The Journal of Nutritional Biochemistry
Volume 21, Issue 4 , Pages 317-324 , April 2010

Docosahexaenoic acid regulates serum amyloid A protein to promote lipolysis through down regulation of perilipin

  • Ya C. Wang

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
    • These authors contributed equally to this work.
  • ,
  • Wen H. Kuo

      Affiliations

    • Department of Surgery, National Taiwan University Hospital and College of Medicine, Taipei 100, Taiwan
    • These authors contributed equally to this work.
  • ,
  • Ching Y. Chen

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
  • ,
  • Hsin Y. Lin

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
  • ,
  • Hsin T. Wu

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
  • ,
  • Bing H. Liu

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
  • ,
  • Chia H. Chen

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
  • ,
  • Harry J. Mersmann

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
    • Visiting Professor at National Taiwan University.
  • ,
  • King J. Chang

      Affiliations

    • Department of Surgery, National Taiwan University Hospital and College of Medicine, Taipei 100, Taiwan
    • Corresponding Author InformationCorresponding authors. Tel.: +886 2 33664175; fax: +886 2 27324070.
  • ,
  • Shih T. Ding

      Affiliations

    • Department of Animal Science and Technology/Institute of Biotechnology, National Taiwan University, Taipei 106, Taiwan
    • Corresponding Author InformationCorresponding authors. Tel.: +886 2 33664175; fax: +886 2 27324070.

Received 20 September 2008 ,Revised 31 December 2008 ,Accepted 6 January 2009.

