A Causative Role of Stromelysin-3 in Extracellular Matrix Remodeling and Epithelial Apoptosis during Intestinal Metamorphosis in Xenopus laevis

Fu, Longsheng; Ishizuya‐Oka, Atsuko; Buchholz, Daniel R.; Amano, Tsuyoshi; Matsuda, Hiroki; Shi, Yun‐Bo

doi:10.1074/jbc.m413275200

Cited by 60 publications

(71 citation statements)

References 63 publications

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“…Next, to determine ST3 function in vivo, we used transgenic Xenopus tadpoles that express ST3 under a heat shock-inducible promoter (Fu et al, 2005). Overexpression of ST3 induced the larval epithelial apoptosis even in the absence of TH.…”

Section: Matrix Metalloproteinasesmentioning

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: Matrix Metalloproteinasesmentioning

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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“…Another approach involves the heat-shock promoter (Wheeler et al, 2000) to drive expression of the recombinase and has already been applied in transgenic zebrafish (Thummel et al, 2005). As the heat-shock promoter has been used most successfully for conditional transgenesis in Xenopus without showing any basal activity (Buchholz et al, 2004;Fu et al, 2005), a heat-shock promoter-controlled Cre strain would be the most promising approach to ubiquitously activate silent reporter genes in transgenic reporter strains. Importantly, both conditional systems will allow a defined activation of the recombinase at any time of Xenopus development.…”

Section: Discussionmentioning

confidence: 99%

Transgenic Xenopus laevis strain expressing cre recombinase in muscle cells

Waldner

Sakamaki

Ueno

et al. 2006

Developmental Dynamics

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For reproducible analyses of gene function in Xenopus, the use of transgenic strains is a promising approach but has limitations when investigating factors interfering with development. Therefore, inducible systems are attractive alternatives, and a binary system based on recombinases is a most versatile approach. We have shown previously that Cre and FLP recombinases are active in Xenopus laevis and can induce a silent reporter gene in a corresponding reporter strain. Here, we describe the establishment of the transgenic Xenopus laevis strain A7 expressing Cre recombinase under the control of the muscle-specific cardiac actin promoter. Upon crossing to several distinct reporter strains, A7 is able to induce EYFP, DsRed2, or LacZ reporter genes in a muscle-specific manner. This first Cre-expressing strain allows conditional activation of any gene of interest in muscle cells and, thus, opens up the use of recombinases as a new experimental strategy in Xenopus. Developmental Dynamics 235:2220 -2228, 2006.

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“…Transgenic animals and their wild type siblings were obtained by mating parental lines generated as previously described, and the transgenic animals were identified by the expression of GFP in the lens of their eyes (33). Wild type and transgenic tadpoles were heat-shocked twice at 34°C for 30 min, separated by 30 min at 18°C (33,53).…”

Section: Methodsmentioning

confidence: 99%

“…Microscopic and histochemical analyses have shown that at least the muscle and epidermal cells undergo T3-dependent apoptosis during metamorphosis (23,29,51,52). To study whether ST3 regulates apoptosis of these two cell types, we have made use of the transgenic animals that express a transgenic ST3 under the control of a heat shock-inducible promoter (33). We show that whereas extensive apoptosis is present in both the epidermis and muscles during natural as well as T3-induced metamorphosis, transgenic expression of ST3 induces cell death predominantly in the muscles.…”

mentioning

confidence: 99%

“…Organ culture studies on intestinal remodeling have directly substantiated an essential role of ST3 in larval epithelial cell death and ECM remodeling (32). Furthermore, precocious expression of ST3 alone in premetamorphic tadpoles through transgenesis is sufficient to induce ECM remodeling and larval epithelial apoptosis in the tadpole intestine (33). Thus, ST3 appears to be necessary and sufficient for intestinal epithelial cell death during metamorphosis.…”

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confidence: 99%

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Differential Regulation of Cell Type-specific Apoptosis by Stromelysin-3

Mathew

Fiorentino

et al. 2009

Journal of Biological Chemistry

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Matrix metalloproteinases (MMPs) have been extensively studied because of their functional attributes in development and diseases. However, relatively few in vivo functional studies have been reported on the roles of MMPs in postembryonic organ development. Amphibian metamorphosis is a unique model for studying MMP function during vertebrate development because of its dependence on thyroid hormone (T3) and the ability to easily manipulate this process with exogenous T3. The MMP stromelysin-3 (ST3) is induced by T3, and its expression correlates with cell death during metamorphosis. We have previously shown that ST3 is both necessary and sufficient for larval epithelial cell death in the remodeling intestine. To investigate the roles of ST3 in other organs and especially on different cell types, we have analyzed the effect of transgenic overexpression of ST3 in the tail of premetamorphic tadpoles. We report for the first time that ST3 expression, in the absence of T3, caused significant muscle cell death in the tail of premetamorphic transgenic tadpoles. On the other hand, only relatively low levels of epidermal cell death were induced by precocious ST3 expression in the tail, contrasting what takes place during natural and T3-induced metamorphosis when ST3 expression is high. This cell type-specific apoptotic response to ST3 in the tail suggests distinct mechanisms regulating cell death in different tissues. Furthermore, our analyses of laminin receptor, an in vivo substrate of ST3 in the intestine, suggest that laminin receptor cleavage may be an underlying mechanism for the cell type-specific effects of ST3. The extracellular matrix (ECM),3 the dynamic milieu of the cell microenvironment, plays a critical role in dictating the fate of the cell. The cross-talk between the cell and ECM and the timely catabolism of the ECM are crucial for tissue remodeling during development (1). Matrix metalloproteinases (MMPs), extrinsic proteolytic regulators of the ECM, mediate this process to a large extent. MMPs are a large family of Zn 2ϩ -dependent endopeptidases potentially capable of cleaving the extracellular as well as nonextracellular proteins (2-9). The MMP superfamily includes collagenases, gelatinases, stromelysins, and membrane-type MMPs based on substrate specificity and domain organization (2-4). MMPs have been implicated to influence a wide range of physiological and pathological processes (10 -13). The roles of MMPs appear to be very complex. For example, MMPs have been suggested to play roles in both tumor promotion and suppression (13-19). Unfortunately, relatively few functional studies have been carried out in vivo, especially in relation to the mechanisms involved during vertebrate development.Amphibian metamorphosis presents a fascinating experimental model to study MMP function during postembryonic development. A unique and salient feature of the metamorphic process is the absolute dependence on the signaling of thyroid hormone (20 -23). This makes it possible to prevent metamorphosis by simply inhibit...

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A Causative Role of Stromelysin-3 in Extracellular Matrix Remodeling and Epithelial Apoptosis during Intestinal Metamorphosis in Xenopus laevis

Cited by 60 publications

References 63 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

Transgenic Xenopus laevis strain expressing cre recombinase in muscle cells

Differential Regulation of Cell Type-specific Apoptosis by Stromelysin-3

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