Rapeseed oil-rich diet alters hepatic mitochondrial membrane lipid composition and disrupts bioenergetics

Abstract

Diet is directly related with physiological alterations occurring at a cell and subcellular level. However, the role of diet manipulation on mitochondrial physiology is still largely unexplored. Aiming at correlating diet with alterations of mitochondrial membrane composition and bioenergetics, Wistar-Han male rats were fed for 11, 22 and 33 days with a rapeseed oil-based diet and mitochondrial bioenergetics, and membrane composition were compared at each time point with a standard diet group. Considerable differences were noticed in mitochondrial membrane lipid composition, namely in terms of fatty acyl chains and relative proportions of phospholipid classes, the modified diet inducing a decrease in the saturated to unsaturated molar ratio and an increase in the phosphatidylcholine to phosphatidylethanolamine molar ratio. Mass spectrometry lipid analysis showed significant differences in the major species of cardiolipin, with an apparent increased incorporation of oleic acid as a result of exposure to the modified diet. Rats fed the modified diet during 22 days showed decreased hepatic mitochondrial state 3 respiration and were more susceptible to Ca2+-induced transition pore opening. Rapeseed oil-enriched diet also appeared to promote a decrease in hydroperoxide production by the respiratory chain, although a simultaneous decrease in vitamin E content was detected. In conclusion, our data indicate that the rapeseed oil diet causes negative alterations on hepatic mitochondrial bioenergetics, which may result from membrane remodeling. Such alterations may have an impact not only on energy supply to the cell, but also on drug-induced hepatic mitochondrial liabilities.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Abdellatif AMM, Vles RO (1970) Pathological effects of dietary rapeseed oil in rats. Ann Nutr Metab 12(5):285–295

    CAS  Article  Google Scholar 

  2. Attorri L, Di Biase A, Di Benedetto R, Rigato P, Di Virgilio A, Salvati S (2010) Micronutrient-enriched rapeseed oils reduce cardiovascular disease risk factors in rats fed a high-fat diet. Atherosclerosis 213(2):422–428

    PubMed  CAS  Article  Google Scholar 

  3. Barja G (1999) Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr 31(4):347–366. doi:10.1023/a:1005427919188

    PubMed  CAS  Article  Google Scholar 

  4. Bartlett GR (1959) Phosphorus assay in column chromatography. J Biol Chem 234(3):466–468

    PubMed  CAS  Google Scholar 

  5. Barzanti V, Battino M, Baracca A et al (1994) The effect of dietary lipid changes on the fatty acid composition and function of liver, heart and brain mitochondria in the rat at different ages. Br J Nutr 71(02):193–202. doi:10.1079/BJN19940126

    PubMed  CAS  Article  Google Scholar 

  6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    PubMed  CAS  Article  Google Scholar 

  7. Blomstrand R, Svensson L (1975) Observations on lipid composition with particular reference to cardiolipin of rat heart after feeding rapeseed oil. Acta Med Scand 198(S585):51–73. doi:10.1111/j.0954-6820.1975.tb06559.x

    Article  Google Scholar 

  8. Bottcher CJF, van Gent CM, Pries C (1961) A rapid and sensitive sub-micro phosphorus determination. Anal Chim Acta 24:203–204

    CAS  Article  Google Scholar 

  9. Broekemeier KM, Pfeiffer DR (1989) Cyclosporin A-sensitive and insensitive mechanisms produce the permeability transition in mitochondria. Biochem Biophys Res Commun 163(1):561–566

    PubMed  CAS  Article  Google Scholar 

  10. Català-Niell A, Estrany ME, Proenza AM, Gianotti M, Lladó I (2008) Skeletal muscle and liver oxidative metabolism in response to a voluntary isocaloric intake of a high fat diet in male and female rats. Cell Physiol Biochem 22(1–4):327–336

