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

Neurobiology of Disease

Volumn 55, Issue , 2013, Pages 26-35

  Zhang, Yi ^a,b   Cook, Anna ^a   Kim, Jinho ^c   Baranov, Sergei V ^d   Jiang, Jiying ^a,e   Smith, Karen ^f   Cormier, Kerry ^f   Bennett, Erik ^d   Browser, Robert P ^d,g   Day, Arthur L ^a,h   Carlisle, Diane L ^d   Ferrante, Robert J ^c,i   Wang, Xin ^a   Friedlander, Robert M ^a,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e WEIFANG MEDICAL UNIVERSITY   (China)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g BARROW NEUROLOGICAL INSTITUTE   (United States)

^h UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

ⁱ VA Pittsburgh Healthcare System   (United States)

Author keywords

Amyotrophic lateral sclerosis; Apoptosis; Caspases; Cytochrome c; Melatonin; Melatonin receptor 1A

Indexed keywords

CASPASE 3; CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; INTERLEUKIN 1BETA CONVERTING ENZYME; MELATONIN; MELATONIN 1 RECEPTOR; RECEPTOR INTERACTING PROTEIN 2; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL DEATH; CELL LOSS; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN TISSUE; MICROGLIA; MOTONEURON; MOUSE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SPINAL CORD ATROPHY; SPINAL CORD VENTRAL HORN; UPREGULATION;

AMYOTROPHIC LATERAL SCLEROSIS; ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; CASPASE 3; CELL DEATH; CYTOCHROMES C; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; MELATONIN; MICE; MICE, TRANSGENIC; RECEPTOR, MELATONIN, MT1; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84876721837     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.03.008     Document Type: Article

References (54)

