Skip to main content
SpringerLink
Log in

Dietary fatty acids affect mitochondrial phospholipid compositions and mitochondrial gene expression of rainbow trout liver at different ages

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Mitochondria are among the first responders to various stressors that challenge the homeostasis of cells and organisms. Mitochondrial decay is generally associated with impairment in the organelle bioenergetics function and increased oxidative stress, and it appears that deterioration of mitochondrial inner membrane phospholipids (PL), particularly cardiolipin (CL), and accumulation of mitochondrial DNA (mtDNA) mutations are among the main mechanisms involved in this process. In the present study, liver mitochondrial membrane PL compositions, lipid peroxidation, and mtDNA gene expression were analyzed in rainbow trout fed three diets with the same base formulation but with lipid supplied either by fish oil (FO), rapeseed oil (RO), or high DHA oil (DHA) during 6 weeks. Specifically, two feeding trials were performed using fish from the same population of two ages (1 and 3 years), and PL class compositions of liver mitochondria, fatty acid composition of individual PL classes, TBARS content, and mtDNA expression were determined. Dietary fatty acid composition strongly affected mitochondrial membrane composition from trout liver but observed changes did not fully reflect the diet, particularly when it contained high DHA. The changes were PL specific, CL being particularly resistant to changes in DHA. Some significant differences observed in expression of mtDNA with diet may suggest long-term dietary effects in mitochondrial gene expression which could affect electron transport chain function. All the changes were influenced by fish age, which could be related to the different growth rates observed between 1- and 3-year-old trout but that could also indicate age-related changes in the ability to maintain structural homeostasis of mitochondrial membranes.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ANT:

Nucleotide translocase

BHT:

Butylated hydroxytoluene

cDNA:

Complementary DNA

CL:

Cardiolipin

COX:

Cytochrome c oxidase complex

DHA:

Docosahexaenoic acid

E:

PCR efficiency

EPA:

Eicosapentaenoic acid

ETC:

Electron transport chain

FA:

Fatty acid

FAME:

Fatty acid methyl esters

HPTLC:

High performance thin layer chromatography

HUFA:

Highly unsaturated fatty acids

LA:

Linoleic acid

LC-PUFA:

Long-chain polyunsaturated fatty acid

MPH:

Membrane pacemaker hypothesis

mtDNA:

Mitochondrial DNA

MUFA:

Monounsaturated fatty acids

NAC:

No-amplification control

ND:

NADH-coenzyme Q oxidoreductase complex

NTC:

No-template control

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PI:

Phosphatidylinositol

PIn:

Peroxidation index

PL:

Phospholipid

PS:

Phosphatidylserine

PUFA:

Polyunsaturated fatty acid

RO:

Rapeseed oil

ROS:

Reactive oxygen species

SFA:

Saturated fatty acids

FO:

Fish oil

SM:

Sphingomyelin

RT-PCR:

Real-time PCR

TBARS:

Thiobarbituric acid reactive substances

TBA:

Thiobarbituric acid

TCA:

Trichloroacetic acid

TLC:

Thin layer chromatography

References

  • Abbott SK, Else PL, Hulbert AJ (2010) Membrane fatty acid composition of rat skeletal muscle is most responsive to the balance of dietary n−3 and n−6 PUFA. Br J Nutr 103:522–529

    Article  CAS  PubMed  Google Scholar 

  • Almaida-Pagán PF, de Costa J, Mendiola P, Tocher DR (2012) Age-related changes in mitochondrial membrane composition of rainbow trout (Oncorhynchus mykiss) heart and brain. Comp Biochem Physiol B 163:129–137

    Article  PubMed  Google Scholar 

  • Almroth BC, Johansson A, Förlin L, Sturve J (2010) Early-age changes in oxidative stress in brown trout, Salmo trutta. Comp Biochem Physiol B 155:442–448

    Article  Google Scholar 

  • Barzanti V, Battino M, Baracca A, Cavazzoni M, Cocchi M, Noble R, Maranesi M, Turchetto E, Lenaz G (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(2):193–202

    Article  CAS  PubMed  Google Scholar 

  • Bell JG, Henderson RJ, Tocher DR, Sargent JR (2004) Replacement of dietary fish oil with increasing levels of linseed oil: modification of flesh fatty acid compositions in Atlantic salmon (Salmo salar) using a fish oil finishing diet. Lipids 39(3):223–232

