Hydrogen sulfide selectively potentiates central preganglionic fast nicotinic synaptic input in mouse superior mesenteric ganglion

Journal of Neuroscience

Volumn 33, Issue 31, 2013, Pages 12638-12646

  Sha, Lei ^a,b   Linden, David R ^a,b   Farrugia, Gianrico ^a,b   Szurszewski, Joseph H ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; HYDROGEN SULFIDE;

ADRENERGIC SYSTEM; ANIMAL TISSUE; ARTICLE; COLON MOTILITY; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE MICROSCOPY; GUINEA PIG; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINE PRESSURE; MOUSE; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PREGANGLIONIC NERVE; PRIORITY JOURNAL; SPLANCHNIC NERVE; SUPERIOR MESENTERIC GANGLION; SYNAPTIC TRANSMISSION;

ACETYLCHOLINE; ANIMALS; AUTONOMIC FIBERS, PREGANGLIONIC; CHOLINERGIC AGONISTS; COLON, DESCENDING; CYSTATHIONINE GAMMA-LYASE; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA-A RECEPTOR ANTAGONISTS; GANGLIA, SYMPATHETIC; GASTROINTESTINAL MOTILITY; GUINEA PIGS; HYDROGEN SULFIDE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SPLANCHNIC NERVES; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 84880836935     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4429-12.2013     Document Type: Article

References (42)

1. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066-1071. Medline
2. Austgen JR, Hermann GE, Dantzler HA, Rogers RC, Kline DD (2011) Hydrogen sulfide augments synaptic neurotransmission in the nucleus of the solitary tract. J Neurophysiol 106:1822-1832. CrossRef Medline
3. De Groat WC, Krier J (1979) The central control of the lumbar sympathetic pathway to the large intestine of the cat. J Physiol 289:449-468. Medline
4. Ercoli J, Miolan JP, Niel JP, Quinson N (2007) Presynaptic GABA-A receptors prevent depression of nicotinic transmission in rabbit coeliac ganglion neurones. Eur J Neurosci 25:1307-1318. CrossRef Medline
5. Ermilov LG, Schmalz PF, Miller SM, Szurszewski JH (2004) PACAP modulation of the colon-inferior mesenteric ganglion reflex in the guinea pig. J Physiol 560:231-247. CrossRef Medline
6. 2+ channels. Antioxid Redox Signal 10: 31-42. CrossRef Medline
7. Gibbins IL, Jobling P, Teo EH, Matthew SE, Morris JL (2003) Heterogeneous expression of SNAP-25 and synaptic vesicle proteins by central and peripheral inputs to sympathetic neurons. J Comp Neurol 459:25-43. CrossRef Medline
8. Hosoki R, Matsuki N, Kimura H (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237:527-531. CrossRef Medline
9. Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285:21903-21907. CrossRef Medline
10. Kawabata A, Ishiki T, Nagasawa K, Yoshida S, Maeda Y, Takahashi T, Sekiguchi F, Wada T, Ichida S, Nishikawa H (2007) Hydrogen sulfide as a novel nociceptive messenger. Pain 132:74-81. CrossRef Medline
11. Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDAreceptor. Biochem Biophys Res Commun 267:129-133. CrossRef Medline
12. Kombian SB, Reiffenstein RJ, Colmers WF (1993) The actions of hydrogen sulfide on dorsal raphe serotonergic neurons in vitro. J Neurophysiol 70:81-96. Medline
13. Krueger D, Foerster M, Mueller K, Zeller F, Slotta-Huspenina J, Donovan J, Grundy D, Schemann M (2010) Signaling mechanisms involved in the intestinal pro-secretory actions of hydrogen sulfide. Neurogastroenterol Motil 22:1224-1231. CrossRef Medline
14. Lagoutte E, Mimoun S, Andriamihaja M, Chaumontet C, Blachier F, Bouillaud F (2010) Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim Biophys Acta 1797:1500-1511. CrossRef Medline
15. Lee SW, Hu YS, Hu LF, Lu Q, Dawe GS, Moore PK, Wong PT, Bian JS (2006) Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 54:116-124. CrossRef Medline
16. Levitt MD, Furne J, Springfield J, Suarez F, DeMaster E (1999) Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest 104:1107-1114. CrossRef Medline
17. Linden DR, Sha L, Mazzone A, Stoltz GJ, Bernard CE, Furne JK, Levitt MD, Farrugia G, Szurszewski JH (2008) Production of the gaseous signal molecule hydrogen sulfide in mouse tissues. J Neurochem 106: 1577-1585. CrossRef Medline
18. Linden DR, Levitt MD, Farrugia G, Szurszewski JH (2010) Endogenous production of H2S in the gastrointestinal tract: still in search of a physiologic function. Antioxid Redox Signal 12:1135-1146. CrossRef Medline
19. Linden DR, Furne J, Stoltz GJ, Abdel-Rehim MS, Levitt MD, Szurszewski JH (2012) Sulphide quinone reductase contributes to hydrogen sulphide metabolism in murine peripheral tissues but not in the CNS. Br J Pharmacol 165:2178-2190. CrossRef Medline
20. Maeda Y, Aoki Y, Sekiguchi F, Matsunami M, Takahashi T, Nishikawa H, Kawabata A (2009) Hyperalgesia induced by spinal and peripheral hydrogen sulfide: evidence for involvement of Cav3.2 T-type calcium channels. Pain 142:127-132. CrossRef Medline
21. Matsunami M, Tarui T, Mitani K, Nagasawa K, Fukushima O, Okubo K, Yoshida S, Takemura M, Kawabata A (2009) Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut 58:751-761. CrossRef Medline
22. Miller SM, Szurszewski JH (1997) Colonic mechanosensory afferent input to neurons in the mouse superior mesenteric ganglion. Am J Physiol 272:G357-G366. Medline
23. Miller SM, Szurszewski JH (2002) Relationship between colonic motility and cholinergic mechanosensory afferent synaptic input to mouse superior mesenteric ganglion. Neurogastroenterol Motil 14:339-348. CrossRef Medline
24. Mimoun S, Andriamihaja M, Chaumontet C, Atanasiu C, Benamouzig R, Blouin JM, Tomé D, Bouillaud F, Blachier F (2012) Detoxification of H(2)S by differentiated colonic epithelial cells: implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid Redox Signal 17:1-10. CrossRef Medline
25. Nagai Y, Tsugane M, Oka J, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18:557-559. CrossRef Medline
26. Pagliusi SR, Gomes C, Leite JR, Trolin G (1983) Aminooxyacetic acid induced accumulation of GABA in the rat brain. Interaction with GABA receptors and distribution in compartments. Naunyn Schmiedebergs Arch Pharmacol 322:210-215. CrossRef Medline
27. Parkman HP, Stapelfeldt WH, Williams CL, Lennon VA, Szurszewski JH (1993) Enteric GABA-containing nerves projecting to the guinea-pig inferior mesenteric ganglion modulate acetylcholine release. J Physiol 471: 191-207. Medline
28. Patacchini R, Santicioli P, Giuliani S, Maggi CA (2004) Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder. Br J Pharmacol 142:31-34. CrossRef Medline
29. Sarna SK (1991) Physiology and pathophysiology of colonic motor activity (2). Dig Dis Sci 36:998-1018. CrossRef Medline
30. Sawynok J, LaBella FS (1982) On the involvement of GABA in the analgesia produced by baclofen, muscimol and morphine. Neuropharmacology 21:397-403. CrossRef Medline
31. Schicho R, Krueger D, Zeller F, Von Weyhern CW, Frieling T, Kimura H, Ishii I, De Giorgio R, Campi B, Schemann M (2006) Hydrogen sulfide is a novel prosecretory neuromodulator in the Guinea-pig and human colon. Gastroenterology 131:1542-1552. CrossRef Medline
32. Sha L, Farrugia G, Linden DR, Szurszewski JH (2010) The transwall gradient across the mouse colonic circular muscle layer is carbon monoxide dependent. FASEB J 24:3840-3849. CrossRef Medline
33. StapelfeldtWH, Parkman HP, Szurszewski JH (1993) The electrophysiological effects of endogenous GABA in the guinea-pig inferior mesenteric ganglion. J Physiol 471:175-189. Medline
34. Stevens CF, Wang Y (1995) Facilitation and depression at single central synapses. Neuron 14:795-802. CrossRef Medline
35. Szurszewski JH, Linden DR (2012) Physiology of prevertebral sympathetic ganglia. In: Physiology of the gastrointestinal tract (Johnson LR, Ghishan FK, Kaunitz JD, Merchant JL, Hamid SM, Wood JD, eds), pp 583-627. Boston: Academic.
36. Tan BH, Wong PT, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3-10. CrossRef Medline
37. 2+ channels determines fast neurotransmitter release. Neuron 53:563-575. CrossRef Medline
38. Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791-896. CrossRef Medline
39. Wood JD (1999) Neurotransmission at the interface of sympathetic and enteric divisions of the autonomic nervous system. Chin J Physiol 42:201-210. Medline
40. Wu LG, Borst JG (1999) The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23: 821-832. CrossRef Medline
41. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322:587-590. CrossRef Medline
42. Yong QC, Choo CH, Tan BH, Low CM, Bian JS (2010) Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells. Neurochem Int 56:508-515. CrossRef Medline