MIM-Induced Membrane Bending Promotes Dendritic Spine Initiation

Dev Cell. 2015 Jun 22;33(6):644-59. doi: 10.1016/j.devcel.2015.04.014. Epub 2015 Jun 4.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin-Related Protein 2-3 Complex / metabolism
  • Actins / metabolism
  • Animals
  • Behavior, Animal / physiology
  • Cerebellum / metabolism
  • Dendritic Spines / physiology*
  • Dendritic Spines / ultrastructure
  • Female
  • Hippocampus / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microfilament Proteins / deficiency
  • Microfilament Proteins / genetics
  • Microfilament Proteins / physiology*
  • Models, Neurological
  • Neoplasm Proteins / deficiency
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Nerve Net / growth & development
  • Nerve Net / physiology
  • Nerve Net / ultrastructure
  • Neurogenesis / genetics
  • Neurogenesis / physiology*
  • Phosphatidylinositol 4,5-Diphosphate / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Synapses / physiology
  • Synapses / ultrastructure
  • Synaptic Transmission / genetics
  • Synaptic Transmission / physiology
  • Tissue Distribution

Substances

  • Actin-Related Protein 2-3 Complex
  • Actins
  • Microfilament Proteins
  • Mtss1 protein, mouse
  • Neoplasm Proteins
  • Phosphatidylinositol 4,5-Diphosphate
  • RNA, Messenger