Dietary linoleic acid and α-linolenic acid differentially affect renal oxylipins and phospholipid fatty acids in diet-induced obese rats

Journal of Nutrition

Volumn 143, Issue 9, 2013, Pages 1421-1431

  Caligiuri, Stephanie P B ^a,b   Love, Karin ^a,b   Winter, Tanja ^a,b   Gauthier, Joy ^a,b   Taylor, Carla G ^a,b   Blydt Hansen, Tom ^a   Zahradka, Peter ^a,b   Aukema, Harold M ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b ST BONIFACE GENERAL HOSPITAL RESEARCH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CANOLA OIL; LARD; LINOLEIC ACID; LINOLENIC ACID; LINSEED OIL; LIPOXYGENASE; OXYLIPIN; POLYUNSATURATED FATTY ACID; SAFFLOWER OIL; SOYBEAN OIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; FAT INTAKE; GLOMERULOMEGALY; GLOMERULOPATHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KIDNEY DISEASE; LIPID DIET; LIPIDOMICS; LOW FAT DIET; MALE; NONHUMAN; OBESITY; RAT; RENAL PROTECTION; TANDEM MASS SPECTROMETRY; TISSUE LEVEL;

ALPHA-LINOLENIC ACID; ANIMALS; DIET; DIETARY FATS; DIETARY FATS, UNSATURATED; FATTY ACIDS, MONOUNSATURATED; KIDNEY; KIDNEY DISEASES; LINOLEIC ACID; MALE; OBESITY; OXYLIPINS; PHOSPHOLIPIDS; RATS; RATS, SPRAGUE-DAWLEY; SAFFLOWER OIL; SOYBEAN OIL;

EID: 84883292084     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.113.177360     Document Type: Article

References (58)

