金雀异黄素对尼罗罗非鱼（Oreochromis niloticus）生长的影响及其机制研究
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摘要
目前，随着水产养殖业的发展，对水产饲料的需求量大增。由于饲料中的主要原料动物蛋白的价格高且来源有限，大豆蛋白逐步成为首选替代品。大豆蛋白粉中富含大豆异黄酮，弄清大豆异黄酮对鱼类生长的影响对其生产应用十分重要。金雀异黄素(Genistein，4’,5,7-三羟基异黄酮)是大豆异黄酮中含量最高、活性最强的一种异黄酮类植物雌激素，化学结构类似于17β-雌二醇(E2)。
本论文以“新吉富”品系尼罗罗非鱼为实验动物，以含金雀异黄素浓度为0、30、300和3000g/g的饲料饲喂罗非鱼幼鱼8周，观察了金雀异黄素对罗非鱼生长的影响，并从营养和内分泌两方面初步探讨了金雀异黄素影响罗非鱼生长的作用机制。为科学评价大豆异黄酮对鱼类生长的影响，推广以大豆粉为蛋白源的新型鱼饲料提供重要的理论基础。研究结果表明：
1、以含0～3000g/g金雀异黄素的饵料饲喂罗非鱼幼鱼8周，30和300μg/g组鱼的终末均重和特定生长率与对照组无显著差异，而3000μg/g组比对照组显著降低。各处理组的摄食率、饲料系数、肝体比、脏体比和鱼体组成成分与对照组相比，没有显著差异。说明低浓度的金雀异黄素对罗非鱼的生长没有影响，而高浓度的金雀异黄素能够抑制罗非鱼的生长。
2、对罗非鱼主要消化酶的研究表明，含300μg/g金雀异黄素的饲料饲喂罗非鱼幼鱼8周后，其胃蛋白酶和肠淀粉酶的活性比对照组显著降低。3000μg/g饲料组罗非鱼胃蛋白酶、胰蛋白酶、肝淀粉酶和肠淀粉酶的活性与对照组相比均显著降低。胃淀粉酶和SOD的活性，各处理组与对照组相比没有显著差异。结果显示较高浓度的金雀异黄素能干扰罗非鱼的蛋白和糖代谢，降低罗非鱼对营养物质的吸收和转化。
3、鱼类的生长主要受下丘脑-垂体-肝脏的GH/IGF-I轴调控，垂体GH合成和分泌受到下丘脑分泌产生的ghrelin、GnRHs、NPY和PACAP等因子的调控。本文以含0～3000g/g金雀异黄素的饵料饲喂罗非鱼幼鱼8周后，采用RIA分析法和实时定量RT-PCR方法分别检测了血浆中GH和垂体GHmRNA，以及脑中调控垂体GH表达的因子如ghrelin、GnRHs、GnRHRs、NPY、NPYRs、PACAP等的mRNA表达水平。结果表明：随着饲料中金雀异黄素含量的增加，罗非鱼血浆GH水平和垂体GH mRNA表达量逐步降低，而且3000μg/g饲料组比对照组显著降低。这一变化趋势与罗非鱼生长状况相一致，证实了垂体GH在调控罗非鱼生长中的重要作用。对脑中调节垂体GH表达的主要因子的检测表明，3000μg/g金雀异黄素组鱼脑ghrelin mRNA表达量比对照组显著降低，其对垂体GH合成的促进作用受到抑制。此外，虽然3000μg/g组NPY mRNA表达量显著升高，但其受体基因NPY R1mRNA表达量却显著降低，因此NPY促进垂体合成GH的作用也被抑制。而各处理组中GnRHs、GnRHRs、NPY R2、PACAP mRNA的表达量与对照相比，均没有发生显著变化。说明高浓度金雀异黄素可能通过抑制GH/IGF-I生长轴线上游脑ghrelin、NPY R1的表达，进而降低了GH合成与分泌。
4、GH在脑垂体合成后，经血液循环运送到肝脏，与肝细胞表面的GHR结合，刺激肝细胞释放IGF-I， IGF-I与IGFBP3结合，经内分泌途径作用于靶细胞的IGF-IR，促进细胞的增殖和生长。以含0～3000g/g金雀异黄素的饵料饲喂罗非鱼幼鱼8周后，采用RIA分析法和实时定量RT-PCR方法分别检测了血浆中IGF-I和肝脏IGF-I、GHR1、GHR2、IGF-IR、IGFBP3mRNA水平。结果表明：随着饲料中金雀异黄素含量不断增加，罗非鱼血浆IGF-I水平和IGF-I mRNA表达量逐步降低，而且3000μg/g饲料组IGF-I mRNA表达量比对照组显著降低，这与生长及GH的表现一致。此外，3000μg/g饲料组的肝脏GHR2及IGF-IRmRNA表达量也比对照组显著降低，而肝脏IGFBP3mRNA表达水平比对照组显著升高。说明金雀异黄素可能通过抑制肝脏GHR2表达造成IGF-I合成的降低，并通过促进IGFBP3的合成使鱼体内具有活性的游离IGF-I水平降低，造成IGF-IR表达的减少，从而抑制了IGF-I介导的GH促生长作用。
综上所述，饵料中含较低浓度的金雀异黄素(0～300μg/g)对罗非鱼的生长无显著影响，高于3000μg/g的金雀异黄素能够显著抑制罗非鱼生长。其作用机理一方面通过抑制罗非鱼胃蛋白酶、胰蛋白酶、肝淀粉酶和肠淀粉酶等主要消化酶的活性，抑制罗非鱼蛋白质和糖的代谢，从而阻遏了罗非鱼对营养物质的消化和吸收；另一方面也通过影响罗非鱼的生长内分泌调控，高浓度金雀异黄素抑制了GH/IGF-I生长轴线上游脑ghrelin、NPY R1的表达，进而降低GH合成与分泌；通过抑制肝脏GHR2、IGF-IR表达和促进IGFBP3表达，造成IGF-I合成的降低和游离IGF-I的减少，从而抑制了IGF-I介导的GH促生长作用。
With the development of aquaculture, the demand for aquatic feed increasedgreatly. Moreover, Because of the high price and limited supply of animal protein, thesoybean protein has gradually become the preferred alternative. Soybean isoflavone isrich in soybean protein powder, so it is very important to find out the influence ofsoybean isoflavones on the growth of fish. Genistein shares structural features with17β-estradiol(E2) and it is one of the most potent and higest levels phytoestrogens insoybean and soy products.
