The endogenous hydrogen sulfide producing enzyme cystathionine-β synthase contributes to visceral hypersensitivity in a rat model of irritable bowel syndrome

Molecular Pain

Volumn 5, Issue , 2009, Pages

  Xu, Guang Yin ^a   Winston, John H ^a   Shenoy, Mohan ^b   Zhou, Shufang ^a   Chen, Jiande D Z ^a   Pasricha, Pankai J ^b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; CYSTATHIONINE BETA SYNTHASE; HYDROGEN SULFIDE; HYDROXYLAMINE; PURINERGIC P2X3 RECEPTOR; VANILLOID RECEPTOR 1;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC VISCERAL HYPERALGESIA; COLON DILATATION; CONTROLLED STUDY; ELECTROSTIMULATION; ENTEROPATHY; IMMUNOREACTIVITY; IRRITABLE COLON; MALE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; SPINAL GANGLION; UPREGULATION; WESTERN BLOTTING; ABDOMINAL REFLEX; ANIMAL; CHEMICALLY INDUCED DISORDER; COLON; FLUORESCENT ANTIBODY TECHNIQUE; HYPERALGESIA; INNERVATION; METABOLISM; PATCH CLAMP; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VISCERA;

ACETIC ACID; ANIMALS; BLOTTING, WESTERN; COLON; CYSTATHIONINE BETA-SYNTHASE; FLUORESCENT ANTIBODY TECHNIQUE; GANGLIA, SPINAL; HYDROGEN SULFIDE; HYPERALGESIA; IRRITABLE BOWEL SYNDROME; MALE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; REFLEX, ABDOMINAL; VISCERA;

EID: 69549118509     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-5-44     Document Type: Article

References (38)