1. Hammond VJ, O'Donnell VB. Esterified eicosanoids: generation, characterization and function. Biochim Biophys Acta. 2012;1818: 2403-12.
2. Buczynski MW, Dumlao DS, Dennis EA. Proteomics: an integrated omics analysis of eicosanoid biology. J Lipid Res. 2009;50:1015-38.
3. Serhan CN, Krishnamoorthy S, Recchiuti A, Chiang N. Novel antiinflammatory- pro-resolving mediators and their receptors. Curr Top Med Chem. 2011;11:629-47.
4. Psychogios N, Hau DD, Peng J, Guo AC, Mandal R, Bouatra S, Sinelnikov I, Krishnamurthy R, Eisner R, Gautum B, et al. The human serum metabolome. PLoS ONE. 2011;6:e16957.
5. Honn KV, Nelson KK, Renaud C, Bazaz R, Diglio CA, Timar J. Fatty acid modulation of tumor cell adhesion to microvessel endothelium and experimental metastasis. Prostaglandins. 1992;44:413-29.
6. Ziboh VA, Miller C, Cho Y. Significance of lipoxygenase-derived monohydroxy fatty acids in cutaneous biology. Prostaglandins Other Lipid Mediat. 2000;63:3-13.
7. Camp RD, Fincham N. Inhibition of ionophore-stimulated leukotriene B4 production in human leucocytes by monohydroxy fatty acids. Br J Pharmacol. 1985;85:837-41.
8. Kaduce TL, Figard P, Leifur R, Spector A. Formation of 9-hydroxyoctadecadienoic acid from linoleic acid in endothelial cells. J Biol Chem. 1989;264:6823-30.
9. Yamaja Setty BN, Berger M, Stuart MJ. 13-Hydroxyoctadeca-9,11- dienoic acid (13-HODE) inhibits thromboxane A2 synthesis, and stimulates 12-HETE production in human platelets. Biochem Biophys Res Commun. 1987;148:528-33.
10. Kämmerer I, Ringseis R, Biemann R, Wen G, Eder K. 13-Hydroxy linoleic acid increases expression of the cholesterol transporters ABCA1, ABCG1 and SR-BI and stimulates apoA-I-dependent cholesterol efflux in RAW264.7 macrophages. Lipids Health Dis. 2011;10: 222.
11. Kim YI, Hirai S, Takahashi H, Goto T, Ohyane C, Tsugane T, Konishi C, Fujii T, Inai S. 9-Oxo-10(E),12(E)-octadecadienoic acid derived from tomato is a potent PPAR alpha agonist to decrease triglyceride accumulation in mouse primary hepatocytes. Mol Nutr Food Res. 2011; 55:585-93.
12. Horie M, Fukui H, Endoh S, Maru J, Miyauchi A, Shichiri M, Fujita K, Niki E, Hagihara Y, Yoshida Y, et al. Comparison of acute oxidative stress on rat lung induced by nano and fine-scale, soluble and insoluble metal oxide particles: NiO and TiO(2). Inhal Toxicol. 2012;24:391-400.
13. Spiteller G. Linoleic acid peroxidation-the dominant lipid peroxidation process in low density lipoprotein-and its relationship to chronic diseases. Chem Phys Lipids. 1998;95:105-62.
14. Schulze-Tanzil G, de Souza P, Behnke B, Klingelhoefer S, Scheid A, Shakibaei M. Effects of the antirheumatic remedy hox alpha-a new stinging nettle leaf extract-on matrix metalloproteinases in human chondrocytes in vitro. Histol Histopathol. 2002;17:477-85.
15. Keenan AH, Pedersen TL, Fillaus K, Larson MK, Shearer GC, Newman JW. Basal omega-3 fatty acid status affects fatty acid and oxylipin responses to high-dose n3-HUFA in healthy volunteers. J Lipid Res. 2012;53:1662-9.
16. Calder PC. Omega-3 fatty acids and inflammatory processes. Nutrients. 2010;2:355-74.
17. Serhan CN, Petasis NA. Resolvins and protectins in inflammation resolution. Chem Rev. 2011;111:5922-43.
18. Ramsden CE, Ringel A, Feldstein AE, Taha AY, Macintosh BA, Hibbeln JR, Majchrzak-Hong SF, Faurot KR, Rapoport SI, Cheon Y, et al. Lowering dietary linoleic acid reduces bioactive oxidized linoleic acid metabolites in humans. Prostaglandins Leukot Essent Fatty Acids. 2012;87:135-41.
19. Blank C, Neumann MA, Makrides M, Gibson RA. Optimizing DHA levels in piglets by lowering the linoleic acid to alpha-linolenic acid ratio. J Lipid Res. 2002;43:1537-43.
