The allosteric role of the Ca2+ switch in adhesion and elasticity of C-cadherin

Biophysical Journal

Volumn 94, Issue 12, 2008, Pages 4621-4633

  Sotomayor, Marcos ^a   Schulten, Klaus ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

C CADHERIN PROTEIN, XENOPUS; C-CADHERIN PROTEIN, XENOPUS; CADHERIN; CALCIUM; XENOPUS PROTEIN;

ARTICLE; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ELASTICITY; MECHANICAL STRESS; PROTEIN BINDING; PROTEIN CONFORMATION; ULTRASTRUCTURE;

BINDING SITES; CADHERINS; CALCIUM; COMPUTER SIMULATION; ELASTICITY; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; STRESS, MECHANICAL; XENOPUS PROTEINS;

EID: 45849137475     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.125591     Document Type: Article

References (91)

1. Takeichi, M. 1990. Cadherins: a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 59:237-252.
2. Hynes, R. O. 1999. Cell adhesion: old and new questions. Trends Cell Biol. 9:M33-M37.
3. Takeichi, M. 2005. Looking for cell-cell adhesion molecules: a cadherin story. Proc. Jpn. Acad. 81:321-328.
4. Gumbiner, B. M. 2005. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6:622-634.
5. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1451-1455.
6. Takeichi, M. 1995. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7:619-627.
7. Takeichi, M. 2007. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8:11-20.
8. Leckband, D., and A. Prakasam. 2006. Mechanism and dynamics of cadherin adhesion. Annu. Rev. Biomed. Eng. 8:259-287.
9. Corey, D. P., and M. Sotomayor. 2004. Tightrope act. Nature. 428:901-902.
10. Söllner, C., G.-J. Rauch, J. Siemens, R. Geisler, S. C. Schuster, U. Müller, and T. Nicolson. 2004. The Tübingen 2000 Screen Consortium. Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature. 428:955-958.
11. Siemens, J., C. Lillo, R. A. Dumont, A. Reynolds, D. S. Williams, P. G. Gillespie, and U. Müller. 2004. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature. 428:950-955.
12. Kazmierczak, P., H. Sakaguchi, J. Tokita, E. M. Wilson-Kubalek, R. A. Milligan, U. Müller, and B. Kachar. 2007. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature. 449:87-91.
13. Shapiro, L., P. D. Kwong, A. M. Fannon, D. R. Colman, and W. A. Hendrickson. 1995. Consideration on the folding topology and evolutionary origin of cadherin domains. Proc. Natl. Acad. Sci. USA. 92:6793-6797.
14. Nollet, F., P. Kools, and F. van Roy. 2000. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299:551-572.
15. Patel, S. D., C. P. Chen, F. Bahna, B. Honig, and L. Shapiro. 2003. Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13:690-698.
16. Koch, A. W., D. Bozi, O. Pertz, and J. Engel. 1999. Homophilic adhesion by cadherins. Curr. Opin. Struct. Biol. 9:275-281.
17. Nagar, B., M. Overdulin, M. Ikura, and J. Rini. 1996. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature. 380:360-364.
18. Tomschy, A., C. Fauser, R. Landwehr, and J. Engel. 1996. Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N-terminal domains. EMBO J. 15:3507-3514.
19. Yap, A. S., W. M. Brieher, M. Pruschy, and B. M. Gumbiner. 1997. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 7:308-315.
20. Takeda, H., Y. Shimoyama, A. Nagafuchi, and S. Hirohashi. 1999. E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat. Struct. Biol. 6:310-312.
21. Klingelhöfer, J., O. Y. Laur, R. B. Troyanovsky, and S. M. Troyanovsky. 2002. Dynamic interplay between adhesive and lateral E-cadherin dimers. Mol. Cell. Biol. 22:7449-7458.
22. Ahrens, T., M. Lambert, O. Pertz, T. Sasaki, T. Schulthess, R.-M. Mège, R. Timpl, and J. Engel. 2003. Homoassociation of VE-cadherin follows a mechanism common to "classical" cadherins. J. Mol. Biol. 325:733-742.
