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The effects of dietary lipids on adrenergically-stimulated lipolysis in perinodal adipose tissue following prolonged activation of a single lymph node

Published online by Cambridge University Press:  09 March 2007

Christine A. Mattacks ,
Dawn Sadler  and
Caroline M. Pond
Christine A. Mattacks
Affiliation:
Department of Biological Sciences, The Open University, Milton Keynes, Bucks. MK7 6AA, UK
Dawn Sadler
Affiliation:
Department of Biological Sciences, The Open University, Milton Keynes, Bucks. MK7 6AA, UK
Caroline M. Pond*
Affiliation:
Department of Biological Sciences, The Open University, Milton Keynes, Bucks. MK7 6AA, UK
*
*Corresponding author: Dr Caroline M. Pond, fax +44 1908 654167, email [email protected]
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Abstract

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The effects of feeding beef suet (mostly saturated and monoenoic fatty acids), sunflower oil (rich in n-6 fatty acids) and fish oil (rich in n-3 fatty acids) on the response of mesenteric, omental, popliteal and perirenal adipocytes to experimentally-induced local inflammation were studied in adult guinea pigs. After 6 weeks on the experimental diets, the animals were fed standard chow, and lipopolysaccharide was injected unilaterally daily for 4 d to induce swelling of one popliteal lymph node. Basal lipolysis in the perinodal adipocytes of all depots studied was higher in the sunflower oil-fed animals than in the controls fed on standard chow, and lower in those fed on suet or fish oil. Dietary lipids altered rates of lipolysis during incubation with 10-5 M noradrenaline in all samples studied from the locally-activated popliteal depot, but only in adipocytes within 5 mm of a large lymph node in the other depots. The fish-oil diet attenuated the spread of increased lipolysis within the locally-activated popliteal adipose tissue, and from this depot to other node-containing depots. These experiments show that n-6 polyunsaturated fatty acids promote and n-3 fatty acids suppress the spread of immune activation to adipocytes within and between depots, and alter the sensitivity of perinodal adipocytes to noradrenaline. Dietary effects are reduced or absent in adipocytes in sites remote from lymph nodes, and thus such samples do not adequately represent processes in perinodal adipose tissue. These results are consistent with the hypothesis that perinodal adipocytes interact with adjacent lymphoid cells during immune responses.

Keywords

Site-specific propertiesFish oiln-6 Polyunsaturated fatty acidsLocal interactionsGuinea pig
Type
Research Article
Information
British Journal of Nutrition , Volume 87 , Issue 4 , April 2002 , pp. 375 - 382
Copyright
Copyright © The Nutrition Society 2002

