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Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation

Author

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  • Vikas A. Tillu

    (The University of Queensland)

  • James Rae

    (The University of Queensland
    Centre for Microscopy and Microanalysis)

  • Ya Gao

    (The University of Queensland)

  • Nicholas Ariotti

    (The University of New South Wales
    The University of New South Wales Kensington)

  • Matthias Floetenmeyer

    (Centre for Microscopy and Microanalysis)

  • Oleksiy Kovtun

    (The University of Queensland
    MRC Laboratory of Molecular Biology)

  • Kerrie-Ann McMahon

    (The University of Queensland)

  • Natasha Chaudhary

    (The University of Queensland
    Mount Sinai Hospital)

  • Robert G. Parton

    (The University of Queensland
    Centre for Microscopy and Microanalysis)

  • Brett M. Collins

    (The University of Queensland)

Abstract

Caveolae are spherically shaped nanodomains of the plasma membrane, generated by cooperative assembly of caveolin and cavin proteins. Cavins are cytosolic peripheral membrane proteins with negatively charged intrinsically disordered regions that flank positively charged α-helical regions. Here, we show that the three disordered domains of Cavin1 are essential for caveola formation and dynamic trafficking of caveolae. Electrostatic interactions between disordered regions and α-helical regions promote liquid-liquid phase separation behaviour of Cavin1 in vitro, assembly of Cavin1 oligomers in solution, generation of membrane curvature, association with caveolin-1, and Cavin1 recruitment to caveolae in cells. Removal of the first disordered region causes irreversible gel formation in vitro and results in aberrant caveola trafficking through the endosomal system. We propose a model for caveola assembly whereby fuzzy electrostatic interactions between Cavin1 and caveolin-1 proteins, combined with membrane lipid interactions, are required to generate membrane curvature and a metastable caveola coat.

Suggested Citation

  • Vikas A. Tillu & James Rae & Ya Gao & Nicholas Ariotti & Matthias Floetenmeyer & Oleksiy Kovtun & Kerrie-Ann McMahon & Natasha Chaudhary & Robert G. Parton & Brett M. Collins, 2021. "Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-21035-4
    DOI: 10.1038/s41467-021-21035-4
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