Skip to main content Accessibility help
×
Home

Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice

  • Céline Druart (a1), Audrey M. Neyrinck (a1), Evelyne M. Dewulf (a1), Fabienne C. De Backer (a1), Sam Possemiers (a2), Tom Van de Wiele (a2), Frédéric Moens (a3), Luc De Vuyst (a3), Patrice D. Cani (a1), Yvan Larondelle (a4) and Nathalie M. Delzenne (a1)...

Abstract

In vitro experiments have shown that isolated human gut bacteria are able to metabolise PUFA into conjugated PUFA like conjugated linoleic acids (CLA). The hypothesis of the present paper was that high-fat (HF) diet feeding and supplementation with fermentable carbohydrates that have prebiotic properties modulate the in vivo production of CLA by the mouse gut microbiota. Mice were treated for 4 weeks as follows: control (CT) groups were fed a standard diet; HF groups were fed a HF diet rich in linoleic acid (18 : 2n-6); the third groups were fed with the HF diet supplemented with either inulin-type fructans (HF-ITF) or arabinoxylans (HF-Ax). HF diet feeding increased rumenic acid (cis-9, trans-11-18 : 2 CLA) content both in the caecal and liver tissues compared with the CT groups. ITF supplementation had no major effect compared with the HF diet whereas Ax supplementation increased further rumenic acid (cis-9, trans-11-18 : 2 CLA) in the caecal tissue. These differences between both prebiotics may be linked to the high fat-binding capacity of Ax that provides more substrates for bacterial metabolism and to differential modulation of the gut microbiota (specific increase in Roseburia spp. in HF-Ax v. HF). In conclusion, these experiments supply the proof of concept that the mouse gut microbiota produces CLA in vivo, with consequences on the level of CLA in the caecal and liver tissues. We postulate that the CLA-producing bacteria could be a mediator to consider in the metabolic effects of both HF diet feeding and prebiotic supplementation.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Professor Nathalie M. Delzenne, fax +32 2 764 73 59, email nathalie.delzenne@uclouvain.be