1. Eto K Kimura H A novel enhancing mechanism for hydrogen sulfide-producing activity of cystathionine beta-synthase J Biol Chem 2002, 277:42680-5. 10.1074/jbc.M205835200 12213817
2. Julian D Statile JL Wohlgemuth SE Arp AJ Enzymatic hydrogen sulfide production in marine invertebrate tissues Comp Biochem Physiol A Mol Integr Physiol 2002, 133:105-15. 10.1016/S1095-6433(02)00122-8 12160876
3. Levonen AL Lapatto R Saksela M Raivio KO Human cystathionine gamma-lyase: Developmental and in vitro expression of two isoforms Biochem J 2000, 347(Pt 1):291-5. 10.1042/0264-6021:3470291 1220959 10727430
4. Chen X Jhee KH Kruger WD Production of the neuromodulator H2S by cystathionine beta-synthase via the condensation of cysteine and homocysteine J Biol Chem 2004, 279:52082-6. 10.1074/jbc.C400481200 15520012
5. Yusuf M Kwong Huat BT Hsu A Whiteman M Bhatia M Moore PK Streptozotocin-induced diabetes in the rat is associated with enhanced tissue hydrogen sulfide biosynthesis Biochem Biophys Res Commun 2005, 333:1146-52. 10.1016/j.bbrc.2005.06.021 15967410
6. Li L Bhatia M Moore PK Hydrogen sulphide - a novel mediator of inflammation? Curr Opin Pharmacol 2006, 6:125-9. 10.1016/ j.coph.2005.10.007 16487749
7. Zanardo RC Brancaleone V Distrutti E Fiorucci S Cirino G Wallace JL Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation Faseb J 2006, 20:2118-20. 10.1096/fj.06-6270fje 16912151
8. Patacchini R Santicioli P Giuliani S Maggi CA Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder Br J Pharmacol 2004, 142:31-4. 10.1038/sj.bjp.0705764 1574935 15051627
9. Trevisani M Patacchini R Nicoletti P Gatti R Gazzieri D Lissi N Zagli G Creminon C Geppetti P Harrison S Hydrogen sulfide causes vanilloid receptor 1-mediated neurogenic inflammation in the airways Br J Pharmacol 2005, 145:1123-31. 10.1038/sj.bjp.0706277 1576227 15937520
10. Schicho R Krueger D Zeller F Von Weyhern CW Frieling T Kimura H Ishii I De Giorgio R Campi B Schemann M Hydrogen sulfide is a novel prosecretory neuromodulator in the Guinea-pig and human colon Gastroenterology 2006, 131:1542-52. 10.1053/j.gastro.2006.08.035 17101327
11. Matsunami M Tarui T Mitani K Nagasawa K Fukushima O Okubo K Yoshida S Takemura M Kawabata A Luminal hydrogen sulfide plays a pro-nociceptive role in mouse colon Gut 2009, 58:751-761. 10.1136/gut.2007.144543 18852258
12. Lee AT Shah JJ Li L Cheng Y Moore PK Khanna S A nociceptive-intensity-dependent role for hydrogen sulphide in the formalin model of persistent inflammatory pain Neuroscience 2008, 152:89-96. 10.1016/j.neuroscience.2007.11.052 18248901
13. Bhatia M Sidhapuriwala J Moochhala SM Moore PK Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat Br J Pharmacol 2005, 145:141-4. 10.1038/sj.bjp.0706186 1576135 15753944
14. Distrutti E Sediari L Mencarelli A Renga B Orlandi S Antonelli E Roviezzo F Morelli A Cirino G Wallace JL Fiorucci S Evidence that hydrogen sulfide exerts antinociceptive effects in the gastrointestinal tract by activating KATP channels J Pharmacol Exp Ther 2006, 316:325-35. 10.1124/jpet.105.091595 16192316
15. Distrutti E Sediari L Mencarelli A Renga B Orlandi S Russo G Caliendo G Santagada V Cirino G Wallace JL Fiorucci S 5-Amino-2-hydroxybenzoic acid 4-(5-thioxo-5H-[1,2]dithiol-3yl)-phenyl ester (ATB-429), a hydrogen sulfide-releasing derivative of mesalamine, exerts antinociceptive effects in a model of postinflammatory hypersensitivity J Pharmacol Exp Ther 2006, 319:447-58. 10.1124/jpet.106.106435 16855178
16. Winston J Shenoy M Medley D Naniwadekar A Pasricha PJ The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats Gastroenterology 2007, 132:615-27. 10.1053/j.gastro.2006.11.014 17258716
17. Xu GY Shenoy M Winston JH Mittal S Pasricha PJ P2X receptor-mediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity Gut 2008, 57:1230-7. 10.1136/gut.2007.134221 18270243
18. Xu GY Shenoy M Winston JH Micici M-A Pasricha PJ A pro-nociceptive role for hydrogen sulfide in irritable bowel syndrome [Abstract] Gastroenterology 2008, 134:A-560. 10.1016/S0016-5085(08)62614-1
19. Xu GY Winston JH Shenoy M Yin H Pendyala S Pasricha PJ Transient Receptor Potential Vanilloid 1 Mediates Hyperalgesia and Is Up-Regulated in Rats With Chronic Pancreatitis Gastroenterology 2007, 133:1282-92. 10.1053/j.gastro.2007.06.015 17698068
20. Al-Chaer ED Kawasaki M Pasricha PJ A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development Gastroenterology 2000, 119:1276-85. 10.1053/ gast.2000.19576 11054385
21. Xu GY Huang LY Ca2+/calmodulin-dependent protein kinase II potentiates ATP responses by promoting trafficking of P2X receptors Proc Natl Acad Sci USA 2004, 101:11868-73. 10.1073/pnas.0401490101 511066 15292517
22. Qu K Chen CP Halliwell B Moore PK Wong PT Hydrogen sulfide is a mediator of cerebral ischemic damage Stroke 2006, 37:889-93. 10.1161/ 01.STR.0000204184.34946.41 16439695
23. Xu GY Winston JH Chen JD Electroacupuncture attenuates visceral hyperalgesia and inhibits the enhanced excitability of colon specific sensory neurons in a rat model of irritable bowel syndrome Neurogastroenterol Motil 2009. 19558427
24. Abe K Kimura H The possible role of hydrogen sulfide as an endogenous neuromodulator J Neurosci 1996, 16:1066-71. 8558235
25. Kimura H Hydrogen sulfide as a neuromodulator Mol Neurobiol 2002, 26:13-9. 10.1385/MN:26:1:013 12392053
26. Moore PK Bhatia M Moochhala S Hydrogen sulfide: From the smell of the past to the mediator of the future? Trends Pharmacol Sci 2003, 24:609-11. 10.1016/j.tips.2003.10.007 14654297
27. Wang R Two's company, three's a crowd: Can H2S be the third endogenous gaseous transmitter? Faseb J 2002, 16:1792-8. 10.1096/fj.02-0211hyp 12409322
28. Eto K Ogasawara M Umemura K Nagai Y Kimura H Hydrogen sulfide is produced in response to neuronal excitation J Neurosci 2002, 22:3386-91. 11978815
29. Kombian SB Reiffenstein RJ Colmers WF The actions of hydrogen sulfide on dorsal raphe serotonergic neurons in vitro J Neurophysiol 1993, 70:81-96. 8395590
30. Dello Russo C Tringali G Ragazzoni E Maggiano N Menini E Vairano M Preziosi P Navarra P Evidence that hydrogen sulphide can modulate hypothalamo-pituitary-adrenal axis function: In vitro and in vivo studies in the rat J Neuroendocrinol 2000, 12:225-33. 10.1046/ j.1365-2826.2000.00441.x 10718918
31. Li L Bhatia M Zhu YZ Zhu YC Ramnath RD Wang ZJ Anuar FB Whiteman M Salto-Tellez M Moore PK Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse Faseb J 2005, 19:1196-8. 15863703
32. Kawabata A Ishiki T Nagasawa K Yoshida S Maeda Y Takahashi T Sekiguchi F Wada T Ichida S Nishikawa H Hydrogen sulfide as a novel nociceptive messenger Pain 2007, 132:74-81. 10.1016/j.pain.2007.01.026 17346888
33. Cunha TM Dal-Secco D Verri WA Jr Guerrero AT Souza GR Vieira SM Lotufo CM Neto AF Ferreira SH Cunha FQ Dual role of hydrogen sulfide in mechanical inflammatory hypernociception Eur J Pharmacol 2008, 590:127-35. 10.1016/j.ejphar.2008.05.048 18585702
34. Bao L Vlcek C Paces V Kraus JP Identification and tissue distribution of human cystathionine beta-synthase mRNA isoforms Arch Biochem Biophys 1998, 350:95-103. 10.1006/abbi.1997.0486 9466825
35. Hosoki R Matsuki N Kimura H The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide Biochem Biophys Res Commun 1997, 237:527-31. 10.1006/bbrc.1997.6878 9299397
36. Evans CL The toxicity of hydrogen sulphide and other sulphides Q J Exp Physiol Cogn Med Sci 1967, 52:231-48. 5182405
37. Pace NR A molecular view of microbial diversity and the biosphere Science 1997, 276:734-40. 10.1126/science.276.5313.734 9115194
38. Deplancke B Gaskins HR Hydrogen sulfide induces serum-independent cell cycle entry in nontransformed rat intestinal epithelial cells Faseb J 2003, 17:1310-2. 12738807