Melatonin maintains calcium-binding calretinin-positive neurons in the dentate gyrus during aging of Balb/C mice

Experimental Gerontology

Volumn 60, Issue , 2014, Pages 147-152

  Ramírez Rodríguez, Gerardo ^a   Gómez Sánchez, Ariadna ^a   Ortíz López, Leonardo ^a  

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

Author keywords

Adult hippocampal neurogenesis; Aging; Calretinin; Dentate gyrus; Dorsal ventral; Hippocampus; Melatonin

Indexed keywords

CALRETININ; MELATONIN;

ADULT; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL COUNT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; SUPPLEMENTATION;

EID: 84909982068     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.10.014     Document Type: Article

References (81)

1. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., Feldon J. Regional dissociations within the hippocampus-memory and anxiety. Neurosci. Biobehav. Rev. 2004, 28:273-283.
2. Bellon A., Ortiz-Lopez L., Ramirez-Rodriguez G., Anton-Tay F., Benitez-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.
3. Benitez-King G. Melatonin as a cytoskeletal modulator: implications for cell physiology and disease. J. Pineal Res. 2006, 40:1-9.
4. Benitez-King G., Anton-Tay F. Calmodulin mediates melatonin cytoskeletal effects. Experientia 1993, 49:635-641.
5. Benitez-King G., Huerto-Delgadillo L., Anton-Tay F. Melatonin effects on the cytoskeletal organization of MDCK and neuroblastoma N1E-115 cells. J. Pineal Res. 1990, 9:209-220.
6. Benitez-King G., Huerto-Delgadillo L., Anton-Tay F. Binding of 3H-melatonin to calmodulin. Life Sci. 1993, 53:201-207.
7. Benitez-King G., Hernandez M.E., Tovar R., Ramirez G. Melatonin activates PKC-alpha but not PKC-epsilon in N1E-115 cells. Neurochem. Int. 2001, 39:95-102.
8. Brandt M.D., Jessberger S., Steiner B., Kronenberg G., Reuter K., Bick-Sander A., von der Behrens W., Kempermann G. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol. Cell. Neurosci. 2003, 24:603-613.
9. Brusco L.I., Marquez M., Cardinali D.P. Melatonin treatment stabilizes chronobiologic and cognitive symptoms in Alzheimer's disease. Neuro Endocrinol. Lett. 2000, 21:39-42.
10. Bu J., Sathyendra V., Nagykery N., Geula C. Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Exp. Neurol. 2003, 182:220-231.
11. Caballero B., Vega-Naredo I., Sierra V., Huidobro-Fernandez C., Soria-Valles C., De Gonzalo-Calvo D., Tolivia D., Pallas M., Camins A., Rodriguez-Colunga M.J., Coto-Montes A. Melatonin alters cell death processes in response to age-related oxidative stress in the brain of senescence-accelerated mice. J. Pineal Res. 2009, 46:106-114.
12. Cardinali D.P., Srinivasan V., Brzezinski A., Brown G.M. Melatonin and its analogs in insomnia and depression. J. Pineal Res. 2012, 52:365-375.
13. Carvalho L.A., Gorenstein C., Moreno R., Pariante C., Markus R.P. Effect of antidepressants on melatonin metabolite in depressed patients. J. Psychopharmacol. 2009, 23:315-321.
14. Catapano F., Monteleone P., Fuschino A., Mag M., Kemali D. Melatonin and cortisol secretion in patients with primary obsessive-compulsive disorder. Psychiatry Res. 1992, 44:217-225.
15. Corrales A., Vidal R., Garcia S., Vidal V., Martinez P., Garcia E., Florez J., Sanchez-Barcelo E.J., Martinez-Cue C., Rueda N. Chronic melatonin treatment rescues electrophysiological and neuromorphological deficits in a mouse model of Down syndrome. J. Pineal Res. 2014, 56:51-61.
16. Couillard-Despres S., Wuertinger C., Kandasamy M., Caioni M., Stadler K., Aigner R., Bogdahn U., Aigner L. Ageing abolishes the effects of fluoxetine on neurogenesis. Mol. Psychiatry 2009, 14:856-864.
17. Crupi R., Mazzon E., Marino A., La Spada G., Bramanti P., Cuzzocrea S., Spina E. Melatonin treatment mimics the antidepressant action in chronic corticosterone-treated mice. J. Pineal Res. 2010, 49:123-129.