23. Sivasankar, S., W. Brieher, N. Lavrik, B. Gumbiner, and D. Leckband. 1999. Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl. Acad. Sci. USA. 96:11820-11824.
24. Sivasankar, S., B. Gumbiner, and D. Leckband. 2001. Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains. Biophys. J. 80:1758-1768.
25. Chappuis-Flament, S., E. Wong, L. D. Hicks, C. M. Kay, and B. M. Gumbiner. 2001. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 154:231-243.
26. Zhu, B., S. Chappuis-Flament, E. Wong, I. E. Jensen, B. M. Gumbiner, and D. Leckband. 2003. Functional analysis of the structural basis of homophilic cadherin adhesion. Biophys. J. 84:4033-4042.
27. Perret, E., A. Leung, and E. Evans. 2004. Trans-bonded pairs of E-cadherin exhibit a remarkable hierarchy of mechanical strengths. Proc. Natl. Acad. Sci. USA. 101:16472-16477.
28. Bayas, M. V., A. Leung, E. Evans, and D. Leckband. 2006. Lifetime measurements reveal kinetic differences between homophilic cadherin bonds. Biophys. J. 90:1385-1395.
29. Tsukasaki, Y., K. Kitamura, K. Shimizu, A. H. Iwane, Y. Takai, and T. Yanagida. 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.
30. Pokutta, K., S. Herrenknecht, R. Kemler, and J. Engel. 1994. Conformational changes of the recombinant extracellular domain of E-cadherin upon calcium binding. Eur. J. Biochem. 223:1019-1026.
31. Alattia, J.-R., J. B. Ames, T. Porumb, K. I. Tong, Y. M. Heng, P. Ottensmeyer, C. M. Kay, and M. Ikura. 1997. Lateral self-assembly of E-cadherin directed by cooperative calcium binding. FEBS Lett. 417:405-408.
32. Koch, A. W., S. Pokutta, A. Lustig, and J. Engel. 1997. Calcium binding and homoassociation of E-cadherin domains. Biochemistry. 36:7696-7705.
33. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18:1738-1747.
34. Häussinger, D., T. Ahrens, H.-J. Sass, O. Pertz, J. Engel, and S. Grzesiek. 2002. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation and mapping of contact regions. J. Mol. Biol. 324:823-839.
35. Boggon, T. J., J. Murray, S. Chappuis-Flament, E. Wong, B. M. Gumbiner, and L. Shapiro. 2002. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science. 296:1308-1313.
36. Prasad, A., and S. Pedigo. 2005. Calcium-dependent stability studies of domains 1 and 2 of epithelial cadherin. Biochemistry. 44:13692-13701.
37. Prasad, A., H. Zhao, J. M. Rutherford, H. N. C. Nichols, and S. Pedigo. 2006. Effect of linker segments on the stability of epithelial cadherin domain 2. Proteins Struct. Funct. Bioinform. 62:111-121.
38. Prakasam, A., Y.-H. Chien, V. Maruthamuthu, and D. E. Leckband. 2006. Calcium site mutations in cadherin: impact on adhesion and evidence of cooperativity. Biochemistry. 45:6930-6939.
39. Sotomayor, M., D. P. Corey, and K. Schulten. 2005. In search of the hair-cell gating spring: elastic properties of ankyrin and cadherin repeats. Structure. 13:669-682.
40. Cailliez, F., and R. Lavery. 2005. Cadherin mechanics and complexation: the importance of calcium binding. Biophys. J. 89:3895-3903.
41. Cailliez, F., and R. Lavery. 2006. Dynamics and stability of E-cadherin dimers. Biophys. J. 91:3964-3971.
42. Shapiro, L., A. M. Fannon, P. D. Kwong, A. Thompson, M. S. Lehmann, G. Grübel, J. F. Legrand, J. Als-Nielsen, D. R. Colman, and W. A. Hendrickson. 1995. Structural basis of cell-cell adhesion by cadherins. Nature. 374:327-336.
43. Häussinger, D., T. Ahrens, T. Aberle, J. Engel, J. Stetefeld, and S. Grzesiek. 2004. Proteolytic E-cadherin activation followed by solution NMR and x-ray crystallography. EMBO J. 23:1699-1708.
44. Bayas, M. V., K. Schulten, and D. Leckband. 2004. Forced dissociation of the strand dimer interface between C-cadherin ectodomains. Mech. Chem. Biosystems. 1:101-111.
45. Harrison, O. J., E. M. Corps, T. Berge, and P. J. Kilshaw. 2005. The mechanism of cell adhesion by classical cadherins: the role of domain 1. J. Cell Sci. 118:711-721.
46. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.
47. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
48. MacKerell, A. D., Jr., D. Bashford, M. Bellott, J. R. L. Dunbrack, J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1992. Self-consistent parameterization of biomolecules for molecular modeling and condensed phase simulations. FASEB J. 6:A143.
49. MacKerell, A., Jr., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, I. W. E. Reiher, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
50. MacKerell, A. D., M. Feig, and C. L. Brooks III. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25:1400-1415.
51. Young, A., J. Dewan, C. Nave, and R. Tilton. 1993. Comparison of radiation-induced decay and structure refinement from x-ray data collected from lysozyme crystals at low and ambient temperatures. J. Appl. Cryst. 26:309-319.
52. Buck, M., S. Bouguet-Bonnet, R. W. Pastor, and A. D. MacKerell. 2006. Importance of the CMAP correction to the CHARMM22 protein force field: dynamics of hen lysozyme. Biophys. J. 90:L36-L38.
53. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
54. 9k in the apo and singly and doubly calcium-loaded states. Proteins Struct. Funct. Genet. 33:265-284.
55. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
56. Ortiz, V., S. O. Nielsen, M. L. Klein, and D. E. Discher. 2005. Unfolding a linker between helical repeats. J. Mol. Biol. 349:638-647.
57. Zhong, Y., W. M. Brieher, and B. M. Gumbiner. 1999. Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody. J. Cell Biol. 144:351-359.
58. Baumgartner, W., P. Hinterdorfer, W. Ness, A. Raab, D. Vestweber, H. Schindler, and D. Drenckhahn. 2000. Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 97:4005-4010.
59. Izrailev, S., S. Stepaniants, B. Isralewitz, D. Kosztin, H. Lu, F. Molnar, W. Wriggers, and K. Schulten. 1998. Steered molecular dynamics. In Computational Molecular Dynamics: Challenges, Methods, Ideas, Vol. 4 of Lecture Notes in Computational Science and Engineering. P. Deuflhard, J. Hermans, B. Leimkuhler, A. E. Mark, S. Reich, and R. D. Skeel, editors. Springer-Verlag, Berlin.
60. Isralewitz, B., J. Baudry, J. Gullingsrud, D. Kosztin, and K. Schulten. 2001. Steered molecular dynamics investigations of protein function. J. Mol. Graphics Modeling. 19:13-25.
61. Isralewitz, B., M. Gao, and K. Schulten. 2001. Steered molecular dynamics and mechanical functions of proteins. Curr. Opin. Struct. Biol. 11:224-230.
62. Gao, M., M. Sotomayor, E. Villa, E. Lee, and K. Schulten. 2006. Molecular mechanisms of cellular mechanics. Phys. Chem. Chem. Phys. 8:3692-3706.
63. Sotomayor, M., and K. Schulten. 2007. Single-molecule experiments in vitro and in silico. Science. 316:1144-1148.
64. Gräter, F., J. Shen, H. Jiang, M. Gautel, and H. Grubmüller. 2005. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88:790-804.
65. Lee, E. H., J. Hsin, O. Mayans, and K. Schulten. 2007. Secondary and tertiary structure elasticity of titin Z1Z2 and a titin chain model. Biophys. J. 93:1719-1735.
66. Lee, G., K. Abdi, Y. Jiang, P. Michaely, V. Bennett, and P. E. Marszalek. 2006. Nanospring behavior of ankyrin repeats. Nature. 440:246-249.
67. Michaely, P., D. R. Tomchick, M. Machius, and R. G. W. Anderson. 2002. Crystal structure of a 12 ANK repeat stack from human ankyrin-R. EMBO J. 21:6387-6396.
68. Silver, F. H., D. Christiansen, P. B. Snowhill, Y. Chen, and W. J. Landis. 2000. The role of mineral in the storage of elastic energy in turkey tendons. Biomacromolecules. 1:180-185.
69. Izrailev, S., S. Stepaniants, M. Balsera, Y. Oono, and K. Schulten. 1997. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72:1568-1581.
70. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
