Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Advertisement

Springer Nature Link
Log in

A New Hope for a Devastating Disease: Hydrogen Sulfide in Parkinson’s Disease

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Hydrogen sulfide (H2S) has been regarded as the third gaseous transmitter alongside nitric oxide (NO) and carbon monoxide (CO). In mammalian brain, H2S is produced redundantly by four enzymatic pathways, implying its abundance in the organ. In physiological conditions, H2S has been found to induce the formation of long-term potential in neuronal cells by augmenting the activity of N-methyl-D-aspartate (NMDA) receptor. Likewise, it also actively takes part in the regulation of intracellular Ca2+ and pH homeostasis in both neuronal cells and glia cells. Intriguingly, emerging evidence indicates a connection of H2S with Parkinson’s disease. Specifically, the endogenous H2S level in the substantia nigra (SN) is significantly reduced along with 6-hydroxydopamine (6-OHDA) treatment in rats, while supplementation of H2S not only reverses 6-OHDA-induced neuronal loss but also attenuates the following disorders of movement, suggesting a protective effect of H2S in Parkinson’s disease (PD). Remarkably, the protective effect has been extensively demonstrated with various in vitro and in vivo PD models. These suggest that H2S may be a new hope for the treatment of PD. Further studies have shown that the protective effects can be ascribed to H2S-mediated anti-oxidation, anti-inflammation, anti-apoptosis, and pro-survival activity, which are also summarized in the review. Moreover, the progresses on the development of H2S donors are also conveyed with an emphasis on the treatment of PD. Nevertheless, one should bear in mind that the precise role of H2S in the pathogenesis of PD remains largely elusive. Therefore, more studies are warranted before turning the hope into a real therapy for PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Smith RP, Gosselin RE (1979) Hydrogen sulfide poisoning. Journal of occupational medicine : official publication of the Industrial Medical Association 21(2):93–97

    Article  CAS  Google Scholar 

  2. Reiffenstein RJ, Hulbert WC, Roth SH (1992) Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 32:109–134. doi:10.1146/annurev.pa.32.040192.000545

    Article  CAS  PubMed  Google Scholar 

  3. Nicholson RA, Roth SH, Zhang A, Zheng J, Brookes J, Skrajny B, Bennington R (1998) Inhibition of respiratory and bioenergetic mechanisms by hydrogen sulfide in mammalian brain. Journal of toxicology and environmental health Part A 54(6):491–507

    Article  CAS  PubMed  Google Scholar 

  4. Warenycia MW, Smith KA, Blashko CS, Kombian SB, Reiffenstein RJ (1989) Monoamine oxidase inhibition as a sequel of hydrogen sulfide intoxication: increases in brain catecholamine and 5-hydroxytryptamine levels. Arch Toxicol 63(2):131–136

    Article  CAS  PubMed  Google Scholar 

  5. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. The Journal of neuroscience : the official journal of the Society for Neuroscience 16(3):1066–1071

    Article  CAS  Google Scholar 

  6. Zhang X, Bian JS (2014) Hydrogen sulfide: a neuromodulator and neuroprotectant in the central nervous system. ACS Chem Neurosci 5(10):876–883. doi:10.1021/cn500185g

    Article  CAS  PubMed  Google Scholar 

  7. Liu YH, Lu M, Hu LF, Wong PT, Webb GD, Bian JS (2012) Hydrogen sulfide in the mammalian cardiovascular system. Antioxid Redox Signal 17(1):141–185. doi:10.1089/ars.2011.4005

    Article  CAS  PubMed  Google Scholar 

  8. Cao X, Bian J (2016) The role of hydrogen sulfide in renal system. Front Pharmacol 7:385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhu X-Y, Gu H, Ni X (2011) Hydrogen sulfide in the endocrine and reproductive systems. Expert Rev Clin Pharmacol 4(1):75–82

    Article  CAS  PubMed  Google Scholar 

  10. Wu CHK (2013) The role of hydrogen sulphide in lung diseases. Bioscience Horizons 6:hzt009

    Google Scholar 

  11. Magierowski M, Jasnos K, Kwiecień S, Brzozowski T (2012) Role of hydrogen sulfide in the physiology of gastrointestinal tract and in the mechanism of gastroprotection. Postepy higieny i medycyny doswiadczalnej (Online) 67:150–156

