A dynamin mutant defines a superconstricted prefission state

Cell Reports

Volumn 8, Issue 3, 2014, Pages 734-742

  Sundborger, Anna C ^a   Fang, Shunming ^a   Heymann, Jürgen A ^a   Ray, Pampa ^a   Chappie, Joshua S ^b   Hinshaw, Jenny E ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; GUANOSINE TRIPHOSPHATE;

ARTICLE; CONTROLLED STUDY; MATHEMATICAL COMPUTING; MOLECULAR DOCKING; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN LIPID INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; CLATHRIN-COATED VESICLE; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; CELL MEMBRANE; CLATHRIN-COATED VESICLES; DYNAMINS; GUANOSINE TRIPHOSPHATE; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84924528319     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.054     Document Type: Article

References (39)

1. Anggono, V., and Robinson, P.J. (2007). Syndapin I and endophilin I bind overlapping proline-rich regions of dynamin I: role in synaptic vesicle endocytosis. J. Neurochem. 102, 931-943.
2. Bashkirov, P.V., Akimov, S.A., Evseev, A.I., Schmid, S.L., Zimmerberg, J., and Frolov, V.A. (2008). GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135, 1276-1286.
3. Bethoney, K.A., King, M.C., Hinshaw, J.E., Ostap, E.M., and Lemmon, M.A. (2009). A possible effector role for the pleckstrin homology (PH) domain of dynamin. Proc. Natl. Acad. Sci. USA 106, 13359-13364.
4. Burger, K.N., Demel, R.A., Schmid, S.L., and de Kruijff, B. (2000). Dynamin is membrane-active: lipid insertion is induced by phosphoinositides and phosphatidic acid. Biochemistry 39, 12485-12493.
5. Chappie, J.S., and Dyda, F. (2013). Building a fission machine-structural insights into dynamin assembly and activation. J. Cell Sci. 126, 2773-2784.
6. Chappie, J.S., Acharya, S., Liu, Y.W., Leonard, M., Pucadyil, T.J., and Schmid, S.L. (2009). An intramolecular signaling element that modulates dynamin function in vitro and in vivo. Mol. Biol. Cell 20, 3561-3571.
7. Chappie, J.S., Acharya, S., Leonard, M., Schmid, S.L., and Dyda, F. (2010). G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature 465, 435-440.
8. Chappie, J.S., Mears, J.A., Fang, S., Leonard, M., Schmid, S.L., Milligan, R.A., Hinshaw, J.E., and Dyda, F. (2011). A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209-222.
9. Chen, Y.J., Zhang, P., Egelman, E.H., and Hinshaw, J.E. (2004). The stalk region of dynamin drives the constriction of dynamin tubes. Nat. Struct. Mol. Biol. 11, 574-575.
10. 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.
11. Danino, D., Moon, K.H., and Hinshaw, J.E. (2004). Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J. Struct. Biol. 147, 259-267.
12. Egelman, E.H. (2007). The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J. Struct. Biol. 157, 83-94.
13. Faelber, K., Posor, Y., Gao, S., Held, M., Roske, Y., Schulze, D., Haucke, V., Noé, F., and Daumke, O. (2011). Crystal structure of nucleotide-free dynamin. Nature 477, 556-560.
14. Ferguson, S.M., and De Camilli, P. (2012). Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13, 75-88.
15. Ferguson, K.M., Lemmon, M.A., Schlessinger, J., and Sigler, P.B. (1994). Crystal structure at 2.2 A resolution of the pleckstrin homology domain from human dynamin. Cell 79, 199-209.
16. Ford, M.G., Jenni, S., and Nunnari, J. (2011). The crystal structure of dynamin. Nature 477, 561-566.
17. Henderson, R. (2013). Avoiding the pitfalls of single particle cryo-electron microscopy: Einstein from noise. Proc. Natl. Acad. Sci. USA 110, 18037-18041.
