Gene Expression Analysis of Zebrafish Melanocytes, Iridophores, and Retinal Pigmented Epithelium Reveals Indicators of Biological Function and Developmental Origin

Higdon, Charles W.; Mitra, Robi D.; Johnson, Stephen L.

doi:10.1371/journal.pone.0067801

Cited by 101 publications

(118 citation statements)

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“…The expression of cx39.4 in melanophores was independently reported by the Johnson group (52). Cx39.4 expression was detected by the transcriptome analysis of melanophores using NGS (next-generation sequencing) (52). Our RT-PCR results and transgenic experiments also suggested the expression of Cx39.4 in pigment cells.…”

Section: Discussionsupporting

confidence: 73%

“…Recently, Irion et al (36) successfully showed that Cx39.4 is also involved in skin pattern formation and that Cx39.4 functions in melanophores and xanthophores. The expression of cx39.4 in melanophores was independently reported by the Johnson group (52). Cx39.4 expression was detected by the transcriptome analysis of melanophores using NGS (next-generation sequencing) (52).…”

Section: Discussionmentioning

confidence: 99%

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The Physiological Characterization of Connexin41.8 and Connexin39.4, Which Are Involved in the Striped Pattern Formation of Zebrafish

Watanabe

Sawada

Aramaki

et al. 2016

Journal of Biological Chemistry

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The zebrafish has a striped skin pattern on its body, and Connexin41.8 (Cx41.8) and Cx39.4 are involved in striped pattern formation. Mutations in these connexins change the striped pattern to a spot or labyrinth pattern. In this study, we characterized Cx41.8 and Cx39.4 after expression in Xenopus oocytes. In addition, we analyzed Cx41.8 mutants Cx41.8I203F and Cx41.8M7, which caused spot or labyrinth skin patterns, respectively, in transgenic zebrafish. In the electrophysiological analysis, the gap junctions formed by Cx41.8 and Cx39.4 showed distinct sensitivity to transjunctional voltage. Analysis of nonjunctional (hemichannel) currents revealed a large voltage-dependent current in Cx39.4-expressing oocytes that was absent in cells expressing Cx41.8. Junctional currents induced by both Cx41.8 and Cx39.4 were reduced by co-expression of Cx41.8I203F and abolished by co-expression of Cx41.8M7. In the transgenic experiment, Cx41.8I203F partially rescued the Cx41.8 null mutant phenotype, whereas Cx41.8M7 failed to rescue the null mutant, and it elicited a more severe phenotype than the Cx41.8 null mutant, as evidenced by a smaller spot pattern. Our results provide evidence that gap junctions formed by Cx41.8 play an important role in stripe/spot patterning and suggest that mutations in Cx41.8 can effect patterning by way of reduced function (I203F) and dominant negative effects (M7). Our results suggest that functional differences in Cx41.8 and Cx39.4 relate to spot or labyrinth mutant phenotypes and also provide evidence that these two connexins interact in vivo and in vitro.Connexin proteins are the major constituents of gap junctions and are four-pass transmembrane proteins. Six connexin proteins make up a hexamer called a connexon, which acts as a hemichannel at the cell membrane. Each gap junction is a large molecular unit formed by the docking of connexons, allowing ϳ1,000-Da small molecules to be transferred between neighboring cells (1,2). Approximately 20 connexins exist in mammalian genomes, and connexins are categorized into five subgroups (␣, ␤, ␥, ␦, and ), depending on their molecular weight and amino acid sequences (3, 4). In zebrafish, ϳ36 connexins are predicted to exist (5). This higher gene number might be due to genome duplication events during fish evolution. As in mammals, connexins are expressed in tissue-specific but overlapping patterns. A combination of connexins in the same or adjacent cells can lead to several types of gap junctions. Uniform connexins create homomeric homotypic gap junctions, whereas two or more types of connexins form gap junctions that are heteromeric (different connexins within a connexon), heterotypic (different connexins in two opposing connexons), or a combination of both. The composition of heteromeric and heterotypic gap junctions is expected to create gap junctions with a wide range of properties in vivo, although relatively little is known about their importance or complexity due to technical difficulties associated with their analysis (6 -12).The zebrafish i...