References 

  1. Yang RZ, Lee MJ, Hu H, Pollin TI, Ryan AS, Nicklas BJ, et al. Acute-phase serum amyloid A: an inflammatory adipokine and potential link between obesity and its metabolic complications. PLoS Med. 2006;3:e287
  2. Stulnig TM. Immunomodulation by polyunsaturated fatty acids: mechanisms and effects. Int Arch Allergy Immunol. 2003;132:310–321
  3. Suresh Y, Das UN. Long-chain polyunsaturated fatty acids and chemically induced diabetes mellitus. Effect of omega-3 fatty acids. Nutrition. 2003;19:213–228
  4. Narayanan BA, Narayanan NK, Reddy BS. Docosahexaenoic acid regulated genes and transcription factors inducing apoptosis in human colon cancer cells. Int J Oncol. 2001;19:1255–1262
  5. Rojas CV, Martinez JI, Flores I, Hoffman DR, Uauy R. Gene expression analysis in human fetal retinal explants treated with docosahexaenoic acid. Invest Ophthalmol Vis Sci. 2003;44:3170–3177
  6. Duplus E, Glorian M, Forest C. Fatty acid regulation of gene transcription. J Biol Chem. 2000;275:30749–30752
  7. Hsu JM, Ding ST. Effect of polyunsaturated fatty acids on the expression of transcription factor adipocyte determination and differentiation-dependent factor 1 and of lipogenic and fatty acid oxidation enzymes in porcine differentiating adipocytes. Br J Nutr. 2003;90:507–513
  8. Hsu JM, Wang PH, Liu BH, Ding ST. The effect of dietary docosahexaenoic acid on the expression of porcine lipid metabolism-related genes. J Anim Sci. 2004;82:683–689
  9. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 1997;89:331–340
  10. Gomez-Ambrosi J, Salvador J, Rotellar F, Silva C, Catalan V, Rodriguez A, et al. Increased serum amyloid A concentrations in morbid obesity decrease after gastric bypass. Obes Surg. 2006;16:262–269
  11. Jernas M, Palming J, Sjoholm K, Jennische E, Svensson PA, Gabrielsson BG, et al. Separation of human adipocytes by size: hypertrophic fat cells display distinct gene expression. Faseb J. 2006;20:1540–1542
  12. Poitou C, Viguerie N, Cancello R, De Matteis R, Cinti S, Stich V, et al. Serum amyloid A: production by human white adipocyte and regulation by obesity and nutrition. Diabetologia. 2005;48:519–528
  13. Urieli-Shoval S, Cohen P, Eisenberg S, Matzner Y. Widespread expression of serum amyloid A in histologically normal human tissues. Predominant localization to the epithelium. J Histochem Cytochem. 1998;46:1377–1384
  14. Chen CH, Wang PH, Liu BH, Mersmann HJ, Ding ST. Serum amyloid A protein regulates the expression of porcine genes related to lipid metabolism. J Nutr. 2008;138:674–679
  15. Festuccia WT, Laplante M, Berthiaume M, Gelinas Y, Deshaies Y. PPARgamma agonism increases rat adipose tissue lipolysis, expression of glyceride lipases, and the response of lipolysis to hormonal control. Diabetologia. 2006;49:2427–2436
  16. Liu BH, Kuo CF, Wang YC, Ding ST. Effect of docosahexaenoic acid and arachidonic acid on the expression of adipocyte determination and differentiation-dependent factor 1 in differentiating porcine adipocytes. J Anim Sci. 2005;83:1516–1525
  17. Pawlosky RJ, Hibbeln JR, Herion D, Kleiner DE, Salem N. Compartmental analysis of plasma and liver n-3 essential fatty acids in alcohol-dependent men during withdrawal. J Lipid Res. 2008;
  18. Attar-Bashi NM, Weisinger RS, Begg DP, Li D, Sinclair AJ. Failure of conjugated linoleic acid supplementation to enhance biosynthesis of docosahexaenoic acid from alpha-linolenic acid in healthy human volunteers. Prostaglandins Leukot Essent Fatty Acids. 2007;76:121–130
  19. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45
  20. Chang WJ, Chen CH, Cheng WTK, Ding ST. The effects of dietary docosahexaenoic acid enrichment on the expression of porcine genes. Asian-Aust J Anim Sci. 2007;20:768–774
  21. Seo JB, Moon HM, Kim WS, Lee YS, Jeong HW, Yoo EJ, et al. Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol. 2004;24:3430–3444
  22. Diraison F, Parton L, Ferre P, Foufelle F, Briscoe CP, Leclerc I, et al. Over-expression of sterol-regulatory-element-binding protein-1c (SREBP1c) in rat pancreatic islets induces lipogenesis and decreases glucose-stimulated insulin release: modulation by 5-aminoimidazole-4-carboxamide ribonucleoside (AICAR). Biochem J. 2004;378:769–778
