Lipids

, Volume 47, Issue 4, pp 425–434 | Cite as

Plasma Phospholipid Fatty Acid and Ex Vivo Neutrophil Responses are Differentially Altered in Dogs Fed Fish- and Linseed-Oil Containing Diets at the Same n-6:n-3 Fatty Acid Ratio

  • Mark K. Waldron
  • Steven S. Hannah
  • John E. Bauer
Original Article

Abstract

The effect of diets containing either 18-carbon n-3 fatty acids (FA) or 20/22-carbon n-3 FA on canine plasma and neutrophil membrane fatty acid composition, superoxide and leukotriene B4 and B5 production when fed at the same n-6:n-3 fatty acid ratio was investigated. Four groups of ten dogs each were fed a low fat basal diet supplemented with safflower oil (SFO), beef tallow (BTO), linseed oil (LSO), or Menhaden fish oil (MHO) for 28 days. Dietary fat provided 40.8% of energy and the n-6:n-3 of the diets were ~100:1, 9.7:1, 0.38:1, and 0.34:1 for the SFO, BTO, LSO and MHO groups, respectively. The MHO and LSO groups had increased incorporation of EPA and DPA in both the plasma and neutrophil membranes compared to the BTO and SFO groups. DHA was observed in the MHO but not in the LSO group. Neutrophils from the MHO diet fed dogs had less LTB4 and greater LTB5 than the other three groups. The LSO group also showed a reduction in LTB4 and greater LTB5 production compared to the SFO and BTO groups. Both LSO and MHO groups had lower superoxide production compared to the SFO and BTO groups. Diets containing 18 or 20/22 carbon n-3 FA fed at the same n-6:n-3 resulted in differential incorporation of long chain n-3 FA into neutrophil membranes. Thus, fatty acid type and chain length individually affect neutrophil membrane structure and function and these effects exist independent of dietary total n-6:total n-3 FA ratios.

Keywords

Neutrophils Canine n-3 fatty acids Leukotrienes Superoxide anion 

Abbreviations

AAFCO

Association of American Feed Control Officials

ALA

Alpha-linolenic acid

ARA

Arachidonic acid

BTO

Beef tallow enriched diet

DPAn-3

Docosapentaenoic acid n-3

DHA

Docosahexaenoic acid

EPA

Eicosapentaenoic acid

FA

Fatty acids

FAME

Fatty acid methyl ester(s)

LNA

Linoleic acid

LSO

Linseed oil enriched diet

LTB4

Leukotriene B4

LTB5

Leukotriene B5

MHO

Menhaden oil enriched diet

PMA

Phorbol myristic acetate

SAF

Safflower oil enriched diet

SOD

Super oxide dismutase

TBHQ

tert-butylhydroquinone

tot(n-6):tot(n-3)

