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Spa2 remodels ADP-actin via molecular condensation under glucose starvation

Author

Listed:
  • Qianqian Ma

    (Nanyang Technological University)

  • Wahyu Surya

    (Nanyang Technological University)

  • Danxia He

    (Nanyang Technological University)

  • Hanmeng Yang

    (Nanyang Technological University)

  • Xiao Han

    (Nanyang Technological University)

  • Mui Hoon Nai

    (National University of Singapore)

  • Chwee Teck Lim

    (National University of Singapore
    National University of Singapore)

  • Jaume Torres

    (Nanyang Technological University)

  • Yansong Miao

    (Nanyang Technological University
    Nanyang Technological University)

Abstract

Actin nucleotide-dependent actin remodeling is essential to orchestrate signal transduction and cell adaptation. Rapid energy starvation requires accurate and timely reorganization of the actin network. Despite distinct treadmilling mechanisms of ADP- and ATP-actin filaments, their filament structures are nearly identical. How other actin-binding proteins regulate ADP-actin filament assembly is unclear. Here, we show that Spa2 which is the polarisome scaffold protein specifically remodels ADP-actin upon energy starvation in budding yeast. Spa2 triggers ADP-actin monomer nucleation rapidly through a dimeric core of Spa2 (aa 281-535). Concurrently, the intrinsically disordered region (IDR, aa 1-281) guides Spa2 undergoing phase separation and wetting on the surface of ADP-G-actin-derived F-actin and bundles the filaments. Both ADP-actin-specific nucleation and bundling activities of Spa2 are actin D-loop dependent. The IDR and nucleation core of Spa2 are evolutionarily conserved by coexistence in the fungus kingdom, suggesting a universal adaptation mechanism in the fungal kingdom in response to glucose starvation, regulating ADP-G-actin and ADP-F-actin with high nucleotide homogeneity.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48863-4
    DOI: 10.1038/s41467-024-48863-4
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    References listed on IDEAS

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    1. Ying Xie & Jialin Sun & Xiao Han & Alma Turšić-Wunder & Joel D. W. Toh & Wanjin Hong & Yong-Gui Gao & Yansong Miao, 2019. "Polarisome scaffolder Spa2-mediated macromolecular condensation of Aip5 for actin polymerization," Nature Communications, Nature, vol. 10(1), pages 1-18, December.
    2. Margot E. Quinlan & John E. Heuser & Eugen Kerkhoff & R. Dyche Mullins, 2005. "Drosophila Spire is an actin nucleation factor," Nature, Nature, vol. 433(7024), pages 382-388, January.
    3. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    4. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    5. He Sun & Xinlu Zhu & Chuanxi Li & Zhiming Ma & Xiao Han & Yuanyuan Luo & Liang Yang & Jing Yu & Yansong Miao, 2021. "Xanthomonas effector XopR hijacks host actin cytoskeleton via complex coacervation," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    6. Matthew J. Reynolds & Carla Hachicho & Ayala G. Carl & Rui Gong & Gregory M. Alushin, 2022. "Bending forces and nucleotide state jointly regulate F-actin structure," Nature, Nature, vol. 611(7935), pages 380-386, November.
    7. Silvia Jansen & Agnieszka Collins & Samantha M. Chin & Casey A. Ydenberg & Jeff Gelles & Bruce L. Goode, 2015. "Single-molecule imaging of a three-component ordered actin disassembly mechanism," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    8. Andrew R. Harris & Pamela Jreij & Brian Belardi & Aaron M. Joffe & Andreas R. Bausch & Daniel A. Fletcher, 2020. "Biased localization of actin binding proteins by actin filament conformation," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    9. 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.
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