Role of Transient Receptor Potential Ankyrin 1 in Gastric Accommodation in Conscious Guinea Pigs

We report the establishment of a new model for measuring gastric tone and liquid meal-induced accommodation in conscious guinea pigs and the role played by transient receptor potential ankyrin 1 (TRPA1). An indwelling polyethylene bag was placed in proximal stomachs of 5-week-old male Hartley guinea pigs. Gastric tone was measured by distending the bag and recording changes in intrabag pressure at various volumes. Gastric accommodation was measured by administering liquid meals and recording intrabag pressure over time. Nω-nitro-l-arginine methyl ester hydrochloride (l-NAME) (a nitric-oxide synthase inhibitor), atropine sulfate (atropine) (a muscarinic receptor antagonist), allyl isothiocyanate (AITC) (a TRPA1 agonist), or theophylline-7-(N-4-isopropylphenyl) acetamide (HC-030031) (a selective TRPA1 antagonist) was administered 15 to 60 min before measurement. Gastric tone was increased by stepwise distension of the bag and was further significantly increased by l-NAME and significantly decreased by atropine. A liquid meal (15% w/v; 1.7 kcal) significantly decreased intrabag pressure 5 to 20 min after administration, indicating gastric accommodation; this was completely suppressed by l-NAME and further enhanced by atropine. AITC significantly increased gastric tone; this increase was decreased by HC-030031 and atropine. A combination of AITC and l-NAME significantly increased gastric tone compared with l-NAME alone. HC-030031 alone significantly decreased gastric tone. Liquid meal-induced gastric accommodation was significantly suppressed by pretreatment with AITC. We established a new model for measuring gastric tone and accommodation in conscious guinea pigs. TRPA1 activation suppresses gastric accommodation by increasing gastric tone through cholinergic neuronal pathways.

[1]  J. Tack,et al.  Intragastric pressure during food intake: a physiological and minimally invasive method to assess gastric accommodation , 2011, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[2]  K. Nozawa,et al.  Molecular cloning and characterization of dog TRPA1 and AITC stimulate the gastrointestinal motility through TRPA1 in conscious dogs. , 2009, European journal of pharmacology.

[3]  K. Nozawa,et al.  TRPA1 agonists delay gastric emptying in rats through serotonergic pathways , 2009, Naunyn-Schmiedeberg's Archives of Pharmacology.

[4]  K. Noguchi,et al.  Transient receptor potential A1 mediates gastric distention-induced visceral pain in rats , 2009, Gut.

[5]  H. Matsushime,et al.  TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells , 2009, Proceedings of the National Academy of Sciences.

[6]  K. Schulze,et al.  Visceral hypersensitivity and impaired accommodation in refractory diabetic gastroparesis , 2008, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[7]  C. Owyang,et al.  Spatial organization of neurons in the dorsal motor nucleus of the vagus synapsing with intragastric cholinergic and nitric oxide/VIP neurons in the rat. , 2008, American journal of physiology. Gastrointestinal and liver physiology.

[8]  P. Janssen,et al.  A novel method to assess gastric accommodation and peristaltic motility in conscious rats , 2008, Scandinavian journal of gastroenterology.

[9]  Kenjiro Matsumoto,et al.  Contractile effect of TRPA1 receptor agonists in the isolated mouse intestine. , 2007, European journal of pharmacology.

[10]  Clifford J. Woolf,et al.  TRPA1 Contributes to Cold, Mechanical, and Chemical Nociception but Is Not Essential for Hair-Cell Transduction , 2006, Neuron.

[11]  David Julius,et al.  TRPA1 Mediates the Inflammatory Actions of Environmental Irritants and Proalgesic Agents , 2006, Cell.

[12]  Yi Dai,et al.  TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. , 2005, The Journal of clinical investigation.

[13]  F. De Ponti,et al.  Effect of muscarinic receptor blockade on canine gastric tone and compliance in vivo. , 2005, Pharmacological research.

[14]  J. Tack,et al.  Effects of capsaicin on the sensorimotor function of the proximal stomach in humans , 2004, Alimentary pharmacology & therapeutics.

[15]  D. McKemy,et al.  Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1 , 2004, Nature.

[16]  A. Crema,et al.  Role of 5-HT1B/D receptors in canine gastric accommodation: effect of sumatriptan and 5-HT1B/D receptor antagonists. , 2003, American journal of physiology. Gastrointestinal and liver physiology.

[17]  Peter McIntyre,et al.  ANKTM1, a TRP-like Channel Expressed in Nociceptive Neurons, Is Activated by Cold Temperatures , 2003, Cell.

[18]  J. Tack,et al.  Role of nitric oxide in the gastric accommodation reflex and in meal induced satiety in humans , 2002, Gut.

[19]  G. Boeckxstaens,et al.  Role of nitric oxide in gastric motor and sensory functions in healthy subjects , 2002, Gut.

[20]  M. Fox,et al.  Non-invasive measurement of gastric accommodation in humans , 2002, Gut.

[21]  G. Barbara,et al.  Role of nitric oxide‐ and vasoactive intestinal polypeptide‐containing neurones in human gastric fundus strip relaxations , 2000, British journal of pharmacology.

[22]  B. Trueb,et al.  An Ankyrin-like Protein with Transmembrane Domains Is Specifically Lost after Oncogenic Transformation of Human Fibroblasts* , 1999, The Journal of Biological Chemistry.

[23]  J. Tack,et al.  Role of nitric oxide in fasting gastric fundus tone and in 5-HT1 receptor-mediated relaxation of gastric fundus. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[24]  J. Tack,et al.  Role of impaired gastric accommodation to a meal in functional dyspepsia. , 1998, Gastroenterology.

[25]  D. Thompson,et al.  Evidence for a lipid specific effect in nutrient induced human proximal gastric relaxation , 1998, Gut.

[26]  K. Higuchi,et al.  Involvement of capsaicin-sensitive sensory nerves in gastric adaptive relaxation in isolated guinea-pig stomachs. , 1997, Digestion.

[27]  D. Thompson,et al.  Effect of distension and feeding on phasic changes in human proximal gastric tone. , 1996, Gut.

[28]  J. Galmiche,et al.  Erythromycin enhances fasting and postprandial proximal gastric tone in humans. , 1995, Gastroenterology.

[29]  J. Vane,et al.  Nitroxergic nerves mediate vagally induced relaxation in the isolated stomach of the guinea pig. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Vane,et al.  Involvement of nitric oxide in the reflex relaxation of the stomach to accommodate food or fluid , 1991, Nature.

[31]  R. Lefebvre,et al.  Relaxant effect of capsaicin in the rat gastric fundus. , 1991, European journal of pharmacology.

[32]  M. Gibney,et al.  Dietary intakes and adipose tissue levels of linoleic acid in peptic ulcer disease , 1989, British Journal of Nutrition.

[33]  F. Azpiroz,et al.  Importance of vagal input in maintaining gastric tone in the dog. , 1987, The Journal of physiology.

[34]  J. Malagelada,et al.  Vagally mediated gastric relaxation induced by intestinal nutrients in the dog. , 1986, The American journal of physiology.

[35]  J. Malagelada,et al.  Physiological variations in canine gastric tone measured by an electronic barostat. , 1985, The American journal of physiology.

[36]  J. Szurszewski,et al.  The electrical basis for contraction and relaxation in canine fundal smooth muscle , 1981, The Journal of physiology.