The Neuronal Arf GAP Centaurin Alpha1 Modulates Dendritic Differentiation

Overview

Journal J Cell Sci

Specialty Cell Biology

Date 2007 Jul 20

PMID 17635995

Citations 21

Authors

Carlene D Moore

Erin E Thacker

Jennifer Larimore

David Gaston

Alison Underwood

Brian Kearns

Sean I Patterson

Trevor Jackson

Chris Chapleau

Lucas Pozzo-Miller

Anne Theibert

Affiliations

Soon will be listed here.

Abstract

Centaurin alpha1 is an Arf GTPase-activating protein (GAP) that is highly expressed in the nervous system. In the current study, we show that endogenous centaurin alpha1 protein is localized in the synaptosome fraction, with peak expression in early postnatal development. In cultured dissociated hippocampal neurons, centaurin alpha1 localizes to dendrites, dendritic spines and the postsynaptic region. siRNA-mediated knockdown of centaurin alpha1 levels or overexpression of a GAP-inactive mutant of centaurin alpha1 leads to inhibition of dendritic branching, dendritic filopodia and spine-like protrusions in dissociated hippocampal neurons. Overexpression of wild-type centaurin alpha1 in cultured hippocampal neurons in early development enhances dendritic branching, and increases dendritic filopodia and lamellipodia. Both filopodia and lamellipodia have been implicated in dendritic branching and spine formation. Following synaptogenesis in cultured neurons, wild-type centaurin alpha1 expression increases dendritic filopodia and spine-like protrusions. Expression of a GAP-inactive mutant diminishes spine density in CA1 pyramidal neurons within cultured organotypic hippocampal slice cultures. These data support the conclusion that centaurin alpha1 functions through GAP-dependent Arf regulation of dendritic branching and spines that underlie normal dendritic differentiation and development.

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References

Kohrmann M, Haubensak W, Hemraj I, Kaether C, Lessmann V, Kiebler M . Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J Neurosci Res. 1999; 58(6):831-5. View

Donaldson J, Jackson C . Regulators and effectors of the ARF GTPases. Curr Opin Cell Biol. 2000; 12(4):475-82. DOI: 10.1016/s0955-0674(00)00119-8. View

Jackson T, Kearns B, Theibert A . Cytohesins and centaurins: mediators of PI 3-kinase-regulated Arf signaling. Trends Biochem Sci. 2000; 25(10):489-95. DOI: 10.1016/s0968-0004(00)01644-3. View

Zhai R, Becker B, Gundelfinger E, Ziv N, Garner C . Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron. 2001; 29(1):131-43. DOI: 10.1016/s0896-6273(01)00185-4. View

Dubois T, Kerai P, Zemlickova E, Howell S, Jackson T, Venkateswarlu K . Casein kinase I associates with members of the centaurin-alpha family of phosphatidylinositol 3,4,5-trisphosphate-binding proteins. J Biol Chem. 2001; 276(22):18757-64. DOI: 10.1074/jbc.M010005200. View

Tyler W . BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci. 2001; 21(12):4249-58. PMC: 2806848. View

Kaech S, Parmar H, Roelandse M, Bornmann C, MATUS A . Cytoskeletal microdifferentiation: a mechanism for organizing morphological plasticity in dendrites. Proc Natl Acad Sci U S A. 2001; 98(13):7086-92. PMC: 34627. DOI: 10.1073/pnas.111146798. View

Santy L, Casanova J . Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J Cell Biol. 2001; 154(3):599-610. PMC: 2196419. DOI: 10.1083/jcb.200104019. View

Bresler T, Ramati Y, Zamorano P, Zhai R, Garner C, Ziv N . The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol Cell Neurosci. 2001; 18(2):149-67. DOI: 10.1006/mcne.2001.1012. View

10.

Katso R, Okkenhaug K, Ahmadi K, White S, Timms J, Waterfield M . Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu Rev Cell Dev Biol. 2001; 17:615-75. DOI: 10.1146/annurev.cellbio.17.1.615. View

11.

Klimaschewski L, Nindl W, Pimpl M, Waltinger P, Pfaller K . Biolistic transfection and morphological analysis of cultured sympathetic neurons. J Neurosci Methods. 2001; 113(1):63-71. DOI: 10.1016/s0165-0270(01)00473-3. View

12.

Randazzo P, Nie Z, Miura K, Hsu V . Molecular aspects of the cellular activities of ADP-ribosylation factors. Sci STKE. 2001; 2000(59):re1. DOI: 10.1126/stke.2000.59.re1. View

13.

Sedehizade F, Hanck T, Stricker R, Horstmayer A, Bernstein H, Reiser G . Cellular expression and subcellular localization of the human Ins(1,3,4,5)P(4)-binding protein, p42(IP4), in human brain and in neuronal cells. Brain Res Mol Brain Res. 2002; 99(1):1-11. DOI: 10.1016/s0169-328x(01)00335-7. View

14.

Hernandez-Deviez D, Casanova J, Wilson J . Regulation of dendritic development by the ARF exchange factor ARNO. Nat Neurosci. 2002; 5(7):623-4. DOI: 10.1038/nn865. View

15.

Venkateswarlu K, Brandom K, Lawrence J . Centaurin-alpha1 is an in vivo phosphatidylinositol 3,4,5-trisphosphate-dependent GTPase-activating protein for ARF6 that is involved in actin cytoskeleton organization. J Biol Chem. 2003; 279(8):6205-8. DOI: 10.1074/jbc.C300482200. View

16.

Sakagami H, Matsuya S, Nishimura H, Suzuki R, Kondo H . 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. 2004; 19(4):863-70. DOI: 10.1111/j.0953-816x.2004.03195.x. View

17.

Alonso M, Medina J, Pozzo-Miller L . ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem. 2004; 11(2):172-8. PMC: 379687. DOI: 10.1101/lm.67804. View

18.

Gauthier-Campbell C, Bredt D, Murphy T, El-Husseini A . Regulation of dendritic branching and filopodia formation in hippocampal neurons by specific acylated protein motifs. Mol Biol Cell. 2004; 15(5):2205-17. PMC: 404016. DOI: 10.1091/mbc.e03-07-0493. View

19.

Rodgers E, Theibert A . Functions of PI 3-kinase in development of the nervous system. Int J Dev Neurosci. 2002; 20(3-5):187-97. DOI: 10.1016/s0736-5748(02)00047-3. View

20.

Uylings H, van Pelt J . Measures for quantifying dendritic arborizations. Network. 2002; 13(3):397-414. View