Mice lacking ras-GRF1 show contextual fear conditioning but not spatial memory impairments: Convergent evidence from two independently generated mouse mutant lines

Frontiers in Behavioral Neuroscience

Volumn , Issue DECEMBER, 2011, Pages

  D'Isa, Raffaele ^a   Clapcote, Steven J ^b   Voikar, Vootele ^c   Wolfer, David P ^c   Giese, Karl Peter ^d   Brambilla, Riccardo ^a,e   Fasano, Stefania ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Body weight reduction; Fear conditioning; Intellicage; Ras ERK; Ras GRF1; Spatial memory

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAS GUANINE NUCLEOTIDE RELEASING FACTOR 1; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BODY WEIGHT; CONDITIONING; CONTEXTUAL FEAR CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; LEARNING; MALE; MAZE TEST; MOUSE; NONHUMAN; NONSENSE MUTATION; PLACE PREFERENCE; POINT MUTATION; SPATIAL MEMORY; TASK PERFORMANCE;

EID: 84855210520     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2011.00078     Document Type: Article

References (69)

1. Adams, J. P., and Sweatt, J. D. (2002). Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu. Rev. Pharmacol. Toxicol. 42, 135-163.
2. Alberini, C. M. (2005). Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci. 28, 51-56.
3. 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.
4. Barlind, A., Karlsson, N., BjorkEriksson, T., Isgaard, J., and Blomgren, K. (2010). Decreased cytogenesis in the granule cell layer of the hippocampus and impaired place learning after irradiation of the young mouse brain evaluated using the IntelliCage platform. Exp. Brain Res. 201, 781-787.
5. Berardi, N., Silingardi, D., Angelucci, A., De Pasquale, R., Borsotti, M., Squitieri, G., Putignano, E., Brambilla, R., and Pizzorusso, T. (2011). ERK pathway activation bidirectionally affects visual recognition memory and synaptic plasticity in the perirhinal cortex. Front. Behav. Neurosci. (in press).
6. Blum, S., and Dash, P. K. (2009). "MAP kinase signaling in learning and memory," in Encyclopedia of Neuroscience, Vol. 5, ed. L. R. Squire (San Diego: Elsevier), 657-662.
7. Boguski, M. S., and McCormick, F. (1993). Proteins regulating Ras and its relatives. Nature 366, 643-654.
8. Borras, C., Monleon, D., Lopez-Grueso, R., Gambini, J., Orlando, L., Pallardo, F. V., Santos, E., Vina, J., and Font de Mora, J. (2011). RasGrf1 deficiency delays aging in mice. Aging (Albany N. Y.) 3, 262-276.
9. Boulton, T. G., Nye, S. H., Robbins, D. J., Ip, N. Y., Radziejewska, E., Morgenbesser, S. D., De, P. R., Panayotatos, N., Cobb, M. H., and Yancopoulos, G. D. (1991). ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65, 663-675
10. Brambilla, R., Gnesutta, N., Minichiello, L., White, G., Roylance, A. J., Herron, C. E., Ramsey, M., Wolfer, D. P., Cestari, V., Rossi-Arnaud, C., Grant, S. G., Chapman, P. F., Lipp, H. P., Sturani, E., and Klein, R. (1997). A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature 390, 281-286.
11. Clapcott, S. J., Peters, J., Orban, P. C., Brambilla, R., and Graham, C. F. (2003). Two ENU-induced mutations in Rasgrf1 and early mouse growth retardation. Mamm. Genome 14, 495-505.
12. Coogan, A. N., O'Leary, D. M., and O'Connor, J. J. (1999). P42/44 MAP kinase inhibitor PD98059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro. J. Neurophysiol. 81, 103-110.
