Epac2-mediated dendritic spine remodeling: Implications for disease

Molecular and Cellular Neuroscience

Volumn 46, Issue 2, 2011, Pages 368-380

  Penzes, Peter ^a   Woolfrey, Kevin M ^a   Srivastava, Deepak P ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Autism; CAMP; Dendritic spine; Dopamine; GEF; GluR2; GTPase; Neuroligin; Rap

Indexed keywords

AMPA RECEPTOR; CYCLIC AMP; DOPAMINE 1 RECEPTOR STIMULATING AGENT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; NEUROLIGIN; RAP PROTEIN;

AUTISM; BRAIN FUNCTION; CELL STRUCTURE; COGNITION; DENDRITIC SPINE; DOWN SYNDROME; EXCHANGE PROTEIN ACTIVATED BY CAMP GENE; GENE; GENE EXPRESSION; GENE LOCATION; GENE MUTATION; HUMAN; LONG TERM DEPRESSION; MACROMOLECULE; MENTAL DEFICIENCY; MOLECULAR PATHOLOGY; NEUROLOGIC DISEASE; NONHUMAN; PHARMACOLOGICAL STIMULATION; PHENOTYPE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DENDRITIC SPINES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; NEURONAL PLASTICITY; PROSENCEPHALON;

MAMMALIA;

EID: 78751703574     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.11.008     Document Type: Review

References (133)

1. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 2007, 30:79-97.
2. Armstrong D.D. Neuropathology of Rett syndrome. J. Child Neurol. 2005, 20:747-753.
3. Bacchelli E., Blasi F., Biondolillo M., Lamb J.A., Bonora E., Barnby G., Parr J., Beyer K.S., Klauck S.M., Poustka A., Bailey A.J., Monaco A.P., Maestrini E. Screening of nine candidate genes for autism on chromosome 2q reveals rare nonsynonymous variants in the cAMP-GEFII gene. Mol. Psychiatry 2003, 8:916-924.
4. Beene D.L., Scott J.D. A-kinase anchoring proteins take shape. Curr. Opin. Cell Biol. 2007, 19:192-198.
5. Belmonte M.K., Allen G., Beckel-Mitchener A., Boulanger L.M., Carper R.A., Webb S.J. Autism and abnormal development of brain connectivity. J. Neurosci. 2004, 24:9228-9231.
6. Berkel S., Marshall C.R., Weiss B., Howe J., Roeth R., Moog U., Endris V., Roberts W., Szatmari P., Pinto D., Bonin M., Riess A., Engels H., Sprengel R., Scherer S.W., Rappold G.A. Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation. Nat. Genet. 2010, 42:489-491.
7. Berry-Kravis E., Ciurlionis R. Overexpression of fragile X gene (FMR-1) transcripts increases cAMP production in neural cells. J. Neurosci. Res. 1998, 51:41-48.
8. Bhatt D.H., Zhang S., Gan W.B. Dendritic spine dynamics. Annu. Rev. Physiol. 2009, 71:261-282.
9. Bonhoeffer T., Yuste R. Spine motility. Phenomenology, mechanisms, and function. Neuron 2002, 35:1019-1027.
10. Bos J.L. Epac: a new cAMP target and new avenues in cAMP research. Nat. Rev. Mol. Cell Biol. 2003, 4:733-738.
11. Bos J.L. Linking Rap to cell adhesion. Curr. Opin. Cell Biol. 2005, 17:123-128.
12. Bose M., Munoz-Llancao P., Roychowdhury S., Nichols J.A., Jakkamsetti V., Porter B., Byrapureddy R., Salgado H., Kilgard M.P., Aboitiz F., Dagnino-Subiabre A., Atzori M. Effect of the environment on the dendritic morphology of the rat auditory cortex. Synapse 2009, 64:97-110.
13. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 2008, 31:47-67.
14. Buxbaum J.D., Silverman J.M., Smith C.J., Kilifarski M., Reichert J., Hollander E., Lawlor B.A., Fitzgerald M., Greenberg D.A., Davis K.L. Evidence for a susceptibility gene for autism on chromosome 2 and for genetic heterogeneity. Am. J. Hum. Genet. 2001, 68:1514-1520.
15. Canitano R. Self injurious behavior in autism: clinical aspects and treatment with risperidone. J. Neural Transm. 2006, 113:425-431.
16. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClay J., Mill J., Martin J., Braithwaite A., Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
17. CDC Prevalence of autism spectrum disorders - Autism and Developmental Disabilities Monitoring Network, United States, 2006. MMWR Surveill. Summ. 2009, 58:1-20.
18. Chen Z., Ito K., Fujii S., Miura M., Furuse H., Sasaki H., Kaneko K., Kato H., Miyakawa H. Roles of dopamine receptors in long-term depression: enhancement via D1 receptors and inhibition via D2 receptors. Recept. Channels 1996, 4:1-8.
19. Chen X., Wu B., Kendler K.S. Association study of the Epac gene and tobacco smoking and nicotine dependence. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2004, 129:116-119.
20. Chen Y., Wang P.Y., Ghosh A. Regulation of cortical dendrite development by Rap1 signaling. Mol. Cell. Neurosci. 2005, 28:215-228.
21. Cheung U., Atwood H.L., Zucker R.S. Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J. Neurobiol. 2006, 66:273-280.
22. Chih B., Afridi S.K., Clark L., Scheiffele P. Disorder-associated mutations lead to functional inactivation of neuroligins. Hum. Mol. Genet. 2004, 13:1471-1477.
23. Chih B., Engelman H., Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
24. Cook E.H. Autism: review of neurochemical investigation. Synapse 1990, 6:292-308.
25. Cooper D.M. Compartmentalization of adenylate cyclase and cAMP signalling. Biochem. Soc. Trans. 2005, 33:1319-1322.
26. Social Brain Circuitry in Autism 2007, Guilford Press, New York. G.B.R. Dawson (Ed.).
27. Dierssen M., Ramakers G.J. Dendritic pathology in mental retardation: from molecular genetics to neurobiology. Genes Brain Behav. 2006, 5(Suppl. 2):48-60.
28. DSM-IV Diagnostic and Statistical Manual of Mental Disorders 2000, Washington, DC. 4th Edition.
29. Durand C.M., Betancur C., Boeckers T.M., Bockmann J., Chaste P., Fauchereau F., Nygren G., Rastam M., Gillberg I.C., Anckarsater H., Sponheim E., Goubran-Botros H., Delorme R., Chabane N., Mouren-Simeoni M.C., de Mas P., Bieth E., Roge B., Heron D., Burglen L., Gillberg C., Leboyer M., Bourgeron T. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 2007, 39:25-27.
30. Dwivedi Y., Mondal A.C., Rizavi H.S., Faludi G., Palkovits M., Sarosi A., Conley R.R., Pandey G.N. Differential and brain region-specific regulation of Rap-1 and Epac in depressed suicide victims. Arch. Gen. Psychiatry 2006, 63:639-648.
