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2013, Number 3

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Salud Mental 2013; 36 (3)

La melatonina como un factor promotor de la diferenciación neuronal: implicaciones en el tratamiento de las demencias

Benítez-King G, Valdés-Tovar M, Maya-Ampudia V, Jiménez-Rubio G, Domínguez-Alonso A, Riquelme A, Galván-Arrieta T, Solís-Chagoyán H, Alarcón S, Moreno J, Ugalde Ó, Berlanga C

Language: Spanish
References: 102
Page: 193-199
PDF size: 271.82 Kb.


ABSTRACT

Dementias are progressive and neurodegenerative neuropsychiatric disorders, with a high worldwide prevalence. These disorders affect memory and behavior, causing impairment in the performance of daily activities and general disability in the elders. Cognitive impairment in these patients is related to anatomical and structural alterations at cellular and sub-cellular levels in the Central Nervous System. In particular, amyloid plaques and neurofibrillar tangles have been defined as histopathological hallmarks of Alzheimer’s disease. Likewise, oxidative stress and neuroinflammation are implicated in the etiology and progression of the disease.
Neuronal precursors from human olfactory neuroepithelium have been recently characterized as an experimental model to identify neuropsychiatric disease biomarkers. Moreover, this model not only allows the study of neuropsychiatric physiopathology, but also the process of neurodevelopment at cellular, molecular and pharmacological levels.
This review gathers the evidence to support the potential therapeutic use of melatonin for dementias, based on its antioxidant properties, its anti-inflammatory effect in the brain, and its ability to inhibit both tau hyper-phosphorylation and amyloid plaque formation. Furthermore, since melatonin stimulates neurogenesis, and promotes neuronal differentiation by inducing the early stages of neuritogenesis and dendrite formation, it has been suggested that melatonin could be useful to counteract the cognitive impairment in dementia patients.


REFERENCES

  1. Secretaría de Salud (SSA). México Sano. 2008; enero;1(1):11; http://portal. salud.gob.mx/descargas/pdf/period_mexsano/mexicosano_ene08. pdf, 26 de noviembre de 2012.

  2. Llibre Rodríguez JJ, Ferri CP, Acosta D, Guerra M et al. Prevalence of dementia in Latin America, India, and China: a population-based cross-sectional survey. Lancet 2008;372(9637):464-474.

  3. Baldereschi M, Di Carlo A, Amaducci L. Epidemiology of dementias. Drugs Today 1998;34(9):747-758.

  4. American Psychiatric Association. Delirium, dementia, and amnestic and other cognitive disorders. En: First M (ed). Diagnostic and Statistical Manual of Mental Disorders. Cuarta edición. DSM-IV-TR®. Arlington, VA: American Psychiatric Publishing; 2000.

  5. Rabins PV, Blacker D, Rovner BW, Rummans T Et al. American Psychiatric Association practice guideline for the treatment of patients with Alzheimer’s disease and other dementias. Second edition. Am J Psychiatry 2007;164(12Supl):5-56.

  6. Burns A, Byrne EJ, Maurer K. Alzheimer’s disease. Lancet 2002;360(9327):163-165.

  7. Pasantes H, Arias C, Massieu L, Zentella A et al. Enfermedades neurodegenerativas: mecanismos celulares y moleculares. México: Fondo de Cultura Económica; 1999.

  8. Williams DR. Tauopathies: classification and clinical update on neurodegenerative diseases associated with microtubule-associated protein tau. Intern Med J Australia 2006;36(10):652-660.

  9. Andersen P, Morris R, Amaral D, Bliss T, O’Keefe J. The Hippocampus Book. EUA: Oxford University Press; 2006.

  10. Thompson PM, Hayashi KM, de Zubicaray G, Janke AL et al. Dynamics of gray matter loss in Alzheimer’s disease. J Neurosci 2003;23(3):994-1005.

  11. Squire L, Bloom FE, Spitzer NC, Squire LR et al. Fundamental Neuroscience. USA: Academic Press; 2008.

  12. Caserta MT, Bannon Y, Fernandez F, Giunta B et al. Chapter 1 normal brain aging: Clinical, immunological, neuropsychological, and neuroimaging features. En: Minagar A (ed). International review of neurobiology, neurobiology of dementia. USA: Academic Press; 2009.

  13. West MJ, Kawas CH, Stewart WF, Rudow GL et al. Hippocampal neurons in pre-clinical Alzheimer’s disease. Neurobiol Aging 2004;25(9):1205-1212.

  14. Zarow C, Vinters HV, Ellis WG, Weiner MW et al. Correlates of hippocampal neuron number in Alzheimer’s disease and ischemic vascular dementia. Ann Neurol 2005;57(6):896-903.

