Overexpression of the full-length neurotrophin receptor trkB regulates the expression of plasticity-related genes in mouse brain

Molecular Brain Research

Volumn 130, Issue 1-2, 2004, Pages 81-94

  Koponen, Eija ^a   Lakso, Merja ^a   Castrén, Eero ^b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

CaMKII; BDNF; GAP 43; Immediate early genes; In situ hybridization; Transgenic mice

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MESSENGER RNA; NEUROMODULIN; NEUROPEPTIDE Y; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; DATA ANALYSIS; DENTATE GYRUS; GENE OVEREXPRESSION; HIPPOCAMPUS; LEARNING; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM; NONHUMAN; ONCOGENE C FOS; ONCOGENE C JUN; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL COUNT; FEMALE; GAP-43 PROTEIN; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; NEUROPEPTIDE Y; ONCOGENE PROTEIN P65(GAG-JUN); ONCOGENE PROTEINS V-FOS; RECEPTOR, TRKB; RNA, MESSENGER;

MUS MUSCULUS;

EID: 7444243313     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbrainres.2004.07.010     Document Type: Article

References (91)

1. L. Aigner, S. Arber, J.P. Kapfhammer, T. Laux, C. Schneider, F. Botteri, H.R. Brenner, and P. Caroni Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice Cell 83 1995 269 278
2. K.L. Allendoerfer, R.J. Cabelli, E. Escandon, D.R. Kaplan, K. Nikolics, and C.J. Shatz Regulation of neurotrophin receptors during the maturation of the mammalian visual system J. Neurosci. 14 1994 1795 1811
3. C.A. Altar, J.A. Siuciak, P. Wright, N.Y. Ip, R.M. Lindsay, and S.J. Wiegand In situ hybridization of trkB and trkC receptor mRNA in rat forebrain and association with high-affinity binding of [125I]BDNF, [125I]NT-4/5 and [125I]NT-3 Eur. J. Neurosci. 6 1994 1389 1405
4. K. Andra, D. Abramowski, M. Duke, A. Probst, K.H. Wiederhold, K. Burki, M. Goedert, B. Sommer, and M. Staufenbiel Expression of APP in transgenic mice: a comparison of neuron-specific promoters Neurobiol. Aging 17 1996 183 190
5. M. Barbacid The Trk family of neurotrophin receptors J. Neurobiol. 25 1994 1386 1403
6. A. Barco, J.M. Alarcon, and E.R. Kandel Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture Cell 108 2002 689 703
7. L.I. Benowitz, and A. Routtenberg GAP-43: an intrinsic determinant of neuronal development and plasticity Trends Neurosci. 20 1997 84 91
8. P.R. Blanquet, J. Mariani, and P. Derer A calcium/calmodulin kinase pathway connects brain-derived neurotrophic factor to the cyclic AMP-responsive transcription factor in the rat hippocampus Neuroscience 118 2003 477 490
9. R.J. Cabelli, K.L. Allendoerfer, M.J. Radeke, A.A. Welcher, S.C. Feinstein, and C.J. Shatz Changing patterns of expression and subcellular localization of TrkB in the developing visual system J. Neurosci. 16 1996 7965 7980
10. M. Caprini, A. Gomis, H. Cabedo, R. Planells-Cases, C. Belmonte, F. Viana, and A. Ferrer-Montiel GAP43 stimulates inositol trisphosphate-mediated calcium release in response to hypotonicity EMBO J. 22 2003 3004 3014
11. P. Caroni Overexpression of growth-associated proteins in the neurons of adult transgenic mice J. Neurosci. Methods 71 1997 3 9
12. E. Castren, B. Berninger, A. Leingartner, and D. Lindholm Regulation of brain-derived neurotrophic factor mRNA levels in hippocampus by neuronal activity Prog. Brain Res. 117 1998 57 64
13. S.D. Croll, S.J. Wiegand, K.D. Anderson, R.M. Lindsay, and H. Nawa Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF Eur. J. Neurosci. 6 1994 1343 1353
