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The source of fatty acids incorporated into proliferating lymphoid cells in immune-stimulated lymph nodes

Published online by Cambridge University Press:  09 March 2007

Caroline M. Pond  and
Christine A. Mattacks
Caroline M. Pond*
Affiliation:
Department of Biological Sciences, The Open University, Milton Keynes, Buckinghamshire MK7 6AA, UK
Christine A. Mattacks
Affiliation:
Department of Biological Sciences, The Open University, Milton Keynes, Buckinghamshire MK7 6AA, UK
*
*Corresponding author: Professor Caroline M. Pond, fax +44 1908 654167, email C.M.Pond@open.ac.uk
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Abstract

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To explore the hypothesis that proliferating lymphoid cells in immune-stimulated lymph nodes obtain nutrients locally from adjacent adipose tissue, adult guinea pigs were fed for 6 weeks on standard chow or on chow supplemented with 100 g suet, sunflower oil or fish oi/g. All the guinea pigs ate standard chow for the last 5 d, during which swelling of one popliteal lymph node was stimulated by repeated local injection of lipopolysaccharide. The fatty acid compositions of phospholipids in both popliteal and in several mesenteric lymph nodes, and of triacylglycerols in eleven samples of adipose tissue defined by their anatomical relations to lymph nodes, were determined by GC. The proportions of fatty acids in the phospholipids extracted from the stimulated popliteal node correlated best with those of triacylglycerols in the surrounding adipocytes, less strongly with those of adipocytes elsewhere in depots associated with lymphoid tissue, but not with those of nodeless depots. The composition of triacylglycerols in the perinodal adipose tissue changed under local immune stimulation. We conclude that proliferating lymphoid cells in activated lymph nodes obtain fatty acids mainly from the triacylglycerols in adjacent perinodal adipose tissue. Immune stimulation prompts changes in the fatty acid composition of the triacylglycerols of adipocytes in node-containing depots that equip the adipose tissue for provisioning immune responses. Such local interactions show that specialised adipocytes can act as an interface between whole-body and cellular nutrition, and may explain why mammalian adipose tissue is partitioned into a few large and many small depots.

Keywords

Perinodal adipose tissueParacrine interactionsAdipocyte site-specific propertiesPoplitealMesenteric
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue 3 , March 2003 , pp. 375 - 382
Copyright
Copyright © The Nutrition Society 2003

