Morphological and Molecular Characterization of Adult Midgut Compartmentalization in Drosophila

Buchon, Nicolas; Osman, Dani; David, Fabrice; Fang, Hsiao Yu; Boquete, Jean-Philippe; Deplancke, Bart; Lemaître, Bruno

doi:10.1016/j.celrep.2013.05.019

Cited by 102 publications

(176 citation statements)

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“…Recently, these data were supported by the finding that genetic regulatory networks and compartment-specific stem cell differences direct regional diversity in the Drosophila midgut [34,35]. Furthermore, the GATAe transcription factor, a master regulator of midgut development, was shown to control compartment-specific gene expression along the length of the adult intestine, whereas gradients of WNT activity were shown to refine the location of boundaries [34].…”

Section: Discussionsupporting

confidence: 53%

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Adult Stem Cells in the Small Intestine Are Intrinsically Programmed with Their Location‐Specific Function

et al. 2014

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Differentiation and specialization of epithelial cells in the small intestine are regulated in two ways. First, there is differentiation along the crypt-villus axis of the intestinal stem cells into absorptive enterocytes, Paneth, goblet, tuft, enteroendocrine, or M cells, which is mainly regulated by WNT. Second, there is specialization along the cephalocaudal axis with different absorptive and digestive functions in duodenum, jejunum, and ileum that is controlled by several transcription factors such as GATA4. However, so far it is unknown whether locationspecific functional properties are intrinsically programmed within stem cells or if continuous signaling from mesenchymal cells is necessary to maintain the location-specific identity of the small intestine. Using the pure epithelial organoid technique, we show that region-specific gene expression profiles are conserved throughout long-term cultures of both mouse and human intestinal stem cells and correlated with differential Gata4 expression. Furthermore, the human organoid culture system demonstrates that Gata4-regulated gene expression is only allowed in absence of WNT signaling. These data show that location-specific function is intrinsically programmed in the adult stem cells of the small intestine and that their differentiation fate is independent of location-specific extracellular signals. In light of the potential future clinical application of small intestine-derived organoids, our data imply that it is important to generate GATA4-positive and GATA4-negative cultures to regenerate all essential functions of the small intestine.

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Section: Discussionsupporting

confidence: 53%

“…Furthermore, the GATAe transcription factor, a master regulator of midgut development, was shown to control compartment-specific gene expression along the length of the adult intestine, whereas gradients of WNT activity were shown to refine the location of boundaries [34].…”

Section: Discussionmentioning

confidence: 99%

Adult Stem Cells in the Small Intestine Are Intrinsically Programmed with Their Location‐Specific Function

et al. 2014

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“…1B). Specifically, in females there was a high level of Tomato fluorescence at the posterior cardia (R0 section) (34) and adjoining anterior ventriculus (R1a and maybe R1b sections) (34) (illustrated by the orange color in Fig. 1C), whereas fluorescence was barely detectable in males in this tissue (Fig.…”

Section: Resultsmentioning

confidence: 99%

Constraints on the evolution of a doublesex target gene arising from doublesex’s pleiotropic deployment

Luo

Baker

2015

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

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"Regulatory evolution," that is, changes in a gene's expression pattern through changes at its regulatory sequence, rather than changes at the coding sequence of the gene or changes of the upstream transcription factors, has been increasingly recognized as a pervasive evolution mechanism. Many somatic sexually dimorphic features of Drosophila melanogaster are the results of gene expression regulated by the doublesex (dsx) gene, which encodes sex-specific transcription factors (DSX F in females and DSX M in males). Rapid changes in such sexually dimorphic features are likely a result of changes at the regulatory sequence of the target genes. We focused on the Flavin-containing monooxygenase-2 (Fmo-2) gene, a likely direct dsx target, to elucidate how sexually dimorphic expression and its evolution are brought about. We found that dsx is deployed to regulate the Fmo-2 transcription both in the midgut and in fat body cells of the spermatheca (a female-specific tissue), through a canonical DSX-binding site in the Fmo-2 regulatory sequence. In the melanogaster group, Fmo-2 transcription in the midgut has evolved rapidly, in contrast to the conserved spermathecal transcription. We identified two cis-regulatory modules (CRM-p and CRM-d) that direct sexually monomorphic or dimorphic Fmo-2 transcription, respectively, in the midguts of these species. Changes of Fmo-2 transcription in the midgut from sexually dimorphic to sexually monomorphic in some species are caused by the loss of CRM-d function, but not the loss of the canonical DSX-binding site. Thus, conferring transcriptional regulation on a CRM level allows the regulation to evolve rapidly in one tissue while evading evolutionary constraints posed by other tissues.sex determination | transcription factors | DNA binding site | evolution H ow sex-specific characteristics are generated during development, what roles they have in the biology of an organism, and how they have evolved are fundamental questions in biology. In Drosophila melanogaster, the molecular mechanisms leading to the sex-specific and temporally and spatially restricted deployment of the transcription factors encoded by the terminal genes in the sex-determination regulatory hierarchy, doublesex (dsx) and fruitless (fru), have been well documented (1-4). In addition, although it has been established that the FRU M and DSX M and DSX F proteins control nearly all aspects of somatic sexual differentiation, including anatomical and behavioral differences, much less is known about the direct target genes through which these transcription factors act (2, 3, 5-11).It has been increasingly recognized that evolutionary significant changes in gene expression are often a result of mutations in the regulatory sequences of genes, rather than in their coding sequences (12). Furthermore, it has been noted that evolutionary changes are most likely in the cis-acting regulatory elements of the downstream targets of transcription factors, rather than in the genes encoding the transcription factors (13,14). This finding...

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“…The midgut extends from the cardia until the junction with the hindgut, where the Malpighian tubules connect with the gut ( Figure 1B). Detailed histological and molecular analysis demonstrates a complex degree of compartmentalization in the adult fly midgut (Buchon et al, 2013b) (Marianes and Spradling, 2013) (Li et al, 2013a). Further details on gut compartmentalization, the perithropic membrane and Malpighian tubules can be found in different articles of this issue.…”

Section: Structure Of the Adult Drosophila Midgutmentioning

confidence: 99%

Intestinal stem cell proliferation and epithelial homeostasis in the adult Drosophila midgut

Nászai

Carroll

Cordero

2015

Insect Biochemistry and Molecular Biology

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Adult tissue homeostasis requires a tight balance between the removal of old or damaged cells and the production of new ones. Such processes are usually driven by dedicated stem cells that reside within specific tissue locations or niches (Nystul and Spradling, 2006).The intestinal epithelium has a remarkable regenerative capacity, which has made it a prime paradigm for the study of stem cell-driven tissue self-renewal. The discovery of the presence of stem cells in the adult midgut of the fruit fly Drosophila melanogaster has significantly impacted our understanding of the role of stem cells in intestinal homeostasis. Here we will review the current knowledge of the main mechanisms involved in the regulation of tissue homeostasis in the adult Drosophila midgut, with a focus on the role of stem cells in this process. We will also discuss processes involving acute or chronic disruption of normal intestinal homeostasis such as damage-induced regeneration and ageing.3

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Morphological and Molecular Characterization of Adult Midgut Compartmentalization in Drosophila

Cited by 102 publications

References 0 publications

Adult Stem Cells in the Small Intestine Are Intrinsically Programmed with Their Location‐Specific Function

Adult Stem Cells in the Small Intestine Are Intrinsically Programmed with Their Location‐Specific Function

Constraints on the evolution of a doublesex target gene arising from doublesex’s pleiotropic deployment

Intestinal stem cell proliferation and epithelial homeostasis in the adult Drosophila midgut

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