Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Animal Models

Cafeteria diet overfeeding in young male rats impairs the adaptive response to fed/fasted conditions and increases adiposity independent of body weight

International Journal of Obesity volume 39, pages 430–437 (2015)Cite this article

Subjects

Abstract

Objective:

We analyzed the effects of a short exposure to a cafeteria diet during early infancy in rats on their metabolic response to fed/fasting conditions in key tissues involved in energy homeostasis.

Methods:

Ten-day-old male pups were fed a control or a cafeteria diet for 12 days and then killed under ad libitum feeding conditions or 12 h fasting. The expression of key genes related to energy metabolism in liver, retroperitoneal white adipose tissue (WAT) and hypothalamus were analyzed.

Results:

Despite no differences in body weight, cafeteria-fed animals had almost double the fat mass of control rats. They also showed higher food intake, higher leptinemia and altered hypothalamic expression of Neuropetide Y, suggesting a dysfunction in the control of food intake. Unlike controls, cafeteria-fed animals did not decrease WAT expression of Pparg, sterol regulatory element binding transcription factor 1 or Cidea under fasting conditions, and displayed lower Pnpla2 expression than controls. In liver, compared with controls, cafeteria animals presented: (i) lower expression of genes related with fatty acid uptake and lipogenesis under ad libitum-fed conditions; (ii) higher expression of fatty acid oxidation-related genes and glucokinase under fasting conditions; (iii) greater expression of leptin and insulin receptors; and higher protein levels of insulin receptor and the pAMPK/AMPK ratio.

Conclusion:

A short period of exposure to a cafeteria diet in early infancy in rat pups is enough to disturb the metabolic response to fed/fasting conditions in key tissues involved in energy homeostasis, particularly in WAT, and hence induces an exacerbated body fat accumulation and increased metabolic risk, with no apparent effects on body weight.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Ahrens W, Bammann K, de Henauw S, Halford J, Palou A, Pigeot I et al. Understanding and preventing childhood obesity and related disorders—IDEFICS: a European multilevel epidemiological approach. Nutr Metab Cardiovasc Dis 2006; 16: 302–308.

    Article  CAS  PubMed  Google Scholar 

  2. Lobstein T, Baur L, Uauy R . Obesity in children and young people: a crisis in public health. Obes Rev 2004; 5: 4–104.

    PubMed  Google Scholar 

  3. Hebestreit A, Bornhorst C, Barba G, Siani A, Huybrechts I, Tognon G et al. Associations between energy intake, daily food intake and energy density of foods and BMI z-score in 2-9-year-old European children. Eur J Nutr 2014; 53: 673–681.

    Article  CAS  PubMed  Google Scholar 

  4. Kral TV, Rolls BJ . Energy density and portion size: their independent and combined effects on energy intake. Physiol Behav 2004; 82: 131–138.

    Article  CAS  PubMed  Google Scholar 

  5. McConahy KL, Smiciklas-Wright H, Mitchell DC, Picciano MF . Portion size of common foods predicts energy intake among preschool-aged children. J Am Diet Assoc 2004; 104: 975–979.

    Article  PubMed  Google Scholar 

  6. Oliver P, Reynes B, Caimari A, Palou A . Peripheral blood mononuclear cells: a potential source of homeostatic imbalance markers associated with obesity development. Pflugers Arch 2013; 465: 459–468.

    Article  CAS  PubMed  Google Scholar 

  7. Pico C, Pons A, Gianotti M, Palou A . Sustained changes in blood alpha amino nitrogen compartmentation during recovery from cafeteria feeding in rats. Arch Int Physiol Biochim Biophys 1991; 99: 345–348.

    CAS  PubMed  Google Scholar 

  8. Akyol A, McMullen S, Langley-Evans SC . Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr 2012; 107: 964–978.

    Article  CAS  PubMed  Google Scholar 

  9. Llado I, Proenza AM, Serra F, Palou A, Pons A . Dietary-induced permanent changes in brown and white adipose tissue composition in rats. Int J Obes 1991; 15: 415–419.

