Epigenetic targets for melatonin: Induction of histone H3 hyperacetylation and gene expression in C17.2 neural stem cells

Journal of Pineal Research

Volumn 45, Issue 3, 2008, Pages 277-284

  Sharma, Rohita ^a   Ottenhof, Thomas ^a   Rzeczkowska, Paulina A ^a   Niles, Lennard P ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

III tubulin; Differentiation; Histone deacetylase mRNA; Histone H3 hyperacetylation; Melatonin MT1 receptor; Nestin; Nurr1

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 7; HISTONE H3; MELATONIN; MELATONIN 1 RECEPTOR; NEUROTROPHIC FACTOR;

ACETYLATION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DRUG EFFECT; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN VITRO STUDY; MOUSE; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HISTONES; INTERMEDIATE FILAMENT PROTEINS; MELATONIN; METHYL-CPG-BINDING PROTEIN 2; MICE; NERVE TISSUE PROTEINS; NEURITES; NEURONS; RECEPTOR, MELATONIN, MT1; RECEPTOR, MELATONIN, MT2; STEM CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUBULIN;

EID: 51649128880     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2008.00587.x     Document Type: Article

References (75)

1. Taupin P, Gage FH. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 2002 69: 745 749.
2. Geraerts M, Krylyshkina O, Debyser Z, et al. Concise review: therapeutic strategies for Parkinson disease based on the modulation of adult neurogenesis. Stem Cells 2007 25: 263 270.
3. Snyder EY, Deitcher DL, Walsh C, et al. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 1992 68: 33 51.
4. Ryder EF, Snyder EY, Cepko CL. Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J Neurobiol 1990 21: 356 375.
5. Yang M, Stull ND, Berk MA, et al. Neural stem cells spontaneously express dopaminergic traits after transplantation into the intact or 6-hydroxydopamine-lesioned rat. Exp Neurol 2002 177: 50 60.
6. Ryu MY, Lee MA, Ahn YH, et al. Brain transplantation of neural stem cells cotransduced with tyrosine hydroxylase and GTP cyclohydrolase 1 in Parkinsonian rats. Cell Transplant 2005 14: 193 202.
7. Liu WG, Lu GQ, Li B, et al. Dopaminergic neuroprotection by neurturin-expressing c17.2 neural stem cells in a rat model of Parkinson's disease. Parkinsonism Relat Disord 2007 13: 77 88.
8. Lu P, Jones LL, Snyder EY, et al. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 2003 181: 115 129.
9. Niles LP, Armstrong KJ, Rincon Castro LM, et al. Neural stem cells express melatonin receptors and neurotrophic factors: colocalization of the MT1 receptor with neuronal and glial markers. BMC Neurosci 2004 5: 41.
10. Sainz RM, Mayo JC, Tan DX, et al. Melatonin reduces prostate cancer cell growth leading to neuroendocrine differentiation via a receptor and PKA independent mechanism. Prostate 2005 63: 29 43.
11. Uysal N, Ozdemir D, Dayi A, et al. Effects of maternal deprivation on melatonin production and cognition in adolescent male and female rats. Neuro Endocrinol Lett 2005 26: 555 560.
12. Radio NM, Doctor JS, Witt-Enderby PA. Melatonin enhances alkaline phosphatase activity in differentiating human adult mesenchymal stem cells grown in osteogenic medium via MT2 melatonin receptors and the MEK/ERK (1/2) signaling cascade. J Pineal Res 2006 40: 332 342.
13. Sharma R, Niles LP. Induction of Nurr1 by melatonin in a neural stem cell line. Program No. 784.16. 2006 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Atlanta, GA, 2006 abstract (online).
14. Ajamian F, Suuronen T, Salminen A, et al. Upregulation of class II histone deacetylases mRNA during neural differentiation of cultured rat hippocampal progenitor cells. Neurosci Lett 2003 346: 57 60.
15. Cunliffe VT, Casaccia-Bonnefil P. Histone deacetylase 1 is essential for oligodendrocyte specification in the zebrafish CNS. Mech Dev 2006 123: 24 30.
16. Jung BP, Jugloff DG, Zhang G, et al. The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells. J Neurobiol 2003 55: 86 96.
17. Castro LM, Gallant M, Niles LP. Novel targets for valproic acid: up-regulation of melatonin receptors and neurotrophic factors in C6 glioma cells. J Neurochem 2005 95: 1227 1236.
18. Yang M, Donaldson AE, Jiang Y, et al. Factors influencing the differentiation of dopaminergic traits in transplanted neural stem cells. Cell Mol Neurobiol 2003 23: 851 864.
19. Kim JY, Koh HC, Lee JY, et al. Dopaminergic neuronal differentiation from rat embryonic neural precursors by Nurr1 overexpression. J Neurochem 2003 85: 1443 1454.
20. Arenas E. Engineering a dopaminergic phenotype in stem/precursor cells: role of Nurr1, glia-derived signals, and Wnts. Ann NY Acad Sci 2005 1049: 51 66.
