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An adaptable ankyrin-based mechanism for vertebrate (...)

Lundi 14 septembre 2015 - 11 heures.

Docteur Vann BENNETT Duke University, USA.

An adaptable ankyrin-based mechanism for vertebrate evolution of specialized plasma membranes.

Invité par Christophe LETERRIER – CRN2M UMR7286 - tél : 04 91 69 89 30.

Résumé :

Ankyrins are membrane-associated proteins that together with their spectrin partners promote assembly of specialized vertebrate plasma membranes, including those of erythrocytes, excitable membranes of neurons and heart, lateral membrane domains of columnar epithelial cells, and costameres of 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 bind to spectrins, which are elongated organelle-sized proteins that form mechanically resilient arrays through crosslinking by specialized actin filaments. Spectrin and ankyrin form microdomains that depend on palmitoylation of ankyrin-G, as well as interaction of beta-2 spectin with phosphoinositide lipids. Spectrin/ankyrin-based microdomains 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. This basic 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 such as voltage-gated sodium channels. 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 included spectrin-ankyrin-cell adhesion molecule assemblies and subsequently served as “incubators”, where ion transporters acquired ankyrin-binding activity through positive selection.

Bibliographie :

Tseng WC, Jenkins PM, Tanaka M, Mooney R, Bennett V. Giant ankyrin-G stabilizes somatodendritic GABAergic synapses through opposing endocytosis of GABAA receptors. Proc Natl Acad Sci U S A. 2015 Jan 27 ;112(4):1214-9. doi : 10.1073/pnas.1417989112. Epub 2014 Dec 31. PubMed PMID : 25552561 ; PubMed Central PMCID : PMC4313813.

Jenkins PM, Kim N, Jones SL, Tseng WC, Svitkina TM, Yin HH, Bennett V. Giant ankyrin-G : a critical innovation in vertebrate evolution of fast and integrated neuronal signaling. Proc Natl Acad Sci U S A. 2015 Jan 27 ;112(4):957-64. doi : 10.1073/pnas.1416544112. Epub 2014 Dec 31. PubMed PMID : 25552556 ; PubMed Central PMCID : PMC4313853.

Zhong G, He J, Zhou R, Lorenzo D, Babcock HP, Bennett V, Zhuang X. Developmental mechanism of the periodic membrane skeleton in axons. Elife. 2014 Dec 23 ;3. doi : 10.7554/eLife.04581. PubMed PMID : 25535840 ; PubMed Central PMCID : PMC4337613.

Lorenzo DN, Badea A, Davis J, Hostettler J, He J, Zhong G, Zhuang X, Bennett V. A PIK3C3-ankyrin-B-dynactin pathway promotes axonal growth and multiorganelle transport. J Cell Biol. 2014 Dec 22 ;207(6):735-52. doi : 10.1083/jcb.201407063. PubMed PMID : 25533844 ; PubMed Central PMCID : PMC4274267.

Wang C, Wei Z, Chen K, Ye F, Yu C, Bennett V, Zhang M. Structural basis of diverse membrane target recognitions by ankyrins. Elife. 2014 Nov 10 ;3. doi : 10.7554/eLife.04353. PubMed PMID : 25383926 ; PubMed Central PMCID : PMC4358367.

Ho TS, Zollinger DR, Chang KJ, Xu M, Cooper EC, Stankewich MC, Bennett V, Rasband MN. A hierarchy of ankyrin-spectrin complexes clusters sodium channels at nodes of Ranvier. Nat Neurosci. 2014 Dec ;17(12):1664-72. doi : 10.1038/nn.3859. Epub 2014 Nov 2. PubMed PMID : 25362473 ; PubMed Central PMCID : PMC4271271.

Chang KJ, Zollinger DR, Susuki K, Sherman DL, Makara MA, Brophy PJ, Cooper EC, Bennett V, Mohler PJ, Rasband MN. Glial ankyrins facilitate paranodal axoglial junction assembly. Nat Neurosci. 2014 Dec ;17(12):1673-81. doi : 10.1038/nn.3858. Epub 2014 Nov 2. PubMed PMID : 25362471 ; PubMed Central PMCID : PMC4260775.

He M, Abdi KM, Bennett V. Ankyrin-G palmitoylation and βII-spectrin binding to phosphoinositide lipids drive lateral membrane assembly. J Cell Biol. 2014 Jul 21 ;206(2):273-88. doi : 10.1083/jcb.201401016. PubMed PMID : 25049274 ; PubMed Central PMCID : PMC4107783.

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