14. S.D. Croll, C. Suri, D.L. Compton, M.V. Simmons, G.D. Yancopoulos, R.M. Lindsay, S.J. Wiegand, J.S. Rudge, and H.E. Scharfman Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex Neuroscience 93 1999 1491 1506
15. C. Dolci, A. Montaruli, E. Roveda, I. Barajon, L. Vizzotto, G. Grassi Zucconi, and F. Carandente Circadian variations in expression of the trkB receptor in adult rat hippocampus Brain Res. 994 2003 67 72
16. C.T. Drake, T.A. Milner, and S.L. Patterson Ultrastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity J. Neurosci. 19 1999 8009 8026
17. J. Du, L. Feng, F. Yang, and B. Lu Activity- and Ca(2+)-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons J. Cell Biol. 150 2000 1423 1434
18. E. Elmer, M. Kokaia, Z. Kokaia, I. Ferencz, and O. Lindvall Delayed kindling development after rapidly recurring seizures: relation to mossy fiber sprouting and neurotrophin, GAP-43 and dynorphin gene expression Brain Res. 712 1996 19 34
19. E. Elmer, M. Kokaia, P. Ernfors, I. Ferencz, Z. Kokaia, and O. Lindvall Suppressed kindling epileptogenesis and perturbed BDNF and TrkB gene regulation in NT-3 mutant mice Exp. Neurol. 145 1997 93 103
20. P.C. Emson In-situ hybridization as a methodological tool for the neuroscientist Trends Neurosci. 16 1993 9 16
21. C.C. Fink, and T. Meyer Molecular mechanisms of CaMKII activation in neuronal plasticity Curr. Opin. Neurobiol. 12 2002 293 299
22. S. Finkbeiner, S.F. Tavazoie, A. Maloratsky, K.M. Jacobs, K.M. Harris, and M.E. Greenberg CREB: a major mediator of neuronal neurotrophin responses Neuron 19 1997 1031 1047
23. W. Fischer, A. Sirevaag, S.J. Wiegand, R.M. Lindsay, and A. Bjorklund Reversal of spatial memory impairments in aged rats by nerve growth factor and neurotrophins 3 and 4/5 but not by brain-derived neurotrophic factor Proc. Natl. Acad. Sci. U. S. A. 91 1994 8607 8611
24. R.H. Fryer, D.R. Kaplan, S.C. Feinstein, M.J. Radeke, D.R. Grayson, and L.F. Kromer Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain J. Comp. Neurol. 374 1996 21 40
25. C. Gall, J. Lauterborn, P. Isackson, and J. White Seizures, neuropeptide regulation, and mRNA expression in the hippocampus Prog. Brain Res. 83 1990 371 390
26. K.P. Giese, N.B. Fedorov, R.K. Filipkowski, and A.J. Silva Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning Science 279 1998 870 873
27. S. Glazewski, K.P. Giese, A. Silva, and K. Fox The role of alpha-CaMKII autophosphorylation in neocortical experience-dependent plasticity Nat. Neurosci. 3 2000 911 918
28. M. Gonzalez, F.P. Ruggiero, Q. Chang, Y.J. Shi, M.M. Rich, S. Kraner, and R.J. Balice-Gordon Disruption of trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions Neuron 24 1999 567 583
29. L.J. Goodman, J. Valverde, F. Lim, M.D. Geschwind, H.J. Federoff, A.I. Geller, and F. Hefti Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons Mol. Cell. Neurosci. 7 1996 222 238
30. T. Herdegen, and J.D. Leah Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins Brain Res. Rev. 28 1998 370 490
31. A.J. Holtmaat, P.A. Dijkhuizen, A.B. Oestreicher, H.J. Romijn, N.M. Van der Lugt, A. Berns, F.L. Margolis, W.H. Gispen, and J. Verhaagen Directed expression of the growth-associated protein B-50/GAP-43 to olfactory neurons in transgenic mice results in changes in axon morphology and extraglomerular fiber growth J. Neurosci. 15 1995 7953 7965
32. E.J. Huang, and L.F. Reichardt TRK receptors: roles in neuronal signal transduction Annu. Rev. Biochem. 27 2003 27
33. N.Y. Ip, T.N. Stitt, P. Tapley, R. Klein, D.J. Glass, J. Fandl, L.A. Greene, M. Barbacid, and G.D. Yancopoulos Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells Neuron 10 1993 137 149
