刀鲚PPARγ基因的cDNA克隆及其应激应答
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摘要
旨在研究刀鲚(Coilia nasus)过氧化物酶体增殖物激活受体γ(peroxisome proliferator activated receptor, PPARγ)基因的应激调控表达,克隆并获得了刀鲚PPARγ基因的cDNA全长。刀鲚PPARγ基因的cDNA全长1951 bp,开放阅读框1470 bp,预测编码489个氨基酸。刀鲚PPARγ包括4个功能结构域,即A/B区, DNA结合区(DNA binding domain, DBD区),铰链区,配体结合区(ligand binding domain, LBD区)。运用荧光定量PCR (real time quantitative PCR, RT-qPCR)检测刀鲚PPARγ基因在不同组织、运输胁迫和胚胎发育时期的表达。结果显示,刀鲚PPARγ在各组织中均有表达,其中在肝中表达量最高,在脑、肠、心脏、肾、头肾、肌肉中相对高表达,在鳃和脾中微量表达。运输胁迫过程中, PPARγ基因表达显著上调(P<0.05),在4 h达到峰值,随后显著降低,但仍高于对照组。PPARγ在胚胎发育时期各时期均表达,其中在受精卵时期高表达,随后表达量急剧降低,并在此后的时期一直处于较低的表达水平。PPARγ基因在应激过程中发挥重要作用,也是胚胎发育过程中重要的基因。本研究为刀鲚的人工繁育和应激调控提供了理论基础。
Coilia nasus is a commercially important fish species that is valued for its nutritive value and is used as a delicacy. It is widely distributed in the Yangtze River, coastal waters of China and Korea, and Ariake Sound in Japan. C. nasus is highly responsive to stress, which often causes tissue damage, apoptosis, and ultimately death during loading and transport, hampering the development of this industry. Peroxisome proliferator-activated receptors(PPARs) are ligand-dependent transcription factors belonging to the nuclear receptor superfamily. Like other nuclear receptors, PPARs consist of four domains that have distinct functions. The A/B domain, located in conserved N-terminus, is responsible for ligand-independent transcription activity. The C domain, which is the DNA-binding domain(DBD), contains two zinc finger structures. The D domain, the hinge region, connects the DBD with the ligand-binding domain(LBD) and is involved in the conformational changes of PPARs. The E/F domain is an LBD. Transcriptional activation by PPARs requires the presence of PPAR response elements(PPREs)in the promoter of the target gene. PPARs bind PPREs as heterodimers with retinoid X receptor. Three isoforms of PPARs, PPARα, PPARβ, and PPARγ, have been cloned in various mammals and fish. PPARγ is involved in many processes such as ontogenesis, lipid metabolism regulation, peroxisome biogenesis, immune functions and inflammation, and oxidative stress. The aim of this study was to investigate the stress response and expression of PPARγ during the embryonic development of C. nasus. Full-length PPARγ cDNA was obtained, which contained1951 base pairs with an open reading frame of 1470 base pairs, encoding 489 amino acids. PPARγ has four functional domains, A/B region, DBD, hinge region, and LBD. Real-time quantitative PCR was used to detect the expression of PPARγ in different tissues and under transport stress. The results showed that C. nasus PPARγ was expressed in all tissues, with the highest expression observed in the liver, relatively high expression detected in the brain, intestine, heart, kidney, head kidney, and muscle, and low expression in the gill and spleen. During transport stress, PPARγ expression was significantly up-regulated(P<0.05), peaked at 4 h, and was then significantly down-regulated. High expression of PPARγ may increase lipid metabolism and relieve inflammation and apoptosis.PPARγ plays an important role in lipid metabolism and stress responses. During embryonic development, PPARγshows the highest expression in the fertilized egg stage, after which its expression is rapidly decreased and then remains at a lower level. Lower expression of PPARγ may down-regulate lipid metabolism and transportation. This study provides information regarding the theoretical basis of stress regulation.
