Forebrain-specific knockout of B-raf kinase leads to deficits in hippocampal long-term potentiation, learning, and memory

Journal of Neuroscience Research

Volumn 83, Issue 1, 2006, Pages 28-38

  Chen, Adele P ^a   Ohno, Masuo ^a,c   Giese, K Peter ^a,d   Kühn, Ralf ^b,e   Chen, Rachel L ^a   Silva, Alcino J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e Artemis Pharmaceuticals GmbH   (Germany)

Author keywords

Conditional knockout water maze; Conditioned taste aversion; Contextual discrimination; Cre LoxP; Fear conditioning; MEK ERK; Ras

Indexed keywords

B RAF KINASE; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; RAS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; ENZYME ACTIVATION; FEAR; FOREBRAIN; GENE MUTATION; GENE TARGETING; HIPPOCAMPUS; KNOCKOUT MOUSE; LEARNING; LONG TERM POTENTIATION; MAZE TEST; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TASTE AVERSION;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; DISCRIMINATION (PSYCHOLOGY); DOWN-REGULATION; ELECTROPHYSIOLOGY; FEAR; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; LONG-TERM POTENTIATION; MAZE LEARNING; MEMORY; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS B-RAF; TASTE;

EID: 30344451387     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20703     Document Type: Article

References (58)

