MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation

Juha Saarikangas; Nazim Kourdougli; Yosuke Senju; Genevieve Chazal; Mikael Segerstråle; Rimante Minkeviciene; Jaakko Kuurne; Pieta K. Mattila; Lillian Garrett; Sabine M. Hölter; Lore Becker; Ildikó Racz; Wolfgang Hans; Thomas Klopstock; Wolfgang Wurst; Andreas Zimmer; Helmut Fuchs; Valérie Gailus-Durner; Martin Hrabě de Angelis; Lotta von Ossowski; Tomi Taira; Pekka Lappalainen; Claudio Rivera; Pirta Hotulainen

doi:10.1016/j.devcel.2015.04.014

MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation

Juha Saarikangas, Nazim Kourdougli, Yosuke Senju, Genevieve Chazal, Mikael Segerstråle, Rimante Minkeviciene, Jaakko Kuurne, Pieta K. Mattila, Lillian Garrett, Sabine M. Hölter, Lore Becker, Ildikó Racz, Wolfgang Hans, Thomas Klopstock, Wolfgang Wurst, Andreas Zimmer, Helmut Fuchs, Valérie Gailus-Durner, Martin Hrabě de Angelis, Lotta von OssowskiTomi Taira, Pekka Lappalainen, Claudio Rivera, Pirta Hotulainen

Research output: Contribution to journal › Article

38 Citations (Scopus)

Abstract

Proper morphogenesis of neuronal dendritic spines is essential for the formation of functional synaptic networks. However, it is not known how spines are initiated. Here, we identify the inverse-BAR (I-BAR) protein MIM/MTSS1 as a nucleator of dendritic spines. MIM accumulated to future spine initiation sites in a PIP₂-dependent manner and deformed the plasma membrane outward into a proto-protrusion via its I-BAR domain. Unexpectedly, the initial protrusion formation did not involve actin polymerization. However, PIP₂-dependent activation of Arp2/3-mediated actin assembly was required for protrusion elongation. Overexpression of MIM increased the density of dendritic protrusions and suppressed spine maturation. In contrast, MIM deficiency led to decreased density of dendritic protrusions and larger spine heads. Moreover, MIM-deficient mice displayed altered glutamatergic synaptic transmission and compatible behavioral defects. Collectively, our data identify an important morphogenetic pathway, which initiates spine protrusions by coupling phosphoinositide signaling, direct membrane bending, and actin assembly to ensure proper synaptogenesis.

Original language	English
Pages (from-to)	644-659
Number of pages	16
Journal	Developmental Cell
Volume	33
Issue number	6
DOIs	https://doi.org/10.1016/j.devcel.2015.04.014
Publication status	Published - Jun 22 2015

ASJC Scopus subject areas

Molecular Biology
Biochemistry, Genetics and Molecular Biology(all)
Developmental Biology
Cell Biology

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Saarikangas, J., Kourdougli, N., Senju, Y., Chazal, G., Segerstråle, M., Minkeviciene, R., Kuurne, J., Mattila, P. K., Garrett, L., Hölter, S. M., Becker, L., Racz, I., Hans, W., Klopstock, T., Wurst, W., Zimmer, A., Fuchs, H., Gailus-Durner, V., Hrabě de Angelis, M., ... Hotulainen, P. (2015). MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation. Developmental Cell, 33(6), 644-659. https://doi.org/10.1016/j.devcel.2015.04.014

MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation. / Saarikangas, Juha; Kourdougli, Nazim; Senju, Yosuke; Chazal, Genevieve; Segerstråle, Mikael; Minkeviciene, Rimante; Kuurne, Jaakko; Mattila, Pieta K.; Garrett, Lillian; Hölter, Sabine M.; Becker, Lore; Racz, Ildikó; Hans, Wolfgang; Klopstock, Thomas; Wurst, Wolfgang; Zimmer, Andreas; Fuchs, Helmut; Gailus-Durner, Valérie; Hrabě de Angelis, Martin; von Ossowski, Lotta; Taira, Tomi; Lappalainen, Pekka; Rivera, Claudio; Hotulainen, Pirta.

