Microvillus Inclusion Disease: Loss of Myosin Vb Disrupts Intracellular Traffic and Cell Polarity

Traffic

Volumn 15, Issue 1, 2014, Pages 22-42

  Thoeni, Cornelia E ^a,b   Vogel, Georg F ^a   Tancevski, Ivan ^a   Geley, Stephan ^a   Lechner, Silvia ^a   Pfaller, Kristian ^a   Hess, Michael W ^a   Müller, Thomas ^a   Janecke, Andreas R ^a   Avitzur, Yaron ^b   Muise, Aleixo ^b   Cutz, Ernest ^b   Huber, Lukas A ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Congenital enteropathies; Epithelial cell polarity; Intracellular trafficking; Microvillus inclusion disease; MYO5B mutations; Myosin Vb; Protracted diarrhea

Indexed keywords

MYOSIN V; MYOSIN VB; RAB PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CASE REPORT; CELL DISRUPTION; CELL FUNCTION; CELL INCLUSION; CELL MATURATION; CELL MIGRATION; CELL POLARITY; CELL SURFACE; CELLULAR DISTRIBUTION; CHILD; CHILD DEATH; CONTROLLED STUDY; DIARRHEA; DUODENUM BIOPSY; ENTEROPATHY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INFANT; INTESTINE EPITHELIUM CELL; INTRACELLULAR TRANSPORT; LOSS OF FUNCTION MUTATION; MICROVILLUS INCLUSION DISEASE; MISSENSE MUTATION; MOLECULAR PATHOLOGY; ORGAN TRANSPLANTATION; POSTTRANSPLANT LYMPHOPROLIFERATIVE DISEASE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEPTICEMIA; TRANSCELLULAR CELL MIGRATION;

CONGENITAL ENTEROPATHIES; EPITHELIAL CELL POLARITY; INTRACELLULAR TRAFFICKING; MICROVILLUS INCLUSION DISEASE; MYO5B MUTATIONS; MYOSIN VB; PROTRACTED DIARRHEA;

CELL LINE, TUMOR; CELL POLARITY; ENTEROCYTES; HETEROZYGOTE; HUMANS; INFANT, NEWBORN; MALABSORPTION SYNDROMES; MALE; MICROVILLI; MUCOLIPIDOSES; MUTATION; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PROTEIN TRANSPORT;

EID: 84889575311     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12131     Document Type: Article

References (47)

