Alterations in brain-derived neurotrophic factor (BDNF) and its precursor proBDNF in the brain regions of a learned helplessness rat model and the antidepressant effects of a TrkB agonist and antagonist

European Neuropsychopharmacology

Volumn 25, Issue 12, 2015, Pages 2449-2458

  Shirayama, Yukihiko ^a,b   Yang, Chun ^b   Zhang, Ji chun ^b   Ren, Qian ^b   Yao, Wei ^b   Hashimoto, Kenji ^b  

^a TEIKYO UNIVERSITY CHIBA MEDICAL CENTER   (Japan)

^b CHIBA UNIVERSITY   (Japan)

Author keywords

Brain derived neurotrophic factor; Hippocampus; Infralimbic cortex; Nucleus accumbens; Prelimbic cortex; ProBDNF

Indexed keywords

7,8 DIHYDROXYFLAVONE; AMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; N2 [2 [[(2 OXOAZEPAN 3 YL)AMINO]CARBONYL]PHENYL]BENZO[B]THIOPHENE 2 CARBOXAMIDE; UNCLASSIFIED DRUG; 6,7-DIHYDROXYFLAVONE; ANA 12 COMPOUND; ANTIDEPRESSANT AGENT; AZEPINE DERIVATIVE; BENZAMIDE DERIVATIVE; BRAIN-DERIVED NEUROTROPHIC FACTOR PRECURSOR; FLAVONE DERIVATIVE; PROTEIN PRECURSOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LEARNED HELPLESSNESS; MEDIAL PREFRONTAL CORTEX; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; AGONISTS; ANALYSIS OF VARIANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; DRUG THERAPY; MALE; MENTAL STRESS; METABOLISM; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS; AZEPINES; BENZAMIDES; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVONES; HELPLESSNESS, LEARNED; MALE; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 84945448917     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2015.09.002     Document Type: Article

References (61)

