Goblet cells: multifaceted players in immunity at mucosal surfaces

Knoop, Kathryn A.; Newberry, Rodney D.

doi:10.1038/s41385-018-0039-y

Cited by 218 publications

(142 citation statements)

References 117 publications

(153 reference statements)

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“…Planarian goblet cells (44, 111) (also called “Minotian gland cells” (112), “granular club” cells (30), “sphere cells” (31), or “pyriform cells” (113)) have been proposed to secrete digestive enzymes into the intestinal lumen (104), or store protein reserves (29). Ultrastructurally, planarian goblet cells possess numerous large proteinaceous granules and abundant rough endoplasmic reticulum (30, 104, 113), resembling mammalian goblet cells that produce a protective mucous barrier and mount innate immune responses (114–118). However, although numerous markers and reagents have been identified that label planarian goblet cells (32, 43, 53, 64, 106, 107), to our knowledge, genes required for goblet cell differentiation, maintenance, or physiological roles have not been reported.…”

Section: Resultsmentioning

confidence: 99%

Cell-type diversity and regionalized gene expression in the planarian intestine revealed by laser-capture microdissection transcriptome profiling

Forsthoefel

Cejda

Khan

et al. 2019

Preprint

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Organ regeneration requires precise coordination of new cell differentiation and remodeling of uninjured tissue to faithfully re-establish organ morphology and function. An atlas of gene expression and cell types in the uninjured state is therefore an essential pre-requisite for understanding how damage is repaired. Here, we use laser-capture microdissection (LCM) and RNA-Seq to define the transcriptome of the intestine of Schmidtea mediterranea, a planarian flatworm with exceptional regenerative capacity. Bioinformatic analysis of 1,844 intestine-enriched transcripts suggests extensive conservation of digestive physiology with other animals, including humans. Comparison of the intestinal transcriptome to purified absorptive intestinal cell (phagocyte) and published single-cell expression profiles confirms the identities of known intestinal cell types, and also identifies hundreds of additional transcripts with previously undetected intestinal enrichment. Furthermore, by assessing the expression patterns of 143 transcripts in situ, we discover unappreciated mediolateral regionalization of gene expression and cell-type diversity, especially among goblet cells. Demonstrating the utility of the intestinal transcriptome, we identify 22 intestine-enriched transcription factors, and find that several have distinct functional roles in the regeneration and maintenance of goblet cells. Furthermore, depletion of goblet cells inhibits planarian feeding and reduces viability. Altogether, our results show that LCM is a viable approach for assessing tissue-specific gene expression in planarians, and provide a new resource for further investigation of digestive tract regeneration, the physiological roles of intestinal cell types, and axial polarity.

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Section: Resultsmentioning

confidence: 99%

Cell-type diversity and regionalized gene expression in the planarian intestine revealed by laser-capture microdissection transcriptome profiling

Forsthoefel

Cejda

Khan

et al. 2019

Preprint

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“…Macromolecules such as intact proteins are transported by a variety of receptor-mediated endocytic mechanisms [15]. Intact bacteria, antigens, and particulate matter are transported by specialized M-cells overlying intestinal lymphoid aggregates (Peyer's patches) in the distal small intestine [16][17][18] and are sensed by goblet cell-associated antigen pathways (GAPs) [19], with some data indicating that LPS is absorbed through the lamina propria by GAPs in the small intestine [20].…”

Section: Overview Of Intestinal Mucosal Structure and Barrier Functionmentioning

confidence: 99%

The “Leaky Gut”: Tight Junctions but Loose Associations?

Hollander

Kaunitz

2019

Dig Dis Sci

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“…At first glance, it is surprising that Xpod has no vertebrate homolog, not even in its sister species Xenopus tropicalis . The basic process of mucus release via exocytic vesicles, however, is conserved throughout the vertebrates and beyond (Knoop & Newberry, ; Perez‐Vilar, ; Ridley & Thornton, ). This raises the question on the evolutionary origin of Xpod .…”

Section: Discussionmentioning

confidence: 99%

Serotonin and MucXS release by small secretory cells depend on Xpod, a SSC specific marker gene

Kurrle

Kunesch

Bogusch

et al. 2019

Genesis

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Summary Mucus secretion and ciliary motility are hallmarks for muco‐ciliary epithelia (MCE). Both, mammalian airways as well as the less complex epidermis of Xenopus embryos show cilia‐driven mucus flow to protect the organism against harmful effects by exogenous pathogens or pollutants. Four cell types set up the epidermal MCE in Xenopus. Multi‐ciliated cells (MCCs) generate an anterior to posterior flow of mucus. Ion secreting cells (ISCs) are characterized by the expression of ion transporters, presumably to maintain a favorable homeostasis. The largest cell type is represented by goblet cells, which cover most of the epidermis and exhibit secretory properties. Additionally, small secretory cells (SSCs) release mucus, antibiotic compounds, and the monoamine serotonin (5‐hydroxytryptamine; 5‐HT). We have recently shown that serotonin regulates flow velocity by acting on ciliary beat frequency. Here, we describe the identification and functional characterization of Xenopus polka‐dots (Xpod). No homologous genes or proteins were found in other vertebrates, including Xenopus tropicalis. We demonstrate that Xpod serves as an SSC‐specific marker, starting to be expressed shortly after SSC specification at neurula stages. Overexpression of a tagged Xpod protein resulted in the localization of secretory granules. Notch signaling induced SSC cell fate, in contrast to its repressing effect on MCC and ISC specification. Xpod loss‐of‐function revealed that mucus and 5‐HT release by SSCs was severely diminished, which impaired the ciliary beating of MCCs. In summary, Xpod specifically marked SSCs and was required for muco‐ciliary secretion in Xenopus laevis.

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Goblet cells: multifaceted players in immunity at mucosal surfaces

Cited by 218 publications

References 117 publications

Cell-type diversity and regionalized gene expression in the planarian intestine revealed by laser-capture microdissection transcriptome profiling

Cell-type diversity and regionalized gene expression in the planarian intestine revealed by laser-capture microdissection transcriptome profiling

The “Leaky Gut”: Tight Junctions but Loose Associations?

Serotonin and MucXS release by small secretory cells depend on Xpod, a SSC specific marker gene

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