Contribution of cysteine aminotransferase and mercaptopyruvate sulfurtransferase to hydrogen sulfide production in peripheral neurons

Journal of Neurochemistry

Volumn 130, Issue 1, 2014, Pages 29-40

  Miyamoto, Ryo ^a   Otsuguro, Ken Ichi ^a   Yamaguchi, Soichiro ^a   Ito, Shigeo ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

cysteine aminotransferase; dorsal root ganglion; hydrogen sulfide; mercaptopyruvate sulfurtransferase; mitochondria; peripheral neuron

Indexed keywords

3 MERCAPTOPYRUVATE SULFURTRANSFERASE; AMINOTRANSFERASE; ASPARTIC ACID; CATALASE; CYSTATHIONINE BETA SYNTHASE; CYSTEINE AMINOTRANSFERASE; HYDROGEN SULFIDE; OXALOACETIC ACID; RNA; SULFURTRANSFERASE; UNCLASSIFIED DRUG; 3-MERCAPTOPYRUVATE SULPHURTRANSFERASE; MITOCHONDRIAL PROTEIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME LOCALIZATION; ENZYME SUBSTRATE; IMMUNOCYTOCHEMISTRY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR DYNAMICS; NERVE CELL; NONHUMAN; PH MEASUREMENT; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPINAL GANGLION; ANIMAL; ENZYMOLOGY; METABOLISM; PC12 CELL LINE; PHYSIOLOGY; WISTAR RAT;

RATTUS;

ANIMALS; GANGLIA, SPINAL; HYDROGEN SULFIDE; MITOCHONDRIAL PROTEINS; NEURONS; PC12 CELLS; RATS; RATS, WISTAR; SULFURTRANSFERASES; TRANSAMINASES;

EID: 84903160999     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12698     Document Type: Article

References (50)

