Scientia Agricultura Sinica ›› 2012, Vol. 45 ›› Issue (16): 3391-3398.doi: 10.3864/j.issn.0578-1752.2012.16.019

• ANIMAL SCIENCE·RESOURCE INSECT • Previous Articles     Next Articles

Influence of High Temperature on Oxidative Damage and Follicle Development of Laying Hens

 YANG  Xiao-Lan, ZHANG  Min-Hong, FENG  Jing-Hai, DI  Li-Li, JIANG  Li-Wen   

  1. 中国农业科学院北京畜牧兽医研究所/动物营养学国家重点实验室，北京100193
  • Received:2012-02-24 Online:2012-08-15 Published:2012-05-08

PDF

965

Cited

6

Abstract: 【Objective】 Two experiments were conducted to assess the relationship between follicle development of heat stressed laying hens and oxidative stress induced by high temperature, and then to reveal the mechanism of lower egg production of heat stressed laying hens.【Method】In experiment 1, 180 Hy-line Brown hens, 27 wk of age, were randomly divided into three groups and housed into three controlled environment chambers. Three groups were respectively normal thermal group (NT group: 28℃, basal diet), daily cyclic high temperature group (HT group: 28-35-28℃, basal diet) and daily cyclic high temperature and supplemented with Vitamin E (VE) group (HT+VE group: 28-35-28℃, basal diet supplemented with 250 IU•kg-1 VE).  In experiment two, granulosa cells dissociated from F1 and F2 follicles were incubated under either 39℃ or 44℃. 【Result】The results of experiment 1 showed that daily cyclic high temperature significantly inhibited follicle development of laying hens, which mainly manifested as decreasing in egg production (P＜0.05), ovary weight (P＜0.05) and large follicle number (P＜0.05) as well as inhibition in P450 cholesterol side-chain cleavage enzyme (P450scc ) mRNA expression (P＜0.05) and progesterone (P4) production (P＜0.05) in granulosa cell. The results also showed that daily cyclic high temperature induced hens oxidative stress, which manifested as higher malondialdehyde (MDA) concentration (P＜0.05) in plasma, liver tissue and egg yolk. When exposed to cyclic high temperature, 250 IU•kg-1 VE supplementation decreased MDA concentration significantly in plasma (P＜0.05), liver tissue (P＜0.05), egg yolk (P＜0.05), and alleviated (P＜0.05) inhibition in follicle development of laying hens. The results of experiment 2 showed that high temperature increased reactive oxygen species (ROS) level (P＜0.05) in granulosa cells and decreased proliferation of granulosa cells (P＜0.05). VE supplemented into medium alleviated the negative effects of chronic heat stress, manifested as decreasing in ROS level (P＜0.05) and increasing in proliferation of granulosa cells (P＜0.05). 【Conclusion】 The results demonstrated that heat stress increased ROS level in granulosa cell and induced hens (liver, plasma and egg yolk) oxidative stress, in addition, heat stress inhibited P4 production, proliferation of granulosa cells and follicle development of laying hen, while VE depressed oxidative damage induced by heat stress, promoted follicle development of heat stressed laying hens. All the results suggest that the mechanism of poor follicle development of heat stressed hens involves in oxidative stress induced by high temperature.

Key words: high temperature, follicle development, granulosa cells, oxidative damage, laying hen

[1]Bollengier-Lee S, Mitchell M A, Utomo D B, Williams P E V; Whitehead C C. Influence of high dietary vitamin E supplementation on egg production and plasma characteristics in hens subjected to heat stress. British Poultry Science, 1998, 39(1): 106-112.

[2]Bollengier-Lee S, Williams P E V, Whitehead C C. Optimal dietary concentration of vitamin E for alleviating the effect of heat stress on egg production in laying hens. British Poultry Science, 1999, 40(1): 102-107.

[3]Puthpongsiriporn U, Scheideler S E, Sell J L, Beck M M. Effects of vitamin E and C supplementation on performance, in vitro lymphocyte proliferation, and antioxidant status of laying hens during heat stress. Poultry Science, 2001, 80(8): 1190-1200.

[4]Kirunda D F K, Scheideler S E, McKee S R. The efficacy of vitamin E (DL-alpha-tocopheryla acetate) supplementation in hen diets to alleviate egg quality deterioration associated with high temperature exposure. Poultry Science, 2001, 80(9): 1378-1383.