    Article  Google Scholar 

  12. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285(29):21903–21907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Li L, Hsu A, Moore PK (2009) Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation—a tale of three gases! Pharmacol Ther 123(3):386–400. doi:10.1016/j.pharmthera.2009.05.005

    Article  CAS  PubMed  Google Scholar 

  15. Mathai JC, Missner A, Kugler P, Saparov SM, Zeidel ML, Lee JK, Pohl P (2009) No facilitator required for membrane transport of hydrogen sulfide. Proc Natl Acad Sci U S A 106(39):16633–16638. doi:10.1073/pnas.0902952106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Filipovic MR, Miljkovic J, Allgäuer A, Chaurio R, Shubina T, Herrmann M, Ivanovic-Burmazovic I (2012) Biochemical insight into physiological effects of H2S: reaction with peroxynitrite and formation of a new nitric oxide donor, sulfinyl nitrite. Biochem J 441(2):609–621

    Article  CAS  PubMed  Google Scholar 

  17. Filipovic MR, Miljkovic JL, Nauser T, Royzen M, Klos K, Shubina T, Koppenol WH, Lippard SJ et al (2012) Chemical characterization of the smallest S-nitrosothiol, HSNO; cellular cross-talk of H2S and S-nitrosothiols. J Am Chem Soc 134(29):12016–12027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wedmann R, Bertlein S, Macinkovic I, Böltz S, Miljkovic JL, Muñoz LE, Herrmann M, Filipovic MR (2014) Working with “H 2 S”: facts and apparent artifacts. Nitric oxide : biology and chemistry / official journal of the Nitric Oxide Society 41:85–96

    Article  CAS  Google Scholar 

  19. Kolluru GK, Shen X, Bir SC, Kevil CG (2013) Hydrogen sulfide chemical biology: pathophysiological roles and detection. Nitric oxide : biology and chemistry / official journal of the Nitric Oxide Society 35:5–20. doi:10.1016/j.niox.2013.07.002

    Article  CAS  Google Scholar 

  20. Xie L, Gu Y, Wen M, Zhao S, Wang W, Ma Y, Meng G, Han Y et al (2016) Hydrogen sulfide induces Keap1 S-sulfhydration and suppresses diabetes-accelerated atherosclerosis via Nrf2 activation. Diabetes 65(10):3171–3184. doi:10.2337/db16-0020

    Article  CAS  PubMed  Google Scholar 

  21. Zhou H, Ding L, Wu Z, Cao X, Zhang Q, Lin L, Bian JS (2017) Hydrogen sulfide reduces RAGE toxicity through inhibition of its dimer formation. Free Radic Biol Med 104:262–271. doi:10.1016/j.freeradbiomed.2017.01.026

    Article  CAS  PubMed  Google Scholar 

  22. Li Q, Lancaster JR (2013) Chemical foundations of hydrogen sulfide biology. Nitric oxide : biology and chemistry / official journal of the Nitric Oxide Society 35:21–34

    Article  Google Scholar 

  23. Kimura Y, Toyofuku Y, Koike S, Shibuya N, Nagahara N, Lefer D, Ogasawara Y, Kimura H (2015) Identification of H2S3 and H2S produced by 3-mercaptopyruvate sulfurtransferase in the brain. Scientific reports 5:14774. doi:10.1038/srep14774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kimura H (2014) The physiological role of hydrogen sulfide and beyond. Nitric oxide : biology and chemistry / official journal of the Nitric Oxide Society 41:4–10. doi:10.1016/j.niox.2014.01.002

    Article  CAS  Google Scholar 

  25. Fu M, Zhang W, Wu L, Yang G, Li H, Wang R (2012) Hydrogen sulfide (H2S) metabolism in mitochondria and its regulatory role in energy production. Proc Natl Acad Sci U S A 109(8):2943–2948. doi:10.1073/pnas.1115634109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Teng H, Wu B, Zhao K, Yang G, Wu L, Wang R (2013) Oxygen-sensitive mitochondrial accumulation of cystathionine β-synthase mediated by Lon protease. Proc Natl Acad Sci 110(31):12679–12684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Qian Y, Zhang L, Ding S, Deng X, He C, Zheng XE, Zhu H-L, Zhao J (2012) A fluorescent probe for rapid detection of hydrogen sulfide in blood plasma and brain tissues in mice. Chem Sci 3(10):2920–2923

