Hydrogen sulfide's involvement in modulating nociception

Pain Physician

Volumn 12, Issue 5, 2009, Pages 901-910

  Smith, Howard S ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Analgesia; Calcium channels; Hydrogen sulfide; Nociception; Pain; Potassium channels

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM CHANNEL T TYPE; CORTICOTROPIN RELEASING FACTOR; CYCLIC AMP; HYDROGEN SULFIDE; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ANALGESIA; DRUG TARGETING; FACILITATION; GLIA CELL; HIPPOCAMPUS; HUMAN; HYPERPOLARIZATION; LEARNING; LONG TERM POTENTIATION; MEMORY; MOLECULAR INTERACTION; NERVE CELL; NERVE FUNCTION; NEUROMODULATION; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM CHANNELS; CALCIUM CHANNELS, T-TYPE; HUMANS; HYDROGEN SULFIDE; ION CHANNEL GATING; NERVE TISSUE PROTEINS; NOCICEPTORS; PAIN; RECEPTORS, N-METHYL-D-ASPARTATE; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 70449646830     PISSN: 15333159     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (81)

1. Wang R. Two's company, three's a crowd: Can H2S be the third endogenous gaseous transmitter? Faseb J 2002; 16:1792-1798. (Pubitemid 35340360)
2. 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; 131:1542-1552. (Pubitemid 44708939)
3. Roediger WE, Moore J, Babidge W. Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Dig Dis Sci 1997; 42:1571-1579. (Pubitemid 27394576)
4. Huycke MM, Gaskins HR. Commensal bacteria, redox stress, and colorectal cancer: Mechanisms and models. Exp Biol Med (Maywood) 2004; 229:586-597.
5. Ohge H, Furne JK, Springfield J, Sueda T, Madoff RD, Levitt MD. The effect of antibiotics and bismuth on fecal hydrogen sulfide and sulfate-reducing bacteria in the rat. FEMS Microbiol Lett 2003; 228:137-142. (Pubitemid 37377958)
6. Reiffenstein RJ, Hulbert WC, Roth SH. Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 1992; 32:109-134.
7. Tang G, Wu L, Liang W, Wang R. Direct stimulation of KATP channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells. Mol Pharmacol 2005; 68:1757-1764. (Pubitemid 41654358)
8. Ali MY, Ping CY, Mok YY, Ling L, Whiteman M, Bhatia M, Moore PK. Regulation of vascular nitric oxide in vitro and in vivo: A new role for endogenous hydrogen sulphide? Br J Pharmacol 2006; 149:625-634. (Pubitemid 44748055)
9. Kubo S, Doe I, Kurokawa Y, Nishikawa H, Kawabata A. Direct inhibition of endothelial nitric oxide synthase by hydrogen sulfide: contribution to dual modulation of vascular tension. Toxicology 2007; 232:138-146. (Pubitemid 46283181)
10. Oh GS, Pae HO, Lee BS, Kim BN, Kim JM, Kim HR, Jeon SB, Jeon WK, Chae HJ, Chung HT. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med 2006;41:106-119.
11. 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. (Pubitemid 47494563)
12. Todorovic SM, Jevtovic-Todorovic V, Meyenburg A, Mennerick S, Perez-Reyes E, Romano C, Olney JW, Zorumski CF. Redox modulation of T-type calcium channels in rat peripheral nociceptors. Neuron 2001; 31:75-85. (Pubitemid 32757090)
13. Nelson MT, Joksovic PM, Perez-Reyes E, Todorovic SM. The endogenous redox agent L-cysteine induces T-type Ca2+ channel-dependent sensitization of a novel subpopulation of rat peripheral nociceptors. J Neurosci 2005; 25:8766-8775. (Pubitemid 41362055)
14. Joksovic PM, Nelson MT, Jevtovic-Todorovic V, Patel MK, Perez-Reyes E, Campbell KP, Chen CC, Todorovic SM. Cav3.2 is the major molecular substrate for redox regulation of T-type Ca2+ channels in the rat and mouse thalamus. J Physiol 2006; 574:415-430.