References

Berkowitz, DE, Brown, D, Lee, KM, Emala, C, Palmer, D, An, Y & Breslow, M (1998) Endotoxin-induced alteration in the expression of leptin and β3-adrenergic receptor in adipose tissue. American Journal of Physiology 274, E992–E997.Google ScholarPubMed
Bernlohr, DA, Coe, NR, Simpson, MA & Hertzel, AV (1997) Regulation of gene expression in adipose cells by polyunsaturated fatty acids. Advances in Experimental Medicine and Biology 422, 145–156.CrossRefGoogle ScholarPubMed
Björntorp, P (1996) Growth hormone treatment of hypophysectomized rats increases catecholamine-induced lipolysis and the number of β-adrenergic receptors in adipocytes - no differences in the effects of growth hormone on different fat depots. Obesity Research 4, 471–478.Google Scholar
Calder, PC (2001) The effect of dietary fatty acids on the immune response and susceptibility to infection. In Nutrition, Immunity, and Infection in Infants and Children, pp. 137–172 [Sus-kind, RM and Tontisirin, K, editors]. Philadelphia, PA: Lippincott, Williams and Wilkins.Google Scholar
Calder, PC & Miles, EA (2000) Fatty acids and atopic disease. Pediatric Allergy and Immunology 11, Suppl. 13, 29–36.CrossRefGoogle ScholarPubMed
Cinti, S (2001) The adipose organ: morphological perspectives of adipose tissues. Proceedings of the Nutrition Society 60, 319–328.CrossRefGoogle ScholarPubMed
Colby, RH & Pond, CM (1993) Site-specific differences in the responses of guinea-pig adipose tissue to changes in the fatty acid composition of the diet. Nutrition Research 13, 1203–1212.CrossRefGoogle Scholar
Coppack, SW (2001) Pro-inflammatory cytokines and adipose tissue. Proceedings of the Nutrition Society 60, 349–356.CrossRefGoogle ScholarPubMed
El Hadri, K, Courtalon, A, Gauthereau, X, Chambaut-Guérin, AM, Pairault, J & Fève, B (1997) Differential regulation by tumor necrosis factor-α of β1- β2-, and β3-adrenoreceptor gene expression in 3T3-F442A adipocytes. Journal of Biological Chemistry 272, 24514–24521.CrossRefGoogle Scholar
Grimaldi, PA (1999) Roles of lipid-activated receptors in the adipogenic action of fatty acids. Lipids 34, S205–S208.CrossRefGoogle ScholarPubMed
Grimble, RF (1998) Nutritional modulation of cytokine biology. Nutrition 14, 634–640.CrossRefGoogle ScholarPubMed
Guthrie, N & Carroll, KK (1999) Specific versus non-specific effects of dietary fat on carcinogenesis. Progress in Lipid Research 38, 261–271.CrossRefGoogle ScholarPubMed
Harris, RBS, Zhou, J, Youngblood, BD, Rybkin, II, Smagin, GN & Ryan, DH (1998) Effect of repeated stress on body weight and body composition of rats fed low- and high-fat diets. American Journal of Physiology 275, R1928–R1938.Google ScholarPubMed
Heath, T & Brandon, R (1983) Lymphatic and blood vessels of the popliteal node in sheep. Anatomical Record 207, 461–472.CrossRefGoogle ScholarPubMed
Hwang, D (2000) Fatty acids and immune responses – A new perspective in searching for clues to mechanism. Annual Review of Nutrition 20, 431–456.CrossRefGoogle ScholarPubMed
Jump, DB & Clarke, SD (1999) Regulation of gene expression by dietary fat. Annual Review of Nutrition 19, 63–90.CrossRefGoogle ScholarPubMed
Langhans, W (2000) Anorexia of infection: Current prospects. Nutrition 16, 996–1005.CrossRefGoogle ScholarPubMed
Londos, C, Brasaemle, DL, Schultz, CJ, Adler-Wailes, DC, Levin, DM, Kimmel, AR & Rondinone, CM (1999) On the control of lipolysis in adipocytes. Annals of the New York Academy of Sciences 892, 155–168.CrossRefGoogle ScholarPubMed
MacQueen, HA, Sadler, D & Mattacks, CA (2000) Dietary fatty acids influence the appearance of tumour necrosis factor-α receptors on adipocytes following an immune challenge. British Journal of Nutrition 84, 387–392.CrossRefGoogle ScholarPubMed
Maestroni, GJM (2000) Dendritic cell migration controlled by α1β-adrenergic receptors. Journal of Immunology 165, 6743–6747.CrossRefGoogle ScholarPubMed
Mattacks, CA & Pond, CM (1997) The effects of feeding suet-enriched chow on site-specific differences in the composition of triacylglycerol fatty acids in adi-pose tissue and its interactions in vitro with lymphoid cells. British Journal of Nutrition 77, 621–643.CrossRefGoogle Scholar
Mattacks, CA & Pond, CM (1999) Interactions of noradrenalin and tumour necrosis factor-α, interleukin-4 and interleukin-6 in the control of lipolysis from adipocytes around lymph nodes. Cytokine 11, 334–346.CrossRefGoogle ScholarPubMed
Mersmann, HJ, McNeel, RL, Akanbi, KA, Shparber, A & Hachey, DL (1995) Influence of dietary fat on β-adrenergic receptors and receptor-controlled metabolic function in porcine adipocytes. Journal of Nutritional Biochemistry 6, 302–309.CrossRefGoogle Scholar
