Dataset Information

Tissue-Specific Transcriptomes Reveal Gene Expression Trajectories in Two Maturing Skin Epithelial Layers in Zebrafish Embryos.

ABSTRACT: Epithelial cells are the building blocks of many organs, including skin. The vertebrate skin initially consists of two epithelial layers, the outer periderm and inner basal cell layers, which have distinct properties, functions, and fates. The embryonic periderm ultimately disappears during development, whereas basal cells proliferate to form the mature, stratified epidermis. Although much is known about mechanisms of homeostasis in mature skin, relatively little is known about the two cell types in pre-stratification skin. To define the similarities and distinctions between periderm and basal skin epithelial cells, we purified them from zebrafish at early development stages and deeply profiled their gene expression. These analyses identified groups of genes whose tissue enrichment changed at each stage, defining gene flow dynamics of maturing vertebrate epithelia. At each of 52 and 72 hr post-fertilization (hpf), more than 60% of genes enriched in skin cells were similarly expressed in both layers, indicating that they were common epithelial genes, but many others were enriched in one layer or the other. Both expected and novel genes were enriched in periderm and basal cell layers. Genes encoding extracellular matrix, junctional, cytoskeletal, and signaling proteins were prominent among those distinguishing the two epithelial cell types. In situ hybridization and BAC transgenes confirmed our expression data and provided new tools to study zebrafish skin. Collectively, these data provide a resource for studying common and distinguishing features of maturing epithelia.

SUBMITTER: Cokus SJ

PROVIDER: S-EPMC6778804 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Tissue-Specific Transcriptomes Reveal Gene Expression Trajectories in Two Maturing Skin Epithelial Layers in Zebrafish Embryos.

Cokus Shawn J SJ De La Torre Maricruz M Medina Eric F EF Rasmussen Jeffrey P JP Ramirez-Gutierrez Joselyn J Sagasti Alvaro A Wang Fang F

G3 (Bethesda, Md.) 20191007 10

Epithelial cells are the building blocks of many organs, including skin. The vertebrate skin initially consists of two epithelial layers, the outer periderm and inner basal cell layers, which have distinct properties, functions, and fates. The embryonic periderm ultimately disappears during development, whereas basal cells proliferate to form the mature, stratified epidermis. Although much is known about mechanisms of homeostasis in mature skin, relatively little is known about the two cell type ...[more]

PMID: 31431477

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Project description:The lake sturgeon (Acipenser fulvescens) is an ancient, octoploid fish faced with conservation challenges across its range in North America, but a lack of genomic resources has hindered molecular research in the species. To support such research, we created a transcriptomic database from 13 tissues: brain, esophagus, gill, head kidney, heart, white muscle, liver, glandular stomach, muscular stomach, anterior intestine, pyloric cecum, spiral valve and rectum. The transcriptomes for each tissue were sequenced and assembled individually from a mean of 98.3 million (±38.9 million SD) reads each. In addition, an overall transcriptome was assembled and annotated with all data used for each tissue-specific transcriptome. All assembled transcriptomes and their annotations were made publicly available as a scientific resource. The non-gut transcriptomes provide important resources for many research avenues. However, we focused our analysis on messenger ribonucleic acid (mRNA) observations in the gut because the gut represents a compartmentalized organ system with compartmentalized functions, and seven of the sequenced tissues were from each of these portions. These gut-specific analyses were used to probe evidence of microbiome regulation by studying heterogeneity in microbial genes and genera identified from mRNA annotations. Gene set enrichment analyses were used to reveal the presence of photoperiod and circadian-related transcripts in the pyloric cecum, which may support periodicity in lake sturgeon digestion. Similar analyses were used to identify different types of innate immune regulation across the gut, while analyses of unique transcripts annotated to microbes revealed heterogeneous genera and genes among different gut tissues. The present results provide a scientific resource and information about the mechanisms of compartmentalized function across gut tissues in a phylogenetically ancient vertebrate. Database URL: https://figshare.com/projects/Lake_Sturgeon_Transcriptomes/133143.

Project description:BackgroundMycobacterium avium subsp. paratuberculosis (MAP) persistently infects intestines and mesenteric lymph nodes leading to a prolonged subclinical disease. The MAP genome sequence was published in 2005, yet its transcriptional organization in natural infection is unknown. While prior research analyzed regulated gene sets utilizing defined, in vitro stress related or advanced surgical methods with various animal species, we investigated the intracellular lifestyle of MAP in the intestines and lymph nodes to understand the MAP pathways that function to govern this persistence.ResultsOur transcriptional analysis shows that 21%, 8% and 3% of the entire MAP genome was represented either inside tissues, macrophages or both, respectively. Transcripts belonging to latency and cell envelope biogenesis were upregulated in the intestinal tissues whereas those belonging to intracellular trafficking and secretion were upregulated inside the macrophages. Transcriptomes of natural infection and in vitro macrophage infection shared genes involved in transcription and inorganic ion transport and metabolism. MAP specific genes within large sequence polymorphisms of ancestral M. avium complex were downregulated exclusively in natural infection.ConclusionsWe have unveiled common and unique MAP pathways associated with persistence, cell wall biogenesis and virulence in naturally infected cow intestines, lymph nodes and in vitro infected macrophages. This dichotomy also suggests that in vitro macrophage models may be insufficient in providing accurate information on the events that transpire during natural infection. This is the first report to examine the primary transcriptome of MAP at the local infection site (i.e. intestinal tissue). Regulatory pathways that govern the lifecycle of MAP appear to be specified by tissue and cell type. While tissues show a "shut-down" of major MAP metabolic genes, infected macrophages upregulate several MAP specific genes along with a putative pathogenicity island responsible for iron acquisition. Many of these regulatory pathways rely on the advanced interplay of host and pathogen and in order to decipher their message, an interactome must be established using a systems biology approach. Identified MAP pathways place current research into direct alignment in meeting the future challenge of creating a MAP-host interactome.

Dataset Information

Tissue-Specific Transcriptomes Reveal Gene Expression Trajectories in Two Maturing Skin Epithelial Layers in Zebrafish Embryos.

Publications

Tissue-Specific Transcriptomes Reveal Gene Expression Trajectories in Two Maturing Skin Epithelial Layers in Zebrafish Embryos.

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