    Article  CAS  PubMed  Google Scholar 

  • Burk RF, Trumble MJ, Lawrence RA (1980) Rat hepatic cytosolic GSH-dependent enzyme protection against lipid peroxidation in the NADPH microsomal lipid peroxidation system. Biochim Biophys Acta 618:35–41

    Article  CAS  PubMed  Google Scholar 

  • Chicco AJ, Sparagna GC (2007) Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol 292:C33–C44

    Article  CAS  PubMed  Google Scholar 

  • Chomczynski P, Mackey K (1995) Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. Biotechniques 19:942–945

    CAS  PubMed  Google Scholar 

  • Christie WW (2003) Lipid analysis: isolation, separation, identification and structural analysis of lipids, 3rd edn. Oily Press, Somerset

    Google Scholar 

  • Clandinin MT, Field CJ, Hargraves K, Morson L, Zsigmond E (1985) Role of diet fat in subcellular structure and function. Can J Physiol Pharm 63(546):556

    Google Scholar 

  • Cortopassi GA, Wong A (1999) Mitochondria in organismal aging and degeneration. Biochim Biophys Acta 1410:183–193

    Article  CAS  PubMed  Google Scholar 

  • Crimi M, Esposti MD (2011) Apoptosis-induced changes in mitochondrial lipids. Biochim Biophys Acta Mol Cell Res 1813:551–557

    Article  CAS  Google Scholar 

  • Cutler RG, Mattson MP (2001) Sphingomyelin and ceramide as regulators of development and lifespan. Mech Ageing Dev 122:895–908

    Article  CAS  PubMed  Google Scholar 

  • Daum G (1985) Lipids of mitochondria. Biochim Biophys Acta 822:1–42

    Article  CAS  PubMed  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Guderley H, Kraffe E, Bureau W (2008) Dietary fatty acid composition changes mitochondrial phospholipids and oxidative capacities in rainbow trout red muscle. J Comp Physiol B 178:385–399

    Article  CAS  PubMed  Google Scholar 

  • Hannum YA, Obeid LM (1997) Ceramide and the eukaryotic stress response. Biochem Soc Trans 25:1171–1175

    Google Scholar 

  • Hansford RG, Castro F (1982) Age-linked changes in the activity of enzymes of the tricarboxylate cycle and lipid oxidation, and of carnitine content in muscles of the rat. Mech Ageing Dev 19:191–201

    Article  CAS  PubMed  Google Scholar 

  • Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227

    Article  CAS  PubMed  Google Scholar 

  • Henderson RJ, Tocher (1992) Thin-layer chromatography. In: Hamilton RJ, Hamilton S (eds) Lipid analysis. A practical approach. IRL Press, Oxford, pp 65–111

    Google Scholar 

  • Hoch FL (1992) Cardiolipins and biomembrane function. Biochim Biophys Acta 1113:71–133

    Article  CAS  PubMed  Google Scholar 

  • Hulbert AJ (2007) Membrane fatty acids as pacemaker of animal metabolism. Lipids 42:811–819

    Article  CAS  PubMed  Google Scholar 

  • Hulbert AJ (2008) The links between membrane composition, metabolic rate and lifespan. Comp Biochem Physiol Part A 150:196–203

    Article  CAS  Google Scholar 

  • Hulbert AJ, Turner N, Storlien LH, Else PL (2005) Dietary fats and membrane function: implications for metabolism and disease. Biol Rev 80:155–169

    Article  CAS  PubMed  Google Scholar 

  • Hulbert AJ, Faulks SC, Buffenstein R (2006) Oxidation-resistant membrane phospholipids can explain longevity differences among the longest living rodents and similarly-sized mice. J Gerontol A Biol Sci Med Sci 61:1009–1018

    Article  CAS  PubMed  Google Scholar 

  • Hulbert AJ, Pamplona R, Buffenstein R, Buttemer A (2007) Life and death: metabolic rate, membrane composition and life span of animals. Physiol Rev 87:1175–1213

    Article  CAS  PubMed  Google Scholar 

  • Jaya-Ram A, Kuah M, Lim P, Kolkovski S, Shu-Chien AC (2008) Influence of dietary HUFA levels on reproductive performance, tissue fatty acid profile and desaturase and elongase mRNAs expression in female zebrafish Danio rerio. Aquaculture 277:275–281

