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The effects of dietary lipids on dendritic cells in perinodal adipose tissue during chronic mild inflammation

Published online by Cambridge University Press:  09 March 2007

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

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The effects of dietary lipids on the abundance of dendritic cells in adipose tissue in anatomically defined relationships to chronically inflamed lymph nodes were investigated in mature male rats fed plain chow or chow plus 20 % sunflower-seed or fish oil. The popliteal lymph nodes were stimulated by local subcutaneous injection of 20 μg lipopolysaccharide to both hindlegs three times/week for 2 weeks. The masses of the major adipose depots and the numbers of dendritic cells emerging from perinodal adipose tissue and samples 5 and 10 mm from the popliteal lymph nodes were measured, and those from omental and mesenteric adipose tissue around and remote from lymphoid tissue, and mesenteric and popliteal lymph nodes. Dendritic cells were most numerous in the perinodal adipose tissue, with the corresponding ‘remote’ samples containing 25–50 % fewer such cells under all conditions studied. Dietary sunflower-seed oil increased the numbers of dendritic cells by about 17 % in all adipose samples and fish oil reduced the numbers in perinodal tissue by about 5 %. The fish-oil diet diminished responses of the intra-abdominal adipose depots to local stimulation of the popliteal node. Correlations in dendritic cell numbers were stronger between perinodal samples from different depots than between remote and perinodal samples from the same depot and after the sunflower-seed-oil diet compared with fish oil. These data show that dietary lipids modulate the number of dendritic cells in lymphoid tissue-containing adipose depots and support the hypothesis that perinodal adipose tissue interacts locally with lymphoid cells.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2004

