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Parental high-fat high-sugar diet programming and hypothalamus adipose tissue axis in male Wistar rats

A Correction to this article was published on 08 November 2021

This article has been updated

Abstract

Purpose

Maternal nutrition during early development and paternal nutrition pre-conception can programme offspring health status. Hypothalamus adipose axis is a target of developmental programming, and paternal and maternal high-fat, high-sugar diet (HFS) may be an important factor that predisposes offspring to develop obesity later in life. This study aims to investigate Wistar rats’ maternal and paternal HFS differential contribution on the development, adiposity, and hypothalamic inflammation in male offspring from weaning until adulthood.

Methods

Male progenitors were fed a control diet (CD) or HFS for 10 weeks before mating. After mating, dams were fed CD or HFS only during pregnancy and lactation. Forming the following male offspring groups: CD—maternal and paternal CD; MH—maternal HFS and paternal CD; PH—maternal CD and paternal HFS; PMH—maternal and paternal HFS. After weaning, male offspring were fed CD until adulthood.

Results

Maternal HFS diet increased weight, visceral adiposity, and serum total cholesterol levels, and decreased hypothalamic weight in weanling male rats. In adult male offspring, maternal HFS increased weight, glucose levels, and hypothalamic NFκBp65. Paternal HFS diet lowered hypothalamic insulin receptor levels in weanling offspring and glucose and insulin levels in adult offspring. The combined effects of maternal and paternal HFS diets increased triacylglycerol, leptin levels, and hypothalamic inflammation in weanling rats, and increased visceral adiposity in adulthood.

Conclusion

Male offspring intake of CD diet after weaning reversed part of the effects of parental HFS diet during the perinatal period. However, maternal and paternal HFS diet affected adiposity and hypothalamic inflammation, which remained until adulthood.

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Change history

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Funding

This study was supported by Fundação do Amparo à Pesquisa do Estado de São Paulo (FAPESP)—no. 2017/09646–1; 2019/09724–8, and financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. LPP is recipient of National Council for Scientific and Technological Development (CNPq) fellowship and supported by FAPESP—no. 2019/09724–8.

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Authors

Contributions

HC contributed with the animal care, experimental procedures, statistical analysis and writing. MNS, EAS, GJ, AS and AJ contributed to the animal care and experimental procedures. BC contributed with the statistical analysis. LPP contributed with the drafting and revising critical intellectual content. All authors have approved the final article.

Corresponding author

Correspondence to Luciana Pellegrini Pisani.

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The authors declare no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

394_2021_2690_MOESM1_ESM.tif

Supplementary file1 (TIF 571 kb) Paternal differences in body measurements, metabolic efficiency and adiposity between control diet (CD) and high-fat high-sugar (HFS) groups. A. Paternal body weight progress (g); B. Paternal weight gain (g) (Final weight – Initial weight); C. Paternal diet intake (g/week); D. Paternal metabolic efficiency weight gain (g)/ diet intake (g); E. Paternal Retroperitoneal Adipose Tissue (RET) relative weight (%); F. Paternal Total Visceral Adipose Tissue (VAT) relative weight (%); Data are expressed as mean ± SEM and *p≤0.05 was considered statistically significant compared to CD. Statistical test: ANOVA for repeated measures was used for A; U-Mann Whitney test (non-parametric data) was used for B and C, and unpaired T-test (parametric data) for D, E and F

394_2021_2690_MOESM2_ESM.tif

Supplementary file2 (TIF 604 kb) Maternal differences in body measurements, metabolic efficiency and adiposity between control diet (CD) and high-fat high-sugar (HFS) groups. A. Maternal body weight progress (g) during pregnancy and lactation; B. Maternal Weight gain (g) (Final weight – Initial weight) during pregnancy and lactation; C. Maternal diet intake (g) during pregnancy and lactation; D. Maternal metabolic efficiency (weight gain (g)/ diet intake (g) during pregnancy and lactation; E. Maternal Retroperitoneal Adipose Tissue (RET) relative weight (%); F. Maternal Total Visceral Adipose Tissue (VAT) relative weight (%); Data are expressed as mean ± SEM and *p≤0.05 was considered statistically significant compared to CD. Statistical test: ANOVA for repeated measures was used for A; U-Mann Whitney test (non-parametric data) was used for E and F, and unpaired T-test (parametric data) for B, C and D.

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César, H., Sertorio, M.N., de Souza, E.A. et al. Parental high-fat high-sugar diet programming and hypothalamus adipose tissue axis in male Wistar rats. Eur J Nutr 61, 523–537 (2022). https://doi.org/10.1007/s00394-021-02690-1

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Keywords

  • Developmental programming
  • Hypothalamic inflammation
  • Adiposity
  • High-fat high-sugar diet
  • Low-grade inflammation
  • Paternal diet