References

Hide All
1Benjamin, S & Spener, F (2009) Conjugated linoleic acids as functional food: an insight into their health benefits. Nutr Metab (Lond) 6, 36.
2Churruca, I, Fernandez-Quintela, A & Portillo, MP (2009) Conjugated linoleic acid isomers: differences in metabolism and biological effects. Biofactors 35, 105111.
3Clément, L, Poirier, H, Niot, I, et al. (2002) Dietary trans-10, cis-12 conjugated linoleic acid induces hyperinsulinemia and fatty liver in the mouse. J Lipid Res 43, 14001409.
4Taylor, CG & Zahradka, P (2004) Dietary conjugated linoleic acid and insulin sensitivity and resistance in rodent models. Am J Clin Nutr 79, 1164S1168S.
5Stout, MB, Liu, LF & Belury, MA (2011) Hepatic steatosis by dietary-conjugated linoleic acid is accompanied by accumulation of diacylglycerol and increased membrane-associated protein kinase C epsilon in mice. Mol Nutr Food Res 55, 10101017.
6Chin, SF, Liu, W, Storkson, JM, et al. (1992) Dietary sources of conjugated dienoic isomers of linoleic acid, a newly recognized class of anticarcinogens. J Food Compos Anal 5, 185197.
7Jenkins, TC, Wallace, RJ, Moate, PJ, et al. (2008) Board-invited review: recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J Anim Sci 86, 397412.
8Bauman, DE, Baumgard, LH, Corl, BA, et al. (2000) Biosynthesis of conjugated linoleic acid in ruminants. J Anim Sci 77, 1ae15ae.
9Chilliard, Y, Glasser, F, Ferlay, A, et al. (2007) Diet, rumen biohydrogenation and nutritional quality of cow and goat milk fat. Eur J Lipid Sci Technol 109, 828855.
10Coakley, M, Ross, RP, Nordgren, M, et al. (2003) Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. J Appl Microbiol 94, 138145.
11Maia, MR, Chaudhary, LC, Bestwick, CS, et al. (2010) Toxicity of unsaturated fatty acids to the biohydrogenating ruminal bacterium, Butyrivibrio fibrisolvens. BMC Microbiol 10, 52.
12Griinari, JM, Corl, BA, Lacy, SH, et al. (2000) Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by Δ9-desaturase. J Nutr 130, 22852291.
13Turpeinen, AM, Mutanen, M, Aro, A, et al. (2002) Bioconversion of vaccenic acid to conjugated linoleic acid in humans. Am J Clin Nutr 76, 504510.
14Santora, JE, Palmquist, DL & Roehrig, KL (2000) Trans-vaccenic acid is desaturated to conjugated linoleic acid in mice. J Nutr 130, 208215.
15Cani, PD & Delzenne, NM (2011) The gut microbiome as therapeutic target. Pharmacol Ther 130, 202212.
16Devillard, E, McIntosh, FM, Duncan, SH, et al. (2007) Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J Bacteriol 189, 25662570.
17McIntosh, FM, Shingfield, KJ, Devillard, E, et al. (2009) Mechanism of conjugated linoleic acid and vaccenic acid formation in human faecal suspensions and pure cultures of intestinal bacteria. Microbiology 155, 285294.
18Barrett, E, Ross, RP, Fitzgerald, GF, et al. (2007) Rapid screening method for analyzing the conjugated linoleic acid production capabilities of bacterial cultures. Appl Environ Microbiol 73, 23332337.
19Rosberg-Cody, E, Ross, RP, Hussey, S, et al. (2004) Mining the microbiota of the neonatal gastrointestinal tract for conjugated linoleic acid-producing bifidobacteria. Appl Environ Microbiol 70, 46354641.
20Lee, HY, Park, JH, Seok, SH, et al. (2006) Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim Biophys Acta 1761, 736744.
21Macouzet, M, Robert, N & Lee, BH (2010) Genetic and functional aspects of linoleate isomerase in Lactobacillus acidophilus. Appl Microbiol Biotechnol 87, 17371742.
22Macouzet, M, Lee, BH & Robert, N (2010) Genetic and structural comparison of linoleate isomerases from selected food-grade bacteria. J Appl Microbiol 109, 21282134.
23Wall, R, Ross, RP, Shanahan, F, et al. (2009) Metabolic activity of the enteric microbiota influences the fatty acid composition of murine and porcine liver and adipose tissues. Am J Clin Nutr 89, 13931401.
24Chin, SF, Storkson, JM, Liu, W, et al. (1994) Conjugated linoleic acid (9,11- and 10,12-octadecadienoic acid) is produced in conventional but not germ-free rats fed linoleic acid. J Nutr 124, 694701.
25Delzenne, NM, Neyrinck, AM, Backhed, F, et al. (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7, 639646.
26Cani, PD, Neyrinck, AM, Fava, F, et al. (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50, 23742383.
27Cani, PD, Amar, J, Iglesias, MA, et al. (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 17611772.
28Dewulf, EM, Cani, PD, Neyrinck, AM, et al. (2011) Inulin-type fructans with prebiotic properties counteract GPR43 overexpression and PPARγ-related adipogenesis in the white adipose tissue of high-fat diet-fed mice. J Nutr Biochem 22, 712722.
29Neyrinck, AM, Possemiers, S, Druart, C, et al. (2011) Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS One 6, e20944.
30Samuel, BS, Shaito, A, Motoike, T, et al. (2008) Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A 105, 1676716772.
31Neish, AS (2009) Microbes in gastrointestinal health and disease. Gastroenterology 136, 6580.
32Roberfroid, M, Gibson, GR, Hoyles, L, et al. (2010) Prebiotic effects: metabolic and health benefits. Br J Nutr 104, Suppl. 2, S1S63.
33Cani, PD, Dewever, C & Delzenne, NM (2004) Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr 92, 521526.
