Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice

Journal of Pineal Research

Volumn 50, Issue 1, 2011, Pages 29-37

  Ramirez Rodriguez, Gerardo ^a   Ortíz Lõpez, Leonardo ^a   Domínguez Alonso, Aline ^a   Benítez King, Gloria A ^a   Kempermann, Gerd ^b  

^a INSTITUTO NACIONAL DE PSIQUIATRÍA RAMÓN DE LA FUENTE MUÑIZ   (Mexico)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

adult neurogenesis; cytoskeleton; dendrites; doublecortin; melatonin

Indexed keywords

DOUBLECORTIN; MELATONIN;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL POPULATION; CONTROLLED STUDY; DEMENTIA; DENDRITE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROTUBULE ASSEMBLY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; DENDRITES; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MELATONIN; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEUROGENESIS; NEURONS; NEUROPEPTIDES;

EID: 78650117283     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2010.00802.x     Document Type: Article

References (50)

1. Ming GL, Song H,. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28: 223-250.
2. Kempermann G, Jessberger S, Steiner B, et al. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27: 447-452.
3. Kuhn HG, Dickinson-Anson H, Gage FH,. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16: 2027-2033.
4. Kempermann G, Kronenberg G,. Depressed new neurons-adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biol Psychiatry 2003; 54: 499-503.
5. Kempermann G, Krebs J, Fabel K,. The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr Opin Psychiatry 2008; 21: 290-295.
6. Kempermann G, Chesler EJ, Lu L, et al. Natural variation and genetic covariance in adult hippocampal neurogenesis. Proc Natl Acad Sci U S A 2006; 103: 780-785.
7. Gould E, Beylin A, Tanapat P, et al. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999; 2: 260-265. (Pubitemid 30491297)
8. Fabel K, Kempermann G,. Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromol Med 2008; 10: 59-66.
9. Ramirez-Rodriguez G, Klempin F, Babu H, et al. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 2009; 34: 2180-2191.
10. Plumpe T, Ehninger D, Steiner B, et al. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 2006; 7: 77.
11. Ge S, Yang CH, Hsu KS, et al. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 2007; 54: 559-566.
12. Ma DK, Kim WR, Ming GL, et al. Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann N Y Acad Sci 2009; 1170: 664-673.
13. Zhao C, Teng EM, Summers RG Jr, et al. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006; 26: 3-11.
14. Deuel TA, Liu JS, Corbo JC, et al. Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006; 49: 41-53.
15. Brandt MD, Jessberger S, Steiner B, et al. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 2003; 24: 603-613.
16. Filippov V, Kronenberg G, Pivneva T, et al. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 2003; 23: 373-382.
17. Huerto-Delgadillo L, Anton-Tay F, Benitez-King G,. Effects of melatonin on microtubule assembly depend on hormone concentration: role of melatonin as a calmodulin antagonist. J Pineal Res 1994; 17: 55-62.
18. Benitez-King G,. Melatonin as a cytoskeletal modulator: implications for cell physiology and disease. J Pineal Res 2006; 40: 1-9.
19. Bellon A, Ortiz-Lopez L, Ramirez-Rodriguez G, et al. Melatonin induces neuritogenesis at early stages in N1E-115 cells through actin rearrangements via activation of protein kinase C and Rho-associated kinase. J Pineal Res 2007; 42: 214-221.
20. Reiter RJ,. Oxidative damage in the central nervous system: protection by melatonin. Prog Neurobiol 1998; 56: 359-384.
21. Reiter RJ,. Melatonin, active oxygen species and neurological damage. Drug News Perspect 1998; 11: 291-296.
22. Peyrot F, Ducrocq C,. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008; 45: 235-246.
23. Hardeland R, Tan DX, Reiter RJ,. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009; 47: 109-126.
24. Reiter RJ, Paredes SD, Manchester LC, et al. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit Rev Biochem Mol Biol 2009; 44: 175-200.
25. Liu RY, Zhou JN, Van Heerikhuize J, et al. Decreased melatonin levels in postmortem cerebrospinal fluid in relation to aging, Alzheimer's disease, and apolipoprotein E-epsilon4/4 genotype. J Clin Endocrinol Metab 1999; 84: 323-327.
