Small G Protein Signaling in Neuronal Plasticity and Memory Formation: The Specific Role of Ras Family Proteins

Neuron

Volumn 68, Issue 3, 2010, Pages 340-361

  Ye, Xiaojing ^a   Carew, Thomas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATE; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NEUROFIBROMIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; SCAFFOLD PROTEIN;

AMYGDALOID NUCLEUS; BRAIN ELECTROPHYSIOLOGY; COGNITION; COGNITIVE DEFECT; ENZYME ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; HETEROZYGOSITY; HIPPOCAMPUS; HUMAN; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; MEMORY CONSOLIDATION; MUTATIONAL ANALYSIS; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

CELL MEMBRANE; GENES, RAS; HUMANS; MEMORY; MONOMERIC GTP-BINDING PROTEINS; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; PROTEIN CONFORMATION; RAS PROTEINS; RECEPTORS, PRESYNAPTIC; SIGNAL TRANSDUCTION;

EID: 78049309392     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.09.013     Document Type: Review

References (241)

1. Adams J.P., Sweatt J.D. Molecular psychology: Roles for the ERK MAP kinase cascade in memory. Annu. Rev. Pharmacol. Toxicol. 2002, 42:135-163.
2. Ahn Y.H., Han J.H., Hong S.H. Rap1 and p38 MAPK mediate 8-chloro-cAMP-induced growth inhibition in mouse fibroblast DT cells. J. Cell. Physiol. 2006, 209:1039-1045.
3. Alpár A., Palm K., Schierwagen A., Arendt T., Gärtner U. Expression of constitutively active p21H-rasval12 in postmitotic pyramidal neurons results in increased dendritic size and complexity. J. Comp. Neurol. 2003, 467:119-133.
4. Alpár A., Gärtner U., Seeger G., Härtig W., Brauer K., Arendt T. Constitutive expression of p21H-ras(Val12) in pyramidal neurons results in reorganization of mouse neocortical afferents. J. Neurobiol. 2004, 60:263-274.
5. Arai J.A., Li S., Hartley D.M., Feig L.A. Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment. J. Neurosci. 2009, 29:1496-1502.
6. Arendt T., Gärtner U., Seeger G., Barmashenko G., Palm K., Mittmann T., Yan L., Hümmeke M., Behrbohm J., Brückner M.K., et al. Neuronal activation of Ras regulates synaptic connectivity. Eur. J. Neurosci. 2004, 19:2953-2966.
7. Bailey C.H. Structural changes and the storage of long-term memory in Aplysia. Can. J. Physiol. Pharmacol. 1999, 77:738-747.
8. Bailey C.H., Chen M., Keller F., Kandel E.R. Serotonin-mediated endocytosis of apCAM: An early step of learning-related synaptic growth in Aplysia. Science 1992, 256:645-649.
9. Banko J.L., Hou L., Poulin F., Sonenberg N., Klann E. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 2006, 26:2167-2173.
10. Barbacid M. ras genes. Annu. Rev. Biochem. 1987, 56:779-827.
11. Barros D.M., Mello e Souza T., de Souza M.M., Choi H., DeDavid e Silva T., Lenz G., Medina J.H., Izquierdo I. LY294002, an inhibitor of phosphoinositide 3-kinase given into rat hippocampus impairs acquisition, consolidation and retrieval of memory for one-trial step-down inhibitory avoidance. Behav. Pharmacol. 2001, 12:629-634.
12. Beaumont V., Zhong N., Fletcher R., Froemke R.C., Zucker R.S. Phosphorylation and local presynaptic protein synthesis in calcium- and calcineurin-dependent induction of crayfish long-term facilitation. Neuron 2001, 32:489-501.
13. Beaumont V., Zhong N., Froemke R.C., Ball R.W., Zucker R.S. Temporal synaptic tagging by I(h) activation and actin: involvement in long-term facilitation and cAMP-induced synaptic enhancement. Neuron 2002, 33:601-613.
14. Bernards A., Settleman J. GAP control: regulating the regulators of small GTPases. Trends Cell Biol. 2004, 14:377-385.
15. Bilbo S.D., Nelson R.J. Behavioral phenotyping of transgenic and knockout animals: a cautionary tale. Lab Anim. (N.Y.) 2001, 30:24-29.
16. Biou V., Brinkhaus H., Malenka R.C., Matus A. Interactions between drebrin and Ras regulate dendritic spine plasticity. Eur. J. Neurosci. 2008, 27:2847-2859.
17. Bivona T.G., Pérez De Castro I., Ahearn I.M., Grana T.M., Chiu V.K., Lockyer P.J., Cullen P.J., Pellicer A., Cox A.D., Philips M.R. Phospholipase Cgamma activates Ras on the Golgi apparatus by means of RasGRP1. Nature 2003, 424:694-698.
18. Bliss J.M., Gray E.E., Dhaka A., O'Dell T.J., Colicelli J. Fear learning and extinction are linked to neuronal plasticity through Rin1 signaling. J. Neurosci. Res. 2010, 88:917-926.
19. Bolshakov V.Y., Carboni L., Cobb M.H., Siegelbaum S.A., Belardetti F. Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3-CA1 synapses. Nat. Neurosci. 2000, 3:1107-1112.
20. Bos J.L., Rehmann H., Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007, 129:865-877.
21. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
22. Brambilla R., Gnesutta N., Minichiello L., White G., Roylance A.J., Herron C.E., Ramsey M., Wolfer D.P., Cestari V., Rossi-Arnaud C., et al. A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature 1997, 390:281-286.
23. Brown T.C., Tran I.C., Backos D.S., Esteban J.A. NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 2005, 45:81-94.
24. Capogna M., Gähwiler B.H., Thompson S.M. Presynaptic enhancement of inhibitory synaptic transmission by protein kinases A and C in the rat hippocampus in vitro. J. Neurosci. 1995, 15:1249-1260.
25. Carey K.D., Watson R.T., Pessin J.E., Stork P.J. The requirement of specific membrane domains for Raf-1 phosphorylation and activation. J. Biol. Chem. 2003, 278:3185-3196.
26. Carlisle H.J., Kennedy M.B. Spine architecture and synaptic plasticity. Trends Neurosci. 2005, 28:182-187.
27. Carlisle H.J., Manzerra P., Marcora E., Kennedy M.B. SynGAP regulates steady-state and activity-dependent phosphorylation of cofilin. J. Neurosci. 2008, 28:13673-13683.