1. Adams JP, Sweatt JD. 2002. Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu Rev Pharmacol Toxicol 42:135-163.
2. Anagnostaras SG, Josselyn SA, Frankland PW, Silva AJ. 2000. Computer-assisted behavioral assessment of Pavlovian fear conditioning in mice. Learn Mem 7:58-72.
3. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD. 1998. The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
4. Bailey CH, Bartsch D, Kandel ER. 1996. Toward a molecular definition of long-term memory storage. Proc Nad Acad Sci U S A 93:13445-13452.
5. Berman DE, Hazvi S, Rosenblum K, Seger R, Dudai Y. 1998. Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J Neurosci 18:10037-10044.
6. Blum S, Moore AN, Adams F, Dash PK. 1999. A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J Neurosci 19:3535-3544.
7. Bonner TI, Kerby SB, Sutrave P, Gunnell MA, Mark G, Rapp UR. 1985. Structure and biological activity of human homologs of the raf/mil oncogene. Mol Cell Biol 5:1400-1407.
8. Bossemeyer D. 1994. The glycine-rich sequence of protein kinases: a multifunctional element. Trends Biochem Sci 19:201-205.
9. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted disruption of the cAMP-responsive element-binding protein. Cell 79:59-68.
10. Brambilla R, Gnesutta N, Minichiello L, White G, Roylance AJ, Herron CE, Ramsey M, Wolfer DP, Cestari V, Rossi-Arnaud C, Grant SG, Chapman PF, Lipp HP, Sturani E, Klein R. 1997. A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature 390:281-286.
11. Brandeis R, Brandys Y, Yehuda S. 1989. The use of the Morris Water Maze in the study of memory and learning. Int J Neurosci 48:29-69.
12. Cho YH, Friedman E, Silva AJ. 1999. Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behav Brain Res 98:77-87.
13. Costa RM, Silva AJ. 2002. Molecular and cellular mechanisms underlying the cognitive deficits associated with neurofibromatosis 1. J Child Neurol 17:622-626 [discussion 627-629, 646-651].
14. Dhaka A, Costa RM, Hu H, Irvin DK, Patel A, Kornblum HI, Silva AJ, O'Dell TJ, Colicelli J. 2003. The RAS effector RIN1 modulates the formation of aversive memories. J Neurosci 23:748-757.
15. Dugan LL, Kim JS, Zhang Y, Bart RD, Sun Y, Holtzman DM, Gutmann DH. 1999. Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem 274:25842-25848.
16. English JD, Sweatt JD. 1996. Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271:24329-24332.
17. English JD, Sweatt JD. 1997. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
18. Eychene A, Dusanter-Fourt I, Barnier JV, Papin C, Charon M, Gisselbrecht S, Calothy G. 1995. Expression and activation of B-Raf kinase isoforms in human and murine leukemia cell lines. Oncogene 10:1159-1165.
19. Frankland PW, Cestari V, Filipkowski R, McDonald RJ, Silva AJ. 1998. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112:863-874.
20. Gallagher M, Burwell R, Burchinal M. 1993. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 107:618-626.
21. Giese KP, Friedman E, Telliez JB, Fedorov NB, Wines M, Feig LA, Silva AJ. 2001. Hippocampus-dependent learning and memory is impaired in mice lacking the Ras-guanine-nucleotide releasing factor 1 (Ras-GRF1). Neuropharmacology 41:791-800.
22. Grewal SS, Fass DM, Yao H, Ellig CL, Goodman RH, Stork PJ. 2000. Calcium and cAMP signals differentially regulate cAMP-responsive element-binding protein function via a Rap 1-extracellular signal- regulated kinase pathway. J Biol Chem 275:34433-34441.
23. Hugues S, Deschaux O, Garcia R. 2004. Postextinction infusion of a mitogen-activated protein kinase inhibitor into the medial prefrontal cortex impairs memory of the extinction of conditioned fear. Learn Mem 11:540-543.
24. Huleihel M, Goldsborough M, Cleveland J, Gunnell M, Bonner T, Rapp UR. 1986. Characterization of murine A-raf, a new oncogene related to the v-raf oncogene. Mol Cell Biol 6:2655-2662.
25. Huser M, Luckett J, Chiloeches A, Mercer K, Iwobi M, Giblett S, Sun XM, Brown J, Marais R, Pritchard C. 2001. MEK kinase activity is not necessary for Raf-1 function. EMBO J 20:1940-1951.
26. Ikawa S, Fukui M, Ueyama Y, Tamaoki N, Yamamoto T, Toyoshima K. 1988. B-raf, a new member of the raf family, is activated by DNA rearrangement. Mol Cell Biol 8:2651-2654.
27. Jaiswal RK, Moodie SA, Wolfman A, Landreth GE. 1994. The mitogen-activated protein kinase cascade is activated by B-Raf in response to nerve growth factor through interaction with p21ras. Mol Cell Biol 14:6944-6953.
28. Kelleher RJ 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S. 2004. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479.
29. Kelly A, Laroche S, Davis S. 2003. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23:5354-5360.
30. Lin CH, Yeh SH, Lu KT, Leu TH, Chang WC, Gean PW. 2001. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31:841-851.
31. Marais R, Light Y, Paterson HF, Mason CS, Marshall CJ. 1997. Differential regulation of Raf-1, A-Raf, and B-Raf by oncogenic ras and tyrosine kinases. J Biol Chem 272:4378-4383.
32. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER. 1997. MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
33. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER. 1996a. Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
34. Mayford M, Baranes D, Podsypanina K, Kandel ER. 1996b. The 3′-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc Natl Acad Sci U S A 93:13250-13255.
35. Mazzucchelli C, Vantaggiato C, Ciamei A, Fasano S, Pakhotin P, Krezel W, Welzl H, Wolfer DP, Pages G, Valverde O, Marowsky A, Porrazzo A, Orban PC, Maldonado R, Ehrengruber MU, Cestari V, Lipp HP, Chapman PF, Pouyssegur J, Brambilla R. 2002. Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34:807-820.
36. Mikula M, Schreiber M, Husak Z, Kucerova L, Ruth J, Wieser R, Zatloukal K, Beug H, Wagner EF, Baccarini M. 2001. Embryonic lethality and fetal liver apoptosis in mice lacking the c-raf-1 gene. EMBO J 20:1952-1962.
37. Morice C, Nothias F, Konig S, Vernier P, Baccarini M, Vincent JD, Barnier JV. 1999. Raf-1 and B-Raf proteins have similar regional distributions but differential subcellular localization in adult rat brain. Eur J Neurosci 11:1995-2006.
38. Morozov A, Muzzio IA, Bourtchouladze R, Van-Strien N, Lapidus K, Yin D, Winder DG, Adams JP, Sweatt JD, Kandel ER. 2003. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 39:309-325.
39. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 90:8424-8428.
40. Ohno M, Frankland PW, Chen AP, Costa RM, Silva AJ. 2001. Inducible, pharmacogenetic approaches to the study of learning and memory. Nat Neurosci 4:1238-1243.
41. Otto T, Eichenbaum H, Wiener SI, Wible CG. 1991. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181-192.
42. Papin C, Denouel-Galy A, Laugier D, Calothy G, Eychene A. 1998. Modulation of kinase activity and oncogenic properties by alternative splicing reveals a novel regulatory mechanism for B-Raf. J Biol Chem 273:24939-24947.
43. Ranck JB Jr. 1973. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41:461-531.
44. Richter-Levin G, Thomas KL, Hunt SP, Bliss TV. 1998. Dissociation between genes activated in long-term potentiation and in spatial learning in the rat. Neurosci Lett 251:41-44.
45. Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE. 2000. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 20:8177-8187.
46. Selcher JC, Nekrasova T, Paylor R, Landreth GE, Sweatt JD. 2001. Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning. Learn Mem 8:11-19.
47. Silva AJ, Frankland PW, Marowitz Z, Friedman E, Lazlo G, Cioffi D, Jacks T, Bourtchuladze R. 1997. A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat Genet 15:281-284.
48. Storm SM, Cleveland JL, Rapp UR. 1990. Expression of raf family protooncogenes in normal mouse tissues. Oncogene 5:345-351.
49. Sweatt JD. 2001. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
50. Thomas KL, Laroche S, Errington ML, Bliss TVP, Hunt SP. 1994. Spatial and temporal changes in signal transduction pathways during LTP. Neuron 13:737-745.
51. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, Anderson DJ, Mayford M, Kandel ER, Tonegawa S. 1996. Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87:1317-1326.
52. Vossler MR, Yao H, York RD, Pan MG, Rim CS, Stork PJ. 1997. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73-82.
53. Welzl H, D'Adamo P, Lipp HP. 2001. Conditioned taste aversion as a learning and memory paradigm. Behav Brain Res 125:205-213.
54. Wixler V, Smola U, Schuler M, Rapp U. 1996. Differential regulation of Raf isozymes by growth vs. differentiation inducing factors in PC12 pheochromocytoma cells. FEBS Lett 385:131-137.
55. Wojnowski L, Zimmer AM, Beck TW, Hahn H, Bernal R, Rapp UR, Zimmer A. 1997. Endothelial apoptosis in Braf-deficient mice. Nat Genet 16:293-297.
56. Wojnowski L, Stancato LF, Larner AC, Rapp UR, Zimmer A. 2000. Overlapping and specific functions of Braf and Craf-1 protooncogenes during mouse embryogenesis. Mech Dev 91:97-104.
57. Wu SP, Lu KT, Chang WC, Gean PW. 1999. Involvement of mitogen-activated protein kinase in hippocampal long-term potentiation. J Biomed Sci 6:409-417.
58. Zinyk DL, Mercer EH, Harris E, Anderson DJ, Joyner AL. 1998. Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr Biol 8:665-668.