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Section: Discussionsupporting

confidence: 73%

Section: Discussionmentioning

confidence: 99%

The Physiological Characterization of Connexin41.8 and Connexin39.4, Which Are Involved in the Striped Pattern Formation of Zebrafish

Watanabe

Sawada

Aramaki

et al. 2016

Journal of Biological Chemistry

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“…Higdon and Johnson showed by RNA-seq that mpv17 is highly enriched in iridophores compared to other pigment cells such as melanocytes (Higdon et al, 2013). Krauss, et al, also recently noted that zebrafish mpv17 also localizes to the mitochondria, similar the the human and mouse protein.…”

Section: Resultsmentioning

confidence: 99%

A defect in the mitochondrial protein Mpv17 underlies the transparent casper zebrafish

D'Agati

Beltre

Sessa

et al. 2017

Developmental Biology

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The casper strain of zebrafish is widely used in studies ranging from cancer to neuroscience. casper offers the advantage of relative transparency throughout adulthood, making it particularly useful for in vivo imaging by epifluorescence, confocal, and light sheet microscopy. casper was developed by selective breeding of two previously described recessive pigment mutants: 1) nacre, which harbors an inactivating mutation of the mitfa gene, rendering the fish devoid of pigmented melanocytes; and 2) roy orbison, a mutant with so-far unidentified genetic cause that lacks reflective iridophores. To clarify the molecular nature of the roy orbison mutation, such that it can inform studies using casper, we undertook an effort to positionally clone the roy orbison mutation. We find that roy orbison is caused by an intronic defect in the gene mpv17, encoding an inner mitochondrial membrane protein that has been implicated in human mitochondrial DNA depletion syndrome. The roy orbison mutation is phenotypically and molecularly remarkably similar to another zebrafish iridophore mutant called transparent. Using Cas9-induced crispants and germline mutants with disrupted mpv17 open reading frame, we show in trans-heterozygote embryos that new frameshift alleles of mpv17, roy orbison, and transparent fail to complement each other. Our work provides genetic evidence that both roy orbison and transparent affect the mpv17 locus by a similar if not identical genetic lesion. Identification of mpv17 mutants will allow for further work probing the relationship between mitochondrial function and pigmentation, which has to date received little attention.

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“…In zebrafish, an attempt to find overlapping transcriptional signature between melanophores and iridophores identified 62 genes with similar expression patterns in both chromatophores, but igsf11 and pmel were not among them (Higdon, Mitra & Johnson, 2013). However, the study was done using larval melanophores and iridophores from the body and not from the fins (Higdon, Mitra & Johnson, 2013).…”

Section: Discussionmentioning

confidence: 99%

A gene expression study of dorso-ventrally restricted pigment pattern in adult fins ofNeolamprologus meeli, an African cichlid species

Ahi

Sefc

2017

PeerJ

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Fish color patterns are among the most diverse phenotypic traits found in the animal kingdom. Understanding the molecular and cellular mechanisms that control in chromatophore distribution and pigmentation underlying this diversity is a major goal in developmental and evolutionary biology, which has predominantly been pursued in the zebrafish model system. Here, we apply results from zebrafish work to study a naturally occurring color pattern phenotype in the fins of an African cichlid species from Lake Tanganyika. The cichlid fish Neolamprologus meeli displays a distinct dorsal color pattern, with black and white stripes along the edges of the dorsal fin and of the dorsal half of the caudal fin, corresponding with differences in melanophore density. To elucidate the molecular mechanisms controlling the differences in dorsal and ventral color patterning in the fins, we quantitatively assessed the expression of 15 candidate target genes involved in adult zebrafish pigmentation and stripe formation. For reference gene validation, we screened the expression stability of seven widely expressed genes across the investigated tissue samples and identified tbp as appropriate reference. Relative expression levels of the candidate target genes were compared between the dorsal, striped fin regions and the corresponding uniform, grey-colored regions in the anal and ventral caudal fin. Dorso-ventral expression differences, with elevated levels in both white and black stripes, were observed in two genes, the melanosome protein coding gene pmel and in igsf11, which affects melanophore adhesion, migration and survival. Next, we predicted potential shared upstream regulators of pmel and igsf11. Testing the expression patterns of six predicted transcriptions factors revealed dorso-ventral expression difference of irf1 and significant, negative expression correlation of irf1 with both pmel and igsf11. Based on these results, we propose pmel, igsf11 and irf1 as likely components of the genetic mechanism controlling distinct dorso-ventral color patterns in N. meeli fins.

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Gene Expression Analysis of Zebrafish Melanocytes, Iridophores, and Retinal Pigmented Epithelium Reveals Indicators of Biological Function and Developmental Origin

Cited by 101 publications

References 107 publications

The Physiological Characterization of Connexin41.8 and Connexin39.4, Which Are Involved in the Striped Pattern Formation of Zebrafish

The Physiological Characterization of Connexin41.8 and Connexin39.4, Which Are Involved in the Striped Pattern Formation of Zebrafish

A defect in the mitochondrial protein Mpv17 underlies the transparent casper zebrafish

A gene expression study of dorso-ventrally restricted pigment pattern in adult fins ofNeolamprologus meeli, an African cichlid species

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