Stomach remodeling‐associated changes of H+/K+‐ATPase β subunit expression in Xenopus laevis and H+/K+‐ATPase‐dependent acid secretion in tadpole stomach

Ikuzawa, Masayuki; Yasumasu, Shigeki; Kobayashi, Kenichiro; Inokuchi, Tomofumi; Iuchi, Ichiro

doi:10.1002/jez.a.127

Cited by 9 publications

(5 citation statements)

References 27 publications

(8 reference statements)

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“…High levels of atp4a transcripts were found in the stomach of the tadpole ( Fig. 5 A and C), where ATP4 localization and function have been previously described [8] . We also observed weaker atp4a expression in the embryonic esophagus and the proximal small intestine ( Fig.…”

Section: Analysis Of Atp4a and Foxj1 supporting

confidence: 70%

ATP4 and ciliation in the neuroectoderm and endoderm of Xenopus embryos and tadpoles

et al. 2015

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During gastrulation and neurulation, foxj1 expression requires ATP4a-dependent Wnt/β-catenin signaling for ciliation of the gastrocoel roof plate (Walentek et al. Cell Rep. 1 (2012) 516–527.) and the mucociliary epidermis (Walentek et al. Dev. Biol. (2015)) of Xenopus laevis embryos. These data suggested that ATP4a and Wnt/β-catenin signaling regulate foxj1 throughout Xenopus development. Here we analyzed whether foxj1 expression was also ATP4a-dependent in other ciliated tissues of the developing Xenopus embryo and tadpole. We found that in the floor plate of the neural tube ATP4a-dependent canonical Wnt signaling was required for foxj1 expression, downstream of or in parallel to Hedgehog signaling. In the developing tadpole brain, ATP4-function was a prerequisite for the establishment of cerebrospinal fluid flow. Furthermore, we describe foxj1 expression and the presence of multiciliated cells in the developing tadpole gastrointestinal tract. Our work argues for a general requirement of ATP4-dependent Wnt/β-catenin signaling for foxj1 expression and motile ciliogenesis throughout Xenopus development.

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Section: Analysis Of Atp4a and Foxj1 supporting

confidence: 70%

ATP4 and ciliation in the neuroectoderm and endoderm of Xenopus embryos and tadpoles

et al. 2015

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“…A second class is the inverse of the first; gene expression is high before climax, then drops at climax (''eclipses'') and rises again at the end of metamorphosis. This eclipse has also been described for genes expressed specifically in the epithelium of the posterior intestine (6) and in the epithelium of the stomach (8). To date, no gene that is expressed exclusively in the larval intestine has been identified.…”

mentioning

confidence: 60%

Remodeling of the intestine during metamorphosis of Xenopus laevis

Schreiber

Cai

Brown

2005

Proc. Natl. Acad. Sci. U.S.A.

125

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Thyroid hormone controls remodeling of the tadpole intestine during the climax of amphibian metamorphosis. In 8 days, the Xenopus laevis tadpole intestine shortens in length by 75%. Simultaneously, the longitudinal muscle fibers contract by about the same extent. The radial muscle fibers also shorten as the diameter narrows. Many radial fibers undergo programmed cell death. We conclude that muscle remodeling and contraction play key roles in the shortening process. Shortening is accompanied by a temporary ''heaping'' of the epithelial cells into many layers at climax. Cells that face the lumen undergo apoptosis. By the end of metamorphosis, when the epithelium is folded into crypts and villi, the epithelium is a single-cell layer once again. Throughout this remodeling, DNA replication occurs uniformly throughout the epithelium, as do changes in gene expression. The larval epithelial cells as a whole, rather than a subpopulation of stem cells, are the progenitors of the adult epithelial cells.BrdUrd ͉ caspase-3 ͉ smooth muscle ͉ epithelium ͉ thyroid hormone

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“…S. purpuratus and Ptychodera flava representing the ambulacraria have alkaline conditions (pH 9-10) in their stomachs. Neutral to acidic conditions are a character of chordate larvae including the cephalochordate B. floridae , teleost fish 37 and amphibians 38 . Alkaline digestive systems were also found in the anterior midgut of some insect larvae.…”

Section: Figurementioning

confidence: 99%

Evolution of extreme stomach pH in bilateria inferred from gastric alkalization mechanisms in basal deuterostomes

Stumpp

Tseng

et al. 2015

Sci Rep

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The stomachs of most vertebrates operate at an acidic pH of 2 generated by the gastric H + / K + -ATPase located in parietal cells. The acidic pH in stomachs of vertebrates is believed to aid digestion and to protect against environmental pathogens. Little attention has been placed on whether acidic gastric pH regulation is a vertebrate character or a deuterostome ancestral trait. Here, we report alkaline conditions up to pH 10.5 in the larval digestive systems of ambulacraria (echinoderm + hemichordate), the closest relative of the chordate. Microelectrode measurements in combination with specific inhibitors for acid-base transporters and ion pumps demonstrated that the gastric alkalization machinery in sea urchin larvae is mainly based on direct H + secretion from the stomach lumen and involves a conserved set of ion pumps and transporters. Hemichordate larvae additionally utilized HCO 3 − transport pathways to generate even more alkaline digestive conditions. Molecular analyses in combination with acidification experiments supported these findings and identified genes coding for ion pumps energizing gastric alkalization. Given that insect larval guts were also reported to be alkaline, our discovery raises the hypothesis that the bilaterian ancestor utilized alkaline digestive system while the vertebrate lineage has evolved a strategy to strongly acidify their stomachs.The highly acidic pH of most vertebrate stomachs is believed to protect against environmental pathogens and the mechanisms of gastric acidification are well described [1][2][3] . The H + /K + -ATPase (HKA) in luminal membranes of parietal cells drives H + ions into the stomach lumen leading to an accumulation of hydrochloric acid 4 . This enables vertebrates to generate highly acidic conditions in their digestive systems. In contrast, midgut alkalization in lepidopteran and dipteran insect larvae, is energized by an V-H + -ATPase (VHA) coupled to processes that result in net export of H + from the luminal space [5][6][7] . These observations demonstrate that different gastric pH regulatory mechanisms have evolved in the animal kingdom. An interest is thus raised in regard to whether the highly acidic or alkaline digestive system is an ancestral character of the bilaterian.Although marine invertebrates were described to have slightly acidic to neutral pH in their digestive systems 8,9 virtually nothing is known regarding gastric pH regulation of their larval stages. In a previous study we demonstrated that larvae of the green sea urchin, Strongylocentrotus droebachiensis, have alkaline conditions in their digestive systems 10 . This study also demonstrated that their digestive enzymes are adapted to alkaline conditions and the digestive efficiency is reduced when gastric pH is decreased.

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Stomach remodeling‐associated changes of H⁺/K⁺‐ATPase β subunit expression in Xenopus laevis and H⁺/K⁺‐ATPase‐dependent acid secretion in tadpole stomach

Cited by 9 publications

References 27 publications

ATP4 and ciliation in the neuroectoderm and endoderm of Xenopus embryos and tadpoles

ATP4 and ciliation in the neuroectoderm and endoderm of Xenopus embryos and tadpoles

Remodeling of the intestine during metamorphosis of Xenopus laevis

Evolution of extreme stomach pH in bilateria inferred from gastric alkalization mechanisms in basal deuterostomes

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