BDNF-TrkB pathway mediates neuroprotection of hydrogen sulfide against formaldehyde-induced toxicity to PC12 cells

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Jiang, Jia Mei ^a   Zhou, Cheng Fang ^a   Gao, Sheng Lan ^a   Tian, Ying ^a   Wang, Chun Yan ^a   Wang, Li ^a   Gu, Hong Feng ^a   Tang, Xiao Qing ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CASPASE 3; FORMALDEHYDE; HYDROGEN SULFIDE; K 252A; MALONALDEHYDE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; CARBAZOLE DERIVATIVE; INDOLE ALKALOID; NEUROPROTECTIVE AGENT; PROTEIN KINASE INHIBITOR; STAUROSPORINE AGLYCONE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVATION; INHIBITION KINETICS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PC12 CELL LINE; PROTEIN EXPRESSION; RAT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; SIGNAL TRANSDUCTION;

RATTUS;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CARBAZOLES; FORMALDEHYDE; GENE EXPRESSION REGULATION; HYDROGEN SULFIDE; INDOLE ALKALOIDS; NEUROPROTECTIVE AGENTS; PC12 CELLS; PROTEIN KINASE INHIBITORS; RATS; RECEPTOR, TRKB; SIGNAL TRANSDUCTION;

EID: 84924161942     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119478     Document Type: Article

References (73)

1. Flyvholm MA, Andersen P. Identification of formaldehyde releasers and occurrence of formaldehyde and formaldehyde releasers in registered chemical products. Am J Ind Med. 1993; 24:533-552. PMID: 8266930
2. Messiha FS, Price J. Properties and regional distribution of ocular aldehyde dehydrogenase in the rat. Neurobehav Toxicol Teratol. 1983; 5:251-254. PMID: 6346129
3. Flo-Neyret C, Lorenzi-Filho G, Macchione M, Garcia ML, Saldiva PH. Effects of formaldehyde on the frog's mucociliary epithelium as a surrogate to evaluate air pollution effects on the respiratory epithelium. Braz J Med Biol Res. 2001; 34:639-643. PMID: 11323751
4. Franklin P, Dingle P, Stick S. Raised exhaled nitric oxide in healthy children is associated with domestic formaldehyde levels. Am J Respir Crit Care Med. 2000; 161:1757-1759. PMID: 10806184
5. Arici S, Karaman S, Dogru S, Cayli S, Arici A, Suren M, et al. Central nervous system toxicity after acute oral formaldehyde exposure in rabbits: An experimental study. Hum Exp Toxicol. 2014.
6. Songur A, Ozen OA, Sarsilmaz M. The toxic effects of formaldehyde on the nervous system. Rev Environ Contam Toxicol. 2010; 203:105-118. doi: 10.1007/978-1-4419-1352-4-3 PMID: 19957118
7. Zararsiz I, Kus I, Akpolat N, Songur A, Ogeturk M, Sarsilmaz M. Protective effects of omega-3 essential fatty acids against formaldehyde-induced neuronal damage in prefrontal cortex of rats. Cell Biochem Funct. 2006; 24:237-244. PMID: 15648056
8. Liu Y, Ye Z, Yang H, Zhou L, Fan D, He S, et al. Disturbances of soluble N-ethylmaleimide-sensitive factor attachment proteins in hippocampal synaptosomes contribute to cognitive impairment after repetitive formaldehyde inhalation in male rats. Neuroscience. 2010; 169:1248-1254. doi: 10.1016/j.neuroscience.2010.05.061 PMID: 20609425
9. Lu Z, Li CM, Qiao Y, Yan Y, Yang X. Effect of inhaled formaldehyde on learning and memory of mice. Indoor Air. 2008; 18:77-83. doi: 10.1111/j.1600-0668.2008.00524.x PMID: 18333987
10. Yu J, Su T, Zhou T, He Y, Lu J, Li J, et al. Uric formaldehyde levels are negatively correlated with cognitive abilities in healthy older adults. Neurosci Bull. 2014; 30:172-184. doi: 10.1007/s12264-013-1416-x PMID: 24733650
