Brain-derived neurotrophic factor Val66Met allele impairs basal and ketamine-stimulated synaptogenesis in prefrontal cortex

Biological Psychiatry

Volumn 71, Issue 11, 2012, Pages 996-1005

  Liu, Rong Jian ^a   Lee, Francis S ^b   Li, Xiao Yuan ^a   Bambico, Francis ^a   Duman, Ronald S ^a   Aghajanian, George K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Antidepressant; dendritic spines; EPSC; hypocretin; major depression; N methyl D aspartate; serotonin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; KETAMINE; METHIONINE; OREXIN; SEROTONIN; VALINE;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN ATROPHY; CELL MATURATION; CONTROLLED STUDY; DENDRITE; EXCITATORY POSTSYNAPTIC POTENTIAL; FORCED SWIMMING TEST; FREQUENCY MODULATION; MOUSE; NONHUMAN; POSTSYNAPTIC DENSITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPTOGENESIS;

ALLELES; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENDRITES; DEPRESSIVE DISORDER, MAJOR; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; KETAMINE; MICE; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; POLYMORPHISM, GENETIC; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SYNAPSES;

EID: 84857083262     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.09.030     Document Type: Article

References (59)

1. R.S. Duman, L.M. Monteggia A neurotrophic model for stress-related mood disorders Biol Psychiatry 59 2006 1116 1127
2. E. Castren, V. Voikar, Rantamaki Role of neurotrophic factors in depression Curr Opin Pharmacol 7 2007 18 21 (Pubitemid 46238033)
3. K. Martinowich, H. Manji, B. Lu New insights into BDNF function in depression and anxiety Nat Neurosci 10 2007 1089 1093 (Pubitemid 47339961)
4. Y. Dwivedi Brain-derived neurotrophic factor: Role in depression and suicide Ann Med 42 2009 87 96
5. M.F. Egan, M. Kojima, J.H. Callicott, T.E. Goldberg, B.S. Kolachana, A. Bertolino The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function Cell 112 2003 257 269 (Pubitemid 36144114)
6. A.R. Hariri, T.E. Goldberg, V.S. Mattay, B.S. Kolachana, J.H. Callicott, M.F. Egan, D.R. Weinberger Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance J Neurosci 23 2003 6690 6694 (Pubitemid 36951196)
7. S.E. Harris, H. Fox, A.F. Wright, C. Hayward, J.M. Starr, L.J. Whalley, I.J. Deary The brain-derived neurotrophic factor Val66Met polymorphism is associated with age-related change in reasoning skills Mol Psychiatry 11 2006 505 513
8. J.-M. Kim, R. Stewart, S.-W. Kim, S.-J. Yang, I.-S. Shin, Y.-H. Kim, J.-S. Yoon Interactions between life stressors and susceptibility genes (5-HTTLPR and BDNF) on depression in Korean elders Biol Psychiatry 62 2007 423 428 (Pubitemid 47284032)
9. F. Miyajima, W. Ollier, A. Mayes, A. Jackson, N. Thacker, P. Rabbitt Brain-derived neurotrophic factor polymorphism Val66Met influences cognitive abilities in the elderly Genes Brain Behav 7 2008 411 417 (Pubitemid 351590926)
10. J.M. Gatt, C.B. Nemeroff, C. Dobson-Stone, R.H. Paul, R.A. Bryant, P.R. Schofield Interactions between BDNF Val66Met polymorphism and early life stress predict brain and arousal pathways to syndromal depression and anxiety Mol Psychiatry 14 2009 681 695
11. Z.Y. Chen, P.D. Patel, G. Sant, C.X. Meng, K.K. Teng, B.L. Hempstead, F.S. Lee Variant brain-derived neurotrophic factor (BDNF) (Met66) alters the intracellular trafficking and activity-dependent secretion of WT BDNF in neurosecretory cells and cortical neurons J Neurosci 24 2004 4401 4411 (Pubitemid 38608151)
12. C. Chiaruttini, A. Vicario, Z. Li, G. Baj, P. Braiuca, Y. Wu Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation Proc Natl Acad Sci U S A 106 2009 16481 16486
13. Z.Y. Chen, D. Jing, K.G. Bath, A. Ieraci, T. Khan, C.J. Siao Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior Science 314 2006 140 143 (Pubitemid 44547760)
14. W.C. Drevets, J.L. Price, M.L. Furey Brain structural and functional abnormalities in mood disorders: Implications for neurocircuitry models of depression Brain Struct Funct 213 2008 93 118
15. H.S. Mayberg Targeted electrode-based modulation of neural circuits for depression J Clin Invest 119 2009 717 725
16. V. Krishnan, E.J. Nestler Linking molecules to mood: New insight into the biology of depression Am J Psychiatry 167 2010 1305 1320
17. R.J. Liu, G.K. Aghajanian Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: Role of corticosterone-mediated apical dendritic atrophy Proc Natl Acad Sci U S A 105 2008 359 364
18. G.K. Aghajanian, G.J. Marek Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells Neuropharmacology 36 1997 589 599 (Pubitemid 27272104)
19. E.K. Lambe, G.K. Aghajanian Hypocretin (orexin) induces calcium transients in single spines postsynaptic to identified thalamocortical boutons in prefrontal slice Neuron 40 2003 139 150 (Pubitemid 37222469)
20. M.M. Poo Neurotrophins as synaptic modulators Nat Rev Neurosci 2 2001 24 32
21. B. Lu Acute and long-term synaptic modulation by neurotrophins Prog Brain Res 146 2004 137 150 (Pubitemid 37541381)
22. N. Li, B. Lee, R.J. Liu, M. Banasr, J.M. Dwyer, M. Iwata mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists Science 329 2010 959 964
23. C.A. Hoeffer, Klann mTOR signaling: At the crossroads of plasticity, memory and disease Trends Neurosci 33 2009 67 75
24. N. Takei, N. Inamura, M. Kawamura, H. Namba, K. Hara, K. Yonezawa, H. Nawa Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites J Neurosci 24 2004 9760 9769 (Pubitemid 39463557)
25. R.D. Porsolt, A. Bertin, M. Jalfre Behavioral despair in mice: A primary screening test for antidepressants Arch Int Pharmacodyn Ther 229 1977 327 336 (Pubitemid 8225714)
26. E. Hayashi, M. Shimamura, K. Kuratani, M. Kinoshita, H. Hara Automated experimental system capturing three behavioral components during murine forced swim test Life Sci 88 2011 411 417
27. P. Kelliher, T.J. Connor, A. Harkin, C. Sanchez, J.P. Kelly, B.E. Leonard Varying responses to the rat forced-swim test under diurnal and nocturnal conditions Physiol Behav 69 2000 531 539 (Pubitemid 30460092)
28. A.V. Kulikov, M.V. Morozova, V.A. Kulikov, V.S. Kirichuk, N.K. Popova Automated analysis of antidepressants' effect in the forced swim test J Neurosci Methods 191 2010 26 31
29. H. Yu, Y. Wang, S. Pattwell, D. Jing, T. Liu, Y. Zhang Variant BDNF Val66Met polymorphism affects extinction of conditioned aversive memory Neurosci 29 2009 4056 4064
30. S. Chakravarthy, M.H. Saiepour, M. Bence, S. Perry, R. Hartman, J.J. Couey Postsynaptic TrkB signaling has distinct roles in spine maintenance in adult visual cortex and hippocampus Proc Natl Acad Sci U S A 103 2006 1071 1076 (Pubitemid 43212223)
31. B.W. Luikart, W. Zhang, G.A. Wayman, C.H. Kwon, G.L. Westbrook, L.F. Parada Neurotrophin-dependent dendritic filopodial motility: a convergence on PI3K signaling J Neurosci 28 2008 7006 7012
32. H. Jourdi, Y.T. Hsu, M. Zhou, Q. Qin, X. Bi, M. Baudry Positive AMPA receptor modulation rapidly stimulates BDNF release and increases dendritic mRNA translation J Neurosci 29 2009 8688 8697
33. L. Slipczuk, P. Bekinschtein, C. Katche, M. Cammarota, I. Izquierdo, J.H. Medina BDNF activates mTOR to regulate GluR1 expression required for memory formation PLoS One 4 2009 e6007
34. S. Maeng, C.A. Zarate Jr, J. Du, R.J. Schloesser, J. McCammon, G. Chen, H.K. Manji Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors Biol Psychiatry 63 2008 349 352 (Pubitemid 351146651)
35. A.E. Autry, M. Adachi, E. Nosyreva, E.S. Na, M.F. Los, P.F. Cheng NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses Nature 475 2011 91 95
36. E. Tongiorgi, G. Baj Functions and mechanisms of BDNF mRNA trafficking Novartis Found Symp 289 2008 136 147
37. J.J. An, K. Gharami, G.Y. Liao, N.H. Woo, A.G. Lau, F. Vanevski Distinct role of long 3' UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons Cell 134 2008 175 187 (Pubitemid 351905742)
38. J. Soulé, E. Messaoudi, C.R. Bramham Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain Biochem Soc Trans 34 2006 600 604 (Pubitemid 44230773)
39. D.S. Goldwater, C. Pavlides, R.G. Hunter, E.B. Bloss, P.R. Hof, B.S. McEwen, J.H. Morrison Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery Neuroscience 164 2009 798 808
40. S.M. Brown, S. Henning, C.L. Wellman Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex Cereb Cortex 15 2005 1714 1722 (Pubitemid 41447036)
41. J.J. Radley, A.B. Rocher, M. Miller, W.G. Janssen, C. Liston, P.R. Hof Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex Cereb Cortex 16 2006 313 320 (Pubitemid 43209205)
42. I.E. Nagel, C. Chicherio, S.C. Li, T. von Oertzen, T. Sander, A. Villringer Human aging magnifies genetic effects on executive functioning and working memory Front Hum Neurosci 2 2008 1 8
43. F. Soliman, C.E. Glatt, K.G. Bath, L. Levita, R.M. Jones, S.S. Pattwell A genetic variant BDNF polymorphism alters extinction learning in both mouse and human Science 327 2010 863 866
44. L.M. Hilt, L.C. Sander, S. Nolen-Hoeksema, A.A. Simen The BDNF Val66Met polymorphism predicts rumination and depression differently in young adolescent girls and their mothers Neurosci Lett 429 2007 12 16 (Pubitemid 350116345)
45. L.E. Duncan, K.E. Hutchison, G. Carey, W.E. Craighead Variation in brain-derived neurotrophic factor (BDNF) gene is associated with symptoms of depression J Affect Disord 115 2009 215 219
46. B. Moghaddam, B. Adams, A. Verma, D. Daly Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex J Neurosci 17 1997 2921 2927 (Pubitemid 27155025)
47. W.C. Drevets, J.L. Price, J.R. Simpson Jr, R.D. Todd, T. Reich, M. Vannier, M.E. Raichle Subgenual prefrontal cortex abnormalities in mood disorders Nature 386 1997 824 827 (Pubitemid 27181254)
48. L. Pezawas, B.A. Verchinski, V.S. Mattay, J.H. Callicott, B.S. Kolachana, R.E. Straub The brain-derived neurotrophic factor val66met polymorphism and variation in human cortical morphology J Neurosci 24 2004 10099 10102 (Pubitemid 39492034)
49. Frodl, C. Schule, G. Schmitt, C. Born, T. Baghai, P. Zill Association of the brain-derived neurotrophic factor Val66Met polymorphism with reduced hippocampal volumes in major depression Arch Gen Psychiatry 64 2007 410 416 (Pubitemid 46556460)
50. K. Matsuo, C. Walss-Bass, F.G. Nery, M.A. Nicoletti, J.P. Hatch, B.N. Frey Neuronal correlates of brain-derived neurotrophic factor Val66Met polymorphism and morphometric abnormalities in bipolar disorder Neuropsychopharmacology 34 2009 1904 1913
51. P.L. Gabbott, T.A. Warner, P.R. Jays, P. Salway, S.J. Busby Prefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers J Comp Neurol 492 2005 145 177 (Pubitemid 41443719)
52. J. Savitz, W.C. Drevets Bipolar and major depressive disorder: Neuroimaging the developmental-degenerative divide Neurosci Biobehav Rev 33 2009 699 771
53. R.M. Berman, A. Cappiello, A. Anand, D.A. Oren, G.R. Heninger, D.S. Charney, J.H. Krystal Antidepressant effects of ketamine in depressed patients Biol Psychiatry 47 2000 351 354 (Pubitemid 30109248)
54. C.A. Zarate Jr, J.B. Singh, P.J. Carlson, N.E. Brutsche, R. Ameli, D.A. Luckenbaugh A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression Arch Gen Psychiatry 63 2006 856 864 (Pubitemid 44188478)
55. N. Diazgranados, L. Ibrahim, N.E. Brutsche, A. Newberg, P. Kronstein, S. Khalife A randomized add-on trial of an N-methyl-D-aspartate antagonist in treatment-resistant bipolar depression Arch Gen Psychiatry 67 2010 793 802
56. R.B. Price, M.K. Nock, D.S. Charney, S.J. Mathew Effects of intravenous ketamine on explicit and implicit measures of suicidality in treatment-resistant depression Biol Psychiatry 66 2009 522 526
57. N. Diazgranados, L.A. Ibrahim, N.E. Brutsche, R. Ameli, I.D. Henter, D.A. Luckenbaugh Rapid resolution of suicidal ideation after a single infusion of an N-methyl-D-aspartate antagonist in patients with treatment-resistant major depressive disorder J Clin Psychiatry 71 2010 1605 1611
58. S.-J. Tsai1, C.-J. Hong, Y.-J. Liou Effects of BDNF polymorphisms on antidepressant action Psychiatry Investig 7 2010 236 242
59. T. Rantamäki, L. Vesa, H. Antila, A. Di Lieto, P. Tammela, A. Schmitt Antidepressant drugs transactivate TrkB neurotrophin receptors in the adult rodent brain independently of BDNF and monoamine transporter blockade PLoS One 6 2011 e20567