SPECIAL COLUMN:RESEARCH PROGRESS ON FEED NUTRITION

Advances in Nutritional Regulation of Follicular Development Quality of Sows

  • XU Baoyang ,
  • QIN Wenxia ,
  • YAN Xianghua
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  • Hubei Hongshan Laboratory, State Key Laboratory of Agricultural Microbiology, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan 430070, China

Received date: 2022-08-01

  Online published: 2022-10-17

Abstract

Follicle development quality is one of the key factors determining the reproductive performance of mammals. Nutrients can directly or indirectly regulate follicle development quality of mammals through their metabolites. In this review, we summarized the recent progress of follicular development in sows and its nutritional control approaches, combined with the role of gut microbiota in this process, discussed the possible mechanism of "nutrients-gut microbiota-ovary axis", it may provide possible strategies for improving the quality of follicular development of sows by targeting and controlling gut microbiota.

Cite this article

XU Baoyang , QIN Wenxia , YAN Xianghua . Advances in Nutritional Regulation of Follicular Development Quality of Sows[J]. Chinese Journal of Animal Nutrition, 2022 , 34(10) : 6334 -6342 . DOI: 10.3969/j.issn.1006-267x.2022.10.026

References

[1] CHRISTENSON R K.Ovulation rate and embryonic survival in Chinese Meishan and white crossbred pigs[J].Journal of Animal Science,1993,71(11):3060-3066.  
[2] KNOX R V.Follicle development in pigs:state of the art[J/OL].Molecular Reproduction&Development:1-11[2022-07-15].https://doi.org/10.1002/mrd.23576.DOI:10.1002/mrd.23576.
[3] COSTERMANS N G J.Physiological and molecular aspects of ovarian follicular developmental competence in sows[D].Ph.D.Thesis.Wageningen:Wageningen University&Research,2020.
[4] ZHUO Y,CAO M,GONG Y C,et al.Gut microbial metabolism of dietary fibre protects against high energy feeding induced ovarian follicular atresia in a pig model[J].British Journal of Nutrition,2021,125(1):38-49.  
[5] GRAHAM M E,HERBERT W G,SONG S D,et al.Gut and vaginal microbiomes on steroids:implications for women's health[J].Trends in Endocrinology&Metabolism,2021,32(8):554-565.  
[6] HAN Q X,WANG J,LI W P,et al.Androgen-induced gut dysbiosis disrupts glucolipid metabolism and endocrinal functions in polycystic ovary syndrome[J].Microbiome,2021,9(1):101.
[7] SILVA M S B,GIACOBINI P.Don't trust your gut:when gut microbiota disrupt fertility[J].Cell Metabolism,2019,30(4):616-618.  
[8] JIANG X Y,LU N S,XUE Y,et al.Crude fiber modulates the fecal microbiome and steroid hormones in pregnant Meishan sows[J].General and Comparative Endocrinology,2019,277:141-147.
[9] QI X Y,YUN C Y,PANG Y L,et al.The impact of the gut microbiota on the reproductive and metabolic endocrine system[J].Gut Microbes,2021,13(1):1894070.
[10] HUSSAIN T,MURTAZA G,KALHORO D H,et al.Relationship between gut microbiota and host-metabolism:emphasis on hormones related to reproductive function[J].Animal Nutrition,2021,7(1):1-10.  
[11] NURIEL-OHAYON M,NEUMAN H,ZIV O,et al.Progesterone increases Bifidobacterium relative abundance during late pregnancy[J].Cell Reports,2019,27(3):730-736.e3.  
[12] KNOX R V.Physiology and endocrinology symposium:factors influencing follicle development in gilts and sows and management strategies used to regulate growth for control of estrus and ovulation[J].Journal of Animal Science,2019,97(4):1433-1445.  
[13] UYAR A,TORREALDAY S,SELI E.Cumulus and granulosa cell markers of oocyte and embryo quality[J].Fertility and Sterility,2013,99(4):979-997.  
[14] EPPIG J J.Reproduction:oocytes call,granulosa cells connect[J].Current Biology,2018,28(8):R354-R356.