  15. Stuart G, Spruston N, Hausser M. Dendrites. USA: Oxford University Press; 2007.

  16. Xekardaki A, Giannakopoulos P, Haller S. White matter changes in bipolar disorder, Alzheimer disease, and mild cognitive impairment: New insights from DTI. J Aging Res 2011;2011:286564.

  17. Jawhar S, Trawicka A, Jenneckens C, Bayer TA et al. Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Abeta aggregation in the 5XFAD mouse model of Alzheimer’s disease. Neurobiol Aging 2012;33(1):196 e29-40.

  18. Yamada M, Wada Y, Tsukagoshi H, Otomo E et al. A quantitative Golgi study of basal dendrites of hippocampal CA1 pyramidal cells in senile dementia of Alzheimer type. J Neurol Neurosurg Psychiatry 1988;51(8):1088-1090.

  19. Buell SJ, Coleman PD. Dendritic growth in the aged human brain and failure of growth in senile dementia. Science 1979;206(4420):854-856.

  20. Samuel W, Masliah E, Hill LR, Butters N et al. Hippocampal connectivity and Alzheimer’s dementia: effects of synapse loss and tangle frequency in a two-component model. Neurology 1994;44(11):2081-2088.

  21. Tiraboschi P, Hansen LA, Alford M, Masliah E et al. Corey-Bloom J. The decline in synapses and cholinergic activity is asynchronous in Alzheimer’s disease. Neurology 2000;55(9):1278-1283.

  22. Hamos JE, DeGennaro LJ, Drachman DA. Synaptic loss in Alzheimer’s disease and other dementias. Neurology 1989;39(3):355-361.

  23. Lassmann H, Fischer P, Jellinger K. Synaptic pathology of Alzheimer’s disease. Ann N Y Acad Sci 1993;695:59-64.

  24. Scheff SW, Price DA, Schmitt FA, Mufson EJ. Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 2006;27(10):1372-1384.

  25. Mandal PK, Tripathi M, Sugunan S. Brain oxidative stress: detection and mapping of anti-oxidant marker ‘Glutathione’ in different brain regions of healthy male/female, MCI and Alzheimer patients using non-invasive magnetic resonance spectroscopy. Biochem Biophys Res Commun 2012;417(1):43-48.

  26. Repetto MG, Reides CG, Evelson P, Kohan S et al. Peripheral markers of oxidative stress in probable Alzheimer patients. Eur J Clin Invest 1999;29(7):643-649.

  27. Kermer P, Liman J, Weishaupt JH, Bahr M. Neuronal apoptosis in neurodegenerative diseases: from basic research to clinical application. Neurodegener Dis 2004;1(1):9-19.

  28. Benítez-King G, Ortiz-López L, Jiménez G. Melatonin precludes cytoskeletal collapse caused by hydrogen peroxide: participation of protein kinase C. Therapy 2005;2(5):767-778.

  29. Selkoe DJ. Toward a comprehensive theory for Alzheimer’s disease. Hypothesis: Alzheimer’s disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann N Y Acad Sci 2000;924:17-25.

  30. Brandt R, Lee G. Orientation, assembly, and stability of microtubule bundles induced by a fragment of tau protein. Cell Motil Cytoskeleton 1994;28(2):143-154.

  31. Alonso AD, Grundke-Iqbal I, Barra HS, Iqbal K. Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc Natl Acad Sci USA 1997;94(1):298-303.

  32. Griffin JW, Watson DF. Axonal transport in neurological disease. Ann Neurol 1988;23(1):3-13.

  33. Rubio-Perez JM, Morillas-Ruiz JM. A review: inflammatory process in Alzheimer’s disease, role of cytokines. Scientific World J 2012;2012:756357.

  34. Agostinho P, Cunha RA, Oliveira C. Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer’s disease. Curr Pharm Des 2010;16(25):2766-2778.

  35. Azizi G, Mirshafiey A. The potential role of proinflammatory and antiinflammatory cytokines in Alzheimer disease pathogenesis. Immunopharmacol Immunotoxicol 2012; DOI: 10.3109/08923973.2012.705292, ISSN: 1532-2513 (Electronic).

  36. Schlachetzki JC, Hull M. Microglial activation in Alzheimer’s disease. Curr Alzheimer Res 2009;6(6):554-563.

  37. Rossner S, Lange-Dohna C, Zeitschel U, Perez-Polo JR. Alzheimer’s disease beta-secretase BACE1 is not a neuron-specific enzyme. J Neurochem 2005;92(2):226-234.

