Amigo Adhesion Protein Regulates Development of Neural Circuits in Zebrafish Brain

Zhao, Xiang; Kuja-Panula, Juha; Sundvik, Maria; Chen, Yu‐Chia; Aho, Velma; Peltola, Marjaana A.; Porkka‐Heiskanen, Tarja; Panula, Pertti; Rauvala, Heikki

doi:10.1074/jbc.m113.545582

Cited by 16 publications

(20 citation statements)

References 47 publications

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“…In addition, we tested if subtle developmental differences across the larvae could lead to differences in activity and radial index. Using larval size and amigo1 gene expression as known reporters of developmental changes during zebrafish development [ 14 , 15 ], we did not find any significant correlation between these reporters and the individual activity or radial index of the population at 7 dpf (Additional file 1 : Figure S3D, E; P > 0.05 for all the comparisons, using two-sided t -tests). Finally, we showed that activity and radial index can describe inter-individual variability not only during free-swimming behavior but also in response to stimuli like light flashes, mechanical perturbation, or being in a novel tank (“ Methods ”; Additional file 1 : Figure S3F).…”

Section: Resultsmentioning

confidence: 98%

Histone H4 acetylation regulates behavioral inter-individual variability in zebrafish

et al. 2018

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BackgroundAnimals can show very different behaviors even in isogenic populations, but the underlying mechanisms to generate this variability remain elusive. We use the zebrafish (Danio rerio) as a model to test the influence of histone modifications on behavior.ResultsWe find that laboratory and isogenic zebrafish larvae show consistent individual behaviors when swimming freely in identical wells or in reaction to stimuli. This behavioral inter-individual variability is reduced when we impair the histone deacetylation pathway. Individuals with high levels of histone H4 acetylation, and specifically H4K12, behave similarly to the average of the population, but those with low levels deviate from it. More precisely, we find a set of genomic regions whose histone H4 acetylation is reduced with the distance between the individual and the average population behavior. We find evidence that this modulation depends on a complex of Yin-yang 1 (YY1) and histone deacetylase 1 (HDAC1) that binds to and deacetylates these regions. These changes are not only maintained at the transcriptional level but also amplified, as most target regions are located near genes encoding transcription factors.ConclusionsWe suggest that stochasticity in the histone deacetylation pathway participates in the generation of genetic-independent behavioral inter-individual variability.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1428-y) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 98%

Histone H4 acetylation regulates behavioral inter-individual variability in zebrafish

et al. 2018

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“…The clustered localization of AMIGO-1 on the soma and proximal dendrites of adult brain neurons is interesting in light of the role of AMIGO-1 during development as an adhesion molecule involved in development of neuronal circuitry. Knockdown of AMIGO-1 expression in developing zebrafish impairs the formation of fasciculated fiber tracts and disturbs the development of dopaminergic circuits (Zhao et al, 2014 ). However there are no gross anatomical abnormalities in the brains of constitutive global AMIGO-1 KO mice (Peltola et al, 2016 ), or, as shown here, in Kv2 dKO mice, which also have greatly reduced levels of AMIGO-1 expression, particularly in the neuronal PM.…”

Section: Discussionmentioning

confidence: 99%

Kv2 Ion Channels Determine the Expression and Localization of the Associated AMIGO-1 Cell Adhesion Molecule in Adult Brain Neurons

Bishop

Cobb

Kirmiz

et al. 2018

Front. Mol. Neurosci.

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137

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Voltage-gated K+ (Kv) channels play important roles in regulating neuronal excitability. Kv channels comprise four principal α subunits, and transmembrane and/or cytoplasmic auxiliary subunits that modify diverse aspects of channel function. AMIGO-1, which mediates homophilic cell adhesion underlying neurite outgrowth and fasciculation during development, has recently been shown to be an auxiliary subunit of adult brain Kv2.1-containing Kv channels. We show that AMIGO-1 is extensively colocalized with both Kv2.1 and its paralog Kv2.2 in brain neurons across diverse mammals, and that in adult brain, there is no apparent population of AMIGO-1 outside of that colocalized with these Kv2 α subunits. AMIGO-1 is coclustered with Kv2 α subunits at specific plasma membrane (PM) sites associated with hypolemmal subsurface cisternae at neuronal ER:PM junctions. This distinct PM clustering of AMIGO-1 is not observed in brain neurons of mice lacking Kv2 α subunit expression. Moreover, in heterologous cells, coexpression of either Kv2.1 or Kv2.2 is sufficient to drive clustering of the otherwise uniformly expressed AMIGO-1. Kv2 α subunit coexpression also increases biosynthetic intracellular trafficking and PM expression of AMIGO-1 in heterologous cells, and analyses of Kv2.1 and Kv2.2 knockout mice show selective loss of AMIGO-1 expression and localization in neurons lacking the respective Kv2 α subunit. Together, these data suggest that in mammalian brain neurons, AMIGO-1 is exclusively associated with Kv2 α subunits, and that Kv2 α subunits are obligatory in determining the correct pattern of AMIGO-1 expression, PM trafficking and clustering.

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“…The AMIGO family with leucine-rich repeats is identified by ordered differential display, which reveals a novel sequence induced by amphoterin, the neurite-stimulating factor [121]. In addition, the role of AMIGO2 in neurovascular units has been demonstrated, such as neuronal development and neural circuit in zebrafish brain [122].…”

Section: Pi3k-akt Pathwaymentioning

confidence: 99%

Regenerative Potential of Carbon Monoxide in Adult Neural Circuits of the Central Nervous System

Jung

Koh

Yoo

et al. 2020

IJMS

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Regeneration of adult neural circuits after an injury is limited in the central nervous system (CNS). Heme oxygenase (HO) is an enzyme that produces HO metabolites, such as carbon monoxide (CO), biliverdin and iron by heme degradation. CO may act as a biological signal transduction effector in CNS regeneration by stimulating neuronal intrinsic and extrinsic mechanisms as well as mitochondrial biogenesis. CO may give directions by which the injured neurovascular system switches into regeneration mode by stimulating endogenous neural stem cells and endothelial cells to produce neurons and vessels capable of replacing injured neurons and vessels in the CNS. The present review discusses the regenerative potential of CO in acute and chronic neuroinflammatory diseases of the CNS, such as stroke, traumatic brain injury, multiple sclerosis and Alzheimer’s disease and the role of signaling pathways and neurotrophic factors. CO-mediated facilitation of cellular communications may boost regeneration, consequently forming functional adult neural circuits in CNS injury.

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Amigo Adhesion Protein Regulates Development of Neural Circuits in Zebrafish Brain

Cited by 16 publications

References 47 publications

Histone H4 acetylation regulates behavioral inter-individual variability in zebrafish

Histone H4 acetylation regulates behavioral inter-individual variability in zebrafish

Kv2 Ion Channels Determine the Expression and Localization of the Associated AMIGO-1 Cell Adhesion Molecule in Adult Brain Neurons

Regenerative Potential of Carbon Monoxide in Adult Neural Circuits of the Central Nervous System

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