Oxidative stress and bivalves: A proteomic approach

Invertebrate Survival Journal

Volumn 5, Issue 2, 2008, Pages 110-123

  Sheehan, David ^a   McDonagh, B ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Bivalve; Clam; Ecotoxicology; Mussel; Oxidative stress

Indexed keywords

EID: 77957076445     PISSN: None     EISSN: 1824307X     Source Type: Journal    
DOI: None     Document Type: Review

References (116)

1. Aebersold R, Mann M. Mass spectrometry-based proteomics. Nature 422: 198-207, 2003.
2. Altieri AH. Inducible variation in hypoxia tolerance across the intertidal subtidal distribution of the blue mussel Mytilus edulis. Mar. Ecol. Prog. Ser. 325: 295-300, 2006.
3. Apraiz I, Mi J, Cristobal S. Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Mol. Cell Proteomics 5: 1274-1285, 2006.
4. Baty JW, Hampton MB, Winterbourn CC. Proteomic detection of hydrogen peroxide-sensitive thiol proteins in Jurkat cells. Biochem. J. 389: 785-95, 2005.
5. Bayne BL (ed.). Marine Mussels: Their Ecology and Physiology. Cambridge University Press, Cambridge, UK, 1976.
6. Bayne BL. Assessing effects of marine pollution. Nature 280: 14, 1979.
7. Biswas S, Chida AS, Rahnam I. Redox modifications of protein thiols: Emerging roles in cell signaling. Biochem. Pharmacol. 71: 551-564, 2006.
8. Buckley BA, Owen ME, Hofmann, GE. Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels genus (Mytilus) changes as a function of thermal history. J. Exp. Biol. 204: 3571-3579, 2001.
9. Bjørnstad A, Larse BK, Skadsheim A, Jones MB, Andersen OK. The potential of ecotoxicoproteomics in environmental monitoring: biomarker profiling in mussel plasma using proteinChip array technology. J. Toxicol. Environ. Health A 69: 77-96, 2006.
10. Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: A practical approach. Sci. Total Environ. 247: 295-311, 2000.
11. Cheung CCC, Zheng GJ, Li AMY, Richardson BJ, Lam PKS. Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquat. Toxicol. 52: 189-203, 2001.
12. Chora S, McDonagh B, Sheehan D, Starita-Geribaldi M, Roméo M, Bebianno MJ. Ubiquitination and carbonylation as markers of oxidative-stress in Ruditapes decussatus. Mar. Environ. Res. 66: 95-97, 2008.
13. Corzett TH, Fodor IK, Choi MW, Walsworth VL, Chromy BA, Turteltaub KW, et al. Statistical analysis of the experimental variation in the proteomic characterization of human plasma by two-dimensional difference gel electrophoresis. J. Proteome Res. 5: 2611-2619, 2006.
14. Cretich M, Damin F, Pirri G, Chiari M. Protein and peptide arrays: Recent trends and new directions. Biomol. Eng. 23: 77-88, 2006.
15. Davies M J. The oxidative environment and protein damage. Biochim. Biophys. Acta 1703: 93-109, 2005.
16. Depledge MH, Galloway TS. Healthy animals, healthy ecosystems. Front. Ecol. Environ. 3: 252-258, 2005.
17. Domon B, Aebersold R. Mass spectrometry and protein analysis. Science 312: 212-217, 2006a
18. Domon B, Aebersold R. Challenges and opportunities in proteomics data analysis. Mol. Cell Proteomics 5: 1921-1926, 2006b.
19. Dowling VA, Sheehan D. Proteomics as a route to identification of toxicity targets in ecotoxicology. Proteomics 6: 5597-5604, 2006.
20. Dowling V, Hoarau PC, Romeo M, O'Halloran J, van Pelt F, O'Brien N, et al. Protein carbonylation and heat shock response in Ruditapes decussatus following p, p'-dichlorodiphenyldichloroethylene (DDE) exposure: a proteomic approach reveals that DDE causes oxidative stress. Aquat. Toxicol. 77: 11-18, 2006.
21. Dowling V, McDonagh B, Cotter EM, O'Brien N, van Pelt F, O'Halloran J, et al. Two-dimensional electrophoresis analysis of glutathione affinity-selected proteins from the clam Tapes semidecussatus: evidence for tissue-specific expression of redox proteins. Comp. Biochem. Physiol. 1D: 267-272, 2006.