15. Bourinet E, Alloui A, Monteil A, Barrère C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, Eschalier A, Nargeot J. Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. Embo J 2005; 24:315-324. (Pubitemid 40216136)
16. 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; 142:31-34. (Pubitemid 38698190)
17. 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; 145:1123-1131. (Pubitemid 43079985)
18. Boehning D, Snyder SH. Novel neural modulators. Annu Rev Neurosci 2003; 26:105-131.
19. Zhao W, Zhang J, Lu Y, Wang R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO (Eur Mol Biol Organ) J 2001; 20:6008-6016. (Pubitemid 33049276)
20. Awata S, Nakayama R, Suzuki I, Sugahara K, Kodama H. Change in cystathionine gamma-lyase in various regions of rat brain during development. Biochem Mol Biol Int 1995; 35:1331-1338. (Pubitemid 26172945)
21. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 1996; 16:1066-1071. (Pubitemid 26140863)
22. Kimura H. Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptors. Biochem Biophys Res Commun 2000; 267:129-133. (Pubitemid 30072519)
23. Russo CD, Tringali G, Ragazzoni E, Maggiano N, Menini E, Vairano M, Preziosi P, Navarra P. Evidence that hydrogen sulphide can modulate hypothalamuspituitary-adrenal axis function: in vitro and in vivo studies in the rat. J Neuroendocrinol 2000; 12:225-233. (Pubitemid 30156514)
24. 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: 609-611. (Pubitemid 37494778)
25. 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; 237:527-531. (Pubitemid 27434718)
26. Eto K, Kimura H. A novel enhancing mechanism for hydrogen sulfide-producing activity of cystathionine-synthase. J Biol Chem 2002; 277:42680-42685. (Pubitemid 35285637)
27. 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 activiating KATP channels. J Pharmacol Exp Ther 2006; 316: 325-335. (Pubitemid 41832612)
28. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R. H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine-lyase. Science Magazine 2008; 322:587-1509
29. Lee A T-H, Li L, Shah JJ, 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.
30. Jevtovic-Todorovic V, Todorovic SM. The role of peripheral T-type calcium channels in pain transmission. Cell Calcium 2006; 40:197-203. (Pubitemid 43942301)
31. 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 200; 58:751-761. Epub 2008 Oct 13.
32. Nelson MT, Woo J, Kang HW, Vitko I, Barrett PQ, Perez-Reyes E, Lee JH, Shin HS, Todorovic SM. Reducing agents sensitize C-type nociceptors by relieving high-affinity zinc inhibition of T-type calcium channels. J Neurosci 2007; 27:8250-8260. (Pubitemid 47219607)
33. Chemin J, Nargeot J, Lory P. Neuronal T-type alpha 1H calcium channels induce neuritogenesis and expression of high-voltage activated calcium channels in the NG108-15 cell line. J Neurosci 2002; 22:6856-6862. (Pubitemid 35379143)
34. Kawabata A, Ishiki T, Nagasawa K, Yoshia S, Maeda Y, Takahashi T, Sekiquichi F, Wada T, Ichida S, Nishikawa H. Hydrogen sulfide as a novel nociceptive messenger. Pain 2007; 132:74-81. (Pubitemid 47494563)
35. Nishimura S, Fukushima O, Ishikura H, Takahashi T, Matsunami M, Tsujiuchi T, Sekiguchi F, Naruse M, Kamanaka Y, Kawabata A. Hydrogen sulfide as a novel mediator for pancreatic pain in rodents. Gut 2009; 58:762-770. Epub 2009 Feb 6
36. Matsunami M, Tarui T, Mitani K, Nagasawa K, Fukushima O, Okubo K, Yoshida S, Takemura M, Kawabata A. Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut 2009; 58:751-761. Epub 2008 Oct 13
37. Kawabata A. Novel functions of hydrogen sulfide through T-type calcium channels: Its involvement in pain processing. J Pharmacol Sci 2008; 106:47P.
38. Maeda Y, Aoki Y, Sekiguchi F, Matsunami M, Takahashi T, Nishikawa H, Kawabata A. Hyperalgesia induced by spinal and peripheral hydrogen sulfide: Evidence for involvement of Cav3.2 T-type calcium channels. Pain 2009; 142:127-132.
39. Lee AT, Shah JJ, Li L, Cheng Y, Moore PK, Khanna S. A nociceptive-intensitydependent role for hydrogen sulphide in the formalin model of persistent inflammatory pain. Neuroscience 2008; 152:89-96.
