Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (17): 3437-3449.doi: 10.3864/j.issn.0578-1752.2022.17.014

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Effects and Mechanisms of Exogenous GABA Against Oxidative Stress in Piglets

YANG ChangPei1(),WANG NaiXiu1,WANG Kai1,HUANG ZiQing1,LIN HaiLan1,ZHANG Li1,ZHANG Chen1,FENG LuQiu1,GAN Ling1,2,*()   

  1. 1College of Veterinary Medicine, Southwest University, Chongqing 402460
    2Chongqing Veterinary Engineering Research Center/ Key Laboratory of Pig Raising Science, Ministry of Agriculture and Rural Affairs/Chongqing Municipal Key Laboratory of Pig Raising Science, Chongqing 402460
  • Received:2021-07-25 Accepted:2022-06-16 Online:2022-09-01 Published:2022-09-07
  • Contact: Ling GAN E-mail:924927733@qq.com;gl9089@sina.com

Abstract:

【Objective】 The purpose of this paper is to study the effect of exogenous γ-aminobutyric acid against oxidative stress in piglets, and the possible mediating role of hippocampal neuron γ-aminobutyric acid receptors regulating apoptosis signaling pathways in it, which will provide scientific basis for the application of γ-aminobutyric acid as animal stress regulator. 【Method】 bbbbbBased on the successful establishment of oxidative stress model in piglet and rat hippocampal neurons, the effects of exogenous GABA on piglets under oxidative stress, including oxidative / antioxidant related indexes, growth performance related indexes and GABA receptor in serum and hippocampus, along with the GABA receptor and apoptosis signal pathway related indexes in hippocampal neurons were investigated. 【Result】 The serum MDA levels of piglets in the low, medium, and high concentration GABA feeding groups (LD+OS; MD+OS; HD+OS) were extremely significantly lower than those in the oxidative stress (OS) group (P<0.01), the GSH level was extremely significantly higher than that in the OS group (P<0.01), and the T-AOC level in the HD+OS group was extremely significantly higher than that in the OS group and control group (P<0.01). And the high concentration (100 mg·kg-1 BW) of GABA more decreased the MDA level and more increased the GSH level in serum of piglets than those of the low concentration (20 mg·kg-1 BW) and middle concentration (60 mg·kg-1 BW) of GABA. Therefore, the follow-up study only investigated the anti-oxidative stress effect and mechanism of 100 mg·kg-1 BW. The daily gains of piglets at 0-7 days, 8-14 days and 0-28 days in the OS group were extremely significantly lower than those in the control group (P<0.01),the daily gains of piglets at 0-7 days, 8-14 days and 0-28 days in the HD+OS group were extremely significantly higher than those in the OS group (P<0.01), the daily gain of piglets aged 15-28 days in the OS group was significantly lower than that in the control group (P<0.05),the daily gain of piglets aged 15-28 days in the HD+OS group was extremely significantly higher than that in the OS group (P<0.01). The above results showed that the 100 mg·kg-1 BW GABA feeding extremely significantly increased the daily gain of piglets. There was no significant difference in the diarrhea rate of the control group, OS group and HD+OS group in the first, middle and late stages (P>0.05). The MDA level of hippocampus in the OS group was significantly higher than that of the control group and HD+OS group (P<0.01), the T-AOC and GSH levels were extremely significantly lower than the other two groups (P<0.01), which showed that GABA feeding would improve the antioxidant capacity of hippocampus. The levels of GABAA and GABAB receptors in the hippocampus of the HD+OS group were extremely significantly higher than those in the control group and the OS group (P<0.01), which showed that GABA feeding increased the levels of GABAA and GABAB in hippocampus. The Bcl-2 level in the hippocampus of the OS group was significantly lower than that of the control group (P<0.05), and the Bax and Caspase-3 levels were extremely significantly higher than those of the control group (P<0.01). The Bcl-2 level of the HD+OS group was extremely significantly higher than that of the OS group (P<0.01), the Bax level was extremely significantly lower than that of the OS group (P<0.01), and the Caspase-3 level was significantly lower than that of the OS group (P<0.05). Consistent with this, the Bax and Caspase-3 levels in hippocampal neurons of rats in the OS group, GABA+OS+Picrotoxin group and GABA+OS+CGP54626 group were significantly higher than those in the control group and GABA group (P<0.05), which indicated that GABA alleviated the damage of hippocampal neurons under oxidative stress, and the addition of GABA receptor inhibitors blocked the anti-stress damage effect of GABA. 【Conclusion】 GABA reduced the level of oxidative stress in the hippocampus of piglets. The anti-stress mechanism of GABA could be related to the decrease of the expression of apoptotic protein gene, while GABAA and GABAB receptors mediated this process.