    Article  CAS  Google Scholar 

  28. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16(3):1066–1071

    Article  CAS  PubMed  Google Scholar 

  29. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11(4):703–714

    Article  CAS  PubMed  Google Scholar 

  30. Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 267(1):129–133

    Article  CAS  PubMed  Google Scholar 

  31. Aizenman E, Lipton SA, Loring RH (1989) Selective modulation of NMDA responses by reduction and oxidation. Neuron 2(3):1257–1263

    Article  CAS  PubMed  Google Scholar 

  32. Kimura H (2013) Physiological role of hydrogen sulfide and polysulfide in the central nervous system. Neurochem Int 63(5):492–497

    Article  CAS  PubMed  Google Scholar 

  33. Nagai Y, Tsugane M, Oka J-I, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18(3):557–559

    Article  CAS  PubMed  Google Scholar 

  34. Lee SW, Hu YS, Hu LF, Lu Q, Dawe GS, Moore PK, Wong PTH, Bian JS (2006) Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 54(2):116–124

    Article  PubMed  Google Scholar 

  35. Yong QC, Choo CH, Tan BH, Low C-M, Bian J-S (2010) Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells. Neurochem Int 56(3):508–515

    Article  CAS  PubMed  Google Scholar 

  36. Lu M, Choo CH, Hu L-F, Tan BH, Hu G, Bian J-S (2010) Hydrogen sulfide regulates intracellular pH in rat primary cultured glia cells. Neurosci Res 66(1):92–98

    Article  CAS  PubMed  Google Scholar 

  37. Shrode LD, Tapper H, Grinstein S (1997) Role of intracellular pH in proliferation, transformation, and apoptosis. J Bioenerg Biomembr 29(4):393–399

    Article  CAS  PubMed  Google Scholar 

  38. Kida M, Fujiwara H, Ishida M, Kawai C, Ohura M, Miura I, Yabuuchi Y (1991) Ischemic preconditioning preserves creatine phosphate and intracellular pH. Circulation 84(6):2495–2503

    Article  CAS  PubMed  Google Scholar 

  39. Eto K, Asada T, Arima K, Makifuchi T, Kimura H (2002) Brain hydrogen sulfide is severely decreased in Alzheimer’s disease. Biochem Biophys Res Commun 293(5):1485–1488

    Article  CAS  PubMed  Google Scholar 

  40. Paul BD, Sbodio JI, Xu R, Vandiver MS, Cha JY, Snowman AM, Snyder SH (2014) Cystathionine [ggr]-lyase deficiency mediates neurodegeneration in Huntington/’s disease. Nature 509(7498):96–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hu LF, Lu M, Tiong CX, Dawe GS, Hu G, Bian JS (2010) Neuroprotective effects of hydrogen sulfide on Parkinson’s disease rat models. Aging Cell 9(2):135–146

    Article  CAS  PubMed  Google Scholar 

  42. Vandiver MS, Paul BD, Xu R, Karuppagounder S, Rao F, Snowman AM, Ko HS, Lee YI et al (2013) Sulfhydration mediates neuroprotective actions of parkin. Nat Commun 4:1626

    Article  PubMed  PubMed Central  Google Scholar 

  43. Du H-P, Li J, You S-J, Wang Y-L, Wang F, Cao Y-J, Hu L-F, Liu C-F (2016) DNA methylation in cystathionine-γ-lyase (CSE) gene promoter induced by ox-LDL in macrophages and in apoE knockout mice. Biochem Biophys Res Commun 469(3):776–782

    Article  CAS  PubMed  Google Scholar 

  44. Kida K, Yamada M, Tokuda K, Marutani E, Kakinohana M, Kaneki M, Ichinose F (2011) Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson’s disease. Antioxid Redox Signal 15(2):343–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lu M, Zhao F-F, Tang J-J, Su C-J, Fan Y, Ding J-H, Bian J-S, Hu G (2012) The neuroprotection of hydrogen sulfide against MPTP-induced dopaminergic neuron degeneration involves uncoupling protein 2 rather than ATP-sensitive potassium channels. Antioxid Redox Signal 17(6):849–859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Xie L, Hu L-F, Teo XQ, Tiong CX, Tazzari V, Sparatore A, Del Soldato P, Dawe GS et al (2013) Therapeutic effect of hydrogen sulfide-releasing L-Dopa derivative ACS84 on 6-OHDA-induced Parkinson’s disease rat model. PLoS One 8(4):e60200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Yin W-L, He J-Q, Hu B, Jiang Z-S, Tang X-Q (2009) Hydrogen sulfide inhibits MPP+-induced apoptosis in PC12 cells. Life Sci 85(7):269–275

