The relationship between inflammation-induced neuronal excitability and disrupted motor activity in the guinea pig distal colon

Neurogastroenterology and Motility

Volumn 23, Issue 7, 2011, Pages

  Hoffman, J M ^a   Mcknight, N D ^a   Sharkey, K A ^a,b   Mawe, G M ^a,b  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Colitis; Gastrointestinal motility; Myenteric neurons; Neuronal hyperexcitability; Peristaltic reflex

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; CALCIUM ION; CYCLIC NUCLEOTIDE GATED CHANNEL; POTASSIUM CHANNEL; SEROTONIN 4 RECEPTOR; SODIUM CHANNEL; TEGASEROD; TRINITROBENZENESULFONIC ACID;

AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLITIS; CONTROLLED STUDY; DESCENDING COLON; GANGLION; GUINEA PIG; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MOTOR ACTIVITY; MOTOR DYSFUNCTION; MYENTERIC PLEXUS; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE;

ANIMALS; COLITIS; COLON; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL MOTILITY; GUINEA PIGS; INDOLES; MODELS, ANIMAL; MOTOR ACTIVITY; MYENTERIC PLEXUS; PYRAZOLES; PYRIMIDINES; TRINITROBENZENESULFONIC ACID; VERATRIDINE;

EID: 79959341247     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2011.01702.x     Document Type: Article

References (36)

