日粮鱼油对高脂日粮饲喂小鼠发情周期和机体产热的影响

doi:10.11843/j.issn.0366-6964.2021.07.012

Abstract

Abstract: This study aimed to investigate the effects of dietary fish oil on estrous cycles and body heat production of mice fed high-fat diets (HFD). Thirty-six C57BL/6 J female mice at 4-week-old were randomly divided into 3 groups (n=12):control group, HFD group and HFD + fish oil group, respectively. The control group was fed with a standard rodent chow diet (AIN-93G). The HFD group and HFD + fish oil group were fed HFD (60% energy from fat) without or with 5% fish oil (equally replace lard energy), respectively. During the trial, the mice were used for various examinations, including body composition (12-week-old), body energy metabolism (16-week-old), brown adipose tissue(BAT) temperature (18-week-old), body core temperature (rectum temperature, 18-week-old) and estrous cycles (20-week-old). At the end of the experiment, the blood sample was collected from eye sockets, and the serum was isolated for examination of follicle-stimulating hormone (FSH) and estradiol (E2). In addition, the subcutaneous fat, abdominal fat and interscapular BAT were collected, weighed and used for detection of the protein expression of genes related to thermogenic program in adipose tissues (UCP1, Cyto C) by Western blot, and the mRNA expression of genes related to thermogenic program in brown adipose tissues (UCP1, PRDM16, PGC1α, Cidea, Elovl3) by real-time fluorescence quantitative PCR. The results showed that HFD induced a significant increase in body fat content (12-week-old), and subcutaneous fat and abdominal fat mass (21-week-old) compared with the control diet (P<0.05). Notably, the HFD-induced increase of fat content was significantly reduced by fish oil supplementation (P<0.05). In addition, HFD led irregular estrous cycles, with prolonged cycle duration and shortened estrus period, and decreased the level of FSH and E2 in serum (P<0.05). However, the HFD-induced estrous cycle irregularity of mice was alleviated by fish oil supplementation and the level of FSH and E2 in serum was increased (P<0.05). Meanwhile, fish oil supplementation increased BAT activation/thermogenesis and promoted white adipose tissue(WAT) browning in HFD-fed mice, with enhanced the expression of thermogenic marker genes in interscapular brown adipose tissue (iBAT) and inguinal white adipose tissue (iWAT) (P<0.05). These findings suggest that dietary fish oil can alleviate HFD-induced estrous cycle irregularity, possibly associate with enhanced body thermogenesis via BAT activation and WAT browning.

Key words: fish oil, estrous cycle, BAT thermogenesis, WAT browning, mouse

CLC Number:

Q493.99

YANG Xiaohua, LIU Fangfang, ZHANG Fenglin, YI Xin, CHEN Lin, SHU Gang, WANG Lina, ZHU Xiaotong, GAO Ping, JIANG Qingyan, WANG Songbo. Effects of Dietary Fish Oil on Estrous Cycles and Body Heat Production in Mice Fed High-fat Diets[J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(7): 1891-1902.