  38. Bulbarelli A, Lonati E, Brambilla A, Orlando A et al. Abeta42 production in brain capillary endothelial cells after oxygen and glucose deprivation. Mol Cell Neurosci 2012;49(4):415-422.

  39. Rodriguez JJ, Olabarria M, Chvatal A, Verkhratsky A. Astroglia in dementia and Alzheimer’s disease. Cell Death Differ 2009;16(3):378- 385.

  40. Koyama A, O’Brien J, Weuve J, Blacker D, Metti AL, Yaffe K. The Role of Peripheral Inflammatory Markers in Dementia and Alzheimer’s Disease: A Meta-Analysis. J Gerontol A Biol Sci Med Sci. 2012. DOI: 10.1093/gerona/gls187, ISSN: 1758-535X (Electronic).

  41. Holmes C. Systemic inflammation and Alzheimer’s Disease. Neuropathol Appl Neurobiol 2012. DOI: 10.1111/j.1365-2990.2012.01307.x, ISSN: 1365-2990 (Electronic).

  42. Hoozemans JJ, Veerhuis R, Rozemuller JM, Eikelenboom P. Soothing the inflamed brain: effect of non-steroidal anti-inflammatory drugs on Alzheimer’s disease pathology. CNS Neurol Disord Drug Targets 2011;10(1):57-67.

  43. Lewis TL, Cao D, Lu H, Mans RA, Su YR et al. Overexpression of human apolipoprotein A-I preserves cognitive function and attenuates neuroinflammation and cerebral amyloid angiopathy in a mouse model of Alzheimer disease. J Biol Chem 2010;285(47):36958-968.

  44. Hoppe JB, Frozza RL, Horn AP, Comiran RA et al. Amyloid-beta neurotoxicity in organotypic culture is attenuated by melatonin: involvement of GSK-3beta, tau and neuroinflammation. J Pineal Res 2010;48(3):230-238.

  45. He FQ, Qiu BY, Zhang XH, Li TK et al. Tetrandrine attenuates spatial memory impairment and hippocampal neuroinflammation via inhibiting NF-kappaB activation in a rat model of Alzheimer’s disease induced by amyloid-beta(1-42). Brain Res 2011;1384:89-96.

  46. Garcia-Chavez D, Gonzalez-Burgos I, Letechipia-Vallejo G, Lopez-Loeza E 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(1):148-152.

  47. Noraberg J, Poulsen FR, Blaabjerg M, Kristensen BW et al. Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr Drug Targets CNS Neurol Disord 2005;4(4):435-152.

  48. Cho S, Wood A, Bowlby MR. Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr Neuropharmacol 2007;5(1):19-33.

  49. Gogolla N, Galimberti I, DePaola V, Caroni P. Staining protocol for organotypic hippocampal slice cultures. Nat Protoc 2006;1(5):2452-2456.

  50. Benítez-King G, Domínguez-Alonso A, Ramírez-Rodríguez G. Neurocytoskeletal protective effect of melatonin: importance for morpho- functional neuronal polarization. Open Neuroendocrinology J 2010;3:105-111.

  51. Ramírez-Rodríguez G, Ortiz-López L, Domínguez-Alonso A, Benitez- King GA et al. Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J Pineal Res 2011;50(1):29-37.

  52. Domínguez-Alonso A, Ramírez-Rodríguez G, Benítez-King G. Melatonin increases dendritogenesis in the hilus of hippocampal organotypic cultures. J Pineal Res 2012;52(4):427-436.

  53. Tabaton M, Cammarata S, Mancardi GL, Cordone G et al. Abnormal taureactive filaments in olfactory mucosa in biopsy specimens of patients with probable Alzheimer’s disease. Neurology 1991;41(3):391-394.

  54. Talamo BR, Rudel R, Kosik KS, Lee VM et al. Pathological changes in olfactory neurons in patients with Alzheimer’s disease. Nature 1989;337(6209):736-739.

  55. Lee JH, Goedert M, Hill WD, Lee VM et al. Tau proteins are abnormally expressed in olfactory epithelium of Alzheimer patients and developmentally regulated in human fetal spinal cord. Exp Neurol 1993;121(1):93-105.

  56. Jafek B, Johnson E, Eller P, Murrow B. Olfactory mucosal biopsy and related histology. En: Seiden A (ed). Taste and Smell Disorders. New York, NY: Thieme; 1997.

  57. Lane AP, Gomez G, Dankulich T, Wang H et al. The superior turbinate as a source of functional human olfactory receptor neurons. Laryngoscope 2002;112(7 Pt1):1183-1189.

  58. Lanza DC, Deems DA, Doty RL, Moran D et al. The effect of human olfactory biopsy on olfaction: a preliminary report. Laryngoscope 1994;104(7):837-840.

