Maternal Interferon Regulatory Factor 6 is required for the differentiation of primary superficial epithelia in Danio and Xenopus embryos

Jaime L Sabel; Claudia d'Alençon; Erin K O'Brien; Eric Van Otterloo; Katie Lutz; Tawny N Cuykendall; Brian C Schutte; Douglas W Houston; Robert A Cornell

doi:10.1016/j.ydbio.2008.10.031

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Maternal Interferon Regulatory Factor 6 is required for the differentiation of primary superficial epithelia in Danio and Xenopus embryos

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Maternal Interferon Regulatory Factor 6 is required for the differentiation of primary superficial epithelia in Danio and Xenopus embryos

Jaime L Sabel, Claudia d'Alençon, Erin K O'Brien, Eric Van Otterloo, Katie Lutz, Tawny N Cuykendall, Brian C Schutte, Douglas W Houston and Robert A Cornell

Developmental biology, Vol.325(1), pp.249-262

2009

DOI: 10.1016/j.ydbio.2008.10.031

PMCID: PMC2706144

PMID: 19013452

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Abstract

Early in the development of animal embryos, superficial cells of the blastula form a distinct lineage and adopt an epithelial morphology. In different animals, the fate of these primary superficial epithelial (PSE) cells varies, and it is unclear whether pathways governing segregation of blastomeres into the PSE lineage are conserved. Mutations in the gene encoding Interferon Regulatory Factor 6 (IRF6) are associated with syndromic and non-syndromic forms of cleft lip and palate, consistent with a role for Irf6 in development of oral epithelia, and mouse Irf6 targeted null mutant embryos display abnormal differentiation of oral epithelia and skin. In Danio rerio (zebrafish) and Xenopus laevis (African clawed frog) embryos, zygotic irf6 transcripts are present in many epithelial tissues including the presumptive PSE cells and maternal irf6 transcripts are present throughout all cells at the blastula stage. Injection of antisense oligonucleotides with ability to disrupt translation of irf6 transcripts caused little or no effect on development. By contrast, injection of RNA encoding a putative dominant negative Irf6 caused epiboly arrest, loss of gene expression characteristic of the EVL, and rupture of the embryo at late gastrula stage. The dominant negative Irf6 disrupted EVL gene expression in a cell autonomous fashion. These results suggest that Irf6 translated in the oocyte or unfertilized egg suffices for early development. Supporting the importance of maternal Irf6, we show that depletion of maternal irf6 transcripts in X. laevis embryos leads to gastrulation defects and rupture of the superficial epithelium. These experiments reveal a conserved role for maternally-encoded Irf6 in differentiation of a simple epithelium in X. laevis and D. rerio. This epithelium constitutes a novel model tissue in which to explore the Irf6 regulatory pathway.

Trophectoderm

Interferon Regulatory Factor 6

Keratin

Gastrulation

Epiboly

Superficial epithelium

Enveloping layer

Details

Title: Subtitle: Maternal Interferon Regulatory Factor 6 is required for the differentiation of primary superficial epithelia in Danio and Xenopus embryos
Creators: Jaime L Sabel - Interdisciplinary Graduate Program in Genetics, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Claudia d'Alençon - Facultad de Ciencias de la Salud, Universidad Andrés Bello, Santiago, Chile
Erin K O'Brien - Department of Otolaryngology, University of Iowa Hospitals and Clinics, USA
Eric Van Otterloo - Department of Anatomy and Cell Biology, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Katie Lutz - Department of Anatomy and Cell Biology, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Tawny N Cuykendall - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Brian C Schutte - Interdisciplinary Graduate Program in Genetics, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Douglas W Houston - Interdisciplinary Graduate Program in Genetics, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Robert A Cornell - Interdisciplinary Graduate Program in Genetics, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Resource Type: Journal article
Publication Details: Developmental biology, Vol.325(1), pp.249-262
DOI: 10.1016/j.ydbio.2008.10.031
PMID: 19013452
PMCID: PMC2706144
NLM abbreviation: Dev Biol
ISSN: 0012-1606
eISSN: 1095-564X
Publisher: Elsevier Inc
Grant note: DOI: 10.13039/100001024, name: Roy J. Carver Charitable Trust, award: 1-FY05-922, GM067841, DE13513; DOI: 10.13039/100000002, name: National Institutes of Health, award: 1-FY05-922, GM067841, DE13513; DOI: 10.13039/100000057, name: National Institute of General Medical Sciences, award: 1-FY05-922, GM067841, DE13513; DOI: 10.13039/100000912, name: March of Dimes Foundation, award: 1-FY05-922, GM067841, DE13513; DOI: 10.13039/501100001853, name: Recruitment and Assesment Centre, award: 1-FY05-922, GM067841, DE13513; DOI: 10.13039/100000072, name: National Institute of Dental and Craniofacial Research, award: 1-FY05-922, GM067841, DE13513
Language: English
Date published: 2009
Academic Unit: Anatomy and Cell Biology; Stead Family Department of Pediatrics; Biology; Craniofacial Anomalies Research Center; Neurology (Pediatrics); Dental Research; Periodontics
Record Identifier: 9983992094002771

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