Key words: GABA, piglet, oxidative stress, receptor, apoptosis

Table 1

Effects of different concentrations of GABA on serum oxidation/antioxidation indexes and ACTH levels of piglets"

项目
Items
组别 Groups P
P value
Con OS HD+OS MD+OS LD+OS
丙二醛 Malondialdehyde (nmol·mL-1) 6.56±0.95 33.88±1.97## 4.98±0.5** 13.43±0.86** 16.42±0.86** <0.001
谷胱甘肽 Glutathione (μmol·L-1) 19.20±0.4 12.56±1.26## 37.15±1.14** 32.71±0.21** 28.89±0.24** <0.001
总抗氧化能力 Total antioxidant capacity (U·mL-1) 2.82±0.06 2.19±0.13## 4.26±0.07** <0.001
促肾上腺皮质激素 Adreno-cortico-tropic-hormone (ng·L-1) 70.85±7.22 100.09±4.67## 72.91±2.91* 0.01

Table 2

Effect of GABA with high concentration on the diarrhea rate of piglets (Mean±SEM,n=5)"

试验分组
Experimental grouping
腹泻率 Diarrhea rate (%)
0-3 d 4-7 d 8-14 d 0-14 d
Con 7±4.08 5.56±3.51 0 1.53±0.94
OS 7±4.08 6±3.71 0 1.67±1.02
HD+OS 3.33±3.33 3.33±3.33 0 0.83±0.83

Fig. 1

Effect of GABA with high concentration on the daily gain of piglets ##:Compared with the control group P<0.01;#: Compared with the control group P<0.05; **: Compared with oxidative stress group P<0.01;*: Compared with oxidative stress group P<0.05"

Table 3

Effects of GABA with high concentration on oxidation/antioxidation related indexes in hippocampus of piglets (Mean± SEM, n=5)"

项目
Items
组别 Groups P
P value
Con OS HD+OS
丙二醛 Malondialdehyde (nmol·mL-1) 137.4±1.43 430.27±2.33## 148.06±4.07** <0.001
谷胱甘肽 Glutathione (μmol·L-1) 34.3±2.11 14.72±1.4## 29.91±2.08** <0.001
总抗氧化能力 Total antioxidant capacity (U·mL-1) 1.94±0.07 0.19±0.05## 2.87±0.23** <0.001

Table 4

Effects of GABA with high concentration on the content of GABA receptors in hippocampus of piglets (Mean±SEM,n=5)"

项目
Items
组别 Groups P
P value
Con OS HD+OS
GABAA型受体 GABAA receptor (μmol·L-1) 14.35±0.52 14.71±0.47 18.93±0.56## <0.001
GABAB型受体 GABAB receptor (μmol·L-1) 28.15±2.01 27.41±1.38 41.65±4.7## 0.01

Fig. 2

Effects of GABA with high concentration on expression levels of Bax, Bcl-2 and Caspase-3 genes in hippocampus of piglets A: Western blot detection of Bcl-2, Bax and Caspase-3 protein levels; B: Relative expression of Bax protein; C: Relative expression of Bcl-2 protein; D: Relative expression of Caspase protein; ##: Compared with the control group P<0.01; #: Compared with the control group P<0.05; **: Compared with oxidative stress group P<0.01; *: Compared with oxidative stress group P<0.05"

