Resistant starch can improve insulin sensitivity independently of the gut microbiota

Laure B. Bindels, Rafael R. Segura Munoz, João Carlos Gomes-Neto, Valentin Mutemberezi, Inés Martínez, Nuria Salazar, Elizabeth A. Cody, Maria I. Quintero-Villegas, Hatem Kittana, Clara G. de los Reyes-Gavilán, Robert J. Schmaltz, Giulio G. Muccioli, Jens Walter, Amanda E. Ramer-Tait

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

Background: Obesity-related diseases, including type 2 diabetes and cardiovascular disease, have reached epidemic proportions in industrialized nations, and dietary interventions for their prevention are therefore important. Resistant starches (RS) improve insulin sensitivity in clinical trials, but the mechanisms underlying this health benefit remain poorly understood. Because RS fermentation by the gut microbiota results in the formation of physiologically active metabolites, we chose to specifically determine the role of the gut microbiota in mediating the metabolic benefits of RS. To achieve this goal, we determined the effects of RS when added to a Western diet on host metabolism in mice with and without a microbiota. Results: RS feeding of conventionalized mice improved insulin sensitivity and redressed some of the Western diet-induced changes in microbiome composition. However, parallel experiments in germ-free littermates revealed that RS-mediated improvements in insulin levels also occurred in the absence of a microbiota. RS reduced gene expression of adipose tissue macrophage markers and altered cecal concentrations of several bile acids in both germ-free and conventionalized mice; these effects were strongly correlated with the metabolic benefits, providing a potential microbiota-independent mechanism to explain the physiological effects of RS. Conclusions: This study demonstrated that some metabolic benefits exerted by dietary RS, especially improvements in insulin levels, occur independently of the microbiota and could involve alterations in the bile acid cycle and adipose tissue immune modulation. This work also sets a precedent for future mechanistic studies aimed at establishing the causative role of the gut microbiota in mediating the benefits of bioactive compounds and functional foods.

Original languageEnglish (US)
Article number12
JournalMicrobiome
Volume5
Issue number1
DOIs
StatePublished - Jan 1 2017

Fingerprint

Starch
Insulin Resistance
Microbiota
Bile Acids and Salts
Adipose Tissue
Insulin
Gastrointestinal Microbiome
Functional Food
Insurance Benefits
Developed Countries
Type 2 Diabetes Mellitus
Fermentation
Cardiovascular Diseases
Obesity
Macrophages
Clinical Trials
Gene Expression

Keywords

  • Adipose tissue macrophages
  • Gut microbiota
  • Insulin sensitivity
  • Resistant starch

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Bindels, L. B., Segura Munoz, R. R., Gomes-Neto, J. C., Mutemberezi, V., Martínez, I., Salazar, N., ... Ramer-Tait, A. E. (2017). Resistant starch can improve insulin sensitivity independently of the gut microbiota. Microbiome, 5(1), [12]. https://doi.org/10.1186/s40168-017-0230-5

Resistant starch can improve insulin sensitivity independently of the gut microbiota. / Bindels, Laure B.; Segura Munoz, Rafael R.; Gomes-Neto, João Carlos; Mutemberezi, Valentin; Martínez, Inés; Salazar, Nuria; Cody, Elizabeth A.; Quintero-Villegas, Maria I.; Kittana, Hatem; de los Reyes-Gavilán, Clara G.; Schmaltz, Robert J.; Muccioli, Giulio G.; Walter, Jens; Ramer-Tait, Amanda E.

In: Microbiome, Vol. 5, No. 1, 12, 01.01.2017.

