Implications of adult hippocampal neurogenesis in antidepressant action

Journal of Psychiatry and Neuroscience

Volumn 29, Issue 3, 2004, Pages 196-205

  Malberg, Jessica E ^a,b  

^a PFIZER INC   (United States)

^b Discovery Research   (United States)

Author keywords

Antidepressive agents; Depression; Hippocampus; Models, animal; Neurons

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; BROXURIDINE; CORTICOSTERONE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIZOCILPINE; DNA; ESTROGEN; FLUOXETINE; HALOPERIDOL; REBOXETINE; ROLIPRAM; THYMIDINE; TIANEPTINE; TRANYLCYPROMINE;

BRAIN CORTEX; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONFERENCE PAPER; CORRELATION ANALYSIS; CORTICOSTERONE RELEASE; DENTATE GYRUS; DEPRESSION; DRUG EFFECT; ELECTRIC SHOCK; ENVIRONMENTAL FACTOR; GLIA; GLIA CELL; HIPPOCAMPUS; HORMONAL REGULATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATHOPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; SEX DIFFERENCE; SOCIAL PSYCHOLOGY; STRESS; TRANSCRANIAL MAGNETIC STIMULATION;

ANTIDEPRESSIVE AGENTS; CELL MOVEMENT; DEPRESSIVE DISORDER, MAJOR; HIPPOCAMPUS; HUMANS; NEURONS; STRESS, PSYCHOLOGICAL;

EID: 3042660266     PISSN: 11804882     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Conference Paper

References (94)

1. Gould E, Gross CG. Neurogenesis in adult mammals: some progress and problems. J Neurosci 2002;22(3):619-23.
2. Kaplan MS. Environment complexity stimulates visual cortex neurogenesis: death of a dogma and a research career. Trends Neurosci 2001;24(10):617-20.
3. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003;301(5634): 805-9.
4. Duman RS, Nakagawa S, Malberg J, Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 2001;25(6):836-44.
5. D'Sa C, Duman RS. Antidepressants and neuroplasticity. Bipolar Disord 2002;4(3):183-94.
6. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997;386(6624):493-5.
7. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med 1998;4(11):1313-7.
8. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, Fuchs E. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci U S A 1999;96(9):5263-7.
9. Altman J, Das GD. Postnatal neurogenesis in the guinea-pig. Nature 1967;214(93):1098-101.
10. Cameron HA, Woolley CS, McEwen BS, Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993;56(2):337-44.
11. Hastings NB, Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 1999;413(1):146-54.
12. Van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature 2002;415(6875):1030-4.
13. Altman J, Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124(3):319-35.
14. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977;197 (4308):1092-4.
15. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991;231(4):482-97.
16. Malberg JE, Eisch AJ, Nestler EJ, Duman RS. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000;20(24):9104-10.
17. Nakagawa S, Kim JE, Lee R, Chen J, Fujioka T, Malberg J, et al. Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 2002;22(22):9868-76.
18. Nowakowski RS, Lewin SB, Miller MW. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 1989;18(3):311-8.
19. Eisch AJ. Adult neurogenesis: implications for psychiatry. Prog Brain Res 2002;138:315-42.
20. Cameron HA, McKay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001;435(4):406-17.
21. Hayes N, Nowakowski R. Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res Dev Brain Res 2002;134(1-2):77-85.
22. Gould E, Reeves AJ, Graziano MS, Gross CG. Neurogenesis in the neocortex of adult primates. Science 1999;286(5439):548-52.
23. Gould E, Vail N, Wagers M, Gross CG. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci U S A 2001;98(19):10910-7.
24. Rakic P. Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci 2002;3(1):65-71.
25. Kempermann G. Regulation of adult hippocampal neurogenesis - implications for novel theories of major depression. Bipolar Disord 2002;4(1):17-33.
26. Duman RS, Heninger GR, Nestler EJ. A molecular and cellular theory of depression. Arch Gen Psychiatry 1997;54(7):597-606.
27. Cryan JF, Markou A, Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002;23(5):238-45.
28. Tanapat P, Galea LA, Gould E. Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int J Dev Neurosci 1998;16(3-4):235-9.
29. Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 2001;437(4):496-504.
30. Malberg JE, Duman RS. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003;28(9):1562-71.
31. Pham K, Nacher J, Hof PR, McEwen BS. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 2003;17(4):879-86.
32. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997;17(7):2492-8.
33. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A 1998;95(6):3168-71.
34. Czeh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M, et al. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci U S A 2001;98(22):12796-801.
35. Czeh B, Welt T, Fischer AK, Erhardt A, Schmitt W, Muller MB, et al. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 2002;52(11):1057-65.
36. Malberg JE, Shirayama Y, Duman RS. Effects of antidepressant treatment and learned helplessness training on hippocampal neurogenesis in the adult rat [poster]. Presented at the Society for Neuroscience meeting; 2001 Nov 10-15; San Diego (CA).
37. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 2000;3(8):799-806.
38. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 2000;97(20):11032-7.
39. Schmitz C, Rhodes ME, Bludau M, Kaplan S, Ong P, Ueffing I, et al. Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry 2002;7(7):810-3.
40. Shors TJ, Chua C, Falduto J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 2001;21(16):6292-7.
41. Ustun TB. Cross-national epidemiology of depression and gender. J Gend Specif Med 2000;3(2):54-8.
42. Tanapat P, Hastings NB, Reeves AJ, Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 1999;19(14):5792-801.
43. McEwen BS. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 2001;933: 265-77.
44. Duman RS, Malberg J, Nakagawa S. Regulation of adult neurogenesis by psychotropic drugs and stress. J Pharmacol Exp Ther 2001;299(2):401-7.
45. Magarinos AM, Deslandes A, McEwen BS. Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur J Pharmacol 1999;371(2-3):113-22.
46. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999;22:105-22.
47. Watanabe Y, Gould E, Daniels DC, Cameron H, McEwen BS. Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur J Pharmacol 1992;222:157-62.
48. McKittrick CR, Magarinos AM, Blanchard DC, Blanchard RJ, McEwen BS, Sakai RR. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000;36(2):85-94.
49. Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatrie disorders. Arch Gen Psychiatry 2000;57(10): 925-35.
50. Cameron HA, Tanapat P, Gould E. Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998;82(2):349-54.
51. Cameron HA, Woolley CS, Gould E. Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Res 1993;611(2):342-6.
52. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM. Neurobiology of depression. Neuron 2002;34(1):13-25.
