镉和铅联合作用对黑腹果蝇发育及抗氧化的影响
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摘要
作为主要的重金属污染物,镉(Cd~(2+))和铅(Pb~(2+))对生物体具有不同影响和毒作用机制,然而当它们同时存在于机体内常会表现出不同的联合效应,因此研究以上两种重金属的联合作用极其重要。本研究以模式生物黑腹果蝇(Drosophila melanogaster)为研究对象,采用原子吸收、发育实验、酶学测定以及荧光定量PCR评估Cd~(2+)和Pb~(2+)以及二者联合对果蝇的影响。向果蝇分别饲喂不同剂量的Cd~(2+)(0.05、0.1、0.3、0.5 mmol?L~(-1))和Pb~(2+)(0.2、0.5、1.5、2.9 mmol?L~(-1))以及Cd~(2+)+Pb~(2+)(0.05+0.2、0.1+0.5、0.3+1.5、0.5+2.9 mmol?L~(-1)),测定果蝇成虫体内Cd~(2+)和Pb~(2+)积累量,以及化蛹率、羽化率、抗氧化能力、金属硫蛋白(metallothionein,MTNs)和谷胱甘肽S转移酶(glutathione S-transferase,GST)基因的表达水平。结果表明,果蝇中Cd~(2+)和Pb~(2+)浓度随着培养基中重金属浓度的上升而增加,当同时加入Cd~(2+)和Pb~(2+)后,二者积累量进一步增加。单独添加Pb~(2+)(0.2、0.5、1.5、2.9 mmol?L~(-1))或共同添加Cd~(2+)+Pb~(2+)(0.1+0.5、0.3+1.5、0.5+2.9 mmol?L~(-1))显著降低果蝇化蛹率和羽化率,而Cd~(2+)+Pb~(2+)联合处理较单独Cd~(2+)/Pb~(2+)处理表现出更强的效果,且这种效果随着Cd~(2+)/Pb~(2+)浓度的增加而增强。Cd~(2+)+Pb~(2+)处理CAT活性较单独Cd~(2+)/Pb~(2+)处理显著提高。Cd~(2+)+Pb~(2+)(0.05+0.2、0.1+0.5、0.3+1.5 mmol?L~(-1))处理组SOD活性较单独Cd~(2+)/Pb~(2+)处理,SOD活性无明显变化,但在Cd~(2+)+Pb~(2+)(0.5+2.9 mmol?L~(-1))处理组中SOD活性显著上升;Cd~(2+)+Pb~(2+)(0.05+0.2 mmol?L~(-1))处理组MDA含量较单独Cd~(2+)/Pb~(2+)处理显著提升,但在处理组Cd~(2+)+Pb~(2+)(1+0.5、0.3+1.5、0.5+2.9mmol?L~(-1))中MDA含量反而较单独的Cd~(2+)/Pb~(2+)处理有所下降。荧光定量PCR结果表明,在Cd~(2+)/Pb~(2+)处理下MTNs和Gsts表达水平显著升高。本研究表明重金属联合作用会对生物体产生不同的毒性效应,而MTNs和Gsts两类基因在生物体重金属胁迫下的解毒机制中发挥着至关重要的作用。
As the main heavy metal pollutant,Cd~(2+)and Pb~(2+)have different effect and toxic effects on organisms,however they have a joint effect when they exist simultaneously on organisms.So it is extremely important to study the joint actin of the two heavy metals.In this study,the model organism Drosophila melanogaster was used as the research object,the effects of Cd~(2+),Pb~(2+)and their joint action on D.melanogaster were evaluated by atomic absorption,developmental experiments,enzymatic activity determination and real-time quantitative PCR.After feeding D.melanogaster with different doses of Cd~(2+)(0.05,0.1,0.3,0.5 mmol?L~(-1)),Pb~(2+)(0.2,0.5,1.5,2.9 mmol?L~(-1)),and Cd~(2+)+Pb~(2+)(0.05+0.2,0.1+0.5,0.3+1.5,0.5+2.9 mmol?L~(-1)),the accumulation of Cd~(2+)and Pb~(2+)in the body,as well as the pupation rate,emergence rate,anti-oxidative capacity,expression levels of metallothionein(MTNs)and glutathione S-transferase(GST)genes,were measured.The results showed that the concentration of Cd~(2+)and Pb~(2+)in D.melanogaster increased with the increase of heavy metal concentration in the medium.When Cd~(2+)and Pb~(2+)were jointly supplemented,the accumulation of Cd~(2+)and Pb~(2+)further increased.The supplementation of Pb~(2+)(0.2,0.5,1.5,2.9 mmol?L~(-1))alone and joint supplementation of Cd~(2+)+Pb~(2+)(0.1+0.5,0.3+1.5,0.5+2.9 mmol?L~(-1))significantly reduced the rate of pupation and emergence,also Cd~(2+)+Pb~(2+)joint treatment had a stronger effect than that of Cd~(2+)or Pb~(2+)alone.Moreover,the effect also increased with the increase of Cd~(2+)/Pb~(2+)concentration.The joint supplementation of Cd~(2+)and Pb~(2+)in each treatment group significantly increased CAT activity compared with Cd~(2+)or Pb~(2+)treatment alone.In the treatment groups of Cd~(2+)+Pb~(2+)(0.05+0.2,0.1+0.5,0.3+1.5 mmol?L~(-1)),the joint supplementation of Cd~(2+)and Pb~(2+)was compared with Cd~(2+)or Pb~(2+)alone,and the activity of SOD was not significantly changed,however the activity of SOD significant increased in the treatment group of Cd~(2+)+Pb~(2+)(0.5+2.9mmol?L~(-1)).The joint supplementation of Cd~(2+)and Pb~(2+)significantly increased the MDA content compared with Cd~(2+)or Pb~(2+)alone in the treatment