Research output: Contribution to journalArticle

Bindels, LB, Segura Munoz, RR, Gomes-Neto, JC, Mutemberezi, V, Martínez, I, Salazar, N, Cody, EA, Quintero-Villegas, MI, Kittana, H, de los Reyes-Gavilán, CG, Schmaltz, RJ, Muccioli, GG, Walter, J & Ramer-Tait, AE 2017, 'Resistant starch can improve insulin sensitivity independently of the gut microbiota', Microbiome, vol. 5, no. 1, 12. https://doi.org/10.1186/s40168-017-0230-5
Bindels LB, Segura Munoz RR, Gomes-Neto JC, Mutemberezi V, Martínez I, Salazar N et al. Resistant starch can improve insulin sensitivity independently of the gut microbiota. Microbiome. 2017 Jan 1;5(1). 12. https://doi.org/10.1186/s40168-017-0230-5
Bindels, Laure B. ; Segura Munoz, Rafael R. ; Gomes-Neto, João Carlos ; Mutemberezi, Valentin ; Martínez, Inés ; Salazar, Nuria ; Cody, Elizabeth A. ; Quintero-Villegas, Maria I. ; Kittana, Hatem ; de los Reyes-Gavilán, Clara G. ; Schmaltz, Robert J. ; Muccioli, Giulio G. ; Walter, Jens ; Ramer-Tait, Amanda E. / Resistant starch can improve insulin sensitivity independently of the gut microbiota. In: Microbiome. 2017 ; Vol. 5, No. 1.
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AU - Segura Munoz, Rafael R.

AU - Gomes-Neto, João Carlos

AU - Mutemberezi, Valentin

AU - Martínez, Inés

AU - Salazar, Nuria

AU - Cody, Elizabeth A.

AU - Quintero-Villegas, Maria I.

AU - Kittana, Hatem

AU - de los Reyes-Gavilán, Clara G.

AU - Schmaltz, Robert J.

AU - Muccioli, Giulio G.

AU - Walter, Jens

AU - Ramer-Tait, Amanda E.

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N2 - Background: Obesity-related diseases, including type 2 diabetes and cardiovascular disease, have reached epidemic proportions in industrialized nations, and dietary interventions for their prevention are therefore important. Resistant starches (RS) improve insulin sensitivity in clinical trials, but the mechanisms underlying this health benefit remain poorly understood. Because RS fermentation by the gut microbiota results in the formation of physiologically active metabolites, we chose to specifically determine the role of the gut microbiota in mediating the metabolic benefits of RS. To achieve this goal, we determined the effects of RS when added to a Western diet on host metabolism in mice with and without a microbiota. Results: RS feeding of conventionalized mice improved insulin sensitivity and redressed some of the Western diet-induced changes in microbiome composition. However, parallel experiments in germ-free littermates revealed that RS-mediated improvements in insulin levels also occurred in the absence of a microbiota. RS reduced gene expression of adipose tissue macrophage markers and altered cecal concentrations of several bile acids in both germ-free and conventionalized mice; these effects were strongly correlated with the metabolic benefits, providing a potential microbiota-independent mechanism to explain the physiological effects of RS. Conclusions: This study demonstrated that some metabolic benefits exerted by dietary RS, especially improvements in insulin levels, occur independently of the microbiota and could involve alterations in the bile acid cycle and adipose tissue immune modulation. This work also sets a precedent for future mechanistic studies aimed at establishing the causative role of the gut microbiota in mediating the benefits of bioactive compounds and functional foods.

AB - Background: Obesity-related diseases, including type 2 diabetes and cardiovascular disease, have reached epidemic proportions in industrialized nations, and dietary interventions for their prevention are therefore important. Resistant starches (RS) improve insulin sensitivity in clinical trials, but the mechanisms underlying this health benefit remain poorly understood. Because RS fermentation by the gut microbiota results in the formation of physiologically active metabolites, we chose to specifically determine the role of the gut microbiota in mediating the metabolic benefits of RS. To achieve this goal, we determined the effects of RS when added to a Western diet on host metabolism in mice with and without a microbiota. Results: RS feeding of conventionalized mice improved insulin sensitivity and redressed some of the Western diet-induced changes in microbiome composition. However, parallel experiments in germ-free littermates revealed that RS-mediated improvements in insulin levels also occurred in the absence of a microbiota. RS reduced gene expression of adipose tissue macrophage markers and altered cecal concentrations of several bile acids in both germ-free and conventionalized mice; these effects were strongly correlated with the metabolic benefits, providing a potential microbiota-independent mechanism to explain the physiological effects of RS. Conclusions: This study demonstrated that some metabolic benefits exerted by dietary RS, especially improvements in insulin levels, occur independently of the microbiota and could involve alterations in the bile acid cycle and adipose tissue immune modulation. This work also sets a precedent for future mechanistic studies aimed at establishing the causative role of the gut microbiota in mediating the benefits of bioactive compounds and functional foods.

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