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Dietary fish oil enhances adhesion molecule and interleukin-6 expression in mice with polymicrobial sepsis

Published online by Cambridge University Press:  08 March 2007

Chun-Sen Hsu
Affiliation:
Department of Obstetrics and Gynecology, Taipei Medical University Associated Wan-Fang Hospital, 111 Hsing-Long Road, Sec 3, Taipei, Taiwan 116, ROC
Wan-Chun Chiu
Affiliation:
School of Nutrition and Health Sciences, Taipei Medical University, 250 Wu-Hsing Street, Taipei, Taiwan 110, ROC
Chiu-Li Yeh
Affiliation:
School of Nutrition and Health Sciences, Taipei Medical University, 250 Wu-Hsing Street, Taipei, Taiwan 110, ROC
Yu-Chen Hou
Affiliation:
School of Nutrition and Health Sciences, Taipei Medical University, 250 Wu-Hsing Street, Taipei, Taiwan 110, ROC
Szu-Yuan Chou
Affiliation:
Department of Obstetrics and Gynecology, Taipei Medical University Associated Wan-Fang Hospital, 111 Hsing-Long Road, Sec 3, Taipei, Taiwan 116, ROC
Sung-Ling Yeh*
Affiliation:
School of Nutrition and Health Sciences, Taipei Medical University, 250 Wu-Hsing Street, Taipei, Taiwan 110, ROC
*
*Corresponding author: Dr Sung-Ling Yeh, fax +8862 27373112, email [email protected]
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Abstract

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This study investigated the effects of fish oil (FO) diet on plasma intercellular adhesion molecule 1 (ICAM-1) levels and leucocyte integrin expression in polymicrobial sepsis. Mice were randomly assigned to a control group and an FO group. The control group was fed a medium-fat diet containing soyabean oil, whereas in the FO group, 70 % of the soyabean oil was replaced by FO for 3 weeks. After that, sepsis was induced by caecal ligation and puncture (CLP) in the experimental groups and mice were killed at 0, 6, 12 and 24 h, respectively, after CLP. Results showed that compared with the control group, plasma ICAM-1 levels were higher in the FO group 6 h after CLP. Intra-lymphocyte interferon-γ expression in the FO group was lower, whereas IL-4 expression was higher than in the control group 12 and 24 h after CLP. The expression of leucocyte integrin was significantly higher in the FO group 12 and 24 h after CLP. The FO group had higher IL-6 levels at 12 h in the lungs, at 6 and 12 h in the kidneys, and at 6, 12 and 24 h in the intestines after CLP. The survival rate did not differ between the two groups after CLP. The present findings suggest that pretreatment with an FO diet enhances adhesion molecule and inflammatory cytokine expressions during sepsis, which might aggravate the inflammatory reaction and increase neutrophil infiltration into tissues. In addition, FO diet promotes the Th2-type response and suppresses cellular immune response in polymicrobial sepsis.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Ayala, A & Chaudry, IH (1996) Immune dysfunction in murine polymicrobial sepsis: mediators, macrophages, lymphocytes and apoptosis. Shock 6, Suppl. 1, S27S38.CrossRefGoogle ScholarPubMed
Ayala, A, Deol, ZK, Lehman, DL, Herdon, CD & Chaudry, IH (1994) Polymicrobial sepsis but not low-dose endotoxin infusion causes decreased splenocyte IL-2/IFN-gamma release while increasing IL-4/IL-10 production. J Surg Res 56, 579585.CrossRefGoogle Scholar
Biffl, WL, Moore, EE, Moore, FA & Peterson, VM (1996) Interleukin-6 in the injured patient: marker of injury or mediator of inflammation?. Ann Surg 224, 647664.CrossRefGoogle ScholarPubMed
Bradley, PP, Priebat, DA, Christersen, RD & Rothstein, G (1982) Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78, 206209.CrossRefGoogle ScholarPubMed
