4uuk › Citations

A dynamin mutant defines a superconstricted prefission state.

Sundborger AC, Fang S, Heymann JA, Ray P, Chappie JS, Hinshaw JE
Cell Rep 8 734-42 (2014)
Cited: 55 times
EuropePMC logo PMID: 25088425

Abstract

Dynamin is a 100 kDa GTPase that organizes into helical assemblies at the base of nascent clathrin-coated vesicles. Formation of these oligomers stimulates the intrinsic GTPase activity of dynamin, which is necessary for efficient membrane fission during endocytosis. Recent evidence suggests that the transition state of dynamin's GTP hydrolysis reaction serves as a key determinant of productive fission. Here, we present the structure of a transition-state-defective dynamin mutant K44A trapped in a prefission state at 12.5 Å resolution. This structure constricts to 3.7 nm, reaching the theoretical limit required for spontaneous membrane fission. Computational docking indicates that the ground-state conformation of the dynamin polymer is sufficient to achieve this superconstricted prefission state and reveals how a two-start helical symmetry promotes the most efficient packing of dynamin tetramers around the membrane neck. These data suggest a model for the assembly and regulation of the minimal dynamin fission machine.

Articles - 4uuk mentioned but not cited (1)

  1. Truncated DNM1 variant underlines developmental delay and epileptic encephalopathy. Afsar T, Huang X, Shah AA, Abbas S, Bano S, Mahmood A, Hu J, Razak S, Umair M. Front Pediatr 11 1266376 (2023)


Reviews citing this publication (12)

  1. Membrane fission by dynamin: what we know and what we need to know. Antonny B, Burd C, De Camilli P, Chen E, Daumke O, Faelber K, Ford M, Frolov VA, Frost A, Hinshaw JE, Kirchhausen T, Kozlov MM, Lenz M, Low HH, McMahon H, Merrifield C, Pollard TD, Robinson PJ, Roux A, Schmid S. EMBO J 35 2270-2284 (2016)
  2. The constriction and scission machineries involved in mitochondrial fission. Kraus F, Ryan MT. J Cell Sci 130 2953-2960 (2017)
  3. Structural Insights into the Mechanism of Dynamin Superfamily Proteins. Jimah JR, Hinshaw JE. Trends Cell Biol 29 257-273 (2019)
  4. Mitochondrial dynamics: The dynamin superfamily and execution by collusion. Ramachandran R. Semin Cell Dev Biol 76 201-212 (2018)
  5. Physical Constraints and Forces Involved in Phagocytosis. Jaumouillé V, Waterman CM. Front Immunol 11 1097 (2020)
  6. Regulating dynamin dynamics during endocytosis. Sundborger AC, Hinshaw JE. F1000Prime Rep 6 85 (2014)
  7. The structural biology of the dynamin-related proteins: New insights into a diverse, multitalented family. Ford MGJ, Chappie JS. Traffic 20 717-740 (2019)
  8. Reaching a consensus on the mechanism of dynamin? Roux A. F1000Prime Rep 6 86 (2014)
  9. Insight into the role of clathrin-mediated endocytosis inhibitors in SARS-CoV-2 infection. Alkafaas SS, Abdallah AM, Ghosh S, Loutfy SA, Elkafas SS, Abdel Fattah NF, Hessien M. Rev Med Virol 33 e2403 (2023)
  10. Open and cut: allosteric motion and membrane fission by dynamin superfamily proteins. Kalia R, Frost A. Mol Biol Cell 30 2097-2104 (2019)
  11. Structure Versus Stochasticity-The Role of Molecular Crowding and Intrinsic Disorder in Membrane Fission. Snead WT, Stachowiak JC. J Mol Biol 430 2293-2308 (2018)
  12. Value of models for membrane budding. Lee CT, Akamatsu M, Rangamani P. Curr Opin Cell Biol 71 38-45 (2021)

Articles citing this publication (42)