28. Chang L., Alicata D., Ernst T., Volkow N. Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 2007, 102(Suppl 1):16-32.
29. Chavez-Noriega L.E., Stevens C.F. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J. Neurosci. 1994, 14:310-317.
30. Chen C., Regehr W.G. The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J. Neurosci. 1997, 17:8687-8694.
31. Chen L., Zhang L.J., Greer P., Tung P.S., Moran M.F. A murine CDC25/ras-GRF-related protein implicated in Ras regulation. Dev. Genet. 1993, 14:339-346.
32. Chen H.J., Rojas-Soto M., Oguni A., Kennedy M.B. A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 1998, 20:895-904.
33. Chen X., Garelick M.G., Wang H., Lil V., Athos J., Storm D.R. PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat. Neurosci. 2005, 8:925-931.
34. Chen A.P., Ohno M., Giese K.P., Kühn R., Chen R.L., Silva A.J. Forebrain-specific knockout of B-raf kinase leads to deficits in hippocampal long-term potentiation, learning, and memory. J. Neurosci. Res. 2006, 83:28-38.
35. Cheung U., Atwood H.L., Zucker R.S. Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J. Neurobiol. 2006, 66:273-280.
36. Chiang H.C., Wang L., Xie Z., Yau A., Zhong Y. PI3 kinase signaling is involved in Abeta-induced memory loss in Drosophila. Proc. Natl. Acad. Sci. USA 2010, 107:7060-7065.
37. Chin J., Angers A., Cleary L.J., Eskin A., Byrne J.H. Transforming growth factor beta1 alters synapsin distribution and modulates synaptic depression in Aplysia. J. Neurosci. 2002, 22:RC220.
38. Chiu V.K., Bivona T., Hach A., Sajous J.B., Silletti J., Wiener H., Johnson R.L., Cox A.D., Philips M.R. Ras signalling on the endoplasmic reticulum and the Golgi. Nat. Cell Biol. 2002, 4:343-350.
39. Cingolani L.A., Thalhammer A., Yu L.M., Catalano M., Ramos T., Colicos M.A., Goda Y. Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 2008, 58:749-762.
40. Cook S.J., Rubinfeld B., Albert I., McCormick F. RapV12 antagonizes Ras-dependent activation of ERK1 and ERK2 by LPA and EGF in Rat-1 fibroblasts. EMBO J. 1993, 12:3475-3485.
41. Costa R.M., Yang T., Huynh D.P., Pulst S.M., Viskochil D.H., Silva A.J., Brannan C.I. Learning deficits, but normal development and tumor predisposition, in mice lacking exon 23a of Nf1. Nat. Genet. 2001, 27:399-405.
42. Costa R.M., Federov N.B., Kogan J.H., Murphy G.G., Stern J., Ohno M., Kucherlapati R., Jacks T., Silva A.J. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002, 415:526-530.
43. Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 1999, 835:18-26.
44. Crawley J.N., Paylor R. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm. Behav. 1997, 31:197-211.
45. Cui Y., Costa R.M., Murphy G.G., Elgersma Y., Zhu Y., Gutmann D.H., Parada L.F., Mody I., Silva A.J. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 2008, 135:549-560.
46. Daston M.M., Scrable H., Nordlund M., Sturbaum A.K., Nissen L.M., Ratner N. The protein product of the neurofibromatosis type 1 gene is expressed at highest abundance in neurons, Schwann cells, and oligodendrocytes. Neuron 1992, 8:415-428.
47. de Rooij J., Zwartkruis F.J., Verheijen M.H., Cool R.H., Nijman S.M., Wittinghofer A., Bos J.L. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998, 396:474-477.
48. Denayer E., Ahmed T., Brems H., Van Woerden G., Borgesius N.Z., Callaerts-Vegh Z., Yoshimura A., Hartmann D., Elgersma Y., D'Hooge R., et al. Spred1 is required for synaptic plasticity and hippocampus-dependent learning. J. Neurosci. 2008, 28:14443-14449.
49. Denayer E., de Ravel T., Legius E. Clinical and molecular aspects of RAS related disorders. J. Med. Genet. 2008, 45:695-703.
50. Der C. RAS family GTPases, 1 edn 2006, Springer, Dordrecht, The Netherlands.
51. Dhaka A., Costa R.M., Hu H., Irvin D.K., Patel A., Kornblum H.I., Silva A.J., O'Dell T.J., Colicelli J. The RAS effector RIN1 modulates the formation of aversive memories. J. Neurosci. 2003, 23:748-757.
52. Easton D.F., Ponder M.A., Huson S.M., Ponder B.A. An analysis of variation in expression of neurofibromatosis (NF) type 1 (NF1): evidence for modifying genes. Am. J. Hum. Genet. 1993, 53:305-313.
53. Eckel-Mahan K.L., Phan T., Han S., Wang H., Chan G.C., Scheiner Z.S., Storm D.R. Circadian oscillation of hippocampal MAPK activity and cAmp: implications for memory persistence. Nat. Neurosci. 2008, 11:1074-1082.
54. Ehninger D., Han S., Shilyansky C., Zhou Y., Li W., Kwiatkowski D.J., Ramesh V., Silva A.J. Reversal of learning deficits in a Tsc2+/- mouse model of tuberous sclerosis. Nat. Med. 2008, 14:843-848.
55. Eickholt B.J., Ahmed A.I., Davies M., Papakonstanti E.A., Pearce W., Starkey M.L., Bilancio A., Need A.C., Smith A.J., Hall S.M., et al. Control of axonal growth and regeneration of sensory neurons by the p110delta PI 3-kinase. PLoS ONE 2007, 2:e869.
56. Engelhardt C.M., Bundschu K., Messerschmitt M., Renné T., Walter U., Reinhard M., Schuh K. Expression and subcellular localization of Spred proteins in mouse and human tissues. Histochem. Cell Biol. 2004, 122:527-538.
57. Fan W.T., Koch C.A., de Hoog C.L., Fam N.P., Moran M.F. The exchange factor Ras-GRF2 activates Ras-dependent and Rac-dependent mitogen-activated protein kinase pathways. Curr. Biol. 1998, 8:935-938.
58. Farnsworth C.L., Freshney N.W., Rosen L.B., Ghosh A., Greenberg M.E., Feig L.A. Calcium activation of Ras mediated by neuronal exchange factor Ras-GRF. Nature 1995, 376:524-527.
