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Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes

Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes
Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes
Short-chain fatty acids (SCFA) are produced by fermentation of water-soluble fiber by anaerobic bacteria in the large bowel. Fiber-rich diets decrease the risk of developing inflammatory bowel disease (IBD) and butyrate enemas are effective as a therapy in some patients. Crohn's disease, one form of IBD, appears to involve an exagerated T helper-1 (Th1) lymphocyte phenotype, characterised by production of interleukin (IL)-2 and interferon (IFN)-?, that drives the inflammation. To examine whether SCFA influence pro- and anti-inflammatory cytokine production, rat mesenteric lymph node lymphocytes were cultured in the presence of acetate (10 mM), butyrate (1.5 mM) or propionate (2 mM) and the production of cytokines in response to concanavalin A determined. Butyrate, but not acetate or propionate, inhibited lymphocyte proliferation and IL-2 production. Acetate and propionate were able to partly prevent the inhibitory effect of butyrate on IL-2 production. Acetate and propionate increased IFN-? production, whereas butyrate inhibited it. Acetate and propionate in combination were able to prevent the inhibitory effect of butyrate on IFN-? production. IL-4 was not detected in any cultures. Acetate and propionate increased IL-10 production, which was not affected by butyrate. It is concluded that butyrate significantly inhibits Th1-type responses and that this might explain the therapeutic effect of butyrate in IBD patients. Acetate and propionate have less marked modulatory actions, and in some cases have effects that oppose those of butyrate. A combination of the three SCFA causes a shift in the T helper lymphocyte phenotype towards a more anti-inflammatory phenotype and this might explain the protective effects of fiber.
lymphocyte, cytokine, short-chain fatty acid, lymphocyte proliferation
0024-3205
1683-1690
Cavaglieri, Claudia R.
7da5188c-0da7-4c28-8e5f-38a7a3df795c
Nishiyama, Anita
b2db3009-1444-4182-ac0d-1be1ea1b7578
Fernandes, Luis Claudio
6445f548-9999-4c6d-acba-846a87b1354f
Curi, Rui
87abee54-a75d-4e94-b9b9-2169d8f97fec
Miles, Elizabeth A.
20332899-ecdb-4214-95bc-922dde36d416
Calder, Philip C.
1797e54f-378e-4dcb-80a4-3e30018f07a6
Cavaglieri, Claudia R.
7da5188c-0da7-4c28-8e5f-38a7a3df795c
Nishiyama, Anita
b2db3009-1444-4182-ac0d-1be1ea1b7578
Fernandes, Luis Claudio
6445f548-9999-4c6d-acba-846a87b1354f
Curi, Rui
87abee54-a75d-4e94-b9b9-2169d8f97fec
Miles, Elizabeth A.
20332899-ecdb-4214-95bc-922dde36d416
Calder, Philip C.
1797e54f-378e-4dcb-80a4-3e30018f07a6

Cavaglieri, Claudia R., Nishiyama, Anita, Fernandes, Luis Claudio, Curi, Rui, Miles, Elizabeth A. and Calder, Philip C. (2003) Differential effects of short-chain fatty acids on proliferation and production of pro- and anti-inflammatory cytokines by cultured lymphocytes. Life Sciences, 73 (13), 1683-1690. (doi:10.1016/S0024-3205(03)00490-9).

Record type: Article

Abstract

Short-chain fatty acids (SCFA) are produced by fermentation of water-soluble fiber by anaerobic bacteria in the large bowel. Fiber-rich diets decrease the risk of developing inflammatory bowel disease (IBD) and butyrate enemas are effective as a therapy in some patients. Crohn's disease, one form of IBD, appears to involve an exagerated T helper-1 (Th1) lymphocyte phenotype, characterised by production of interleukin (IL)-2 and interferon (IFN)-?, that drives the inflammation. To examine whether SCFA influence pro- and anti-inflammatory cytokine production, rat mesenteric lymph node lymphocytes were cultured in the presence of acetate (10 mM), butyrate (1.5 mM) or propionate (2 mM) and the production of cytokines in response to concanavalin A determined. Butyrate, but not acetate or propionate, inhibited lymphocyte proliferation and IL-2 production. Acetate and propionate were able to partly prevent the inhibitory effect of butyrate on IL-2 production. Acetate and propionate increased IFN-? production, whereas butyrate inhibited it. Acetate and propionate in combination were able to prevent the inhibitory effect of butyrate on IFN-? production. IL-4 was not detected in any cultures. Acetate and propionate increased IL-10 production, which was not affected by butyrate. It is concluded that butyrate significantly inhibits Th1-type responses and that this might explain the therapeutic effect of butyrate in IBD patients. Acetate and propionate have less marked modulatory actions, and in some cases have effects that oppose those of butyrate. A combination of the three SCFA causes a shift in the T helper lymphocyte phenotype towards a more anti-inflammatory phenotype and this might explain the protective effects of fiber.

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More information

Published date: 2003
Keywords: lymphocyte, cytokine, short-chain fatty acid, lymphocyte proliferation

Identifiers

Local EPrints ID: 25351
URI: http://eprints.soton.ac.uk/id/eprint/25351
ISSN: 0024-3205
PURE UUID: 2db6d2c2-8ca1-4e58-9916-9fe02424cfc1
ORCID for Elizabeth A. Miles: ORCID iD orcid.org/0000-0002-8643-0655
ORCID for Philip C. Calder: ORCID iD orcid.org/0000-0002-6038-710X

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Date deposited: 10 Apr 2006
Last modified: 09 Jan 2022 02:49

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Author: Claudia R. Cavaglieri
Author: Anita Nishiyama
Author: Luis Claudio Fernandes
Author: Rui Curi

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