Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-23T20:55:11.616Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  24 July 2007

Christine A. Mattacks
Affiliation:
Department of Biology, The Open University, Milton Keynes MK7 6AA
Caroline M. Pond
Affiliation:
Department of Biology, The Open University, Milton Keynes MK7 6AA
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The effects of diet on the composition and properties of adipose tissue in relation to lymph nodes were studied in adult guinea-pigs. The proportions of monoenoic triacylglycerol fatty acids were constant in all sites in adipose tissue of similarly fed guinea-pigs, but were substantially greater in samples from guinea-pigs fed on suet-enriched chow. Triacylglycerols in adipose tissue from near nodes contained significantly fewer saturated fatty acids, and significantly more 18:2n−6 and 18:3n−3 than those in samples from sites remote from nodes within the same depot. Depots that interact most strongly with lymphoid cells in vitro had the largest and most consistent within-depot differences. The gradients of triacylgiycerol fatty acid composition with distance from lymph nodes in two small intermuscular depots were similar in guinea-pigs fed on plain or suet-enriched chow. These findings are consistent with the hypothesis that adipose tissue around lymph nodes is specialized for local interactions with the lymphoid cells therein, and help to explain the variability of serial or duplicate measurements of adipose tissue composition. When cultured alone, lipopolysaccharide-stimulated lymph node lymphoid cells from suet-fed guinea-pigs incorporated as much labelled thymidine as the controls. Adipose tissue explants from suet-fed guinea-pigs inhibited lymphocyte proliferation much less than those of the controls, although the site-specific differences were similar. The pattern of site-specific differences in glycerol released from explants incubated alone was generally similar for both dietary groups, but except in the popliteal depot, the increases following co-culturing with lymphoid cells were smaller for samples from suet-fed guinea-pigs. These experiments show that minor changes in the fatty acid composition of the diet can substantially alter the interactions between adipose tissue and lymphoid cells.

Type
General Nutrition
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Anel, A., Naval, J., Gonzalez, B., Torres, J. M., Mishal, Z., Uriel, J. & Pineiro, A. (1990 a). Fatty acid metabolism in human lymphocytes. I. Time course of changes in fatty acid composition and membrane fluidity during blastic transformation of peripheral blood lymphocytes. Biochimica et Biophysica Acta 1044, 323331.CrossRefGoogle ScholarPubMed
Anel, A., Naval, J., Gonzalez, B., Uriel, J. & Pineiro, A. (1990 b). Fatty acid metabolism in human lymphocytes. II. Activation of fatty acid desaturase-elongase systems during blastic formation. Biochimica et Biophysica Acta 1044, 332337.CrossRefGoogle Scholar
Buttke, T. M. (1984). Inhibition of lymphocyte proliferation by free fatty acids. 1. Differential effects on mouse B and Tlymphocytes. Immunology 53, 235242.Google Scholar
Calder, P. C. (1995). Fatty acids, dietary lipids and lymphocyte functions. Biochemical Society Transnctions 23, 302309.CrossRefGoogle ScholarPubMed
Calder, P. C., Bond, J. A., Bevan, S. J., Hunt, S. V. & Newsholme, E. A. (1991). Effect of fatty acids in the proliferation of concanavalin A-stimulated rat lymph node lymphocytes. International Journal of Biochemistry 23, 579588.CrossRefGoogle ScholarPubMed
Calder, P. C., Harvey, D. J., Pond, C. M. & Newsholme, E. A. (1992). Site-specific differences in the fatty acid composition of human adipose tissue. Lipids 27, 716720.CrossRefGoogle ScholarPubMed
Calder, P. C., Yaqoob, P., Harvey, D. J., Watts, A. & Newsholme, E. A. (1994). Incorporation of fatty acids by concanavalin A-stimulated lymphocytes and the effect on fatty acid composition and membrane fluidity. Biochemical Journal 300, 509518.CrossRefGoogle ScholarPubMed
Clarke, S. D. & Jump, D. B. (1994). Dietary polyunsaturated fatty acid regulation of gene transcription. Annual Review of Nutrition 14, 8398.CrossRefGoogle ScholarPubMed
Colby, R. H. & Pond, C. M. (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, 12031212.CrossRefGoogle Scholar