Coilia nasus is a commercially important fish species that is valued for its nutritive value and is used as a delicacy. It is widely distributed in the Yangtze River, coastal waters of China and Korea, and Ariake Sound in Japan. C. nasus is highly responsive to stress, which often causes tissue damage, apoptosis, and ultimately death during loading and transport, hampering the development of this industry. Peroxisome proliferator-activated receptors(PPARs) are ligand-dependent transcription factors belonging to the nuclear receptor superfamily. Like other nuclear receptors, PPARs consist of four domains that have distinct functions. The A/B domain, located in conserved N-terminus, is responsible for ligand-independent transcription activity. The C domain, which is the DNA-binding domain(DBD), contains two zinc finger structures. The D domain, the hinge region, connects the DBD with the ligand-binding domain(LBD) and is involved in the conformational changes of PPARs. The E/F domain is an LBD. Transcriptional activation by PPARs requires the presence of PPAR response elements(PPREs)in the promoter of the target gene. PPARs bind PPREs as heterodimers with retinoid X receptor. Three isoforms of PPARs, PPARα, PPARβ, and PPARγ, have been cloned in various mammals and fish. PPARγ is involved in many processes such as ontogenesis, lipid metabolism regulation, peroxisome biogenesis, immune functions and inflammation, and oxidative stress. The aim of this study was to investigate the stress response and expression of PPARγ during the embryonic development of C. nasus. Full-length PPARγ cDNA was obtained, which contained1951 base pairs with an open reading frame of 1470 base pairs, encoding 489 amino acids. PPARγ has four functional domains, A/B region, DBD, hinge region, and LBD. Real-time quantitative PCR was used to detect the expression of PPARγ in different tissues and under transport stress. The results showed that C. nasus PPARγ was expressed in all tissues, with the highest expression observed in the liver, relatively high expression detected in the brain, intestine, heart, kidney, head kidney, and muscle, and low expression in the gill and spleen. During transport stress, PPARγ expression was significantly up-regulated(P<0.05), peaked at 4 h, and was then significantly down-regulated. High expression of PPARγ may increase lipid metabolism and relieve inflammation and apoptosis.PPARγ plays an important role in lipid metabolism and stress responses. During embryonic development, PPARγshows the highest expression in the fertilized egg stage, after which its expression is rapidly decreased and then remains at a lower level. Lower expression of PPARγ may down-regulate lipid metabolism and transportation. This study provides information regarding the theoretical basis of stress regulation.
引文
[1]Jiang T,Yang J,Liu H B,et al.Life history of Coilia nasus,from the Yellow Sea inferred from otolith Sr:Ca ratios[J].Environmental Biology of Fishes,2012,95(4):503-508.
[2]Xu G C,Du F K,Nie Z J,et al.Effects of 10‰salinity to the plasma osmotic pressure,cortisol,glucose and liver glycogen in Colilia nasus stressed during loading and transportation[J].Acta Hydrobiologica Sinica,2015,39(1):66-72.[徐钢春,杜富宽,聂志娟,等.10‰盐度对长江刀鲚幼鱼装载和运输胁迫中应激指标的影响[J].水生生物学报,2015,39(1):66-72.]
[3]Gao J W,Du F K,Gu R B,et al.Effect of transport stress on physiological-biochemical indices and expression of HPIgenes and roles of glycyrrhizia on transport response in Coilia nasus[J].Journal of Shanghai Ocean University,2015,24(6):817-825.[高金伟,杜富宽,顾若波,等.运输应激对刀鲚生理生化指标和HPI轴基因表达影响及甘草甜素的作用[J].上海海洋大学学报,2015,24(6):817-825.]
[4]Du F K,Xu G C,Nie Z J,et al.Transcriptome analysis gene expression in the liver of Coilia nasus during the stress response[J].BMC Genomics,2014,15(1):558.
[5]Issemann I,Green S.Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators[J].Nature,1990,347:645-650.
