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Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 2735347, 10 pages
http://dx.doi.org/10.1155/2016/2735347
Research Article

Hydrogen Sulfide Regulates the [Ca2+]i Level in the Primary Medullary Neurons

1Department of Physiology and Pathophysiology, Shanghai Medical College, Fudan University, Shanghai 200032, China
2Department of Neurology, Huashan Hospital, Fudan University, Shanghai 200040, China
3Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, China
4The Cardiovascular and Metabolic Research Unit, Laurentian University, Sudbury, ON, Canada P3E 2C6

Received 23 June 2016; Revised 12 September 2016; Accepted 27 September 2016

Academic Editor: Marta C. Monteiro

Copyright © 2016 Xiaoni Liu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. H. Tan, P. T.-H. Wong, and J.-S. Bian, “Hydrogen sulfide: a novel signaling molecule in the central nervous system,” Neurochemistry International, vol. 56, no. 1, pp. 3–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Wang, “Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter?” The FASEB Journal, vol. 16, no. 13, pp. 1792–1798, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Wang, “Gasotransmitters: growing pains and joys,” Trends in Biochemical Sciences, vol. 39, no. 5, pp. 227–232, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Wang, “Physiological implications of hydrogen sulfide: a whiff exploration that blossomed,” Physiological Reviews, vol. 92, no. 2, pp. 791–896, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. N. Shibuya, M. Tanaka, M. Yoshida et al., “3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain,” Antioxidants & Redox Signaling, vol. 11, no. 4, pp. 703–714, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. J. C. Savage and D. H. Gould, “Determination of sulfide in brain tissue and rumen fluid by ion-interaction reversed-phase high-performance liquid chromatography,” Journal of Chromatography B: Biomedical Sciences and Applications, vol. 526, pp. 540–545, 1990. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Wang, C. Szabo, F. Ichinose, A. Ahmed, M. Whiteman, and A. Papapetropoulos, “The role of H2S bioavailability in endothelial dysfunction,” Trends in Pharmacological Sciences, vol. 36, no. 9, pp. 568–578, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Abe and H. Kimura, “The possible role of hydrogen sulfide as an endogenous neuromodulator,” The Journal of Neuroscience, vol. 16, no. 3, pp. 1066–1071, 1996. View at Google Scholar · View at Scopus
  9. P. K. Kamat, P. Kyles, A. Kalani, and N. Tyagi, “Hydrogen sulfide ameliorates homocysteine-induced Alzheimer’s disease-like pathology, blood–brain barrier disruption, and synaptic disorder,” Molecular Neurobiology, vol. 53, no. 4, pp. 2451–2467, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. L.-F. Hu, P. T.-H. Wong, P. K. Moore, and J.-S. Bian, “Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia,” Journal of Neurochemistry, vol. 100, no. 4, pp. 1121–1128, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Stubbert, O. Prysyazhna, O. Rudyk, J. Scotcher, J. R. Burgoyne, and P. Eaton, “Protein kinase G Iα oxidation paradoxically underlies blood pressure lowering by the reductant hydrogen sulfide,” Hypertension, vol. 64, no. 6, pp. 1344–1351, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Yang, L. Wu, B. Jiang et al., “H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase,” Science, vol. 322, no. 5901, pp. 587–590, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Yan, J. Du, and C. Tang, “The possible role of hydrogen sulfide on the pathogenesis of spontaneous hypertension in rats,” Biochemical and Biophysical Research Communications, vol. 313, no. 1, pp. 22–27, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Yu, H. Xu, X. Liu et al., “Superoxide mediates depressive effects induced by hydrogen sulfide in rostral ventrolateral medulla of spontaneously hypertensive rats,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 927686, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. M. R. Al-Magableh, B. K. Kemp-Harper, and J. L. Hart, “Hydrogen sulfide treatment reduces blood pressure and oxidative stress in angiotensin II-induced hypertensive mice,” Hypertension Research, vol. 38, no. 1, pp. 13–20, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. M. J. Berridge, “Neuronal calcium signaling,” Neuron, vol. 21, no. 1, pp. 13–26, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. M. A. Lynch, “Long-term potentiation and memory,” Physiological Reviews, vol. 84, no. 1, pp. 87–136, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Rizzuto, “Intracellular Ca2+ pools in neuronal signalling,” Current Opinion in Neurobiology, vol. 11, no. 3, pp. 306–311, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. C. Yong, C. H. Choo, B. H. Tan, C.-M. Low, and J.-S. Bian, “Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells,” Neurochemistry International, vol. 56, no. 3, pp. 508–515, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Nagai, M. Tsugane, J.-I. Oka, and H. Kimura, “Hydrogen sulfide induces calcium waves in astrocytes,” The FASEB Journal, vol. 18, no. 3, pp. 557–559, 2004. View at Google Scholar · View at Scopus
