The dual role of annexin II in targeting of brush border proteins and in intestinal cell polarity

Differentiation

Volumn 81, Issue 4, 2011, Pages 243-252

  Hein, Zeynep ^a   Schmidt, Sonja ^a   Zimmer, Klaus Peter ^b   Naim, Hassan Y ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Brush border membrane; Caco 2 cells; Cell differentiation; Cytokeratin 19

Indexed keywords

CYTOKERATIN 19; EZRIN; INTESTINE ENZYME; LIPOCORTIN 2; SUCRASE ISOMALTASE;

APICAL MEMBRANE; ARTICLE; CELL ADHESION; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL JUNCTION; CELL POLARITY; CELL STRAIN CACO 2; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; LIPID RAFT; MICROVILLUS; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; ULTRASTRUCTURE;

ACTINS; ANNEXIN A2; CACO-2 CELLS; CELL DIFFERENTIATION; CELL POLARITY; CYTOSKELETAL PROTEINS; ENTEROCYTES; GENE EXPRESSION REGULATION; HUMANS; INTESTINAL MUCOSA; INTRACELLULAR MEMBRANES; KERATIN-19; MEMBRANE MICRODOMAINS; MICROVILLI; PROTEIN TRANSPORT; SUCRASE-ISOMALTASE COMPLEX;

EID: 79954603156     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.01.009     Document Type: Article

References (60)