Therefore, we chose "New GIFT Strain Nile tilapia" as the experimental animalin this paper, and fed tilapia diets for8weeks with dietary genistein concentration0,30g/g,300g/g and3000g/g, and determined the effect of genistein on the growthof tilapia, and from the two aspects of nutrition and endocrine discussed themechanism of genistein affecting the growth of Nile tilapia. Our study provided thetheoretical basis for the future scientific evaluation of genistein on fish and exploringnew type of fish feed which was taken soybean meal as protein source. The resultsshowed that:
1、With dietary genistein concentration0~3000g/g feeding tilapia diets for8weeks,30and300μg/g group of fish final weight and specific growth rate were notsignificantly different from control, while3000μg/g group decreased significantlycompared with control. Among each treatment group, feed intake, feed efficiencyratio, hepatosomatic index, viscerosomatic index and the fish body composition didnot differ significantly. It showed that low concentration of genistein had no effect onthe growth of tilapia, and high concentration of genistein could inhibit the growth oftilapia.
2、From the study on the main digestive enzymes of tilapia showed that theactivities of stomach protease and intestinal amylase of300μg/g group feeding tilapiaafter8weeks were significantly lower than those of the control. In the3000μg/g group, the activities of stomach protease, trypsin, liver amylase and intestinal amylasewere significantly lower than those of the control. There were no significantdifference in SOD activity and stomach amylase among each treatment. The resultssuggested high level of genistein could interfere in the proteometabolism andglycometabolism, and reduce the tilapia conversion and absorption of nutrients.
3、The growth of fish was mainly regulated by GH/IGF-I axis, and GH synthesisand secretion were regulated by ghrelin, GnRHs, NPY and PACAP which weresecreted by hyothalamus. With dietary genistein concentration0~3000g/g feedingtilapia diets for8weeks, GH levels in plasma were examined by radioimmunoassay.GH、ghrelin、GnRHs、GnRHRs、NPY、NPYRs and PACAP mRNA expression levelswere examined by real-time PCR. It turned out, GH levels in plasma and theexpression of mRNA decreased gradually in tilapia, and3000g/g group wassignificantly lower than that of the control, the changing trend was consistent with thegrowth of tilapia, and it confirmed the important role of pituitary GH in regulating thegrowth of tilapia. The detection on the main factors of hyothalamus which regulatedthe pituitary GH showed, the expression of ghrelin mRNA in3000μg/g group wassignificantly lower than that of the control treatment, so its promoting effect onpituitary GH was restrained. In addition, NPY mRNA expression reached the highestlevel in3000μg/g group, however, the expression level of NPY R1mRNA decreasedsignificantly. Its promoting effect on pituitary GH was also restrained. With theconcentration of dietary genistein increasing, the expressions of GnRHs, GnRHRs,NPYR2and PACAPmRNA were not significantly changed. It showed that highconcentration of genistein ruduced the synthesis and secretion of GH by inhibiting theexpression of ghrelin and NPY R1which were located on the up-stream of GH/IGF–Iaxis.
