Leptin modifies the prosecretory and prokinetic effects of the inflammatory cytokine interleukin‐6 on colonic function in Sprague–Dawley rats
New Findings What is the central question of this study? Does crosstalk exist between leptin and interleukin‐6 in colonic enteric neurons, and is this a contributory factor in gastrointestinal dysfunction associated with irritable bowel syndrome? What is the main finding and its importance? Leptin a...
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Published in | Experimental physiology Vol. 101; no. 12; pp. 1477 - 1491 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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England
John Wiley & Sons, Inc
01.12.2016
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Abstract | New Findings
What is the central question of this study?
Does crosstalk exist between leptin and interleukin‐6 in colonic enteric neurons, and is this a contributory factor in gastrointestinal dysfunction associated with irritable bowel syndrome?
What is the main finding and its importance?
Leptin ameliorates the prosecretory and prokinetic effects of the pro‐inflammatory cytokine interleukin‐6 on rat colon. Leptin also suppresses the neurostimulatory effects of irritable bowel syndrome plasma, which has elevated concentrations of interleukin‐6, on enteric neurons. This may indicate a regulatory role for leptin in immune‐mediated bowel dysfunction.
In addition to its role in regulating energy homeostasis, the adipokine leptin modifies gastrointestinal (GI) function. Indeed, leptin‐resistant obese humans and leptin‐deficient obese mice exhibit altered GI motility. In the functional GI disorder irritable bowel syndrome (IBS), circulating leptin concentrations are reported to differ from those of healthy control subjects. Additionally, IBS patients display altered cytokine profiles, including elevated circulating concentrations of the pro‐inflammatory cytokine interleukin‐6 (IL‐6), which bears structural homology and similarities in intracellular signalling to leptin. This study aimed to investigate interactions between leptin and IL‐6 in colonic neurons and their possible contribution to IBS pathophysiology. The functional effects of leptin and IL‐6 on colonic contractility and absorptosecretory function were assessed in organ baths and Ussing chambers in Sprague–Dawley rat colon. Calcium imaging and immunohistochemical techniques were used to investigate the neural regulation of GI function by these signalling molecules. Our findings provide a neuromodulatory role for leptin in submucosal neurons, where it inhibited the stimulatory effects of IL‐6. Functionally, this translated to suppression of IL‐6‐evoked potentiation of veratridine‐induced secretory currents. Leptin also attenuated IL‐6‐induced colonic contractions, although it had little direct effect on myenteric neurons. Calcium responses evoked by IBS plasma in both myenteric and submucosal neurons were also suppressed by leptin, possibly through interactions with IL‐6, which is elevated in IBS plasma. As leptin has the capacity to ameliorate the neurostimulatory effects of soluble mediators in IBS plasma and modulated IL‐6‐evoked changes in bowel function, leptin may have a role in immune‐mediated bowel dysfunction in IBS patients. |
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AbstractList | New Findings
What is the central question of this study?
Does crosstalk exist between leptin and interleukin‐6 in colonic enteric neurons, and is this a contributory factor in gastrointestinal dysfunction associated with irritable bowel syndrome?
What is the main finding and its importance?
Leptin ameliorates the prosecretory and prokinetic effects of the pro‐inflammatory cytokine interleukin‐6 on rat colon. Leptin also suppresses the neurostimulatory effects of irritable bowel syndrome plasma, which has elevated concentrations of interleukin‐6, on enteric neurons. This may indicate a regulatory role for leptin in immune‐mediated bowel dysfunction.
