The Actin Nucleator Cobl Organises the Terminal Web of Enterocytes

Overview

Journal Sci Rep

Specialty Science

Date 2020 Jul 9

PMID 32636403

Citations 7

Authors

Anne J Beer

Jule Gonzalez Delgado

Frank Steiniger

Britta Qualmann

Michael M Kessels

Affiliations

Soon will be listed here.

Abstract

Brush borders of intestinal epithelial cells are mandatory for nutrient uptake. Yet, which actin nucleators are crucial for forming the F-actin bundles supporting microvilli and the actin filaments of the terminal web, in which microvilli are rooted, is unknown. We show that mice lacking the actin nucleator Cobl surprisingly did not display reduced microvilli densities or changes in microvillar F-actin bundles or microvilli diameter but particularly in the duodenum displayed increased microvillar length. Interestingly, Cobl-deficient mice furthermore showed a significant widening of the terminal web. Quantitative analyses of high-resolution cryo-scanning electron microscopy (EM) of deep-etched duodenum samples revealed that Cobl is specifically important for the formation of fine filaments in the central terminal web that connect the apical structure of the terminal web underlying the plasma membrane, the microvilli rootlets and the basal structure of the terminal web with each other. Thus, the actin nucleator Cobl is critically involved in generating one of the cellular structures of the brush border-decorated apical cortex of enterocytes representing the absorptive intestinal surface.

Citing Articles

The Evolutionary Young Actin Nucleator Cobl Is Important for Proper Amelogenesis.

Janitzek H, Gonzalez Delgado J, Haag N, Seemann E, Nietzsche S, Sigusch B Cells. 2025; 14(5).

PMID: 40072087 PMC: 11898890. DOI: 10.3390/cells14050359.

Building the brush border, one microvillus at a time.

Morales E, Gaeta I, Tyska M Curr Opin Cell Biol. 2023; 80:102153.

PMID: 36827850 PMC: 10033394. DOI: 10.1016/j.ceb.2023.102153.

GRP75 as a functional element of cholix transcytosis.

Liu K, Hunter T, Taverner A, Yin K, MacKay J, Colebrook K Tissue Barriers. 2022; 11(1):2039003.

PMID: 35262466 PMC: 9870019. DOI: 10.1080/21688370.2022.2039003.

Poststroke dendritic arbor regrowth requires the actin nucleator Cobl.

Ji Y, Koch D, Gonzalez Delgado J, Gunther M, Witte O, Kessels M PLoS Biol. 2021; 19(12):e3001399.

PMID: 34898601 PMC: 8699704. DOI: 10.1371/journal.pbio.3001399.

Functional interdependence of the actin nucleator Cobl and Cobl-like in dendritic arbor development.

Izadi M, Seemann E, Schlobinski D, Schwintzer L, Qualmann B, Kessels M Elife. 2021; 10.

PMID: 34264190 PMC: 8282341. DOI: 10.7554/eLife.67718.

References

Ruemmele F, Schmitz J, Goulet O . Microvillous inclusion disease (microvillous atrophy). Orphanet J Rare Dis. 2006; 1:22. PMC: 1523325. DOI: 10.1186/1750-1172-1-22. View

Muller T, Hess M, Schiefermeier N, Pfaller K, Ebner H, Heinz-Erian P . MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat Genet. 2008; 40(10):1163-5. DOI: 10.1038/ng.225. View

Sauvanet C, Wayt J, Pelaseyed T, Bretscher A . Structure, regulation, and functional diversity of microvilli on the apical domain of epithelial cells. Annu Rev Cell Dev Biol. 2015; 31:593-621. DOI: 10.1146/annurev-cellbio-100814-125234. View

Crawley S, Mooseker M, Tyska M . Shaping the intestinal brush border. J Cell Biol. 2014; 207(4):441-51. PMC: 4242837. DOI: 10.1083/jcb.201407015. View

Pelaseyed T, Bretscher A . Regulation of actin-based apical structures on epithelial cells. J Cell Sci. 2018; 131(20). PMC: 6215389. DOI: 10.1242/jcs.221853. View