11. Kilburn KH. Neurobehavioral impairment and seizures from formaldehyde. Arch Environ Health. 1994; 49:37-44. PMID: 8117145
12. Tang XQ, Ren YK, Chen RQ, Zhuang YY, Fang HR, Xu JH, et al. Formaldehyde induces neurotoxicity to PC12 cells involving inhibition of paraoxonase-1 expression and activity. Clin Exp Pharmacol Physiol. 2011; 38:208-214. doi: 10.1111/j.1440-1681.2011.05485.x PMID: 21261675
13. Luo FC, Zhou J, Lv T, Qi L, Wang SD, Nakamura H, et al. Induction of endoplasmic reticulum stress and the modulation of thioredoxin-1 in formaldehyde-induced neurotoxicity. Neurotoxicology. 2012; 33:290-298. doi: 10.1016/j.neuro.2012.02.004 PMID: 22342837
14. Wang R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J. 2002; 16:1792-1798. PMID: 12409322
15. Wang R. Hydrogen sulfide: the third gasotransmitter in biology and medicine. Antioxid Redox Signal. 2010; 12:1061-1064. doi: 10.1089/ars.2009.2938 PMID: 19845469
16. Zhang M, Shan H, Chang P, Wang T, Dong W, Chen X, et al. Hydrogen sulfide offers neuroprotection on traumatic brain injury in parallel with reduced apoptosis and autophagy in mice. PLoS One. 2014; 9: e87241. doi: 10.1371/journal.pone.0087241 PMID: 24466346
17. Lee M, McGeer E, Kodela R, Kashfi K, McGeer PL. NOSH-aspirin (NBS-1120), a novel nitric oxide and hydrogen sulfide releasing hybrid, attenuates neuroinflammation induced by microglial and astrocytic activation: a new candidate for treatment of neurodegenerative disorders. Glia. 2013; 61:1724-1734. doi: 10.1002/glia.22553 PMID: 23918470
18. Kamat PK, Kalani A, Givvimani S, Sathnur PB, Tyagi SC, Tyagi N. Hydrogen sulfide attenuates neurodegeneration and neurovascular dysfunction induced by intracerebral-administered homocysteine in mice. Neuroscience. 2013; 252:302-319. doi: 10.1016/j.neuroscience.2013.07.051 PMID: 23912038
19. Kimura H, Nagai Y, Umemura K, Kimura Y. Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation. Antioxid Redox Signal. 2005; 7:795-803. PMID: 15890027
20. Lu M, Hu LF, Hu G, Bian JS. Hydrogen sulfide protects astrocytes against H(2)O(2)-induced neural injury via enhancing glutamate uptake. Free Radic Biol Med. 2008; 45:1705-1713. doi: 10.1016/j. freeradbiomed.2008.09.014 PMID: 18848879
21. Jia J, Xiao Y, Wang W, Qing L, Xu Y, Song H, et al. Differential mechanisms underlying neuroprotection of hydrogen sulfide donors against oxidative stress. Neurochem Int. 2013; 62:1072-1078. doi: 10. 1016/j.neuint.2013.04.001 PMID: 23587562
22. Sakamoto K, Suzuki Y, Kurauchi Y, Mori A, Nakahara T, Ishii K. Hydrogen sulfide attenuates NMDA-induced neuronal injury via its anti-oxidative activity in the rat retina. Exp Eye Res. 2014; 120:90-96. doi: 10.1016/j.exer.2014.01.008 PMID: 24451906
23. Yin WL, He JQ, Hu B, Jiang ZS, Tang XQ. Hydrogen sulfide inhibits MPP(+)-induced apoptosis in PC12 cells. Life Sci. 2009; 85:269-275. doi: 10.1016/j.lfs.2009.05.023 PMID: 19540852
24. Tang XQ, Fang HR, Zhou CF, Zhuang YY, Zhang P, Gu HF, et al. A novel mechanism of formaldehyde neurotoxicity: inhibition of hydrogen sulfide generation by promoting overproduction of nitric oxide. PLoS One. 2013; 8:e54829. doi: 10.1371/journal.pone.0054829 PMID: 23359814
25. Tang XQ, Zhuang YY, Zhang P, Fang HR, Zhou CF, Gu HF, et al. Formaldehyde impairs learning and memory involving the disturbance of hydrogen sulfide generation in the hippocampus of rats. J Mol Neurosci. 2013; 49:140-149. doi: 10.1007/s12031-012-9912-4 PMID: 23108488
