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Influence of leptin administration to pregnant female mice on obesity development, taste preferences, and gene expression in the liver and muscles of their male and female offspring

https://doi.org/10.18699/VJ21.076

Abstract

The consumption of food rich in sugar and fat provokes obesity. Prenatal conditions have an impact on taste preferences and metabolism in the adult offspring, and this impact may manifest differently in different sexes. An increase in blood leptin level in pregnant females reduces the risk of obesity and insulin resistance in the offspring, although the mechanisms mediating this effect are unknown. Neither is it known whether maternal leptin affects taste preferences. In this study, we investigated the effect of leptin administration to pregnant mice on the development of diet-induced obesity, food choice, and gene expression in the liver and muscles of the offspring with regard to sex. Leptin was administered to female mice on days 11, 12, and 13 of pregnancy. In male and female offspring, growth rate and intake of standard chow after weaning, obesity development, gene expression in the liver and muscles, and food choice when kept on a high-calorie diet (standard chow, lard, sweet cookies) were recorded. Leptin administration to pregnant females reduced body weight in the female offspring fed on the standard diet. When the offspring were given a high-calorie diet, leptin administration inhibited obesity development and reduced the consumption of cookies only in males. It also increased the consumption of standard chow and the mRNA levels of genes for the insulin receptor and glucose transporter type 4 in the muscles of both male and female offspring. The results demonstrate that an increase in blood leptin levels in pregnant females has a sex-specific effect on the metabolism of the offspring increasing resistance to obesity only in male offspring. The mechanism underlying this effect includes a shift in food preference in favor of a balanced diet and maintenance of insulin sensitivity in muscle tissues.

About the Authors

E. I. Denisova
Institute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences
Russian Federation

Novosibirsk



M. M. Savinkova
Novosibirsk State University
Russian Federation

Novosibirsk



E. N. Makarova
Institute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences
Russian Federation

Novosibirsk



References

1. Astrup A., Dyerberg J., Selleck M., Stender S. Nutrition transition and its relationship to the development of obesity and related chronic diseases. Obes. Rev. 2008;9(1):48-52. DOI 10.1111/j.1467-789X.2007.00438.x.

2. Bale T.L. Epigenetic and transgenerational reprogramming of brain development. Nat. Rev. Neurosci. 2015;16(6):332-344. DOI 10.1038/nrn3818.

3. Barker D.J., Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489): 1077-1081. DOI 10.1016/s0140-6736(86)91340-1.

4. Bazhan N., Jakovleva T., Balyibina N., Dubinina A., Denisova E., Feofanova N., Makarova E. Sex dimorphism in the Fg f 21 gene expression in liver and adipose tissues is dependent on the metabolic condition. OnLine J. Biol. Sci. 2019;19(1):28-36. DOI 10.3844/ojbsci.2019.28.36.

5. Buczek L., Migliaccio J., Petrovich G.D. Hedonic eating: sex differences and characterization of orexin activation and signaling. Neuroscience. 2020;436:34-45. DOI 10.1016/j.neuroscience.2020.04.008.

6. Chmurzynska A., Mlodzik M.A. Genetics of fat intake in the determination of body mass. Nutr. Res. Rev. 2017;30(1):106-117. DOI 10.1017/S0954422417000014.

7. Denisova E.I., Kozhevnikova V.V., Bazhan N.M., Makarova E.N. Sexspecific effects of leptin administration to pregnant mice on the placentae and the metabolic phenotypes of offspring. FEBS Open Bio. 2020;10(1):96-106. DOI 10.1002/2211-5463.12757.

8. Denisova E., Makarova E. Sex-specific effect of leptin on gene expression in placentas and fetal tissues in mice. In: Bioinformatics of Genome Regulation and StructureSystems Biology (BGRS SB-2018) The Eleventh International Conference (20–25 Aug. 2018, Novosibirsk, Russia); Abstracts/Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences; Novosibirsk State University. Novosibirsk: ICG SB RAS, 2018. DOI 10.18699/BGRSSB-2018-174.

9. Diószegi J., Llanaj E., Ádány R. Genetic background of taste perception, taste preferences, and its nutritional implications: a systematic review. Front. Genet. 2019;10:1272. DOI 10.3389/fgene.2019.01272.

10. Duffy V.B., Hayes J.E., Sullivan B.S., Faghri P. Surveying food and beverage liking: a tool for epidemiological studies to connect chemosensation with health outcomes. Ann. NY Acad. Sci. 2009;1170: 558-568. DOI 10.1111/j.1749-6632.2009.04593.x.

11. Enriori P.J., Evans A.E., Sinnayah P., Jobst E.E., Tonelli-Lemos L., Billes S.K., Glavas M.M., Grayson B.E., Perello M., Nillni E.A., Grove K.L., Cowley M.A. Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell Metab. 2007;5(3):181-194. DOI 10.1016/j.cmet.2007.02.004.

12. Gabory A., Roseboom T.J., Moore T., Moore L.G., Junien C. Placental contribution to the origins of sexual dimorphism in health and diseases: sex chromosomes and epigenetics. Biol. Sex Differ. 2013; 4(1):5. DOI 10.1186/2042-6410-4-5.

13. Grissom N.M., Lyde R., Christ L., Sasson I.E., Carlin J., Vitins A.P., Simmons R.A., Reyes T.M. Obesity at conception programs the opioid system in the offspring brain. Neuropsychopharmacology. 2014;39(4):801-810. DOI 10.1038/npp.2013.193.

