A molecular and cellular theory of depression.

Recent studies have begun to characterize the actions of stress and antidepressant treatments beyond the neurotransmitter and receptor level. This work has demonstrated that long-term antidepressant treatments result in the sustained activation of the cyclic adenosine 3',5'-monophosphate system in specific brain regions, including the increased function and expression of the transcription factor cyclic adenosine monophosphate response element-binding protein. The activated cyclic adenosine 3',5'-monophosphate system leads to the regulation of specific target genes, including the increased expression of brain-derived neurotrophic factor in certain populations of neurons in the hippocampus and cerebral cortex. The importance of these changes is highlighted by the discovery that stress can decrease the expression of brain-derived neurotrophic factor and lead to atrophy of these same populations of stress-vulnerable hippocampal neurons. The possibility that the decreased size and impaired function of these neurons may be involved in depression is supported by recent clinical imaging studies, which demonstrate a decreased volume of certain brain structures. These findings constitute the framework for an updated molecular and cellular hypothesis of depression, which posits that stress-induced vulnerability and the therapeutic action of antidepressant treatments occur via intracellular mechanisms that decrease or increase, respectively, neurotrophic factors necessary for the survival and function of particular neurons. This hypothesis also explains how stress and other types of neuronal insult can lead to depression in vulnerable individuals and it outlines novel targets for the rational design of fundamentally new therapeutic agents.

[1]  J. Siuciak,et al.  Antidepressant-Like Effect of Brain-derived Neurotrophic Factor (BDNF) , 1997, Pharmacology Biochemistry and Behavior.

[2]  R. Sapolsky Why Stress Is Bad for Your Brain , 1996, Science.

[3]  B. McEwen,et al.  Chronic Psychosocial Stress Causes Apical Dendritic Atrophy of Hippocampal CA3 Pyramidal Neurons in Subordinate Tree Shrews , 1996, The Journal of Neuroscience.

[4]  J. Csernansky,et al.  Hippocampal atrophy in recurrent major depression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Duman,et al.  Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  R. Salomon,et al.  Clinical and biochemical effects of catecholamine depletion on antidepressant-induced remission of depression. , 1996, Archives of general psychiatry.

[7]  E. Nestler,et al.  Regulation of CREB expression: in vivo evidence for a functional role in morphine action in the nucleus accumbens. , 1996, The Journal of pharmacology and experimental therapeutics.

[8]  E. Nestler,et al.  Opposing effects of morphine and the neurotrophins, NT-3, NT-4, and BDNF, on locus coeruleus neurons in vitro , 1995, Brain Research.

[9]  C. Altar,et al.  Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  L. Fitzgerald,et al.  Review : Stress, Antidepressant Treatments, and Neurotrophic Factors: Molecular and Cellular Mechanisms , 1995 .

[11]  R. Duman,et al.  Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  D. Lo Neurotrophic factors and synaptic plasticity , 1995, Neuron.

[13]  H. Thoenen Neurotrophins and Neuronal Plasticity , 1995, Science.

[14]  L. Friedman,et al.  Meta-analyses of studies of ventricular enlargement and cortical sulcal prominence in mood disorders. Comparisons with controls or patients with schizophrenia. , 1995, Archives of general psychiatry.

[15]  I. Black,et al.  Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[16]  J. Habener,et al.  Expression of the gene encoding transcription factor cyclic adenosine 3',5'-monophosphate (cAMP) response element-binding protein (CREB): regulation by follicle-stimulating hormone-induced cAMP signaling in primary rat Sertoli cells. , 1995, Endocrinology.

[17]  H. Manji,et al.  Signal transduction pathways. Molecular targets for lithium's actions. , 1995, Archives of general psychiatry.

[18]  S. Southwick,et al.  MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. , 1995, The American journal of psychiatry.

[19]  M. Schwaninger,et al.  Inhibition by antidepressant drugs of cyclic AMP response element-binding protein/cyclic AMP response element-directed gene transcription. , 1995, Molecular pharmacology.

[20]  R. Duman,et al.  Chronic Antidepressant Treatment Down-Regulates the Induction of c-fos mRNA in Response to Acute Stress in Rat Frontal Cortex , 1995, Neuropsychopharmacology.

[21]  E. Azmitia,et al.  5-HT1A agonist and dexamethasone reversal of para-chloroamphetamine induced loss of MAP-2 and synaptophysin immunoreactivity in adult rat brain , 1995, Brain Research.

[22]  M E Greenberg,et al.  Calcium signaling in neurons: molecular mechanisms and cellular consequences. , 1995, Science.

[23]  E. Schuman,et al.  Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus , 1995, Science.