In: Developmental Cell, Vol. 33, No. 6, 22.06.2015, p. 644-659.

Research output: Contribution to journal › Article

Saarikangas, J, Kourdougli, N, Senju, Y, Chazal, G, Segerstråle, M, Minkeviciene, R, Kuurne, J, Mattila, PK, Garrett, L, Hölter, SM, Becker, L, Racz, I, Hans, W, Klopstock, T, Wurst, W, Zimmer, A, Fuchs, H, Gailus-Durner, V, Hrabě de Angelis, M, von Ossowski, L, Taira, T, Lappalainen, P, Rivera, C & Hotulainen, P 2015, 'MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation', Developmental Cell, vol. 33, no. 6, pp. 644-659. https://doi.org/10.1016/j.devcel.2015.04.014

Saarikangas, Juha ; Kourdougli, Nazim ; Senju, Yosuke ; Chazal, Genevieve ; Segerstråle, Mikael ; Minkeviciene, Rimante ; Kuurne, Jaakko ; Mattila, Pieta K. ; Garrett, Lillian ; Hölter, Sabine M. ; Becker, Lore ; Racz, Ildikó ; Hans, Wolfgang ; Klopstock, Thomas ; Wurst, Wolfgang ; Zimmer, Andreas ; Fuchs, Helmut ; Gailus-Durner, Valérie ; Hrabě de Angelis, Martin ; von Ossowski, Lotta ; Taira, Tomi ; Lappalainen, Pekka ; Rivera, Claudio ; Hotulainen, Pirta. / MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation. In: Developmental Cell. 2015 ; Vol. 33, No. 6. pp. 644-659.

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AU - Fuchs, Helmut

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AU - Hrabě de Angelis, Martin

AU - von Ossowski, Lotta

AU - Taira, Tomi

AU - Lappalainen, Pekka

AU - Rivera, Claudio

AU - Hotulainen, Pirta

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N2 - Proper morphogenesis of neuronal dendritic spines is essential for the formation of functional synaptic networks. However, it is not known how spines are initiated. Here, we identify the inverse-BAR (I-BAR) protein MIM/MTSS1 as a nucleator of dendritic spines. MIM accumulated to future spine initiation sites in a PIP2-dependent manner and deformed the plasma membrane outward into a proto-protrusion via its I-BAR domain. Unexpectedly, the initial protrusion formation did not involve actin polymerization. However, PIP2-dependent activation of Arp2/3-mediated actin assembly was required for protrusion elongation. Overexpression of MIM increased the density of dendritic protrusions and suppressed spine maturation. In contrast, MIM deficiency led to decreased density of dendritic protrusions and larger spine heads. Moreover, MIM-deficient mice displayed altered glutamatergic synaptic transmission and compatible behavioral defects. Collectively, our data identify an important morphogenetic pathway, which initiates spine protrusions by coupling phosphoinositide signaling, direct membrane bending, and actin assembly to ensure proper synaptogenesis.

AB - Proper morphogenesis of neuronal dendritic spines is essential for the formation of functional synaptic networks. However, it is not known how spines are initiated. Here, we identify the inverse-BAR (I-BAR) protein MIM/MTSS1 as a nucleator of dendritic spines. MIM accumulated to future spine initiation sites in a PIP2-dependent manner and deformed the plasma membrane outward into a proto-protrusion via its I-BAR domain. Unexpectedly, the initial protrusion formation did not involve actin polymerization. However, PIP2-dependent activation of Arp2/3-mediated actin assembly was required for protrusion elongation. Overexpression of MIM increased the density of dendritic protrusions and suppressed spine maturation. In contrast, MIM deficiency led to decreased density of dendritic protrusions and larger spine heads. Moreover, MIM-deficient mice displayed altered glutamatergic synaptic transmission and compatible behavioral defects. Collectively, our data identify an important morphogenetic pathway, which initiates spine protrusions by coupling phosphoinositide signaling, direct membrane bending, and actin assembly to ensure proper synaptogenesis.

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