21. Kim DW, Chung S, Hwang M, et al. Stromal cell-derived inducing activity, Nurr1, and signaling molecules synergistically induce dopaminergic neurons from mouse embryonic stem cells. Stem Cells 2006 24: 557 567.
22. Bordt SL, Mckeon RM, Li PK, et al. N1E-115 mouse neuroblastoma cells express MT1 melatonin receptors and produce neurites in response to melatonin. Biochim Biophys Acta 2001 1499: 257 264.
23. Witt-Enderby PA, Mackenzie RS, Mckeon RM, et al. Melatonin induction of filamentous structures in non-neuronal cells that is dependent on expression of the human mt1 melatonin receptor. Cell Motil Cytoskeleton 2000 46: 28 42.
24. Bazan E, Alonso FJ, Redondo C, et al. In vitro and in vivo characterization of neural stem cells. Histol Histopathol 2004 19: 1261 1275.
25. Chan AS, Lai FP, Lo RK, et al. Melatonin mt1 and MT2 receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins. Cell Signal 2002 14: 249 257.
26. Kilic U, Kilic E, Reiter RJ, et al. Signal transduction pathways involved in melatonin-induced neuroprotection after focal cerebral ischemia in mice. J Pineal Res 2005 38: 67 71.
27. Lee SH, Chun W, Kong PJ, et al. Sustained activation of Akt by melatonin contributes to the protection against kainic acid-induced neuronal death in hippocampus. J Pineal Res 2006 40: 79 85.
28. Mani N, Khaibullina A, Krum JM, et al. Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: receptor mediation and signal transduction pathways. Exp Neurol 2005 192: 394 406.
29. Forte G, Minieri M, Cossa P, et al. Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 2006 24: 23 33.
30. Perlmann T, Wallen-Mackenzie A. Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res 2004 318: 45 52.
31. Jankovic J, Chen S, Le WD. The role of Nurr1 in the development of dopaminergic neurons and Parkinson's disease. Prog Neurobiol 2005 77: 128 138.
32. Andersson EK, Irvin DK, Ahlsio J, et al. Ngn2 and Nurr1 act in synergy to induce midbrain dopaminergic neurons from expanded neural stem and progenitor cells. Exp Cell Res 2007 313: 1172 1180.
33. Shim JW, Park CH, Bae YC, et al. Generation of functional dopamine neurons from neural precursor cells isolated from the subventricular zone and white matter of the adult rat brain using nurr1 overexpression. Stem Cells 2007 25: 1252 1262.
34. Sousa KM, Mira H, Hall AC, et al. Microarray analyses support a role for Nurr1 in resistance to oxidative stress and neuronal differentiation in neural stem cells. Stem Cells 2007 25: 511 519.
35. Moriya T, Horie N, Mitome M, et al. Melatonin influences the proliferative and differentiative activity of neural stem cells. J Pineal Res 2007 42: 411 418.
36. Ma H, Zhang Z, Tong T. The effects of epidermal growth factor on gene expression in human fibroblasts. In Vitro Cell Dev Biol Anim 2002 38: 481 486.
37. Ajamian F, Salminen A, Reeben M. Selective regulation of class I and class II histone deacetylases expression by inhibitors of histone deacetylases in cultured mouse neural cells. Neurosci Lett 2004 365: 64 68.
38. Hsieh J, Nakashima K, Kuwabara T, et al. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci USA 2004 101: 16659 16664.
39. Marin-Husstege M, Muggironi M, Liu A, et al. Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 2002 22: 10333 10345.
40. Stockhausen MT, Sjolund J, Manetopoulos C, et al. Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br J Cancer 2005 92: 751 759.
41. Balasubramaniyan V, Boddeke E, Bakels R, et al. Effects of histone deacetylation inhibition on neuronal differentiation of embryonic mouse neural stem cells. Neuroscience 2006 143: 939 951.
42. Witt-Enderby PA, Bennett J, Jarzynka MJ, et al. Melatonin receptors and their regulation: biochemical and structural mechanisms. Life Sci 2003 72: 2183 2198.
43. Benitez-King G, Hernandez ME, Tovar R, et al. Melatonin activates PKC-alpha but not PKC-epsilon in N1E-115 cells. Neurochem Int 2001 39: 95 102.
44. Soto-Vega E, Meza I, Ramirez-Rodriguez G, et al. Melatonin stimulates calmodulin phosphorylation by protein kinase C. J Pineal Res 2004 37: 98 106.
45. Lee ER, Mccool KW, Murdoch FE, et al. Dynamic changes in histone H3 phosphoacetylation during early embryonic stem cell differentiation are directly mediated by mitogen- and stress-activated protein kinase 1 via activation of MAPK pathways. J Biol Chem 2006 281: 21162 21172.
46. Cohen-Armon M, Visochek L, Rozensal D, et al. DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 2007 25: 297 308.
