Rigidity of wedge loop in PACSIN 3 protein is a key factor in dictating diameters of tubules

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 22387-22396

  Bai, Xiaoyun ^a   Meng, Geng ^a   Luo, Ming ^b   Zheng, Xiaofeng ^a  

^a PEKING UNIVERSITY   (China)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR MEMBRANES; CRYSTAL PACKINGS; DOMAIN-CONTAINING PROTEINS; KEY FACTORS; LATERAL INTERACTIONS;

CELL MEMBRANES; PROTEINS;

RIGIDITY;

PHOSPHOTRANSFERASE; PROTEIN KINASE C AND CASEIN KINASE SUBSTRATE IN NEURON 1 PROTEIN; PROTEIN KINASE C AND CASEIN KINASE SUBSTRATE IN NEURON 2 PROTEIN; PROTEIN KINASE C AND CASEIN KINASE SUBSTRATE IN NEURON 3 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL INTERACTION; CRYSTAL STRUCTURE; CYTOSKELETON; MEMBRANE STRUCTURE; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; RIGIDITY; STRUCTURE ACTIVITY RELATION; TUBULE; WEDGE LOOP;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; GOLD; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOSOMES; METAL NANOPARTICLES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84862675287     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.358960     Document Type: Article

References (38)

1. Merrifield, C. J., Perrais, D., and Zenisek, D. (2005) Coupling between clathrin-coated pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121, 593-606
2. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., and McMahon, H. T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366
3. Scott, I. C., and Stainier, D. Y. (2003) Developmental biology: twisting the body into shape. Nature 425, 461-463
4. Dvorak, A. M., and Feng, D. (2001) The vesiculo-vacuolar organelle (VVO): a new endothelial cell permeability organelle. J. Histochem. Cytochem. 49, 419-432
5. Rippe, B., Rosengren, B. I., Carlsson, O., and Venturoli, D. (2002) Transendothelial transport: the vesicle controversy. J. Vasc. Res. 39, 375-390
6. Gallop, J. L., Jao, C. C., Kent, H. M., Butler, P. J., Evans, P. R., Langen, R., and McMahon, H. T. (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25, 2898-2910
7. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R., and McMahon, H. T. (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499
8. Itoh, T., Erdmann, K. S., Roux, A., Habermann, B., Werner, H., and De Camilli, P. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804
9. Bhatia, V. K., Madsen, K. L., Bolinger, P. Y., Kunding, A., Hedegård, P., Gether, U., and Stamou, D. (2009) Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J. 28, 3303-3314
10. Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., and Mochizuki, N. (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25, 2889-2897
11. Takei, K., Slepnev, V. I., Haucke, V., and De Camilli, P. (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1, 33-39
12. Farsad, K., Ringstad, N., Takei, K., Floyd, S. R., Rose, K., and De Camilli, P. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200
13. Mattila, P. K., Pykäläinen, A., Saarikangas, J., Paavilainen, V. O., Vihinen, H., Jokitalo, E., and Lappalainen, P. (2007) Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 176, 953-964
14. Pykäläinen, A., Boczkowska, M., Zhao, H., Saarikangas, J., Rebowski, G., Jansen, M., Hakanen, J., Koskela, E. V., Peränen, J., Vihinen, H., Jokitalo, E., Salminen, M., Ikonen, E., Dominguez, R., and Lappalainen, P. (2011) Pinkbar is an epithelial-specific BAR domain protein that generates planar membrane structures. Nat. Struct. Mol. Biol. 18, 902-907
15. Fütterer, K., and Machesky, L. M. (2007) "Wunder" F-BAR domains: going from pits to vesicles. Cell 129, 655-657
16. Shimada, A., Niwa, H., Tsujita, K., Suetsugu, S., Nitta, K., Hanawa-Suetsugu, K., Akasaka, R., Nishino, Y., Toyama, M., Chen, L., Liu, Z. J., Wang, B. C., Yamamoto, M., Terada, T., Miyazawa, A., Tanaka, A., Sugano, S., Shirouzu, M., Nagayama, K., Takenawa, T., and Yokoyama, S. (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772
