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

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.
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