1. Babbin B.A., Parkos C.A., Mandell K.J., Winfree L.M., Laur O., Ivanov A.I., Nusrat A. Annexin 2 regulates intestinal epithelial cell spreading and wound closure through Rho-related signaling. Am. J. Pathol. 2007, 170:951-966.
2. Beaulieu J.F., Quaroni A. Clonal analysis of sucrose-isomaltase expression in the human colon adenocarcinoma Caco-2 cells. Biochem. J. 1991, 280(Pt. 3):599-608.
3. Benaud C., Gentil B.J., Assard N., Court M., Garin J., Delphin C., Baudier J. AHNAK interaction with the annexin 2/S100A10 complex regulates cell membrane cytoarchitecture. J. Cell Biol. 2004, 164:133-144.
4. Bianchi R., Garbuglia M., Verzini M., Giambanco I., Donato R. Calpactin I binds to the glial fibrillary acidic protein (GFAP) and cosediments with glial filaments in a Ca(2+)-dependent manner: implications for concerted regulatory effects of calpactin I and S100 protein on glial filaments. Biochim. Biophys. Acta 1994, 1223:361-367.
5. Borthwick L.A., Neal A., Hobson L., Gerke V., Robson L., Muimo R. The annexin 2-S100A10 complex and its association with TRPV6 is regulated by cAMP/PKA/CnA in airway and gut epithelia. Cell Calcium 2008, 44:147-157.
6. Borthwick L.A., Riemen C., Goddard C., Colledge W.H., Mehta A., Gerke V., Muimo R. Defective formation of PKA/CnA-dependent annexin 2-S100A10/CFTR complex in DeltaF508 cystic fibrosis cells. Cell Signal. 2008, 20:1073-1083.
7. Boucher M.J., Laprise P., Rivard N. Cyclic AMP-dependent protein kinase A negatively modulates adherens junction integrity and differentiation of intestinal epithelial cells. J. Cell Physiol. 2005, 202:178-190.
8. Bretscher A., Reczek D., Berryman M. Ezrin: a protein requiring conformational activation to link microfilaments to the plasma membrane in the assembly of cell surface structures. J. Cell Sci. 1997, 110(Pt. 24):3011-3018.
9. Cereijido M., Shoshani L., Contreras R.G. Molecular physiology and pathophysiology of tight junctions. I. Biogenesis of tight junctions and epithelial polarity. Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 279:G477-G482.
10. Chantret I., Barbat A., Dussaulx E., Brattain M.G., Zweibaum A. Epithelial polarity, villin expression, and enterocytic differentiation of cultured human colon carcinoma cells: a survey of twenty cell lines. Cancer Res. 1988, 48:1936-1942.
11. Chantret I., Rodolosse A., Barbat A., Dussaulx E., Brot-Laroche E., Zweibaum A., Rousset M. Differential expression of sucrose-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J. Cell Sci. 1994, 107(Pt. 1):213-225.
12. Chou C.F., Riopel C.L., Rott L.S., Omary M.B. A significant soluble keratin fraction in 'simple' epithelial cells. Lack of an apparent phosphorylation and glycosylation role in keratin solubility. J. Cell Sci. 1993, 105(Pt. 2):433-444.
13. de Graauw M., Tijdens I., Smeets M.B., Hensbergen P.J., Deelder A.M., van de Water B. Annexin A2 phosphorylation mediates cell scattering and branching morphogenesis via cofilin Activation. Mol. Cell Biol. 2008, 28:1029-1040.
14. Delacour D., Cramm-Behrens C.I., Drobecq H., Le Bivic A., Naim H.Y., Jacob R. Requirement for galectin-3 in apical protein sorting. Curr. Biol. 2006, 16:408-414.
15. Drust D.S., Creutz C.E. Aggregation of chromaffin granules by calpactin at micromolar levels of calcium. Nature 1988, 331:88-91.
16. Gerke V., Moss S.E. Annexins: from structure to function. Physiol. Rev. 2002, 82:331-371.
17. Gerke V., Weber K. Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J. 1984, 3:227-233.
18. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
19. Halbleib J.M., Saaf A.M., Brown P.O., Nelson W.J. Transcriptional modulation of genes encoding structural characteristics of differentiating enterocytes during development of a polarized epithelium in vitro. Mol. Biol. Cell 2007, 18:4261-4278.
20. Hastie C., Masters J.R., Moss S.E., Naaby-Hansen S. Interferon-gamma reduces cell surface expression of annexin 2 and suppresses the invasive capacity of prostate cancer cells. J. Biol. Chem. 2008, 283:12595-12603.
21. Hauri H.P., Sterchi E.E., Bienz D., Fransen J.A., Marxer A. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells. J. Cell Biol. 1985, 101:838-851.
22. Hayes M.J., Rescher U., Gerke V., Moss S.E. Annexin-actin interactions. Traffic 2004, 5:571-576.
23. Hayes M.J., Shao D., Bailly M., Moss S.E. Regulation of actin dynamics by annexin 2. EMBO J. 2006, 25:1816-1826.
24. Hegan P.S., Mermall V., Tilney L.G., Mooseker M.S. Roles for Drosophila melanogaster myosin IB in maintenance of enterocyte brush-border structure and resistance to the bacterial pathogen Pseudomonas entomophila. Mol. Biol. Cell 2007, 18:4625-4636.
25. Heine M., Cramm-Behrens C.I., Ansari A., Chu H.P., Ryazanov A.G., Naim H.Y., Jacob R. Alpha-kinase 1, a new component in apical protein transport. J. Biol. Chem. 2005, 280:25637-25643.
26. Heyraud S., Jaquinod M., Durmort C., Dambroise E., Concord E., Schaal J.P., Huber P., Gulino-Debrac D. Contribution of annexin 2 to the architecture of mature endothelial adherens junctions. Mol. Cell Biol. 2008, 28:1657-1668.
27. Jacob R., Heine M., Eikemeyer J., Frerker N., Zimmer K.P., Rescher U., Gerke V., Naim H.Y. Annexin II is required for apical transport in polarized epithelial cells. J. Biol. Chem. 2004, 279:3680-3684.
28. Jacob R., Naim H.Y. Apical membrane proteins are transported in distinct vesicular carriers. Curr. Biol. 2001, 11:1444-1450.
29. Kenny A.J., Maroux S. Topology of microvillar membrance hydrolases of kidney and intestine. Physiol. Rev. 1982, 62:91-128.
30. Le Bivic A., Quaroni A., Nichols B., Rodriguez-Boulan E. Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line. J. Cell Biol. 1990, 111:1351-1361.