4、GH was synthesised in the pituitary, following the blood circulation to theliver, then combined with the GHR in liver cells and stimulated the liver cells toreleasing IGF-I which combined with the IGFBP3, through the endocrine function tothe target cells, and promoted cell proliferation and growth ultimately. With dietarygenistein concentration0~3000g/g feeding tilapia diets for8weeks, IGF-I levels in plasma were examined by radioimmunoassay. IGF-I、GHR1、GHR2、IGF-IR、IGFBP3mRNA expression levels in liver were examined by real-time PCR. IGF-I level inplasma and the expression of mRNA decreased gradually in tilapia, and3000g/ggroup was significantly lower than that of the control, which was consistent with theperformance of growth and GH. In addition, the expression level of GHR2andIGF-IR mRNA in3000μg/g group decreased significantly compared to the controltreatment, while IGFBP3mRNA increased significantly compared to the controltreatment. It suggested that genistein may reduce the synthesis of IGF-I by inhibitingthe expression of liver GHR2, and also reduced the levels of free IGF-I by promotingthe synthesis of IGFBP3, then resulted in the decrease of the expression of IGF-IR,thus inhibited the function of GH mediated by IGF–I.
In conclusion, it had no significant effect on the growth of tilapia in the lowconcentration (0~300g/g) of genistein, while it had significant effect when the theconcentration was higher than3000g/g. For its machanism, on one hand, it couldreduce the protein metabolism and glycometabolism of the tilapia by inhibiting themain activities of digestive enzymes of tilapia including stomach protease, trypsin,liver amylase and intestinal amylase, thus, reduce the tilapia conversion andabsorption of nutrients. On the other hand, it also could affect the GH/IGF–I axis.The high concentration of genistein could inhibit the expression of ghrelin and NPYR1, and thus reduced the synthesis and secretion of GH; By inhibiting the expressionof liver GHR2, IGF-IR, and IGFBP3, it reduced the synthesis of IGF-I and free IGF-I,resulting in inhibiting the function of GH mediated by IGF–I.
本论文以“新吉富”品系尼罗罗非鱼为实验动物，以含金雀异黄素浓度为0、30、300和3000g/g的饲料饲喂罗非鱼幼鱼8周，观察了金雀异黄素对罗非鱼生长的影响，并从营养和内分泌两方面初步探讨了金雀异黄素影响罗非鱼生长的作用机制。为科学评价大豆异黄酮对鱼类生长的影响，推广以大豆粉为蛋白源的新型鱼饲料提供重要的理论基础。研究结果表明：
1、以含0～3000g/g金雀异黄素的饵料饲喂罗非鱼幼鱼8周，30和300μg/g组鱼的终末均重和特定生长率与对照组无显著差异，而3000μg/g组比对照组显著降低。各处理组的摄食率、饲料系数、肝体比、脏体比和鱼体组成成分与对照组相比，没有显著差异。说明低浓度的金雀异黄素对罗非鱼的生长没有影响，而高浓度的金雀异黄素能够抑制罗非鱼的生长。
2、对罗非鱼主要消化酶的研究表明，含300μg/g金雀异黄素的饲料饲喂罗非鱼幼鱼8周后，其胃蛋白酶和肠淀粉酶的活性比对照组显著降低。3000μg/g饲料组罗非鱼胃蛋白酶、胰蛋白酶、肝淀粉酶和肠淀粉酶的活性与对照组相比均显著降低。胃淀粉酶和SOD的活性，各处理组与对照组相比没有显著差异。结果显示较高浓度的金雀异黄素能干扰罗非鱼的蛋白和糖代谢，降低罗非鱼对营养物质的吸收和转化。