    Article  CAS  Google Scholar 

  • Kjaer MA, Todorčević M, Torstensen B, Vegusdal A, Ruyter B (2008) Dietary n−3 HUFA affects mitochondrial fatty acid b-oxidation capacity and susceptibility to oxidative stress in Atlantic Salmon. Lipids 43:813–827

    Article  CAS  PubMed  Google Scholar 

  • Kraffe E, Marty Y, Guderley H (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210:149–165

    Article  CAS  PubMed  Google Scholar 

  • Lemieux H, Blier PU, Tardif JC (2008) Does membrane fatty acid composition modulate mitochondrial functions and their thermal sensitivity? Comp Biochem Physiol A 149:20–29

    Article  CAS  Google Scholar 

  • Manoli I, Alesci S, Blackman MR, Sun YA, Rennert OM, Chrousos GP (2007) Mitochondria as key components of the stress response. TRENDS Endocrin Met 18(5):190–198

    Article  CAS  Google Scholar 

  • Marshall O (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20(15):2471–2472

    Article  CAS  PubMed  Google Scholar 

  • Martin N, Bureau DP, Marty Y, Kraffe E, Guderley H (2013) Dietary lipid quality and mitochondrial membrane composition in trout: responses of membrane enzymes and oxidative capacities. J Comp Physiol B 183:393–408

    Article  CAS  PubMed  Google Scholar 

  • Modi HR, Katyare SS (2008) Ageing-Induced alterations in lipid/phospholipid profiles of rat brain and liver mitochondria: implications for mitochondrial energy-linked functions. J Membrane Biol 221:51–60

    Article  CAS  Google Scholar 

  • Monteiro JP, Oliveira PJ, Jurado AS (2013) Mitochondrial membrane lipid remodelling in pathophysiology: a new target for diet and therapeutic interventions. Prog Lipid Res 52(4):513–528

    Article  CAS  PubMed  Google Scholar 

  • Moyes CD, Ballantyne JS (2011) Membranes and temperature: homeoviscous adaptation. In: Farrell A (ed) Encyclopedia of fish physiology: from genome to environment. Academic Press, Elsevier Inc, New York, pp 1725–1731

    Chapter  Google Scholar 

  • National Research Council (NRC) (2011) Nutrient requirements of fish and shrimp. The National Academies Press, Washington D.C.

  • Olsen RE, Henderson RJ (1989) The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. J Exp Mar Biol Ecol 129:189–197

    Article  CAS  Google Scholar 

  • Østbye TK, Kjaer MA, Rorá AMB, Torstensen B, Ruyter B (2011) High n-3 HUFA levels in the diet of Atlantic salmon affect muscle and mitochondrial membrane lipids and their susceptibility to oxidative stress. Aquacult Nutr 17(2):177–190

    Article  Google Scholar 

  • Otto D, Moon T (1996) Endogenous antioxidant systems of two teleost fish, the rainbow trout and the black bullhead. Fish Physiol Biochem 15:349–358

    Article  CAS  PubMed  Google Scholar 

  • Pamplona R, Barja G, Portero-Otin M (2002) Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span—a homeoviscous-longevity adaptation? Ann N Y Acad Sci 959:475–490

    Article  CAS  PubMed  Google Scholar 

  • Paradies G, Ruggiero FM, Quagliariello E (1992) Age-dependent changes in the activity of anion carriers and in the lipid composition in rat heart mitochondria. Ann N Y Acad Sci 673:160–164

    Article  CAS  PubMed  Google Scholar 

  • Paradies G, Petrosillo G, Pistolese M, Ruggiero FM (2002) Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 286:135–141

    Article  CAS  PubMed  Google Scholar 

  • Paradies G, Petrosillo G, Paradies V, Ruggiero FM (2011) Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem Int 58:447–457

    Article  CAS  PubMed  Google Scholar 

  • Rajapakse N, Shimizu K, Payne M, Busija D (2001) Isolation and characterization of intact mitochondria from neonatal rat brain. Brain Res Prot 8:176–183

    Article  CAS  Google Scholar 

  • Richter C (1995) Oxidative damage to mitochondrial DNA and its relationship to ageing. Int J Biochem Cell Biol 27(7):647–653

