Site-specific differences in fatty acid composition of dendritic cells and associated adipose tissue in popliteal depot, mesentery, and omentum and their modulation by chronic inflammation and dietary lipids.

BACKGROUND: This study explores the role of lymphatics-associated adipocytes in determining the lipid composition of dendritic cells. METHODS AND RESULTS: Adult male rats were fed plain chow, or chow supplemented with 20% sunflower or fish oil. Chronic local inflammation was induced by subcutaneous injection of 20 microg lipopolysaccharide three times a week for 2 weeks near the popliteal lymph nodes. Chemokine-stimulated dendritic cells were collected over 4 hours from popliteal and mesenteric lymph nodes, and perinodal and other samples of mesenteric, popliteal, and omental adipose tissue. Fatty acids extracted from triacylglycerols and/or phospholipids were separated and quantified by gas chromatography from each sample of dendritic cells and intracellular lipids, membranes, stroma and isolated adipocytes from the adipose tissue. Dendritic cells from lymph nodes and adipose tissue samples differed in fatty acid composition, and were modulated by diet. The site-specific differences of dendritic cells correlated with those of the contiguous adipocytes. Chronic mild stimulation altered the lipid composition of dendritic cells near the inflamed site and elsewhere; changes were minimal after the fish-oil diet. The composition of adipocyte triacylglycerol and phospholipid fatty acids also changed near the stimulation site in ways that counteracted alterations induced by the experimental diets. CONCLUSIONS: Fatty acids in dendritic cells differed with anatomical site, and were determined by the adjacent adipocytes, which actively regulated their own lipid composition. These findings demonstrated functional bases for the anatomical associations between adipose and lymphoid tissues and may be a mechanism by which dietary lipids modulate the immune system.

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

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 microg 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.

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

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 oil/kg. 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.

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

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 l0(-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.