A Novel Mechanism of Formaldehyde Neurotoxicity: Inhibition of Hydrogen Sulfide Generation by Promoting Overproduction of Nitric Oxide

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Tang, Xiao Qing ^a   Fang, Heng Rong ^a,b   Zhou, Cheng Fang ^a   Zhuang, Yuan Yuan ^a   Zhang, Ping ^a   Gu, Hong Feng ^a   Hu, Bi ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b Hengyang Central Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTATHIONINE BETA SYNTHASE; FORMALDEHYDE; HYDROGEN SULFIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G),N(G) DIMETHYLARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; MOLECULAR PATHOLOGY; NEUROTOXICITY; NONHUMAN; PC12 CELL; PROTEIN EXPRESSION; RAT;

ANIMALS; ARGININE; BLOTTING, WESTERN; CYSTATHIONINE BETA-SYNTHASE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FORMALDEHYDE; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HYDROGEN SULFIDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PC12 CELLS; RATS;

EID: 84872859898     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054829     Document Type: Article

References (55)

1. Nilsson JA, Zheng X, Sundqvist K, Liu Y, Atzori L, et al. (1998) Toxicity of formaldehyde to human oral fibroblasts and epithelial cells: influences of culture conditions and role of thiol status. J Dent Res 77: 1896-1903.
2. Kilburn KH, (1994) Neurobehavioral impairment and seizures from formaldehyde. Arch Environ Health 49: 37-44.
3. Kilburn KH, Warshaw R, Thornton JC, (1987) Formaldehyde impairs memory, equilibrium, and dexterity in histology technicians: effects which persist for days after exposure. Arch Environ Health 42: 117-120.
4. Song MS, Baker GB, Dursun SM, Todd KG, (2010) The antidepressant phenelzine protects neurons and astrocytes against formaldehyde-induced toxicity. J Neurochem 114: 1405-1413.
5. Tang XQ, Ren YK, Chen RQ, Zhuang YY, Fang HR, et al. (2011) Formaldehyde induces neurotoxicity to PC12 cells involving inhibition of paraoxonase-1 expression and activity. Clin Exp Pharmacol Physiol 38: 208-214.
6. Luo FC, Zhou J, Lv T, Qi L, Wang SD, et al. (2012) Induction of endoplasmic reticulum stress and the modulation of thioredoxin-1 in formaldehyde-induced neurotoxicity. Neurotoxicology 33: 290-298.
7. Aslan H, Songur A, Tunc AT, Ozen OA, Bas O, et al. (2006) Effects of formaldehyde exposure on granule cell number and volume of dentate gyrus: a histopathological and stereological study. Brain Res 1122: 191-200.
8. Zararsiz I, Kus I, Akpolat N, Songur A, Ogeturk M, et al. (2006) Protective effects of omega-3 essential fatty acids against formaldehyde-induced neuronal damage in prefrontal cortex of rats. Cell Biochem Funct 24: 237-244.
9. Zararsiz I, Kus I, Ogeturk M, Akpolat N, Kose E, et al. (2007) Melatonin prevents formaldehyde-induced neurotoxicity in prefrontal cortex of rats: an immunohistochemical and biochemical study. Cell Biochem Funct 25: 413-418.
10. Lu Z, Li CM, Qiao Y, Yan Y, Yang X, (2008) Effect of inhaled formaldehyde on learning and memory of mice. Indoor Air 18: 77-83.
11. Pitten FA, Kramer A, Herrmann K, Bremer J, Koch S, (2000) Formaldehyde neurotoxicity in animal experiments. Pathol Res Pract 196: 193-198.
12. Liu Y, Ye Z, Yang H, Zhou L, Fan D, et al. (2010) 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: 1248-1254.
13. Ferrer I, Lizcano JM, Hernandez M, Unzeta M, (2002) Overexpression of semicarbazide sensitive amine oxidase in the cerebral blood vessels in patients with Alzheimer's disease and cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurosci Lett 321: 21-24.
14. Teng S, Beard K, Pourahmad J, Moridani M, Easson E, et al. (2001) The formaldehyde metabolic detoxification enzyme systems and molecular cytotoxic mechanism in isolated rat hepatocytes. Chem Biol Interact 130-132: 285-296.
15. Yu PH, (2001) Involvement of cerebrovascular semicarbazide-sensitive amine oxidase in the pathogenesis of Alzheimer's disease and vascular dementia. Med Hypotheses 57: 175-179.
16. Unzeta M, Sole M, Boada M, Hernandez M, (2007) Semicarbazide-sensitive amine oxidase (SSAO) and its possible contribution to vascular damage in Alzheimer's disease. J Neural Transm 114: 857-862.
17. Jiang ZJ, Richardson JS, Yu PH, (2008) The contribution of cerebral vascular semicarbazide-sensitive amine oxidase to cerebral amyloid angiopathy in Alzheimer's disease. Neuropathol Appl Neurobiol 34: 194-204.
18. Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA, (2005) Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat 29: 173-178.
19. Zhou DX, Qiu SD, Zhang J, Tian H, Wang HX, (2006) The protective effect of vitamin E against oxidative damage caused by formaldehyde in the testes of adult rats. Asian J Androl 8: 584-588.
20. Kovacic P, Somanathan R, (2010) Dermal toxicity and environmental contamination: electron transfer, reactive oxygen species, oxidative stress, cell signaling, and protection by antioxidants. Rev Environ Contam Toxicol 203: 119-138.
21. Maiese K, Chong ZZ, Hou J, Shang YC, (2010) Oxidative stress: Biomarkers and novel therapeutic pathways. Exp Gerontol 45: 217-234.
22. Nakao A, Sugimoto R, Billiar TR, McCurry KR, (2009) Therapeutic antioxidant medical gas. J Clin Biochem Nutr 44: 1-13.
23. Kimura Y, Kimura H, (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18: 1165-1167.
24. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, et al. (2004) The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90: 765-768.
25. Whiteman M, Cheung NS, Zhu YZ, Chu SH, Siau JL, et al. (2005) Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun 326: 794-798.
26. Yin WL, He JQ, Hu B, Jiang ZS, Tang XQ, (2009) Hydrogen sulfide inhibits MPP(+)-induced apoptosis in PC12 cells. Life Sci 85: 269-275.
27. Tang XQ, Yang CT, Chen J, Yin WL, Tian SW, et al. (2008) Effect of hydrogen sulphide on beta-amyloid-induced damage in PC12 cells. Clin Exp Pharmacol Physiol 35: 180-186.
28. Tang XQ, Shen XT, Huang YE, Ren YK, Chen RQ, et al. (2010) Hydrogen sulfide antagonizes homocysteine-induced neurotoxicity in PC12 cells. Neurosci Res 68: 241-249.
29. Hu LF, Lu M, Tiong CX, Dawe GS, Hu G, et al. (2010) Neuroprotective effects of hydrogen sulfide on Parkinson's disease rat models. Aging Cell 9: 135-146.
30. Meng JL, Mei WY, Dong YF, Wang JH, Zhao CM, et al. (2011) Heat shock protein 90 mediates cytoprotection by HS against chemical hypoxia-induced injury in PC12 cells. Clin Exp Pharmacol Physiol 38: 42-49.
31. Tang XQ, Fan LL, Li YJ, Shen XT, Zhuan YY, et al. (2011) Inhibition of hydrogen sulfide generation contributes to 1-methy-4-phenylpyridinium ion-induced neurotoxicity. Neurotox Res 19: 403-411.
32. Tang XQ, Shen XT, Huang YE, Chen RQ, Ren YK, et al. (2011) Inhibition of endogenous hydrogen sulfide generation is associated with homocysteine-induced neurotoxicity: role of ERK1/2 activation. J Mol Neurosci 45: 60-67.
33. Abe K, Kimura H, (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16: 1066-1071.
34. Hosoki R, Matsuki N, Kimura H, (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237: 527-531.
35. Enokido Y, Suzuki E, Iwasawa K, Namekata K, Okazawa H, et al. (2005) Cystathionine beta-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.
36. Songur A, Sarsilmaz M, Ozen O, Sahin S, Koken R, et al. (2008) The effects of inhaled formaldehyde on oxidant and antioxidant systems of rat cerebellum during the postnatal development process. Toxicol Mech Methods 18: 569-574.
37. Taoka S, Banerjee R, (2001) Characterization of NO binding to human cystathionine beta-synthase: possible implications of the effects of CO and NO binding to the human enzyme. J Inorg Biochem 87: 245-251.
38. Prathapasinghe GA, Siow YL, Xu Z, O K, (2008) Inhibition of cystathionine-beta-synthase activity during renal ischemia-reperfusion: role of pH and nitric oxide. Am J Physiol Renal Physiol 295: F912-922.
39. Cathcart R, Schwiers E, Ames BN, (1983) Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal Biochem 134: 111-116.
40. Grieve A, Butcher SP, Griffiths R, (1992) Synaptosomal plasma membrane transport of excitatory sulphur amino acid transmitter candidates: kinetic characterisation and analysis of carrier specificity. J Neurosci Res 32: 60-68.
41. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, et al. (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11: 703-714.
42. Ahmed S, Tsukahara S, Tin Tin Win S, Yamamoto S, Kunugita N, et al. (2007) Effects of low-level formaldehyde exposure on synaptic plasticity-related gene expression in the hippocampus of immunized mice. J Neuroimmunol 186: 104-111.
43. Wang R, (2002) Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16: 1792-1798.
44. Kamoun P, (2004) Endogenous production of hydrogen sulfide in mammals. Amino Acids 26: 243-254.
45. Lowicka E, Beltowski J, (2007) Hydrogen sulfide (H2S)- the third gas of interest for pharmacologists. Pharmacol Rep 59: 4-24.
46. Wang R, (2010) Hydrogen sulfide: the third gasotransmitter in biology and medicine. Antioxid Redox Signal 12: 1061-1064.
47. Schafer FQ, Buettner GR, (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212.
48. Tang XQ, Ren YK, Zhou CF, Yang CT, Gu HF, et al. (2012) Hydrogen sulfide prevents formaldehyde-induced neurotoxicity to PC12 cells by attenuation of mitochondrial dysfunction and pro-apoptotic potential. Neurochem Int 61: 16-24.
49. Kamoun P, Belardinelli MC, Chabli A, Lallouchi K, Chadefaux-Vekemans B, (2003) Endogenous hydrogen sulfide overproduction in Down syndrome. Am J Med Genet A 116A: 310-311.
50. Qu K, Chen CP, Halliwell B, Moore PK, Wong PT, (2006) Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke 37: 889-893.
51. Dwyer BE, Raina AK, Perry G, Smith MA, (2004) Homocysteine and Alzheimer's disease: a modifiable risk? Free Radic Biol Med 36: 1471-1475.
52. Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, et al. (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N Engl J Med 346: 476-483.
53. Morrison LD, Smith DD, Kish SJ, (1996) Brain S-adenosylmethionine levels are severely decreased in Alzheimer's disease. J Neurochem 67: 1328-1331.
54. Oh GS, Pae HO, Lee BS, Kim BN, Kim JM, et al. (2006) Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med 41: 106-119.
55. Kubo S, Kurokawa Y, Doe I, Masuko T, Sekiguchi F, et al. (2007) Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 241: 92-97.