1. Cutz E, Rhoads JM, Drumm B, Sherman PM, Durie PR, Forstner GG. Microvillus inclusion disease: an inherited defect of brush-border assembly and differentiation. N Engl J Med 1989;320:646-651.
2. Couper R. Microvillus inclusion disease. Gastroenterology 1991;101:1755-1756.
3. Rhoads JM, Vogler RC, Lacey SR, Reddick RL, Keku EO, Azizkhan RG, Berschneider HM. Microvillus inclusion disease. In vitro jejunal electrolyte transport. Gastroenterology 1991;100:811-817.
4. Cutz E, Sherman PM, Davidson GP. Enteropathies associated with protracted diarrhea of infancy: clinicopathological features, cellular and molecular mechanisms. Pediatr Pathol Lab Med 1997;17:335-368.
5. Sherman PM, Mitchell DJ, Cutz E. Neonatal enteropathies: defining the causes of protracted diarrhea of infancy. J Pediatr Gastroenterol Nutr 2004;38:16-26.
6. Reinshagen K, Naim H, Heusipp G, Zimmer KP. Pathophysiology in Microvillus inclusion disease. Z Gastroenterol 2006;44:667-671.
7. Lake BD. Microvillus inclusion disease: specific diagnostic features shown by alkaline phosphatase histochemistry. J Clin Pathol 1988;41:880-882.
8. Muller T, Hess MW, Schiefermeier N, Pfaller K, Ebner HL, Heinz-Erian P, Ponstingl H, Partsch J, Rollinghoff B, Kohler H, Berger T, Lenhartz H, Schlenck B, Houwen RJ, Taylor CJ, et al. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat Genet 2008;40:1163-1165.
9. Ruemmele FM, Muller T, Schiefermeier N, Ebner HL, Lechner S, Pfaller K, Thoni CE, Goulet O, Lacaille F, Schmitz J, Colomb V, Sauvat F, Revillon Y, Canioni D, Brousse N, et al. 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 2010;31:544-551.
10. Szperl AM, Golachowska MR, Bruinenberg M, Prekeris R, Thunnissen AM, Karrenbeld A, Dijkstra G, Hoekstra D, Mercer D, Ksiazyk J, Wijmenga C, Wapenaar MC, Rings EH, van Ijzendoorn SC. Functional characterization of mutations in the myosin Vb gene associated with microvillus inclusion disease. J Pediatr Gastroenterol Nutr 2011;52:307-313.
11. Golachowska MR, Dael CM, Keuning H, Karrenbeld A, Hoekstra D, Gijsbers CF, Benninga MA, Rings EH, van Ijzendoorn SC. Divergent effects of MYO5B mutations on apical brush border and apical recycling endosome organization in kidney and intestinal epithelial cells of microvillus inclusion disease patients presenting with transient renal Fanconi syndrome. J Pediatr Gastroenterol Nutr 2011.
12. Golachowska MR, van Dael CM, Keuning H, Karrenbeld A, Hoekstra D, Gijsbers CF, Benninga MA, Rings EH, van Ijzendoorn SC. MYO5B mutations in patients with microvillus inclusion disease presenting with transient renal Fanconi syndrome. J Pediatr Gastroenterol Nutr 2012;54:491-498.
13. Huber LA, de Hoop MJ, Dupree P, Zerial M, Simons K, Dotti C. Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J Cell Biol 1993;123:47-55.
14. Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K. Rab8, a small GTPase involved in intracellular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 1993;123:35-45.
15. Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance DW Jr, Mercer JA, Bahler M, Goldenring JR. Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 2001;12:1843-1857.
16. Hales CM, Vaerman JP, Goldenring JR. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 2002;277:50415-50421.
17. Volpicelli LA, Lah JJ, Fang G, Goldenring JR, Levey AI. Rab11a and myosin Vb regulate recycling of the M4 muscarinic acetylcholine receptor. J Neurosci 2002;22:9776-9784.
18. Fan GH, Lapierre LA, Goldenring JR, Sai J, Richmond A. Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol Biol Cell 2004;15:2456-2469.
19. Provance DW Jr, Gourley CR, Silan CM, Cameron LC, Shokat KM, Goldenring JR, Shah K, Gillespie PG, Mercer JA. Chemical-genetic inhibition of a sensitized mutant myosin Vb demonstrates a role in peripheral-pericentriolar membrane traffic. Proc Natl Acad Sci USA 2004;101:1868-1873.
20. Lapierre LA, Goldenring JR. Interactions of myosin vb with rab11 family members and cargoes traversing the plasma membrane recycling system. Methods Enzymol 2005;403:715-723.
21. Wakabayashi Y, Dutt P, Lippincott-Schwartz J, Arias IM. Rab11a and myosin Vb are required for bile canalicular formation in WIF-B9 cells. Proc Natl Acad Sci USA 2005;102:15087-15092.
22. Nedvetsky PI, Stefan E, Frische S, Santamaria K, Wiesner B, Valenti G, Hammer JA 3rd, Nielsen S, Goldenring JR, Rosenthal W, Klussmann E. A role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle. Traffic 2007;8:110-123.
23. Roland JT, Kenworthy AK, Peranen J, Caplan S, Goldenring JR. Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 2007;18:2828-2837.