Mersmann, HJ, McNeel, RL, Morkeberg, JC, Shparber, A & Hachey, DL (1992) β-Adrenergic receptor mediated functions in porcine adipose tissue are not affected differently by saturated vs unsaturated dietary fats. Journal of Nutrition 122, 1952–1959.CrossRefGoogle Scholar
Moussa, M, Tkaczuk, J, Ragab, J, Garcia, J, Abbal, M, Ohayon, E, Ghisolfi, J & Thouvenot, J-P (2000) Relationship between the fatty acid composition of rat lymphocytes and immune functions. British Journal of Nutrition 83, 327–333.CrossRefGoogle ScholarPubMed
Orban, Z, Remaley, AT, Sampson, M, Trajanoski, Z & Chrousos, GP (1999) The differential effect of food intake and β-adrenergic stimulation on adipose-derived hormones and cytokines in man. Journal of Clinical Endocrinology and Metabolism 84, 2126–2133.Google ScholarPubMed
Pond, CM (1996) Interactions between adipose tissue and the immune system. Proceedings of the Nutrition Society 55, 111–126.CrossRefGoogle ScholarPubMed
Pond, CM (1999) Physiological specialisation of adipose tissue. Progress in Lipid Research 38, 225–248.CrossRefGoogle ScholarPubMed
Pond, CM (2001) Long-term changes in adipose tissue in human disease. Proceedings of the Nutrition Society 60, 365–374.CrossRefGoogle ScholarPubMed
Pond, CM & Mattacks, CA (1991) The effects of noradrenaline and insulin on lipolysis in adipocytes isolated from nine different adipose depots of guinea-pigs. International Journal of Obesity 15, 609–618.Google ScholarPubMed
Pond, CM & Mattacks, CA (1995) Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro. Journal of Lipid Research 36, 2219–2231.CrossRefGoogle ScholarPubMed
Pond, CM & Mattacks, CA (1998) In vivo evidence for the involvement of the adipose tissue surrounding lymph nodes in immune responses. Immunology Letters 63, 159–167.CrossRefGoogle ScholarPubMed
Pond, CM & Mattacks, CA (2002) The activation of adipose tissue associated with lymph nodes during the early stages of an immune response. Cytokine 17 (In the Press).CrossRefGoogle ScholarPubMed
Pond, CM, Mattacks, CA & Sadler, D (1984) The effects of food restriction and exercise on site-specific differences in adipocyte volume and adipose tissue cellularity. 1. Superficial and intra-abdominal sites. British Journal of Nutrition 51, 415–424.CrossRefGoogle ScholarPubMed
Pöschl, JMB, Paul, K, Leichsenring, M, Han, SR, Pfisterer, M, Bremer, HJ & Linderkamp, O (1999) Effects of dietary supplementation of saturated fatty acids and of n-6 or n-3 polyunsaturated fatty acids on plasma and red blood cell membrane phospholipids and deformability in weanling guinea pigs. Lipids 34, 467–473.CrossRefGoogle ScholarPubMed
Rayner, DV (2001) The sympathetic nervous system in white adipose tissue regulation. Proceedings of the Nutrition Society 60, 357–364.CrossRefGoogle ScholarPubMed
Rogausch, H, Del Rey, A, Oertel, J & Besedovsky, HO (1999) Norepinephrine stimulates lymphoid cell mobilization from the perfused rat spleen via β-adrenergic receptors. American Journal of Physiology 276, R724–R730.Google ScholarPubMed
Sadeghi, S, Wallace, FA & Calder, PC (1999) Dietary lipids modify the cytokine response to bacterial lipopolysaccharide in mice. Immunology 96, 404–410.CrossRefGoogle ScholarPubMed
Sanderson, P, Yaqoob, P & Calder, PC (1995) Effects of dietary lipid manipulation on graft vs host and host vs graft responses in the rat. Cellular Immunology 164, 240–247.CrossRefGoogle ScholarPubMed
Sanderson, P, MacPherson, GG, Jenkins, CH & Calder, PC (1997) Dietary fish oil diminishes the antigen presentation activity of rat dendritic cells. Journal of Leukocyte Biology 62, 771–777.CrossRefGoogle ScholarPubMed
Shimotsuma, M, Shields, JW, Simpson-Morgan, MW, Sakuyama, A, Shirasu, M, Hagiwara, A & Takahashi, T (1993) Morpho-physiological function and role of omental milky spots as omentum-associated lymphoid tissue (OALT) in the peritoneal cavity. Lymphology 26, 90–101.Google ScholarPubMed
Simons, K & Ikonen, E (1997) Functional rafts in cell membranes. Nature 387, 569–572.CrossRefGoogle ScholarPubMed
Wallace, FA, Miles, EA & Calder, PC (2000) Activation state alters the effect of dietary fatty acids on pro-inflammatory mediator production by murine macrophages. Cytokine 12, 1374–1379.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. Journal of Leukocyte Biology 69, 449–457.CrossRefGoogle Scholar
Yam, D, Eliraz, A & Berry, EM (1996) Diet and disease – The Israeli paradox: Possible dangers of a high omega-6 polyunsaturated fatty acid diet. Israel Journal of Medical Sciences 32, 1134–1143.Google ScholarPubMed
Yaqoob, P, Newsholme, EA & Calder, PC (1994) The effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation. Immunology 82, 603–610.Google ScholarPubMed