Signaling mechanisms mediating BDNF modulation of memory formation in vivo in the hippocampus

Cellular and Molecular Neurobiology

Volumn 22, Issue 5-6, 2002, Pages 663-674

  Alonso, Mariana ^a   Vianna, Monica R M ^b   Izquierdo, Ivan ^b   Medina, Jorge H ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Anti BDNF antibody; CREB; Endogenous BDNF; ERK1 2; Inhibitory avoidance learning; Memory consolidation; Signaling pathways

Indexed keywords

ANTIBODY; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1;

ALPHA CHAIN; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BETA CHAIN; CONTROLLED STUDY; ENZYME SUBUNIT; FEAR; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; ANTIBODIES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME INHIBITORS; FEAR; HIPPOCAMPUS; LEARNING; MALE; MAP KINASE SIGNALING SYSTEM; MEMORY; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONAL PLASTICITY; PHOSPHORYLATION; RATS; RATS, WISTAR; RECOMBINANT FUSION PROTEINS;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0036973397     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1021848706159     Document Type: Article

References (57)

1. Alonso, M., Vianna, M. R. M., Depino, A. M., Mello e Souza, T., Pereira, P., Szapiro, G., Viola, H., Pitossi, E, Izquierdo, I., and Medina, J. H. (2002). BNDF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12:551-560.
2. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., and Sweatt, J. D. (1998). The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1:602-609.
3. Bernabeu, R., Bevilaqua, L., Ardenghi, P., Bromberg, E., Schmitz, P., Bianchin, M., Izquierdo, I., and Medina, J. H. (1997). Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc. Natl. Acad. Sci. U.S.A. 94,7041-7046.
4. Bevilaqua, L., Ardenghi, P., Schroder, N., Bromberg, E., Schmitz, R K., Schaeffer, E., Quevedo, J., Bianchin, M., Walz, R., Medina, J. H., and Izquierdo, I, (1997). Drug acting upon the protein kinase A/CREB pathways modulate memory consolidation when given late after training into rat hippocampus but not amygdala. Behav Pharmacol. 8:331-338.
5. Blanquet, P. R. (2000). Identification of two persistently activated neurotrophin-regulated pathways in rat hippocampus. Neuroscience 95:705-719.
6. 2+/calmodulin-dependent protein kinase 2 activity in hippocampus. J. Biol. Chem. 272:24133-24136.
7. Bourtchuladze, R., Frenguelli, B., Blendy, J., Schutz, G., and Silva, A. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element binding protein. Cell 79:59-68.
8. Burgering, B. M., and Coffer, P. J. (1995). Protein kinase B (c-AKT) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376:599-602.
9. Cammarota, M., Bevilaqua, L. R. M., Ardenghi, P., Paratcha, G., Levi de Stein, M., Izquierdo, I., and Medina, J. H. (2000). Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: Abolition by NMDA receptor blockade. Mol. Brain Res. 76:36-46.
10. Cavanaugh, J. E., Ham, J., Hetman, M., Poser, S., Yan, C., and Xia, Z. (2001). Differential regulation of mitogen-activated protein kinases ERK1/2 and ERK5 by neurotrophins, neural activity, and cAMP in neurons. J. Neurosci. 21:434-443.
11. Chen, G., Kolbeck, R., Barde, Y-A., Bonhoeffer, T., and Kossel, A. (1999). Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. J. Neurosci. 19(18):7983-7990.
12. Cirulli, F., Berry, A., and Alleva, E. (2000) Intracerebroventricular administration of brain-derived neurotrophic factor in adult rats affects analgesia and spontanous behavior but not memory retention in a Morris water maze task. Neurosci. Lett. 287:207-210.
13. Croll, S. D., Suri, C., Compton, D. L., Simmons, M. V., Yancopoulos, G. D., Lindsay, R. M., Wiegand, S. J., Rudge, J. S., and Scharfman, H. E. (1999). Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93:1491-1506.
