Role of the Lower and Upper Intestine in the Production and Absorption of Gut Microbiota-derived PUFA Metabolites

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 Jan 30

PMID 24475308

Citations 39

Authors

Celine Druart

Audrey M Neyrinck

Bruno Vlaeminck

Veerle Fievez

Patrice D Cani

Nathalie M Delzenne

Affiliations

Soon will be listed here.

Abstract

In vitro studies have suggested that isolated gut bacteria are able to metabolize PUFA into CLA (conjugated linoleic acids) and CLnA (conjugated linolenic acids). However, the bioavailability of fatty acid metabolites produced in vivo by the gut microbes remains to be studied. Therefore, we measured intestinal concentration and plasma accumulation of bacterial metabolites produced from dietary PUFA in mice, first injected with a lipoprotein lipase inhibitor, then force-fed with either sunflower oil (200 µl) rich in n-6 PUFA or linseed oil (200 µl) rich in n-3 PUFA. The greatest production of bacterial metabolites was observed in the caecum and colon, and at a much lesser extent in the jejunum and ileum. In the caecal content, CLA proportions were higher in sunflower oil force-fed mice whereas CLnA proportions were higher in linseed oil force-fed mice. The accumulation of the main metabolites (CLA cis-9,trans-11-18:2 and CLnA cis-9,trans-11,cis-15-18:3) in the caecal tissue was not associated with their increase in the plasma, therefore suggesting that, if endogenously produced CLA and CLnA have any biological role in host metabolism regulation, their effect would be confined at the intestinal level, where the microbiota is abundant.

Citing Articles

A Swedish dietary guideline index, gut microbial α-diversity and prevalence of metabolic syndrome - observations in the Swedish CArdioPulmonary bioImage Study (SCAPIS).

Ericson U, Hellstrand S, Larsson A, Miari M, Sayols-Baixeras S, Dekkers K Food Nutr Res. 2024; 68.

PMID: 39691688 PMC: 11650442. DOI: 10.29219/fnr.v68.10547.

Antibiotics and probiotics-induced effects on the total fatty acid composition of feces in a rat model.

Marosvolgyi T, Mintal K, Farkas N, Sipos Z, Makszin L, Szabo E Sci Rep. 2024; 14(1):6542.

PMID: 38503819 PMC: 10951306. DOI: 10.1038/s41598-024-57046-6.

Immunomodulatory effect of marine lipids on food allergy.

Abril A, Carrera M, Pazos M Front Nutr. 2023; 10:1254681.

PMID: 38035353 PMC: 10683508. DOI: 10.3389/fnut.2023.1254681.

Identification of metabolic biomarkers of chronic vagus nerve stimulation (VNS) in subjects with drug-resistant epilepsy (DRE).

Manca C, Coa R, Murru E, Carta G, Pinna G, Sanfilippo R Epilepsia Open. 2023; 9(1):432-438.

PMID: 38016924 PMC: 10839364. DOI: 10.1002/epi4.12871.

Mechanism of Guilu Erxian ointment based on targeted metabolomics in intervening fertilization and embryo transfer outcome in older patients with poor ovarian response of kidney-qi deficiency type.

Ma Y, Song J, Cao X, Sun Z Front Endocrinol (Lausanne). 2023; 14:1045384.

PMID: 36742408 PMC: 9897313. DOI: 10.3389/fendo.2023.1045384.

References

Druart C, Neyrinck A, Dewulf E, De Backer F, Possemiers S, Van de Wiele T . Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice. Br J Nutr. 2013; 110(6):998-1011. DOI: 10.1017/S0007114513000123. View

Devillard E, McIntosh F, Duncan S, Wallace R . Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J Bacteriol. 2007; 189(6):2566-70. PMC: 1899373. DOI: 10.1128/JB.01359-06. View

OShea E, Cotter P, Stanton C, Ross R, Hill C . Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol. 2011; 152(3):189-205. DOI: 10.1016/j.ijfoodmicro.2011.05.025. View

Cotter P . Small intestine and microbiota. Curr Opin Gastroenterol. 2010; 27(2):99-105. DOI: 10.1097/MOG.0b013e328341dc67. View