[6]Gao J,Xu G C,Du F K,et al.Tissue expressions and functions of PPARs genes in fish[J].Journal of Yangtze University:Natural Science Edition,2016,13(33):43-46.[高俊,徐钢春,杜富宽,等.鱼类PPARs基因组织表达及功能研究进展[J].长江大学学报:自然科学版,2016,13(33):43-46.]
[7]Schadinger S E,Bucher N L R,Schreiber B M,et al.PPARγ2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes[J].American Journal of Physiology Endocrinology and Metabolism,2005,288(6):1195-1205.
[8]Yu Y H,Wu S C,Cheng W T,et al.The function of porcine PPARγand dietary fish oil effect on the expression of lipid and glucose metabolism related genes[J].Journal of Nutritional Biochemistry,2011,22(2):179-186.
[9]Thomas A W,Davies N A,Moir H,et al.Exercise-associated generation of PPARγligands activates PPARγsignaling events and upregulates genes related to lipid metabolism[J].Journal of Applied Physiology,2012,112(5):806-815.
[10]Almeida P E,Carneiro A B,Silva A R,et al.PPARγExpression and function in mycobacterial infection:Roles in lipid metabolism,immunity,and bacterial killing[J].PPAR Research,2012,2012:Article ID 383829.
[11]Savage D B,Tan G D,Acerini C L,et al.Human metabolic syndrome resulting from dominant-negative mutations in the nuclear receptor peroxisome proliferator-activated receptor-γ[J].Diabetes,2003,52(4):910-917.
[12]Alvares K,Fan C,Dadras S S,et al.An upstream region of the enoyl-coenzyme A hydratase/3-hydroxyacyl-coenzyme Adehydrogenase gene directs luciferase expression in liver in response to peroxisome proliferators in transgenic mice[J].Cancer Research,1994,54(9):2303-2306.
[13]Bardot O,Aldridge T C,Latruffe N,et al.PPAR-RXR heterodimer activates a peroxisome proliferator response element upstream of the bifunctional enzyme gene[J].Biochemical and Biophysical Research Communications,1993,192(1):37-45.
[14]Marcus S L,Miyata K S,Zhang B,et al.Diverse peroxisome proliferator-activated receptors bind to the peroxisome proliferator-responsive elements of the rat hydratase/dehydrogenase and fatty acyl-Co A oxidase genes but differentially induce expression[J].Proceedings of the National Academy of Sciences of the United States of America,1993,90(12):5723-5727.
[15]Osumi T,Osada S,Tsukamoto T.Analysis of peroxisome proliferator-responsive enhancer of the rat acyl-CoA oxidase gene[J].Annals of the New York Academy of Sciences,1996,804:706-708.
[16]Zhang Y,Cui Y,Wang X L,et al.PPARα/γagonists and antagonists differently affect hepatic lipid metabolism,oxidative stress and inflammatory cytokine production in steatohepatitic rats[J].Cytokine,2015,75(1):127-135.
[17]Girnun G D,Domann F E,Moore S A,et al.Identification of a functional peroxisome proliferator-activated receptor response element in the rat catalase promoter[J].Molecular Endocrinology,2003,16:2793-2801.
[18]Collino M,Aragno M,Mastrocola R,et al.Modulation of the oxidative stress and inflammatory response by PPAR-γagonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion[J].European Journal of Pharmacology,2006,530(1-2):70-80.
[19]Varga T,Czimmerer Z,Nagy L.PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation[J].Biochimica et Biophysica Acta(BBA)-Molecular Basis of Disease,2011,1812(8):1007-1022.
[20]Peng S Y,Xu J M,Ruan W B,et al.PPAR-γactivation prevents septic cardiac dysfunction via inhibition of apoptosis and necroptosis[J].Oxidative Medicine and Cellular Longevity,2017,2017:Article ID 8326749.
