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Katanin Grips the β-Tubulin Tail through an Electropositive Double Spiral to Sever Microtubules.

Zehr EA, Szyk A, Szczesna E, Roll-Mecak A
Dev Cell 52 118-131.e6 (2020)
Related entries: 6ugd, 6ugf

Cited: 28 times
EuropePMC logo PMID: 31735665

Abstract

The AAA ATPase katanin severs microtubules. It is critical in cell division, centriole biogenesis, and neuronal morphogenesis. Its mutation causes microcephaly. The microtubule templates katanin hexamerization and activates its ATPase. The structural basis for these activities and how they lead to severing is unknown. Here, we show that β-tubulin tails are necessary and sufficient for severing. Cryoelectron microscopy (cryo-EM) structures reveal the essential tubulin tail glutamates gripped by a double spiral of electropositive loops lining the katanin central pore. Each spiral couples allosterically to the ATPase and binds alternating, successive substrate residues, with consecutive residues coordinated by adjacent protomers. This tightly couples tail binding, hexamerization, and ATPase activation. Hexamer structures in different states suggest an ATPase-driven, ratchet-like translocation of the tubulin tail through the pore. A disordered region outside the AAA core anchors katanin to the microtubule while the AAA motor exerts the forces that extract tubulin dimers and sever the microtubule.

Articles - 6uge mentioned but not cited (4)

  1. Katanin Grips the β-Tubulin Tail through an Electropositive Double Spiral to Sever Microtubules. Zehr EA, Szyk A, Szczesna E, Roll-Mecak A. Dev Cell 52 118-131.e6 (2020)
  2. Active conformation of the p97-p47 unfoldase complex. Xu Y, Han H, Cooney I, Guo Y, Moran NG, Zuniga NR, Price JC, Hill CP, Shen PS. Nat Commun 13 2640 (2022)
  3. Conserved structural elements specialize ATAD1 as a membrane protein extraction machine. Wang L, Toutkoushian H, Belyy V, Kokontis CY, Walter P. Elife 11 e73941 (2022)
  4. Factors underlying asymmetric pore dynamics of disaggregase and microtubule-severing AAA+ machines. Damre M, Dayananda A, Varikoti RA, Stan G, Dima RI. Biophys J 120 3437-3454 (2021)


Reviews citing this publication (6)

  1. Cutting, Amplifying, and Aligning Microtubules with Severing Enzymes. Kuo YW, Howard J. Trends Cell Biol 31 50-61 (2021)
  2. Tubulin post-translational modifications control neuronal development and functions. Moutin MJ, Bosc C, Peris L, Andrieux A. Dev Neurobiol 81 253-272 (2021)
  3. AAA+ ATPases: structural insertions under the magnifying glass. Jessop M, Felix J, Gutsche I. Curr Opin Struct Biol 66 119-128 (2021)
  4. The Mammalian Family of Katanin Microtubule-Severing Enzymes. Lynn NA, Martinez E, Nguyen H, Torres JZ. Front Cell Dev Biol 9 692040 (2021)
  5. Impact of the 'tubulin economy' on the formation and function of the microtubule cytoskeleton. Ohi R, Strothman C, Zanic M. Curr Opin Cell Biol 68 81-89 (2021)
  6. Finding a right place to cut: How katanin is targeted to cellular severing sites. Nakamura M, Yagi N, Hashimoto T. Quant Plant Biol 3 e8 (2022)

Articles citing this publication (18)

  1. α-tubulin tail modifications regulate microtubule stability through selective effector recruitment, not changes in intrinsic polymer dynamics. Chen J, Kholina E, Szyk A, Fedorov VA, Kovalenko I, Gudimchuk N, Roll-Mecak A. Dev Cell 56 2016-2028.e4 (2021)
  2. Structure of the AAA protein Msp1 reveals mechanism of mislocalized membrane protein extraction. Wang L, Myasnikov A, Pan X, Walter P. Elife 9 e54031 (2020)
  3. Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor. Pajak J, Dill E, Reyes-Aldrete E, White MA, Kelch BA, Jardine PJ, Arya G, Morais MC. Nucleic Acids Res 49 6474-6488 (2021)
  4. Combinatorial and antagonistic effects of tubulin glutamylation and glycylation on katanin microtubule severing. Szczesna E, Zehr EA, Cummings SW, Szyk A, Mahalingan KK, Li Y, Roll-Mecak A. Dev Cell 57 2497-2513.e6 (2022)
  5. Tubulin polyglutamylation differentially regulates microtubule-interacting proteins. Genova M, Grycova L, Puttrich V, Magiera MM, Lansky Z, Janke C, Braun M. EMBO J 42 e112101 (2023)
  6. Phosphorylation of the microtubule-severing AAA+ enzyme Katanin regulates C. elegans embryo development. Joly N, Beaumale E, Van Hove L, Martino L, Pintard L. J Cell Biol 219 e201912037 (2020)
  7. Viral packaging ATPases utilize a glutamate switch to couple ATPase activity and DNA translocation. Pajak J, Atz R, Hilbert BJ, Morais MC, Kelch BA, Jardine PJ, Arya G. Proc Natl Acad Sci U S A 118 e2024928118 (2021)
  8. The force required to remove tubulin from the microtubule lattice by pulling on its α-tubulin C-terminal tail. Kuo YW, Mahamdeh M, Tuna Y, Howard J. Nat Commun 13 3651 (2022)
  9. Long-range intramolecular allostery and regulation in the dynein-like AAA protein Mdn1. Mickolajczyk KJ, Olinares PDB, Niu Y, Chen N, Warrington SE, Sasaki Y, Walz T, Chait BT, Kapoor TM. Proc Natl Acad Sci U S A 117 18459-18469 (2020)
  10. AAA+ protease-adaptor structures reveal altered conformations and ring specialization. Kim S, Fei X, Sauer RT, Baker TA. Nat Struct Mol Biol 29 1068-1079 (2022)
  11. Exploring the Effect of Mechanical Anisotropy of Protein Structures in the Unfoldase Mechanism of AAA+ Molecular Machines. Varikoti RA, Fonseka HYY, Kelly MS, Javidi A, Damre M, Mullen S, Nugent JL, Gonzales CM, Stan G, Dima RI. Nanomaterials (Basel) 12 1849 (2022)
  12. SUMOylation of microtubule-cleaving enzyme KATNA1 promotes microtubule severing and neurite outgrowth. Li S, Liang Y, Zou J, Cai Z, Yang H, Yang J, Zhang Y, Lin H, Zhang G, Tan M. J Biol Chem 298 102292 (2022)
  13. Spastin is an essential regulator of male meiosis, acrosome formation, manchette structure and nuclear integrity. Cheers SR, O'Connor AE, Johnson TK, Merriner DJ, O'Bryan MK, Dunleavy JEM. Development 150 dev201183 (2023)
  14. The minus-end depolymerase KIF2A drives flux-like treadmilling of γTuRC-uncapped microtubules. Henkin G, Brito C, Thomas C, Surrey T. J Cell Biol 222 e202304020 (2023)
  15. Communication network within the essential AAA-ATPase Rix7 drives ribosome assembly. Kocaman S, Lo YH, Krahn JM, Sobhany M, Dandey VP, Petrovich ML, Etigunta SK, Williams JG, Deterding LJ, Borgnia MJ, Stanley RE. PNAS Nexus 1 pgac118 (2022)
  16. Crystal structure of the Arabidopsis SPIRAL2 C-terminal domain reveals a p80-Katanin-like domain. Bolhuis DL, Dixit R, Slep KC. PLoS One 18 e0290024 (2023)
  17. Microtubule-binding domains in Katanin p80 subunit are essential for severing activity in C. elegans. Beaumale E, Van Hove L, Pintard L, Joly N. J Cell Biol 223 e202308023 (2024)
  18. Molecular dynamics of DNA translocation by FtsK. Pajak J, Arya G. Nucleic Acids Res 50 8459-8470 (2022)


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