[15] MATSUDA F,INOUE N,MANABE N,et al.Follicular growth and atresia in mammalian ovaries:regulation by survival and death of granulosa cells[J].The Journal of Reproduction and Development,2012,58(1):44-50.  
[16] COSTERMANS N G J,TEERDS K J,MIDDELKOOP A,et al.Consequences of negative energy balance on follicular development and oocyte quality in primiparous sows[J].Biology of Reproduction,2020,102(2):388-398.  
[17] KAUFFOLD J,GOTTSCHALK J,SCHNEIDER F,et al.Effects of feeding level during lactation on FSH and LH secretion patterns,and follicular development in primiparous sows[J].Reproduction in Domestic Animals,2008,43(2):234-238.  
[18] KNOX R V,VATZIAS G,NABER C H,et al.Plasma gonadotropins and ovarian hormones during the estrous cycle in high compared to low ovulation rate gilts[J].Journal of Animal Science,2003,81(1):249-260.  
[19] HAN T,BJÖRKMAN S,SOEDE N M,et al.IGF-1 concentration patterns and their relationship with follicle development after weaning in young sows fed different pre-mating diets[J].Animal,2020,14(7):1493-1501.  
[20] CHEN T Y,STOTT P,ATHORN R Z,et al.Undernutrition during early follicle development has irreversible effects on ovulation rate and embryos[J].Reproduction,Fertility,and Development,2012,24(6):886-892.  
[21] TOKACH M D,MENEGAT M B,GOURLEY K M,et al.Review:nutrient requirements of the modern high-producing lactating sow,with an emphasis on amino acid requirements[J].Animal,2019,13(12):2967-2977.  
[22] HUBER L,DE LANGE C F M,KROGH U,et al.Impact of feeding reduced crude protein diets to lactating sows on nitrogen utilization[J].Journal of Animal Science,2015,93(11):5254-5264.  
[23] DING S J,AZAD M A K,FANG J,et al.Impact of sulfur-containing amino acids on the plasma metabolomics and intestinal microflora of the sow in late pregnancy[J].Food&Function,2019,10(9):5910-5921.  
[24] BEEBE L F S,VASSILIEV I,MCILFATRICK S,et al.Adding essential amino acids at a low concentration improves the development of in vitro fertilized porcine embryos[J].The Journal of Reproduction and Development,2009,55(4):373-377.  
[25] YANG H,FOXCROFT G R,PETTIGREW J E,et al.Impact of dietary lysine intake during lactation on follicular development and oocyte maturation after weaning in primiparous sows[J].Journal of Animal Science,2000,78(4):993-1000.  
[26] HUSSAIN T, TAN B, MURTAZA G, et al. Role of dietary amino acids and nutrient sensing system in pregnancy associated disorders[J].Frontiers in Pharmacology,2020,11:586979.
[27] SUI S Y,JIA Y M,HE B,et al.Maternal low-protein diet alters ovarian expression of folliculogenic and steroidogenic genes and their regulatory microRNAs in neonatal piglets[J].Asian-Australasian Journal of Animal Sciences,2014,27(12):1695-1704.  
[28] WEAVER A C,KELLY J M,KIND K L,et al.Oocyte maturation and embryo survival in nulliparous female pigs (gilts) is improved by feeding a lupin-based high-fibre diet[J].Reproduction,Fertility,and Development,2013,25(8):1216-1223.  
[29] URYU H,TSUKAHARA T,ISHIKAWA H,et al.Comparison of productivity and fecal microbiotas of sows in commercial farms[J].Microorganisms,2020,8(10):1469.
[30] KHAN R,JIANG X H,HAMEED U,et al.Role of lipid metabolism and signaling in mammalian oocyte maturation,quality,and acquisition of competence[J].Frontiers in Cell and Developmental Biology,2021,9:639704.
[31] MCEVOY T G,COULL G D,BROADBENT P J,et al.Fatty acid composition of lipids in immature cattle,pig and sheep oocytes with intact zona pellucida[J].Journal of Reproduction and Fertility,2000,118(1):163-170.  
[32] STURMEY R G,LEESE H J.Energy metabolism in pig oocytes and early embryos[J].Reproduction,2003,126(2):197-204.  
[33] CHEN M X,ZHANG B,CAI S,et al.Metabolic disorder of amino acids,fatty acids and purines reflects the decreases in oocyte quality and potential in sows[J].Journal of Proteomics,2019,200:134-143.