18. Heymann, J.B., and Belnap, D.M. (2007). Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157, 3-18.
19. Heymann, J.A., and Hinshaw, J.E. (2009). Dynamins at a glance. J. Cell Sci. 122, 3427-3431.
20. Kozlovsky, Y., and Kozlov, M.M. (2003). Membrane fission: model for intermediate structures. Biophys. J. 85, 85-96.
21. Liu, Y.W., Mattila, J.P., and Schmid, S.L. (2013). Dynamin-catalyzed membrane fission requires coordinated GTP hydrolysis. PLoS ONE 8, e55691.
22. Mears, J.A., Ray, P., and Hinshaw, J.E. (2007). A corkscrew model for dynamin constriction. Structure 15, 1190-1202.
23. Mears, J.A., Lackner, L.L., Fang, S., Ingerman, E., Nunnari, J., and Hinshaw, J.E. (2011). Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat. Struct. Mol. Biol. 18, 20-26.
24. Mehrotra, N., Nichols, J., and Ramachandran, R. (2014). Alternate pleckstrin homology domain orientations regulate dynamin-catalyzed membrane fission. Mol. Biol. Cell 25, 879-890.
25. Mim, C., Cui, H., Gawronski-Salerno, J.A., Frost, A., Lyman, E., Voth, G.A., and Unger, V.M. (2012). Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149, 137-145.
26. Morlot, S., Galli, V., Klein, M., Chiaruttini, N., Manzi, J., Humbert, F., Dinis, L., Lenz, M., Cappello, G., and Roux, A. (2012). Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction. Cell 151, 619-629.
27. Pucadyil, T.J., and Schmid, S.L. (2008). Real-time visualization of dynamincatalyzed membrane fission and vesicle release. Cell 135, 1263-1275.
28. Ramachandran, R., and Schmid, S.L. (2008). Real-time detection reveals that effectors couple dynamin's GTP-dependent conformational changes to the membrane. EMBO J. 27, 27-37.
29. Ramachandran, R., Pucadyil, T.J., Liu, Y.W., Acharya, S., Leonard, M., Lukiyanchuk, V., and Schmid, S.L. (2009). Membrane insertion of the pleckstrin homology domain variable loop 1 is critical for dynamin-catalyzed vesicle scission. Mol. Biol. Cell 20, 4630-4639.
30. Roux, A., Uyhazi, K., Frost, A., and De Camilli, P. (2006). GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441, 528-531.
31. Roux, A., Koster, G., Lenz, M., Sorre, B., Manneville, J.B., Nassoy, P., and Bassereau, P. (2010). Membrane curvature controls dynamin polymerization. Proc. Natl. Acad. Sci. USA 107, 4141-4146.
32. Schmid, S.L., and Frolov, V.A. (2011). Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol. 27, 79-105.
33. Shnyrova, A.V., Bashkirov, P.V., Akimov, S.A., Pucadyil, T.J., Zimmerberg, J., Schmid, S.L., and Frolov, V.A. (2013). Geometric catalysis ofmembrane fission driven by flexible dynamin rings. Science 339, 1433-1436.
34. Sundborger, A., Soderblom, C., Vorontsova, O., Evergren, E., Hinshaw, J.E., and Shupliakov, O. (2011). An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J. Cell Sci. 124, 133-143.
35. Sweitzer, S.M., and Hinshaw, J.E. (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029.
36. Tan, R.K., Devkota, B., and Harvey, S.C. (2008). YUP.SCX: coaxing atomic models into medium resolution electron density maps. J. Struct. Biol. 163, 163-174.
37. van der Bliek, A.M., and Payne, G.S. (2010). Dynamin subunit interactions revealed. Dev. Cell 18, 687-688.
38. Warnock, D.E., Hinshaw, J.E., and Schmid, S.L. (1996). Dynamin self-assembly stimulates its GTPase activity. J. Biol. Chem. 271, 22310-22314.
39. Zhang, P., and Hinshaw, J.E. (2001). Three-dimensional reconstruction of dynamin in the constricted state. Nat. Cell Biol. 3, 922-926.