393.
81. Bohler, S.; Bagard, M.; Oufir, M.; Planchon, S.; Hoffmann, L.; Jolivet, Y.; Hausman, J. F.; Dizengremel, P.; Renaut, J. A DIGE analysis of developing poplar leaves subjected to ozone reveals major changes in carbon metabolism. Proteomics 2007, 7, 1584-1599.
82. Chen, S.; Smith, D. F. Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J. Biol. Chem. 1998, 273, 35194-35200.
83. Hartwig, A. Zinc finger proteins as potential targets for toxic metal ions: differential effects on structure and function. Antioxid. Redox Signal. 2001, 3 (4), 625-634.
84. Casadevall, M.; Sarkar, B. Effect of redox conditions on the DNAbinding efficiency of the retinoic acid receptor zinc-finger. J. Inorg. Biochem. 1998, 71 (3-4), 147-152.
85. Moore, M. N.; Viarengo, A. Lysosomal membrane fragility and catabolism of cytosolic proteins: evidence for a direct relationship. Cell. Mol. Life Sci. 1987, 43 (3), 320-323.
86. Vernile, P.; Fornelli, F.; Bari, G.; Spagnuolo, M.; Minervini, F.; de Lillo, E.; Ruggiero, P. Bioavailability and toxicity of pentachlorophenol in contaminated soil evaluated on coelomocytes of Eisenia andrei (Annelida: Lumbricidae). Toxicol. In Vitro 2007, 21 (2), 302-307.
87. Viarengo, A.; Lowe, D.; Bolognesi, C.; Fabbri, E.; Koehler, A. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2007, 146 (3), 281-300, Epub 2007 May 3
88. Mart́nez-Gómez, C.; Benedicto, J.; Campillo, J. A.; Moore, M. Application and evaluation of the neutral red retention (NRR) assay for lysosomal stability in mussel populations along the Iberian Mediterranean coast. J. Environ. Monit. 2008, 10 (4), 490-499.
89. Oshiro, S.; Nozawa, K.; Hori, M.; Zhang, C.; Hashimoto, Y.; Kitajima, S.; Kawamura, K. Modulation of Iron Regulatory Protein-1 by Various Metals. Biochem. Biophys. Res. Commun. 2002, 290 (1), 213-218.
90. Kondoh, H.; Lleonart, M. E.; Bernard, D.; Gil, J. Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization. Histol. Histopathol. 2007, 22 (1-3), 85-90.
91. Alex, D.; Bach, T. J.; Chye, M.-L. Expression of Brassica juncea 3-hydroxy-3-methylglutaryl CoA synthase is developmentally regulated and stress-responsive. Plant J. 2000, 22 (5), 415-426.
92. Markovitz, P. J.; Chuang, D. T.; Cox, R. P. Familial Hyperlysinemias: Purification and Characterization of the Bifunctional Aminoadipic Semialdehyde Synthase with Lysine-Ketoglutarate Reductase and Saccharopine Dehydrogenase Activities. J. Biol. Chem. 1984, 259 (19), 11643-11646.
93. Prudova, A.; Bauman, Z.; Braun, A.; Vitvitsky, V.; Lu, S. C.; Banerjee, R. S-adenosylmethionine stabilizes cystathionine-synthase and modulates redox capacity. Proc Natl. Acad. Sci. USA 2006, 103 (17), 6489-6494.
94. Mizunuma, M.; Miyamura, K.; Hirata, D.; Yokoyama, H.; Miyakawa, T. Involvement of S-adenosylmethionine in G1 cell-cycle regulation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2004, 101, 6086-6091.
95. Aragão, K. S.; Satre, M; Imberty, A; Varrot, A. Structure determination of Discoidin II from Dictyostelium discoideum and carbohydrate binding properties of the lectin domain. Proteins 2008, 73 (1), 43-52.
96. Blusch, J.; Alexander, S.; Nellen, W. Multiple signal transduction pathways regulate discoidin I gene expression in Dictyostelium discoideum. Differentiation 1995, 58 (4), 253-260.