[5]Rozenboim I, Tako E, Gal-Garber O, Proudman J A, Uni Z. The effect of heat stress on ovarian function of laying hens. Poultry Science, 2007, 86(8): 1760-1765.

[6]Star L, Nieuwland M, Kemp B, Parmentier H K. Effect of single or combined climatic and hygienic stress on natural and specific humoral immune competence in four layer lines. Poultry Science, 2007, 86(9): 1894-1903.

[7]Mashaly M M, Hendricks Rd G L, Kalama M A, Gehad A E, Abbas A O, Patterson P H. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poultry Science, 2004, 83(6): 889-894.

[8]Mujahid A, Yoshiki Y, Akiba Y, Toyomizu M. Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poultry Science, 2005, 84(2): 307-314.

[9]Feng J H, Zhang M H, Zheng S S, Xie P, Ma A P. Effects of high temperature on multiple parameters of broilers in vitro and in vivo. Poultry Science, 2008, 87(10): 2133-2139.

[10]Lin H, de Vos D, Decuypere E, Buyse J. Dynamic changes in parameters of redox balance after mild heat stress in aged laying hens (Gallus gallus domesticus). Comparative Biochemistry and Physiology, Part C, 2008, 147(1): 30-35.

[11]Margolin Y, Aten R F, Behrman H R. Antigonadotropic and antisteroidogenic actions of peroxide in rat granulosa cells. Endocrinology, 1990, 127(1): 245-250.

[12]Marrone B L, Jamaluddin M, Hertelendy F. Regional pattern of cell maturation and progesterone biosynthesis in the avian granulosa cell layer. Biology of Reproduction, 1990, 42(3): 405-412.

[13]Johnson A L. Regulation of follicle differentiation by gonadotropins and growth factors. Poultry Science, 1993, 72(5): 867-873.

[14]Tilly J L. Commuting the death sentence: how oocytes strive to survive. Nature Reviews Molecular Cell Biology, 2001, 2: 838-848.

[15]Sahin K, Sahin N, Yaralioglu S. Effects of vitamin C and vitamin E on lipid peroxidation, blood serum metabolites, and mineral concentrations of laying hens reared at high ambient temperature. Biological Trace Element Research, 2002, 85(1): 35-45.

[16]Gilbert A B, Evans A J, Perry M M, Davidson M H. A method for separating the granulosa cells, the basal lamina and the theca of the preovulatory ovarian follicle of the domestic fowl (Gallus domesticus). Journal of Reproduction and Fertility, 1977, 50(1): 179-181.

[17]Jakubowski W, Bartosz G. 2, 7-dichlorofluorescin oxidation and reactive oxygen species: what does it measure? Cell Biology International, 2000, 24(10): 757-760.

[18]Johnson P A, Stoklosowa S, Bahr J M. Interaction of granulosa and theca layers in the control of progesterone secretion in the domestic hen. Biology of Reproduction, 1987, 37(5): 1149-1155.

[19]Kossowska-Tomaszczuk K, Pelczar P, Güven S, Kowalski J, Volpi E, de Geyter C, Scherberich A. A novel three-dimensional culture system allows prolonged culture of functional human granulosa cells and mimics the ovarian environment. Tissue Engineering, Part A, 2010, 16(6): 2063-2073.

[20]Yoshida N, Fujita M, Nakahara M, Kuwahara T, Kawakami S I, Bungo T. Effect of high environmental temperature on egg production, serum lipoproteins and follicle steroid hormones in laying hens. The Journal of Poultry Science, 2011, 48: 207-211.

[21]Novero R P, Beck M M, Gleaves E W, Johnson A L, Deshazer J. Plasma progesterone, luteinizing hormone concentrations, and granulosa cell responsiveness in heat-stressed hens. Poultry Science, 1991, 70(11): 2335-2339.

[22]Elnagar S A, Scheideler S E, Beck M M. Reproductive hormones, hepatic deiodinase messenger ribonucleic acid, and vasoactive intestinal polypeptide-immunoreactive cells in hypothalamus in the heat stress-induced or chemically induced hypothyroid laying hen. Poultry Science, 2010, 89(9): 2001-2009.

[23]Donoghue D J, Krueger B F, Hargis B M, Miller A M, El Halawani  M. Thermal stress reduces serum luteinizing hormone and bioassayable hypothalamic content of luteinizing hormone-releasing hormone in hens. Biology of Reproduction, 1989, 41(3): 419-424.