18. Crupi R., Mazzon E., Marino A., La Spada G., Bramanti P., Spina E., Cuzzocrea S. Melatonin's stimulatory effect on adult hippocampal neurogenesis in mice persists after ovariectomy. J. Pineal Res. 2011, 51:353-360.
19. de Faria Poloni J., Feltes B.C., Bonatto D. Melatonin as a central molecule connecting neural development and calcium signaling. Funct. Integr. Genomics 2011, 11:383-388.
20. Dominguez-Alonso A., Ramirez-Rodriguez G., Benitez-King G. Melatonin increases dendritogenesis in the hilus of hippocampal organotypic cultures. J. Pineal Res. 2012, 52:427-436.
21. Dubocovich M.L. Melatonin receptors: role on sleep and circadian rhythm regulation. Sleep Med. 2007, 8(Suppl. 3):34-42.
22. Dubocovich M.L., Markowska M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 2005, 27:101-110.
23. Farajnia S., Michel S., Deboer T., vanderLeest H., Houben T., Rohling J.H.T., Ramkisoensing A., Yasenkov R., Meijer J.H. Evidence for neuronal desynchrony in the aged suprachiasmatic nucleus clock. J. Neurosci. 2012, 32:5891-5899.
24. Ferrari E., Fioravanti M., Magri F., Solerte S.B. Variability of interactions between neuroendocrine and immunological functions in physiological aging and dementia of the Alzheimer's type. Ann. N. Y. Acad. Sci. 2000, 917:582-596.
25. Ge S., Goh E.L., Sailor K.A., Kitabatake Y., Ming G.L., Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006, 439:589-593.
26. Gomez-Corvera A., Cerrillo I., Molinero P., Naranjo M.C., Lardone P.J., Sanchez-Hidalgo M., Carrascosa-Salmoral M.P., Medrano-Campillo P., Guerrero J.M., Rubio A. Evidence of immune system melatonin production by two pineal melatonin deficient mice, C57BL/6 and Swiss strains. J. Pineal Res. 2009, 47:15-22.
27. Hardeland R. Neurobiology, pathophysiology, and treatment of melatonin deficiency and dysfunction. Sci. World J. 2012, 640389.
28. Hardeland R. Chronobiology of melatonin beyond the feedback to the suprachiasmatic nucleus-consequences to melatonin dysfunction. Int. J. Mol. Sci. 2013, 14:5817-5841.
29. 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.
30. Jinno S. Decline in adult neurogenesis during aging follows a topographic pattern in the mouse hippocampus. J. Comp. Neurol. 2011, 519:451-466.
31. Kempermann G., Gast D., Kronenberg G., Yamaguchi M., Gage F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003, 130:391-399.
32. Kjelstrup K.G., Tuvnes F.A., Steffenach H.A., Murison R., Moser E.I., Moser M.B. Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10825-10830.
33. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 1996, 16:2027-2033.
34. Kuznicki J., Isaacs K.R., Jacobowitz D.M. The expression of calretinin in transfected PC12 cells provides no protection against Ca(2+)-overload or trophic factor deprivation. Biochim. Biophys. Acta 1996, 1313:194-200.
35. Lee C.H., Hwang I.K., Choi J.H., Yoo K.Y., Park O.K., Huh S.O., Lee Y.L., Shin H.C., Won M.H. Age-dependent changes in calretinin immunoreactivity and its protein level in the gerbil hippocampus. Neurochem. Res. 2010, 35:122-129.
36. Leonardo E.D., Richardson-Jones J.W., Sibille E., Kottman A., Hen R. Molecular heterogeneity along the dorsal-ventral axis of the murine hippocampal CA1 field: a microarray analysis of gene expression. Neuroscience 2006, 137:177-186.
37. Liu R.Y., Zhou J.N., van Heerikhuize J., Hofman M.A., Swaab D.F. 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.
38. Liu J., Somera-Molina K.C., Hudson R.L., Dubocovich M.L. Melatonin potentiates running wheel-induced neurogenesis in the dentate gyrus of adult C3H/HeN mice hippocampus. J. Pineal Res. 2013, 54:222-231.
39. McHugh S.B., Deacon R.M., Rawlins J.N., Bannerman D.M. Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav. Neurosci. 2004, 118:63-78.