20. Hastings N, Agaba MK, Tocher DR, Zheng X, Dickson CA, Dick JR, Teale AJ. Molecular cloning and functional characterization of fatty acyl desaturase and elongase cDNAs involved in the production of eicosapentaenoic and docosahexaenoic acids from alpha-linolenic acid in Atlantic salmon (Salmo salar). Mar Biotechnol (NY). 2004;6:463-74.
21. Toledo L, Masgrau L, Lluch JM, Gonzalez-Lafont A. Substrate binding to mammalian 15-lipoxygenase. J Comput Aided Mol Des. 2011;25: 825-35.
22. Imig JD, Zhao X, Dey A, Shaw M. CYP450, COX-2 and obesity related renal damage. Toxicol Mech Methods. 2005;15:125-36.
23. Wu Y, Liu Z, Xiang Z, Zeng C, Chen Z, Ma X, Li L. Obesity-related glomerulopathy: insights from gene expression profiles of the glomeruli derived from renal biopsy samples. Endocrinology. 2006;147:44-50.
24. Chagnac A, Weinstein T, Herman M, Hirsh J, Gafter U, Ori Y. The effects of weight loss on renal function in patients with severe obesity. J Am Soc Nephrol. 2003;14:1480-6.
25. Kambham N, Markowitz GS, Valeri AM, Lin J, D'Agati VD. Obesityrelated glomerulopathy: an emerging epidemic. Kidney Int. 2001;59: 1498-509.
26. Reeves PG. Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr. 1997;127:838S-41S.
27. Deems R, Buczynski MW, Bowers-Gentry R, Harkewicz R, Dennis EA. Detection and quantitation of eicosanoids via high performance liquid chromatography-electrospray ionization-mass spectrometry. Methods Enzymol. 2007;432:59-82.
28. Hall LM, Murphy RC. Electrospray mass spectrometric analysis of 5-hydroperoxy and 5-hydroxyeicosatetraenoic acids generated by lipid peroxidation of red blood cell ghost phospholipids. J Am Soc Mass Spectrom. 1998;9:527-32.
29. Sankaran D, Lu J, Bankovic-Calic N, Ogborn MR, Aukema HM. Modulation of renal injury in pcy mice by dietary fat containing n3 fatty acids depends on the level and type of fat. Lipids. 2004;39:207-14.
30. Warford-Woolgar L, Peng CY, Shuhyta J, Wakefield A, Sankaran D, Ogborn M, Aukema HM. Selectivity of cyclooxygenase isoform activity and prostanoid production in normal and diseased Han:SPRD-cy rat kidneys. Am J Physiol Renal Physiol. 2006;290:F897-904.
31. Sankaran D, Bankovic-Calic N, Ogborn MR, Crow G, Aukema HM. Selective COX-2 inhibition markedly slows disease progression and attenuates altered prostanoid production in Han:SPRD-cy rats with inherited kidney disease. Am J Physiol Renal Physiol. 2007;293:F821-30.
32. Weibel ER. Numerical density: shape and size of particles. In: Weibel ER, editor. Stereological methods. 2nd ed. London: Academic Press; 1980. p. 149-52.
33. Sankaran D, Bankovic-Calic N, Peng CY, Ogborn MR, Aukema HM. Dietary flax oil during pregnancy and lactation retards disease progression in rat offspring with inherited kidney disease. Pediatr Res. 2006;60:729-33.
34. Galliard T, Phillips DR. Lipoxygenase from potato tubers: partial purification and properties of an enzyme that specifically oxygenates the 9-position of linoleic acid. Biochem J. 1971;124:431-8.
35. Ghosh J, Myers CE. Arachidonic acid stimulates prostate cancer cell growth: critical role of 5-lipoxygenase. Biochem Biophys Res Commun. 1997;235:418-23.
36. Laegreid WW, Taylor SM, Silflow RM, Straub KM, Breeze RG, Liggitt HD, Leid RW. Production of lipoxygenase metabolites of eicosapentaenoic acid by bovine alveolar macrophages in vitro. Inflammation. 1988;12:503-14.
37. Lee TH, Mencia-Huerta JM, Shih C, Corey EJ, Lewis RA, Austen KF. Effects of exogenous arachidonic, eicosapentaenoic, and docosahexaenoic acids on the generation of 5-lipoxygenase pathway products by ionophore-activated human neutrophils. J Clin Invest. 1984;74: 1922-33.
38. Collins JF, Hu Z, Ranganathan PN, Feng D, Garrick LM, Garrick MD, Browne RW. Induction of arachidonate 12-lipoxygenase (Alox15) in intestine of iron-deficient rats correlates with the production of biologically active lipid mediators. Am J Physiol Gastrointest Liver Physiol. 2008;294:G948-62.