31. Enserink J.M., Christensen A.E., de Rooij J., van Triest M., Schwede F., Genieser H.G., Doskeland S.O., Blank J.L., Bos J.L. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 2002, 4:901-906.
32. Ernst M., Zametkin A.J., Matochik J.A., Pascualvaca D., Cohen R.M. Low medial prefrontal dopaminergic activity in autistic children. Lancet 1997, 350:638.
33. Feldman D.E. Synaptic mechanisms for plasticity in neocortex. Annu. Rev. Neurosci. 2009, 32:33-55.
34. Fiala J.C., Spacek J., Harris K.M. Dendritic spine pathology: cause or consequence of neurological disorders?. Brain Res. Brain Res. Rev. 2002, 39:29-54.
35. Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 1993, 260:1661-1664.
36. Frost N.A., Kerr J.M., Lu H.E., Blanpied T.A. A network of networks: cytoskeletal control of compartmentalized function within dendritic spines. Curr. Opin. Neurobiol. 2010.
37. Gallagher L., Becker K., Kearney G., Dunlop A., Stallings R., Green A., Fitzgerald M., Gill M. Brief report: A case of autism associated with del(2)(q32.1q32.2) or (q32.2q32.3). J. Autism Dev. Disord. 2003, 33:105-108.
38. Gekel I., Neher E. Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J. Neurosci. 2008, 28:7991-8002.
39. 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. (Cold Spring Harbor, N. Y.) 2008, 15:403-411.
40. Gereau R.W.t., Conn P.J. Potentiation of cAMP responses by metabotropic glutamate receptors depresses excitatory synaptic transmission by a kinase-independent mechanism. Neuron 1994, 12:1121-1129.
41. Geschwind D.H. Autism: many genes, common pathways?. Cell 2008, 135:391-395.
42. Geschwind D.H., Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr. Opin. Neurobiol. 2007, 17:103-111.
43. Glantz L.A., Lewis D.A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch. Gen. Psychiatry 2000, 57:65-73.
44. Gloerich M., Bos J.L. Epac: defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol. 2010, 50:355-375.
45. Goodnough D.B., Baker G.B. 5-Hydroxytryptamine2 and beta-adrenergic receptor regulation in rat brain following chronic treatment with desipramine and fluoxetine alone and in combination. J. Neurochem. 1994, 62:2262-2268.
46. Gorman J.M., Docherty J.P. A hypothesized role for dendritic remodeling in the etiology of mood and anxiety disorders. J. Neuropsychiatry Clin. Neurosci. 2010, 22:256-264.
47. Grandoch M., Roscioni S.S., Schmidt M. The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Br. J. Pharmacol. 2010, 159:265-284.
48. Grutzendler J., Gan W.B. Two-photon imaging of synaptic plasticity and pathology in the living mouse brain. NeuroRx 2006, 3:489-496.
49. Grutzendler J., Kasthuri N., Gan W.B. Long-term dendritic spine stability in the adult cortex. Nature 2002, 420:812-816.
50. Helms M.N., Chen X.J., Ramosevac S., Eaton D.C., Jain L. Dopamine regulation of amiloride-sensitive sodium channels in lung cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 290:L710-L722.
51. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009, 10:647-658.
52. Hotulainen P., Hoogenraad C.C. Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 2010, 189:619-629.
53. Huang Y.Y., Simpson E., Kellendonk C., Kandel E.R. Genetic evidence for the bidirectional modulation of synaptic plasticity in the prefrontal cortex by D1 receptors. Proc. Natl Acad. Sci. USA 2004, 101:3236-3241.
54. Hutsler J.J., Zhang H. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res. 2010, 1309:83-94.
55. Imamura Y., Matsumoto N., Kondo S., Kitayama H., Noda M. Possible involvement of Rap1 and Ras in glutamatergic synaptic transmission. NeuroReport 2003, 14:1203-1207.
56. IMGSAC A genomewide screen for autism: strong evidence for linkage to chromosomes 2q, 7q, and 16p. Am. J. Hum. Genet. 2001, 69:570-581.
57. Irwin S.A., Galvez R., Greenough W.T. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb. Cortex 2000, 10:1038-1044.
58. Isaac J.T., Crair M.C., Nicoll R.A., Malenka R.C. Silent synapses during development of thalamocortical inputs. Neuron 1997, 18:269-280.
59. Johnson-Farley N.N., Kertesy S.B., Dubyak G.R., Cowen D.S. Enhanced activation of Akt and extracellular-regulated kinase pathways by simultaneous occupancy of Gq-coupled 5-HT2A receptors and Gs-coupled 5-HT7A receptors in PC12 cells. J. Neurochem. 2005, 92:72-82.
60. Jones K.A., Srivastava D.P., Allen J.A., Strachan R.T., Roth B.L., Penzes P. Rapid modulation of spine morphology by the 5-HT2A serotonin receptor through kalirin-7 signaling. Proc. Natl Acad. Sci. USA 2009, 106:19575-19580.
61. Jordan B.A., Fernholz B.D., Boussac M., Xu C., Grigorean G., Ziff E.B., Neubert T.A. Identification and verification of novel rodent postsynaptic density proteins. Mol. Cell. Proteomics 2004, 3:857-871.
