Flotillins directly interact with γ-catenin and regulate epithelial cell-cell adhesion

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Kurrle, Nina ^a   Völlner, Frauke ^a   Eming, Rüdiger ^b   Hertl, Michael ^b   Banning, Antje ^a   Tikkanen, Ritva ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLOTILLIN 1; FLOTILLIN 2; PLAKOGLOBIN; UVOMORULIN;

AMINO ACID SEQUENCE; ARMADILLO; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL STRAIN; CELL STRAIN MCF10A; CELL STRUCTURE; CONTROLLED STUDY; DESMOSOME; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID RAFT; MEMBRANE STRUCTURE; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE;

ADHERENS JUNCTIONS; ANALYSIS OF VARIANCE; BLOTTING, WESTERN; CADHERINS; CELL ADHESION; CELL LINE; DNA PRIMERS; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA CATENIN; HUMANS; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; PLASMIDS; RNA INTERFERENCE;

EID: 84896719298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084393     Document Type: Article

References (71)

1. Halbleib JM, Nelson WJ (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20: 3199-3214. (Pubitemid 44904842)
2. Giehl K, Menke A (2008) Microenvironmental regulation of E-cadherin-mediated adherens junctions. Front Biosci 13: 3975-3985. (Pubitemid 351594675)
3. Yap AS (1998) The morphogenetic role of cadherin cell adhesion molecules in human cancer: a thematic review. Cancer Invest 16: 252-261.
4. Green KJ, Getsios S, Troyanovsky S, Godsel LM (2010) Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol 2: a000125.
5. Chappuis-Flament S, Wong E, Hicks LD, Kay CM, Gumbiner BM (2001) Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J Cell Biol 154: 231-243. (Pubitemid 34289291)
6. Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6: 622-634.
7. Zhang Y, Sivasankar S, Nelson WJ, Chu S (2009) Resolving cadherin interactions and binding cooperativity at the single-molecule level. Proc Natl Acad Sci U S A 106: 109-114.
8. McCrea PD, Gu D (2010) The catenin family at a glance. J Cell Sci 123: 637-642.
9. Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. Embo J 8: 1711-1717. (Pubitemid 19273986)
10. Perez-Moreno M, Fuchs E (2006) Catenins: keeping cells from getting their signals crossed. Dev Cell 11: 601-612. (Pubitemid 44644972)
11. Pokutta S, Drees F, Yamada S, Nelson WJ, Weis WI (2008) Biochemical and structural analysis of alpha-catenin in cell-cell contacts. Biochem Soc Trans 36: 141-147. (Pubitemid 351570583)
12. Yang J, Dokurno P, Tonks NK, Barford D (2001) Crystal structure of the M-fragment of alpha-catenin: implications for modulation of cell adhesion. Embo J 20: 3645-3656. (Pubitemid 32691776)
13. Hatzfeld M (1999) The armadillo family of structural proteins. Int Rev Cytol 186: 179-224.
14. Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76: 789-791. (Pubitemid 24085316)
15. Yin T, Green KJ (2004) Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 15: 665-677. (Pubitemid 39550246)
16. Cowin P, Kapprell HP, Franke WW, Tamkun J, Hynes RO (1986) Plakoglobin: a protein common to different kinds of intercellular adhering junctions. Cell 46: 1063-1073. (Pubitemid 17182730)
17. Franke WW, Mueller H, Mittnacht S, Kapprell HP, Jorcano JL (1983) Significance of two desmosome plaque-associated polypeptides of molecular weights 75 000 and 83 000. Embo J 2: 2211-2215.
18. Knudsen KA, Wheelock MJ (1992) Plakoglobin, or an 83-kD homologue distinct from beta-catenin, interacts with E-cadherin and N-cadherin. J Cell Biol 118: 671-679.
19. McCrea PD, Turck CW, Gumbiner B (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254: 1359-1361. (Pubitemid 21917467)
20. Obama H, Ozawa M (1997) Identification of the domain of alpha-catenin involved in its association with beta-catenin and plakoglobin (gamma-catenin). J Biol Chem 272: 11017-11020. (Pubitemid 27184089)
21. Delva E, Tucker DK, Kowalczyk AP (2009) The desmosome. Cold Spring Harb Perspect Biol 1: a002543.
22. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11: 688-699.
23. Brennan D, Peltonen S, Dowling A, Medhat W, Green KJ, et al. (2011) A role for caveolin-1 in desmoglein binding and desmosome dynamics. Oncogene 31: 1636-1648.
24. Seveau S, Bierne H, Giroux S, Prevost MC, Cossart P (2004) Role of lipid rafts in E-cadherin- and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J Cell Biol 166: 743-753. (Pubitemid 39181011)