1. Abad M. F., Di Benedetto G., Magalhães P. J., Filippin L., and, Pozzan T., (2004) Mitochondrial pH monitored by a new engineered green fluorescent protein mutant. J. Biol. Chem. 279, 11521-11529. (Pubitemid 38401652)
2. Abeles R. H., and, Walsh C. T., (1973) Acetylenic enzyme inactivators. Inactivation of γ-cystathionase, in vitro and in vivo, by propargylglycine. J. Am. Chem. Soc. 95, 6124-6125.
3. Akagi R., (1982) Purification and characterization of cysteine aminotransferase from rat liver cytosol. Acta Med. Okayama 36, 187-197. (Pubitemid 12020399)
4. Andersson D. A., Gentry C., and, Bevan S., (2012) TRPA1 has a key role in the somatic pro-nociceptive actions of hydrogen sulfide. PLoS ONE 7, e46917.
5. Asimakopoulou A., Panopoulos P., Chasapis C. T., Coletta C., Zhou Z., Cirino G., Giannis A., Szabo C., Spyroulias G. A., and, 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.
6. Casey J. R., Grinstein S., and, Orlowski J., (2010) Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11, 50-61.
7. 2S by cystathionine β-synthase via the condensation of cysteine and homocysteine. J. Biol. Chem. 279, 52082-52086. (Pubitemid 39656580)
8. Enokido Y., Suzuki E., Iwasawa K., Namekata K., Okazawa H., and, Kimura H., (2005) Cystathionine β-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. FASEB J. 19, 1854-1856. (Pubitemid 41598773)
9. Flannigan K. L., Ferraz J. G., Wang R., and, Wallace J. L., (2013) Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: a site-specific, pro-resolution mechanism. PLoS ONE 8, e71962.
10. 2S) metabolism in mitochondria and its regulatory role in energy production. Proc. Natl Acad. Sci. USA 109, 2943-2948.
11. Fu M., Zhang W., Yang G., and, Wang R., (2012b) Is cystathionine gamma-lyase protein expressed in the heart? Biochem. Biophys. Res. Commun. 428, 469-474.
12. Haddad P. R., and, Heckenberg A. L., (1988) Trace determination of sulfide by reversed-phase ion-interaction chromatography using pre-column derivatization. J. Chromatogr. 447, 415-420.
13. Hanson G. T., Aggeler R., Oglesbee D., Cannon M., Capaldi R. A., Tsien R. Y., and, Remington S. J., (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13044-13053. (Pubitemid 38445882)
14. Hems D. A., and, Brosnan J. T., (1971) Effects of metabolic acidosis and starvation on the content of intermediary metabolites in rat kidney. Biochem. J. 123, 391-397.
15. Higashi T., Tateishi N., Naruse A., and, Sakamoto Y., (1976) Decrease of glutathione and induction of γ-glutamyltransferase by dibutyryl-3?, 5?-cyclic AMP in rat liver. Biochem. Biophys. Res. Commun. 68, 1280-1286.
16. Hu S., Xu W., Miao X., Gao Y., Zhu L., Zhou Y., Xiao Y., and, Xu G. Y., (2013) Sensitization of sodium channels by cystathionine β-synthetase activation in colon sensory neurons in adult rats with neonatal maternal deprivation. Exp. Neurol. 248, 275-285.
17. 2S production. J. Mol. Biol. 396, 708-718.
18. Ishii I., Akahoshi N., Yu X. N., Kobayashi Y., Namekata K., Komaki G., and, Kimura H., (2004) Murine cystathionine γ-lyase: complete cDNA and genomic sequences, promoter activity, tissue distribution and developmental expression. Biochem. J. 381, 113-123. (Pubitemid 38932217)
19. Jalil M. A., Begum L., Contreras L., et al,. (2005) Reduced N-acetylaspartate levels in mice lacking aralar, a brain- and muscle-type mitochondrial aspartate-glutamate carrier. J. Biol. Chem. 280, 31333-31339. (Pubitemid 41294508)
20. John R. A., and, Charteris A., (1978) The reaction of amino-oxyacetate with pyridoxal phosphate-dependent enzymes. Biochem. J. 171, 771-779. (Pubitemid 8348755)
21. 2S production in murine tissues. Antioxid. Redox Signal. 15, 363-372.
22. Kimura Y., Goto Y., and, Kimura H., (2010) Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid. Redox Signal. 12, 1-13.
23. 2S-derived signaling molecules in rat brain. FASEB J. 27, 2451-2457.
24. Llopis J., McCaffery J. M., Miyawaki A., Farquhar M. G., and, Tsien R. Y., (1998) Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. USA 95, 6803-6808. (Pubitemid 28278061)
25. Mathai J. C., Missner A., Kügler P., Saparov S. M., Zeidel M. L., Lee J. K., and, Pohl P., (2009) No facilitator required for membrane transport of hydrogen sulfide. Proc. Natl Acad. Sci. USA 106, 16633-16638.
26. Matsuyama S., Llopis J., Deveraux Q. L., Tsien R. Y., and, Reed J. C., (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat. Cell Biol. 2, 318-325.
27. McKenna M. C., Waagepetersen H. S., Schousboe A., and, Sonnewald U., (2006) Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: current evidence and pharmacological tools. Biochem. Pharmacol. 71, 399-407. (Pubitemid 43077074)
