Neurogenesis as a new target for the development of antidepressant drugs

Current Pharmaceutical Design

Volumn 20, Issue 23, 2014, Pages 3763-3775

  Pascual Brazo, Jesus ^a   Baekelandt, Veerle ^a   Encinas, Juan Manuel ^b,c,d  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b ACHUCARRO BASQUE CENTER FOR NEUROSCIENCE   (Spain)

^c BASQUE FOUNDATION FOR SCIENCE   (Spain)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Adult hippocampal neurogenesis; Depression; Stress

Indexed keywords

1 (4 AMINO 5 CHLORO 2 METHOXYPHENYL) 3 (1 BUTYL 4 PIPERIDINYL) 1 PROPANONE; AGOMELATINE; ANTIDEPRESSANT AGENT; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1 ANTAGONIST; FLUOXETINE; IMIPRAMINE; KETAMINE; MELATONIN RECEPTOR; MIFEPRISTONE; MONOAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTRANSMITTER; SEROTONIN; UNCLASSIFIED DRUG; BIOGENIC AMINE;

ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN DEPTH STIMULATION; CELL PROLIFERATION; DEPRESSION; DRUG EFFECT; DRUG TARGETING; ELECTROCONVULSIVE THERAPY; HIPPOCAMPUS; HUMAN; MONOAMINERGIC SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; STRESS; ANIMAL; DISEASE MODEL; DRUG DEVELOPMENT; DRUG EFFECTS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES;

ANIMALS; ANTIDEPRESSIVE AGENTS; BIOGENIC AMINES; DEPRESSION; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; ELECTROCONVULSIVE THERAPY; HIPPOCAMPUS; HUMANS; NEURAL STEM CELLS; NEUROGENESIS;

EID: 84916205330     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113196660739     Document Type: Article

References (155)

1. Muzina DJ, Kemp DE, McIntyre RS. Differentiating bipolar disorders from major depressive disorders: treatment implications. Ann Clin Psychiatry 2007; 19: 305-12.
2. Rakofsky JJ, Holtzheimer PE, Nemeroff CB. Emerging targets for antidepressant therapies. Curr Opin Chem Biol 2009; 13: 291-302.
3. Hirschfeld RM. History and evolution of the monoamine hypothesis of depression. The Journal of clinical psychiatry 2000; 61 Suppl 6: 4-6.
4. Malagié I, Trillat AC, Jacquot C, et al. Effects of acute fluoxetine on extracellular serotonin levels in the raphe: an in vivo microdialysis study. Eur J Pharmacol 1995; 286: 213-17.
5. Maione S, Palazzo E, Pallotta M, et al. Effects of imipramine on raphe nuclei and prefrontal cortex extracellular serotonin levels in the rat. Psychopharmacology (Berl.) 1997; 134: 401-05.
6. Duman RS, Monteggia LM. A neurotrophic model for stressrelated mood disorders. Biological psychiatry 2006; 59: 1116-27.
7. Sahay A, Hen R. Adult hippocampal neurogenesis in depression. Nature neuroscience 2007; 10: 1110-15.
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:
9. Santarelli L, Saxe M, Gross C, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-9.
10. Williams JW, Jr., Mulrow CD, Chiquette E, et al. A systematic review of newer pharmacotherapies for depression in adults: evidence report summary. Ann. Intern. Med 2000; 132: 743-56.
11. Kupfer DJ, Frank E, Phillips ML. Major depressive disorder: new clinical, neurobiological, and treatment perspectives. Lancet 2012; 379: 1045-55.
12. Gartlehner G, Gaynes BN, Hansen RA, et al. Comparative benefits and harms of second-generation antidepressants: background paper for the American College of Physicians. Ann Intern Med 2008; 149: 734-50.