Table 5

Effects of GABA receptor inhibitors on GABA receptors content of hippocampal neurons in rats (Mean±SEM, n=3)"

项目
Items
组别 Groups P
P value
Con OS GABA+OS GABA+OS+
Picrotoxin
GABA+OS+
CGP54626
GABAA型受体 GABAA receptor (μmol·L-1) 12.25±0.16 13.18±0.46 13.85±0.15## 9.97±0.50## 13.93±0.22## <0.001
GABAB型受体 GABAB receptor (μmol·L-1) 7.18±0.43 8.50±0.19 9.67±0.54## 9.56±0.62## 6.92±0.37 0.004

Fig. 3

Effects of different treatment on the expression levels of Bax and Caspase-3 genes in hippocampal neurons of rats A: Relative expression of Bax protein; B: Western blot detection of Bax and Caspase-3 protein levels; C: Relative expression of Caspase protein; #: Compared with the control group P<0.05; *: Compared with oxidative stress group P<0.05"

[1] 林厦菁, 陈芳, 蒋守群, 蒋宗勇. 大豆异黄酮对早期断奶仔猪生长性能、抗氧化功能及肠黏膜形态结构的影响. 中国农业科学, 2020, 53(10): 2101-2111. doi: 10.3864/j.issn.0578-1752.2020.10.016.
doi: 10.3864/j.issn.0578-1752.2020.10.016
LIN X J, CHEN F, JIANG S Q, JIANG Z Y. Effects of soybean isoflavones on growth performance, antioxidant performance and intestinal morphology of early-weaned piglets. Scientia Agricultura Sinica, 2020, 53(10): 2101-2111. doi: 10.3864/j.issn.0578-1752.2020.10.016. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2020.10.016
[2] 韩佳良, 刘建新, 刘红云. 热应激对奶牛泌乳性能的影响及其机制. 中国农业科学, 2018, 51(16): 3159-3170. doi: 10.3864/j.issn.0578-1752.2018.16.012.
doi: 10.3864/j.issn.0578-1752.2018.16.012
HAN J L, LIU J X, LIU H Y. Effect of heat stress on lactation performance in dairy cows. Scientia Agricultura Sinica, 2018, 51(16): 3159-3170. doi: 10.3864/j.issn.0578-1752.2018.16.012. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2018.16.012
[3] MCEWEN B S, SEEMAN T. Protective and damaging effects of mediators of stress. Elaborating and testing the concepts of allostasis and allostatic load. Annals of the New York Academy of Sciences, 1999, 896: 30-47. doi: 10.1111/j.1749-6632.1999.tb08103.x.
doi: 10.1111/j.1749-6632.1999.tb08103.x
[4] SAPOLSKY R M, KREY L C, MCEWEN B S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. The Journal of Neuroscience, 1985, 5(5): 1222-1227.
doi: 10.1523/JNEUROSCI.05-05-01222.1985
[5] SAPOLSKY R M, UNO H, REBERT C S, FINCH C E. Hippocampal damage associated with prolonged glucocorticoid exposure in Primates. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 1990, 10(9): 2897-2902. doi: 10.1523/JNEUROSCI.10-09-02897.1990.
doi: 10.1523/JNEUROSCI.10-09-02897.1990
[6] HUOT R L, PLOTSKY P M, LENOX R H, MCNAMARA R K. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Research, 2002, 950(1/2): 52-63. doi: 10.1016/S0006-8993(02)02985-2.
doi: 10.1016/S0006-8993(02)02985-2
[7] MCEWEN B S. The ever-changing brain: cellular and molecular mechanisms for the effects of stressful experiences. Developmental Neurobiology, 2012, 72(6): 878-890. doi: 10.1002/dneu.20968.
doi: 10.1002/dneu.20968
[8] GERLACH J L, MCEWEN B S. Rat brain binds adrenal steroid hormone: Radioautography of hippocampus with corticosterone. Science, 1972, 175(4026): 1133-1136. doi: 10.1126/science.175.4026.1133.
doi: 10.1126/science.175.4026.1133
[9] GERLACH J L, MCEWEN B S, PFAFF D W, MOSKOVITZ S, FERIN M, CARMEL P W, ZIMMERMAN E A. Cells in regions of rhesus monkey brain and pituitary retain radioactive estradiol, corticosterone and cortisol differentially. Brain Research, 1976, 103(3): 603-612. doi: 10.1016/0006-8993(76)90463-7.
doi: 10.1016/0006-8993(76)90463-7
[10] MCEWEN B S, WEISS J M, SCHWARTZ L S. Selective retention of corticosterone by limbic structures in rat brain. Nature, 1968, 220(5170): 911-912. doi: 10.1038/220911a0.
doi: 10.1038/220911a0
[11] DECAVEL C, VAN DEN POL A N. GABA: A dominant neurotransmitter in the hypothalamus. The Journal of Comparative Neurology, 1990, 302(4): 1019-1037. doi: 10.1002/cne.903020423.
doi: 10.1002/cne.903020423
[12] HERMAN J P, MUELLER N K, FIGUEIREDO H. Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Annals of the New York Academy of Sciences, 2004, 1018: 35-45. doi: 10.1196/annals.1296.004.
doi: 10.1196/annals.1296.004
[13] PAN F Y, YANG C Y, XIE Q, YANG Y, LUO X M, GAN L. Glucocorticoids change the transcript levels of galanin, galanin receptor-2 and brain-derived neurotrophic factor in rat hippocampal neurons. Indian Journal of Animal Research, 2019(53):1583-1588. doi: 10.18805/ijar.b-975.
doi: 10.18805/ijar.b-975
[14] 夏颖华, 孔晓冬, 雷平, 张释双, 张明义, 赵子龙, 葛歆瞳. 神经生长因子对糖皮质激素诱导大鼠海马神经元凋亡的保护作用. 中国现代神经疾病杂志, 2017, 17(3): 209-213. doi: 10.3969/j.issn.1672-6731.2017.03.009.
doi: 10.3969/j.issn.1672-6731.2017.03.009
XIA Y H, KONG X D, LEI P, ZHANG S S, ZHANG M Y, ZHAO Z L, GE X T. Protective effect of nerve growth factor on glucocorticoid- induced apoptosis of primary cultured rat hippocampal neurons. Chinese Journal of Contemporary Neurology and Neurosurgery, 2017, 17(3): 209-213. doi: 10.3969/j.issn.1672-6731.2017.03.009. (in Chinese)
doi: 10.3969/j.issn.1672-6731.2017.03.009
[15] 张建宁, 孙红宇, 杨树源, 张卉, 张文治. 糖皮质激素对大鼠海马神经元影响的体外研究. 中国神经精神疾病杂志, 2003, 29(3): 196-198. doi: 10.3969/j.issn.1002-0152.2003.03.013.
doi: 10.3969/j.issn.1002-0152.2003.03.013
ZHANG J N, SUN H Y, YANG S Y, ZHANG H, ZHANG W Z. Effect of glucocorticoid on hippocampal neurons in rats in vitro. Chinese Journal of Nervous and Mental Diseases, 2003, 29(3): 196-198. doi: 10.3969/j.issn.1002-0152.2003.03.013. (in Chinese)
doi: 10.3969/j.issn.1002-0152.2003.03.013
[16] 蔺忆, 高翠翠, 陈立立, 唐雪, 施用晖, 乐国伟. GABA对高糖诱导氧化损伤的RIN-m5f细胞的保护作用和机制. 食品与生物技术学报, 2015, 34(2): 195-200.
LIN Y, GAO C C, CHEN L L, TANG X, SHI Y H, YUE G W. Effect of GABA on RIN-m5f cells in high glucose-induced oxidative injury model. Journal of Food Science and Biotechnology, 2015, 34(2): 195-200. (in Chinese)
