Crossref journal-article
Rockefeller University Press
The Journal of Cell Biology (291)
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.

Bibliography

Kessels, M. M., Engqvist-Goldstein, Å. E. Y., Drubin, D. G., & Qualmann, B. (2001). Mammalian Abp1, a Signal-Responsive F-Actin–Binding Protein, Links the Actin Cytoskeleton to Endocytosis via the Gtpase Dynamin. The Journal of Cell Biology, 153(2), 351–366.

Authors 4
  1. Michael M. Kessels (first)
  2. Åsa E.Y. Engqvist-Goldstein (additional)
  3. David G. Drubin (additional)
  4. Britta Qualmann (additional)
References 55 Referenced 196
  1. 10.1074/jbc.274.3.1185 / J. Biol. Chem / Src-mediated tyrosine phosphorylation of dynamin is required for beta2-adrenergic receptor internalization and mitogen-activated protein kinase signaling by Ahn (1999)
  2. 10.1016/S0959-4388(00)00097-0 / Curr. Opin. Neurobiol / Sequential steps in clathrin-mediated synaptic vesicle endocytosis by Brodin (2000)
  3. 10.1091/mbc.9.9.2595 / Mol. Biol. Cell / Differential distribution of dynamin isoforms in mammalian cells by Cao (1998)
  4. 10.1038/356340a0 / Nature / C. elegans cell-signaling gene sem-5 encodes a protein with SH2 and SH3 domains by Clark (1992)
  5. 10.1083/jcb.127.4.915 / J. Cell Biol / Induction of mutant dynamin specifically blocks endocytic coated vesicle formation by Damke (1994)
  6. {'key': '2023072902565099400_delaRocheandCote1999', 'first-page': '165a', 'article-title': 'Characterization of a dyctiostelium homolog of yeast ABP1 that interacts with the N-terminus of myosin I heavy chain kinase', 'volume': '10', 'author': 'de la Roche', 'year': '1999', 'journal-title': 'Mol. Biol. Cell.'} / Mol. Biol. Cell. / Characterization of a dyctiostelium homolog of yeast ABP1 that interacts with the N-terminus of myosin I heavy chain kinase by de la Roche (1999)
  7. 10.1083/jcb.107.6.2551 / J. Cell Biol. / Yeast actin-binding proteinsevidence for a role in morphogenesis by Drubin (1988)
  8. 10.1016/S0962-8924(99)01710-9 / Trends Cell Biol / Regulation of endocytic traffic by rho family GTPases by Ellis (2000)
  9. 10.1083/jcb.147.7.1503 / J. Cell Biol / An actin-binding protein of the Sla2/Huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles by Engqvist-Goldstein (1999)
  10. 10.1074/jbc.274.48.33945 / J. Biol. Chem / A novel src homology 3 domain-containing adaptor protein, HIP-55, that interacts with hematopoietic progenitor kinase 1 by Ensenat (1999)
  11. 10.1038/44860 / Nature / Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling by Frischknecht (1999)
  12. 10.1034/j.1600-0854.2000.010208.x / Traffic / Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells by Fujimoto (2000)
  13. 10.1038/8971 / Nat. Cell Biol / Spatial control of coated-pit dynamics in living cells by Gaidarov (1999)
  14. 10.1242/jcs.111.8.1031 / J. Cell Sci / Endocytic internalization in yeast and animal cellssimilar and different by Geli (1998)
  15. {'key': '2023072902565099400_Goodeetal2000', 'first-page': '378a', 'article-title': 'Reconstitution of actin assembly in Saccharomyces cerevisiae extracts and identification of new regulators of the Arp2/3 complex', 'volume': '11', 'author': 'Goode', 'year': '2000', 'journal-title': 'Mol. Biol. Cell.'} / Mol. Biol. Cell. / Reconstitution of actin assembly in Saccharomyces cerevisiae extracts and identification of new regulators of the Arp2/3 complex by Goode (2000)
  16. {'key': '2023072902565099400_GoslinandBanker1991', 'first-page': '251', 'article-title': 'Rat hippocampal neurons in low-density culture', 'volume-title': 'Culturing Nerve Cells', 'author': 'Goslin', 'year': '1991'} / Culturing Nerve Cells / Rat hippocampal neurons in low-density culture by Goslin (1991)