group of Cd~(2+)+Pb~(2+)(0.05+0.2 mmol?L~(-1)),but decreased the MDA content in the treatment groups of Cd~(2+)+Pb~(2+)(1+0.5,0.3+1.5,0.5+2.9 mmol?L~(-1))compared with the Cd~(2+)or Pb~(2+)treatment alone.The results of real-time quantitative PCR showed that the expression levels of MTNs and Gsts genes were significantly increased after Cd~(2+)/Pb~(2+)treatment.This study showed that the joint treatment of heavy metals can produce different toxic effects on organisms,while regulation of the expression of the two types of genes,MTNs and Gsts genes,playes a crucial role in the detoxification of organisms under heavy metal stress.
As the main heavy metal pollutant,Cd~(2+)and Pb~(2+)have different effect and toxic effects on organisms,however they have a joint effect when they exist simultaneously on organisms.So it is extremely important to study the joint actin of the two heavy metals.In this study,the model organism Drosophila melanogaster was used as the research object,the effects of Cd~(2+),Pb~(2+)and their joint action on D.melanogaster were evaluated by atomic absorption,developmental experiments,enzymatic activity determination and real-time quantitative PCR.After feeding D.melanogaster with different doses of Cd~(2+)(0.05,0.1,0.3,0.5 mmol?L~(-1)),Pb~(2+)(0.2,0.5,1.5,2.9 mmol?L~(-1)),and Cd~(2+)+Pb~(2+)(0.05+0.2,0.1+0.5,0.3+1.5,0.5+2.9 mmol?L~(-1)),the accumulation of Cd~(2+)and Pb~(2+)in the body,as well as the pupation rate,emergence rate,anti-oxidative capacity,expression levels of metallothionein(MTNs)and glutathione S-transferase(GST)genes,were measured.The results showed that the concentration of Cd~(2+)and Pb~(2+)in D.melanogaster increased with the increase of heavy metal concentration in the medium.When Cd~(2+)and Pb~(2+)were jointly supplemented,the accumulation of Cd~(2+)and Pb~(2+)further increased.The supplementation of Pb~(2+)(0.2,0.5,1.5,2.9 mmol?L~(-1))alone and joint supplementation of Cd~(2+)+Pb~(2+)(0.1+0.5,0.3+1.5,0.5+2.9 mmol?L~(-1))significantly reduced the rate of pupation and emergence,also Cd~(2+)+Pb~(2+)joint treatment had a stronger effect than that of Cd~(2+)or Pb~(2+)alone.Moreover,the effect also increased with the increase of Cd~(2+)/Pb~(2+)concentration.The joint supplementation of Cd~(2+)and Pb~(2+)in each treatment group significantly increased CAT activity compared with Cd~(2+)or Pb~(2+)treatment alone.In the treatment groups of Cd~(2+)+Pb~(2+)(0.05+0.2,0.1+0.5,0.3+1.5 mmol?L~(-1)),the joint supplementation of Cd~(2+)and Pb~(2+)was compared with Cd~(2+)or Pb~(2+)alone,and the activity of SOD was not significantly changed,however the activity of SOD significant increased in the treatment group of Cd~(2+)+Pb~(2+)(0.5+2.9mmol?L~(-1)).The joint supplementation of Cd~(2+)and Pb~(2+)significantly increased the MDA content compared with Cd~(2+)or Pb~(2+)alone in the treatment group of Cd~(2+)+Pb~(2+)(0.05+0.2 mmol?L~(-1)),but decreased the MDA content in the treatment groups of Cd~(2+)+Pb~(2+)(1+0.5,0.3+1.5,0.5+2.9 mmol?L~(-1))compared with the Cd~(2+)or Pb~(2+)treatment alone.The results of real-time quantitative PCR showed that the expression levels of MTNs and Gsts genes were significantly increased after Cd~(2+)/Pb~(2+)treatment.This study showed that the joint treatment of heavy metals can produce different toxic effects on organisms,while regulation of the expression of the two types of genes,MTNs and Gsts genes,playes a crucial role in the detoxification of organisms under heavy metal stress.
