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Journal of Oceanology and Limnology

, Volume 37, Issue 2, pp 685–693 | Cite as

Proteomic responses induced by metal pollutions in oysters Crassostrea sikamea

  • Zhen Lu
  • Xiujuan Shan
  • Chenglong JiEmail author
  • Jianmin Zhao
  • Huifeng Wu
Biology
  • 15 Downloads

Abstract

There exist severe metal pollutions along the Jiulongjiang estuary in South China. In order to unravel the biological effects caused by metal pollutions, proteomic responses were investigated by two-dimensional electrophoresis-based proteomics in oysters Crassostrea sikamea from metal pollution sites, Jinshan (JS) and Baijiao (BJ), and a relatively clean site, Jiuzhen (JZ), along the Jiulongjiang estuary. Results indicated that metal pollutions mainly induced cellular injuries, oxidative and immune stresses, and disturbed ion homeostasis in oysters C. sikamea from both JS and BJ sites via differential pathways. Furthermore, metal pollution enhanced transcriptional initiation in oysters from JS site. In addition, the Cu and Fe pollution might be indicated by the 78 kDa glucose regulated protein and ferritin GF1 in oysters C. sikamea, respectively. The study confirms that proteomics is a promising approach to characterize the underlying mechanisms of responses to metal pollution in oysters.

Keyword

metal pollution Crassostrea sikamea biological effect proteomics 

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References

  1. Bertin G, Averbeck D. 2006. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie, 88 (11): 1 549–1 559.CrossRefGoogle Scholar
  2. Campos A, Tedesco S, Vasconcelos V, Cristobal S. 2012. Proteomic research in bivalves: towards the identification of molecular markers of aquatic pollution. J. Proteomics, 75 (14): 4 346–4 359.CrossRefGoogle Scholar
  3. Capková M, Houštek J, Hansíková H, Hainer V, Kunešová M, Zeman J. 2002. Activities of cytochrome c oxidase and citrate synthase in lymphocytes of obese and normalweight subjects. Int. J. Obes., 26 (8): 1 110–1 117.CrossRefGoogle Scholar
  4. Cappello T, Mauceri A, Corsaro C, Maisano M, Parrino V, Lo Paro G, Messina G, Fasulo S. 2013. Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR–based metabolomics. Mar. Pollut. Bull et., 77 (1–2): 132–139.CrossRefGoogle Scholar
  5. Cecconi I, Scaloni A, Rastelli G, Moroni M, Vilardo P G, Costantino L, Cappiello M, Garland D, Carper D, Petrash J M, Del Corso A, Mura U. 2002. Oxidative modification of aldose reductase induced by copper ion. Definition of the metal–protein interaction mechanism. J. Biol. Chem., 277 (44): 42 017–42 027.Google Scholar
  6. Dorts J, Kestemont P, Dieu M, Raes M, Silvestre F. 2011. Proteomic response to sublethal cadmium exposure in a sentinel fish species, Cottus gobio. J. Proteome Res., 10 (2): 470–478.CrossRefGoogle Scholar
  7. Durand J P, Goudard F, Pieri J, Escoubas J M, Schreiber N, Cadoret J P. 2004. Crassostrea gigas ferritin: cDNA sequence analysis for two heavy chain type subunits and protein purification. Gene, 338 (2): 187–195.CrossRefGoogle Scholar
  8. Esperanza M, Seoane M, Rioboo C, Herrero C, Cid Á. 2015. Chlamydomonas reinhardtii cells adjust the metabolism to maintain viability in response to atrazine stress. Aquat. Toxicol., 165: 64–72.CrossRefGoogle Scholar
  9. Exton J H. 2002. Regulation of phospholipase D. FEBS Lett., 531 (1): 58–61.CrossRefGoogle Scholar
  10. Fontaine J M, Rest J S, Welsh M J, Benndorf R. 2003. The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins. Cell Stress Chaperon., 8 (1): 62–69.CrossRefGoogle Scholar
  11. Freedman R B, Hirst T R, Tuite M F. 1994. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci., 19 (8): 331–336.CrossRefGoogle Scholar
  12. Fujinoki M, Ueda M, Inoue T, Yasukawa N, Inoue R, Ishimoda–Takagi T. 2006. Heterogeneity and tissue specificity of tropomyosin isoforms from four species of bivalves. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 143 (4): 500–506.CrossRefGoogle Scholar
  13. Gao Y P, Gillen C M, Wheatly M G. 2006. Molecular characterization of the sarcoplasmic calcium–binding protein (SCP) from crayfish Procambarus clarki i. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 144 (4): 478–487.CrossRefGoogle Scholar
  14. Geysens S, Pakula T, Uusitalo J, Dewerte I, Penttilä M, Contreras R. 2005. Cloning and characterization of the glucosidase II alpha subunit gene of Trichoderma reesei: a frameshift mutation results in the aberrant glycosylation profile of the hypercellulolytic strain Rut–C30. Appl. Environ. Microbiol., 71 (6): 2 910–2 924.CrossRefGoogle Scholar
  15. Giffard R G, Weeds A G, Spudich J A. 1984. Ca 2+–dependent binding of severin to actin: a one–to–one complex is formed. J. Cell Biol., 98 (5): 1 796–1 803.CrossRefGoogle Scholar
  16. Goldberg E D, Koide M, Hodge V, Flegal A R, Martin J. 1983. U. S. mussel watch: 1977–1978 results on trace metals and radionuclides. Est. Coast. Shelf Sci., 16 (1): 69–93.CrossRefGoogle Scholar
  17. Hartmann H, Noegel A A, Eckerskorn C, Rapp S, Schleicher M. 1989. Ca 2+–independent F–actin capping proteins. Cap 32/34, a capping protein from Dictyostelium discoideum, does not share sequence homologies with known actinbinding proteins. J. Biol. Chem., 264 (21): 12 639–12 647.Google Scholar
  18. Hines A, Oladiran G S, Bignell J P, Stentiford G D, Viant M R. 2007. Direct sampling of organisms from the field and knowledge of their phenotype: key recommendations for environmental metabolomics. Environ. Sci. Technol., 41 (9): 3 375–3 381.CrossRefGoogle Scholar
  19. Ji C L, Wang Q, Wu H F, Tan Q G, Wang W X. 2016. A metabolomic study on the biological effects of metal pollutions in oysters Crassostrea sikamea. Mar. Pollut. Bullet., 102 (1): 216–222.CrossRefGoogle Scholar
  20. Jiang W D, Liu Y, Hu K, Jiang J, Li S H, Feng L, Zhou X Q. 2014. Copper exposure induces oxidative injury, disturbs the antioxidant system and changes the Nrf2/ARE (CuZnSOD) signaling in the fish brain: protective effects of myo–inositol. Aquat. Toxicol., 155: 301–333.CrossRefGoogle Scholar
  21. Katayama H, Nagasu T, Oda Y. 2001. Improvement of in–gel digestion protocol for peptide mass fingerprinting by matrix–assisted laser desorption/ionization time–of–flight mass spectrometry. Rapid Commun. Mass Spectrom., 15 (16): 1 416–1 421.CrossRefGoogle Scholar
  22. Kim S H, Jung M Y, Lee Y M. 2011. Effect of heavy metals on the antioxidant enzymes in the marine ciliate Euplotes crassus. Toxicol. Environ. Health Sci., 3 (4): 213–219.CrossRefGoogle Scholar
  23. Knigge T, Monsinjon T. Andersen O K. 2004. Surfaceenhanced 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 (9): 2 722–2 727.CrossRefGoogle Scholar
  24. Krumschnabel G, Manzl C, Berger C, Hofer B. 2005. Oxidative stress, mitochondrial permeability transition, and cell death in Cu–exposed trout hepatocytes. Toxicol. Appl. Pharmacol., 209 (1): 62–73.CrossRefGoogle Scholar
  25. Kurzik–Dumke U, Lohmann E. 1995. Sequence of the new Drosophila melanogaster small heat–shock–related gene, lethal ( 2 ) essential for life [ l ( 2 ) efl], at locus 59F4,5. Gene, 154 (2): 171–175.CrossRefGoogle Scholar
  26. Lin C Q, Yu R L, Hu G R, Yang Q L, Wang X M. 2016. Contamination and isotopic composition of Pb and Sr in offshore surface sediments from Jiulong River, Southeast China. Environ. Pollut., 218: 644–650.CrossRefGoogle Scholar
  27. Liu F J, Wang W–X. 2012. Proteome pattern in oysters as a diagnostic tool for metal pollution. J. Hazard. Mat er., 239–240: 241–248.CrossRefGoogle Scholar
  28. Luo L Z, Ke C H, Guo X Y, Shi B, Huang M Q. 2014. Metal accumulation and differentially expressed proteins in gill of oyster ( Crassostrea hongkongensis ) exposed to longterm heavy metal–contaminated estuary. Fish Shellfish Immunol., 38 (2): 318–329.CrossRefGoogle Scholar
  29. Magalhães G S, Lopes–Ferreira M, Junqueira–de–Azevedo I L M, Spencer P J, Araújo M S, Portaro F C V, Ma L, Valente R H, Juliano L, Fox J W, Ho P L, Moura–da–Silva A M. 2005. Natterins, a new class of proteins with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie, 87 (8): 687–699.CrossRefGoogle Scholar
  30. Monsinjon T, Knigge T. 2007. Proteomic applications in ecotoxicology. Proteomics, 7 (16): 2 997–3 009.CrossRefGoogle Scholar
  31. Muslin A J, Tanner J W, Allen P M, Shaw A S. 1996. Interaction of 14–3–3 with signaling proteins is mediated by the recognition of phosphoserine. Cell, 84 (6): 889–897.CrossRefGoogle Scholar
  32. Puerto M, Campos A, Prieto A, Cameán A, de Almeida A M, Coelho A V, Vasconcelos V. 2011. Differential protein expression in two bivalve species; Mytilus galloprovincialis and Corbicula fluminea; exposed to Cylindrospermopsis raciborskii cells. Aquat. Toxicol., 101 (1): 109–116.CrossRefGoogle Scholar
  33. Rank J, Lehtonen K K, Strand J, Laursen M. 2007. DNA damage, acetylcholinesterase activity and lysosomal stability in native and transplanted mussels ( Mytilus edulis ) in areas close to coastal chemical dumping sites in Denmark. Aquat. Toxicol., 84 (1): 50–61.CrossRefGoogle Scholar
  34. Sahoo S K, Kim T, Kang G B, Lee J G, Eom S H, Kim DH. 2009. Characterization of calumenin–SERCA2 interaction in mouse cardiac sarcoplasmic reticulum. J. Biol. Chem., 284 (45): 31 109–31 121.CrossRefGoogle Scholar
  35. Saito T, Yamasaki S. 2003. Negative feedback of T cell activation through inhibitory adapters and costimulatory receptors. Immunol. Rev., 192 (1): 143–160.CrossRefGoogle Scholar
  36. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins from silver–stained polyacrylamide gels. Anal. Chem., 68 (5): 850–858.CrossRefGoogle Scholar
  37. Stiburek L, Hansikova H, Tesarova M, Cerna L, Zeman J. 2006. Biogenesis of eukaryotic cytochrome c oxidase. Physiol. Res., 55 (S2): S27–S41.Google Scholar
  38. Tan Q G, Wang Y, Wang W X. 2015. Speciation of Cu and Zn in two colored oyster species determined by X–ray absorption spectroscopy. Environ. Sci. Technol., 49 (11): 6 919–6 925.CrossRefGoogle Scholar
  39. Taylor M A, Ross H A, McRae D, Stewart D, Roberts I, Duncan G, Wright F, Millam S, Davies H V. 2000. A potato a–glucosidase gene encodes a glycoproteinprocessing a–glucosidase II–like activity. Demonstration of enzyme activity and effects of down–regulation in transgenic plants. Plant J., 24 (3): 305–316.Google Scholar
  40. Tian L, Wang M H, Li X M, Lam P K S, Wang M F, Wang D Z, Chou H N, Li Y, Chan L L. 2011. Proteomic modification in gills and brains of medaka fish ( Oryzias melastigma ) after exposure to a sodium channel activator neurotoxin. brevetoxin–1. Aquat. Toxicol., 104 (3–4): 211–217.CrossRefGoogle Scholar
  41. Tomanek L. 2014. Proteomics to study adaptations in marine organisms to environmental stress. J. Proteomics, 105: 92–106.CrossRefGoogle Scholar
  42. Vidal–Liñán L, Bellas J. 2013. Practical procedures for selected biomarkers in mussels, Mytilus galloprovincialis —implications for marine pollution monitoring. Sci. Total Environ., 461–462: 56–64.CrossRefGoogle Scholar
  43. Wang J Y, Lan P, Gao H M, Zheng L, Li W F, Schmidt W. 2013. Expression changes of ribosomal proteins in phosphate–and iron–deficient Arabidopsis roots predict stress–specific alterations in ribosome composition. BMC Genomics, 14: 783.CrossRefGoogle Scholar
  44. Weng N, Wang W X. 2014. Variations of trace metals in two estuarine environments with contrasting pollution histories. Sci. Total Environ., 485–486: 604–614.CrossRefGoogle Scholar
  45. Wu H F, Ji C L, Wei L, Zhao J M. 2013a. Evaluation of protein extraction protocols for 2DE in marine ecotoxicoproteomics. Proteomics, 13 (21): 3 205–3 210.CrossRefGoogle Scholar
  46. Wu H F, Liu X L, Zhang X Y, Ji C L, Zhao J M, Yu J B. 2013b. Proteomic and metabolomic responses of clam Ruditapes philippinarum to arsenic exposure under different salinities. Aquat. Toxicol., 136–137: 91–100.CrossRefGoogle Scholar
  47. Xu L L, Ji C L, Wu H F, Tan Q G, Wang W–X. 2016. A comparative proteomic study on the effects of metal pollution in oysters Crassostrea hongkongensis. Mar. Pollut. Bullet., 112 (1–2): 436–442.CrossRefGoogle Scholar
  48. Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F, Yang P C, Zhang L L, Wang X T, Qi H G, Xiong Z Q, Que H Y, Xie Y L, Holland P W H, Paps J, Zhu Y B, Wu F C, Chen Y X, Wang J F, Peng C F, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z Y, Zhu Q H, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y J, Domazet–Lošo T, Du Y S, Sun X Q, Zhang S D, Liu B H, Cheng P Z, Jiang X T, Li J, Fan D D, Wang W, Fu W J, Wang T, Wang B, Zhang J B, Peng Z Y, Li Y X, Li N, Wang J P, Chen M S, He Y, Tan F J, Song X R, Zheng Q M, Huang R L, Yang H L, Du X D, Chen L, Yang M, Gaffney P M, Wang S, Luo L H, She Z C, Ming Y, Huang W, Zhang S, Huang B Y, Zhang Y, Qu T, Ni P X, Miao G Y, Wang J Y, Wang Q, Steinberg C E, Wang H Y, Li N, Qian L M, Zhang G J, Li Y R, Yang H M, Liu X, Wang J, Yin Y, Wang J. 2012a. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490 (7418): 49–54.CrossRefGoogle Scholar
  49. Zhang L B, Gan J L, Ke C L, Liu X L, Zhao J M, You L P, Yu J B, Wu H F. 2012b. Identification and expression profile of a new cytochrome P450 isoform (CYP414A1) in the hepatopancreas of Venerupis (Ruditapes) philippinarum exposed to benzo[a]pyrene, cadmium and copper. Environ. Toxicol. Pharmacol., 33 (1): 85–91.CrossRefGoogle Scholar
  50. Zhang W, Wei Q. 2011. Calcineurin stimulates the expression of inflammatory factors in RAW 264.7 cells by interacting with proteasome subunit alpha type 6. Biochem. Biophys. Res. Commun., 407 (4): 668–673.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zhen Lu
    • 1
    • 3
  • Xiujuan Shan
    • 2
    • 4
  • Chenglong Ji
    • 1
    • 2
    Email author
  • Jianmin Zhao
    • 1
  • Huifeng Wu
    • 1
    • 2
  1. 1.Key Laboratory of Coastal Zone Environmental Processes, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences (CAS)Shandong Provincial Key Laboratory of Coastal Zone Environmental ProcessesYICCAS, YantaiChina
  2. 2.Function Laboratory for Marine Fisheries Science and Food Production ProcessesQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture; Shandong Provincial Key Laboratory of Fishery Resources and Ecological Environment, Yellow Sea Fisheries Research InstituteChinese Academy of Fishery SciencesQingdaoChina

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