  21. S. W. Lee, Y.-S. Hu, L.-F. Hu et al., “Hydrogen sulphide regulates calcium homeostasis in microglial cells,” GLIA, vol. 54, no. 2, pp. 116–124, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. A. García-Bereguiaín, A. K. Samhan-Arias, F. J. Martín-Romero, and C. Gutiérrez-Merino, “Hydrogen sulfide raises cytosolic calcium in neurons through activation of L-type Ca2+ channels,” Antioxidants & Redox Signaling, vol. 10, no. 1, pp. 31–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Subramanian, C. Hahn-Townsend, K. A. Clark, S. M. J. MohanKumar, and P. S. MohanKumar, “Chronic estrogen exposure affects gene expression in the rostral ventrolateral medulla of young and aging rats: possible role in hypertension,” Brain Research, vol. 1627, pp. 134–142, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. Y.-M. Chao, M.-D. Lai, and J. Y. H. Chan, “Redox-sensitive endoplasmic reticulum stress and autophagy at rostral ventrolateral medulla contribute to hypertension in spontaneously hypertensive rats,” Hypertension, vol. 61, no. 6, pp. 1270–1280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. P. G. Guyenet, “The sympathetic control of blood pressure,” Nature Reviews Neuroscience, vol. 7, no. 5, pp. 335–346, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Jin, S.-X. Pu, C.-L. Hou et al., “Cardiac H2S generation is reduced in ageing diabetic mice,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 758358, 14 pages, 2015. View at Publisher · View at Google Scholar
  27. G. Zhong, F. Chen, Y. Cheng, C. Tang, and J. Du, “The role of hydrogen sulfide generation in the pathogenesis of hypertension in rats induced by inhibition of nitric oxide synthase,” Journal of Hypertension, vol. 21, no. 10, pp. 1879–1885, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Zhao, J. Zhang, Y. Lu, and R. Wang, “The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener,” The EMBO Journal, vol. 20, no. 21, pp. 6008–6016, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. Q. Guo, S. Jin, X.-L. Wang et al., “Hydrogen sulfide in the rostral ventrolateral medulla inhibits sympathetic vasomotor tone through ATP-Sensitive K+ Channels,” The Journal of Pharmacology and Experimental Therapeutics, vol. 338, no. 2, pp. 458–465, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. G. S. Dawe, S. P. Han, J.-S. Bian, and P. K. Moore, “Hydrogen sulphide in the hypothalamus causes an ATP-sensitive K+ channel-dependent decrease in blood pressure in freely moving rats,” Neuroscience, vol. 152, no. 1, pp. 169–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Lu, B. Li, H. Y. Cai, D. S. Cheng, D. H. Li, and H. Li, “The cardiovascular effects of hydrogen sulfide injected within the caudal ventrolateral medulla are associated with the opening of ATP-sensitive potassium channels and activation of glutamate receptors,” Chinese Jouanal of Hypertension, pp. 463–467, 2014. View at Google Scholar
  32. W. Q. Liu, C. Chai, X. Y. Li, W. J. Yuan, W. Z. Wang, and Y. Lu, “The cardiovascular effects of central hydrogen sulfide are related to K(ATP) channels activation,” Physiological Research, vol. 60, no. 5, pp. 729–738, 2011. View at Google Scholar
  33. G. Tang, L. Wu, and R. Wang, “Interaction of hydrogen sulfide with ion channels,” Clinical and Experimental Pharmacology and Physiology, vol. 37, no. 7, pp. 753–763, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Nagasawa, T. Tarui, S. Yoshida et al., “Hydrogen sulfide evokes neurite outgrowth and expression of high-voltage-activated Ca2+ currents in NG108-15 cells: involvement of T-type Ca2+ channels,” Journal of Neurochemistry, vol. 108, no. 3, pp. 676–684, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Miyamoto, K.-I. Otsuguro, and S. Ito, “Time- and concentration-dependent activation of TRPA1 by hydrogen sulfide in rat DRG neurons,” Neuroscience Letters, vol. 499, no. 2, pp. 137–142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. D. E. Clapham, “Calcium signaling,” Cell, vol. 131, no. 6, pp. 1047–1058, 2007. View at Publisher · View at Google Scholar · View at Scopus