53. Nakagawa S, Kim JE, Lee R, Malberg JE, Chen J, Steffen C, et al. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 2002;22(9):3673-82.
54. Madsen TM, Treschow A, Bengzon J, Bolwig TG, Lindvall O, Tingstrom A. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000;47(12):1043-9.
55. Hellsten J, Wennstrom M, Mohapel P, Ekdahl CT, Bengzon J, Tingstrom A. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. Eur J Neurosci 2002;16(2):283-90.
56. Manev H, Uz T, Smalheiser NR, Manev R. Antidepressants alter cell proliferation in the adult brain in vivo and in neural cultures in vitro. Eur J Pharmacol 2001;411(1-2):67-70.
57. Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci 2002;22(3):629-34.
58. Rupniak NM. Elucidating the antidepressant actions of substance P (NK1 receptor) antagonists. Curr Opin Investig Drugs 2002;3(2):257-61.
59. Bai F, Bergeron M, Nelson DL. Chronic AMPA receptor potentiator (LY451646) treatment increases cell proliferation in adult rat hippocampus. Neuropharmacology 2003;44(8):1013-21.
60. Ballas C, Staab JP, Evans DL. Strategies for treatment-resistant depression. Psychopharmacol Bull 2002;36(4 Suppl 3):39-62.
61. Nibuya M, Morinobu S, Duman RS. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 1995;15(11): 7539-47.
62. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS. Hippocampal volume reduction in major depression. Am J Psychiatry 2000;157(1):115-8.
63. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, et al. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry 1995;152(7):973-81.
64. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci U S A 1996;93(9):3908-13.
65. Manji HK, Quiroz JA, Sporn J, Payne JL, Denicoff K, A Gray N, et al. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 2003;53(8):707-42.
66. Ongur D, Drevets WC, Price JL. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 1998;95(22):13290-5.
67. Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, Meltzer HY, et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999;45(9):1085-98.
68. Cotter D, Mackay D, Landau S, Kerwin R, Everall I. Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 2001;58(6):545-53.
69. Drevets WC. Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog Brain Res 2000;126:413-31.
70. Sheline YI, Gado MH, Kraemer HC. Untreated depression and hippocampal volume loss. Am J Psychiatry 2003;160(8):1516-8.
71. Sheline YI, Sanghavi M, Mintun MA, Gado MH. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 1999;19(12):5034-43.
72. MacQueen GM, Campbell S, McEwen BS, Macdonald K, Amano S, Joffe RT, et al. Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci U S A 2003;100(3):1387-92.
73. Vermetten E, Vythilingam M, Southwick SM, Charney DS, Bremner JD. Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry 2003;54(7):693-702.
74. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci 2002;5(11):1242-7.
75. Miller DB, O'Callaghan JP. Effects of aging and stress on hippocampal structure and function. Metabolism 2003;52(10 Suppl 2):17-21.
76. Starkman MN, Giordani B, Gebarski SS, Berent S, Schork MA, Schteingart DE. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol Psychiatry 1999;46(12):1595-602.
77. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 2001;21(17):6706-17.
78. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 2000;20(8):2896-903.
79. Poe BH, Linville C, Riddle DR, Sonntag WE, Brunso-Bechtold JK. Effects of age and insulin-like growth factor-1 on neuron and synapse numbers in area CA3 of hippocampus. Neuroscience 2001;107(2):231-8.
80. Coppell AL, Pei Q, Zetterstrom TS. Bi-phasic change in BDNF gene expression following antidepressant drug treatment. Neuropharmacology 2003;44(7):903-10.
81. Siuciak JA, Lewis DR, Wiegand SJ, Lindsay RM. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav 1997;56(1):131-7.
82. Shirayama Y, Chen AC, Nakagawa S, Russell DS, Duman RS. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 2002;22(8): 3251-61.
83. Chen B, Dowlatshahi D, MacQueen GM, Wang JF, Young LT. Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol Psychiatry 2001;50(4):260-5.
84. Saarelainen T, Hendolin P, Lucas G, Koponen E, Sairanen M, MacDonald E, et al. Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J Neurosci 2003;23 (1):349-57.
85. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 1996;726(1-2):49-56.
86. Greenwood BN, Foley TE, Day HE, Campisi J, Hammack SH, Campeau S, et al. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 2003;23(7):2889-98.
87. Russo-Neustadt A, Ha T, Ramirez R, Kesslak JP. Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model. Behav Brain Res 2001;120(1):87-95.
88. Conti AC, Cryan JF, Dalvi A, Lucki I, Blendy JA. cAMP response element-binding protein is essential for the upregulation of brain-derived neurotrophic factor transcription, but not the behavioral or endocrine responses to antidepressant drugs. J Neurosci 2002;22(8):3262-8.
89. Zimmer DB, Cornwall EH, Landar A, Song W. The S100 protein family: history, function, and expression. Brain Res Bull 1995;37(4):417-29.
90. Nishiyama H, Knopfel T, Endo S, Itohara S. Glial protein S100B modulates long-term neuronal synaptic plasticity. Proc Natl Acad Sci U S A 2002;99(6):4037-42.
91. Manev R, Uz T, Manev H. Fluoxetine increases the content of neurotrophic protein SlOObeta in the rat hippocampus. Eur J Pharmacol 2001;420(2-3):R1-2.
92. Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult neural stem cells [comment]. Nature 2002;417 (6884):39-44.
93. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001;410(6826):372-6.
94. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002;12(5):578-84.