  59. Arnold SE, Lee EB, Moberg PJ, Stutzbach L et al. Olfactory epithelium amyloid-beta and paired helical filament-tau pathology in Alzheimer disease. Ann Neurol 2010;67(4):462-469.

  60. Graziadei P, Monti-Graziadei G. The olfactory system: a model for the study of neurogenesis and axon regeneration in mammals. En: Cotman C (ed). Neuronal plasticity. New York: Raven Press; 1978.

  61. Hahn CG, Han LY, Rawson NE, Mirza N et al. In vivo and in vitro neurogenesis in human olfactory epithelium. J Comp Neurol 2005;483(2):154-163.

  62. Benítez-King G, Riquelme A, Ortiz-López L, Berlanga C et al. A noninvasive method to isolate the neuronal linage from the nasal epithelium from schizophrenic and bipolar diseases. J Neurosci Methods 2011;201(1):35-45.

  63. Rosales-Corral SA, Acuna-Castroviejo D, Coto-Montes A, Boga JA et al. Alzheimer’s disease: pathological mechanisms and the beneficial role of melatonin. J Pineal Res 2012;52(2):167-202.

  64. Cardinali DP, Furio AM, Brusco LI. Clinical aspects of melatonin intervention in Alzheimer’s disease progression. Curr Neuropharmacol 2010;8(3):218-227.

  65. Brusco LI, Marquez M, Cardinali DP. Monozygotic twins with Alzheimer’s disease treated with melatonin: Case report. J Pineal Res 1998;25(4):260-263.

  66. Jean-Louis G, Zizi F, von Gizycki H, Taub H. Effects of melatonin in two individuals with Alzheimer’s disease. Percept Mot Skills 1998;87(1):331-339.

  67. Brusco LI, Marquez M, Cardinali DP. Melatonin treatment stabilizes chronobiologic and cognitive symptoms in Alzheimer’s disease. Neuro Endocrinol Lett 2000;21(1):39-42.

  68. Reiter RJ. Oxidative damage in the central nervous system: protection by melatonin. Prog Neurobiol 1998;56(3):359-384.

  69. Acuña-Castroviejo D, Coto-Montes A, Gaia Monti M, Ortiz GG et al. Melatonin is protective against MPTP-induced striatal and hippocampal lesions. Life Sci 1997;60(2):PL23-29.

  70. Mayo JC, Sainz RM, Uria H, Antolin I et al. Inhibition of cell proliferation: a mechanism likely to mediate the prevention of neuronal cell death by melatonin. J Pineal Res 1998;25(1):12-18.

  71. Tan DX, Manchester LC, Reiter RJ, Qi W et al. Melatonin protects hippocampal neurons in vivo against kainic acid-induced damage in mice. J Neurosci Res 1998;54(3):382-389.

  72. Zhou J, Zhang S, Zhao X, Wei T. Melatonin impairs NADPH oxidase assembly and decreases superoxide anion production in microglia exposed to amyloid-beta1-42. J Pineal Res 2008;45(2):157-165.

  73. Arendt T, Holzer M, Bruckner MK, Janke C et al. The use of okadaic acid in vivo and the induction of molecular changes typical for Alzheimer’s disease. Neuroscience 1998;85(4):1337-1340.

  74. Bialojan C, Takai A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 1988;256(1):283-290.

  75. Lee J, Hong H, Im J, Byun H et al. The formation of PHF-1 and SMI- 31 positive dystrophic neurites in rat hippocampus following acute injection of okadaic acid. Neurosci Lett 2000;282(1-2):49-52.

  76. Jiménez-Rubio G, Benítez-King G, Ortiz-López L. Melatonin elicits neuritogenesis and reverses tau hyperphosphorylation in N1E-115 neuroblastoma cells treated with okadaic acid. En: Fernández A (ed). Focus on neuroblastoma research. Hauppauge, NY: Nova Science Publisher; 2007.

  77. Benítez-King G, Ortiz-López L, Jiménez-Rubio G, Ramírez-Rodríguez G. Haloperidol causes cytoskeletal collapse in N1E-115 cells through tau hyperphosphorylation induced by oxidative stress: Implications for neurodevelopment. Eur J Pharmacol 2010;644(1-3):24-31.

  78. Reiter RJ, Tan D, Kim SJ, Manchester LC et al. Augmentation of indices of oxidative damage in life-long melatonin-deficient rats. Mech Ageing Dev 1999;110(3):157-173.

