Crystal structure of the dynamin tetramer

Nature

Volumn 525, Issue 7569, 2015, Pages 404-408

  Reubold, Thomas F ^a   Faelber, Katja ^b   Plattner, Nuria ^c   Posor, York ^d   Ketel, Katharina ^d,e   Curth, Ute ^a   Schlegel, Jeanette ^b   Anand, Roopsee ^a   Manstein, Dietmar J ^a   Noé, Frank ^c   Haucke, Volker ^c,d   Daumke, Oliver ^b,c   Eschenburg, Susanne ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; NUCLEOTIDE; TETRAMER; MUTANT PROTEIN;

CRYSTAL STRUCTURE; DISABILITY; ENZYME ACTIVITY; INHIBITION; MOLECULAR ANALYSIS; MORPHOLOGY; MUSCLE; MUTATION; PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUTATION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; METABOLISM; MYOPATHY; PROBABILITY; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

CHARCOT-MARIE-TOOTH DISEASE; CRYSTALLOGRAPHY, X-RAY; DYNAMINS; HUMANS; MARKOV CHAINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTANT PROTEINS; MUTATION; MYOPATHIES, STRUCTURAL, CONGENITAL; NUCLEOTIDES; PROTEIN MULTIMERIZATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84942047414     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14880     Document Type: Article

References (53)

