Melatonin ameliorates dexamethasone-induced inhibitory effects on the proliferation of cultured progenitor cells obtained from adult rat hippocampus

Journal of Steroid Biochemistry and Molecular Biology

Volumn 145, Issue , 2015, Pages 38-48

  Ekthuwapranee, Kasima ^a   Sotthibundhu, Areechun ^b   Tocharus, Chainarong ^c   Govitrapong, Piyarat ^a,b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b Chiang Mai University ^*  (Thailand)

^c Faculty of Medicine Chiang Mai University   (Thailand)

Author keywords

Adult neurogenesis; Dexamethasone; Glucocorticoid; Melatonin; Proliferation; Stress

Indexed keywords

CYCLIN DEPENDENT KINASE 2; CYCLIN E; DEXAMETHASONE; GLUCOCORTICOID RECEPTOR; LUZINDOLE; MELATONIN; MELATONIN 1 RECEPTOR; MIFEPRISTONE; MITOGEN ACTIVATED PROTEIN KINASE 1; ANTIOXIDANT; GLUCOCORTICOID; MELATONIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE;

ADULT; ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; G1 PHASE CELL CYCLE CHECKPOINT; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MALE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; STEM CELL CULTURE; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL CYCLE; DRUG EFFECTS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHOSPHORYLATION; STEM CELL; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; DEXAMETHASONE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUCOCORTICOIDS; HIPPOCAMPUS; MALE; MELATONIN; NEUROGENESIS; NEURONS; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MELATONIN; STEM CELLS;

EID: 84908181395     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.10.003     Document Type: Article

References (82)