    Article  CAS  PubMed  Google Scholar 

  • Robin JH, Regost C, Kaushik SJ (2003) Fatty acid profile of fish following a change in dietary fatty acid source: model of fatty acid composition with a dilution hypothesis. Aquaculture 225:283–293

    Article  CAS  Google Scholar 

  • Rohrbach S (2009) Effects of dietary polyunsaturated fatty acids on mitochondria. Curr Pharm Des 15:4103–4116

    Article  CAS  PubMed  Google Scholar 

  • Sanz A, Pamplona R, Barja G (2006) Is the mitochondrial free radical theory of aging intact? Antioxid Redox Sign 8:582–599

    Article  CAS  Google Scholar 

  • Shigenaga MK, Hagen TM, Ames BN (1994) Oxidative damage and mitochondrial decay in aging. Proc Nat Acad Sci USA 91:10771–10778

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Subbaiah PV, Subramanian VS, Wang K (1999) Novel physiological function of sphingomyelin in plasma. J Biol Chem 274(51):36409–36414

    Article  CAS  PubMed  Google Scholar 

  • Tocher DR, Bell JG, MacGlaughlin P, McGhee F, Dick JR (2001) Hepatocyte fatty acid desaturation and polyunsaturated fatty acid composition of liver in salmonids: effects of dietary vegetable oil. Comp Biochem Physiol B 130:257–270

    Article  CAS  PubMed  Google Scholar 

  • Tocher DR, Agaba M, Hastings N, Bell JG, Dick JR, Teale AJ (2002) Nutritional regulation of hepatocyte fatty acid desaturation and polyunsaturated fatty acid composition in zebrafish (Danio rerio) and tilapia (Oreochromis niloticus). Fish Physiol Biochem 24:309–320

    Article  Google Scholar 

  • Trifunovic A, Larsson NG (2008) Mitochondrial dysfunction as a cause of ageing. J Intern Med 263:167–178

    Article  CAS  PubMed  Google Scholar 

  • Ushio H, Muramatsu M, Ohshima T, Koizumi C (1997) Fatty acid compositions of biological membranes from fast skeletal muscle of carp. Fisheries Sci 62(3):427–434

    Google Scholar 

  • Vu TH, Tanji K, Pallotti F, Golzi V, Hirano M, DiMauro S, Bonilla E (2000) Analysis of mtDNA deletions in muscle by in situ hybridization. Muscle Nerve 23:80–85

    Article  CAS  PubMed  Google Scholar 

  • Wiseman H (1996) Dietary influences on membrane function: importance in protection against oxidative damage and disease. J Nutr Biochem 7:2–15

    Article  CAS  Google Scholar 

  • Witting LA, Horwitt MK (1964) Effect of degree of fatty acid unsaturation in tocopherol deficiency-induced Creatinuria. J Nutr 82:19–33

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zabelinskii SA, Chebotareva MA, Kostkin VB, Krivchenko AI (1999) Phospholipids and their fatty acids in mitochondria, synaptosomes and myelin from the liver and brain of trout and rat: a new view on the role of fatty acids in membranes. Comp Biochem Physiol Part B 124:187–193

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge our colleagues Professor Gordon Bell for formulation and manufacture of the experimental feeds and Niall Auchinachie for fish husbandry. This research and P.F.A.-P. were funded by a Marie Curie Intra-European Fellowship within the 7th Community Framework Programme (PIEF-GA-2011-297964, OLDMITO). The authors report no conflicts of interest.

Author information

Authors and Affiliations

  1. School of Natural Sciences, Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA, Scotland, UK

    P. F. Almaida-Pagán, C. De Santis, O. L. Rubio-Mejía & D. R. Tocher

Authors
  1. P. F. Almaida-Pagán
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. De Santis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. L. Rubio-Mejía
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. R. Tocher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. F. Almaida-Pagán.

Additional information

Communicated by G. Heldmaier.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Almaida-Pagán, P.F., De Santis, C., Rubio-Mejía, O.L. et al. Dietary fatty acids affect mitochondrial phospholipid compositions and mitochondrial gene expression of rainbow trout liver at different ages. J Comp Physiol B 185, 73–86 (2015). https://doi.org/10.1007/s00360-014-0870-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-014-0870-8

Keywords

Search

Navigation