Hydrogen sulfide prevents formaldehyde-induced neurotoxicity to PC12 cells by attenuation of mitochondrial dysfunction and pro-apoptotic potential

Neurochemistry International

Volumn 61, Issue 1, 2012, Pages 16-24

  Tang, Xiao Qing ^a   Ren, Yan Kai ^a   Zhou, Cheng Fang ^a   Yang, Chun Tao ^b   Gu, Hong Feng ^a   He, Jian Qin ^a   Chen, Rong Qian ^a   Zhuang, Yuan Yuan ^a   Fang, Heng Rong ^a   Wang, Chun Yan ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Bcl 2; Formaldehyde; Hydrogen sulfide; Mitochondria; Neuroprotection; Reactive oxygen species

Indexed keywords

CASPASE 3; CYTOCHROME C; FORMALDEHYDE; HYDROGEN SULFIDE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; DRUG ACTIVITY; ENZYME ACTIVATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CYTOCHROMES C; ENZYME ACTIVATION; FLOW CYTOMETRY; FORMALDEHYDE; HYDROGEN SULFIDE; MITOCHONDRIA; NEURONS; OXIDATIVE STRESS; PC12 CELLS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84861368697     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.04.011     Document Type: Article

References (55)

1. S. Ahmed, S. Tsukahara, S. Tin Tin Win, S. Yamamoto, N. Kunugita, K. Arashidani, and H. Fujimaki Effects of low-level formaldehyde exposure on synaptic plasticity-related gene expression in the hippocampus of immunized mice J. Neuroimmunol. 186 2007 104 111
2. M.E. Andersen, H.J. Clewell 3rd, E. Bermudez, D.E. Dodd, G.A. Willson, J.L. Campbell, and R.S. Thomas Formaldehyde: integrating dosimetry, cytotoxicity, and genomics to understand dose-dependent transitions for an endogenous compound Toxicol. Sci. 118 2010 716 731
3. H. Aslan, A. Songur, A.T. Tunc, O.A. Ozen, O. Bas, M. Yagmurca, M. Turgut, M. Sarsilmaz, and S. Kaplan Effects of formaldehyde exposure on granule cell number and volume of dentate gyrus: a histopathological and stereological study Brain Res. 1122 2006 191 200
4. R. Binetti, F.M. Costamagna, and I. Marcello Development of carcinogenicity classifications and evaluations: the case of formaldehyde Ann. Ist. Super Sanita 42 2006 132 143
5. R. Cathcart, E. Schwiers, and B.N. Ames Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay Anal. Biochem. 134 1983 111 116
6. W.G. Duan, J. Shang, Z.Z. Jiang, J.C. Yao, Y. Yun, M. Yan, B. Shu, Q. Lin, Z.P. Yu, and L.Y. Zhang Rho kinase inhibitor Y-27632 down-regulates norepinephrine synthesis and release in PC12 cells Basic Clin. Pharmacol. Toxicol. 104 2009 434 440
7. P. Franklin, P. Dingle, and S. Stick Raised exhaled nitric oxide in healthy children is associated with domestic formaldehyde levels Am. J. Respir. Crit. Care Med. 161 2000 1757 1759
8. A. Grieve, S.P. Butcher, and R. Griffiths Synaptosomal plasma membrane transport of excitatory sulphur amino acid transmitter candidates: kinetic characterisation and analysis of carrier specificity J. Neurosci. Res. 32 1992 60 68
9. A. Gurel, O. Coskun, F. Armutcu, M. Kanter, and O.A. Ozen Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies J. Chem. Neuroanat. 29 2005 173 178
10. D.M. Hockenbery, Z.N. Oltvai, X.M. Yin, C.L. Milliman, and S.J. Korsmeyer Bcl-2 functions in an antioxidant pathway to prevent apoptosis Cell 75 1993 241 251
11. L.F. Hu, M. Lu, Z.Y. Wu, P.T. Wong, and J.S. Bian Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function Mol. Pharmacol. 75 2009 27 34
12. L.F. Hu, M. Lu, C.X. Tiong, G.S. Dawe, G. Hu, and J.S. Bian Neuroprotective effects of hydrogen sulfide on Parkinson's disease rat models Aging Cell 9 2010 135 146
13. Z.J. Jiang, J.S. Richardson, and P.H. Yu The contribution of cerebral vascular semicarbazide-sensitive amine oxidase to cerebral amyloid angiopathy in Alzheimer's disease Neuropathol. Appl. Neurobiol. 34 2008 194 204
14. D.J. Kane, T.A. Sarafian, R. Anton, H. Hahn, E.B. Gralla, J.S. Valentine, T. Ord, and D.E. Bredesen Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species Science 262 1993 1274 1277