[34] ROSERO D S,BOYD R D,MCCULLEY M,et al.Essential fatty acid supplementation during lactation is required to maximize the subsequent reproductive performance of the modern sow[J].Animal Reproduction Science,2016,168:151-163.
[35] KURLAK L O,STEPHENSON T J.Plausible explanations for effects of long chain polyunsaturated fatty acids (LCPUFA) on neonates[J].Archives of Disease in Childhood:Fetal and Neonatal Edition,1999,80(2):F148-F154.
[36] SMITS R J,LUXFORD B G,MITCHELL M,et al.Sow litter size is increased in the subsequent parity when lactating sows are fed diets containing n-3 fatty acids from fish oil[J].Journal of Animal Science,2011,89(9):2731-2738.  
[37] MATEO R D,CARROLL J A,HYUN Y,et al.Effect of dietary supplementation of n-3 fatty acids and elevated concentrations of dietary protein on the performance of sows[J].Journal of Animal Science,2009,87(3):948-959.  
[38] SMIT M N,PATTERSON J L,WEBEL S K,et al.Responses to n-3 fatty acid (LCPUFA) supplementation of gestating gilts,and lactating and weaned sows[J].Animal,2013,7(5):784-792.  
[39] ROSSI R,PASTORELLI G,CANNATA S,et al.Recent advances in the use of fatty acids as supplements in pig diets:a review[J].Animal Feed Science and Technology,2010,162(1/2):1-11.
[40] OTTE M V,MOREIRA F,BIANCHI I,et al.Effects of supplying omega-3 polyunsaturated fatty acids to gilts after weaning on metabolism and ovarian gene expression[J].Journal of Animal Science,2019,97(1):374-384.  
[41] BARBE A,BONGRANI A,MELLOUK N,et al.Mechanisms of adiponectin action in fertility:an overview from gametogenesis to gestation in humans and animal models in normal and pathological conditions[J].International Journal of Molecular Sciences,2019,20(7):1526.
[42] MOREIRA F,CHEUICHE Z M G,RIZZOTO G,et al.Metabolic and reproductive parameters in prepubertal gilts after omega-3 supplementation in the diet[J].Animal Reproduction Science,2016,170:178-183.
[43] TIAN M,CHEN J M,LIU J X,et al.Dietary fiber and microbiota interaction regulates sow metabolism and reproductive performance[J].Animal Nutrition,2020,6(4):397-403.  
[44] COSTERMANS N G J,SOEDE N M,VAN TRICHT F,et al.Follicular fluid steroid profile in sows:relationship to follicle size and oocyte quality[J].Biology of Reproduction,2020,102(3):740-749.  
[45] KORDOWITZKI P,KRAJNIK K,SKOWRONSKA A,et al.Pleiotropic effects of IGF1 on the oocyte[J].Cells,2022,11(10):1610.
[46] ODLE A K,AKHTER N,SYED M M,et al.Leptin regulation of gonadotrope gonadotropin-releasing hormone receptors as a metabolic checkpoint and gateway to reproductive competence[J].Frontiers in Endocrinology,2018,8:367.
[47] WOLFE A,DIVALL S,WU S.The regulation of reproductive neuroendocrine function by insulin and insulin-like growth factor-1(IGF-1)[J].Frontiers in Neuroendocrinology,2014,35(4):558-572.  
[48] LIU J,KOENIGSFELD A T,CANTLEY T C,et al.Growth and the initiation of steroidogenesis in porcine follicles are associated with unique patterns of gene expression for individual components of the ovarian insulin-like growth factor system[J].Biology of Reproduction,2000,63(3):942-952.  
[49] RUIZ-CORTÉS Z T,MARTEL-KENNES Y,GÉVRY N Y,et al.Biphasic effects of leptin in porcine granulosa cells[J].Biology of Reproduction,2003,68(3):789-796.  
[50] BJERRE-HARPØTH V, FRIGGENS NC, THORUP V M,et al. Metabolic and production profiles of dairy cows in response to decreased nutrient density to increase physiological imbalance at different stages of lactation[J].Journal of Dairy Science,2012,95(5):2362-2380.  
[51] WALLACE M,COTTELL E,GIBNEY M J,et al.An investigation into the relationship between the metabolic profile of follicular fluid,oocyte developmental potential,and implantation outcome[J].Fertility and Sterility,2012,97(5):1078-1084.e8.  