13. Machado-Vieira R, Salvadore G, Luckenbaugh DA, et al. Rapid Onset of Antidepressant Action: A New Paradigm in the Research and Treatment of Major Depression. The Journal of clinical psychiatry 2008; 69:
14. Eriksson PS, Perfilieva E, Bjork-Eriksson T, et al. Neurogenesis in the adult human hippocampus. Nat Med 1998; 4: 1313-7.
15. Seri B, Garcia-Verdugo JM, McEwen BS, et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001; 21: 7153-60.
16. Farioli-Vecchioli S, Saraulli D, Costanzi M, et al. The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol 2008; 6: e246.
17. Zhang CL, Zou Y, He W, et al. A role for adult TLX-positive neural stem cells in learning and behavior. Nature 2008; 451: 1004-7.
18. Saxe MD, Battaglia F, Wang JW, et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 2006; 103: 17501-6.
19. Bergami M, Rimondini R, Santi S, et al. Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci USA 2008; 105: 15570-5.
20. Snyder JS, Soumier A, Brewer M, et al. Adult hippocampal neurogenesis buffers stress responses and depressive behavior. Nature 2011; 476: 458-61.
21. David DJ, Samuels BA, Rainer Q, et al. Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009; 62: 479-93.
22. Jacobs BL, van Praag H, Gage FH. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 2000; 5: 262-9.
23. Malberg JE, Eisch AJ, Nestler EJ, et al. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus J Neurosci 2000; 20: 9104-10.
24. Drew MR, Hen R. Adult hippocampal neurogenesis as target for the treatment of depression. CNS Neurol Disord Drug Targets 2007; 6: 205-18.
25. van Praag H, Schinder AF, Christie BR, et al. Functional neurogenesis in the adult hippocampus. Nature 2002; 415: 1030-4.
26. Kronenberg G, Reuter K, Steiner B, et al. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 2003; 467: 455-63.
27. 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: 373-82.
28. Mignone JL, Kukekov V, Chiang AS, et al. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 2004; 469: 311-24.
29. Ferri AL, Cavallaro M, Braida D, et al. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 2004; 131: 3805-19.
30. Kempermann G, Jessberger S, Steiner B, et al. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27: 447-52.
31. Ahn S, Joyner AL. In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005; 437: 894-7.
32. Encinas JM, Enikolopov G. Identifying and quantitating neural stem and progenitor cells in the adult brain. Methods Cell Biol 2008; 85: 243-72.
33. Mira H, Andreu Z, Suh H, et al. Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 2010; 7: 78-89.
34. Bonaguidi MA, Peng CY, McGuire T, et al. Noggin expands neural stem cells in the adult hippocampus. J Neurosci 2008; 28: 9194-204.
35. Lugert S, Basak O, Knuckles P, et al. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 2010; 6: 445-56.
36. Venere M, Han YG, Song JS, et al. Sox1 marks an activated neural stem/progenitor cell in the hippocampus. Development 2012;
37. Gao X, Enikolopov G, Chen J Moderate traumatic brain injury promotes proliferation of quiescent neural progenitors in the adult hippocampus. Exp Neurol 2009; 219: 516-23.
38. Song J, Zhong C, Bonaguidi MA, et al. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 2012; 489: 150-4.
39. Encinas JM, Michurina TV, Peunova N, et al. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 2011; 8: 566-79.
40. Encinas JM, Sierra A. Neural stem cell deforestation as the main force driving the age-related decline in adult hippocampal neurogenesis. Behav. Brain Res 2012; 227: 433-39.
41. Steiner B, Klempin F, Wang L, et al. Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 2006; 54: 805-14.
42. Bonaguidi MA, Wheeler MA, Shapiro JS, et al. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011; 145: 1142-55.
43. Encinas JM, Vaahtokari A, Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 2006; 103: 8233-8.
44. Suh H, Consiglio A, Ray J, et al. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 2007; 1: 515-28.
45. Sierra A, Encinas JM, Deudero JJ, et al. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010; 7: 483-95.
46. Tozuka Y, Fukuda S, Namba T, et al. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 2005; 47: 803-15.
47. Seri B, Garcia-Verdugo JM, Collado-Morente L, et al. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 2004; 478: 359-78.
