ARF6 and EFA6A regulate the development and maintenance of dendritic spines

Journal of Neuroscience

Volumn 26, Issue 18, 2006, Pages 4811-4819

  Choi, Seungwon ^a   Ko, Jaewon ^a   Lee, Jae Ran ^a   Hyun, Woo Lee ^a   Kim, Karam ^a   Hye, Sun Chung ^b   Kim, Hyun ^b   Kim, Eunjoon ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea University College of Medicine   (South Korea)

Author keywords

ARF6; EFA6A; Filopodia; Rac1; Spine; Synapse

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; EXCHANGE FACTOR ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; GUANOSINE TRIPHOSPHATASE; RAC1 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6; DLGH4 PROTEIN, RAT; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LOCAL ANESTHETIC AGENT; MEMBRANE PROTEIN; PSD PROTEIN, RAT; SIGNAL PEPTIDE; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; FILOPODIUM; HUMAN; HUMAN TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINE; ANIMAL; BRAIN; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DIAGNOSTIC IMAGING; DRUG EFFECT; DRUG INTERACTION; EMBRYO; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; MUTAGENESIS; NERVE CELL; NEWBORN; NORTHERN BLOTTING; PHYSIOLOGY; PSEUDOPODIUM; TIME;

ADP-RIBOSYLATION FACTORS; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; BLOTTING, NORTHERN; BRAIN; CELLS, CULTURED; DENDRITIC SPINES; DIAGNOSTIC IMAGING; DRUG INTERACTIONS; EMBRYO; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MUTAGENESIS; NEURONS; PSEUDOPODIA; RATS; RNA, SMALL INTERFERING; TETRODOTOXIN; TIME FACTORS; TRANSFECTION;

EID: 33646934083     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4182-05.2006     Document Type: Article

References (49)