References 51

[1]	BIVENS C L M,OLSTER D H.Abnormal estrous cyclicity and behavioral hyporesponsiveness to ovarian hormones in genetically obese Zucker female rats[J].Endocrinology,1997,138(1):143-148.
[2]	SCHILLO K K.Effects of dietary energy on control of luteinizing hormone secretion in cattle and sheep[J].J Anim Sci,1992,70(4):1271-1282.
[3]	FULLSTON T,PALMER N O,OWENS J A,et al.Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice[J].Hum Reprod,2012,27(5):1391-1400.
[4]	GIL-CAMPOS M,CAÑETE R,GIL A.Hormones regulating lipid metabolism and plasma lipids in childhood obesity[J].Int J Obes Relat Metab Disord,2004,28(Suppl 3):S75-S80.
[5]	NGADJUI E,NKENG-EFOUET P A,NGUELEFACK T B,et al.High fat diet-induced estrus cycle disruption:effects of Ficus asperifolia[J].J Complement Integr Med,2015,12(3):205-215.
[6]	CROSIGNANI P G,COLOMBO M,VEGETTI W,et al.Overweight and obese anovulatory patients with polycystic ovaries:parallel improvements in anthropometric indices,ovarian physiology and fertility rate induced by diet[J].Hum Reprod,2003,18(9):1928-1932.
[7]	古兰·托合提木拉提,叶尔努尔·吐苏甫汗,马玉兰,等.高脂高糖饮食暴露诱导大鼠多囊卵巢综合征研究[J].生殖医学杂志,2019,28(2):169-173.GULAN T,ELNUR T,MA Y L,et al.Exposure of high fat and high sugar diet induces polycystic ovarian syndrome in rats[J].Journal of Reproductive Medicine,2019,28(2):169-173.(in Chinese)
[8]	BERMEJO-ALVAREZ P,ROSENFELD C S,ROBERTS R M.Effect of maternal obesity on estrous cyclicity,embryo development and blastocyst gene expression in a mouse model[J].Hum Reprod,2012,27(12):3513-3522.
[9]	HARTZ A J,BARBORIAK P N,WONG A,et al.The association of obesity with infertility and related menstural abnormalities in women[J].Int J Obes,1979,3(1):57-73.
[10]	金金,张家瑞,矫健.营养因素对猪繁殖性能的影响[J].养殖技术顾问,2010,(8):49.JIN J,ZHANG J R,JIAO J.Effects of nutritional factors on reproductive performance of pigs[J].Technical Advisor for Animal Husbandry,2010,(8):49.(in Chinese)
[11]	田亮,姚姣姣,胡健,等.妊娠期脂肪沉积对母猪繁殖性能及胎盘脂代谢基因表达的影响[C]//中国畜牧兽医学会家畜环境卫生学分会2014年学术年会论文集.武汉:中国畜牧兽医学会家畜环境卫生学分会,2014.TIAN L,YAO J J,HU J,et al.Effects of fat deposition during pregnancy on reproductive performance and gene expression of placental lipid metabolism in sows[C]//Proceedings of the 2014 Annual Meeting of Livestock Environmental Hygiene Branch,Chinese Society of Animal Science and Veterinary Medicine.2014.(in Chinese)
[12]	ROSEN E D,SPIEGELMAN B M.What we talk about when we talk about fat[J].Cell,2014,156(1-2):20-44.
[13]	CANNON B,NEDERGAARD J.Brown adipose tissue:function and physiological significance[J].Physiol Rev,2004,84(1):277-359.
[14]	INAGAKI T,SAKAI J,KAJIMURA S.Transcriptional and epigenetic control of brown and beige adipose cell fate and function[J].Nat Rev Mol Cell Biol,2016,17(8):480-495.
[15]	HOFFMANN J M,GRVNBERG J R,CHURCH C,et al.BMP4 gene therapy in mature mice reduces BAT activation but protects from obesity by browning subcutaneous adipose tissue[J].Cell Rep,2017,20(5):1038-1049.
[16]	MIN B K,KANG H J,CHOI B J,et al.Phenylbutyrate ameliorates high-fat diet-induced obesity via brown adipose tissue activation[J].Biol Pharm Bull,2019,42(9):1554-1561.
[17]	SRIVASTAVA S,VEECH R L.Brown and brite:the fat soldiers in the anti-obesity fight[J].Front Physiol,2019,10:38.
[18]	SYMONDS M E,ALDISS P,DELLSCHAFT N,et al.Brown adipose tissue development and function and its impact on reproduction[J].J Endocrinol,2018,238(1):R53-R62.