    PubMed  Article  Google Scholar 

  11. Cavalcanti T, Marques D, Guimaratilde es F, Tahin Q (1996) Liver mitochondria swelling in rats treated with two lipid diets. Prog Biophys Mol Bio 65(1):117–117(1)

    Google Scholar 

  12. Chanadiri TV, Esaiashvili MV, Chkhikvishvili ID (2006) Disorders of liver oxidative metabolism during experimental obesity. Georgian Med News 131:85–87

    PubMed  Google Scholar 

  13. Cioffi F, Senese R, de Lange P, Goglia F, Lanni A, Lombardi A (2009) Uncoupling proteins: a complex journey to function discovery. BioFactors 35(5):417–428. doi:10.1002/biof.54

    PubMed  CAS  Article  Google Scholar 

  14. Clandinin MT (1978) The role of dietary long chain fatty acids in mitochondrial structure and function. Effects on rat cardiac mitochondrial respiration. J Nutr 108(2):273–281

    PubMed  CAS  Google Scholar 

  15. Clandinin MT, Field CJ, Hargreaves K, Morson L, Zsigmond E (1985) Role of diet fat in subcellular structure and function. Can J Physiol Pharmacol 63(5):546–556. doi:10.1139/y85-094

    PubMed  CAS  Article  Google Scholar 

  16. Claypool SM (2009) Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. BBA Biomembr 1788(10):2059–2068

    CAS  Article  Google Scholar 

  17. de Kroon AIPM, Dolis D, Mayer A, Lill R, de Kruijff B (1997) Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim Biophys Acta Biomembr 1325(1):108–116

    Article  Google Scholar 

  18. Dewailly P, Sezille G, Nouvelot A, Fruchart JC, Jaillard J (1977) Changes in rat heart phospholipid composition after rapeseed oil feeding. Lipids 12(3):301–306

    PubMed  CAS  Article  Google Scholar 

  19. Estabrook RW (1967) Mitochondrial respiratory control and the polarographic measurement of ADP:O ratios. Methods Enzymol 10:41–47

    CAS  Google Scholar 

  20. Faulks SC, Turner N, Else PL, Hulbert AJ (2006) Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J Gerontol A Biol Sci Med Sci 61(8):781–794

    PubMed  Article  Google Scholar 

  21. Gonzalvez F, Gottlieb E (2007) Cardiolipin: setting the beat of apoptosis. Apoptosis 12(5):877–885. doi:10.1007/s10495-007-0718-8

    PubMed  CAS  Article  Google Scholar 

  22. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177(2):751–766

    PubMed  CAS  Google Scholar 

  23. Gruner SM (1985) Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc Natl Acad Sci USA 82(11):3665–3669

    Google Scholar 

  24. Haeffner E, Privett O (1975) Influence of dietary fatty acids on membrane properties and enzyme activities of liver mitochondria of normal and hypophysectomized rats. Lipids 10(2):75–81. doi:10.1007/bf02532159

    PubMed  CAS  Article  Google Scholar 

  25. Houtsmuller UMT, Struijk CB, Van der Beek A (1970) Decrease in rate of ATP synthesis of isolated rat heart mitochondria induced by dietary erucic acid. BBA Lipid Lipid Met 218(3):564–566

    CAS  Article  Google Scholar 

  26. Huertas JR, Battino M, Lenaz G, Mataix FJ (1991) Changes in mitochondrial and microsomal rat liver coenzyme Q9, and Q10 content induced by dietary fat and endogenous lipid peroxidation. FEBS Lett 287(1–2):89–92

    PubMed  CAS  Article  Google Scholar 

  27. Innis SM, Clandinin MT (1981a) Dynamic modulation of mitochondrial inner-membrane lipids in rat heart by dietary fat. Biochem J 193(1):155–167

    PubMed  CAS  Google Scholar 

  28. Innis SM, Clandinin MT (1981b) Mitochondrial-membrane polar-head-group composition is influenced by diet fat. Biochem J 198(1):231–234

    PubMed  CAS  Google Scholar 

  29. Iossa S, Lionetti L, Mollica MP, Crescenzo R, Barletta A, Liverini G (2000) Effect of long-term high-fat feeding on energy balance and liver oxidative activity in rats. Br J Nutr 84(3):377–385

    PubMed  CAS  Google Scholar 

  30. Israelachvili JN, Marcelja S, Horn RG (1980) Physical principles of membrane organization. R Rev Biophys 13(02):121–200. doi:10.1017/S0033583500001645

    CAS  Article  Google Scholar 

  31. Kagan VE, Bayir A, Bayir H et al (2009) Mitochondria-targeted disruptors and inhibitors of cytochrome c/cardiolipin peroxidase complexes: a new strategy in anti-apoptotic drug discovery. Mol Nutr Food Res 53(1):104–114. doi:10.1002/mnfr.200700402

    PubMed  CAS  Article  Google Scholar 

  32. Kamo N, Muratsugu M, Ruji H, Kobatake Y (1979) Membrane potencial of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol 49:105–121

    PubMed  CAS  Article  Google Scholar 

  33. Kass GEN (2006) Mitochondrial involvement in drug-induced hepatic injury. Chem Biol Interact 163(1–2):145–159

    PubMed  CAS  Article  Google Scholar 

  34. Kuznetsov AV, Strobl D, Ruttmann E, Königsrainer A, Margreiter R, Gnaiger E (2002) Evaluation of mitochondrial respiratory function in small biopsies of liver. Anal Biochem 305(2):186–194

    PubMed  CAS  Article  Google Scholar 

  35. Maciel E, Domingues P, Domingues MRM (2011) Liquid chromatography/tandem mass spectrometry analysis of long-chain oxidation products of cardiolipin induced by the hydroxyl radical. Rapid Commun Mass Spectrom 25(2):316–326. doi:10.1002/rcm.4866

    PubMed  CAS  Article  Google Scholar 

  36. Mataix J, Mañas M, Quiles J et al (1997) Coenzyme Q content depends upon oxidative stress and dietary fat unsaturation. Mol Aspects Med 18(1):129–135

    Article  Google Scholar 

  37. Neuburger M, Journet E-P, Bligny R, Carde J-P, Douce R (1982) Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch Biochem Biophys 217(1):312–323

    PubMed  CAS  Article  Google Scholar 

  38. Nguemeni C, Delplanque B, Rovère C et al (2010) Dietary supplementation of alpha-linolenic acid in an enriched rapeseed oil diet protects from stroke. Pharmacol Res 61(3):226–233

    PubMed  CAS  Article  Google Scholar 

  39. Ohara N, Naito Y, Nagata T, Tachibana S, Okimoto M, Okuyama H (2008) Dietary intake of rapeseed oil as the sole fat nutrient in wistar rats—Lack of increase in plasma lipids and renal lesions. J Toxicol Sci 33(5):641–645

    PubMed  CAS  Article  Google Scholar 

  40. O’Shea KM, Khairallah RJ, Sparagna GC et al (2009) Dietary [omega]-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2+-induced permeability transition. J Mol Cell Cardiol 47(6):819–827

    PubMed  Article  Google Scholar 

  41. Osman C, Voelker, Langer T (2011) Making heads or tails of phospholipids in mitochondria. J Cell Biol 192(1):7–16. doi:10.1083/jcb.201006159

    PubMed  CAS  Article  Google Scholar 

  42. Pepe S, Tsuchiya N, Lakatta EG, Hansford RG (1999) PUFA and aging modulate cardiac mitochondrial membrane lipid composition and Ca2 + activation of PDH. Am J Physiol Heart Circ Physiol 276(1):H149–H158