Total n-6 to total n-3 fatty acid ratio

References

  1. 1.
    Weiss SJ (1984) Tissue destruction by neutrophils. New Engl J Med 320:365–376Google Scholar
  2. 2.
    Smith JA (1984) Neutrophils, host defense, and inflammation: a double edge sword. J Leukocyte Biol 56:672–686Google Scholar
  3. 3.
    Chanock SJ, el Benna J, Smith RM, Babior BM (1994) The respiratory burst oxidase. J Biol Chem 269:24519–24522PubMedGoogle Scholar
  4. 4.
    Ricevetti G, Mazzone A, Pasotti D, de Servi S, Specchi G (1991) Roles of granulocytes in endothelial injury in coronary heart disease in humans. Atherosclerosis 91:1–14CrossRefGoogle Scholar
  5. 5.
    Wang C, Harris WS, Chung MM, Lichtenstein AH, Balk EM, Kupelnick B, Jordan HS, Lau J (2006) Fatty acids from fish or fish-oil supplements, but not linolenic acid, benefit cardiovascular disease outcomes in primary and secondary prevention studies; asystematic review. Am J Clin Nutr 83:5–17Google Scholar
  6. 6.
    James MJ, Cleland LG (1997) Dietary n-3 FA and therapy for rheumatoid arthritis. Semin Arthritis Rheum 27:85–97PubMedCrossRefGoogle Scholar
  7. 7.
    Appel LJ, Miller ER, Seidler AJ, Whelton PK (1993) Does supplementation of diet with “fish oil” reduce blood pressure? A meta-analysis of controlled clinical trials. Arch Intern Med 153:1429–1438PubMedCrossRefGoogle Scholar
  8. 8.
    De Caterina R, Caprioli R, Giannessi D, Sicari R, Galli C, Lazzerini G, Bernini W, Carr L, Rindi P (1993) n-3 FA reduce proteinuria in patients with chronic glomerular disease. Kidney Int 44:843–850PubMedCrossRefGoogle Scholar
  9. 9.
    Calder PC (2002) Dietary modification of inflammation with lipids. Proc Nutr Soc 61:345–358PubMedCrossRefGoogle Scholar
  10. 10.
    Schwerbrock NM, Karlsson EA, Shi Q, Sheridan PA, Beck MA (2009) Fish oil-fed mice have impaired resistance to influenza infection. J Nutr 139:1588–1594PubMedCrossRefGoogle Scholar
  11. 11.
    Tisset H, Pierre M, Desseyn J-L, Guery B, Beermann C, Galabert C, Gottrand F, Husson M-O (2009) Dietary (n-3) polyunsaturated fatty acids affect the kinetics of anti-inflammatory responses in mice with Pseudomonas aeruginosa lung infection. J Nutr 139:82–89Google Scholar
  12. 12.
    Broughton KS, Wadde JW (2002) Total fat and (n-3):(n-6) fat ratios influence eicosanoid production in mice. J Nutr 132:88–94PubMedGoogle Scholar
  13. 13.
    Serhan CN (2005) Novel eicosanoid and docosanoid mediators: resolvins, docosatrienes, and neuroprotectins. Curr Opin Clin Nutr Metab Care 8:115–121PubMedCrossRefGoogle Scholar
  14. 14.
    Healy DA, Wallace FA, Miles EA, Calder PC, Newsholme P (2000) Effect of low-to-moderate amounts of dietary fish oil on neutrophil lipid composition and function. Lipids 35:763–886PubMedCrossRefGoogle Scholar
  15. 15.
    von Schacky C, Fisher S, Weber PC (1985) Long-term effects of marine ω-3 fatty acids upon plasma and cellular lipids, platelet function, and eicosanoids formation in humans. J Clin Invest 76:1626–1631CrossRefGoogle Scholar
  16. 16.
    Prisco D, Filippini M, Francalanci I, Paniccia R, Gensine GF, Abbate K, Neri Serneri GG (1996) Effect of n-3 polyunsaturated fatty acid intake on phospholipid fatty acid composition in plasma and erythrocytes. Am J Clin Nutr. 63:925–932PubMedGoogle Scholar
  17. 17.
    Fisher M, Upchurch KS, Levine OPH, Johnson MH, Vaudruil CH, Natale A, Hoogasian JJ (1986) Effects of dietary fish oil supplementation on polymorphonuclear leukocyte inflammatory potential. Inflammation 10:387–392PubMedCrossRefGoogle Scholar
  18. 18.
    Gibney MJ, Hunter B (1992) The effects of short- and long-term supplementation with fish oil on the incorporation of n-3 polyunsaturated fatty acids into cells of the immune system of healthy individuals. Eur J Clin Nutr 47:255–259Google Scholar
