不同饲喂水平对绵羊睾丸发育、睾酮合成相关基因及雄激素受体(AR)表达的影响

doi:10.11843/j.issn.0366-6964.2021.05.017

Abstract

Abstract: The objective of this study was to investigate the effects of different feeding levels on testicular development, testosterone (T) concentration, the expression of testosterone synthesis-related genes and androgen receptor (AR) in testis of sheep. Eighteen healthy 4-month-old Dorper×Jinzhong crossed F1 ram lambs with similar body weight of ((35±0.5) kg) were selected and randomly divided into 3 groups for a comparative slaughter trial. They were offered one type of feed at 100%(AL group), 65%(AL65 group) and 40%(AL40 group) of ad libitum intake, respectively. When any lamb in AL group reached a body weight of 50 kg, all animals were slaughtered. After the testicular circumference and length were examined, tissue samples were collected for analyzing testosterone concentration and histological parameters using ELISA and H-E staining method, respectively. The expression of testosterone synthesis-related genes and AR mRNA were detected using quantitative real-time PCR. Localization and quantification of AR in testis of lambs were determined by immunohistochemistry and Western blotting analysis. The results showed that the length and circumference of testis in the AL40 group were significantly lower than those in the AL group(P<0.05), no significant difference was observed between the AL40 and AL65 groups(P>0.05). The thickness of germinal epithelium of lambs in AL40 group was not significantly different from that in AL65 group, but both were significantly lower than that in AL group (P<0.05). The density of spermatogenic cells and leydig cells were remarkably increased with the increasing feeding levels(P<0.05). Testosterone concentration, the expression of STAR, 3β-HSD and AR genes and AR protein were also significantly increased(P<0.05). Immunopositive product of AR was detected in leydig cells,primary spermatocytes, spermatids, peritubular myoid cells and perivascular smooth muscle cells. In conclusion, the testicular development, T level, the expression of testosterone synthesis-related genes and AR were regulated by dietary nutrition level. Dietary nutrition could modulate the process of spermatogenesis by regulating T concentration and the sensitivity of spermatogenic cells to T, which could influence the sexual maturation and reproductive performance of male animals.

Key words: feeding level, sheep, testis, testosterone, androgen receptor

CLC Number:

S826.4

SHI Lei, NIU Hongze, YAO Xiaolei, SONG Ruigao, Lü Lihua, ZHANG Chunxiang, ZHANG Jianxin, REN Youshe. Effects of Different Feeding Levels on Testis Development and the Expression of Steroidogenesis-Related Genes and Androgen Receptor (AR) in Sheep[J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(5): 1317-1327.