    CAS  Google Scholar 

  43. Pereira GC, Branco AF, Matos JAC et al (2007) Mitochondrially targeted effects of berberine (natural yellow 18, 5,6-dihydro-9,10-dimethoxybenzo(g)-1,3-benzodioxolo(5,6-a) quinolizinium) on K1735-M2 mouse melanoma cells: comparison with direct effects on isolated mitochondrial fractions. J Pharmacol Exp Ther 323(2):636–649. doi:10.1124/jpet.107.128017

    PubMed  CAS  Article  Google Scholar 

  44. Ramsey JJ, Harper M-E, Humble SJ et al (2005) Influence of mitochondrial membrane fatty acid composition on proton leak and H2O2 production in liver. Comp Biochem Physiol B: Biochem Mol Biol 140(1):99–108

    Article  Google Scholar 

  45. Reddy JK, Sambasiva Rao M (2006) Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation. Am J Physiol Gastrointest Liver Physiol 290(5):G852–G858

    PubMed  CAS  Article  Google Scholar 

  46. Renner R, Innis SM, Clandinin MT (1979) Effects of high and low erucic acid rapeseed oils on energy metabolism and mitochondrial function of the chick. J Nutr 109(3):378–387

    PubMed  CAS  Google Scholar 

  47. Robinson CE, Keshavarzian A, Pasco DS, Frommel TO, Winship DH, Holmes EW (1999) Determination of protein carbonyl groups by immunoblotting. Anal Biochem 266(1):48–57

    PubMed  CAS  Article  Google Scholar 

  48. Rosa SMLJ, MdC Antunes-Madeira, Matos MJ, Jurado AS, Madeira VMC (2000) Lipid composition and dynamics of cell membranes of Bacillus stearothermophilus adapted to amiodarone. Biochim Biophys Acta Mol Cell Biol Lipids 1487(2–3):286–295

    CAS  Article  Google Scholar 

  49. Rosillo-Calle F, Pelkmans L, Walter A (2009) A global overview of vegetable oils, with reference to biodiesel. A Report for the IEA bioenergy task 40, IEA bioenergy

  50. Scaini G, Rochi N, Benedet J et al (2011) Inhibition of brain citrate synthase activity in an animal model of sepsis. Braz J Intens Care 23(2):158–163

    Google Scholar 

  51. Vatassery G, Younoszai R (1978) Alpha tocopherol levels in various regions of the central nervous systems of the rat and guinea pig. Lipids 13(11):828–831. doi:10.1007/bf02533486

    PubMed  CAS  Article  Google Scholar 

  52. Xu Y, Malhotra A, Ren M, Schlame M (2006) The enzymatic function of tafazzin. J Biol Chem 281(51):39217–39224. doi:10.1074/jbc.M606100200

    PubMed  CAS  Article  Google Scholar 

  53. Yamaoka S, Urade R, Kito M (1988) Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J Nutr 118(3):290–296

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The project was supported by the Foundation for Science and Technology with FEDER/COMPETE/National Budget funds (research grants PTDC/QUI–QUI/101409/2008 to P. J. O., PTDC/QUI-BIQ/103001/2008 to A. S. J. and strategic grant PEst-C/SAU/LA0001/2011to the CNC). J. P. M. and A. M. S. acknowledge FCT for Ph.D. grants SFRH/BD/37626/2007 and PTDC/AGR-ALI/108326/2008, respectively.

Conflict of interest

The authors declare that they have no conflicts of interest. The Funding Agency, which is supported by the Portuguese Government, had no role in the decision to publish the data or in the data presented.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Paulo J. Oliveira.

Additional information

Amália S. Jurado and Paulo J. Oliveira share senior authorship.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 379 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Monteiro, J.P., Pereira, C.V., Silva, A.M. et al. Rapeseed oil-rich diet alters hepatic mitochondrial membrane lipid composition and disrupts bioenergetics. Arch Toxicol 87, 2151–2163 (2013). https://doi.org/10.1007/s00204-013-1068-7

Download citation

Keywords

  • Rapeseed oil
  • Diet
  • Liver mitochondria
  • Wistar rat
  • Toxicity
  • Mitochondrial membrane