An inducible mouse model for microvillus inclusion disease reveals a role for myosin Vb in apical and basolateral trafficking

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 40, 2015, Pages 12408-12413

  Schneeberger, Kerstin ^a   Vogel, Georg F ^b   Teunissen, Hans ^a   Van Ommen, Domenique D ^a   Begthel, Harry ^c   Bouazzaoui, Layla El ^a   Van Vugt, Anke H M ^a   Beekman, Jeffrey M ^a   Klumperman, Judith ^c   Müller, Thomas ^b   Janecke, Andreas ^b   Gerner, Patrick ^d   Huber, Lukas A ^b   Hess, Michael W ^b   Clevers, Hans ^c   VanEs, Johan H ^c   Nieuwenhuis, Edward E S ^a   Middendorp, Sabine ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Intestinal enteropathy; Microvillus inclusion disease; Mouse model|myosin vb|epithelila polarity

Indexed keywords

ALKALINE PHOSPHATASE; MYOSIN V; MYOSIN VB; PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG; MYO5B PROTEIN, MOUSE;

ALKALINE PHOSPHATASE STAINING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BASOLATERAL MEMBRANE; BRUSH BORDER VESICLE; CASE REPORT; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; ENTEROPATHY; EXPERIMENTAL DIARRHEA; FEMALE; GENE DELETION; HUMAN; HUMAN TISSUE; INTERCELLULAR SPACE; INTESTINE BRUSH BORDER; INTESTINE EPITHELIUM CELL; MALABSORPTION; MALE; MICROVILLUS INCLUSION DISEASE; MOLECULAR PATHOLOGY; MOUSE; NEWBORN; NONHUMAN; PERIODIC ACID SCHIFF STAIN; PRIORITY JOURNAL; PROTEIN FUNCTION; RARE DISEASE; SECRETORY GRANULE; STAINING; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; C57BL MOUSE; CBA MOUSE; CHEMICALLY INDUCED; CONFOCAL MICROSCOPY; DISEASE MODEL; EPITHELIUM CELL; GENETICS; IMMUNOHISTOCHEMISTRY; INTESTINE; INTESTINE CELL; KNOCKOUT MOUSE; METABOLISM; MICROVILLUS; MUCOLIPIDOSIS; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; DISEASE MODELS, ANIMAL; ENTEROCYTES; EPITHELIAL CELLS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINES; MALABSORPTION SYNDROMES; MALE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROVILLI; MUCOLIPIDOSES; MYOSIN TYPE V; ORGAN CULTURE TECHNIQUES; PROTEIN TRANSPORT; TAMOXIFEN;

EID: 84943370122     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516672112     Document Type: Article

References (32)