25. Solis GP, Schrock Y, Hulsbusch N, Wiechers M, Plattner H, et al. (2012) Reggies/flotillins regulate E-cadherin-mediated cell contact formation by affecting EGFR trafficking. Mol Biol Cell 23: 1812-1825.
26. Causeret M, Taulet N, Comunale F, Favard C, Gauthier-Rouviere C (2005) N-cadherin association with lipid rafts regulates its dynamic assembly at cell-cell junctions in C2C12 myoblasts. Mol Biol Cell 16: 2168-2180. (Pubitemid 40632203)
27. Taulet N, Comunale F, Favard C, Charrasse S, Bodin S, et al. (2009) 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 284: 23137-23145.
28. Bickel PE, Scherer PE, Schnitzer JE, Oh P, Lisanti MP, et al. (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 272: 13793-13802. (Pubitemid 27225457)
29. Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, et al. (2004) Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J 378: 509-518. (Pubitemid 38367240)
30. Salzer U, Prohaska R (2001) Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood 97: 1141-1143. (Pubitemid 32154306)
31. Schulte T, Paschke KA, Laessing U, Lottspeich F, Stuermer CA (1997) Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124: 577-587. (Pubitemid 27101691)
32. Amaddii M, Meister M, Banning A, Tomasovic A, Mooz J, et al. (2012) Flotillin-1/reggie-2 protein plays dual role in activation of receptor-tyrosine kinase/mitogen-activated protein kinase signaling. J Biol Chem 287: 7265-7278.
33. Dermine JF, Duclos S, Garin J, St-Louis F, Rea S, et al. (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276: 18507-18512.
34. Glebov OO, Bright NA, Nichols BJ (2006) Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 8: 46-54. (Pubitemid 43064796)
35. Neumann-Giesen C, Fernow I, Amaddii M, Tikkanen R (2007) Role of EGF-induced tyrosine phosphorylation of reggie-1/flotillin-2 in cell spreading and signaling to the actin cytoskeleton. J Cell Sci 120: 395-406. (Pubitemid 46332503)
36. Tomasovic A, Traub S, Tikkanen R (2012) Molecular networks in FGF signaling: flotillin-1 and cbl-associated protein compete for the binding to fibroblast growth factor receptor substrate 2. PLoS One 7: e29739.
37. Berger T, Ueda T, Arpaia E, Chio II, Shirdel EA, et al. (2012) Flotillin-2 deficiency leads to reduced lung metastases in a mouse breast cancer model. Oncogene.
38. Ludwig A, Otto GP, Riento K, Hams E, Fallon PG, et al. (2010) Flotillin microdomains interact with the cortical cytoskeleton to control uropod formation and neutrophil recruitment. J Cell Biol 191: 771-781.
39. Banning A, Regenbrecht CR, Tikkanen R (2013) Increased activity of mitogen activated protein kinase pathway in flotillin-2 knockout mouse model. Cell Signal DOI: 10.1016/j.cellsig.2013.11.001.
40. Lin C, Wu Z, Lin X, Yu C, Shi T, et al. (2011) Knockdown of FLOT1 impairs cell proliferation and tumorigenicity in breast cancer through upregulation of FOXO3a. Clin Cancer Res 17: 3089-3099.
41. Schroeder WT, Stewart-Galetka S, Mandavilli S, Parry DA, Goldsmith L, et al. (1994) Cloning and characterization of a novel epidermal cell surface antigen (ESA). J Biol Chem 269: 19983-19991. (Pubitemid 24250918)
42. Deininger SO, Rajendran L, Lottspeich F, Przybylski M, Illges H, et al. (2003) Identification of teleost Thy-1 and association with the microdomain/lipid raft reggie proteins in regenerating CNS axons. Mol Cell Neurosci 22: 544-554. (Pubitemid 36513575)
43. Hazarika P, Dham N, Patel P, Cho M, Weidner D, et al. (1999) Flotillin 2 is distinct from epidermal surface antigen (ESA) and is associated with filopodia formation. J Cell Biochem 75: 147-159. (Pubitemid 29402553)
44. Hoehne M, de Couet HG, Stuermer CA, Fischbach KF (2005) 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 30: 326-338. (Pubitemid 41416552)
45. Malaga-Trillo E, Solis GP, Schrock Y, Geiss C, Luncz L, et al. (2009) Regulation of embryonic cell adhesion by the prion protein. PLoS Biol 7: e55.
46. Raemaekers T, Peric A, Baatsen P, Sannerud R, Declerck I, et al. (2012) ARF6-mediated endosomal transport of Telencephalin affects dendritic filopodia-tospine maturation. Embo J 31: 3252-3269.
47. Bodrikov V, Solis GP, Stuermer CA (2011) Prion protein promotes growth cone development through reggie/flotillin-dependent N-cadherin trafficking. J Neurosci 31: 18013-18025.
48. Guillaume E, Comunale F, Do Khoa N, Planchon D, Bodin S, et al. (2013) Flotillin micro-domains stabilize Cadherins at cell-cell junctions. J Cell Sci.