[21]Ren Y S,Sun C B,Sun Y,et al.PPAR gamma protects cardiomyocytes against oxidative stress and apoptosis via Bcl-2 upregulation[J].Vascular Pharmacology,2009,51(2-3):169-174.
[22]Zheng J L,Zhuo M Q,Luo Z,et al.Peroxisome proliferator-activated receptor gamma(PPARγ)in yellow catfish Pelteobagrus fulvidraco:molecular characterization,mRNAexpression and transcriptional regulation by insulin in vivo and in vitro[J].General and Comparative Endocrinology,2015,212:51-62.
[23]Cho H K,Kong H J,Nam B H,et al.Molecular cloning and characterization of olive flounder(Paralichthys olivaceus)peroxisome proliferator-activated receptorγ[J].General and Comparative Endocrinology,2009,163(3):251-258.
[24]Dong X J,Xu H G,Mai K S,et al.Cloning and characterization of SREBP-1 and PPAR-αin Japanese seabass Lateolabrax japonicus,and their gene expressions in response to different dietary fatty acid profiles[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2015,180:48-56.
[25]Luo S W,Huang Y H,Xie F X,et al.Molecular cloning,characterization and expression analysis of PPAR gamma in the orange-spotted grouper(Epinephelus coioides)after the Vibrio alginolyticus challenge[J].Fish&Shellfish Immunology,2015,43(2):310-324.
[26]Press C M,Evensen?.The morphology of the immune system in teleost fishes[J].Fish&Shellfish Immunology,1999,9(4):309-318.
[27]Du F K,Xu G C,Li Y,et al.Cloning of POMC c DNA and the stress response in Coilia nasus[J].Journal of Fishery Sciences of China,2017,24(2):231-238.[杜富宽,徐钢春,黎燕,等.刀鲚POMC基因的c DNA克隆及其应激应答[J].中国水产科学,2017,24(2):231-238.]
[28]Ibabe A,Bilbao E,Cajaraville M P.Expression of peroxisome proliferator-activated receptors in zebrafish(Danio rerio)depending on gender and developmental stage[J].Histochemistry and Cell Biology,2005,123(1):75-87.
[29]Ibabe A,Grabenbauer M,Baumgart E,et al.Expression of peroxisome proliferator-activated receptors in the liver of gray mullet(Mugil cephalus)[J].Acta Histochemica,2004,106(1):11-19.
[30]Tsai M L,Chen H Y,Tseng M C,et al.Cloning of peroxisome proliferators activated receptors in the cobia(Rachycentron canadum)and their expression at different life-cycle stages under cage aquaculture[J].Gene,2008,425(1-2):69-78.
[31]Du F K,Xu G C,Gao J W,et al.Transport-induced changes in hypothalamic-pituitary-interrenal axis gene expression and oxidative stress responses in Coilia nasus[J].Aquaculture Research,2016,47(11):3599-3607.
[32]Collino M,Aragno M,Mastrocola R,et al.Modulation of the oxidative stress and inflammatory response by PPAR-γagonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion[J].European Journal of Pharmacology,2006,530(1-2):70-80.
[33]Liu Y L,Shi J X,Lu J,et al.Effects of lipopolysaccharide challenge on PPARγexpression in hypothalamus pituitary gland adrenal gland axis of weanling pigs[J].Chinese Journal of Animal Science,2011,47(1):25-28.[刘玉兰,石君霞,鲁晶,等.脂多糖刺激对断奶仔猪下丘脑-垂体-肾上腺轴PPARγ表达的影响[J].中国畜牧杂志,2011,47(1):25-28.]
[34]Winczyk K,Pawlikowski M.Immunohistochemical detection of PPARgamma receptors in the human pituitary adenomas:correlation with PCNA[J].Folia Histochemica et Cytobiologica,2005,43(3):137-141.
[35]Betz M J,Shapiro I,Fassnacht M,et al.Peroxisome proliferator-activated receptor-γagonists suppress adrenocortical tumor cell proliferation and induce differentiation[J].The Journal of Clinical Endocrinology&Metabolism,2005,90(7):3886-3896.