Cooper, G. & Schiller, A. L. (1975). Anatomy of the Guinea Pig. Cambridge, MA: Harvard University Press.Google Scholar
Erickson, K. L., Adams, D. A. & McNeill, C. J. (1983). Dietary lipid modulation of immune responsiveness. Lipids 18, 468474.CrossRefGoogle ScholarPubMed
Field, C. J. & Clandinin, M. T. (1984). Modulation of adipose tissue fat composition by diet: a review. Nutrition Research 4, 743755.CrossRefGoogle Scholar
Fielding, C. J. (1993). Lipid transfer proteins, catalysts, transmembrane carriers and signalling intermediates for intracellular and extracellular lipid reactions. Current Opinion in Lipidology 4, 218222.CrossRefGoogle Scholar
Frank, C. L. (1991). Adaptations for hibernation in the depot fats of a ground squirrel (Spermophilus beldingi). Canadian Journal of Zoology 69, 27072711.CrossRefGoogle Scholar
Gavino, V. C. & Gavino, G. R. (1992). Adipose hormone-sensitive lipase preferentially releases polyunsaturated fatty acids from triglycerides. Lipids 27, 950954.CrossRefGoogle ScholarPubMed
Hadek, R. (1951). The lymph nodes of the guinea-pig. British Veterinary Journal 107, 487493.CrossRefGoogle Scholar
Haugen, M. A., Kjeldsen-Kragh, J., Bjerve, K. S., Høstmark, A. T. & Førre, Ø. (1994). Changes in plasma phospholipid fatty acids and their relationship to disease activity in rheumatoid arthritis patients treated with a vegetarian diet. British Journal of Nutrition 72, 555566.CrossRefGoogle ScholarPubMed
Hennig, B., Toborek, M., Joshi-Barve, S., Barger, S. W., Barve, S., Mattson, M. P. & McClain, C. J. (1996). Linoleic acid activates nuclear transcription factor-kB (NFkB) and reduces NFkB-dependent transcription in cultured cells. American Journal of Clinical Nutrition 63, 322328.CrossRefGoogle Scholar
Hunter, D. J., Rimm, E. B., Sacks, F. M., Stampfer, M. J., Coldtiz, G. A., Litin, L. B. & Willett, W. C. (1992). Comparison of measures of fatty acid intake by subcutaneous fat aspirate, food frequency questionnaire, and diet records in a free-living population of US men. American Journal of Epidemiology 135, 418427.CrossRefGoogle Scholar
Lin, D. S., Connor, W. E. & Spenler, C. W. (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, 174179.CrossRefGoogle Scholar
Maalouf, H., Gagnon, R. & Bois, P. (1967). Étude descriptive et topographique des ganglions lymphatiques du cobaye (Descriptive and topographic study of the lymph nodes of the guinea-pig). Revue Canadienne de Biologie 26, 323334.Google ScholarPubMed
Malcom, G. T., Bhattacharyya, A. K., Velez-Duran, M., Guzman, M. A., Oalmann, M. C. & Strong, J. P. (1989). Fatty acid composition of adipose tissue in humans, differences between subcutaneous sites. American Journal of Clinical Nutrition 50, 288291.CrossRefGoogle ScholarPubMed
Mattacks, C. A., Sadler, D. & Pond, C. M. (1987). The effects of exercise on the activities of hexokinase and phosphofructokinase in superficial, intra-abdominal and intermuscular adipose tissue of guinea-pigs. Comparative Biochemistry and Physiology 87B, 533542.Google Scholar
May, C. L., Southworth, A. J. &. Calder, P. C. (1993). Inhibition of lymphocyte protein kinase C by unsaturated fatty acids. Biochemical and Biophysical Research Communications 195, 823828.CrossRefGoogle ScholarPubMed
McGowan, M. W., Artiss, J. D., Strandberg, D. R. & Zak, B. (1983). A peroxidase-coupled method for the colorimetric determination of serum triglycerides. Clinical Chemistry 29, 538542.CrossRefGoogle ScholarPubMed
Merrill, A. H. & Schroeder, J. J. (1993). Lipid modulation of cell function. Annual Review of Nutrition 13, 539559.CrossRefGoogle ScholarPubMed
Paul, A. A., Southgate, D. A. T. & Russell, J. (1980). First Supplement to McCance and Widdowson's The Composition of Foods. London: H.M. Stationery Office.Google Scholar
Phinney, S. D., Stern, J. S., Burke, K. E., Tang, A. B., Miller, G. & Holman, R. T. (1994). Human subcutaneous adipose tissue shows site-specific differences in fatty acid composition. American Journal of Clinical Nutrition 60, 725729.CrossRefGoogle ScholarPubMed
Pond, C. M. (1992). An evolutionary and functional view of mammalian adipose tissue. Proceedings of the Nutrition Society 51, 367377.CrossRefGoogle ScholarPubMed