  1. Relaxation of Loaded ESCRT-III Spiral Springs Drives Membrane Deformation. Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M, Scheuring S, Roux A. Cell 163 866-879 (2015)
  2. Dynamin-related protein 1 has membrane constricting and severing abilities sufficient for mitochondrial and peroxisomal fission. Kamerkar SC, Kraus F, Sharpe AJ, Pucadyil TJ, Ryan MT. Nat Commun 9 5239 (2018)
  3. The 2018 biomembrane curvature and remodeling roadmap. Bassereau P, Jin R, Baumgart T, Deserno M, Dimova R, Frolov VA, Bashkirov PV, Grubmüller H, Jahn R, Risselada HJ, Johannes L, Kozlov MM, Lipowsky R, Pucadyil TJ, Zeno WF, Stachowiak JC, Stamou D, Breuer A, Lauritsen L, Simon C, Sykes C, Voth GA, Weikl TR. J Phys D Appl Phys 51 343001 (2018)
  4. Crystal structure of the dynamin tetramer. Reubold TF, Faelber K, Plattner N, Posor Y, Ketel K, Curth U, Schlegel J, Anand R, Manstein DJ, Noé F, Haucke V, Daumke O, Eschenburg S. Nature 525 404-408 (2015)
  5. The mechanoenzymatic core of dynamin-related protein 1 comprises the minimal machinery required for membrane constriction. Francy CA, Alvarez FJ, Zhou L, Ramachandran R, Mears JA. J Biol Chem 290 11692-11703 (2015)
  6. A hemi-fission intermediate links two mechanistically distinct stages of membrane fission. Mattila JP, Shnyrova AV, Sundborger AC, Hortelano ER, Fuhrmans M, Neumann S, Müller M, Hinshaw JE, Schmid SL, Frolov VA. Nature 524 109-113 (2015)
  7. Cryo-EM Studies of Drp1 Reveal Cardiolipin Interactions that Activate the Helical Oligomer. Francy CA, Clinton RW, Fröhlich C, Murphy C, Mears JA. Sci Rep 7 10744 (2017)
  8. Energetic cost of building a virus. Mahmoudabadi G, Milo R, Phillips R. Proc Natl Acad Sci U S A 114 E4324-E4333 (2017)
  9. Time-resolved cryo-EM using Spotiton. Dandey VP, Budell WC, Wei H, Bobe D, Maruthi K, Kopylov M, Eng ET, Kahn PA, Hinshaw JE, Kundu N, Nimigean CM, Fan C, Sukomon N, Darst SA, Saecker RM, Chen J, Malone B, Potter CS, Carragher B. Nat Methods 17 897-900 (2020)
  10. Cryo-EM of the dynamin polymer assembled on lipid membrane. Kong L, Sochacki KA, Wang H, Fang S, Canagarajah B, Kehr AD, Rice WJ, Strub MP, Taraska JW, Hinshaw JE. Nature 560 258-262 (2018)
  11. Lipid-mediated PX-BAR domain recruitment couples local membrane constriction to endocytic vesicle fission. Schöneberg J, Lehmann M, Ullrich A, Posor Y, Lo WT, Lichtner G, Schmoranzer J, Haucke V, Noé F. Nat Commun 8 15873 (2017)
  12. Dynamin regulates the dynamics and mechanical strength of the actin cytoskeleton as a multifilament actin-bundling protein. Zhang R, Lee DM, Jimah JR, Gerassimov N, Yang C, Kim S, Luvsanjav D, Winkelman J, Mettlen M, Abrams ME, Kalia R, Keene P, Pandey P, Ravaux B, Kim JH, Ditlev JA, Zhang G, Rosen MK, Frost A, Alto NM, Gardel M, Schmid SL, Svitkina TM, Hinshaw JE, Chen EH. Nat Cell Biol 22 674-688 (2020)
  13. Role of nucleotide binding and GTPase domain dimerization in dynamin-like myxovirus resistance protein A for GTPase activation and antiviral activity. Dick A, Graf L, Olal D, von der Malsburg A, Gao S, Kochs G, Daumke O. J Biol Chem 290 12779-12792 (2015)
  14. CryoEM structure of MxB reveals a novel oligomerization interface critical for HIV restriction. Alvarez FJD, He S, Perilla JR, Jang S, Schulten K, Engelman AN, Scheres SHW, Zhang P. Sci Adv 3 e1701264 (2017)
  15. Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. Liu J, Tassinari M, Souza DP, Naskar S, Noel JK, Bohuszewicz O, Buck M, Williams TA, Baum B, Low HH. Cell 184 3660-3673.e18 (2021)
  16. ESCRT-mediated vesicle concatenation in plant endosomes. Buono RA, Leier A, Paez-Valencia J, Pennington J, Goodman K, Miller N, Ahlquist P, Marquez-Lago TT, Otegui MS. J Cell Biol 216 2167-2177 (2017)
  17. A high-throughput platform for real-time analysis of membrane fission reactions reveals dynamin function. Dar S, Kamerkar SC, Pucadyil TJ. Nat Cell Biol 17 1588-1596 (2015)
  18. Adult-onset autosomal dominant spastic paraplegia linked to a GTPase-effector domain mutation of dynamin 2. Sambuughin N, Goldfarb LG, Sivtseva TM, Davydova TK, Vladimirtsev VA, Osakovskiy VL, Danilova AP, Nikitina RS, Ylakhova AN, Diachkovskaya MP, Sundborger AC, Renwick NM, Platonov FA, Hinshaw JE, Toro C. BMC Neurol 15 223 (2015)
  19. Identification and function of conformational dynamics in the multidomain GTPase dynamin. Srinivasan S, Dharmarajan V, Reed DK, Griffin PR, Schmid SL. EMBO J 35 443-457 (2016)