22. Downs CA, Shigenaka G, Fauth JE, Robinson CE, Huang A. Cellular physiological assessment of bivalves after chronic exposure to spilled Exxon Valdez crude oil using a novel molecular diagnostic biotechnology. Environ. Sci. Technol. 36: 2987-2993, 2002.
23. Dupont S, Wilson K, Obst M, Skold H, Nakano H, Thorndyke MC. Marine ecological genomics: When genomics meets marine ecology. Mar. Ecol. Prog. Ser. 332: 257-273, 2007.
24. Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. Electrospray ionization - principles and practice. Mass Spectrometry Rev. 9: 37-70, 1990.
25. Fitzpatrick PJ, Sheehan D, Livingstone, DR. Studies on isoenzymes of glutathione S-transferase in digestive gland of Mytilus galloprovincialis with exposure to pollution. Mar. Environ. Res. 39: 241-244, 1995.
26. Gade G, Thiermann J, Markowsky D, Rabus R. Evaluation of two-dimensional difference gel electrophoresis for protein profiling. J. Mol. Microbiol. Biotechnol. 5: 240-251, 2003.
27. Galloway TS. Biomarkers in environmental and human health risk assessment. Mar. Pollut. Bull. 53: 606-613, 2006.
28. Goldberg ED, Bertine KK. Beyond the mussel watch - new directions for monitoring marine pollution. Sci. Total Environ. 247: 165-174, 2000.
29. Görg A, Obermaier C, Boguth G, Harder A, Scheibe B, Wildgruber R, et al. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21: 1037-1053, 2000.
30. Görg A, Weiss W, Dunn MJ. Current two-dimensional electrophoresis technology for proteomics. Proteomics 4: 3665-3685, 2004.
31. Gould SC, Calloway SB. Clams and brachiopods; ships that pass in the night. Palaeobiology 6: 383-396, 1980.
32. Grace PA. Ischemia-reperfusion injury. Brit. J. Surgery 81: 637-647, 1994.
33. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. Fourth Edition, Oxford University Press, Oxford, UK, 2007
34. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D'Agrosa C, et al. A global map of human impact on marine ecosystems. Science 319: 946-948, 2008.
35. Handy RD, Galloway TS, Depledge MH. A proposal for the use of biomarkers for the assessment of chronic pollution and in regulatory toxicology. Ecotoxicology 12: 331-343, 2003.
36. Heijne WHM, Kienhuis AS, van Ommen B, Stierum RH, Groten JP. Systems toxicology: Applications of toxicogenomics, transcriptomics, proteomics and metabolomics in toxicology. Expert Rev. Proteomics 2: 767-780, 2005.
37. Hofmann G, Somero G. Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and hsp70 in the intertidal mussel Mytilus trossulus. J. Exp. Biol. 198: 1509-1518, 1995.
38. Hu A, Tsai PJ, Ho YP. Identification of microbial mixtures by capillary electrophoresis/selective tandem mass spectrometry. Anal. Chem. 77: 1488-1497, 2005.
39. Karp NA, Lilley KS. Design and analysis issues in quantitative proteomics studies. Proteomics S1: 42-50, 2007.
40. Karp NA, Spencer M, Lindsay H, O'Dell K, Lilley KS. Impact of replicate types on proteomic expression analysis. J. Proteome Res. 4: 1867-1871, 2005.
41. Kislinger T, Cox B, Kannan A, Chung C, Hu PZ, Ignatchenko A, et al. Global survey of organ and organelle protein expression in mouse; Combined proteomic and transcriptomic profiling. Cell 125: 173-186, 2006.
42. Knigge T, Monsinjon T, Andersen OK. Surface-enhanced laser desorption/ionization-time of flight-mass spectrometry approach to biomarker discovery in blue mussels (Mytilus edulis) exposed to polyaromatic hydrocarbons and heavy metals under field conditions. Proteomics 4: 2722-2727, 2004.
43. Krause F. Detection and analysis of protein-protein interactions in organellar and prokaryotic proteomes by native blue electrophoresis: (Membrane) protein complexes and supercomplexes. Electrophoresis 27: 2759-2781, 2006.
44. Lee WC, Lee KH. Applications of affinity chromatography in proteomics. Anal. Biochem. 324: 1-10, 2004.
45. Lehtonen KK, Leinio S, Schneider R, Leivuori M. Biomarkers of pollution effects in the bivalves Mytilus edulis and Macoma balthica collected from the southern coast if Finland (Baltic Sea). Mar. Ecol. Prog. Ser. 322: 155-168, 2006.
46. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, et al. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc. Natl. Acad. Sci. USA 105: 8197-8202, 2008.
47. Lesser MP. Oxidative stress in marine environments: Biochemistry and physiological ecology. Ann. Rev. Physiol. 68: 253-278, 2006.
48. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186: 464-78, 1990.
49. Livingstone DR. The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp. Biochem. Physiol. 120A: 43-49, 1998.
50. Lognonne JL. 2D-PAGE analysis - a practical guide to principal critical parameters. Cell. Mol. Biol. 40: 41-55, 1994.
51. López-Barea J, Pueyo C. Mutagen content and metabolic activation of promutagens by mollusks as biomarkers of marine pollution. Mutat. Res. 399: 3-15, 1998.
52. Lutz RA, Kennish MJ. Ecology of deep-sea hydrothermal vent communities; a review. Rev. Geophys. 31: 211-242, 1993.
53. Lyons C, Dowling V, Tedengren M, Gardestrőm, J, Hartl MG, O'Brien N, et al. Variablity of heat shock proteins and glutathione S-transferases in gill and digestive gland of blue mussel, Mytilus edulis. Mar. Environ. Res. 56: 585-597, 2003.
54. Manduzio H, Monsinjon T, Galap C, Leboulanger F, Rocher W. Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat. Toxicol. 70: 83-93, 2004.
55. Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nature Biotechnol. 21: 255-261, 2003.
56. Marques C, Pereira P, Taylor A, Liang JN, Reddy VN, Szweda LI, et al. Ubiquitin-dependent lysosomal degradation of the HNE-modified proteins in lens epithelial cells. FASEB J. 18: 1424-1426, 2004.
57. McDonagh B, Sheehan D. Redox proteomics in the blue mussel Mytilus edulis: carbonylation is not a pre-requisite for ubiquitination in acute free radical-mediated oxidative stress. Aquat. Toxicol. 79: 325-333, 2006.
58. McDonagh B, Tyther R, Sheehan D. Carbonylation and glutathionylation of proteins in the blue mussel Mytilus edulis detected by proteomic analysis and Western blotting: actin as a target for oxidative stress. Aquat. Toxicol. 73: 315-326, 2005.
59. McDonagh B, Tyther R, Sheehan D. 2006. Redox proteomics in the mussel, Mytilus edulis. Mar. Environ. Res. 62: S101-S104.
60. McDonagh B, Sheehan D. Effect of oxidative stress on protein thiols in the blue mussel Mytilus edulis: proteomic identification of target proteins. Proteomics 7: 3395-3403, 2007.
61. McDonagh B, Sheehan D. Effects of oxidative stress on protein thiols and disulphides in Mytilus edulis revealed by proteomics: actin and protein disulphide isomerase are redox targets. Mar. Environ. Res. 66: 193-195, 2008.
62. McDonald WH, Yates JR. Proteomics and biomarker discovery. Dis. Markers 18: 99-105, 2002.
63. McKillen DJ, Chen YA, Chen CM, Jenny MJ, Trent HF, Robalino J, et al. Marine genomics: a clearing house for genomic and transcriptomic data of marine organisms. BMC Genomics 6: 34-39, 2005.
64. Merchant M, Weinberger SR. Recent advancements in surface-enhanced laser desorption/ionization-time of flight-mass spectrometry. Electrophoresis 21: 1164-1177, 2000.
65. Mi J, Apraiz I, Cristobal S. Peroxisomal proteomic approach for protein profiling in blue mussels (Mytilus edulis) exposed to crude oil. Biomarkers 12: 47-60, 2007.
66. Miller AI. Biotic transitions in global marine diversity. Science 281: 1157-1160, 1998.
67. 2+ -dependent mechanisms. Arch. Biochem. Biophys. 270: 478-488, 1989.
68. Monsinjon T, Knigge T. Proteomic applications in ecotoxicology. Proteomics 7: 2997-3009, 2007.
69. Monsinjon T, Andersen OK, Leboulanger F, Knigge T. Data processing and classification analysis of proteomic changes: A case study of oil pollution in the mussel, Mytilus edulis. Proteome Sci. 4: 17, 2006.
70. Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, et al. Effect of aquaculture on world fish supplies. Nature 405: 1017-1024, 2000.
71. Nesatyy VJ, Suter MJF. Proteomics for the analysis of environmental stress responses in organisms. Environ. Sci. Technol. 41: 6891-6900, 2007.
