Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce β-oxidation in white fat

Diabetologia

Volumn 48, Issue 11, 2005, Pages 2365-2375

  Flachs, P ^a   Horakova, O ^a   Brauner, P ^a   Rossmeisl, M ^a   Pecina, P ^a   Franssen Van Hal, N ^b   Ruzickova, J ^a   Sponarova, J ^a   Drahota, Z ^a   Vlcek, C ^c   Keijer, J ^b   Houstek, J ^a   Kopecky, J ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Adipose tissue; Carnitine palmitoyltransferase 1; Fish oil; Flax seed oil; Metabolism; Mitochondria; n 3 Polyunsaturated fatty acids; PGC 1; PPARGC1A

Indexed keywords

DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; POLYUNSATURATED FATTY ACID;

ABDOMEN; AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; GENE EXPRESSION; LIPID DIET; LIPID METABOLISM; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OBESITY; OXIDATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ADIPOCYTES; ADIPOSE TISSUE; ALPHA-LINOLENIC ACID; ANIMALS; CARNITINE O-PALMITOYLTRANSFERASE; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; EPIDIDYMIS; FATTY ACIDS, UNSATURATED; FISH OILS; GENE EXPRESSION REGULATION; LIPOGENESIS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NF-E2-RELATED FACTOR 1; OBESITY; OXIDATION-REDUCTION; SUBCUTANEOUS FAT; TRANS-ACTIVATORS;

EID: 27744482030     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-005-1944-7     Document Type: Article

References (49)

