Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin

Journal of Structural Biology

Volumn 147, Issue 3, 2004, Pages 259-267

  Danino, Dganit ^a   Moon, Kwan Hoon ^b   Hinshaw, Jenny E ^b  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Dynamin; Endocytosis; GTPase; Membrane fission; Self assembly; Time resolved cryo EM

Indexed keywords

DYNAMIN; GUANOSINE TRIPHOSPHATE; PROLINE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; ENDOCYTOSIS; HYDROLYSIS; LIGHT SCATTERING; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; STAINING;

ANIMALS; BACULOVIRIDAE; CODON, TERMINATOR; CRYOELECTRON MICROSCOPY; DYNAMINS; INSECTS; KINETICS; LIGHT; LIPID BILAYERS; MICROSCOPY, ELECTRON; MUTAGENESIS; RECOMBINANT PROTEINS; SCATTERING, RADIATION; TRANSFECTION;

EID: 4344586301     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsb.2004.04.005     Document Type: Article

References (52)

1. Achiriloaie M., Barylko B., Albanesi J.P. Essential role of the dynamin pleckstrin homology domain in receptor-mediated endocytosis. Mol. Cell. Biol. 19:1999;1410-1415
2. Barylko B., Binns D., Lin K.M., Atkinson M.A., Jameson D.M., Yin H.L., Albanesi J.P. Synergistic activation of dynamin GTPase by Grb2 and phosphoinositides. J. Biol. Chem. 273:1998;3791-3797
3. Bellare J.R., Davis H.T., Scriven L.E., Talmon Y. Controlled environment vitrification system (CEVS). J. Electron Microsc. Tech. 10:1988;87-111
4. Carr J.F., Hinshaw J.E. Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gamma-phosphate analogues. J. Biol. Chem. 272:1997;28030-28035
5. Conway J.F., Wikoff W.R., Cheng N., Duda R.L., Hendrix R.W., Johnson J.E., Steven A.C. Virus maturation involving large subunit rotations and local refolding. Science. 292:2001;744-748
6. Damke H., Muhlberg A.B., Sever S., Sholly S., Warnock D.E., Schmid S.L. Expression, purification, and functional assays for self-association of dynamin-1. Methods Enzymol. 329:2001;447-457
7. Danino D., Hinshaw J.E. Dynamin family of mechanoenzymes. Curr. Opin. Cell Biol. 13:2001;454-460
8. Danino D., Talmon Y., Levy H., Beinert G., Zana R. Branched thread-like micelles in an aqueous solution of a trimeric surfactant. Science. 269:1995;1420-1421
9. David C., McPherson P.S., Mundigl O., De Camilli P. A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Natl. Acad. Sci. USA. 93:1996;331-335
10. Dubochet J., Adrian M., Chang J.J., Homo J.C., Lepault J., McDowall A.W., Schultz P. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:1988;129-228
11. Dubochet J., Lepault J., Freeman R., Berriman J.A., Homo J.C. Electron microscopy of frozen water and aqueous solutions. J. Microsc. 128:1982;219-237
12. Eccleston J.F., Binns D.D., Davis C.T., Albanesi J.P., Jameson D.M. Oligomerization and kinetic mechanism of the dynamin GTPase. Eur. Biophys. J. 31:2002;275-282
13. Farsad K., Ringstad N., Takei K., Floyd S.R., Rose K., De C.P. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell. Biol. 155(2):2001;193-200
14. Fish K.N., Schmid S.L., Damke H. Evidence that dynamin-2 functions as a signal-transducing GTPase. J. Cell. Biol. 150(1):2000;145-154
15. Gad H., Ringstad N., Low P., Kjaerulff O., Gustafsson J., Wenk M., Di P.G., Nemoto Y., Crun J., Ellisman M.H., De C.P., Shupliakov O., Brodin L. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron. 27(2):2000;301-312
16. Hinshaw J.E. Dynamin spirals. Curr. Opin. Struct. Biol. 9:1999;260-267
17. Hinshaw J.E. Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16:2000;483-519
18. Hinshaw J.E., Schmid S.L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature. 374(6518):1995;190-192
19. Klein D.E., Lee A., Frank D.W., Marks M.S., Lemmon M.A. The pleckstrin homology domains of dynamin isoforms require oligomerization for high affinity phosphoinositide binding. J. Biol. Chem. 273(42):1998;27725-27733
20. Klockow B., Tichelaar W., Madden D.R., Niemann H.H., Akiba T., Hirose K., Manstein D.J. The dynamin A ring complex: molecular organization and nucleotide-dependent conformational changes. EMBO J. 21:2002;240-250
21. Koenig J.H., Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9:1989;3844-3860
22. Konikoff F.M., Danino D., Weihs D., Rubin M., Talmon Y. Microstructural evolution of lipid aggregates in nucleating model and native biles visualized by cryo-transmission electron microcopy. Hepatology. 31:2000;261-268