[52] O'GORMAN A,WALLACE M,COTTELL E,et al.Metabolic profiling of human follicular fluid identifies potential biomarkers of oocyte developmental competence[J].Reproduction,2013,146(4):389-395.  
[53] 徐保阳.肠道菌群干预对母猪卵巢和子宫发育的作用及其机制[D].博士学位论文.武汉:华中农业大学,2021. XU B Y.Effect and mechanism of gut microbiota intervention on the development of sow's ovary and uterus[D].Ph.D.Thesis.Wuhan:Huazhong Agricultural University,2021.(in Chinese)
[54] XU B Y,QIN W X,YAN Y Q,et al.Gut microbiota contributes to the development of endometrial glands in gilts during the ovary-dependent period[J].Journal of Animal Science and Biotechnology,2021,12(1):57.
[55] KWA M,PLOTTEL C S,BLASER M J,et al.The intestinal microbiome and estrogen receptor-positive female breast cancer[J].Journal of the National Cancer Institute,2016,108(8):djw029.
[56] HUNTER M G.Comparison of ovarian function and embryo development in Meishan and large white hybrid pigs[J].Reproduction in Domestic Animals,1994,29(4):343-345.  
[57] LEEMING E R,LOUCA P,GIBSON R,et al.The complexities of the diet-microbiome relationship:advances and perspectives[J].Genome Medicine,2021,13(1):10.
[58] ZHOU H,YU B,CHEN H,et al.Carbohydrates effects on nutrition and health functions in pigs[J].Animal Science Journal,2021,92(1):e13557.
[59] VAN DER HEE B,WELLS J M.Microbial regulation of host physiology by short-chain fatty acids[J].Trends in Microbiology,2021,29(8):700-712.  
[60] YE Q H,ZENG X F,WANG S,et al.Butyrate drives the acetylation of histone H3K9 to activate steroidogenesis through PPARγ and PGC1α pathways in ovarian granulosa cells[J].The FASEB Journal,2021,35(2):e21316.
[61] LU N S,LI M J,LEI H L,et al.Butyric acid regulates progesterone and estradiol secretion via cAMP signaling pathway in porcine granulosa cells[J].The Journal of Steroid Biochemistry and Molecular Biology,2017,172:89-97.
[62] KOH A,DE VADDER F,KOVATCHEVA-DATCHARY P,et al.From dietary fiber to host physiology:short-chain fatty acids as key bacterial metabolites[J].Cell,2016,165(6):1332-1345.  
[63] YAN J,HERZOG J W,TSANG K,et al.Gut microbiota induce IGF-1 and promote bone formation and growth[J].Proceedings of the National Academy of Sciences of the United States of America,2016,113(47):E7554-E7563.
[64] SPICER L J,ALPIZAR E,ECHTERNKAMP S E.Effects of insulin,insulin-like growth factor Ⅰ,and gonadotropins on bovine granulosa cell proliferation,progesterone production,estradiol production,and (or) insulin-like growth factor Ⅰ production in vitro[J].Journal of Animal Science,1993,71(5):1232-1241.  
[65] MAZERBOURG S,BONDY C A,ZHOU J,et al.The insulin-like growth factor system:a key determinant role in the growth and selection of ovarian follicles?A comparative species study[J].Reproduction in Domestic Animals,2003,38(4):247-258.  
[66] ZAIBI MS, STOCKER CJ, O'DOWD J,et al.Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids[J]. FEBS letters,2010,584(11):2381-2386.  
[67] XIONG Y M,MIYAMOTO N,SHIBATA K,et al.Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41[J].Proceedings of the National Academy of Sciences of the United States of America,2004,101(4):1045-1050.  
[68] CATTEAU A,CAILLON H,BARRIōRE P,et al.Leptin and its potential interest in assisted reproduction cycles[J].Human Reproduction Update,2016,22(3):320-341.  
[69] KITAWAKI J,KUSUKI I,KOSHIBA H,et al.Leptin directly stimulates aromatase activity in human luteinized granulosa cells[J].Molecular Human Reproduction,1999,5(8):708-713.  
[70] HUNTER M G,BIGGS C,FAILLACE L S.Endocrine and follicular studies in Meishan pigs[J].Journal of Reproduction and Fertility,1993,48:261-270.
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