15. K.H. Kilburn Neurobehavioral impairment and seizures from formaldehyde Arch. Environ. Health 49 1994 37 44
16. K.H. Kilburn, R. Warshaw, and J.C. Thornton Formaldehyde impairs memory, equilibrium, and dexterity in histology technicians: effects which persist for days after exposure Arch. Environ. Health 42 1987 117 120
17. W.H. Kim, W.B. Park, B. Gao, and M.H. Jung Critical role of reactive oxygen species and mitochondrial membrane potential in Korean mistletoe lectin-induced apoptosis in human hepatocarcinoma cells Mol. Pharmacol. 66 2004 1383 1396
18. Y. Kimura, and H. Kimura Hydrogen sulfide protects neurons from oxidative stress FASEB J. 18 2004 1165 1167
19. R.A. Kirkland, and J.L. Franklin Bax, reactive oxygen, and cytochrome c release in neuronal apoptosis Antioxid. Redox Signaling 5 2003 589 596
20. R. Li, Y. Kong, and S. Ladisch Nerve growth factor-induced neurite formation in PC12 cells is independent of endogenous cellular gangliosides Glycobiology 8 1998 597 603
21. S.K. Lim, J.C. Kim, C.J. Moon, G.Y. Kim, H.J. Han, and S.H. Park Formaldehyde induces apoptosis through decreased Prx 2 via p38 MAPK in lung epithelial cells Toxicology 271 2010 100 106
22. Y. Liu, Z. Ye, H. Yang, L. Zhou, D. Fan, S. He, and D. Chui Disturbances of soluble N-ethylmaleimide-sensitive factor attachment proteins in hippocampal synaptosomes contribute to cognitive impairment after repetitive formaldehyde inhalation in male rats Neuroscience 169 2010 1248 1254
23. 2S) - the third gas of interest for pharmacologists Pharmacol. Rep. 59 2007 4 24
24. M. Lu, L.F. Hu, G. Hu, and J.S. Bian Hydrogen sulfide protects astrocytes against H(2)O(2)-induced neural injury via enhancing glutamate uptake Free Radic. Biol. Med. 45 2008 1705 1713
25. Z. Lu, C.M. Li, Y. Qiao, Y. Yan, and X. Yang Effect of inhaled formaldehyde on learning and memory of mice Indoor Air 18 2008 77 83
26. W. Luo, H. Li, Y. Zhang, and C.Y. Ang Determination of formaldehyde in blood plasma by high-performance liquid chromatography with fluorescence detection J. Chromatogr. B Biomed. Sci. Appl. 753 2001 253 257
27. G.A. Lyles Mammalian plasma and tissue-bound semicarbazide-sensitive amine oxidases: biochemical, pharmacological and toxicological aspects Int. J. Biochem. Cell Biol. 28 1996 259 274
28. M.P. Mattson, Y. Zhang, and S. Bose Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose Exp. Neurol. 121 1993 1 13
29. J.L. Meng, W.Y. Mei, Y.F. Dong, J.H. Wang, C.M. Zhao, A.P. Lan, C.T. Yang, P.X. Chen, J.Q. Feng, and C.H. Hu Heat shock protein 90 mediates cytoprotection by HS against chemical hypoxia-induced injury in PC12 cells Clin. Exp. Pharmacol. Physiol. 38 2011 42 49
30. P.K. Moore, M. Bhatia, and S. Moochhala Hydrogen sulfide: from the smell of the past to the mediator of the future? Trends Pharmacol. Sci. 24 2003 609 611
31. A. Nakao, R. Sugimoto, T.R. Billiar, and K.R. McCurry Therapeutic antioxidant medical gas J. Clin. Biochem. Nutr. 44 2009 1 13
32. J.A. Nilsson, X. Zheng, K. Sundqvist, Y. Liu, L. Atzori, A. Elfwing, K. Arvidson, and R.C. Grafstrom Toxicity of formaldehyde to human oral fibroblasts and epithelial cells: influences of culture conditions and role of thiol status J. Dent. Res. 77 1998 1896 1903
33. S. Orrenius Reactive oxygen species in mitochondria-mediated cell death Drug Metab. Rev. 39 2007 443 455
34. V. Petronilli, D. Penzo, L. Scorrano, P. Bernardi, and F. Di Lisa The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ J. Biol. Chem. 276 2001 12030 12034
35. F.A. Pitten, A. Kramer, K. Herrmann, J. Bremer, and S. Koch Formaldehyde neurotoxicity in animal experiments Pathol. Res. Pract. 196 2000 193 198
36. M.S. Song, G.B. Baker, S.M. Dursun, and K.G. Todd The antidepressant phenelzine protects neurons and astrocytes against formaldehyde-induced toxicity J. Neurochem. 114 2010 1405 1413
37. A. Songur, O.A. Ozen, and M. Sarsilmaz The toxic effects of formaldehyde on the nervous system Rev. Environ. Contam. Toxicol. 203 2010 105 118
38. X.Q. Tang, C.T. Yang, J. Chen, W.L. Yin, S.W. Tian, B. Hu, J.Q. Feng, and Y.J. Li Effect of hydrogen sulphide on beta-amyloid-induced damage in PC12 cells Clin. Exp. Pharmacol. Physiol. 35 2008 180 186
39. X.Q. Tang, X.T. Shen, Y.E. Huang, Y.K. Ren, R.Q. Chen, B. Hu, J.Q. He, W.L. Yin, J.H. Xu, and Z.S. Jiang Hydrogen sulfide antagonizes homocysteine-induced neurotoxicity in PC12 cells Neurosci. Res. 68 2010 241 249
40. X.Q. Tang, Y.K. Ren, R.Q. Chen, Y.Y. Zhuang, H.R. Fang, J.H. Xu, C.Y. Wang, and B. Hu Formaldehyde induces neurotoxicity to PC12 cells involving inhibition of paraoxonase-1 expression and activity Clin. Exp. Pharmacol. Physiol. 38 2011 208 214
41. J.D. Thrasher, and K.H. Kilburn Embryo toxicity and teratogenicity of formaldehyde Arch. Environ. Health 56 2001 300 311
42. M. Unzeta, M. Sole, M. Boada, and M. Hernandez Semicarbazide-sensitive amine oxidase (SSAO) and its possible contribution to vascular damage in Alzheimer's disease J. Neural Transm. 114 2007 857 862
43. 2S be the third endogenous gaseous transmitter? FASEB J. 16 2002 1792 1798
44. R. Wang Hydrogen sulfide: the third gasotransmitter in biology and medicine Antioxid. Redox Signaling 12 2010 1061 1064
45. S. Wang, C.P. Hu, D.J. Jiang, J. Peng, Z. Zhou, Q. Yuan, S.D. Nie, J.L. Jiang, Y.J. Li, and K.L. Huang All-trans retinoic acid inhibits cobalt chloride-induced apoptosis in PC12 cells: role of the dimethylarginine dimethylaminohydrolase/asymmetric dimethylarginine pathway J. Neurosci. Res. 87 2009 1938 1946
46. M. Whiteman, J.S. Armstrong, S.H. Chu, S. Jia-Ling, B.S. Wong, N.S. Cheung, B. Halliwell, and P.K. Moore The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J. Neurochem. 90 2004 765 768
47. M. Whiteman, N.S. Cheung, Y.Z. Zhu, S.H. Chu, J.L. Siau, B.S. Wong, J.S. Armstrong, and P.K. Moore Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem. Biophys. Res. Commun. 326 2005 794 798
48. L.Y. Wu, A.S. Ding, T. Zhao, Z.M. Ma, F.Z. Wang, and M. Fan Involvement of increased stability of mitochondrial membrane potential and overexpression of Bcl-2 in enhanced anoxic tolerance induced by hypoxic preconditioning in cultured hypothalamic neurons Brain Res. 999 2004 149 154
49. J. Yang, X. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J. Cai, T.I. Peng, D.P. Jones, and X. Wang Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked Science 275 1997 1129 1132
50. W.L. Yin, J.Q. He, B. Hu, Z.S. Jiang, and X.Q. Tang Hydrogen sulfide inhibits MPP(+)-induced apoptosis in PC12 cells Life Sci. 85 2009 269 275
51. P.H. Yu Involvement of cerebrovascular semicarbazide-sensitive amine oxidase in the pathogenesis of Alzheimer's disease and vascular dementia Med. Hypotheses 57 2001 175 179
52. P.H. Yu, C. Cauglin, K.L. Wempe, and D. Gubisne-Haberle A novel sensitive high-performance liquid chromatography/electrochemical procedure for measuring formaldehyde produced from oxidative deamination of methylamine and in biological samples Anal. Biochem. 318 2003 285 290
53. I. Zararsiz, I. Kus, N. Akpolat, A. Songur, M. Ogeturk, and M. Sarsilmaz Protective effects of omega-3 essential fatty acids against formaldehyde-induced neuronal damage in prefrontal cortex of rats Cell. Biochem. Funct. 24 2006 237 244
54. I. Zararsiz, I. Kus, M. Ogeturk, N. Akpolat, E. Kose, S. Meydan, and M. Sarsilmaz Melatonin prevents formaldehyde-induced neurotoxicity in prefrontal cortex of rats: an immunohistochemical and biochemical study Cell. Biochem. Funct. 25 2007 413 418
55. D.X. Zhou, S.D. Qiu, J. Zhang, H. Tian, and H.X. Wang The protective effect of vitamin E against oxidative damage caused by formaldehyde in the testes of adult rats Asian J. Androl. 8 2006 584 588