References

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 [Suskind, RM and Tontisirin, K, editors]. Philadelphia, PA: Lippincott, Williams & Wilkins.Google Scholar
Calder, PC, Harvey, DJ, Pond, CM & Newsholme, EA (1992) Site-specific differences in the fatty acid composition of human adipose tissue. Lipids 27, 716–720.CrossRefGoogle ScholarPubMed
Calder, PC & Newsholme, EA (1993) Effects of omega-3 fatty acids on lymphocyte functions. In Omega-3 Fatty Acids: Metabolism and Biological Effects, pp. 293 –303 [Drevon, CA, Baksaas, I and Krokan, HE, editors]. Basel: Birkhäuser Verlag.Google Scholar
Calder, PC, Yaqoob, P, Harvey, DJ, Watts, A & Newsholme, EA (1994) Incorporation of fatty acids by concanavalin-A stimulated lymphocytes and the effect on fatty acid composition and membrane fluidity. Biochemical Journal 300, 509–518.CrossRefGoogle ScholarPubMed
Clandinin, MT, Cheema, S, Field, CJ, Garg, ML, Venkatraman, J & Clandinin, TR (1991) Dietary fat: exogenous determination of membrane structure and cell function. FASEB Journal 5, 2761–2769.CrossRefGoogle ScholarPubMed
Decsi, T & Koletzko, B (2000) Effects of protein–energy malnutrition and human immunodeficiency virus-1 infection on essential fatty acid metabolism in children. Nutrition 16, 447–453.CrossRefGoogle ScholarPubMed
Diener, E (1970) Evolutionary aspects of immunity and lymphoid organs in vertebrates. Transplantation Proceedings 2, 309–317.Google Scholar
Garg, A, Peshock, RM & Fleckenstein, JL (1999) Adipose tissue distribution pattern in patients with familial partial lipodystrophy (Dunnigan variety). Journal of Clinical Endocrinology and Metabolism 84, 170–174.Google ScholarPubMed
Geerling, BJ, van Houwelingen, AC, Badart-Smook, A, Stockbrugger, RW & Brummer, JM (1999) Fat intake and fatty acid profile in plasma phospholipids and adipose tissue in patients with Crohn's disease, compared with controls. American Journal of Gastroenterology 94, 410–417.CrossRefGoogle ScholarPubMed
Goodpaster, BH, Thaete, FL & Kelley, DE (2000) Composition of skeletal muscle evaluated with computed tomography. Annals of the New York Academy of Sciences 904, 18–24.CrossRefGoogle ScholarPubMed
Gyllensten, L (1950) The postnatal histogenesis of the lymphatic system of guinea-pigs. Acta Anatomica 10, 130–160.CrossRefGoogle ScholarPubMed
Henry, K & Symmers, WSC (1992) Thymus, Lymph Nodes, Spleen and Lymphatics, 3rd ed. Edinburgh: Churchill Livingstone.Google Scholar
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
Jonsdottir, IH, Schjerling, P, Ostrowski, K, Asp, S, Richter, EA & Pedersen, BK (2000) Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. Journal of Physiology, London 528, 157–163.CrossRefGoogle ScholarPubMed
Lin, DS, Connor, WE & Spenler, CW (1993) Are dietary saturated, monounsaturated, and polyunsaturated fatty acids deposited to the same extent in adipose tissue of rabbits? American Journal of Clinical Nutrition 58, 174–179.CrossRefGoogle Scholar
Luiken, JJFP, Glatz, JFC & Bonen, A (2000) Fatty acid transport proteins facilitate fatty acid uptake in skeletal muscle. Canadian Journal of Applied Physiology 25, 333–351.CrossRefGoogle ScholarPubMed
MacQueen, HA, Waights, V & Pond, CM (1999) Vascularisation in adipose depots surrounding immune-stimulated lymph nodes. Journal of Anatomy, London 194, 33–38.CrossRefGoogle ScholarPubMed
Malcom, GT, Bhattacharyya, AK, Velez-Duran, M, Guzman, MA, Oalmann, MC & Strong, JP (1989) Fatty acid composition of adipose tissue in humans, differences between subcutaneous sites. American Journal of Clinical Nutrition 50, 288–291.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. British Journal of Nutrition 77, 621–643.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, 334–346.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. British Journal of Nutrition 87, 375–382.CrossRefGoogle ScholarPubMed
Moussa, M, Tkaczuk, J, Ragab, J, Garcia, J, Abbal, M, Ohayon, E, Ghisolfi, J & Thouvenot, JP (2000) Relationship between the fatty acid composition of rat lymphocytes and immune functions. British Journal of Nutrition 83, 327–333.CrossRefGoogle ScholarPubMed
Murphy, MG, Wright, V, Scott, J, Timmins, A & Ackman, RG (1999) Dietary menhaden, seal, and corn oils differentially affect lipid and ex vivo eicosanoid and thiobarbituric acid-reactive substances generation in the guinea pig. Lipids 34, 115–124.CrossRefGoogle ScholarPubMed
Pedersen, BK, Steensberg, A, Fischer, C, Keller, C, Ostrowski, K & Schjerling, P (2001) Exercise and cytokines with particular focus on muscle-derived IL-6. Exercise Immunology Reviews 7, 18–31.Google ScholarPubMed
Pond, CM (1992) An evolutionary and functional view of mammalian adipose tissue. Proceedings of the Nutrition Society 51, 367–377.CrossRefGoogle 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 (2002) Adipose tissue, the immune system and exercise fatigue: how activated lymphocytes compete for lipids. Biochemical Society Transactions 30, 270–275.CrossRefGoogle ScholarPubMed
Pond, CM (2003 a) Paracrine interactions of mammalian adipose tissue. Journal of Experimental Zoology 295, 99–110.CrossRefGoogle ScholarPubMed
Pond, CM (2003 b) Paracrine relationships between adipose and lymphoid tissues: implications for the mechanism of HIV-associated adipose redistribution syndrome. Trends in Immunology 24, 13–18.CrossRefGoogle 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, 131–139.CrossRefGoogle ScholarPubMed
Priddle, JD, Mattacks, CA, Sadler, D, MacQueen, HA & Pond, CM (2003) Changes in lymphokine receptor expression and fatty acid composition of phospholipids and triacylglycerols in rat adipocytes associated with lymph nodes following a transient immune challenge. Cell Biology International 27, 23–29.CrossRefGoogle ScholarPubMed
Raclot, T, Mioskowski, E, Bach, AC & Groscolas, R (1995) Selectivity of fatty acid mobilization: a general metabolic feature of adipose tissue. American Journal of Physiology 269, R1060–R1067.Google ScholarPubMed
Roth, J, McClellan, JL, Kluger, MJ & Zeisberger, E (1994) Attenuation of fever and release of cytokines after repeated injections of lipopolysaccharide in guinea-pigs. Journal of Physiology, London 477, 177–185.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
Smith, JB & Morris, B (1970) The response of the popliteal lymph node of the sheep to swine influenza virus. Australian Journal of Experimental Medicine 48, 47–55.Google ScholarPubMed
Stremmel, W, Pohl, J, Ring, A & Herrmann, T (2001) A new concept of cellular uptake and intracellular trafficking of long-chain fatty acids. Lipids 36, 981–989.CrossRefGoogle ScholarPubMed
Thies, F, Peterson, LD, Powell, JR, Nebe-von-Caron, G, Hurst, TL, Matthews, KR, Newsholme, EA & Calder, PC (1999) Manipulation of the type of fat consumed by growing pigs affects plasma and mononuclear cell fatty acid compositions and lymphocyte and phagocyte functions. Journal of Animal Science 77, 137–147.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