N-acetyl-serotonin offers neuroprotection through inhibiting mitochondrial death pathways and autophagic activation in experimental models of ischemic injury

Journal of Neuroscience

Volumn 34, Issue 8, 2014, Pages 2967-2978

  Zhou, Hua ^a,e   Wang, Jian ^a   Jiang, Jiying ^a,f   Stavrovskaya, Irina G ^a   Li, Mingchang ^a,b   Li, Wei ^a   Wu, Qiaofeng ^a   Zhang, Xinmu ^a   Luo, Chengliang ^a   Zhou, Shuanhu ^a   Sirianni, Ana C ^a   Sarkar, Sovan ^c   Kristal, Bruce S ^a   Friedlander, Robert M ^d   Wang, Xin ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^e SICHUAN UNIVERSITY   (China)

^f WEIFANG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BRAIN ISCHEMIA; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; HIPPOCAMPUS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NEUROPROTECTIVE AGENTS; PERMEABILITY; SEROTONIN; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS;

EID: 84894101380     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1948-13.2014     Document Type: Article

References (66)

1. Aguiar LM, Macedo DS, de Freitas RM, de Albuquerque Oliveira A, Vasconcelos SM, de Sousa FC, de Barros Viana GS (2005) Protective effects of N-acetylserotonin against 6-hydroxydopamine-induced neurotoxicity. Life Sci 76:2193-2202. CrossRef Medline
2. Azad MB, Chen Y, Henson ES, Cizeau J, McMillan-Ward E, Israels SJ, Gibson SB (2008) Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 4:195-204. Medline
3. Bai JZ, Lipski J (2010) Differential expression of TRPM2 and TRPV4 channels and their potential role in oxidative stress-induced cell death in organotypic hippocampal culture. Neurotoxicology 31:204-214. CrossRef Medline
4. Baranov SV, Stavrovskaya IG, Brown AM, Tyryshkin AM, Kristal BS (2008) Kinetic model for Ca2+-induced permeability transition in energized liver mitochondria discriminates between inhibitor mechanisms. J Biol Chem 283:665-676. CrossRef Medline
5. Büki A, Okonkwo DO, Wang KK, Povlishock JT (2000) Cytochrome c release and caspase activation in traumatic axonal injury. J Neurosci 20: 2825-2834. Medline
6. Chang LK, Johnson EM Jr (2002) Cyclosporin A inhibits caspaseindependent death of NGF-deprived sympathetic neurons: a potential role for mitochondrial permeability transition. J Cell Biol 157:771-781. CrossRef Medline
7. Cho S, Wood A, Bowlby MR (2007) Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr Neuropharmacol 5:19-33. CrossRef Medline
8. Cohen Z, Bonvento G, Lacombe P, Hamel E (1996) Serotonin in the regulation of brain microcirculation. Prog Neurobiol 50:335-362. CrossRef Medline
9. Cotran RS, Kumar V, Collins T, Robbins SL (1999) Robbins pathologic basis of disease. Philadelphia: W.B. Saunders.
10. Cui D, Wang L, Qi A, Zhou Q, Zhang X, Jiang W (2012) Propofol prevents autophagic cell death following oxygen and glucose deprivation in PC12 cells and cerebral ischemia-reperfusion injury in rats. PLo S One 7:e35324. CrossRef Medline
11. Dejean LM, Martinez-Caballero S, Kinnally KW (2006a) Is MAC the knife that cuts cytochrome c from mitochondria during apoptosis? Cell Death Differ 13:1387-1395. CrossRef Medline
12. Dejean LM, Martinez-Caballero S, Manon S, Kinnally KW (2006b) Regulation of the mitochondrial apoptosis-induced channel, MAC, by BCL-2 family proteins. Biochim Biophys Acta 1762:191-201. CrossRef Medline
13. DeSimoni A, Yu LM (2006) Preparation of organotypic hippocampal slice cultures: interface method. Nat Protoc 1:1439-1445. CrossRef Medline
14. Domañska-Janik K, Buzañska L, Dłuzniewska J, Kozłowska H, Sarnowska A, Zabłocka B (2004) Neuroprotection by cyclosporin A following transient brain ischemia correlates with the inhibition of the early efflux of cytochrome C to cytoplasm. Brain Res Mol Brain Res 121:50-59. CrossRef Medline
15. Friedlander RM (2003) Apoptosis and caspases in neurodegenerative diseases. N Engl J Med 348:1365-1375. CrossRef Medline
16. Gao L, Jiang T, Guo J, Liu Y, Cui G, Gu L, Su L, Zhang Y (2012) Inhibition of autophagy contributes to ischemic postconditioning-induced neuroprotection against focal cerebral ischemia in rats. Plo S one 7:e46092. CrossRef Medline
17. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309-1312. CrossRef Medline
18. Ha JH, Noh HS, Shin IW, Hahm JR, Kim DR (2012) Mitigation of H2O2-induced autophagic cell death by propofol in H9c2 cardiomyocytes. Cell Biol Toxicol 28:19-29. CrossRef Medline
19. Higgins GC, Devenish RJ, Beart PM, Nagley P (2011) Autophagic activity in cortical neurons under acute oxidative stress directly contributes to cell death. Cell Mol Life Sci 68:3725-3740. CrossRef Medline