1. Adachi M., Barrot M., Autry A.E., Theobald D., Monteggia L.M. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatry 2008, 63:642-649.
2. Altar C.A. Neurotrophins and depression. Trends Pharmacol. Sci. 1999, 20:59-61.
3. Altar C.A., Cai N., Bliven T., Juhasz M., Conner J.M., Acheson A.L., Lindsay R.M., Wiegand S.J. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 1997, 389:856-860.
4. Autry A.E., Monteggia L.M. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol. Rev. 2012, 64:238-258.
5. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., Graham D., Tsankova N.M., Bolanos C.A., Rios M., Monteggia L.M., Self D.W., Nestler E.J. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
6. Brown V.J., Bowman E.M. Rodent models of prefrontal cortical function. Trends Neurosci. 2002, 25:340-343.
7. Burgos-Robles A., Bravo-Rivera H., Quirk G.J. Prelimbic and inflalimbic neurons signal distinct aspects of appetite instrumental behavior. PLoS One 2013, 8:e57575.
8. Castren E. Neurotrophins and psychiatric disorders. Handb. Exp. Pharmacol. 2014, 220:461-479.
9. Cazorla M., Prémont J., Mann A., Girard N., Kellendonk C., Rognan D. Identification of a low-molecular weight TrkB antagonist with anxiolytic and antidepressant activity in mice. J. Clin. Invest. 2011, 121:1846-1857.
10. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 1997, 17:2295-2313.
11. Di Lieto A., Rantamäki T., Vesa L., Yanpallewar S., Antila H., Lindholm J., Rios M., Tessarollo L., Castrén E. The responsiveness of TrkB to BDNF and antidepressant drugs is differentially regulated during mouse development. PLoS One 2012, 7:e32869.
12. Duman R.S. Pathophysiology of depression and innovative treatments: remodeling glutamatergic synaptic connections. Dialogues Clin. Neurosci. 2014, 16:11-27.
13. Duman R.S., Aghajanian G.K. Synaptic dysfunction in depression: potential therapeutic targets. Science 2012, 338:68-72.
14. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59:1116-1127.
15. Dwivedi Y., Rizavi H.S., Conley R.R., Roberts R.C., Tamminga C.A., Pandey G.N. Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch. Gen. Psychiatry 2003, 60:804-815.
16. Eisch A.J., Bolaños C.A., de Wit J., Simonak R.D., Pudiak C.M., Barrot M., Verhaagen J., Nestler E.J. Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression. Biol. Psychiatry 2003, 54:994-1005.
17. Ethell I.M., Ethel D.W. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J. Neurosci. Res. 2007, 85:2813-2823.
18. Gipson C.D., Kupchik Y.M., Kalivas P.W. Rapid, transient synaptic plasticity in addiction. Neuropharmacology 2014, 76(Pt B):276-286.
19. Hashimoto K. Brain-derived neurotrophic factor as a biomarker for mood disorders: an historical overview and future directions. Psychiatry Clin. Neurosci. 2010, 64:341-357.
20. Hashimoto K. Sigma-1 receptor chaperone and brain-derived neurotrophic factor: emerging links between cardiovascular disease and depression. Prog. Neurobiol. 2013, 100:15-29.
21. Hashimoto K. Brain-derived neurotrophic factor and its precursor proBDNF as predictable biomarkers for bipolar disorder. Bri. J. Psychiatry 2014, 205:410.
22. Hashimoto K. Brain-derived neurotrophic factor (BDNF) and its precursor proBDNF as diagnostic biomarkers for major depressive disorder and bipolar disorder. Eur. Arch. Psychiatry Clin. Neurosci. 2015, 265:83-84.
23. Hashimoto K., Shimizu E., Iyo M. Critical role of brain-derived neurotrophic factor in mood disorders. Brain Res. Rev. 2004, 45:104-114.
24. Heidbreder C.A., Groenewegen H.J. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 2003, 27:555-579.
25. Hwang J.J., Park M.H., Choi S.Y., Koh J.Y. Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases. J. Biol. Chem. 2005, 280:11995-12001.
26. Iwata M., Shirayama Y., Ishida H., Hazama G.I., Nakagome K. Hippocampal astrocytes are necessary for antidepressant treatment of learned helplessness rats. Hippocampus 2011, 21:877-884.
27. Jang S.W., Liu X., Yepes M., Stepherd K.R., Miller G.W., Liu Y., Wilson W.D., Xiao G., Blanchi B., Sun Y.E., Ye K. A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc. Natl. Acad. Sci. USA 2010, 107:2687-2692.
28. Karege F., Vaudan G., Schwald M., Perround N., La Harpe R. Neurotrophin levels in postmortem brains of suicide victims and the effects of antemortem diagnosis and psychotropic drugs. Brain Res. Mol. Brain Res. 2005, 136:29-37.
29. Karpova N.N., Lindholm J., Pruunsild P., Timmusk T., Castrén E. Long-lasting behavioral and molecular alterations induced by early postnatal fluoxetine exposure are restored by chronic fluoxetine treatment in adult mice. Eur. Neuropsychopharmacol. 2009, 19:97-108.
30. Karpova N.N., Pickenhagen A., Lindholm J., Tiraboschi E., Kulesskaya N., Agústsdóttir A., Antila H., Popova D., Akamine Y., Bahi A., Sullivan R., Hen R., Drew L.J., Castrén E. Fear erasure in mice requires synergy between antidepressant drugs and extinction training. Science 2011, 334:1731-1734.
31. Kesner R.P., Churchwell J.C. An analysis of rat prefrontal cortex in mediating executive function. Neurobiol. Learn Mem. 2011, 96:417-431.
32. Krishnan V., Han M.H., Graham D.L., Berton O., Renthal W., Russo S.J., Laplant Q., Graham A., Lutter M., Lagace D.C., Ghose S., Reister R., Tannous P., Green T.A., Neve R.L., Chakravarty S., Kumar A., Eisch A.J., Self D.W., Lee F.S., Tamminga C.A., Cooper D.C., Gershenfeld H.K., Nestler E.J. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
33. Lindholm J.S., Castrén E. Mice with altered BDNF signaling as models for mood disorders and antidepressant effects. Front. Behav. Neurosci. 2014, 8:143.
34. Lu B., Pang P.T., Woo N.H. The Yin and Yang of neurotrophin action. Nat. Rev. Neurosci. 2005, 6:603-614.
35. Martinowich K., Manji H., Lu B. New insights into BDNF function in depression and anxiety. Nat. Neurosci. 2007, 10:1089-1093.
36. Matsumoto T., Rauskolb S., Polack M., Klose J., Kolbeck R., Korte M., Barde Y.A. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat. Neurosci. 2008, 11:131-133.
37. Monteggia L.M., Barrot M., Powell C.M., Berton O., Galanis V., Gemelli T., Meuth S., Nagy A., Greene R.W., Nestler E.J. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. USA 2004, 101:10827-10832.
38. Monteggia L.M., Luikart B., Barrot M., Theobold D., Malkovska I., Nef S., Parada L.F., Nestler E.J. Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors. Biol. Psychiatry 2007, 61:187-197.
39. Muneoka K., Shirayama Y., Horio M., Iyo M., Hashimoto K. Differential levels of brain amino acids in rat models presenting learned helplessness or non-learned helplessness. Psychopharmacology 2013, 226:63-71.
40. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
41. Nestler E.J., Carlezon W.A. The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 2006, 59:1151-1159.
42. Ongür D., Price J.L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 2000, 10:206-219.
43. Otis J.M., Fitzgerald M.K., Mueller D. Inflalimbic BDNF/TrkB enhancement of GluN2B currents facilitates extinction of a cocaine-conditioned place preference. J. Neurosci. 2014, 34:6057-6064.
44. Overmier J.O., Seligman M.E. Effects of inescapable shock upon subsequent escape and avoidance responding. J. Comp. Physiol. Psychol. 1967, 63:28-33.
45. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego, CA. 4th edition.
46. Peters J., Dieppa-Perea L.M., Melendez L.M., Quirk G.J. Induction of fear extinction with hippocampal-inflalimbic BDNF. Science 2010, 328:1288-1290.
47. Peters J., Kalivas P.W., Quirk G.J. Extinction circuits for fear and addiction overlap in prefrontal cortex. Lean. Mem. 2009, 16:279-288.
48. Rantamäki T., Vesa L., Antila H., Di Lieto A., Tammela P., Schmitt A., Lesch K.P., Rios M., Castrén E. Antidepressant drugs transactivate TrkB neurotrophin receptors in the adult rodent brain independently of BDNF and monoamine transporter blockade. PLoS One 2011, 6:e20567.
49. Ren Q., Zhang J.C., Fujita Y., Ma M., Wu J., Hashimoto K. Effects of TrkB agonist 7,8-dihydroxyflavone on sensory gating deficits in mice after administration of methamphetamine. Pharmacol. Biochem. Behav. 2013, 106:124-127.
50. Ren Q., Zhang J.C., Ma M., Fujita Y., Wu J., Hashimoto K. 7,8-Dihydroxyflavone, a TrkB agonist, attenuates behavioral abnormalities and neurotoxicity in mice after administration of methamphetamine. Psychopharmacology 2014, 231:159-166.
51. Saarelainen T., Hendolin P., Lucas G., Koponen E., Sairanen M., MacDonald E., Agerman K., Haapasalo A., Nawa H., Aloyz R., Ernfors P., Castrén E. Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J. Neurosci. 2003, 23:349-357.
52. Shen H.W., Gipson C.D., Huits M., Kalivas P.W. Prelimbic cortex and ventral tegmental area modulate synaptic plasticity differentially in nucleus accumbens during cocaine-reinstated drug seeking. Neuropsychopharmacology 2014, 39:1169-1177.
53. Shirayama Y., Chaki S. Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents. Curr. Neuropharmacol. 2006, 4:277-291.
54. Shirayama Y., Chen A.C.-H., Nakagawa S., Russell D.S., Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 2002, 22:3251-3261.
55. Shirayama Y., Muneoka K., Fukumoto M., Tadokoro S., Fukami G., Hashimoto K., Iyo M. Infusions of allopregnanolone into the hippocampus and amygdala, but not into the nucleus accumbens and medial prefrontal cortex, produce antidepressant effects on the learned helplessness rats. Hippocampus 2011, 21:1105-1113.
56. Sun H., Kennedy P.J., Nestler E.J. Epigenetics of the depressed brain: role of histone acetylation and methylation. Neuropsychopharmacology 2013, 38:124-137.
57. Vialou V., Bagot R.C., Cahill M.E., Ferguson D., Robison A.J., Dietz D.M., Fallon B., Mazei-Robison M., Ku S.M., Harrigan E., Winstanley C.A., Joshi T., Feng J., Berton O., Nestler E.J. Prefrontal cortical circuit for depression- and anxiety-related behaviors mediated by cholecystokinin: role of δFosB. J. Neurosci. 2014, 34:3878-3887.
58. Walsh J.J., Han M.H. The heterogeneity of ventral tegmental area neurons: projection functions in a mood-related context. Neuroscience 2014, 282C:101-108.
59. Yang C., Shirayama Y., Zhang J.C., Ren Q., Hashimoto K. Regional differences in brain-derived neurotrophic factor levels and dendritic spine density confer resilience to inescapable stress. Int. J. Neuropsychopharmacol. 2015, 18:pyu121.
60. Yang C., Shirayama Y., Zhnag J.C., Ren Q., Hashimoto K. Peripheral interlukin-6 promotes resilience versus susceptibility to inescapable electric stress. Acta. Neuropsychiatr. 2015, 27:312-316.
61. Zhang J.C., Wu J., Fujita Y., Yao W., Ren Q., Yang C., Shirayama Y., Hashimoto K. Antidepressant effects of TrkB ligands on depression-like behaviors and dendritic changes in mice after inflammation. Int. J. Neuropsychopharmacol. 2015, 18:pyu077.