The Drosophila p21-activated kinase Mbt modulates DE-cadherin-mediated cell adhesion by Phosphorylation of Armadillo

Biochemical Journal

Volumn 416, Issue 2, 2008, Pages 231-241

  Menzel, Nicolas ^a,e   Melzer, Juliane ^a   Waschke, Jens ^b   Lenz, Christof ^c   Wecklein, Heike ^a   Lochnits, Günter ^d   Drenckhahn, Detlev ^b   Raabe, Thomas ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c Applera Deutschland GmbH   (Germany)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cadherin catenin complex; Drosophila; Kinase activity; P21 activated kinase (PAK)

Indexed keywords

ACTIN CYTOSKELETON; ADHERENS JUNCTIONS; CADHERIN-CATENIN COMPLEX; DROSOPHILA; DYNAMIC MODULATION; FUNCTIONAL LINKS; KINASE ACTIVITY; MOLECULAR MECHANISM; MUTATIONAL ANALYSIS; P-21 ACTIVATED KINASE; P21-ACTIVATED KINASE (PAK); PHENOTYPIC ANALYSIS; PHOSPHORYLATION SITES;

AMINO ACIDS; CELL ADHESION; PHOSPHORYLATION;

ADHESION;

ALPHA CATENIN; ARMADILLO DOMAIN PROTEIN; BETA CATENIN; CADHERIN; P21 ACTIVATED KINASE; PROTEIN MBT; SERINE; UNCLASSIFIED DRUG; ARMADILLO PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; MUSHROOM BODIES TINY PROTEIN, DROSOPHILA; PAK4 PROTEIN, HUMAN; PROTEIN KINASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL STRAIN HEK293; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; ANIMAL; CELL LINE; GENETICS; KIDNEY; METABOLISM; MOLECULAR CLONING; PHOSPHORYLATION; PHYSIOLOGY;

ARMADILLO; VERTEBRATA;

ANIMALS; ARMADILLO DOMAIN PROTEINS; CADHERINS; CELL LINE; CLONING, MOLECULAR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; KIDNEY; P21-ACTIVATED KINASES; PHOSPHORYLATION; PROTEIN KINASES; TRANSCRIPTION FACTORS;

EID: 58149293388     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20080465     Document Type: Article

References (51)