1. Kopelman PG (2000) Obesity as a medical problem. Nature 404:635-643
2. Oudart H, Groscolas R, Calgari C et al (1997) Brown fat thermogenesis in rats fed high-fat diets enriched with n-3 polyunsaturated fatty acids. Int J Obes Relat Metab Disord 21:955-962
3. Hun CS, Hasegawa K, Kawabata T, Kato M, Shimokawa T, Kagawa Y (1999) Increased uncoupling protein 2 mRNA in white adipose tissue, and decrease in leptin, visceral fat, blood glucose, and cholesterol in KK-Ay mice fed with eicosapentaenoic and docosahexaenoic acids in addition to linolenic acid. Biochem Biophys Res Commun 259:85-90
4. Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, Ezaki O (1996) High-fat diet-induced hyperglycemia and obesity in mice: differential effects of dietary oils. Metabolism 45:1539-1546
5. Raclot T, Groscolas R, Langin D, Ferre P (1997) Site-specific regulation of gene expression by n-3 polyunsaturated fatty acids in rat white adipose tissues. J Lipid Res 38:1963-1972
6. Azain MJ (2004) Role of fatty acids in adipocyte growth and development. J Anim Sci 82:916-924
7. Hill JO, Peters JC, Lin D, Yakubu F, Greene H, Swift L (1993) Lipid accumulation and body fat distribution is influenced by type of dietary fat fed to rats. Int J Obes Relat Metab Disord 17:223-236
8. Ruzickova J, Rossmeisl M, Prazak T et al (2004) Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 39:1177-1185
9. Ruxton CH, Reed SC, Simpson MJ, Millington KJ (2004) The health benefits of omega-3 polyunsaturated fatty acids: a review of the evidence. J Hum Nutr Diet 17:449-459
10. Sinclair AJ, Attar-Bashi NM, Li D (2002) What is the role of alpha-linolenic acid for mammals? Lipids 37:1113-1123
11. Couet C, Delarue J, Ritz P, Antoine J-M, Lamisse F (1997) Effect of dietary fish oil on body fat mass and basal fat oxidation in healthy adults. Int J Obes Relat Metab Disord 21:637-643
12. Lapillonne A, Clarke SD, Heird WC (2004) Polyunsaturated fatty acids and gene expression. Curr Opin Clin Nutr Metab Care 7:151-156
13. Baillie RA, Takada R, Nakamura M, Clarke SD (1999) Coordinate induction of peroxisomal acyl-CoA oxidase and UCP-3 by dietary fish oil: a mechanism for decreased body fat deposition. Prostaglandins Leukot Essent Fat Acids 60:351-356
14. Takahashi Y, Ide T (2000) Dietary n-3 fatty acids affect mRNA level of brown adipose tissue uncoupling protein 1, and white adipose tissue leptin and glucose transporter 4 in the rat. Br J Nutr 84:175-184
15. Raclot T, Oudart H (1999) Selectivity of fatty acids on lipid metabolism and gene expression. Proc Nutr Soc 58:633-646
16. Newman RE, Bryden WL, Fleck E et al (2002) Dietary n-3 and n-6 fatty acids alter avian metabolism: metabolism and abdominal fat deposition. Br J Nutr 88:11-18
17. Kopecky J, Hodny Z, Rossmeisl M, Syrovy I, Kozak LP (1996) Reduction of dietary obesity in the aP2-Ucp transgenic mice: physiology and adipose tissue distribution. Am J Physiol 270:E768-E775
18. Puigserver P, Spiegelman BM (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 24:78-90
19. Kelly DP, Scarpulla RC (2004) Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18:357-368
20. Tiraby C, Tavernier G, Lefort C et al (2003) Acquirement of brown fat cell features by human white adipocytes. J Biol Chem 278:33370-33376
21. Lin J, Wu PH, Tarr PT et al (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119:121-135
22. Rossmeisl M, Syrový I, Baumruk F, Flachs P, Janovská P, Kopecký J (2000) Decreased fatty acid synthesis due to mitochondrial uncoupling in adipose tissue. FASEB J 14:1793-1800
23. Rossmeisl M, Barbatelli G, Flachs P et al (2002) Expression of the uncoupling protein 1 from the aP2 gene promoter stimulates mitochondrial biogenesis in unilocular adipocytes in vivo. Eur J Biochem 269:1-10
24. Henegariu O, Bray-Ward P, Ward DC (2000) Custom fluorescent-nucleotide synthesis as an alternative method for nucleic acid labeling. Nat Biotechnol 18:345-348
25. Pellis L, Franssen-van Hal NL, Burema J, Keijer J (2003) The intraclass correlation coefficient applied for evaluation of data correction, labeling methods, and rectal biopsy sampling in DNA microarray experiments. Physiol Genomics 16:99-106
26. Antonicka H, Floryk D, Klement P et al (1999) Defective kinetics of cytochrome c oxidase and alteration of mitochondrial membrane potential in fibroblasts and cytoplasmic hybrid cells with the mutation for myoclonus epilepsy with ragged-red fibres ('MERRF') at position 8344 nt. Biochem J 342:537-544
27. Moradi-Ameli M, Godinot C (1983) Characterization of monoclonal antibodies against mitochondrial F1-ATPase. Proc Natl Acad Sci U S A 80:6167-6171
28. Matejkova O, Mustard KJ, Sponarova J et al (2004) Possible involvement of AMP-activated protein kinase in obesity resistance induced by respiratory uncoupling in white fat. FEBS Lett 569:245-248
29. Cianflone K, Xia Z, Chen LY (2003) Critical review of acylation-stimulating protein physiology in humans and rodents. Biochim Biophys Acta 1609:127-143
30. Dobrzyn A, Ntambi JM (2004) The role of stearoyl-CoA desaturase in body weight regulation. Trends Cardiovasc Med 14:77-81
31. Song S, Zhang Y, Ma K et al (2004) Peroxisomal proliferator activated receptor gamma coactivator (PGC-1alpha) stimulates carnitine palmitoyltransferase I (CPT-Ialpha) though the first intron. Biochim Biophys Acta 1679:164-173
32. Forman BM, Chen J, Evans RM (1997) Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci U S A 94:4312-4317
33. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839
34. Vega RB, Huss JM, Kelly DP (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20:1868-1876
35. Wang YX, Lee CH, Tiep S et al (2003) Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 113:159-170
36. Wilson-Fritch L, Nicoloro S, Chouinard M et al (2004) Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest 114:1281-1289
37. Watkins SM, Reifsnyder PR, Pan HJ, German JB, Leiter EH (2002) Lipid metabolome-wide effects of the PPARgamma agonist rosiglitazone. J Lipid Res 43:1809-1817
38. Orci L, Cook WS, Ravazzola M et al (2004) Rapid transformation of white adipocytes into fat-oxidizing machines. Proc Natl Acad Sci U S A 101:2058-2063
39. Wang MY, Lee Y, Unger RH (1999) Novel form of lipolysis induced by leptin. J Biol Chem 274:17541-17544
40. Himms-Hagen J, Melnyk A, Zingaretti MC, Ceresi E, Barbatelli G, Cinti S (2000) Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol 279:C670-C681
41. Cabrero A, Alegret M, Sanchez RM, Adzet T, Laguna JC, Vazquez M (2001) Bezafibrate reduces mRNA levels of adipocyte markers and increases fatty acid oxidation in primary culture of adipocytes. Diabetes 50:1883-1890
42. Brown NF, Hill JK, Esser V et al (1997) Mouse white adipocytes and 3T3-L1 cells display an anomalous pattern of carnitine palmitoyltransferase (CPT) I isoform expression during differentiation. Inter-tissue and inter-species expression of CPT I and CPT II enzymes. Biochem J 327:225-231
43. Martin BR, Denton RM (1970) The intracellular localization of enzymes in white-adipose-tissue fat-cells and permeability properties of fat-cell mitochondria. Biochem J 117:861-877
44. Ruderman NB, Saha AK, Kraegen EW (2003) Minireview: malonyl CoA, AMP-activated protein kinase, and adiposity. Endocrinology 144:5166-5171
45. Semple RK, Crowley VC, Sewter CP et al (2004) Expression of the thermogenic nuclear hormone receptor coactivator PGC-lalpha is reduced in the adipose tissue of morbidly obese subjects. Int J Obes Relat Metab Disord 28:176-179
46. Yang X, Enerback S, Smith U (2003) Reduced expression of FOXC2 and brown adipogenic genes in human subjects with insulin resistance. Obes Res 11:1182-1191
47. Esterbauer H, Oberkofler H, Linnemayr V et al (2002) Peroxisome proliferator-activated receptor-gamma coactivator-1 gene locus: associations with obesity indices in middle-aged women. Diabetes 51:1281-1286
48. Oberkofler H, Linnemayr V, Weitgasser R et al (2004) Complex haplotypes of the PGC-1alpha gene are associated with carbohydrate metabolism and type 2 diabetes. Diabetes 53:1385-1393
49. Bottcher H, Furst P (1997) Decreased white fat cell thermogenesis in obese individuals. Int J Obes 21:439-444