31. Ling Q., Jacovina A.T., Deora A., Febbraio M., Simantov R., Silverstein R.L., Hempstead B., Mark W.H., Hajjar K.A. Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J. Clin. Invest. 2004, 113:38-48.
32. Liu L., Fisher A.B., Zimmerman U.J. Lung annexin II promotes fusion of isolated lamellar bodies with liposomes. Biochim. Biophys. Acta 1995, 1259:166-172.
33. Martin-Belmonte F., Gassama A., Datta A., Yu W., Rescher U., Gerke V., Mostov K. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 2007, 128:383-397.
34. Matter K., Brauchbar M., Bucher K., Hauri H.P. Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2). Cell 1990, 60:429-437.
35. Mayran N., Parton R.G., Gruenberg J. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 2003, 22:3242-3253.
36. Merrifield C.J., Rescher U., Almers W., Proust J., Gerke V., Sechi A.S., Moss S.E. Annexin 2 has an essential role in actin-based macropinocytic rocketing. Curr. Biol. 2001, 11:1136-1141.
37. Muller T., Hess M.W., Schiefermeier N., Pfaller K., Ebner H.L., Heinz-Erian P., Ponstingl H., Partsch J., Rollinghoff B., Kohler H., Berger T., Lenhartz H., Schlenck B., Houwen R.J., Taylor C.J., Zoller H., Lechner S., Goulet O., Utermann G., Ruemmele F.M., Huber L.A., Janecke A.R. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet. 2008, 40:1163-1165.
38. Oriolo A.S., Wald F.A., Ramsauer V.P., Salas P.J. Intermediate filaments: a role in epithelial polarity. Exp. Cell Res. 2007, 313:2255-2264.
39. Osborn M., Johnsson N., Wehland J., Weber K. The submembranous location of p11 and its interaction with the p36 substrate of pp60 src kinase in situ. Exp. Cell Res. 1988, 175:81-96.
40. Peterson M.D., Mooseker M.S. An in vitro model for the analysis of intestinal brush border assembly. I. Ultrastructural analysis of cell contact-induced brush border assembly in Caco-2BBe cells. J. Cell Sci. 1993, 105(Pt. 2):445-460.
41. Pinto M., Robine-Leon S., Appay M.D., Kedinger M., Triadou N., Dussaulx E., Lacroix B., Simon-Assmann P., Haffen K., Fogh J., Zweibaum A. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol. Cell 1983, 47:323-330.
42. Pshezhetsky A.V., Fedjaev M., Ashmarina L., Mazur A., Budman L., Sinnett D., Labuda D., Beaulieu J.F., Menard D., Nifant'ev I., Levy E. Subcellular proteomics of cell differentiation: quantitative analysis of the plasma membrane proteome of Caco-2 cells. Proteomics 2007, 7:2201-2215.
43. Quaroni A., Calnek D., Quaroni E., Chandler J.S. Keratin expression in rat intestinal crypt and villus cells. Analysis with a panel of monoclonal antibodies. J. Biol. Chem. 1991, 266:11923-11931.
44. Salas P.J. Insoluble gamma-tubulin-containing structures are anchored to the apical network of intermediate filaments in polarized CACO-2 epithelial cells. J. Cell Biol. 1999, 146:645-658.
45. Salas P.J., Rodriguez M.L., Viciana A.L., Vega-Salas D.E., Hauri H.P. The apical submembrane cytoskeleton participates in the organization of the apical pole in epithelial cells. J. Cell Biol. 1997, 137:359-375.
46. Saotome I., Curto M., McClatchey A.I. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 2004, 6:855-864.
47. Schmitz J., Preiser H., Maestracci D., Ghosh B.K., Cerda J.J., Crane R.K. Purification of the human intestinal brush border membrane. Biochim. Biophys. Acta 1973, 323:98-112.
48. 2+-induced granule-granule fusion. Cell Tissue Res. 1998, 292:513-519.
49. Shaw R.J., Henry M., Solomon F., Jacks T. RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol. Biol. Cell 1998, 9:403-419.
50. Soellner P., Quinlan R.A., Franke W.W. Identification of a distinct soluble subunit of an intermediate filament protein: tetrameric vimentin from living cells. Proc. Natl. Acad. Sci. USA 1985, 82:7929-7933.
51. Steinert P., Zackroff R., Aynardi-Whitman M., Goldman R.D. Isolation and characterization of intermediate filaments. Methods Cell Biol. 1982, 24:399-419.
52. Sterchi E.E., Woodley J.F. Peptide hydrolases of the human small intestinal mucosa: distribution of activities between brush border membranes and cytosol. Clin. Chim. Acta 1980, 102:49-56.
53. Stevenson B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 1986, 103:755-766.
54. Tatenhorst L., Rescher U., Gerke V., Paulus W. Knockdown of annexin 2 decreases migration of human glioma cells in vitro. Neuropathol. Appl. Neurobiol. 2006, 32:271-277.
55. Wald F.A., Oriolo A.S., Casanova M.L., Salas P.J. Intermediate filaments interact with dormant ezrin in intestinal epithelial cells. Mol. Biol. Cell 2005, 16:4096-4107.
56. Wice B.M., Trugnan G., Pinto M., Rousset M., Chevalier G., Dussaulx E., Lacroix B., Zweibaum A. The intracellular accumulation of UDP-N-acetylhexosamines is concomitant with the inability of human colon cancer cells to differentiate. J. Biol. Chem. 1985, 260:139-146.
57. Yamada A., Irie K., Hirota T., Ooshio T., Fukuhara A., Takai Y. Involvement of the annexin II-S100A10 complex in the formation of E-cadherin-based adherens junctions in Madin-Darby canine kidney cells. J. Biol. Chem. 2005, 280:6016-6027.
58. Zobiack N., Rescher U., Laarmann S., Michgehl S., Schmidt M.A., Gerke V. Cell-surface attachment of pedestal-forming enteropathogenic E. coli induces a clustering of raft components and a recruitment of annexin 2. J. Cell Sci. 2002, 115:91-98.
59. Zobiack N., Rescher U., Ludwig C., Zeuschner D., Gerke V. The annexin 2/S100A10 complex controls the distribution of transferrin receptor-containing recycling endosomes. Mol. Biol. Cell 2003, 14:4896-4908.
60. Zweibaum A., Triadou N., Kedinger M., Augeron C., Robine-Leon S., Pinto M., Rousset M., Haffen K. Sucrase-isomaltase: a marker of foetal and malignant epithelial cells of the human colon. Int. J. Cancer 1983, 32:407-412.