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Phase separation of TPX2 enhances and spatially coordinates microtubule nucleation

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  • Matthew R. King

    (Princeton University
    Washington University)

  • Sabine Petry

    (Princeton University)

Abstract

Phase separation of substrates and effectors is proposed to enhance biological reaction rates and efficiency. Targeting protein for Xklp2 (TPX2) is an effector of branching microtubule nucleation in spindles and functions with the substrate tubulin by an unknown mechanism. Here we show that TPX2 phase separates into a co-condensate with tubulin, which mediates microtubule nucleation in vitro and in isolated cytosol. TPX2-tubulin co-condensation preferentially occurs on pre-existing microtubules, the site of branching microtubule nucleation, at the endogenous and physiologically relevant concentration of TPX2. Truncation and chimera versions of TPX2 suggest that TPX2-tubulin co-condensation enhances the efficiency of TPX2-mediated branching microtubule nucleation. Finally, the known inhibitor of TPX2, the importin-α/β heterodimer, regulates TPX2 condensation in vitro and, consequently, branching microtubule nucleation activity in isolated cytosol. Our study demonstrates how regulated phase separation can simultaneously enhance reaction efficiency and spatially coordinate microtubule nucleation, which may facilitate rapid and accurate spindle formation.

Suggested Citation

  • Matthew R. King & Sabine Petry, 2020. "Phase separation of TPX2 enhances and spatially coordinates microtubule nucleation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-019-14087-0
    DOI: 10.1038/s41467-019-14087-0
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    Cited by:

    1. Changmiao Guo & Raymundo Alfaro-Aco & Chunting Zhang & Ryan W. Russell & Sabine Petry & Tatyana Polenova, 2023. "Structural basis of protein condensation on microtubules underlying branching microtubule nucleation," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Beatrice Ramm & Dominik Schumacher & Andrea Harms & Tamara Heermann & Philipp Klos & Franziska Müller & Petra Schwille & Lotte Søgaard-Andersen, 2023. "Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    3. Jun Sun & Jiale Qu & Cai Zhao & Xinyao Zhang & Xinyu Liu & Jia Wang & Chao Wei & Xinyi Liu & Mulan Wang & Pengguihang Zeng & Xiuxiao Tang & Xiaoru Ling & Li Qing & Shaoshuai Jiang & Jiahao Chen & Tara, 2024. "Precise prediction of phase-separation key residues by machine learning," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Erik Zupa & Martin Würtz & Annett Neuner & Thomas Hoffmann & Mandy Rettel & Anna Böhler & Bram J. A. Vermeulen & Sebastian Eustermann & Elmar Schiebel & Stefan Pfeffer, 2022. "The augmin complex architecture reveals structural insights into microtubule branching," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Qianqian Ma & Wahyu Surya & Danxia He & Hanmeng Yang & Xiao Han & Mui Hoon Nai & Chwee Teck Lim & Jaume Torres & Yansong Miao, 2024. "Spa2 remodels ADP-actin via molecular condensation under glucose starvation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Maruša Ramšak & Dominique A. Ramirez & Loren E. Hough & Michael R. Shirts & Sara Vidmar & Kristina Eleršič Filipič & Gregor Anderluh & Roman Jerala, 2023. "Programmable de novo designed coiled coil-mediated phase separation in mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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