Regulation of the postsynaptic cytoskeleton: Roles in development, plasticity, and disorders

Journal of Neuroscience

Volumn 30, Issue 45, 2010, Pages 14937-14942

  Svitkina, Tatyana ^a   Lin, Wan Hsin ^b,c   Webb, Donna J ^b,c,d   Yasuda, Ryohei ^e   Wayman, Gary A ^f   Van Aelst, Linda ^g   Soderling, Scott H ^e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f WASHINGTON STATE UNIVERSITY   (United States)

^g Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR;

ACTIN FILAMENT; CELL MATURATION; CELL SIZE; CONFERENCE PAPER; CYTOARCHITECTURE; CYTOSKELETON; DENDRITIC SPINE; HIPPOCAMPUS; HUMAN; MENTAL DEFICIENCY; NERVE CELL PLASTICITY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

ACTINS; ANIMALS; CYTOSKELETON; DENDRITIC SPINES; MICROTUBULES; NEURONAL PLASTICITY; NEURONS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 78149475575     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4276-10.2010     Document Type: Conference Paper

References (76)

1. Ackermann M, Matus A (2003) Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat Neurosci 6:1194-1200.
2. Angeloni D, Lindor NM, Pack S, Latif F, Wei MH, Lerman MI (1999) CALL gene is haploinsufficient in a 3p-syndrome patient. Am J Med Genet 86:482-485.
3. Applewhite DA, Barzik M, Kojima S, Svitkina TM, Gertler FB, Borisy GG (2007) Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol Biol Cell 18:2579-2591.
4. Aspenström P (2009) Roles of F-BAR/PCH proteins in the regulation of membrane dynamics and actin reorganization. Int Rev Cell Mol Biol 272:1-31.
5. Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, Gertler FB, Schafer DA (2005) Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J Biol Chem 280:28653-28662.
6. Bear JE, Loureiro JJ, Libova I, Fässler R, Wehland J, Gertler FB (2000) Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101:717-728.
7. Bergmann C, Zerres K, Senderek J, Rudnik-Schoneborn S, Eggermann T, Häusler M, Mull M, Ramaekers VT (2003) Oligophrenin 1 (OPHN1) gene mutation causes syndromic X-linked mental retardation with epilepsy, rostral ventricular enlargement and cerebellar hypoplasia. Brain 126:1537-1544.
8. Bienvenu T, Der-Sarkissian H, Billuart P, Tissot M, Des Portes V, Brüls T, Chabrolle JP, Chauveau P, Cherry M, Kahn A, Cohen D, Beldjord C, Chelly J, Cherif D (1997) Mapping of the X-breakpoint involved in a balanced X;12 translocation in a female with mild mental retardation. Eur J Hum Genet 5:105-109.
9. Billuart P, Bienvenu T, Ronce N, des Portes V, Vinet MC, Zemni R, Carrié A, Beldjord C, Kahn A, Moraine C, Chelly J (1998) Oligophrenin 1 encodes a rho-GAP protein involved in X-linked mental retardation. Pathol Biol (Paris) 46:678.
10. Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67.
11. Carlson B, Soderling SH (2009) Mechanisms of cellular protrusions branch out. Dev Cell 17:307-309.
12. Chardin P (2006) Function and regulation of Rnd proteins. Nat Rev Mol Cell Biol 7:54-62.
13. Chhabra ES, Higgs HN (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9:1110-1121.
14. Cingolani LA, Thalhammer A, Yu LM, Catalano M, Ramos T, Colicos MA, Goda Y (2008) Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 58:749-762.
15. des Portes V, Boddaert N, Sacco S, Briault S, Maincent K, Bahi N, Gomot M, Ronce N, Bursztyn J, Adamsbaum C, Zilbovicius M, Chelly J, Moraine C (2004) Specific clinical and brain MRI features in mentally retarded patients with mutations in the Oligophrenin-1 gene. Am J Med Genet A 124A:364-371.
16. Endris V, Wogatzky B, Leimer U, Bartsch D, Zatyka M, Latif F, Maher ER, Tariverdian G, Kirsch S, Karch D, Rappold GA (2002) The novel Rho-GTPase activating gene MEGAP/ srGAP3 has a putative role in severe mental retardation. Proc Natl Acad Sci U S A 99:11754-11759.
17. Ethell IM, Pasquale EB (2005) Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75:161-205.
18. Fernandez T, Morgan T, Davis N, Klin A, Morris A, Farhi A, Lifton RP, State MW (2008a) Disruption of Contactin 4 (CNTN4) results in developmental delay and other features of 3p deletion syndrome. Am J Hum Genet 82:1385.
19. Fernandez TV, García-González IJ, Mason CE, Hernández-Zaragoza G, Ledezma-Rodríguez VC, Anguiano-Alvarez VM, E'Vega R, Gutiérrez-Angulo M, Maya ML, García-Bejarano HE, González-Cruz M, Barrios S, Atorga R, López-Cardona MG, Armendariz-Borunda J, State MW, Dávalos NO (2008b) Molecular characterization of a patient with 3p deletion syndrome and a review of the literature. Am J Med Genet A 146A:2746-2752.