  79. Galano A, Tan DX, Reiter RJ. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011;51(1):1-16.

  80. Ling ZQ, Tian Q, Wang L, Fu ZQ et al. Constant illumination induces Alzheimer-like damages with endoplasmic reticulum involvement and the protection of melatonin. J Alzheimers Dis 2009;16(2):287-300.

  81. Jiménez-Rubio G, Ortiz-López L, Benítez-King G. Melatonin modulates cytoskeletal organization in the rat brain hippocampus. Neurosci Lett 2012;511(1):47-51.

  82. Benítez-King G, Tunez I, Bellon A, Ortiz GG et al. Melatonin prevents cytoskeletal alterations and oxidative stress induced by okadaic acid in N1E-115 cells. Exp Neurol 2003;182(1):151-159.

  83. García-Mesa Y, López-Ramos JC, Gimenez-Llort L, Revilla S et al. Physical exercise protects against Alzheimer’s disease in 3xTg-AD mice. J Alzheimers Dis 2011;24(3):421-454.

  84. Tahirovic S, Bradke F. Neuronal polarity. Cold Spring Harb Perspect Biol 2009;1(3):a001644.

  85. Vaillant AR, Zanassi P, Walsh GS, Aumont A et al. Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 2002;34(6):985-998.

  86. Baratier J, Peris L, Brocard J, Gory-Faure S et al. Phosphorylation of microtubule-associated protein STOP by calmodulin kinase II. J Biol Chem 2006;281(28):19561-19569.

  87. Guillaud L, Bosc C, Fourest-Lieuvin A, Denarier E et al. STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J Cell Biol 1998;142(1):167-179.

  88. Slaughter T, Black MM. STOP (stable-tubule-only-polypeptide) is preferentially associated with the stable domain of axonal microtubules. J Neurocytol 2003;32(4):399-413.

  89. Huerto-Delgadillo L, Antón-Tay F, Benítez-King G. Effects of melatonin on microtubule assembly depend on hormone concentration: role of melatonin as a calmodulin antagonist. J Pineal Res 1994;17(2):55-62.

  90. Bellon A, Ortiz-López L, Ramírez-Rodríguez G, Antón-Tay F 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(3):214-221.

  91. 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(5):774-781.

  92. Xavier GF, Costa VC. Dentate gyrus and spatial behaviour. Prog Neuropsychopharmacol Biol Psychiatry 2009;33(5):762-773.

  93. Benítez-King G, Huerto-Delgadillo L, Antón-Tay F. Melatonin modifies calmodulin cell levels in MDCK and N1E-115 cell lines and inhibits phosphodiesterase activity in vitro. Brain Res 1991;557(1-2):289-292.

  94. Soto-Vega E, Meza I, Ramírez-Rodríguez G, Benítez-King G. Melatonin stimulates calmodulin phosphorylation by protein kinase C. J Pineal Res 2004;37(2):98-106.

  95. Wu UI, Mai FD, Sheu JN, Chen LY et al. Melatonin inhibits microglial activation, reduces pro-inflammatory cytokine levels, and rescues hippocampal neurons of adult rats with acute Klebsiella pneumoniae meningitis. J Pineal Res 2011;50(2):159-170.

  96. Lee MY, Kuan YH, Chen HY, Chen TY et al. Intravenous administration of melatonin reduces the intracerebral cellular inflammatory response following transient focal cerebral ischemia in rats. J Pineal Res 2007;42(3):297-309.

  97. Min KJ, Jang JH, Kwon TK. Inhibitory effects of melatonin on the lipopolysaccharide- induced CC chemokine expression in BV2 murine microglial cells are mediated by suppression of Akt-induced NF-kappaB and STAT/GAS activity. J Pineal Res 2012;52(3):296-304.

  98. Clapp-Lilly KL, Smith MA, Perry G, Duffy LK. Melatonin reduces interleukin secretion in amyloid-beta stressed mouse brain slices. Chem Biol Interact 2001;134(1):101-107.

  99. Esposito E, Iacono A, Muia C, Crisafulli C et al. Signal transduction pathways involved in protective effects of melatonin in C6 glioma cells. J Pineal Res 2008;44(1):78-87.

  100. Esposito E, Cuzzocrea S. Antiinflammatory activity of melatonin in central nervous system. Curr Neuropharmacol 2010;8(3):228-242.

  101. Negi G, Kumar A, Sharma SS. Melatonin modulates neuroinflammation and oxidative stress in experimental diabetic neuropathy: effects on NF-kappaB and Nrf2 cascades. J Pineal Res 2011;50(2):124-131.

  102. Korkmaz A, Rosales-Corral S, Reiter RJ. Gene regulation by melatonin linked to epigenetic phenomena. Gene 2012;503(1):1-11.




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