59. Fasano S., Brambilla R. Cellular mechanisms of striatum-dependent behavioral plasticity and drug addiction. Curr. Mol. Med. 2002, 2:649-665.
60. Fasano S., D'Antoni A., Orban P.C., Valjent E., Putignano E., Vara H., Pizzorusso T., Giustetto M., Yoon B., Soloway P., et al. Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) controls activation of extracellular signal-regulated kinase (ERK) signaling in the striatum and long-term behavioral responses to cocaine. Biol. Psychiatry 2009, 66:758-768.
61. Feig L.A. Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol. 2003, 13:419-425.
62. Fivaz M., Meyer T. Reversible intracellular translocation of KRas but not HRas in hippocampal neurons regulated by Ca2+/calmodulin. J. Cell Biol. 2005, 170:429-441.
63. Garcia A.M., Rowell C., Ackermann K., Kowalczyk J.J., Lewis M.D. Peptidomimetic inhibitors of Ras farnesylation and function in whole cells. J. Biol. Chem. 1993, 268:18415-18418.
64. Gärtner U., Alpár A., Reimann F., Seeger G., Heumann R., Arendt T. Constitutive Ras activity induces hippocampal hypertrophy and remodeling of pyramidal neurons in synRas mice. J. Neurosci. Res. 2004, 77:630-641.
65. Gärtner U., Alpár A., Seeger G., Heumann R., Arendt T. Enhanced Ras activity in pyramidal neurons induces cellular hypertrophy and changes in afferent and intrinsic connectivity in synRas mice. Int. J. Dev. Neurosci. 2004, 22:165-173.
66. Gekel I., Neher E. Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J. Neurosci. 2008, 28:7991-8002.
67. Gelinas J.N., Banko J.L., Peters M.M., Klann E., Weeber E.J., Nguyen P.V. Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus. Learn. Mem. 2008, 15:403-411.
68. Gibbs J.B., Pompliano D.L., Mosser S.D., Rands E., Lingham R.B., Singh S.B., Scolnick E.M., Kohl N.E., Oliff A. Selective inhibition of farnesyl-protein transferase blocks ras processing in vivo. J. Biol. Chem. 1993, 268:7617-7620.
69. Gibbs J.B., Oliff A., Kohl N.E. Farnesyltransferase inhibitors: Ras research yields a potential cancer therapeutic. Cell 1994, 77:175-178.
70. Giese K.P., Friedman E., Telliez J.B., Fedorov N.B., Wines M., Feig L.A., Silva A.J. Hippocampus-dependent learning and memory is impaired in mice lacking the Ras-guanine-nucleotide releasing factor 1 (Ras-GRF1). Neuropharmacology 2001, 41:791-800.
71. Graupera M., Guillermet-Guibert J., Foukas L.C., Phng L.K., Cain R.J., Salpekar A., Pearce W., Meek S., Millan J., Cutillas P.R., et al. Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature 2008, 453:662-666.
72. Grewal S.S., Horgan A.M., York R.D., Withers G.S., Banker G.A., Stork P.J. Neuronal calcium activates a Rap1 and B-Raf signaling pathway via the cyclic adenosine monophosphate-dependent protein kinase. J. Biol. Chem. 2000, 275:3722-3728.
73. Guan Z., Kim J.H., Lomvardas S., Holick K., Xu S., Kandel E.R., Schwartz J.H. p38 MAP kinase mediates both short-term and long-term synaptic depression in aplysia. J. Neurosci. 2003, 23:7317-7325.
74. Guilding C., McNair K., Stone T.W., Morris B.J. Restored plasticity in a mouse model of neurofibromatosis type 1 via inhibition of hyperactive ERK and CREB. Eur. J. Neurosci. 2007, 25:99-105.
75. Guo H.F., Tong J., Hannan F., Luo L., Zhong Y. A neurofibromatosis-1-regulated pathway is required for learning in Drosophila. Nature 2000, 403:895-898.
76. Gutmann D.H., Wood D.L., Collins F.S. Identification of the neurofibromatosis type 1 gene product. Proc. Natl. Acad. Sci. USA 1991, 88:9658-9662.
77. Han L., Colicelli J. A human protein selected for interference with Ras function interacts directly with Ras and competes with Raf1. Mol. Cell. Biol. 1995, 15:1318-1323.
78. Harvey C.D., Yasuda R., Zhong H., Svoboda K. The spread of Ras activity triggered by activation of a single dendritic spine. Science 2008, 321:136-140.
79. Hayashi K., Shirao T. Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons. J. Neurosci. 1999, 19:3918-3925.
80. Heumann R., Goemans C., Bartsch D., Lingenhöhl K., Waldmeier P.C., Hengerer B., Allegrini P.R., Schellander K., Wagner E.F., Arendt T., et al. Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J. Cell Biol. 2000, 151:1537-1548.
81. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., Greengard P. Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:269-279.
82. Ho I.S., Hannan F., Guo H.F., Hakker I., Zhong Y. Distinct functional domains of neurofibromatosis type 1 regulate immediate versus long-term memory formation. J. Neurosci. 2007, 27:6852-6857.
83. Hoeffer C.A., Klann E. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 2010, 33:67-75.
84. Hoffman K.B. The relationship between adhesion molecules and neuronal plasticity. Cell. Mol. Neurobiol. 1998, 18:461-475.
85. Horwood J.M., Dufour F., Laroche S., Davis S. Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur. J. Neurosci. 2006, 23:3375-3384.
86. Hou L., Klann E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 2004, 24:6352-6361.
87. Hu J.Y., Wu F., Schacher S. Two signaling pathways regulate the expression and secretion of a neuropeptide required for long-term facilitation in Aplysia. J. Neurosci. 2006, 26:1026-1035.
88. Hu H., Qin Y., Bochorishvili G., Zhu Y., van Aelst L., Zhu J.J. Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. J. Neurosci. 2008, 28:7847-7862.
89. Huang C.C., You J.L., Wu M.Y., Hsu K.S. Rap1-induced p38 mitogen-activated protein kinase activation facilitates AMPA receptor trafficking via the GDI.Rab5 complex. Potential role in (S)-3,5-dihydroxyphenylglycene-induced long term depression. J. Biol. Chem. 2004, 279:12286-12292.