40. Mirochnic S., Wolf S., Staufenbiel M., Kempermann G. Age effects on the regulation of adult hippocampal neurogenesis by physical activity and environmental enrichment in the APP23 mouse model of Alzheimer disease. Hippocampus 2009, 19:1008-1018.
41. Monteleone P., Maj M., Fusco M., Kemali D., Reiter R.J. Depressed nocturnal plasma melatonin levels in drug-free paranoid schizophrenics. Schizophr. Res. 1992, 7:77-84.
42. Moser M.B., Moser E.I., Forrest E., Andersen P., Morris R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9697-9701.
43. Nakamura T.J., Nakamura W., Yamazaki S., Kudo T., Cutler T., Colwell C.S., Block G.D. Agre-related decline in circadian output. J. Neurosci. 2011, 31:10201-10205.
44. Ohashi Y., Okamoto N., Uchida K., Iyo M., Mori N., Morita Y. Daily rhythm of serum melatonin levels and effect of light exposure in patients with demential of the Alzheimer's type. Biol. Psychiatry 1999, 45:1646-1652.
45. Plumpe T., Ehninger D., Steiner B., Klempin F., Jessberger S., Brandt M., Romer B., Ramirez Rodriguez G., Kronenberg G., Kempermann G. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci. 2006, 7:77.
46. 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. Neuropsychopharmacology 2009, 34:2180-2191.
47. Ramirez-Rodriguez G., Ortiz-Lopez L., Dominguez-Alonso A., Benitez-King G.A., Kempermann G. Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J. Pineal Res. 2011, 50:29-37.
48. Ramirez-Rodriguez G., Vega-Rivera N.M., Benitez-King G., Castro-Garcia M., Ortiz-Lopez L. Melatonin supplementation delays the decline of adult hippocampal neurogenesis during normal aging of mice. Neurosci. Lett. 2012, 530:53-58.
49. Ramirez-Rodriguez G., Vega-Rivera N.M., Oikawa-Sala J., Gomez-Sanchez A., Ortiz-Lopez L., Estrada-Camarena E. Melatonin synergizes with citalopram to induce antidepressant-like behavior and to promote hippocampal neurogenesis in adult mice. J. Pineal Res. 2014, 56:450-461.
50. Reiter R.J. Pineal melatonin: cell biology of its synthesis and of its physiological interactions. Endocr. Rev. 1991, 12:151-180.
51. Reiter R.J. Melatonin, active oxygen species and neurological damage. Drug News Perspect 1998, 11:291-296.
52. Reiter R.J. Oxidative damage in the central nervous system: protection by melatonin. Prog. Neurobiol. 1998, 56:359-384.
53. Reiter R.J., Tan D.X., Qi W., Manchester L.C., Karbownik M., Calvo J.R. Pharmacology and physiology of melatonin in the reduction of oxidative stress in vivo. Biol. Signals Recept. 2000, 9:160-171.
54. Reiter R.J., Tan D.X., Manchester L.C., Pilar Terron M., Flores L.J., Koppisepi S. Medical implications of melatonin: receptor-mediated and receptor-independent actions. Adv. Med. Sci. 2007, 52:11-28.
55. Reiter R.J., Paredes S.D., Manchester L.C., Tan D.X. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit. Rev. Biochem. Mol. Biol. 2009, 44:175-200.
56. Rennie K., De Butte M., Pappas B.A. Melatonin promotes neurogenesis in dentate gyrus in the pinealectomized rat. J. Pineal Res. 2009, 47:313-317.
57. Rogers J.H. Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J. Cell Biol. 1987, 105:1343-1353.
58. Romero M.P., Garcia-Perganeda A., Guerrero J.M., Osuna C. Membrane-bound calmodulin in Xenopus laevis oocytes as a novel binding site for melatonin. FASEB J. 1998, 12:1401-1408.
59. Savaskan E., Olivieri G., Brydon L., Jockers R., Krauchi K., Wirz-Justice A., Muller-Spahn F. Cerebrovascular melatonin MT1-receptor alterations in patients with Alzheimer's disease. Neurosci. Lett. 2001, 308:9-12.
60. Savaskan E., Olivieri G., Meier F., Brydon L., Jockers R., Ravid R., Wirz-Justice A., Muller-Spahn F. Increased melatonin 1a-receptor immunoreactivity in the hippocampus of Alzheimer's disease patients. J. Pineal Res. 2002, 32:59-62.
61. Savaskan E., Ayoub M.A., Ravid R., Angeloni D., Fraschini F., Meier F., Eckert A., Muller-Spahn F., Jockers R. Reduced hippocampal MT2 melatonin receptor expression in Alzheimer's disease. J. Pineal Res. 2005, 38:10-16.