    Article  CAS  PubMed  Google Scholar 

  48. Tiong CX, Lu M, Bian JS (2010) Protective effect of hydrogen sulphide against 6-OHDA-induced cell injury in SH-SY5Y cells involves PKC/PI3K/Akt pathway. Br J Pharmacol 161(2):467–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Xie L, Tiong CX, Bian J-S (2012) Hydrogen sulfide protects SH-SY5Y cells against 6-hydroxydopamine-induced endoplasmic reticulum stress. Am J Phys Cell Phys 303(1):C81–C91

    Article  CAS  Google Scholar 

  50. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443(7113):787–795

    Article  CAS  PubMed  Google Scholar 

  51. Jenner P (2003) Oxidative stress in Parkinson’s disease. Ann Neurol 53(S3):S26–S38

    Article  CAS  PubMed  Google Scholar 

  52. Xie Z-Z, Shi M-M, Xie L, Wu Z-Y, Li G, Hua F, Bian J-S (2014) Sulfhydration of p66Shc at cysteine59 mediates the antioxidant effect of hydrogen sulfide. Antioxid Redox Signal 21(18):2531–2542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Clancy R, Leszczynska-Piziak J, Abramson S (1992) Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Investig 90(3):1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L et al (2013) Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18(15):1906–1919

    Article  CAS  PubMed  Google Scholar 

  55. Whiteman M, Li L, Rose P, Tan C-H, Parkinson DB, Moore PK (2010) The effect of hydrogen sulfide donors on lipopolysaccharide-induced formation of inflammatory mediators in macrophages. Antioxid Redox Signal 12(10):1147–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Gong Q-H, Wang Q, Pan L-L, Liu X-H, Xin H, Zhu Y-Z (2011) S-propargyl-cysteine, a novel hydrogen sulfide-modulated agent, attenuates lipopolysaccharide-induced spatial learning and memory impairment: involvement of TNF signaling and NF-κB pathway in rats. Brain Behav Immun 25(1):110–119

    Article  CAS  PubMed  Google Scholar 

  57. Mok Y-YP, Moore P (2008) Hydrogen sulphide is pro-inflammatory in haemorrhagic shock. Inflamm Res 57(11):512–518

    Article  CAS  PubMed  Google Scholar 

  58. Bhatia M (2005) Inflammatory response on the pancreatic acinar cell injury. Scand J Surg 94(2):97–102

    Article  CAS  PubMed  Google Scholar 

  59. Hu LF, Wong PTH, Moore PK, Bian JS (2007) Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem 100(4):1121–1128

    Article  CAS  PubMed  Google Scholar 

  60. Lee M, Sparatore A, Del Soldato P, Mcgeer E, McGeer PL (2010) Hydrogen sulfide-releasing NSAIDs attenuate neuroinflammation induced by microglial and astrocytic activation. Glia 58(1):103–113

    Article  PubMed  Google Scholar 

  61. Abeliovich A (2007) Parkinson’s disease: pro-survival effects of PINK1. Nature 448(7155):759–760

    Article  CAS  PubMed  Google Scholar 

  62. Suzuki K, Olah G, Modis K, Coletta C, Kulp G, Gerö D, Szoleczky P, Chang T et al (2011) Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci 108(33):13829–13834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Mustafa AK, Sikka G, Gazi SK, Steppan J, Jung SM, Bhunia AK, Barodka VM, Gazi FK et al (2011) Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 109(11):1259–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN et al (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288(5467):870–874

    Article  CAS  PubMed  Google Scholar 

  65. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281(5381):1309

    Article  CAS  PubMed  Google Scholar 

  66. Ulusoy A, Kirik D (2008) Can overexpression of parkin provide a novel strategy for neuroprotection in Parkinson’s disease? Exp Neurol 212(2):258–260

    Article  CAS  PubMed  Google Scholar 

  67. Baskar R, Bian J (2011) Hydrogen sulfide gas has cell growth regulatory role. Eur J Pharmacol 656(1–3):5–9. doi:10.1016/j.ejphar.2011.01.052

    Article  CAS  PubMed  Google Scholar 

  68. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R et al (2008) Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117(18):2351–2360. doi:10.1161/CIRCULATIONAHA.107.753467

