Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0010
Animal Reproduction (AR)
ORIGINAL ARTICLE

Trans 10, cis 12-conjugated linoleic acid reduced reproductive ability by disrupting the estrus cycle in female mice

Shuai Yu; Baozhu Wang; Yu Rao; Mei Liu; Luwen Liang; Kemian Gou

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Abstract

As a positional and geometrical isomer of linoleic acid, trans 10, cis 12 conjugated linoleic acid (t10c12-CLA) reduces white fat by reducing food intake, modulating lipid metabolism, and stimulating energy expenditure. However, the t10c12-CLA products are mostly mixtures, making it difficult to obtain accurate results. Studies are needed to investigate the effects of pure t10c12-CLA on animals and humans. In this study, we used the biallelic transgenic (tg) mice, which could produce t10c12-CLA itself, to investigate the effects of pure t10c12-CLA on female reproductive ability. The results showed that the body and relative ovary weights had no significant difference between tg and wild-type (wt) littermates at ages 3 or 10 weeks. While the fecundity test found that tg mice had a significantly longer first litter time (32.0 ± 4.70 days vs. 21.3 ± 2.31 days, P<0.05), and a significantly lower number of litters (4.75 ± 2.75 vs. 6.67 ± 0.57, P<0.05) when compared with wt mice during continuous mating within seven months. Hormone profiles showed that serum estradiol levels did not change in tg mice; however, significantly (P<0.05) decreased progesterone and increased prostaglandin E2 levels were observed in tg mice compared with those of wt mice. Hematoxylin-eosin staining showed no pathological characteristics in tg ovaries, except for the increased atresia follicles (P<0.05). Moreover, the tg mice had a significantly more extended diestrus period than the wt mice (48.4 ± 6.38% vs. 39.6 ± 3.81%, P<0.05). In summary, t10c12-CLA could affect serum progesterone and prostaglandin E2 levels, lead to a disordered estrus cycle, and impact the reproductive performance of female mice. This study provided theoretical and biosafety recommendations for applying t10c12-CLA in female mammals.

Keywords

trans 10, cis 12-conjugated linoleic acid (t10c12-CLA), estrous cycle, fertility, progesterone

References

Badawy S, Liu Y, Guo M, Liu Z, Xie C, Marawan MA, Ares I, Lopez-Torres B, Martínez M, Maximiliano JE, Martínez-Larrañaga MR, Wang X, Anadón A, Martínez MA. Conjugated linoleic acid (CLA) as a functional food: is it beneficial or not? Food Res Int. 2023;172:113158. http://doi.org/10.1016/j.foodres.2023.113158. PMid:37689911.

Bui AH, Timmons DB, Young SL. Evaluation of endometrial receptivity and implantation failure. Curr Opin Obstet Gynecol. 2022;34(3):107-13. http://doi.org/10.1097/GCO.0000000000000783. PMid:35645008.

Cora MC, Kooistra L, Travlos G. Vaginal cytology of the laboratory rat and mouse: review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol Pathol. 2015;43(6):776-93. http://doi.org/10.1177/0192623315570339. PMid:25739587.

Csillik Z, Faigl V, Keresztes M, Galamb E, Hammon HM, Tröscher A, Fébel H, Kulcsár M, Husvéth F, Huszenicza G, Butler WR. Effect of pre- and postpartum supplementation with lipid-encapsulated conjugated linoleic acid on reproductive performance and the growth hormone-insulin-like growth factor-I axis in multiparous high-producing dairy cows. J Dairy Sci. 2017;100(7):5888-98. http://doi.org/10.3168/jds.2016-12124. PMid:28456404.

den Hartigh LJ. Conjugated linoleic acid effects on cancer, obesity, and atherosclerosis: a review of pre-clinical and human trials with current perspectives. Nutrients. 2019;11(2):370. http://doi.org/10.3390/nu11020370. PMid:30754681.

Fontana R, Della Torre S. The deep correlation between energy metabolism and reproduction: a view on the effects of nutrition for women fertility. Nutrients. 2016;8(2):87. http://doi.org/10.3390/nu8020087. PMid:26875986.

