Tau phosphorylation regulates the interaction between BIN1’s SH3 domain and Tau’s proline-rich domain

Sottejeau, Yoann; Bretteville, Alexis; Cantrelle, François-Xavier; Malmanche, Nicolas; Demiaute, Florie; Mendes, Tiago; Delay, Charlotte; Alves, Harmony Alves Dos; Flaig, Amandine; Davies, Peter; Dourlen, Pierre; Dermaut, Bart; Laporte, Jocelyn; Amouyel, Philippe; Lippens, Guy; Chapuis, Julien; Landrieu, Isabelle; Lambert, Jean‐Charles

doi:10.1186/s40478-015-0237-8

Cited by 69 publications

(108 citation statements)

References 32 publications

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“…Direct interactions between tau and SH3-containing proteins have been reported [36, 273, 278, 411, 462, 483] and these interactions are likely to have roles in modulating the signalling functions of tau. Additionally, signalling roles have been postulated from the identification of phosphatidylinositol and phosphatidylinositol bisphosphate as tau binding partners of the proline-rich domain [134, 468].…”

Section: Tau Structure and Functionmentioning

confidence: 99%

Roles of tau protein in health and disease

2017

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Tau is well established as a microtubule-associated protein in neurons. However, under pathological conditions, aberrant assembly of tau into insoluble aggregates is accompanied by synaptic dysfunction and neural cell death in a range of neurodegenerative disorders, collectively referred to as tauopathies. Recent advances in our understanding of the multiple functions and different locations of tau inside and outside neurons have revealed novel insights into its importance in a diverse range of molecular pathways including cell signalling, synaptic plasticity, and regulation of genomic stability. The present review describes the physiological and pathophysiological properties of tau and how these relate to its distribution and functions in neurons. We highlight the post-translational modifications of tau, which are pivotal in defining and modulating tau localisation and its roles in health and disease. We include discussion of other pathologically relevant changes in tau, including mutation and aggregation, and how these aspects impinge on the propensity of tau to propagate, and potentially drive neuronal loss, in diseased brain. Finally, we describe the cascade of pathological events that may be driven by tau dysfunction, including impaired axonal transport, alterations in synapse and mitochondrial function, activation of the unfolded protein response and defective protein degradation. It is important to fully understand the range of neuronal functions attributed to tau, since this will provide vital information on its involvement in the development and pathogenesis of disease. Such knowledge will enable determination of which critical molecular pathways should be targeted by potential therapeutic agents developed for the treatment of tauopathies.

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Section: Tau Structure and Functionmentioning

confidence: 99%

Roles of tau protein in health and disease

2017

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“…In addition, in a Drosophila melanogaster model overexpressing Tau, bin1 homologue Amph mediates Tau toxicity [11,16], and an increase in bin1 expression is observed in AD [11]. In line with Tau, it has been suggested that the BIN1-Tau complex could be at the interface between the actin and microtubule network and that its deregulation may impact neuronal function [12]. In line with Tau, it has been suggested that the BIN1-Tau complex could be at the interface between the actin and microtubule network and that its deregulation may impact neuronal function [12].…”

Section: Introductionmentioning

confidence: 98%

“…BIN1 has been described to directly interact with the Tau protein [11,12], using NMR spectroscopy with recombinant proteins, in vitro glutathion S-transferase (GST) pulldown from HEK293 lysates, polymerase ligation assays in primary neuronal culture [12], as well as reciprocal coimmunoprecipitations from wild-type mouse brain homogenates, which confirm interaction at the physiological level [11]. BIN1 has been described to directly interact with the Tau protein [11,12], using NMR spectroscopy with recombinant proteins, in vitro glutathion S-transferase (GST) pulldown from HEK293 lysates, polymerase ligation assays in primary neuronal culture [12], as well as reciprocal coimmunoprecipitations from wild-type mouse brain homogenates, which confirm interaction at the physiological level [11].…”

Section: Introductionmentioning

confidence: 99%

“…This would lead to the propagation of Tau pathology from neuron to neuron after aggregates of Tau permeabilize the endosome membrane [18]. We have previously shown direct interaction of the SH3 domain of BIN1 with the proline-rich domain of Tau (PRD, Tau [165-245]) [12]. Finally, BIN1 has been reported to increase cellular BACE1 levels through impaired endosomal trafficking and reduced BACE1 lysosomal degradation, resulting in increased Ab production [21].…”