Nicholson J, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W . Host-gut microbiota metabolic interactions. Science. 2012; 336(6086):1262-7. DOI: 10.1126/science.1223813. View

Zoetendal E, Raes J, van den Bogert B, Arumugam M, Booijink C, Troost F . The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 2012; 6(7):1415-26. PMC: 3379644. DOI: 10.1038/ismej.2011.212. View

Lerch S, Shingfield K, Ferlay A, Vanhatalo A, Chilliard Y . Rapeseed or linseed in grass-based diets: effects on conjugated linoleic and conjugated linolenic acid isomers in milk fat from Holstein cows over 2 consecutive lactations. J Dairy Sci. 2012; 95(12):7269-87. DOI: 10.3168/jds.2012-5654. View

Wang M, Ahrne S, Jeppsson B, Molin G . Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol. 2005; 54(2):219-31. DOI: 10.1016/j.femsec.2005.03.012. View

Churruca I, Fernandez-Quintela A, Portillo M . Conjugated linoleic acid isomers: differences in metabolism and biological effects. Biofactors. 2009; 35(1):105-11. DOI: 10.1002/biof.13. View

10.

Stefanov I, Baeten V, Abbas O, Colman E, Vlaeminck B, De Baets B . Analysis of milk odd- and branched-chain fatty acids using Fourier transform (FT)-Raman spectroscopy. J Agric Food Chem. 2010; 58(20):10804-11. DOI: 10.1021/jf102037g. View

11.

Kramer J, Hernandez M, Cruz-Hernandez C, Kraft J, Dugan M . Combining results of two GC separations partly achieves determination of all cis and trans 16:1, 18:1, 18:2 and 18:3 except CLA isomers of milk fat as demonstrated using Ag-ion SPE fractionation. Lipids. 2008; 43(3):259-73. DOI: 10.1007/s11745-007-3143-4. View

12.

Szentkuti L, Lorenz K . The thickness of the mucus layer in different segments of the rat intestine. Histochem J. 1995; 27(6):466-72. View

13.

Coakley M, Ross R, Nordgren M, Fitzgerald G, Devery R, Stanton C . Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. J Appl Microbiol. 2002; 94(1):138-45. DOI: 10.1046/j.1365-2672.2003.01814.x. View

14.

Cani P, Bibiloni R, Knauf C, Waget A, Neyrinck A, Delzenne N . Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008; 57(6):1470-81. DOI: 10.2337/db07-1403. View

15.

Coakley M, Banni S, Johnson M, Mills S, Devery R, Fitzgerald G . Inhibitory effect of conjugated alpha-linolenic acid from bifidobacteria of intestinal origin on SW480 cancer cells. Lipids. 2008; 44(3):249-56. DOI: 10.1007/s11745-008-3269-z. View

16.

Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Carbo A, Shaykhutdinov R . Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR γ to suppress colitis. PLoS One. 2012; 7(2):e31238. PMC: 3283634. DOI: 10.1371/journal.pone.0031238. View

17.

Schmidt J, Liebscher K, Merten N, Grundmann M, Mielenz M, Sauerwein H . Conjugated linoleic acids mediate insulin release through islet G protein-coupled receptor FFA1/GPR40. J Biol Chem. 2011; 286(14):11890-4. PMC: 3069391. DOI: 10.1074/jbc.C110.200477. View

18.

Or-Rashid M, AlZahal O, McBride B . Comparative studies on the metabolism of linoleic acid by rumen bacteria, protozoa, and their mixture in vitro. Appl Microbiol Biotechnol. 2010; 89(2):387-95. DOI: 10.1007/s00253-010-2865-z. View

19.

Evans M, Brown J, McIntosh M . Isomer-specific effects of conjugated linoleic acid (CLA) on adiposity and lipid metabolism. J Nutr Biochem. 2002; 13(9):508. DOI: 10.1016/s0955-2863(02)00211-5. View

20.

Miranda J, Lasa A, Fernandez-Quintela A, Garcia-Marzo C, Ayo J, Dentin R . cis-9,trans-11,cis-15 and cis-9,trans-13,cis-15 CLNA mixture activates PPARα in HEK293 and reduces triacylglycerols in 3T3-L1 cells. Lipids. 2011; 46(11):1005-12. DOI: 10.1007/s11745-011-3615-4. View