  19. 19.
    Terrano T, Seya A, Hirai A, Saito H, Tamura Y, Yoshida S (1987) Effect of oral administration of highly purified eicosapentaenoic acid and docosahexaenoic acid on eicosanoids formation and neutrophil function in healthy subjects. In: Lands WEM (ed) Polyunsaturated fatty acids and eicosanoids. American Oil Chemists Society, Champaign, pp 133–138Google Scholar
  20. 20.
    Sperline RI, Benincaso AI, Knoell CT, Larkin JK, Austen KF, Robinson DR (1993) Dietary n-3 polyunsaturated fatty acids FA inhibit phosphoinositide formation and chemotaxis in neutrophils. J Clin Invest 91:651–660CrossRefGoogle Scholar
  21. 21.
    Luostarinen R, Saldeen T (1996) Dietary fish oil decreases superoxide generation by human neutrophils: Relation to cyclooxygenase pathway and lysosomal enzyme release. Prost Leuk Essen Fatty Acids 55:167–172CrossRefGoogle Scholar
  22. 22.
    Varming K, Schmidt EB, Svaneborg N, Moller JM, Lervang HH, Grunnet N, Jersild C, Dyerberg J (1995) The effect of n-3 fatty acid on neutrophil chemiluminescence. Scand J Clin Lab Invest 55:47–52PubMedCrossRefGoogle Scholar
  23. 23.
    Sperling RI (1991) Effects of dietary fish oil on leukocyte leukotriene production and PAF generation and on neutrophil chemotaxis. World Rev Nutr Diet 66:391–400PubMedGoogle Scholar
  24. 24.
    Charleson S, Evans JF, Leblanc Y, Fitzsimmons BJ, Leveille C, Dupuis P, Ford-Hutchinson AW (1986) Leukotriene B3, leukotriene B4 and leukotriene B5; binding to leukotriene B4 receptor on rat and human leukocyte membranes. Prostaglandins 32:503–516PubMedCrossRefGoogle Scholar
  25. 25.
    Seya A, Terrano T, Tamura Y, Yoshida S (1988) Comparative effect of leukotriene B4 and leukotriene B5 on calcium mobilization in human neutrophils. Prost Leuk Essen Fatty Acids 34:47–50CrossRefGoogle Scholar
  26. 26.
    Lee TH, Sethi T, Crea AA, Peters W, Arm JP, Horton CE, Walpodrt MJ, Supr BW (1988) Characterization of leukotriene B3: Comparison of its biological activities with leukotriene B4 and leukotriene B5 in complement receptor enhancement, lysozyme release and chemotaxis of human neutrophils. Clin Sci 74:467–475PubMedGoogle Scholar
  27. 27.
    Payan DG, Wong MYS, Chernow-Rogan T, Valone FH, Pickett WC, Blake VA, Gold WM, Goetzl EJ (1986) Alteration in human leukocyte function induced by ingestion of eicosapentaenoic acid. J Clin Immunol 6:402–410PubMedCrossRefGoogle Scholar
  28. 28.
    Neuringer M, Anderson GJ, Conner WE (1988) The essentiality of the n-3 fatty acids for the development of the retina and the brain. Annu Rev Nutr 8:517–541PubMedCrossRefGoogle Scholar
  29. 29.
    Lee JL, Fukumoto M, Nishida H, Ikeda I, Sugano M (1989) The interrelated effects of n-6/n-3 and polyunsaturated/saturated ratios of dietary fats on the regulation of lipid metabolism in rats. J Nutr 119:1893–1899PubMedGoogle Scholar
  30. 30.
    Goyens PLL, Spilker ME, Zock PL, Katan MB, Mensink RP (2005) Compartmental modeling to quantify α-linolenic acid conversion after longer term intake of multiple tracer boluses. J Lipid Res 46:1474–1483PubMedCrossRefGoogle Scholar
  31. 31.
    Su HM, Bernardo L, Mirmiran M, Ma XH, Nathanielsz PW, Brenna JT (1999) Dietary 18:3n-3 and 22:6n-3 as sources of 22:6n-3 accretion in neonatal baboon brain and associated organs. Lipids 34:S347–S350PubMedCrossRefGoogle Scholar
  32. 32.
    Brenna JT, Salem N Jr, Sinclair AJ, Cunnane SC, International Society for the Study of Fatty Acids and Lipids, ISSFAL (2009) Alpha-linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prost Leuk Essen Fatty Acids 80:85–91CrossRefGoogle Scholar
  33. 33.
    Ziboh VA, Fletcher MP (1992) Dose-response effects of dietary α-linoleic acid-enriched oils on human polymorphonuclear-neutrophil biosynthesis of leukotriene B4. Am J Clin Nutr 55:39–45PubMedGoogle Scholar