1. Ashery U, Koch H, Scheuss V, Brose N, Rettig J (1999) A presynaptic role for the ADP ribosylation factor (ARF)-specific GDP/GTP exchange factor msec7-1. Proc Natl Acad Sci USA 96:1094-1099.
2. Carlisle HJ, Kennedy MB (2005) Spine architecture and synaptic plasticity. Trends Neurosci 28:182-187.
3. Chavrier P, Goud B (1999) The role of ARF and Rab GTPases in membrane transport. Curr Opin Cell Biol 11:466-475.
4. Czech MP (2003) Dynamics of phosphoinositides in membrane retrieval and insertion. Annu Rev Physiol 65:791-815.
5. Dailey ME, Smith SJ (1996) The dynamics of dendritic structure in developing hippocampal slices. J Neurosci 16:2983-2994.
6. Derrien V, Couillault C, Franco M, Martineau S, Montcourrier P, Houlgatte R, Chavrier P (2002) A conserved C-terminal domain of EFA6-family ARF6-guanine nucleotide exchange factors induces lengthening of microvilli-like membrane protrusions. J Cell Sci 115:2867-2879.
7. Donaldson JG (2003) Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem 278:41573-41576.
8. Ethell IM, Pasquale EB (2005) Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75:161-205.
9. Fiala JC, Feinberg M, Popov V, Harris KM (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911.
10. Fiala JC, Spacek J, Harris KM (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Brain Res Rev 39:29-54.
11. Franco M, Peters PJ, Boretto J, van Donselaar E, Neri A, D'Souza-Schorey C, Chavrier P (1999) EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization. EMBO J 18:1480-1491.
12. Hayashi Y, Majewska AK (2005) Dendritic spine geometry: functional implication and regulation. Neuron 46:529-532.
13. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880-888.
14. Hernandez-Deviez DJ, Casanova JE, Wilson JM (2002) Regulation of dendritic development by the ARF exchange factor ARNO. Nat Neurosci 5:623-624.
15. Hernandez-Deviez DJ, Roth MG, Casanova JE, Wilson JM (2004) ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase alpha. Mol Biol Cell 15:111-120.
16. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, Kanaho Y (1999) Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521-532.
17. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, Neubert TA (2004) Identification and verification of novel rodent postsynaptic density proteins. Mol Cell Proteomics 3:857-871.
18. Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V (2003) ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J Cell Biol 162:113-124.
19. 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.
20. Maletic-Savatic M, Malinow R, Svoboda K (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923-1927.
21. Marrs GS, Green SH, Dailey ME (2001) Rapid formation and remodeling of postsynaptic densities in developing dendrites. Nat Neurosci 4:1006-1013.
22. Matsuya S, Sakagami H, Tohgo A, Owada Y, Shin HW, Takeshima H, Nakayama K, Kokubun S, Kondo H (2005) Cellular and subcellular localization of EFA6C, a third member of the EFA6 family, in adult mouse Purkinje cells. J Neurochem 93:674-685.
23. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
24. Matus A (2005) Growth of dendritic spines: a continuing story. Curr Opin Neurobiol 15:67-72.
25. 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.
26. Nie Z, Hirsch DS, Randazzo PA (2003) Arf and its many interactors. Curr Opin Cell Biol 15:396-404.
27. Nimchinsky EA, Sabatini BL, Svoboda K (2002) Structure and function of dendritic spines. Annu Rev Physiol 64:313-353.
28. Okabe S, Miwa A, Okado H (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21:6105-6114.
29. Papa M, Segal M (1996) Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience 71:1005-1011.
30. Parnass Z, Tashiro A, Yuste R (2000) Analysis of spine morphological plasticity in developing hippocampal pyramidal neurons. Hippocampus 10:561-568.
31. Peng J, Kim MJ, Cheng D, Duong DM, Gygi SP, Sheng M (2004) Semi-quantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J Biol Chem 279:21003-21011.
32. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL (2003) Rapid induction of dendritic spine morphogenesis by transsynaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
33. Perletti L, Talarico D, Trecca D, Ronchetti D, Fracchiolla NS, Maiolo AT, Neri A (1997) Identification of a novel gene, PSD, adjacent to NFKB2/lyt-10, which contains Sec7 and pleckstrin-homology domains. Genomics 46:251-259.
34. Peters PJ, Hsu VW, Ooi CE, Finazzi D, Teal SB, Oorschot V, Donaldson JG, Klausner RD (1995) Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J Cell Biol 128:1003-1017.
35. Pilpel Y, Segal M (2004) Activation of PKC induces rapid morphological plasticity in dendrites of hippocampal neurons via Rac and Rho-dependent mechanisms. Eur J Neurosci 19:3151-3164.
36. Portera-Cailliau C, Pan DT, Yuste R (2003) Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J Neurosci 23:7129-7142.
37. Sakagami H, Matsuya S, Nishimura H, Suzuki R, Kondo H (2004) Somatodendritic localization of the mRNA for EFA6A, a guanine nucleotide exchange protein for ARF6, in rat hippocampus and its involvement in dendritic formation. Eur J Neurosci 19:863-870.
38. Santy LC (2002) Characterization of a fast cycling ADP-ribosylation factor 6 mutant. J Biol Chem 277:40185-40188.
39. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284.
40. Someya A, Sata M, Takeda K, Pacheco-Rodriguez G, Ferrans VJ, Moss J, Vaughan M (2001) ARF-GEP(100), a guanine nucleotide-exchange protein for ADP-ribosylation factor 6. Proc Natl Acad Sci USA 98:2413-2418.
41. Suzuki I, Owada Y, Suzuki R, Yoshimoto T, Kondo H (2001) Localization of mRNAs for six ARFs (ADP-ribosylation factors) in the brain of developing and adult rats and changes in the expression in the hypoglossal nucleus after its axotomy. Brain Res Mol Brain Res 88:124-134.
42. Suzuki I, Owada Y, Suzuki R, Yoshimoto T, Kondo H (2002) Localization of mRNAs for subfamily of guanine nucleotide-exchange proteins (GEP) for ARFs (ADP-ribosylation factors) in the brain of developing and mature rats under normal and postaxotomy conditions. Brain Res Mol Brain Res 98:41-50.
43. 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.
44. 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.
45. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761-789.
46. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.
47. Yuste R, Bonhoeffer T (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24-34.
48. Zhang H, Webb DJ, Asmussen H, Horwitz AF (2003) Synapse formation is regulated by the signaling adaptor GIT1. J Cell Biol 161:131-142.
49. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.