Original Article
Copyright ©2012 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Feb 14, 2012; 18(6): 522-531
Published online Feb 14, 2012. doi: 10.3748/wjg.v18.i6.522
Hyperpolarization-activated cyclic nucleotide-gated cation channel subtypes differentially modulate the excitability of murine small intestinal afferents
Ying-Ping Wang, Bi-Ying Sun, Qian Li, Li Dong, Guo-Hua Zhang, David Grundy, Wei-Fang Rong
Ying-Ping Wang, Bi-Ying Sun, Qian Li, Li Dong, Guo-Hua Zhang, Wei-Fang Rong, Department of Physiology, Shanghai Jiaotong University School of Medicine, Shanghai 200025, China
David Grundy, Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom
Author contributions: Rong WF and Grundy D designed the study; Wang YP, Sun BY, Li Q and Dong L performed the experiments and analyzed the data; Wang YP, Zhang GH, Rong WF and Grundy D wrote the manuscript.
Supported by Science and Technology Commission of Shanghai Municipality, No. 10ZR1417300; Educational Commission of Shanghai Municipality, No. 10ZZ69
Correspondence to: Wei-Fang Rong, PhD, Department of Physiology, Shanghai Jiaotong University School of Medicine, 280 South Chongqing Road, Shanghai 200025, China. weifangrong@hotmail.com
Telephone: +86-21-63846590-776476 Fax: +86-21-63846590
Received: April 2, 2011
Revised: June 21, 2011
Accepted: June 28, 2011
Published online: February 14, 2012
Abstract

AIM: To assess the role of hyperpolarization-activated cyclic nucleotide-gated cation (HCN) channels in regulating the excitability of vagal and spinal gut afferents.

METHODS: The mechanosensory response of mesenteric afferent activity was measured in an ex vivo murine jejunum preparation. HCN channel activity was recorded through voltage and current clamp in acutely dissociated dorsal root ganglia (DRG) and nodose ganglia (NG) neurons retrogradely labeled from the small intestine through injection of a fluorescent marker (DiI). The isoforms of HCN channels expressed in DRG and NG neurons were examined by immunohistochemistry.

RESULTS: Ramp distension of the small intestine evoked biphasic increases in the afferent nerve activity, reflecting the activation of low- and high-threshold fibers. HCN blocker CsCl (5 mmol/L) preferentially inhibited the responses of low-threshold fibers to distension and showed no significant effects on the high-threshold responses. The effect of CsCl was mimicked by the more selective HCN blocker ZD7288 (10 μmol/L). In 71.4% of DiI labeled DRG neurons (n = 20) and 90.9% of DiI labeled NG neurons (n = 10), an inward current (Ih current) was evoked by hyperpolarization pulses which was fully eliminated by extracellular CsCl. In neurons expressing Ih current, a typical “sag” was observed upon injection of hyperpolarizing current pulses in current-clamp recordings. CsCl abolished the sag entirely. In some DiI labeled DRG neurons, the Ih current was potentiated by 8-Br-cAMP, which had no effect on the Ih current of DiI labeled NG neurons. Immunohistochemistry revealed differential expression of HCN isoforms in vagal and spinal afferents, and HCN2 and HCN3 seemed to be the dominant isoform in DRG and NG, respectively.

CONCLUSION: HCNs differentially regulate the excitability of vagal and spinal afferent of murine small intestine.

Keywords: Hyperpolarization-activated cyclic nucleotide-gated cation; Vagal afferent; Spinal afferent; Gastrointestinal tract; CsCl