34Cani, PD, Neyrinck, AM, Maton, N, et al. (2005) Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like peptide-1. Obes Res 13, 10001007.
35Delmee, E, Cani, PD, Gual, G, et al. (2006) Relation between colonic proglucagon expression and metabolic response to oligofructose in high fat diet-fed mice. Life Sci 79, 10071013.
36Everard, A, Lazarevic, V, Derrien, M, et al. (2011) Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60, 27752786.
37Cani, PD, Possemiers, S, Van de Wiele, T, et al. (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58, 10911103.
38Neyrinck, AM & Delzenne, NM (2010) Potential interest of gut microbial changes induced by non-digestible carbohydrates of wheat in the management of obesity and related disorders. Curr Opin Clin Nutr Metab Care 13, 722728.
39No, HK, Lee, SH, Park, NY, et al. (2003) Comparison of physicochemical, binding, and antibacterial properties of chitosans prepared without and with deproteinization process. J Agric Food Chem 51, 76597663.
40Possemiers, S, Bolca, S, Grootaert, C, et al. (2006) The prenylflavonoid isoxanthohumol from hops (Humulus lupulus L.) is activated into the potent phytoestrogen 8-prenylnaringenin in vitro and in the human intestine. J Nutr 136, 18621867.
41Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCt method. Methods 25, 402408.
42Alonso, L, Cuesta, EP & Gilliland, SE (2003) Production of free conjugated linoleic acid by Lactobacillus acidophilus and Lactobacillus casei of human intestinal origin. J Dairy Sci 86, 19411946.
43Devillard, E, McIntosh, FM, Paillard, D, et al. (2009) Differences between human subjects in the composition of the faecal bacterial community and faecal metabolism of linoleic acid. Microbiology 155, 513520.
44Gorissen, L, Raes, K, Weckx, S, et al. (2010) Production of conjugated linoleic acid and conjugated linolenic acid isomers by Bifidobacterium species. Appl Microbiol Biotechnol 87, 22572266.
45Coakley, M, Banni, S, Johnson, MC, et al. (2009) Inhibitory effect of conjugated α-linolenic acid from bifidobacteria of intestinal origin on SW480 cancer cells. Lipids 44, 249256.
46Hennessy, AA, Ross, RP, Devery, R, et al. (2011) The health promoting properties of the conjugated isomers of α-linolenic acid. Lipids 46, 105119.
47Park, HG, Cho, HT, Song, MC, et al. (2012) Production of a conjugated fatty acid by Bifidobacterium breve LMC520 from α-linolenic acid: conjugated linolenic acid (CLnA). J Agric Food Chem 60, 32043210.
48Burdge, GC & Calder, PC (2005) Conversion of α-linolenic acid to longer-chain polyunsaturated fatty acids in human adults. Reprod Nutr Dev 45, 581597.
49O'Shea, EF, Cotter, PD, Stanton, C, et al. (2012) Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol 152, 189205.
50Bauman, DE, Harvatine, KJ & Lock, AL (2011) Nutrigenomics, rumen-derived bioactive fatty acids, and the regulation of milk fat synthesis. Annu Rev Nutr 31, 299319.
51Lee, KN, Pariza, MW & Ntambi, JM (1998) Conjugated linoleic acid decreases hepatic stearoyl-CoA desaturase mRNA expression. Biochem Biophys Res Commun 248, 817821.
52Attie, AD, Krauss, RM, Gray-Keller, MP, et al. (2002) Relationship between stearoyl-CoA desaturase activity and plasma triglycerides in human and mouse hypertriglyceridemia. J Lipid Res 43, 18991907.
53Wall, R, Ross, RP, Shanahan, F, et al. (2010) Impact of administered Bifidobacterium on murine host fatty acid composition. Lipids 45, 429436.
54Wall, R, Marques, TM, O'Sullivan, O, et al. (2012) Contrasting effects of Bifidobacterium breve NCIMB 702258 and Bifidobacterium breve DPC 6330 on the composition of murine brain fatty acids and gut microbiota. Am J Clin Nutr 95, 12781287.
55Banni, S, Petroni, A, Blasevich, M, et al. (2004) Conjugated linoleic acids (CLA) as precursors of a distinct family of PUFA. Lipids 39, 11431146.
56Cho, HP, Nakamura, MT & Clarke, SD (1999) Cloning, expression, and nutritional regulation of the mammalian Δ-6 desaturase. J Biol Chem 274, 471477.
57Wang, Y, Botolin, D, Christian, B, et al. (2005) Tissue-specific, nutritional, and developmental regulation of rat fatty acid elongases. J Lipid Res 46, 706715.
58Nakamura, MT & Nara, TY (2004) Structure, function, and dietary regulation of Δ6, Δ5, and Δ9 desaturases. Annu Rev Nutr 24, 345376.
59Ogawa, J, Kishino, S, Ando, A, et al. (2005) Production of conjugated fatty acids by lactic acid bacteria. J Biosci Bioeng 100, 355364.
60Roche, HM, Noone, E, Sewter, C, et al. (2002) Isomer-dependent metabolic effects of conjugated linoleic acid: insights from molecular markers sterol regulatory element-binding protein-1c and LXRα. Diabetes 51, 20372044.
61Brown, JM, Boysen, MS, Jensen, SS, et al. (2003) Isomer-specific regulation of metabolism and PPARγ signaling by CLA in human preadipocytes. J Lipid Res 44, 12871300.
62Kohno, H, Suzuki, R, Yasui, Y, et al. (2004) Pomegranate seed oil rich in conjugated linolenic acid suppresses chemically induced colon carcinogenesis in rats. Cancer Sci 95, 481486.
63Yuan, G, Sun, H, Sinclair, AJ, et al. (2009) Effects of conjugated linolenic acid and conjugated linoleic acid on lipid metabolism in mice. Eur J Lipid Sci Technol 111, 537545.
64Ross, RP, Mills, S, Hill, C, et al. (2010) Specific metabolite production by gut microbiota as a basis for probiotic function. Int Dairy J 20, 269276.