[17] YANG L J, XU T, ZHANG K, WEI Z S, LI X R, HUANG M F, ROSE G M, CAI X. The essential role of hippocampal alpha6 subunit-containing GABAA receptors in maternal separation stress- induced adolescent depressive behaviors. Behavioural Brain Research, 2016, 313: 135-143. doi: 10.1016/j.bbr.2016.07.002.
doi: 10.1016/j.bbr.2016.07.002
[18] SKILBECK K J, JOHNSTON G A R, HINTON T. Stress and GABAAreceptors. Journal of Neurochemistry, 2010, 112(5): 1115-1130. doi: 10.1111/j.1471-4159.2009.06539.x.
doi: 10.1111/j.1471-4159.2009.06539.x
[19] 陈芬, 顾永健. 外源性γ-氨基丁酸和舍曲林对急性应激抑郁大鼠海马神经元GABA受体的影响. 中华行为医学与脑科学杂志, 2010, 19(7): 632-634. doi: 10.3760/cma.j.issn.1674-6554.2010.07.018.
doi: 10.3760/cma.j.issn.1674-6554.2010.07.018
CHEN F, GU Y J. The effects of γ-aminobutyric acid and sertraline on the GABA receptor of hippocampus neuron in rats of depression induced by acute stress. Chinese Journal of Behavioral Medical Science, 2010, 19(7): 632-634. doi: 10.3760/cma.j.issn.1674-6554.2010.07.018. (in Chinese)
doi: 10.3760/cma.j.issn.1674-6554.2010.07.018
[20] 郭浩浩. GABAB受体介导的JNK激活分子机制及其功能的初步研究[D]. 武汉: 华中科技大学, 2013.
GUO H H. Molecular mechanism and function of GABAB receptor mediated JNK activation[D]. Wuhan: Huazhong University of SCience and Technology. 2013. (in Chinese)
[21] LANGIE S A S, KOWALCZYK P, TUDEK B, ZABIELSKI R, DZIAMAN T, OLIŃSKI R, VAN SCHOOTEN F J, GODSCHALK R W L. The effect of oxidative stress on nucleotide-excision repair in colon tissue of newborn piglets. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 2010, 695(1/2): 75-80. doi: 10.1016/j.mrgentox.2009.12.005.
doi: 10.1016/j.mrgentox.2009.12.005
[22] DE CUPERE F, DEPREZ P, DEMEULENAERE D, MUYLLE E. Evaluation of the effect of 3 probiotics on experimental Escherichia coli enterotoxaemia in weaned piglets. Zentralblatt Fur Veterinarmedizin Reihe B Journal of Veterinary Medicine Series B, 1992, 39(4): 277-284. doi: 10.1111/j.1439-0450.1992.tb01169.x.
doi: 10.1111/j.1439-0450.1992.tb01169.x
[23] GIANG H H, VIET T Q, OGLE B, LINDBERG J E. Growth performance, digestibility, gut environment and health status in weaned piglets fed a diet supplemented with potentially probiotic complexes of lactic acid bacteria. Livestock Science, 2010, 129(1/2/3): 95-103. doi: 10.1016/j.livsci.2010.01.010.
doi: 10.1016/j.livsci.2010.01.010
[24] CHAND N, MUHAMMAD S, KHAN R U, ALHIDARY I A, REHMAN Z U. Ameliorative effect of synthetic γ-aminobutyric acid (GABA) on performance traits, antioxidant status and immune response in broiler exposed to cyclic heat stress. Environmental Science and Pollution Research International, 2016, 23(23): 23930-23935. doi: 10.1007/s11356-016-7604-2.
doi: 10.1007/s11356-016-7604-2