34. N. Irwin, S. Chao, L. Goritchenko, A. Horiuchi, P. Greengard, A.C. Nairn, and L.I. Benowitz Nerve growth factor controls GAP-43 mRNA stability via the phosphoprotein ARPP-19 Proc. Natl. Acad. Sci. U. S. A. 99 2002 12427 12431
35. K.R. Jones, I. Farinas, C. Backus, and L.F. Reichardt Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron Dev. Cell 76 1994 989 999
36. R. Klein, D. Conway, L.F. Parada, and M. Barbacid The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain Cell 61 1990 647 656
37. R. Klein, D. Martin-Zanca, M. Barbacid, and L.F. Parada Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system Development 109 1990 845 850
38. N. Klocker, M. Jung, C.A. Stuermer, and M. Bahr BDNF increases the number of axotomized rat retinal ganglion cells expressing GAP-43, L1, and TAG-1 mRNA-a supportive role for nitric oxide? Neurobiol. Dis. 8 2001 103 113
39. Z. Kokaia, J. Bengzon, M. Metsis, M. Kokaia, H. Persson, and O. Lindvall Coexpression of neurotrophins and their receptors in neurons of the central nervous system Proc. Natl. Acad. Sci. U. S. A. 90 1993 6711 6715
40. E. Koponen, V. Voikar, R. Riekki, T. Saarelainen, T. Rauramaa, H. Rauvala, T. Taira, and E. Castren Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLC[gamma] pathway, reduced anxiety, and facilitated learning Mol. Cell. Neurosci. 26 2004 166 1181
41. M. Korte, P. Carroll, E. Wolf, G. Brem, H. Thoenen, and T. Bonhoeffer Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor Proc. Natl. Acad. Sci. U. S. A. 92 1995 8856 8860
42. K.J. Kovacs c-Fos as a transcription factor: a stressful (re)view from a functional map Neurochem. Int. 33 1998 287 297
43. S. Lahteinen, A. Pitkanen, T. Saarelainen, J. Nissinen, E. Koponen, and E. Castren Decreased BDNF signalling in transgenic mice reduces epileptogenesis Eur. J. Neurosci. 15 2002 721 734
44. S. Lahteinen, A. Pitkanen, E. Koponen, T. Saarelainen, and E. Castren Exacerbated status epilepticus and acute cell loss, but no changes in epileptogenesis, in mice with increased brain-derived neurotrophic factor signaling Neuroscience 122 2003 1081 1092
45. O. Lindvall, Z. Kokaia, J. Bengzon, E. Elmer, and M. Kokaia Neurotrophins and brain insults Trends Neurosci. 17 1994 490 496
46. A. Luthi, H. Van der Putten, F.M. Botteri, I.M. Mansuy, M. Meins, U. Frey, G. Sansig, C. Portet, M. Schmutz, M. Schroder, C. Nitsch, J.P. Laurent, and D. Monard Endogenous serine protease inhibitor modulates epileptic activity and hippocampal long-term potentiation J. Neurosci. 17 1997 4688 4699
47. P.C. Maisonpierre, L. Belluscio, B. Friedman, R.F. Alderson, S.J. Wiegand, M.E. Furth, R.M. Lindsay, and G.D. Yancopoulos NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression Neuron 5 1990 501 509
48. Y. Masana, A. Wanaka, H. Kato, T. Asai, and M. Tohyama Localization of trkB mRNA in postnatal brain Development J Neurosci. Res. 35 1993 468 479
49. R.K. McNamara, U. Namgung, and A. Routtenberg Distinctions between hippocampus of mouse and rat: protein F1/GAP-43 gene expression, promoter activity, and spatial memory Mol. Brain Res. 40 1996 177 187
50. P.J. Meberg, and A. Routtenberg Selective expression of protein F1/(GAP-43) mRNA in pyramidal but not granule cells of the hippocampus Neuroscience 45 1991 721 733
51. P.J. Meberg, C.M. Gall, and A. Routtenberg Induction of F1/GAP-43 gene expression in hippocampal granule cells after seizures Mol. Brain Res. 17 1993 295 299 ([corrected][erratum appears in Mol Brain Res 1993 Jul;19(1-2):179])