1. Furness JB. The Enteric Nervous System. Malden, MA: Blackwell Publishing, Inc., 2006.
2. Blackshaw LA, Brookes SJ, Grundy D, Schemann M. Sensory transmission in the gastrointestinal tract. Neurogastroenterol Motil 2007; 19(Suppl. 1): 1-19.
3. Brookes SJ. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 2001; 262: 58-70.
4. Furness JB, Jones C, Nurgali K, Clerc N. Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol 2004; 72: 143-64.
5. Kunze WA, Mao YK, Wang B et al. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med 2009; 13: 2261-70.
6. Nguyen TV, Matsuyama H, Baell J et al. Effects of compounds that influence IK (KCNN4) channels on afterhyperpolarizing potentials and determination of IK channel sequence, in guinea pig enteric neurons. J Neurophysiol 2007; 97: 2024-31.
7. Galligan JJ, Tatsumi H, Shen KZ, Surprenant A, North RA. Cation current activated by hyperpolarization (IH) in guinea pig enteric neurons. Am J Physiol 1990; 259: G966-72.
8. Rugiero F, Gola M, Kunze WA, Reynaud JC, Furness JB, Clerc N. Analysis of whole-cell currents by patch clamp of guinea-pig myenteric neurones in intact ganglia. J Physiol 2002; 538: 447-63.
9. Ferens D, Baell J, Lessene G, Smith JE, Furness JB. Effects of modulators of Ca(2+)-activated, intermediate-conductance potassium channels on motility of the rat small intestine, in vivo. Neurogastroenterol Motil 2007; 19: 383-9.
10. Thomas EA, Bertrand PP, Bornstein JC. A computer simulation of recurrent, excitatory networks of sensory neurons of the gut in guinea-pig. Neurosci Lett 2000; 287: 137-40.
11. Mawe GM, Coates MD, Moses PL. Review article: intestinal serotonin signaling in irritable bowel syndrome. Aliment Pharmacol Ther 2006; 23: 1067-76.
12. Linden DR, Sharkey KA, Mawe GM. Enhanced excitability of myenteric AH neurones in the inflamed guinea-pig distal colon. J Physiol 2003; 54 7: 589-601.
13. Krauter EM, Linden DR, Sharkey KA, Mawe GM. Synaptic plasticity in myenteric neurons of the guinea-pig distal colon: presynaptic mechanisms of inflammation-induced synaptic facilitation. J Physiol 2007; 581: 787-800.
14. Linden DR, Chen JX, Gershon MD, Sharkey KA, Mawe GM. Serotonin availability is increased in mucosa of guinea pigs with TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 2003; 285: G207-16.
15. Strong DS, Cornbrooks CF, Roberts JA, Hoffman JM, Sharkey KA, Mawe GM. Purinergic neuromuscular transmission is selectively attenuated in ulcerated regions of inflamed guinea pig distal colon. J Physiol 2010; 588: 847-59.
16. McCafferty DM, Wallace JL, Sharkey KA. Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat. Am J Physiol 1997; 272: G272-80.
17. Krauter EM, Strong DS, Brooks EM, Linden DR, Sharkey KA, Mawe GM. Changes in colonic motility and the electrophysiological properties of myenteric neurons persist following recovery from trinitrobenzene sulfonic acid colitis in the guinea pig. Neurogastroenterol Motil 2007; 19: 990-1000.
18. Mawe GM, Gershon MD. Functional heterogeneity in the myenteric plexus: demonstration using cytochrome oxidase as a verified cytochemical probe of the activity of individual enteric neurons. J Comp Neurol. 1986; 249: 381-91.
19. Nurgali K, Nguyen TV, Matsuyama H, Thacker M, Robbins HL, Furness JB. Phenotypic changes of morphologically identified guinea-pig myenteric neurons following intestinal inflammation. J Physiol 2007; 583: 593-609.
20. Wang B, Mao YK, Diorio C et al. Lactobacillus reuteri ingestion and IK(Ca) channel blockade have similar effects on rat colon motility and myenteric neurones. Neurogastroenterol Motil 2010;22:98-107, e33.
21. Linden DR, Sharkey KA, Ho W, Mawe GM. Cyclooxygenase-2 contributes to dysmotility and enhanced excitability of myenteric AH neurones in the inflamed guinea pig distal colon. J Physiol 2004; 557: 191-205.
22. Palmer JM, Wong-Riley M, Sharkey KA. Functional alterations in jejunal myenteric neurons during inflammation in nematode-infected guinea pigs. Am J Physiol 1998; 275: G922-35.
23. Chen Z, Suntres Z, Palmer J et al. Cyclic AMP signaling contributes to neural plasticity and hyperexcitability in AH sensory neurons following intestinal Trichinella spiralis-induced inflammation. Int J Parasitol 2007; 37: 743-61.
24. Loganathan A, Linley JE, Rajput I, Hunter M, Lodge JP, Sandle GI. Basolateral potassium (IKCa) channel inhibition prevents increased colonic permeability induced by chemical hypoxia. Am J Physiol Gastrointest Liver Physiol 2011; 300: G146-53.
25. Furness JB, Robbins HL, Selmer IS et al. Expression of intermediate conductance potassium channel immunoreactivity in neurons and epithelial cells of the rat gastrointestinal tract. Cell Tissue Res 2003; 314: 179-89.
26. Galligan JJ, Pan H, Messori E. Signalling mechanism coupled to 5-hydroxytryptamine4 receptor-mediated facilitation of fast synaptic transmission in the guinea-pig ileum myenteric plexus. Neurogastroenterol Motil 2003; 15: 523-9.
27. Ren J, Zhou X, Galligan JJ. 5-HT4 receptor activation facilitates recovery from synaptic rundown and increases transmitter release from single varicosities of myenteric neurons. Am J Physiol Gastrointest Liver Physiol 2008; 294: G1376-83.
28. Linden DR, Couvrette JM, Ciolino A et al. Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil 2005; 17: 751-60.
29. Marlow SL, Blennerhassett MG. Deficient innervation characterizes intestinal strictures in a rat model of colitis. Exp Mol Pathol 2006; 80: 54-66.
30. Lomax AE, Mawe GM, Sharkey KA. Synaptic facilitation and enhanced neuronal excitability in the submucosal plexus during experimental colitis in guinea-pig. J Physiol 2005; 564: 863-75.
31. Wang B, Mao YK, Diorio C et al. Luminal administration ex vivo of a live Lactobacillus species moderates mouse jejunal motility within minutes. FASEB J 2010; 24: 4078-88.
32. Liu M, Geddis MS, Wen Y, Setlik W, Gershon MD. Expression and function of 5-HT4 receptors in the mouse enteric nervous system. Am J Physiol Gastrointest Liver Physiol 2005; 289: G1148-63.
33. Jin JG, Foxx-Orenstein AE, Grider JR. Propulsion in guinea pig colon induced by 5-hydroxytryptamine (HT) via 5-HT4 and 5-HT3 receptors. J Pharmacol Exp Ther 1999; 288: 93-7.
34. Foxx-Orenstein AE, Jin JG, Grider JR. 5-HT4 receptor agonists and delta-opioid receptor antagonists act synergistically to stimulate colonic propulsion. Am J Physiol 1998; 275: G979-83.
35. Linden DR, Foley KF, McQuoid C, Simpson J, Sharkey KA, Mawe GM. Serotonin transporter function and expression are reduced in mice with TNBS-induced colitis. Neurogastroenterol Motil 2005; 17: 565-74.
36. Coates MD, Mahoney CR, Linden DR et al. Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 2004; 126: 1657-64.