[19]	YUAN X X,HU T,ZHAO H,et al.Brown adipose tissue transplantation ameliorates polycystic ovary syndrome[J].Proc Natl Acad Sci U S A,2016,113(10):2708-2713.
[20]	ZHANG F L,SU H,SONG M,et al.Calcium supplementation alleviates high-fat diet-induced estrous cycle irregularity and subfertility associated with concomitantly enhanced thermogenesis of brown adipose tissue and browning of white adipose tissue[J].J Agric Food Chem,2019,67(25):7073-7081.
[21]	WANG S,LIANG X,YANG Q,et al.Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) α1[J].Int J Obes,2015,39(6):967-976.
[22]	YUAN X X,WEI G,YOU Y L,et al.Rutin ameliorates obesity through brown fat activation[J].FASEB J,2017,31(1):333-345.
[23]	ZHANG F L,AI W,HU X Q,et al.Phytol stimulates the browning of white adipocytes through the activation of AMP-activated protein kinase (AMPK) α in mice fed high-fat diet[J].Food Funct,2018,9(4):2043-2050.
[24]	WANG B,FU X,LIANG X W,et al.Retinoic acid induces white adipose tissue browning by increasing adipose vascularity and inducing beige adipogenesis of PDGFRα+ adipose progenitors[J].Cell Discov,2017,3:17036.
[25]	CALDER P C.Omega-3 fatty acids and inflammatory processes:from molecules to man[J].Biochem Soc Trans,2017,45(5):1105-1115.
[26]	SCHUNCK W H,KONKEL A,FISCHER R,et al.Therapeutic potential of omega-3 fatty acid-derived epoxyeicosanoids in cardiovascular and inflammatory diseases[J].Pharmacol Ther,2017,183:177-204.
[27]	MARTINS A R,CRISMA A R,MASI L N,et al.Attenuation of obesity and insulin resistance by fish oil supplementation is associated with improved skeletal muscle mitochondrial function in mice fed a high-fat diet[J].J Nutr Biochem,2018,55:76-88.
[28]	BARGUT T C L,SOUZA-MELLO V,MANDARIM-DE-LACERDA C A,et al.Fish oil diet modulates epididymal and inguinal adipocyte metabolism in mice[J].Food Funct,2016,7(3):1468-1476.
[29]	MA X S,WENG X C,HU X S,et al.Roles of different n-3/n-6 PUFA ratios in ovarian cell development and steroidogenesis in PCOS rats[J].Food Funct,2019,10(11):7397-7406.
[30]	HALADE G V,RAHMAN M M,WILLIAMS P J,et al.Combination of conjugated linoleic acid with fish oil prevents age-associated bone marrow adiposity in C57Bl/6 J mice[J].J Nutr Biochem,2011,22(5):459-469.
[31]	ARAI T,KIM H J,CHIBA H,et al.Anti-obesity effect of fish oil and fish oil-fenofibrate combination in female KK mice[J].J Atheroscler Thromb,2009,16(5):674-683.
[32]	韩海银.受精母鸡日粮中添加鱼油可有效降低仔鸡脂肪沉积水平[J].北方牧业,2018(5):29.HAN H Y.Fish oil supplementation in the diet of fertilized hens can effectively reduce the fat deposition level of broilers[J].Northern Animal Husbandry,2018,(5):29.(in Chinese)
[33]	LOPES P A,MARTINS R,DA SILVA I V,et al.Modulation of aquaporin gene expression by n-3 long-chain PUFA lipid structures in white and brown adipose tissue from hamsters[J].Br J Nutr,2018,120(10):1098-1106.
[34]	OUDART H,GROSCOLAS R,CALGARI C,et al.Brown fat thermogenesis in rats fed high-fat diets enriched with n-3 polyunsaturated fatty acids[J].Int J Obes Relat Metab Disord,1997,21(11):955-962.
[35]	AKAMINE E H,MARCAL A C,CAMPOREZ J P,et al.Obesity induced by high-fat diet promotes insulin resistance in the ovary[J].J Endocrinol,2010,206(1):65-74.
[36]	WEI S Y,SCHMIDT M D,DWYER T,et al.Obesity and menstrual irregularity:associations with SHBG,testosterone,and insulin[J].Obesity,2009,17(5):1070-1076.