  34. 34.
    Carletto Bellavite P, Guarinin P, Biasi D, Chirumbolo S, Caramaschi P, Bambara LM, Corrocher R (1996) Changes of fatty acid composition and oxidative metabolism of human neutrophils migrating into inflammatory exudates. Inflammation 20:123–127PubMedCrossRefGoogle Scholar
  35. 35.
    Schneider SM, Fung VS, Palmblad J, Babior BM (2001) Activity of the leukocyte NADPH oxidase in whole neutrophils and cell-free neutrophil preparations stimulated with long-chain polyunsaturated fatty acids. Inflammation 1:17–23CrossRefGoogle Scholar
  36. 36.
    Gibson RA, Neuman MA, James MJ, Hawkes JS, Hall C, Cleland LG (1992) Effect of n-3 and n-6 dietary fats on the lipoxygenase products from stimulated rat neutrophils. Prost Leuk Essen Fatty Acids 46:87–91CrossRefGoogle Scholar
  37. 37.
    LeBlanc CJ, Horohov DW, Bauer JE, Hosgood G, Mauldin GE (2008) Effects of dietary supplementation with fish oil on in vivo production of inflammatory mediators in clinically normal dogs. Am J Vet Res 69:486–493PubMedCrossRefGoogle Scholar
  38. 38.
    Byrne KP, Campbell KL, Davis CA, Schaffer DJ, Troutt HF (2000) The effects of dietary n-3 vs. n-6 fatty acids on ex vivo LTB4 generation by canine neutrophils. Vet Derm 11:123–131CrossRefGoogle Scholar
  39. 39.
    Vaughn DM, Rheinhart GA, Swaim SF, Laurten SD, Garner CA, Boudreaux MK, Spano JS, Hoffman CE, Conner B (1994) Evaluation of dietary n-6 to n-3 fatty acid ratios on leukotriene synthesis in dog skin and neutrophils. Vet Derm 5:163–173CrossRefGoogle Scholar
  40. 40.
    LeBlanc CJ, Dietrich MA, Horohov DW, Bauer JE, Hosgood G, Mauldin GE (2007) Effects of dietary fatty fish oil and vitamin E supplementation on canine lymphocyte proliferation evaluated using a flow cytometric technique. Vet Immunol Immunopath 119:180–188CrossRefGoogle Scholar
  41. 41.
    Hall JA, Picton RA, Skinner MM, Jewell DE, Wander RC (2006) The (n-3) fatty acid dose, independent of the (n-6) to (n-3) fatty acid ratio, affects the plasma fatty acid profile of normal dogs. J Nutr 136:2338–2344PubMedGoogle Scholar
  42. 42.
    Markert M, Andrews PC, Babior BM (1984) Measurement of O2 production by human neutrophils. The preparation and assay of NADPH oxidase-containing particles from human neutrophils. Methods Enzymol 105:358–365PubMedCrossRefGoogle Scholar
  43. 43.
    Folch K, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:497–509PubMedGoogle Scholar
  44. 44.
    Hansen J-B, Grimsgard S, Nilsen H, Nordoy A, Bonna KH (1999) Effects of highly purified eicosapentaenoic acid and docosahexaenoic acid on fatty acid absorption, incorporation into serum phospholipids and postprandial triglyceridemia. Lipids 33:131–138CrossRefGoogle Scholar
  45. 45.
    Burdge GC, Jones AE, Wootton SA (2002) Eicosapentaenoic acid and docosapentaenoic acids are the principal products of α-linolenic acid metabolism in young men. Br J Nutr 88:355–363PubMedCrossRefGoogle Scholar
  46. 46.
    Bauer JE, Dunbar BL, Bigley KE (1998) Dietary flaxseed in dogs results in differential transport and metabolism of (n-3) polyunsaturated fatty acids. J Nutr 128:2641S–2644SPubMedGoogle Scholar
  47. 47.
    Dunbar BL, Bigley KE, Bauer JE (2010) Early and sustained enrichment of serum n-3 long chain polyunsaturated fatty acids in dogs fed a flaxseed supplemented diet. Lipids 45:1–10PubMedCrossRefGoogle Scholar
  48. 48.
    Gavino GR, Gavino GC (1991) Rat liver outer mitochondrial carnitine palmitoyltransferase activity toward long chain polyunsaturated fatty acids and CoA esters. Lipids 26:266–270PubMedCrossRefGoogle Scholar
  49. 49.
    MacDonald JIS, Sprecher H (1991) Phospholipid remodeling in mammalian cells. Biochim Biophys Acta 1084:105–121PubMedGoogle Scholar
  50. 50.