[25] 邹晓庭, 胡家澄, 曹德瑞, 董金格. γ-氨基丁酸对夏季高温期生长肥育猪生产性能、抗氧化及HPA、HPT轴激素分泌的影响. 畜牧兽医学报, 2009, 40(8): 1196-1201. doi: 10.3321/j.issn:0366-6964.2009.08.011.
doi: 10.3321/j.issn:0366-6964.2009.08.011
ZOU X T, HU J C, CAO D R, DONG J G. Effect of γ-aminobutyric acid on growth performance, antioxidation and hormones of HPA, HPT axis in growth-finishing swine in hot summer. Acta Veterinaria et Zootechnica Sinica, 2009, 40(8): 1196-1201. doi: 10.3321/j.issn:0366-6964.2009.08.011. (in Chinese)
doi: 10.3321/j.issn:0366-6964.2009.08.011
[26] 曹德瑞, 邹晓庭, 顾林英. γ-氨基丁酸对温热环境中生长肥育猪生产性能和抗氧化功能的影响. 中国饲料, 2008(5): 21-23, 26. doi: 10.3969/j.issn.1004-3314.2008.05.006.
doi: 10.3969/j.issn.1004-3314.2008.05.006
CAO D R, ZOU X T, GU L Y. Effects of γ-aminobutyric acid on growth performance and antioxidant capacity in finishing pigs housed in thermal environment. China Feed, 2008(5): 21-23, 26. doi: 10.3969/j.issn.1004-3314.2008.05.006. (in Chinese)
doi: 10.3969/j.issn.1004-3314.2008.05.006
[27] 张铭, 陈立祥, 范志勇, 伍应松. γ-氨基丁酸对热应激哺乳母猪生产性能的影响. 养猪, 2009(3): 9-10. doi: 10.3969/j.issn.1002-1957.2009.03.007.
doi: 10.3969/j.issn.1002-1957.2009.03.007
ZHANG M, CHEN L X, FAN Z Y, WU Y S. GABA for effect of heat stress lactationsows performance. Swine Production, 2009(3): 9-10. doi: 10.3969/j.issn.1002-1957.2009.03.007. (in Chinese)
doi: 10.3969/j.issn.1002-1957.2009.03.007
[28] 尹佳佳, 李耀华, 单安山. γ-氨基丁酸对猪生长性能的影响和抗运输应激的作用.中国畜牧兽医学会动物营养学分会第十一次全国动物营养学术研讨会论文集. 2012.
YIN J J, LI Y H, SHAN A S. Effects of GABA on growth performance and anti transport stress in pigs//Proceedings of the 11th National Symposium on Animal Nutrition, Animal Nutrition Branch, Chinese Society of Animal Husbandry and Veterinary. 2012. (in Chinese)
[29] LIPIŃSKI P, STARZYŃSKI R R, CANONNE-HERGAUX F, TUDEK B, OLIŃSKI R, KOWALCZYK P, DZIAMAN T, THIBAUDEAU O, GRALAK M A, SMUDA E, WOLIŃSKI J, USIŃSKA A, ZABIELSKI R. Benefits and risks of iron supplementation in anemic neonatal pigs. The American Journal of Pathology, 2010, 177(3): 1233-1243. doi: 10.2353/ajpath.2010.091020.
doi: 10.2353/ajpath.2010.091020
[30] 党晓伟. 不同铁负荷对仔猪Hepcidin mRNA表达量的影响[D]. 河南农业大学, 2010.
DANG X W. Effects of different iron loads on hepcidin mRNA expression in piglets[D]. Henan Agricultural University, 2010. (in Chinese)
[31] 杨兵, 夏先林, 施晓丽, 韩晓洁. γ-氨基丁酸对仔猪免疫和抗氧化性能的影响. 饲料研究, 2012(10): 8-10, 32. doi: 10.13557/j.cnki.issn1002-2813.2012.10.005.
doi: 10.13557/j.cnki.issn1002-2813.2012.10.005
YANG B, XIA X L, SHI X L, HAN X J. Effects of GABA on immunity and antioxidant properties of piglets. Feed Research, 2012(10): 8-10, 32. doi: 10.13557/j.cnki.issn1002-2813.2012.10.005. (in Chinese)
doi: 10.13557/j.cnki.issn1002-2813.2012.10.005
[32] 李耀华, 尹佳佳, 石宝明, 单安山. γ-氨基丁酸对断奶仔猪生长性能和行为的影响. 中国畜牧兽医学会动物营养学分会全国动物营养学术研讨会. 2012.