In addition to its role in regulating energy homeostasis, the adipokine leptin modifies gastrointestinal (GI) function. Indeed, leptin‐resistant obese humans and leptin‐deficient obese mice exhibit altered GI motility. In the functional GI disorder irritable bowel syndrome (IBS), circulating leptin concentrations are reported to differ from those of healthy control subjects. Additionally, IBS patients display altered cytokine profiles, including elevated circulating concentrations of the pro‐inflammatory cytokine interleukin‐6 (IL‐6), which bears structural homology and similarities in intracellular signalling to leptin. This study aimed to investigate interactions between leptin and IL‐6 in colonic neurons and their possible contribution to IBS pathophysiology. The functional effects of leptin and IL‐6 on colonic contractility and absorptosecretory function were assessed in organ baths and Ussing chambers in Sprague–Dawley rat colon. Calcium imaging and immunohistochemical techniques were used to investigate the neural regulation of GI function by these signalling molecules. Our findings provide a neuromodulatory role for leptin in submucosal neurons, where it inhibited the stimulatory effects of IL‐6. Functionally, this translated to suppression of IL‐6‐evoked potentiation of veratridine‐induced secretory currents. Leptin also attenuated IL‐6‐induced colonic contractions, although it had little direct effect on myenteric neurons. Calcium responses evoked by IBS plasma in both myenteric and submucosal neurons were also suppressed by leptin, possibly through interactions with IL‐6, which is elevated in IBS plasma. As leptin has the capacity to ameliorate the neurostimulatory effects of soluble mediators in IBS plasma and modulated IL‐6‐evoked changes in bowel function, leptin may have a role in immune‐mediated bowel dysfunction in IBS patients. New Findings What is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a contributory factor in gastrointestinal dysfunction associated with irritable bowel syndrome? What is the main finding and its importance? Leptin ameliorates the prosecretory and prokinetic effects of the pro-inflammatory cytokine interleukin-6 on rat colon. Leptin also suppresses the neurostimulatory effects of irritable bowel syndrome plasma, which has elevated concentrations of interleukin-6, on enteric neurons. This may indicate a regulatory role for leptin in immune-mediated bowel dysfunction. In addition to its role in regulating energy homeostasis, the adipokine leptin modifies gastrointestinal (GI) function. Indeed, leptin-resistant obese humans and leptin-deficient obese mice exhibit altered GI motility. In the functional GI disorder irritable bowel syndrome (IBS), circulating leptin concentrations are reported to differ from those of healthy control subjects. Additionally, IBS patients display altered cytokine profiles, including elevated circulating concentrations of the pro-inflammatory cytokine interleukin-6 (IL-6), which bears structural homology and similarities in intracellular signalling to leptin. This study aimed to investigate interactions between leptin and IL-6 in colonic neurons and their possible contribution to IBS pathophysiology. The functional effects of leptin and IL-6 on colonic contractility and absorptosecretory function were assessed in organ baths and Ussing chambers in Sprague-Dawley rat colon. Calcium imaging and immunohistochemical techniques were used to investigate the neural regulation of GI function by these signalling molecules. Our findings provide a neuromodulatory role for leptin in submucosal neurons, where it inhibited the stimulatory effects of IL-6. Functionally, this translated to suppression of IL-6-evoked potentiation of veratridine-induced secretory currents. Leptin also attenuated IL-6-induced colonic contractions, although it had little direct effect on myenteric neurons. Calcium responses evoked by IBS plasma in both myenteric and submucosal neurons were also suppressed by leptin, possibly through interactions with IL-6, which is elevated in IBS plasma. As leptin has the capacity to ameliorate the neurostimulatory effects of soluble mediators in IBS plasma and modulated IL-6-evoked changes in bowel function, leptin may have a role in immune-mediated bowel dysfunction in IBS patients. What is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a contributory factor in gastrointestinal dysfunction associated with irritable bowel syndrome? What is the main finding and its importance? Leptin ameliorates the prosecretory and prokinetic effects of the pro-inflammatory cytokine interleukin-6 on rat colon. Leptin also suppresses the neurostimulatory effects of irritable bowel syndrome plasma, which has elevated concentrations of interleukin-6, on enteric neurons. This may indicate a regulatory role for leptin in immune-mediated bowel dysfunction. In addition to its role in regulating energy homeostasis, the adipokine leptin modifies gastrointestinal (GI) function. Indeed, leptin-resistant obese humans and leptin-deficient obese mice exhibit altered GI motility. In the functional GI disorder irritable bowel syndrome (IBS), circulating leptin concentrations are reported to differ from those of healthy control subjects. Additionally, IBS patients display altered cytokine profiles, including elevated circulating concentrations of the pro-inflammatory cytokine interleukin-6 (IL-6), which bears structural homology and similarities in intracellular signalling to leptin. This study aimed to investigate interactions between leptin and IL-6 in colonic neurons and their possible contribution to IBS pathophysiology. The functional effects of leptin and IL-6 on colonic contractility and absorptosecretory function were assessed in organ baths and Ussing chambers in Sprague-Dawley rat colon. Calcium imaging and immunohistochemical techniques were used to investigate the neural regulation of GI function by these signalling molecules. Our findings provide a neuromodulatory role for leptin in submucosal neurons, where it inhibited the stimulatory effects of IL-6. Functionally, this translated to