Melatonin increases dendritogenesis in the hilus of hippocampal organotypic cultures

Journal of Pineal Research

Volumn 52, Issue 4, 2012, Pages 427-436

  Dominguez Alonso A ^a   Ramirez Rodriguez G ^a   Benitez King G ^a  

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

Author keywords

dendritogenesis; hippocampus; melatonin; synapses

Indexed keywords

MELATONIN; SCAVENGER;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL GROWTH; CELL LOSS; CELL MATURATION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; RAT;

ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MELATONIN; NEUROGENESIS; RATS; RATS, WISTAR; SYNAPSES; VESICULAR TRANSPORT PROTEINS;

EID: 84859724554     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00957.x     Document Type: Article

References (77)

1. Kempton MJ, Salvador Z, Munafo MR, et al., Structural neuroimaging studies in major depressive disorder: meta-analysis and comparison with bipolar disorder. Arch Gen Psychiatry 2011; 68: 675-690.
2. Blumberg HP, Kaufman J, Martin A, et al., Amygdala and hippocampal volumes in adolescents and adults with bipolar disorder. Arch Gen Psychiatry 2003; 60: 1201-1208.
3. Thompson PM, Hayashi KM, De Zubicaray G, et al., Dynamics of gray matter loss in Alzheimer's disease. J Neurosci 2003; 23: 994-1005.
4. Narr KL, Van Erp TG, Cannon TD, et al., A twin study of genetic contributions to hippocampal morphology in schizophrenia. Neurobiol Dis 2002; 11: 83-95.
5. Rosoklija G, Toomayan G, Ellis SP, et al., Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 2000; 57: 349-356.
6. Arnold SE, Lee VM, Gur RE, Trojanowski JQ,. Abnormal expression of two microtubule-associated proteins (MAP2 and MAP5) in specific subfields of the hippocampal formation in schizophrenia. Proc Natl Acad Sci U S A 1991; 88: 10850-10854.
7. Buell SJ, Coleman PD,. Dendritic growth in the aged human brain and failure of growth in senile dementia. Science 1979; 206: 854-856.
8. Yamada M, Wada Y, Tsukagoshi H, Otomo E, Hayakawa M,. A quantitative Golgi study of basal dendrites of hippocampal CA1 pyramidal cells in senile dementia of Alzheimer type. J Neurol Neurosurg Psychiatry 1988; 51: 1088-1090.
9. Stone WS, Hsi X,. Declarative memory deficits and schizophrenia: problems and prospects. Neurobiol Learn Mem 2011; 96: 544-552.
10. Bearden CE, Woogen M, Glahn DC,. Neurocognitive and neuroimaging predictors of clinical outcome in bipolar disorder. Curr Psychiatry Rep 2010; 12: 499-504.
11. Murrough JW, Iacoviello B, Neumeister A, Charney DS, Iosifescu DV,. Cognitive dysfunction in depression: neurocircuitry and new therapeutic strategies. Neurobiol Learn Mem 2011; 96: 553-563.
12. Kurtz MM, Gerraty RT,. A meta-analytic investigation of neurocognitive deficits in bipolar illness: profile and effects of clinical state. Neuropsychology 2009; 23: 551-562.
13. West MJ, Coleman PD, Flood DG, Troncoso JC,. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994; 344: 769-772.
14. West MJ, Kawas CH, Stewart WF, Rodow GL, Troncoso JC,. Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 2004; 25: 1205-1212.
15. West MJ,. Regionally specific loss of neurons in the aging human hippocampus. Neurobiol Aging 1993; 14: 287-293.
16. Neves G, Cooke SF, Bliss TV,. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci, 2008; 9: 65-75.
17. Van Strien NM, Cappaert NL, Witter MP,. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 2009; 10: 272-282.
18. Amaral DG,. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 1978; 182: 851-914.
19. Amaral DG, Scharfman HE, Lavenex P,. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 2007; 163: 3-22.
20. Myers CE, Scharfman HE,. A role for hilar cells in pattern separation in the dentate gyrus: a computational approach. Hippocampus 2009; 19: 321-337.
21. Gilbert PE, Brushfield AM,. The role of the CA3 hippocampal subregion in spatial memory: a process oriented behavioral assessment. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33: 774-781.
22. Xavier GF, Costa VC,. Dentate gyrus and spatial behaviour. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33: 762-773.
23. Wong RO, Ghosh A,. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 2002; 3: 803-812.
