Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

J. Cell Biol. 153 (2): 351-366

Copyright © 2001 by the Rockefeller University Press.


Original Article

Mammalian Abp1, a Signal-Responsive F-Actin–Binding Protein, Links the Actin Cytoskeleton to Endocytosis via the Gtpase Dynamin

Michael M. Kesselsa, Åsa E.Y. Engqvist-Goldsteinb, David G. Drubinb, , and Britta Qualmanna

a Department of Neurochemistry and Molecular Biology, Leibniz Institute for Neurobiology, D-39008 Magdeburg, Germany
b Department of Molecular and Cell Biology, University of California, Berkeley, California 94720-3202
Department of Neurochemistry and Molecular Biology, Leibniz Institute for Neurobiology, Postfach 1860, D-39008 Magdeburg, Germany.49 391 6263 22949 391 6263 225

kessels{at}ifn-magdeburg.de

Abstract: The actin cytoskeleton has been implicated in endocytosis, yet few molecular links to the endocytic machinery have been established. Here we show that the mammalian F-actin–binding protein Abp1 (SH3P7/HIP-55) can functionally link the actin cytoskeleton to dynamin, a GTPase that functions in endocytosis. Abp1 binds directly to dynamin in vitro through its SH3 domain. Coimmunoprecipitation and colocalization studies demonstrated the in vivo relevance of this interaction. In neurons, mammalian Abp1 and dynamin colocalized at actin-rich sites proximal to the cell body during synaptogenesis. In fibroblasts, mAbp1 appeared at dynamin-rich sites of endocytosis upon growth factor stimulation. To test whether Abp1 functions in endocytosis, we overexpressed several Abp1 constructs in Cos-7 cells and assayed receptor-mediated endocytosis. While overexpression of Abp1's actin-binding modules did not interfere with endocytosis, overexpression of the SH3 domain led to a potent block of transferrin uptake. This implicates the Abp1/dynamin interaction in endocytic function. The endocytosis block was rescued by cooverexpression of dynamin. Since the addition of the actin-binding modules of Abp1 to the SH3 domain construct also fully restored endocytosis, Abp1 may support endocytosis by combining its SH3 domain interactions with cytoskeletal functions in response to signaling cascades converging on this linker protein.

Key Words: actin cytoskeleton • dynamin • endocytosis • SH3P7 • neuronal plasticity



Abbreviations used in this paper: ADF-H, actin-depolymerizing factor homology; GFP, green fluorescent protein; GST, glutathione-S-transferase; HA, hemagglutinin; HEK, human endothelial kidney; SH3, Src homology 3.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Regulation of glutamate receptor internalization by the spine cytoskeleton is mediated by its PKA-dependent association with CPG2.
S. Loebrich, B. Djukic, Z. J. Tong, J. R. Cottrell, G. G. Turrigiano, and E. Nedivi (2013)
PNAS 110, E4548-E4556
   Abstract »    Full Text »    PDF »
FMRP regulates actin filament organization via the armadillo protein p0071.
A. Nolze, J. Schneider, R. Keil, M. Lederer, S. Huttelmaier, M. M. Kessels, B. Qualmann, and M. Hatzfeld (2013)
RNA 19, 1483-1496
   Abstract »    Full Text »    PDF »
PakB binds to the SH3 domain of Dictyostelium Abp1 and regulates its effects on cell polarity and early development.
Y. Yang, M. d. l. Roche, S. W. Crawley, Z. Li, E. Furmaniak-Kazmierczak, and G. P. Cote (2013)
Mol. Biol. Cell 24, 2216-2227
   Abstract »    Full Text »    PDF »
The Actin Nucleator Cobl Is Crucial for Purkinje Cell Development and Works in Close Conjunction with the F-Actin Binding Protein Abp1.
N. Haag, L. Schwintzer, R. Ahuja, N. Koch, J. Grimm, H. Heuer, B. Qualmann, and M. M. Kessels (2012)
J. Neurosci. 32, 17842-17856
   Abstract »    Full Text »    PDF »
The Importance of Conserved Features of Yeast Actin-Binding Protein 1 (Abp1p): The Conditional Nature of Essentiality.