48. Stanfield BB, Trice JE. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 1988; 72: 399-406.
49. 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.
50. Overstreet Wadiche L, Bromberg DA, Bensen AL, et al. GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 2005; 94: 4528-32.
51. Wang LP, Kempermann G, Kettenmann H. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 2005; 29: 181-9.
52. 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: 559-66.
53. Toni N, Teng EM, Bushong EA, et al. Synapse formation on neurons born in the adult hippocampus. Nature neuroscience 2007; 10: 727-34.
54. Aimone JB, Deng W, Gage FH. Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 2011; 70: 589-96.
55. Lacefield CO, Itskov V, Reardon T, et al. Effects of adultgenerated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 2012; 22: 106-16.
56. Hodge RD, Kowalczyk TD, Wolf SA, et al. Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J Neurosci 2008; 28: 3707-17.
57. Encinas JM, Hamani C, Lozano AM, et al. Neurogenic hippocampal targets of deep brain stimulation. J Comp Neurol 2011; 519: 6-20.
58. Huttmann K, Sadgrove M, Wallraff A, et al. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur J Neurosci 2003; 18: 2769-78.
59. Segi-Nishida E, Warner-Schmidt JL, Duman RS. Electroconvulsive seizure and VEGF increase the proliferation of neural stem-like cells in rat hippocampus. Proc Natl Acad Sci USA 2008; 105: 11352-7.
60. Namba T, Maekawa M, Yuasa S, et al. The Alzheimer's disease drug memantine increases the number of radial glia-like progenitor cells in adult hippocampus. Glia 2009; 57: 1082-90.
61. Maekawa M, Namba T, Suzuki E, et al. NMDA receptor antagonist memantine promotes cell proliferation and production of mature granule neurons in the adult hippocampus. Neurosci Res 2009; 63: 259-66.
62. Czeh B, Welt T, Fischer AK, et al. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 2002; 52: 1057-65.
63. Shors TJ, Townsend DA, Zhao M, et al. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002; 12: 578-84.
64. Dupret D, Revest J-M, Koehl M, et al. Spatial Relational Memory Requires Hippocampal Adult Neurogenesis. PLoS One 2008; 3:
65. Rolls ET, Kesner RP. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 2006; 79: 1-48.
66. Clelland CD, Choi M, Romberg C, et al. A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation. Science (New York, N.Y.) 2009; 325: 210-13.
67. Sahay A, Scobie KN, Hill AS, et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011; 472: 466-70.
68. Richter-Levin G, Segal M. Effects of serotonin releasers on dentate granule cell excitability in the rat. Experimental brain research. Experimentelle Hirnforschung. Expérimentation cérébrale 1990; 82: 199-207.
69. Kitchigina V, Vankov A, Harley C, et al. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur J Neurosci 1997; 9: 41-47.
70. Levkovitz Y, Segal M. Serotonin 5-HT1A receptors modulate hippocampal reactivity to afferent stimulation J Neurosci 1997; 17: 5591-98.
71. Castro M, Diaz A, del Olmo E, et al. Chronic fluoxetine induces opposite changes in G protein coupling at pre and postsynaptic 5-HT1A receptors in rat brain. Neuropharmacology 2003; 44: 93-101.
72. Brezun JM, Daszuta A. Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 1999; 89: 999-1002.
73. Soumier A, Banasr M, Goff LK, et al. Region-and phasedependent effects of 5-HT(1A) and 5-HT(2C) receptor activation on adult neurogenesis. Eur Neuropsychopharmacol 2010; 20: 336-45.
74. Lucas G, Rymar VV, Du J, et al. Serotonin(4) (5-HT(4)) receptor agonists are putative antidepressants with a rapid onset of action. Neuron 2007; 55: 712-25.