26. Brusco LI, Marquez M, Cardinali DP,. Melatonin treatment stabilizes chronobiologic and cognitive symptoms in Alzheimer's disease. Neuro Endocrinol Lett 2000; 21: 39-42.
27. Kilic E, Kilic U, Bacigaluppi M, et al. 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 2008; 45: 142-148.
28. Rennie K, De Butte M, Pappas BA,. Melatonin promotes neurogenesis in dentate gyrus in the pinealectomized rat. J Pineal Res 2009; 47: 313-317.
29. Manda K, Ueno M, Anzai K,. Cranial irradiation-induced inhibition of neurogenesis in hippocampal dentate gyrus of adult mice: attenuation by melatonin pretreatment. J Pineal Res 2009; 46: 71-78.
30. Manda K, Ueno M, Anzai K,. Space radiation-induced inhibition of neurogenesis in the hippocampal dentate gyrus and memory impairment in mice: ameliorative potential of the melatonin metabolite, AFMK. J Pineal Res 2008; 45: 430-438.
31. Chen HY, Hung YC, Chen TY, et al. Melatonin improves presynaptic protein, SNAP-25, expression and dendritic spine density and enhances functional and electrophysiological recovery following transient focal cerebral ischemia in rats. J Pineal Res 2009; 47: 260-270.
32. Gomez-Corvera A, Cerrillo I, Molinero P, et al. Evidence of immune system melatonin production by two pineal melatonin deficient mice, C57BL/6 and Swiss strains. J Pineal Res 2009; 47: 15-22.
33. Reiter RJ, Tan DX, Qi W, et al. Pharmacology and physiology of melatonin in the reduction of oxidative stress in vivo. Biol Signals Recept 2000; 9: 160-171.
34. Kempermann G, Gast D, Kronenberg G, et al. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003; 130: 391-399.
35. Revest JM, Dupret D, Koehl M, et al. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 2009; 14: 959-967.
36. Redwine JM, Kosofsky B, Jacobs RE, et al. Dentate gyrus volume is reduced before onset of plaque formation in PDAPP mice: a magnetic resonance microscopy and stereologic analysis. Proc Natl Acad Sci U S A 2003; 100: 1381-1386.
37. 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. Neuropsychopharmacology 2009; 34: 2390-2403.
38. Da Silva JS, Dotti CG,. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 2002; 3: 694-704.
39. 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.
40. Ramirez-Rodriguez G, Ortiz-Lopez L, Benitez-King G,. Melatonin increases stress fibers and focal adhesions in MDCK cells: participation of Rho-associated kinase and protein kinase C. J Pineal Res 2007; 42: 180-190.
41. Babu H, Ramirez-Rodriguez G, Fabel K, et al. Synaptic network activity induces neuronal differentiation of adult hippocampal precursor cells through BDNF signaling. Front Neurosci 2009; 1: 1-49.
42. Barnabe-Heider F, Miller FD,. Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J Neurosci 2003; 23: 5149-5160.
43. Lee J, Duan W, Mattson MP,. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 2002; 82: 1367-1375.
44. Imbesi M, Uz T, Manev H,. Role of melatonin receptors in the effects of melatonin on BDNF and neuroprotection in mouse cerebellar neurons. J Neural Transm 2008; 115: 1495-1499.
45. Sapolsky RM,. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 2000; 57: 925-935.
46. West MJ, Kawas CH, Stewart WF, et al. Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 2004; 25: 1205-1212.
47. Garcia-Chavez D, Gonzalez-Burgos I, Letechipia-Vallejo G, et al. Long-term evaluation of cytoarchitectonic characteristics of prefrontal cortex pyramidal neurons, following global cerebral ischemia and neuroprotective melatonin treatment, in rats. Neurosci Lett 2008; 448: 148-152.
48. De Butte M, Pappas BA,. Pinealectomy causes hippocampal CA1 and CA3 cell loss: reversal by melatonin supplementation. Neurobiol Aging 2007; 28: 306-313.
49. Gonzalez-Burgos I, Letechipia-Vallejo G, Lopez-Loeza E, et al. Long-term study of dendritic spines from hippocampal CA1 pyramidal cells, after neuroprotective melatonin treatment following global cerebral ischemia in rats. Neurosci Lett 2007; 423: 162-166.
50. Letechipia-Vallejo G, Lopez-Loeza E, Espinoza-Gonzalez V, et al. Long-term morphological and functional evaluation of the neuroprotective effects of post-ischemic treatment with melatonin in rats. J Pineal Res 2007; 42: 138-146.