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The Journal of Neuroscience, March 9, 2005, 25(10):2617-2627; doi:10.1523/JNEUROSCI.2894-04.2005

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Neurobiology of Disease
Acid-Sensing Properties in Rat Gastric Sensory Neurons from Normal and Ulcerated Stomach

Takeshi Sugiura,^1,2 Khoa Dang,¹ Kenneth Lamb,¹ Klaus Bielefeldt,³ and G. F. Gebhart¹

¹Department of Pharmacology, Carver College of Medicine, The University of Iowa, Iowa City, Iowa 52242, ²Department of Anesthesiology and Medical Crisis Management, Nagoya City University Graduate School of Medical Sciences, Nagoya 467-8601, Japan, and ³Division of Gastroenterology, Department of Internal Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261

Gastric acid contributes to dyspeptic symptoms, including abdominal pain, in patients with disorders of the proximal gastrointestinal tract. To examine the molecular sensor(s) of gastric acid chemonociception, we characterized acid-elicited currents in dorsal root ganglion (DRG) and nodose ganglion (NG) neurons that innervate the stomach and examined their modulation after induction of gastric ulcers. A fluorescent dye (DiI) was injected into the stomach wall to retrogradely label gastric sensory neurons. After 1-2 weeks, gastric ulcers were induced by 45 s of luminal exposure of the stomach to 60% acetic acid injected into a clamped area of the distal stomach; control animals received saline. In whole-cell voltage-clamp recordings, all gastric DRG neurons and 55% of NG neurons exhibited transient, amiloride-sensitive, acid-sensing ion-channel (ASIC) currents. In the remaining 45% of NG neurons, protons activated a slow, sustained current that was attenuated by the transient receptor potential vanilloid subtype 1 antagonist, capsazepine. The kinetics and proton sensitivity of amiloride-sensitive ASIC currents differed between NG and DRG neurons. NG neurons had a lower proton sensitivity and faster kinetics, suggesting expression of specific subtypes of ASICs in the vagal and splanchnic innervation of the stomach. Effects of Zn²⁺ and N,N,N',N'-tetrakis-(2-pyridylmethyl)-ethylenediamine on acid-elicited currents suggest contributions of ASIC1a and ASIC2a subunits. Gastric ulcers altered the properties of acid-elicited currents by increasing pH sensitivity and current density and changing current kinetics in gastric DRG neurons. The distinct properties of NG and DRG neurons and their modulation after injury suggest differential contributions of vagal and spinal afferent neurons to chemosensation and chemonociception.

Key words: visceral hypersensitivity; proton; DRG; ASIC; TRPV1; DiI; gastric chemonociception; TPEN

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Received July 16, 2004; revised January 14, 2005; accepted January 17, 2005.

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