75. Pascual-Brazo J, Castro E, Diaz A, et al. Modulation of neuroplasticity pathways and antidepressant-like behavioral responses following the short-term (3 and 7 days) administration of the 5-HT(4) receptor agonist RS67333. Int J Neuropsychopharmacol 2012; 15: 631-43.
76. Banasr M, Hery M, Printemps R, et al. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 2004; 29: 450-60.
77. Klempin F, Babu H, De Pietri Tonelli D, et al. Oppositional effects of serotonin receptors 5-HT1a, 2, and 2c in the regulation of adult hippocampal neurogenesis. Front Mol Neurosci 2010; 3:
78. Navailles S, Hof PR, Schmauss C. Antidepressant drug-induced stimulation of mouse hippocampal neurogenesis is age-dependent and altered by early life stress. J Comp. Neurol 2008; 509: 372-81.
79. Miller BH, Schultz LE, Gulati A, et al. Genetic Regulation of Behavioral and Neuronal Responses to Fluoxetine. Neuropsychopharmacology 2008; 33: 1312-22.
80. Malberg JE, Duman RS. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003; 28: 1562-71.
81. Wang J-W, David DJ, Monckton JE, et al. Chronic Fluoxetine Stimulates Maturation and Synaptic Plasticity of Adult-Born Hippocampal Granule Cells. J Neurosci 2008; 28: 1374-84.
82. Couillard-Despres S, Wuertinger C, Kandasamy M, et al. Ageing abolishes the effects of fluoxetine on neurogenesis. Mol. Psychiatry 2009; 14: 856-64.
83. Surget A, Tanti A, Leonardo ED, et al. Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 2011; 16: 1177-88.
84. Bessa JM, Ferreira D, Melo I, et al. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 2009; 14: 764-73, 39.
85. Surget A, Saxe M, Leman S, et al. Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biological psychiatry 2008; 64: 293-301.
86. Alonso R, Griebel G, Pavone G, et al. Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol. Psychiatry 2004; 9: 278-86, 24.
87. Bourin M, Mocaër E, Porsolt R. Antidepressant-like activity of S 20098 (agomelatine) in the forced swimming test in rodents: involvement of melatonin and serotonin receptors. J Psychiatry Neurosci 2004; 29: 126-33.
88. Papp M, Gruca P, Boyer P-A, et al. Effect of agomelatine in the chronic mild stress model of depression in the rat. Neuropsychopharmacology 2003; 28: 694-703.
89. Lôo H, Hale A, D'Haenen H. Determination of the dose of agomelatine, a melatoninergic agonist and selective 5-HT(2C) antagonist, in the treatment of major depressive disorder: a placebo-controlled dose range study. Int Clin Psychopharmacol 2002; 17: 239-47.
90. Lôo H, Daléry J, Macher JP, et al. [Pilot study comparing in blind the therapeutic effect of two doses of agomelatine, melatoninagonist and selective 5HT2c receptors antagonist, in the treatment of major depressive disorders]. Encephale 2003; 29: 165-71.
91. Tardito D, Molteni R, Popoli M, et al. Synergistic mechanisms involved in the antidepressant effects of agomelatine. Eur Neuropsychopharmacol 2012; 22 Suppl 3: S482-6.
92. Banasr M, Soumier A, Hery M, et al. Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis. Biol Psychiatry 2006; 59: 1087-96.
93. 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: 2390-403.
94. Ramírez-Rodríguez G, Klempin F, Babu H, et al. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 2009; 34: 2180-91.
95. Dagytė G, Crescente I, Postema F, et al. Agomelatine reverses the decrease in hippocampal cell survival induced by chronic mild stress. Behav Brain Res 2011; 218: 121-28.
96. Morley-Fletcher S, Mairesse J, Soumier A, et al. Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats. Psychopharmacology (Berl.) 2011; 217: 301-13.
