Yu CHANG, Jinghai FENG, Minhong ZHANG, Liwen JIANG, Lili ZHAI, Xiaolan YANG

Effects of massive ovulation on oxidation state and function of the ovaries in laying hens

Modern laying hens show fast reduction in egg production rate after 60 weeks of age, which is associated with the decline in ovarian function. The aim of this study was to examine the influence of massive ovulation on the oxidation state and ovarian function in hens. In total, 48 Jing Hong hens aged 17 weeks were randomly divided into high ovulation (HO) and low ovulation (LO) groups. The LO hens were exposed to 6 h of light per day (6 L:18 D) up to 32 weeks to delay the initiation of egg production and then were switched to 16 L:8 D. The HO hens were reared at 16 L:8 D from 19 weeks. The treatment effects were analyzed by the independent samples t-test using SAS 9.0 software (SAS Institute, Cary, NC, USA). At 36 weeks, there were no significant differences in body weight (P > 0.05) between the two groups and the egg production rate of both groups reached 98%; however, the cumulative egg number in the HO group was much higher than that in the LO group (71.3 versus 18.5, respectively; P < 0.001). The following parameters decreased in the HO hens compared with the LO hens: the number of small yellow follicles (SYFs, P < 0.001) and large white follicles (LWFs, P < 0.01), mRNA expression of luteinizing hormone receptor (P < 0.001), and follicle-stimulating hormone receptor (P < 0.001), while the atretic rates of SYFs and LWFs increased (P < 0.001 and P < 0.01, respectively). In addition, compared with the LO group, the HO hens had reduced activity of superoxide dismutase (plasma: P < 0.01; liver: P < 0.001; ovary: P < 0.001) and glutathione peroxidase (plasma: P < 0.01; liver: P < 0.01; ovary: P < 0.01), while the levels of methane dicarboxylic aldehyde (plasma: P < 0.01; liver: P < 0.001; ovary: P < 0.001) and mRNA expression of mitochondrial transcription factor A (P < 0.001) in granulosa cells were higher. These results indicated that massive ovulation aggravated oxidative stress and had adverse effects on ovarian function in laying hens.

Keywords:

Laying hens, massive ovulation, ovarian function, oxidative stress,

PDF

___

Tůmová E, Gous RM. Interaction of hen production type, age, and temperature on laying pattern and egg quality. Poultry Sci 2012; 91: 1269-1275.
Joyner CJ, Peddie MJ, Taylor TG. The effect of age on egg production in the domestic hen. Gen Comp Endocr 1987; 65: 331-336.
Lebedeva IY, Lebedev VA, Grossmann R, Parvizi N. Age- dependent role of steroids in the regulation of growth of the hen follicular wall. Reprod Biol Endocrinol 2010; 8: 15.
Waddington D, Perry MM, Gilbert AB, Hardie MA. Follicular growth and atresia in the ovaries of hens ( Gallus domesticus ) with diminished egg production rates. J Reprod Fertil 1985; 74: 399-405.
Lillpers K, Wilhelmson M. Age-dependent changes in oviposition pattern and egg production traits in the domestic hen. Poultry Sci 1993; 72: 2005-2011.
Yang N, Wu C, McMillan I. New mathematical model of poultry egg production. Poultry Sci 1989; 68: 476-481.
Palmer SS, Bahr JM. Follicle stimulating hormone increases serum oestradial-17β concentrations, number of growing follicles and yolk deposition in aging hens ( Gallus gallus domesticus ) with decreased egg production. Brit Poultry Sci 1992; 33: 403-414.
Zakaria AH. Ovarian follicular development in young and old laying hens. Arch Geflugelkd 1999; 63: 6-12.
Holmes DJ, Ottinger MA. Birds as long-lived animal models for the study of aging. Exp Gerontol 2003; 38: 1365-1375.
Liu HK, Long DW, Bacon WL. Preovulatory luteinizing hormone surge interval in old and young laying turkey hens early in the egg production period. Poultry Sci 2001; 80: 1364- 1370.
Miyamoto K, Sato EF, Kasahara E, Jikumaru M, Hiramoto K, Tabata H, Katsuragi M, Odo S, Utsumi K, Inoue M. Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radical Bio Med 2010; 49: 674-681.
Gilbert AB, Evans AJ, Perry MM, Davidson MH. A method of separating the granulosa cells, the basal lamina and the theca of the preovulatory ovarian follicle of the domestic fowl ( Gallus domesticus ). Reproduction 1977; 50: 179-181.
Gilbert AB, Perry MM, Waddington D, Hardie MA. Role of atresia in establishing the follicular hierarchy in the ovary of the domestic hen ( Gallus domesticus ). J Reprod Fertil 1983; 69: 221-227.
Yilmaz-Ozden T, Kurt-Sirin O, Tunali S, Akev N, Can A, Yanardag R. Ameliorative effect of vanadium on oxidative stress in stomach tissue of diabetic rats. Bosn J Basic Med Sci 2014; 14: 105-109.
Nøddegaard F, Talbot R, Sharp PJ. Effect of delayed step-up lighting on plasma LH and reproductive function in broiler breeders. Poultry Sci 2000; 79: 778-783.
Li G, Sun DX, Yu Y, Liu WJ, Tang SQ, Zhang Y, Wang YC, Zhang SL, Zhang Y. Genetic effect of the follicle-stimulating hormone receptor gene on reproductive traits in Beijing You chickens. Poultry Sci 2011; 90: 2487-2492.
Zhu GY, Kang L, Wei QQ, Cui XX, Wang SZ, Chen YX, Jiang YL. Expression and regulation of MMP1, MMP3, and MMP9 in the chicken ovary in response to gonadotropins, sex hormones, and TGFB1. Biol Reprod 2014; 90: 57.
Johnson PA, Dickerman RW, Bahr JM. Decreased granulosa cell luteinizing hormone sensitivity and altered thecal estradiol concentration in the aged hen ( Gallus domesticus ). Biol Reprod 1986; 35: 641-646.
Moudgal RP, Razdan MN. Induction of ovulation in vitro in the hen: dependency of the response to LH on age and rate of lay. J Endocrinol 1985; 106: 67-69.
Di Nardo A, Vitiello A, Gallo RL. Cutting edge: mast cell antimicrobial activity is mediated by expression of cathelicidin antimicrobial peptide. J Immunol 2003; 170: 2274-2278.
Lezza AM, Pesce V, Cormio A, Fracasso F, Vecchiet J, Felzani G, Cantatore P, Gadaleta MN. Increased expression of mitochondrial transcription factor A and nuclear respiratory factor-1 in skeletal muscle from aged human subjects. FEBS Lett 2001; 501: 74-78.
Yao J, Zhou E, Wang YC, Xu F, Zhang DH, Zhong DW. MicroRNA-200a inhibits cell proliferation by targeting mitochondrial transcription factor A in breast cancer. DNA Cell Biol 2014; 33: 291-300.
Kang D, Kim SH, Hamasaki N. Mitochondrial transcription factor A (TFAM): roles in maintenance of mtDNA and cellular functions. Mitochondrion 2007; 7: 39-44.
Ma YS, Wu SB, Lee WY, Cheng JS, Wei YH. Response to the increase of oxidative stress and mutation of mitochondrial DNA in aging. BBA-Gen Subjects 2009; 1790: 1021-1029.
Tsutsui H. Mitochondrial oxidative stress and heart failure. Internal Med 2006; 45: 809-813.
Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell B 2010; 42: 1634- 1650.
Kaipia A, Hsueh AJW. Regulation of ovarian follicle atresia. Annu Rev Physiol 1997; 59: 349-363.
Sato N, Funayama N, Nagafuchi A, Yonemura S, Tsukita S. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J Cell Sci 1992; 103: 131-143.
Tamura H, Takasaki A, Miwa I, Taniguchi K, Maekawa R, Asada H, Taketani T, Matsuoka A, Yamagata Y, Shimamura K et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 2008; 44: 280-287.
Tsai-Turton M, Luderer U. Opposing effects of glutathione depletion and follicle- stimulating hormone on reactive oxygen species and apoptosis in cultured preovulatory rat follicles. Endocrinology 2006; 147: 1224-1236.