Brunialti, MKC, Martins, PS, de Carvalho, HB, Machado, FR, Barbosa, LM & Salomao, R (2006) TLR2, TLR4, CD14, CD11b and CD11c expressions on monocytes surface and cytokine production in patients with sepsis, severe sepsis, and septic shock. Shock 25, 351357.CrossRefGoogle ScholarPubMed
Calder, PC (1997) n-3 polyunsaturated fatty acids as pharmacologic agents: a fishy tale?. Nutrition 13, 10021004.CrossRefGoogle ScholarPubMed
Calder, PC & Grimble, RF (2002) Polyunsaturated fatty acids, inflammation and immunity. Eur J Clin Nutr 56, Suppl. 3, S14S19.CrossRefGoogle ScholarPubMed
Chao, CY, Yeh, SL, Lin, MT & Chen, WJ (2000) Effects of parenteral infusion with fish oil or safflower oil emulsions on hepatic lipids, plasma amino acids and inflammatory mediators in septic rats. Nutrition 16, 284288.CrossRefGoogle ScholarPubMed
Chyi, AC & Yeh, SL (2000) Effects of dietary fish oil on survival rate, plasma amino acid pattern, and inflammatory-related mediators in diabetic rats with sepsis. Clin Nutr 19, 313318.CrossRefGoogle ScholarPubMed
Deutschman, CS, Andrejko, KM, Haber, BA, Elenko, E, Harrison, R & Taub, R (1997) Sepsis-induced depression of rat glucose-6-phosphatase gene expression and activity. Am J Physiol 271, R1709R1718.Google Scholar
Diehl, S & Rincon, M (2002) The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol 39, 531536.CrossRefGoogle ScholarPubMed
DiPiro, JT (1997) Cytokine networks with infection: mycobacterial infections, leishmaniasis, human immunodeficiency virus infection, and sepsis. Pharmacotherapy 17, 205223.CrossRefGoogle Scholar
Endo, S, Inada, K, Kasai, T, Takakuwa, T, Yamada, Y, Koike, S, Wakabayashi, G, Niimi, M, Taniguchi, S & Yoshida, M (1995) Level of soluble adhesion molecules and cytokines in patients with septic multiple organ failure. J Inflamm 46, 212219.Google ScholarPubMed
Ferguson, NR, Galley, HF & Webster, NR (1999) T helper cell subset ratios in patients with severe sepsis. Intensive Care Med 25, 106109.CrossRefGoogle ScholarPubMed
Gaut, JP, Yeh, GC & Tran, HD (2001) Neutrophils employ the myeloperoxidase system to generate antimicrobial brominating and chlorinating oxidants during sepsis. Proc Natl Acad Sci USA 98, 1196111966.CrossRefGoogle ScholarPubMed
Grimm, H, Mayer, K, Mayser, P & Eigenbordt, E (2002) Regulatory potential of n-3 fatty acids in immunological and inflammatory process. Br J Nutr 87, S59S67.CrossRefGoogle Scholar
Groeneveld, AB, Tacx, AN, Bossink, AW, van Mierlo, GJ & Hack, CE (2003) Circulating inflammatory mediators predict shock and mortality in febrile patients with microbial infection. Clin Immunol 106, 106115.CrossRefGoogle ScholarPubMed
Henderson, RB, Lim, LHK, Tessier, PA, Gavins, FNE, Mathies, M, Perretti, M & Hogg, N (2001) The use of lymphocyte function-associated antigen (LFA)-1-deficient mice to determine the role of LFA-1, Mac-1 and α4 integrin in the inflammatory response of neutrophils. J Exp Med 194, 219226.CrossRefGoogle ScholarPubMed
Heuer, JG, Bailey, DL & Sharma, GR (2004) Cecal ligation and puncture with total parenteral nutrition: a clinically relevant model of the metabolic, hormonal, and inflammatory dysfunction associated with critical illness. J Surg Res 121, 178186.CrossRefGoogle ScholarPubMed
Hillegass, LM, Griswold, DE, Brickson, B & Albrightson-Winslow, C (1990) Assessment of myeloperoxidase activity in whole rat kidney. J Pharmacol Methods 24, 285295.CrossRefGoogle ScholarPubMed
Iseri, SO, Sener, G, Saglam, B, Gedik, N, Ercan, F & Yegen, BC (2005) Oxytocin protects against sepsis-induced multiple organ damage: role of neutrophils. J Surg Res 126, 7381.CrossRefGoogle ScholarPubMed