97. Rainer Q, Xia L, Guilloux JP, et al. Beneficial behavioral and neurogenic effects of agomelatine in a model of depression/anxiety. Int J Neuropsychopharmacol 2011; 1-15.
98. Païzanis E, Renoir T, Lelievre V, et al. Behavioral and neuroplastic effects of the new-generation antidepressant agomelatine compared to fluoxetine in glucocorticoid receptor-impaired mice. Int J Neuropsychopharmacol 2010; 13: 759-74.
99. Murphy BE, Filipini D, Ghadirian AM. Possible use of glucocorticoid receptor antagonists in the treatment of major depression: preliminary results using RU 486. J Psychiatry Neurosci 1993; 18: 209-13.
100. [100] Blasey CM, Block TS, Belanoff JK, et al. Efficacy and safety of mifepristone for the treatment of psychotic depression. J Clin Psychopharmacol 2011; 31: 436-40.
101. [101] Oomen CA, Mayer JL, de Kloet ER, et al. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 2007; 26: 3395-401.
102. [102] Mayer JL, Klumpers L, Maslam S, et al. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol 2006; 18: 629-31.
103. [103] Hu P, Oomen C, van Dam A-M, et al. A single-day treatment with mifepristone is sufficient to normalize chronic glucocorticoid induced suppression of hippocampal cell proliferation. PLoS One 2012; 7:
104. [104] Llorens-Martín M, Trejo JL. Mifepristone prevents stress-induced apoptosis in newborn neurons and increases AMPA receptor expression in the dentate gyrus of C57/BL6 mice. PLoS One 2011; 6:
105. [105] Garcia A, Steiner B, Kronenberg G, et al. Age-dependent expression of glucocorticoid-and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 2004; 3: 363-71.
106. [106] de Kloet ER, Sutanto W, van den Berg DT, et al. Brain mineralocorticoid receptor diversity: functional implications. J Steroid Biochem. Mol. Biol 1993; 47: 183-90.
107. [107] Alfarez DN, Wiegert O, Joels M, et al. Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience 2002; 115: 1119-26.
108. [108] Berman RM, Cappiello A, Anand A, et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000; 47: 351-4.
109. [109] Machado-Vieira R, Salvadore G, Diazgranados N, et al. Ketamine and the next generation of antidepressants with a rapid onset of action. Pharmacol Ther 2009; 123: 143-50.
110. [110] Covvey JR, Crawford AN, Lowe DK. Intravenous ketamine for treatment-resistant major depressive disorder. Ann Pharmacother 2012; 46: 117-23.
111. [111] Li N, Lee B, Liu R-J, et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science (New York, N.Y.) 2010; 329: 959-64.
112. [112] Mathews DC, Henter ID, Zarate CA. Targeting the glutamatergic system to treat major depressive disorder: rationale and progress to date. Drugs 2012; 72: 1313-33.
113. [113] Keilhoff G, Bernstein H-G, Becker A, et al. Increased neurogenesis in a rat ketamine model of schizophrenia. Biological Psychiatry 2004; 56: 317-22.
114. [114] Tung A, Herrera S, Fornal CA, et al. The effect of prolonged anesthesia with isoflurane, propofol, dexmedetomidine, or ketamine on neural cell proliferation in the adult rat. Anesth Analg 2008; 106: 1772-7.
115. [115] Zarate CA, Jr., Singh JB, Quiroz JA, et al. A double-blind, placebo-controlled study of memantine in the treatment of major depression. Am J Psychiatry 2006; 163: 153-55.
116. [116] Réus GZ, Abelaira HM, Stringari RB, et al. Memantine treatment reverses anhedonia, normalizes corticosterone levels and increases BDNF levels in the prefrontal cortex induced by chronic mild stress in rats. Metab Brain Dis 2012; 27: 175-82.
117. [117] Jin K, Xie L, Mao XO, et al. Alzheimer's disease drugs promote neurogenesis. Brain Res 2006; 1085: 183-8.