14. Hacker A., Capel B., Goodfellow P., Lovell-Badge R. Expression of Sry, the mouse sex determining gene. Development. 1995;121(6): 1603-1614.

15. Ishii Y., Bouret S.G. Embryonic birthdate of hypothalamic leptin-activated neurons in mice. Endocrinology. 2012;153(8):3657-3667. DOI 10.1210/en.2012-1328.

16. Laker R.C., Lillard T.S., Okutsu M., Zhang M., Hoehn K.L., Connelly J.J., Yan Z. Exercise prevents maternal high-fat diet-induced hypermethylation of the Pgc-1α gene and age-dependent metabolic dysfunction in the offspring. Diabetes. 2014;63(5):1605-1611. DOI 10.2337/db13-1614.

17. Larson K.R., Chaffin A.T., Goodson M.L., Fang Y., Ryan K.K. Fibroblast growth factor-21 controls dietary protein intake in male mice. Endocrinology. 2019;160(5):1069-1080. DOI 10.1210/en.2018-01056.

18. Makarova E.N., Chepeleva E.V., Panchenko P.E., Bazhan N.M. Influence of abnormally high leptin levels during pregnancy on metabolic phenotypes in progeny mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013;305(11):R1268-R1280. DOI 10.1152/ajpregu.00162.2013.

19. Makarova E.N., Yakovleva T.V., Shevchenko A.Y., Bazhan N.M. Pregnancy and lactation have anti-obesity and anti-diabetic effects in A(y)/a mice. Acta Physiol. (Oxf. ). 2010;198(2):169-177. DOI 10.1111/j.1748-1716.2009.02046.x.

20. May C.E., Dus M. Confection confusion: interplay between diet, taste, and nutrition. Trends Endocrinol. Metab. 2021;32(2):95-105. DOI 10.1016/j.tem.2020.11.011.

21. Mezei G.C., Ural S.H., Hajnal A. Differential effects of maternal high fat diet during pregnancy and lactation on taste preferences in rats. Nutrients. 2020;12(11):3553. DOI 10.3390/nu12113553.

22. Ong Z.Y., Gugusheff J.R., Muhlhausler B.S. Perinatal overnutrition and the programming of food preferences: pathways and mechanisms. J. Dev. Orig. Health Dis. 2012;3(5):299-308. DOI 10.1017/S204017441200030X.

23. Pennington K.A., Harper J.L., Sigafoos A.N., Beffa L.M., Carleton S.M., Phillips C.L., Schulz L.C. Effect of food restriction and leptin supplementation on fetal programming in mice. Endocrinology. 2012;153(9):4556-4567. DOI 10.1210/en.2012-1119.

24. Pollock K.E., Stevens D., Pennington K.A., Thaisrivongs R., Kaiser J., Ellersieck M.R., Miller D.K., Schulz L.C. Hyperleptinemia during pregnancy decreases adult weight of offspring and is associated with increased offspring locomotor activity in mice. Endocrinology. 2015;156(10):3777-3790. DOI 10.1210/en.2015-1247.

25. Sinclair E.B., Hildebrandt B.A., Culbert K.M., Klump K.L., Sisk C.L. Preliminary evidence of sex differences in behavioral and neural responses to palatable food reward in rats. Physiol. Behav. 2017;176: 165-173. DOI 10.1016/j.physbeh.2017.03.042.

26. Spinelli S., Monteleone E. Food preferences and obesity. Endocrinol. Metab. (Seoul ). 2021;36(2):209-219. DOI 10.3803/EnM.2021.105.

27. Stocker C.J., Wargent E., O’Dowd J., Cornick C., Speakman J.R., Arch J.R., Cawthorne M.A. Prevention of diet-induced obesity and impaired glucose tolerance in rats following administration of leptin to their mothers. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007; 292(5):1810-1818. DOI 10.1152/ajpregu.00676.2006.

28. Talton O.O., Pennington K.A., Pollock K.E., Batesa K., Mad L., Ellersieck M.R., Schulz L.C. Maternal hyperleptinemia improves offspring insulin sensitivity in mice. Endocrinology. 2016;157(7): 2636-2648. DOI 10.1210/en.2016-1039.

29. Talukdar S., Owen B.M., Song P., Hernandez G., Zhang Y., Zhou Y., Scott W.T., Paratala B., Turner T., Smith A., Bernardo B., Müller C.P., Tang H., Mangelsdorf D.J., Goodwin B., Kliewer S.A. FGF21 Regulates sweet and alcohol preference. Cell Metab. 2016;23(2):344-349. DOI 10.1016/j.cmet.2015.12.008.

30. Valenstein E.S., Cox V.C., Kakolewski J.W. Further studies of sex differences in taste preferences with sweet solutions. Psychol. Rep. 1967;20(3):1231-1234. DOI 10.2466/pr0.1967.20.3c.1231.

31. Yamashita H., Shao J., Ishizuka T., Klepcyk P.J., Muhlenkamp P., Qiao L., Hoggard N., Friedman J.E. Leptin administration prevents spontaneous gestational diabetes in heterozygous Lepr(db/+) mice: effects on placental leptin and fetal growth. Endocrinology. 2001; 142(7):2888-2897. DOI 10.1210/endo.142.7.8227.

32. Zucker I., Wade G.N., Ziegler R. Sexual and hormonal influences on eating, taste preferences, and body weight of hamsters. Physiol. Behav. 1972;8(1):101-111. DOI 10.1016/0031-9384(72)90135-7


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