    CAS  PubMed  Google Scholar 

  10. Matamala JC, Gianotti M, Pericas J, Quevedo S, Roca P, Palou A et al. Changes induced by fasting and dietetic obesity in thermogenic parameters of rat brown adipose tissue mitochondrial subpopulations. Biochem J 1996; 319: 529–534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Proenza AM, Llado I, Serra F, Pico C, Pons A, Palou A . Tissue composition in persistent dietary obesity after early and adulthood overfeeding in the rat. Arch Int Physiol Biochim Biophys 1992; 100: 147–154.

    CAS  PubMed  Google Scholar 

  12. Levin BE, Sullivan AC . Regulation of thermogenesis in obesity. Int J Obes 1984; 8: 159–180.

    CAS  PubMed  Google Scholar 

  13. Xiao XQ, Williams SM, Grayson BE, Glavas MM, Cowley MA, Smith MS et al. Excess weight gain during the early postnatal period is associated with permanent reprogramming of brown adipose tissue adaptive thermogenesis. Endocrinology 2007; 148: 4150–4159.

    Article  CAS  PubMed  Google Scholar 

  14. Palou A, Remesar X, Arola L, Herrera E, Alemany M . Metabolic effects of short term food deprivation in the rat. Horm Metab Res 1981; 13: 326–330.

    Article  CAS  PubMed  Google Scholar 

  15. Palou M, Priego T, Sanchez J, Villegas E, Rodriguez AM, Palou A et al. Sequential changes in the expression of genes involved in lipid metabolism in adipose tissue and liver in response to fasting. Pflugers Arch 2008; 456: 825–836.

    Article  CAS  PubMed  Google Scholar 

  16. Sanchez J, Palou A, Pico C . Response to carbohydrate and fat refeeding in the expression of genes involved in nutrient partitioning and metabolism: striking effects on fibroblast growth factor-21 induction. Endocrinology 2009; 150: 5341–5350.

    Article  CAS  PubMed  Google Scholar 

  17. Caimari A, Oliver P, Palou A . Regulation of adiponutrin expression by feeding conditions in rats is altered in the obese state. Obesity 2007; 15: 591–599.

    Article  CAS  PubMed  Google Scholar 

  18. Caimari A, Oliver P, Rodenburg W, Keijer J, Palou A . Feeding conditions control the expression of genes involved in sterol metabolism in peripheral blood mononuclear cells of normoweight and diet-induced (cafeteria) obese rats. J Nutr Biochem 2010; 21: 1127–1133.

    Article  CAS  PubMed  Google Scholar 

  19. Llado I, Pons A, Palou A . Effects of fasting on lipoprotein lipase activity in different depots of white and brown adipose tissues in diet-induced overweight rats. J Nutr Biochem 1999; 10: 609–614.

    Article  CAS  PubMed  Google Scholar 

  20. Pico C, Oliver P, Sanchez J, Miralles O, Caimari A, Priego T et al. The intake of physiological doses of leptin during lactation in rats prevents obesity in later life. Int J Obes (Lond) 2007; 31: 1199–1209.

    Article  CAS  Google Scholar 

  21. Ribot J, Rodriguez AM, Rodriguez E, Palou A . Adiponectin and resistin response in the onset of obesity in male and female rats. Obesity 2008; 16: 723–730.

    Article  CAS  PubMed  Google Scholar 

  22. Gabriely I, Ma XH, Yang XM, Atzmon G, Rajala MW, Berg AH et al. Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process? Diabetes 2002; 51: 2951–2958.

    Article  CAS  PubMed  Google Scholar 

  23. Oliver P, Pico C, De Matteis R, Cinti S, Palou A . Perinatal expression of leptin in rat stomach. Dev Dyn 2002; 223: 148–154.

    Article  CAS  PubMed  Google Scholar 

  24. Brisbois TD, Farmer AP, McCargar LJ . Early markers of adult obesity: a review. Obes Rev 2012; 13: 347–367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bayol SA, Simbi BH, Bertrand JA, Stickland NC . Offspring from mothers fed a 'junk food' diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol 2008; 586: 3219–3230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bayol SA, Simbi BH, Stickland NC . A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 2005; 567: 951–961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bayol SA, Farrington SJ, Stickland NC . A maternal 'junk food' diet in pregnancy and lactation promotes an exacerbated taste for 'junk food' and a greater propensity for obesity in rat offspring. Br J Nutr 2007; 98: 843–851.