LI Y H, YIN J J, SHI B M, SHAN A S. Effect of GABA on growth performance and behavior of weaned piglets//National Symposium on Animal Nutrition, Animal Nutrition Branch of China Animal Husbandry and Veterinary Society. 2012. (in Chinese)
[33] 韦习会, 夏东. 日粮中添加GABA对断奶仔猪增重和饲料利用的影响//南京农业大学畜牧兽医学术年会. 2009.
WEI X H, XIA D. Effects of dietary GABA supplementation on weight gain and feed utilization of weaned piglets//Annual Meeting of Animal Husbandry and Veterinary Science, Nanjing Agricultural University. 2009. (in Chinese)
[34] 刘振军. γ-氨基丁酸对早期断奶仔猪生长性能和血液指标的影响[D]. 四川农业大学, 2006.
LIU Z J. Effects of GABA on growth performance and blood parameters of early weaned piglets[D]. Sichuan Agricultural University, 2006. (in Chinese)
[35] MAGUIRE J. GABAergic Control of the Hypothalamic-Pituitary- Adrenal (HPA) Axis: Role of Extrasynaptic GABA_A Receptors Extrasynaptic GABAA Receptors, 2014: 239-270. doi: 10.1007/978-1-4939-1426-5_12.
doi: 10.1007/978-1-4939-1426-5_12
[36] 袁雄坤, 姜丽丽, 陶诗煜, 臧建军, 王军军. 母猪热应激敏感指标体系的研究进展. 中国农业科学, 2020, 53(22): 4691-4699. doi: 10.3864/j.issn.0578-1752.2020.22.015.
doi: 10.3864/j.issn.0578-1752.2020.22.015
YUAN X K, JIANG L L, TAO S Y, ZANG J J, WANG J J. Research progresses on sensitive index system of heat stress in sows. Scientia Agricultura Sinica, 2020, 53(22): 4691-4699. doi: 10.3864/j.issn.0578-1752.2020.22.015. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2020.22.015
[37] 张美琦, 李妍, 李树静, 高艳霞, 李建国, 曹玉凤, 李秋凤. 饲粮能量水平对荷斯坦阉牛生产性能、血液指标、屠宰性能及肉品质的影响. 中国农业科学, 2021, 54(1): 203-212. doi: 10.3864/j.issn.0578-1752.2021.01.015.
doi: 10.3864/j.issn.0578-1752.2021.01.015
ZHANG M Q, LI Y, LI S J, GAO Y X, LI J G, CAO Y F, LI Q F. Effects of dietary energy levels on production performance, blood index, slaughter performance and meat quality of Holstein steers. Scientia Agricultura Sinica, 2021, 54(1): 203-212. doi: 10.3864/j.issn.0578-1752.2021.01.015. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2021.01.015
[38] KUIDA K, ZHENG T S, NA S Q, KUAN C Y, YANG D, KARASUYAMA H, RAKIC P, FLAVELL R A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature, 1996, 384(6607): 368-372. doi: 10.1038/384368a0.
doi: 10.1038/384368a0
[39] KUWANA T, SMITH J J, MUZIO M, DIXIT V, NEWMEYER D D, KORNBLUTH S. Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome C. Journal of Biological Chemistry, 1998, 273(26): 16589-16594. doi: 10.1074/jbc.273.26.16589.
doi: 10.1074/jbc.273.26.16589
[40] 胡震, 张建宁, 杨树源, 杨新宇. 糖皮质激素对颅脑损伤后海马神经元凋亡的影响. 中华实验外科杂志, 2003, 20(4): 376. doi: 10.3760/j.issn:1001-9030.2003.04.041.
doi: 10.3760/j.issn:1001-9030.2003.04.041
HU Z, ZHANG J N, YANG S Y, YANG X Y. The effect of glucocorticoids on apoptosis of hippocampal neurons after brain injury. Chinese Journal of Experimental Surgery, 2003, 20(4): 376. doi: 10.3760/j.issn:1001-9030.2003.04.041. (in Chinese)