17. Henne, W. M., Kent, H. M., Ford, M. G., Hegde, B. G., Daumke, O., Butler, P. J., Mittal, R., Langen, R., Evans, P. R., and McMahon, H. T. (2007) Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839-852
18. Frost, A., Perera, R., Roux, A., Spasov, K., Destaing, O., Egelman, E. H., De Camilli, P., and Unger, V. M. (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132, 807-817
19. Damke, H., Baba, T., Warnock, D. E., and Schmid, S. L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934
20. Takei, Y., Harada, A., Takeda, S., Kobayashi, K., Terada, S., Noda, T., Takahashi, T., and Hirokawa, N. (1995) Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system. J. Cell Biol. 131, 1789-1800
21. 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
22. Qualmann, B., and Kelly, R. B. (2000) Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J. Cell Biol. 148, 1047-1062
23. Braun, A., Pinyol, R., Dahlhaus, R., Koch, D., Fonarev, P., Grant, B. D., Kessels, M. M., and Qualmann, B. (2005) EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol. Biol. Cell 16, 3642-3658
24. Kessels, M. M., Dong, J., Leibig, W., Westermann, P., and Qualmann, B. (2006) Complexes of syndapin II with dynamin II promote vesicle formation at the trans-Golgi network. J. Cell Sci. 119, 1504-1516
25. Grimm-Günter, E. M., Milbrandt, M., Merkl, B., Paulsson, M., and Plomann, M. (2008) PACSIN proteins bind tubulin and promote microtubule assembly. Exp. Cell Res. 314, 1991-2003
26. Halbach, A., Mörgelin, M., Baumgarten, M., Milbrandt, M., Paulsson, M., and Plomann, M. (2007) PACSIN 1 forms tetramers via its N-terminal F-BAR domain. FEBS J. 274, 773-782
27. Plomann, M., Lange, R., Vopper, G., Cremer, H., Heinlein, U. A., Scheff, S., Baldwin, S. A., Leitges, M., Cramer, M., Paulsson, M., and Barthels, D. (1998) PACSIN, a brain protein that is up-regulated upon differentiation into neuronal cells. Eur. J. Biochem. 256, 201-211
28. 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
29. Rao, Y., Ma, Q., Vahedi-Faridi, A., Sundborger, A., Pechstein, A., Puchkov, D., Luo, L., Shupliakov, O., Saenger, W., and Haucke, V. (2010) Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc. Natl. Acad. Sci. U.S.A. 107, 8213-8218
30. 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
31. Wang, Q., Navarro, M. V., Peng, G., Molinelli, E., Goh, S. L., Judson, B. L., Rajashankar, K. R., and Sondermann, H. (2009) Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein PACSIN/syndapin. Proc. Natl. Acad. Sci. U.S.A. 106, 12700-12705
32. Plomann, M., Wittmann, J. G., and Rudolph, M. G. (2010) A hinge in the distal end of the PACSIN 2 F-BAR domain may contribute to membrane-curvature sensing. J. Mol. Biol. 400, 129-136
33. Bai, X., Meng, G., Li, G., Luo, M., and Zheng, X. (2010) Crystallization and preliminary x-ray crystallographic analysis of human PACSIN 1 protein. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 73-75
34. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
35. Powell, H. R. (1999) The Rossmann Fourier autoindexing algorithm in MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 55, 1690-1695
36. Emsley, P., and Cowtan, K. (2004) COOT: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
37. Senju, Y., Itoh, Y., Takano, K., Hamada, S., and Suetsugu, S. (2011) Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J. Cell Sci. 124, 2032-2040
38. Shimada, A., Takano, K., Shirouzu, M., Hanawa-Suetsugu, K., Terada, T., Toyooka, K., Umehara, T., Yamamoto, M., Yokoyama, S., and Suetsugu, S. (2010) Mapping of the basic amino acid residues responsible for tubulation and cellular protrusion by the EFC/F-BAR domain of PACSIN2/syndapin II. FEBS Lett. 584, 1111-1118