26. Tang XQ, Ren YK, Zhou CF, Yang CT, Gu HF, He JQ, et al. Hydrogen sulfide prevents formaldehyde-induced neurotoxicity to PC12 cells by attenuation of mitochondrial dysfunction and pro-apoptotic potential. Neurochem Int. 2012; 61:16-24. doi: 10.1016/j.neuint.2012.04.011 PMID: 22542418
27. Li X, Zhang KY, Zhang P, Chen LX, Wang L, Xie M, et al. Hydrogen sulfide inhibits formaldehyde-induced endoplasmic reticulum stress in PC12 cells by upregulation of SIRT-1. PLoS One. 2014; 9: e89856. doi: 10.1371/journal.pone.0089856 PMID: 24587076
28. Binder DK, Scharfman HE. Brain-derived neurotrophic factor. Growth Factors. 2004; 22:123-131. PMID: 15518235
29. Zhang J, Yu Z, Yu Z, Yang Z, Zhao H, Liu L, et al. rAAV-mediated delivery of brain-derived neurotrophic factor promotes neurite outgrowth and protects neurodegeneration in focal ischemic model. Int J Clin Exp Pathol. 2011; 4:496-504. PMID: 21738820
30. Kong S, Cheng Z, Liu J, Wang Y. Downregulated GABA and BDNF-TrkB Pathway in Chronic Cyclothiazide Seizure Model. Neural Plast. 2014; 2014:310146. doi: 10.1155/2014/310146 PMID: 24757570
31. Bifrare YD, Kummer J, Joss P, Tauber MG, Leib SL. Brain-derived neurotrophic factor protects against multiple forms of brain injury in bacterial meningitis. J Infect Dis. 2005; 191:40-45. PMID: 15593001
32. Han BH, Holtzman DM. BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J Neurosci. 2000; 20:5775-5781. PMID: 10908618
33. Pandya CD, Kutiyanawalla A, Pillai A. BDNF-TrkB signaling and neuroprotection in schizophrenia. Asian J Psychiatr. 2013; 6:22-28. doi: 10.1016/j.ajp.2012.08.010 PMID: 23380313
34. Okoye G, Zimmer J, Sung J, Gehlbach P, Deering T, Nambu H, et al. Increased expression of brain-derived neurotrophic factor preserves retinal function and slows cell death from rhodopsin mutation or oxidative damage. J Neurosci. 2003; 23:4164-4172. PMID: 12764104
35. Zhao X, Rebeck GW, Hoe HS, Andrews PM. Tarenflurbil protection from cytotoxicity is associated with an upregulation of neurotrophins. J Alzheimers Dis. 2008; 15:397-407. PMID: 18997293
36. Huang YZ, McNamara JO. Neuroprotective effects of reactive oxygen species mediated by BDNF-independent activation of TrkB. J Neurosci. 2012; 32:15521-15532. doi: 10.1523/JNEUROSCI.0755- 12.2012 PMID: 23115189
37. Boyadjieva NI, Sarkar DK. Cyclic adenosine monophosphate and brain-derived neurotrophic factor decreased oxidative stress and apoptosis in developing hypothalamic neuronal cells: role of microglia. Alcohol Clin Exp Res. 2013; 37:1370-1379. doi: 10.1111/acer.12104 PMID: 23550806
38. Wei HJ, Xu JH, Li MH, Tang JP, Zou W, Zhang P, et al. Hydrogen sulfide inhibits homocysteine-induced endoplasmic reticulum stress and neuronal apoptosis in rat hippocampus via upregulation of the BDNF-TrkB pathway. Acta Pharmacol Sin. 2014; 35:707-715. doi: 10.1038/aps.2013.197 PMID: 24747165
39. Greene LA, Tischler AS. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976; 73:2424-2428. PMID: 1065897
40. Li R, Kong Y, Ladisch S. Nerve growth factor-induced neurite formation in PC12 cells is independent of endogenous cellular gangliosides. Glycobiology. 1998; 8:597-603. PMID: 9592126
41. Wang S, Hu CP, Jiang DJ, Peng J, Zhou Z, Yuan Q, et al. All-trans retinoic acid inhibits cobalt chloride-induced apoptosis in PC12 cells: role of the dimethylarginine dimethylaminohydrolase/asymmetric dimethylarginine pathway. J Neurosci Res. 2009; 87:1938-1946. doi: 10.1002/jnr.21999 PMID: 19156866
42. Ding J, Huang S, Wu S, Zhao Y, Liang L, Yan M, et al. Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol. 2010; 12:390-399. doi: 10.1038/ncb2039 PMID: 20305651
43. Choi HS, Kim JW, Cha YN, Kim C. A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoassay Immunochem. 2006; 27:31-44. PMID: 16450867
44. Jourdi H, Hamo L, Oka T, Seegan A, Baudry M. BDNF mediates the neuroprotective effects of positive AMPA receptor modulators against MPP+-induced toxicity in cultured hippocampal and mesencephalic slices. Neuropharmacology. 2009; 56:876-885. doi: 10.1016/j.neuropharm.2009.01.015 PMID: 19371576
45. Almeida RD, Manadas BJ, Melo CV, Gomes JR, Mendes CS, Graos MM, et al. Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 2005; 12:1329-1343. PMID: 15905876
46. Chen A, Xiong LJ, Tong Y, Mao M. The neuroprotective roles of BDNF in hypoxic ischemic brain injury. Biomed Rep. 2013; 1:167-176. PMID: 24648914
47. Lauterbach EC. Neuroprotective effects of psychotropic drugs in Huntington's disease. Int J Mol Sci. 2013; 14:22558-22603. doi: 10.3390/ijms141122558 PMID: 24248060
48. Usanmaz SE, Akarsu ES, Vural N. Neurotoxic effects of acute and subacute formaldehyde exposures in mice. Environ Toxicol Pharmacol. 2002; 11:93-100. PMID: 21782590
49. Tulpule K, Dringen R. Formaldehyde in brain: an overlooked player in neurodegeneration? J Neurochem. 2013; 127:7-21. doi: 10.1111/jnc.12356 PMID: 23800365
50. Zhang R, Lee IK, Kang KA, Piao MJ, Kim KC, Kim BJ, et al. Cytoprotective effects of triphlorethol-A against formaldehyde-induced oxidative damage and apoptosis: role of mitochondria-mediated caspase-dependent pathway. J Toxicol Environ Health A. 2010; 73:1477-1489. doi: 10.1080/15287394. 2010.511564 PMID: 20954074
51. Li WW, Guo H, Fan GW, Wang XM. [Advance in study on endogenous formaldehyde and pathogenesis of Alzheimer's disease]. Zhongguo Zhong Yao Za Zhi. 2012; 37:3017-3020. PMID: 23311145
52. Ozen OA, Kus MA, Kus I, Alkoc OA, Songur A. Protective effects of melatonin against formaldehyde-induced oxidative damage and apoptosis in rat testes: an immunohistochemical and biochemical study. Syst Biol Reprod Med. 2008; 54:169-176. doi: 10.1080/19396360802422402 PMID: 18942024
53. Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci. 1997; 17:2295-2313. PMID: 9065491
54. Yan Q, Radeke MJ, Matheson CR, Talvenheimo J, Welcher AA, Feinstein SC. Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J Comp Neurol. 1997; 378:135-157. PMID: 9120052
55. Degos V, Charpentier TL, Chhor V, Brissaud O, Lebon S, Schwendimann L, et al. Neuroprotective effects of dexmedetomidine against glutamate agonist-induced neuronal cell death are related to increased astrocyte brain-derived neurotrophic factor expression. Anesthesiology. 2013; 118:1123-1132. doi: 10.1097/ALN.0b013e318286cf36 PMID: 23353792
56. Nguyen TL, Kim CK, Cho JH, Lee KH, Ahn JY. Neuroprotection signaling pathway of nerve growth factor and brain-derived neurotrophic factor against staurosporine induced apoptosis in hippocampal H19-7/IGF-IR. Exp Mol Med. 2010; 42:583-595. PMID: 20644345
57. Su B, Ji YS, Sun XL, Liu XH, Chen ZY. Brain-derived neurotrophic factor (BDNF)-induced mitochondrial motility arrest and presynaptic docking contribute to BDNF-enhanced synaptic transmission. J Biol Chem. 2014; 289:1213-1226. doi: 10.1074/jbc.M113.526129 PMID: 24302729