1. Bensimon G., et al. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/riluzole study group. N. Engl. J. Med. 1994, 330:585-591.
2. Caballero B., et al. Favorable effects of a prolonged treatment with melatonin on the level of oxidative damage and neurodegeneration in senescence-accelerated mice. J. Pineal Res. 2008, 45:302-311.
3. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2001, 2:806-819.
4. Das A., et al. Cytoprotective effects of melatonin on C6 astroglial cells exposed to glutamate excitotoxicity and oxidative stress. J. Pineal Res. 2008, 45:117-124.
5. Drachman D.B., et al. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann. Neurol. 2002, 52:771-778.
6. Dupuis L., et al. Mitochondria in amyotrophic lateral sclerosis: a trigger and a target. Neurodegener. Dis. 2004, 1:245-254.
7. Ferrante R.J., et al. Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J. Neurochem. 1997, 69:2064-2074.
8. Friedlander R.M. Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med. 2003, 348:1365-1375.
9. Friedlander R.M., et al. Inhibition of ICE slows ALS in mice. Nature 1997, 388:31.
10. Friedlander R.M., et al. Expression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by trophic factor withdrawal and ischemic brain injury. J. Exp. Med. 1997, 185:933-940.
11. Fujita K., et al. Increase of glial fibrillary acidic protein fragments in the spinal cord of motor neuron degeneration mutant mouse. Brain Res. 1998, 785:31-40.
12. Guegan C., et al. Recruitment of the mitochondrial-dependent apoptotic pathway in amyotrophic lateral sclerosis. J. Neurosci. 2001, 21:6569-6576.
13. Guegan C., et al. Instrumental activation of bid by caspase-1 in a transgenic mouse model of ALS. Mol. Cell. Neurosci. 2002, 20:553-562.
14. Hardeland R. Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine 2005, 27:119-130.
15. Henkel J.S., et al. Microglia in ALS: the good, the bad, and the resting. J. Neuroimmune Pharmacol. 2009, 4:389-398.
16. Jacob S., et al. Melatonin as a candidate compound for neuroprotection in amyotrophic lateral sclerosis (ALS): high tolerability of daily oral melatonin administration in ALS patients. J. Pineal Res. 2002, 33:186-187.
17. Jemmerson R., et al. Cytochrome C release from CNS mitochondria and potential for clinical intervention in apoptosis-mediated CNS diseases. Antioxid. Redox Signal. 2005, 7:1158-1172.
18. Julien J.P., Beaulieu J.M. Cytoskeletal abnormalities in amyotrophic lateral sclerosis: beneficial or detrimental effects?. J. Neurol. Sci. 2000, 180:7-14.
19. Keller A.F., et al. Live imaging of amyotrophic lateral sclerosis pathogenesis: disease onset is characterized by marked induction of GFAP in Schwann cells. Glia 2009, 57:1130-1142.
20. Kostic V., et al. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 1997, 277:559-562.
21. Li M., et al. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000, 288:335-339.
22. Liu X., et al. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996, 86:147-157.
23. Martin L.J. Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J. Neuropathol. Exp. Neurol. 1999, 58:459-471.
24. Martin L.J., et al. Mechanisms for neuronal degeneration in amyotrophic lateral sclerosis and in models of motor neuron death (review). Int. J. Mol. Med. 2000, 5:3-13.
25. Mazzucchelli C., et al. The melatonin receptor in the human brain: cloning experiments and distribution studies. Brain Res. Mol. Brain Res. 1996, 39:117-126.
26. McGeer P.L., McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 2002, 26:459-470.
27. Miller R.G., et al. Practice parameter: the care of the patient with amyotrophic lateral sclerosis (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology: ALS practice parameters task force. Neurology 1999, 52:1311-1323.
28. Morrison K.E. Therapies in amyotrophic lateral sclerosis-beyond riluzole. Curr. Opin. Pharmacol. 2002, 2:302-309.
29. Naji L., et al. Expression of membrane and nuclear melatonin receptors in mouse peripheral organs. Life Sci. 2004, 74:2227-2236.
30. Pasinelli P., et al. Caspase-1 and -3 are sequentially activated in motor neuron death in Cu, Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13901-13906.
31. Pasinelli P., et al. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 2004, 43:19-30.
32. Rodriguez C., et al. Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 2004, 36:1-9.
33. Rowland L.P., Shneider N.A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 2001, 344:1688-1700.
34. Ryu H., et al. Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J. Neurochem. 2005, 93:1087-1098.
35. Sanchez-Hidalgo M., et al. Decreased MT1 and MT2 melatonin receptor expression in extrapineal tissues of the rat during physiological aging. J. Pineal Res. 2009, 46:29-35.
36. Sathasivam S., et al. Apoptosis in amyotrophic lateral sclerosis: a review of the evidence. Neuropathol. Appl. Neurobiol. 2001, 27:257-274.
37. Savaskan E., et al. Cerebrovascular melatonin MT1-receptor alterations in patients with Alzheimer's disease. Neurosci. Lett. 2001, 308:9-12.
38. Savaskan E., et al. Reduced hippocampal MT2 melatonin receptor expression in Alzheimer's disease. J. Pineal Res. 2005, 38:10-16.
39. Shefner J.M., et al. Effect of neurophilin ligands on motor units in mice with SOD1 ALS mutations. Neurology 2001, 57:1857-1861.
40. Shi P., et al. Mitochondrial dysfunction in amyotrophic lateral sclerosis. Biochim. Biophys. Acta 2010, 1802:45-51.
41. Thome M., et al. Identification of CARDIAK, a RIP-like kinase that associates with caspase-1. Curr. Biol. 1998, 8:885-888.
42. Veldink J.H., et al. Sexual differences in onset of disease and response to exercise in a transgenic model of ALS. Neuromuscul. Disord. 2003, 13:737-743.
43. Vukosavic S., et al. Bax and Bcl-2 interaction in a transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 1999, 73:2460-2468.
44. Wang H., et al. Nortriptyline delays disease onset in models of chronic neurodegeneration. Eur. J. Neurosci. 2007, 26:633-641.
45. Wang X., et al. Inhibitors of cytochrome c release with therapeutic potential for Huntington's disease. J. Neurosci. 2008, 28:9473-9485.
46. Wang X., et al. Methazolamide and melatonin inhibit mitochondrial cytochrome C release and are neuroprotective in experimental models of ischemic injury. Stroke 2009, 40:1877-1885.
47. Wang X., et al. The melatonin MT1 receptor axis modulates mutant Huntingtin-mediated toxicity. J. Neurosci. 2011, 31:14496-14507.
48. Weishaupt J.H., et al. Reduced oxidative damage in ALS by high-dose enteral melatonin treatment. J. Pineal Res. 2006, 41:313-323.
49. Weydt P., et al. Assessing disease onset and progression in the SOD1 mouse model of ALS. Neuroreport 2003, 14:1051-1054.
50. Yang J., et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 1997, 275:1129-1132.
51. Zhang W., et al. Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann. Neurol. 2003, 53:267-270.
52. Zhang W.H., et al. Fundamental role of the Rip2/caspase-1 pathway in hypoxia and ischemia-induced neuronal cell death. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:16012-16017.
53. Zhang Y., et al. Dipyrone inhibits neuronal cell death and diminishes hypoxic/ischemic brain injury. Neurosurgery 2011, 69:942-956.
54. Zhu S., et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002, 417:74-78.