Shh/BMP‐4 signaling pathway is essential for intestinal epithelial development during <i>Xenopus</i> larval‐to‐adult remodeling

Ishizuya‐Oka, Atsuko; Hasebe, Takashi; Shimizu, Katsuhiko; Suzuki, Ken; Ueda, Seinosuke

doi:10.1002/dvdy.20969

Cited by 57 publications

(62 citation statements)

References 59 publications

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“…One of the major type I receptors for BMP-4, BMPR-1A, which binds BMP-4 with a high affinity (Suzuki et al, 1994;ten Dijke et al, 1994;Ikeda et al, 1996), is weakly but clearly expressed in both the connective tissue and the adult epithelial primordia but not the larval epithelium ( Fig. 4C; Ishizuya-Oka et al, 2006), suggesting that BMP-4 has effects on both tissues.…”

Section: Shh/bone Morphogenetic Protein-4 Signaling Pathwaymentioning

confidence: 99%

Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis

Ishizuya‐Oka

Shi

2007

Developmental Dynamics

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During amphibian metamorphosis, most or all of the larval intestinal epithelial cells undergo apoptosis. In contrast, stem cells of yet-unknown origin actively proliferate and, under the influence of the connective tissue, differentiate into the adult epithelium analogous to the mammalian counterpart. Thus, amphibian intestinal remodeling is useful for studying the stem cell niche, the clarification of which is urgently needed for regenerative therapies. This review highlights the molecular aspects of the niche using the Xenopus laevis intestine as a model. Because amphibian metamorphosis is completely controlled by thyroid hormone (TH), the analysis of TH response genes serves as a powerful means for clarifying its molecular mechanisms. Although functional analysis of the genes is still on the way, recent progresses in organ culture and transgenic studies have gradually uncovered important roles of cell-cell and cell-extracellular matrix interactions through stromelysin-3 and sonic hedgehog/bone morphogenetic protein-4 signaling pathway in the epithelial stem cell development. Developmental Dynamics 236:3358 -3368, 2007.

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Section: Shh/bone Morphogenetic Protein-4 Signaling Pathwaymentioning

confidence: 99%

Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis

Ishizuya‐Oka

Shi

2007

Developmental Dynamics

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“…Some of these factors may also participate in regulating PRMT1 expression. For example, SMAD, a downstream mediator of bore morphogenetic protein receptors, may be involved in the intestinal stem cell development and PMRT1 expression because the BMP/BMP receptor signaling pathway plays a role in the amphibian metamorphosis (76,77). Thus, it will be interesting to investigate the roles of these other putative transcription factor binding sites in PRMT1 promoter function in the future.…”

Section: Discussionmentioning

confidence: 99%

Thyroid Hormone Activates Protein Arginine Methyltransferase 1 Expression by Directly Inducing c-Myc Transcription during Xenopus Intestinal Stem Cell Development

Fujimoto

Matsuura

Hu-Wang

et al. 2012

Journal of Biological Chemistry

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Background: PRMT1 is highly up-regulated in and plays an important role for developing adult intestinal stem cells during thyroid hormone-dependent Xenopus metamorphosis. Results: Liganded thyroid hormone receptor activates c-Myc transcription. c-Myc, in turn, activates PRMT1. Conclusion: Thyroid hormone up-regulates PRMT1 indirectly via c-Myc. Significance: The finding reveals an important gene regulation pathway by which thyroid hormone controls stem cell development.

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“…In the Xenopus model, our culture studies have shown that BMP-4 protein also represses the proliferating activity of the connective tissue cells [18] as well as in the embryonic gut. In addition, we demonstrated that BMP-4 protein promotes the differentiation of descendants of the stem cells into the absorptive epithelium expressing intestinal fatty acid-binding protein, a marker for the differentiated absorptive cells.…”

Section: Amphibian Intestinal Model For the Study Of The Radial Axismentioning

confidence: 99%

“…In contrast, BMP-4 expression is highest in the subepithelial fibroblasts surrounding the stem cells. Using the organ culture of the Xenopus tadpole intestine, we have shown that Shh protein can induce BMP-4 expression only in fibroblasts [18], similar to the case in the avian gut during embryogenesis, where the endoderm-specific expression of Shh induces BMP-4 expression in the mesenchyme [24, 25]. In the mammalian intestine, Shh is first expressed in the endoderm during embryogenesis and then, with the progress of the morphogenesis of villi, Shh expression becomes localized in the intervillus region, that is, the precrypt region, where stem cells will be localized [26].…”

Section: Amphibian Intestinal Model For the Study Of The Radial Axismentioning

confidence: 99%

“…By the expression analysis of such TH response genes, we have shown that Shh and BMP-4 correlate well with the development of the adult intestinal epithelium originating from the stem cells. Moreover, their functional analysis in vitro has shed light on the key roles of the Shh/BMP-4 signaling pathway in the establishment and/or maintenance of the radial axis [18]. …”

Section: Amphibian Intestinal Model For the Study Of The Radial Axismentioning

confidence: 99%

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Sonic Hedgehog and Bone Morphogenetic Protein-4 Signaling Pathway Involved in Epithelial Cell Renewal along the Radial Axis of the Intestine

Ishizuya‐Oka

Hasebe²

2008

Digestion

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The organogenesis of the digestive tract proceeds according to the positional information along the cephalo-caudal, dorsal-ventral and left-right axes of the embryonic body and the radial axis of the tract during development. Among them the radial axis, which corresponds to the crypt-villus axis in the adult small intestine, is essential for a rapid cell renewal of the epithelium throughout adulthood and is important from the clinical viewpoint. All of the adult intestinal epithelial cells originate from multipotent stem cells localized in the basal region of the crypt. Descendants of the stem cells, as they migrate up or down along the crypt-villus axis, actively proliferate, differentiate and finally undergo apoptosis. Recently, there has been a growing body of evidence that the Wnt and Notch signaling pathways are involved in cell proliferation and cell fate determination, respectively, during the epithelial cell renewal. However, the molecular mechanisms by which the radial axis is established and/or is maintained to enable the epithelial cell renewal have not yet been fully understood, and their clarification is urgently needed for stem cell therapies. In the amphibian intestine during metamorphosis, stem cells analogous to the mammalian ones appear and newly form the epithelium that undergoes the cell renewal along the radial axis by the inductive action of thyroid hormone. Thus, this animal model provides us with a good opportunity to clarify the molecular mechanisms of radial axis formation. By using the Xenopus laevis intestine, we found that sonic hedgehog (Shh), which is secreted by the stem cells, induces bone morphogenetic protein-4 (BMP-4) in subepithelial fibroblasts and that both Shh and BMP-4 are involved in the development of the cell-renewable epithelium. In this review, we highlight the molecular aspects of the cell renewal of the adult intestinal epithelium and propose important roles of the Shh/BMP-4 signaling pathway in the establishment and/or maintenance of the radial axis common to the human intestine.

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Shh/BMP‐4 signaling pathway is essential for intestinal epithelial development during Xenopus larval‐to‐adult remodeling

Cited by 57 publications

References 59 publications

Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis

Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis

Thyroid Hormone Activates Protein Arginine Methyltransferase 1 Expression by Directly Inducing c-Myc Transcription during Xenopus Intestinal Stem Cell Development

Sonic Hedgehog and Bone Morphogenetic Protein-4 Signaling Pathway Involved in Epithelial Cell Renewal along the Radial Axis of the Intestine

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