Hydrogen sulphide inhibits Ca2+ release through InsP3 receptors and relaxes airway smooth muscle

Journal of Physiology

Volumn 591, Issue 23, 2013, Pages 5999-6015

  Castro Piedras, Isabel ^a,b   Perez Zoghbi, Jose F ^a,b  

^a Department of Cell Physiology and Molecular Biophysics ^*  (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN SULFIDE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ANIMAL TISSUE; ARTICLE; BREATHING MUSCLE; BRONCHODILATATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; PHASE CONTRAST MICROSCOPY; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE RELAXATION; VIDEO MICROSCOPY;

ANIMALS; CALCIUM; HYDROGEN SULFIDE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LUNG; MALE; MICE; MICE, INBRED C3H; MUSCLE RELAXATION; MUSCLE, SMOOTH;

EID: 84888431888     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.257790     Document Type: Article

References (64)

1. Asimakopoulou A, Panopoulos P, Chasapis CT, Coletta C, Zhou Z, Cirino G, Giannis A, Szabo C, Spyroulias GA & Papapetropoulos A (2013). Selectivity of commonly used pharmacological inhibitors for cystathionine β synthase (CBS) and cystathionine γ lyase (CSE). Br J Pharmacol 169, 922-932.
2. 2+ signalling of airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 297, L347-L361.
3. 3 receptor. Respir Res 7, 34.
4. 2+ sensitivity of airway smooth muscle cells in murine lung slices. Am J Physiol Lung Cell Mol Physiol 291, L208-L221.
5. Bergner A & Sanderson MJ (2002). Acetylcholine-induced calcium signaling and contraction of airway smooth muscle cells in lung slices. J Gen Physiol 119, 187-198.
6. 2+ spikes in HeLa cells by sensitizing the inositol 1, 4, 5-trisphosphate receptor. J Biol Chem 267, 25113-25119.
7. Broderius SJ & Smith LLJ (1977). Direct determination and calculation of aqueous hydrogen sulfide. Anal Chem 49, 424-428.
8. Bucci M, Papapetropoulos A, Vellecco V, Zhou Z, Pyriochou A, Roussos C, Roviezzo F, Brancaleone V & Cirino G (2010). Hydrogen sulfide is an endogenous inhibitor of phosphodiesterase activity. Arterioscler Thromb Vasc Biol 30, 1998-2004.
9. Bucci M, Papapetropoulos A, Vellecco V, Zhou Z, Zaid A, Giannogonas P, Cantalupo A, Dhayade S, Karalis KP, Wang R, Feil R & Cirino G (2012). cGMP-dependent protein kinase contributes to hydrogen sulfide-stimulated vasorelaxation. PLoS One 7, e53319.
10. Burgel PR (2011). The role of small airways in obstructive airway diseases. Eur Respir Rev 20, 23-33.
11. Chen YH, Wu R, Geng B, Qi YF, Wang PP, Yao WZ & Tang CS (2009). Endogenous hydrogen sulfide reduces airway inflammation and remodeling in a rat model of asthma. Cytokine 45, 117-123.
12. Cheng Y, Ndisang JF, Tang G, Cao K & Wang R (2004). Hydrogen sulfide-induced relaxation of resistance mesenteric artery beds of rats. Am J Physiol Heart Circ Physiol 287, H2316-H2323.
13. DeLeon ER, Stoy GF & Olson KR (2012). Passive loss of hydrogen sulfide in biological experiments. Anal Biochem 421, 203-207.
14. 2+ signaling of small airways in mouse lung slices. Am J Respir Cell Mol Biol 38, 524-531.
15. 2+ signalling of mouse airway smooth muscle cells. Am J Respir Cell Mol Biol 42, 373-381.
16. d'Emmanuele di Villa Bianca R, Sorrentino R, Maffia P, Mirone V, Imbimbo C, Fusco F, De Palma R, Ignarro LJ & Cirino G (2009). Hydrogen sulfide as a mediator of human corpus cavernosum smooth-muscle relaxation. Proc Natl Acad Sci U S A 106, 4513-4518.