References 41

[1]	GAUVIN M C,PILLAI S M,REED S A,et al.Poor maternal nutrition during gestation in sheep alters prenatal muscle growth and development in offspring[J].J Anim Sci,2020,98(1):skz388.
[2]	MASSUQUETTO A,PANISSON J C,SCHRAMM V G,et al.Effects of feed form and energy levels on growth performance,carcass yield and nutrient digestibility in broilers[J].Animal,2020,14(6):1139-1146.
[3]	LI H,SONG H,HUANG M,et al.Impact of food restriction on ovarian development,RFamide-related peptide-3 and the hypothalamic-pituitary-ovarian axis in pre-pubertal ewes[J].Reprod Domest Anim,2014,49(5):831-838.
[4]	YING S J,WANG Z Y,WANG C L,et al.Effect of different levels of short-term feed intake on folliculogenesis and follicular fluid and plasma concentrations of lactate dehydrogenase,glucose,and hormones in Hu sheep during the luteal phase[J]. Reproduction,2011,142(5):699-710.
[5]	GUAN Y J,LIANG G X,HAWKEN P A R,et al.Roles of small RNAs in the effects of nutrition on apoptosis and spermatogenesis in the adult testis[J].Sci Rep,2015,5:10372.
[6]	WEBB R,GARNSWORTHY P C,GONG J G,et al.Control of follicular growth:local interactions and nutritional influences[J]. J Anim Sci,2004,82(E-Suppl):E63-E74.
[7]	PANG J,LI F Z,FENG X,et al.Influences of different dietary energy level on sheep testicular development associated with AMPK/ULK1/autophagy pathway[J].Theriogenology,2018,108:362-370.
[8]	李碧波,雷耀庚,王兴涛,等.不同能量水平和采精频率对绒山羊种公羊精液品质的影响[J].中国畜牧兽医,2015,42(8): 2116-2123.LI B B,LEI Y G,WANG X T,et al.Effects of different dietary energy level and semen collection frequency on buck’s semen quality in cashmere goats[J].China Animal Husbandry & Veterinary Medicine,2015,42(8):2116-2123.(in Chinese)
[9]	郑王龙,刘青,王亚军,等.玉米赤霉烯酮对小鼠睾丸间质细胞内StAR蛋白及类固醇合成关键酶表达的影响[J].畜牧兽医学报,2014,45(7):1091-1096.ZHENG W L,LIU Q,WANG Y J,et al.Effects of Zearalenone on the expression of Steroidogenic acute regulatory protein and key enzymes in primary Leydig cells[J].Acta Veterinaria et Zootechnica Sinica,2014,45(7):1091-1096.(in Chinese)
[10]	WALTERS K A,SIMANAINEN U,HANDELSMAN D J.Molecular insights into androgen actions in male and female reproductive function from androgen receptor knockout models[J].Hum Reprod Update,2010,16(5):543-558.
[11]	ZHANG Q X,ZHANG X Y,ZHANG Z M,et al.Identification of testosterone-/androgen receptor-regulated genes in mouse Sertoli cells[J].Asian J Androl,2012,14(2):294-300.
[12]	SHEN H,FAN X R,ZHANG Z,et al.Effects of elevated ambient temperature and local testicular heating on the expressions of heat shock protein 70 and androgen receptor in boar testes[J].Acta Histochem,2019,121(3):297-302.
[13]	PEARL C A,MASON H,ROSER J F.Immunolocalization of estrogen receptor alpha,estrogen receptor beta and androgen receptor in the pre-,peri- and post-pubertal stallion testis[J].Anim Reprod Sci,2011,125(1-4):103-111.
[14]	BOUKENAOUI N,MOUDILOU E,CHEVALIER C,et al.Postnatal changes in testicular development and androgen receptors immunolocalization in D’Man ram lambs[J].Folia Histochem Cytobiol,2012,50(1):38-45.
[15]	WANG Q B,LI W,LIU X S,et a1.A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth[J].Mol Cell,2007,27(3):380-392.
[16]	KENNY D A,BYRNE C J.Review:The effect of nutrition on timing of pubertal onset and subsequent fertility in the bull[J].Animal,2018,12(s1):s36-s44.
[17]	董志岩,刘亚轩,方桂友,等.不同氨基酸水平的低蛋白质饲粮对后备母猪初情日龄、血清代谢产物和激素浓度的影响[J].畜牧兽医学报,2018,49(1):131-138.DONG Z Y,LIU Y X,FANG G Y,et al.Effects of different dietary amino acid levels on age of puberty,serum metabolites and hormone concentration of replacement gilts fed low protein diets[J].Acta Veterinaria et Zootechnica Sinica,2018,49(1): 131-138.(in Chinese)
[18]	DE BRUN V,LOOR J J,NAYA H,et al.The embryo affects day 14 uterine transcriptome depending on nutritional status in sheep.a.Metabolic adaptation to pregnancy in nourished and undernourished ewes[J].Theriogenology,2020,146:14-19.
[19]	VONNAHME K A,WILSON M E,FORD S P.Conceptus competition for uterine space:different strategies exhibited by the Meishan and Yorkshire pig[J].J Anim Sci,2002,80(5):1311-1316.
[20]	FAIR S,DOYLE D N,DISKIN M G,et al.The effect of dietary n-3 polyunsaturated fatty acids supple-mentation of rams on semen quality and subsequent quality of liquid stored semen[J].Theriogenology,2014,81(2):210-219.
[21]	QU Y H,JIAN L Y,LIU C,et al.Identification of candidate genes in regulation of spermatogenesis in sheep testis following dietary vitamin E supplementation[J].Anim Reprod Sci,2019,205:52-61.
[22]	MERINO O,SÁNCHEZ R,GREGORIO M B,et al.Effect of high-fat and vitamin D deficient diet on rat sperm quality and fertility[J].Theriogenology,2019,125:6-11.
