The syndapin protein family: Linking membrane trafficking with the cytoskeleton

Journal of Cell Science

Volumn 117, Issue 15, 2004, Pages 3077-3086

  Kessels, Michael M ^a   Qualmann, Britta ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Actin polymerization; Syndapin; Vesicle trafficking

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; CELL PROTEIN; CYTOSKELETON PROTEIN; DYNAMIN; ISOPROTEIN; MEMBRANE PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; OLIGOMER; PROTEIN SYNDAPIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; CELL MEMBRANE; CELL VACUOLE; ENDOCYTOSIS; EUKARYOTIC CELL; GENETIC CONSERVATION; GOLGI COMPLEX; HUMAN; MEMBRANE TRANSPORT; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; REVIEW; RNA SPLICING; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; UNINDEXED SEQUENCE;

ACTIN-RELATED PROTEIN 2; ACTIN-RELATED PROTEIN 3; ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CELL MEMBRANE; CHICKENS; CYTOSKELETAL PROTEINS; CYTOSKELETON; ENDOCYTOSIS; GOLGI APPARATUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PHOSPHOPROTEINS; PHYLOGENY; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEINS; RATS; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EUKARYOTA; VESPIDAE;

EID: 4344619558     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01290     Document Type: Review

References (65)

1. Beck, K. A. and Nelson, W. J. (1998). A spectrin membrane skeleton of the Golgi complex. Biochim. Biophys. Acta. Mol. Cell Res. 1404, 153-160.
2. Braun, A., Pinyol i Agelet, R., Dahlhaus, R., Grant, B. D., Kessels, M. M. and Qualmann, B. (2004). Interaction of EHD proteins with syndapin I and II, a basis for functional connections between membrane trafficking and the actin cytoskeleton. Eur. J. Cell Biol. 83 Suppl. 54, 81 (Abstract MS10-3).
3. Cao, H., Orth, J. D., Chen, J., Weller, S. G., Heuser, J. E. and McNiven, M. A. (2003). Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis. Mol. Biol. Cell 23, 2162-2170.
4. Cousin, H., Gaultier, A., Bleux, C., Darribère, T. and Alfandari, D. (2000). PACSIN2 is a regulator of the metalloprotease/disintegrin ADAM13. Dev. Biol. 227, 197-210.
5. Cremona, O., di Paolo, G., Wenk, M. R., Lüthi, A., Kim, W. T., Takei, K., Daniell, L., Nemoto, Y., Shears, S. B., Flavell, R. A. et al. (1999). Essential role of phosphomositide metabolism in synaptic vesicle recycling. Cell 99, 179-188.
6. da Costa, S. R., Sou, E., Xie, J., Yarber, F. A., Okamoto, C. T., Pidgeon, M., Kessels, M. M., Mircheff, A. K., Schechter, J. E., Qualmann, B. et al. (2003). Impairing actin filament or syndapin functions promotes accumulation of clathrin-coated vesicles at the apical plasma membrane of acinar epithelial cells. Mol. Biol. Cell 14, 4397-4413.
7. De Matteis, M. A. and Morrow, J. S. (2000). Spectrin tethers and mesh in the biosynthetic pathway. J. Cell Sci. 113, 2331-2343.
8. di Campli, A., Valderrama, F., Babià, T., de Matteis, M. A., Luini, A. and Egea, G. (1999). Morphological changes in the Golgi complex correlate with actin cytoskeleton rearrangements. Cell Motil. Cytoskeleton 43, 334-348.
9. Engqvist-Goldstein, Å. E. Y. and Drubin, D. G. (2003). Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19, 287-332.
10. Fucini, R. V., Chen, J. L., Sharma, C., Kessels, M. M. and Stamnes, M. (2002). Golgi vesicle proteins are linked to the assembly of an actin complex defined by mAbp1. Mol. Biol. Cell 13, 621-631.
11. Ghadimi, M. P., Sanzenbacher, R., Thiede, B., Wenzel, J., Jing, Q., Plomann, M., Burkhardt, A., Kabelitz, D. and Janssen, O. (2002). Identification of interaction partners of the cytosolic polyproline region of CD95 ligand (CD178). FEBS Lett. 519, 50-58.
12. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H. and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579.
13. Guilherme, A., Soriano, N. A., Bose, S., Holik, J., Bose, A., Pomerleau, D. P., Furcinitti, P., Leszyk, J., Corvera, S. and Czech, M. P. (2004). EHD2 and the novel EH-domain binding protein EHBP1 couple endocytosis to the actin cytoskeleton. J. Biol. Chem. 279, 10593-10605.
14. Gundelfinger, E. D., Kessels, M. M. and Qualmann, B. (2003). Temporal and spatial coordination of exocytosis and endocytosis. Nat. Rev. Mol. Cell. Biol. 4, 127-139.