14. Davis, H. P., and Squire, L. R. (2000). Protein synthesis and memory: A review. Psychol. Bull. 96:518-559.
15. Figurov, A., Pozzo-Miller, L., Olafsson, P., Wang, T., and Lu, B. (1996). Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381:706-709.
16. Finkbeiner, S., Tavazoie, S., Maloratsky, A., Jacobs, K., Harris, K., and Greenberg, M. (1997). CREB: A major mediator of neuronal neurotrophin responses. Neuron 19:1031-1047.
17. Fischer, W., Strevaag, A., Wiegand, S. J., Lindsay, R. M., and Björklund, A. (1994). 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. 91:8607-8611.
18. Franke, T. F, Yang, S. I., Chan, T. O., Datta, K., Kazlauskas, A., Morrison, D. K., Kaplan, D. R., and Tsichlis, P. N. (1995). The protein kinase encoded by akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
19. Gottschalk, W. A., Jiang, H., Tartaglia, N., Feng, L., Figurov, A., and Lu, B. (1999). Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. Learn. Mem. 6:243-256.
20. Han, B. H., and Holtzman, D. M. (2000). BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J. Neurosci. 20:5775-5781.
21. Impey, S., Smith, D. M., Obrietan, K., Donahue, R., Wade, C., and Storm, D. R. (1998). Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat. Neurosci. 1:595-601.
22. Izquierdo, I., Barros, D. M., Izquierdo, L., Mello e Souza, T., Souza, M., and Medina, J. H. (1998). Mechanisms for memory types differ. Nature 393:635-636.
23. Johnston, A. N. B., Clements, M. P., and Rose, S. P. R. (1999). Role of brain-derived neurotrophic factor and presynaptic proteins in passive avoidance learning in day-old domestic chicks. Neuroscience 88:1033-1042.
24. Johnston, A. N. B., and Rose, S. P. R. (2001). Memory consolidation in day-old chicks requires BDNF but not NGF or NT-3: An antisense study. Mol. Brain Res. 88:26-36.
25. Kafitz, K. W., Rose, C. R., Thoenen, H., and Konnerth, A. (1999). Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 401:918-921.
26. Kang, H., Welcher, A. A., Shelton, D., and Schuman, E. M. (1997). Neurotrophins and time: Differents roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19:653-664.
27. Kaplan, D. R., and Stephens, R. M. (1994). Neurotrophin signal transduction by trk receptor. J. Neurobiol. 25:1404-1417.
28. Korte, M., Kang, H. B., Bonhoeffer, T., and Schuman, E. (1998). A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacol. 37:553-559.
29. Kossel, A. H., Cambridge, S. B., Wagner, U., and Bonhoeffer, T. (2001). A caged Ab reveals an immediate/instructive effect of BDNF during hippocampal synaptic potentiation. Proc. Natl. Acad. Sci. U.S.A. 98:14702-14707.
30. Li, Y. X., Zhang, Y., Lester, H. A., Schuman, E. M., and Davidson, N. (1998). Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J. Neurosci. 18:10231-10240.
31. Linnarsson, S., Björklund, A., and Ernfors, P. (1997). Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 9:2581-2587.
32. Lu, B., and Chow, A. (1999). Neurotrophins and hippocampal synaptic transmission and plasticity. J. Neurosci. Res. 58:76-87.
33. Ma, Y. L., Wang, H. L., Wu, H. C., Wei, C. L., and Lee, E. H. (1998). Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82:957-967.
34. McAllister, A. K., Katz, L. C., and Lo, D. C. (1999). Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22:295-318.
35. Mizuno, M., Yamada, K., Olariu, A., Nawa, H., and Nabeshima, T. (2000). Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci. 20:7116-7121.
36. Mu, J. S., Li, W. P., Yao, Z. B., and Zhou, X. F. (1999). Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res. 835:259-265.
37. Patterson, S. L., Pittenger, C., Morozov, A., Martin, K. C., Scanlin, H., Drake, C., and Kandel, E. (2001). Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123-140.
38. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA.
39. Pelleymounter, M. A., Cullen, M. J., Baker, M. B., Gollub, M., and Wellman, C. (1996). The effects of intrahippocampal BDNF and NGF on spatial learning in aged Long Evans rats. Mol. Chem. Neuropathol. 29:211-226.
40. Pizzorusso, T., Ratto, G. M., Putignano, E., and Maffei, L. (2000). Brain-derived neurotrophic factor causes cAMP response element-binding protein phosphorylation in absence of calcium increase in slices and cultured neurons from rat visual cortex. J. Neurosci. 20:2809-2816.
41. Poo, M. (2001). Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2:24-32.
42. Roberson, E. D., English, J. D., Adams, J. P., Selcher, J. C., Kondratick. C., and Sweatt, J. D. (1999). The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci. 19:4337-4348.
43. Rutherford, L. C., Nelson, S. B., and Turrigiano, G. G. (1998). BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21:521-530.
44. Schinder, A. F., and Poo, M. (2000). The neurotrophin hypothesis for synaptic plasticity. TINS 23:639-645.
45. Segal, R. A., and Greenberg, M. E. (1996). Intracellular signaling pathways activated by neurotrophic factor. Annu. Rev. Neurosci. 19:463-489.
46. Silva, A. J., Kogan, J. H., Frankland, P. W., and Kida, S. (1998). CREB and memory. Annu. Rev. Neurosci. 21:127-148.
47. Soppet, D. E., Escandon, E., Maragos, J., Middlemas, D. S., Reid, S. W., Blair, J., Burton, L. E., Stanton, B. R., Kaplan, T., Hunter, T., and Kaptan, D. R. (1991). The neurotrophic factors, brain-derived neurotrophic factor, and neurotrophin-3 are ligands for the trkB tyrosine receptor. Cell 65:895-903.
48. Stephens, R. M., Loeb, D. M., Copeland, T. D., Pawson, T., Greene, L. A., and Kaplan, D. R. (1994). Trk receptors use redundant signal transduction pathways involving SHC and PLC-gamma] to mediate NGF responses. Neuron 12:691-705.
49. Sweatt, J. D. (2001). The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem. 76:1-10.
50. Taubenfeld, S. M., Wiig, K. A., Bear, M. F., and Alberini, C. M. (1999). A molecular correlate of memory and amnesia in the hippocampus. Nat. Neurosci. 2:309-310.
51. Tyler, W. J., and Pozzo-Miller, L. D. (2001). BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J. Neurosci. 21:4249-4258.
52. Vianna, M. R. M., Izquierdo, L. A., Barros, D. M., Medina, J. H., and Izquierdo, I. (1999). Intrahippocampal infusion of inhibitor of protein kinase A separates short-from long-term memory. Behav. Pharmacol. 10:223-227.
53. Viola, H., Furman, M., Izquierdo, L. A., Alonso, M., Barros, D. M., de Souza, M. M., Izquierdo, I., and Medina, J. H. (2000). Phosphorylated cAMP response element-binding protein as a molecular marker of memory processing in rat hippocampus: Effect of novelty. J. Neurosci. 20:RC112 (1-5).
54. Walz, R., Roesler, R., Quevedo, J., Sant'Anna, M. K., Madruga, M., Rodrigues, C., Gottfried, C., Medina, J. H., and lzquierdo, I. (1999). Time-dependent impairment of inhibitory avoidance retention in rats by posttraining infusion of a mitogen-activated protein kinase inhibitor into cortical and limbic structures. Neurobiol. Learn. Mem. 73:11-20.
55. Xing, J., Ginty, D. D., and Greenberg, M. E. (1996). Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273:959-963.
56. Yamada, K., Mizuno. M., and Nabeshina, T. (2002). Role for brain-derived neurotrophic factor in learning and memory. Life Sci. 70:735-744.
57. Ying. S.-W., Futter, M., Rosenblum, K., Webber, M. J.,Hunt, S. R., Bliss,T. V. P., and Bramham, C. R. (2002). Brain-derived neurotrophic factor induced long-term potentiation in intact adult hippocampus: Requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci. 22:1532-1540.