24. Da Silva JS, Dotti CG,. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 2002; 3: 694-704.
25. Dailey ME, Smith SJ,. The dynamics of dendritic structure in developing hippocampal slices. J Neurosci 1996; 16: 2983-2994.
26. Scott EK, Luo L,. How do dendrites take their shape?. Nat Neurosci 2001; 4: 359-365.
27. Baas PW, Black MM, Banker GA,. Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J Cell Biol 1989; 109: 3085-3094.
28. Wuerker RB, Kirkpatrick JB,. Neuronal microtubules, neurofilaments and microfilaments. In: International Review of Cytology, Bourne GH, Dianielli JF, eds., Elsevier, Academic Press Inc., New York, USA, 1972; pp. 45-70.
29. Forehand CJ,. The action potential, synaptic transmission, and maintenance of nerve function. In: Medical Physiology: Principles for Clinical Medicine, Rhoades RA, Bell DR, eds., Lippincott Williams & Wilkins, a Wolters Kluwer business, Philadelphia, USA, 2009; pp. 38-64.
30. Caceres A, Banker GA, Binder L,. Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J Neurosci 1986; 6: 714-722.
31. Sanchez C, Diaz-Nido J, Avila J,. Phosphorylation of microtubule- associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol 2000; 61: 133-168.
32. Tan DX, Chen LD, Poeggeler B, Manchester LC, Reiter RJ,. Melatonin: a potent endogenous hydroxyl radical scavenger. Endrocr J 1993; 1: 57-60.
33. Paradies G, Petrosillo G, Paradies V, Reiter RJ, Ruggiero FM,. Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res 2010; 48: 297-310.
34. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
35. De Butte M, Pappas BA,. Pinealectomy causes hippocampal CA1 and CA3 cell loss: reversal by melatonin supplementation. Neurobiol Aging 2007; 28: 306-313.
36. Masilamoni JG, Jesudason EP, Dhandayuthapani S, et al., The neuroprotective role of melatonin against amyloid beta peptide injected mice. Free Radic Res 2008; 42: 661-673.
37. Chang HM, Wu UI, Lan CT,. Melatonin preserves longevity protein (sirtuin 1) expression in the hippocampus of total sleep-deprived rats. J Pineal Res 2009; 47: 211-220.
38. Gonzalez-Burgos I, Letechipia-Vallejo G, Lopez-Loeza E, Morali G, Cervantes M,. 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.
39. Garcia-Chavez D, Gonzalez-Burgos I, Letechipia-Vallejo G, Loacute;pez-Loeza E, Moralí G, Cervantes M,. 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.
40. Pascual R, Bustamante C,. Melatonin promotes distal dendritic ramifications in layer II/III cortical pyramidal cells of rats exposed to toluene vapors. Brain Res 2010; 1355: 214-220.
41. Bellon A, Ortiz-Lopez L, Ramirez-Rodriguez G, Antoacute;n-Tay F, Benítez-King G,. 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.
42. Ramirez-Rodriguez G, Ortiz-Lopez L, Dominguez-Alonso A, Benítez-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.
43. Pichugin Y, Fahy GM, Morin R,. Cryopreservation of rat hippocampal slices by vitrification. Cryobiology 2006; 52: 228-240.
44. Stoppini L, Buchs PA, Muller D,. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991; 37: 173-182.
45. Prieto-Gomez B, Velazquez-Paniagua M, Cisneros LO, et al., Melatonin attenuates the decrement of dendritic protein MAP-2 immuno-staining in the hippocampal CA1 and CA3 fields of the aging male rat. Neurosci Lett 2008; 448: 56-61.
46. Sholl DA,. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 1953; 87: 387-406.
47. Calhoun ME, Jucker M, Martin LJ, Thinakaran G, Price DL, Mouton PR,. Comparative evaluation of synaptophysin-based methods for quantification of synapses. J Neurocytol 1996; 25: 821-828.
48. Noraberg J, Poulsen FR, Blaabjerg M, et al., Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr Drug Targets CNS Neurol Disord 2005; 4: 435-452.
49. Cho S, Wood A, Bowlby MR,. Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr Neuropharmacol 2007; 5: 19-33.
50. Ortiz GG, Sanchez-Ruiz Y, Tan DX, Reiter RJ, Benítez-King G, Beas-Zárate C,. Melatonin, vitamin E, and estrogen reduce damage induced by kainic acid in the hippocampus: potassium-stimulated GABA release. J Pineal Res 2001; 31: 62-67.
51. Tran TS, Rubio ME, Clem RL, et al., Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 2009; 462: 1065-1069.
52. Ji Y, Lu Y, Yang F, et al., Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat Neurosci 2010; 13: 302-309.