    Article  CAS  PubMed  Google Scholar 

  28. Wright TM, Fone KC, Langley-Evans SC, Voigt JP . Exposure to maternal consumption of cafeteria diet during the lactation period programmes feeding behaviour in the rat. Int J Dev Neurosci 2011; 29: 785–793.

    Article  CAS  PubMed  Google Scholar 

  29. Schwartz M, Woods S, Porte DJ, Seeley R, Baskin D . Central nervous system control of food intake. Nature 2000; 404: 661–671.

    Article  CAS  PubMed  Google Scholar 

  30. Morrison CD, Huypens P, Stewart LK, Gettys TW . Implications of crosstalk between leptin and insulin signaling during the development of diet-induced obesity. Biochim Biophys Acta 2009; 1792: 409–416.

    Article  CAS  PubMed  Google Scholar 

  31. Boren J, Taskinen MR, Olofsson SO, Levin M . Ectopic lipid storage and insulin resistance: a harmful relationship. J Intern Med 2013; 274: 25–40.

    Article  CAS  PubMed  Google Scholar 

  32. Zhou Z, Yon Toh S, Chen Z, Guo K, Ng CP, Ponniah S et al. Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat Genet 2003; 35: 49–56.

    Article  PubMed  Google Scholar 

  33. Puri V, Ranjit S, Konda S, Nicoloro SM, Straubhaar J, Chawla A et al. Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc Natl Acad Sci USA 2008; 105: 7833–7838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hardie DG, Ross FA, Hawley SA . AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012; 13: 251–262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hardie DG . AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007; 8: 774–785.

    Article  CAS  PubMed  Google Scholar 

  36. Canto C, Auwerx J . AMP-activated protein kinase and its downstream transcriptional pathways. Cell Mol Life Sci 2010; 67: 3407–3423.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Lindholm CR, Ertel RL, Bauwens JD, Schmuck EG, Mulligan JD, Saupe KW . A high-fat diet decreases AMPK activity in multiple tissues in the absence of hyperglycemia or systemic inflammation in rats. J Physiol Biochem 2013; 69: 165–175.

    Article  CAS  PubMed  Google Scholar 

  38. Pico C, Jilkova ZM, Kus V, Palou A, Kopecky J . Perinatal programming of body weight control by leptin: putative roles of AMP kinase and muscle thermogenesis. Am J Clin Nutr 2011; 94: 1830S–1837S.

    Article  CAS  PubMed  Google Scholar 

  39. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, Carling D et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 2002; 415: 339–343.

    Article  CAS  PubMed  Google Scholar 

  40. Hasenour CM, Berglund ED, Wasserman DH . Emerging role of AMP-activated protein kinase in endocrine control of metabolism in the liver. Mol Cell Endocrinol 2013; 366: 152–162.

    Article  CAS  PubMed  Google Scholar 

  41. Yuan HX, Xiong Y, Guan KL . Nutrient sensing, metabolism, and cell growth control. Mol Cell 2013; 49: 379–387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B et al. AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab 2011; 13: 376–388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Foretz M, Pacot C, Dugail I, Lemarchand P, Guichard C, Le Liepvre X et al. ADD1/SREBP-1c is required in the activation of hepatic lipogenic gene expression by glucose. Mol Cell Biol 1999; 19: 3760–3768.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Spanish Government (AGL2012-33692), and the Instituto de Salud Carlos III, Centro de Investigación Biomédica en Red Fisiopatología de la Obesidad y Nutrición, CIBERobn. Our Laboratory is a member of the European Research Network of Excellence NuGO (The European Nutrigenomics Organization, EU Contract: no. FP6-506360).

Author information

Authors and Affiliations

  1. Molecular Biology, Nutrition and Biotechnology (Nutrigenomics), University of the Balearic Islands (UIB), Cra, Palma de Mallorca and CIBER de Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Spain

    H Castro, C A Pomar, C Picó, J Sánchez & A Palou

Authors
  1. H Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C A Pomar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C Picó
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A Palou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A Palou.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castro, H., Pomar, C., Picó, C. et al. Cafeteria diet overfeeding in young male rats impairs the adaptive response to fed/fasted conditions and increases adiposity independent of body weight. Int J Obes 39, 430–437 (2015). https://doi.org/10.1038/ijo.2014.125

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2014.125

This article is cited by

Search

Advanced search

Quick links