Keywords

Type Description Title
UNKNOWN
Supplementary materials

Druart Supplemental Table 1. Body and tissue weights
Mice were fed a standard diet (CT), a high-fat diet (HF) or a high-fat diet and a supplementation with ITF (HF-ITF) or Ax (HF-Ax) after 4 weeks of dietary treatment. Data are mean ± SEM. Values in the same line with no common superscript letter are significantly different (p < 0.05) according to the Tukey’s post hoc ANOVA statistical analysis.

 Unknown (777 KB)
777 KB
UNKNOWN
Supplementary materials

Druart Supplemental Table 2. Fatty acid profile in the liver tissue.
Mice were fed a standard diet (CT), a high-fat diet (HF) or a high-fat diet and a supplementation with ITF (HF-ITF) or Ax (HF-Ax) after 4 weeks of dietary treatment. Results are expressed as a percentage of total identified fatty acids. Data are mean ± SEM. Values in the same line with no common superscript letter are significantly different (p < 0.05) according to the Tukey’s post hoc ANOVA statistical analysis.

 Unknown (2.3 MB)
2.3 MB
UNKNOWN
Supplementary materials

Druart Supplemental Table 3. Fatty acid profile in the caecal tissue.
Mice were fed a standard diet (CT), a high-fat diet (HF) or a high-fat diet and a supplementation with ITF (HF-ITF) or Ax (HF-Ax) after 4 weeks of dietary treatment. Results are expressed as a percentage of total identified fatty acids. Data are mean ± SEM. Values in the same line with no common superscript letter are significantly different (p < 0.05) according to the Tukey’s post hoc ANOVA statistical analysis.

 Unknown (2.3 MB)
2.3 MB

Implication of fermentable carbohydrates targeting the gut microbiota on conjugated linoleic acid production in high-fat-fed mice

  • Céline Druart (a1), Audrey M. Neyrinck (a1), Evelyne M. Dewulf (a1), Fabienne C. De Backer (a1), Sam Possemiers (a2), Tom Van de Wiele (a2), Frédéric Moens (a3), Luc De Vuyst (a3), Patrice D. Cani (a1), Yvan Larondelle (a4) and Nathalie M. Delzenne (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed