Mechanistic Origin of Microtubule Dynamic Instability and Its Modulation by EB Proteins

Akhmanova, 2008, Tracking the ends: a dynamic protein network controls the fate of microtubule tips, Nat. Rev. Mol. Cell Biol., 9, 309, 10.1038/nrm2369 Allegretti, 2014, Atomic model of the F420-reducing [NiFe] hydrogenase by electron cryo-microscopy using a direct electron detector, eLife, 3, e01963, 10.7554/eLife.01963 Alushin, 2010, The Ndc80 kinetochore complex forms oligomeric arrays along microtubules, Nature, 467, 805, 10.1038/nature09423 Alushin, 2014, High-resolution microtubule structures reveal the structural transitions in αβ-tubulin upon GTP hydrolysis, Cell, 157, 1117, 10.1016/j.cell.2014.03.053 Amunts, 2014, Structure of the yeast mitochondrial large ribosomal subunit, Science, 343, 1485, 10.1126/science.1249410 Anders, 2001, Dominant-lethal alpha-tubulin mutants defective in microtubule depolymerization in yeast, Mol. Biol. Cell, 12, 3973, 10.1091/mbc.12.12.3973 Brown, 2015, Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions, Acta Crystallogr. D Biol. Crystallogr., 71, 136, 10.1107/S1399004714021683 Campbell, 2012, Movies of ice-embedded particles enhance resolution in electron cryo-microscopy, Structure, 20, 1823, 10.1016/j.str.2012.08.026 Caplow, 1994, The free energy for hydrolysis of a microtubule-bound nucleotide triphosphate is near zero: all of the free energy for hydrolysis is stored in the microtubule lattice, J. Cell Biol., 127, 779, 10.1083/jcb.127.3.779 des Georges, 2008, Mal3, the Schizosaccharomyces pombe homolog of EB1, changes the microtubule lattice, Nat. Struct. Mol. Biol., 15, 1102, 10.1038/nsmb.1482 Desai, 1997, Microtubule polymerization dynamics, Annu. Rev. Cell Dev. Biol., 13, 83, 10.1146/annurev.cellbio.13.1.83 Dumontet, 2010, Microtubule-binding agents: a dynamic field of cancer therapeutics, Nat. Rev. Drug Discov., 9, 790, 10.1038/nrd3253 Emsley, 2010, Features and development of Coot, Acta Crystallogr. D Biol. Crystallogr., 66, 486, 10.1107/S0907444910007493 Galjart, 2010, Plus-end-tracking proteins and their interactions at microtubule ends, Curr. Biol., 20, R528, 10.1016/j.cub.2010.05.022 Galkin, 2008, High-resolution cryo-EM structure of the F-actin-fimbrin/plastin ABD2 complex, Proc. Natl. Acad. Sci. USA, 105, 1494, 10.1073/pnas.0708667105 Hamel, 1984, Guanosine 5′-O-(3-thiotriphosphate), a potent nucleotide inhibitor of microtubule assembly, J. Biol. Chem., 259, 11060, 10.1016/S0021-9258(18)90622-8 Hayashi, 2003, Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1), J. Biol. Chem., 278, 36430, 10.1074/jbc.M305773200 Honnappa, 2009, An EB1-binding motif acts as a microtubule tip localization signal, Cell, 138, 366, 10.1016/j.cell.2009.04.065 Howard, 2003, Dynamics and mechanics of the microtubule plus end, Nature, 422, 753, 10.1038/nature01600 Hyman, 1992, Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP, Mol. Biol. Cell, 3, 1155, 10.1091/mbc.3.10.1155 Komarova, 2009, Mammalian end binding proteins control persistent microtubule growth, J. Cell Biol., 184, 691, 10.1083/jcb.200807179 Kueh, 2009, Structural plasticity in actin and tubulin polymer dynamics, Science, 325, 960, 10.1126/science.1168823 Li, 2013, Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM, Nat. Methods, 10, 584, 10.1038/nmeth.2472 Mandelkow, 1986, On the surface lattice of microtubules: helix starts, protofilament number, seam and handedness, J. Cell Biol., 102, 1067, 10.1083/jcb.102.3.1067 Maurer, 2011, GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs), Proc. Natl. Acad. Sci. USA, 108, 3988, 10.1073/pnas.1014758108 Maurer, 2012, EBs recognize a nucleotide-dependent structural cap at growing microtubule ends, Cell, 149, 371, 10.1016/j.cell.2012.02.049 Maurer, 2014, EB1 accelerates two conformational transitions important for microtubule maturation and dynamics, Curr. Biol., 24, 372, 10.1016/j.cub.2013.12.042 Menéndez, 1998, Control of the structural stability of the tubulin dimer by one high affinity bound magnesium ion at nucleotide N-site, J. Biol. Chem., 273, 167, 10.1074/jbc.273.1.167 Mitchison, 1984, Dynamic instability of microtubule growth, Nature, 312, 237, 10.1038/312237a0 Nawrotek, 2011, The determinants that govern microtubule assembly from the atomic structure of GTP-tubulin, J. Mol. Biol., 412, 35, 10.1016/j.jmb.2011.07.029 Nogales, 1998, Tubulin and FtsZ form a distinct family of GTPases, Nat. Struct. Biol., 5, 451, 10.1038/nsb0698-451 Nogales, 1998, Structure of the alpha beta tubulin dimer by electron crystallography, Nature, 391, 199, 10.1038/34465 Nogales, 1999, High-resolution model of the microtubule, Cell, 96, 79, 10.1016/S0092-8674(00)80961-7 Oliva, 2004, Structural insights into FtsZ protofilament formation, Nat. Struct. Mol. Biol., 11, 1243, 10.1038/nsmb855 Prota, 2013, Molecular mechanism of action of microtubule-stabilizing anticancer agents, Science, 339, 587, 10.1126/science.1230582 Rice, 2008, The lattice as allosteric effector: structural studies of alphabeta- and gamma-tubulin clarify the role of GTP in microtubule assembly, Proc. Natl. Acad. Sci. USA, 105, 5378, 10.1073/pnas.0801155105 Slep, 2007, Structural basis of microtubule plus end tracking by XMAP215, CLIP-170 and EB1, Mol. Cell, 27, 976, 10.1016/j.molcel.2007.07.023 Song, 2013, High-resolution comparative modeling with RosettaCM, Structure, 21, 1735, 10.1016/j.str.2013.08.005 Sui, 2010, Structural basis of interprotofilament interaction and lateral deformation of microtubules, Structure, 18, 1022, 10.1016/j.str.2010.05.010 Suloway, 2005, Automated molecular microscopy: the new Leginon system, J. Struct. Biol., 151, 41, 10.1016/j.jsb.2005.03.010 Vitre, 2008, EB1 regulates microtubule dynamics and tubulin sheet closure in vitro, Nat. Cell Biol., 10, 415, 10.1038/ncb1703 Zhu, 2009, Interactions between EB1 and microtubules: dramatic effect of affinity tags and evidence for cooperative behavior, J. Biol. Chem., 284, 32651, 10.1074/jbc.M109.013466