Cadherin point mutations alter cell sorting and modulate GTPase signaling

Journal of Cell Science

Volumn 125, Issue 14, 2012, Pages 3299-3309

  Tabdili, Hamid ^a   Barry, Adrienne K ^b   Langer, Matthew D ^a   Chien, Yuan Hung ^b,d   Shi, Quanming ^a,e   Lee, Keng Jin ^a,f   Lu, Shaoying ^c   Leckband, Deborah E ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c University of Illinois at Urbana Champaign   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cadherin; Cell sorting; GTPase; Micropipette manipulation; Recognition

Indexed keywords

CADHERIN; GUANOSINE TRIPHOSPHATASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE; CELL SELECTION; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; CADHERINS; CALCIUM; CALCIUM SIGNALING; CELL ADHESION; CHO CELLS; CRICETINAE; ENZYME ACTIVATION; ERYTHROCYTES; FLOW CYTOMETRY; GTP PHOSPHOHYDROLASES; HUMANS; MICE; POINT MUTATION; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

EID: 84867855562     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.087395     Document Type: Article

References (80)

1. Anastasiadis, P. Z., Moon, S. Y., Thoreson, M. A., Mariner, D. J., Crawford, H. C., Zheng, Y. and Reynolds, A. B. (2000). Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2, 637-644.
2. Bayas, M. V., Leung, A., Evans, E. and Leckband, D. (2006). Lifetime measurements reveal kinetic differences between homophilic cadherin bonds. Biophys. J. 90, 1385- 1395.
3. Becker, K. F., Kremmer, E., Eulitz, M., Becker, I., Handschuh, G., Schuhmacher, C., Müller, W., Gabbert, H. E., Ochiai, A., Hirohashi, S. et al. (1999). Analysis of E-cadherin in diffuse-type gastric cancer using a mutation-specific monoclonal antibody. Am. J. Pathol. 155, 1803-1809.
4. Benard, V. and Bokoch, G. M. (2002). Assay of Cdc42, Rac, and Rho GTPase activation by affinity methods. Methods Enzymol. 345, 349-359.
5. Bibert, S., Jaquinod, M., Concord, E., Ebel, C., Hewat, E., Vanbelle, C., Legrand, P., Weidenhaupt, M., Vernet, T. and Gulino-Debrac, D. (2002). Synergy between extracellular modules of vascular endothelial cadherin promotes homotypic hexameric interactions. J. Biol. Chem. 277, 12790-12801.
6. Boggon, T. J., Murray, J., Chappuis-Flament, S., Wong, E., Gumbiner, B. M. and Shapiro, L. (2002). C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296, 1308-1313.
7. Boulter, E., Garcia-Mata, R., Guilluy, C., Dubash, A., Rossi, G., Brennwald, P. J. and Burridge, K. (2010). Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat. Cell Biol. 12, 477-483.
8. Braga, V. M. (2002). Cell-cell adhesion and signalling. Curr. Opin. Cell Biol. 14, 546- 556.
9. Brieher, W. M., Yap, A. S. and Gumbiner, B. M. (1996). Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 135, 487-496.
10. Burridge, K. and Doughman, R. (2006). Front and back by Rho and Rac. Nat. Cell Biol. 8, 781-782.
11. Chappuis-Flament, S., Wong, E., Hicks, L. D., Kay, C. M. and Gumbiner, B. M. (2001). Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 154, 231-243.
12. Charrasse, S., Meriane, M., Comunale, F., Blangy, A. and Gauthier-Rouvière, C. (2002). N-cadherin-dependent cell-cell contact regulates Rho GTPases and beta- catenin localization in mouse C2C12 myoblasts. J. Cell Biol. 158, 953-965.
13. Chesla, S. E., Selvaraj, P. and Zhu, C. (1998). Measuring two-dimensional receptor- ligand binding kinetics by micropipette. Biophys. J. 75, 1553-1572.
14. Chesla, S. E., Li, P., Nagarajan, S., Selvaraj, P. and Zhu, C. (2000). The membrane anchor influences ligand binding two-dimensional kinetic rates and three-dimensional affinity of FcgammaRIII (CD16). J. Biol. Chem. 275, 10235-10246.