15. Harjes, P. and Wanker, E. E. (2003). The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem. Sci. 28, 425-433.
16. Higgs, H. N. and Pollard, T. D. (2001). Regulation of actin filament network formation through Arp2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70, 649-676.
17. Hilfiker, S., Pieribone, V. A., Czernik, A. J., Kao, H. T., Augustine, G. J. and Greengard, P. (1999). Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. London B. Biol. Sci. 354, 269-279.
18. Hilton, J. M., Plomann, M., Ritter, B., Modregger, J., Freeman, H. N., Falck, J. R., Krishna, U. M. and Tobin, A. B. (2001). Phosphorylation of a synaptic vesicle-associated protein by an inositol hexakisphosphate-regulated protein kinase. J. Biol. Chem. 276, 16341-16347.
19. Hinshaw, J. E. (2000). Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16, 483-519.
20. Howard, L., Nelson, K. K., Maciewicz, R. A. and Blobel, C. P. (1999). Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J. Biol. Chem. 274, 31693-31699.
21. Janssen, O., Qian, J., Linkermann, A. and Kabelitz, D. (2003). CD95 ligand-death factor and costimulatory molecule? Cell Death Differ. 10, 1215-1225.
22. Jones, S. M., Howell, K. E., Henley, J. R., Cao, H. and McNiven, M. A. (1998). Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279, 573-577.
23. Kessels, M. M., Engqvist-Goldstein, Å. E. Y., Drubin, D. G. and Qualmann, B. (2001). Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J. Cell Biol. 153, 351-366.
24. Kessels, M. M. and Qualmann, B. (2002). Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 21, 6083-6094.
25. Kessels, M. M., Dong, J., Westermann, P. and Qualmann, B. (2003). Dynamin II and syndapin II form heterodimeric complexes promoting vesicle formation at the trans-Golgi network. Mol. Biol. Cell 14 Suppl., 377a (Abstract 2111).
26. Kim, A. S., Kakalis, L. T., Abdul-Manan, N., Liu, G. A. and Rosen, M. K. (2000). Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404, 151-158.
27. Lee, E. and de Camilli, P. (2002). Dynamin at actin tails. Proc. Natl. Acad. Sci. USA 99, 161-166.
28. Lin, S. X., Grant, B., Hirsh, D. and Maxfield, F. R. (200). Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3, 567-572.
29. Luna, A., Matas, O. B., Martínez-Menárguez, J. A., Mato, E., Durán, J. M., Ballesta, J., Way, M. and Egea, G. (2002). Regulation of protein transport from the Golgi complex to the endoplasmic reticulum by CDC42 and N-WASP. Mol. Biol. Cell 13, 866-879.
30. McFarlane, S. (2003). Metalloproteases: carving out a role in axon guidance. Neuron 37, 559-562.
31. McNiven, M. A., Kim, L., Krueger, E. W., Orth, J. D., Cao, H. and Wong, T. W. (2000). Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol. 151, 187-198.
32. Meriläinen, J., Lehto, V. P. and Wasenius, V. M. (1997). FAP52, a novel, SH3 domain-containing focal adhesion protein. J. Biol. Chem. 272, 23278-23284.
33. Merrifield, C. J., Feldman, M. E., Wan, L. and Almers, W. (2002). Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat. Cell Biol. 4, 691-698.
34. Merrifield, C. J., Qualmann, B., Kessels, M. M. and Almers, W. (2004). Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts. Eur. J. Cell Biol. 83, 13-18.
35. Miki, H., Sasaki, T., Takai, Y. and Takenawa, T. (1998). Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93-96.
36. Mise-Omata, S., Montague, B., Deckert, M., Wienands, J. and Acuto, O. (2003). Mammalian actin binding protein 1 is essential for endocytosis but not lamellipodia formation: functional analysis by RNA interference. Biochem. Biophys. Res. Commun. 301, 704-710.
37. Modregger, J., Ritter, B., Witter, B., Paulsson, M. and Plomann, M. (2000). All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J. Cell Sci. 113, 4511-4521.
38. Modregger, J., DiProspero, N. A., Charles, V., Tagle, D. A. and Plomann, M. (2002). PACSIN 1 interacts with huntingtin and is absent from synaptic varicosities in presymptomatic Huntington's disease brains. Hum. Mol. Genet. 11, 2547-2558.
39. Mori, S., Tanaka, M., Nanba, D., Nishiwaki, E., Ishiguro, H., Higashiyama, S. and Matsuura, N. (2003). PACSIN3 binds ADAM12/meltrin α and up-regulates ectodomain shedding of heparin-binding epidermal growth factor-like growth factor. J. Biol. Chem. 278, 46029-46034.
40. Morris, S. A. and Schmid, S. L. (1995). Synaptic vesicle recycling. The Ferrari of epdocytosis? Curr. Biol. 5, 113-115.
