Expression and dendritic trafficking of BDNF-6 splice variant are impaired in knock-in mice carrying human BDNF Val66Met polymorphism

International Journal of Neuropsychopharmacology

Volumn 18, Issue 12, 2015, Pages 1-10

  Mallei, Alessandra ^a   Baj, Gabriele ^b   Ieraci, Alessandro ^a   Corna, Stefano ^a   Musazzi, Laura ^a   Lee, Francis S ^c   Tongiorgi, Enrico ^b   Popoli, Maurizio ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

BDNF; Dendritic trafficking; Epigenetics; Histone; Val66Met polymorphism

Indexed keywords

3 DEAZANEPLANOCIN A; ACETYLHISTONE H3; BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE H3; METHIONINE; PILOCARPINE; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; VALINE; BRAIN-DERIVED NEUROTROPHIC FACTOR, HUMAN; EZH2 PROTEIN, MOUSE; HISTONE DEMETHYLASE; ISOPROTEIN; KDM6B PROTEIN, MOUSE; MUSCARINIC AGENT; POLYCOMB REPRESSIVE COMPLEX 2;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DENDRITE; EPIGENETICS; EXON; GENE EXPRESSION; GENETIC POLYMORPHISM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IN SITU HYBRIDIZATION; MALE; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; ANIMAL; COMPARATIVE STUDY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE TARGETING; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHROMATIN IMMUNOPRECIPITATION; DENDRITES; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE KNOCK-IN TECHNIQUES; HUMANS; IN SITU HYBRIDIZATION; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; MICE, TRANSGENIC; MUSCARINIC AGONISTS; PILOCARPINE; POLYCOMB REPRESSIVE COMPLEX 2; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; PROTEIN TRANSPORT;

EID: 84955593283     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyv069     Document Type: Article

References (49)

1. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T (2007) Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85:525-535.
2. Baj G, Leone E, Chao MV, Tongiorgi E (2011) Spatial segregation of BDNF transcripts enables BDNF to differentially shape distinct dendritic compartments. Proc Natl Acad Sci USA 108:16813-16818.
3. Baj G, D'Alessandro V, Musazzi L, Mallei A, Sartori CR, Sciancalepore M, Tardito D, Langone F, Popoli M, Tongiorgi E (2012) Physical exercise and antidepressants enhance BDNF targeting in hippocampal CA3 dendrites: further evidence of a spatial code for BDNF splice variants. Neuropsychopharmacology 37:1600-1611.
4. Baj G, Carlino D, Gardossi L and Tongiorgi E (2013a) Toward a unified biological hypothesis for the BDNF Val66Met-associated memory deficits in humans: a model of impaired dendritic mRNA trafficking. Front Neurosci 7:188. doi: 10.3389/fnins.2013.00188
5. Baj G, Del Turco D, Schlaudraff J, Torelli L, Deller T, Tongiorgi E (2013b) Regulation of the spatial code for BDNF mRNA isoforms in the rat hippocampus following pilocarpine-treatment: a systematic analysis using laser microdissection and quantitative real-time PCR. Hippocampus 23:413-423.
6. Bath KG, Jing DQ, Dincheva I, Neeb CC, Pattwell SS, Chao MV, Lee FS, Ninan I (2012) BDNF Val66Met impairs fluoxetine-induced enhancement of adult hippocampus plasticity. Neuropsychopharmacology 37:1297-1304.
7. Castren E, Voikar V, Rantamaki T (2007) Role of neurotrophic factors in depression. Curr Opin Pharmacol 7:18-21.
8. Chang CJ, Hung MC (2012) The role of EZH2 in tumour progression. Br J Cancer 106:243-247.
9. Chen ZY, Jing D, Bath KG, Ieraci A, Khan T, Siao CJ, Herrera DG, Toth M, Yang C, McEwen BS, Hempstead BL, Lee FS (2006) Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314:140-143.
10. Chiaruttini C, Sonego M, Baj G, Simonato M, Tongiorgi E (2008) BDNF mRNA splice variants display activity-dependent targeting to distinct hippocampal laminae. Mol Cell Neurosci 37:11-19.
11. Chiaruttini C, Vicario A, Li Z, Baj G, Braiuca P, Wu Y, Lee FS, Gardossi L, Baraban JM, Tongiorgi E (2009) Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation. Proc Natl Acad Sci USA 106:16481-16486.
12. Deb G, Singh AK, Gupta S (2014) EZH2: not EZHY (easy) to deal. Mol Cancer Res 12:639-653.
13. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116-1127.
14. Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112:257-269.
15. Frielingsdorf H, Bath KG, Soliman F, Difede J, Casey BJ, Lee FS (2010) Variant brain-derived neurotrophic factor Val66Met endophenotypes: implications for posttraumatic stress disorder. Ann NY Acad Sci 1208:150-157.
16. Frodl T, Schule C, Schmitt G, Born C, Baghai T, Zill P, Bottlender R, Rupprecht R, Bondy B, Reiser M, Moller HJ, Meisenzahl EM (2007) Association of the brain-derived neurotrophic factor Val66Met polymorphism with reduced hippocampal volumes in major depression. Arch Gen Psychiatry 64:410-416.
17. Fukumoto N et al. (2010) Sexually dimorphic effect of the Val-66Met polymorphism of BDNF on susceptibility to Alzheimer's disease: new data and meta-analysis. Am J Med Genet B Neuropsychiatr Genet 153B:235-242.
18. Hariri AR, Goldberg TE, Mattay VS, Kolachana BS, Callicott JH, Egan MF, Weinberger DR (2003) Brain-derived neurotrophic factor val66met polymorphism affects human memoryrelated hippocampal activity and predicts memory performance. J Neurosci 23:6690-6694.
19. Hong CJ, Liou YJ, Tsai SJ (2011) Effects of BDNF polymorphisms on brain function and behavior in health and disease. Brain Res Bull 86:287-297.
20. Ieraci A, Mallei A, Musazzi L and Popoli M (2015) Physical exercise and acute restraint stress differentially modulate hippocampal brain-derived neurotrophic factor transcripts and epigenetic mechanisms in the mouse. Hippocampus. Advance online publication. Retrieved 14 May 2015. doi: 10.11002/hipo.22458
21. Kikuchi J, Takashina T, Kinoshita I, Kikuchi E, Shimizu Y, Sakakibara-Konishi J, Oizumi S, Marquez VE, Nishimura M, Dosaka-Akita H (2012) Epigenetic therapy with 3-deazaneplanocin A, an inhibitor of the histone methyltransferase EZH2, inhibits growth of non-small cell lung cancer cells. Lung Cancer 78:138-143.
22. Laugesen A, Helin K (2014) Chromatin repressive complexes in stem cells, development, and cancer. Cell Stem Cell 14:735-751.
23. Li WJ, Yu H, Yang JM, Gao J, Jiang H, Feng M, Zhao YX, Chen ZY (2010) Anxiolytic effect of music exposure on BDNFMet/Met transgenic mice. Brain Res 1347:71-79.
24. Mallei A, Rabin SJ, Mocchetti I (2004) Autocrine regulation of nerve growth factor expression by Trk receptors. J Neurochem 90:1085-1093.
25. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343-349.
26. Martinez-Levy GA, Cruz-Fuentes CS (2014) Genetic and epigenetic regulation of the brain-derived neurotrophic factor in the central nervous system. Yale J Biol Med 87:173-186.
27. Martinowich K, Manji H, Lu B (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10:1089-1093.
28. Mitić T, Caporali A, Floris I, Meloni M, Marchetti M, Urrutia R, Angelini GD, Emanueli C (2015) EZH2 modulates angiogenesis in vitro and in a mouse model of limb ischemia. Mol Ther 23:32-42.
29. Musazzi L, Rimland JM, Ieraci A, Racagni G, Domenici E, Popoli M (2014) Pharmacological characterization of BDNF promoters I, II and IV reveals that serotonin and norepinephrine input is sufficient for transcription activation. Int J Neuropsychop 17:779-91.
30. Ninan I, Bath KG, Dagar K, Perez-Castro R, Plummer MR, Lee FS, Chao MV (2010) The BDNF Val66Met polymorphism impairs NMDA receptor-dependent synaptic plasticity in the hippocampus. J Neurosci 30:8866-8870.
31. Pasini D, Bracken AP, Helin K (2004) Polycomb group proteins in cell cycle progression and cancer. Cell Cycle 3:396-400.
32. Popoli M (2012) Multi-method approaches to pharmacogenomics in animal models. Int J Neuropsychop 15(Supp 1):p. 25.
33. Poulsen FR, Lauterborn J, Zimmer J, Gall CM (2004) Differential expression of brain-derived neurotrophic factor transcripts after pilocarpine-induced seizure-like activity is related to mode of Ca2+ entry. Neuroscience 126:665-676.
34. Qi C, Liu S, Qin R, Zhang Y, Wang G, Shang Y, Wang Y, Liang J (2014) Coordinated regulation of dendrite arborization by epigenetic factors CDYL and EZH2. J Neurosci 34:4494-4508.
35. Sanacora G, Treccani G, Popoli M (2012) Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 62:63-77.
36. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108.
37. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.
38. Soliman F, Glatt CE, Bath KG, Levita L, Jones RM, Pattwell SS, Jing D, Tottenham N, Amso D, Somerville LH, Voss HU, Glover G, Ballon DJ, Liston C, Teslovich T, Van Kempen T, Lee FS, Casey BJ (2010) A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 327:863-866.
39. Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741-751.
40. Tardito D, Perez J, Tiraboschi E, Musazzi L, Racagni G, Popoli M (2006) Signaling pathways regulating gene expression, neuroplasticity, and neurotrophic mechanisms in the action of antidepressants: a critical overview. Pharmacol Rev 58:115-134.
41. Tongiorgi E, Righi M, Cattaneo A (1998) A non-radioactive in situ hybridization method that does not require RNAse-free conditions. J Neurosci Methods 85:129-139.
42. Tongiorgi E, Armellin M, Giulianini PG, Bregola G, Zucchini S, Paradiso B, Steward O, Cattaneo A, Simonato M (2004) Brainderived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis. J Neurosci 24:6842-6852.
43. Tsankova NM, Kumar A, Nestler EJ (2004) Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci 24:5603-5610.
44. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006) Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519-525.
45. Verhagen M, van der Meij A, van Deurzen PA, Janzing JG, Arias-Vasquez A, Buitelaar JK, Franke B (2010) Meta-analysis of the BDNF Val66Met polymorphism in major depressive disorder: effects of gender and ethnicity. Mol Psychiatry 15:260-271.
46. Weinmann AS, Bartley SM, Zhang T, Zhang MQ, Farnham PJ (2001) Use of chromatin immunoprecipitation to clone novel E2F target promoters. Mol Cell Biol 21:6820-6832.
47. Wibrand K, Messaoudi E, Havik B, Steenslid V, Lovlie R, Steen VM, Bramham CR (2006) Identification of genes co-upregulated with Arc during BDNF-induced long-term potentiation in adult rat dentate gyrus in vivo. Eur J Neurosci 23:1501-1511.
48. Yasuda M, Fukuchi M, Tabuchi A, Kawahara M, Tsuneki H, Azuma Y, Chiba Y, Tsuda M (2007) Robust stimulation of TrkB induces delayed increases in BDNF and Arc mRNA expressions in cultured rat cortical neurons via distinct mechanisms. J Neurochem 103:626-636.
49. Yu H, Wang DD, Wang Y, Liu T, Lee FS, Chen ZY (2012) Variant brain-derived neurotrophic factor Val66Met polymorphism alters vulnerability to stress and response to antidepressants. J Neurosci 32:4092-4101.