  17. 10.1016/S0092-8674(05)80081-9 / Cell / The GTPase dynamin binds to and is activated by a subset of SH3 domains by Gout (1993)
  18. 10.1098/rstb.1999.0378 / Philos. Trans. R. Soc. Lond. B Biol. Sci / Synapsins as regulators of neurotransmitter release by Hilfiker (1999)
  19. 10.1083/jcb.122.3.635 / J. Cell Biol. / Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae by Holtzman (1993)
  20. 10.1091/mbc.11.1.393 / Mol. Biol. Cell / Association of mouse actin-binding protein 1 (mAbp1/SH3P7), an Src kinase target, with dynamic regions of the cortical actin cytoskeleton in response to Rac1 activation by Kessels (2000)
  21. 10.1091/mbc.9.8.1951 / Mol. Biol. Cell / The ADF homology (ADF-H) domaina highly exploited actin-binding module by Lappalainen (1998)
  22. 10.1128/MCB.19.2.1539 / Mol. Cell. Biol / SH3P7 is a cytoskeleton adapter protein and is coupled to signal transduction from lymphocyte antigen receptors by Larbolette (1999)
  23. 10.1091/mbc.8.2.367 / Mol. Biol. Cell / Evidence for physical and functional interactions among two Saccharomyces cerevisiae SH3 domain proteins, an adenylyl cyclase-associated protein and the actin cytoskeleton by Lila (1997)
  24. 10.1093/emboj/17.15.4346 / EMBO (Eur. Mol. Biol. Organ.) J / A new method for isolating tyrosine kinase substrates used to identify Fish, an SH3 and PX domain-containing protein, and Src substrate by Lock (1998)
  25. 10.1016/S0896-6273(00)81067-3 / Neuron / Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization by Man (2000)
  26. 10.1073/pnas.79.23.7590 / Proc. Natl. Acad. Sci. USA / High actin concentration in brain dendritic spines and postsynaptic densities by Matus (1982)
  27. {'key': '2023072902565099400_McNivenetal2000', 'first-page': '115', 'article-title': 'The dynamin family of mechanoenzymespinching in new places', 'volume': '25', 'author': 'McNiven', 'year': '2000', 'journal-title': 'Trends Cell Biol.'} / Trends Cell Biol. / The dynamin family of mechanoenzymespinching in new places by McNiven (2000)
  28. 10.1016/S0021-9258(18)43787-8 / J. Biol. Chem / p145, a major Grb2-binding protein in brain, is co-localized with dynamin in nerve terminals where it undergoes activity-dependent dephosphorylation by McPherson (1994)
  29. 10.1038/9048 / Nat. Cell. Biol / Endocytic vesicles move at the tips of actin tails in cultured mast cells by Merrifield (1999)
  30. 10.1074/jbc.272.43.27239 / J. Biol. Chem / Synaptojanin forms two separate complexes in the nerve terminal. Interactions with endophilin and amphiphysin by Micheva (1997)
  31. 10.1016/S0169-328X(99)00213-2 / Brain Res. Mol. Brain Res / Modulation of gene expression following long-term synaptic depression in the striatum by Napolitano (1999)
  32. 10.1083/jcb.150.2.377 / J. Cell Biol / A functional link between dynamin and the actin cytoskeleton at podosomes by Ochoa (2000)
  33. 10.1083/jcb.148.5.1047 / J. Cell Biol / Syndapin isoforms participate in receptor-mediated endocytosis and actin organization by Qualmann (2000)
  34. 10.1091/mbc.10.2.501 / Mol. Biol. Cell / Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein by Qualmann (1999)
  35. 10.1083/jcb.150.5.F111 / J. Cell Biol. / Molecular links between endocytosis and the actin cytoskeleton by Qualmann (2000)
  36. 10.1083/jcb.120.1.55 / J. Cell Biol. / End3 and end4two mutations defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae by Raths (1993)
