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An Adaptable Spectrin/Ankyrin-Based Mechanism for Long-Range Organization of Plasma Membranes in Vertebrate Tissues.

Publication ,  Journal Article
Bennett, V; Lorenzo, DN
Published in: Curr Top Membr
2016

Ankyrins are membrane-associated proteins that together with their spectrin partners are responsible for micron-scale organization of vertebrate plasma membranes, including those of erythrocytes, excitable membranes of neurons and heart, lateral membrane domains of columnar epithelial cells, and striated muscle. Ankyrins coordinate functionally related membrane transporters and cell adhesion proteins (15 protein families identified so far) within plasma membrane compartments through independently evolved interactions of intrinsically disordered sequences with a highly conserved peptide-binding groove formed by the ANK repeat solenoid. Ankyrins are coupled to spectrins, which are elongated organelle-sized proteins that form mechanically resilient arrays through cross-linking by specialized actin filaments. In addition to protein interactions, cellular targeting and assembly of spectrin/ankyrin domains also critically depend on palmitoylation of ankyrin-G by aspartate-histidine-histidine-cysteine 5/8 palmitoyltransferases, as well as interaction of beta-2 spectrin with phosphoinositide lipids. These lipid-dependent spectrin/ankyrin domains are not static but are locally dynamic and determine membrane identity through opposing endocytosis of bulk lipids as well as specific proteins. A partnership between spectrin, ankyrin, and cell adhesion molecules first emerged in bilaterians over 500 million years ago. Ankyrin and spectrin may have been recruited to plasma membranes from more ancient roles in organelle transport. The basic bilaterian spectrin-ankyrin toolkit markedly expanded in vertebrates through gene duplications combined with variation in unstructured intramolecular regulatory sequences as well as independent evolution of ankyrin-binding activity by ion transporters involved in action potentials and calcium homeostasis. In addition, giant vertebrate ankyrins with specialized roles in axons acquired new coding sequences by exon shuffling. We speculate that early axon initial segments and epithelial lateral membranes initially were based on spectrin-ankyrin-cell adhesion molecule assemblies and subsequently served as "incubators," where ion transporters independently acquired ankyrin-binding activity through positive selection.

Duke Scholars

Published In

Curr Top Membr

DOI

ISSN

1063-5823

Publication Date

2016

Volume

77

Start / End Page

143 / 184

Location

United States

Related Subject Headings

  • Vertebrates
  • Spectrin
  • Humans
  • Cell Membrane
  • Biophysics
  • Ankyrins
  • Animals
  • Adaptation, Physiological
  • 3101 Biochemistry and cell biology
  • 0601 Biochemistry and Cell Biology
 

Citation

APA
Chicago
ICMJE
MLA
NLM
Bennett, V., & Lorenzo, D. N. (2016). An Adaptable Spectrin/Ankyrin-Based Mechanism for Long-Range Organization of Plasma Membranes in Vertebrate Tissues. Curr Top Membr, 77, 143–184. https://doi.org/10.1016/bs.ctm.2015.10.001
Bennett, Vann, and Damaris N. Lorenzo. “An Adaptable Spectrin/Ankyrin-Based Mechanism for Long-Range Organization of Plasma Membranes in Vertebrate Tissues.Curr Top Membr 77 (2016): 143–84. https://doi.org/10.1016/bs.ctm.2015.10.001.
Bennett, Vann, and Damaris N. Lorenzo. “An Adaptable Spectrin/Ankyrin-Based Mechanism for Long-Range Organization of Plasma Membranes in Vertebrate Tissues.Curr Top Membr, vol. 77, 2016, pp. 143–84. Pubmed, doi:10.1016/bs.ctm.2015.10.001.
Journal cover image

Published In

Curr Top Membr

DOI

ISSN

1063-5823

Publication Date

2016

Volume

77

Start / End Page

143 / 184

Location

United States

Related Subject Headings

  • Vertebrates
  • Spectrin
  • Humans
  • Cell Membrane
  • Biophysics
  • Ankyrins
  • Animals
  • Adaptation, Physiological
  • 3101 Biochemistry and cell biology
  • 0601 Biochemistry and Cell Biology