The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents

Background and Objectives: The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite...

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Vydané v:International Journal of Obesity Ročník 39; číslo 3; s. 424 - 429
Hlavní autori: Psichas, A, Sleeth, M L, Murphy, K G, Brooks, L, Bewick, G A, Hanyaloglu, A C, Ghatei, M A, Bloom, S R, Frost, G
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: London Nature Publishing Group UK 01.03.2015
Nature Publishing Group
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ISSN:0307-0565, 1476-5497, 1476-5497
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Abstract Background and Objectives: The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice. Methods: We used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout (FFA −/− ) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro . We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate. Results: Propionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from FFA2 −/− mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in FFA2 −/− mice. Conclusions: Intra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo .
AbstractList The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice. We used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout (FFA(-/-)) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro. We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate. Propionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from FFA2(-/-) mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in FFA2(-/-) mice. Intra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo.
BACKGROUND AND OBJECTIVES: The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice. METHODS: We used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout ([FFA.sup.-/-]) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro. We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate. RESULTS: Propionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from [FFA2.sup.-/-] mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in [FFA2.sup.-/-] mice. CONCLUSIONS: Intra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo. International Journal of Obesity (2015) 39, 424-429; doi: 10.1038/ijo.2014.153
Background and Objectives:The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice.Methods:We used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout (FFA-/- ) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro. We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate.Results:Propionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from FFA2-/- mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in FFA2-/- mice.Conclusions:Intra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo.
The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice.BACKGROUND AND OBJECTIVESThe gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice.We used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout (FFA(-/-)) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro. We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate.METHODSWe used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout (FFA(-/-)) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro. We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate.Propionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from FFA2(-/-) mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in FFA2(-/-) mice.RESULTSPropionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from FFA2(-/-) mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in FFA2(-/-) mice.Intra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo.CONCLUSIONSIntra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo.
International Journal of Obesity (2015) 39, 424-429; doi: 10.1038/ijo.2014.153
Background and Objectives: The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid receptor 2 (FFA2) is present on colonic enteroendocrine L cells, and a role has been suggested for SCFAs in appetite regulation. Here, we characterise the in vitro and in vivo effects of colonic propionate on PYY and GLP-1 release in rodents, and investigate the role of FFA2 in mediating these effects using FFA2 knockout mice. Methods: We used Wistar rats, C57BL6 mice and free fatty acid receptor 2 knockout (FFA −/− ) mice on a C57BL6 background to explore the impact of the SCFA propionate on PYY and GLP-1 release. Isolated colonic crypt cultures were used to assess the effects of propionate on gut hormone release in vitro . We subsequently developed an in vivo technique to assess gut hormone release into the portal vein following colonic infusion of propionate. Results: Propionate stimulated the secretion of both PYY and GLP-1 from wild-type primary murine colonic crypt cultures. This effect was significantly attenuated in cultures from FFA2 −/− mice. Intra-colonic infusion of propionate elevated PYY and GLP-1 levels in jugular vein plasma in rats and in portal vein plasma in both rats and mice. However, propionate did not significantly stimulate gut hormone release in FFA2 −/− mice. Conclusions: Intra-colonic administration of propionate stimulates the concurrent release of both GLP-1 and PYY in rats and mice. These data demonstrate that FFA2 deficiency impairs SCFA-induced gut hormone secretion both in vitro and in vivo .
Audience Academic
Author Brooks, L
Murphy, K G
Bewick, G A
Frost, G
Ghatei, M A
Sleeth, M L
Psichas, A
Bloom, S R
Hanyaloglu, A C
Author_xml – sequence: 1
  givenname: A
  surname: Psichas
  fullname: Psichas, A
  organization: Division of Diabetes, Department of Medicine, Nutrition and Dietetic Research Group, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
– sequence: 2
  givenname: M L
  surname: Sleeth
  fullname: Sleeth, M L
  organization: Division of Diabetes, Department of Medicine, Nutrition and Dietetic Research Group, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
– sequence: 3
  givenname: K G
  surname: Murphy
  fullname: Murphy, K G
  organization: Division of Diabetes, Department of Medicine, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
– sequence: 4
  givenname: L
  surname: Brooks
  fullname: Brooks, L
  organization: Division of Diabetes, Department of Medicine, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
– sequence: 5
  givenname: G A
  surname: Bewick
  fullname: Bewick, G A
  organization: Division of Diabetes, Department of Medicine, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College, Division of Diabetes & Nutritional Sciences, Kings College London
– sequence: 6
  givenname: A C
  surname: Hanyaloglu
  fullname: Hanyaloglu, A C
  organization: Department of Surgery and Cancer, Institute of Reproductive and Developmental Biology, Imperial College
– sequence: 7
  givenname: M A
  surname: Ghatei
  fullname: Ghatei, M A
  organization: Division of Diabetes, Department of Medicine, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
– sequence: 8
  givenname: S R
  surname: Bloom
  fullname: Bloom, S R
  organization: Division of Diabetes, Department of Medicine, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
– sequence: 9
  givenname: G
  surname: Frost
  fullname: Frost, G
  email: g.frost@imperial.ac.uk
  organization: Division of Diabetes, Department of Medicine, Nutrition and Dietetic Research Group, Section of Investigative Medicine, Endocrinology and Metabolism, Imperial College
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25109781$$D View this record in MEDLINE/PubMed
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Snippet Background and Objectives: The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA)...
The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA) receptor, free fatty acid...
BACKGROUND AND OBJECTIVES: The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA)...
International Journal of Obesity (2015) 39, 424-429; doi: 10.1038/ijo.2014.153
Background and Objectives:The gut hormones peptide YY (PYY) and glucagon-like peptide 1 (GLP-1) acutely suppress appetite. The short chain fatty acid (SCFA)...
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SubjectTerms 13
13/106
631/443/163
631/443/319
631/45/287/1183
631/45/776/198
631/80/86
64
64/110
Animals
Appetite
Biological control systems
Colon - metabolism
Colon - pathology
Diabetes
Diet
Endocrinology
Epidemiology
Fatty acids
Gastrointestinal hormones
Gastrointestinal Hormones - metabolism
Glucagon
Glucagon-Like Peptide 1 - drug effects
Glucagon-Like Peptide 1 - metabolism
Glucose
Health Promotion and Disease Prevention
Hormones
Internal Medicine
Measurement
Medical research
Medicine
Medicine & Public Health
Metabolic Diseases
Metabolism
Mice
Mice, Inbred C57BL
Microbiota
Nutrients
Nutrition research
Obesity
Original
original-article
Peptide YY - metabolism
Peptides
Physiological research
Properties
Propionates - pharmacology
Public Health
Rats
Rats, Wistar
Receptors, G-Protein-Coupled - drug effects
Receptors, G-Protein-Coupled - metabolism
Rodents
Small intestine
Weight control
Title The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents
URI https://link.springer.com/article/10.1038/ijo.2014.153
https://www.ncbi.nlm.nih.gov/pubmed/25109781
https://www.proquest.com/docview/1661605682
https://www.proquest.com/docview/1662431580
https://pubmed.ncbi.nlm.nih.gov/PMC4356745
Volume 39
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