15. Chien, Y. H., Jiang, N., Li, F., Zhang, F., Zhu, C. and Leckband, D. (2008). Two stage cadherin kinetics require multiple extracellular domains but not the cytoplasmic region. J. Biol. Chem. 283, 1848-1856.
16. Comunale, F., Causeret, M., Favard, C., Cau, J., Taulet, N., Charrasse, S. and Gauthier-Rouvière, C. (2007). Rac1 and RhoA GTPases have antagonistic functions during N-cadherin-dependent cell-cell contact formation in C2C12 myoblasts. Biol. Cell 99, 503-517.
17. Deplazes, J., Fuchs, M., Rauser, S., Genth, H., Lengyel, E., Busch, R. and Luber, B. (2009). Rac1 and Rho contribute to the migratory and invasive phenotype associated with somatic E-cadherin mutation. Hum. Mol. Genet. 18, 3632-3644.
18. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005). Alpha- catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin- filament assembly. Cell 123, 903-915.
19. Duguay, D., Foty, R. A. and Steinberg, M. S. (2003). Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev. Biol. 253, 309- 323.
20. Dumaswala, U. J., Wilson, M. J., José, T. and Daleke, D. L. (1996). Glutamine- and phosphate-containing hypotonic storage media better maintain erythrocyte membrane physical properties. Blood 88, 697-704.
21. Evans, E., Leung, A., Heinrich, V. and Zhu, C. (2004). Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl. Acad. Sci. USA 101, 11281-11286.
22. Foty, R. A. and Steinberg, M. S. (2004). Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int. J. Dev. Biol. 48, 397-409.
23. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
24. Fournier, A. K., Campbell, L. E., Castagnino, P., Liu, W. F., Chung, B. M., Weaver, V. M., Chen, C. S. and Assoian, R. K. (2008). Rac-dependent cyclin D1 gene expression regulated by cadherin- and integrin-mediated adhesion. J. Cell Sci. 121, 226-233.
25. Gao, Y., Dickerson, J. B., Guo, F., Zheng, J. and Zheng, Y. (2004). Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA 101, 7618-7623.
26. Gold, E. R. and Fudenberg, H. H. (1967). Chromic chloride: a coupling reagent for passive hemagglutination reactions. J. Immunol. 99, 859-866.
27. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
28. Handschuh, G., Candidus, S., Luber, B., Reich, U., Schott, C., Oswald, S., Becke, H., Hutzler, P., Birchmeier, W., Höfler, H. et al. (1999). Tumour-associated E-cadherin mutations alter cellular morphology, decrease cellular adhesion and increase cellular motility. Oncogene 18, 4301-4312.
29. Handschuh, G., Luber, B., Hutzler, P., Höfler, H. and Becker, K. F. (2001). Single amino acid substitutions in conserved extracellular domains of E-cadherin differ in their functional consequences. J. Mol. Biol. 314, 445-454.
30. Harrison, O. J., Corps, E. M., Berge, T. and Kilshaw, P. J. (2005). The mechanism of cell adhesion by classical cadherins: the role of domain 1. J. Cell Sci. 118, 711-721.
31. Häussinger, D., Ahrens, T., Aberle, T., Engel, J., Stetefeld, J. and Grzesiek, S. (2004). Proteolytic E-cadherin activation followed by solution NMR and X-ray crystallography. EMBO J. 23, 1699-1708.
32. Hilgenfeldt, S., Erisken, S. and Carthew, R. W. (2008). Physical modeling of cell geometric order in an epithelial tissue. Proc. Natl. Acad. Sci. USA 105, 907-911.
33. Huang, J., Chen, J., Chesla, S. E., Yago, T., Mehta, P., McEver, R. P., Zhu, C. and Long, M. (2004). Quantifying the effects of molecular orientation and length on two- dimensional receptor-ligand binding kinetics. J. Biol. Chem. 279, 44915-44923.
34. Huang, J., Edwards, L. J., Evavold, B. D. and Zhu, C. (2007). Kinetics of MHC-CD8 interaction at the T cell membrane. J. Immunol. 179, 7653-7662.
35. Huang, J., Zarnitsyna, V. I., Liu, B., Edwards, L. J., Jiang, N., Evavold, B. D. and Zhu, C. (2010). The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464, 932-936.