[24]Murphy B D, Lalli E, Walsh L P, Liu Z, Soh J, Stocco D M, Sassone-Corsi P. Heat shock interferes with steroidogenesis by reducing transcription of the steroidogenic acute regulatory protein gene. Molecular Endocrinology, 2001, 15(8): 1255-1263.

[25]Shimizu T, Ohshima I, Ozawa M, Takahashi S, Tajima A, Shiota M, Miyazaki H, Kanai Y. Heat stress diminishes gonadotropin receptor expression and enhances susceptibility to apoptosis of rat granulosa cells. Reproduction, 2005, 129(4): 463-472.

[26]Altan Ö, Pabuçcuo?lu A, Altan A, Konyalio?lu S, Bayraktar H. Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. British Poultry Science, 2003, 44(4): 545-550.

[27]Lin H, Decuypere E, Buyse J. Acute heat stress induces oxidative stress in broiler chickens. Comparative Biochemistry and Physiology, Part A, 2006, 144(1): 11-17.

[28]王兰芳, 林  海, 杨全明, 朱立贤. 日粮维生素A水平对免疫接种及热应激下蛋鸡脂质过氧化反应的影响. 畜牧兽医学报, 2002, 33(5): 443-447.

Wang L F, Lin H, Yang Q M, Zhu L X. The effect of dietary vitamin A levels on lipid peroxidatic reaction of inoculated and heatstressed laying hens. Acta Veterinaria et Zootechinca Sinica, 2002, 33(5): 443-447. (in Chinese)

[29]Ealy A D, Howell J L, Monterroso V H, Aréchiga C F, Hansen P J. Developmental changes in sensitivity of bovine embryos to heat shock and use of antioxidants as thermoprotectants. Journal of Animal Science, 1995, 73(5): 1401-1407.

[30]Aréchiga C F, Ealy A D, Hansen P J. Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos. Biology of Reproduction, 1995, 52(6): 1296-1301.

[31]Malayer J R, Pollard J W, Hansen P J. Modulation of thermal killing of bovine lymphocytes and preimplantation mouse embryos by alanine and taurine. American Journal of Veterinary Research, 1992, 53(5): 689-694.

[32]Ealy A D, Drost M, Barros C M, Hansen P J. Thermoprotection of preimplantation bovine embryos from heat shock by glutathione and taurine. Cell Biology International Reports, 1992, 16(2): 125-131.

[33]Ozawa M, Hirabayashi M, Kanai Y. Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reproduction, 2002, 124(5): 683-689.

[34]Sakatani M, Kobayashi S I, Takahashi M. Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Molecular Reproduction and Development, 2004, 67(1): 77-82.

