Skip to main content

Advertisement

Springer Nature Link
Log in

The effect of high-fat–high-fructose diet on skeletal muscle mitochondrial energetics in adult rats

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

To study the effect of isoenergetic administration to adult rats of high-fat or high-fat–high-fructose diet for 2 weeks on skeletal muscle mitochondrial energetic.

Methods

Body and skeletal muscle composition, energy balance, plasma lipid profile and glucose tolerance were measured, together with mitochondrial functionality, oxidative stress and antioxidant defense.

Results

Rats fed high-fat–high-fructose diet exhibited significantly higher plasma triglycerides and non-esterified fatty acids, together with significantly higher plasma glucose and insulin response to glucose load. Skeletal muscle triglycerides and ceramide were significantly higher in rats fed high-fat–high-fructose diet. Skeletal muscle mitochondrial energetic efficiency and uncoupling protein 3 content were significantly higher, while adenine nucleotide translocase content was significantly lower, in rats fed high-fat or high-fat–high-fructose diet.

Conclusions

The results suggest that a high-fat–high-fructose diet even without hyperphagia is able to increase lipid flow to skeletal muscle and mitochondrial energetic efficiency, with two detrimental effects: (a) energy sparing that contributes to the early onset of obesity and (b) reduced oxidation of fatty acids and lipid accumulation in skeletal muscle, which could generate insulin resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  1. Ritov VB, Menshikova EV, Azuma K, Wood R, Toledo FG, Goodpaster BH, Ruderman NB, Kelley DE (2010) Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. Am J Physiol Endocrinol Metab 298:E49–E58

    Article  CAS  Google Scholar 

  2. Ara I, Larsen S, Stallknecht B, Guerra B, Morales-Alamo D, Andersen JL, Ponce-González JG, Guadalupe-Grau A, Galbo H et al (2011) Normal mitochondrial function and increased fat oxidation capacity in leg and arm muscles in obese humans. Int J Obes (Lond) 35:99–108

    Article  CAS  Google Scholar 

  3. Martins AR, Nachbar RT, Gorjao R, Vinolo MA, Festuccia WT, Lambertucci RH, Cury-Boaventura MF, Silveira LR, Curi R, Hirabara SM (2012) Mechanisms underlying skeletal muscle insulin resistance induced by fatty acids: importance of the mitochondrial function. Lipids Health Dis 11:30

    Article  CAS  Google Scholar 

  4. Turner N, Bruce CR, Beale SM, Hoehn KL, So T, Rolph MS, Cooney GJ (2007) Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 56:2085–2092

    Article  CAS  Google Scholar 

  5. Hancock CR, Han DH, Chen M, Terada S, Yasuda T, Wright DC, Holloszy JO (2008) High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci USA 105:7815–7820

    Article  CAS  Google Scholar 

  6. Little JP, Safdar A, Benton CR, Wright DC (2011) Skeletal muscle and beyond: the role of exercise as a mediator of systemic mitochondrial biogenesis. Appl Physiol Nutr Metab 36(5):598–607

    Article  CAS  Google Scholar 

  7. Spangenberg EM, Augustsson H, Dahlborn K, Essén-Gustavsson B, Cvek K (2005) Housing-related activity in rats: effects on body weight, urinary corticosterone levels, muscle properties and performance. Lab Anim 39(1):45–57

    Article  CAS  Google Scholar 

  8. Crescenzo R, Bianco F, Coppola P, Mazzoli A, Valiante S, Liverini G, Iossa S (2013) Adipose tissue remodeling in rats exhibiting fructose-induced obesity. Eur J Nutr. doi:10.1007/s00394-013-0538-2

    Google Scholar 

  9. Crescenzo R, Bianco F, Falcone I, Coppola P, Liverini G, Iossa S (2013) Increased hepatic de novo lipogenesis and mitochondrial efficiency in a model of obesity induced by diets rich in fructose. Eur J Nutr 52:537–545