1. K.J. Anand, and D.B. Carr The neuroanatomy, neurophysiology, and neurochemistry of pain, stress, and analgesia in newborns and children Pediatr. Clin. North Am. 36 1989 795 822
2. M. Morimoto, N. Morita, H. Ozawa, K. Yokoyama, and M. Kawata Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study Neurosci. Res. 26 1996 235 269
3. R.G. Hunter, K.J. Mccarthy, T.A. Milne, D.W. Pfaff, and B.S. Mcewen Regulation of hippocampal H3 histone methylation by acute and chronic stress Proc. Nat. Acad. Sci. U. S. A. 106 2009 20912 20917
4. J. Veena, B.S. Rao, and B.N. Srikumar Regulation of adult neurogenesis in the hippocampus by stress, acetylcholine and dopamine J. Nat. Sci. Biol. Med. 2 2011 26 37
5. J.E. Malberg Implications of adult hippocampal neurogenesis in antidepressant action J. Psychiatry Neurosci. 29 2004 196 205
6. T.D. Perera, J.D. Coplan, S.H. Lisanby, C.M. Lipira, M. Arif, C. Carpio, G. Spitzer, L. Santarelli, B. Scharf, R. Hen, G. Rosoklija, H.A. Sackeim, and A.J. Dwork Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates J. Neurosci. 27 2007 4894 4901
7. R.N. Pechnick, S. Zonis, K. Wawrowsky, R. Cosgayon, C. Farrokhi, L. Lacayo, and V. Chesnokova Antidepressants stimulate hippocampal neurogenesis by inhibiting p21 expression in the subgranular zone of the hipppocampus PLoS One 6 2011 e27290
8. M. Aboukhatwa, L. Dosanjh, and Y. Luo Antidepressants are a rational complementary therapy for the treatment of Alzheimer's disease Mol. Neurodegener. 5 2010 10
9. G. Jean-Louis, H. Von Gizycki, and F. Zizi Melatonin effects on sleep, mood, and cognition in elderly with mild cognitive impairment J. Pineal Res. 25 1998 177 183
10. V. Srinivasan, D. De Berardis, S.D. Shillcutt, and A. Brzezinski Role of melatonin in mood disorders and the antidepressant effects of agomelatine Expert Opin. Invest. Drugs 21 2012 1503 1522
11. E. Kilic, U. Kilic, M. Bacigaluppi, Z. Guo, N.B. Abdallah, D.P. Wolfer, R.J. Reiter, D.M. Hermann, and C.L. Bassetti Delayed melatonin administration promotes neuronal survival, neurogenesis and motor recovery, and attenuates hyperactivity and anxiety after mild focal cerebral ischemia in mice J. Pineal Res. 45 2008 142 148
12. G. Ramirez-Rodriguez, F. Klempin, H. Babu, G. Benitez-King, and G. Kempermann Melatonin modulates cell survival of new neurons in the hippocampus of adult mice Neuropsychopharmacology 34 2009 2180 2191
13. M.J. Kim, H.K. Kim, B.S. Kim, and S.V. Yim Melatonin increases cell proliferation in the dentate gyrus of maternally separated rats J. Pineal Res. 37 2004 193 197
14. I. Quiros, J.C. Mayo, O. Garcia-Suarez, D. Hevia, V. Martin, C. Rodriguez, and R.M. Sainz Melatonin prevents glucocorticoid inhibition of cell proliferation and toxicity in hippocampal cells by reducing glucocorticoid receptor nuclear translocation J. Steroid Biochem. Mol. Biol. 110 2008 116 124
15. W. Tongjaroenbuangam, N. Ruksee, T. Mahanam, and P. Govitrapong Melatonin attenuates dexamethasone-induced spatial memory impairment and dexamethasone-induced reduction of synaptic protein expressions in the mouse brain Neurochem. Int. 63 2013 482 491
16. N. Ruksee, W. Tongjaroenbuangam, T. Mahanam, and P. Govitrapong Melatonin pretreatment prevented the effect of dexamethasone negative alterations on behavior and hippocampal neurogenesis in the mouse brain J. Steroid Biochem. Mol. Biol. 143C 2014 72 80
17. C. Tocharus, Y. Puriboriboon, T. Junmanee, J. Tocharus, K. Ekthuwapranee, and P. Govitrapong Melatonin enhances adult rat hippocampal progenitor cell proliferation via ERK signaling pathway through melatonin receptor Neuroscience 275 2014 314 321
18. O.N. Suslov, V.G. Kukekov, T.N. Ignatova, and D.A. Steindler Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres Proc. Nat. Acad. Sci. U. S. A. 99 2002 14506 14511
19. D. Park, A.P. Xiang, F.F. Mao, L. Zhang, C.G. Di, X.M. Liu, Y. Shao, B.F. Ma, J.H. Lee, K.S. Ha, N. Walton, and B.T. Lahn Nestin is required for the proper self-renewal of neural stem cells Stem Cells 28 2010 2162 2171
20. M.S. Rao, and A.K. Shetty Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus Eur. J. Neurosci. 19 2004 234 246