1. Davidson GP, Cutz E, Hamilton JR, Gall DG (1978) Familial enteropathy: A syndrome of protracted diarrhea from birth, failure to thrive, and hypoplastic villus atrophy. Gastroenterology 75(5):783-790.
2. Ameen NA, Salas PJ (2000) Microvillus inclusion disease: A genetic defect affecting apical membrane protein traffic in intestinal epithelium. Traffic 1(1):76-83.
3. Cutz E, et al. (1989) Microvillus inclusion disease: An inherited defect of brush-border assembly and differentiation. N Engl J Med 320(10):646-651.
4. Dhekne HS, et al. (2014) Myosin Vb and Rab11a regulate phosphorylation of ezrin in enterocytes. J Cell Sci 127(Pt 5):1007-1017.
5. Müller T, et al. (2008) MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat Genet 40(10):1163-1165.
6. Thoeni CE, et al. (2014) Microvillus inclusion disease: Loss of Myosin vb disrupts intracellular traffic and cell polarity. Traffic 15(1):22-42.
7. Wiegerinck CL, et al. (2014) Loss of syntaxin 3 causes variant microvillus inclusion disease. Gastroenterology 147(1):65-68.e10.
8. Ruemmele FM, et al. (2010) Loss-of-function of MYO5B is the main cause of microvillus inclusion disease: 15 novel mutations and a CaCo-2 RNAi cell model. Hum Mutat 31(5):544-551.
9. Szperl AM, et al. (2011) Functional characterization of mutations in the myosin Vb gene associated with microvillus inclusion disease. J Pediatr Gastroenterol Nutr 52(3):307-313.
10. van der Velde KJ, et al. (2013) An overview and online registry of microvillus inclusion disease patients and their MYO5B mutations. Hum Mutat 34(12):1597-1605.
11. Erickson RP, Larson-Thomé K, Valenzuela RK, Whitaker SE, Shub MD (2008) Navajo microvillous inclusion disease is due to a mutation in MYO5B. Am J Med Genet A 146(24):3117-3119.
12. Knowles BC, et al. (2014) Myosin Vb uncoupling from RAB8A and RAB11A elicits microvillus inclusion disease. J Clin Invest 124(7):2947-2962.
13. Roland JT, et al. (2011) Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc Natl Acad Sci USA 108(7):2789-2794.
14. Sato T, et al. (2007) The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448(7151):366-369.
15. Melendez J, et al. (2013) Cdc42 coordinates proliferation, polarity, migration, and differentiation of small intestinal epithelial cells in mice. Gastroenterology 145(4):808-819.
16. Sakamori R, et al. (2012) Cdc42 and Rab8a are critical for intestinal stem cell division, survival, and differentiation in mice. J Clin Invest 122(3):1052-1065.
17. Knowles BC, et al. (2015) Rab11a regulates syntaxin 3 localization and microvillus assembly in enterocytes. J Cell Sci 128(8):1617-1626.
18. Sobajima T, et al. (2014) Rab11a is required for apical protein localisation in the intestine. Biol Open 4(1):86-94.
19. Kravtsov D, et al. (2014) Myosin 5b loss of function leads to defects in polarized signalling: Implication for Microvillus Inclusion Disease pathogenesis and treatment. Am J Physiol Gastrointest Liver Physiol 307(10):G992-G1001.
20. el Marjou F, et al. (2004) Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39(3):186-193.
21. Reinshagen K, Naim HY, Zimmer KP (2002) Autophagocytosis of the apical membrane in microvillus inclusion disease. Gut 51(4):514-521.
22. Hales CM, Vaerman JP, Goldenring JR (2002) Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 277(52):50415-50421.
23. Swiatecka-Urban A, et al. (2007) Myosin Vb is required for trafficking of the cystic fibrosis transmembrane conductance regulator in Rab11a-specific apical recycling endosomes in polarized human airway epithelial cells. JBiolChem282(32):23725-23736.
24. Garbett D, LaLonde DP, Bretscher A (2010) The scaffolding protein EBP50 regulates microvillar assembly in a phosphorylation-dependent manner. JCellBiol191(2):397-413.
25. Morales FC, Takahashi Y, Kreimann EL, Georgescu MM (2004) Ezrin-radixin-moesin (ERM)-binding phosphoprotein 50 organizes ERM proteins at the apical membrane of polarized epithelia. Proc Natl Acad Sci USA 101(51):17705-17710.
26. Saotome I, Curto M, McClatchey AI (2004) Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell 6(6):855-864.
27. Dukes JD, et al. (2011) Functional ESCRT machinery is required for constitutive recycling of claudin-1 and maintenance of polarity in vertebrate epithelial cells. Mol Biol Cell 22(17):3192-3205.
28. Sato T, et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459(7244):262-265.
29. Dekkers JF, et al. (2013) A functional CFTR assay using primary cystic fibrosis intestinal organoids. Nat Med 19(7):939-945.
30. Raymond CS, Soriano P (2007) High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PLoS One 2(1):e162.
31. Cartón-Garcia F, et al. (2015) Myo5b knockout mice as a model of microvillus inclusion disease. Sci Rep 5:12312.
32. Middendorp S, et al. (2014) Adult stem cells in the small intestine are intrinsically programmed with their location-specific function. Stem Cells 32(5):1083-1091.