B. Garcia, E. J. Stollar, and A. R. Davidson (2012)
Genetics 191, 1199-1211
   Abstract »    Full Text »    PDF »
The Mammalian Actin-Binding Protein 1 Is Critical for Spreading and Intraluminal Crawling of Neutrophils under Flow Conditions.
I. Hepper, J. Schymeinsky, L. T. Weckbach, S. M. Jakob, D. Frommhold, M. Sixt, M. Laschinger, M. Sperandio, and B. Walzog (2012)
J. Immunol. 188, 4590-4601
   Abstract »    Full Text »    PDF »
Src-mediated phosphorylation of mammalian Abp1 (DBNL) regulates podosome rosette formation in transformed fibroblasts.
L. R. Boateng, C. L. Cortesio, and A. Huttenlocher (2012)
J. Cell Sci. 125, 1329-1341
   Abstract »    Full Text »    PDF »
Endocytosis and Signaling: Cell Logistics Shape the Eukaryotic Cell Plan.
S. Sigismund, S. Confalonieri, A. Ciliberto, S. Polo, G. Scita, and P. P. Di Fiore (2012)
Physiol Rev 92, 273-366
   Abstract »    Full Text »    PDF »
Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I.
D. Koch, I. Spiwoks-Becker, V. Sabanov, A. Sinning, T. Dugladze, A. Stellmacher, R. Ahuja, J. Grimm, S. Schuler, A. Muller, et al. (2011)
EMBO J. 30, 4955-4969
   Abstract »    Full Text »    PDF »
Piccolo Regulates the Dynamic Assembly of Presynaptic F-Actin.
C. L. Waites, S. A. Leal-Ortiz, T. F. M. Andlauer, S. J. Sigrist, and C. C. Garner (2011)
J. Neurosci. 31, 14250-14263
   Abstract »    Full Text »    PDF »
Processing and Localization of the African Swine Fever Virus CD2v Transmembrane Protein.
L. C. Goatley and L. K. Dixon (2011)
J. Virol. 85, 3294-3305
   Abstract »    Full Text »    PDF »
A Myosin IK-Abp1-PakB Circuit Acts as a Switch to Regulate Phagocytosis Efficiency.
R. Dieckmann, Y. von Heyden, C. Kistler, N. Gopaldass, S. Hausherr, S. W. Crawley, E. C. Schwarz, R. P. Diensthuber, G. P. Cote, G. Tsiavaliaris, et al. (2010)
Mol. Biol. Cell 21, 1505-1518
   Abstract »    Full Text »    PDF »
Actin-binding Protein-1 Interacts with WASp-interacting Protein to Regulate Growth Factor-induced Dorsal Ruffle Formation.
C. L. Cortesio, B. J. Perrin, D. A. Bennin, and A. Huttenlocher (2010)
Mol. Biol. Cell 21, 186-197
   Abstract »    Full Text »    PDF »
A fundamental role of mAbp1 in neutrophils: impact on {beta}2 integrin-mediated phagocytosis and adhesion in vivo.
J. Schymeinsky, R. Gerstl, I. Mannigel, K. Niedung, D. Frommhold, K. Panthel, J. Heesemann, M. Sixt, T. Quast, W. Kolanus, et al. (2009)
Blood 114, 4209-4220
   Abstract »    Full Text »    PDF »
An Ehrlichia chaffeensis Tandem Repeat Protein Interacts with Multiple Host Targets Involved in Cell Signaling, Transcriptional Regulation, and Vesicle Trafficking.
A. Wakeel, J. A. Kuriakose, and J. W. McBride (2009)
Infect. Immun. 77, 1734-1745
   Abstract »    Full Text »    PDF »
The Actin-Binding Protein Abp1 Controls Dendritic Spine Morphology and Is Important for Spine Head and Synapse Formation.