53. Wang ZJ, Liang CL, Li GM, Yu CY, Yin M,. Neuroprotective effects of arachidonic acid against oxidative stress on rat hippocampal slices. Chem Biol Interact 2006; 163: 207-217.
54. Galimberti I, Gogolla N, Alberi S, Santos AF, Muller D, Caroni P,. Long-term rearrangements of hippocampal mossy fiber terminal connectivity in the adult regulated by experience. Neuron 2006; 50: 749-763.
55. Gogolla N, Galimberti I, Depaola V, Caroni P,. Staining protocol for organotypic hippocampal slice cultures. Nat Protoc 2006; 1: 2452-2456.
56. Gahwiler BH,. Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 1981; 4: 329-342.
57. Gahwiler BH, Capogna M, Debanne D, Mckinney RA, Thompson SM,. Organotypic slice cultures: a technique has come of age. Trends Neurosci 1997; 20: 471-477.
58. Baydas G, Reiter RJ, Nedzvetskii VS, et al., Melatonin protects the central nervous system of rats against toluene-containing thinner intoxication by reducing reactive gliosis. Toxicol Lett 2003; 137: 169-174.
59. Pascual R, Pilar Zamora-Leon S, Pérez N, et al., Melatonin ameliorates neocortical neuronal dendritic impairment induced by toluene inhalation in the rat. Exp Toxicol Pathol 2011; 63: 467-471.
60. Touitou Y, Fevre M, Lagoguey M, et al., Age- and mental health-related circadian rhythms of plasma levels of melatonin, prolactin, luteinizing hormone and follicle-stimulating hormone in man. J Endocrinol 1981; 91: 467-475.
61. Tricoire H, Locatelli A, Chemineau P, Malpaux B,. Melatonin enters the cerebrospinal fluid through the pineal recess. Endocrinology 2002; 143: 84-90.
62. Crumeyrolle-Arias M, Tournaire MC, Rabot S, Malpaux B, Thiéry JC,. 5-hydroxyoxindole, an indole metabolite, is present at high concentrations in brain. J Neurosci Res 2008; 86: 202-207.
63. Bernhardt R, Matus A,. Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between dendritic and axonal cytoskeletons. J Comp Neurol 1984; 226: 203-221.
64. Duvocovich ML,. Pharmacology and function of melatonin receptors. FASEB J 1988; 2: 2765-2773.
65. Duvocovich ML, Delagrange P, Krause DN, Sugden D, Cardinali DP, Olcese J,. International Union of basic and clinical pharmacology of G protein coupled melatonin receptors. Pharmacol Rev 2011; 62: 343-380.
66. Benítez-King G, Ramírez-Rodríguez G, Ortíz L, Meza I,. The neuronal cytoskeleton as a potential therapeutical target in neurodegenerative diseases and schizophrenia. Curr Drug Targets CNS Neurol Disord 2004; 3: 515-533.
67. Benítez-King G, Ortiz-Loacute;pez L, Morales-Mulia S, Jiménez-Rubio G, Ramírez-Rodriguez G, Meza I,. Phosphorylation-dephosphorylation imbalance of cytoskeletal associated-proteins in neurodegenerative diseases. Recent Pat CNS Drug Discov 2006; 1: 219-230.
68. Becker-André M, Wiesenber I, Schaeren-Wiemers N, et al., Pineal gland hormone melatonin binds and activates an orphan of nuclear receptor superfamily. J Biol Chem 1994; 269: 28531-28534.
69. + cells. J Immunol 1997; 159: 574-581.
70. Kloosterman F, Peloquin P, Leung LS,. Apical and basal orthodromic populations spikes in hippocampal CA1 in vivo show different origin and patterns of propagation. J Neurophysiol 2001; 86: 2435-2444.
71. Thiel G,. Synapsin I, synapsin II, and synaptophysin: marker proteins of synaptic vesicles. Brain Pathol 1993; 3: 87-95.
72. Zhang W, Benson DL,. Stages of synapse development defined by dependence on F-actin. J Neurosci 2001; 21: 5169-5181.
73. Swartz BE, Houser CR, Tomiyasu U, et al., Hippocampal cell loss in posttraumatic human epilepsy. Epilepsia 2006; 47: 1373-1382.
74. Zhang W, Yamawaki R, Wen X, et al., Surviving hilar somatostatin interneurons enlarge, sprout axons, and form new synapses with granule cells in a mouse model of temporal lobe epilepsy. J Neurosci 2009; 29: 14247-14256.
75. Ling ZQ, Tian Q, Wang L, et al., Constant illumination induces Alzheimer-like damages with endoplasmic reticulum involvement and the protection of melatonin. J Alzheimers Dis 2009; 16: 287-300.
76. Furio AM, Brusco LI, Cardinali DP,. Possible therapeutic value of melatonin in mild cognitive impairment: a retrospective study. J Pineal Res, 2007; 43: 404-409.
77. Brusco LI, Marquez M, Cardinali DP,. Melatonin treatment stabilizes chronobiologic and cognitive symptoms in Alzheimer's disease. Neuro Endocrinol Lett 2000; 21: 39-42.