A novel role of intestine epithelial GABAergic signaling in regulating intestinal fluid secretion

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 303, Issue 4, 2012, Pages

  Li, Yan ^a,b   Xiang, Yun Yan ^c   Lu, Wei Yang ^c   Liu, Chuanyong ^a,b   Li, Jingxin ^a,b  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANDONG UNIVERSITY   (China)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Aminobutyric acid; Allergic diarrhea; Electrolyte transport; Intestinal epithelial cell; Type a aminobutyric acid receptor

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; CELL PROTEIN; GLUTAMATE DECARBOXYLASE; MUSCIMOL; OVALBUMIN; PICROTOXIN; TETRODOTOXIN;

ALLERGIC DIARRHEA; ALLERGY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIARRHEA; GABAERGIC SYSTEM; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE FLUID; INTESTINE FUNCTION; INTESTINE SECRETION; MALE; MEMBRANE CURRENT; MOUSE; NONHUMAN; ORGAN WEIGHT; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMALL INTESTINE; SWINE; UPREGULATION; WESTERN BLOTTING;

ADULT; ANIMALS; AUTOCRINE COMMUNICATION; BLOTTING, WESTERN; CELL LINE; DIARRHEA; DISEASE MODELS, ANIMAL; GABA-A RECEPTOR AGONISTS; GABA-A RECEPTOR ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; INTESTINAL SECRETIONS; INTESTINE, SMALL; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; MIDDLE AGED; OVALBUMIN; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SWINE; YOUNG ADULT;

EID: 84865132169     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00497.2011     Document Type: Article

References (40)

1. Akhondzadeh S, Stone TW. Induction of a novel form of hippocampal long-term depression by muscimol: involvement of GABAA but not glutamate receptors. Br J Pharmacol 115: 527-533, 1995.
2. Amenta F, Cavallotti C, Ferrante F, Erdo SL. Autoradiographic visualization of the GABA-A receptor agonist, 3H-muscimol in the rat uterus. Pharmacol Res Commun 20: 863-868, 1988.
3. Barrett KE. New ways of thinking about (and teaching about) intestinal epithelial function. Advances Physiol Education 32: 25-34, 2008.
4. Basavappa S, Vulapalli SR, Zhang H, Yule D, Coon S, Sundaram U. Chloride channels in the small intestinal cell line IEC-18. J Cell Physiol 202: 21-31, 2005.
5. Ben-Ari Y, Tseeb V, Raggozzino D, Khazipov R, Gaiarsa JL. gamma-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog Brain Res 102: 261-273, 1994.
6. Bormann J, Clapham DE. gamma-Aminobutyric acid receptor channels in adrenal chromaffin cells: a patch-clamp study. Proc Natl Acad Sci USA 82: 2168-2172, 1985.
7. Brandt EB, Munitz A, Orekov T, Mingler MK, McBride M, Finkelman FD, Rothenberg ME. Targeting IL-4/IL-13 signaling to alleviate oral allergen-induced diarrhea. J Allergy Clin Immunol 123: 53-58, 2009.
8. Brandt EB, Strait RT, Hershko D, Wang Q, Muntel EE, Scribner TA, Zimmermann N, Finkelman FD, Rothenberg ME. Mast cells are required for experimental oral allergen-induced diarrhea. J Clin Invest 112: 1666-1677, 2003.
9. Davanger S, Hjelle OP, Babaie E, Larsson LI, Hougaard D, Storm-Mathisen J, Ottersen OP. Colocalization of gamma-aminobutyrate and gastrin in the rat antrum: an immunocytochemical and in situ hybridization study. Gastroenterology 107: 137-148, 1994.
10. Demeneix BA, Taleb O, Loeffler JP, Feltz P. GABAA and GABAB receptors on porcine pars intermedia cells in primary culture: functional role in modulating peptide release. Neuroscience 17: 1275-1285, 1986.
11. Dong H, Kumar M, Zhang Y, Gyulkhandanyan A, Xiang YY, Ye B, Perrella J, Hyder A, Zhang N, Wheeler M, Lu WY, Wang Q. Gamma-aminobutyric acid up- and downregulates insulin secretion from beta cells in concert with changes in glucose concentration. Diabetologia 49: 697-705, 2006.
12. Erdo SL, De Vincentis G, Amenta F. Autoradiographic localization of [3H]muscimol binding sites in rat stomach: evidence for mucosal GABAA receptors. Eur J Pharmacol 175: 351-354, 1990.
13. Erdo SL, Ezer E, Matuz J, Wolff JR, Amenta F. GABAA receptors in the rat stomach may mediate mucoprotective effects. Eur J Pharmacol 165: 79-86, 1989.
14. 3H]-muscimol to GABAA sites in the guinea-pig urinary bladder: biochemical assay and autoradiography. Br J Pharmacol 96: 313-318, 1989.
15. Fiszman ML, Borodinsky LN, Neale JH. GABA induces proliferation of immature cerebellar granule cells grown in vitro. Brain Res Dev Brain Res 115: 1-8, 1999.
16. Ganguly K, Schinder AF, Wong ST, Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105: 521-532, 2001.
17. Gliddon CM, Darlington CL, Smith PF. GABAergic systems in the vestibular nucleus and their contribution to vestibular compensation. Prog Neurobiol 75: 53-81, 2005.
18. Hino A, Fukuyama S, Kataoka K, Kweon MN, Fujihashi K, Kiyono H. Nasal IL-12p70 DNA prevents and treats intestinal allergic diarrhea. J Immunol 174: 7423-7432, 2005.
19. Jentsch TJ, Friedrich T, Schriever A, Yamada H. The CLC chloride channel family. Pflugers Arch 437: 783-795, 1999.
20. Jin N, Kolliputi N, Gou D, Weng T, Liu L. A novel function of ionotropic gamma-aminobutyric acid receptors involving alveolar fluid homeostasis. J Biol Chem 281: 36012-36020, 2006.
21. Kidd M, Modlin IM, Eick GN, Champaneria MC. Isolation, functional characterization, and transcriptome of Mastomys ileal enterochromaffin cells. Am J Physiol Gastrointest Liver Physiol 291: G778-G791, 2006.
22. Krantis A. GABA in the mammalian enteric nervous system. News Physiol Sci 15: 284-290, 2000.
23. Krantis A, Nichols K, de Blas A, Staines W. Demonstration of benzodiazepine receptors in submucosal neurons of the gastrointestinal tract. Neurosci Lett 176: 32-36, 1994.
24. Licht P, Harbarth P, Merz WE. Evidence for a modulation of human chorionic gonadotropin (hCG) subunit messenger ribonucleic acid levels and hCG secretion by gamma-aminobutyric acid in human first trimester placenta in vitro. Endocrinology 130: 490-496, 1992.
25. MacNaughton WK, Pineau BC, Krantis A. gamma-Aminobutyric acid stimulates electrolyte transport in the guinea pig ileum in vitro. Gastroenterology 110: 498-507, 1996.
26. 3H]SR 95531: microscopic analysis of binding in the rat brain and allosteric modulation by several benzodiazepine and barbiturate receptor ligands. Synapse 2: 163-173, 1988.
27. Mindell JA, Maduke M. ClC chloride channels. Genome Biol 2: REVIEWS3003, 2001.
28. Olsen RW, Ban M, Miller T. Studies on the neuropharmacological activity of bicuculline and related compounds. Brain Res 102: 283-299, 1976.
29. Rorsman P, Berggren PO, Bokvist K, Ericson H, Mohler H, Ostenson CG, Smith PA. Glucose-inhibition of glucagon secretion involves activation of GABAA-receptor chloride channels. Nature 341: 233-236, 1989.
30. Sampson HA. Food allergy. J Am Med Assoc 278: 1888-1894, 1997.
31. Tillakaratne NJ, Medina-Kauwe L, Gibson KM. gamma-Aminobutyric acid (GABA) metabolism in mammalian neural and nonneural tissues. Comp Biochem Physiol 112: 247-263, 1995.
32. Ueno S, Bracamontes J, Zorumski C, Weiss DS, Steinbach JH. Bicuculline and gabazine are allosteric inhibitors of channel opening of the GABAA receptor. J Neurosci 17: 625-634, 1997.
33. Wang FY, Watanabe M, Zhu RM, Maemura K. Characteristic expression of gamma-aminobutyric acid and glutamate decarboxylase in rat jejunum and its relation to differentiation of epithelial cells. World J Gastroenterol 10: 3608-3611, 2004.
34. Watanabe M, Maemura K, Kanbara K, Tamayama T, Hayasaki H. GABA and GABA receptors in the central nervous system and other organs. Int Rev Cytol 213: 1-47, 2002.
35. Welsh MJ, Smith PL, Fromm M, Frizzell RA. Crypts are the site of intestinal fluid and electrolyte secretion. Science 218: 1219-1221, 1982.
36. Wermuth CG, Biziere K. Pyridazinyl-GABA derivatives: a newclass of synthetic GABAA antagonists. TiPS 8: 421-424, 1986.
37. Woodward RM, Polenzani L, Miledi R. Characterization of bicuculline/baclofen-insensitive (rho-like) gamma-aminobutyric acid receptors expressed in Xenopus oocytes. II. Pharmacology of gamma-aminobutyric acidA and gamma-aminobutyric acidB receptor agonists and antagonists. Mol Pharmacol 43: 609-625, 1993.
38. Xiang YY, Wang S, Liu M, Hirota JA, Li J, Ju W, Fan Y, Kelly MM, Ye B, Orser B, O'Byrne PM, Inman MD, Yang X, Lu WY. A GABAergic system in airway epithelium is essential for mucus overproduction in asthma. Nat Med 13: 862-867, 2007.
39. Yu S, Ho IK. Effects of GABA antagonists, SR 95531 and bicuculline, on GABAA receptor-regulated chloride flux in rat cortical synaptoneurosomes. Neurochem Res 15: 905-910, 1990.
40. Zund G, Madara JL, Dzus AL, Awtrey CS, Colgan SP. Interleukin-4 and interleukin-13 differentially regulate epithelial chloride secretion. J Biol Chem 271: 7460-7464, 1996.