97. Sutherland, E. W. Activation of phosphoglucomutase by metalbinding agents. J. Biol. Chem. 1949, 180 (3), 1279-1284.
98. Ohsawa, I.; Nishimaki, K.; Yasuda, C.; Kamino, K.; Ohta, S. Deficiency in a mitochondrial aldehyde dehydrogenase increases vulnerability to oxidative stress in PC12 cells. J. Neurochem. 2003, 84, 1110-1117.
99. Toda, T.; Nakamura, M.; Morisawa, H.; Hirota, M. Proteomic identification of oxidative-stress-reporting biomarkers differentially secreted from human neuroblastoma SH-SY5Y cells. J. Electrophoresis 2007, 51 (3-4), 21-26.
100. Zhang, B.; Zhang, Y.; Dagher, M. C.; Shacter, E. Rho GDP dissociation inhibitor protects cancer cells against drug-induced apoptosis. Cancer Res. 2005, 65 (14), 6054-6062.
101. Custodis, F.; Eberl, M.; Kilter, H.; Böhm, M.; Laufs, U. Association of RhoGDIalpha with Rac1 GTPase mediates free radical production during myocardial hypertrophy. Cardiovasc. Res. 2006, 71 (2), 342-351.
102. Kil, I. S.; Shin, S. W.; Yeo, H. S.; Lee, Y. S.; Park, J. W. Mitochondrial NADP+-Dependent Isocitrate Dehydrogenase Protects Cadmium-Induced Apoptosis. Mol. Pharmacol. 2006, 70, 1053-1061.
103. Meany, D. L.; Xie, H.; Thompson, L. V.; Arriaga, E. A.; Griffin, T. J. Identification of carbonylated proteins from enriched rat skeletal muscle mitochondria using affinity chromatography-stable isotope labeling and tandem mass spectrometry. Proteomics 2007, 7, 1150-1163.
104. Holtgrefe, S.; Gohlke, J.; Starmann, J.; Druce, S.; Klocke, S.; Altmann, B.; Wojtera, J.; Lindermayr, C.; Scheibe, R. Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiol. Plant. 2008, 133, 211-228.
105. Nystrom, T. Translational fidelity, protein oxidation, and senescence: lessons from bacteria. Ageing Res. Rev. 2002, 1, 693-703.
106. Shenton, D.; Grant, C. M. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem. J. 2003, 374, 513-519.
107. Shanmuganathan, A.; Avery, S. V.; Willetts, S. A.; Houghton, J. E. Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway. FEBS Lett. 2004, 556 (1-3), 253-259.
108. Gonzalez, C. F.; Ackerley, D. F.; Lynch, S. V.; Matin, A. ChrR, a Soluble Quinone Reductase of Pseudomonas putida That Defends against H2O2. Biol. Chem. 2005, 280 (24), 22590-22595.
109. Men, L.; Wang, Y. The Oxidation of Yeast Alcohol Dehydrogenase-1 by Hydrogen Peroxide in Vitro. J. Proteome Res. 2007, 6, 216-225.
110. Dong, Z.; Wolfer, D. P.; Lipp, H. P.; Büeler, H. Hsp70 gene transfer by adeno-associated virus inhibits MPTP-induced nigrostriatal degeneration in the mouse model of Parkinson disease. Mol Ther. 2005, 11 (1), 80-88.
111. Sánchez-Reus, I.; Bando, I.; Andrés, D.; Cascales, M. Relationship between expression of HSP70 and metallothionein and oxidative stress during mercury chloride induced acute liver injury in rats. J. Biochem. Mol. Toxicol. 2003, 17 (3), 161-168.
112. Wolf, M. B.; Baynes, J. W. Cadmium and mercury cause an oxidative stress-induced endothelial dysfunction. BioMetals 2007, 20 (1), 73-81.
113. Campostrini, N.; Areces, L. B.; Rappsilber, J.; Pietrogrande, M. C.; Dondi, F.; Pastorino, F.; Ponzoni, M.; Righetti, G. Spot overlapping in two-dimensional maps: a serious problem ignored for much too long. Proteomics 2005, 5 (9), 2385-2395.