3、鱼类的生长主要受下丘脑-垂体-肝脏的GH/IGF-I轴调控，垂体GH合成和分泌受到下丘脑分泌产生的ghrelin、GnRHs、NPY和PACAP等因子的调控。本文以含0～3000g/g金雀异黄素的饵料饲喂罗非鱼幼鱼8周后，采用RIA分析法和实时定量RT-PCR方法分别检测了血浆中GH和垂体GHmRNA，以及脑中调控垂体GH表达的因子如ghrelin、GnRHs、GnRHRs、NPY、NPYRs、PACAP等的mRNA表达水平。结果表明：随着饲料中金雀异黄素含量的增加，罗非鱼血浆GH水平和垂体GH mRNA表达量逐步降低，而且3000μg/g饲料组比对照组显著降低。这一变化趋势与罗非鱼生长状况相一致，证实了垂体GH在调控罗非鱼生长中的重要作用。对脑中调节垂体GH表达的主要因子的检测表明，3000μg/g金雀异黄素组鱼脑ghrelin mRNA表达量比对照组显著降低，其对垂体GH合成的促进作用受到抑制。此外，虽然3000μg/g组NPY mRNA表达量显著升高，但其受体基因NPY R1mRNA表达量却显著降低，因此NPY促进垂体合成GH的作用也被抑制。而各处理组中GnRHs、GnRHRs、NPY R2、PACAP mRNA的表达量与对照相比，均没有发生显著变化。说明高浓度金雀异黄素可能通过抑制GH/IGF-I生长轴线上游脑ghrelin、NPY R1的表达，进而降低了GH合成与分泌。
4、GH在脑垂体合成后，经血液循环运送到肝脏，与肝细胞表面的GHR结合，刺激肝细胞释放IGF-I， IGF-I与IGFBP3结合，经内分泌途径作用于靶细胞的IGF-IR，促进细胞的增殖和生长。以含0～3000g/g金雀异黄素的饵料饲喂罗非鱼幼鱼8周后，采用RIA分析法和实时定量RT-PCR方法分别检测了血浆中IGF-I和肝脏IGF-I、GHR1、GHR2、IGF-IR、IGFBP3mRNA水平。结果表明：随着饲料中金雀异黄素含量不断增加，罗非鱼血浆IGF-I水平和IGF-I mRNA表达量逐步降低，而且3000μg/g饲料组IGF-I mRNA表达量比对照组显著降低，这与生长及GH的表现一致。此外，3000μg/g饲料组的肝脏GHR2及IGF-IRmRNA表达量也比对照组显著降低，而肝脏IGFBP3mRNA表达水平比对照组显著升高。说明金雀异黄素可能通过抑制肝脏GHR2表达造成IGF-I合成的降低，并通过促进IGFBP3的合成使鱼体内具有活性的游离IGF-I水平降低，造成IGF-IR表达的减少，从而抑制了IGF-I介导的GH促生长作用。
综上所述，饵料中含较低浓度的金雀异黄素(0～300μg/g)对罗非鱼的生长无显著影响，高于3000μg/g的金雀异黄素能够显著抑制罗非鱼生长。其作用机理一方面通过抑制罗非鱼胃蛋白酶、胰蛋白酶、肝淀粉酶和肠淀粉酶等主要消化酶的活性，抑制罗非鱼蛋白质和糖的代谢，从而阻遏了罗非鱼对营养物质的消化和吸收；另一方面也通过影响罗非鱼的生长内分泌调控，高浓度金雀异黄素抑制了GH/IGF-I生长轴线上游脑ghrelin、NPY R1的表达，进而降低GH合成与分泌；通过抑制肝脏GHR2、IGF-IR表达和促进IGFBP3表达，造成IGF-I合成的降低和游离IGF-I的减少，从而抑制了IGF-I介导的GH促生长作用。
With the development of aquaculture, the demand for aquatic feed increasedgreatly. Moreover, Because of the high price and limited supply of animal protein, thesoybean protein has gradually become the preferred alternative. Soybean isoflavone isrich in soybean protein powder, so it is very important to find out the influence ofsoybean isoflavones on the growth of fish. Genistein shares structural features with17β-estradiol(E2) and it is one of the most potent and higest levels phytoestrogens insoybean and soy products.
Therefore, we chose "New GIFT Strain Nile tilapia" as the experimental animalin this paper, and fed tilapia diets for8weeks with dietary genistein concentration0,30g/g,300g/g and3000g/g, and determined the effect of genistein on the growthof tilapia, and from the two aspects of nutrition and endocrine discussed themechanism of genistein affecting the growth of Nile tilapia. Our study provided thetheoretical basis for the future scientific evaluation of genistein on fish and exploringnew type of fish feed which was taken soybean meal as protein source. The resultsshowed that:
1、With dietary genistein concentration0~3000g/g feeding tilapia diets for8weeks,30and300μg/g group of fish final weight and specific growth rate were notsignificantly different from control, while3000μg/g group decreased significantlycompared with control. Among each treatment group, feed intake, feed efficiencyratio, hepatosomatic index, viscerosomatic index and the fish body composition didnot differ significantly. It showed that low concentration of genistein had no effect onthe growth of tilapia, and high concentration of genistein could inhibit the growth oftilapia.
