Melatonin potentiates running wheel-induced neurogenesis in the dentate gyrus of adult C3H/HeN mice hippocampus

Journal of Pineal Research

Volumn 54, Issue 2, 2013, Pages 222-231

  Liu, Jiabei ^a   Somera Molina, Kathleen C ^b,c   Hudson, Randall L ^a   Dubocovich, Margarita L ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ACORDA THERAPEUTICS INC   (United States)

Author keywords

C3H HeN mouse; cell proliferation; melatonin; melatonin receptors; neurogenesis; running wheel

Indexed keywords

MELATONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFICACY; HIPPOCAMPUS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; TREADMILL; TREADMILL EXERCISE; TREATMENT DURATION;

ANIMALS; BLOTTING, WESTERN; DENTATE GYRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MELATONIN; MICE; NEURALGIA; NEUROGENESIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS, SPRAGUE-DAWLEY;

EID: 84873424827     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12023     Document Type: Article

References (57)

1. Kempermann G, Kuhn HG, Gage FH,. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 1998; 18: 3206-3212.
2. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E,. Hippocampal neurogenesis in adult old world primates. Proc Natl Acad Sci USA 1999; 96: 5263-5267.
3. Kempermann G, Wiskott L, Gage FH,. Functional significance of adult neurogenesis. Curr Opin Neurobiol 2004; 14: 186-191.
4. Duman RS, Monteggia LM,. A neurotrophic model for stress-related mood disorders. Biol Psychiat 2006; 59: 1116-1127.
5. Jacobs BL, Van Praag H, Gage FH,. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatr 2000; 5: 262-269.
6. Kempermann G, Kronenberg G,. Depressed new neurons-adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biol Psychiat 2003; 54: 499-503.
7. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA,. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011; 476: 458-461.
8. Perera TD, Dwork AJ, Keegan KA, et al. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS ONE 2011; 6: 13.
9. Santarelli L, Saxe M, Gross C, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-809.
10. Boldrini M, Underwood MD, Hen R, et al. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacol 2009; 34: 2376-2389.
11. Pinnock SB, Blake AM, Platt NJ, Herbert J,. The roles of BDNF, pCREB and Wnt3a in the latent period preceding activation of progenitor cell mitosis in the adult dentate gyrus by fluoxetine. PLoS ONE 2010; 5.
12. Reiter RJ,. Pineal melatonin-cell biology of its synthesis and of its physiological interactions. Endocr Rev 1991; 12: 151-180.
13. Maronde E, Saade A, Ackermann K, et al. Dynamics in enzymatic protein complexes offer a novel principle for the regulation of melatonin synthesis in the human pineal gland. J Pineal Res 2011; 51: 145-155.
14. Dubocovich ML,. Melatonin receptors: role on sleep and circadian rhythm regulation. Sleep Med 2007; 8 (Suppl 3): 34-42.
15. Dubocovich ML, Markowska M,. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 2005; 27: 101-110.
16. Benloucif S, Dubocovich ML,. Melatonin and light induce phase shifts of circadian activity rhythms in the C3H/HeN mouse. J Biol Rhythms 1996; 11: 113-125.
17. Barrett P, Bolborea M,. Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin. J Pineal Res 2012; 52: 376-388.
18. Reiter RJ,. Oxidative damage in the central nervous system: Protection by melatonin. Prog Neurobiol 1998; 56: 359-384.
19. Reiter RJ, Tan DX, Manchester LC, Tamura H,. Melatonin defeats neurally-derived free radicals and reduces the associated neuromorphological and neurobehavioral damage. J Physiol Pharmacol 2007; 58: 5-22.
20. Musshoff U, Riewenherm D, Berger E, Fauteck JD, Speckmann EJ,. Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus 2002; 12: 165-173.
21. Moriya T, Horie N, Mitome M, Shinohara K,. Melatonin influences the proliferative and differentiative activity of neural stem cells. J Pineal Res 2007; 42: 411-418.
22. Kim MJ, Kim HK, Kim BS, Yim SV,. Melatonin increases cell proliferation in the dentate gyrus of maternally separated rats. J Pineal Res 2004; 37: 193-197.
23. Ramirez-Rodriguez G, Klempin F, Babu H, Benitez-King G, Kempermann G,. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacol 2009; 34: 2180-2191.
24. Ramirez-Rodriguez G, Ortiz-Lopez L, Dominguez-Alonso A, Benitez-King GA, Kempermann G,. Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J Pineal Res 2011; 50: 29-37.
25. Crupi R, Mazzon E, Marino A, et al. Melatonin's stimulatory effect on adult hippocampal neurogenesis in mice persists after ovariectomy. J Pineal Res 2011; 51: 353-360.
26. Overstreet DH, Pucilowski O, Retton MC, Delagrange P, Guardiola-Lemaitre B,. Effects of melatonin receptor ligands on swim test immobility. NeuroReport 1998; 9: 249-253.
27. Detanico BC, Piato AL, Freitas JJ, et al. Antidepressant-like effects of melatonin in the mouse chronic mild stress model. Eur J Pharmacol 2009; 607: 121-125.
