Enterocytic differentiation is modulated by lipid rafts-dependent assembly of adherens junctions

Experimental Cell Research

Volumn 317, Issue 10, 2011, Pages 1422-1436

  Chartier, Nicolas T ^a,b   Lainé, Michèle G ^a,b   Ducarouge, Benjamin ^a,b   Oddou, Christiane ^a,c   Bonaz, Bruno ^b   Albiges Rizo, Corinne ^a,b,c   Jacquier Sarlin, Muriel R ^a,b  

^a INSERM   (France)

^b UNIV GRENOBLE ALPES   (France)

^c CNRS   (France)

Author keywords

Flotillin; Intestinal cell differentiation; Lipid rafts; Rac1, adherens junctions

Indexed keywords

FLOTILLIN 1; GLYCOPROTEIN GP 120; RAC1 PROTEIN; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL JUNCTION; CELL STRAIN HT29; COLON; CONTROLLED STUDY; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; INTESTINE CELL; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

RATTUS;

EID: 79955970303     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.03.009     Document Type: Article

References (57)

1. Clayburgh D., Shen L., Turner J. A porous defense: the leaky epithelial barrier in intestinal disease. Lab. Invest. 2004, 84:282-291.
2. Gumbiner B.M. Regulation of cadherin adhesive activity. J. Cell Biol. 2000, 148:399-404.
3. Perez-Moreno M., Fuchs E. Catenins: keeping cells from getting their signals crossed. Dev. Cell 2006, 11:601-612.
4. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
5. Laprise P., Chailler P., Houde M., Beaulieu J.F., Boucher M.J., Rivard N. Phosphatidylinositol 3-kinase controls human intestinal epithelial cell differentiation by promoting adherens junction assembly and p38 MAPK activation. J. Biol. Chem. 2002, 277:8226-8234.
6. Peignon G., Thenet S., Schreider C., Fouquet S., Ribeiro A., Dussaulx E., Chambaz J., Cardot P., Pincon-Raymond M., Le Beyec J. E-cadherin-dependent transcriptional control of apolipoprotein A-IV gene expression in intestinal epithelial cells: a role for the hepatic nuclear factor 4. J. Biol. Chem. 2006, 281:3560-3568.
7. Mariadason J.M., Bordonaro M., Aslam F., Shi L., Kuraguchi M., Velcich A., Augenlicht L.H. Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res. 2001, 61:3465-3471.
8. Reynolds A.B., Carnahan R.H. Regulation of cadherin stability and turnover by p120ctn: implications in disease and cancer. Semin. Cell Dev. Biol. 2004, 15:657-663.
9. Davis M.A., Ireton R.C., Reynolds A.B. A core function for p120-catenin in cadherin turnover. J. Cell Biol. 2003, 163:525-534.
10. Ireton R.C., Davis M.A., van Hengel J., Mariner D.J., Barnes K., Thoreson M.A., Anastasiadis P.Z., Matrisian L., Bundy L.M., Sealy L., Gilbert B., van Roy F., Reynolds A.B. A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 2002, 159:465-476.
11. Gout S., Marie C., Laine M., Tavernier G., Block M.R., Jacquier-Sarlin M. Early enterocytic differentiation of HT-29 cells: biochemical changes and strength increases of adherens junctions. Exp. Cell Res. 2004, 299:498-510.
12. Anastasiadis P.Z. p120-ctn: a nexus for contextual signaling via Rho GTPases. Biochim. Biophys. Acta 2007, 1773:34-46.
13. jaffe, in: Hall (Ed.), 2005.
14. Fukata M., Kaibuchi K. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat. Rev. Mol. Cell Biol. 2001, 2:887-897.
15. Samarin S., Nusrat A. Regulation of epithelial apical junctional complex by Rho family GTPases. Front. Biosci. 2009, 14:1129-1142.
16. Braga V.M., Del Maschio A., Machesky L., Dejana E. Regulation of cadherin function by Rho and Rac: modulation by junction maturation and cellular context. Mol. Biol. Cell 1999, 10:9-22.
17. Yap A.S., Kovacs E.M. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 2003, 160:11-16.
18. Takaishi K., Sasaki T., Kotani H., Nishioka H., Takai Y. Regulation of cell-cell adhesion by rac and rho small G proteins in MDCK cells. J. Cell Biol. 1997, 139:1047-1059.
