WRP/srGAP3 facilitates the initiation of spine development by an inverse F-BAR domain, and its loss impairs long-term memory

Journal of Neuroscience

Volumn 31, Issue 7, 2011, Pages 2447-2460

  Carlson, Benjamin R ^a   Lloyd, Krissey E ^a   Kruszewski, Allison ^a   Kim, Il Hwan ^a   Rodriguiz, Ramona M ^a   Heindel, Clifford ^a   Faytell, Marika ^a   Dudek, Serena M ^b   Wetsel, William C ^a   Soderling, Scott H ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INVERSE F BAR DOMAIN; PROTEIN; PROTEIN SRGAP3; UNCLASSIFIED DRUG; WAVE ASSOCIATED RAC GTPASE ACTIVATING PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITE; FILOPODIUM; LEARNING DISORDER; LONG TERM MEMORY; MEMORY DISORDER; MENTAL DEFICIENCY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SPINE;

ANIMALS; ANIMALS, NEWBORN; AVOIDANCE LEARNING; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; ELECTROSHOCK; GREEN FLUORESCENT PROTEINS; GTPASE-ACTIVATING PROTEINS; HIPPOCAMPUS; HUMANS; LIPID METABOLISM; LIPOSOMES; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, SCANNING; MODELS, CHEMICAL; NEURONS; NEUROPSYCHOLOGICAL TESTS; PHOSPHATIDYLINOSITOLS; PROTEIN INTERACTION DOMAINS AND MOTIFS; SENSATION;

EID: 79951823003     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4433-10.2011     Document Type: Article

References (61)

1. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18:2423-2436. (Pubitemid 28141791)
2. 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.
3. Banker G, Goslin K (1988) Developments in neuronal cell culture. Nature 336:185-186.
4. Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67.
5. Carlisle HJ, Kennedy MB (2005) Spine architecture and synaptic plasticity. Trends Neurosci 28:182-187. (Pubitemid 40445524)
6. Carlson B, Soderling SH (2009) Mechanisms of cellular protrusions branch out. Dev Cell 17:307-309.
7. Chen PS, Toribara TY, Warner H (1956) Microdetermination of phosphorus. Anal Chem 28:1756-1758.
8. Choi J, Ko J, Racz B, Burette A, Lee JR, Kim S, Na M, Lee HW, Kim K, Weinberg RJ, Kim E (2005) Regulation of dendritic spine morphogenesis by insulin receptor substrate 53, a downstream effector of Rac1 and Cdc42 small GTPases. J Neurosci 25:869-879. (Pubitemid 40171002)
9. 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. (Pubitemid 34994471)
10. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
11. Fiala JC, Feinberg M, Popov V, Harris KM (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911. (Pubitemid 28491754)
12. Fischer M, Kaech S, Wagner U, Brinkhaus H, Matus A (2000) Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci 3:887-894.
13. Ford MG, Mills IG, Peter BJ, Vallis Y, Praefcke GJ, Evans PR, McMahon HT (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419:361-366.
14. Frost A, Perera R, Roux A, Spasov K, Destaing O, Egelman EH, De Camilli P, Unger VM (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132:807-817. (Pubitemid 351320580)
15. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447-460. (Pubitemid 36579146)
16. Grove M, Demyanenko G, Echarri A, Zipfel PA, Quiroz ME, Rodriguiz RM, Playford M, Martensen SA, Robinson MR, Wetsel WC, Maness PF, Pendergast AM (2004) ABI2-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory. Mol Cell Biol 24:10905-10922. (Pubitemid 39603145)
17. 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.
18. Hamdan FF, Gauthier J, Pellerin S, Dobrzeniecka S, Marineau C, Fombonne E, Mottron L, Lafrenière RG, Drapeau P, Lacaille JC, Rouleau GA, Michaud JL (2009) No association between SRGAP3/MEGAP haploinsufficiency and mental retardation. Arch Neurol 66:675-676.
19. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, Zhang D, Chattarji S, Kirkwood A, Tonegawa S (2004) Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominantnegative PAK transgenic mice. Neuron 42:773-787. (Pubitemid 38748791)
20. Honkura N, Matsuzaki M, Noguchi J, Ellis-Davies GC, Kasai H (2008) The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57:719-729. (Pubitemid 351335344)
21. 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.
22. Icking A, Schilling K, Wiesenthal A, Opitz N, Müller-Esterl W (2006) FCH/Cdc15 domain determines distinct subcellular localization of NOSTRIN. FEBS Lett 580:223-228. (Pubitemid 43005340)
23. Itoh T, Koshiba S, Kigawa T, Kikuchi A, Yokoyama S, Takenawa T (2001) Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291:1047-1051. (Pubitemid 32157414)
24. 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. (Pubitemid 41724107)
25. Kamioka Y, Fukuhara S, Sawa H, Nagashima K, Masuda M, Matsuda M, Mochizuki N (2004) A novel dynamin-associating molecule, formin-binding protein 17, induces tubular membrane invaginations and participates in endocytosis. J Biol Chem 279:40091-40099. (Pubitemid 39258284)
26. Kariya S, Aoji K, Akagi H, Fukushima K, Chikumoto E, Ogawa T, Karaki M, Nishizaki K (2000) A terminal deletion of the short arm of chromosome 3: karyotype 46, XY, del (3) (p25-pter); a case report and literature review. Int J Pediatr Otorhinolaryngol 56:71-78.
27. Kayser MS, Nolt MJ, Dalva MB (2008) EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59:56-69. (Pubitemid 351905850)
28. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-371.
29. Konur S, Yuste R (2004) Developmental regulation of spine and filopodial motility in primary visual cortex: reduced effects of activity and sensory deprivation. J Neurobiol 59:236-246. (Pubitemid 38507129)
30. 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.
31. Lendvai B, Stern EA, Chen B, Svoboda K (2000) Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404:876-881. (Pubitemid 30230339)
32. Lohmann C, Bonhoeffer T (2008) A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron 59:253-260. (Pubitemid 352033683)
33. Luo L, Hensch TK, Ackerman L, Barbel S, Jan LY, Jan YN (1996) Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 379:837-840. (Pubitemid 26067727)
34. Mattila PK, Salminen M, Yamashiro T, Lappalainen P (2003) Mouse MIM, a tissue-specific regulator of cytoskeletal dynamics, interacts with ATP-actin monomers through its C-terminal WH2 domain. J Biol Chem 278:8452-8459. (Pubitemid 36800596)
35. Matus A (2000) Actin-based plasticity in dendritic spines. Science 290:754-758.
36. McAllister AK (2007) Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30:425-450.
37. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58:167-176. (Pubitemid 38509178)
38. Nadif Kasri N, Van Aelst L (2008) Rho-linked genes and neurological disorders. Pflugers Arch 455:787-797. (Pubitemid 50003204)
39. 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.
40. Nakayama AY, Harms MB, Luo L (2000) Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J Neurosci 20:5329-5338. (Pubitemid 30457730)
41. Purpura DP (1974) Dendritic spine "dysgenesis" and mental retardation. Science 186:1126-1128.
42. Ramakers GJ (2002) Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci 25:191-199.
43. Raucher D, Stauffer T, Chen W, Shen K, Guo S, York JD, Sheetz MP, Meyer T (2000) Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100:221-228. (Pubitemid 30064910)
44. Roberts AC, Díez-García J, Rodriguiz RM, López IP, Luján R, Martínez-Turrillas R, Picó E, Henson MA, Bernardo DR, Jarrett TM, Clendeninn DJ, Ló pez-Mascaraque L, Feng G, Lo DC, Wesseling JF, Wetsel WC, Philpot BD, Pérez-Otaño I (2009) Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation. Neuron 63:342-356.
45. Rodriguiz RM, Gadnidze K, Ragnauth A, Dorr N, Yanagisawa M, Wetsel WC, Devi LA (2008) Animals lacking endothelin converting enzyme-2 are deficient in learning and memory. Genes Brain Behav 7:418-426. (Pubitemid 351590928)
46. Saarikangas J, Zhao H, Pykäläinen A, Laurinmäki P, Mattila PK, Kinnunen PK, Butcher SJ, Lappalainen P (2009) Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr Biol 19:95-107.
47. Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, Hanawa-Suetsugu K, Akasaka R, Nishino Y, Toyama M, Chen L, Liu ZJ, Wang BC, Yamamoto M, Terada T, Miyazawa A, Tanaka A, Sugano S, Shirouzu M, Nagayama K, Takenawa T, Yokoyama S (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129:761-772. (Pubitemid 46813111)
48. 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.
49. 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. (Pubitemid 35469427)
50. 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. (Pubitemid 46106009)
51. Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1:33-39. (Pubitemid 129495007)
52. 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. (Pubitemid 38968436)
53. Tashiro A, Minden A, Yuste R (2000) Regulation of dendritic spine morphology by the rho family of small GTPases: antagonistic roles of Rac and Rho. Cereb Cortex 10:927-938.
54. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10:727-734. (Pubitemid 46828514)
55. Tsujita K, Suetsugu S, Sasaki N, Furutani M, Oikawa T, Takenawa T (2006) Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J Cell Biol 172:269-279. (Pubitemid 43112973)
56. Wang Z, Edwards JG, Riley N, Provance DW Jr, Karcher R, Li XD, Davison IG, Ikebe M, Mercer JA, Kauer JA, Ehlers MD (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135:535-548.
57. Wegner AM, Nebhan CA, Hu L, Majumdar D, Meier KM, Weaver AM, Webb DJ (2008) N-wasp and the arp2/3 complex are critical regulators of actin in the development of dendritic spines and synapses. J Biol Chem 283:15912-15920.
58. Young P, Qiu L, Wang D, Zhao S, Gross J, Feng G (2008) Single-neuron labeling with inducible Cre-mediated knockout in transgenic mice. Nat Neurosci 11:721-728. (Pubitemid 351748115)
59. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089. (Pubitemid 32695254)
60. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102. (Pubitemid 26251594)
61. Zuo Y, Lin A, Chang P, Gan WB (2005) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181-189. (Pubitemid 40545775)