Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain–like mechanism (original) (raw)

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Article| March 19 2007

Pieta K. Mattila,

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Anette Pykäläinen,

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Juha Saarikangas,

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Ville O. Paavilainen,

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Helena Vihinen,

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Eija Jokitalo,

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Pekka Lappalainen

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

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Pieta K. Mattila

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

Anette Pykäläinen

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

Juha Saarikangas

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

Ville O. Paavilainen

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

Helena Vihinen

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

Eija Jokitalo

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

Pekka Lappalainen

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland

A. Pykäläinen and J. Saarikangas contributed equally to this paper.

Abbreviations used in this paper: Bar, Bin/amphiphysin/Rvs; DLS, dynamic light scattering; IMD, IRSp53/MIM domain; IRS, insulin receptor substrate; MIM, missing-in-metastasis; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PS, phosphatidylserine; SPR, surface plasmon resonance; WASP, Wiskott-Aldrich syndrome protein; WAVE, WASP family verprolin homologous protein.

Received: September 28 2006

Accepted: February 09 2007

Online ISSN: 1540-8140

Print ISSN: 0021-9525

The Rockefeller University Press

2007

J Cell Biol (2007) 176 (7): 953–964.

The actin cytoskeleton plays a fundamental role in various motile and morphogenetic processes involving membrane dynamics. We show that actin-binding proteins MIM (missing-in-metastasis) and IRSp53 directly bind PI(4,5)P2-rich membranes and deform them into tubular structures. This activity resides in the N-terminal IRSp53/MIM domain (IMD) of these proteins, which is structurally related to membrane-tubulating BAR (Bin/amphiphysin/Rvs) domains. We found that because of a difference in the geometry of the PI(4,5)P2-binding site, IMDs induce a membrane curvature opposite that of BAR domains and deform membranes by binding to the interior of the tubule. This explains why IMD proteins induce plasma membrane protrusions rather than invaginations. We also provide evidence that the membrane-deforming activity of IMDs, instead of the previously proposed F-actin–bundling or GTPase-binding activities, is critical for the induction of the filopodia/microspikes in cultured mammalian cells. Together, these data reveal that interplay between actin dynamics and a novel membrane-deformation activity promotes cell motility and morphogenesis.

The Rockefeller University Press

2007

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