1. Gumbiner, B. M. (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634
2. Halbleib, J. M. and Nelson, W. J. (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20, 3199-3214
3. Perez-Moreno, M., Jamora, C. and Fuchs, E. (2003) Sticky business: orchestrating cellular signals at adherens junctions. Cell 112, 535-548
4. Weis, W. I. and Nelson, W. J. (2006) Re-solving the cadherin-catenin-actin conundrum. J. Biol. Chem. 281, 35593-35597
5. Brembeck, F. H., Rosario, M. and Birchmeier, W. (2006) Balancing cell adhesion and Wnt signaling, the key role of β-catenin. Curr. Opin. Genet. Dev. 16, 1-9
6. Daugherty, R. L. and Gottardi, J. C. (2007) Phospho-regulation of β-catenin adhesion and signaling functions. Physiology 22, 303-309
7. Rhee, J., Buchan, T., Zukerberg, L., Lilien, J. and Balsamo, J. (2007) Cables links Robo-bound Abl kinase to N-cadherin-bound β-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat. Cell Biol. 9, 883-892
8. Bek, S. and Kemler, R. (2002) Protein kinase CKII regulates the interaction of β-catenin with α-catenin and its protein stability. J. Cell Sci. 115, 4743-4753
9. Pai, L. M., Orsulic, S., Bejsovec, A. and Peifer, M. (1997) Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124, 2255-2266
10. Arias-Romero, L. E. and Chernoff, J. (2008) A tale of two Paks. Biol. Cell 100, 97-108
11. Braga, V. M. M. and Yap, A. S. (2005) The challenges of abundance: epithelial junctions and small GTPase signalling. Curr. Opin. Cell Biol. 17, 466-474
12. Jaffer, Z. M. and Chernoff, J. (2004) The cross-Rho'ds of cell-cell adhesion. J. Biol. Chem. 279, 35123-35126
13. Qu, J., Cammarano, M. S., Shi, Q., Ha, K. C., de Lanerolle, P. and Minden, A. (2001) Activated PAK4 regulates cell adhesion and anchorage-independent growth. Mol. Cell. Biol. 21, 3523-3533
14. Callow, M. G., Clairvoyant, F., Zhu, S., Schryver, B., Whyte, D. B., Bischoff, J. R., Jallal, B. and Smeal, T. (2002) Requirement for PAK4 in the anchorage-independent growth of human cancer cell lines. J. Biol. Chem. 277, 550-558
15. Faure, S., Cau, J., de Santa Barbara, P., Bigou, S., Ge, Q., Delsert, C. and Morin, N. (2005) Xenopus p21-activated kinase 5 regulates blastomeres' adhesive properties during convergent extension movements. Dev. Biol. 277, 472-492
16. Menzel, N., Schneeberger, D. and Raabe, T. (2007) The Drosophila p21 activated kinase Mbt regulates the actin cytoskeleton and adherens junctions to control photoreceptor cell morphogenesis. Mech. Dev. 124, 78-90
17. Schneeberger, D. and Raabe, T. (2003) Mbt, a Drosophila PAK protein, combines with Cdc42 to regulate photoreceptor cell morphogenesis. Development 130, 427-437
18. Menzel, N., Chari, A., Fischer, U., Linder, M. and Raabe, T. (2007) A 5′-fluorosulfonylbenzoyladenosine-based method to identify physiological substrates of a Drosophila p21-activated kinase. Anal. Biochem. 368, 178-184
19. Yanagawa, S.-I., Lee, J.-S. and Ishimoto, A. (1998) Identification and characterization of a novel line of Drosophila Schneider S2 cells that respond to Wingless signaling. J. Biol. Chem. 273, 32353-32359
20. Wodarz, A., Stewart, D. B., Nelson, W. J. and Nusse, R. (2006) Wingless signaling modulates cadherin-mediated cell adhesion in Drosophila imaginal disc cells. J. Cell Sci. 119, 2425-2434
21. Baumgartner, W., Schutz, G. J., Wiegand, J., Golenhofen, N. and Drenckhahn, D. (2003) Cadherin function probed by laser tweezer and single molecule fluorescence in vascular endothelial cells. J. Cell Sci. 116, 1001-1011
22. Williamson, B. L., Marchese, J. and Morrice, N. A. (2006) Automated identification and quantification of protein phosphorylation sites by LC/ MS on a hybrid triple quadrupole linear ion trap mass spectrometer. Mol. Cell. Proteomics 5, 337-346
23. Cordero, J. B., Larson, D. E., Craig, C. R., Hays, R. and Cagan, R. (2007) Dynamic decapentaplegic signaling regulates patterning and adhesion in the Drosophila pupal retina. Development 134, 1861-1871
24. Tepass, U. and Harris, K. P. (2007) Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol. 17, 26-35
25. Wang, F., Dumstrei, K., Haag, T. and Hartenstein, V. (2004) The role of DE-cadherin during cellularization, germ layer formation and early neurogenesis in the Drosophila embryo. Dev. Biol. 270, 350-363
26. Lambert, M., Padilla, F. and Mege, R. M. (2000) Immobilized dimers of N-cadherin-Fc chimera mimic cadherin-mediated cell contact formation: contribution of both outside-in and inside-out signals. J. Cell Sci. 113, 2207-2219