suppression of IL-6-evoked potentiation of veratridine-induced secretory currents. Leptin also attenuated IL-6-induced colonic contractions, although it had little direct effect on myenteric neurons. Calcium responses evoked by IBS plasma in both myenteric and submucosal neurons were also suppressed by leptin, possibly through interactions with IL-6, which is elevated in IBS plasma. As leptin has the capacity to ameliorate the neurostimulatory effects of soluble mediators in IBS plasma and modulated IL-6-evoked changes in bowel function, leptin may have a role in immune-mediated bowel dysfunction in IBS patients. NEW FINDINGSWhat is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a contributory factor in gastrointestinal dysfunction associated with irritable bowel syndrome? What is the main finding and its importance? Leptin ameliorates the prosecretory and prokinetic effects of the pro-inflammatory cytokine interleukin-6 on rat colon. Leptin also suppresses the neurostimulatory effects of irritable bowel syndrome plasma, which has elevated concentrations of interleukin-6, on enteric neurons. This may indicate a regulatory role for leptin in immune-mediated bowel dysfunction. In addition to its role in regulating energy homeostasis, the adipokine leptin modifies gastrointestinal (GI) function. Indeed, leptin-resistant obese humans and leptin-deficient obese mice exhibit altered GI motility. In the functional GI disorder irritable bowel syndrome (IBS), circulating leptin concentrations are reported to differ from those of healthy control subjects. Additionally, IBS patients display altered cytokine profiles, including elevated circulating concentrations of the pro-inflammatory cytokine interleukin-6 (IL-6), which bears structural homology and similarities in intracellular signalling to leptin. This study aimed to investigate interactions between leptin and IL-6 in colonic neurons and their possible contribution to IBS pathophysiology. The functional effects of leptin and IL-6 on colonic contractility and absorptosecretory function were assessed in organ baths and Ussing chambers in Sprague-Dawley rat colon. Calcium imaging and immunohistochemical techniques were used to investigate the neural regulation of GI function by these signalling molecules. Our findings provide a neuromodulatory role for leptin in submucosal neurons, where it inhibited the stimulatory effects of IL-6. Functionally, this translated to suppression of IL-6-evoked potentiation of veratridine-induced secretory currents. Leptin also attenuated IL-6-induced colonic contractions, although it had little direct effect on myenteric neurons. Calcium responses evoked by IBS plasma in both myenteric and submucosal neurons were also suppressed by leptin, possibly through interactions with IL-6, which is elevated in IBS plasma. As leptin has the capacity to ameliorate the neurostimulatory effects of soluble mediators in IBS plasma and modulated IL-6-evoked changes in bowel function, leptin may have a role in immune-mediated bowel dysfunction in IBS patients. |
Author | Quigley, Eamonn M. M. Devlin, Michelle Hyland, Niall P. Creed, Aisling A. O'Malley, Dervla Buckley, Maria M. O'Brien, Rebecca Rae, Mark G. McKernan, Declan P. |
Author_xml | – sequence: 1 givenname: Maria M. surname: Buckley fullname: Buckley, Maria M. organization: University College Cork – sequence: 2 givenname: Rebecca surname: O'Brien fullname: O'Brien, Rebecca organization: University College Cork – sequence: 3 givenname: Michelle surname: Devlin fullname: Devlin, Michelle organization: University College Cork – sequence: 4 givenname: Aisling A. surname: Creed fullname: Creed, Aisling A. organization: University College Cork – sequence: 5 givenname: Mark G. surname: Rae fullname: Rae, Mark G. organization: University College Cork – sequence: 6 givenname: Niall P. surname: Hyland fullname: Hyland, Niall P. organization: University College Cork – sequence: 7 givenname: Eamonn M. M. surname: Quigley fullname: Quigley, Eamonn M. M. organization: Houston Methodist Hospital and Weill Cornell Medical College – sequence: 8 givenname: Declan P. surname: McKernan fullname: McKernan, Declan P. organization: National University of Ireland – sequence: 9 givenname: Dervla orcidid: 0000-0002-7031-4879 surname: O'Malley fullname: O'Malley, Dervla email: d.omalley@ucc.ie organization: University College Cork |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27676233$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1111_nmo_14160 crossref_primary_10_1152_ajpregu_00426_2016 crossref_primary_10_1111_nmo_13684 crossref_primary_10_3389_fnins_2023_934341 crossref_primary_10_3390_ijms23136917 crossref_primary_10_2174_1389203720666190121115356 |
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Keywords | enteric neurons colonic contractility leptin colonic secretion interleukin-6 |
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What is the central question of this study?
Does crosstalk exist between leptin and interleukin‐6 in colonic enteric neurons, and is this a... What is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a contributory factor... New Findings What is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a... NEW FINDINGSWhat is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a... New Findings * What is the central question of this study? Does crosstalk exist between leptin and interleukin-6 in colonic enteric neurons, and is this a... |
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SubjectTerms | Adolescent Adult Aged Animals Colon - drug effects Colon - metabolism colonic contractility colonic secretion Cytokines - metabolism enteric neurons Gastrointestinal Motility - drug effects Humans Interleukin-6 - metabolism interleukin‐6 Irritable Bowel Syndrome - metabolism leptin Leptin - pharmacology Male Middle Aged Neurons - drug effects Pneumoviridae Rats Rats, Sprague-Dawley Young Adult |
Title | Leptin modifies the prosecretory and prokinetic effects of the inflammatory cytokine interleukin‐6 on colonic function in Sprague–Dawley rats |
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