19. Schuck S., Simons K. Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 2004, 117:5955-5964.
20. Niethammer P., Delling M., Sytnyk V., Dityatev A., Fukami K., Schachner M. Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J. Cell Biol. 2002, 157:521-532.
21. van Deurs B., Roepstorff K., Hommelgaard A.M., Sandvig K. Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol. 2003, 13:92-100.
22. Nusrat A., Parkos C.A., Verkade P., Foley C.S., Liang T.W., Innis-Whitehouse W., Eastburn K.K., Madara J.L. Tight junctions are membrane microdomains. J. Cell Sci. 2000, 113(Pt 10):1771-1781.
23. Taulet N., Comunale F., Favard C., Charrasse S., Bodin S., Gauthier-Rouviere C. N-cadherin/P120 catenin association at cell-cell contacts occurs in cholesterol-rich membrane domains and is required for rhoa activation and myogenesis. J. Biol. Chem. 2009.
24. Langhorst M.F., Reuter A., Stuermer C.A. Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell. Mol. Life Sci. 2005, 62:2228-2240.
25. Vassilieva E.V., Ivanov A.I., Nusrat A. Flotillin-1 stabilizes caveolin-1 in intestinal epithelial cells. Biochem. Biophys. Res. Commun. 2009, 379:460-465.
26. Babuke T., Tikkanen R. Dissecting the molecular function of reggie/flotillin proteins. Eur. J. Cell Biol. 2007, 86:525-532.
27. Liu J., Deyoung S.M., Zhang M., Dold L.H., Saltiel A.R. The stomatin/prohibitin/flotillin/HflK/C domain of flotillin-1 contains distinct sequences that direct plasma membrane localization and protein interactions in 3T3-L1 adipocytes. J. Biol. Chem. 2005, 280:16125-16134.
28. Langhorst M.F., Jaeger F.A., Mueller S., Sven Hartmann L., Luxenhofer G., Stuermer C.A. Reggies/flotillins regulate cytoskeletal remodeling during neuronal differentiation via CAP/ponsin and Rho GTPases. Eur. J. Cell Biol. 2008, 87:921-931.
29. Chartier N.T., Laine M., Gout S., Pawlak G., Marie C.A., Matos P., Block M.R., Jacquier-Sarlin M.R. Laminin-5-integrin interaction signals through PI 3-kinase and Rac1b to promote assembly of adherens junctions in HT-29 cells. J. Cell Sci. 2006, 119:31-46.
30. Sander E.E., van Delft S., ten Klooster J.P., Reid T., van der Kammen R.A., Michiels F., Collard J.G. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 1998, 143:1385-1398.
31. Stieger B., Marxer A., Hauri H.P. Isolation of brush-border membranes from rat and rabbit colonocytes: is alkaline phosphatase a marker enzyme?. J. Membr. Biol. 1986, 91:19-31.
32. Merritt E.A., Sarfaty S., van den Akker F., L'Hoir C., Martial J.A., Hol W.G. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 1994, 3:166-175.
33. Smart E.J., Anderson R.G. Alterations in membrane cholesterol that affect structure and function of caveolae. Meth. Enzymol. 2002, 353:131-139.
34. Kowalczyk A.P., Reynolds A.B. Protecting your tail: regulation of cadherin degradation by p120-catenin. Curr. Opin. Cell Biol. 2004, 16:522-527.
35. Quaroni A., Tian J.Q., Seth P., Ap Rhys C. p27(Kip1) is an inducer of intestinal epithelial cell differentiation. Am. J. Physiol. Cell Physiol. 2000, 279:C1045-C1057.
36. Betson M., Lozano E., Zhang J., Braga V.M. Rac activation upon cell-cell contact formation is dependent on signaling from the epidermal growth factor receptor. J. Biol. Chem. 2002, 277:36962-36969.
37. Wildenberg G.A., Dohn M.R., Carnahan R.H., Davis M.A., Lobdell N.A., Settleman J., Reynolds A.B. p120-Catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 2006, 127:1027-1039.
38. Moreno-Altamirano M.M., Aguilar-Carmona I., Sanchez-Garcia F.J. Expression of GM1, a marker of lipid rafts, defines two subsets of human monocytes with differential endocytic capacity and lipopolysaccharide responsiveness. Immunology 2007, 120:536-543.