24. Swiatecka-Urban A, Talebian L, Kanno E, Moreau-Marquis S, Coutermarsh B, Hansen K, Karlson KH, Barnaby R, Cheney RE, Langford GM, Fukuda M, Stanton BA. 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. J Biol Chem 2007;282:23725-23736.
25. Ishikura S, Klip A. Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am J Physiol Cell Physiol 2008;295:C1016-1025.
26. Millman EE, Zhang H, Zhang H, Godines V, Bean AJ, Knoll BJ, Moore RH. Rapid recycling of beta-adrenergic receptors is dependent on the actin cytoskeleton and myosin Vb. Traffic 2008;9:1958-1971.
27. Provance DW Jr, Addison EJ, Wood PR, Chen DZ, Silan CM, Mercer JA. Myosin-Vb functions as a dynamic tether for peripheral endocytic compartments during transferrin trafficking. BMC Cell Biol 2008;9:44.
28. Wang Z, Edwards JG, Riley N, Provance DW Jr, Karcher R, Li XD, Davison IG, Ikebe M, Mercer JA, Kauer JA, Ehlers MD. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 2008;135:535-548.
29. Chu BB, Ge L, Xie C, Zhao Y, Miao HH, Wang J, Li BL, Song BL. Requirement of myosin Vb.Rab11a.Rab11-FIP2 complex in cholesterol-regulated translocation of NPC1L1 to the cell surface. J Biol Chem 2009;284:22481-22490.
30. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009;10:513-525.
31. Roland JT, Bryant DM, Datta A, Itzen A, Mostov KE, Goldenring JR. Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc Natl Acad Sci USA 2011;108:2789-2794.
32. Schuh M. An actin-dependent mechanism for long-range vesicle transport. Nat Cell Biol 2011;13:1431-1436.
33. Gidon A, Bardin S, Cinquin B, Boulanger J, Waharte F, Heliot L, de la Salle H, Hanau D, Kervrann C, Goud B, Salamero J. A Rab11A/myosin Vb/Rab11-FIP2 complex frames two late recycling steps of langerin from the ERC to the plasma membrane. Traffic 2012;13:815-833.
34. Michail S, Collins JF, Xu H, Kaufman S, Vanderhoof J, Ghishan FK. Abnormal expression of brush-border membrane transporters in the duodenal mucosa of two patients with microvillus inclusion disease. J Pediatr Gastroenterol Nutr 1998;27:536-542.
35. Ameen NA, Salas PJ. Microvillus inclusion disease: a genetic defect affecting apical membrane protein traffic in intestinal epithelium. Traffic 2000;1:76-83.
36. Fogh J, Trempe G. In: Fogh J, editor. Human Tumor Cells in Vitro. Plenum; 1975, pp. 115-141.
37. Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, Ozono K, Miki K, Kubo Y, Tsuji A, Harada R, Harada A. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 2007;448:366-369.
38. Sakamori R, Das S, Yu S, Feng S, Stypulkowski E, Guan Y, Douard V, Tang W, Ferraris RP, Harada A, Brakebusch C, Guo W, Gao N. Cdc42 and Rab8a are critical for intestinal stem cell division, survival, and differentiation in mice. J Clin Invest 2012;122:1052-1065.
39. Bryant DM, Datta A, Rodrigez-Fraticelli AE, Peränen J, Martin-Belmonte F, Mostov KE. A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 2010;12:1035-1045.
40. Galvez-Santisteban M, Rodriguez-Fraticelli AE, Bryant DM, Vergarajauregui S, Yasuda T, Banon-Rodriguez I, Bernascone I, Datta A, Spivak N, Young K, Slim CL, Brakeman PR, Fukada M, Mostov KE, Martin-Belmonte F. Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells. Nat Cell Biol 2012;14:838-849.
41. Ramel D, Wang X, Laflamme C, Montell DJ, Emery G. Rab11 regulates cell-cell communication during collective cell movements. Nat Cell Biol 2013;15:317-324.
42. Ploner C, Rainer J, Niederegger H, Eduardoff M, Villunger A, Geley S, Kofler R. The BCL2 rheostat in glucocorticoid-induced apoptosis of acute lymphoblastic leukemia. Leukemia 2008;22:370-377.
43. Campeau E, Ruhl VE, Rodier F, Smith CL, Rahmberg BL, Fuss JO, Campisi J, Yaswen P, Cooper PK, Kaufman PD. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS One 2009;4:e6529.
44. Rodriguez OC, Cheney RE. Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J Cell Sci 2002;115:991-1004.
45. Pearse AGE. Histochemistry: theoretical and applied. In: Preparative and Optical Technology, 4th edn, Volume 1. London: Churchill-Livingstone; 1980, pp. 1-439.
46. Fialka I, Pasquali C, Lottspeich F, Ahorn H, Huber LA. Subcellular fractionation of polarized epithelial cells and identification of organelle-specific proteins by two-dimensional gel electrophoresis. Electrophoresis 1997;18:2582-2590.
47. Drover VA, Nguyen DV, Bastie CC, Darlington YF, Abumrad NA, Pessin JE, London E, Sahoo D, Phillips MC. CD36 mediates both cellular uptake of very long chain fatty acids and their intestinal absorption in mice. J Biol Chem 2008;283:13108-13115.