20. Gertler FB, Niebuhr K, Reinhard M, Wehland J, Soriano P (1996) Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell 87:227-239.
21. Govek EE, Newey SE, Akerman CJ, Cross JR, Van der Veken L, Van Aelst L (2004) The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat Neurosci 7:364-372.
22. Guerrier S, Coutinho-Budd J, Sassa T, Gresset A, Jordan NV, Chen K, Jin WL, Frost A, Polleux F (2009) The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138:990-1004.
23. Halpain S (2000) Actin and the agile spine: how and why do dendritic spines dance? Trends Neurosci 23:141-146.
24. Harvey CD, Yasuda R, Zhong H, Svoboda K (2008) The spread of Ras activity triggered by activation of a single dendritic spine. Science 321:136-140.
25. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880-888.
26. Higgins JJ, Rosen DR, Loveless JM, Clyman JC, Grau MJ (2000) A gene for nonsyndromic mental retardation maps to chromosome 3p25-pter. Neurology 55:335-340.
27. Hotulainen P, Llano O, Smirnov S, Tanhuanpää K, Faix J, Rivera C, Lappalainen P (2009) Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J Cell Biol 185:323-339.
28. Ikeda Y, Dick KA, Weatherspoon MR, Gincel D, Armbrust KR, Dalton JC, Stevanin G, Dürr A, Zühlke C, Bürk K, Clark HB, Brice A, Rothstein JD, Schut LJ, Day JW, Ranum LP (2006) Spectrin mutations cause spinocerebellar ataxia type 5. Nat Genet 38:184-190.
29. Impey S, Davare M, Lasiek A, Fortin D, Ando H, Varlamova O, Obrietan K, Soderling TR, Goodman RH, Wayman GA (2010) An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol Cell Neurosci 43:146-156.
30. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9:791-804.
31. Kang F, Laine RO, Bubb MR, Southwick FS, Purich DL (1997) Profilin interacts with the Gly-Pro-Pro-Pro-Pro-Pro sequences of vasodilator-stimulated phosphoprotein (VASP): implications for actin-based Listeria motility. Biochemistry 36:8384-8392.
32. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26:360-368.
33. Khelfaoui M, Denis C, van Galen E, de Bock F, Schmitt A, Houbron C, Morice E, Giros B, Ramakers G, Fagni L, Chelly J, Nosten-Bertrand M, Billuart P (2007) Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J Neurosci 27:9439-9450.
34. Khelfaoui M, Pavlowsky A, Powell AD, Valnegri P, Cheong KW, Blandin Y, Passafaro M, Jefferys JG, Chelly J, Billuart P (2009) Inhibition of RhoA pathway rescues the endocytosis defects in Oligophrenin1 mouse model of mental retardation. Hum Mol Genet 18:2575-2583.
35. Komander D, Garg R, Wan PT, Ridley AJ, Barford D (2008) Mechanism of multi-site phosphorylation from a ROCK-I:RhoE complex structure. EMBO J 27:3175-3185.
36. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000-2009.
37. Korobova F, Svitkina T (2010) Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell 21:165-176.
38. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458:299-304.
39. Lin WH, Nebhan CA, Anderson BR, Webb DJ (2010) Vasodilator-stimulated phosphoprotein (VASP) induces actin assembly in dendritic spines to promote their development and potentiate synaptic strength. J Biol Chem 285:36010-36020.
40. Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752.
41. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
42. Matus A (2000) Actin-based plasticity in dendritic spines. Science 290:754-758.
43. Nadif Kasri N, Van Aelst L (2008) Rho-linked genes and neurological disorders. Pflugers Arch 455:787-797.
44. Nadif Kasri N, Nakano-Kobayashi A, Malinow R, Li B, Van Aelst L (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev 23:1289-1302.
45. Nakano-Kobayashi A, Kasri NN, Newey SE, Van Aelst L (2009) The Rho-linked mental retardation protein OPHN1 controls synaptic vesicle endocytosis via endophilin A1. Curr Biol 19:1133-1139.
46. Newey SE, Velamoor V, Govek EE, Van Aelst L (2005) Rho GTPases, dendritic structure, and mental retardation. J Neurobiol 64:58-74.
47. Nimchinsky EA, Sabatini BL, Svoboda K (2002) Structure and function of dendritic spines. Annu Rev Physiol 64:313-353.
48. Okada H, Soderling SH (2009) Signaling through actin to regulate spine formation and function. Open Neurosci J 3:97-107.
49. Okamoto K, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
