纳米氧化镍颗粒对长牡蛎(Crassostrea gigas)抗氧化防御体系的影响Effects of Nickel Oxide Nanoparticles on Antioxidant Defense System of Crassostrea gigas
张钰昆;巩宁;车程;邵魁双;王迪;林正志;孙野青;
摘要(Abstract):
纳米氧化镍(nNiO)作为一种广泛使用的纳米颗粒,其水生毒理效应研究还很有限。为探索n Ni O对海洋贝类的毒性机制,本研究将长牡蛎(Crassostrea gigas)置于不同浓度(0、1、10、100 mg·L~(-1))的n Ni O中暴露96 h,分别测定鳃和消化腺组织的丙二醛(MDA)含量和超氧化物歧化酶(SOD)、过氧化物酶(POD)以及过氧化氢酶(CAT)活性,并通过实时荧光定量PCR技术测定了鳃和消化腺中应激蛋白HSP70和AOX基因的表达变化。结果显示:在100 mg·L~(-1)n Ni O处理下,2种组织中MDA含量均显著性升高(P<0.01),显示纳米颗粒造成了长牡蛎的脂质过氧化,并可能引起相应的氧化损伤。同时,n Ni O暴露也诱导了长牡蛎抗氧化酶(SOD、CAT和POD)活性的改变。其中,SOD和CAT活性在10 mg·L~(-1)浓度处理组达到最高,而POD活性在1 mg·L~(-1)浓度组即达最高值。在高浓度n Ni O(100 mg·L~(-1))胁迫下,3种抗氧化酶的活性均比低浓度(1和10 mg·L~(-1))处理组降低,表明抗氧化酶的保护作用在较低浓度暴露下更有效;而热激蛋白(hsp70)和交替氧化酶(aox)基因却分别在长牡蛎消化腺和鳃组织中上调表达(P<0.01),并表现出一定的组织差异。说明高浓度纳米颗粒暴露中主要是应激蛋白发挥了作用。本文结果为纳米氧化镍对海洋双壳贝类的毒性机制研究及生态风险评估提供了基础数据。
关键词(KeyWords): 纳米氧化镍;长牡蛎;氧化应激;抗氧化酶;应激蛋白
基金项目(Foundation): 国家重点研发计划资助项目“浒苔着生机理与防控技术(2016YFC1402104)”;; 国家自然科学基金(No.41301560)
作者(Author): 张钰昆;巩宁;车程;邵魁双;王迪;林正志;孙野青;
Email:
DOI:
参考文献(References):
- [1] Gui X, He X, Ma Y, et al. Quantifying the distribution of ceria nanoparticles in cucumber roots:The influence of labeling[J]. RSC Advances, 2014, 5(6):4554-4560
- [2]石清清,邓代莉,颜椿,等.纳米金属氧化物对土壤酶活性的影响研究进展[J].生态毒理学报, 2018, 13(2):47-56Shi Q Q, Deng D L, Yan C, et al. Review on effects of engineered nano-metal oxide particles to soil enzyme activities[J]. Asian Journal of Ecotoxicology, 2018, 13(2):47-56(in Chinese)
- [3] Wang Y L, Ding L, Yao C J, et al. Toxic effects of metal oxide nanoparticles and their underlying mechanisms[J].Science China Materials, 2017, 60(2):93-108
- [4] Colvin V L. The potential environmental impact of engineered nanomaterials[J]. Nature Biotechnology, 2003, 21(10):1166-1170
- [5] Hoet P H, Nemmar A, Nemery B. Health impact of nanomaterials?[J]. Nature Biotechnology, 2004, 22(1):19
- [6] Ahamed M, Ali D, Alhadlaq H A, et al. Nickel oxide nanoparticles exert cytotoxicity via oxidative stress and induce apoptotic response in human liver cells(HepG2)[J].Chemosphere, 2013, 93(10):2514-2522
- [7] Salvadori M R, Ando R A, Nascimento C A, et al. Extra and intracellular synthesis of nickel oxide nanoparticles mediated by dead fungal biomass[J]. Plos One, 2015, 10(6):1-15
- [8] Bi H, Li S, Zhang Y, et al. Ferromagnetic-like behavior of ultrafine Ni O nanocrystallites[J]. Journal of Magnetism&Magnetic Materials, 2004, 277(3):363-367
- [9] Nogueira V, Lopes I, Rochasantos T A, et al. Assessing the ecotoxicity of metal nano-oxides with potential for wastewater treatment[J]. Environmental Science&Pollution Research, 2015, 22(17):13212-13224
- [10] Oukarroum A, Barhoumi L, Samadani M, et al. Toxic effects of nickel oxide bulk and nanoparticles on the aquatic plant Lemna gibba L.[J]. Biomed Research International, 2015, 2015:501326
- [11] Capasso L, Camatini M, Gualtieri M. Nickel oxide nanoparticles induce inflammation and genotoxic effect in lung epithelial cells[J]. Toxicology Letters, 2014, 226(1):28-34
- [12] Siddiqui M A, Ahamed M, Ahmad J, et al. Nickel oxide nanoparticles induce cytotoxicity, oxidative stress and apoptosis in cultured human cells that is abrogated by the dietary antioxidant curcumin[J]. Food&Chemical Toxicology, 2012, 50(3-4):641-647
- [13] Horie M, Fukui H, Endoh S, et al. Comparison of acute oxidative stress on rat lung induced by nano and finescale, soluble and insoluble metal oxide particles:Ni O and Ti O2[J]. Inhalation Toxicology, 2012, 24(7):391-400