Fox EM, Andrade J, Shupnik MA. Novel actions of estrogen to promote proliferation: integration of cytoplasmic and nuclear pathways. Steroids. 2009;74(7):622-7. http://doi.org/10.1016/j.steroids.2008.10.014. PMid:18996136.

Fransolet M, Henry L, Labied S, Masereel MC, Blacher S, Noël A, Foidart JM, Nisolle M, Munaut C. Influence of mouse strain on ovarian tissue recovery after engraftment with angiogenic factor. J Ovarian Res. 2015;8(1):14. http://doi.org/10.1186/s13048-015-0142-6. PMid:25824856.

Freitas DS, Lopes GAG, Nascimento BR, Madureira AP, Campos-Junior PHA. Cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid gastric administration during the pregestational and gestational periods does not influence the follicular endowment of the progeny. Anim Reprod. 2023;20(3):e20220124. http://doi.org/10.1590/1984-3143-ar2022-0124. PMid:37795199.

Freitas DS, Lopes GAG, Nascimento BR, Magalhães BA, Madureira AP, Campos-Junior PHA. Effects of cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid supplementation on maternal reproductive parameters. Zygote. 2022;30(6):863-71. http://doi.org/10.1017/S0967199422000405. PMid:36148787.

Hashimoto M, Makino N, Inazumi T, Yoshida R, Sugimoto T, Tsuchiya S, Sugimoto Y. Effects of an ω3 fatty acid-biased diet on luteolysis, parturition, and uterine prostanoid synthesis in pregnant mice. Biochem Biophys Res Commun. 2022;589:139-46. http://doi.org/10.1016/j.bbrc.2021.12.029. PMid:34920379.

Innocenti F, Cerquetti L, Pezzilli S, Bucci B, Toscano V, Canipari R, Stigliano A. Effect of mitotane on mouse ovarian follicle development and fertility. J Endocrinol. 2017;234(1):29-39. http://doi.org/10.1530/JOE-17-0203. PMid:28450646.

Jazwiec PA, Sloboda DM. Nutritional adversity, sex and reproduction: 30 years of DOHaD and what have we learned? J Endocrinol. 2019;242(1):T51-68. http://doi.org/10.1530/JOE-19-0048. PMid:31013473.

Kim HJJ, Zagzoog A, Black T, Baccetto SL, Laprairie RB. Molecular and cellular mechanisms underlying brain region-specific endocannabinoid system modulation by estradiol across the rodent estrus cycle. Prog Mol Biol Transl Sci. 2023;195:27-45. http://doi.org/10.1016/bs.pmbts.2022.06.010. PMid:36707154.

Kim SO, Duffy DM. Mapping PTGERs to the ovulatory follicle: regional responses to the ovulatory PGE2 signal. Biol Reprod. 2016;95(2):33. http://doi.org/10.1095/biolreprod.116.140574. PMid:27307073.

Knott B, Kocher MA, Paz HA, Hamm SE, Fink W, Mason J, Grange RW, Wankhade UD, Good DJ. Dietary conjugated linoleic acid reduces body weight and fat in Snord116m+/p- and Snord116m-/p- mouse models of Prader-Willi Syndrome. Nutrients. 2022;14(4):860. http://doi.org/10.3390/nu14040860. PMid:35215509.

Li SL, Ma SY, Xu BR, Fan ZY, Li MJ, Cao WG, Gou KM. Effects of trans-10, cis-12-conjugated linoleic acid on mice are influenced by the dietary fat content and the degree of murine obesity. Eur J Lipid Sci Technol. 2015;117(12):1908-18. http://doi.org/10.1002/ejlt.201400568.

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods. 2001;25(4):402-8. http://doi.org/10.1006/meth.2001.1262. PMid:11846609.

Lundberg PS, Moskowitz GJ, Bellacose C, Demirel E, Trau HA, Duffy DM. Granulosa cell proliferation is inhibited by PGE2 in the primate ovulatory follicle. Anim Cells Syst. 2020;24(3):125-35. http://doi.org/10.1080/19768354.2020.1764385. PMid:33209192.

Luo C, Zuñiga J, Edison E, Palla S, Dong W, Parker-Thornburg J. Superovulation strategies for 6 commonly used mouse strains. J Am Assoc Lab Anim Sci. 2011;50(4):471-8. PMid:21838974.