    Article  CAS  Google Scholar 

  10. Crescenzo R, Bianco F, Coppola P, Mazzoli A, Cigliano L, Liverini G, Iossa S (2013) Increased skeletal muscle mitochondrial efficiency in rats with fructose-induced alteration in glucose tolerance. Br J Nutr 110:1996–2003

    Article  CAS  Google Scholar 

  11. Lionetti L, Mollica MP, Crescenzo R, D’Andrea E, Ferraro M, Bianco F, Liverini G, Iossa S (2007) Skeletal muscle subsarcolemmal mitochondrial dysfunction in high-fat fed rats exhibiting impaired glucose homeostasis. Int J Obes 31(10):1596–1604

    Article  CAS  Google Scholar 

  12. Crescenzo R, Bianco F, Falcone I, Prisco M, Liverini G, Iossa S (2008) Alterations in hepatic mitochondrial compartment in a model of obesity and insulin resistance. Obesity 16(5):958–964

    Article  CAS  Google Scholar 

  13. Iossa S, Lionetti L, Mollica MP, Crescenzo R, Botta M, Barletta A, Liverini G (2003) Effect of high-fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats. Br J Nutr 90(5):953–960

    Article  CAS  Google Scholar 

  14. Cacho J, Sevillano J, de Castro J, Herrera E, Ramos MP (2008) Validation of simple indexes to assess insulin sensitivity during pregnancy in Wistar and Sprague–Dawley rats. Am J Physiol 295:E1269–E1276

    CAS  Google Scholar 

  15. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–510

    CAS  Google Scholar 

  16. Dulloo AG, Girardier L (1992) Influence of dietary composition on energy expenditure during recovery of body weight in the rat: implications for catch-up growth and obesity relapse. Metabolism 41:1336–1342

    Article  CAS  Google Scholar 

  17. Roehrig KL, Allred JB (1974) Direct enzymatic procedure for the determination of liver glycogen. Anal Biochem 58:414–421

    Article  CAS  Google Scholar 

  18. Crescenzo R, Bianco F, Falcone I, Prisco M, Dulloo AG, Liverini G, Iossa S (2010) Hepatic mitochondrial energetic during catch-up fat after caloric restriction. Metabolism 59:1221–1230

    Article  CAS  Google Scholar 

  19. Iossa S, Lionetti L, Mollica MP, Crescenzo R, Botta M, Barletta A, Liverini G (2003) Effect of high-fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats. Br J Nutr 90:953–960

    Article  CAS  Google Scholar 

  20. Pullar JD, Webster AJF (1977) The energy cost of fat and protein deposition in the rat. Br J Nutr 37:355–363

    Article  CAS  Google Scholar 

  21. Rothwell NJ, Stock MJ, Warwick BP (1985) Energy balance and brown fat activity in rats fed cafeteria diets or high fat, semisynthetic diets at several levels of intake. Metabolism 34:474–480

    Article  CAS  Google Scholar 

  22. Iossa S, Mollica MP, Lionetti L, Crescenzo R, Tasso R, Liverini G (2004) A possible link between skeletal muscle mitochondrial efficiency and age-induced insulin resistance. Diabetes 53:2861–2866

    Article  CAS  Google Scholar 

  23. Cairns CB, Walther J, Harken AH, Banerjee A (1998) Mitochondrial oxidative phosphorylation efficiencies reflect physiological organ roles. Am J Physiol 274:R1376–R1383

    CAS  Google Scholar 

  24. Fernandes MA, Custódio JB, Santos MS, Moreno AJ, Vicente JA (2006) Tetrandrine concentrations not affecting oxidative phosphorylation protect rat liver mitochondria from oxidative stress. Mitochondrion 6:176–185

    Article  CAS  Google Scholar 

  25. Gardner PR (2002) Aconitase: sensitive target and measure of superoxide. Meth Enzymol 349:9–16

    Article  CAS  Google Scholar 

  26. Flohè L, Otting F (1974) Superoxide dismutase assay. Methods Enzymol 105:93–104

    Article  Google Scholar 

  27. Abdul-Ghani MA, Matsuda M, Balas B, DeFronzo RA (2007) Muscle and liver insulin resistance indexes derived from the oral glucose tolerance test. Diabetes Care 30(1):89–94

