Effects of dietary oat bran and diabetes on plasma and caecal volatile fatty acids in the rat

Storer, Gerald B.; Trimble, Rodney P.; Illman, Richard J.; Snoswell, Alan M.; Topping, David L.

doi:10.1016/s0271-5317(83)80013-x

Cited by 36 publications

(25 citation statements)

References 14 publications

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“…Using physiologic pH and blood level concentrations (14) for treatment, we compared the ability of SCFAs with different carbon chain lengths or biologically relevant structural analogs of SB to induce neurotransmitterrelated gene expression in our model system (9). PC12 cells were treated with vehicle or with 1 mM of each SCFA or an SB derivative.…”

Section: Resultsmentioning

confidence: 99%

“…To further define the requirements for the effect of different SCFAs on neurotransmitter-related gene expression, we performed concentration-dependence studies. The capacity of SB and propionate to alter neurotransmitter gene expression was compared at low (1 mM), physiologic concentrations (7,14) and at relatively high (6 mM) doses (Fig. 2).…”

Section: Metabolic Regulation Of Neuronal Genesmentioning

confidence: 99%

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Stereospecific Regulation of Tyrosine Hydroxylase and Proenkephalin Genes by Short-Chain Fatty Acids in Rat PC12 Cells

et al. 2004

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Circulating short-chain fatty acids (SCFAs) are primarily derived from bacterial fermentation of carbohydrates in the colon where they function as physiologic modulators of epithelial cell maturation. Butyrate has been shown to induce tyrosine hydroxylase, the rate-limiting enzyme of catecholamine synthesis, and enkephalin neuropeptide gene transcription, suggesting a role in perinatal sympathoadrenal stress-adaptation. We sought to determine whether there were SCFA structural requirements for this effect. Nine biologically relevant SCFAs and butyrate derivatives were tested in an in vitro model (PC12, rat pheochromocytoma cells) for their ability to regulate neurotransmitter-related gene expression. Our results revealed that among all the studied SCFAs, only propionate and butyrate increased tyrosine hydroxylase and proenkephalin mRNA levels. The functional activity was selective to the carbon atom chain length and associated with the presence of an ethyl moiety in the carbon atom backbone chain. Modifications or absence of this domain affected the gene induction response, suggesting a receptor-mediated mechanism(s). Moreover, propionate, butyrate, and the drug 4-phenylbutyrate were each shown to regulate transmitter genes via at least three independent mechanisms: histone hyperacetylation, cAMP signaling, or peroxisome proliferator-activated receptor gamma-mediated pathways. Thus, the biologic impact of SCFAs on catecholaminergic and opioid systems depend on the activation of SCFA-specific, dose-specific, and gene-specific molecular mechanisms. We speculate that 1) circulating levels of SCFAs may influence sympathoadrenal transmitter biosynthesis and hence whole animal stress-adaptive responsiveness after birth, and 2) the adverse effects of antibiotics on delayed acquisition of postnatal gut flora may affect this apparent evolutionary advantage of gut colonization. Sympathoadrenal transmitter systems mature to adult capacity a week or more after birth in response to progressive cholinergic innervation, exposure to growth factors, and hormonal influences from both the hypothalamic-pituitary-adrenal cortical and thyroid hormonal systems (1-6). Although the importance of these conventional control mechanisms is well established, the evolutionary significance of other exogenous stimuli can be considered in a broader view of environmentally derived signal-transduction. For example, the delayed period of adrenal transmitter accumulation after birth coincides with the time taken to establish full enteral feedings, colonization of the intestine, and attendant production of SCFA (7). Moreover, in the rat (as well as in humans), this time frame is far longer than the capacity of the chromaffin cell to rapidly induce biosynthesis of either catecholamines or enkephalins, which can occur in a matter of hours (8)

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Section: Resultsmentioning

confidence: 99%

Section: Metabolic Regulation Of Neuronal Genesmentioning

confidence: 99%

Stereospecific Regulation of Tyrosine Hydroxylase and Proenkephalin Genes by Short-Chain Fatty Acids in Rat PC12 Cells

et al. 2004

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“…A number of cell wall polysaccharides and gums that are constituents of dietary plant fibre do not completely survive transit through the gastrointestinal tract of humans and other omnivores such as the rat and pig (for a brief review, see Topping & Illman, 1986). In these species, the breakdown of such polysaccharides is effected through a bacterial fermentation, especially in the large bowel, which closely resembles that occurring in the rumen and with similar end-products, the volatile fatty acids (VFA) acetate, propionate and butyrate (Remesy et al 1980; Argenzio & Stevens, 1984).…”

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confidence: 99%

“…Thus cellulose has been reported to be a relatively poor substrate, whereas non-cellulosic polysaccharides such as pectins and (1 + 3,l -+ 4)-P-glucans are extensively degraded. Lignin, which is a complex polyphenolic polymer that is a component of certain plant cell walls, passes through the gastrointestinal tract almost completely unaltered (Topping & Illman, 1986).…”