118. [118] Zarate CA, Jr., Payne JL, Quiroz J, et al. An open-label trial of riluzole in patients with treatment-resistant major depression. Am J Psychiatry 2004; 161: 171-74.
119. [119] Sanacora G, Kendell SF, Levin Y, et al. Preliminary evidence of riluzole efficacy in antidepressant-treated patients with residual depressive symptoms. Biological psychiatry 2007; 61: 822-25.
120. [120] Katoh-Semba R, Asano T, Ueda H, et al. Riluzole enhances expression of brain-derived neurotrophic factor with consequent proliferation of granule precursor cells in the rat hippocampus. FASEB J 2002; 16: 1328-30.
121. [121] Zhao C, Warner-Schmidt J, Duman RS, et al. Electroconvulsive seizure promotes spine maturation in newborn dentate granule cells in adult rat. Dev Neurobiol 2012; 72: 937-42.
122. [122] Madsen TM, Treschow A, Bengzon J, et al. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000; 47: 1043-9.
123. [123] Scott BW, Wojtowicz JM, Burnham WM. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 2000; 165: 231-6.
124. [124] Hellsten J, Wennstrom M, Mohapel P, et al. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. Eur J Neurosci 2002; 16: 283-90.
125. [125] Kaae SS, Chen F, Wegener G, et al. Quantitative hippocampal structural changes following electroconvulsive seizure treatment in a rat model of depression. Synapse 2012; 66: 667-76.
126. [126] Malone DA, Jr., Dougherty DD, Rezai AR, et al. Deep brain stimulation of the ventral capsule/ventral striatum for treatmentresistant depression. Biol Psychiatry 2009; 65: 267-75.
127. [127] Lozano AM, Giacobbe P, Hamani C, et al. A multicenter pilot study of subcallosal cingulate area deep brain stimulation for treatment-resistant depression. J Neurosurg 2012; 116: 315-22.
128. [128] Bewernick BH, Kayser S, Sturm V, et al. Long-term effects of nucleus accumbens deep brain stimulation in treatment-resistant depression: evidence for sustained efficacy. Neuropsychopharmacology 2012; 37: 1975-85.
129. [129] Schmuckermair C, Gaburro S, Sah A, et al. Behavioral and Neurobiological Effects of Deep Brain Stimulation in a Mouse Model of High Anxiety and Depression-Like Behavior. Neuropsychopharmacology 2013;
130. [130] Scobie KN, Hall BJ, Wilke SA, et al. Kruppel-like factor 9 is necessary for late-phase neuronal maturation in the developing dentate gyrus and during adult hippocampal neurogenesis. J Neurosci 2009; 29: 9875-87.
131. [131] Young SZ, Taylor MM, Wu S, et al. NKCC1 knockdown decreases neuron production through GABA(A)-regulated neural progenitor proliferation and delays dendrite development. J Neurosci 2012; 32: 13630-8.
132. [132] Gould E, McEwen BS, Tanapat P, et al. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997; 17: 2492-8.
133. [133] Pereira AC, Huddleston DE, Brickman AM, et al. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 2007; 104: 5638-43.
134. [134] Manganas LN, Zhang X, Li Y, et al. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 2007; 318: 980-5.
135. [135] Reif A, Fritzen S, Finger M, et al. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 2006; 11: 514-22.
136. [136] Boldrini M, Underwood MD, Hen R, et al. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 2009; 34: 2376-89.
137. [137] Boldrini M, Hen R, Underwood MD, et al. Hippocampal Angiogenesis and Progenitor Cell Proliferation Are Increased with Antidepressant Use in Major Depression. Biological psychiatry 2012;
138. [138] Hickie I, Naismith S, Ward PB, et al. Reduced hippocampal volumes and memory loss in patients with early-and late-onset depression. Br J Psychiatry 2005; 186: 197-202.