13. Costa, R. M., Federov, N. B., Kogan, J. H., Murphy, G. G., Stern, J., Ohno, M., Kucherlapati, R., Jacks, T., and Silva, A. J. (2002). Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 415, 526-530.
14. Cui, Y., Costa, R. M., Murphy, G. G., Elgersma, Y., Zhu, Y., Gutmann, D. H., Parada, L. F., Mody, I., and Silva, A. J. (2008). Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135, 549-560.
15. Davis, H. P., and Squire, L. R. (1984). Protein synthesis and memory: a review. Psychol. Bull. 96, 518-559
16. Davis, S., and Laroche, S. (2006). Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review. Genes Brain Behav. 5(Suppl. 2), 61-72.
17. de Magalhaes, J. P. (2010). Paternal genome effects on aging: evidence for a role of Rasgrf1 in longevity determination? Mech. Ageing Dev. 132, 72-73.
18. Dhaka, A., Costa, R. M., Hu, H., Irvin, D. K., Patel, A., Kornblum, H. I., Silva, A. J., O'Dell, T. J., and Colicelli, J. (2003). The RAS effector RIN1 modulates the formation of aversive memories. J. Neurosci. 23, 748-757
19. Di Cristo, G., Berardi, N., Cancedda, L., Pizzorusso, T., Putignano, E., Ratto, G. M., and Maffei, L. (2001). Requirement of ERK activation for visual cortical plasticity. Science 292, 2337-2340.
20. D'isa, R., Solari, N., and Brambilla, R. (2011). "Biological memory in animals and in man," in Memory Mass Storage, eds G. Campardo, F. Tiziani, and M. Iaculo (Berlin-Heidelberg: Springer), 417-441.
21. English, J. D., and Sweatt, J. D. (1996). Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J. Biol. Chem. 271, 24329-24332.
22. English, J. D., and Sweatt, J. D. (1997). A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J. Biol. Chem. 272, 19103-19106.
23. Fanselow, M. S., and Poulos, A. M. (2005). The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 56, 207-234.
24. Fasano, S., and Brambilla, R. (2011). Ras-ERK signaling in behavior: old questions and new perspectives. Front. Behav. Neurosci. 5:79. doi: 10.3389/fnbeh.2011.00079.
25. Fasano, S., D'Antoni, A., Orban, P. C., Valjent, E., Putignano, E., Vara, H., Pizzorusso, T., Giustetto, M., Yoon, B., Soloway, P., Maldonado, R., Caboche, J., and Brambilla, R. (2009). Ras-guanine nucleotidereleasing factor 1 (Ras-GRF1) controls activation of extracellular signal-regulated kinase (ERK) signaling in the striatum and long-term behavioral responses to cocaine. Biol. Psychiat. 66, 758-768.
26. Fendt, M., and Fanselow, M. S. (1999). The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev. 23, 743-760
27. Fernandez-Medarde, A., and Santos, E. (2011a). Ras in cancer and developmental diseases. Genes Cancer 2, 344-358.
28. Fernandez-Medarde, A., and Santos, E. (2011b). The RasGrf family of mammalian guanine nucleotide exchange factors. Biochim. Biophys. Acta 1815, 170-188.
29. Galsworthy, M. J., Amrein, I., Kuptsov, P. A., Poletaeva, II, Zinn, P., Rau, A., Vyssotski, A., and Lipp, H. P. (2005). A comparison of wild-caught wood mice and bank voles in the Intellicage: assessing exploration, daily activity patterns and place learning paradigms. Behav. Brain Res. 157, 211-217.
30. Giese, K. P., Friedman, E., Telliez, J. B., Fedorov, N. B., Wines, M., Feig, L. A., and Silva, A. J. (2001). Hippocampus-dependent learning and memory is impaired in mice lacking the Ras-guanine-nucleotide releasing factor 1 (Ras-GRF1). Neuropharmacology 41, 791-800.
31. Hebert, A. E., and Dash, P. K. (2002). Extracellular signal-regulated kinase activity in the entorhinal cortex is necessary for long-term spatial memory. Learn. Mem. 9, 156-166.