90. Innocenti M., Zippel R., Brambilla R., Sturani E. CDC25(Mm)/Ras-GRF1 regulates both Ras and Rac signaling pathways. FEBS Lett. 1999, 460:357-362.
91. Isiegas C., McDonough C., Huang T., Havekes R., Fabian S., Wu L.J., Xu H., Zhao M.G., Kim J.I., Lee Y.S., et al. A novel conditional genetic system reveals that increasing neuronal cAMP enhances memory and retrieval. J. Neurosci. 2008, 28:6220-6230.
92. Izquierdo L.A., Barros D.M., Ardenghi P.G., Pereira P., Rodrigues C., Choi H., Medina J.H., Izquierdo I. Different hippocampal molecular requirements for short- and long-term retrieval of one-trial avoidance learning. Behav. Brain Res. 2000, 111:93-98.
93. Jacks T., Shih T.S., Schmitt E.M., Bronson R.T., Bernards A., Weinberg R.A. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat. Genet. 1994, 7:353-361.
94. James G.L., Goldstein J.L., Brown M.S., Rawson T.E., Somers T.C., McDowell R.S., Crowley C.W., Lucas B.K., Levinson A.D., Marsters J.C. Benzodiazepine peptidomimetics: potent inhibitors of Ras farnesylation in animal cells. Science 1993, 260:1937-1942.
95. Jovanovic J.N., Czernik A.J., Fienberg A.A., Greengard P., Sihra T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 2000, 3:323-329.
96. Kanda Y., Watanabe Y. Adrenaline increases glucose transport via a Rap1-p38MAPK pathway in rat vascular smooth muscle cells. Br. J. Pharmacol. 2007, 151:476-482.
97. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294:1030-1038.
98. Kaneko M., Takahashi T. Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. J. Neurosci. 2004, 24:5202-5208.
99. Karpova A., Sanna P.P., Behnisch T. Involvement of multiple phosphatidylinositol 3-kinase-dependent pathways in the persistence of late-phase long term potentiation expression. Neuroscience 2006, 137:833-841.
100. Kawasaki H., Springett G.M., Mochizuki N., Toki S., Nakaya M., Matsuda M., Housman D.E., Graybiel A.M. A family of cAMP-binding proteins that directly activate Rap1. Science 1998, 282:2275-2279.
101. Kelleher R.J., Bear M.F. The autistic neuron: troubled translation?. Cell 2008, 135:401-406.
102. Kelly A., Lynch M.A. Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3-kinase inhibitor, wortmannin. Neuropharmacology 2000, 39:643-651.
103. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61:340-350.
104. Kikuchi A., Williams L.T. Regulation of interaction of ras p21 with RalGDS and Raf-1 by cyclic AMP-dependent protein kinase. J. Biol. Chem. 1996, 271:588-594.
105. Kim J.H., Liao D., Lau L.F., Huganir R.L. SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 1998, 20:683-691.
106. Kim J.H., Lee H.K., Takamiya K., Huganir R.L. The role of synaptic GTPase-activating protein in neuronal development and synaptic plasticity. J. Neurosci. 2003, 23:1119-1124.
107. Kim J., Lee S., Park K., Hong I., Song B., Son G., Park H., Kim W.R., Park E., Choe H.K., et al. Amygdala depotentiation and fear extinction. Proc. Natl. Acad. Sci. USA 2007, 104:20955-20960.
108. Kitayama H., Sugimoto Y., Matsuzaki T., Ikawa Y., Noda M. A ras-related gene with transformation suppressor activity. Cell 1989, 56:77-84.
109. Koh Y.H., Ruiz-Canada C., Gorczyca M., Budnik V. The Ras1-mitogen-activated protein kinase signal transduction pathway regulates synaptic plasticity through fasciclin II-mediated cell adhesion. J. Neurosci. 2002, 22:2496-2504.
110. Kohl N.E., Mosser S.D., deSolms S.J., Giuliani E.A., Pompliano D.L., Graham S.L., Smith R.L., Scolnick E.M., Oliff A., Gibbs J.B. Selective inhibition of ras-dependent transformation by a farnesyltransferase inhibitor. Science 1993, 260:1934-1937.
111. Kohl N.E., Omer C.A., Conner M.W., Anthony N.J., Davide J.P., deSolms S.J., Giuliani E.A., Gomez R.P., Graham S.L., Hamilton K., et al. Inhibition of farnesyltransferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat. Med. 1995, 1:792-797.
112. Komiyama N.H., Watabe A.M., Carlisle H.J., Porter K., Charlesworth P., Monti J., Strathdee D.J., O'Carroll C.M., Martin S.J., Morris R.G., et al. SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J. Neurosci. 2002, 22:9721-9732.
113. Konstantinopoulos P.A., Karamouzis M.V., Papavassiliou A.G. Post-translational modifications and regulation of the RAS superfamily of GTPases as anticancer targets. Nat. Rev. Drug Discov. 2007, 6:541-555.
114. Krab L.C., Goorden S.M., Elgersma Y. Oncogenes on my mind: ERK and MTOR signaling in cognitive diseases. Trends Genet. 2008, 24:498-510.
115. Krapivinsky G., Medina I., Krapivinsky L., Gapon S., Clapham D.E. SynGAP-MUPP1-CaMKII synaptic complexes regulate p38 MAP kinase activity and NMDA receptor-dependent synaptic AMPA receptor potentiation. Neuron 2004, 43:563-574.
116. Kushner S.A., Elgersma Y., Murphy G.G., Jaarsma D., van Woerden G.M., Hojjati M.R., Cui Y., LeBoutillier J.C., Marrone D.F., Choi E.S., et al. Modulation of presynaptic plasticity and learning by the H-ras/extracellular signal-regulated kinase/synapsin I signaling pathway. J. Neurosci. 2005, 25:9721-9734.
117. Lambert J.M., Lambert Q.T., Reuther G.W., Malliri A., Siderovski D.P., Sondek J., Collard J.G., Der C.J. Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism. Nat. Cell Biol. 2002, 4:621-625.
118. Lange-Carter C.A., Johnson G.L. Ras-dependent growth factor regulation of MEK kinase in PC12 cells. Science 1994, 265:1458-1461.
119. Li W., Cui Y., Kushner S.A., Brown R.A., Jentsch J.D., Frankland P.W., Cannon T.D., Silva A.J. The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Curr. Biol. 2005, 15:1961-1967.
120. Li S., Tian X., Hartley D.M., Feig L.A. Distinct roles for Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J. Neurosci. 2006, 26:1721-1729.