[36]Michalik L,Desvergne B,Dreyer C,et al.PPAR expression and function during vertebrate development[J].Bioinformatiocs,2004,46(1):105-114.
[37]Cunha I,Galante-Oliveira S,Rocha E,et al.Dynamics of PPARs,fatty acid metabolism genes and lipid classes in eggs and early larvae of a teleost[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2013,164(4):247-258.
[38]Cunha I,Galante-Oliveira S,Rocha E,et al.Expression of intercellular lipid transport and cholesterol metabolism genes in eggs and early larvae stages of turbot,Scophthalmus maximus,a marine aquaculture species[J].Marine Biology,2015,162(8):1673-1683.
[39]Boulekbache H.Energy metabolism in fish development[J].American Zoologist,1981,21(2):377-389.
[40]Ohkubo N,Sawaguchi S,Hamatsu T,et al.Utilization of free amino acids,yolk proteins and lipids in developing eggs and yolk-sac larvae of walleye pollock Theragra chalcogramma[J].Fisheries Science,2006,72(3):620-630.
[41]Zhu P,Parrish C C,Brown J A.Lipid and amino acid metabolism during early development of Atlantic halibut(Hippoglossus hippoglossus)[J].Aquaculture International,2003,11(1-2):43-52.
[2]Xu G C,Du F K,Nie Z J,et al.Effects of 10‰salinity to the plasma osmotic pressure,cortisol,glucose and liver glycogen in Colilia nasus stressed during loading and transportation[J].Acta Hydrobiologica Sinica,2015,39(1):66-72.[徐钢春,杜富宽,聂志娟,等.10‰盐度对长江刀鲚幼鱼装载和运输胁迫中应激指标的影响[J].水生生物学报,2015,39(1):66-72.]
[3]Gao J W,Du F K,Gu R B,et al.Effect of transport stress on physiological-biochemical indices and expression of HPIgenes and roles of glycyrrhizia on transport response in Coilia nasus[J].Journal of Shanghai Ocean University,2015,24(6):817-825.[高金伟,杜富宽,顾若波,等.运输应激对刀鲚生理生化指标和HPI轴基因表达影响及甘草甜素的作用[J].上海海洋大学学报,2015,24(6):817-825.]
[4]Du F K,Xu G C,Nie Z J,et al.Transcriptome analysis gene expression in the liver of Coilia nasus during the stress response[J].BMC Genomics,2014,15(1):558.
[5]Issemann I,Green S.Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators[J].Nature,1990,347:645-650.
[6]Gao J,Xu G C,Du F K,et al.Tissue expressions and functions of PPARs genes in fish[J].Journal of Yangtze University:Natural Science Edition,2016,13(33):43-46.[高俊,徐钢春,杜富宽,等.鱼类PPARs基因组织表达及功能研究进展[J].长江大学学报:自然科学版,2016,13(33):43-46.]
[7]Schadinger S E,Bucher N L R,Schreiber B M,et al.PPARγ2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes[J].American Journal of Physiology Endocrinology and Metabolism,2005,288(6):1195-1205.
[8]Yu Y H,Wu S C,Cheng W T,et al.The function of porcine PPARγand dietary fish oil effect on the expression of lipid and glucose metabolism related genes[J].Journal of Nutritional Biochemistry,2011,22(2):179-186.
[9]Thomas A W,Davies N A,Moir H,et al.Exercise-associated generation of PPARγligands activates PPARγsignaling events and upregulates genes related to lipid metabolism[J].Journal of Applied Physiology,2012,112(5):806-815.
[10]Almeida P E,Carneiro A B,Silva A R,et al.PPARγExpression and function in mycobacterial infection:Roles in lipid metabolism,immunity,and bacterial killing[J].PPAR Research,2012,2012:Article ID 383829.