引文
ALSLAIBI T M,ABUSTAN I,AHMAD M A,et al.,2014.Preparation of Activated Carbon From Olive Stone Waste:Optimization Study on the Removal of Cu2+,Cd2+,Ni2+,Pb2+,Fe2+,and Zn2+from Aqueous Solution Using Response Surface Methodology[J].Journal of Dispersion Science and Technology,35(7):913-925.
ANNABI A,KESSABI K,KERKENI A,et al.,2012.Influence of Cadmium Exposure on Growth and Fecundity of Freshwater Mosquitofish Gambusia affinis:In Situ and In Vivo Studies[J].Biological Trace Element Research,148(3):345-355.
ANTONIO M T,CORREDOR L,LEET M L,2003.Study of the activity of several brain enzymes like markers of the neurotoxicity induced by perinatal exposure to lead and/or cadmium[J].Toxicology Letters(Shannon),143(3):331-340.
BIZARRO P,ACEVEDO S,NIO-CABRERA G,et al.,2013.Ultrastructural modifications in the mitochondrion of mouse Sertoli cells after inhalation of lead,cadmium or lead-cadmium mixture[J].Reproductive Toxicology,17(5):561-566.
CHANDLER J D,CHERRY W,BANTON S A,et al.,2016.Low-dose oral cadmium increases airway reactivity and lung neuronal gene expression in mice[J].Physiological Reports,4(13):e12821.
CHEREDDY N R,THENNARASU S,2011.Synthesis of a highly selective bis-rhodamine chemosensor for naked-eye detection of Cu2+ions and its application in bio-imaging[J].Dyes&Pigments,91(3):378-382.
CHIAVERINI N,LEY M D,2010.Protective effect of metallothionein on oxidative stress-induced DNA damage[J].Free Radical Research Communications,44(6):605-613.
EGLI D,DOMA NECH J,SELVARAJ A,et al.,2010.The four members of the drosophila metallothionein family exhibit distinct yet overlapping roles in heavy metal homeostasis and detoxification[J].Genes to Cells,11(6):647-658.
FORTOUL T I,LILIANA S O,Espejel-Maya G,et al.,2005.Inhalation of cadmium,lead or its mixture:Effects on the bronchiolar structure and its relation with metal tissue concentrations[J].Environ Toxicol Pharmacol,19(2):329-334.
GARCIA T A,CORREDOR L,2004.Biochemical changes in the kidneys after perinatal intoxication with lead and/or cadmium and their antagonistic effects when coadministered[J].Ecotoxicology&Environmental Safety,57(2):184-189.
GE H C,FAN X H,2011.Adsorption of Pb2+and Cd2+onto a novel activated carbon-chitosan complex[J].Chemical Engineering&Technology,34(10):1745-1752.
HE B,YUN Z J,SHI J B,et al.,2013.Research progress of heavy metal pollution in China:Sources,analytical methods,status,and toxicity[J].Chinese Science Bulletin,58(2):134-140.
JENSEN K P,RYKAER M,2010.The building blocks of metallothioneins:heterometallic Zn(2+)and Cd(2+)clusters from first-principles calculations[J].Dalton Trans,39(40):9684-9695.
