G domain dimerization controls dynamin's assembly-stimulated GTPase activity (original) (raw)

References

  1. Mettlen, M., Pucadyil, T. J., Ramachandran, R. & Schmid, S. L. Dissecting dynamin’s role in clathrin-mediated endocytosis. Biochem. Soc. Trans. 37, 1022–1026 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  2. Praefcke, G. J. & McMahon, H. T. The dynamin superfamily: universal membrane tubulation and fission molecules? Nature Rev. Mol. Cell Biol. 5, 133–147 (2004)
    Article CAS Google Scholar
  3. Muhlberg, A. B., Warnock, D. E. & Schmid, S. L. Domain structure and intramolecular regulation of dynamin GTPase. EMBO J. 16, 6676–6683 (1997)
    Article CAS PubMed PubMed Central Google Scholar
  4. Stowell, M. H., Marks, B., Wigge, P. & McMahon, H. T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nature Cell Biol. 1, 27–32 (1999)
    Article CAS PubMed Google Scholar
  5. Damke, H., Baba, T., Warnock, D. E. & Schmid, S. L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915–934 (1994)
    Article CAS PubMed Google Scholar
  6. Damke, H., Binns, D. D., Ueda, H., Schmid, S. L. & Baba, T. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12, 2578–2589 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  7. Song, B. D., Leonard, M. & Schmid, S. L. Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J. Biol. Chem. 279, 40431–40436 (2004)
    Article CAS PubMed Google Scholar
  8. Pucadyil, T. J. & Schmid, S. L. Real-time visualization of dynamin-catalyzed membrane fission and vesicle release. Cell 135, 1263–1275 (2008)
    Article CAS PubMed PubMed Central Google Scholar
  9. Danino, D., Moon, K. H. & Hinshaw, J. E. Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J. Struct. Biol. 147, 259–267 (2004)
    Article CAS PubMed Google Scholar
  10. Ramachandran, R. & Schmid, S. L. Real-time detection reveals that effectors couple dynamin's GTP-dependent conformational changes to the membrane. EMBO J. 27, 27–37 (2008)
    Article CAS PubMed Google Scholar
  11. Bashkirov, P. V. et al. GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135, 1276–1286 (2008)
    Article CAS PubMed PubMed Central Google Scholar
  12. Zhang, P. & Hinshaw, J. E. Three-dimensional reconstruction of dynamin in the constricted state. Nature Cell Biol. 3, 922–926 (2001)
    Article CAS PubMed Google Scholar
  13. 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)
    Article CAS Google Scholar
  14. Song, B. D., Yarar, D. & Schmid, S. L. An assembly-incompetent mutant establishes a requirement for dynamin self-assembly in clathrin-mediated endocytosis in vivo . Mol. Biol. Cell 15, 2243–2252 (2004)
    Article CAS PubMed PubMed Central Google Scholar
  15. Sever, S. et al. Physical and functional connection between auxilin and dynamin during endocytosis. EMBO J. 25, 4163–4174 (2006)
    Article CAS PubMed PubMed Central Google Scholar
  16. Ramachandran, R. et al. The dynamin middle domain is critical for tetramerization and higher-order self-assembly. EMBO J. 26, 559–566 (2007)
    Article CAS PubMed Google Scholar
  17. Sever, S., Muhlberg, A. B. & Schmid, S. L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481–486 (1999)
    Article ADS CAS PubMed Google Scholar
  18. Narayanan, R., Leonard, M., Song, B. D., Schmid, S. L. & Ramaswami, M. An internal GAP domain negatively regulates presynaptic dynamin in vivo: a two-step model for dynamin function. J. Cell Biol. 169, 117–126 (2005)
    Article CAS PubMed PubMed Central Google Scholar
  19. Chappie, J. S. et al. An intramolecular signaling element that modulates dynamin function in vitro and in vivo . Mol. Biol. Cell 20, 3561–3571 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  20. 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, 14942–14947 (1999)
    Article CAS PubMed Google Scholar
  21. Reubold, T. F. et al. Crystal structure of the GTPase domain of rat dynamin 1. Proc. Natl Acad. Sci. USA 102, 13093–13098 (2005)
    Article ADS CAS PubMed PubMed Central Google Scholar
  22. Niemann, H. H., Knetsch, M. L. W., Scherer, A., Manstein, D. J. & Kull, F. J. Crystal structure of a dynamin GTPase domain in both nucleotide-free and GDP-bound forms. EMBO J. 20, 5813–5821 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  23. Bourne, H. R., Sanders, D. A. & McCormick, F. The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117–127 (1991)
    Article ADS CAS PubMed Google Scholar
  24. Li, G. & Zhang, X. C. GTP hydrolysis mechanism of Ras-like GTPases. J. Mol. Biol. 340, 921–932 (2004)
    Article CAS PubMed Google Scholar
  25. Scheffzek, K., Ahmadian, M. R. & Wittinghofer, A. GTPase-activating proteins: helping hands to complement an active site. Trends Biochem. Sci. 23, 257–262 (1998)
    Article CAS PubMed Google Scholar
  26. Tesmer, J. J. G., Berman, D. M., Gilman, A. G. & Sprang, S. R. Structure of RGS4 bound to AlF4 --activated Giα1: stabilization of the transition state for GTP hydrolysis. Cell 89, 251–261 (1997)