41. Müsch, A., Cohen, D., Kreitzer, G. and Rodriguez-Boulan, E. (2001). cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J. 20, 2171-2179.
42. Nikki, M., Meriläinen, J. and Lebto, V. P. (2002a). FAP52 regulates actin organization via binding to filamin. J. Biol. Chem. 277, 11432-11440.
43. Nikki, M., Meriläinen, J. and Lehto, V. P. (2002b). Focal adhesion protein FAP52 self-associates through a sequence conserved among the members of the PCH family proteins. Biochemistry 41, 6320-6329.
44. Olazabal, I. M. and Machesky, L. M. (2001). Abp1p and cortactin, new 'hand-holds' for actin. J. Cell Biol. 154, 679-682.
45. Orth, J. D. and McNiven, M. A. (2003). Dynamin at the actin-membrane interface. Curr. Opin. Cell Biol. 15, 31-39.
46. Orth, J. D., Krueger, E. W., Cao, H. and McNiven, M. A. (2002). The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc. Natl. Acad. Sci. USA 99, 167-172.
47. Plomann, M., Lange, R., Vopper, G., Cremer, H., Heinlein, U. A. O., Scheff, S., Baldwin, S. A., Leitges, M., Cramer, M., Paulsson, M. et al. (1998). PACSIN, a brain protein that is upregulated upon differentiation into neuronal cells. Eur. J. Biochem. 256, 201-211.
48. Qualmann, B. and Kelly, R. B. (2000). Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J. Cell Biol. 148, 1047-1061.
49. Qualmann, B. and Kessels, M. M. (2002). Endocytosis and the cytoskeleton. Int. Rev. Cytol. 220, 93-144.
50. Qualmann, B., Roos, J., DiGregorio, P. J. and Kelly, R. B. (1999). Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol. Biol. Cell 10, 501-513.
51. Qualmann, B., Gundelfinger, E. D. and Kessels, M. M. (2000a). Regulated function of syndapins at the interconnection of endocytosis, cytoskeletal dynamics and signal transduction. Mol. Biol. Cell 11, 216a (Abstr.).
52. Qualmann, B., Kessels, M. M. and Kelly, R. B. (2000b). Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150, F111-F116.
53. Ritter, B., Modregger, J., Paulsson, M. and Plomann, M. (1999). PACSIN 2, a novel member of the PACSIN family of cytoplasmic adapter proteins. FEBS Lett. 454, 356-362.
54. Schlöndorff, J. and Blobel, C. P. (1999). Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J. Cell Sci. 112, 3603-3617.
55. Scita, G., Nordstrom, J., Carbone, R., Tenca, P., Giardina, G., Gutkind, S., Bjarnegård, M., Betsholtz, C. and di Fiore, P. P. (1999). EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401, 290-293.
56. Sever, S., Damke, H. and Schmid, S. L. (2000). Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1, 385-392.
57. Simpson, F., Hussain, N. K., Qualmann, B., Kelly, R. B., Kay, B. K., McPherson, P. S. and Schmid, S. L. (1999). SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat. Cell Biol. 1, 119-124.
58. Stamnes, M. (2002). Regulating the actin cytoskeleton during vesicular transport. Curr. Opin. Cell Biol. 14, 428-433.
59. Sumoy, L., Pluvinet, R., Andreu, N., Estivill, X. and Escarceller, M. (2001). PACSIN 3 is a novel SH3 domain cytoplasmic adapter protein of the pacsin-syndapin-FAP52 gene family. Gene 262, 199-205.
60. Taunton, J. (2001). Actin filament nucleation by endosomes, lysosomes and secretory vesicles. Curr. Opin. Cell Biol. 13, 85-91.
61. Valderrama, F., Babià, T., Ayala, I, Kok, J. W., Renau-Piqueras, J. and Egea, G. (1998). Actin microfilaments are essential for the cytological positioning and morphology of the Golgi complex. Eur. J. Cell Biol. 76, 9-17.
62. Valderrama, F., Durán, J. M., Babià, T., Barth, H., Renau-Piqueras, J. and Egea, G. (2001). Actin microfilaments facilitate the retrograde transport from the Golgi complex to the endoplasmic reticulum in mammalian cells. Traffic 2, 717-726.
63. Wasiak, S., Quinn, C. C., Ritter, B., de Heuvel, E., Baranes, D., Plomann, M. and McPherson, P. S. (2001). The Ras/Rac guanine nucleotide exchange factor mSos interacts with PACSIN 1/syndapin I, a regulator of endocytosis and the actin cytoskeleton. J. Biol. Chem. 276, 26622-26628.
64. Welch, M. D. and Mullins, R. D. (2002). Cellular control of actin nucleation. Annu. Rev. Cell Dev. Biol. 18, 247-288.
65. Zhang, J., Shehabeldin, A., da Cruz, L. A. G., Butler, J., Somani, A. K., McGavin, M., Kozieradzki, I., dos Santos, A. O., Nagy, A., Grinstein, S. et al. (1999). Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J. Exp. Med. 190, 1329-1342.