Efecto del consumo de la fibra dietética en la expresión cuantitativa del receptor de butirato GPR43 en colon de ratas

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Abstract

Introducción: Los ácidos grasos de cadena corta (AGCC) acetato, propionato y butirato, son productos de fermentación de la fibra dietética (FD) en el intestino grueso. Recientemente, el butirato ha sido estudiado ya que es considerado indispensable para el mantenimiento de las funciones del colon y por su relación con la protección del cáncer colorrectal. Esto se atribuye a la capacidad de butirato de regular la expresión génica por mecanismos como la inhibición de la enzima histona deacetilasa. Se ha reportado que el receptor de AGCC, GPR43 está involucrado en el proceso de transducción de señales intracelulares una vez que se unen a ligandos como butirato para generar los efectos fisiológicos del butirato en los colonocitos. Objetivo: Determinar si el consumo de FD de nopal (Opuntia ficus I) tiene influencia directa sobre la expresión cuantitativa del receptor específico de butirato GPR43. Métodos: Ratas adultas Wistar se sometieron a cuatro diferentes dietas variando el contenido de FD en 0, 5, 15 y 25% de FD denopal, respectivamente. Resultados y discusión: Los resultados mostraron un aumento significativo de la expresión relativa de GPR43 (93,1%) cuando se suministró a las ratas una dieta conteniendo 5% de FD de nopal, usando como gen de referencia β-actina. Los resultados de esta investigación aportarán nuevos datos a los estudios que determinan la relación de la dieta con la salud intestinal, con el fin de ampliar el conocimiento sobre los efectos del ácido butírico en las funciones colónicas.

Translated abstract

Introduction: Short chain fatty acids (SCFA) acetate, propionate and butyrate are the major anions produced by the bacterial fermentation of dietary fiber (DF) in colon. Recently, butyrate has been recently studied because is important to maintain colonic functions and because it has been related with a protective effect in colorectal cancer, which is mainly, explained by its potential to regulate gene expression by inhibiting enzyme histonedeacetylase (HDAC). Several investigationsshown that SCFAreceptor GPR43 is involved insignal transduction mechanisms once they bind to ligands such as butyrate to generate different physiological effects in colonocytes. Objective: Determine if dietary fiber consumption from nopal (Opuntia ficus I.) containing a ratio of soluble-insoluble fiber 40/60, has a direct influence on the quantitative expression of butyrate-specific receptor GPR43. Methods: Wistar rats were fed with four different diets formulated at different concentrations of dietary fiber of 0, 5, 15 and 25% of dietary fiber from opuntia, respectively. Results and discussion: The results shown an increase in the expression of GPR43 (93.1%) when rats was fed with a 5% fiber diet, using β-actin as a reference gene. The results of this investigation will contribute to determinate the relation of diet with intestinal health for the purpose of expanding the knowledge of butyric acid on colonic functions.

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Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation.

Emmanuel Le Poul, Cécile Loison, Sofie Struyf … (2003)

Short chain fatty acids (SCFAs), including acetate, propionate, and butyrate, are produced at high concentration by bacteria in the gut and subsequently released in the bloodstream. Basal acetate concentrations in the blood (about 100 microm) can further increase to millimolar concentrations following alcohol intake. It was known previously that SCFAs can activate leukocytes, particularly neutrophils. In the present work, we have identified two previously orphan G protein-coupled receptors, GPR41 and GPR43, as receptors for SCFAs. Propionate was the most potent agonist for both GPR41 and GPR43. Acetate was more selective for GPR43, whereas butyrate and isobutyrate were more active on GPR41. The two receptors were coupled to inositol 1,4,5-trisphosphate formation, intracellular Ca2+ release, ERK1/2 activation, and inhibition of cAMP accumulation. They exhibited, however, a differential coupling to G proteins; GPR41 coupled exclusively though the Pertussis toxin-sensitive Gi/o family, whereas GPR43 displayed a dual coupling through Gi/o and Pertussis toxin-insensitive Gq protein families. The broad expression profile of GPR41 in a number of tissues does not allow us to infer clear hypotheses regarding its biological functions. In contrast, the highly selective expression of GPR43 in leukocytes, particularly polymorphonuclear cells, suggests a role in the recruitment of these cell populations toward sites of bacterial infection. The pharmacology of GPR43 matches indeed the effects of SCFAs on neutrophils, in terms of intracellular Ca2+ release and chemotaxis. Such a neutrophil-specific SCFA receptor is potentially involved in the development of a variety of diseases characterized by either excessive or inefficient neutrophil recruitment and activation, such as inflammatory bowel diseases or alcoholism-associated immune depression. GPR43 might therefore constitute a target allowing us to modulate immune responses in these pathological situations.

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W E W Roediger (1980)

Suspensions of isolated epithelial cells (colonocytes) from the human colon were used to assess utilisation of respiratory fuels which are normally available to the colonic mucosa in vivo. Cells were prepared from operative specimens of the ascending colon (seven) and descending colon (seven). The fuels that were used were the short chain fatty acid n-butyrate, produced only by anaerobic bacteria in the colonic lumen, together with glucose and glutamine, normally present in the circulation. The percentage oxygen consumption attributable to n-butyrate, when this was the only substrate, was 73% in the ascending colon and 75% in the descending colon. In the presence of 10 mM glucose these proportions changed to 59% and 72%. Aerobic glycolysis was observed in both the ascending and descending colon. Glucose oxidation accounted for 85% of the oxygen consumption in the ascending colon and 30% in the descending colon. In the presence of 10 mM n-butyrate these proportions decreased to 41% in the ascending colon and 16% in the descending colon. Based on the assumption that events in the isolated colonocytes reflect utilization of fuels in vivo, the hypothesis is put forward that fatty acids of anaerobic bacteria are a major source of energy for the colonic mucosa, particularly of the distal colon.

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Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose.

P Jäger, E Gaudier, C Cherbut … (2004)

The mucus layer covering the gastrointestinal mucosa is considered the first line of defense against aggressions arising from the luminal content. It is mainly composed of high molecular weight glycoproteins called mucins. Butyrate, a short-chain fatty acid produced during carbohydrate fermentation, has been shown to increase mucin secretion. The aim of this study was to test 1) whether butyrate regulates the expression of various MUC genes, which are coding for protein backbones of mucins, and 2) whether this effect depends on butyrate status as the major energy source of colonocytes. Butyrate was provided at the apical side of human polarized colonic goblet cell line HT29-Cl.16E in glucose-rich or glucose-deprived medium. In glucose-rich medium, butyrate significantly increased MUC3 and MUC5B expression (1.6-fold basal level for both genes), tended to decrease MUC5AC expression, and had no effect on MUC2 expression. In glucose-deprived medium, i.e., when butyrate was the only energy source available, MUC3 and MUC5B increase persisted, whereas MUC5AC expression was significantly enhanced (3.7-fold basal level) and MUC2 expression was strikingly increased (23-fold basal level). Together, our findings show that butyrate is able to upregulate colonic mucins at the transcriptional level and even better when it is the major energy source of the cells. Thus the metabolism of butyrate in colonocytes is closely linked to some of its gene-regulating effects. The distinct effects of butyrate according to the different MUC genes could influence the composition and properties of the mucus gel and thus its protective function.