72. Nesvizhskii AI, Vitek O, Aebersold R. Analysis and validation of proteomic data generated by tandem mass spectrometry. Nature Methods 4: 787-797, 2007.
73. Newell, RIE. Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J. Shellfish Res. 23: 51-61, 2004.
74. O'Farrell PH. High resolution 2-dimensional electrophoresis of proteins. J. Biol. Chem. 250: 4007-4021, 1975.
75. Oktyabrsky ON, Smirnova GV. Redox regulation of cellular functions. Biochemistry (Moscow) 72: 132-145, 2007.
76. Palagi PM, Hernandez P, Walther D, Appel RD. Proteome informatics I: bioinformatics tools for processing experimental data. Proteomics 6: 5435-5444, 2006.
77. Pampanin DM, Viarengo A, Garrigues P, Andersen OK. Background for the BEEP Stavanger workshops: Biological effects on marine organisms in two common, large, laboratory experiments and in a field study. Comparison of the value (sensitivity, specificity, etc.) of core and new biomarkers. Aquat. Toxicol., 78, S1-S4, 2006.
78. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2: 43-50, 2003.
79. Poole LB, Nelson KJ. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr. Opin. Chem. Biol. 12: 18-24, 2008.
80. Poon TCW. Opportunities and limitations of SELDI-TOF-MS in biomedical research: practical advices. Expert Rev. Proteomics 4: 51-65, 2007.
81. Powell DW, Merchant ML, Link AJ. Discovery of regulatory molecular events and biomarkers using 2D capillary chromatography and mass spectrometry. Expert Rev. Proteomics 3: 63-74, 2006.
82. Power A, Sheehan D. Seasonal variation in the antioxidant defence systems of gill and digestive glands of the blue mussel, Mytilus edulis. Comp. Biochem. Physiol. 114C: 99-103, 1996.
83. Prevodnik A, Gardeström J, Lilja K, Elfwing T, McDonagh B, Petrović N, et al. Oxidative stress in response to xenobiotics in the blue mussel Mytilus edulis L.: evidence for variation along a natural salinity gradient of the Baltic Sea. Aquat. Toxicol. 82: 63-71, 2007.
84. Rabilloud T A comparison between low background silver diammine and silver-nitrate protein stains. Electrophoresis 13: 429-439, 1992.
85. Regoli F, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S, et al. Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Mar. Environ. Res. 54: 419-423, 2002.
86. Rodríguez-Ariza A, Abril N, Navas JL, Dorado G, López-Barea J, Pueyo C. Metal mutagenicity and biochemical studies on bivalve molluscs from Spanish coasts. Environ. Mol. Mutagen. 19: 112-124, 1992.
87. Rodríguez-Ariza A, Martínez-Lara E, Pascual P, Pedrajas JR, Abril N, Dorado G, et al. Biochemical and genetic indices of marine pollution in the Spanish littoral. Sci. Total Environ. (Suppl. 1): 109-116, 1993.
88. Rodríguez-Ariza A, Rodriguez-Ortega MJ, Marenco JL, Amezcua O, Alhama J, López-Barea J. Uptake and clearance of PCB congeners in Chamaelea gallina: Response of oxidative stress biomarkers. Comp. Biochem. Physiol. 134C: 57-67, 2003.
89. Rodríguez-Ortega MJ, Alhama J, Funes V, Romero-Ruíz A, Rodríguez-Ariza A, López-Barea J. Biochemical biomarkers of pollution in the clam Chamaelea gallina from the South-Spanish littoral. Environ. Toxicol. Chem. 21: 542-549, 2002.
90. Rodriguez-Ortega MJ, Grosvik BE, Rodriguez-Ariza A, Goksoyr A, Lopez-Barea J. Changes in protein expression profiles in bivalve molluscs (Chamaelea gallina) exposed to four model environmental pollutants. Proteomics 3: 1535-1543, 2003.
91. Romero-Ruiz A, Carrascal M, Alhama J, Gómez-Ariza JL, Abian J, López-Barea J. Environmental proteomics studies in clams from the Donaña bank of Guadalquivir Estuary (SW Spain). Proteomics 6 (Suppl 1): S245-S255, 2006.
92. Sanders BM. Stress proteins in aquatic organisms: an environmental perspective. Crit Rev. Toxicol. 23: 49-75, 1993.
93. Sheehan, D. Detection of redox-based modification in two dimensional electrophoresis proteomic separations. Biochem. Biophys. Res. Commun. 349: 455-462, 2006.