2、From the study on the main digestive enzymes of tilapia showed that theactivities of stomach protease and intestinal amylase of300μg/g group feeding tilapiaafter8weeks were significantly lower than those of the control. In the3000μg/g group, the activities of stomach protease, trypsin, liver amylase and intestinal amylasewere significantly lower than those of the control. There were no significantdifference in SOD activity and stomach amylase among each treatment. The resultssuggested high level of genistein could interfere in the proteometabolism andglycometabolism, and reduce the tilapia conversion and absorption of nutrients.
3、The growth of fish was mainly regulated by GH/IGF-I axis, and GH synthesisand secretion were regulated by ghrelin, GnRHs, NPY and PACAP which weresecreted by hyothalamus. With dietary genistein concentration0~3000g/g feedingtilapia diets for8weeks, GH levels in plasma were examined by radioimmunoassay.GH、ghrelin、GnRHs、GnRHRs、NPY、NPYRs and PACAP mRNA expression levelswere examined by real-time PCR. It turned out, GH levels in plasma and theexpression of mRNA decreased gradually in tilapia, and3000g/g group wassignificantly lower than that of the control, the changing trend was consistent with thegrowth of tilapia, and it confirmed the important role of pituitary GH in regulating thegrowth of tilapia. The detection on the main factors of hyothalamus which regulatedthe pituitary GH showed, the expression of ghrelin mRNA in3000μg/g group wassignificantly lower than that of the control treatment, so its promoting effect onpituitary GH was restrained. In addition, NPY mRNA expression reached the highestlevel in3000μg/g group, however, the expression level of NPY R1mRNA decreasedsignificantly. Its promoting effect on pituitary GH was also restrained. With theconcentration of dietary genistein increasing, the expressions of GnRHs, GnRHRs,NPYR2and PACAPmRNA were not significantly changed. It showed that highconcentration of genistein ruduced the synthesis and secretion of GH by inhibiting theexpression of ghrelin and NPY R1which were located on the up-stream of GH/IGF–Iaxis.
4、GH was synthesised in the pituitary, following the blood circulation to theliver, then combined with the GHR in liver cells and stimulated the liver cells toreleasing IGF-I which combined with the IGFBP3, through the endocrine function tothe target cells, and promoted cell proliferation and growth ultimately. With dietarygenistein concentration0~3000g/g feeding tilapia diets for8weeks, IGF-I levels in plasma were examined by radioimmunoassay. IGF-I、GHR1、GHR2、IGF-IR、IGFBP3mRNA expression levels in liver were examined by real-time PCR. IGF-I level inplasma and the expression of mRNA decreased gradually in tilapia, and3000g/ggroup was significantly lower than that of the control, which was consistent with theperformance of growth and GH. In addition, the expression level of GHR2andIGF-IR mRNA in3000μg/g group decreased significantly compared to the controltreatment, while IGFBP3mRNA increased significantly compared to the controltreatment. It suggested that genistein may reduce the synthesis of IGF-I by inhibitingthe expression of liver GHR2, and also reduced the levels of free IGF-I by promotingthe synthesis of IGFBP3, then resulted in the decrease of the expression of IGF-IR,thus inhibited the function of GH mediated by IGF–I.
In conclusion, it had no significant effect on the growth of tilapia in the lowconcentration (0~300g/g) of genistein, while it had significant effect when the theconcentration was higher than3000g/g. For its machanism, on one hand, it couldreduce the protein metabolism and glycometabolism of the tilapia by inhibiting themain activities of digestive enzymes of tilapia including stomach protease, trypsin,liver amylase and intestinal amylase, thus, reduce the tilapia conversion andabsorption of nutrients. On the other hand, it also could affect the GH/IGF–I axis.The high concentration of genistein could inhibit the expression of ghrelin and NPYR1, and thus reduced the synthesis and secretion of GH; By inhibiting the expressionof liver GHR2, IGF-IR, and IGFBP3, it reduced the synthesis of IGF-I and free IGF-I,resulting in inhibiting the function of GH mediated by IGF–I.
引文
艾庆辉,谢小军.南方鲇的营养学研究:饲料中大豆蛋白水平对摄食率和消化率的影响.水生生物学报,2002b,26(3):215-220.
蔡英华,几种大豆抗营养因子对牙鲆(Paralichthys olivaceus)生长和消化生理的影响,中国海洋大学,2006.
陈洁，金雀异黄素对雄性斑马鱼VTG的诱导及其机理研究，中国海洋大学,2010.
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