121. Li S., Tian X., Hartley D.M., Feig L.A. The environment versus genetics in controlling the contribution of MAP kinases to synaptic plasticity. Curr. Biol. 2006, 16:2303-2313.
122. Lin C.H., Yeh S.H., Lin C.H., Lu K.T., Leu T.H., Chang W.C., Gean P.W. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 2001, 31:841-851.
123. Lu X., Chou T.B., Williams N.G., Roberts T., Perrimon N. Control of cell fate determination by p21ras/Ras1, an essential component of torso signaling in Drosophila. Genes Dev. 1993, 7:621-632.
124. Ma N., Abel T., Hernandez P.J. Exchange protein activated by cAMP enhances long-term memory formation independent of protein kinase A. Learn. Mem. 2009, 16:367-370.
125. Machida N., Umikawa M., Takei K., Sakima N., Myagmar B.E., Taira K., Uezato H., Ogawa Y., Kariya K. Mitogen-activated protein kinase kinase kinase kinase 4 as a putative effector of Rap2 to activate the c-Jun N-terminal kinase. J. Biol. Chem. 2004, 279:15711-15714.
126. Manabe T., Aiba A., Yamada A., Ichise T., Sakagami H., Kondo H., Katsuki M. Regulation of long-term potentiation by H-Ras through NMDA receptor phosphorylation. J. Neurosci. 2000, 20:2504-2511.
127. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 2000, 23:649-711.
128. Maruta H., Burgess A.W. Regulation of the RAS Signaling Network 1edn 1996, R.G. Landes Co, Austin.
129. Matallanas D., Sanz-Moreno V., Arozarena I., Calvo F., Agudo-Ibáñez L., Santos E., Berciano M.T., Crespo P. Distinct utilization of effectors and biological outcomes resulting from site-specific Ras activation: Ras functions in lipid rafts and Golgi complex are dispensable for proliferation and transformation. Mol. Cell. Biol. 2006, 26:100-116.
130. Matozaki T., Murata Y., Saito Y., Okazawa H., Ohnishi H. Protein tyrosine phosphatase SHP-2: a proto-oncogene product that promotes Ras activation. Cancer Sci. 2009, 100:1786-1793.
131. Mauelshagen J., Sherff C.M., Carew T.J. Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. Learn. Mem. 1998, 5:246-256.
132. Merino S.M., Maren S. Hitting Ras where it counts: Ras antagonism in the basolateral amygdala inhibits long-term fear memory. Eur. J. Neurosci. 2006, 23:196-204.
133. Mizuno M., Yamada K., Takei N., Tran M.H., He J., Nakajima A., Nawa H., Nabeshima T. Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol. Psychiatry 2003, 8:217-224.
134. Moressis A., Friedrich A.R., Pavlopoulos E., Davis R.L., Skoulakis E.M. A dual role for the adaptor protein DRK in Drosophila olfactory learning and memory. J. Neurosci. 2009, 29:2611-2625.
135. Morozov A., Muzzio I.A., Bourtchouladze R., Van-Strien N., Lapidus K., Yin D., Winder D.G., Adams J.P., Sweatt J.D., Kandel E.R. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 2003, 39:309-325.
136. Mozzachiodi R., Byrne J.H. More than synaptic plasticity: role of nonsynaptic plasticity in learning and memory. Trends Neurosci. 2010, 33:17-26.
137. Muhia M., Feldon J., Knuesel I., Yee B.K. Appetitively motivated instrumental learning in SynGAP heterozygous knockout mice. Behav. Neurosci. 2009, 123:1114-1128.
138. Muhia M., Yee B.K., Feldon J., Markopoulos F., Knuesel I. Disruption of hippocampus-regulated behavioural and cognitive processes by heterozygous constitutive deletion of SynGAP. Eur. J. Neurosci. 2010, 31:529-543.
139. Murray H.J., O'Connor J.J. A role for monomeric G-proteins in synaptic plasticity in the rat dentate gyrus in vitro. Brain Res. 2004, 1000:85-91.
140. Neves G., Cooke S.F., Bliss T.V. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 2008, 9:65-75.
141. Newey S.E., Velamoor V., Govek E.E., Van Aelst L. Rho GTPases, dendritic structure, and mental retardation. J. Neurobiol. 2005, 64:58-74.
142. Nordlund M.L., Rizvi T.A., Brannan C.I., Ratner N. Neurofibromin expression and astrogliosis in neurofibromatosis (type 1) brains. J. Neuropathol. Exp. Neurol. 1995, 54:588-600.
143. North K.N., Riccardi V., Samango-Sprouse C., Ferner R., Moore B., Legius E., Ratner N., Denckla M.B. Cognitive function and academic performance in neurofibromatosis. 1: consensus statement from the NF1 Cognitive Disorders Task Force. Neurology 1997, 48:1121-1127.
144. North K., Hyman S., Barton B. Cognitive deficits in neurofibromatosis 1. J. Child Neurol. 2002, 17:605-612, discussion 627-629, 646-651.
145. O'Kane E.M., Stone T.W., Morris B.J. Increased long-term potentiation in the CA1 region of rat hippocampus via modulation of GTPase signalling or inhibition of Rho kinase. Neuropharmacology 2004, 46:879-887.
146. Ohno M., Frankland P.W., Chen A.P., Costa R.M., Silva A.J. Inducible, pharmacogenetic approaches to the study of learning and memory. Nat. Neurosci. 2001, 4:1238-1243.
147. Ohtsuka T., Shimizu K., Yamamori B., Kuroda S., Takai Y. Activation of brain B-Raf protein kinase by Rap1B small GTP-binding protein. J. Biol. Chem. 1996, 271:1258-1261.
148. Oishi K., Gaengel K., Krishnamoorthy S., Kamiya K., Kim I.K., Ying H., Weber U., Perkins L.A., Tartaglia M., Mlodzik M., et al. Transgenic Drosophila models of Noonan syndrome causing PTPN11 gain-of-function mutations. Hum. Mol. Genet. 2006, 15:543-553.
149. Omerovic J., Prior I.A. Compartmentalized signalling: Ras proteins and signalling nanoclusters. FEBS J. 2009, 276:1817-1825.
150. Opazo P., Watabe A.M., Grant S.G., O'Dell T.J. Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J. Neurosci. 2003, 23:3679-3688.
151. Orme M.H., Alrubaie S., Bradley G.L., Walker C.D., Leevers S.J. Input from Ras is required for maximal PI(3)K signalling in Drosophila. Nat. Cell Biol. 2006, 8:1298-1302.
152. Ostroveanu A., van der Zee E.A., Eisel U.L., Schmidt M., Nijholt I.M. Exchange protein activated by cyclic AMP 2 (Epac2) plays a specific and time-limited role in memory retrieval. Hippocampus 2009, 20:1018-1026.
153. Ou L.C., Gean P.W. Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol-3-kinase. Neuropsychopharmacology 2006, 31:287-296.
154. Ouyang M., Zhang L., Zhu J.J., Schwede F., Thomas S.A. Epac signaling is required for hippocampus-dependent memory retrieval. Proc. Natl. Acad. Sci. USA 2008, 105:11993-11997.
155. Overbeck A.F., Brtva T.R., Cox A.D., Graham S.M., Huff S.Y., Khosravi-Far R., Quilliam L.A., Solski P.A., Der C.J. Guanine nucleotide exchange factors: activators of Ras superfamily proteins. Mol. Reprod. Dev. 1995, 42:468-476.
156. Owe-Larsson B., Chaves-Olarte E., Chauhan A., Kjaerulff O., Brask J., Thelestam M., Brodin L., Löw P. Inhibition of hippocampal synaptic transmission by impairment of Ral function. Neuroreport 2005, 16:1805-1808.
157. Ozonoff S. Cognitive impairment in neurofibromatosis type 1. Am. J. Med. Genet. 1999, 89:45-52.
158. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 1996, 65:65-72.
159. Pagani M.R., Oishi K., Gelb B.D., Zhong Y. The phosphatase SHP2 regulates the spacing effect for long-term memory induction. Cell 2009, 139:186-198.
160. Pak D.T., Yang S., Rudolph-Correia S., Kim E., Sheng M. Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 2001, 31:289-303.
161. Pan B.X., Vautier F., Ito W., Bolshakov V.Y., Morozov A. Enhanced cortico-amygdala efficacy and suppressed fear in absence of Rap1. J. Neurosci. 2008, 28:2089-2098.
162. Papakonstanti E.A., Ridley A.J., Vanhaesebroeck B. The p110delta isoform of PI 3-kinase negatively controls RhoA and PTEN. EMBO J. 2007, 26:3050-3061.
163. Papakonstanti E.A., Zwaenepoel O., Bilancio A., Burns E., Nock G.E., Houseman B., Shokat K., Ridley A.J., Vanhaesebroeck B. Distinct roles of class IA PI3K isoforms in primary and immortalised macrophages. J. Cell Sci. 2008, 121:4124-4133.
164. Papin C., Denouel A., Calothy G., Eychène A. Identification of signalling proteins interacting with B-Raf in the yeast two-hybrid system. Oncogene 1996, 12:2213-2221.
165. Pena V., Hothorn M., Eberth A., Kaschau N., Parret A., Gremer L., Bonneau F., Ahmadian M.R., Scheffzek K. The C2 domain of SynGAP is essential for stimulation of the Rap GTPase reaction. EMBO Rep. 2008, 9:350-355.
166. Perkins L.A., Johnson M.R., Melnick M.B., Perrimon N. The nonreceptor protein tyrosine phosphatase corkscrew functions in multiple receptor tyrosine kinase pathways in Drosophila. Dev. Biol. 1996, 180:63-81.
167. Pham N., Cheglakov I., Koch C.A., de Hoog C.L., Moran M.F., Rotin D. The guanine nucleotide exchange factor CNrasGEF activates ras in response to cAMP and cGMP. Curr. Biol. 2000, 10:555-558.
168. Philips G.T., Tzvetkova E.I., Carew T.J. Transient mitogen-activated protein kinase activation is confined to a narrow temporal window required for the induction of two-trial long-term memory in Aplysia. J. Neurosci. 2007, 27:13701-13705.
169. Pizon V., Chardin P., Lerosey I., Olofsson B., Tavitian A. Human cDNAs rap1 and rap2 homologous to the Drosophila gene Dras3 encode proteins closely related to ras in the 'effector' region. Oncogene 1988, 3:201-204.
170. Polzin A., Shipitsin M., Goi T., Feig L.A., Turner T.J. Ral-GTPase influences the regulation of the readily releasable pool of synaptic vesicles. Mol. Cell. Biol. 2002, 22:1714-1722.
171. Pouzet B., Zhang W.N., Feldon J., Rawlins J.N. Hippocampal lesioned rats are able to learn a spatial position using non-spatial strategies. Behav. Brain Res. 2002, 133:279-291.
172. Powell C.M. Gene targeting of presynaptic proteins in synaptic plasticity and memory: across the great divide. Neurobiol. Learn. Mem. 2006, 85:2-15.
173. Qin Y., Zhu Y., Baumgart J.P., Stornetta R.L., Seidenman K., Mack V., van Aelst L., Zhu J.J. State-dependent Ras signaling and AMPA receptor trafficking. Genes Dev. 2005, 19:2000-2015.
174. Raymond C.R., Redman S.J., Crouch M.F. The phosphoinositide 3-kinase and p70 S6 kinase regulate long-term potentiation in hippocampal neurons. Neuroscience 2002, 109:531-536.
175. Riccardi V.M. Von Recklinghausen neurofibromatosis. N. Engl. J. Med. 1981, 305:1617-1627.
176. Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J., Waterfield M.D., Downward J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 1994, 370:527-532.
177. Rodriguez-Viciana P., Marte B.M., Warne P.H., Downward J. Phosphatidylinositol 3′ kinase: one of the effectors of Ras. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1996, 351:225-231, discussion 231-232.
178. Rodriguez-Viciana P., Warne P.H., Vanhaesebroeck B., Waterfield M.D., Downward J. Activation of phosphoinositide 3-kinase by interaction with Ras and by point mutation. EMBO J. 1996, 15:2442-2451.
179. Rosen L.B., Ginty D.D., Weber M.J., Greenberg M.E. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 1994, 12:1207-1221.
180. Roy S., Wyse B., Hancock J.F. H-Ras signaling and K-Ras signaling are differentially dependent on endocytosis. Mol. Cell. Biol. 2002, 22:5128-5140.
181. Rumbaugh G., Adams J.P., Kim J.H., Huganir R.L. SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons. Proc. Natl. Acad. Sci. USA 2006, 103:4344-4351.
182. Ryu J., Futai K., Feliu M., Weinberg R., Sheng M. Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J. Neurosci. 2008, 28:8178-8188.
183. Sampson J.R. Therapeutic targeting of mTOR in tuberous sclerosis. Biochem. Soc. Trans. 2009, 37:259-264.
184. Sanna P.P., Cammalleri M., Berton F., Simpson C., Lutjens R., Bloom F.E., Francesconi W. Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J. Neurosci. 2002, 22:3359-3365.
185. Sawada Y., Nakamura K., Doi K., Takeda K., Tobiume K., Saitoh M., Morita K., Komuro I., De Vos K., Sheetz M., Ichijo H. Rap1 is involved in cell stretching modulation of p38 but not ERK or JNK MAP kinase. J. Cell Sci. 2001, 114:1221-1227.
186. Schenk U., Menna E., Kim T., Passafaro M., Chang S., De Camilli P., Matteoli M. A novel pathway for presynaptic mitogen-activated kinase activation via AMPA receptors. J. Neurosci. 2005, 25:1654-1663.
187. Schmid R.S., Graff R.D., Schaller M.D., Chen S., Schachner M., Hemperly J.J., Maness P.F. NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells. J. Neurobiol. 1999, 38:542-558.
188. Schmitt J.M., Stork P.J. Cyclic AMP-mediated inhibition of cell growth requires the small G protein Rap1. Mol. Cell. Biol. 2001, 21:3671-3683.
189. Seeger G., Yan L., Gärtner U., Huemmeke M., Barmashenko G., Mittmann T., Heumann R., Arendt T. Activation of Ras in neurons modifies synaptic vesicle docking and release. Neuroreport 2004, 15:2651-2654.
190. Seeger G., Gärtner U., Arendt T. Transgenic activation of Ras in neurons increases synapse formation in mouse neocortex. J. Neural Transm. 2005, 112:751-761.
191. Segal M. Dendritic spines and long-term plasticity. Nat. Rev. Neurosci. 2005, 6:277-284.
192. Shalin S.C., Hernandez C.M., Dougherty M.K., Morrison D.K., Sweatt J.D. Kinase suppressor of Ras1 compartmentalizes hippocampal signal transduction and subserves synaptic plasticity and memory formation. Neuron 2006, 50:765-779.
193. Sharma S.K., Sherff C.M., Shobe J., Bagnall M.W., Sutton M.A., Carew T.J. Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J. Neurosci. 2003, 23:3899-3907.
194. Shimizu K., Okada M., Takano A., Nagai K. SCOP, a novel gene product expressed in a circadian manner in rat suprachiasmatic nucleus. FEBS Lett. 1999, 458:363-369.
195. Shimizu K., Okada M., Nagai K., Fukada Y. Suprachiasmatic nucleus circadian oscillatory protein, a novel binding partner of K-Ras in the membrane rafts, negatively regulates MAPK pathway. J. Biol. Chem. 2003, 278:14920-14925.
196. Shimizu K., Phan T., Mansuy I.M., Storm D.R. Proteolytic degradation of SCOP in the hippocampus contributes to activation of MAP kinase and memory. Cell 2007, 128:1219-1229.
197. Shirazi Fard S., Kele J., Vilar M., Paratcha G., Ledda F. Tiam1 as a signaling mediator of nerve growth factor-dependent neurite outgrowth. PLoS ONE 2010, 5:e9647.
198. Shobe J.L., Zhao Y., Stough S., Ye X., Hsuan V., Martin K.C., Carew T.J. Temporal phases of activity-dependent plasticity and memory are mediated by compartmentalized routing of MAPK signaling in aplysia sensory neurons. Neuron 2009, 61:113-125.
199. Shou C., Farnsworth C.L., Neel B.G., Feig L.A. Molecular cloning of cDNAs encoding a guanine-nucleotide-releasing factor for Ras p21. Nature 1992, 358:351-354.
200. Silva A.J., Frankland P.W., Marowitz Z., Friedman E., Laszlo G.S., Cioffi D., Jacks T., Bourtchuladze R., Lazlo G. A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat. Genet. 1997, 15:281-284.
201. Sjölander A., Yamamoto K., Huber B.E., Lapetina E.G. Association of p21ras with phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 1991, 88:7908-7912.
202. Son H., Seuk Kim J., Mogg Kim J., Lee S.H., Lee Y.S. Reciprocal actions of NCAM and tPA via a Ras-dependent MAPK activation in rat hippocampal neurons. Biochem. Biophys. Res. Commun. 2002, 298:262-268.
203. Srivastava D.P., Woolfrey K.M., Woolfrey K., Jones K.A., Shum C.Y., Lash L.L., Swanson G.T., Penzes P. Rapid enhancement of two-step wiring plasticity by estrogen and NMDA receptor activity. Proc. Natl. Acad. Sci. USA 2008, 105:14650-14655.
204. Ster J., de Bock F., Bertaso F., Abitbol K., Daniel H., Bockaert J., Fagni L. Epac mediates PACAP-dependent long-term depression in the hippocampus. J. Physiol. 2009, 587:101-113.
205. Storm S.M., Cleveland J.L., Rapp U.R. Expression of raf family proto-oncogenes in normal mouse tissues. Oncogene 1990, 5:345-351.
206. Stornetta R.L., Zhu J.J. Ras and Rap signaling in synaptic plasticity and mental disorders. Neuroscientist 2010, in press. Published online April 29, 2010. 10.1177/1073858410365562.
207. Sui L., Wang J., Li B.M. Role of the phosphoinositide 3-kinase-Akt-mammalian target of the rapamycin signaling pathway in long-term potentiation and trace fear conditioning memory in rat medial prefrontal cortex. Learn. Mem. 2008, 15:762-776.
208. Sun J., Qian Y., Hamilton A.D., Sebti S.M. Ras CAAX peptidomimetic FTI 276 selectively blocks tumor growth in nude mice of a human lung carcinoma with K-Ras mutation and p53 deletion. Cancer Res. 1995, 55:4243-4247.
209. Sutton M.A., Carew T.J. Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia. Neuron 2000, 26:219-231.
210. Sutton M.A., Masters S.E., Bagnall M.W., Carew T.J. Molecular mechanisms underlying a unique intermediate phase of memory in aplysia. Neuron 2001, 31:143-154.