References

Bagga, D, Wang, L, Farias-Eisner, R, Glaspy, JA & Reddy, ST (2003) Differential effects of prostaglandin derived from ω-6 and ω-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proc Natl Acad Sci U S A 100, 17511756.CrossRefGoogle ScholarPubMed
Belzung, F, Raclot, T & Groscolas, R (1993) Fish oil n-3 fatty acids selectively limit hypertrophy of abdominal fat depots in growing rats fed high-fat diets. Am J Physiol 264, R1111R1118.Google ScholarPubMed
Calder, PC (2001) Polyunsaturated fatty acids, inflammation and immunity. Lipids 36, 10041024.CrossRefGoogle ScholarPubMed
Choi, YK, Fallert, BA, Murphey-Corb, MA & Reinhart, TA (2003) Simian immunodeficiency virus dramatically alters expression of homeostatic chemokines and dendritic cell markers during infection in vivo. Blood 101, 16841691.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. Nutr Res 13, 2031212.CrossRefGoogle Scholar
Cui, L, Johkura, K, Liang, Y, Teng, R, Ogiwara, N, Okouchi, Y, Asanuma, K & Sasaki, K (2002) Biodefense function of omental milky spots through cell adhesion molecules and leukocyte proliferation. Cell Tissue Res 310, 321330.CrossRefGoogle ScholarPubMed
De Libero, G & Mori, L (2003) Self glycosphingolipids: new antigens recognized by autoreactive T lymphocytes. News Physiol Sci 18, 7176.Google Scholar
Harizi, H & Gualde, N (2002) Dendritic cells produce eicosanoids, which modulate generation and functions of antigen-presenting cells. Prostagland Leukot Essent Fatty Acids 66, 459466.CrossRefGoogle ScholarPubMed
Hart, DNJ (1997) Dendritic cells: unique leukocyte populations which control the primary immune response. Blood 90, 32453287.CrossRefGoogle ScholarPubMed
Hazan, U, Romero, IA, Cancello, R et al. (2002) Human adipose cells express CD4, CXCR4, and CCR5 receptors: a new target cell type for the immunodeficiency virus-1? FASEB J 16, U58U71.Google Scholar
Hertz, CJ, Kiertscher, SM, Godowski, PJ, Bouis, DA, Norgard, MV, Roth, MD & Modlin, RL (2001) Microbial lipopeptides stimulate dendritic cell maturation via toll-like receptor 2. J Immunol 166, 24442450.CrossRefGoogle ScholarPubMed
Hill, S, Edwards, AJ, Kimber, I & Knight, SC (1990) Systemic migration of dendritic cells during contact sensitization. Immunology 71, 277281.Google ScholarPubMed
Huang, F-P, Platt, N, Wykes, M, Major, JR, Powell, TJ, Jenkins, CD & MacPherson, GG (2000) A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med 191, 435443.CrossRefGoogle Scholar
Jenski, LJ (2000) Omega-3 fatty acids and the expression of membrane proteins: emphasis on molecules of immunologic importance. Curr Org Chem 4, 11851200.CrossRefGoogle Scholar
John, M, Nolan, D & Mallal, S (2001) Antiretroviral therapy and the lipodystrophy syndrome. Antivir Therap 6, 920.CrossRefGoogle ScholarPubMed
Lauritzen, L, Hansen, HS, Jørgensen, MH & Michaelsen, KF (2001) The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 40, 194.CrossRefGoogle ScholarPubMed
Lee, JY, Plakidas, A, Lee, WH, Heikkinen, A, Chanmugam, P, Bray, G & Hwang, DH (2003) Differential modulation of Toll-like receptors by fatty acids: preferential inhibition by n-3 polyunsaturated fatty acids. J Lipid Res 44, 479486.CrossRefGoogle ScholarPubMed
Levine, TP & Chain, BM (1992) Endocytosis by antigen presenting cells: dendritic cells are as endocytically active as other antigen presenting cells. Proc Natl Acad Sci U S A 89, 83428346.CrossRefGoogle ScholarPubMed
Lo, P (2003) HIV hijacks dendritic cells. Nat Med 9, 650.CrossRefGoogle ScholarPubMed
Lopez, MC, Huang, DS & Watson, RR (2002) Changes in mesenteric lymph node T cell phenotype and B and T cell homing properties after murine AIDS infection. Lymphology 35, 7686.Google Scholar
Luft, T, Jefford, M, Luetjens, P, Toy, T, Hochrein, H, Masterman, K-A, Maliszewski, C, Shortman, K, Cebon, J & Maraskovsky, E (2002) Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E 2 regulates the migratory capacity of specific DC subsets. Blood 100, 13621372.CrossRefGoogle ScholarPubMed
Maestroni, GJM (2000) Dendritic cell migration controlled by α 1b -adrenergic receptors. J Immunol 165, 67436747.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 adipose tissue and its interactions in vitro with lymphoid cells. Br J Nutr 77, 621643.CrossRefGoogle ScholarPubMed
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, 334346.CrossRefGoogle ScholarPubMed
Mattacks, CA, Sadler, D & Pond, CM (2002) The effects of dietary lipids on adrenergically stimulated lipolysis in perinodal adipose tissue following prolonged activation of a single lymph node. Br J Nutr 87, 375382.CrossRefGoogle ScholarPubMed