    Brossard N, Croset M, Pachiaudi C, Riou JP, Tayot JL, Lagarde M (1996) Retroconversion and metabolism of [13C]22:6n–3 in humans and rats after intake of a single dose of [13C]22:6n–3-triacylglycerols. Am J Clin Nutr 64:577–586PubMedGoogle Scholar
  51. 51.
    Conquer JA, Holub BJ (1997) Dietary docosahexaenoic acid as a source of eicosapentaenoic acid in vegetarians and omnivores. Lipids 32:341–345PubMedCrossRefGoogle Scholar
  52. 52.
    Chen H, Ray J, Scarpino V, Acland GM, Aguirre GD, Anderson RE (1999) Synthesis and release of docosahexaenoic acid by the RPE cells of prcd-affected dogs. Invest Ophthmalol Vis Sci 10:2418–2422Google Scholar
  53. 53.
    Lands WEM, Morris A, Libelt B (1990) Quantitative effects of dietary polyunsaturated fats on the composition of fatty acids in rat tissues. Lipids 25:505–516Google Scholar
  54. 54.
    Bauer JE, Waldron MK, Spencer AL, Hannah SS (2002) Predictive equations for the quantitation of polyunsaturated fatty acids in canine plasma and neutrophils from dietary fatty acid profiles. J Nutr 132:1642S–1645SPubMedGoogle Scholar
  55. 55.
    Klingenberg IL, Knabe DA, Smith SB (1995) Lipid metabolism in pigs fed beef tallow or high-oleic acid sunflower oil. Comp Biochem Physiol Part B110:183–192CrossRefGoogle Scholar
  56. 56.
    Carletto A, Bellavite P, Guarinin P, Biasi D, Chirumbolo S, Caramaschi P, Bambara LM, Corrocher R (1996) Changes of fatty acid composition and oxidative metabolism of human neutrophils migrating into inflammatory exudates. Inflammation 20:123–127PubMedCrossRefGoogle Scholar
  57. 57.
    Schneider SM, Fung VS, Palmblad J, Babior BM (2001) Activity of the leukocyte NADPH oxidase in whole neutrophils and cell-free neutrophil preparations stimulated with long-chain polyunsaturated fatty acids. Inflammation 1:17–23CrossRefGoogle Scholar
  58. 58.
    Edwards SW (1994) Biochemistry physiology of the neutrophil. Cambridge University Press, New York, pp 1–69CrossRefGoogle Scholar
  59. 59.
    Abramson SB, Leszczynska-Piziak J, Weissmann G (1991) Arachidonic acid as a second messenger: interactions with GTP—binding protein of human neutrophils. J Immunol 147:231–236PubMedGoogle Scholar
  60. 60.
    Harris WS (2006) The omega-6/omega-3 ratio and cardiovascular disease risk: uses and abuses. Curr Athero Rep 8:453–459CrossRefGoogle Scholar
  61. 61.
    Stanley JC, Elsom RL, Calder PC, Griffin BA, Harris WS, Jebb SA, Lovegrove JA, Moore CS, Riemersma RA, Sanders TAB (2007) UK food standards agency workshop report: the effects of dietary n-6:n-3 fatty acid ratio on cardiovascular health. Br J Nutr 98:1305–1310PubMedCrossRefGoogle Scholar
  62. 62.
    Wall R, Ross RP, Fitzgerald GF, Stanton C (2010) Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 68:280–289PubMedCrossRefGoogle Scholar
  63. 63.
    Anonymous (1992) Functions of unsaturated fatty acids. In: Unsaturated Fatty Acids: Nutritional and Physiological Significance. The Report of the British Nutrition Foundation’s Task Force, Chapman & Hall, London, pp 48–62 Google Scholar
  64. 64.
    deDeckere EAM, Korver O, Verschuren PM, Katan MB (1998) Health aspect of fish and n-3 polyunsaturated acids from plant and marine origin. Eur J Clin Nutr 52:749–753CrossRefGoogle Scholar
  65. 65.
    Simopoulos AP, Leaf A, Salem N Jr (1999) Workshop on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. J Am Coll Nutr 8:4878–4889Google Scholar

Copyright information

© AOCS 2012

Authors and Affiliations

  • Mark K. Waldron
    • 1
    • 3
  • Steven S. Hannah
    • 2
  • John E. Bauer
    • 1
  1. 1.Department of Small Animal Clinical Sciences, College of Veterinary MedicineTexas A&M UniversityCollege StationUSA
  2. 2.Nestlé Purina PetCareSt. LouisUSA
  3. 3.Nestlé Purina PetCareCheckerboard Square ResearchSt. LouisUSA

Personalised recommendations