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Kinesin-binding-triggered conformation switching of microtubules contributes to polarized transport.

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Shima T, Morikawa M, Kaneshiro J, Kambara T, Kamimura S, Yagi T, Iwamoto H, Uemura S, Shigematsu H, Shirouzu M, Ichimura T, Watanabe TM, Nitta R, Okada Y, Hirokawa N
OpenAccess logo J Cell Biol 217 4164-4183 (2018)
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Cited: 41 times
EuropePMC logo PMID: 30297389

Abstract

Kinesin-1, the founding member of the kinesin superfamily of proteins, is known to use only a subset of microtubules for transport in living cells. This biased use of microtubules is proposed as the guidance cue for polarized transport in neurons, but the underlying mechanisms are still poorly understood. Here, we report that kinesin-1 binding changes the microtubule lattice and promotes further kinesin-1 binding. This high-affinity state requires the binding of kinesin-1 in the nucleotide-free state. Microtubules return to the initial low-affinity state by washing out the binding kinesin-1 or by the binding of non-hydrolyzable ATP analogue AMPPNP to kinesin-1. X-ray fiber diffraction, fluorescence speckle microscopy, and second-harmonic generation microscopy, as well as cryo-EM, collectively demonstrated that the binding of nucleotide-free kinesin-1 to GDP microtubules changes the conformation of the GDP microtubule to a conformation resembling the GTP microtubule.

Articles - 5xxv mentioned but not cited (1)

  1. Kinesin-binding-triggered conformation switching of microtubules contributes to polarized transport. Shima T, Morikawa M, Kaneshiro J, Kambara T, Kamimura S, Yagi T, Iwamoto H, Uemura S, Shigematsu H, Shirouzu M, Ichimura T, Watanabe TM, Nitta R, Okada Y, Hirokawa N. J. Cell Biol. 217 4164-4183 (2018)


Reviews citing this publication (10)

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Articles citing this publication (30)

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  4. Concerted action of kinesins KIF5B and KIF13B promotes efficient secretory vesicle transport to microtubule plus ends. Serra-Marques A, Martin M, Katrukha EA, Grigoriev I, Peeters CA, Liu Q, Hooikaas PJ, Yao Y, Solianova V, Smal I, Pedersen LB, Meijering E, Kapitein LC, Akhmanova A. Elife 9 e61302 (2020)
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  7. Modeling spatiotemporally varying protein-protein interactions in CyLaKS, the Cytoskeleton Lattice-based Kinetic Simulator. Fiorenza SA, Steckhahn DG, Betterton MD. Eur Phys J E Soft Matter 44 105 (2021)
  8. Lattice defects induced by microtubule-stabilizing agents exert a long-range effect on microtubule growth by promoting catastrophes. Rai A, Liu T, Katrukha EA, Estévez-Gallego J, Manka SW, Paterson I, Díaz JF, Kapitein LC, Moores CA, Akhmanova A. Proc Natl Acad Sci U S A 118 e2112261118 (2021)
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  10. Altered proteomics profile in the amnion of patients with oligohydramnios. Cheung CY, Brace RA. Physiol Rep 8 e14381 (2020)
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  12. Interplay between the Kinesin and Tubulin Mechanochemical Cycles Underlies Microtubule Tip Tracking by the Non-motile Ciliary Kinesin Kif7. Jiang S, Mani N, Wilson-Kubalek EM, Ku PI, Milligan RA, Subramanian R. Dev Cell 49 711-730.e8 (2019)
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  15. Modeling a disease-correlated tubulin mutation in budding yeast reveals insight into MAP-mediated dynein function. Denarier E, Ecklund KH, Berthier G, Favier A, O'Toole ET, Gory-Fauré S, De Macedo L, Delphin C, Andrieux A, Markus SM, Boscheron C. Mol Biol Cell 32 ar10 (2021)
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  17. Multiomics analyses of vesicular transport pathway-specific transcripts and proteins in ovine amnion: responses to altered intramembranous transport. Cheung CY, Anderson DF, Brace RA. Physiol Genomics 51 267-278 (2019)
  18. Nano-positioning and tubulin conformation contribute to axonal transport regulation of mitochondria along microtubules. Van Steenbergen V, Lavoie-Cardinal F, Kazwiny Y, Decet M, Martens T, Verstreken P, Boesmans W, De Koninck P, Vanden Berghe P. Proc Natl Acad Sci U S A 119 e2203499119 (2022)
  19. Structural model of microtubule dynamics inhibition by kinesin-4 from the crystal structure of KLP-12 -tubulin complex. Taguchi S, Nakano J, Imasaki T, Kita T, Saijo-Hamano Y, Sakai N, Shigematsu H, Okuma H, Shimizu T, Nitta E, Kikkawa S, Mizobuchi S, Niwa S, Nitta R. Elife 11 e77877 (2022)
  20. A live-cell marker to visualize the dynamics of stable microtubules throughout the cell cycle. Jansen KI, Iwanski MK, Burute M, Kapitein LC. J Cell Biol 222 e202106105 (2023)
  21. Causes, costs and consequences of kinesin motors communicating through the microtubule lattice. Verhey KJ, Ohi R. J Cell Sci 136 jcs260735 (2023)
  22. Estimation of crossbridge-state during cardiomyocyte beating using second harmonic generation. Fujita H, Kaneshiro J, Takeda M, Sasaki K, Yamamoto R, Umetsu D, Kuranaga E, Higo S, Kondo T, Asano Y, Sakata Y, Miyagawa S, Watanabe TM. Life Sci Alliance 6 e202302070 (2023)
  23. KLC4 shapes axon arbors during development and mediates adult behavior. Haynes EM, Burnett KH, He J, Jean-Pierre MW, Jarzyna M, Eliceiri KW, Huisken J, Halloran MC. Elife 11 e74270 (2022)
  24. Local changes in microtubule network mobility instruct neuronal polarization and axon specification. Burute M, Jansen KI, Mihajlovic M, Vermonden T, Kapitein LC. Sci Adv 8 eabo2343 (2022)
  25. Microtubule detyrosination by VASH1/SVBP is regulated by the conformational state of tubulin in the lattice. Yue Y, Hotta T, Higaki T, Verhey KJ, Ohi R. Curr Biol 33 4111-4123.e7 (2023)
  26. Microtubule lattice spacing governs cohesive envelope formation of tau family proteins. Siahaan V, Tan R, Humhalova T, Libusova L, Lacey SE, Tan T, Dacy M, Ori-McKenney KM, McKenney RJ, Braun M, Lansky Z. Nat Chem Biol 18 1224-1235 (2022)
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  28. Preference of CAMSAP3 for expanded microtubule lattice contributes to stabilization of the minus end. Liu H, Shima T. Life Sci Alliance 6 e202201714 (2023)
  29. Second harmonic generation polarization microscopy as a tool for protein structure analysis. Kaneshiro J, Okada Y, Shima T, Tsujii M, Imada K, Ichimura T, Watanabe TM. Biophys Physicobiol 16 147-157 (2019)
  30. Taxol acts differently on different tubulin isotypes. Chew YM, Cross RA. Commun Biol 6 946 (2023)


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