20. Jahani-Asl A, Cheung EC, Neuspiel M, MacLaurin JG, Fortin A, Park DS, McBride HM, Slack RS (2007) Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J Biol Chem 282:23788-23798. CrossRef Medline
21. Jang SW, Liu X, Pradoldej S, Tosini G, Chang Q, Iuvone PM, Ye K (2010) N-acetylserotonin activates Trk B receptor in a circadian rhythm. Proc Natl Acad Sci U S A 107:3876-3881. CrossRef Medline
22. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445-544. CrossRef Medline
23. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K, Uchiyama Y (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172:454-469. CrossRef Medline
24. Komatsu M, Wang QJ, Holstein GR, Friedrich VL Jr, Iwata J, Kominami E, Chait BT, Tanaka K, Yue Z (2007) Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci U S A 104:14489-14494. CrossRef Medline
25. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N (2004) The role of autophagy during the early neonatal starvation period. Nature 432:1032-1036. CrossRef Medline
26. Li LY, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412:95-99. CrossRef Medline
27. Li P, Yang X, Wasser M, Cai Y, Chia W (1997) Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNAduring Drosophila neuroblast cell divisions. Cell 90:437-447. CrossRef Medline
28. Matsumoto S, Friberg H, Ferrand-Drake M, Wieloch T (1999) Blockade of the mitochondrial permeability transition pore diminishes infarct size in the rat after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 19:736-741. CrossRef Medline
29. Moosmann B, Behl C (1999) The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc Natl Acad Sci U S A 96:8867-8872. CrossRef Medline
30. Nagley P, Higgins GC, Atkin JD, Beart PM (2010) Multifaceted deaths orchestrated by mitochondria in neurones. Biochim Biophys Acta 1802: 167-185. CrossRef Medline
31. Nopparat C, Porter JE, Ebadi M, Govitrapong P (2010) The mechanism for the neuroprotective effect of melatonin against methamphetamineinduced autophagy. J Pineal Res 49:382-389. CrossRef Medline
32. Oxenkrug G, Requintina P, Bachurin S (2001) Antioxidant and antiaging activity of N-acetylserotonin and melatonin in the in vivo models. Ann N Y Acad Sci 939:190-199. CrossRef Medline
33. Pan R (2013) Autophagy in cerebral ischemia: therapist or killer. J Biomol Res Ther 2:1000e111. CrossRef
34. Pandya RS, Mao L, Zhou H, Zhou S, Zeng J, Popp AJ, Wang X (2011) Central nervous system agents for ischemic stroke: neuroprotection mechanisms. Cent Nerv Syst Agents Med Chem 11:81-97. CrossRef Medline
35. Pandya RS, Zhu H, Li W, Bowser R, Friedlander RM, Wang X (2013) Therapeutic neuroprotective agents for amyotrophic lateral sclerosis. Cell Mol Life Sci 70:4729-4745. CrossRef Medline
36. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Øvervatn A, Bjørkøy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131-24145. CrossRef Medline
37. Pellegrini-Giampietro DE, Cozzi A, Peruginelli F, Leonardi P, Meli E, Pellicciari R, Moroni F (1999) 1-Aminoindan-1,5-dicarboxylic acid and (S)-(+)-2-(3'-carboxybicyclo[1.1.1] pentyl)-glycine, two m Glu1 receptor-preferring antagonists, reduce neuronal death in in vitro and in vivo models of cerebral ischaemia. Eur J Neurosci 11:3637-3647. CrossRef Medline
38. Plesnila N, Zinkel S, Le DA, Amin-Hanjani S, Wu Y, Qiu J, Chiarugi A, Thomas SS, Kohane DS, Korsmeyer SJ, Moskowitz MA (2001) BID mediates neuronal cell death after oxygen/ glucose deprivation and focal cerebral ischemia. Proc Natl Acad Sci U S A 98:15318-15323. CrossRef Medline
39. Pringle AK, Iannotti F, Wilde GJ, Chad JE, Seeley PJ, Sundstrom LE (1997) Neuroprotection by both NMDA and non-NMDA receptor antagonists in in vitro ischemia. Brain Res 755:36-46. CrossRef Medline
40. Puyal J, Vaslin A, Mottier V, Clarke PG (2009) Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 66:378-389. CrossRef Medline
41. Sheng R, Zhang LS, Han R, Liu XQ, Gao B, Qin ZH (2010) Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 6:482-494. CrossRef Medline
42. Sheng R, Liu XQ, Zhang LS, Gao B, Han R, Wu YQ, Zhang XY, Qin ZH (2012) Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 8:310-325. CrossRef Medline
43. Shi R, Weng J, Zhao L, Li XM, Gao TM, Kong J (2012) Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci Ther 18:250-260. CrossRef Medline
44. Siesjö BK (1992) Pathophysiology and treatment of focal cerebral ischemia: Part II. Mechanisms of damage and treatment. J Neurosurg 77:337-354. CrossRef Medline