139. [139] Huang GJ, Ben-David E, Tort Piella A, et al. Neurogenomic evidence for a shared mechanism of the antidepressant effects of exercise and chronic fluoxetine in mice. PLoS One 2012; 7:
140. [140] Su XW, Li XY, Banasr M, et al. Eszopiclone and fluoxetine enhance the survival of newborn neurons in the adult rat hippocampus. Int J Neuropsychopharmacol 2009; 12: 1421-28.
141. [141] Wu X, Castrén E. Co-treatment with diazepam prevents the effects of fluoxetine on the proliferation and survival of hippocampal dentate granule cells. Biological Psychiatry 2009; 66: 5-8.
142. [142] Zhou Q-G, Hu Y, Wu D-L, et al. Hippocampal telomerase is involved in the modulation of depressive behaviors. J Neurosci 2011; 31: 12258-69.
143. [143] Colditz MJ, Catts VS, Al-menhali N, et al. p75 neurotrophin receptor regulates basal and fluoxetine-stimulated hippocampal neurogenesis. Experimental brain research. Experimentelle Hirnforschung. Expérimentation cérébrale 2010; 200: 161-67.
144. [144] Diaz SL, Doly S, Narboux-Nême N, et al. 5-HT(2B) receptors are required for serotonin-selective antidepressant actions. Mol. Psychiatry 2012; 17: 154-63.
145. [145] Eitan R, Landshut G, Lifschytz T, et al. The thyroid hormone, triiodothyronine, enhances fluoxetine-induced neurogenesis in rats: possible role in antidepressant-augmenting properties. Int J Neuropsychopharmacol 2010; 13: 553-61.
146. [146] Fournier NM, Lee B, Banasr M, et al. Vascular endothelial growth factor regulates adult hippocampal cell proliferation through MEK/ERK-and PI3K/Akt-dependent signaling. Neuropharmacology 2012;
147. [147] Hodes GE, Hill-Smith TE, Lucki I. Fluoxetine treatment induces dose dependent alterations in depression associated behavior and neural plasticity in female mice. Neurosci Lett 2010; 484: 12-16.
148. [148] Marlatt MW, Lucassen PJ, van Praag H. Comparison of neurogenic effects of fluoxetine, duloxetine and running in mice. Brain Res 2010; 1341: 93-99.
149. [149] Pechnick RN, Zonis S, Wawrowsky K, et al. Antidepressants stimulate hippocampal neurogenesis by inhibiting p21 expression in the subgranular zone of the hipppocampus. PLoS One 2011; 6:
150. [150] Spoelgen R, Meyer A, Moraru A, et al. A novel flow cytometrybased technique to measure adult neurogenesis in the brain. J Neurochem 2011; 119: 165-75.
151. [151] Bilsland JG, Haldon C, Goddard J, et al. A rapid method for the quantification of mouse hippocampal neurogenesis in vivo by flow cytometry. Validation with conventional and enhanced immunohistochemical methods. J Neurosci Methods 2006; 157: 54-63.
152. [152] Manev H, Uz T, Smalheiser NR, et al. Antidepressants alter cell proliferation in the adult brain in vivo and in neural cultures in vitro. Eur J Pharmacol 2001; 411: 67-70.
153. [153] Sairanen M, Lucas G, Ernfors P, et al. Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci 2005; 25: 1089-94.
154. [154] Lyons L, ElBeltagy M, Umka J, et al. Fluoxetine reverses the memory impairment and reduction in proliferation and survival of hippocampal cells caused by methotrexate chemotherapy. Psychopharmacology (Berl.) 2011; 215: 105-15.
155. [155] David DJ, Klemenhagen KC, Holick KA, et al. Efficacy of the MCHR1 antagonist N-[3-(1-{[4-(3,4-difluorophenoxy)phenyl] methyl}(4-piperidyl))-4-methylphenyl]-2-methylpropanamide (SNAP 94847) in mouse models of anxiety and depression following acute and chronic administration is independent of hippocampal neurogenesis. J Pharmacol Exp Ther 2007; 321: 237-48.