40. Nelson MT, Woo J, Kang HW, Vitko I, Barrett PQ, Perez-Reyes E, Lee JH, Shin HS, Todorovic SM. Reducing agents sensitize C-type nociceptors by relieving high-affinity zinc inhibition of T-type calcium channels. J Neurosci 2007; 27:8250-8260. (Pubitemid 47219607)
41. 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: 447-458. (Pubitemid 44455152)
42. Cunha TM, Dal-Secco D, Verri Jr. WA, Guerrero AT, Souza GR, Viera SM, Lotufo CM, Neto AF, Ferreira SH, Cunha FQ. Dual role of hydrogen sulfide in mechanical inflammatory hypernociception. Eur J Pharmacol 2008; 590:127-135.
43. Cunha FQ, Poole S, Lorenzetti BB, Ferreira SH. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol 1992; 107:660-664.
44. Cunha TM, Verri Jr WA, Schivo IR, Napimoga MH, Parada CA, Poole S, Teixeira MM, Ferreira SH, Cunha FQ. Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J Leukoc Biol 2008; 83:824-832. (Pubitemid 351959862)
45. Cunha TM, Barsante MM, Guerrero AT, Verri Jr WA, Ferreira SH, Coelho FM, Bertini R, Di Giacinto C, Allegretti M, Cunha FQ, Teixeira MM. Treatment with DF 2162, a non-competitive allosteric inhibitor of CXCR1/2, diminishes neutrophil influx and inflammatory hypernociception in mice. Br J Pharmacol 2008; 154:460-470. (Pubitemid 351670607)
46. 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; 145:141-144. (Pubitemid 40756518)
47. Zhang H, Zhi L, Moochhala SM, Moore PK, Bhatia M. Endogenous hydrogen sulfide regulates leukocyte trafficking in cecal ligation and puncture-induced sepsis. J Leukoc Biol 2007; 82:894-905. (Pubitemid 47511050)
48. Soares AC, Duarte ID. Dibutyryl-cyclic GMP induces peripheral antinociception via activation of ATP-sensitive K(+) channels in the rat PGE2-induced hyperalgesic paw. Br J Pharmacol 2001; 134:127-131.
49. Soares AC, Leite R, Tatsuo MA, Duarte ID. Activation of ATP-sensitive K(+) channels: Mechanism of peripheral antinociceptive action of the nitric oxide donor, sodium nitroprusside. Eur J Pharmacol 2000; 400:67-71. (Pubitemid 30412110)
50. Rodrigues AR, Duarte ID. The peripheral antinociceptive effect induced by morphine is associated with ATP-sensitive K(+) channels. Br J Pharmacol 2000; 129:110-114. (Pubitemid 30072676)
51. Sachs D, Cunha FQ, Ferreira SH. Peripheral analgesic blockade of hypernociception: Activation of arginine/NO/ cGMP/protein kinase G/ATP-sensitive K+ channel pathway. Proc Natl Acad Sci U S A 2004; 101:3680-3685. (Pubitemid 38338254)
52. Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia- reperfusion injury - evidence for a role of K ATP channels. Basic Res Cardiol 2006; 101:53-60. (Pubitemid 43323432)
53. Yang W, Yang G, Jia X, Wu L, Wang R. Activation of KATP channels by H2S in rat insulin-secreting cells and the underlying mechanisms. J Physiol 2005; 569:519-531. (Pubitemid 41830119)
54. Chi XX, Jiang X, Nicol GD. ATP-sensitive potassium currents reduce the PGE2- mediated enhancement of excitability in adult rat sensory neurons. Brain Res 2007; 1145:28-40. (Pubitemid 46497981)
55. Granger DN, Kubes P. The microcirculation and inflammation: Modulation of leukocyte-endothelial cell adhesion. J Leukoc Biol 1994; 55:662-675. (Pubitemid 24171735)
56. Kubes P, Heit B, van Marle G, Johnston JB, Knight D, Khan A, Power C. In vivo impairment of neutrophil recruitment during lentivirus infection. J Immunol 2003; 171:4801-4808. (Pubitemid 37310600)
57. Gal I, Bajnok E, Szanto S, Sarraj B, Glant TT, Mikecz K. Visualization and in situ analysis of leukocyte trafficking into the ankle joint in a systemic murine model of rheumatoid arthritis. Arthritis Rheum 2005; 52:3269-3278. (Pubitemid 41447110)
58. Gregory JL, Leech MT, David JR, Yang YH, Dacumos A, Hickey MJ. Reduced leukocyte-endothelial cell interactions in the inflamed microcirculation of macrophage migration inhibitory factor-deficient mice. Arthritis Rheum 2004; 50:3023-3034. (Pubitemid 39209542)
59. Veihelmann A, Szczesny G, Nolte D, Krombach F, Refior HJ, Messmer K. A novel model for the study of synovial microcirculation in the mouse knee joint in vivo. Res Exp Med (Berlin) 1998; 198:43-54. (Pubitemid 28376864)
60. Andruski B, McCafferty D-M, Ignacy T, Millen B, McDougall JJ. Leukocyte trafficking and pain behavioral responses to a hydrogen sulfide donor in acute monoarthritis. Am J Physiol Integr Comp Physiol 2008; 295:R814-R820.
61. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Benjamin F. Cravatt BF, Patapoutian A. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 2007; 445:541-545. (Pubitemid 46197634)
62. Dinkova-Kostova AT, Massiah MA, Bozak RE, Hicks RJ, Talalay P. Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc. Natl Acad Sci USA 2001; 98:3404-3409. (Pubitemid 32220858)
63. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006; 124:1269-1282.
64. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 2004; 41:849-857. (Pubitemid 38429729)
65. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P. Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: Metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev 2001; 10:501-508. (Pubitemid 32701637)
66. Eggler AL, Liu G, Pezzuto JM, van Breemen RB, Mesecar AD. Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc Natl Acad. Sci USA 2005; 102:10070-10075. (Pubitemid 41023327)
67. Fearon IM, Palmer AC, Balmforth AJ, Ball SG, Varadi G, Peers C. Modulation of recombinant human cardiac L-type Ca21 channel alpha 1C subunits by redox agents and hypoxia. J Physiol (Lond) 1999; 514:629-637. (Pubitemid 29060310)
68. Grabarek Z, Gergely J. Zero-length crosslinking procedure with the use of active esters. Anal Biochem 1990; 185:131-135. (Pubitemid 20082102)
69. Streng T, Axelsson HE, Hedlund P, Andersson DA, Jord S-E, Stuart Bevan S, Andersson K-E, Högestätt ED, Zygmunt PM. Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder. Eur Urology 2008; 53:391-400. (Pubitemid 350296588)
70. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003; 112:819-829. (Pubitemid 36378884)
71. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Högestätt ED, Meng ID, Julius D. Mustard oils and cannabinoids excite sensory nerve fi- bres through the TRP channel ANKTM1. Nature 2004; 427:260-265. (Pubitemid 38112043)
72. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Högestätt ED, Julius D, Jordt SE, Zygmunt PM. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 2005; 102:12248-12252. (Pubitemid 41291160)
73. Patacchini R, Santicioli P, Giuliani S, Maggi CA. Pharmacological investigation of hydrogen sulfide (H2S) contractile activity in rat detrusor muscle. Eur J Pharmacol 2005; 509:171-177. (Pubitemid 40279075)
74. Cox PJ. Cyclophosphamide cystitis - identification of acrolein as the causative agent. Biochem Pharmacol 1979; 28:2045-2049.
75. McMahon SB, Abel C. A model for the study of visceral pain states: Chronic inflammation of the chronic decerebrate rat urinary bladder by irritant chemicals. Pain 1987; 28:109-127. (Pubitemid 17210463)
76. Hjerling-Leffer J, Alqatari M, Ernfors P, Koltzenburg M. Emergemce of functional sensory subtypes as defined by transient receptor potential channel expression. J Neurosci 2007; 27:2435-2443. (Pubitemid 46393589)
77. Hu H, Bandell M, Petrus MJ, Zhu MX, Patapoutian A. Zinc activates damagesensing TRPA1 ion channels. Nat Chem Biol 2009; 5:183-190.
78. Kimura H. Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 2000; 267:129-133. (Pubitemid 30072519)
79. Lefer DJ. A new gaseous signaling molecule emerges: Cardioprotective role of hydrogen sulfide. Proc Natl Acad Sci USA 2007; 104:17907-17908.
80. Blackstone E, Morrison M, Roth MB. H2S induces a suspended animation- like state in mice. Science 2005; 308:518. (Pubitemid 40570576)
81. d'Emmanuele di Villa Bianca R, Sorrentino R, Maffia P, Mirone V, Imbimbo C, Fusco F, De Palma R, Ignarro LJ, Cirino G. Hydrogen sulfide as a mediator of human corpus cavernosum smooth-muscle relaxation. Proc Natl Acad Sci USA 2009; 106:4513-4518. Epub 2009 Mar 2