[37]	BROUGHTON K S,BAYES J,CULVER B.High α-linolenic acid and fish oil ingestion promotes ovulation to the same extent in rats[J].Nut Res,2010,30(10):731-738.
[38]	MAHLA A S,CHAUDHARI R K,VERMA A K,et al.Effect of dietary supplementation of omega-3 polyunsaturated fatty acid (PUFA) rich fish oil on reproductive performance of the goat (Capra hircus)[J].Theriogenology,2017,99:79-89.
[39]	PERGOLA G D,MALDERA S,TARTAGNI M,et al.Inhibitory effect of obesity on gonadotropin,estradiol,and inhibin B levels in fertile women[J].Obesity(Silver Spring),2006,14(11):1954-1960.
[40]	MAILLARD V,DESMARCHAIS A,DURCIN M,et al.Docosahexaenoic acid (DHA) effects on proliferation and steroidogenesis of bovine granulosa cells[J].Reprod Biol Endocrinol,2018,16:40.
[41]	BAUER J L,KUHN K,BRADFORD A P,et al.Reduction in FSH throughout the menstrual cycle after omega-3 fatty acid supplementation in young normal weight but not obese women[J].Reprod Sci,2019,26(8):1025-1033.
[42]	KIM M,GOTO T,YU R,et al.Fish oil intake induces UCP1 upregulation in brown and white adipose tissue via the sympathetic nervous system[J].Sci Rep,2015,5:18013.
[43]	CAREY A L,VORLANDER C,REDDY-LUTHMOODOO M,et al.Reduced UCP-1 content in In vitro differentiated beige/brite adipocytes derived from preadipocytes of human subcutaneous white adipose tissues in obesity[J].PLoS One,2014,9(3):e91997.
[44]	LI H Y,XI Q Y,XIONG Y Y,et al.Identification and comparison of microRNAs from skeletal muscle and adipose tissues from two porcine breeds[J].Anim Genet,2012,43(6):704-713.
[45]	HU T,YUAN X X,YE R C,et al.Brown adipose tissue activation by rutin ameliorates polycystic ovary syndrome in rat[J].J Nutr Biochem,2017,47:21-28.
[46]	WANG W S,SEALE P.Control of brown and beige fat development[J].Nat Rev Mol Cell Biol,2016,17(11):691-702.
[47]	严琴慧,周炜,朱晓蕾,等.ω3-长链多不饱和脂肪酸改善早期过度营养导致的大鼠成年期代谢异常[J].中华内分泌代谢杂志,2020,36(1):63-71.YAN Q H,ZHOU W,ZHU X L,et al.Omega3-polyunsaturated fatty acid ameliorates metabolic disorders in adulthood rats caused by postnatal early overfeeding[J].Chinese Journal of Endocrinology and Metabolism,2020,36(1):63-71.(in Chinese)
[48]	ZHAO M,CHEN X L.Eicosapentaenoic acid promotes thermogenic and fatty acid storage capacity in mouse subcutaneous adipocytes[J].Biochem Biophys Res Commun,2014,450(4):1446-1451.
[49]	PAHLAVANI M,RAZAFIMANJATO F,RAMALINGAM L,et al.Eicosapentaenoic acid regulates brown adipose tissue metabolism in high-fat-fed mice and in clonal brown adipocytes[J].J Nutr Biochem,2017,39:101-109.
[50]	DHILLON S S,BELSHAM D D.Estrogen inhibits NPY secretion through membrane-associated estrogen receptor (ER)-α in clonal,immortalized hypothalamic neurons[J].Int J Obes (Lond),2011,35(2):198-207.
[51]	LOH K,LEE K,CLARKS I,et al.Peripheral Y1 receptor antagonism promotes browning of white adipose tissue and protects from diet-induced obesity[C]//第三届中国生物物理学会代谢生物学分会学术研讨会论文集.上海:中国生物物理学会,2019.LOH K, LEE K, CLARKS I,et al.Peripheral Y1 receptor antagonism promotes browning of white adipose tissue and protects from diet-induced obesity[C]//Proceedings of the 3rd Symposium of metabolic biology branch of Biophysical Society of China. Shanghai:Biophysical Society of China, 2019. (in Chinese)

Effects of Dietary Fish Oil on Estrous Cycles and Body Heat Production in Mice Fed High-fat Diets

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