32. Huang, Y. Y., Martin, K. C., and Kandel, E. R. (2000). Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J. Neurosci. 20, 6317-6325.
33. Itier, J. M., Tremp, G. L., Leonard, J. F., Multon, M. C., Ret, G., Schweighoffer, F., Tocque, B., Bluet-Pajot, M. T., Cormier, V., and Dautry, F. (1998). Imprinted gene in postnatal growth role. Nature 393, 125-126.
34. Jaholkowski, P., Kiryk, A., Jedynak, P., Ben Abdallah, N. M., Knapska, E., Kowalczyk, A., Piechal, A., Blecharz-Klin, K., Figiel, I., Lioudyno, V., Widy-Tyszkiewicz, E., Wilczynski, G. M., Lipp, H. P., Kaczmarek, L., and Filipkowski, R. K. (2009). New hippocampal neurons are not obligatory for memory formation; cyclin D2 knockout mice with no adult brain neurogenesis show learning. Learn. Mem. 16, 439-451.
35. Kelly, A., Laroche, S., and 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
36. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256, 675-677.
37. Kiryk, A., Aida, T., Tanaka, K., Banerjee, P., Wilczynski, G. M., Meyza, K., Knapska, E., Filipkowski, R. K., Kaczmarek, L., and Danysz, W. (2008). Behavioral characterization of GLT1(+/-) mice as a model of mild glutamatergic hyperfunction. Neurotox. Res. 13, 19-30.
38. Knapska, E., Walasek, G., Nikolaev, E., Neuhausser-Wespy, F., Lipp, H. P., Kaczmarek, L., and Werka, T. (2006). Differential involvement of the central amygdala in appetitive versus aversive learning. Learn. Mem. 13, 192-200.
39. LeDoux, J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184.
40. Li, S., Tian, X., Hartley, D. M., and Feig, L. A. (2006). Distinct roles for Rasguanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J. Neurosci. 26, 1721-1729.
41. Lipp, H. P. (2005). High-throughput and automated behavioural screening of normal and genetically modified mice. Bus. Brief. Future Drug Discov. 1-5.
42. Malumbres, M., and Barbacid, M. (2003). RAS oncogenes: the first 30 years. Nat. Rev. Cancer 3, 459-465.
43. Maren, S. (2001). Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 24, 897-931.
44. Maren, S., and Fanselow, M. S. (1996). The amygdala and fear conditioning: has the nut been cracked? Neuron 16, 237-240.
45. Marshall, C. (1995). "The Ras/Raf/ERK pathway," in Guidebook to the Small GTPases, eds M. Zerial and L. A. Hubery (Oxford: Oxford University Press), 65-73.
46. Mazzucchelli, C., and Brambilla, R. (2000). Ras-related and MAPK signalling in neuronal plasticity and memory formation. Cell. Mol. Life Sci. 57, 604-611.
47. Mazzucchelli, C., Vantaggiato, C., Ciamei, A., Fasano, S., Porrazzo, A., Orban, P. C., Pakhotin, P., Krezel, W., Wezl, H., Wolfer, D. P., Pagès, G., Valverde, O., Marowsky, A., Porrazzo, A., Orban, P. C., Maldonado, R., Ehrengruber, M. U., Cestari, V., Lipp, H. P., Chapman, P. F., Pouysségur, J., and Brambilla, (2002). Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34, 807-820.
48. McGaugh, J. L. (2000). Memory a century of consolidation. Science 287, 248-251.
49. Milner, B., Squire, L. R., and Kandel, E. R. (1998). Cognitive neuroscience and the study of memory. Neuron 20, 445-468.
50. Mizuno, K., and Giese, K. P. (2005). Hippocampus-dependent memory formation: do memory type-specific mechanisms exist? J. Pharmacol. Sci. 98, 191-197.
51. Morris, R. G., Garrud, P., Rawlins, J. N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