28. Hirsch-Rodriguez E, Imbesi M, Manev R, Uz T, Manev H,. The pattern of melatonin receptor expression in the brain may influence antidepressant treatment. Med Hypotheses 2007; 69: 120-124.
29. Nair NPV, Hariharasubramanian N, Pilapil C,. Circadian-rhythm of plasma melatonin in endogenous-depression. Prog Neuropsychopharmacol Biol Psychiatry 1984; 8: 715-718.
30. Van Praag H, Christie BR, Sejnowski TJ, Gage FH,. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 1999; 96: 13427-13431.
31. Van Praag H, Kempermann G, Gage FH,. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2: 266-270.
32. Brown J, Cooper-Kuhn CM, Kempermann G, et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003; 17: 2042-2046.
33. Jeffrey SL, Johnson RA, Rhodes JS, Garland T, Mitchell GS,. Hippocampal brain-derived neurotrophic factor (BDNF) increases in mice artificially selected for increased voluntary wheel running. Faseb J 2001; 15: A428-A428.
34. Kempermann G, Kuhn HG, Gage FH,. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997; 386: 493-495.
35. Dranovsky A, Hen R,. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiat 2006; 59: 1136-1143.
36. Gould E, Tanapat P,. Stress and hippocampal neurogenesis. Biol Psychiat 1999; 46: 1472-1479.
37. Snyder JS, Glover LR, Sanzone KM, Kamhi JF, Cameron HA,. The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 2009; 19: 898-906.
38. Warner-Schmidt JL, Duman RS,. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 2006; 16: 239-249.
39. Holmes MM, Galea LAM, Mistlberger RE, Kempermann G,. Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J Neurosci Res 2004; 76: 216-222.
40. Hunt AE, Al-Ghoul WM, Gillette MU, Dubocovich ML,. Activation of MT(2) melatonin receptors in rat suprachiasmatic nucleus phase advances the circadian clock. Am J Physiol Cell Physiol 2001; 280: C110-C118.
41. Rawashdeh O, Hudson Rl, Stepien I, Dubocovich ML,. Circadian periods of sensitivity for ramelteon on the onset of running-wheel activity and the peak of suprachiasmatic nucleus neuronal firing rhythms in C3H/HeN mice. Chronobiol Int 2011; 28: 31-38.
42. Von Gall C, Lewy A, Schomerus C, et al. Transcription factor dynamics and neuroendocrine signalling in the mouse pineal gland: a comparative analysis of melatonin-deficient C57BL mice and melatonin-proficient C3H mice. Eur J Neurosci 2000; 12: 964-972.
43. Vivien-Roels B, Malan A, Rettori MC, Delagrange P, Jeanniot JP, Pevet P,. Daily variations in pineal melatonin concentrations in inbred and outbred mice. J Biol Rhythms 1998; 13: 403-409.
44. Cajochen C, Krauchi K, Vonarx MA, Mori D, Graw P, Wirzjustice A,. Daytime melatonin administration enhances sleepiness and theta/alpha activity in the waking EEG. Neurosci Lett 1996; 207: 209-213.
45. Rennie K, De Butte M, Pappas BA,. Melatonin promotes neurogenesis in dentate gyrus in the pinealectomized rat. J Pineal Res 2009; 47: 313-317.
46. Banasr M, Soumier A, Hery M, Mocaer E, Daszuta A,. Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis. Biol Psychiat 2006; 59: 1087-1096.
47. Soumier A, Banasr M, Lortet S, et al. Mechanisms contributing to the phase-dependent regulation of neurogenesis by the novel antidepressant, agomelatine, in the adult rat hippocampus. Neuropsychopharmacol 2009; 34: 2390-2403.
48. Racagni G, Riva MA, Molteni R, et al. Mode of action of agomelatine: synergy between melatonergic and 5-HT(2C) receptors. World J Biol Psychiatry 2011; 12: 574-587.
49. De Bodinat C, Guardiola-Lemaitre B, Mocaer E, Renard P, Munoz C, Millan MJ,. Case history agomelatine, the first melatonergic antidepressant: discovery, characterization and development. Nat Rev Drug Discov 2010; 9: 628-642.
50. Moser MB, Moser EI,. Functional differentiation in the hippocampus. Hippocampus 1998; 8: 608-619.
51. Reiter RJ, Tan DX, Mayo JC, Sainz RM, Lopez-Burillo S,. Melatonin, longevity and health in the aged: an assessment. Free Radical Res 2002; 36: 1323-1329.
52. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
53. Benitez-Kin G, Belon-Velasco A, Ramirez-Rodriguez G, Ortiz-Lopez L,. Melatonin stimulates RHO/ROCK activity downstream the PKC pathway and increases microtilament organization in growth cones in N1E-115 cells. Int J Dev Neurosci 2006; 24: 581-581.
54. Imbesi M, Uz T, Dzitoyeva S, Manev H,. Stimulatory effects of a melatonin receptor agonist, ramelteon, on BDNF in mouse cerebellar granule cells. Neurosci Lett 2008; 439: 34-36.
55. Duman RS,. Role of neurotrophic factors in the etiology and treatment of mood disorders. NeuroMol Med 2004; 5: 11-25.
56. Anacker C, Zunszain PA, Cattaneo A, et al. Antidepressants modulate human hippocampal neurogenesis by activating the glucocorticoid receptor. Eur Neuropsychopharmacol 2011; 21: S188-S189.
57. Anderson LB, Dwork AJ, Keegan KA, et al. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. Eur Neuropsychopharmacol 2011; 21: S417-S417.