A. Haeckel, R. Ahuja, E. D. Gundelfinger, B. Qualmann, and M. M. Kessels (2008)
J. Neurosci. 28, 10031-10044
   Abstract »    Full Text »    PDF »
Actin-Binding Protein 1 Regulates B Cell Receptor-Mediated Antigen Processing and Presentation in Response to B Cell Receptor Activation.
O. O. Onabajo, M. K. Seeley, A. Kale, B. Qualmann, M. Kessels, J. Han, T.-H. Tan, and W. Song (2008)
J. Immunol. 180, 6685-6695
   Abstract »    Full Text »    PDF »
ARF1-mediated actin polymerization produces movement of artificial vesicles.
J. Heuvingh, M. Franco, P. Chavrier, and C. Sykes (2007)
PNAS 104, 16928-16933
   Abstract »    Full Text »    PDF »
Sorting Nexin 9 Interacts with Dynamin 1 and N-WASP and Coordinates Synaptic Vesicle Endocytosis.
N. Shin, S. Lee, N. Ahn, S.-A Kim, S.-G. Ahn, Z. YongPark, and S. Chang (2007)
J. Biol. Chem. 282, 28939-28950
   Abstract »    Full Text »    PDF »
Actin regulation in endocytosis.
E. Smythe and K. R. Ayscough (2006)
J. Cell Sci. 119, 4589-4598
   Abstract »    Full Text »    PDF »
Vesicle formation at the plasma membrane and trans-Golgi network: the same but different..
M. A. McNiven and H. M. Thompson (2006)
Science 313, 1591-1594
   Abstract »    Full Text »    PDF »
Syndapin Oligomers Interconnect the Machineries for Endocytic Vesicle Formation and Actin Polymerization.
M. M. Kessels and B. Qualmann (2006)
J. Biol. Chem. 281, 13285-13299
   Abstract »    Full Text »    PDF »
Dynamin as a mover and pincher during cell migration and invasion.
A. E. Kruchten and M. A. McNiven (2006)
J. Cell Sci. 119, 1683-1690
   Abstract »    Full Text »    PDF »
The Actin-depolymerizing Factor Homology and Charged/Helical Domains of Drebrin and mAbp1 Direct Membrane Binding and Localization via Distinct Interactions with Actin.
W. Xu and M. Stamnes (2006)
J. Biol. Chem. 281, 11826-11833
   Abstract »    Full Text »    PDF »
SH3P7/mAbp1 deficiency leads to tissue and behavioral abnormalities and impaired vesicle transport.
S. Connert, S. Wienand, C. Thiel, M. Krikunova, N. Glyvuk, Y. Tsytsyura, D. Hilfiker-Kleiner, J. W. Bartsch, J. Klingauf, and J. Wienands (2006)
EMBO J. 25, 1611-1622
   Abstract »    Full Text »    PDF »
Complexes of syndapin II with dynamin II promote vesicle formation at the trans-Golgi network.
M. M. Kessels, J. Dong, W. Leibig, P. Westermann, and B. Qualmann (2006)
J. Cell Sci. 119, 1504-1516
   Abstract »    Full Text »    PDF »
Abp1 regulates pseudopodium number in chemotaxing Dictyostelium cells.
Y. Wang and T. J. O'Halloran (2006)
J. Cell Sci. 119, 702-710
   Abstract »    Full Text »    PDF »
Mouse Profilin 2 Regulates Endocytosis and Competes with SH3 Ligand Binding to Dynamin 1.
R. Gareus, A. Di Nardo, V. Rybin, and W. Witke (2006)
J. Biol. Chem. 281, 2803-2811
   Abstract »    Full Text »    PDF »
Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis.
K. Tsujita, S. Suetsugu, N. Sasaki, M. Furutani, T. Oikawa, and T. Takenawa (2006)
J. Cell Biol. 172, 269-279
   Abstract »    Full Text »    PDF »
Interaction of SPIN90 with the Arp2/3 Complex Mediates Lamellipodia and Actin Comet Tail Formation.