28. Mikami Y., Shibuya N., Kimura Y., Nagahara N., Ogasawara Y., and, Kimura H., (2011) Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem. J. 439, 479-485.
29. Miyamoto R., Otsuguro K., and, Ito S., (2011) Time- and concentration-dependent activation of TRPA1 by hydrogen sulfide in rat DRG neurons. Neurosci. Lett. 499, 137-142.
30. Mõdis K., Coletta C., Erdélyi K., Papapetropoulos A., and, Szabo C., (2013) Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J. 27, 601-611.
31. Nagahara N., Ito T., Kitamura H., and, Nishino T., (1998) Tissue and subcellular distribution of mercaptopyruvate sulfurtransferase in the rat: confocal laser fluorescence and immunoelectron microscopic studies combined with biochemical analysis. Histochem. Cell Biol. 110, 243-250. (Pubitemid 28401732)
32. Nagahara N., Nagano M., Ito T., Shimamura K., Akimoto T., and, Suzuki H., (2013) Antioxidant enzyme, 3-mercaptopyruvate sulfurtransferase-knockout mice exhibit increased anxiety-like behaviors: a model for human mercaptolactate- cysteine disulfiduria. Sci. Rep. 3, 1986.
33. 2S functions as a nociceptive messenger through transient receptor potential ankyrin 1 (TRPA1) activation. Neuroscience 218, 335-343.
34. Okubo K., Takahashi T., Sekiguchi F., Kanaoka D., Matsunami M., Ohkubo T., Yamazaki J., Fukushima N., Yoshida S., and, Kawabata A., (2011) Inhibition of T-type calcium channels and hydrogen sulfide-forming enzyme reverses paclitaxel-evoked neuropathic hyperalgesia in rats. Neuroscience 188, 148-156.
35. 2S signalling through protein sulfhydration and beyond. Nat. Rev. Mol. Cell Biol. 13, 499-507.
36. Santo-Domingo J., Giacomello M., Poburko D., Scorrano L., and, Demaurex N., (2013) OPA1 promotes pH flashes that spread between contiguous mitochondria without matrix protein exchange. EMBO J. 32, 1927-1940.
37. Shibuya N., Tanaka M., Yoshida M., Ogasawara Y., Togawa T., Ishii K., and, Kimura H., (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal. 11, 703-714.
38. Siegal L. M., (1965) A direct microdetermination for sulfide. Anal. Biochem. 11, 126-132.
39. Siess E. A., Kientsch-Engel R. I., and, Wieland O. H., (1984) Concentration of free oxaloacetate in the mitochondrial compartment of isolated liver cells. Biochem. J. 218, 171-176.
40. Stipanuk M. H., and, Beck P. W., (1982) Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem. J. 206, 267-277.
41. v3.2 T-type calcium channels targeted by endogenous hydrogen sulfide contributes to maintenance of neuropathic pain. Pain 150, 183-191.
42. Tang X. Q., Fan L. L., Li Y. J., Shen X. T., Zhuan Y. Y., He J. Q., Xu J. H., Hu B., and, Li Y. J., (2011) Inhibition of hydrogen sulfide generation contributes to 1-methy-4-phenylpyridinium ion-induced neurotoxicity. Neurotox. Res. 19, 403-411.
43. Ubuka T., Ohta J., Yao W. B., Abe T., Teraoka T., and, Kurozumi Y., (1992) L-Cysteine metabolism via 3-mercaptopyruvate pathway and sulfate formation in rat liver mitochondria. Amino Acids 2, 143-155.
44. Ubuka T., Umemura S., Yuasa S., Kinuta M., and, Watanabe K., (1978) Purification and characterization of mitochondrial cysteine aminotransferase from rat liver. Physiol. Chem. Phys. 10, 483-500.
45. Wang Y., Qu R., Hu S., Xiao Y., Jiang X., and, Xu G. Y., (2012) Upregulation of cystathionine β-synthetase expression contributes to visceral hyperalgesia induced by heterotypic intermittent stress in rats. PLoS ONE 7, e53165.
46. Whiteman M., Armstrong J. S., Chu S. H., Jia-Ling S., Wong B. S., Cheung N. S., Halliwell B., and, Moore P. K., (2004) The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J. Neurochem. 90, 765-768. (Pubitemid 38989409)
47. Whiteman M., Cheung N. S., Zhu Y. Z., Chu S. H., Siau J. L., Wong B. S., Armstrong J. S., and, Moore P. K., (2005) Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem. Biophys. Res. Commun. 326, 794-798. (Pubitemid 39655989)
48. Williamson D. H., Lopes-Vieira O., and, Walker B., (1967) Concentrations of free glucogenic amino acids in livers of rats subjected to various metabolic stresses. Biochem. J. 104, 497-502.
49. 2S production by human mercaptopyruvate sulfurtransferase. J. Biol. Chem. 288, 20002-20013.
50. Yao W. B., Zhao Y. Q., Abe T., Ohta J., and, Ubuka T., (1994) Effect of N-acetylcysteine administration on cysteine and glutathione contents in liver and kidney and in perfused liver of intact and diethyl maleate-treated rats. Amino Acids 7, 255-266. (Pubitemid 24370304)