36. Humphrey, W., Dalke, A. and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-38.
37. Kalantarian, A., Ninomiya, H., Saad, S. M., David, R., Winklbauer, R. and Neumann, A. W. (2009). Axisymmetric drop shape analysis for estimating the surface tension of cell aggregates by centrifugation. Biophys. J. 96, 1606-1616.
38. Katsamba, P., Carroll, K., Ahlsen, G., Bahna, F., Vendome, J., Posy, S., Rajebhosale, M., Price, S., Jessell, T. M., Ben-Shaul, A. et al. (2009). Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc. Natl. Acad. Sci. USA 106, 11594-11599.
39. Klingelhöfer, J., Troyanovsky, R. B., Laur, O. Y. and Troyanovsky, S. (2000). Amino-terminal domain of classic cadherins determines the specificity of the adhesive interactions. J. Cell Sci. 113, 2829-2836.
40. Kofler, R. and Wick, G. (1977). Some methodologic aspects of the chromium chloride method for coupling antigen to erythrocytes. J. Immunol. Methods 16, 201-209.
41. Krieg, M., Arboleda-Estudillo, Y., Puech, P. H., Käfer, J., Graner, F., Müller, D. J. and Heisenberg, C. P. (2008). Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10, 429-436.
42. Langer, M. D., Guo, H. B., Shashikanth, N., Pierce, M. and Leckband, D. E (2012). N-glycosylation alters cadherin-mediated intercellular binding kinetics. J. Cell Sci. 125, 2478-2485.
43. Levenberg, S., Yarden, A., Kam, Z. and Geiger, B. (1999). p27 is involved in N- cadherin-mediated contact inhibition of cell growth and S-phase entry. Oncogene 18, 869-876.
44. Liu, W. F., Nelson, C. M., Pirone, D. M. and Chen, C. S. (2006). E-cadherin engagement stimulates proliferation via Rac1. J. Cell Biol. 173, 431-441.
45. Manning, M. L., Foty, R. A., Steinberg, M. S. and Schoetz, E. M. (2010). Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc. Natl. Acad. Sci. USA 107, 12517-12522.
46. Marrs, G. S., Theisen, C. S. and Brusés, J. L. (2009). N-cadherin modulates voltage activated calcium influx via RhoA, p120-catenin, and myosin-actin interaction. Mol. Cell. Neurosci. 40, 390-400.
47. Neill, J. W. (1988). Testing for Lack of fit in Nonlinear Regression. Ann. Stat. 16, 733-740.
48. Niessen, C. M. and Gumbiner, B. M. (2002). Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J. Cell Biol. 156, 389-400.
49. Noren, N. K., Arthur, W. T. and Burridge, K. (2003). Cadherin engagement inhibits RhoA via p190RhoGAP. J. Biol. Chem. 278, 13615-13618.
50. Nose, A., Nagafuchi, A. and Takeichi, M. (1988). Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993-1001.
51. Nose, A., Tsuji, K. and Takeichi, M. (1990). Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 61, 147-155.
52. Patel, S. D., Chen, C. P., Bahna, F., Honig, B. and Shapiro, L. (2003). Cadherin- mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13, 690-698.
53. Perret, E., Leung, A., Feracci, H. and Evans, E. (2004). Trans-bonded pairs of E- cadherin exhibit a remarkable hierarchy of mechanical strengths. Proc. Natl. Acad. Sci. USA 101, 16472-16477.
54. Pertz, O., Bozic, D., Koch, A. W., Fauser, C., Brancaccio, A. and Engel, J. (1999). A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18, 1738-1747.
55. Pokutta, S. and Weis, W. I. (2007). Structure and mechanism of cadherins and catenins in cell-cell contacts. Annu. Rev. Cell Dev. Biol. 23, 237-261.
56. Potard, U. S., Butler, J. P. and Wang, N. (1997). Cytoskeletal mechanics in confluent epithelial cells probed through integrins and E-cadherins. Am. J. Physiol. 272, C1654- C1663.
57. Prakasam, A., Chien, Y. H., Maruthamuthu, V. and Leckband, D. E. (2006). Calcium site mutations in cadherin: impact on adhesion and evidence of cooperativity. Biochemistry 45, 6930-6939.