1. Ferguson, S. M. & De Camilli, P. Dynamin, a membrane-remodelling GTPase. Nature Rev. Mol. Cell Biol. 13, 75-88 (2012).
2. Faelber, K. et al. Crystal structure of nucleotide-free dynamin. Nature 477, 556-560 (2011).
3. Ford, M. G., Jenni, S. & Nunnari, J. The crystal structure of dynamin. Nature 477, 561-566 (2011).
4. Cowling, B. S., Toussaint, A., Muller, J. & Laporte, J. Defective membrane remodeling in neuromuscular diseases: insights from animal models. PLoS Genet. 8, e1002595 (2012).
5. Durieux, A. C., Prudhon, B., Guicheney, P. & Bitoun, M. Dynamin 2 and human diseases. J. Mol. Med. 88, 339-350 (2010).
6. Daumke, O., Roux, A. & Haucke, V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell 156, 882-892 (2014).
7. Hinshaw, J. E. & Schmid, S. L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190-192 (1995).
8. 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, 186-190 (1995).
9. Chappie, J. S. et al. A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209-222 (2011).
10. Faelber, K. et al. Structural insights into dynamin-mediated membrane fission. Structure 20, 1621-1628 (2012).
11. Ramachandran, R. et al. The dynamin middle domain is critical for tetramerization and higher-order self-assembly. EMBO J. 26, 559-566 (2007).
12. Fröhlich, C. et al. Structural insights into oligomerization and mitochondrial remodelling of dynamin 1-like protein. EMBO J. 32, 1280-1292 (2013).
13. Gao, S. et al. Structure of myxovirus resistance protein a reveals intra- and intermolecular domain interactions required for the antiviral function. Immunity 35, 514-525 (2011).
14. Gao, S. et al. Structural basis of oligomerization in the stalk region of dynamin-like MxA. Nature 465, 502-506 (2010).
15. Srinivasan, S., Mattila, J. P. & Schmid, S. L. Intrapolypeptide Interactions between the GTPase Effector Domain (GED) and the GTPase Domain Form the Bundle Signaling Element in Dynamin Dimers. Biochemistry 53, 5724-5726 (2014).
16. Koutsopoulos, O. S. et al. Mild functional differences of dynamin 2 mutations associated to centronuclear myopathy and Charcot-Marie Tooth peripheral neuropathy. PLoS ONE 6, e27498 (2011).
17. Sidiropoulos, P. N. et al. Dynamin 2 mutations in Charcot-Marie-Tooth neuropathy highlight the importance of clathrin-mediated endocytosis in myelination. Brain 135, 1395-1411 (2012).
18. Liu, Y. W. et al. Differential curvature sensing and generating activities of dynamin isoforms provide opportunities for tissue-specific regulation. Proc. Natl Acad. Sci. USA 108, E234-E242 (2011).
19. Vallis, Y. et al. Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis. Curr. Biol. 9, 257-263 (1999).
20. Kenniston, J. A. & Lemmon, M. A. Dynamin GTPase regulation is altered by PH domain mutations found in centronuclear myopathy patients. EMBO J. 29, 3054-3067 (2010).
21. Bowman, G. R., Pande, V. S. & Noé, F. (eds) An Introduction to Markov State Models and Their Application to Long Timescale Molecular Simulation. (Springer, 2014).
22. Schütte, C. & Sarich, M. Metastability and Markov models in molecular dynamics: modeling, analysis, algorithmic approaches. In Courant Lecture Notes Vol. 24 (American Mathematical Society, 2013).
23. Kohlhoff, K. J. et al. Cloud-based simulations on Google Exacycle reveal ligand modulation of GPCR activation pathways. Nature Chem. 6, 15-21 (2014).
24. Chen, Y. J., Zhang, P., Egelman, E. H. & Hinshaw, J. E. The stalk region of dynamin drives the constriction of dynamin tubes. Nature Struct. Mol. Biol. 11, 574-575 (2004).
25. Roux, A. et al. Membrane curvature controls dynamin polymerization. Proc. Natl Acad. Sci. USA 107, 4141-4146 (2010).
26. Sundborger, A. C. et al. A dynamin mutant defines a super-constricted pre-fission state. Cell Rep. 8, 734-742 (2014).
27. Cocucci, E., Gaudin, R. & Kirchhausen, T. Dynamin recruitment and membrane scission at the neck of a clathrin-coated pit. Mol. Biol. Cell 25, 3595-3609 (2014).
28. Grassart, A. et al. Actin and dynamin2 dynamics and interplay during clathrin-mediated endocytosis. J. Cell Biol. 205, 721-735 (2014).
29. Graham, M. E., O'Callaghan, D. W., McMahon, H. T. & Burgoyne, R. D. Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc. Natl Acad. Sci. USA 99, 7124-7129 (2002).
30. Schmid, E. M. & McMahon, H. T. Integrating molecular and network biology to decode endocytosis. Nature 448, 883-888 (2007).
31. Cao, H., Garcia, F. & McNiven, M. A. Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9, 2595-2609 (1998).
32. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
33. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
34. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
35. Adams, P. D. et al. The Phenix software for automated determination of macromolecular structures. Methods 55, 94-106 (2011).
36. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).
37. The PyMOL Molecular Graphics System. Version 1.7.0.1. (Schrödinger, LLC).
38. Kabsch, W. A solution for the best rotation to relate two sets of vectors. Acta Crystallogr. A 32, 922-923 (1976).
39. Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).
40. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
41. Schuck, P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619 (2000).
42. Laue, T. M. & Stafford, W. F. III. Modern applications of analytical ultracentrifugation. Annu. Rev. Biophys. Biomol. Struct. 28, 75-100 (1999).
43. Laue, M. T., Shah, B. D., Ridgeway, T. M. & Pelletier, S. L. in Analytical Ultracentrifugation in Biochemistry and Polymer Science (eds Harding, S. E. et al.) 90-125 (Royal Society of Chemistry, 1992).
44. Edelstein, A. et al. Computer control of microscopes using μManager. Curr. Protoc. Mol. Biol. http://dx.doi.org/10.1002/0471142727.mb1420592 (2010).
45. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).
46. Lindahl, E., Hess, B. & van der Spoel, D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7, 306-317 (2001).
47. Mackerell, A. D. Jr, Feig, M. & Brooks, C. L. III. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415 (2004).
48. Prinz, J.-H. et al. Markov models of molecular kinetics: Generation and validation. J. Chem. Phys. 134, 174105 (2011).
49. Stanley, N., Esteban-Martin, S. & De Fabritiis, G. Kinetic modulation of a disordered protein domain by phosphorylation. Nature Commun. 5, 5272 (2014).
50. Senne, M. et al. EMMA: A Software Package for Markov Model Building and Analysis. J. Chem. Theory Comput. 8, 2223-2238 (2012).
51. Swope, W. C., Pitera, J. W. & Suits, F. Describing protein folding kinetics by molecular dynamics simulations. 1. Theory. J. Phys. Chem. B 108, 6571-6581 (2004).
52. Deuflhard, P. & Weber, M. Robust Perron cluster analysis in conformation dynamics. Linear Algebra Appl. 398, 161-184 (2005).
53. Chappie, J. S. & Dyda, F. Building a fission machine-structural insights into dynamin assembly and activation. J. Cell Sci. 126, 2773-2784 (2013).