39. Fogh K, Kragballe K. Eicosanoids in inflammatory skin diseases. Prostaglandins Other Lipid Mediat. 2000;63:43-54.
40. Ziboh VA, Miller CC, Cho C. Metabolism of polyunsaturated fatty acids by skin epidermal enzymes: generation of antiinflammatory and antiproliferative metabolites. Am J Clin Nutr. 2000;71:361S-6S.
41. Feldstein AE, Lopez R, Tamimi TA, Yerian L, Chung YM, Berk M, Zhang R, McIntyre TM, Hazen SL. Mass spectrometric profiling of oxidized lipid products in human nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. J Lipid Res. 2010;51:3046-54.
42. Totani Y, Saito Y, Ishizaki T, Sasaki F, Ameshima S, Miyamori I. Leukotoxin and its diol induce neutrophil chemotaxis through signal transduction different from that of fMLP. Eur Respir J. 2000;15:75-9.
43. Moran JH, Weise R, Schnellmann RG, Freeman JP, Grant DF. Cytotoxicity of linoleic acid diols to renal proximal tubular cells. Toxicol Appl Pharmacol. 1997;146:53-9.
44. Dreisbach AW, Rice JC, Japa S, Newman JW, Sigel A, Gill RS, Hess AE, Cemo AC, Fonseca JP, Hammock BD, et al. Salt loading increases urinary excretion of linoleic acid diols and triols in healthy human subjects. Hypertension. 2008;51:755-61.
45. Thrailkill KM, Clay Bunn R, Fowlkes JL. Matrix metalloproteinases: their potential role in the pathogenesis of diabetic nephropathy. Endocrine. 2009;35:1-10.
46. Zeisberg M, Khurana M, Rao VH, Cosgrove D, Rougier JP, Werner MC, Shield CF III, Werb Z, Kalluri R. Stage-specific action of matrix metalloproteinases influences progressive hereditary kidney disease. PLoS Med. 2006;3:e100.
47. Wakefield AP, Ogborn MR, Ibrahim N, Aukema HM. A dietary conjugated linoleic acid treatment that slows renal disease progression alters renal cyclooxygenase-2-derived prostanoids in the Han:SPRD-cy rat. J Nutr Biochem. 2012;23:908-14.
48. Baer PG, McGiff JC. Comparison of effects of prostaglandins E2 and I2 on rat renal vascular resistance. Eur J Pharmacol. 1979;54:359-63.
49. Ogletree ML. Overview of physiological and pathophysiological effects of thromboxane A2. Fed Proc. 1987;46:133-8.
50. Konkel A, Schunck WH. Role of cytochrome P450 enzymes in the bioactivation of polyunsaturated fatty acids. Biochim Biophys Acta. 2011;1814:210-22.
51. Brenna JT. Efficiency of conversion of alpha-linolenic acid to long chain n3 fatty acids in man. Curr Opin Clin Nutr Metab Care. 2002;5: 127-32.
52. Hassid A, Konieczkowski M, Dunn MJ. Prostaglandin synthesis in isolated rat kidney glomeruli. Proc Natl Acad Sci USA. 1979;76: 1155-9.
53. Jim K, Hassid A, Sun F, Dunn MJ. Lipoxygenase activity in rat kidney glomeruli, glomerular epithelial cells, and cortical tubules. J Biol Chem. 1982;257:10294-9.
54. Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ. The effect on human tumor necrosis factor alpha and interleukin 1 beta production of diets enriched in n3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr. 1996;63:116-22.
55. Trebble TM, Wootton SA, Miles EA, Mullee M, Arden NK, Ballinger AB, Stroud MA, Burdge GC, Calder PC. Prostaglandin E2 production and T cell function after fish-oil supplementation: response to antioxidant cosupplementation. Am J Clin Nutr. 2003;78:376-82.
56. Neilson AP, Ren J, Hong YH, Sen A, Smith WL, Brenner DE, Djuric Z. Effect of fish oil on levels of R-and S-enantiomers of 5-, 12-, and 15-hydroxyeicosatetraenoic acids in mouse colonic mucosa. Nutr Cancer. 2012;64:163-72.
57. Broughton KS, Wade JW. Total fat and (n3):(n6) fat ratios influence eicosanoid production in mice. J Nutr. 2002;132:88-94.
58. Rett BS, Whelan J. Increasing dietary linoleic acid does not increase tissue arachidonic acid content in adults consuming Western-type diets: a systematic review. Nutr Metab (Lond). 2011;8:1-15.