62. Schwaller B. Calretinin: from a "simple" Ca buffer to a multifunctional protein implicated in many biological processes. Front. Neuroanat. 2014, 8:3.
63. Schweitzer I., Tuckwell V., O'Brien J., Ames D. Is late onset depression a prodrome to dementia?. Int. J. Geriatr. Psychiatry 2002, 17:997-1005.
64. Shigeta H., Yasui A., Nimura Y., Machida N., Kageyama M., Miura M., Menjo M., Ikeda K. Postoperative delirium and melatonin levels in elderly patients. Am. J. Surg. 2001, 182:449-454.
65. Skene D.J., Swaab D.F. Melatonin rhythmicity: effect of age and Alzheimer's disease. Exp. Gerontol. 2003, 38:199-206.
66. Skene D.J., Vivien-Roelfs B., Sparks D.L., Hunsaker J.C., Pevet P., Ravid D., Swaab D.F. Daily variation in the concentration of melatonin and 5-methoxytryptophol in the human pineal gland: effect of age and Alzheimer's disease. Brain Res. 1990, 528:170-174.
67. Soto-Vega E., Meza I., Ramirez-Rodriguez G., Benitez-King G. Melatonin stimulates calmodulin phosphorylation by protein kinase C. J. Pineal Res. 2004, 37:98-106.
68. Steffenach H.A., Witter M., Moser M.B., Moser E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 2005, 45:301-313.
69. Tan D.X., Manchester L.C., Reiter R.J., Qi W., Kim S.J., El-Sokkary G.H. Melatonin protects hippocampal neurons in vivo against kainic acid-induced damage in mice. J. Neurosci. Res. 1998, 54:382-389.
70. Todkar K., Scotti A.L., Schwaller B. Absence of the calcium-binding protein calretinin, not of calbindin D-28k, causes a permanent impairment of murine adult hippocampal neurogenesis. Front. Mol. Neurosci. 2012, 5:56.
71. Toth K., Eross L., Vajda J., Halasz P., Freund T.F., Magloczky Z. Loss and reorganization of calretinin-containing interneurons in the epileptic human hippocampus. Brain 2010, 133:2763-2777.
72. Uchida K., Okamoto N., Ohara N., Morita Y. Daily rhythm of serum melatonin in patients with dementia of the degenerate type. Brain Res. 1996, 7171:154-159.
73. Vigano D., Lissoni P., Rovelli F., Roselli M.G., Malugani F., Gavazzeni C., Conti A., Maestroni G. A study of light/dark rhythm of melatonin in relation to cortisol and prolactin secretion in schizophrenia. Neuroendocrinol. Lett. 2001, 22:137-141.
74. Villeda S.A., Luo J., Mosher K.I., Zou B., Britschgi M., Bieri G., Stan T.M., Fainberg N., Ding Z., Eggel A., Lucin K.M., Czirr E., Park J.S., Couillard-Despres S., Aigner L., Li G., Peskind E.R., Kaye J.A., Quinn J.F., Galasko D.R., Xie X.S., Rando T.A., Wyss-Coray T. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011, 477:90-94.
75. von Gall C., Weaver D.R. Loss of responsiveness to melatonin in the aging mouse suprachiasmatic nucleus. Neurobiol. Aging 2008, 29:464-470.
76. Waldhauser F., Steger H. Changes in melatonin secretion with age and pubescence. J. Neural Transm. Suppl. 1986, 21:183-197.
77. Waldhauser F., Weiszenbacher G., Tatzer E., Gisinger B., Waldhauser M., Schemper M., Frisch H. Alterations in nocturnal serum melatonin levels in humans with growth and aging. J. Clin. Endocrinol. Metab. 1988, 66:648-652.
78. Waldhauser F., Ehrhart B., Forster E. Clinical aspects of the melatonin action: impact of development, aging, and puberty, involvement of melatonin in psychiatric disease and importance of neuroimmunoendocrine interactions. Experientia 1993, 49:671-681.
79. Waldhauser F., Kovacs J., Reiter E. Age-related changes in melatonin levels in humans and its potential consequences for sleep disorders. Exp. Gerontol. 1998, 33:759-772.
80. Wu Y.H., Swaab D.F. Disturbance and strategies for reactivation of the circadian rhythm system in aging and Alzheimer's diseases. Sleep Med. 2007, 8:623-636.
81. Zeng L., Webster S.V., Newton P.M. The biology of protein kinase C. Adv. Exp. Med. Biol. 2012, 740:639-661.