52. D.S. Middlemas, R.A. Lindberg, and T. Hunter trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors Mol. Cell. Biol. 11 1991 143 153
53. L. Minichiello, M. Korte, D. Wolfer, R. Kuhn, K. Unsicker, V. Cestari, C. Rossi-Arnaud, H.P. Lipp, T. Bonhoeffer, and R. Klein Essential role for TrkB receptors in hippocampus-mediated learning Neuron 24 1999 401 414
54. L. Minichiello, A.M. Calella, D.L. Medina, T. Bonhoeffer, R. Klein, and M. Korte Mechanism of TrkB-mediated hippocampal long-term potentiation Neuron 36 2002 121 137
55. K. Miyake, W. Yamamoto, M. Tadokoro, N. Takagi, K. Sasakawa, A. Nitta, S. Furukawa, and S. Takeo Alterations in hippocampal GAP-43, BDNF, and L1 following sustained cerebral ischemia Brain Res. 935 2002 24 31
56. U. Namgung, S. Matsuyama, and A. Routtenberg Long-term potentiation activates the GAP-43 promoter: selective participation of hippocampal mossy cells Proc. Natl. Acad. Sci. U. S. A. 94 1997 11675 11680
57. E.J. Nestler, M.B. Kelz, and J. Chen DeltaFosB: a molecular mediator of long-term neural and behavioral plasticity Brain Res. 835 1999 10 17
58. K. Obst, M. Bronzel, and P. Wahle Visual activity is required to maintain the phenotype of supragranular NPY neurons in rat area 17 Eur. J. Neurosci. 10 1998 1422 1428
59. Y. Ouyang, A. Rosenstein, G. Kreiman, E.M. Schuman, and M.B. Kennedy Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin- dependent protein kinase II via dendritic protein synthesis in hippocampal neurons J. Neurosci. 19 1999 7823 7833
60. M.A. Paradies, and O. Steward Multiple subcellular mRNA distribution patterns in neurons: a nonisotopic in situ hybridization analysis J. Neurobiol. 33 1997 473 493
61. S.L. Patterson, T. Abel, T.A. Deuel, K.C. Martin, J.C. Rose, and E.R. Kandel Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice Neuron 16 1996 1137 1145
62. C. Pittenger, Y.Y. Huang, R.F. Paletzki, R. Bourtchouladze, H. Scanlin, S. Vronskaya, and E.R. Kandel Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory Neuron 34 2002 447 462
63. W. Plunet, B.K. Kwon, and W. Tetzlaff Promoting axonal regeneration in the central nervous system by enhancing the cell body response to axotomy J. Neurosci. Res. 68 2002 1 6
64. X. Qiao, C. Suri, B. Knusel, and J.L. Noebels Absence of hippocampal mossy fiber sprouting in transgenic mice overexpressing brain-derived neurotrophic factor J. Neurosci. Res. 64 2001 268 276
65. S. Reibel, B. Vivien-Roels, B.T. Le, Y. Larmet, J. Carnahan, C. Marescaux, and A. Depaulis Overexpression of neuropeptide Y induced by brain-derived neurotrophic factor in the rat hippocampus is long lasting Eur. J. Neurosci. 12 2000 595 605
66. M. Righi, E. Tongiorgi, and A. Cattaneo Brain-derived neurotrophic factor (BDNF) induces dendritic targeting of BDNF and tyrosine kinase B mRNAs in hippocampal neurons through a phosphatidylinositol-3 kinase-dependent pathway J. Neurosci. 20 2000 3165 3174
67. T. Ringstedt, H. Lagercrantz, and H. Persson Expression of members of the trk family in the developing postnatal rat brain Dev. Brain Res. 72 1993 119 131
68. A. Routtenberg, I. Cantallops, S. Zaffuto, P. Serrano, and U. Namgung Enhanced learning after genetic overexpression of a brain growth protein Proc. Natl. Acad. Sci. U. S. A. 97 2000 7657 7662
69. T. Saarelainen, R. Pussinen, E. Koponen, L. Alhonen, G. Wong, J. Sirvio, and E. Castren Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons have impaired long-term spatial memory but normal hippocampal LTP Synapse 38 2000 102 104
70. H.E. Scharfman, J.H. Goodman, A.L. Sollas, and S.D. Croll Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor Exp. Neurol. 174 2002 201 214