49. Chartier NT, Laine MG, Ducarouge B, Oddou C, Bonaz B, et al. (2011) Enterocytic differentiation is modulated by lipid rafts-dependent assembly of adherens junctions. Exp Cell Res 317: 1422-1436.
50. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, et al. (1990) Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 50: 6075-6086. (Pubitemid 20331424)
51. Soule HD, Vazguez J, Long A, Albert S, Brennan M (1973) A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 51: 1409-1416.
52. Boukamp P, Tilgen W, Dzarlieva RT, Breitkreutz D, Haag D, et al. (1982) Phenotypic and genotypic characteristics of a cell line from a squamous cell carcinoma of human skin. J Natl Cancer Inst 68: 415-427. (Pubitemid 12156679)
53. Babuke T, Ruonala M, Meister M, Amaddii M, Genzler C, et al. (2009) Hetero-oligomerization of reggie-1/flotillin-2 and reggie-2/flotillin-1 is required for their endocytosis. Cell Signal 21: 1287-1297.
54. Harder T, Scheiffele P, Verkade P, Simons K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942. (Pubitemid 28243961)
55. Pust S, Klokk TI, Musa N, Jenstad M, Risberg B, et al. (2013) Flotillins as regulators of ErbB2 levels in breast cancer. Oncogene 32: 3443-3451.
56. Yaswen P, Stampfer MR (2002) Molecular changes accompanying senescence and immortalization of cultured human mammary epithelial cells. Int J Biochem Cell Biol 34: 1382-1394. (Pubitemid 35245397)
57. Resnik N, Sepcic K, Plemenitas A, Windoffer R, Leube R, et al. (2010) Desmosome assembly and cell-cell adhesion are membrane raft-dependent processes. J Biol Chem 286: 1499-1507.
58. Troyanovsky RB, Chitaev NA, Troyanovsky SM (1996) Cadherin binding sites of plakoglobin: localization, specificity and role in targeting to adhering junctions. J Cell Sci 109 (Pt 13): 3069-3078. (Pubitemid 27029276)
59. Witcher LL, Collins R, Puttagunta S, Mechanic SE, Munson M, et al. (1996) Desmosomal cadherin binding domains of plakoglobin. J Biol Chem 271: 10904-10909. (Pubitemid 26149904)
60. Aberle H, Schwartz H, Hoschuetzky H, Kemler R (1996) Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to alpha-catenin. J Biol Chem 271: 1520-1526. (Pubitemid 26028639)
61. Chitaev NA, Averbakh AZ, Troyanovsky RB, Troyanovsky SM (1998) Molecular organization of the desmoglein-plakoglobin complex. J Cell Sci 111 (Pt 14): 1941-1949. (Pubitemid 28391060)
62. Chitaev NA, Leube RE, Troyanovsky RB, Eshkind LG, Franke WW, et al. (1996) The binding of plakoglobin to desmosomal cadherins: patterns of binding sites and topogenic potential. J Cell Biol 133: 359-369. (Pubitemid 26132534)
63. Sacco PA, McGranahan TM, Wheelock MJ, Johnson KR (1995) Identification of plakoglobin domains required for association with N-cadherin and alpha-catenin. J Biol Chem 270: 20201-20206.
64. Wahl JK, Sacco PA, McGranahan-Sadler TM, Sauppe LM, Wheelock MJ, et al. (1996) Plakoglobin domains that define its association with the desmosomal cadherins and the classical cadherins: identification of unique and shared domains. J Cell Sci 109 (Pt 5): 1143-1154. (Pubitemid 26168265)
65. Baumann CA, Ribon V, Kanzaki M, Thurmond DC, Mora S, et al. (2000) CAP defines a second signalling pathway required for insulin-stimulated glucose transport. Nature 407: 202-207.
66. Mandai K, Nakanishi H, Satoh A, Takahashi K, Satoh K, et al. (1999) Ponsin/SH3P12: an l-afadin- and vinculin-binding protein localized at cell-cell and cell-matrix adherens junctions. J Cell Biol 144: 1001-1017. (Pubitemid 29238974)
67. Misra A, Pandey C, Sze SK, Thanabalu T (2012) Hypoxia activated EGFR signaling induces epithelial to mesenchymal transition (EMT). PLoS One 7: e49766.
68. Foster LJ, De Hoog CL, Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A 100: 5813-5818. (Pubitemid 36576890)
69. Chazal N, Gerlier D (2003) Virus entry, assembly, budding, and membrane rafts. Microbiol Mol Biol Rev 67: 226-237. (Pubitemid 36693473)
70. Schneider A, Rajendran L, Honsho M, Gralle M, Donnert G, et al. (2008) Flotillin-dependent clustering of the amyloid precursor protein regulates its endocytosis and amyloidogenic processing in neurons. J Neurosci 28: 2874-2882. (Pubitemid 351398889)
71. Sorkina T, Caltagarone J, Sorkin A (2013) Flotillins regulate membrane mobility of the dopamine transporter but are not required for its protein kinase C dependent endocytosis. Traffic 14: 709-724.