62. Kasai H., Matsuzaki M., Noguchi J., Yasumatsu N., Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 2003, 26:360-368.
63. Kasai H., Fukuda M., Watanabe S., Hayashi-Takagi A., Noguchi J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 2010, 33:121-129.
64. 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.
65. Kayser M.S., Nolt M.J., Dalva M.B. EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 2008, 59:56-69.
66. Kelleher R.J., Bear M.F. The autistic neuron: troubled translation?. Cell 2008, 135:401-406.
67. Kelley D.J., Davidson R.J., Elliott J.L., Lahvis G.P., Yin J.C., Bhattacharyya A. The cyclic AMP cascade is altered in the fragile X nervous system. PLoS ONE 2007, 2:e931.
68. Kelley D.J., Bhattacharyya A., Lahvis G.P., Yin J.C., Malter J., Davidson R.J. The cyclic AMP phenotype of fragile X and autism. Neurosci. Biobehav. Rev. 2008, 32:1533-1543.
69. Kelly M.P., Stein J.M., Vecsey C.G., Favilla C., Yang X., Bizily S.F., Esposito M.F., Wand G., Kanes S.J., Abel T. Developmental etiology for neuroanatomical and cognitive deficits in mice overexpressing Galphas, a G-protein subunit genetically linked to schizophrenia. Mol. Psychiatry 2009, 14(398-415):347.
70. Lemon N., Manahan-Vaughan D. Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J. Neurosci. 2006, 26:7723-7729.
71. Lewis D.A., Sweet R.A. Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J. Clin. Invest. 2009, 119:706-716.
72. Li Y., Asuri S., Rebhun J.F., Castro A.F., Paranavitana N.C., Quilliam L.A. The RAP1 guanine nucleotide exchange factor Epac2 couples cyclic AMP and Ras signals at the plasma membrane. J. Biol. Chem. 2006, 281:2506-2514.
73. Lise M.F., El-Husseini A. The neuroligin and neurexin families: from structure to function at the synapse. Cell. Mol. Life Sci. 2006, 63:1833-1849.
74. Majewska A.K., Newton J.R., Sur M. Remodeling of synaptic structure in sensory cortical areas in vivo. J. Neurosci. 2006, 26:3021-3029.
75. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
76. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4:1086-1092.
77. 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.
78. Nagerl U.V., Eberhorn N., Cambridge S.B., Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 2004, 44:759-767.
79. Nestler E.J. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2001, 2:119-128.
80. Neuhaus E., Beauchaine T.P., Bernier R. Neurobiological correlates of social functioning in autism. Clin. Psychol. Rev. 2010, 30:733-748.
81. Okamoto K., Bosch M., Hayashi Y. The roles of CaMKII and F-actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag?. Physiology (Bethesda, Md) 2009, 24:357-366.
82. Otmakhov N., Lisman J.E. Postsynaptic application of a cAMP analogue reverses long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2002, 87:3018-3032.
83. 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.
84. 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.
85. Park M., Salgado J.M., Ostroff L., Helton T.D., Robinson C.G., Harris K.M., Ehlers M.D. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 2006, 52:817-830.
86. Peng J., Kim M.J., Cheng D., Duong D.M., Gygi S.P., Sheng M. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 2004, 279:21003-21011.
87. Penzes P., Cahill M.E., Jones K.A., Srivastava D.P. Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol. 2008, 18:405-413.
88. Philippe A., Martinez M., Guilloud-Bataille M., Gillberg C., Rastam M., Sponheim E., Coleman M., Zappella M., Aschauer H., Van Maldergem L., Penet C., Feingold J., Brice A., Leboyer M. Genome-wide scan for autism susceptibility genes. Paris Autism Research International Sibpair Study. Hum. Mol. Genet. 1999, 8:805-812.
89. Pickett J., London E. The neuropathology of autism: a review. J. Neuropathol. Exp. Neurol. 2005, 64:925-935.
90. Ramakers G.J. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 2002, 25:191-199.
91. Rehmann H., Prakash B., Wolf E., Rueppel A., de Rooij J., Bos J.L., Wittinghofer A. Structure and regulation of the cAMP-binding domains of Epac2. Nat. Struct. Biol. 2003, 10:26-32.
92. Rehmann H., Arias-Palomo E., Hadders M.A., Schwede F., Llorca O., Bos J.L. Structure of Epac2 in complex with a cyclic AMP analogue and RAP1B. Nature 2008, 455:124-127.
93. 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.
94. Segal M. Dendritic spines and long-term plasticity. Nat. Rev. Neurosci. 2005, 6:277-284.
95. Segal M. Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. Eur. J. Neurosci. 2010, 31:2178-2184.
96. Shao Y., Raiford K.L., Wolpert C.M., Cope H.A., Ravan S.A., Ashley-Koch A.A., Abramson R.K., Wright H.H., DeLong R.G., Gilbert J.R., Cuccaro M.L., Pericak-Vance M.A. Phenotypic homogeneity provides increased support for linkage on chromosome 2 in autistic disorder. Am. J. Hum. Genet. 2002, 70:1058-1061.