Mattacks, CA, Sadler, D & Pond, CM (2003) The cellular structure and lipid/protein composition of adipose tissue surrounding chronically stimulated lymph nodes in rats. J Anat Lond 202, 551561.CrossRefGoogle ScholarPubMed
Morelli, AE & Thomson, AW (2003) Dendritic cells under the spell of prostaglandins. Trends Immunol 24, 108111.CrossRefGoogle ScholarPubMed
Mueller, A, O'Rourke, J, Chu, P, Kim, CC, Sutton, P, Lee, A & Falkow, S (2003) Protective immunity against Helicobacter is characterized by a unique transcriptional signature. Proc Natl Acad Sci U S A 100, 1228912294.CrossRefGoogle ScholarPubMed
Nestle, FO, Banchereau, J & Hart, D (2001) Dendritic cells: on the move from bench to bedside. Nat Med 7, 761765.CrossRefGoogle ScholarPubMed
O'Neil, SP, Mossman, SP, Maul, DH & Hoover, EA (1999) In vivo cell and tissue tropism of SIVsmmPBj14-bcl.3. AIDS Res Hum Retrovir 15, 203215.Google Scholar
Pond, CM (2001) Long-term changes in adipose tissue in human disease. Proc Nutr Soc 60, 365374.Google Scholar
Pond, CM (2003 a) Paracrine interactions of mammalian adipose tissue. J Exp Zool 295A, 99110.Google Scholar
Pond, CM (2003 b) Paracrine relationships between adipose and lymphoid tissues: implications for the mechanism of HIV-associated adipose redistribution syndrome. Trends Immunol 24, 1318.Google Scholar
Pond, CM & Mattacks, CA (1995) Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro. J Lipid Res 36, 22192231.CrossRefGoogle ScholarPubMed
Pond, CM & Mattacks, CA (1998) In vivo evidence for the involvement of the adipose tissue surrounding lymph nodes in immune responses. Immunol Lett 63, 159167.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 131139.CrossRefGoogle ScholarPubMed
Pond, CM & Mattacks, CA (2003) The source of fatty acids incorporated into proliferating lymphoid cells in immune-stimulated lymph nodes. Br J Nutr 89, 375382.CrossRefGoogle ScholarPubMed
Randolph, GJ, Beaulieu, SLebecque, S, Steinman, RM & Muller, WA (1998) Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282, 480483.CrossRefGoogle Scholar
Raulin, J (2002) Human immunodeficiency virus and host cell lipids. Interesting pathways in research for a new HIV therapy. Prog Lipid Res 41, 2765.CrossRefGoogle ScholarPubMed
Reinhart, TA (2003) Chemokine induction by HIV-1: recruitment to the cause. Trends Immunol 24, 351353.CrossRefGoogle ScholarPubMed
Roman, DAD, Bachiller, P, Izaola, O, Romero, E, Martin, J, Arranz, M, Bouza, JME & Aller, R (2001) Nutritional treatment for acquired immunodeficiency virus infection using an enterotropic peptide-based formula enriched with n-3 fatty acids: a randomized prospective trial. Eur J Clin Nutr 55, 10481052.CrossRefGoogle Scholar
Saeki, H, Moore, AM, Brown, MJ & Hwang, ST (1999) Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J Immunol 162, 24722475.CrossRefGoogle ScholarPubMed
Sanderson, P, MacPherson, GG, Jenkins, CH & Calder, PC (1997) Dietary fish oil diminishes the antigen presentation activity of rat dendritic cells. J Leukoc Biol 62, 771777.CrossRefGoogle ScholarPubMed
Scandella, E, Men, Y, Gillessen, S, Forster, R & Groettrup, M (2002) Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. Blood 100, 13541361.CrossRefGoogle ScholarPubMed
Schreiner, GF, Flye, W, Brunt, E, Korber, K & Lefkowith, JB (1988) Essential fatty-acid depletion of renal-allografts and prevention of rejection. Science 240, 10321033.Google Scholar
Serhan, CN, Hong, S, Gronert, K, Colgan, SP, Devchand, PR, Mirick, G & Moussignac, RL (2002) Resolvins: a family of bioactive products of ω-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 196, 10251037.CrossRefGoogle ScholarPubMed
Smith, JB & Morris, B (1970) The response of the popliteal lymph node of the sheep to swine influenza virus. Aust JExp Biol Med 48, 4755.CrossRefGoogle ScholarPubMed
Tanriverdi, F, Silveira, LFG, MacColl, GS & Bouloux, PMG (2003) The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. J Endocrinol 176, 293304.CrossRefGoogle ScholarPubMed
Van Vugt, E, Van Rijthoven, EAM, Kamperdijk, EWA & Beelen, RHJ (1996) Omental milky spots in the local immune response in the peritoneal cavity of rats. Anat Rec 244, 235245.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Xi, S, Cohen, D & Chen, LH (1998) Effects of fish oil on cytokines and immune functions of mice with murine AIDS. J Lipid Res 39, 16771687.CrossRefGoogle ScholarPubMed