58. Zararsiz I, Kus I, Ogeturk M, Akpolat N, Kose E, Meydan S, et al. Melatonin prevents formaldehyde-induced neurotoxicity in prefrontal cortex of rats: an immunohistochemical and biochemical study. Cell Biochem Funct. 2007; 25:413-418. PMID: 16397905
59. Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA. Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat. 2005; 29:173-178. PMID: 15820619
60. Gabaizadeh R, Staecker H, Liu W, Van De Water TR. BDNF protection of auditory neurons from cisplatin involves changes in intracellular levels of both reactive oxygen species and glutathione. Brain Res Mol Brain Res. 1997; 50:71-78. PMID: 9406919
61. Siegel SJ, Bieschke J, Powers ET, Kelly JW. The oxidative stress metabolite 4-hydroxynonenal promotes Alzheimer protofibril formation. Biochemistry. 2007; 46:1503-1510. PMID: 17279615
62. Shearn CT, Backos DS, Orlicky DJ, Smathers-McCullough RL, Petersen DR. Identification of 5′ AMP activated kinase as a target of reactive aldehydes during chronic ingestion of high concentrations of ethanol. J Biol Chem. 2014.
63. Fournet G, Martin G, Quash G. alpha,beta-Acetylenic amino thiolester inhibitors of aldehyde dehydrogenases 1&3: suppressors of apoptogenic aldehyde oxidation and activators of apoptosis. Curr Med Chem. 2013; 20:527-533. PMID: 23231347
64. Han H, Wang H, Long H, Nattel S, Wang Z. Oxidative preconditioning and apoptosis in L-cells. Roles of protein kinase B and mitogen-activated protein kinases. J Biol Chem. 2001; 276:26357-26364. PMID: 11331278
65. Tamagno E, Robino G, Obbili A, Bardini P, Aragno M, Parola M, et al. H2O2 and 4-hydroxynonenal mediate amyloid beta-induced neuronal apoptosis by activating JNKs and p38MAPK. Exp Neurol. 2003; 180:144-155. PMID: 12684028
66. Konstantinidou AE, Givalos N, Gakiopoulou H, Korkolopoulou P, Kotsiakis X, Boviatsis E, et al. Caspase-3 immunohistochemical expression is a marker of apoptosis, increased grade and early recurrence in intracranial meningiomas. Apoptosis. 2007; 12:695-705. PMID: 17143787
67. Eberhardt O, Schulz JB. Apoptotic mechanisms and antiapoptotic therapy in the MPTP model of Parkinson's disease. Toxicol Lett. 2003; 139:135-151. PMID: 12628749
68. Fukamachi Y, Karasaki Y, Sugiura T, Itoh H, Abe T, Yamamura K, et al. Zinc suppresses apoptosis of U937 cells induced by hydrogen peroxide through an increase of the Bcl-2/Bax ratio. Biochem Biophys Res Commun. 1998; 246:364-369. PMID: 9610364
69. Tapley P, Lamballe F, Barbacid M. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene. 1992; 7:371-381. PMID: 1312698
70. Vandiver MS, Paul BD, Xu R, Karuppagounder S, Rao F, Snowman AM, et al. Sulfhydration mediates neuroprotective actions of parkin. Nat Commun. 2013; 4:1626. doi: 10.1038/ncomms2623 PMID: 23535647
71. Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, et al. Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Mol Cell. 2012; 45:13-24. doi: 10.1016/j.molcel.2011.10.021 PMID: 22244329
72. Krishnan N, Fu C, Pappin DJ, Tonks NK. H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal. 2011; 4:ra86. doi: 10.1126/scisignal.2002329 PMID: 22169477
73. Yang G, Zhao K, Ju Y,Mani S, Cao Q, Puukila S, et al. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal. 2013; 18:1906-1919. doi: 10.1089/ars.2012.4645 PMID: 23176571