JIHEN E,IMED M,FATIMA H,et al.,2009.Protective effects of selenium(Se)and zinc(Zn)on cadmium(Cd)toxicity in the liver of the rat:effects on the oxidative stress[J].Ecotoxicology&Environmental Safety,72(5):1559-1564.
JIN J,BAI F Q,JIA M J,et al.,2013.New Cd2+,Pb2+complexes with acylhydrazidate molecules from in situ acylation reactions[J].Dalton Transactions,42(24):8771-8780.
KARWOWSKA A,LAPINSKI R,GACKO M,et al.,2012.Effect of heavy metal cations on the activity of cathepsin D(in vitro study)[J].Folia Histochemica Et Cytobiologica,50(3):432-435.
KOIVULA M J,EEVA T,2010.Metal-related oxidative stress in birds[J].Environmental Pollution,158(7):2359-2370.
LEE Y F,HUANG C C,2011.Colorimetric Assay of Lead Ions in Biological Samples Using a Nanogold-Based Membrane[J].ACSAPPLIED MATERIALS&INTERFACES,3(7):2747-2754.
LI Y,HUO X,LIU J X,et al.,2011.Assessment of cadmium exposure for neonates in Guiyu,an electronic waste pollution site of China[J].Environmental Monitoring&Assessment,177(1-4):343-351.
LIN Y C,WEI P L,TSAI Y T,et al.,2015.Pb2+induced IL-8 gene expression by extracellular signal-regulated kinases and the transcription factor,activator protein 1,in human gastric carcinoma cells[J].Environmental Toxicology,30(3):315-322.
LIU J,QU W,KADIISKA M B,2009.Role of oxidative stress in cadmium toxicity and carcinogenesis[J].Toxicol.appl.pharmacol,238(3):209-214.
LIVAK K J,SCHMITTGEN T D,2001.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCTmethod[J].Methods,25(4):402-408.
LLOBET J M,FALCóG,CASAS C,et al.,2003.Concentrations of arsenic,cadmium,mercury,and lead in common foods and estimated daily intake by children,adolescents,adults,and seniors of Catalonia,Spain[J].Journal of Agricultural&Food Chemistry,51(3):838-842.
MADSEN K B,ASKOV-HANSEN C,NAIMI R M,et al.,2013.Acute effects of continuous infusions of glucagon-like peptide(GLP)-1,GLP-2 and the combination(GLP-1+GLP-2)on intestinal absorption in short bowel syndrome(SBS)patients.A placebo-controlled study[J].Regulatory Peptides,184:30-39.
MAHAFFEY K R,FOWLER B A,1977.Effects of concurrent administration of lead,cadmium,and arsenic in the rat[J].Environmental Health Perspectives,19(2):165-171.
MASSóE L,CORREDOR L,ANTONIO M T,2007.Oxidative damage in liver after perinatal intoxication with lead and/or cadmium[J].Journal of Trace Elements in Medicine&Biology,21(3):210-216.
MIRANDA J,KRISHNAKUMAR G,D’SILVA A,2012.Removal of Pb2+from aqueous system by live Oscillatoria laete-virens(Crouan and Crouan)Gomont isolated from industrial effluents[J].World Journal of Microbiology&Biotechnology,28(10):3053-3065.
NAWAB J,KHAN S,SHAH M T,et al.,2015.Contamination of soil,medicinal,and fodder plants with lead and cadmium present in mine-affected areas,Northern Pakistan[J].Environmental Monitoring and Assessment,187(9):605.
PAN L Q,LIU N,ZHANG H X,et al.,2011.Effects of heavy metal ions(Cu2+,Pb2+and Cd2+)on DNA damage of the gills,hemocytes and hepatopancreas of marine crab,Charybdis japonica[J].Journal of Ocean University of China,10(2):177-184.
PILLAI A,GUPTA S,2005.Effect of gestational and lactational exposure to lead and/or cadmium on reproductive performance and hepatic oestradiol metabolising enzymes[J].Toxicology Letters,155(1):179-186.
RANI A,KUMAR A,LAL A,et al.,2014.Cellular mechanisms of cadmium-induced toxicity:a review[J].International Journal of Environmental Health Research,24(4):378-399.
ROGGEMAN S,DE BOECKG,DE COCK H,et al.,2014.Accumulation and detoxification of metals and arsenic in tissues of cattle(Bos taurus),and the risks for human consumption[J].Science of The Total Environment,466-467:175-184.