52. Orban, P. C., Chapman, P. F., and Brambilla, R. (1999). Is the Ras-MAPK signalling pathway necessary for long-term memory formation? Trends Neurosci. 22, 38-44.
53. Peng, S., Zhang, Y., Zhang, J., Wang, H., and Ren, B. (2010). ERK in learning and memory: a review of recent research. Int. J. Mol. Sci. 11, 222-232.
54. Phillips, R. G., and LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285.
55. Phillips, R. G., and LeDoux, J. E. (1994). Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn. Mem. 1, 34-44.
56. Phillips, R. G., and LeDoux, J. E. (1995). Lesions of the fornix but not the entorhinal or perirhinal cortex interfere with contexual fear conditioning. J. Neurosci. 15, 5308-5315.
57. Plass, C., Shibata, H., Kalcheva, I., Mullins, L., Kotelevtseva, N., Mullins, J., Kato, R., Sasaki, H., Hirotsune, S., Okazaki, Y., Held, W. A., Hayashizaki, Y., and Chapman, V. M. (1996). Identification of Grf1 on mouse chromosome 9 as an imprinted gene by RLGS-M. Nat. Genet. 14, 106-109.
58. Selcher, J. C., Atkins, C. M., Trzaskos, J. M., Paylor, R., and Sweatt, J. D. (1999). A necessity for MAP kinase activation in mammalian spatial learning. Learn. Mem. 6, 478-490.
59. Shalin, S. C., Zirrgiebel, U., Honsa, K. J., Julien, J. P., Miller, F. D., Kaplan, D. R., and Sweatt, J. D. (2004). Neuronal MEK is important for normal fear conditioning in mice. J. Neurosci. Res. 75, 760-770.
60. Silva, A. J., Frankland, P. W., Marowitz, Z., Friedman, E., Lazlo, G., Cioffi, D., Jacks, T., and Bourtchuladze, R. (1997). A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat. Genet. 15, 281-284.
61. Squire, L. R. (2004). Memory systems of the brain: a brief history and current perspective. Neurobiol. Learn. Mem. 82, 171-177.
62. Squire, L. R., Knowlton, B., and Musen, G. (1993). The structure and organization of memory. Annu. Rev. Psychol. 44, 453-495.
63. Swank, M. W. (2000). Conditioned cFos in mouse NTS during expression of a learned taste aversion depends on contextual cues. Brain Res. 862, 138-144.
64. Thomas, G. M., and Huganir, R. L. (2004). MAPK cascade signaling and synaptic plasticity. Nat. Rev. Neurosci. 5, 173-183.
65. Viosca, J., Schuhmacher, A. J., Guerra, C., and Barco, A. (2009). Germline expression of H-Ras(G12V) causes neurological deficits associated to Costello syndrome. Genes Brain Behav. 8, 60-71.
66. Voikar, V., Colacicco, G., Gruber, O., Vannoni, E., Lipp, H. P., and Wolfer, D. P. (2010). Conditioned response suppression in the IntelliCage: assessment of mouse strain differences and effects of hippocampal and striatal lesions on acquisition and retention of memory. Behav. Brain Res. 213, 304-312.
67. Walz, R., Roesler, R., Quevedo, J., Rockenbach, I. C., Amaral, O. B., Vianna, M. R., Lenz, G., Medina, J. H., and Izquierdo, I. (1999). Dosedependent impairment of inhibitory avoidance retention in rats by immediate post-training infusion of a mitogen-activated protein kinase kinase inhibitor into cortical structures. Behav. Brain Res. 105, 219-223.
68. Yoon, B., Herman, H., Hu, B., Park, Y. J., Lindroth, A., Bell, A., West, A. G., Chang, Y., Stablewski, A., Piel, J. C., Loukinov, D. I., Lobanenkov, V. V., and Soloway, P. D. (2005). Rasgrf1 imprinting is regulated by a CTCFdependent methylation-sensitive enhancer blocker. Mol. Cell. Biol. 25, 11184-11190.
69. Yoon, B. J., Herman, H., Sikora, A., Smith, L. T., Plass, C., and Soloway, P. D. (2002). Regulation of DNA methylation of Rasgrf1. Nat. Genet. 30, 92-96.