94. Sheehan, D. The potential of proteomics for providing new insights into environmental impacts on human health. Rev. Environ. Health 22: 175-194, 2007.
95. Sheehan D, Power A. Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comp. Biochem. Physiol. 123C: 193-199, 1999.
96. Shepard JL, Olsson B, Tedengren M, Bradley BP. Protein expression signatures identified in Mytilus edulis exposed to PCBs, copper and salinity stress. Mar. Environ. Res. 50: 337-340, 2000.
97. Sole M, Livingstone DR. Components of the cytochrome P450-dependent monooxygenase system and 'NADPH-independent benzo[a]pyrene hydroxylase' activity in a wide range of marine invertebrate species. Comp. Biochem. Physiol. 141C: 20-31, 2005.
98. Sole M, Porte C, Biosca X, Mitchelmore CL, Chipman JK, Livingstone DR, et al. Effects of the "Aegean Sea" oil spill on biotransformation enzymes, oxidative stress and DNA-adducts in digestive gland of the mussel (Mytilus edulis L). Comp. Biochem. Physiol. 113C: 257-265, 1996.
99. Spickett CM, Pitt AR, Morrice N, Kolch W. Proteomic analysis of phosphorylation, oxidation and nitrosylation in signal transduction. Biochim. Biophys. Acta 1764: 1823-1841, 2006.
100. Stachowitz M, Riedel B, Zuschin M, Machan R. Oxygen depletion and benthic mortalities: The first in situ experimental approach to documenting an elusive phenomenon. Limnol. Oceanogr. Methods 5: 344-352, 2007.
101. Stadtman ER, Levine RL. Protein oxidation. Ann. NY Acad. Sci. Vol. 899: 191-208, 2000.
102. Steinert SA. DNA damage as a bivalve biomarker. Biomarkers 4: 492-496, 1999.
103. Tanaka K, Waki H, Ido Y, Akita S, Yoshida Y, Yoshida T. Protein and polymer analyses up to m/z 100 000 by laser ionization time-of-flight mass spectrometry. Rapid Commun. Mass Sp. 2: 151-153, 1988.
104. Tanguy A, Bierne N, Saavedra C, Pina B, Bachère E, Kube M, et al. Increasing genomic information in bivalves through new EST collections in four species: development of new genetic markers for environmental studies and genome evolution. Gene 408: 27-36, 2008.
105. Tedesco S, Doyle H, Redmond G, Sheehan D. Gold nanoparticles and oxidative stress in Mytilus edulis. Mar. Environ. Res. 66: 131-133, 2008.
106. Thiede B, Hohenwarter W, Krah A, Mattow J, Schmid M, Schmidt F, et al. Peptide mass fingerprinting. Methods 35: 237-247, 2005.
107. Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Saf. 64:178-189, 2006.
108. Vergani L, Grattarola M, Borghi C, Dondero F, Viarengo A. Fish and molluscan metallothioneins - A structural and functional comparison. FEBS J. 272: 6014-6023, 2005.
109. Viarengo A, Canesi L, Pertica M, Livingstone DR. Seasonal variations in the antioxidant defense systems and lipid peroxidation of the digestive gland of mussels. Comp. Biochem. Physiol. 100C: 187-190, 1991.
110. Widdows J, Shick JM. Physiological response of Mytilus edulis and Cardium edule to aerial exposure. Mar. Biol. 85: 278-286, 1985.
111. Widdows J, Bayne BL, Livingstone DR, Newell RIE, Donkin P. Physiological and biochemical responses of bivalve mollusks to exposure to air. Comp. Biochem. Physiol. 62A: 301-308, 1979.
112. Winston GW. Oxidants and antioxidants in aquatic animals. Comp. Biochem. Physiol. 100C: 173-176, 1991.
113. Winterbourn CC. Reconciling the chemistry and biology of reactive oxygen species. Nature Chem. Biol. 4: 278-286, 2008.
114. Wu X, Edwards N, Tseng CW. Peptide identification via tandem mass spectrometry. Adv. Computers 68: 253-278, 2006.
115. Ying J, Clavreul N, Sethuraman M, Adachi T, Cohen RA. Thiol oxidation in signalling and response to stress: detection and quantification of physiological and pathophysiological thiol modifications. Free Radic. Biol. Med. 43: 1099-1108, 2007.
116. Zhu H, Bilgin M, Snyder M. Proteomics. Annu. Rev. Biochem. 72: 783-812, 2003.