  23. Knight BL, Hebbachi A, Hauton D, Brown AM, Wiggins D, Patel DD, et al. A role for PPARalpha in the control of SREBP activity and lipid synthesis in the liver. Biochem J. 2005;389:413–421
  24. Marcus SL, Miyata KS, Zhang B, Subramani S, Rachubinski RA, Capone JP. Diverse peroxisome proliferator-activated receptors bind to the peroxisome proliferator-responsive elements of the rat hydratase/dehydrogenase and fatty acyl-CoA oxidase genes but differentially induce expression. Proc Natl Acad Sci U S A. 1993;90:5723–5727
  25. Poirier H, Niot I, Monnot MC, Braissant O, Meunier-Durmort C, Costet P, et al. Differential involvement of peroxisome-proliferator-activated receptors alpha and delta in fibrate and fatty-acid-mediated inductions of the gene encoding liver fatty-acid-binding protein in the liver and the small intestine. Biochem J. 2001;355:481–488
  26. Tecles F, Fuentes P, Martinez Subiela S, Parra MD, Munoz A, Ceron JJ. Analytical validation of commercially available methods for acute phase proteins quantification in pigs. Res Vet Sci. 2007;83:133–139
  27. Parra MD, Fuentes P, Tecles F, Martinez-Subiela S, Martinez JS, Munoz A, et al. Porcine acute phase protein concentrations in different diseases in field conditions. J Vet Med B Infect Dis Vet Public Health. 2006;53:488–493
  28. Stauffer F, Petrow EP, Burgmann H, Graninger W, Georgopoulos A. Release of TNF alpha and IL6 from human monocytes infected with Mycobacterium kansasii: a comparison to Mycobacterium avium. Infection. 1994;22:326–329
  29. Ruzek MC, Miller AH, Opal SM, Pearce BD, Biron CA. Characterization of early cytokine responses and an interleukin (IL)-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J Exp Med. 1997;185:1185–1192
  30. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98:1154–1162
  31. Schindler R, Mancilla J, Endres S, Ghorbani R, Clark SC, Dinarello CA. Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononuclear cells: IL-6 suppresses IL-1 and TNF. Blood. 1990;75:40–47
  32. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood. 1994;83:113–118
  33. Bethin KE, Vogt SK, Muglia LJ. Interleukin-6 is an essential, corticotropin-releasing hormone-independent stimulator of the adrenal axis during immune system activation. Proc Natl Acad Sci U S A. 2000;97:9317–9322
  34. Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab. 2003;285:E433–E437
  35. Xing Z, Gauldie J, Cox G, Baumann H, Jordana M, Lei XF, et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest. 1998;101:311–320
  36. Verlengia R, Gorjao R, Kanunfre CC, Bordin S, Martins De Lima T, Martins EF, et al. Comparative effects of eicosapentaenoic acid and docosahexaenoic acid on proliferation, cytokine production, and pleiotropic gene expression in Jurkat cells. J Nutr Biochem. 2004;15:657–665
  37. Fritsche KL, Anderson M, Feng C. Consumption of eicosapentaenoic acid and docosahexaenoic acid impair murine interleukin-12 and interferon-gamma production in vivo. J Infect Dis. 2000;182(Suppl 1):S54–S61
  38. Schadinger SE, Bucher NL, Schreiber BM, Farmer SR. PPARgamma2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. Am J Physiol Endocrinol Metab. 2005;288:E1195–E1205
  39. Ding ST, McNeel RL, Mersmann HJ. Expression of porcine adipocyte transcripts: tissue distribution and differentiation in vitro and in vivo. Comp Biochem Physiol B Biochem Mol Biol. 1999;123:307–318
  40. Holm C. Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans. 2003;31:1120–1124
  41. Path G, Bornstein SR, Gurniak M, Chrousos GP, Scherbaum WA, Hauner H. Human breast adipocytes express interleukin-6 (IL-6) and its receptor system: increased IL-6 production by beta-adrenergic activation and effects of IL-6 on adipocyte function. J Clin Endocrinol Metab. 2001;86:2281–2288
  42. van Hall G, Steensberg A, Sacchetti M, Fischer C, Keller C, Schjerling P, et al. Interleukin-6 stimulates lipolysis and fat oxidation in humans. J Clin Endocrinol Metab. 2003;88:3005–3010