    Article  CAS  PubMed  Google Scholar 

  69. Lin S, Visram F, Liu W, Haig A, Jiang J, Mok A, Lian D, Wood ME et al (2016) GYY4137, a slow-releasing hydrogen sulfide donor, ameliorates renal damage associated with chronic obstructive uropathy. J Urol 196(6):1778–1787. doi:10.1016/j.juro.2016.05.029

    Article  CAS  PubMed  Google Scholar 

  70. Karwi QG, Whiteman M, Wood ME, Torregrossa R, Baxter GF (2016) Pharmacological postconditioning against myocardial infarction with a slow-releasing hydrogen sulfide donor, GYY4137. Pharmacol Res 111:442–451. doi:10.1016/j.phrs.2016.06.028

    Article  CAS  PubMed  Google Scholar 

  71. Juman S, Nara Y, Yasui N, Negishi H, Okuda H, Takado N, Miki T (2016) Reduced production of hydrogen sulfide and sulfane sulfur due to low cystathionine beta-synthase levels in brain astrocytes of stroke-prone spontaneously hypertensive rats. Biol Pharm Bull 39(12):1932–1938. doi:10.1248/bpb.b16-00334

    Article  CAS  PubMed  Google Scholar 

  72. Lee ZW, Teo XY, Tay EY, Tan CH, Hagen T, Moore PK, Deng LW (2014) Utilizing hydrogen sulfide as a novel anti-cancer agent by targeting cancer glycolysis and pH imbalance. Br J Pharmacol 171(18):4322–4336. doi:10.1111/bph.12773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Lee ZW, Zhou J, Chen CS, Zhao Y, Tan CH, Li L, Moore PK, Deng LW (2011) The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLoS One 6(6):e21077. doi:10.1371/journal.pone.0021077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Feng W, Teo XY, Novera W, Ramanujulu PM, Liang D, Huang D, Moore PK, Deng LW et al (2015) Discovery of new H2S releasing phosphordithioates and 2,3-dihydro-2-phenyl-2-sulfanylenebenzo[d][1,3,2]oxazaphospholes with improved antiproliferative activity. J Med Chem 58(16):6456–6480. doi:10.1021/acs.jmedchem.5b00848

    Article  CAS  PubMed  Google Scholar 

  75. Yagdi E, Cerella C, Dicato M, Diederich M (2016) Garlic-derived natural polysulfanes as hydrogen sulfide donors: friend or foe? Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association. doi:10.1016/j.fct.2016.07.016

  76. Tao M, Gao L, Pan J, Wang X (2014) Study on the inhibitory effect of allicin on human gastric cancer cell line SGC-7901 and its mechanism. African journal of traditional, complementary, and alternative medicines : AJTCAM / African Networks on Ethnomedicines 11(1):176–179

    CAS  Google Scholar 

  77. Bat-Chen W, Golan T, Peri I, Ludmer Z, Schwartz B (2010) Allicin purified from fresh garlic cloves induces apoptosis in colon cancer cells via Nrf2. Nutr Cancer 62(7):947–957. doi:10.1080/01635581.2010.509837

    Article  CAS  PubMed  Google Scholar 

  78. Padilla-Camberos E, Zaitseva G, Padilla C, Puebla AM (2010) Antitumoral activity of allicin in murine lymphoma L5178Y. Asian Pacific journal of cancer prevention : APJCP 11(5):1241–1244

    PubMed  Google Scholar 

  79. Munday R, Munday JS, Munday CM (2003) Comparative effects of mono-, di-, tri-, and tetrasulfides derived from plants of the Allium family: redox cycling in vitro and hemolytic activity and phase 2 enzyme induction in vivo. Free Radic Biol Med 34(9):1200–1211

    Article  CAS  PubMed  Google Scholar 

  80. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, Darley-Usmar VM, Doeller JE et al (2007) Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A 104(46):17977–17982. doi:10.1073/pnas.0705710104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Mostafa DK, El Azhary NM, Nasra RA (2016) The hydrogen sulfide releasing compounds ATB-346 and diallyl trisulfide attenuate streptozotocin-induced cognitive impairment, neuroinflammation, and oxidative stress in rats: involvement of asymmetric dimethylarginine. Can J Physiol Pharmacol 94(7):699–708. doi:10.1139/cjpp-2015-0316