Ferrer R, Planas J, Moreto M . Cell apical surface area in enterocytes from chicken small and large intestine during development. Poult Sci. 1995; 74(12):1995-2002. DOI: 10.3382/ps.0741995. View

Grimm-Gunter E, Revenu C, Ramos S, Hurbain I, Smyth N, Ferrary E . Plastin 1 binds to keratin and is required for terminal web assembly in the intestinal epithelium. Mol Biol Cell. 2009; 20(10):2549-62. PMC: 2682596. DOI: 10.1091/mbc.e08-10-1030. View

Hirokawa N, Heuser J . Quick-freeze, deep-etch visualization of the cytoskeleton beneath surface differentiations of intestinal epithelial cells. J Cell Biol. 1981; 91(2 Pt 1):399-409. PMC: 2111975. DOI: 10.1083/jcb.91.2.399. View

Hirokawa N, Tilney L, Fujiwara K, Heuser J . Organization of actin, myosin, and intermediate filaments in the brush border of intestinal epithelial cells. J Cell Biol. 1982; 94(2):425-43. PMC: 2112874. DOI: 10.1083/jcb.94.2.425. View

10.

Zhang D, Piazza V, Perrin B, Rzadzinska A, Poczatek J, Wang M . Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature. 2012; 481(7382):520-4. PMC: 3267870. DOI: 10.1038/nature10745. View

11.

Fettiplace R, Kim K . The physiology of mechanoelectrical transduction channels in hearing. Physiol Rev. 2014; 94(3):951-86. PMC: 4101631. DOI: 10.1152/physrev.00038.2013. View

12.

Crawley S, Shifrin Jr D, Grega-Larson N, McConnell R, Benesh A, Mao S . Intestinal brush border assembly driven by protocadherin-based intermicrovillar adhesion. Cell. 2014; 157(2):433-446. PMC: 3992856. DOI: 10.1016/j.cell.2014.01.067. View

13.

BRETSCHER A, Weber K . Villin: the major microfilament-associated protein of the intestinal microvillus. Proc Natl Acad Sci U S A. 1979; 76(5):2321-5. PMC: 383592. DOI: 10.1073/pnas.76.5.2321. View

14.

BRETSCHER A, Weber K . Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J Cell Biol. 1980; 86(1):335-40. PMC: 2110655. DOI: 10.1083/jcb.86.1.335. View

15.

Bartles J, Zheng L, Li A, Wierda A, Chen B . Small espin: a third actin-bundling protein and potential forked protein ortholog in brush border microvilli. J Cell Biol. 1998; 143(1):107-19. PMC: 2132824. DOI: 10.1083/jcb.143.1.107. View

16.

Revenu C, Ubelmann F, Hurbain I, El-Marjou F, Dingli F, Loew D . A new role for the architecture of microvillar actin bundles in apical retention of membrane proteins. Mol Biol Cell. 2011; 23(2):324-36. PMC: 3258176. DOI: 10.1091/mbc.E11-09-0765. View

17.

Croce A, Cassata G, Disanza A, Gagliani M, Tacchetti C, Malabarba M . A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat Cell Biol. 2004; 6(12):1173-9. DOI: 10.1038/ncb1198. View

18.

Tocchetti A, Soppo C, Zani F, Bianchi F, Gagliani M, Pozzi B . Loss of the actin remodeler Eps8 causes intestinal defects and improved metabolic status in mice. PLoS One. 2010; 5(3):e9468. PMC: 2830459. DOI: 10.1371/journal.pone.0009468. View

19.

Saotome I, Curto M, McClatchey A . Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell. 2004; 6(6):855-64. DOI: 10.1016/j.devcel.2004.05.007. View

20.

Zhou K, Sumigray K, Lechler T . The Arp2/3 complex has essential roles in vesicle trafficking and transcytosis in the mammalian small intestine. Mol Biol Cell. 2015; 26(11):1995-2004. PMC: 4472011. DOI: 10.1091/mbc.E14-10-1481. View