A novel smooth septate junction-associated membrane protein, Snakeskin, is required for intestinal barrier function in<i>Drosophila</i>

Yanagihashi, Yuichi; Usui, Tadao; Izumi, Yasushi; Yonemura, Shigenobu; Sumida, Motoyuki; Tsukita, Shöichiro; Uemura, Tadashi; Furuse, Mikio

doi:10.1242/jcs.096800

Cited by 47 publications

(134 citation statements)

References 51 publications

(78 reference statements)

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“…We next examined whether Tsp2A is involved in the barrier function of the midgut epithelium, as previously observed for Mesh and Ssk Yanagihashi et al, 2012). We designed a dye permeability assay, which analyzed leakage from the midgut to the body cavity of a fluorescent tracer taken with the food Yanagihashi et al, 2012).…”

Section: Tsp2a Is Required For the Barrier Function Of The Midgutmentioning

confidence: 94%

“…By contrast, few genetic and molecular analyses have been carried out on sSJs. Recently, two sSJ-specific membrane proteins, Ssk and Mesh, have been identified and characterized (Izumi and Furuse, 2014;Izumi et al, 2012;Yanagihashi et al, 2012). Ssk consists of 162 amino acids and has four membrane-spanning domains, two short extracellular loops, cytoplasmic N-and C-terminal domains, and a cytoplasmic loop .…”

Section: Introductionmentioning

confidence: 99%

“…In western blot studies, Mesh is detected as a main ∼90 kDa band and a minor ∼200 kDa band . Compromised expression of Ssk or mesh causes defects in the ultrastructure of sSJs and in the barrier function of the midgut against a 10-kDa fluorescent tracer Yanagihashi et al, 2012). Ssk and Mesh physically interact with each other and are mutually dependent for their sSJ localization .…”

Section: Introductionmentioning

confidence: 99%

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A tetraspanin regulates septate junction formation in Drosophila midgut

Izumi¹,

Motoishi²,

Furuse³

et al. 2016

Development

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Septate junctions (SJs) are membrane specializations that restrict the free diffusion of solutes through the paracellular pathway in invertebrate epithelia. In arthropods, two morphologically different types of septate junctions are observed; pleated (pSJs) and smooth (sSJs), which are present in ectodermally and endodermally derived epithelia, respectively. Recent identification of sSJ-specific proteins, Mesh and Ssk, in Drosophila indicates that the molecular compositions of sSJs and pSJs differ. A deficiency screen based on immunolocalization of Mesh identified a tetraspanin family protein, Tsp2A, as a newly discovered protein involved in sSJ formation in Drosophila. Tsp2A specifically localizes at sSJs in the midgut and Malpighian tubules. Compromised Tsp2A expression caused by RNAi or the CRISPR/Cas9 system was associated with defects in the ultrastructure of sSJs, changed localization of other sSJ proteins, and impaired barrier function of the midgut. In most Tsp2A mutant cells, Mesh failed to localize to sSJs and was distributed through the cytoplasm. Tsp2A forms a complex with Mesh and Ssk and these proteins are mutually interdependent for their localization. These observations suggest that Tsp2A cooperates with Mesh and Ssk to organize sSJs.

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Section: Tsp2a Is Required For the Barrier Function Of The Midgutmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A tetraspanin regulates septate junction formation in Drosophila midgut

Izumi¹,

Motoishi²,

Furuse³

et al. 2016

Development

Self Cite

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“…In addition, three D. melanogaster sSJ-specific membrane proteins, snakeskin (Ssk), mesh and Tsp2A, have recently been discovered Izumi et al, 2012Izumi et al, , 2016. All three proteins are localized exclusively in the epithelia of the midgut and Malpighian tubules, where sSJs reside, and are required for the barrier function of the midgut (Izumi et al, , 2016Yanagihashi et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Identification of the septate junction protein gliotactin in the mosquito, Aedes aegypti: evidence for a role in increased paracellular permeability in larvae

Jonusaite

Kelly

Donini

2017

Journal of Experimental Biology

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Septate junctions (SJs) regulate paracellular permeability across invertebrate epithelia. However, little is known about the function of SJ proteins in aquatic invertebrates. In this study, a role for the transmembrane SJ protein gliotactin (Gli) in the osmoregulatory strategies of larval mosquito (Aedes aegypti) was examined. Differences in gli transcript abundance were observed between the midgut, Malpighian tubules, hindgut and anal papillae of A. aegypti, which are epithelia that participate in larval mosquito osmoregulation. Western blotting of Gli revealed its presence in monomer, putative dimer and alternatively processed protein forms in different larval mosquito organs. Gli localized to the entire SJ domain between midgut epithelial cells and showed a discontinuous localization along the plasma membranes of epithelial cells of the rectum as well as the syncytial anal papillae epithelium. In the Malpighian tubules, Gli immunolocalization was confined to SJs between the stellate and principal cells. Rearing larvae in 30% seawater caused an increase in Gli protein abundance in the anterior midgut, Malpighian tubules and hindgut. Transcriptional knockdown of gli using dsRNA reduced Gli protein abundance in the midgut and increased the flux rate of the paracellular permeability marker, polyethylene glycol (molecular weight 400 Da; PEG-400). Data suggest that in larval A. aegypti, Gli participates in the maintenance of salt and water balance and that one role for Gli is to participate in the regulation of paracellular permeability across the midgut of A. aegypti in response to changes in environmental salinity.

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“…, initially identified as effective RNAi targets were subsequently found to be orthologs of Drosophila ssk 30 and mesh 31 proteins, respectively (Table 1, Figs 1 and 2). The first SSJ gene was reported in Bombyx mori (silkworm) using monoclonal antibodies that specifically recognized the apical region of the lateral membrane of midgut epithelial cells.…”

mentioning

confidence: 99%

Discovery of midgut genes for the RNA interference control of corn rootworm

Xu¹

2016

2016 International Congress of Entomology

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RNA interference (RNAi) is a promising new technology for corn rootworm control. This paper presents the discovery of new gene targets -dvssj1 and dvssj2, in western corn rootworm (WCR). Dvssj1 and dvssj2 are orthologs of the Drosophila genes snakeskin (ssk) and mesh, respectively. These genes encode membrane proteins associated with smooth septate junctions (SSJ) which are required for intestinal barrier function. Based on bioinformatics analysis, dvssj1 appears to be an arthropod-specific gene. Diet based insect feeding assays using double-stranded RNA (dsRNA) targeting dvssj1 and dvssj2 demonstrate targeted mRNA suppression, larval growth inhibition, and mortality. In RNAi treated WCR, injury to the midgut was manifested by "blebbing" of the midgut epithelium into the gut lumen. Ultrastructural examination of midgut epithelial cells revealed apoptosis and regenerative activities. Transgenic plants expressing dsRNA targeting dvssj1 show insecticidal activity and significant plant protection from WCR damage. The data indicate that dvssj1 and dvssj2 are effective gene targets for the control of WCR using RNAi technology, by apparent suppression of production of their respective smooth septate junction membrane proteins located within the intestinal lining, leading to growth inhibition and mortality.

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A novel smooth septate junction-associated membrane protein, Snakeskin, is required for intestinal barrier function inDrosophila

Cited by 47 publications

References 51 publications

A tetraspanin regulates septate junction formation in Drosophila midgut

A tetraspanin regulates septate junction formation in Drosophila midgut

Identification of the septate junction protein gliotactin in the mosquito, Aedes aegypti: evidence for a role in increased paracellular permeability in larvae

Discovery of midgut genes for the RNA interference control of corn rootworm

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