RUDEL D,DOUGLAS C D,HUFFNAGLE I M,et al.,2013.Assaying environmental nickel toxicity using model nematodes[J].PLoS ONE,8(10):e77079.
SABOLI?I,BRELJAK D,?KARICA M,et al.,2010.Role of metallothionein in cadmium traffic and toxicity in kidneys and other mammalian organs[J].BioMetal:23(5):897-926.
VALKO M,MORRIS H,2005.Cronin M T.Metals,toxicity and oxidative stress[J].Current Medicinal Chemistry,12(10):1161-1208.
WANG Y K,GAO S T,ZANG X H,et al.,2012.Graphene-based solid-phase extraction combined with flame atomic absorption spectrometry for a sensitive determination of trace amounts of lead in environmental water and vegetable samples[J].Analytica Chimica Acta,716:112-118.
XIA L P,CHEN S H,DAHMS H U,et al.,2016.Cadmium induced oxidative damage and apoptosis in the hepatopancreas of Meretrix meretrix[J].Ecotoxicology,25(5):959-969.
XU G,LIN G,LIN S,et al.,2016.The Reproductive Toxicity of CdSe/ZnSQuantum Dots on the in vivo Ovarian Function and in vitro Fertilization[J].Scientific Reports,6:37677.
XU L,XU Y F,ZHU W P,et al.,2012.Modulating the selectivity by switching sensing media:a bifunctional chemosensor selectivity for Cd2+and Pb2+in different aqueous solutions[J].RSC Advances,2(15):6323-6328.
YANG J L,WANG Y C,LIU G F,et al.,2011.Tamarix hispida metallothionein-like ThMT3,a reactive oxygen species scavenger,increases tolerance against Cd2+,Zn2+,Cu2+,and NaCl in transgenic yeast[J].Molecular Biology Reports,38(3):1567-1574.
ZHANG Y M,LIU X Z,HAO L U,et al.,2009.Lipid Peroxidation and Ultrastructural Modifications in Brain after Perinatal Exposure to Lead and/or Cadmium in Rat Pups[J].Biomedical and Environmental Sciences,22(5):423-429.
万永奇,谢维,2006.生命科学与人类疾病研究的重要模型:果蝇[J].生命科学,18(5):425-429.WAN Y Q,XIE W,2006.Drosophila:an important model organism for understanding basic biological and human disease mechanisms[J].Chinese Bulletin of Life Sciences,18(5):425-429.
郑双艳,刘清,张霞丽,等,2019.重金属胁迫下河蚬内脏中GST mRNA表达及酶活性分析[J].生态环境学报,28(2):369-375.ZHEN S Y,LIU Q,ZHANG X L,et al.,2019.Analysis of GST mRNAExpression and Enzymatic Activities in Corbicula fluminea Viscera Exposed to Heavy Metals[J].Ecology and Environmental Sciences,28(2):369-375.
ANNABI A,KESSABI K,KERKENI A,et al.,2012.Influence of Cadmium Exposure on Growth and Fecundity of Freshwater Mosquitofish Gambusia affinis:In Situ and In Vivo Studies[J].Biological Trace Element Research,148(3):345-355.
ANTONIO M T,CORREDOR L,LEET M L,2003.Study of the activity of several brain enzymes like markers of the neurotoxicity induced by perinatal exposure to lead and/or cadmium[J].Toxicology Letters(Shannon),143(3):331-340.
BIZARRO P,ACEVEDO S,NIO-CABRERA G,et al.,2013.Ultrastructural modifications in the mitochondrion of mouse Sertoli cells after inhalation of lead,cadmium or lead-cadmium mixture[J].Reproductive Toxicology,17(5):561-566.
CHANDLER J D,CHERRY W,BANTON S A,et al.,2016.Low-dose oral cadmium increases airway reactivity and lung neuronal gene expression in mice[J].Physiological Reports,4(13):e12821.
CHEREDDY N R,THENNARASU S,2011.Synthesis of a highly selective bis-rhodamine chemosensor for naked-eye detection of Cu2+ions and its application in bio-imaging[J].Dyes&Pigments,91(3):378-382.
CHIAVERINI N,LEY M D,2010.Protective effect of metallothionein on oxidative stress-induced DNA damage[J].Free Radical Research Communications,44(6):605-613.