21. N. Kee, S. Sivalingam, R. Boonstra, and J.M. Wojtowicz The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis J. Neurosci. Methods 115 2002 97 105
22. Y. Mebratu, and Y. Tesfaigzi How ERK1/2 activation controls cell proliferation and cell death: is subcellular localization the answer? Cell Cycle 8 2009 1168 1175
23. B. Amati, K. Alevizopoulos, and J. Vlach Myc and the cell cycle Front. Biosci. 3 1998 d250 d268
24. Z. Jin, F. Gao, T. Flagg, and X. Deng Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes functional cooperation of Bcl2 and c-Myc through phosphorylation in regulating cell survival and proliferation J. Biol. Chem. 279 40 2004 40209 40219
25. G. Ramirez-Rodriguez, N.M. Vega-Rivera, G. Benitez-King, M. Castro-Garcia, and L. Ortiz-Lopez Melatonin supplementation delays the decline of adult hippocampal neurogenesis during normal aging of mice Neurosci. Lett. 530 2012 53 58
26. G. Ramirez-Rodriguez, N.M. Vega-Rivera, J. Oikawa-Sala, A. Gomez-Sanchez, L. Ortiz-Lopez, and E. Estrada-Camarena Melatonin synergizes with citalopram to induce antidepressant-like behavior and to promote hippocampal neurogenesis in adult mice J. Pineal Res. 56 2014 450 461
27. K. Rennie, M. De Butte, and B.A. Pappas Melatonin promotes neurogenesis in dentate gyrus in the pinealectomized rat J. Pineal Res. 47 2009 313 317
28. J. Ray, and F.H. Gage Differential properties of adult rat and mouse brain-derived neural stem/progenitor cells Mol. Cell. Neurosci. 31 2006 560 573
29. T. Kasahara, K. Abe, K. Mekada, A. Yoshiki, and T. Kato Genetic variation of melatonin productivity in laboratory mice under domestication Proc. Nat. Acad. Sci. U. S. A. 107 2010 6412 6417
30. I. Amrein, K. Isler, and H.P. Lipp Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage Eur. J. Neurosci. 34 2011 978 987
31. C. Anacker, P.A. Zunszain, A. Cattaneo, L.A. Carvalho, M.J. Garabedian, S. Thuret, J. Price, and C.M. Pariante Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor Mol. Psychiatry 16 2011 738 750
32. R. Crupi, E. Mazzon, A. Marino, G. La Spada, P. Bramanti, E. Spina, and S. Cuzzocrea Melatonin's stimulatory effect on adult hippocampal neurogenesis in mice persists after ovariectomy J. Pineal Res. 51 2011 353 360
33. J. Liu, K.C. Somera-Molina, R.L. Hudson, and M.L. Dubocovich Melatonin potentiates running wheel-induced neurogenesis in the dentate gyrus of adult C3H/HeN mice hippocampus J. Pineal Res. 54 2013 222 231
34. K. Manda, and R.J. Reiter Melatonin maintains adult hippocampal neurogenesis and cognitive functions after irradiation Prog. Neurobiol. 90 2010 60 68
35. T. Moriya, N. Horie, M. Mitome, and K. Shinohara Melatonin influences the proliferative and differentiative activity of neural stem cells J. Pineal Res. 42 2007 411 418
36. L. Sommer, and M. Rao Neural stem cells and regulation of cell number Prog. Neurobiol. 66 2002 1 18
37. X.B. Yan, H.L. Hou, L.M. Wu, J. Liu, and J.N. Zhou Lithium regulates hippocampal neurogenesis by ERK pathway and facilitates recovery of spatial learning and memory in rats after transient global cerebral ischemia Neuropharmacology 53 2007 487 495
38. A. Seth, F.A. Gonzalez, S. Gupta, D.L. Raden, and R.J. Davis Signal transduction within the nucleus by mitogen-activated protein kinase J. Biol. Chem. 267 1992 24796 24804
39. S. Meloche, and J. Pouyssegur The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition Oncogene 26 2007 3227 3239
40. O. Kassel, A. Sancono, J. Kratzschmar, B. Kreft, M. Stassen, and A.C. Cato Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1 EMBO J. 20 2001 7108 7116
41. M. Leskiewicz, D. Jantas, M. Regulska, J. Kaczanowska, A. Basta-Kaim, B. Budziszewska, M. Kubera, and W. Lason Antidepressants attenuate the dexamethasone-induced decrease in viability and proliferation of human neuroblastoma SH-SY5Y cells: a involvement of extracellular regulated kinase (ERK1/2) Neurochem. Int. 63 2013 354 362
42. C. Von Gall, J.H. Stehle, and D.R. Weaver Mammalian melatonin receptors: molecular biology and signal transduction Cell Tissue Res. 309 2002 151 162