D. J. Kim, S. H. Kim, C. S. Lim, K. Y. Choi, C. S. Park, B. H. Sung, M. G. Yeo, S. Chang, J.-K. Kim, and W. K. Song (2006)
J. Biol. Chem. 281, 617-625
   Abstract »    Full Text »    PDF »
Interaction of SPIN90 with Dynamin I and Its Participation in Synaptic Vesicle Endocytosis.
Y. Kim, S. Kim, S. Lee, S. H. Kim, Y. Kim, Z. Y. Park, W. K. Song, and S. Chang (2005)
J. Neurosci. 25, 9515-9523
   Abstract »    Full Text »    PDF »
HIP-55 Is Important for T-Cell Proliferation, Cytokine Production, and Immune Responses.
J. Han, J.-W. Shui, X. Zhang, B. Zheng, S. Han, and T.-H. Tan (2005)
Mol. Cell. Biol. 25, 6869-6878
   Abstract »    Full Text »    PDF »
EHD Proteins Associate with Syndapin I and II and Such Interactions Play a Crucial Role in Endosomal Recycling.
A. Braun, R. Pinyol, R. Dahlhaus, D. Koch, P. Fonarev, B. D. Grant, M. M. Kessels, and B. Qualmann (2005)
Mol. Biol. Cell 16, 3642-3658
   Abstract »    Full Text »    PDF »
N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits.
S. Benesch, S. Polo, F. P. L. Lai, K. I. Anderson, T. E. B. Stradal, J. Wehland, and K. Rottner (2005)
J. Cell Sci. 118, 3103-3115
   Abstract »    Full Text »    PDF »
Dynein Light Chain 1 Regulates Dynamin-mediated F-Actin Assembly during Sperm Individualization in Drosophila.
A. Ghosh-Roy, B. S. Desai, and K. Ray (2005)
Mol. Biol. Cell 16, 3107-3116
   Abstract »    Full Text »    PDF »
Structural and Functional Dissection of the Abp1 ADFH Actin-binding Domain Reveals Versatile In Vivo Adapter Functions.
O. Quintero-Monzon, A. A. Rodal, B. Strokopytov, S. C. Almo, and B. L. Goode (2005)
Mol. Biol. Cell 16, 3128-3139
   Abstract »    Full Text »    PDF »
SNX9 Regulates Dynamin Assembly and Is Required for Efficient Clathrin-mediated Endocytosis.
F. Soulet, D. Yarar, M. Leonard, and S. L. Schmid (2005)
Mol. Biol. Cell 16, 2058-2067
   Abstract »    Full Text »    PDF »
PRAM-1 Potentiates Arsenic Trioxide-induced JNK Activation.
F. M. Denis, A. Benecke, Y. Di Gioia, I. P. Touw, Y. E. Cayre, and P. G. Lutz (2005)
J. Biol. Chem. 280, 9043-9048
   Abstract »    Full Text »    PDF »
Actin Filaments Play a Critical Role in Vacuolar Trafficking at the Golgi Complex in Plant Cells.
H. Kim, M. Park, S. J. Kim, and I. Hwang (2005)
PLANT CELL 17, 888-902
   Abstract »    Full Text »    PDF »
Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex.
S. tom Dieck, W. D. Altrock, M. M. Kessels, B. Qualmann, H. Regus, D. Brauner, A. Fejtova, O. Bracko, E. D. Gundelfinger, and J. H. Brandstatter (2005)
J. Cell Biol. 168, 825-836
   Abstract »    Full Text »    PDF »
Regulation of cortactin/dynamin interaction by actin polymerization during the fission of clathrin-coated pits.
J. Zhu, K. Zhou, J.-J. Hao, J. Liu, N. Smith, and X. Zhan (2005)
J. Cell Sci. 118, 807-817
   Abstract »    Full Text »    PDF »
The Abl/Arg substrate ArgBP2/nArgBP2 coordinates the function of multiple regulatory mechanisms converging on the actin cytoskeleton.
G. Cestra, D. Toomre, S. Chang, and P. De Camilli (2005)
PNAS 102, 1731-1736
   Abstract »    Full Text »    PDF »
Cortactin and dynamin are required for the clathrin-independent endocytosis of {gamma}c cytokine receptor.