[24]  R. Kvetňanský,et al.  Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  F. Holsboer,et al.  Do antidepressants stabilize mood through actions on the hypothalamic-pituitary-adrenocortical system? , 1995, Trends in Neurosciences.

[26]  A. Sleight,et al.  Identification of 5-hydroxytryptamine7 receptor binding sites in rat hypothalamus: sensitivity to chronic antidepressant treatment. , 1995, Molecular pharmacology.

[27]  O. Lindvall,et al.  Neurotrophins and brain insults , 1994, Trends in Neurosciences.

[28]  Stanley J. Wiegand,et al.  Neurotrophic factors: from molecule to man , 1994, Trends in Neurosciences.

[29]  E. Nestler,et al.  Regulation of expression of cAMP response element-binding protein in the locus coeruleus in vivo and in a locus coeruleus-like cell line in vitro. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Duman,et al.  Agonist and Cyclic AMP‐Mediated Regulation of β1‐Adrenergic Receptor mRNA and Gene Transcription in Rat C6 Glioma Cells , 1994, Journal of neurochemistry.

[31]  R. Salomon,et al.  Serotonin and the neurobiology of depression. Effects of tryptophan depletion in drug-free depressed patients. , 1994, Archives of general psychiatry.

[32]  M. Mattson,et al.  Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  N. Belluardo,et al.  Expression of Neurotrophins and Their Receptors in Primary Astroglial Cultures: Induction by Cyclic AMP‐Elevating Agents , 1994, Journal of neurochemistry.

[34]  C. Montigny,et al.  Current advances and trends in the treatment of depression. , 1994, Trends in pharmacological sciences.

[35]  E. Nestler,et al.  Chronic electroconvulsive seizure (ECS) treatment results in expression of a long-lasting AP-1 complex in brain with altered composition and characteristics , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  J. Darnell,et al.  Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. , 1994, Science.

[37]  M E Greenberg,et al.  Requirement for BDNF in activity-dependent survival of cortical neurons. , 1994, Science.

[38]  H. Manji,et al.  Lithium Decreases Membrane‐Associated Protein Kinase C in Hippocampus: Selectivity for the α Isozyme , 1993, Journal of neurochemistry.

[39]  J. Warsh,et al.  Lithium Modulation of Phosphoinositide Signaling System in Rat Cortex: Selective Effect on Phorbol Ester Binding , 1993, Journal of neurochemistry.

[40]  R. Duman,et al.  Chronic Electroconvulsive Seizures Increase the Expression of Serotonin2 Receptor mRNA in Rat Frontal Cortex , 1993, Journal of neurochemistry.

[41]  K. Johnson,et al.  Topographic patterns of brain activity in response to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  J. Blenis,et al.  Signal transduction via the MAP kinases: proceed at your own RSK. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[43]  T. Meyer,et al.  Cyclic adenosine 3',5'-monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins. , 1993, Endocrine reviews.

[44]  R. Duman,et al.  Regulation of β1‐Adrenergic Receptor mRNA and Ligand Binding by Antidepressant Treatments and Norepinephrine Depletion in Rat Frontal Cortex , 1993, Journal of neurochemistry.

[45]  C. Hudson,et al.  CNS signal transduction in the pathophysiology and pharmacotherapy of affective disorders and schizophrenia , 1993, Synapse.

[46]  M. Berridge Inositol trisphosphate and calcium signalling , 1993, Nature.

[47]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[48]  Y. Watanabe,et al.  Tianeptine attenuates stress-induced morphological changes in the hippocampus. , 1992, European journal of pharmacology.

[49]  Bruce S. McEwen,et al.  Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons , 1992, Brain Research.

[50]  S. Arndt,et al.  Depression in patients with acute traumatic brain injury. , 1992, The American journal of psychiatry.

[51]  E. Nestler,et al.  Coordinate Regulation of the Cyclic AMP System with Firing Rate and Expression of Tyrosine Hydroxylase in the Rat Locus Coeruleus: Effects of Chronic Stress and Drug Treatments , 1992, Journal of neurochemistry.

[52]  R. Lenox,et al.  Chronic lithium administration alters a prominent PKC substrate in rat hippocampus , 1992, Brain Research.

[53]  E. Nestler,et al.  Chronic lithium regulates the expression of adenylate cyclase and Gi-protein alpha subunit in rat cerebral cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[54]  H. Akil,et al.  Loss of glucocorticoid fast feedback in depression. , 1991, Archives of general psychiatry.

[55]  R. Stern,et al.  Depressive symptoms following stroke. , 1991, The American journal of psychiatry.

[56]  J. Warsh,et al.  Lithium decreases Gs, Gi-1 and Gi-2 α-subunit mRNA levels in rat cortex , 1991 .

[57]  R. Jope,et al.  Effects of chronic lithium treatment on protein kinase c and cyclic AMP-dependent protein phosphorylation , 1991, Biological Psychiatry.

[58]  M. Rasenick,et al.  Chronic Electroconvulsive Treatment Augments Coupling of the GTP‐Binding Protein Gs to the Catalytic Moiety of Adenylyl Cyclase in a Manner Similar to That Seen with Chronic Antidepressant Drugs , 1991, Journal of neurochemistry.

[59]  R. Nicoll,et al.  Mechanisms underlying long-term potentiation of synaptic transmission. , 1991, Annual review of neuroscience.

[60]  Bruce S. McEwen,et al.  Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons , 1990, Brain Research.

[61]  R. Sapolsky,et al.  Hippocampal damage associated with prolonged glucocorticoid exposure in primates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  E. Nestler,et al.  Chronic Electroconvulsive Seizures Down–Regulate Expression of the Immediate‐Early Genes c‐fos and c‐jun in Rat Cerebral Cortex , 1990, Journal of neurochemistry.

[63]  S. Nakamura Antidepressants induce regeneration of catecholaminergic axon terminals in the rat cerebral cortex , 1990, Neuroscience Letters.

[64]  R. Sapolsky Chapter 2 Glucocorticoids, hippocampal damage and the glutamatergic synapse , 1990 .

[65]  R. Duman,et al.  Chronic Antidepressant Administration Alters the Subcellular Distribution of Cyclic AMP‐Dependent Protein Kinase in Rat Frontal Cortex , 1989, Journal of neurochemistry.

[66]  G. Racagni,et al.  cAMP-dependent phosphorylation of soluble and crude microtubule fractions of rat cerebral cortex after prolonged desmethylimipramine treatment. , 1989, European journal of pharmacology.

[67]  I. Creese,et al.  Reevaluation of the regulation of beta-adrenergic receptor binding by desipramine treatment. , 1989, Molecular pharmacology.

[68]  R. Sapolsky,et al.  Hippocampal damage associated with prolonged and fatal stress in primates , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  M. Reding,et al.  Antidepressant therapy after stroke. A double-blind trial. , 1986, Archives of neurology.

[70]  J. Avorn,et al.  Increased Antidepressant Use in Patients Prescribed β-Blockers , 1986 .

[71]  B. McEwen,et al.  Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[72]  R. Horowski,et al.  Clinical effects of the neurotropic selective cAMP phosphodiesterase inhibitor rolipram in depressed patients: global evaluation of the preliminary reports , 1985 .

[73]  H. Wachtel,et al.  Potential antidepressant activity of rolipram and other selective cyclic adenosine 3′,5′-monophosphate phosphodiesterase inhibitors , 1983, Neuropharmacology.

[74]  M. Rasenick,et al.  Guanosine triphosphate activation of brain adenylate cyclase: enhancement by long-term antidepressant treatment. , 1983, Science.

[75]  E. Paykel,et al.  Psychiatric Side Effects of Antihypertensive Drugs Other Than Reserpine , 1982, Journal of clinical psychopharmacology.

[76]  F. Goodwin,et al.  Potentiation of antidepressant effects by L-triiodothyronine in tricyclic nonresponders. , 1982, The American journal of psychiatry.

[77]  D. Charney,et al.  Receptor sensitivity and the mechanism of action of antidepressant treatment. Implications for the etiology and therapy of depression. , 1981, Archives of general psychiatry.

[78]  S H Snyder,et al.  Long-term antidepressant treatment decreases spiroperidol-labeled serotonin receptor binding. , 1980, Science.

[79]  J. Vetulani,et al.  Mode of action of antidepressant drugs. , 1978, Biochemical pharmacology.

[80]  L. S. Kung,et al.  Development of β-adrenergic receptor subsensitivity by antidepressants , 1977, Nature.

[81]  J. Vetulani,et al.  Action of various antidepressant treatments reduces reactivity of noradrenergic cyclic AMP-generating system in limbic forebrain , 1975, Nature.

[82]  S. Gershon,et al.  Use of synthesis inhibitors in defining a role for biogenic amines during imipramine treatment in depressed patients. , 1975, Psychopharmacology communications.

[83]  A. Coppen The Biochemistry of Affective Disorders , 1967, British Journal of Psychiatry.

[84]  W. Bunney,et al.  Norepinephrine in depressive reactions. A review. , 1965, Archives of general psychiatry.

[85]  J. Schildkraut,et al.  The catecholamine hypothesis of affective disorders: a review of supporting evidence. , 1965, The American journal of psychiatry.