  43. Rahn Landstrom T, Mei J, Karlsson M, Manganiello V, Degerman E. Down-regulation of cyclic-nucleotide phosphodiesterase 3B in 3T3-L1 adipocytes induced by tumour necrosis factor alpha and cAMP. Biochem J. 2000;346(Pt 2):337–343
  44. Ryden M, Arvidsson E, Blomqvist L, Perbeck L, Dicker A, Arner P. Targets for TNF-alpha-induced lipolysis in human adipocytes. Biochem Biophys Res Commun. 2004;318:168–175
  45. Fricke K, Heitland A, Maronde E. Cooperative activation of lipolysis by protein kinase A and protein kinase C pathways in 3T3-L1 adipocytes. Endocrinology. 2004;145:4940–4947
  46. Dalen KT, Schoonjans K, Ulven SM, Weedon-Fekjaer MS, Bentzen TG, Koutnikova H, et al. Adipose tissue expression of the lipid droplet-associating proteins S3-12 and perilipin is controlled by peroxisome proliferator-activated receptor-gamma. Diabetes. 2004;53:1243–1252
  47. Gorjao R, Verlengia R, Lima TM, Soriano FG, Boaventura MF, Kanunfre CC, et al. Effect of docosahexaenoic acid-rich fish oil supplementation on human leukocyte function. Clin Nutr. 2006;25:923–938
  48. Tappia PS, Man WJ, Grimble RF. Influence of unsaturated fatty acids on the production of tumour necrosis factor and interleukin-6 by rat peritoneal macrophages. Mol Cell Biochem. 1995;143:89–98
  49. Bradley RL, Fisher FM, Maratos-Flier E. Dietary fatty acids differentially regulate production of TNF-alpha and IL-10 by murine 3T3-L1 adipocytes. Obesity (Silver Spring). 2008;
  50. Trebble T, Arden NK, Stroud MA, Wootton SA, Burdge GC, Miles EA, et al. Inhibition of tumour necrosis factor-alpha and interleukin 6 production by mononuclear cells following dietary fish-oil supplementation in healthy men and response to antioxidant co-supplementation. Br J Nutr. 2003;90:405–412
  51. Delarue J, LeFoll C, Corporeau C, Lucas D. N-3 long chain polyunsaturated fatty acids: a nutritional tool to prevent insulin resistance associated to type 2 diabetes and obesity?. Reprod Nutr Dev. 2004;44:289–299
  52. Diep QN, Touyz RM, Schiffrin EL. Docosahexaenoic acid, a peroxisome proliferator-activated receptor-alpha ligand, induces apoptosis in vascular smooth muscle cells by stimulation of p38 mitogen-activated protein kinase. Hypertension. 2000;36:851–855
  53. Larter CZ, Yeh MM, Cheng J, Williams J, Brown S, dela Pena A, et al. Activation of peroxisome proliferator-activated receptor alpha by dietary fish oil attenuates steatosis, but does not prevent experimental steatohepatitis because of hepatic lipoperoxide accumulation. J Gastroenterol Hepatol. 2008;23:267–275
  54. Li JJ, Huang CJ, Xie D. Anti-obesity effects of conjugated linoleic acid, docosahexaenoic acid, and eicosapentaenoic acid. Mol Nutr Food Res. 2008;52:631–645
  55. LaRosa PC, Miner J, Xia Y, Zhou Y, Kachman S, Fromm ME. Trans-10, cis-12 conjugated linoleic acid causes inflammation and delipidation of white adipose tissue in mice: a microarray and histological analysis. Physiol Genomics. 2006;27:282–294
  56. Park Y, Storkson JM, Albright KJ, Liu W, Pariza MW. Evidence that the trans-10,cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids. 1999;34:235–241
  57. House RL, Cassady JP, Eisen EJ, McIntosh MK, Odle J. Conjugated linoleic acid evokes de-lipidation through the regulation of genes controlling lipid metabolism in adipose and liver tissue. Obes Rev. 2005;6:247–258
  58. Kunesova M, Braunerova R, Hlavaty P, Tvrzicka E, Stankova B, Skrha J, et al. The influence of n-3 polyunsaturated fatty acids and very low calorie diet during a short-term weight reducing regimen on weight loss and serum fatty acid composition in severely obese women. Physiol Res. 2006;55:63–72
  59. Thorsdottir I, Tomasson H, Gunnarsdottir I, Gisladottir E, Kiely M, Parra MD, et al. Randomized trial of weight-loss-diets for young adults varying in fish and fish oil content. Int J Obes (Lond). 2007;31:1560–1566

 The project was funded in part by the National Science Council in Taiwan.

PII: S0955-2863(09)00012-6

doi: 10.1016/j.jnutbio.2009.01.004

The Journal of Nutritional Biochemistry
Volume 21, Issue 4 , Pages 317-324 , April 2010