43. L. Brydon, F. Roka, L. Petit, P. De Coppet, M. Tissot, P. Barrett, P.J. Morgan, C. Nanoff, A.D. Strosberg, and R. Jockers Dual signaling of human Mel1a melatonin receptors via G(i2), G(i3), and G(q/11) proteins Mol. Endocrinol. 13 1999 2025 2038
44. A.S. Chan, F.P. Lai, R.K. Lo, T.A. Voyno-Yasenetskaya, E.J. Stanbridge, and Y.H. Wong Melatonin mt1 and MT2 receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins Cell. Signal. 14 2002 249 257
45. M.L. Dubocovich, M.A. Rivera-Bermudez, M.J. Gerdin, and M.I. Masana Molecular pharmacology, regulation and function of mammalian melatonin receptors Front. Biosci. 8 2003 d1093 d1108
46. L. Li, J.N. Xu, Y.H. Wong, J.T. Wong, S.F. Pang, and S.Y. Shiu Molecular and cellular analyses of melatonin receptor-mediated cAMP signaling in rat corpus epididymis J. Pineal Res. 25 1998 219 228
47. S. Carbajo-Pescador, A. Garcia-Palomo, J. Martin-Renedo, M. Piva, J. Gonzalez-Gallego, and J.L. Mauriz Melatonin modulation of intracellular signaling pathways in hepatocarcinoma HepG2 cell line: role of the MT1 receptor J. Pineal Res. 51 2011 463 471
48. G. Pearson, F. Robinson, T. Beers Gibson, B.E. Xu, M. Karandikar, K. Berman, and M.H. Cobb Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions Endocr. Rev. 22 2001 153 183
49. P.A. Witt-Enderby, J. Bennett, M.J. Jarzynka, S. Firestine, and M.A. Melan Melatonin receptors and their regulation: biochemical and structural mechanisms Life Sci. 72 2003 2183 2198
50. M.L. Dubocovich, P. Delagrange, D.N. Krause, D. Sugden, and D.P.J. Cardinali Olcese International union of basic and clinical pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors Pharmacol. Rev. 62 2010 343 380
51. M. Markowska, A. Mrozkowiak, J. Pawlak, and K. Skwarlo-Sonta Intracellular second messengers involved in melatonin signal transduction in chicken splenocytes in vitro J. Pineal Res. 37 2004 207 212
52. M. Natarajan, R.J. Reiter, M.L. Meltz, and T.S. Herman Effect of melatonin on cell growth, metabolic activity, and cell cycle distribution J. Pineal Res. 31 2001 228 233
53. J. Lu The anti-proliferation mechanism of glucocorticoid mediated by glucocorticoid receptor-regulating gene expression Pathophysiology 16 2009 267 272
54. D.J. Saaltink, and E. Vreugdenhil Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition? Cell. Mol. Life Sci. 2014
55. N. Froger, E. Palazzo, C. Boni, N. Hanoun, F. Saurini, C. Joubert, I. Dutriez-Casteloot, M. Enache, S. Maccari, N. Barden, C. Cohen-Salmon, M. Hamon, and L. Lanfumey Neurochemical and behavioral alterations in glucocorticoid receptor-impaired transgenic mice after chronic mild stress J. Neurosci. 24 2004 2787 2796
56. F. Holsboer The corticosteroid receptor hypothesis of depression Neuropsychopharmacology 23 2000 477 501
57. I. Liberzon, J.F. Lopez, S.B. Flagel, D.M. Vazquez, and E.A. Young Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: relevance to post-traumatic stress disorder J. Neuroendocrinol. 11 1999 11 17
58. B. Li, X. Bai, and H. Wanh Effect of dexamethasone on expression of glucocorticoid receptor in human monocyte cell line THP-1 J. Huazhong Univ. Sci. Technol. Med. Sci. 26 2006 25 27
59. R.M. Sainz, J.C. Mayo, R.J. Reiter, I. Antolin, M.M. Esteban, and C. Rodriguez Melatonin regulates glucocorticoid receptor: an answer to its antiapoptotic action in thymus FASEB J. 13 1999 1547 1556
60. T.L. Kiefer, L. Lai, L. Yuan, C. Dong, M.E. Burow, and S.M. Hill Differential regulation of estrogen receptor alpha, glucocorticoid receptor and retinoic acid receptor alpha transcriptional activity by melatonin is mediated via different G proteins J. Pineal Res. 38 2005 231 239
61. S.P. Persengiev Multiple domains of melatonin receptor are involved in the regulation of glucocorticoid receptor-induced gene expression J. Steroid Biochem. Mol. Biol. 68 1999 181 187
62. Y.H. Wu, J. Ursinus, J.N. Zhou, F.A. Scheer, B. Ai-Min, R. Jockers, J. Van Heerikhuize, and D.F. Swaab Alterations of melatonin receptors MT1 and MT2 in the hypothalamic suprachiasmatic nucleus during depression J. Affective Disord. 148 2013 357 367