[11]Savage D B,Tan G D,Acerini C L,et al.Human metabolic syndrome resulting from dominant-negative mutations in the nuclear receptor peroxisome proliferator-activated receptor-γ[J].Diabetes,2003,52(4):910-917.
[12]Alvares K,Fan C,Dadras S S,et al.An upstream region of the enoyl-coenzyme A hydratase/3-hydroxyacyl-coenzyme Adehydrogenase gene directs luciferase expression in liver in response to peroxisome proliferators in transgenic mice[J].Cancer Research,1994,54(9):2303-2306.
[13]Bardot O,Aldridge T C,Latruffe N,et al.PPAR-RXR heterodimer activates a peroxisome proliferator response element upstream of the bifunctional enzyme gene[J].Biochemical and Biophysical Research Communications,1993,192(1):37-45.
[14]Marcus S L,Miyata K S,Zhang B,et al.Diverse peroxisome proliferator-activated receptors bind to the peroxisome proliferator-responsive elements of the rat hydratase/dehydrogenase and fatty acyl-Co A oxidase genes but differentially induce expression[J].Proceedings of the National Academy of Sciences of the United States of America,1993,90(12):5723-5727.
[15]Osumi T,Osada S,Tsukamoto T.Analysis of peroxisome proliferator-responsive enhancer of the rat acyl-CoA oxidase gene[J].Annals of the New York Academy of Sciences,1996,804:706-708.
[16]Zhang Y,Cui Y,Wang X L,et al.PPARα/γagonists and antagonists differently affect hepatic lipid metabolism,oxidative stress and inflammatory cytokine production in steatohepatitic rats[J].Cytokine,2015,75(1):127-135.
[17]Girnun G D,Domann F E,Moore S A,et al.Identification of a functional peroxisome proliferator-activated receptor response element in the rat catalase promoter[J].Molecular Endocrinology,2003,16:2793-2801.
[18]Collino M,Aragno M,Mastrocola R,et al.Modulation of the oxidative stress and inflammatory response by PPAR-γagonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion[J].European Journal of Pharmacology,2006,530(1-2):70-80.
[19]Varga T,Czimmerer Z,Nagy L.PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation[J].Biochimica et Biophysica Acta(BBA)-Molecular Basis of Disease,2011,1812(8):1007-1022.
[20]Peng S Y,Xu J M,Ruan W B,et al.PPAR-γactivation prevents septic cardiac dysfunction via inhibition of apoptosis and necroptosis[J].Oxidative Medicine and Cellular Longevity,2017,2017:Article ID 8326749.
[21]Ren Y S,Sun C B,Sun Y,et al.PPAR gamma protects cardiomyocytes against oxidative stress and apoptosis via Bcl-2 upregulation[J].Vascular Pharmacology,2009,51(2-3):169-174.
[22]Zheng J L,Zhuo M Q,Luo Z,et al.Peroxisome proliferator-activated receptor gamma(PPARγ)in yellow catfish Pelteobagrus fulvidraco:molecular characterization,mRNAexpression and transcriptional regulation by insulin in vivo and in vitro[J].General and Comparative Endocrinology,2015,212:51-62.
[23]Cho H K,Kong H J,Nam B H,et al.Molecular cloning and characterization of olive flounder(Paralichthys olivaceus)peroxisome proliferator-activated receptorγ[J].General and Comparative Endocrinology,2009,163(3):251-258.
[24]Dong X J,Xu H G,Mai K S,et al.Cloning and characterization of SREBP-1 and PPAR-αin Japanese seabass Lateolabrax japonicus,and their gene expressions in response to different dietary fatty acid profiles[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2015,180:48-56.
[25]Luo S W,Huang Y H,Xie F X,et al.Molecular cloning,characterization and expression analysis of PPAR gamma in the orange-spotted grouper(Epinephelus coioides)after the Vibrio alginolyticus challenge[J].Fish&Shellfish Immunology,2015,43(2):310-324.