211. Sutton M.A., Ide J., Masters S.E., Carew T.J. Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in aplysia. Learn. Mem. 2002, 9:29-40.
212. Sutton M.A., Bagnall M.W., Sharma S.K., Shobe J., Carew T.J. Intermediate-term memory for site-specific sensitization in aplysia is maintained by persistent activation of protein kinase C. J. Neurosci. 2004, 24:3600-3609.
213. Suvarna N., Borgland S.L., Wang J., Phamluong K., Auberson Y.P., Bonci A., Ron D. Ethanol alters trafficking and functional N-methyl-D-aspartate receptor NR2 subunit ratio via H-Ras. J. Biol. Chem. 2005, 280:31450-31459.
214. Sytnyk V., Leshchyns'ka I., Nikonenko A.G., Schachner M. NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J. Cell Biol. 2006, 174:1071-1085.
215. Taira K., Umikawa M., Takei K., Myagmar B.E., Shinzato M., Machida N., Uezato H., Nonaka S., Kariya K. The Traf2- and Nck-interacting kinase as a putative effector of Rap2 to regulate actin cytoskeleton. J. Biol. Chem. 2004, 279:49488-49496.
216. Takahashi H., Sekino Y., Tanaka S., Mizui T., Kishi S., Shirao T. Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis. J. Neurosci. 2003, 23:6586-6595.
217. Tall G.G., Barbieri M.A., Stahl P.D., Horazdovsky B.F. Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell 2001, 1:73-82.
218. Thornton C., Yaka R., Dinh S., Ron D. H-Ras modulates N-methyl-D-aspartate receptor function via inhibition of Src tyrosine kinase activity. J. Biol. Chem. 2003, 278:23823-23829.
219. Tohda C., Nakanishi R., Kadowaki M. Learning deficits and agenesis of synapses and myelinated axons in phosphoinositide-3 kinase-deficient mice. Neurosignals 2007, 15:293-306.
220. Tong J., Hannan F., Zhu Y., Bernards A., Zhong Y. Neurofibromin regulates G protein-stimulated adenylyl cyclase activity. Nat. Neurosci. 2002, 5:95-96.
221. Tonini R., Franceschetti S., Parolaro D., Sala M., Mancinelli E., Tininini S., Brusetti R., Sancini G., Brambilla R., Martegani E., et al. Involvement of CDC25Mm/Ras-GRF1-dependent signaling in the control of neuronal excitability. Mol. Cell. Neurosci. 2001, 18:691-701.
222. Trudeau L.E., Emery D.G., Haydon P.G. Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron 1996, 17:789-797.
223. Udo H., Jin I., Kim J.H., Li H.L., Youn T., Hawkins R.D., Kandel E.R., Bailey C.H. Serotonin-induced regulation of the actin network for learning-related synaptic growth requires Cdc42, N-WASP, and PAK in Aplysia sensory neurons. Neuron 2005, 45:887-901.
224. Urano T., Emkey R., Feig L.A. Ral-GTPases mediate a distinct downstream signaling pathway from Ras that facilitates cellular transformation. EMBO J. 1996, 15:810-816.
225. Vanhaesebroeck B., Guillermet-Guibert J., Graupera M., Bilanges B. The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 2010, 11:329-341.
226. Vara H., Onofri F., Benfenati F., Sassoè-Pognetto M., Giustetto M. ERK activation in axonal varicosities modulates presynaptic plasticity in the CA3 region of the hippocampus through synapsin I. Proc. Natl. Acad. Sci. USA 2009, 106:9872-9877.
227. Wakioka T., Sasaki A., Kato R., Shouda T., Matsumoto A., Miyoshi K., Tsuneoka M., Komiya S., Baron R., Yoshimura A. Spred is a Sprouty-related suppressor of Ras signalling. Nature 2001, 412:647-651.
228. Wellbrock C., Karasarides M., Marais R. The RAF proteins take centre stage. Nat. Rev. Mol. Cell Biol. 2004, 5:875-885.
229. White M.A., Vale T., Camonis J.H., Schaefer E., Wigler M.H. A role for the Ral guanine nucleotide dissociation stimulator in mediating Ras-induced transformation. J. Biol. Chem. 1996, 271:16439-16442.
230. Wood K.W., Sarnecki C., Roberts T.M., Blenis J. ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK. Cell 1992, 68:1041-1050.
231. Woolfrey K.M., Srivastava D.P., Photowala H., Yamashita M., Barbolina M.V., Cahill M.E., Xie Z., Jones K.A., Quilliam L.A., Prakriya M., Penzes P. Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat. Neurosci. 2009, 12:1275-1284.
232. Xie Z., Huganir R.L., Penzes P. Activity-dependent dendritic spine structural plasticity is regulated by small GTPase Rap1 and its target AF-6. Neuron 2005, 48:605-618.
233. Yamauchi J., Miyamoto Y., Tanoue A., Shooter E.M., Chan J.R. Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration. Proc. Natl. Acad. Sci. USA 2005, 102:14889-14894.
234. Ye X., Shobe J.L., Sharma S.K., Marina A., Carew T.J. Small G proteins exhibit pattern sensitivity in MAPK activation during the induction of memory and synaptic facilitation in Aplysia. Proc. Natl. Acad. Sci. USA 2008, 105:20511-20516.
235. York R.D., Yao H., Dillon T., Ellig C.L., Eckert S.P., McCleskey E.W., Stork P.J. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 1998, 392:622-626.
236. Yun H.Y., Gonzalez-Zulueta M., Dawson V.L., Dawson T.M. Nitric oxide mediates N-methyl-D-aspartate receptor-induced activation of p21ras. Proc. Natl. Acad. Sci. USA 1998, 95:5773-5778.
237. Zhang F.L., Casey P.J. Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 1996, 65:241-269.
238. Zhong Y., Wu C.F. Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 1991, 251:198-201.
239. Zhong N., Zucker R.S. cAMP acts on exchange protein activated by cAMP/cAMP-regulated guanine nucleotide exchange protein to regulate transmitter release at the crayfish neuromuscular junction. J. Neurosci. 2005, 25:208-214.
240. Zhu J.J., Qin Y., Zhao M., Van Aelst L., Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002, 110:443-455.
241. Zhu Y., Pak D., Qin Y., McCormack S.G., Kim M.J., Baumgart J.P., Velamoor V., Auberson Y.P., Osten P., van Aelst L., et al. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 2005, 46:905-916.