Abstract
ABSTRACTThe conspicuous striped coloration of zebrafish is produced by cell-cell interactions among three different types of chromatophores: black melanophores, orange/yellow xanthophores and silvery/blue iridophores. During color pattern formation xanthophores undergo dramatic cell shape transitions and acquire different densities, leading to compact and orange xanthophores at high density in the light stripes, and stellate, faintly pigmented xanthophores at low density in the dark stripes. Here, we investigate the mechanistic basis of these cell behaviors in vivo, and show that local, heterotypic interactions with dense iridophores regulate xanthophore cell shape transition and density. Genetic analysis reveals a cell-autonomous requirement of gap junctions composed of Cx41.8 and Cx39.4 in xanthophores for their iridophore-dependent cell shape transition and increase in density in light-stripe regions. Initial melanophore-xanthophore interactions are independent of these gap junctions; however, subsequently they are also required to induce the acquisition of stellate shapes in xanthophores of the dark stripes. In summary, we conclude that, whereas homotypic interactions regulate xanthophore coverage in the skin, their cell shape transitions and density is regulated by gap junction-mediated, heterotypic interactions with iridophores and melanophores.
Highlights
The striped coloration of adult zebrafish has emerged as a model system to study pattern formation by cell-cell interaction in vivo (Irion et al, 2016; Kelsh, 2004; Parichy and Spiewak, 2015; Singh and Nüsslein-Volhard, 2015; Watanabe and Kondo, 2015)
Gap junctions are membrane channels allowing the communication between neighboring cells, and we have previously shown that two different subunits of gap junctions, Cx41.8 and Cx39.4 encoded by the leopard (Watanabe et al, 2006) and luchs (Irion et al, 2014a) genes, respectively, are required in melanophores and xanthophores, but not in iridophores for normal pattern formation
Xanthophore density is reduced in mutants lacking iridophores, and in mutants lacking functional gap junctions In adult zebrafish xanthophores are present in light stripes and dark stripes
Summary
The striped coloration of adult zebrafish has emerged as a model system to study pattern formation by cell-cell interaction in vivo (Irion et al, 2016; Kelsh, 2004; Parichy and Spiewak, 2015; Singh and Nüsslein-Volhard, 2015; Watanabe and Kondo, 2015). The pattern of longitudinal dark and light stripes on the flank of the fish is composed of black melanophores, orange/yellow xanthophores and silvery or bluish iridophores This color pattern is produced during a phase called metamorphosis, by the precise arrangement and superimposition of all three cell types in the skin of the fish (Hirata et al, 2003, 2005; Parichy et al, 2009). §Present address: Max Planck Institute for Infection Biology, Charitéplatz 1, Berlin 10117, Germany.
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