71. Lu, H., B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:662-671.
72. Marszalek, P. E., H. Lu, H. Li, M. Carrion-Vazquez, A. F. Oberhauser, K. Schulten, and J. M. Fernandez. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
73. Krammer, A., H. Lu, B. Isralewitz, K. Schulten, and V. Vogel. 1999. Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc. Natl. Acad. Sci. USA. 96:1351-1356.
74. Lu, H., and K. Schulten. 1999. Steered molecular dynamics simulation of conformational changes of immunoglobulin domain I27 interpret atomic force microscopy observations. Chem. Phys. 247:141-153.
75. 10 by steered molecular dynamics. J. Mol. Biol. 323:939-950.
76. Gao, M., D. Craig, O. Lequin, I. D. Campbell, V. Vogel, and K. Schulten. 2003. Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc. Natl. Acad. Sci. USA. 100:14784-14789.
77. Craig, D., M. Gao, K. Schulten, and V. Vogel. 2004. Tuning the mechanical stability of fibronectin type III modules through sequence variation. Structure. 12:21-30.
78. Lu, H., and K. Schulten. 1999. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins Struct. Funct. Genet. 35:453-463.
79. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.
80. Hynes, R. O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687.
81. Patel, S. D., C. Ciatto, C. P. Chen, F. Bahna, N. A. Rajebhosale, I. Schieren, T. M. Jessell, B. Honig, S. R. Price, and L. Shapiro. 2006. Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell. 124:1255-1268.
82. 2+-induced conformational changes. Science. 261:1321-1324.
83. Sopkova, J., M. Renouard, and A. Lewit-Bentley. 1993. The crystal structure of a new high-calcium form of annexin V. J. Mol. Biol. 234:816-825.
84. He, W., P. Cowin, and D. L. Stokes. 2003. Untangling desmosomal knots with electron tomography. Science. 302:109-113.
85. Chen, C. P., S. Posy, A. Ben-Shaul, L. Shapiro, and B. H. Honig. 2005. Specificity of cell-cell adhesion by classical cadherins: critical role for low-affinity dimerization through β-strand swapping. Proc. Natl. Acad. Sci. USA. 102:8531-8536.
86. Prakasam, A. K., V. Maruthamuthu, and D. E. Leckband. 2006. Similarities between heterophilic and homophilic cadherin adhesion. Proc. Natl. Acad. Sci. USA. 103:15434-15439.
87. Bork, J. M., L. M. Peters, S. Riazuddin, S. L. Bernstein, Z. M. Ahmed, S. L. Ness, R. Polomeno, A. Ramesh, M. Schloss, C. R. S. Srisailpathy, S. Wayne, S. Bellman, D. Desmukh, Z. Ahmed, S. N. Khan, V. M. der Kaloustian, X. C. Li, A. Lalwani, S. Riazuddin, M. Bitner-Glindzicz, W. E. Nance, X.-Z. Liu, G. Wistow, R. J. H. Smith, A. J. Griffith, E. R. Wilcox, T. B. Friedman, and R. J. Morell. 2001. Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am. J. Hum. Genet. 68:26-37.
88. de Brouwer, A. P. M., R. J. Pennings, M. Roeters, P. van Hauwe, L. M. Astuto, L. H. Hoefsloot, P. L. M. Huygen, B. van den Helm, A. F. Deutman, J. M. Bork, W. J. Kimberling, F. P. M. Cremers, C. W. R. J. Cremers, and H. Kremer. 2003. Mutations in the calcium-binding motifs of CDH23 and the 35DELG mutation in gjb2 cause hearing loss in one family. Hum. Genet. 112:156-163.
89. Mirijanian, D. T., J. W. Chu, G. S. Ayton, and G. A. Voth. 2007. Atomistic and coarse-grained analysis of double spectrin repeat units: the molecular origins of flexibility. J. Mol. Biol. 365:523-534.
90. Paramore, S., and G. A. Voth. 2006. Examining the influence of linkers and tertiary structure in the forced unfolding of multiple-repeat spectrin molecules. Biophys. J. 91:3436-3445.
91. Marino, M., P. Zou, D. Svergun, P. Garcia, C. Edlich, B. Simon, M. Wilmanns, C. Muhle-Goll, and O. Mayans. 2006. The Ig doublet Z1Z2: a model system for the hybrid analysis of conformational dynamics in Ig tandems from titin. Structure. 14:1437-1447.