63. S. Gupta, and C. Haldar Physiological crosstalk between melatonin and glucocorticoid receptor modulates T-cell mediated immune responses in a wild tropical rodent, Funambulus pennanti J. Steroid Biochem. Mol. Biol. 134 2013 23 36
64. M. Imbesi, T. Uz, S. Yildiz, A.D. Arslan, and H. Manev Drug- and region-specific effects of protracted antidepressant and cocaine treatment on the content of melatonin MT(1) and MT(2) receptor mRNA in the mouse brain Int. J. Neuroprot. Neuroregener. 2 2006 185 189
65. A. Sotthibundhu, P. Phansuwan-Pujito, and P. Govitrapong Melatonin increases proliferation of cultured neural stem cells obtained from adult mouse subventricular zone J. Pineal Res. 49 2010 291 300
66. A. Garcia, B. Steiner, G. Kronenberg, A. Bick-Sander, and G. Kempermann Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus Aging Cell. 3 2004 363 371
67. S. Boku, S. Nakagawa, T. Masuda, H. Nishikawa, A. Kato, Y. Kitaichi, T. Inoue, and T. Koyama Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3beta and beta-catenin/TCF pathway Neuropsychopharmacology 34 2009 805 815
68. C. Anacker, A. Cattaneo, A. Luoni, K. Musaelyan, P.A. Zunszain, E. Milanesi, J. Rybka, A. Berry, F. Cirulli, S. Thuret, J. Price, M.A. Riva, M. Gennarelli, and C.M. Pariante Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis Neuropsychopharmacology 38 2013 872 883
69. E.Y. Wong, and J. Herbert Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus Eur. J. Neurosci. 22 2005 785 792
70. U. Musshoff, D. Riewenherm, E. Berger, J.D. Fauteck, and E.J. Speckmann Melatonin receptors in rat hippocampus: molecular and functional investigations Hippocampus 12 2002 165 173
71. L.P. Niles, K.J. Armstrong, L.M. Rincon Castro, C.V. Dao, R. Sharma, C.R. Mcmillan, L.C. Doering, and D.L. Kirkham Neural stem cells express melatonin receptors and neurotrophic factors: colocalization of the MT1 receptor with neuronal and glial markers BMC Neurosci. 5 2004 41
72. R. Sharma, T. Ottenhof, P.A. Rzeczkowska, and L.P. Niles Epigenetic targets for melatonin: induction of histone H3 hyperacetylation and gene expression in C17.2 neural stem cells J. Pineal Res. 45 2008 277 284
73. V.A. Doze, and D.M. Perez G-protein-coupled receptors in adult neurogenesis Pharmacol. Rev. 64 2012 645 675
74. J. Fu, S.D. Zhao, H.J. Liu, Q.H. Yuan, S.M. Liu, Y.M. Zhang, E.A. Ling, and A.J. Hao Melatonin promotes proliferation and differentiation of neural stem cells subjected to hypoxia in vitro J. Pineal Res. 51 2011 104 112
75. W.A. Gern, and C.L. Ralph Melatonin synthesis by the retina Science 204 1979 183 184
76. A. Carrillo-Vico, J.R. Calvo, P. Abreu, P.J. Lardone, S. Garcia-Maurino, R.J. Reiter, and J.M. Guerrero Evidence of melatonin synthesis by human lymphocytes and its physiological significance: possible role as intracrine autocrine, and/or paracrine substance FASEB J. 18 2004 537 539
77. Y.J. Liu, J. Zhuang, H.Y. Zhu, Y.X. Shen, Z.L. Tan, and J.N. Zhou Cultured rat cortical astrocytes synthesize melatonin: absence of a diurnal rhythm J. Pineal Res. 43 2007 232 238
78. G. Anderson, and M. Maes Local melatonin regulates inflammation resolution: a common factor in neurodegenerative, psychiatric and systemic inflammatory disorders CNS Neurol. Disord. Drug Targets 13 2014 817 827
79. F.W. Wang, H.B. Hao, S.D. Zhao, Y.M. Zhang, Q. Liu, H.J. Liu, S.M. Liu, Q.H. Yuan, L.J. Bing, E.A. Ling, and A.J. Hao Roles of activated astrocyte in neural stem cell proliferation and differentiation Stem Cell Res. 7 2011 41 53
80. G. Anderson, and M. Maes Reconceptualizing adult neurogenesis: role for sphingosine-1-phosphate and fibroblast growth factor-1 in co-ordinating astrocyte-neuronal precursor interactions CNS Neurol. Disord. Drug Targets 13 2014 126 136
81. V.S. Caviness Jr., T. Takahashi, and R.S. Nowakowski Neuronogenesis and the early events of neocortical histogenesis Results Prob. Cell Differ. 30 2000 107 143
82. W. Deng, J.B. Aimone, and F.H. Gage New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11 2010 339 350