EGLI D,DOMA NECH J,SELVARAJ A,et al.,2010.The four members of the drosophila metallothionein family exhibit distinct yet overlapping roles in heavy metal homeostasis and detoxification[J].Genes to Cells,11(6):647-658.
FORTOUL T I,LILIANA S O,Espejel-Maya G,et al.,2005.Inhalation of cadmium,lead or its mixture:Effects on the bronchiolar structure and its relation with metal tissue concentrations[J].Environ Toxicol Pharmacol,19(2):329-334.
GARCIA T A,CORREDOR L,2004.Biochemical changes in the kidneys after perinatal intoxication with lead and/or cadmium and their antagonistic effects when coadministered[J].Ecotoxicology&Environmental Safety,57(2):184-189.
GE H C,FAN X H,2011.Adsorption of Pb2+and Cd2+onto a novel activated carbon-chitosan complex[J].Chemical Engineering&Technology,34(10):1745-1752.
HE B,YUN Z J,SHI J B,et al.,2013.Research progress of heavy metal pollution in China:Sources,analytical methods,status,and toxicity[J].Chinese Science Bulletin,58(2):134-140.
JENSEN K P,RYKAER M,2010.The building blocks of metallothioneins:heterometallic Zn(2+)and Cd(2+)clusters from first-principles calculations[J].Dalton Trans,39(40):9684-9695.
JIHEN E,IMED M,FATIMA H,et al.,2009.Protective effects of selenium(Se)and zinc(Zn)on cadmium(Cd)toxicity in the liver of the rat:effects on the oxidative stress[J].Ecotoxicology&Environmental Safety,72(5):1559-1564.
JIN J,BAI F Q,JIA M J,et al.,2013.New Cd2+,Pb2+complexes with acylhydrazidate molecules from in situ acylation reactions[J].Dalton Transactions,42(24):8771-8780.
KARWOWSKA A,LAPINSKI R,GACKO M,et al.,2012.Effect of heavy metal cations on the activity of cathepsin D(in vitro study)[J].Folia Histochemica Et Cytobiologica,50(3):432-435.
KOIVULA M J,EEVA T,2010.Metal-related oxidative stress in birds[J].Environmental Pollution,158(7):2359-2370.
LEE Y F,HUANG C C,2011.Colorimetric Assay of Lead Ions in Biological Samples Using a Nanogold-Based Membrane[J].ACSAPPLIED MATERIALS&INTERFACES,3(7):2747-2754.
LI Y,HUO X,LIU J X,et al.,2011.Assessment of cadmium exposure for neonates in Guiyu,an electronic waste pollution site of China[J].Environmental Monitoring&Assessment,177(1-4):343-351.
LIN Y C,WEI P L,TSAI Y T,et al.,2015.Pb2+induced IL-8 gene expression by extracellular signal-regulated kinases and the transcription factor,activator protein 1,in human gastric carcinoma cells[J].Environmental Toxicology,30(3):315-322.
LIU J,QU W,KADIISKA M B,2009.Role of oxidative stress in cadmium toxicity and carcinogenesis[J].Toxicol.appl.pharmacol,238(3):209-214.
LIVAK K J,SCHMITTGEN T D,2001.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCTmethod[J].Methods,25(4):402-408.
LLOBET J M,FALCóG,CASAS C,et al.,2003.Concentrations of arsenic,cadmium,mercury,and lead in common foods and estimated daily intake by children,adolescents,adults,and seniors of Catalonia,Spain[J].Journal of Agricultural&Food Chemistry,51(3):838-842.
MADSEN K B,ASKOV-HANSEN C,NAIMI R M,et al.,2013.Acute effects of continuous infusions of glucagon-like peptide(GLP)-1,GLP-2 and the combination(GLP-1+GLP-2)on intestinal absorption in short bowel syndrome(SBS)patients.A placebo-controlled study[J].Regulatory Peptides,184:30-39.
MAHAFFEY K R,FOWLER B A,1977.Effects of concurrent administration of lead,cadmium,and arsenic in the rat[J].Environmental Health Perspectives,19(2):165-171.
MASSóE L,CORREDOR L,ANTONIO M T,2007.Oxidative damage in liver after perinatal intoxication with lead and/or cadmium[J].Journal of Trace Elements in Medicine&Biology,21(3):210-216.