  20. Mass photometry enables label-free tracking and mass measurement of single proteins on lipid bilayers. Foley EDB, Kushwah MS, Young G, Kukura P. Nat Methods 18 1247-1252 (2021)
  21. Dynamic remodeling of the dynamin helix during membrane constriction. Colom A, Redondo-Morata L, Chiaruttini N, Roux A, Scheuring S. Proc Natl Acad Sci U S A 114 5449-5454 (2017)
  22. Dynamic clustering of dynamin-amphiphysin helices regulates membrane constriction and fission coupled with GTP hydrolysis. Takeda T, Kozai T, Yang H, Ishikuro D, Seyama K, Kumagai Y, Abe T, Yamada H, Uchihashi T, Ando T, Takei K. Elife 7 e30246 (2018)
  23. Cryo-EM structures of S-OPA1 reveal its interactions with membrane and changes upon nucleotide binding. Zhang D, Zhang Y, Ma J, Zhu C, Niu T, Chen W, Pang X, Zhai Y, Sun F. Elife 9 e50294 (2020)
  24. Steric interference from intrinsically disordered regions controls dynamin-related protein 1 self-assembly during mitochondrial fission. Lu B, Kennedy B, Clinton RW, Wang EJ, McHugh D, Stepanyants N, Macdonald PJ, Mears JA, Qi X, Ramachandran R. Sci Rep 8 10879 (2018)
  25. The role of scaffold reshaping and disassembly in dynamin driven membrane fission. Pannuzzo M, McDargh ZA, Deserno M. Elife 7 e39441 (2018)
  26. Event-triggered STED imaging. Alvelid J, Damenti M, Sgattoni C, Testa I. Nat Methods 19 1268-1275 (2022)
  27. Dynamin-dependent vesicle twist at the final stage of clathrin-mediated endocytosis. Cheng X, Chen K, Dong B, Yang M, Filbrun SL, Myoung Y, Huang TX, Gu Y, Wang G, Fang N. Nat Cell Biol 23 859-869 (2021)
  28. Functional recruitment of dynamin requires multimeric interactions for efficient endocytosis. Rosendale M, Van TNN, Grillo-Bosch D, Sposini S, Claverie L, Gauthereau I, Claverol S, Choquet D, Sainlos M, Perrais D. Nat Commun 10 4462 (2019)
  29. Structures of the fungal dynamin-related protein Vps1 reveal a unique, open helical architecture. Varlakhanova NV, Alvarez FJD, Brady TM, Tornabene BA, Hosford CJ, Chappie JS, Zhang P, Ford MGJ. J Cell Biol 217 3608-3624 (2018)
  30. Uncoupling of dynamin polymerization and GTPase activity revealed by the conformation-specific nanobody dynab. Galli V, Sebastian R, Moutel S, Ecard J, Perez F, Roux A. Elife 6 e25197 (2017)
  31. The anti-viral dynamin family member MxB participates in mitochondrial integrity. Cao H, Krueger EW, Chen J, Drizyte-Miller K, Schulz ME, McNiven MA. Nat Commun 11 1048 (2020)
  32. Polymer-like Model to Study the Dynamics of Dynamin Filaments on Deformable Membrane Tubes. Noel JK, Noé F, Daumke O, Mikhailov AS. Biophys J 117 1870-1891 (2019)
  33. Structural and functional characterization of the dominant negative P-loop lysine mutation in the dynamin superfamily protein Vps1. Tornabene BA, Varlakhanova NV, Hosford CJ, Chappie JS, Ford MGJ. Protein Sci 29 1416-1428 (2020)
  34. The tilted helix model of dynamin oligomers. Kadosh A, Colom A, Yellin B, Roux A, Shemesh T. Proc Natl Acad Sci U S A 116 12845-12850 (2019)
  35. Flexible pivoting of dynamin pleckstrin homology domain catalyzes fission: insights into molecular degrees of freedom. Baratam K, Jha K, Srivastava A. Mol Biol Cell 32 1306-1319 (2021)
  36. Helical self-assembly of a mucin segment suggests an evolutionary origin for von Willebrand factor tubules. Javitt G, Fass D. Proc Natl Acad Sci U S A 119 e2116790119 (2022)
  37. Revisiting the endocytosis of the m2 muscarinic acetylcholine receptor. Ockenga W, Tikkanen R. Membranes (Basel) 5 197-213 (2015)
  38. The dynamin-related protein Vps1 and the peroxisomal membrane protein Pex27 function together during peroxisome fission. Ekal L, Alqahtani AMS, Hettema EH. J Cell Sci 136 jcs246348 (2023)
  39. CryoEM structure of the super-constricted two-start dynamin 1 filament. Liu J, Alvarez FJD, Clare DK, Noel JK, Zhang P. Nat Commun 12 5393 (2021)
  40. Biased placement of Mitochondria fission facilitates asymmetric inheritance of protein aggregates during yeast cell division. Sun G, Hwang C, Jung T, Liu J, Li R. PLoS Comput Biol 19 e1011588 (2023)
  41. Dynole 34-2 and Acrylo-Dyn 2-30, Novel Dynamin GTPase Chemical Biology Probes. Baker JR, O'Brien NS, Prichard KL, Robinson PJ, McCluskey A, Russell CC. Methods Mol Biol 2417 221-238 (2022)
  42. Synthesis and Effect of Conformationally Locked Carbocyclic Guanine Nucleotides on Dynamin. Toti KS, Jimah JR, Salmaso V, Hinshaw JE, Jacobson KA. Biomolecules 12 584 (2022)


Quick links