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. 2022 Jun 17:10:390-398.
doi: 10.1016/j.aninu.2022.06.003. eCollection 2022 Sep.

Propionate stimulates the secretion of satiety hormones and reduces acute appetite in a cecal fistula pig model

Yanan Zhang  1   2 , Xuan Li  1   2 , Guowen Huang  1   2 , Haifeng Wang  3 , Huizi Chen  1   2 , Yong Su  1   2 , Kaifan Yu  1   2 , Weiyun Zhu  1   2
Affiliations

Propionate stimulates the secretion of satiety hormones and reduces acute appetite in a cecal fistula pig model

Yanan Zhang et al. Anim Nutr. .

Abstract

Short-chain fatty acids (SCFA) can regulate appetite by stimulating the secretion of satiety hormones. However, the impact of short-chain fatty acid propionate on the release of gut satiety hormones and appetite regulation in pigs is not completely understood. In this study, 16 pigs were infused with saline or sodium propionate through a fistula in the caecum during a 28-day experimental period. We characterized the effects of propionate administration on peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) secretion from colonic tissue, and investigated the role of propionate infusion on the expression of appetite-related genes in the colon and hypothalamus. Further, the direct impact of propionate administration on the expression of orexigenic neuropeptide agouti-related protein (AgRP) in hypothalamic N38 cells was also examined. The results showed that intra-cecal infusion of propionate reduced the short-term feed intake (P < 0.05) but not the long-term feed intake in pigs (P > 0.05). Propionate administration stimulated PYY and GLP-1 release from colon tissue in vivo and ex vivo (P < 0.05). It also upregulated PYY expression in the colonic mucosa (P < 0.05). Meanwhile, the GLP-1 and PYY levels in the blood were increased after intra-cecal infusion of propionate at d 28 (P < 0.05). Additionally, intra-cecal infusion of propionate upregulated the mRNA and protein expression of free fatty acid receptor 2/3 (FFAR2/FFAR3) in the colonic mucosa (P < 0.05). Propionate infusion also downregulated the orexigenic AgRP mRNA expression (P < 0.05) and upregulated the anorexigenic cocaine-and amphetamine-regulated transcript (CART) mRNA expression (P = 0.09) in the hypothalamus. Moreover, propionate administration directly downregulated AgRP expression in hypothalamic N38 cells in a dose-dependent manner (P < 0.05). Collectively, these findings demonstrated that cecal propionate stimulated colonic secretion of satiety hormones and suppressed appetite to reduce the short-term feed intake in pigs. This study highlights that microbial-derived propionate exerts an important role in regulating the physical functions of the host.

Keywords: Appetite; Gut hormones; Hypothalamus; Pig; Propionate.

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Conflict of interest statement

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the content of this paper.

Figures

Fig. 1
Fig. 1
The effects of cecal infusion of propionate on (A) average daily gain, (B) feed intake, (C) feed-to-gain ratio, and (D) short-term feed intake in pigs. The data were expressed as mean ± SEM. ∗P < 0.05.
Fig. 2
Fig. 2
The effects of cecal infusion of propionate on the secretion of gastrointestinal hormones from colon tissue in pigs. (A) Glucagon-like peptide 1 (GLP-1); (B) peptide YY (PYY); (C) cholecystokinin (CCK); (D) insulin; (E) ghrelin. The data were expressed as mean ± SEM. ∗∗P < 0.01; ∗∗∗P < 0.001.
Fig. 3
Fig. 3
The effects of cecal infusion of propionate on (A) the mRNA expression of genes involved in free fatty acid receptors and appetite control and (B) the protein expression of free fatty acid receptors in the colonic mucosa. The data were expressed as mean ± SEM. ∗P < 0.05; ∗∗P < 0.01. FFAR2 = free fatty acid receptor 2; FFAR3 = free fatty acid receptor 3; GCG = glucagon; PYY = peptide YY; GLP-1R = glucagon-like-peptide-1 receptor.
Fig. 4
Fig. 4
The different levels of propionate stimulating (A) peptide YY (PYY) and (B) glucagon-like peptide 1 (GLP-1) secretion from colonic tissue ex vivo. The data were expressed as mean ± SEM. ∗P < 0.05; ∗∗P < 0.01.
Fig. 5
Fig. 5
The effects of cecal infusion of propionate on plasma gastrointestinal (GI) hormone concentration on d 7 (A to E) and d 28 (F to J). The data were expressed as mean ± SEM. ∗P < 0.05. GLP-1 = glucagon-like peptide 1; PYY = peptide YY; CCK = cholecystokinin.
Fig. 6
Fig. 6
The effects of propionate on the mRNA expression of (A) genes involved in appetite regulation in the hypothalamus of pigs and (B) AgRP in N38 cells. The data were expressed as mean ± SEM. ∗P < 0.05. AgRP = agouti-related protein; NPY = neuropeptide Y; POMC = pro-opiomelanocortin; CART = cocaine-amphetamine regulated transcript; GCG = glucagon; GLP-1R = glucagon-like-peptide-1 receptor.
Fig. 7
Fig. 7
The structure of the potential mechanism of intra-cecal infusion of propionate suppressing acute appetite in pigs. The black up and down arrows indicate an increase and decrease after propionate treatment, respectively. The solid and dashed arrows indicate direct and indirect processes, respectively. FFAR2 = free fatty acid receptor 2; FFAR3 = free fatty acid receptor 3; PYY = peptide YY; GLP-1 = glucagon-like peptide 1; AgRP = agouti-related protein.
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