    Article  CAS  PubMed  Google Scholar 

  82. Rao PS, Midde NM, Miller DD, Chauhan S, Kumar A, Kumar S (2015) Diallyl sulfide: potential use in novel therapeutic interventions in alcohol, drugs, and disease mediated cellular toxicity by targeting cytochrome P450 2E1. Curr Drug Metab 16(6):486–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Liu H, Mao P, Wang J, Wang T, Xie CH (2015) Allicin protects PC12 cells against 6-OHDA-induced oxidative stress and mitochondrial dysfunction via regulating mitochondrial dynamics. Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 36(3):966–979. doi:10.1159/000430271

    Article  CAS  Google Scholar 

  84. Mathew B, Biju R (2008) Neuroprotective effects of garlic a review. The Libyan journal of medicine 3(1):23–33. doi:10.4176/071110

    PubMed  PubMed Central  Google Scholar 

  85. Wang Q, Liu H-R, Mu Q, Rose P, Zhu YZ (2009) S-propargyl-cysteine protects both adult rat hearts and neonatal cardiomyocytes from ischemia/hypoxia injury: the contribution of the hydrogen sulfide-mediated pathway. J Cardiovasc Pharmacol 54(2):139–146

    Article  CAS  PubMed  Google Scholar 

  86. Ma K, Liu Y, Zhu Q, Liu CH, Duan JL, Tan BK, Zhu YZ (2011) H2S donor, S-propargyl-cysteine, increases CSE in SGC-7901 and cancer-induced mice: evidence for a novel anti-cancer effect of endogenous H2S? PLoS One 6(6):e20525. doi:10.1371/journal.pone.0020525

    Article  PubMed  PubMed Central  Google Scholar 

  87. Wang M, Tang W, Xin H, Zhu YZ (2016) S-propargyl-cysteine, a novel hydrogen sulfide donor, inhibits inflammatory hepcidin and relieves anemia of inflammation by inhibiting IL-6/STAT3 pathway. PLoS One 11(9):e0163289. doi:10.1371/journal.pone.0163289

    Article  PubMed  PubMed Central  Google Scholar 

  88. Wen YD, Zhu YZ (2015) The pharmacological effects of S-propargyl-cysteine, a novel endogenous H2S-producing compound. Handb Exp Pharmacol 230:325–336. doi:10.1007/978-3-319-18144-8_16

    Article  CAS  PubMed  Google Scholar 

  89. Kashfi K, Olson KR (2013) Biology and therapeutic potential of hydrogen sulfide and hydrogen sulfide-releasing chimeras. Biochem Pharmacol 85(5):689–703. doi:10.1016/j.bcp.2012.10.019

    Article  CAS  PubMed  Google Scholar 

  90. Kashfi K (2014) Anti-cancer activity of new designer hydrogen sulfide-donating hybrids. Antioxid Redox Signal 20(5):831–846. doi:10.1089/ars.2013.5308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Rees K, Stowe R, Patel S, Ives N, Breen K, Clarke CE, Ben-Shlomo Y (2011) Non-steroidal anti-inflammatory drugs as disease-modifying agents for Parkinson’s disease: evidence from observational studies. The Cochrane database of systematic reviews 11:CD008454. doi:10.1002/14651858.CD008454.pub2

    Google Scholar 

  92. Guidotti TL (2010) Hydrogen sulfide: advances in understanding human toxicity. Int J Toxicol 29(6):569–581. doi:10.1177/1091581810384882

    Article  CAS  PubMed  Google Scholar 

  93. Hirose Y (2010) Clinical aspects of hydrogen sulfide poisoning. Chudoku kenkyu : Chudoku Kenkyukai jun kikanshi = The Japanese journal of toxicology 23(3):212–216

    Google Scholar 

  94. Shibuya N, Koike S, Tanaka M, Ishigami-Yuasa M, Kimura Y, Ogasawara Y, Fukui K, Nagahara N et al (2013) A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat Commun 4:1366

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore

    Xu Cao, Lei Cao, Lei Ding & Jin-song Bian

  2. Life Science Institute, National University of Singapore, Singapore, Singapore

    Jin-song Bian

Authors
  1. Xu Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lei Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jin-song Bian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jin-song Bian.

Ethics declarations

Funding

This work was supported by grants from NMRC/CIRG/1432/2015 and NUHSRO/2011/012/STB/B2B-08.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, X., Cao, L., Ding, L. et al. A New Hope for a Devastating Disease: Hydrogen Sulfide in Parkinson’s Disease. Mol Neurobiol 55, 3789–3799 (2018). https://doi.org/10.1007/s12035-017-0617-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-017-0617-0

Keywords

Search

Navigation