39. Danielsen E.M., Hansen G.H. Lipid rafts in epithelial brush borders: atypical membrane microdomains with specialized functions. Biochim. Biophys. Acta 2003, 1617:1-9.
40. Harris T.J., Siu C.H. Reciprocal raft-receptor interactions and the assembly of adhesion complexes. Bioessays 2002, 24:996-1003.
41. Epand R.M. Proteins and cholesterol-rich domains. Biochim. Biophys. Acta 2008, 1778:1576-1582.
42. Lopez-Casas P.P., del Mazo J. Regulation of flotillin-1 in the establishment of NIH-3T3 cell-cell interactions. FEBS Lett. 2003, 555:223-228.
43. Hoehne M., de Couet H.G., Stuermer C.A., Fischbach K.F. Loss- and gain-of-function analysis of the lipid raft proteins Reggie/Flotillin in Drosophila: they are posttranslationally regulated, and misexpression interferes with wing and eye development. Mol. Cell. Neurosci. 2005, 30:326-338.
44. Neumann-Giesen C., Fernow I., Amaddii M., Tikkanen R. Role of EGF-induced tyrosine phosphorylation of reggie-1/flotillin-2 in cell spreading and signaling to the actin cytoskeleton. J. Cell Sci. 2007, 120:395-406.
45. Roitbak T., Surviladze Z., Tikkanen R., Wandinger-Ness A. A polycystin multiprotein complex constitutes a cholesterol-containing signalling microdomain in human kidney epithelia. Biochem. J. 2005, 392:29-38.
46. Stuermer C.A., Lang D.M., Kirsch F., Wiechers M., Deininger S.O., Plattner H. Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol. Biol. Cell 2001, 12:3031-3045.
47. Braga V.M., Betson M., Li X., Lamarche-Vane N. Activation of the small GTPase Rac is sufficient to disrupt cadherin-dependent cell-cell adhesion in normal human keratinocytes. Mol. Biol. Cell 2000, 11:3703-3721.
48. Comunale F., Causeret M., Favard C., Cau J., Taulet N., Charrasse S., Gauthier-Rouviere C. Rac1 and RhoA GTPases have antagonistic functions during N-cadherin-dependent cell-cell contact formation in C2C12 myoblasts. Biol. Cell 2007, 99:503-517.
49. Benoit Y.D., Lussier C., Ducharme P.A., Sivret S., Schnapp L.M., Basora N., Beaulieu J.F. Integrin alpha8beta1 regulates adhesion, migration and proliferation of human intestinal crypt cells via a predominant RhoA/ROCK dependent mechanism. Biol. Cell 2009.
50. Pageot L.P., Perreault N., Basora N., Francoeur C., Magny P., Beaulieu J.F. Human cell models to study small intestinal functions: recapitulation of the crypt-villus axis. Microsc. Res. Tech. 2000, 49:394-406.
51. Ehrlich J.S., Hansen M.D., Nelson W.J. Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev. Cell 2002, 3:259-270.
52. Kovacs E.M., Ali R.G., McCormack A.J., Yap A.S. E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 2002, 277:6708-6718.
53. Shewan A.M., Maddugoda M., Kraemer A., Stehbens S.J., Verma S., Kovacs E.M., Yap A.S. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 2005, 16:4531-4542.
54. del Pozo M.A., Alderson N.B., Kiosses W.B., Chiang H.H., Anderson R.G., Schwartz M.A. Integrins regulate Rac targeting by internalization of membrane domains. Science 2004, 303:839-842.
55. Smalley-Freed W., Efimov A., Burnett P., Short S., Davis M., Gumucio D., Washington M., Coffey R., Reynolds A. p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J. Clin. Invest. 2010, 120:1824-1835.
56. Karayiannakis A.J., Syrigos K.N., Efstathiou J., Valizadeh A., Noda M., Playford R.J., Kmiot W., Pignatelli M. Expression of catenins and E-cadherin during epithelial restitution in inflammatory bowel disease. J. Pathol. 1998, 185:413-418.
57. Li Q., Zhang Q., Zhang M., Wang C., Zhu Z., Li N., Li J. Effect of n-3 polyunsaturated fatty acids on membrane microdomain localization of tight junction proteins in experimental colitis. FEBS J. 2008, 275:411-420.