Section: Introductionmentioning

confidence: 99%

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Regulation of the interaction between the neuronal BIN1 isoform 1 and Tau proteins – role of the SH3 domain

et al. 2017

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Bridging integrator 1 (bin1) gene is a genetic determinant of Alzheimer's disease (AD) and has been reported to modulate Alzheimer's pathogenesis through pathway(s) involving Tau. The functional impact of Tau/BIN1 interaction as well as the molecular details of this interaction are still not fully resolved. As a consequence, how BIN1 through its interaction with Tau affects AD risk is also still not determined. To progress in this understanding, interaction of Tau with two BIN1 isoforms was investigated using Nuclear Magnetic Resonance spectroscopy. H, N spectra showed that the C-terminal SH3 domain of BIN1 isoform 1 (BIN1Iso1) is not mobile in solution but locked with the core of the protein. In contrast, the SH3 domain of BIN1 isoform 9 (BIN1Iso9) behaves as an independent mobile domain. This reveals an equilibrium between close and open conformations for the SH3 domain. Interestingly, a 334-376 peptide from the clathrin and AP-2-binding domain (CLAP) domain of BIN1Iso1, which contains a SH3-binding site, is able to compete with BIN1-SH3 intramolecular interaction. For both BIN1 isoforms, the SH3 domain can interact with Tau(210-240) sequence. Tau(210-240) peptide can indeed displace the intramolecular interaction of the BIN1-SH3 of BIN1Iso1 and form a complex with the released domain. The measured K were in agreement with a stronger affinity of Tau peptide. Both CLAP and Tau peptides occupied the same surface on the BIN1-SH3 domain, showing that their interaction is mutually exclusive. These results emphasize an additional level of complexity in the regulation of the interaction between BIN1 and Tau dependent of the BIN1 isoforms.

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“…Consistent with the role of BIN1 in myelination, BIN1 expression increases at the onset of postnatal brain myelination and during differentiation of cultured oligodendrocytes [105,106]. In contrast, the loss of BIN1 significantly correlates with the extent of demyelination in MS lesions [105,106]. BIN1 undergoes complex alternative splicing to generate multiple isoforms that have diverse functions [105,106].…”

Section: Tau In Oligodendrocytes and Cns Degenerative Diseasesmentioning

confidence: 84%

Tau in Oligodendrocytes Takes Neurons in Sickness and in Health

LoPresti

2018

IJMS

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Oligodendrocytes (OLGs), the myelin-forming cells of the central nervous system (CNS), are lifelong partners of neurons. They adjust to the functional demands of neurons over the course of a lifetime to meet the functional needs of a healthy CNS. When this functional interplay breaks down, CNS degeneration follows. OLG processes are essential features for OLGs being able to connect with the neurons. As many as fifty cellular processes from a single OLG reach and wrap an equal number of axonal segments. The cellular processes extend to meet and wrap axonal segments with myelin. Further, transport regulation, which is critical for myelination, takes place within the cellular processes. Because the microtubule-associated protein tau plays a crucial role in cellular process extension and myelination, alterations of tau in OLGs have deleterious effects, resulting in neuronal malfunction and CNS degeneration. Here, we review current concepts on the lifelong role of OLGs and myelin for brain health and plasticity. We present key studies of tau in OLGs and select important studies of tau in neurons. The extensive work on tau in neurons has considerably advanced our understanding of how tau promotes either health or disease. Because OLGs are crucial to neuronal health at any age, an understanding of the functions and regulation of tau in OLGs could uncover new therapeutics for selective CNS neurodegenerative diseases.

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Tau phosphorylation regulates the interaction between BIN1’s SH3 domain and Tau’s proline-rich domain

Cited by 69 publications

References 32 publications

Roles of tau protein in health and disease

Roles of tau protein in health and disease

Regulation of the interaction between the neuronal BIN1 isoform 1 and Tau proteins – role of the SH3 domain

Tau in Oligodendrocytes Takes Neurons in Sickness and in Health

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