MIRANDA J,KRISHNAKUMAR G,D’SILVA A,2012.Removal of Pb2+from aqueous system by live Oscillatoria laete-virens(Crouan and Crouan)Gomont isolated from industrial effluents[J].World Journal of Microbiology&Biotechnology,28(10):3053-3065.
NAWAB J,KHAN S,SHAH M T,et al.,2015.Contamination of soil,medicinal,and fodder plants with lead and cadmium present in mine-affected areas,Northern Pakistan[J].Environmental Monitoring and Assessment,187(9):605.
PAN L Q,LIU N,ZHANG H X,et al.,2011.Effects of heavy metal ions(Cu2+,Pb2+and Cd2+)on DNA damage of the gills,hemocytes and hepatopancreas of marine crab,Charybdis japonica[J].Journal of Ocean University of China,10(2):177-184.
PILLAI A,GUPTA S,2005.Effect of gestational and lactational exposure to lead and/or cadmium on reproductive performance and hepatic oestradiol metabolising enzymes[J].Toxicology Letters,155(1):179-186.
RANI A,KUMAR A,LAL A,et al.,2014.Cellular mechanisms of cadmium-induced toxicity:a review[J].International Journal of Environmental Health Research,24(4):378-399.
ROGGEMAN S,DE BOECKG,DE COCK H,et al.,2014.Accumulation and detoxification of metals and arsenic in tissues of cattle(Bos taurus),and the risks for human consumption[J].Science of The Total Environment,466-467:175-184.
RUDEL D,DOUGLAS C D,HUFFNAGLE I M,et al.,2013.Assaying environmental nickel toxicity using model nematodes[J].PLoS ONE,8(10):e77079.
SABOLI?I,BRELJAK D,?KARICA M,et al.,2010.Role of metallothionein in cadmium traffic and toxicity in kidneys and other mammalian organs[J].BioMetal:23(5):897-926.
VALKO M,MORRIS H,2005.Cronin M T.Metals,toxicity and oxidative stress[J].Current Medicinal Chemistry,12(10):1161-1208.
WANG Y K,GAO S T,ZANG X H,et al.,2012.Graphene-based solid-phase extraction combined with flame atomic absorption spectrometry for a sensitive determination of trace amounts of lead in environmental water and vegetable samples[J].Analytica Chimica Acta,716:112-118.
XIA L P,CHEN S H,DAHMS H U,et al.,2016.Cadmium induced oxidative damage and apoptosis in the hepatopancreas of Meretrix meretrix[J].Ecotoxicology,25(5):959-969.
XU G,LIN G,LIN S,et al.,2016.The Reproductive Toxicity of CdSe/ZnSQuantum Dots on the in vivo Ovarian Function and in vitro Fertilization[J].Scientific Reports,6:37677.
XU L,XU Y F,ZHU W P,et al.,2012.Modulating the selectivity by switching sensing media:a bifunctional chemosensor selectivity for Cd2+and Pb2+in different aqueous solutions[J].RSC Advances,2(15):6323-6328.
YANG J L,WANG Y C,LIU G F,et al.,2011.Tamarix hispida metallothionein-like ThMT3,a reactive oxygen species scavenger,increases tolerance against Cd2+,Zn2+,Cu2+,and NaCl in transgenic yeast[J].Molecular Biology Reports,38(3):1567-1574.
ZHANG Y M,LIU X Z,HAO L U,et al.,2009.Lipid Peroxidation and Ultrastructural Modifications in Brain after Perinatal Exposure to Lead and/or Cadmium in Rat Pups[J].Biomedical and Environmental Sciences,22(5):423-429.
万永奇,谢维,2006.生命科学与人类疾病研究的重要模型:果蝇[J].生命科学,18(5):425-429.WAN Y Q,XIE W,2006.Drosophila:an important model organism for understanding basic biological and human disease mechanisms[J].Chinese Bulletin of Life Sciences,18(5):425-429.
郑双艳,刘清,张霞丽,等,2019.重金属胁迫下河蚬内脏中GST mRNA表达及酶活性分析[J].生态环境学报,28(2):369-375.ZHEN S Y,LIU Q,ZHANG X L,et al.,2019.Analysis of GST mRNAExpression and Enzymatic Activities in Corbicula fluminea Viscera Exposed to Heavy Metals[J].Ecology and Environmental Sciences,28(2):369-375.