[23]	许贵善,刁其玉,纪守坤,等.不同饲喂水平对肉用绵羊生长性能、屠宰性能及器官指数的影响[J].动物营养学报,2012, 24(5): 953-960.XU G S,DIAO Q Y,JI S K,et al.Effects of different feeding levels on growth performance,slaughter performance and organ indexes of mutton sheep[J].Chinese Journal of Animal Nutrition,2012,24(5):953-960.(in Chinese)
[24]	PANG J,LI F Z,FENG X,et al.Influences of different dietary energy level on sheep testicular development associated with AMPK/ULK1/autophagy pathway[J].Theriogenology,2018,108:362-370.
[25]	ZHAO J X,MA X H,JIN Y Q,et al.Energy requirements for the maintenance and growth of Dorper-Jinzhong crossbred ram lambs[J].Ital J Anim Sci,2016,15(1):94-102.
[26]	杜卫佳,张英杰,李发弟,等.不同饲喂水平对无角陶赛特和小尾寒羊杂交二代母羔生长、屠宰性能及器官指数的影响[J].甘肃农业大学学报,2013,48(4):1-5.DU W J,ZHANG Y J,LI F D,et al.Effects of different feeding levels on growth performance, slaughter performance and organ indexes of Polled Dorset×Small Tailed Han sheep crossbred female lambs[J].Journal of Gansu Agricultural University, 2013,48(4):1-5.(in Chinese)
[27]	GLASS A R,MELLITT R,VIGERSKY R A,et al.Hypoandrogenism and abnormal regulation of gonadotropin secretion in rats fed a low protein diet[J].Endocrinology,1979,104(2):438-442.
[28]	SHI L,SONG R G,YAO X L,et al.Effects of maternal dietary selenium (Se-enriched yeast) on testis development, testosterone level and testicular steroidogenesis-related gene expression of their male kids in Taihang Black goats[J]. Theriogenology,2018,114:95-102.
[29]	SELVARAJU S,SIVASUBRAMANI T,RAGHAVENDRA B S,et al.Effect of dietary energy on seminal plasma insulin-like growth factor-I (IGF-I),serum IGF-I and testosterone levels,semen quality and fertility in adult rams[J].Theriogenology, 2012,78(3):646-655.
[30]	马瑞,吴赛珠,吕红松,等.睾酮对大鼠血管平滑肌细胞增殖的影响及其与雄激素受体水平变化的关系[J].中华心血管病杂志,2003,31(6):440-443.MA R,WU S Z, LÜ H S,et al.Effect of testosterone on the proliferation of vascular smooth muscle cells and its relation with androgen receptor expression[J].Chinese Journal of Cardiology,2003,31(6):440-443.(in Chinese)
[31]	KAMIŃSKA A,PARDYAK L,MAREK S,et al.Notch signaling regulates nuclear androgen receptor AR and membrane androgen receptor ZIP9 in mouse Sertoli cells[J].Andrology,2020,8(2):457-472.
[32]	LUAN Z J,FAN X M,SONG H Z,et al.Testosterone promotes GPX5 expression of goat epididymal epithelial cells cultured in vitro[J].In Vitro Cell Dev Biol Anim,2019,55(9):677-685.
[33]	EDELSZTEIN N Y,RACINE C,DI CLEMENTE N,et al.Androgens downregulate anti-Müllerian hormone promoter activity in the Sertoli cell through the androgen receptor and intact steroidogenic factor 1 sites[J].Biol Reprod,2018,99(6): 1303-1312.
[34]	GENOVESE P,HERRERA E,RIAÑO V,et al.Subnutrition effects during pregnancy and lactation on mitosis,apoptosis and androgen receptor expression in the rat testis[J].Reprod Domest Anim,2019,54(3):506-513.
[35]	于淼瑛,周虚,刘立文,等.代谢信号对能量影响猪卵泡发育的作用[J].动物医学进展,2005,26(11):22-27.YU M Y,ZHOU X,LIU L W,et al.The effects of metabolic signals on swine ovarian follicular development influenced by energy[J].Progress in Veterinary Medicine,2005,26(11):22-27.(in Chinese)
[36]	李振,任有蛇,焦光月,等.雄激素受体基因在绵羊公羔不同组织中的表达特性及性腺中的定位[J].畜牧兽医学报,2013,44(8):1251-1257.LI Z,REN Y S,JIAO G Y,et al.The expression of androgen receptor gene in different tissues and cellular localization in gonad of male sheep lambs[J].Acta Veterinaria et Zootechnica Sinica,2013,44(8):1251-1257.(in Chinese)
[37]	GE W B,XIAO L F,DUAN H W,et al.Androgen receptor,aromatase,oestrogen receptor α/β and G protein-coupled receptor 30 expression in the testes and epididymides of adult sheep[J].Reprod Domest Anim,2020,55(4):460-468.
[38]	王乾梅,袁莉刚,李承晔,等.性激素受体在子午岭黑山羊隐睾及正常睾丸中的分布比较[J].畜牧兽医学报,2020,51(6): 1455-1465.WANG Q M,YUAN L G,LI C Y,et al.Distribution of sex hormone receptors in cryptorchidism and normal testes of Ziwuling black goat[J].Acta Veterinaria et Zootechnica Sinica,2020,51(6):1455-1465.(in Chinese)
[39]	HAZRA R,CORCORAN L,HE X,et al.Effect of temporal Sertoli cell androgen receptor expression on Leydig cell development and function in mice[J].Biol Reprod,2012,87(S1):22.
[40]	HAZRA R,JIMENEZ M,DESAI R,et al.Sertoli cell androgen receptor expression regulates temporal fetal and adult Leydig cell differentiation,function,and population size[J].Endocrinology,2013,154(9):3410-3422.
[41]	O’SHAUGHNESSY P J,MITCHELL R T,MONTRIRO A,et al.Androgen receptor expression is required to ensure development of adult Leydig cells and to prevent development of steroidogenic cells with adrenal characteristics in the mouse testis[J].BMC Dev Biol,2019,19(1):8.

Effects of Different Feeding Levels on Testis Development and the Expression of Steroidogenesis-Related Genes and Androgen Receptor (AR) in Sheep

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