N. Sauvonnet, A. Dujeancourt, and A. Dautry-Varsat (2005)
J. Cell Biol. 168, 155-163
   Abstract »    Full Text »    PDF »
The yeast dynamin-related GTPase Vps1p functions in the organization of the actin cytoskeleton via interaction with Sla1p.
X. Yu and M. Cai (2004)
J. Cell Sci. 117, 3839-3853
   Abstract »    Full Text »    PDF »
The syndapin protein family: linking membrane trafficking with the cytoskeleton.
M. M. Kessels and B. Qualmann (2004)
J. Cell Sci. 117, 3077-3086
   Abstract »    Full Text »    PDF »
Recruitment of the Actin-binding Protein HIP-55 to the Immunological Synapse Regulates T Cell Receptor Signaling and Endocytosis.
S. Le Bras, I. Foucault, A. Foussat, C. Brignone, O. Acuto, and M. Deckert (2004)
J. Biol. Chem. 279, 15550-15560
   Abstract »    Full Text »    PDF »
RNAi-mediated Hip1R Silencing Results in Stable Association between the Endocytic Machinery and the Actin Assembly Machinery.
A. E. Y. Engqvist-Goldstein, C. X. Zhang, S. Carreno, C. Barroso, J. E. Heuser, and D. G. Drubin (2004)
Mol. Biol. Cell 15, 1666-1679
   Abstract »    Full Text »    PDF »
Linkage of the Actin Cytoskeleton to the Postsynaptic Density via Direct Interactions of Abp1 with the ProSAP/Shank Family.
B. Qualmann, T. M. Boeckers, M. Jeromin, E. D. Gundelfinger, and M. M. Kessels (2004)
J. Neurosci. 24, 2481-2495
   Abstract »    Full Text »    PDF »
The CD2v protein of African swine fever virus interacts with the actin-binding adaptor protein SH3P7.
P. C. Kay-Jackson, L. C. Goatley, L. Cox, J. E. Miskin, R. M. E. Parkhouse, J. Wienands, and L. K. Dixon (2004)
J. Gen. Virol. 85, 119-130
   Abstract »    Full Text »    PDF »
The SH3 Domain-containing Adaptor HIP-55 Mediates c-Jun N-terminal Kinase Activation in T Cell Receptor Signaling.
J. Han, R. Kori, J.-W. Shui, Y.-R. Chen, Z. Yao, and T.-H. Tan (2003)
J. Biol. Chem. 278, 52195-52202
   Abstract »    Full Text »    PDF »
Fgd1, the Cdc42 GEF responsible for Faciogenital Dysplasia, directly interacts with cortactin and mAbp1 to modulate cell shape.
P. Hou, L. Estrada, A. W. Kinley, J. T. Parsons, A. B. Vojtek, and J. L. Gorski (2003)
Hum. Mol. Genet. 12, 1981-1993
   Abstract »    Full Text »    PDF »
An interaction between Sla1p and Sla2p plays a role in regulating actin dynamics and endocytosis in budding yeast.
C. W. Gourlay, H. Dewar, D. T. Warren, R. Costa, N. Satish, and K. R. Ayscough (2003)
J. Cell Sci. 116, 2551-2564
   Abstract »    Full Text »    PDF »
Colocalization of synapsin and actin during synaptic vesicle recycling.
O. Bloom, E. Evergren, N. Tomilin, O. Kjaerulff, P. Low, L. Brodin, V. A. Pieribone, P. Greengard, and O. Shupliakov (2003)
J. Cell Biol. 161, 737-747
   Abstract »    Full Text »    PDF »
Interactions between Piccolo and the Actin/Dynamin-binding Protein Abp1 Link Vesicle Endocytosis to Presynaptic Active Zones.
S. D. Fenster, M. M. Kessels, B. Qualmann, W. J. Chung, J. Nash, E. D. Gundelfinger, and C. C. Garner (2003)
J. Biol. Chem. 278, 20268-20277
   Abstract »    Full Text »    PDF »
Cortactin Is a Component of Clathrin-Coated Pits and Participates in Receptor-Mediated Endocytosis.
