Amino- and carboxyl-terminal domains of Filamin-A interact with CRMP1 to mediate Sema3A signalling

Nakamura, Fumio; Kumeta, Kosuke; Hida, Tomonobu; Isono, Toshinari; Nakayama, Yuichiro; Kuramata-Matsuoka, Emiko; Yamashita, Naoya; Uchida, Yutaka; Ogura, Ken-ichi; Gengyo-Ando, Keiko; Mitani, Shohei; Ogino, Toshio; Goshima, Yoshio

doi:10.1038/ncomms6325

Cited by 43 publications

(42 citation statements)

References 56 publications

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“…Of particular interest were the proteins dihydropyrimidinase like 2 (DPYSL2, also known as collapsing response mediator protein 2, CRMP2), and secreted protein acidic and cysteine rich (SPARC). DPYSL2 is a microtubule‐associated protein involved in semaphorin signaling that is phosphorylated by Cdk5 at Ser522 to regulate actin reorganization in growth cones (Nakamura et al, ; Uchida et al, ), and dendritic patterning in vivo (Jin et al, ; Yamashita et al, ). DPYSL2 knockout results in reduced dendritic spine density (Hiroko et al, ), and its dysfunction has been implicated in neurodevelopmental and psychiatric disorders with delayed onset, such as autism spectrum disorders and schizophrenia (Beasley et al, ; Hong et al, ).…”

Section: Discussionmentioning

confidence: 99%

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Stimulus‐dependent modifications in astrocyte‐derived extracellular vesicle cargo regulate neuronal excitability

Chaudhuri

Dasgheyb

DeVine

et al. 2019

Glia

107

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Extracellular vesicles have now emerged as key players in cell‐to‐cell communication. This is particularly important in the central nervous system, where glia–neuron cross‐talk helps maintain normal neuronal function. Astrocyte‐derived extracellular vesicles (ADEVs) secreted constitutively promote neurite outgrowth and neuronal survival. However, extracellular stimuli can alter the cargo and downstream functions of ADEVs. For example, ADEVs secreted in response to inflammation contain cargo microRNAs and proteins that reduce neurite outgrowth, neuronal firing, and promote neuronal apoptosis. We performed a comprehensive quantitative proteomic analysis to enumerate the proteomic cargo of ADEVs secreted in response to multiple stimuli. Rat primary astrocytes were stimulated with a trophic stimulus (adenosine triphosphate, ATP), an inflammatory stimulus (IL‐1β) or an anti‐inflammatory stimulus (IL10) and extracellular vesicles secreted within a 2 hr time frame were collected using sequential ultracentrifugation method. ADEVs secreted constitutively without exposure to any stimulus were used a control. A tandem mass tag‐based proteomic platform was used to identify and quantify proteins in the ADEVs. Ingenuity pathway analysis was performed to predict the downstream signaling events regulated by ADEVs. We found that in response to ATP or IL10, ADEVs contain a set of proteins that are involved in increasing neurite outgrowth, dendritic branching, regulation of synaptic transmission, and promoting neuronal survival. In contrast, ADEVs secreted in response to IL‐1β contain proteins that regulate peripheral immune response and immune cell trafficking to the central nervous system.

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Section: Discussionmentioning

confidence: 99%

“…DPYSL2 is a microtubule-associated protein involved in semaphorin signaling that is phosphorylated by Cdk5 at Ser522 to regulate actin reorganization in growth cones (Nakamura et al, 2014;Uchida et al, 2005), and dendritic patterning in vivo (Jin et al, 2016;Yamashita et al, 2012).…”

Section: Adev-il-10mentioning

confidence: 99%

Stimulus‐dependent modifications in astrocyte‐derived extracellular vesicle cargo regulate neuronal excitability

Chaudhuri

Dasgheyb

DeVine

et al. 2019

Glia

107

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“…; Nakamura et al . ). Phosphorylation of the C‐terminal tail of CRMPs may regulate the interactions with their binding partners.…”