  37. 10.1073/pnas.94.16.8569 / Proc. Natl. Acad. Sci. USA / The SH3p4/Sh3p8/SH3p13 protein familybinding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain by Ringstad (1997)
  38. 10.1074/jbc.273.30.19108 / J. Biol. Chem / Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin by Roos (1998)
  39. 10.1016/S0960-9822(00)80087-1 / Curr. Biol / The endocytic machinery in nerve terminals surrounds sites of exocytosis by Roos (1999)
  40. 10.1016/S0960-9822(00)00384-5 / Curr. Biol / Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3 by Rozelle (2000)
  41. 10.1002/j.1460-2075.1994.tb06547.x / EMBO (Eur. Mol. Biol. Organ.) J / Growth factor-induced binding of dynamin to signal transduction proteins involves sorting to distinct and separate proline-rich dynamin sequences by Scaife (1994)
  42. 10.1034/j.1600-0854.2000.010503.x / Traffic / Garrotes, springs, ratchets, and whipsputting dynamin models to the test by Sever (2000)
  43. 10.1038/10091 / Nat. Cell. Biol / SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation by Simpson (1999)
  44. 10.1038/nbt0696-741 / Nat. Biotechnol / Cloning of ligand targetssystematic isolation of SH3 domain-containing proteins by Sparks (1996)
  45. 10.1038/374186a0 / Nature. / Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals by Takei (1995)
  46. 10.1083/jcb.148.3.519 / J. Cell Biol. / Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP by Taunton (2000)
  47. 10.1074/jbc.271.46.28727 / J. Biol. Chem. / Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits by Tebar (1996)
  48. 10.1074/jbc.272.48.30185 / J. Biol. Chem / Overexpression of cellular Src in fibroblasts enhances endocytic internalization of epidermal growth factor receptor by Ware (1997)
  49. 10.1016/S0955-0674(98)80067-7 / Curr. Opin. Cell Biol / Protein traffic in the yeast endocytic and vacuolar protein sorting pathways by Wendland (1998)
  50. 10.1091/mbc.8.11.2291 / Mol. Biol. Cell / End4p/S1a2p interacts with actin-associated proteins for endocytosis in Saccharomyces cerevisiae by Wesp (1997)
  51. 10.1016/S0166-2236(98)01264-8 / Trends Neurosci / The amphiphysin family of proteins and their role in endocytosis at the synapse by Wigge (1998)
  52. 10.1016/S0960-9822(06)00254-5 / Curr. Biol. / Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain by Wigge (1997)
  53. 10.1016/S0092-8674(00)80578-4 / Cell / EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake by Wilde (1999)
  54. 10.1093/emboj/17.4.967 / EMBO (Eur. Mol. Biol. Organ.) J / In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly by Witke (1998)
  55. 10.1074/jbc.273.47.31401 / J. Biol. Chem / Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains by Yamabhai (1998)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 12:46 p.m.)
Deposited 2 years ago (July 28, 2023, 10:59 p.m.)
Indexed 1 day, 10 hours ago (Aug. 27, 2025, 12:09 p.m.)
Issued 24 years, 4 months ago (April 16, 2001)
Published 24 years, 4 months ago (April 16, 2001)
Published Online 24 years, 4 months ago (April 16, 2001)
Published Print 24 years, 4 months ago (April 16, 2001)
Funders 0

None

@article{Kessels_2001, title={Mammalian Abp1, a Signal-Responsive F-Actin–Binding Protein, Links the Actin Cytoskeleton to Endocytosis via the Gtpase Dynamin}, volume={153}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.153.2.351}, DOI={10.1083/jcb.153.2.351}, number={2}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Kessels, Michael M. and Engqvist-Goldstein, Åsa E.Y. and Drubin, David G. and Qualmann, Britta}, year={2001}, month=apr, pages={351–366} }