17. Denizalti M, Durlu-Kandilci NT, Bozkurt TE & Sahin-Erdemli I (2011). Hydrogen sulphide inhibits carbachol-induced contractile responses in β-escin permeabilized guinea-pig taenia caecum. Eur J Pharmacol 658, 229-235.
18. Dhaese I & Lefebvre RA (2009). Myosin light chain phosphatase activation is involved in the hydrogen sulfide-induced relaxation in mouse gastric fundus. Eur J Pharmacol 606, 180-186.
19. 2+ release channels. Physiol Rev 87, 593-658.
20. 2S) metabolism in mitochondria and its regulatory role in energy production. Proc Natl Acad Sci U S A 109, 2943-2948.
21. Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T & Mikoshiba K (2005). Subtype-specific and ER lumenal environment-dependent regulation of inositol 1, 4, 5-trisphosphate receptor type 1 by ERp44. Cell 120, 85-98.
22. Hilly M, Pietri-Rouxel F, Coquil JF, Guy M & Mauger JP (1993). Thiol reagents increase the affinity of the inositol 1, 4, 5-trisphosphate receptor. J Biol Chem 268, 16488-16494.
23. Ishigami M, Hiraki K, Umemura K, Ogasawara Y, Ishii K & Kimura H (2009). A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid Redox Signal 11, 205-214.
24. Jiang X, Yang F, Brailoiu E, Jakubowski H, Dun NJ, Schafer AI, Yang X, Durante W & Wang H (2007). Differential regulation of homocysteine transport in vascular endothelial and smooth muscle cells. Arterioscler Thromb Vasc Biol 27, 1976-1983.
25. Kabil O & Banerjee R (2010). Redox biochemistry of hydrogen sulfide. J Biol Chem 285, 21903-21907.
26. 2+ on the inositol 1, 4, 5-trisphosphate receptor L3-1 loop region: implications for receptor regulation. J Biol Chem 283, 25567-25575.
27. Kaplin AI, Ferris CD, Voglmaier SM & Snyder SH (1994). Purified reconstituted inositol 1, 4, 5-trisphosphate receptors. Thiol reagents act directly on receptor protein. J Biol Chem 269, 28972-28978.
28. Kimura H (2011). Hydrogen sulfide: its production, release and functions. Amino Acids 41, 113-121.
29. Kubo S, Doe I, Kurokawa Y & Kawabata A (2007). Hydrogen sulfide causes relaxation in mouse bronchial smooth muscle. J Pharmacol Sci 104, 392-396.
30. Lencesova L, Hudecova S, Csaderova L, Markova J, Soltysova A, Pastorek M, Sedlak J, Wood ME, Whiteman M, Ondrias K & Krizanova O (2013). Sulphide signalling potentiates apoptosis through the up-regulation of IP receptor types 1 and 2. Acta Physiol (Oxf) 208, 350-361.
31. Li L, Rose P & Moore PK (2011). Hydrogen sulfide and cell signalling. Annu Rev Pharmacol Toxicol 51, 169-187.
32. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH & Moore PK (2008). Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117, 2351-2360.
33. ATP channels. Am J Physiol Heart Circ Physiol 300, H2088-H2095.
34. 2+ homeostasis in cultured aortic endothelial cells. Am J Physiol Heart Circ Physiol 300, H493-H506.
35. Missiaen L, Taylor CW & Berridge MJ (1991). Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores. Nature 352, 241-244.
36. 2+ oscillations in hamster eggs. FEBS Lett 309, 180-184.
37. 2+ sensitization, and contraction activated by protein kinase C in small airway smooth muscle. J Gen Physiol 141, 165-178.
38. Nagy P, Palinkas Z, Nagy A, Budai B, Toth I & Vasas A (2013). Chemical aspects of hydrogen sulfide measurements in physiological samples. Biochim Biophys Acta xxx, doi: 10.1016.
39. Nishida M, Sawa T, Kitajima N, Ono K, Inoue H, Ihara H, Motohashi H, Yamamoto M, Suematsu M, Kurose H, van der Vliet A, Freeman BA, Shibata T, Uchida K, Kumagai Y & Akaike T (2012). Hydrogen sulfide anion regulates redox signalling via electrophile sulfhydration. Nat Chem Biol 8, 714-724.
40. Ogasawara Y, Ishii K, Togawa T & Tanabe S (1993). Determination of bound sulfur in serum by gas dialysis/high-performance liquid chromatography. Anal Biochem 215, 73-81.
41. Perez JF & Sanderson MJ (2005). The frequency of calcium oscillations induced by 5-HT, ACH, and KCl determine the contraction of smooth muscle cells of intrapulmonary bronchioles. J Gen Physiol 125, 535-553.
42. 2+ oscillations. J Gen Physiol 135, 247-259.
43. Perez-Zoghbi JF, Karner C, Ito S, Shepherd M, Alrashdan Y & Sanderson MJ (2009). Ion channel regulation of intracellular calcium and airway smooth muscle function. Pulm Pharmacol Ther 22, 388-397.
44. 2+ sensitization. Am J Physiol Lung Cell Mol Physiol 293, L1000-L1011.
45. Perry MM, Hui CK, Whiteman M, Wood ME, Adcock I, Kirkham P, Michaeloudes C & Chung KF (2011). Hydrogen sulfide inhibits proliferation and release of IL-8 from human airway smooth muscle cells. Am J Respir Cell Mol Biol 45, 746-752.
46. Rashid S, Heer JK, Garle MJ, Alexander SP & Roberts RE (2013). Hydrogen sulphide-induced relaxation of porcine peripheral bronchioles. Br J Pharmacol 168, 1902-1910.
47. Renga B (2011). Hydrogen sulfide generation in mammals: the molecular biology of cystathionine-β- synthase (CBS) and cystathionine-γ-lyase (CSE). Inflamm Allergy Drug Targets 10, 85-91.
48. Riddles PW, Blakeley RL & Zerner B (1979). Ellman's reagent: 5, 5′-dithiobis(2-nitrobenzoic acid)-a reexamination. Anal Biochem 94, 75-81.
49. Rooney TA, Renard DC, Sass EJ & Thomas AP (1991). Oscillatory cytosolic calcium waves independent of stimulated inositol 1, 4, 5-trisphosphate formation in hepatocytes. J Biol Chem 266, 12272-12282.
50. 2+ oscillations regulate contraction of intrapulmonary smooth muscle cells. Adv Exp Med Biol 661, 77-96.
51. Sanderson MJ & Parker I (2003). Video-rate confocal microscopy. Methods Enzymol 360, 447-481.
52. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83, 1325-1358.
53. Teague B, Asiedu S & Moore PK (2002). The smooth muscle relaxant effect of hydrogen sulphide in vitro: evidence for a physiological role to control intestinal contractility. Br J Pharmacol 137, 139-145.
54. 2S and pulmonary function in children with bronchial asthma. Mol Med Rep 6, 335-338.
55. 2+ sensitization of arterial muscle. Am J Physiol Cell Physiol 285, C1377-C1385.
56. Vandiver M & Snyder SH (2012). Hydrogen sulfide: a gasotransmitter of clinical relevance. J Mol Med (Berl) 90, 255-263.
57. Wang P, Zhang G, Wondimu T, Ross B & Wang R (2011). Hydrogen sulfide and asthma. Exp Physiol 96, 847-852.
58. Wang R (2011). Signaling pathways for the vascular effects of hydrogen sulfide. Curr Opin Nephrol Hypertens 20, 107-112.
59. Wang R (2012). Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92, 791-896.
60. Wu R, Yao WZ, Chen YH, Geng B & Tang CS (2008). [Plasma level of endogenous hydrogen sulfide in patients with acute asthma]. Beijing Da Xue Xue Bao 40, 505-508.
61. Yang G, Pei Y, Teng H, Cao Q & Wang R (2011). Specificity protein-1 as a critical regulator of human cystathionine γ-lyase in smooth muscle cells. J Biol Chem 286, 26450-26460.
62. 2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science 322, 587-590.
63. Zhang G, Wang P, Yang G, Cao Q & Wang R (2013). The inhibitory role of hydrogen sulfide in airway hyperresponsiveness and inflammation in a mouse model of asthma. Am J Pathol 182, 1188-1195.
64. ATP channel opener. EMBO J 20, 6008-6016.