Ishimura, K, Tsubouchi, T, Okano, K, Maeba, T & Maeta, H (1998) Wound healing of intestinal anastomosis after digestive surgery under septic conditions: participation of local interleukin-6 expression. World J Surg 22, 10691075.CrossRefGoogle ScholarPubMed
Johnson, JA III, Griswold, JA & Muakkassa, FF (1993) Essential fatty acids influence survival in sepsis. J Trauma 35, 128131.CrossRefGoogle ScholarPubMed
Kayal, S, Jais, JP, Aguini, N, Chaudiere, J & Labrousse, J (1998) Elevated circulating E-selectin, intercellular adhesion molecule 1, and von Willebrand factor in patients with severe infection. Am J Respir Crit Care Med 157, 776784.CrossRefGoogle ScholarPubMed
Klebanoff, SJ & Seymour, J (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77, 598625.CrossRefGoogle ScholarPubMed
Lanza-Jacoby, S, Flynn, JT & Miller, S (2001) Parenteral supplementation with a fish oil emulsion prolongs survival and improves rat lymphocyte function during sepsis. Nutrition 17, 112116.CrossRefGoogle ScholarPubMed
Muakkassa, FF, Koruda, MJ, Ramadan, FM, Kawakami, M & Meyer, AA (1991) Effect of dietary dish oil on plasma thromboxane B2 and 6-keto-prostaglandin F1α levels in septic rats. Arch Surg 126, 179182.CrossRefGoogle Scholar
Nolte, D, Kuebler, WM, Muller, WA, Wolff, KD & Messmer, K (2004) Attenuation of leukocyte sequestration by selective blockade of PECAM-1 or VCAM-1 in murine endotoxemia. Eur Surg Res 36, 331337.CrossRefGoogle ScholarPubMed
Oberhoffer, M, Karzai, W, Meier-Hellmann, A, Bogel, D, Fassbinder, J & Reinhart, K (1999) Sensitivity and specificity of various markers of inflammation for the prediction of tumor necrosis factor-alpha and interleukin-6 in patients with sepsis. Crit Care Med 27, 18141818.CrossRefGoogle Scholar
Rincon, M, Anguita, J, Nakamura, T, Fikrig, E & Flavell, RA (1997) Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4 T cells. J Exp Med 185, 461469.CrossRefGoogle ScholarPubMed
Somers, SD & Reickson, KL (1994) Alteration of tumor necrosis factor-α production by macrophages from mice fed diets high in eicosapentaenoic and docosahexaenoic fatty acids. Cell Immunol 153, 287297.CrossRefGoogle ScholarPubMed
Ulbrich, H, Eriksson, EE & Lindbom, L (2003) Leukocyte and endothelial cell adhesion molecules as targets for therapeutic interventions in inflammatory disease. Trend Pharmacol Sci 24, 640647.CrossRefGoogle ScholarPubMed
Wallace, FA, Miles, EA, Evans, C, Stock, TE, Yaqoob, P & Calder, PC (2001) Dietary fatty acids influence the production of Th1 but not Th2 type cytokines. J Leukoc Biol 69, 449457.CrossRefGoogle Scholar
Weber, C (2003) Novel mechanistic concepts for the control of leukocyte transmigration: specialization of integrins, chemokines, and junctional molecules. J Mol Med 81, 419.CrossRefGoogle ScholarPubMed
Whalen, MJ, Doughty, LA, Carlos, TM, Wisniewski, SR, Kochanek, PM & Carcillo, JA (2000) Intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 are increased in the plasma of children with sepsis-induced multiple organ failure. Crit Care Med 28, 26002607.CrossRefGoogle ScholarPubMed
Yeh, CL, Hsu, CS, Yeh, SL & Chen, WJ (2005) Dietary glutamine supplementation modulates Th1/Th1 cytokine and interleukin-6 expressions in septic mice. Cytokine 31, 329334.CrossRefGoogle Scholar
Zhang, P, Smith, R, Chapkin, RS & McMurray, DN (2005) Dietary (n-3) polyunsaturated fatty acids modulate murine Th1/Th2 balance toward the Th2 pole by suppression of Th1 development. J Nutr 135, 17451751.CrossRefGoogle ScholarPubMed