[26]Press C M,Evensen?.The morphology of the immune system in teleost fishes[J].Fish&Shellfish Immunology,1999,9(4):309-318.
[27]Du F K,Xu G C,Li Y,et al.Cloning of POMC c DNA and the stress response in Coilia nasus[J].Journal of Fishery Sciences of China,2017,24(2):231-238.[杜富宽,徐钢春,黎燕,等.刀鲚POMC基因的c DNA克隆及其应激应答[J].中国水产科学,2017,24(2):231-238.]
[28]Ibabe A,Bilbao E,Cajaraville M P.Expression of peroxisome proliferator-activated receptors in zebrafish(Danio rerio)depending on gender and developmental stage[J].Histochemistry and Cell Biology,2005,123(1):75-87.
[29]Ibabe A,Grabenbauer M,Baumgart E,et al.Expression of peroxisome proliferator-activated receptors in the liver of gray mullet(Mugil cephalus)[J].Acta Histochemica,2004,106(1):11-19.
[30]Tsai M L,Chen H Y,Tseng M C,et al.Cloning of peroxisome proliferators activated receptors in the cobia(Rachycentron canadum)and their expression at different life-cycle stages under cage aquaculture[J].Gene,2008,425(1-2):69-78.
[31]Du F K,Xu G C,Gao J W,et al.Transport-induced changes in hypothalamic-pituitary-interrenal axis gene expression and oxidative stress responses in Coilia nasus[J].Aquaculture Research,2016,47(11):3599-3607.
[32]Collino M,Aragno M,Mastrocola R,et al.Modulation of the oxidative stress and inflammatory response by PPAR-γagonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion[J].European Journal of Pharmacology,2006,530(1-2):70-80.
[33]Liu Y L,Shi J X,Lu J,et al.Effects of lipopolysaccharide challenge on PPARγexpression in hypothalamus pituitary gland adrenal gland axis of weanling pigs[J].Chinese Journal of Animal Science,2011,47(1):25-28.[刘玉兰,石君霞,鲁晶,等.脂多糖刺激对断奶仔猪下丘脑-垂体-肾上腺轴PPARγ表达的影响[J].中国畜牧杂志,2011,47(1):25-28.]
[34]Winczyk K,Pawlikowski M.Immunohistochemical detection of PPARgamma receptors in the human pituitary adenomas:correlation with PCNA[J].Folia Histochemica et Cytobiologica,2005,43(3):137-141.
[35]Betz M J,Shapiro I,Fassnacht M,et al.Peroxisome proliferator-activated receptor-γagonists suppress adrenocortical tumor cell proliferation and induce differentiation[J].The Journal of Clinical Endocrinology&Metabolism,2005,90(7):3886-3896.
[36]Michalik L,Desvergne B,Dreyer C,et al.PPAR expression and function during vertebrate development[J].Bioinformatiocs,2004,46(1):105-114.
[37]Cunha I,Galante-Oliveira S,Rocha E,et al.Dynamics of PPARs,fatty acid metabolism genes and lipid classes in eggs and early larvae of a teleost[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2013,164(4):247-258.
[38]Cunha I,Galante-Oliveira S,Rocha E,et al.Expression of intercellular lipid transport and cholesterol metabolism genes in eggs and early larvae stages of turbot,Scophthalmus maximus,a marine aquaculture species[J].Marine Biology,2015,162(8):1673-1683.
[39]Boulekbache H.Energy metabolism in fish development[J].American Zoologist,1981,21(2):377-389.
[40]Ohkubo N,Sawaguchi S,Hamatsu T,et al.Utilization of free amino acids,yolk proteins and lipids in developing eggs and yolk-sac larvae of walleye pollock Theragra chalcogramma[J].Fisheries Science,2006,72(3):620-630.
[41]Zhu P,Parrish C C,Brown J A.Lipid and amino acid metabolism during early development of Atlantic halibut(Hippoglossus hippoglossus)[J].Aquaculture International,2003,11(1-2):43-52.