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Cited by 47Cellular transport and secretionLipid Membrane Structure and BehaviorProtein Kinase Regulation and GTPase Signaling

BIN1 Membrane Curvature Sensing and Generation Show Autoinhibition Regulated by Downstream Ligands and PI(4,5)P2

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Wu, Tingting, Baumgart, Tobias·2014·Biochemistry
DOI 10.1021/bi501082rPMC PMC4245986
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Abstract

In striated muscles, invaginations from the plasma membrane, termed transverse tubules (T-tubule), function in the excitation-contraction coupling machinery. BIN1 (isoform8) plays a critical role in the biogenesis of T-tubules. BIN1 contains an N-terminal BAR domain to sense and induce membrane curvature, an isoform8-specific polybasic motif (exon10) as the phosphoinositide binding module and a C-terminal Src homology 3 (SH3) domain for the recruitment of downstream proteins such as dynamin 2. Previous studies of N-BAR domains focused on elucidating mechanisms of membrane curvature sensing and generation (MC-S&G). Less is known about how MC-S&G is regulated. We found that the SH3 domain binds to the exon10 motif more strongly compared to the proline-rich domain (PRD) of dynamin 2. Furthermore, we found that the MC-S&G ability of full-length BIN1 is inhibited on membranes lacking PI(4,5)P2. Addition of PI(4,5)P2 in the membrane activates BIN1 to sense and induce membrane curvature. Co-presence of the SH3 domain and exon10 motif leads to the strongest phosphoinositide-mediated control of BIN1 function. Addition of SH3 domain ligand (such as PRD peptides), as well as addition of the water-soluble PI(4,5)P2 analogue, can both enhance the MC-S&G ability of BIN1 on membranes without PI(4,5)P2, indicating that the key to activate BIN1 is to disrupt the exon10-SH3 interaction. The nonsense mutation K436X, found in centronuclear myopathy (CNM) patients, abolishes SH3 domain binding with either exon10 or the PRD motif, resulting in increased membrane deformation capacity. Our results suggest an autoinhibition model for BIN1 that involves a synergistic regulation by membrane composition and protein-protein interactions.

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Cited by

Sorted by citations

Authors
Wu, T., & Baumgart, T.
Affiliations
University of Pennsylvania (US)
Corresponding author
Baumgart, Tobias
ORCID
Baumgart, Tobias
Venue
Biochemistry
Publisher
American Chemical Society (ACS)
Published
2014-10-28
Volume
53
Issue
46
Pages
7297-7309
ISSN
  • 0006-2960 (ISSN-L)
  • 1520-4995
DOI
10.1021/bi501082r
PMC
PMC4245986
OpenAlex
W2332728879
Cited by
47
References
2
Citations by year
2026: 2 · 2025: 3 · 2024: 10 · 2023: 2 · 2022: 6 · 2021: 3 · 2020: 5 · 2019: 2 · 2018: 5 · 2017: 3 · 2016: 4 · 2015: 1
FWCI
1.33
Type
journal article
Language
en
Open access
Licence
Locations
  • Biochemistry (publishedVersion, other-oa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Institute of General Medical Sciences (R01 GM097552)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Keywords
BIN1, T-tubules, excitation-contraction coupling, BAR domain, SH3 domain, dynamin 2, phosphatidylinositol 4,5-bisphosphate, autoinhibition, centronuclear myopathy, striated muscle, membrane deformation
MeSH terms
Amino Acid Sequence, Cell Line, Cell Membrane, Humans, Liposomes, Molecular Sequence Data, Nuclear Proteins, Phosphatidylinositols, src Homology Domains, Tumor Suppressor Proteins, Dynamin II, Adaptor Proteins, Signal Transducing, Protein Interaction Maps

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