58. Prakasam, A. K., Maruthamuthu, V. and Leckband, D. E. (2006). Similarities between heterophilic and homophilic cadherin adhesion. Proc. Natl. Acad. Sci. USA 103, 15434-15439.
59. Shan, W. S., Tanaka, H., Phillips, G. R., Arndt, K., Yoshida, M., Colman, D. R. and Shapiro, L. (2000). Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol. 148, 579-590.
60. Shapiro, L., Fannon, A. M., Kwong, P. D., Thompson, A., Lehmann, M. S., Grübel, G., Legrand, J. F., Als-Nielsen, J., Colman, D. R. and Hendrickson, W. A. (1995). Structural basis of cell-cell adhesion by cadherins. Nature 374, 327-337.
61. Shi, Q., Chien, Y. H. and Leckband, D. (2008). Biophysical properties of cadherin bonds do not predict cell sorting. J. Biol. Chem. 283, 28454-28463.
62. Sivasankar, S., Brieher, W., Lavrik, N., Gumbiner, B. and Leckband, D. (1999). Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl. Acad. Sci. USA 96, 11820-11824.
63. Sivasankar, S., Gumbiner, B. and Leckband, D. (2001). Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains. Biophys. J. 80, 1758-1768.
64. Steinberg, M. S. (1963). Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141, 401-408.
65. Steinberg, M. S. (2007). Differential adhesion in morphogenesis: a modern view. Curr. Opin. Genet. Dev. 17, 281-286.
66. Steinberg, M. S. and Takeichi, M. (1994). Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl. Acad. Sci. USA 91, 206-209.
67. Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H. and Takai, Y. (1997). Regulation of cell-cell adhesion by rac and rho small G proteins in MDCK cells. J. Cell Biol. 139, 1047-1059.
68. Takeichi, M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
69. Takeichi, M. and Nakagawa, S. (2001). Cadherin-dependent cell-cell adhesion. In Current Protocols in Cell Biology, pp 9.3.1-9.3.15. New York: Wiley.
70. Tamura, K., Shan, W. S., Hendrickson, W. A., Colman, D. R. and Shapiro, L. (1998). Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20, 1153-1163.
71. Taulet, N., Comunale, F., Favard, C., Charrasse, S., Bodin, S. and Gauthier- Rouvière, C. (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.
72. Tomschy, A., Fauser, C., Landwehr, R. and Engel, J. (1996). Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N-terminal domains. EMBO J. 15, 3507-3514.
73. Tsukasaki, Y., Kitamura, K., Shimizu, K., Iwane, A. H., Takai, Y. and Yanagida, T. (2007). Role of multiple bonds between the single cell adhesion molecules, nectin and cadherin, revealed by high sensitive force measurements. J. Mol. Biol. 367, 996-1006.
74. Wang, N., Butler, J. P. and Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127.
75. Wildenberg, G. A., Dohn, M. R., Carnahan, R. H., Davis, M. A., Lobdell, N. A., Settleman, J. and Reynolds, A. B. (2006). p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027- 1039.
76. Winklbauer, R. (2009). Cell adhesion in amphibian gastrulation. Int. Rev. Cell Mol. Biol. 278, 215-275.
77. Yap, A. S. and Kovacs, E. M. (2003). Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 160, 11-16.
78. Yeung, C., Purves, T., Kloss, A. A., Kuhl, T. L., Sligar, S. and Leckband, D. (1999). Cytochrome c Recognition of Immobilized, Orientational Variants of Cytochrome b5: Direct Force and Equilibrium Binding Measurements. Langmuir 15, 6829-6836.
79. Zhang, F., Marcus, W. D., Goyal, N. H., Selvaraj, P., Springer, T. A. and Zhu, C. (2005). Two-dimensional kinetics regulation of alphaLbeta2-ICAM-1 interaction by conformational changes of the alphaL-inserted domain. J. Biol. Chem. 280, 42207- 42218.
80. Zhu, B., Chappuis-Flament, S., Wong, E., Jensen, I. E., Gumbiner, B. M. and Leckband, D. (2003). Functional analysis of the structural basis of homophilic cadherin adhesion. Biophys. J. 84, 4033-4042.