Pond, C. M. (1994). The structure and organization of adipose tissue in naturally obese non-hibernating mammals. In Obesity in Europe '93, pp. 395402 [Ditschuneit, H., Gries, F. A., Hauner, H., Schusdziarra, V. and Wechsler, J. G., editors”. London: J. Libbey & Co.Google Scholar
Pond, C. M. (1996 a). Interactions between adipose tissue and the immune system. Proceedings of the Nutrition Society 55, 111126.CrossRefGoogle ScholarPubMed
Pond, C. M. (1996 b). Functional interpretation of the organisation of mammalian adipose tissue: its relationship to the immune system. Biochemical Society Transactions 24, 393400.CrossRefGoogle ScholarPubMed
Pond, C. M. & Mattacks, C. A. (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, 609618.Google ScholarPubMed
Pond, C. M. & Mattacks, C. A. (1995). Interactions between adipose tissue around lymph nodes and lymphoid cells in vitro. Joumal of Lipid Research 36, 22192231.CrossRefGoogle ScholarPubMed
Pond, C. M., Mattacks, C. A., Colby, R. H. & Tyler, N. J. C. (1993). The anatomy, chemical composition and maximum glycolytic capacity of adipose tissue in wild Svalbard reindeer (Rangifer tarandus platyrhynchus) in winter. Journal of Zoology, London 229, 1740.CrossRefGoogle Scholar
Pond, C. M., Mattacks, C. A. & Sadler, D. (1984 a). 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, 415424.CrossRefGoogle ScholarPubMed
Pond, C. M., Mattacks, C. A. & Sadler, D. (1984 b). The effects of food restriction and exercise on site-specific differences in adipocyte volume and adipose tissue cellularity. 2. Intermuscular sites. British Journal of Nutrition 51, 425433.CrossRefGoogle ScholarPubMed
Pond, C. M., Mattacks, C. A. & Sadler, D. (1992). The effects of exercise and feeding on the activity of lipoprotein lipase in nine different adipose depots of guinea-pigs. International Journal of Biochemistry 24, 18251831.CrossRefGoogle ScholarPubMed
Seidlin, K. N. (1995). Fatty acid composition of adipose tissue in humans. Implications for the dietary fat-serum cholesterol-CHD issue. Progress in Lipid Research 34, 119127.Google Scholar
Raclot, T. & Groscolas, R. (1993). Differential mobilization of white adipose tissue fatty acids according to chain length, unsaturation, and positional isomerism. Journal of Lipid Research 34, 15151526.CrossRefGoogle ScholarPubMed
Raclot, T. & Groscolas, R. (1994). Individual fish-oil n-3 polyunsaturated fatty acid deposition and mobilization rates for adipose tissue of rats in a nutritional steady state. American Journal of Clinical Nutrition 60, 7278.CrossRefGoogle Scholar
Teruya, J., Cluette-Brown, J., Szczepiorkowski, Z. M. & Laposata, M. (1995). Modes of transport of fatty acid to endothelial cells influences intracellular fatty acid metabolism. Journal of Lipid Research 36, 266276.CrossRefGoogle Scholar
Tjønneland, A., Overvad, K., Thorling, E. & Ewertz, M. (1993). Adipose tissue fatty acids as biomarkers of dietary exposure in Danish men and women. American Journal of Clinical Nutrition 57, 629633.CrossRefGoogle ScholarPubMed
Toborek, M., Barger, S. W., Mattson, M. P., Barve, S., McClain, C. J. & Hennig, B. (1996). Linoleic acid and TNF-α cross amplify oxidative injury and dysfunction of endothelial cells. Journal of Lipid Research 37, 123135.CrossRefGoogle ScholarPubMed
Valero-Garrido, D., López-Frias, M., Llopis, J. & López-Jurado, M. (1990). Influence of dietary fats on the lipid composition of perirenal adipose tissue of rats. Annals of Nutrition and Metabolism 34, 327332.CrossRefGoogle Scholar
Yaqoob, P. & Calder, P. C. (1993). The effects of fatty acids on lymphocyte function. International Journal of Biochemistry 25, 17051714.CrossRefGoogle Scholar
Yaqoob, P. & Calder, P. C. (1995 a). Effects of dietary lipid manipulation upon inflammatory mediator production by murine macrophages. Cellular Immunology 163, 120128.CrossRefGoogle ScholarPubMed
Yaqoob, P. & Calder, P. C. (1995 b). The effects of dietary lipid manipulation on the production of murine T cellderived cytokines. Cytokine 7, 548553.CrossRefGoogle ScholarPubMed
Yaqoob, P., Newsholme, E. A. & Calder, P. C. (1994). The effect of dietary lipid manipulation on rat lymphocyte subsets and proliferation. Immunology 82, 603610.Google ScholarPubMed
Yaqoob, P., Newsholme, E. A. & Calder, P. C. (1995). The effect of fatty acids on leucocyte subsets and proliferation in rat whole blood. Nutrition Research 15, 279287.CrossRefGoogle Scholar