50. Philip N, Chabrol B, Lossi AM, Cardoso C, Guerrini R, Dobyns WB, Raybaud C, Villard L (2003) Mutations in the oligophrenin-1 gene (OPHN1) cause X linked congenital cerebellar hypoplasia. J Med Genet 40:441-446.
51. Ramakers GJ (2002) Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci 25:191-199.
52. Rao A, Craig AM (2000) Signaling between the actin cytoskeleton and the postsynaptic density of dendritic spines. Hippocampus 10:527-541.
53. Redmond L, Kashani AH, Ghosh A (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34:999-1010.
54. Reinhard M, Giehl K, Abel K, Haffner C, Jarchau T, Hoppe V, Jockusch BM, Walter U (1995) The proline-rich focal adhesion and microfilament protein VASP is a ligand for profilins. EMBO J 14:1583-1589.
55. Rex CS, Chen LY, Sharma A, Liu J, Babayan AH, Gall CM, Lynch G (2009) Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation. J Cell Biol 186:85-97.
56. Riento K, Villalonga P, Garg R, Ridley A (2005) Function and regulation of RhoE. Biochem Soc Trans 33:649-651.
57. Shuib S, McMullan D, Rattenberry E, Barber RM, Rahman F, Zatyka M, Chapman C, Macdonald F, Latif F, Davison V, Maher ER (2009) Microarray based analysis of 3p25-p26 deletions (3p-syndrome).Am J Med Genet A 149A:2099-2105.
58. Soderling SH, Binns KL, Wayman GA, Davee SM, Ong SH, Pawson T, Scott JD (2002) The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat Cell Biol 4:970-975.
59. Soderling SH, Langeberg LK, Soderling JA, Davee SM, Simerly R, Raber J, Scott JD (2003) Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc Natl Acad Sci U S A 100:1723-1728.
60. Soderling SH, Guire ES, Kaech S, White J, Zhang F, Schutz K, Langeberg LK, Banker G, Raber J, Scott JD (2007) A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J Neurosci 27:355-365.
61. Stankewich MC, Gwynn B, Ardito T, Ji L, Kim J, Robledo RF, Lux SE, Peters LL, Morrow JS (2010) Targeted deletion of betaIII spectrin impairs synaptogenesis and generates ataxic and seizure phenotypes. Proc Natl Acad Sci U S A 107:6022-6027.
62. Tada T, Sheng M (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16:95-101.
63. Tashiro A, Yuste R (2004) Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility. Mol Cell Neurosci 26:429-440.
64. Tentler D, Gustavsson P, Leisti J, Schueler M, Chelly J, Timonen E, Annerén G, Willard HF, Dahl N (1999) Deletion including the oligophrenin-1 gene associated with enlarged cerebral ventricles, cerebellar hypoplasia, seizures and ataxia. Eur J Hum Genet 7:541-548.
65. van Galen EJ, Ramakers GJ (2005) Rho proteins, mental retardation and the neurobiological basis of intelligence. Prog Brain Res 147:295-317.
66. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, Impey S (2005) A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci U S A 102:16426-16431.
67. Wayman GA, Impey S, Marks D, Saneyoshi T, Grant WF, Derkach V, Soderling TR (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50:897-909.
68. Wayman GA, Davare M, Ando H, Fortin D, Varlamova O, Cheng HY, Marks D, Obrietan K, Soderling TR, Goodman RH, Impey S (2008) An activity-regulated microRNA controls dendritic plasticity by downregulating p250GAP. Proc Natl Acad Sci U S A 105:9093-9098.
69. Yasuda R (2006) Imaging spatiotemporal dynamics of neuronal signaling using fluorescence resonance energy transfer and fluorescence lifetime imaging microscopy. Curr Opin Neurobiol 16:551-561.
70. Yasuda R, Harvey CD, Zhong H, Sobczyk A, van Aelst L, Svoboda K (2006) Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat Neurosci 9:283-291.
71. Yoshihara Y, De Roo M, Muller D (2009) Dendritic spine formation and stabilization. Curr Opin Neurobiol 19:146-153.
72. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.
73. Zanni G, Saillour Y, Nagara M, Billuart P, Castelnau L, Moraine C, Faivre L, Bertini E, Durr A, Guichet A, Rodriguez D, des Portes V, Beldjord C, Chelly J (2005) Oligophrenin 1 mutations frequently cause X-linked mental retardation with cerebellar hypoplasia. Neurology 65:1364-1369. (Pubitemid 41552762)
74. Zhang H, Macara IG (2008) The PAR-6 polarity protein regulates dendritic spine morphogenesis through p190 RhoGAP and the Rho GTPase. Dev Cell 14:216-226.
75. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.
76. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.