47. Chwang WB, Arthur JS, Schumacher A, et al. The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 2007 27: 12732 12742.
48. Liu Y, Denlinger CE, Rundall BK, et al. Suberoylanilide hydroxamic acid induces Akt-mediated phosphorylation of p300, which promotes acetylation and transcriptional activation of RelA/p65. J Biol Chem 2006 28: 31359 31368.
49. Kang J, Shi Y, Xiang B, et al. A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 2005 123: 833 847.
50. Dewire SM, Ahn S, Lefkowitz RJ, et al. Beta-arrestins and cell signaling. Annu Rev Physiol 2007 69: 483 510.
51. Park HT, Baek SY, Kim BS, et al. Developmental expression of 'RZR beta, a putative nuclear-melatonin receptor' mRNA in the suprachiasmatic nucleus of the rat. Neurosci Lett 1996 217: 17 20.
52. Naji L, Carrillo-Vico A, Guerrero JM, et al. Expression of membrane and nuclear melatonin receptors in mouse peripheral organs. Life Sci 2004 74: 2227 2236.
53. Agez L, Laurent V, Pévet P, et al. Melatonin affects nuclear orphan receptors mRNA in the rat suprachiasmatic nuclei. Neuroscience 2007 144: 522 530.
54. Lau P, Bailey P, Dowhan DH, et al. Exogenous expression of a dominant negative RORalpha1 vector in muscle cells impairs differentiation: RORalpha1 directly interacts with p300 and myoD. Nucleic Acids Res 1999 27: 411 420.
55. Aranda A, Pascual A. Nuclear hormone receptors and gene expression. Physiol Rev 2001 81: 1269 1304.
56. Zechel C. Requirement of retinoic acid receptor isotypes alpha, beta, and gamma during the initial steps of neural differentiation of PCC7 cells. Mol Endocrinol 2005 19: 1629 1645.
57. Kovalovsky D, Refojo D, Liberman AC, et al. Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: involvement of calcium, protein kinase A, and MAPK pathways. Mol Endocrinol 2002 16: 1638 1651.
58. Kim SY, Choi KC, Chang MS, et al. The dopamine D2 receptor regulates the development of dopaminergic neurons via extracellular signal-regulated kinase and Nurr1 activation. J Neurosci 2006 26: 4567 4576.
59. Arenas E. Stem cells in the treatment of Parkinson's disease. Brain Res Bull 2002 57: 795 808.
60. Vijayalaxmi, Thomas CR Jr., Reiter RJ, et al. Melatonin: from basic research to cancer treatment clinics. J Clin Oncol 2002 20: 2575 2601.
61. Sharma R, Mcmillan CR, Niles LP. Neural stem cell transplantation and melatonin treatment in a 6-hydroxydopamine model of Parkinson's disease. J Pineal Res 2007 43: 245 254.
62. Dubocovich ML, Markowska M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 2005 27: 101 110.
63. Srinivasan V, Pandi-Perumal S, Cardinali D, et al. Melatonin in Alzheimer's disease and other neurodegenerative disorders. Behav Brain Funct 2006 2: 15.
64. Etchegaray JP, Lee C, Wade PA, et al. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 2003 421: 177 182.
65. Naruse Y, Oh-Hashi K, Iijima N, et al. Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation. Mol Cell Biol 2004 24: 6278 6287.
66. Cano P, Poliandri AH, Jimenez V, et al. Cadmium-induced changes in Per 1 and Per 2 gene expression in rat hypothalamus and anterior pituitary: effect of melatonin. Toxicol Lett 2007 172: 131 136.
67. von Gall C, Weaver DR, Moek J, et al. Melatonin plays a crucial role in the regulation of rhythmic clock gene expression in the mouse pars tuberalis. Ann NY Acad Sci 2005 1040: 508 511.
68. Dong E, Guidotti A, Grayson DR, et al. Histone hyperacetylation induces demethylation of reelin and 67-kDa glutamic acid decarboxylase promoters. Proc Natl Acad Sci USA 2007 104: 4676 4681.
69. Chen PS, Peng GS, Li G, et al. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol Psychiatry 2006 11: 1116 1125.
70. Kim SJ, Lee BH, Lee YS, et al. Defective cholesterol traffic and neuronal differentiation in neural stem cells of Niemann-Pick type C disease improved by valproic acid, a histone deacetylase inhibitor. Biochem Biophys Res Commun 2007 360: 593 599.
71. Armstrong KJ, Niles LP. Induction of GDNF mRNA expression by melatonin in rat C6 glioma cells. Neuroreport 2002 13: 473 475.
72. Chen KB, Lin AM, Chiu TH. Oxidative injury to the locus coeruleus of rat brain: neuroprotection by melatonin. J Pineal Res 2003 35: 109 117.
73. Kong X, Li X, Cai Z, et al. Melatonin regulates the viability and differentiation of rat midbrain neural stem cells. Cell Mol Neurobiol 2007 [Epub ahead of print].
74. D'Alessio AC, Szyf M. Epigenetic tête-à-tête: the bilateral relationship between chromatin modifications and DNA methylation. Biochem Cell Biol 2006 84: 463 476.
75. Korkmaz A, Reiter RJ. Epigenetic regulation: a new research area for melatonin? J Pineal Res 2008 44: 41 44.