[35]Parke D V. Antioxidants in Human Health and Disease. Cambridge, MA: CAB International Publishing, 1999: 1-14.
[1] YUE XiaoYu, ZHAO ShiChen, WANG Qin. The miR-362-3p Regulates the Proliferation and Steroid Hormone Synthesis of Mare Follicular Granulosa Cells by Targeting BMPR2 [J]. Scientia Agricultura Sinica, 2026, 59(7): 1564-1575.
[2] CHEN YaRu, WANG Lei, FU Ming, HUANG Tao, ZHANG Hao, LIANG ZhenHua, PI JinSong, WU Yan. Molecular Mechanism of USP18 Facilitating Ferroptosis by Suppressing GPX4 Ubiquitination and Degradation in Duck Granulosa Cells [J]. Scientia Agricultura Sinica, 2026, 59(5): 1128-1140.
[3] MENG Hui, LUO BingYu, LU ZhengYu, WANG Peng, KANG DongRu, ZHENG ChengShu, WANG WenLi. Cloning of CmASMT and Its Role in Thermotolerance of Chrysanthemum [J]. Scientia Agricultura Sinica, 2025, 58(8): 1617-1626.
[4] TANG Yu, LEI BiXin, WANG ChuanWei, YAN XuanTao, WANG Hao, ZHENG Jie, ZHANG WenJing, MA ShangYu, HUANG ZhengLai, FAN YongHui. Response Mechanism of Anthocyanin Accumulation in Colored Wheat to Post-Anthesis High Temperature Stress [J]. Scientia Agricultura Sinica, 2025, 58(6): 1083-1101.
[5] SU Ming, LI FanGuo, HONG ZiQiang, ZHOU Tian, LIU QiangJuan, BAN WenHui, WU HongLiang, KANG JianHong. Antioxidant Characterization of Nitrogen Application for Mitigating Potato Senescence Post-Flowering Under High Temperature Stress [J]. Scientia Agricultura Sinica, 2025, 58(4): 660-675.
[6] DING Ning, QI EnFang, JIA XiaoXia, HUANG Wei, MA LiRong, LI JianWu, YAN RuNan. Screening and Identification of miRNAs in Potato Seedlings in Response to High Temperature Stress [J]. Scientia Agricultura Sinica, 2025, 58(22): 4589-4602.
[7] LEI BiXin, YU YongBo, ZHANG MingTong, CUI GuoJi, HONG JiaWen, HU Tao, YOU AiXin, ZHANG WenJing, MA ShangYu, HUANG ZhengLai, FAN YongHui. Impact of Post-Anthesis Heat Stress on Nitrogen Use Efficiency and Yield Components in Wheat [J]. Scientia Agricultura Sinica, 2025, 58(19): 3837-3856.
[8] XU YuanYuan, HUANG LiQing, LU XingRong, FENG Chao, SHANG JiangHua. Effects of β-mercaptoethanol on Rapamycin Induced Autophagy, Apoptosis and Steroid Hormone Synthesis in Buffalo Granulosa Cells [J]. Scientia Agricultura Sinica, 2025, 58(11): 2265-2274.
[9] LI PeiSong, LU YongDi, GUO Yu, ZHANG QiPeng, LIU TaoFen, WANG TianHe, YANG MingFeng, XIANG Dao, TIAN JingShan, ZHANG WangFeng. The Regional Distribution of Raw Cotton Quality in Xinjiang Based on Notarized Inspection Data for Cotton [J]. Scientia Agricultura Sinica, 2025, 58(1): 58-74.
[10] ZHANG HuaPeng, ZHANG QingZe, HE Fan, QI MengFan, FU BinBin, LI QingChun, LI MengXun, MA LiPeng, LIU Yi, HUANG Tao. Cloning and Identification of Differentially Expressed lncRNAs in Follicles of Meishan Pigs and Duroc Pigs with Their Correlation Analysis with miRNAs [J]. Scientia Agricultura Sinica, 2024, 57(9): 1807-1819.
[11] LI YongFei, LI ZhanKui, ZHANG ZhanSheng, CHEN YongWei, KANG JianHong, WU HongLiang. Effects of Postponing Nitrogen Fertilizer Application on Flag Leaf Physiological Characteristics and Yield of Spring Wheat Under High Temperature Stress [J]. Scientia Agricultura Sinica, 2024, 57(8): 1455-1468.
[12] LUO LiDan, CHEN JiaMing, AN Qi, LIU Lei, SUN QinZhe, LIU Huan, WANG SenShan, SONG LiWen. Effects of Extreme High Temperature on Trehalose Content and Trehalose Transporter Gene in Tetranychus truncatus [J]. Scientia Agricultura Sinica, 2024, 57(6): 1091-1101.
[13] MENG ZhaoYi, WANG YunLu, YAO YiLong, XI GuangYin, NIU JiaQiang, SOLANGSIZHU, GUO Min, XU YeFen. lncRNA-MSTRG.7889.1 Competitively Binds to bta-miR-146a Targeting Smad4 to Regulate Apoptosis of Yak Granulosa Cells [J]. Scientia Agricultura Sinica, 2024, 57(4): 797-809.
[14] SU XiaoYu, TAN ZhengWei, LI ChunMing, LI Lei, LU DanDan, YU YongLiang, DONG Wei, AN SuFang, YANG Qing, SUN Yao, XU LanJie, YANG HongQi, LIANG HuiZhen. Analysis of Genome-Wide Methylation Differences and Associated Gene Expression of Sesame Varieties Under High Temperature Stress [J]. Scientia Agricultura Sinica, 2024, 57(24): 4825-4838.
[15] GUO Ya, REN Hao, WANG HongZhang, ZHANG JiWang, ZHAO Bin, REN BaiZhao, LIU Peng. High Temperature and Drought Combined Stress Inhibited Photosystem Ⅱ Performance and Decreased Grain Yield of Summer Maize [J]. Scientia Agricultura Sinica, 2024, 57(21): 4205-4220.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd