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

Volumn 23, Issue 5, 2013, Pages 413-423

  Baj, Gabriele ^a   Del Turco, Domenico ^b   Schlaudraff, Jessica ^b   Torelli, Lucio ^a   Deller, Thomas ^b   Tongiorgi, Enrico ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

MRNA trafficking; Neuronal dendrites; Neurotrophic factors; Pilocarpine seizures; Untranslated regions

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EPILEPTIC STATE; EXON; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HYPOTHESIS; LASER MICRODISSECTION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPATIAL CODE HYPOTHESIS; STRATUM RADIATUM;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENDRITES; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MICRODISSECTION; MUSCARINIC AGONISTS; NEURONS; PILOCARPINE; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; STATISTICS, NONPARAMETRIC;

EID: 84876120607     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22100     Document Type: Article

References (38)

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. Aliaga EE, Mendoza I, Tapia-Arancibia L. 2009. Distinct subcellular localization of BDNF transcripts in cultured hypothalamic neurons and modification by neuronal activation. J Neural Transm 116: 23-32.
3. Amaral DG, Witter MP. 1989. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31: 571-591.
4. 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 U S A 108: 16813-16818.
5. 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.
6. Burbach GJ, Dehn D, Del Turco D, Deller T. 2003. Quantification of layer-specific gene expression in the hippocampus: effective use of laser microdissection in combination with quantitative RT-PCR. J Neurosci Methods 131: 83-91.
7. 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.
8. 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 U S A 106: 16481-16486.
9. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. 2010. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70: 271-288.
10. de Moor CH, Meijer H, Lissenden S. 2005. Mechanisms of translational control by the 3′ UTR in development and differentiation. Semin Cell Dev Biol 16: 49-58.
11. Ermolinsky B, Arshadmansab MF, Pacheco Otalora LF, Zarei MM, Garrido-Sanabria ER. 2008. Deficit of Kcnma1 mRNA expression in the dentate gyrus of epileptic rats. Neuroreport 19: 1291-1294.
12. Garzon DJ, Fahnestock M. 2007. Oligomeric amyloid decreases basal levels of brain-derived neurotrophic factor (BDNF) mRNA via specific downregulation of BDNF transcripts IV and V in differentiated human neuroblastoma cells. J Neurosci 27: 2628-2635.
13. Grillo G, Turi A, Licciulli F, Mignone F, Liuni S, Banfi S, Gennarino VA, Horner DS, Pavesi G, Picardi E, et al. 2010. UTRdb and UTRsite (RELEASE 2010): A collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res 38(Database issue): D75-D80.
14. Gulyas AI, Miles R, Hajos N, Freund TF. 1993. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5: 1729-1751.
15. Katoh-Semba R, Takeuchi IK, Inaguma Y, Ito H, Kato K. 1999. Brain-derived neurotrophic factor, nerve growth and neurotrophin-3 selected regions of the rat brain following kainic acid-induced seizure activity. Neurosci Res 35: 19-29.
16. Knopp A, Kivi A, Wozny C, Heinemann U, Behr J. 2005. Cellular and network properties of the subiculum in the pilocarpine model of temporal lobe epilepsy. J Comp Neurol 483: 476-488.
17. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH, Bassell GJ, Kosik KS. 1996. Translocation of RNA granules in living neurons. J Neurosci 16: 7812-7820.
18. Koppel I, Aid-Pavlidis T, Jaanson K, Sepp M, Pruunsild P, Palm K, Timmusk T. 2009. Tissue-specific and neural activity-regulated expression of human BDNF gene in BAC transgenic mice. BMC Neurosci 10: 68.
19. Kye MJ, Liu T, Levy SF, Xu NL, Groves BB, Bonneau R, Lao K, Kosik KS. 2007. Somatodendritic microRNAs identified by laser capture and multiplex RT-PCR. RNA 13: 1224-1234.
20. Liu QR, Lu L, Zhu XG, Gong JP, Shaham Y, Uhl GR. 2006. Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res 1067: 1-12.
21. Megias M, Emri Z, Freund TF, Gulyas AI. 2001. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102: 527-540.
22. Mignone F, Gissi C, Liuni S, Pesole G. 2002. Untranslated regions of mRNAs. Genome Biol 3: REVIEWS0004.
23. Pattabiraman PP, Tropea D, Chiaruttini C, Tongiorgi E, Cattaneo A, Domenici L. 2005. Neuronal activity regulates the developmental expression and subcellular localization of cortical BDNF mRNA isoforms in vivo. Mol Cell Neurosci 28: 556-570.
24. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
25. Pruunsild P, Kazantseva A, Aid T, Palm K, Timmusk T. 2007. Dissecting the human BDNF locus: Bidirectional transcription, complex splicing, and multiple promoters. Genomics 90: 397-406.
26. Racine RJ. 1972. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
27. Represa A, Ben-Ari Y. 1992. Kindling is associated with the formation of novel mossy fibre synapses in the CA3 region. Exp Brain Res 92: 69-78.
28. Rocamora N, Pascual M, Acsady L, de Lecea L, Freund TF, Soriano E. 1996. Expression of NGF and NT3 mRNAs in hippocampal interneurons innervated by the GABAergic septohippocampal pathway. J Neurosci 16: 3991-4004.
29. Rook MS, Lu M, Kosik KS. 2000. CaMKIIalpha 3′ untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J Neurosci 20: 6385-6393.
30. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
31. Shabalina SA, Spiridonov AN, Spiridonov NA, Koonin EV. 2010. Connections between alternative transcription and alternative splicing in mammals. Genome Biol Evol 2: 791-799.
32. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, et al. 2008. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321: 956-960.
33. Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M, Persson H. 1993. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10: 475-489.
34. Tongiorgi E. 2008. Activity-dependent expression of brain-derived neurotrophic factor in dendrites: Facts and open questions. Neurosci Res 61: 335-346.
35. Tongiorgi E, Righi M, Cattaneo A. 1997. Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17: 9492-9505.
36. Tongiorgi E, Armellin M, Giulianini PG, Bregola G, Zucchini S, Paradiso B, Steward O, Cattaneo A, Simonato M. 2004. Brain-derived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis. J Neurosci 24: 6842-6852.
37. Tongiorgi E, Domenici L, Simonato M. 2006. What is the biological significance of BDNF mRNA targeting in the dendrites? Clues from epilepsy and cortical development. Mol Neurobiol 33: 17-32.
38. Yoshii A, Constantine-Paton M. 2010. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev Neurobiol 70: 304-322.