Section: Introductionmentioning

confidence: 97%

CRMP1 and CRMP2 have synergistic but distinct roles in dendritic development

et al. 2016

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Collapsin response mediator protein 2, CRMP2, has been identified as an intracellular signaling mediator for Semaphorin 3A (Sema3A). CRMP2 plays a key role in axon guidance, dendritic morphogenesis, and cell polarization. It has been also implicated in a variety of neurological and psychiatric disorders. However, the in vivo functions of CRMP2 remain unknown. We generated CRMP2 gene-deficient (crmp2 À/À ) mice. The crmp2 À/À mice showed irregular development of dendritic spines in cortical neurons. The density of dendritic spines was reduced in the cortical layer V pyramidal neurons of crmp2 À/À mice as well as in those of sema3A À/À and crmp1 À/À mice. However, no abnormality was found in dendritic patterning in crmp2 À/À compared to wild-type (WT) neurons. The level of CRMP1 was increased in crmp2, but the level of CRMP2 was not altered in crmp1 À/À compared to WT cortical brain lysates.Dendritic spine density and branching were reduced in double-heterozygous sema3A +/À ;crmp2 +/À and sema3A +/À ;crmp1 +/À mice. The phenotypic defects had no genetic interaction between crmp1 and crmp2. These findings suggest that both CRMP1 and CRMP2 mediate Sema3A signaling to regulate dendritic spine maturation and patterning, but through overlapping and distinct signaling pathways.

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“…In other systems, CRMP proteins like UNC-33 are implicated in the kinesin-mediated transport of WASP and WAVE complexes (Kawano et al 2005). UNC-33 might also directly facilitate actin cytoskeleton remodeling through its interaction with FLN-1, an actin-binding protein (Nakamura et al 2014). Similar to UNC-44, ERM-1, a member of the ezrin/radixin/moesin family of proteins implicated in linking plasma membrane receptors to the actin cytoskeleton is required in axon guidance, and may be involved in guidance receptor signaling (Teulière et al 2011).…”

Section: Regulation Of the Actin Cytoskeleton In Axon Outgrowthmentioning

confidence: 99%

The Genetics of Axon Guidance and Axon Regeneration in Caenorhabditis elegans

Chisholm¹,

Hutter

Jin

et al. 2016

Genetics

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The correct wiring of neuronal circuits depends on outgrowth and guidance of neuronal processes during development. In the past two decades, great progress has been made in understanding the molecular basis of axon outgrowth and guidance. Genetic analysis in Caenorhabditis elegans has played a key role in elucidating conserved pathways regulating axon guidance, including Netrin signaling, the slit Slit/Robo pathway, Wnt signaling, and others. Axon guidance factors were first identified by screens for mutations affecting animal behavior, and by direct visual screens for axon guidance defects. Genetic analysis of these pathways has revealed the complex and combinatorial nature of guidance cues, and has delineated how cues guide growth cones via receptor activity and cytoskeletal rearrangement. Several axon guidance pathways also affect directed migrations of non-neuronal cells in C. elegans, with implications for normal and pathological cell migrations in situations such as tumor metastasis. The small number of neurons and highly stereotyped axonal architecture of the C. elegans nervous system allow analysis of axon guidance at the level of single identified axons, and permit in vivo tests of prevailing models of axon guidance. C. elegans axons also have a robust capacity to undergo regenerative regrowth after precise laser injury (axotomy). Although such axon regrowth shares some similarities with developmental axon outgrowth, screens for regrowth mutants have revealed regenerationspecific pathways and factors that were not identified in developmental screens. Several areas remain poorly understood, including how major axon tracts are formed in the embryo, and the function of axon regeneration in the natural environment. KEYWORDS netrin; semaphorin; ephrin; Wnt; Slit; Robo; fasciculation; DLK; growth cone; actin; microtubule; WormBook

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Amino- and carboxyl-terminal domains of Filamin-A interact with CRMP1 to mediate Sema3A signalling

Cited by 43 publications

References 56 publications

Stimulus‐dependent modifications in astrocyte‐derived extracellular vesicle cargo regulate neuronal excitability

Stimulus‐dependent modifications in astrocyte‐derived extracellular vesicle cargo regulate neuronal excitability

CRMP1 and CRMP2 have synergistic but distinct roles in dendritic development

The Genetics of Axon Guidance and Axon Regeneration in Caenorhabditis elegans

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