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confidence: 99%

Comparative effects of dietary wheat bran and its morphological components (aleurone and pericarp-seed coat) on volatile fatty acid concentrations in the rat

et al. 1987

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1. Adult male rats were fed on diets containing 100 g dietary fibre/kg either as a-cellulose or wheat bran or the pericarp-seed coat or aleurone layers prepared from that bran by sequential milling and air elutriation and electrostatic separation.2. After 10 d, concentrations of total volatile fatty acids (VFA) in caecal fluid were significantly different between groups and fell in the order: aleurone > wheat bran > pericarp-seed coat > cellulose. This ranking probably reflected the ease of fermentation of fibre polysaccharides by colonic bacteria which also resulted in a considerably higher faecal bacterial mass in the aleurone group.3. Because of the differences in the volume ofcaecal digesta, the mass of caecal VFA was considerably the highest in the aleurone group, intermediate with wheat bran and equally low in the pericarp-seed coat and cellulose groups.4. The diet based on aleurone gave a relatively higher proportion of propionate but with both pericarp-seed coat and wheat bran the contribution of butyrate was raised.5. VFA concentrations in hepatic portal venous plasma were proportional to caecal concentrations with very high (> 3 mM) values being recorded in the aleurone group.6. The findings are discussed in relation to the apparent susceptibility of the morphological components of wheat bran to fermentation by large bowel bacteria.

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“…Moreover, because the blood content of SCFA in rats is found to be at least 1-2 mM (62), its in vivo effect is in the physiologic range with the concentrations of butyrate used in our in vitro study. Therefore, it is attractive to speculate that plasma butyrate may act as a postnatal humoral regulatory factor in vivo by aiding maturation of the autonomic nervous system through an interaction with the more classically defined cholinergic (transsynaptic nicotinic) mechanisms.…”

Section: Discussionmentioning

confidence: 84%

Nicotinic Induction of Preproenkephalin and Tyrosine Hydroxylase Gene Expression in Butyrate-Differentiated Rat PC12 Cells: A Model for Adaptation to Gut-Derived Environmental Signals

Nankova

2003

Pediatric Research

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Accelerated maturation of peripheral sympathoadrenal transmitter levels and function occurs at 7-10 postnatal days in the rat. This event is temporally disconnected from the timing of major changes in physiologic stimuli evident after the birthing process (i.e. temperature, oxygen, sound, light, etc.). Colonization of the gut, fermentation of carbohydrates, and production of short-chain fatty acids (e.g. butyrate) mirrors this postnatal time course. In this report, we examined the interaction between butyrate differentiation of rat pheochromocytoma cells and cholinergicnicotinic induction of the neuropeptide (enkephalin) and catecholamine-related biosynthetic enzymes (tyrosine hydroxylase, dopamine ␤-hydroxylase, phenylethanolamine N-methyltransferase). Our results show that butyrate induces both preproenkephalin and tyrosine hydroxylase mRNA through a proximal promoter region and that this regulatory step is time and dose dependent. Moreover, there is an additional interaction with cholinergic-nicotinic inducible mechanisms consistent with classically described transsynaptic cholinergic regulation of these genes. Dopamine ␤-hydroxylase and phenylethanolamine Nmethyltransferase promoters were not affected by butyrate treatment. We speculate that colonization of the human gut (along with the attendant fermentation of enteral carbohydrates to shortchain fatty acids) may represent a mechanism through which environmental signals affect postnatal maturation of sympathoadrenal transmitter systems. Abbreviations ppENK, preproenkephalin pRPE2, enkephalin gene coding sequence plasmid pREJCAT, enkephalin promoter reporter plasmid TH, tyrosine hydroxylase DBH, dopamine ␤-hydroxylase PNMT, phenylethanolamine N-methyltransferase CAT, chloramphenicol acetyltransferase PC12, rat pheochromocytoma SCFA, short-chain fatty acids NaBtr, sodium butyrate Circulating catecholamines and endogenous opioid peptides arise primarily from the adrenal medulla (1, 2), where they are co-stored and co-released from chromaffin cells (3). In rats, between 7 and 10 days of postnatal life, adrenal transmitter biosynthetic and release mechanisms mature to adult capacity in response to progressive cholinergic innervation, and as a result of the influences of the hypothalamic-pituitary-adrenal cortical and thyroid hormonal systems (4 -13). Because a progressive rise in systemic blood pressure and autonomic reflex responsiveness is well characterized in the first postnatal week in humans (11), similar control mechanisms are thought to apply. Paradoxically, it is well recognized that adrenal transmitter systems can adapt rapidly to change steady-state levels of transmitter-related mRNA in as little as a few hours, not typically a few days (14 -17

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Effects of dietary oat bran and diabetes on plasma and caecal volatile fatty acids in the rat

Cited by 36 publications

References 14 publications

Stereospecific Regulation of Tyrosine Hydroxylase and Proenkephalin Genes by Short-Chain Fatty Acids in Rat PC12 Cells

Stereospecific Regulation of Tyrosine Hydroxylase and Proenkephalin Genes by Short-Chain Fatty Acids in Rat PC12 Cells

Comparative effects of dietary wheat bran and its morphological components (aleurone and pericarp-seed coat) on volatile fatty acid concentrations in the rat

Nicotinic Induction of Preproenkephalin and Tyrosine Hydroxylase Gene Expression in Butyrate-Differentiated Rat PC12 Cells: A Model for Adaptation to Gut-Derived Environmental Signals

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