- [14]谢嘉.典型重金属(Cd2+、Pb2+)和有机污染物(BaP、BDE-47)对长牡蛎的复合毒性效应研究[D].北京:中国科学院大学, 2017:19Xie J. Combined toxic effects of heavy metals(Cd2+、Pb2+)and organic pollutants(BaP, BDE-47)on the oyster Crassostrea gigas[D]. Beijing:University of the Chinese Academy of Sciences, 2017:19(in Chinese)
- [15] Syed S, Zubair A, Frieri M. Immune response to nanomaterials:Implications for medicine and literature review[J].Current Allergy&Asthma Reports, 2013, 13(1):50-57
- [16] Gong N, Shao K S, Li G Y, et al. Nickel oxide nanoparticles induce oxidative stress and morphological changes onmarine Chlorella vulgaris[J]. Advanced Materials Research, 2014, 955-959(11):956-960
- [17] Rikans L E, Hornbrook K R. Lipid peroxidation, antioxidant protection and aging[J]. Biochimica et Biophysica Acta, 1997, 1362(2-3):116-127
- [18] Winston G W, Giulio R T. Prooxidant and antioxidant mechanisms in aquatic organisms[J]. Aquatic Toxicology,1991, 19(2):137-161
- [19]陈剑杰,曹谨玲,李潇,等.氟对中华圆田螺肝胰脏抗氧化酶活性和MDA含量的影响[J].生态毒理学报,2018, 13(1):268-273Chen J J, Cao J L, Li X, et al. Effects of fluoride on the activities of antioxidant enzymes and MDA levels in hepatopancreas of Cipangopaludina cahayensis[J]. Asian Journal of Ecotoxicology, 2018, 13(1):268-273(in Chinese)
- [20]马菲菲,孙雪梅,韩倩,等.不同粒径Ti O2颗粒对海洋微藻的毒性效应[J].海洋学报, 2015, 37(10):100-105Ma F F, Sun X M, Han Q, et al. Toxic effects of Ti O2particles with different size on the marine microalga[J]. Acta Oceanologica Sinica, 2015, 37(10):100-105(in Chinese)
- [21] Slos S, Stoks R. Predation risk induces stress proteins and reduces antioxidant defense[J]. Functional Ecology, 2008,22(4):637-642
- [22] Meng X L, Liu P, Li J, et al. Physiological responses of swimming crab Portunus trituberculatus under cold acclimation:Antioxidant defense and heat shock proteins[J].Aquaculture, 2014, 434:11-17
- [23] Zalutskaya Z, Ostroukhova M, Filina V, et al. Nitric oxide upregulates expression of alternative oxidase 1 in Chlamydomonas reinhardtii[J]. Journal of Plant Physiology, 2017, 219:123-127
- [24] Bhatia M. Understanding toxicology:Mechanisms and applications[J]. Cell Biology&Toxicology, 2017, 33(1):1-4
- [25] Lachapelle G, Radicioni S M, Stankiewicz A R, et al. Acute acidification or amiloride treatment suppresses the ability of Hsp70 to inhibit heat-induced apoptosis[J]. Apoptosis, 2007, 12(8):1479-1488
- [26] Ellison M A, Ferrier M D, Carney S L. Salinity stress results in differential Hsp70 expression in the Exaiptasia pallida and Symbiodinium symbiosis[J]. Marine Environmental Research, 2017, 132:63-67
- [27] Mc Donald A E, Vanlerberghe G C, Staples J F. Alternative oxidase in animals:Unique characteristics and taxonomic distribution[J]. Journal of Experimental Biology,2009, 212(16):2627-2634
- [28]魏磊.长牡蛎(Crassostrea gigas)对海水酸化生理响应的组学研究[D].北京:中国科学院大学, 2015:9-10Wei L. Omics studies on the physiological responses of Pacific oyster(Crassostrea gigas)to CO2-driven ocean acidification[D]. Beijing:University of the Chinese Academy of Sciences, 2015:9-10(in Chinese)
- [29] Canesi L, Ciacci C, Fabbri R, et al. Bivalve molluscs as a unique target group for nanoparticle toxicity[J]. Marine Environmental Research, 2012, 76(4):16-21
- [30] Rocha T L, Gomes T, Sousa V S, et al. Ecotoxicological impact of engineered nanomaterials in bivalve molluscs:An overview[J]. Marine Environmental Research, 2015,111:74-88
- [31] Trevisan R, Delapedra G, Mello D F, et al. Gills are an initial target of zinc oxide nanoparticles in oysters Crassostrea gigas, leading to mitochondrial disruption and oxidative stress[J]. Aquatic Toxicology, 2014, 153(8):27-38
- [32] Meng J, Wang W X, Li L, et al. Respiration disruption and detoxification at the protein expression levels in the Pacific oyster(Crassostrea gigas)under zinc exposure[J].Aquatic Toxicology, 2017, 191:34-41
- [33] Liang Q Q, Li Y S. A rapid and accurate method for determining protein content in dairy products based on asynchronous-injection alternating merging zone flow-injection spectrophotometry[J]. Food Chemistry, 2013, 141(3):2479-2485
- [34] Multhoff G, Pockley A G, Schmid T E, et al. The role of heat shock protein 70(Hsp70)in radiation-induced immunomodulation[J]. Cancer Letters, 2015, 368(2):179-184
- [35]赵情,米铁柱,甄毓,等.诺氟沙星对海月水母螅状体Hsp70基因、GTP结合蛋白基因和氧化应激蛋白基因表达的影响[J].生态毒理学报, 2017, 12(1):201-211Zhao Q, Mi T Z, Zhen Y, et al. Norfloxacin toxicity effects on gene expression of heat shock 70 k Da protein,GTP-binding protein, and oxidative stress protein of Aurelia aurita polyps[J] Asian Journal of Ecotoxicology,2017, 12(1):201-211(in Chinese)
- [36]余璐璐,吴阳晨,王静静,等.交替氧化酶在麻疯树盐胁迫响应中的作用[J].生物技术通报, 2014(7):112-118Yu L L, Wu C Y, Wang J J, et al. The possible role of alternative oxidase in Jatropha curcas L. response to salt stress[J] Biotechnology Bulletin, 2014(7):112-118(in Chinese)
- [37] Mc Donald A, Vanlerberghe G. Branched mitochondrial electron transport in the Animalia:Presence of alternative oxidase in several animal phyla[J]. Iubmb Life, 2004, 56(6):333-341
- [38] Duan Y P, Yuan S, Tu S H, et al. Effects of cadmium stress on alternative oxidase and photosystem II in three wheat cultivars[J]. Zeitschrift Fur Naturforschung C,2010, 65(1-2):87-94
- [39] Mc Carthy M P, Carroll D L, Ringwood A H. Tissue specific responses of oysters, Crassostrea virginica, to silver nanoparticles[J]. Aquatic Toxicology, 2013, 138-139(1):123-128
- [40] Belles M, Alonso V, Linares V, et al. Behavioral effects and oxidative status in brain regions of adult rats exposed to BDE-99[J]. Toxicology Letters, 2010, 194(1):1-7
- [41]唐学玺,张培玉.蒽对黑鲪超氧化物歧化酶活性的影响[J].水产学报, 2000, 24(3):217-220Tang X X, Zhang P Y. Effects of anthracene on activity of superoxide dismutase in Sebastodes fuscescens[J] Journal of Fisheries of China, 2000, 24(3):217-220(in Chinese)
- [42] Stebbing A R. Hormesis—The stimulation of growth by low levels of inhibitors[J]. Science of the Total Environment, 1982, 22(3):213-234
- [43]刘芝余,翟毓秀,姚琳,等.全氟辛酸(PFOA)对菲律宾蛤仔体内酶活性的影响[J].生态毒理学报, 2017, 12(3):695-704Liu Z Y, Zhai Y X, Yao L, et al. The effects of perfluorooctanoic acid(PFOA)on enzyme activities in Ruditapes philippinarum[J]. Asian Journal of Ecotoxicology, 2017,12(3):695-704(in Chinese)
- [44]王贺威,马胜伟,张喆,等.全氟辛烷磺酸盐(PFOS)胁迫对翡翠贻贝抗氧化酶的影响[J].生态毒理学报,2012, 7(5):508-516Wang H W, Ma S W, Zhang Z, et al. Effects of perfluorooctane sulfonate(PFOS)exposure on antioxidant enzymes of Perna viridis[J]. Asian Journal of Ecotoxicology, 2012, 7(5):508-516(in Chinese)
- [45]于庆云,王悠,徐彦,等.镉和铅对菲律宾蛤仔脂质过氧化及抗氧化酶活性的影响[J].生态毒理学报, 2013,8(4):504-512Yu Q Y, Wang Y, Xu Y, et al. Effects of cadmium and lead on the lipid peroxidation and levels of antioxidant enzymes in Ruditapes philippinarum[J]. Asian Journal of Ecotoxicology, 2013, 8(4):504-512(in Chinese)
