Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin i

Dennis Koch, Isabella Spiwoks-Becker, Victor Sabanov, Anne Sinning, Tamar Dugladze, Anne Stellmacher, Rashmi Ahuja, Julia Grimm, Susann Schüler, Anke Müller, Frank Angenstein, Tariq Ahmed, Alexander Diesler, Markus Moser, Susanne Tom Dieck, Rainer Spessert, Tobias Maria Boeckers, Reinhard Fässler, Christian Andreas Hübner, Detlef Balschun & 3 others Tengis Gloveli, Michael Manfred Kessels, Britta Qualmann

Research output: Contribution to journalArticle

46 Citations (Scopus)

Abstract

Synaptic transmission relies on effective and accurate compensatory endocytosis. F-BAR proteins may serve as membrane curvature sensors and/or inducers and thereby support membrane remodelling processes; yet, their in vivo functions urgently await disclosure. We demonstrate that the F-BAR protein syndapin I is crucial for proper brain function. Syndapin I knockout (KO) mice suffer from seizures, a phenotype consistent with excessive hippocampal network activity. Loss of syndapin I causes defects in presynaptic membrane trafficking processes, which are especially evident under high-capacity retrieval conditions, accumulation of endocytic intermediates, loss of synaptic vesicle (SV) size control, impaired activity-dependent SV retrieval and defective synaptic activity. Detailed molecular analyses demonstrate that syndapin I plays an important role in the recruitment of all dynamin isoforms, central players in vesicle fission reactions, to the membrane. Consistently, syndapin I KO mice share phenotypes with dynamin I KO mice, whereas their seizure phenotype is very reminiscent of fitful mice expressing a mutant dynamin. Thus, syndapin I acts as pivotal membrane anchoring factor for dynamins during regeneration of SVs.

Original languageEnglish
Pages (from-to)4955-4969
Number of pages15
JournalEMBO Journal
Volume30
Issue number24
DOIs
Publication statusPublished - 14 Dec 2011
Externally publishedYes

Fingerprint

Synaptic Vesicles
Dynamins
Membranes
Knockout Mice
Phenotype
Seizures
Dynamin I
Fission reactions
Disclosure
Endocytosis
Synaptic Transmission
Regeneration
Brain
Protein Isoforms
Proteins
Defects
Sensors

Keywords

  • F-BAR protein syndapin/PACSIN
  • membrane recruitment of dynamins
  • rod photoreceptor ribbon synapses
  • seizures with tonic-clonic convulsions
  • SV formation and recycling

ASJC Scopus subject areas

  • Neuroscience(all)
  • Molecular Biology
  • Immunology and Microbiology(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Koch, D., Spiwoks-Becker, I., Sabanov, V., Sinning, A., Dugladze, T., Stellmacher, A., ... Qualmann, B. (2011). Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin i. EMBO Journal, 30(24), 4955-4969. https://doi.org/10.1038/emboj.2011.339

Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin i. / Koch, Dennis; Spiwoks-Becker, Isabella; Sabanov, Victor; Sinning, Anne; Dugladze, Tamar; Stellmacher, Anne; Ahuja, Rashmi; Grimm, Julia; Schüler, Susann; Müller, Anke; Angenstein, Frank; Ahmed, Tariq; Diesler, Alexander; Moser, Markus; Tom Dieck, Susanne; Spessert, Rainer; Boeckers, Tobias Maria; Fässler, Reinhard; Hübner, Christian Andreas; Balschun, Detlef; Gloveli, Tengis; Kessels, Michael Manfred; Qualmann, Britta.

In: EMBO Journal, Vol. 30, No. 24, 14.12.2011, p. 4955-4969.

Research output: Contribution to journalArticle

Koch, D, Spiwoks-Becker, I, Sabanov, V, Sinning, A, Dugladze, T, Stellmacher, A, Ahuja, R, Grimm, J, Schüler, S, Müller, A, Angenstein, F, Ahmed, T, Diesler, A, Moser, M, Tom Dieck, S, Spessert, R, Boeckers, TM, Fässler, R, Hübner, CA, Balschun, D, Gloveli, T, Kessels, MM & Qualmann, B 2011, 'Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin i', EMBO Journal, vol. 30, no. 24, pp. 4955-4969. https://doi.org/10.1038/emboj.2011.339
Koch D, Spiwoks-Becker I, Sabanov V, Sinning A, Dugladze T, Stellmacher A et al. Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin i. EMBO Journal. 2011 Dec 14;30(24):4955-4969. https://doi.org/10.1038/emboj.2011.339
Koch, Dennis ; Spiwoks-Becker, Isabella ; Sabanov, Victor ; Sinning, Anne ; Dugladze, Tamar ; Stellmacher, Anne ; Ahuja, Rashmi ; Grimm, Julia ; Schüler, Susann ; Müller, Anke ; Angenstein, Frank ; Ahmed, Tariq ; Diesler, Alexander ; Moser, Markus ; Tom Dieck, Susanne ; Spessert, Rainer ; Boeckers, Tobias Maria ; Fässler, Reinhard ; Hübner, Christian Andreas ; Balschun, Detlef ; Gloveli, Tengis ; Kessels, Michael Manfred ; Qualmann, Britta. / Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin i. In: EMBO Journal. 2011 ; Vol. 30, No. 24. pp. 4955-4969.
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