    Article  CAS  Google Scholar 

  28. Mollica MP, Lionetti L, Crescenzo R, Tasso R, Barletta A, Liverini G, Iossa S (2005) Cold exposure differently influences mitochondrial energy efficiency in rat liver and skeletal muscle. FEBS Lett 579:1978–1982

    Article  CAS  Google Scholar 

  29. Parker N, Affourtit C, Vidal-Puig A, Brand MD (2008) Energization-dependent endogenous activation of proton conductance in skeletal muscle mitochondria. Biochem J 412(1):131–139

    Article  CAS  Google Scholar 

  30. Hariri N, Thibault L (2010) High-fat diet-induced obesity in animal models. Nutr Res Rev 23(2):270–299

    Article  CAS  Google Scholar 

  31. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  Google Scholar 

  32. Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944–2950

    Article  CAS  Google Scholar 

  33. Morino K, Petersen KF, Shulman GI (2006) Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55:S9–S15

    Article  CAS  Google Scholar 

  34. Coen PM, Dube JJ, Amati F, Stefanovic-Racic M, Ferrell RE, Toledo FG, Goodpaster BH (2010) Insulin resistance is associated with higher intramyocellular triglycerides in type I but not type II myocytes concomitant with higher ceramide content. Diabetes 59:80–88

    Article  CAS  Google Scholar 

  35. Dela F, Helge JW (2013) Insulin resistance and mitochondrial function in skeletal muscle. Int J Biochem Cell Biol 45:11–15

    Article  CAS  Google Scholar 

  36. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, Brookes PS, Cornwall EJ (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392:353–362

    Article  CAS  Google Scholar 

  37. Oakes ND, Kjellstedt A, Thalén P, Ljung B, Turner N (2013) Roles of fatty acid oversupply and impaired oxidation in lipid accumulation in tissues of obese rats. J Lipids. doi:10.1155/2013/420754

    Google Scholar 

  38. Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15–18

    Article  CAS  Google Scholar 

  39. Azzu V, Brand MD (2010) The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 35:298–307

    Article  CAS  Google Scholar 

  40. Schrauwen P, Hoeks J, Hesselink MK (2006) Putative function and physiological relevance of the mitochondrial uncoupling protein-3: involvement in fatty acid metabolism? Prog Lipid Res 45:17–41

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from University “Federico II” of Naples and by P.O.R. Campania FSE 2007-2013, Project CREME. The authors thank Dr. Emilia De Santis for skilful management of animal house.

Conflict of interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Biology, University of Naples, Complesso Universitario Monte Sant’Angelo, Edificio 7, Via Cinthia, 80126, Naples, Italy

    Raffaella Crescenzo, Francesca Bianco, Paola Coppola, Arianna Mazzoli, Luisa Cigliano, Giovanna Liverini & Susanna Iossa

Authors
  1. Raffaella Crescenzo
    View author publications

    Search author on:PubMed Google Scholar

  2. Francesca Bianco
    View author publications

    Search author on:PubMed Google Scholar

  3. Paola Coppola
    View author publications

    Search author on:PubMed Google Scholar

  4. Arianna Mazzoli
    View author publications

    Search author on:PubMed Google Scholar

  5. Luisa Cigliano
    View author publications

    Search author on:PubMed Google Scholar

  6. Giovanna Liverini
    View author publications

    Search author on:PubMed Google Scholar

  7. Susanna Iossa
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Susanna Iossa.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crescenzo, R., Bianco, F., Coppola, P. et al. The effect of high-fat–high-fructose diet on skeletal muscle mitochondrial energetics in adult rats. Eur J Nutr 54, 183–192 (2015). https://doi.org/10.1007/s00394-014-0699-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0699-7

Keywords

Profiles

  1. Arianna Mazzoli View author profile
  2. Susanna Iossa View author profile