Skip to main content
SpringerLink
Log in

Brain-Derived Neurotrophic Factor: Effects on Genetically and Epigenetically Determined Behavioral Disorders

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Studies in recent years have significantly widened our understanding of the mechanism of action of brain-derived neurotrophic factor (BDNF) and the potential areas of its application. This review presents results from our own studies, along with published data on the influences of BDNF on epigenetically and genetically determined behavioral disorders. Particular attention is paid to the role of the genotype and the involvement of the brain serotonin system in the effects of BDNF. The material presented in this review provides evidence that: 1) the key genes of the brain serotonin system (tryptophan hydroxylase 2, 5-HT1A and 5-HT2A receptors) are involved in the mechanism of action of BDNF; 2) single central doses of BDNF have long-lasting positive influences on several genetically determined manifestations of pathological behavior; 3) BDNF can weaken the manifestations of behavioral disorders induced by harmful environmental factors acting during the prenatal period.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. O. A. Gomazkov, “Brain neurotrophic and growth factors: specific regulatory features and therapeutic potential,” Usp. Fiziol. Nauk., 36, No. 2, 1–25 (2005).

    Google Scholar 

  2. O. A. Gomazkov, Aging of the Brain and Neurotrophic Therapy, IKAR, Moscow (2011).

    Google Scholar 

  3. E. G. Kuznetsov, T. G. Amstislavskaya,V. V. Bulygina and N. K. Popova, “Effects of stress during the prenatal period on sexual arousal and the sexual orientation in male mice,” Ros. Fiziol. Zh., 92, No. 1, 123–132 (2006).

    Google Scholar 

  4. M. V. Morozova and N. K. Popova, “Combined influence of alcohol and stress during the perinatal period on the behavior of adult mice,” Ros. Fiziol. Zh., 96, No. 11, 72–79 (2010).

    Google Scholar 

  5. J. Alder, S. Thakker-Varia, D. A. Bangasser, et al., “Brain-derived neurotrophic factor-induced gene expression reveals novel actions of NGF in hippocampal synaptic plasticity,” J. Neurosci., 23, 10800–10808 (2003).

    PubMed Central  CAS  PubMed  Google Scholar 

  6. P. Alonso, M. Gratacol, J. N. Menchon, et al., “Extensive genotyping of the BDNF and NTRK2 genes defines protective haplotypes against obsessive-compulsive disorder,” Biol. Psychiatry, 63, No. 6, 619–628 (2008).

    Article  CAS  PubMed  Google Scholar 

  7. J. J. An, K. Gharami, G. Liao, et al., “Distinct role of long 3UTRbdnf mRNA in spine morphology and synaptic plasticity in hippocampal neurons,” Cell, 134, 175–187 (2008).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. D. T. Balu, B. A. Hoshaw, J. E. Malberg, et al., “Differential regulation of central BDNF protein levels by antidepressant and non-antidepressant drug treatments,” Brain Res., 1211, 37–43 (2008).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Y. A. Barde, D. Edgar, and H. Thoenen, “Purification of a new neurotrophic factor from mammalian brain,” EMBO J., 1, 549–553 (1982).

    PubMed Central  CAS  PubMed  Google Scholar 

  10. A. Bartoletti, L. Cancedda, S. W. Reid, et al., “Heterozygous knockout mice for brain-derived neurotrophic factor show a pathway-specific impairment of long-term potentiation but normal critical period for monocular deprivation,” J. Neurosci., 22, No. 23, 10,072–10,077 (2002).

    CAS  Google Scholar 

  11. Z. Bhagwagar, R. Hinz, M. Taylor, et al., “Increased 5-HT(2A) receptor binding in euthymic, medication-free patients recovered from depression: a positron emission study with [(11)C]MDL 100,907,” Am. J. Psychiatry, 163, 1580–1587 (2006).

    PubMed  Google Scholar 

  12. M. Bibel and Y. A. Barde, “Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system,” Genes Dev., 14, No. 23, 2919–2937 (2000).

    Article  CAS  PubMed  Google Scholar 

  13. A. Bird, “Perceptions of epigenetics,” Nature, 447, 396–398 (2007).

    Article  CAS  PubMed  Google Scholar 

  14. Y. Boulougouris, S. R. Chamberlain, and T. W. Robbins, “Crossspecies models of OCD spectrum disorders,” Psychiatry Res., 170, No. 1, 15–21 (2009).

    Article  PubMed  Google Scholar 

  15. C. R. Bramham and E. Messaoudi, “BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis,” Prog. Neurobiol., 76, 99–125 (2005).

    Article  CAS  PubMed  Google Scholar 

  16. I. Branchi, I. D’Andrea, M. Fiore, et al., “Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain,” Biol. Psychiatry, 60, No. 7, 600–606 (2006).

    Article  Google Scholar 

  17. I. Branchi, N. Francia, and E. Alleva, “Epigenetic control of neurobehavioral plasticity: the role of neurotrophins,” Behav. Pharmacol., 15, No. 5–6, 353–362 (2004).

    Article  CAS  PubMed  Google Scholar 

  18. L. Burd, T. M. Cotsonas-Hassler, T. Martsolf, and J. Kerbeshian, “Recognition and management of fetal alcohol syndrome,” Neurotoxicol. Teratol., 25, No. 6, 681–688 (2003).

    Article  CAS  PubMed  Google Scholar 

  19. K. S. Cadenhead, M. A. Geyer, and D. L. Branff, “Impaired startle prepulse inhibition and habituation in patients with schizotypal personality disorder,” Am. J. Psychiatry, 150, 1862–1867 (1993).

    Article  CAS  PubMed  Google Scholar 

  20. M. V. Caldeira, C. V. Melo, D. B. Pereira, et al., “BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons,” Mol. Cell. Neurosci., 35, 208–219 (2007).

    Article  CAS  PubMed  Google Scholar 

  21. L. M. Carneiro, J. P. Diógenes, S. M. Vasconcelos, et al., “Behavioral and neurochemical effects on rat offspring after prenatal exposure to ethanol,” Neurotoxicol. Teratol., 27, No. 4, 585–592 (2005).

    Article  CAS  PubMed  Google Scholar 

  22. E. Castren, “Neurotrophic effect of antidepressant drugs,” Curr. Opin. Pharmacol., 4, 58–64 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. J. P. Chan, J. Cordeira, G. A. Calderon, et al., “Depletion of central BDNF in mice impedes terminal differentiation of new granule neurons in the adult hippocampus,” Mol. Cell. Neurosci., 39, No. 3, 372–383 (2008).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. J. P. Chan, T. J. Under, J. Byrnes, and M. Rios, “Examination of behavioral deficits triggered by targeting BDNF in fetal or postnatal brains of mice,” Neuroscience, 142, No. 1, 49–58 (2006).

    Article  CAS  PubMed  Google Scholar 

  25. M. V. Chao, R. Rajagopal, and F. S. Lee, “Neurotrophin signalling in health and disease,” Clin. Science, 110, 167–173 (2006).

    Article  CAS  Google Scholar 

  26. B. Connor, D. Young, Q. Yan, et al., “Brain-derived neurotrophic factors,” Brain Res. Mol. Brain Res., 49, No. 1–2, 71–81 (1997).

    Article  CAS  PubMed  Google Scholar 

  27. G. Dörner, T. Geier, L. Ahrens, et al., “Prenatal stress as possible aetiogenic factor of homosexuality in human males,” Endokrinologie, 75, No. 3, 365–368 (1980).

    PubMed  Google Scholar 

  28. G. Dörner, B. Schenk, B. Schmiedel, and L. Ahrens, “Stressful events in prenatal life of bi- and homosexual men,” Exp. Clin. Endocrinol., 81, No. 1, 83–87 (1983).

    Article  PubMed  Google Scholar 

  29. M. Fiore, G. Laviola, L. Aloe, et al., “Early exposure to ethanol but not red wine at the same alcohol concentration induces behavioral and brain neurotrophin alterations in young and adult mice,” Neurotoxicology, 30, No. 1, 59–71 (1990).

    Article  Google Scholar 

  30. D. Fiorentino, G. Coriale, P. Spagnolo, et al., “Fetal alcohol syndrome disorders: experience in the field,” in: The Lazio Study Preliminary Report, Ann. 1st Super Sanita, 42, 53–57 (2006).

  31. F. Fumagalli, G. Bedogni, J. Perez, et al., “Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress,” Eur. J. Neurosci., 20, No. 5, 1348–1354 (2004).

    Article  PubMed  Google Scholar 

  32. M. A. Geyer, N. R. Swerdlow, R. S. Mansbach, and D. L. Braff, “Startle response models of sensorimotor gating and habituation deficits in schizophrenia,” Brain Res. Bull., 25, 485–498 (1990).

    Article  CAS  PubMed  Google Scholar 

  33. J. L. Goldberg and B. A. Barres, “The relationship between neuronal survival and regeneration,” Annu. Rev. Neurosci., 23, 579–612 (2000).

    Article  CAS  PubMed  Google Scholar 

  34. M. Greenberg, B. Xu, B. Lu, and B. Hempstead, “New insights in the biology of BDNF synthesis and release: implications in CNS function,” J. Neurosci., 29, No. 4, 12764–12767 (2009).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. D. Hall, A. Dhilla, A. Charalambous, et al., “Sequence variants of the brain-derived neurotrophic factor (BDNF) gene are strongly associated with obsessive-compulsive disorder,” Am. J. Hu. Genet., 73, No. 2, 370–376 (2003).

    Article  CAS  Google Scholar 

  36. B. L. Hempstead, “Dissecting the diverse actions of pro- and mature neurotrophins,” Curr. Alzheimer Res., 3, No. 1, 19–24 (2006).

    Article  CAS  PubMed  Google Scholar 

  37. Y. Hu and S. J. Russek, “BDNF and the diseased nervous system: a delicate balance between adaptive and pathological processes of gene regulation,” J. Neurochem., 105, 1–17 (2008).

    Article  CAS  PubMed  Google Scholar 

  38. T. Itoh, M. Tokumura, and K. Abe, “Effect of rolipram, a phosphodiesterase 4 inhibitor, in combination with imipramine on depressive behavior, CRE binding activity and BDNF level in learned helplessness rats,” Eur. J. Pharmacol., 498, 135–142 (2004).

    Article  CAS  PubMed  Google Scholar 

  39. P. Jansen, K. Giehl, J. Nyengaard, et al., “Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury,” Nat. Neurosci., 10, No. 11, 1449–1457 (2007).

    Article  CAS  PubMed  Google Scholar 

  40. D. Joel, “Current animal models of obsessive compulsive disorder: a critical review,” Neuropsychopharmacol. Biol. Psychiatry, 30, No. 3, 374–388 (2006).

    Article  Google Scholar 

  41. J. E. Johnson, “Neurotrophic factors,” in: Fundamental Neuroscience, M. J. Zigmond et al. (eds.), Oxford University Press (1999), pp. 611–635.

  42. D. R. Kaplan and F. D. Miller, “Neurotrophin signal transduction in the nervous system,” Curr. Opin. Neurobiol., 10, 381–391 (2000).

    Article  CAS  PubMed  Google Scholar 

  43. S. G. Kernie, D. J. Liebl, and L. F. Parada, “BDNF regulates eating behavior and locomotor activity in mice,” EMBO J., 19, No. 6, 1290–1300 (2000).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. A. B. Klein, M. A. Santini, S. Aznar, et al., “Changes in 5-HT2C-mediated behavior and 5-HT2A and 5-HT1A receptor binding and expression in conditional brain-derived neurotrophic factor knockout mice,” Neuroscience, 169, 1007–1016 (2010).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. M. Korte, P. Carroll, E. Wolf, et al., “Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor,” Proc. Natl. Acad. Sci. USA, 92, No. 19, 8856–8860 (1995).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. A. V. Kulikov, D. V. Bazovkina, E. M. Kondaurova, and N. K. Popova, “Genetic structure of hereditary catalepsy in mice,” Genes Brain Behav., 7, 506–512 (2008).

    Article  CAS  PubMed  Google Scholar 

  47. B. W. Lau, S. Y. Yau, T. M. Lee, et al., “Intracerebroventricular infusion of cytosine-arabinoside causes prepulse inhibition disruption,” Neuroreport, 20, 371–377 (2009).

    Article  CAS  PubMed  Google Scholar 

  48. R. Levi-Montalcini, “The nerve growth factor: thirty-five years later,” EMBO J., 6, 1145–1154 (1987).

    PubMed Central  CAS  PubMed  Google Scholar 

  49. G. A. Light and D. I. Braff, “Human and animal studies of schizophrenia-related gating deficits,” Curr. Psychiatry Reports, 1, 31–40 (1999).

    Article  CAS  Google Scholar 

  50. B. Lu, “BDNF and activity-dependent synaptic modulation,” Learn. Mem., 10, 86–98 (2003).

    Article  PubMed  Google Scholar 

  51. K. Ludewig, M. A. Geyer, and F. X. Follenweider, “Deficits in prepulse inhibition and habituation in never-medicated, first-episode schizophrenia,” Biol. Psychiatry, 54, 121–128 (2003).

    Article  PubMed  Google Scholar 

  52. J. N. Lugo, M. D. Marino, J. T. Gass, et al., “Ethanol exposure during development reduces resident aggression and testosterone in rats,” Physiol. Behav., 87, No. 2, 330–337 (2006).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  53. W. E. Lyons, L. A. Mamounas, G. A. Ricarute, et al., “Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities,” Proc. Natl. Acad. Sci. USA, 96, No. 26, 15,239–15,244 (1999).

    Article  CAS  Google Scholar 

  54. A. K. McAllister, L. C. Katz, and D. C. Lo, “Neurotrophins and synaptic plasticity,” Annu. Rev. Neurosci., 22, 295–318 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. L. R. Meek, K. M. Schulz, and C. A. Keith, “Effects of prenatal stress on sexual partner preference in mice,” Physiol. Behav., 89, No. 2, 133–138 (2006).

    Article  CAS  PubMed  Google Scholar 

  56. C. Murgatroyd, A. V. Patchev,Y. Wu, et al., “Dynamic DNA methylation programs persistent adverse effect of early-life stress,” Nat. Neurosci., 12, 1559–1566 (2009).

    Article  CAS  PubMed  Google Scholar 

  57. R. L. Myers, D. C. Airey, D. H. Manier, et al., “Polymorphisms in the regulatory region of the human serotonin 5-HT2A receptor gene (HTR2A) influence gene expression,” Biol. Psychiatry, 61, 167–173 (2007).

    Article  CAS  PubMed  Google Scholar 

  58. A. H. Nagahara, D. A. Merill, G. Coppola, et al., “Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer’s disease,” Nat. Med., 15, No. 3, 331–337 (2009).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. E. V. Naumenko, “Modification in early ontogenesis of the stress response of adults,” News Physiol. Sci., 6, 219–223 (1991).

    Google Scholar 

  60. V. S. Naumenko, D. V. Bazovkina, M. V. Morozova, and N. K. Popova, “Effects of brain-derived and glial cell line-derived neurotrophic factor on startle response and disrupted prepulse inhibition in mice of DBA/2J inbred strain,” Neurosci. Lett. (2013) (in press).

  61. V. S. Naumenko, E. V. Kondaurova, D. V. Bazovkina, et al., “Effect of brain-derived neurotrophic factor on behavior and key members of the brain serotonin system in genetically predisposed to behavioral disorders mouse strains,” Neurosci., 214, 59–67 (2012).

    Article  CAS  Google Scholar 

  62. E. W. Neeley, R. Berger, J. Koenig, and S. Leonard, “Prenatal stress differently alters brain-derived neurotrophic factor expression and signaling across rat strains,” Neurosci., 187, 24–35 (2011).

    Article  CAS  Google Scholar 

  63. M. Nibuya, S. Morinobu, and R. S. Duman, “Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments,” J. Neurosci., 15, No. 11, 7539–7547 (1995).

    CAS  PubMed  Google Scholar 

  64. B. Olivier, C. Leahy, T. Mullen, et al., “The DBA/2J strain and prepulse inhibition of startle: a model system to test antipsychotics?” Psychopharmacology (Berlin), 156, 284–290 (2001).

    Article  CAS  Google Scholar 

  65. F. Papaleo, J. L. Silverman, J. Aney, et al., “Working memory deficits, increased anxiety-like traits, and seizure susceptibility in BDNF overexpressing mice,” Learn. Mem., 18, 534–544 (2011).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. R. Paylor and J. N. Crawley, “Inbred strain differences in prepulse inhibition of the mouse startle response,” Psychopharmacology (Berlin), 132, 169–180 (1997).

    Article  CAS  Google Scholar 

  67. O. C. Pereira, M. M. Bernardi, and D. C. Gerardin, “Could neonatal testosterone replacement prevent alterations induced by prenatal stress in male rats?” Life Sci., 78, No. 24, 2767–2771 (2006).

    Article  CAS  PubMed  Google Scholar 

  68. N. K. Popova, V. S. Naumenko, M. A. Tibeikina, and A. V. Kulikov, “Serotonin transporter, 5-HT1A receptor, and behavior in DBA/2J mice in comparison with four inbred mouse strains,” J. Neurosci. Res., 87, 3649–3657 (2009).

    Article  CAS  PubMed  Google Scholar 

  69. N. K. Popova, M. V. Morozova, and T. G. Amstislavskaya, “Prenatal stress and ethanol exposure produces inversion of sexual partner preference in mice,” Neurosci. Lett., 489, No. 1, 48–52 (2011).

    Article  CAS  PubMed  Google Scholar 

  70. N. K. Popova, M. V. Morozova, and V. S. Naumenko, “Ameliorative effect of BDNF on prenatal stress and ethanol exposure-induced behavioral disorders,” Neurosci. Lett., 505, No. 2, 82–86 (2011).

    Article  CAS  PubMed  Google Scholar 

  71. A. Riccio, S. Ahn, C. M. Davenport, et al., “Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons,” Science, 286, 2358–2361 (1999).

    Article  CAS  PubMed  Google Scholar 

  72. J. J. Rodriguez, H. A. Davies, A. T. Silva, et al., “Long-term potentiation in the rat dentate gyrus is associated with enhanced Arc/Arc3.1 protein expression in spines, dendrites and glia,” Eur. J. Neurosci., 21, No. 9, 2384–2396 (2005).

    Article  CAS  PubMed  Google Scholar 

  73. Z. Ragoz and B. Legutko, “Combined treatment with imipramine and metyrapone induces hippocampal and cortical brain-derived neurotrophic factor gene expression in rats,” Pharmacol. Rep., 57, 849–844 (2005).

    Google Scholar 

  74. T. L. Roth and J. D. Sweatt, “Epigenetic marking on the BDNF genes by early-life adverse experiences,” Horm. Behav., 50, 315–320 (2011).

    Article  Google Scholar 

  75. A. L. Sanchez, B. J. Matthews, M. M. Meynard, et al., “BDNF increases synapse density in dendrites of developing tectal neurons in vivo,” Development, 133, 2477–2486 (2006).

    Article  CAS  PubMed  Google Scholar 

  76. P. M. Schwartz, P. R. Borghesani, R. L. Levy, et al., “Abnormal cerebellar development and foliation in BDNF–/– mice reveals a role for neurotrophins in CNS patterning,” Neuron, 19, No. 2, 269–281 (1997).

    Article  CAS  PubMed  Google Scholar 

  77. R. A. Segal, “Selectivity in neurotrophin signaling: theme and variations,” Annu. Rev. Neurosci., 26, 299–330 (2003).

    Article  CAS  PubMed  Google Scholar 

  78. J. K. Simosky, K. E. Stevens, W. R. Kem, and R. Freedman, “Intragastric DMXB-A, an alpha7 nicotinic agonist, improves deficient sensory inhibition in DBA/2 mice,” Biol. Psychiatry, 50, 493–500 (2001).

    Article  CAS  PubMed  Google Scholar 

  79. J. A. Siuciak, C. Boylan, M. Fritsche, and R. M. Lindsay, “BDNF increases monoaminergic activity in rat brain following intracerebroventricular or intraparenchymal administration,” Brain Res., 710, No. 1–2, 11–20 (1996).

    Article  CAS  PubMed  Google Scholar 

  80. J. Soule, E. Messaoudi, and C. R. Bramham, “Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain,” Biochem. Soc. Trans., 34, No. 4, 600–604 (2006).

    Article  CAS  PubMed  Google Scholar 

  81. O. Steward, C. S. Wallace, G. L. Lyford, and P. F. Worley, “Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites,” Neuron, 21, No. 4, 741–751 (1998).

    Article  CAS  PubMed  Google Scholar 

  82. N. R. Swerdlow, C. H. Benbow, S. Zisook, et al., “A preliminary assessment of sensorimotor gating in patients with obsessive compulsive disorder,” Biol. Psychiatry, 33, 298–301 (1993).

    Article  CAS  PubMed  Google Scholar 

  83. N. R. Swerdlow, K. Ludewig, M. A. Geyer, and F. X. Vollenweider, “Deficits in prepulse inhibition and habituation in never-medicated, first-episode schizophrenia,” Biol. Psychiatry, 54, 121–128 (2003).

    Article  Google Scholar 

  84. M. Takahashi, A. Kakita, T. Futamura, et al., “Sustained brain-derived neurotrophic factor up-regulation and sensorimotor gating abnormality induced by postnatal exposure to phencyclidine: comparison with adult treatment,” J. Neurochem., 99, 770–780 (2006).

    Article  CAS  PubMed  Google Scholar 

  85. H. K. Teng, K. K. Teng, R. Lee, et al., “ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin,” J. Neurosci., 25, No. 22, 5455–5463 (2005).

    Article  CAS  PubMed  Google Scholar 

  86. M. A. Tikhonova, A. V. Kulikov, D. V. Bazovkina, et al., “Antidepressant-like effect of central BDNF administration in mice of Antidepressant-Sensitive Catalepsy (ASC) strain,” Chinese J. Physiol., 55, No. 4, 115–125 (2012).

    Google Scholar 

  87. F. Vanevski and B. Xu, “Molecular and neural bases underlying roles of BDNF in the control of body weight,” Front. Neurosci., 7, 37 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  88. C. T. Wang, H. A. Shui, R. L. Huang, et al., “Sexual motivation is demasculinized, but not feminized, in prenatally stressed male rats,” Neuroscience, 138, No. 2, 357–364 (2006).

    Article  CAS  PubMed  Google Scholar 

  89. I. L. Ward, “Prenatal stress feminizes and demasculinizes the behavior of males,” Science, 175, 82–84 (1972).

    Article  CAS  PubMed  Google Scholar 

  90. I. L. Ward, O. L. Ward, R. J. Winn, and D. Bielawski, “Male and female sexual behavior potential of male rats prenatally exposed to the influence of alcohol, stress or both factors,” Behav. Neurosci., 108, No. 6, 1188–1195 (1994).

    Article  CAS  PubMed  Google Scholar 

  91. O. B. Ward, I. L. Ward, J. H. Denning, et al., “Hormonal mechanisms underlying aberrant sexual differentiation in male rats prenatally exposed to alcohol, stress, or both,” Arch. Sex. Behav., 31, No. 1, 9–16 (2002).

    Article  PubMed  Google Scholar 

  92. N. H. Woo, H. K. Teng, C. Siao, et al., “Activation of p75NTR by proBDNF facilitates hippocampal long-term depression,” Nat. Neurosci., 8, 1069–1077 (2005).

    Article  CAS  PubMed  Google Scholar 

  93. C.-M. Yeh, C. Huang, and K.-S. Hsu, “Prenatal stress alters hippocampal synaptic plasticity in young rat offspring through preventing the proteolytic conversion of pro-BDNF to mature BDNF,” J. Physiol., 590, 1309–1310 (2012).

    Article  Google Scholar 

  94. Y. Yin, G. M. Edelman, and P. W. Vanderkish, “The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes,” Proc. Natl. Acad. Sci. USA, 99, No. 4, 2368–2373 (2002).

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  95. R. Zanardi, F. Artigas, R. Moresco, et al., “Increased 5-hydroxytryptamine-2 receptor binding in the frontal cortex of depressed patients responding to paroxetine treatment: a positron emission tomography scan study,” J. Clin. Psychopharmacol., 21, 53–58 (2001).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia

    N. K. Popova & M. V. Morozova

Authors
  1. N. K. Popova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. V. Morozova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. K. Popova.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 99, No. 10, pp. 1125–1137, October, 2013.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popova, N.K., Morozova, M.V. Brain-Derived Neurotrophic Factor: Effects on Genetically and Epigenetically Determined Behavioral Disorders. Neurosci Behav Physi 45, 568–575 (2015). https://doi.org/10.1007/s11055-015-0111-y

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-015-0111-y

Keywords

Search

Navigation