Role for protease activity in visceral pain in irritable bowel syndrome
Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependen...
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| Published in | The Journal of clinical investigation Vol. 117; no. 3; pp. 636 - 647 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Clinical Investigation
01.03.2007
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0021-9738 1558-8238 |
| DOI | 10.1172/JCI29255 |
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| Abstract | Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependent on the activation of NF-kappaB. In addition, increased proteolytic activity was measured in vivo, in colonic washes from IBS compared with control patients. Trypsin and tryptase expression and release were increased in colonic biopsies from IBS patients compared with control subjects. Biopsies from IBS patients (but not controls) released mediators that sensitized murine sensory neurons in culture. Sensitization was prevented by a serine protease inhibitor and was absent in neurons lacking functional protease-activated receptor-2 (PAR2). Supernatants from colonic biopsies of IBS patients, but not controls, also caused somatic and visceral hyperalgesia and allodynia in mice, when administered into the colon. These pronociceptive effects were inhibited by serine protease inhibitors and a PAR2 antagonist and were absent in PAR2-deficient mice. Our study establishes that proteases are released in IBS and that they can directly stimulate sensory neurons and generate hypersensitivity symptoms through the activation of PAR2. |
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| AbstractList | Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependent on the activation of NF-kappaB. In addition, increased proteolytic activity was measured in vivo, in colonic washes from IBS compared with control patients. Trypsin and tryptase expression and release were increased in colonic biopsies from IBS patients compared with control subjects. Biopsies from IBS patients (but not controls) released mediators that sensitized murine sensory neurons in culture. Sensitization was prevented by a serine protease inhibitor and was absent in neurons lacking functional protease-activated receptor-2 (PAR2). Supernatants from colonic biopsies of IBS patients, but not controls, also caused somatic and visceral hyperalgesia and allodynia in mice, when administered into the colon. These pronociceptive effects were inhibited by serine protease inhibitors and a PAR2 antagonist and were absent in PAR2-deficient mice. Our study establishes that proteases are released in IBS and that they can directly stimulate sensory neurons and generate hypersensitivity symptoms through the activation of PAR2. Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependent on the activation of NF-[kappa]B. In addition, increased proteolytic activity was measured in vivo, in colonic washes from IBS compared with control patients. Trypsin and tryptase expression and release were increased in colonic biopsies from IBS patients compared with control subjects. Biopsies from IBS patients (but not controls) released mediators that sensitized murine sensory neurons in culture. Sensitization was prevented by a serine protease inhibitor and was absent in neurons lacking functional protease-activated receptor-2 (PAR sub(2)). Supernatants from colonic biopsies of IBS patients, but not controls, also caused somatic and visceral hyperalgesia and allodynia in mice, when administered into the colon. These pronociceptive effects were inhibited by serine protease inhibitors and a PAR sub(2) antagonist and were absent in PAR sub(2)-deficient mice. Our study establishes that proteases are released in IBS and that they can directly stimulate sensory neurons and generate hypersensitivity symptoms through the activation of PAR sub(2). Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependent on the activation of NF-kappaB. In addition, increased proteolytic activity was measured in vivo, in colonic washes from IBS compared with control patients. Trypsin and tryptase expression and release were increased in colonic biopsies from IBS patients compared with control subjects. Biopsies from IBS patients (but not controls) released mediators that sensitized murine sensory neurons in culture. Sensitization was prevented by a serine protease inhibitor and was absent in neurons lacking functional protease-activated receptor-2 (PAR2). Supernatants from colonic biopsies of IBS patients, but not controls, also caused somatic and visceral hyperalgesia and allodynia in mice, when administered into the colon. These pronociceptive effects were inhibited by serine protease inhibitors and a PAR2 antagonist and were absent in PAR2-deficient mice. Our study establishes that proteases are released in IBS and that they can directly stimulate sensory neurons and generate hypersensitivity symptoms through the activation of PAR2.Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependent on the activation of NF-kappaB. In addition, increased proteolytic activity was measured in vivo, in colonic washes from IBS compared with control patients. Trypsin and tryptase expression and release were increased in colonic biopsies from IBS patients compared with control subjects. Biopsies from IBS patients (but not controls) released mediators that sensitized murine sensory neurons in culture. Sensitization was prevented by a serine protease inhibitor and was absent in neurons lacking functional protease-activated receptor-2 (PAR2). Supernatants from colonic biopsies of IBS patients, but not controls, also caused somatic and visceral hyperalgesia and allodynia in mice, when administered into the colon. These pronociceptive effects were inhibited by serine protease inhibitors and a PAR2 antagonist and were absent in PAR2-deficient mice. Our study establishes that proteases are released in IBS and that they can directly stimulate sensory neurons and generate hypersensitivity symptoms through the activation of PAR2. Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy samples from IBS patients release increased levels of proteolytic activity (arginine cleavage) compared to asymptomatic controls. This was dependent on the activation of NF-κB. In addition, increased proteolytic activity was measured in vivo, in colonic washes from IBS compared with control patients. Trypsin and tryptase expression and release were increased in colonic biopsies from IBS patients compared with control subjects. Biopsies from IBS patients (but not controls) released mediators that sensitized murine sensory neurons in culture. Sensitization was prevented by a serine protease inhibitor and was absent in neurons lacking functional protease-activated receptor–2 (PAR 2 ). Supernatants from colonic biopsies of IBS patients, but not controls, also caused somatic and visceral hyperalgesia and allodynia in mice, when administered into the colon. These pronociceptive effects were inhibited by serine protease inhibitors and a PAR 2 antagonist and were absent in PAR 2 -deficient mice. Our study establishes that proteases are released in IBS and that they can directly stimulate sensory neurons and generate hypersensitivity symptoms through the activation of PAR 2 . |
| Audience | Academic |
| Author | Vergnolle, Nathalie Shaffer, Eldon Cottrell, Graeme Chapman, Kevin Holzhausen, Marinella Ferraz, Jose Geraldo P. Andrade-Gordon, Patricia Cenac, Nicolas Steinhoff, Martin Beck, Paul Bunnett, Nigel W. Barbara, Giovanni Andrews, Christopher N. Sharkey, Keith A. |
| AuthorAffiliation | 1 Department of Pharmacology and Therapeutics and 2 Department of Medicine, Division of Gastroenterology, University of Calgary, Calgary, Alberta, Canada. 3 Departments of Surgery and Physiology, UCSF, San Francisco, California, USA. 4 R.W. Johnson Pharmaceutical Research Institute, Spring House, Pennsylvania, USA. 5 Department of Dermatology and Interdisciplinary Center for Clinical Research (IZKF) Münster, University of Münster, Münster, Germany. 6 Departments of Internal Medicine and Gastroenterology, University of Bologna, Bologna, Italy. 7 Department of Physiology and Biophysics, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada |
| AuthorAffiliation_xml | – name: 1 Department of Pharmacology and Therapeutics and 2 Department of Medicine, Division of Gastroenterology, University of Calgary, Calgary, Alberta, Canada. 3 Departments of Surgery and Physiology, UCSF, San Francisco, California, USA. 4 R.W. Johnson Pharmaceutical Research Institute, Spring House, Pennsylvania, USA. 5 Department of Dermatology and Interdisciplinary Center for Clinical Research (IZKF) Münster, University of Münster, Münster, Germany. 6 Departments of Internal Medicine and Gastroenterology, University of Bologna, Bologna, Italy. 7 Department of Physiology and Biophysics, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada |
| Author_xml | – sequence: 1 givenname: Nicolas surname: Cenac fullname: Cenac, Nicolas – sequence: 2 givenname: Christopher N. surname: Andrews fullname: Andrews, Christopher N. – sequence: 3 givenname: Marinella surname: Holzhausen fullname: Holzhausen, Marinella – sequence: 4 givenname: Kevin surname: Chapman fullname: Chapman, Kevin – sequence: 5 givenname: Graeme surname: Cottrell fullname: Cottrell, Graeme – sequence: 6 givenname: Patricia surname: Andrade-Gordon fullname: Andrade-Gordon, Patricia – sequence: 7 givenname: Martin surname: Steinhoff fullname: Steinhoff, Martin – sequence: 8 givenname: Giovanni surname: Barbara fullname: Barbara, Giovanni – sequence: 9 givenname: Paul surname: Beck fullname: Beck, Paul – sequence: 10 givenname: Nigel W. surname: Bunnett fullname: Bunnett, Nigel W. – sequence: 11 givenname: Keith A. surname: Sharkey fullname: Sharkey, Keith A. – sequence: 12 givenname: Jose Geraldo P. surname: Ferraz fullname: Ferraz, Jose Geraldo P. – sequence: 13 givenname: Eldon surname: Shaffer fullname: Shaffer, Eldon – sequence: 14 givenname: Nathalie surname: Vergnolle fullname: Vergnolle, Nathalie |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/17304351$$D View this record in MEDLINE/PubMed |
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| Snippet | Mediators involved in the generation of symptoms in patients with irritable bowel syndrome (IBS) are poorly understood. Here we show that colonic biopsy... |
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| SubjectTerms | Abdominal Pain - enzymology Abdominal Pain - etiology Adult alpha 1-Antitrypsin - analysis alpha 1-Antitrypsin - metabolism Biomedical research Biopsy Colon Colon - enzymology Colon - innervation Colon - pathology Constipation Diarrhea Endopeptidases - analysis Endopeptidases - drug effects Endopeptidases - physiology Female Humans Hyperalgesia Hyperalgesia - enzymology Hyperalgesia - etiology Inflammatory bowel disease Irritable bowel syndrome Irritable Bowel Syndrome - complications Irritable Bowel Syndrome - enzymology Irritable Bowel Syndrome - pathology Male Middle Aged Neurons, Afferent - drug effects Neurons, Afferent - metabolism NF-kappa B - metabolism Patients Physiological aspects Proteases Receptor, PAR-2 - agonists Rectum Serine Proteinase Inhibitors - pharmacology Trypsin - analysis Trypsin - drug effects Trypsin - metabolism Tryptases - analysis Tryptases - antagonists & inhibitors Tryptases - metabolism |
| Title | Role for protease activity in visceral pain in irritable bowel syndrome |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/17304351 https://www.proquest.com/docview/200589415 https://www.proquest.com/docview/20750512 https://www.proquest.com/docview/70226082 https://pubmed.ncbi.nlm.nih.gov/PMC1794118 |
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