H. Cao, J. D. Orth, J. Chen, S. G. Weller, J. E. Heuser, and M. A. McNiven (2003)
Mol. Cell. Biol. 23, 2162-2170
   Abstract »    Full Text »    PDF »
Dynamin Participates in Focal Extracellular Matrix Degradation by Invasive Cells.
M. Baldassarre, A. Pompeo, G. Beznoussenko, C. Castaldi, S. Cortellino, M. A. McNiven, A. Luini, and R. Buccione (2003)
Mol. Biol. Cell 14, 1074-1084
   Abstract »    Full Text »    PDF »
Actin-rich Spherical Extrusion Induced in Okadaic Acid-treated K562 Cells by Crosslinking of Membrane Microdomains.
T. Baba, K. Udaka, N. Terada, H. Ueda, Y. Fujii, S. Ohno, and S. B. Sato (2003)
Journal of Histochemistry & Cytochemistry 51, 245-252
   Abstract »    Full Text »    PDF »
Syndapins integrate N-WASP in receptor-mediated endocytosis.
M. M. Kessels and B. Qualmann (2002)
EMBO J. 21, 6083-6094
   Abstract »    Full Text »    PDF »
Structural Conservation between the Actin Monomer-binding Sites of Twinfilin and Actin-depolymerizing Factor (ADF)/Cofilin.
V. O. Paavilainen, M. C. Merckel, S. Falck, P. J. Ojala, E. Pohl, M. Wilmanns, and P. Lappalainen (2002)
J. Biol. Chem. 277, 43089-43095
   Abstract »    Full Text »    PDF »
Novel Proteins Linking the Actin Cytoskeleton to the Endocytic Machinery in Saccharomyces cerevisiae.
H. Dewar, D. T. Warren, F. C. Gardiner, C. G. Gourlay, N. Satish, M. R. Richardson, P. D. Andrews, and K. R. Ayscough (2002)
Mol. Biol. Cell 13, 3646-3661
   Abstract »    Full Text »    PDF »
Scd5p and Clathrin Function Are Important for Cortical Actin Organization, Endocytosis, and Localization of Sla2p in Yeast.
K. R. Henry, K. D'Hondt, J. Chang, T. Newpher, K. Huang, R. T. Hudson, H. Riezman, and S. K. Lemmon (2002)
Mol. Biol. Cell 13, 2607-2625
   Abstract »    Full Text »    PDF »
H-Ras Signaling and K-Ras Signaling Are Differentially Dependent on Endocytosis.
S. Roy, B. Wyse, and J. F. Hancock (2002)
Mol. Cell. Biol. 22, 5128-5140
   Abstract »    Full Text »    PDF »
Cyclase-associated proteins: CAPacity for linking signal transduction and actin polymerization.
A. V. HUBBERSTEY and E. P. MOTTILLO (2002)
FASEB J 16, 487-499
   Abstract »    Full Text »    PDF »
Dynamin at actin tails.
E. Lee and P. De Camilli (2002)
PNAS 99, 161-166
   Abstract »    Full Text »    PDF »
The large GTPase dynamin regulates actin comet formation and movement in living cells.
J. D. Orth, E. W. Krueger, H. Cao, and M. A. McNiven (2002)
PNAS 99, 167-172
   Abstract »    Full Text »    PDF »
The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro.
A. E.Y. Engqvist-Goldstein, R. A. Warren, M. M. Kessels, J. H. Keen, J. Heuser, and D. G. Drubin (2001)
J. Cell Biol. 154, 1209-1224
   Abstract »    Full Text »    PDF »
Golgi Vesicle Proteins Are Linked to the Assembly of an Actin Complex Defined by mAbp1.
R. V. Fucini, J.-L. Chen, C. Sharma, M. M. Kessels, and M. Stamnes (2002)
Mol. Biol. Cell 13, 621-631
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882