    Article CAS PubMed Google Scholar
  27. Gasper, R., Meyer, S., Gotthardt, K., Sirajuddin, M. & Wittinghofer, A. It takes two to tango: regulation of G proteins by dimerization. Nature Rev. Mol. Cell Biol. 10, 423–429 (2009)
    Article CAS Google Scholar
  28. Scrima, A. & Wittinghofer, A. Dimerisation-dependent GTPase reaction of MnmE: how potassium acts as GTPase-activating element. EMBO J. 25, 2940–2951 (2006)
    Article CAS PubMed PubMed Central Google Scholar
  29. Ghosh, A., Praefcke, G. J., Renault, L., Wittinghofer, A. & Herrmann, C. How guanylate-binding proteins achieve assembly-stimulated processive cleavage of GTP to GMP. Nature 440, 101–104 (2006)
    Article ADS CAS PubMed Google Scholar
  30. Marks, B. et al. GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231–235 (2001)
    Article ADS CAS PubMed Google Scholar
  31. Loerke, D. et al. Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol. 7, e57 (2009)
    Article PubMed CAS Google Scholar
  32. Ferguson, S. et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell 17, 811–822 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  33. Low, H. H., Sachse, C., Amos, L. A. & Lowe, J. Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell 139, 1342–1352 (2009)
    Article PubMed PubMed Central Google Scholar
  34. Solomaha, E. & Palfrey, H. C. Conformational changes in dynamin on GTP binding and oligomerization reported by intrinsic and extrinsic fluorescence. Biochem. J. 391, 601–611 (2005)
    Article CAS PubMed PubMed Central Google Scholar
  35. Mears, J. A., Ray, P. & Hinshaw, J. E. A corkscrew model for dynamin constriction. Structure 15, 1190–1202 (2007)
    Article CAS PubMed PubMed Central Google Scholar
  36. 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, 28030–28035 (1997)
    Article CAS PubMed Google Scholar
  37. Hinshaw, J. E. & Schmid, S. L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190–192 (1995)
    Article ADS CAS PubMed Google Scholar
  38. Sweitzer, S. M. & Hinshaw, J. E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021–1029 (1998)
    Article CAS PubMed Google Scholar
  39. Roux, A., Uyhazi, K., Frost, A. & De Camilli, P. GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441, 528–531 (2006)
    Article ADS CAS PubMed Google Scholar
  40. Leonard, M., Song, B. D., Ramachandran, R. & Schimd, S. L. Robust colorimetric assays for dynamin's basal and stimulated GTPase activities. Methods Enzymol. 404, 490–503 (2005)
    Article CAS PubMed Google Scholar
  41. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L. & Clardy, J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105–124 (1993)
    Article CAS PubMed Google Scholar
  42. Diederichs, K., McSweeney, S. & Ravelli, R. B. G. Zero-dose extrapolation as part of macromolecular synchrotron data reduction. Acta Crystallogr. D 59, 903–909 (2003)
    Article PubMed CAS Google Scholar
  43. Kabsch, W. in International Tables for Crystallography Vol. F, Crystallography of Biological Macromolecules (eds Rossmann, M. G. & Arnold, E.) Ch. 11.3 (Kluwer Academic, 2001)
    Google Scholar
  44. Terwillinger, T. C. MAD phasing: treatment of dispersive differences as isomorphous replacement information. Acta Crystallogr. D 50, 17–23 (1994)
    Article Google Scholar
  45. Bruker-AXS data preparation and reciprocal space exploration, 6.12, Unix version. (Bruker, 2001)
  46. Sheldrick, G. M. in Direct Methods for Solving Macromolecular Structures (ed. Fortier, S.) 401–411 (Kluwer Academic, 1998)
    Book Google Scholar
  47. de La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472–494 (1997)
    Article CAS PubMed Google Scholar
  48. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760–763 (1994)
  49. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110–119 (1991)
    Article PubMed Google Scholar
  50. Brünger, A. T. et al. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905–921 (1998)
    Article PubMed Google Scholar
  51. Navaza, J. Implementation of molecular replacement in AMoRe. Acta Crystallogr. D 57, 1367–1372 (2001)
    Article CAS PubMed Google Scholar
  52. Connolly, M. L. The molecular-surface package. J. Mol. Graph. 11, 139–143 (1993)
    Article CAS PubMed Google Scholar
  53. Yap, K. Interhlx. 〈http://nmr.uhnres.utoronto.ca/ikura/resources/data+sw/interhlx/〉 (1998)
  54. DeLano, W. L. The PyMol Molecular Graphics System. (Pymol, 2002); 〈http://www.pymol.org〉.
  55. Leonard, M., Song, B. D., Ramachandran, R. & Schmid, S. L. Robust colorimetric assays for dynamin's basal and stimulated GTPase activities. Methods Enzymol. 404, 490–503 (2005)
    Article CAS PubMed Google Scholar
  56. Schlunck, G. et al. Modulation of Rac localization and function by dynamin. Mol. Biol. Cell 15, 256–267 (2004)
    Article CAS PubMed PubMed Central Google Scholar

Download references