Lyu L, Wen H, Li Y, Wang X, Li J, Zuo C, Yan S, Qi X. PGE2 functions in ovoviviparous teleost black rockfish (Sebastes schlegelii): evolutionary status between parturition and ovulation†. Biol Reprod. 2024;110(1):140-53. http://doi.org/10.1093/biolre/ioad135. PMid:37812450.

McLean AC, Valenzuela N, Fai S, Bennett SA. Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification. J Vis Exp. 2012;(67):e4389. http://doi.org/10.3791/4389. PMid:23007862.

Nicolakis D, Marconi MA, Zala SM, Penn DJ. Ultrasonic vocalizations in house mice depend upon genetic relatedness of mating partners and correlate with subsequent reproductive success. Front Zool. 2020;17(1):10. http://doi.org/10.1186/s12983-020-00353-1. PMid:32265997.

Ramakrishnan U, Grant F, Goldenberg T, Zongrone A, Martorell R. Effect of women’s nutrition before and during early pregnancy on maternal and infant outcomes: a systematic review. Paediatr Perinat Epidemiol. 2012;26(Suppl 1):285-301. http://doi.org/10.1111/j.1365-3016.2012.01281.x. PMid:22742616.

Rao Y, Li SL, Li MJ, Wang BZ, Wang YY, Liang LW, Yu S, Liu ZP, Cui S, Gou KM. Transgenic mice producing the trans 10, cis 12-conjugated linoleic acid present reduced adiposity and increased thermogenesis and fibroblast growth factor 21 (FGF21). J Nutr Biochem. 2023a;120:109419. http://doi.org/10.1016/j.jnutbio.2023.109419. PMid:37487823.

Rao Y, Liang LW, Li MJ, Wang YY, Wang BZ, Gou KM. Lean female mice producing trans 10, cis 12-conjugated linoleic acid present excessive fibroblast growth factor 21, adrenaline, prostaglandin E2, corticosterone, and glucagon. bioRxiv, 2023b. In press. http://doi.org/10.1101/2023.04.21.536206.

Saben JL, Asghar Z, Rhee JS, Drury A, Scheaffer S, Moley KH. Excess maternal fructose consumption increases fetal loss and impairs endometrial decidualization in mice. Endocrinology. 2016;157(2):956-68. http://doi.org/10.1210/en.2015-1618. PMid:26677880.

Safari Hasanabad M, Ghorbanlou M, Masoumi R, Shokri S, Rostami B, Mirzaei-Alamouti H, Catt S, Green MP, Nejatbakhsh R. Effects of dietary supplementation of different oils and conjugated linoleic acid on the reproductive and metabolic aspects of male mice. Andrologia. 2022;54(11):e14598. http://doi.org/10.1111/and.14598. PMid:36161725.

Taraborrelli S. Physiology, production and action of progesterone. Acta Obstet Gynecol Scand. 2015;94(S161, Suppl 161):8-16. http://doi.org/10.1111/aogs.12771. PMid:26358238.

Wang C, Wang YY, Rao Y, Li MJ, Liu ZP, Li SL, Gou KM. Heterologous expression of Propionibacterium acnes isomerase in mouse (Mus musculus) cells and production of t10c12-conjugated linoleic acid. Chin J Agric Biotechnol. 2021;29:2304-11. http://doi.org/10.3969/j.issn.1674-7968.2021.12.004.

Zamberlam G, Lapointe E, Abedini A, Rico C, Godin P, Paquet M, DeMayo FJ, Boerboom D. SFRP4 Is a negative regulator of ovarian follicle development and female fertility. Endocrinology. 2019;160(7):1561-72. http://doi.org/10.1210/en.2019-00212. PMid:30942852.

Zhu J, Zhang J, Li H, Wang TY, Zhang CX, Luo MJ, Tan JH. Cumulus cells accelerate oocyte aging by releasing soluble Fas ligand in mice. Sci Rep. 2015;5(1):8683. http://doi.org/10.1038/srep08683. PMid:25731893.
 


Submitted date:
01/30/2024

Accepted date:
03/18/2024

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