45. Soane L, Polster BM, Fiskum G (2011) Mitochondrial mechanisms of neural cell death in cerebral ischemia. In: Apoptosis physiology and pathology (JC Reed, ed). Cambridge: Cambridge UP.
46. Stavrovskaya IG, Baranov SV, Guo X, Davies SS, Roberts LJ 2nd, Kristal BS (2010) Reactive gamma-ketoaldehydes formed via the isoprostane pathway disrupt mitochondrial respiration and calcium homeostasis. Free Radic Biol Med 49:567-579. CrossRef Medline
47. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182. CrossRef Medline
48. Strasser U, Fischer G (1995) Protection from neuronal damage induced by combined oxygen and glucose deprivation in organotypic hippocampal cultures by glutamate receptor antagonists. Brain Res 687:167-174. CrossRef Medline
49. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446. CrossRef Medline
50. Wang X (2009) The antiapoptotic activity of melatonin in neurodegenerative diseases. CNS Neurosci Ther 15:345-357. CrossRef Medline
51. Wang X, Bauer JH, Li Y, Shao Z, Zetoune FS, Cattaneo E, Vincenz C (2001) Characterization of a p75(NTR) apoptotic signaling pathway using a novel cellular model. J Biol Chem 276:33812-33820. CrossRef Medline
52. Wang X, Bregegere F, Soroka Y, Kayat A, Redziniak G, Milner Y (2004) Enhancement of Fas-mediated apoptosis in ageing human keratinocytes. Mech Ageing Dev 125:237-249. CrossRef Medline
53. Wang X, Zhu S, Pei Z, Drozda M, Stavrovskaya IG, Del Signore SJ, Cormier K, Shimony EM, Wang H, Ferrante RJ, Kristal BS, Friedlander RM (2008) Inhibitors of cytochrome c release with therapeutic potential for Huntington's disease. J Neurosci 28:9473-9485. CrossRef Medline
54. Wang X, Figueroa BE, Stavrovskaya IG, Zhang Y, Sirianni AC, Zhu S, Day AL, Kristal BS, Friedlander RM (2009) Methazolamide and melatonin inhibit mitochondrial cytochrome C release and are neuroprotective in experimental models of ischemic injury. Stroke 40:1877-1885. CrossRef Medline
55. Wang X, Sirianni A, Pei Z, Cormier K, Smith K, Jiang J, Zhou S, Wang H, Zhao R, Yano H, Kim JE, Li W, Kristal BS, Ferrante RJ, Friedlander RM (2011) The melatonin MT1receptor axis modulates mutant Huntingtinmediated toxicity. J Neurosci 31:14496-14507. CrossRef Medline
56. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, Han F, Fukunaga K, Qin ZH (2008) Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 4:762-769. Medline
57. Winters WD, Petit JP, Lakin ML, Miller CH (1984) Effects of amine pretreatment on ketamine catatonia in pinealectomized or hypophysectomized animals. J Pharmacol Exp Ther 230:69-74. Medline
58. Wölfler A, Abuja PM, Schauenstein K, Liebmann PM (1999) N-acetylserotonin is a better extra-and intracellular antioxidant than melatonin. FEBS Lett 449:206-210. CrossRef Medline
59. Young KW, Piñon LG, Bampton ET, Nicotera P (2010) Different pathways lead to mitochondrial fragmentation during apoptotic and excitotoxic cell death in primary neurons. J Biochem Mol Toxicol 24:335-341. CrossRef Medline
60. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU (2006) Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 8:1124-1132. CrossRef Medline
61. Yu S, Zheng J, Jiang Z, Shi C, Li J, Du X, Wang H, Jiang J, Wang X (2013) Protective effect of N-acetylserotonin against acute hepatic ischemiareperfusion injury in mice. Int J Mol Sci 14:17680-17693. CrossRef Medline
62. Zhang WH, Wang X, Narayanan M, Zhang Y, Huo C, Reed JC, Friedlander RM (2003) Fundamental role of the Rip2/caspase-1 pathway in hypoxia and ischemia-induced neuronal cell death. Proc Natl Acad Sci U S A 100: 16012-16017. CrossRef Medline
63. Zhang WH, Wang H, Wang X, Narayanan MV, Stavrovskaya IG, Kristal BS, Friedlander RM (2008) Nortriptyline protects mitochondria and reduces cerebral ischemia/hypoxia injury. Stroke 39:455-462. CrossRef Medline
64. Zhang Y, Wang X, Baranov SV, Zhu S, Huang Z, Fellows-Mayle W, Jiang J, Day AL, Kristal BS, Friedlander RM (2011) Dipyrone inhibits neuronal cell death and diminishes hypoxic/ischemic brain injury. Neurosurgery 69:942-956. CrossRef Medline
65. Zhang Y, Cook A, Kim J, Baranov SV, Jiang J, Smith K, Cormier K, Bennett E, Browser RP, Day AL, Carlisle DL, Ferrante RJ, Wang X, Friedlander RM (2013) Melatonin inhibits the caspase-1/cytochrome c/caspase-3 cell death pathway, inhibits MT1 receptor loss and delays disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 55:26-35. CrossRef Medline
66. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417: 74-78. CrossRef Medline