doi: 10.3760/j.issn:1001-9030.2003.04.041
[41] LI X M, HAN F, LIU D J, SHI Y X. Changes of Bax, Bcl-2 and apoptosis in hippocampus in the rat model of post-traumatic stress disorder. Neurological Research, 2010, 32(6): 579-586. doi: 10.1179/016164110X12556180206194.
doi: 10.1179/016164110X12556180206194
[42] NISWANDER J M, DOKAS L A. Hyperosmotic stress-induced caspase-3 activation is mediated by p38 MAPK in the hippocampus. Brain Research, 2007, 1186: 1-11. doi: 10.1016/j.brainres.2007.10.008.
doi: 10.1016/j.brainres.2007.10.008
[43] 史远, 艾洪滨, 崔希云. 大鼠侧脑室注射GABA对束缚-浸水应激性胃溃疡的影响. 生物医学工程研究, 2007, 26(1): 55-58. doi: 10.19529/j.cnki.1672-6278.2007.01.013.
doi: 10.19529/j.cnki.1672-6278.2007.01.013
SHI Y, AI H B, CUI X Y. Effect of intracerebroventricular injection of γ-aminobutyric acid on restrain water-immersion stress-induced gastric ulcer in rats. Journal of Biomedical Engineering Research, 2007, 26(1): 55-58. doi: 10.19529/j.cnki.1672-6278.2007.01.013. (in Chinese)
doi: 10.19529/j.cnki.1672-6278.2007.01.013
[44] LI H L, KANG Y M, YU L, XU H Y, ZHAO H. Melatonin reduces blood pressure in rats with stress-induced hypertension via GABAA receptors. Clinical and Experimental Pharmacology & Physiology, 2009, 36(4): 436-440. doi: 10.1111/j.1440-1681.2008.05080.x.
doi: 10.1111/j.1440-1681.2008.05080.x
[45] HAWKINS M F, BAUMEISTER A A, LARUE R H, FOUNTAIN L T, HIGHSMITH R W, JEFFRIES S K, DUKE M A. Central GABA activation and behaviors evoked by tail-pinch stress in the rat. Physiology & Behavior, 1999, 67(5): 705-709. doi: 10.1016/s0031-9384(99)00138-9.
doi: 10.1016/s0031-9384(99)00138-9
[46] HOUSTON A J, WONG J C, EBENEZER I S. A study on the involvement of GABAB receptor ligands in stress-induced antinociception in male mice. Methods and Findings in Experimental and Clinical Pharmacology, 1997, 19(3): 167-171.
[47] GAO Y G, ZHOU J J, ZHU Y, WANG L, KOSTEN T A, ZHANG X J, LI D P. Neuroadaptations of presynaptic and postsynaptic GABA B receptor function in the paraventricular nucleus in response to chronic unpredictable stress. British Journal of Pharmacology, 2017, 174(17): 2929-2940. doi: 10.1111/bph.13924.
doi: 10.1111/bph.13924
[48] 陈忠, 李书珍, 朱剑琴. 急性热应激对小鼠大脑皮质GABA受体的影响. 南京大学学报(自然科学版), 1997, 33(3): 386-391.
CHEN Z, LI S Z, ZHU J Q. Effect of acute heat stress on gaba receptors in cerebral cortex of mice. Journal of Naijing University (Natural Sciences), 1997, 33(3): 386-391. (in Chinese)
[49] KUREK A, KUCHARCZYK M, DETKA J, ŚLUSARCZYK J, TROJAN E, GŁOMBIK K, BOJARSKI B, LUDWIKOWSKA A, LASOŃ W, BUDZISZEWSKA B. Pro-apoptotic action of corticosterone in hippocampal organotypic cultures. Neurotoxicity Research, 2016, 30(2): 225-238. doi: 10.1007/s12640-016-9630-8.
doi: 10.1007/s12640-016-9630-8
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