- [46]张喆,马胜伟,王贺威,等.十溴联苯醚(BDE-209)对菲律宾蛤仔外套膜抗氧化酶活性的影响[J].生态学杂志,2013, 32(1):122-128Zhang Z, Ma S W, Wang H W, et al. Effects of decabromodiphenyl ether(BDE-209)on the antioxidant enzyme activities of Lutjanus argentimaculatus mantle membrane[J]. Chinese Journal of Ecology, 2013, 32(1):122-128(in Chinese)
- [47] Martínez-lvarez R M, Morales A E, Sanz A. Antioxidant defenses in fish:Biotic and abiotic factors[J]. Reviews in Fish Biology&Fisheries, 2005, 15(1-2):75-88
- [48]洪美玲,陈立侨,顾顺樟,等.不同温度胁迫方式对中华绒螯蟹免疫化学指标的影响[J].应用与环境生物学报, 2007, 13(6):818-822Hong M L, Chen L Q, Gu S Z, et al. Effect of temperature change on immunochemical indexes of Eriocheir sinensis[J]. Chinese Journal of Applied&Environmental Biology,2007, 13(6):818-822(in Chinese)
- [49] Yeong Y S, Mac Rae T H. Heat shock proteins and disease control in aquatic organisms[J]. Journal of Aquaculture&Research Development, 2013, 3(S2):006
- [50] Gupta S C, Sharma A, Mishra M, et al. Heat shock proteins in toxicology:How close and how far?[J]. Life Sciences, 2010, 86(11-12):377-384
- [51] Cruzrodríguez L A, Chu F L. Heat-shock protein(HSP70)response in the eastern oyster Crassostrea virginica, exposed to PAHs sorbed to suspended artificial clay particles and to suspended field contaminated sediments[J]. Aquatic Toxicology, 2002, 60(3-4):157-168
- [52] Ahamed M, Posgai R, Gorey T J, et al. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster[J]. Toxicology&Applied Pharmacology, 2010, 242(3):263-269
- [53] Selvakumar S, Geraldine P. Heat shock protein induction in the freshwater prawn Macrobrachium malcolmsonii:Acclimation-influenced variations in the induction temperatures for Hsp70[J]. Comparative Biochemistry&Physiology Part A, 2005, 140(2):209-215
- [54] Chapple J P, Smerdon G R, Hawkins A J S, et al. Stress-70 protein induction in Mytilus edulis:Tissue-specific responses to elevated temperature reflect relative vulnerability and physiological function[J]. Journal of Experimental Marine Biology&Ecology, 1997, 217(2):225-235
- [55] Yoo J L, Janz D M. Tissue-specific HSP70 levels and reproductive physiological responses in fishes inhabiting a metal-contaminated creek[J]. Archives of Environmental Contamination&Toxicology, 2003, 45(1):110-120
- [56] Sussarellu R, Fabioux C, Sanchez M C, et al. Molecular and cellular response to short-term oxygen variations in the Pacific oyster Crassostrea gigas[J]. Journal of Experimental Marine Biology&Ecology, 2012, 412(1):87-95
- [57] Buttemer W A, Abele D, Costantini D. From bivalves to birds:Oxidative stress and longevity[J]. Functional Ecology, 2010, 24(5):971-983
- [58] Robertson A, Schaltz K, Neimanis K, et al. Heterologous expression of the Crassostrea gigas(Pacific oyster)alternative oxidase in the yeast Saccharomyces cerevisiae[J].Journal of Bioenergetics&Biomembranes, 2016, 48(5):509-520
- [59] Ortizzarragoitia M, Cajaraville M P. Biomarkers of exposure and reproduction-related effects in mussels exposed to endocrine disruptors[J]. Archives of Environmental Contamination&Toxicology, 2006, 50(3):361-369
- [60] Keunen E, Florezsarasa I, Obata T, et al. Metabolic responses of Arabidopsis thaliana roots and leaves to sublethal cadmium exposure are differentially influenced by alternative oxidase1a[J]. Environmental&Experimental Botany, 2016, 124:64-78