Specific Sorting and Post-Golgi Trafficking of Dendritic Potassium Channels in Living Neurons

Jensen, Camilla Stampe; Watanabe, Shôji; Rasmussen, Hanne B.; Schmitt, Nicole; Olesen, Søren‐Peter; Frost, Nicholas A.; Blanpied, Thomas A.; Misonou, Hiroaki

doi:10.1074/jbc.m113.534495

Cited by 38 publications

(51 citation statements)

References 51 publications

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“…Furthermore, results of functional experiments where myosin motors were inducibly attached to peroxisomes are consistent with actin filaments in the proximal axon having an overall orientation with plus ends facing the cell body (Watanabe et al, 2012). This orientation for actin filaments was corroborated by superresolution microscopy of GFP-Actin (Jensen et al, 2014)(personal communication).…”

Section: Introductionmentioning

confidence: 73%

Structure and Function of an Actin-Based Filter in the Proximal Axon

et al. 2017

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SUMMARY The essential organization of microtubules within neurons has been described, however, less is known about how neuronal actin is arranged and the functional implications of its arrangement. Here we describe in live cells an actin-based structure in the proximal axon that selectively prevents some proteins from entering the axon, while allowing the passage of others. Concentrated patches of actin in proximal axons are present shortly after axonal specification in rat and zebrafish neurons imaged live, and mark positions where anterogradely traveling vesicles carrying dendritic proteins halt and reverse. Patches colocalize with the ARP2/3 complex, and when ARP2/3-mediated nucleation is blocked a dendritic protein mislocalizes to the axon. Patches are highly dynamic, with few persisting longer than 30 minutes. In neurons in culture and in vivo, actin appears to form a contiguous, semipermeable barrier, despite its apparently sparse distribution, preventing axonal localization of constitutively active Myosin Va, but not Myosin VI.

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Section: Introductionmentioning

confidence: 73%

Structure and Function of an Actin-Based Filter in the Proximal Axon

et al. 2017

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“…2). Additional material was also occasionally observed along the NMII tail and probably corresponded to some of NMII interaction partners, whose list is constantly growing [6, 30–32]. Although the gold-labeled NMII monomers in cells less frequently exhibited clearly discernable heads, as compared with preparations of purified myosin II [26], the narrow range of length and thickness distributions of labeled structures, as well as reproducible labeling at the tips, support the idea that these structures are extended NMII monomers.…”

Section: Resultsmentioning

confidence: 99%

“…Moreover, regulators of NMII polymerization at the heavy chain level are enriched in lamellipodia and affect protrusive activity [35–38], thus supporting an idea that NMII monomers are produced within lamellipodia and may provide traction for lamellipodial protrusion by inducing nascent adhesions. Activated NMII monomers can also account for unconventional functions of NMII in membrane organelle dynamics [3–7, 22, 30]. The role of NMII in these processes is often explained by contractile activity of bipolar filaments, which form structures analogous to cytokinetic contractile rings.…”

Section: Discussionmentioning

confidence: 99%

Endogenous Species of Mammalian Nonmuscle Myosin IIA and IIB Include Activated Monomers and Heteropolymers

et al. 2014

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Summary Background Class II myosins generate contractile forces in cells by polymerizing into bipolar filaments and pulling on anchored actin filaments. Nonmuscle myosin II (NMII) plays central roles during cell adhesion, migration, cytokinesis, and tissue morphogenesis. NMII is present in virtually all mammalian cell types as tissue-specific combinations of NMIIA, NMIIB, and NMIIC isoforms. It remains poorly understood how the highly dynamic NMII-actin contractile system begins to assemble at new cellular locations during cell migration and how incorporation of different NMII isoforms into this system is coordinated. Results Using platinum replica electron microscopy in combination with immunogold labeling, we demonstrate that individual activated (phosphorylated on the regulatory light chain and unfolded) NMIIA and NMIIB molecules represent a functional form of NMII in motile cells and that NMIIA and NMIIB copolymerize into nascent bipolar filaments during contractile system assembly. Using subdiffraction STED microscopy together with a pharmacological block-and-release approach, we report that NMIIA and NMIIB simultaneously incorporate into the cytoskeleton during initiation of contractile system assembly, whereas the characteristic rearward shift of NMIIB relative to NMIIA is established later in the course of NMII turnover. Conclusions We show existence of activated NMII monomers in cells, copolymerization of endogenous NMIIA and NMIIB molecules, and contribution of both isoforms, rather than only NMIIA, to early stages of the contractile system assembly. These data change the current paradigms about dynamics and functions of NMII and provide new conceptual insights into organization and dynamics of the ubiquitous cellular machinery for contraction that acts in multiple cellular contexts.

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“…Quantitative immunogold labeling of SDS-FRL samples from adult rat CA1 reveals substantial Kv2.1 labeling on the proximal dendrites, and no detectable labeling at any site distal to this (Kirizs et al, 2014). Live cell imaging of cultured neurons reveals that Kv2.1 is carried in transport vesicles distinct from those containing distally directed Kv4.2, and that selective interaction of Kv2.1-containing vesicles with myosin II is crucial to their proximal localization, perhaps through interaction with a distinct pool of randomly oriented actin filaments present in proximal but not distal dendrites (Jensen et al, 2014). Kv2.1 (Figure 3E) (Trimmer, 1991) and Kv2.2 (Kihira et al, 2010) are prominently expressed in large clusters on somata that define a novel neuronal plasma membrane domain located over subsurface cisternae (Du et al, 1998; Mandikian et al, 2014), sites of intracellular Ca 2+ release, that in certain neurons contain high densities of ryanodine receptor release channels (Figure 3E) that are juxtaposed to plasma membrane Kv2.1 labeling (Antonucci et al, 2001; Mandikian et al, 2014; Misonou et al, 2005).…”

Section: Kv2 Channels: Unique Localization In Proximal Dendritesmentioning

confidence: 99%

Subcellular Localization of K+ Channels in Mammalian Brain Neurons: Remarkable Precision in the Midst of Extraordinary Complexity

Trimmer

2015

Neuron

207

221

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Potassium channels (KChs) are the most diverse ion channels, in part due to extensive combinatorial assembly of a large number of principal and auxiliary subunits into an assortment of KCh complexes. This structural and functional diversity allows KChs to play diverse roles in neuronal function. Localization of KChs within specialized neuronal compartments defines their physiological role, and also fundamentally impacts their activity, due to localized exposure to diverse cellular determinants of channel function. Recent studies in mammalian brain reveal an exquisite refinement of KCh subcellular localization. This includes axonal KChs at the initial segment, and near/within nodes of Ranvier and presynaptic terminals, dendritic KChs found at sites reflecting specific synaptic input, and KChs defining novel compartments. Painting the remarkable diversity of KChs onto the complex architecture of mammalian neurons creates an elegant picture of electrical signal processing underlying the sophisticated function of individual neuronal compartments, and ultimately neurotransmission and behavior.

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Specific Sorting and Post-Golgi Trafficking of Dendritic Potassium Channels in Living Neurons

Abstract: Background: Voltage-gated K ϩ (Kv) channels are localized in specific dendritic subcompartments of neurons to regulate

Cited by 38 publications

References 51 publications

Structure and Function of an Actin-Based Filter in the Proximal Axon

Structure and Function of an Actin-Based Filter in the Proximal Axon

Endogenous Species of Mammalian Nonmuscle Myosin IIA and IIB Include Activated Monomers and Heteropolymers

Subcellular Localization of K+ Channels in Mammalian Brain Neurons: Remarkable Precision in the Midst of Extraordinary Complexity

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