23. Kozlov M.M. Dynamin: possible mechanism of "Pinchase" action. Biophys. J. 77:1999;604-616
24. Kozlov M.M. Fission of biological membranes: interplay between dynamin and lipids. Traffic. 2:2001;51-65
25. Lee A., Frank D.W, Marks M.S., Lemmon M.A. Dominant-negative inhibition of receptor-mediated endocytosis by a dynamin-1 mutant with a defective pleckstrin homology domain. Curr. Biol. 9(5):1999;261-264
26. Marks B., Stowell M.H., Vallis Y., Mills I.G., Gibson A., Hopkins C.R., McMahon H.T. GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature. 410(6825):2001;231-235
27. McNiven M.A. Dynamin: a molecular motor with pinchase action. Cell. 94:1998;151-154
28. McNiven M.A., Cao H., Pitts K.R., Yoon Y. The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem. Sci. 25:2000;115-120
29. Muhlberg A.B., Warnock D.E., Schmid S.L. Domain structure and intramolecular regulation of dynamin GTPase. EMBO J. 16:1997;6676-6683
30. Okamoto P.M., Herskovits J.S., Vallee R.B. Role of the basic, proline-rich region of dynamin in Src homology 3 domain binding and endocytosis. J. Biol. Chem. 272(17):1997;11629-11635
31. Ringstad N., Gad H., Low P., Di Paolo G., Brodin L., Shupliakov O., De Camilli P. Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron. 24:1999;143-154
32. Sever S. Dynamin and endocytosis. Curr. Opin. Cell Biol. 14:2002;463-467
33. Sever S., Damke H., Schmid S.L. Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic. 1:1999;385-392
34. Sever S., Damke H., Schmid S.L. Dynamin: GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J. Cell. Biol. 150:2000;1137-1148
35. Sever S., Muhlberg A.B., Schmid S.L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature. 398(6727):1999;481-486
36. Shpetner H.S., Herskovits J.S., Valee R.B. A binding site for SH3 domains targets dynamin to coated pits. J. Biol. Chem. 271:1996;13-16
37. Simpson F., Hussain N.K., Qualmann B., Kelly R.B., Kay B.K., McPherson P.S., Schmid S.L. SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat. Cell Biol. 1:1999;119-124
38. Smirnova E., Shurland D.L., Newman-Smith E.D., Pishvaee B., van der Bliek A.M. A model for dynamin self-assembly based on binding between three different protein domains. J. Biol. Chem. 274:1999;14942-14947
39. Stowell M.H., Marks B., Wigge P., McMahon H.T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat. Cell. Biol. 1:1999;27-32
40. Sweitzer S.M., Hinshaw J.E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell. 93:1998;1021-1029
41. Szaszak M., Gaborik Z., Turu G., McPherson P.S., Clark A.J., Catt K.J., Hunyady L. Role of the proline-rich domain of dynamin-2 and its interactions with Src homology 3 domains during endocytosis of the AT1 angiotensin receptor. J. Biol. Chem. 277:2002;21650-21656
42. Takei K., Haucke V., Slepnev V., Farsad K., Salazar M., Chen H., De Camilli P. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell. 94:1998;131-141
43. Takei K., McPherson P.S., Schmid S.L., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature. 374(6518):1995;186-190
44. Takei K., Mundigl O., Daniell L., De Camilli P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133:1996;1237-1250
45. Takei K., Slepnev V.I., Haucke V., De Camilli P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell. Biol. 1:1999;33-39
46. Talmon Y. Transmission electron microscopy of complex fluids: the state of the art. Ber. Bunsen. Phys. Chem. 100:1996;364-372
47. Tuma P.L., Stachniak M.C., Collins C.A. Activation of dynamin GTPase by acidic phospholipids and endogenous rat brain vesicles. J. Biol. Chem. 268:1993;17240-17246
48. Warnock D.E., Baba T., Schmid S.L. Ubiquitously expressed dynamin-II has a higher intrinsic GTPase activity and a greater propensity for self-assembly than neuronal dynamin-I. Mol. Biol. Cell. 8:1997;2553-2562
49. Warnock D.E., Hinshaw J.E., Schmid S.L. Dynamin self-assembly stimulates its GTPase activity. J. Biol. Chem. 271:1996;22310-22314
50. Warnock D.E., Terlecky L.J., Schmid S.L. Dynamin GTPase is stimulated by crosslinking through the C-terminal proline-rich domain. EMBO J. 14(7):1995;1322-1328
51. White H.D., Walker M.L., Trinick J. A computer-controlled spraying-freezing apparatus for millisecond time-resolution electron cryomicroscopy. J. Struct. Biol. 121:1998;306-313
52. Zhang P., Hinshaw J.E. Three-dimensional reconstruction of dynamin in the constricted state. Nat. Cell Biol. 3:2001;922-926