71. A.F. Schinder, and M. Poo The neurotrophin hypothesis for synaptic plasticity Trends Neurosci. 23 2000 639 645
72. A.J. Shaywitz, and M.E. Greenberg CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals Annu. Rev. Biochem. 68 1999 821 861
73. M. Sheng, M.A. Thompson, and M.E. Greenberg CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases Science 252 1991 1427 1430
74. A.J. Silva Molecular and cellular cognitive studies of the role of synaptic plasticity in memory J. Neurobiol. 54 2003 224 237
75. A.J. Silva, J.H. Kogan, P.W. Frankland, and S. Kida CREB and memory Annu. Rev. Neurosci. 21 1998 127 148
76. A.P. Silva, C. Cavadas, and E. Grouzmann Neuropeptide Y and its receptors as potential therapeutic drug targets Clin. Chim. Acta 326 2002 3 25
77. T.R. Soderling CaM-kinases: modulators of synaptic plasticity Curr. Opin. Neurobiol. 10 2000 375 380
78. C.A. Tobias, J.S. Shumsky, M. Shibata, M.H. Tuszynski, I. Fischer, A. Tessler, and M. Murray Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration Exp. Neurol. 184 2003 97 113
79. E.A. Tolner, E.A. van Vliet, A.J. Holtmaat, E. Aronica, M.P. Witter, F.H. da Silva, and J.A. Gorter GAP-43 mRNA and protein expression in the hippocampal and parahippocampal region during the course of epileptogenesis in rats Eur. J. Neurosci. 17 2003 2369 2380
80. E. Tongiorgi, M. Righi, and A. Cattaneo Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons J. Neurosci. 17 1997 9492 9505
81. E. Tongiorgi, M. Righi, and A. Cattaneo A non-radioactive in situ hybridization method that does not require RNAse-free conditions J. Neurosci. Methods 85 1998 129 139
82. E. Tongiorgi, A. Cattaneo, and L. Domenici Co-expression of TrkB and the N-methyl-d-aspartate receptor subunits NR1-C1, NR2A and NR2B in the rat visual cortex Neuroscience 90 1999 1361 1369
83. W.J. Tyler, M. Alonso, C.R. Bramham, and L.D. Pozzo-Miller From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning Learn. Mem. 9 2002 224 237
84. A.E. West, W.G. Chen, M.B. Dalva, R.E. Dolmetsch, J.M. Kornhauser, A.J. Shaywitz, M.A. Takasu, X. Tao, and M.E. Greenberg Calcium regulation of neuronal gene expression Proc. Natl. Acad. Sci. U. S. A. 98 2001 11024 11031
85. A. Vezzani, G. Sperk, and W.F. Colmers Neuropeptide Y: emerging evidence for a functional role in seizure modulation Trends Neurosci. 22 1999 25 30
86. W.M.B. Wisden In Situ Hybridization with Synthetic Oligonucleotide Probes 1994 Academic Press London
87. W. Wisden, D. Cope, T. Klausberger, B. Hauer, S.T. Sinkkonen, V. Tretter, R. Lujan, A. Jones, E.R. Korpi, I. Mody, W. Sieghart, and P. Somogyi Ectopic expression of the GABA(A) receptor alpha6 subunit in hippocampal pyramidal neurons produces extrasynaptic receptors and an increased tonic inhibition Neuropharmacology 43 2002 530 549
88. K. Wu, J.L. Xu, P.C. Suen, E. Levine, Y.Y. Huang, H.T. Mount, S.Y. Lin, and I.B. Black Functional trkB neurotrophin receptors are intrinsic components of the adult brain postsynaptic density Mol. Brain Res. 43 1996 286 290
89. S.W. Ying, M. Futter, K. Rosenblum, M.J. Webber, S.P. Hunt, T.V. Bliss, and C.R. Bramham Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis J. Neurosci. 22 2002 1532 1540
90. E.A. Young, E.H. Owen, K.F. Meiri, and J.M. Wehner Alterations in hippocampal GAP-43 phosphorylation and protein level following contextual fear conditioning Brain Res. 860 2000 95 103
91. J. Zhang, D. Zhang, J.S. McQuade, M. Behbehani, J.Z. Tsien, and M. Xu c-fos regulates neuronal excitability and survival Nat. Genet. 30 2002 416 420