97. Shepherd J.D., Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 2007, 23:613-643.
98. Silva A.J., Murphy G.G. cAMP and memory: a seminal lesson from Drosophila and Aplysia. Brain Res. Bull. 1999, 50:441-442.
99. Springett G.M., Kawasaki H., Spriggs D.R. Non-kinase second-messenger signaling: new pathways with new promise. Bioessays 2004, 26:730-738.
100. Srivastava D.P., 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.
101. + channels in cerebellar neurons. Proc. Natl Acad. Sci. USA 2007, 104:2519-2524.
102. 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.
103. Stork P.J. Does Rap1 deserve a bad Rap?. Trends Biochem. Sci. 2003, 28:267-275.
104. Sudhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
105. Sutton M.A., Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 2006, 127:49-58.
106. Tabuchi K., Blundell J., Etherton M.R., Hammer R.E., Liu X., Powell C.M., Sudhof T.C. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 2007, 318:71-76.
107. Tada T., Sheng M. Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 2006, 16:95-101.
108. Takai Y., Sasaki T., Matozaki T. Small GTP-binding proteins. Physiol. Rev. 2001, 81:153-208.
109. Takashima S., Ieshima A., Nakamura H., Becker L.E. Dendrites, dementia and the Down syndrome. Brain Dev. 1989, 11:131-133.
110. Tau G.Z., Peterson B.S. Normal development of brain circuits. Neuropsychopharmacology 2010, 35:147-168.
111. Tavazoie S.F., Alvarez V.A., Ridenour D.A., Kwiatkowski D.J., Sabatini B.L. Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat. Neurosci. 2005, 8:1727-1734.
112. Toda Y., Mori K., Hashimoto T., Miyazaki M., Nozaki S., Watanabe Y., Kuroda Y., Kagami S. Administration of secretin for autism alters dopamine metabolism in the central nervous system. Brain Dev. 2006, 28:99-103.
113. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420:788-794.
114. van Spronsen M., Hoogenraad C.C. Synapse pathology in psychiatric and neurologic disease. Curr. Neurol. Neurosci. Rep. 2010, 10:207-214.
115. Walsh C.A., Morrow E.M., Rubenstein J.L. Autism and brain development. Cell 2008, 135:396-400.
116. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., Nord A.S., Kusenda M., Malhotra D., Bhandari A., Stray S.M., Rippey C.F., Roccanova P., Makarov V., Lakshmi B., Findling R.L., Sikich L., Stromberg T., Merriman B., Gogtay N., Butler P., Eckstrand K., Noory L., Gochman P., Long R., Chen Z., Davis S., Baker C., Eichler E.E., Meltzer P.S., Nelson S.F., Singleton A.B., Lee M.K., Rapoport J.L., King M.C., Sebat J. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science (New York, N.Y) 2008, 320:539-543.
117. Wilbrecht L., Holtmaat A., Wright N., Fox K., Svoboda K. Structural plasticity underlies experience-dependent functional plasticity of cortical circuits. J. Neurosci. 2010, 30:4927-4932.
118. Winsberg B.G., Sverd J., Castells S., Hurwic M., Perel J.M. Estimation of monoamine and cyclic-AMP turnover and amino acid concentrations of spinal fluid in autistic children. Neuropediatrics 1980, 11:250-255.
119. 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.
120. 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.
121. Xie Z., Srivastava D.P., Photowala H., Kai L., Cahill M.E., Woolfrey K.M., Shum C.Y., Surmeier D.J., Penzes P. Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 2007, 56:640-656.
122. Xie Z., Photowala H., Cahill M.E., Srivastava D.P., Woolfrey K.M., Shum C.Y., Huganir R.L., Penzes P. Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7. J. Neurosci. 2008, 28:6079-6091.
123. Yang Y., Wang X.B., Frerking M., Zhou Q. Spine expansion and stabilization associated with long-term potentiation. J. Neurosci. 2008, 28:5740-5751.
124. Yang G., Pan F., Gan W.B. Stably maintained dendritic spines are associated with lifelong memories. Nature 2009, 462:920-924.
125. Yoshihara Y., De Roo M., Muller D. Dendritic spine formation and stabilization. Curr. Opin. Neurobiol. 2009, 19:146-153.
126. Yu T.P., McKinney S., Lester H.A., Davidson N. Gamma-aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3-CA1 synapses. Proc. Natl Acad. Sci. USA 2001, 98:5264-5269.
127. 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.
128. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44:749-757.
129. 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.
130. 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., Sheng M., Zhu J.J. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 2005, 46:905-916.
131. Zoghbi H.Y. Postnatal neurodevelopmental disorders: meeting at the synapse?. Science 2003, 302:826-830.
132. Zuo Y., Lin A., Chang P., Gan W.B. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 2005, 46:181-189.
133. Zuo Y., Yang G., Kwon E., Gan W.B. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 2005, 436:261-265.