27. Drees, F., Reilein, A. and Nelson, W. J. (2005) Cell adhesion assays: fabrication of an E-cadherin substratum and isolation of lateral and basal membrane patches. Methods Mol. Biol. 294, 303-320
28. Matsubayashi, H., Sese, S., Lee, J.-S., Shirakawa, T., Iwatsubo, T., Tomita, T. and Yanagawa, S.-I. (2004) Biochemical characterization of the Drosophila wingless signaling pathway based on RNA interference. Mol. Cell. Biol. 24, 2012-2024
29. Peifer, M., Pai, L.-M. and Casey, M. (1994) Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for Wingless signal and Zeste-white 3 kinase. Dev. Biol. 166, 543-556
30. Yanagawa, S., Matsuda, Y., Lee, J. S., Matsubayashi, H., Sese, S., Kadowaki, T. and Ishimoto, A. (2002) Casein kinase I phosphorylates the Armadillo protein and induces its degradation in Drosophila. EMBO J. 21, 1733-1742
31. Rennefahrt, U. E. E., Deacon, S. W., Parker, S. A., Devarajan, K., Beeser, A., Chernoff, J., Knapp, S., Turk, B. E. and Peterson, J. R. (2007) Specificity profiling of Pak kinases allows identification of novel phosphorylation sites. J. Biol. Chem. 282, 15667-15678
32. Zhu, G., Fujii, K., Liu, Y., Codrea, V., Herrero, J. and Shaw, S. (2005) A single pair of acidic residues in the kinase major groove mediates strong substrate preference for P-2 or P-5 arginine in the AGC, CAMK, and STE kinase families. J. Biol. Chem. 280, 36372-36379
33. Kumar, R., Gururaj, A. E. and Barnes, C. J. (2006) p21-activated kinases in cancer. Nat. Rev. Cancer 6, 459-471
34. Kuroda, S., Fukata, M., Nakagawa, M., Fujii, K., Nakamura, T., Ookubo, T., Izawa, I., Nagase, T., Nomura, N., Tani, H. et al. (1998) Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 281, 832-835
35. Bryant, D. M. and Stow, J. L. (2004) The ins and outs of E-cadherin trafficking. Trends Cell Biol. 14, 427-434
36. Leibfried, A. and Bellaiche, Y. (2007) Functions of endosomal trafficking in Drosophila epithelial cells. Curr. Opin. Cell Biol. 19, 446-452
37. Xiao, K., Oas, R. G., Chiasson, C. M. and Kowalczyk, A. P. (2007) Role of p120-catenin in cadherin trafficking. Biochim. Biophys. Acta 1773, 8-16
38. Huber, A. H. and Weis, W. I. (2001) The structure of the β-catenin-E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell 105, 391-402
39. Lickert, H., Bauer, A., Kemler, R. and Stappert, J. (2000) Casein kinase II phosphorylation of E-cadherin increases E-cadherin/β-catenin interaction and strengthens cell-cell adhesion. J. Biol. Chem. 275, 5090-5095
40. Roura, S., Miravet, S., Piedra, J., de Herreros, A. G. and Dunach, M. (1999) Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J. Biol. Chem. 274, 36734-36740
41. Fang, D., Hawke, D., Zheng, Y., Xia, Y., Meisenhelder, J., Nika, H., Mills, G. B., Kobayashi, R., Hunter, T. and Lu, Z. (2007) Phosphorylation of β-catenin by AKT promotes β-catenin transcriptional activity. J. Biol. Chem. 282, 11221-11229
42. Xing, Y., Takemaru, K.-I., Liu, J., Berndt, J. D., Zheng, J. J., Moon, R. T. and Xu, W. (2008) Crystal structure of a full-length β-catenin. Structure 16, 478-487
43. Hino, S.-I., Tanji, C., Nakayama, K. I. and Kikuchi, A. (2005) Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase stabilizes β-catenin through inhibition of its ubiquitination. Mol. Cell. Biol. 25, 9063-9072
44. Taurin, S., Sandbo, N., Qin, Y., Browning, D. and Dulin, N. O. (2006) Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase. J. Biol. Chem. 281, 9971-9976
45. Wang, F. and Hartenstein, V. (2006) Regulation of cell adhesion in the Drosophila embryo by phosphorylation of the cadherin-catenin complex. Cell Tissue Res. 324, 157-166
46. Pacquelet, A. and Rorth, P. (2005) Regulatory mechanisms required for DE-cadherin function in cell migration and other types of adhesion. J. Cell Biol. 170, 803-812
47. Hayashi, T. and Carthew, R. W. (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431, 647-652
48. Mirkovic, I. and Mlodzik, M. (2006) Cooperative activities of Drosophila DE-Cadherin and DN-Cadherin regulate the cell motility process of ommatidial rotation. Development 133, 3283-3293
49. Bao, S. and Cagan, R. (2005) Preferential adhesion mediated by hibris and roughest regulates morphogenesis and patterning in the Drosophila eye. Dev. Cell 8, 925-935
50. Grzeschik, N. A. and Knust, E. (2005) IrreC/rst-mediated cell sorting during Drosophila pupal eye development depends on proper localisation of DE-cadherin. Development 132, 2035-2045
51. Pai, L.-M., Kirkpatrick, C., Blanton, J., Oda, H., Takeichi, M. and Peifer, M. (1996) Drosophila α-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J. Biol. Chem. 271, 32411-32420