Nanomechanics of the cadherin ectodomain: "Canalization" by Ca2+ binding results in a new mechanical element

Journal of Biological Chemistry

Volumn 286, Issue 11, 2011, Pages 9405-9418

  Oroz, Javier ^a   Valbuena, Alejandro ^a   Vera, Andrés Manuel ^a   Mendieta, Jesús ^b,c   Gómez Puertas, Paulino ^b   Carrión Vázquez, Mariano ^a  

^a INSTITUTO MADRILEÑO DE ESTUDIOS AVANZADOS EN NANOCIENCIA IMDEA NANOCIENCIA   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c Biomol Informatics SL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTENNAS; CALCIUM; CELL ADHESION; GLYCOPROTEINS; MOLECULAR DYNAMICS; MORPHOLOGY; NANOMECHANICS;

CALCIUM CONCENTRATION; EXTRACELLULAR REGION; MECHANICAL CHARACTERIZATIONS; MECHANICAL INTEGRITY; MECHANICAL RESISTANCE; MECHANICAL RESPONSE; MOLECULAR DYNAMICS SIMULATIONS; SINGLE MOLECULE FORCE SPECTROSCOPY;

MECHANISMS;

CADHERIN; CALCIUM ION;

ARTICLE; CALCIUM BINDING; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; MECHANOTRANSDUCTION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; XENOPUS LAEVIS;

EID: 79953183005     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M110.170399     Document Type: Article

References (93)

1. Hynes, R. O. (1999) Trends Cell Biol. 9, M33-M37
2. Vogel, V., and Sheetz, M. (2006) Nat. Rev. Mol. Cell Biol. 7, 265-275
3. Schwartz, M. A., and DeSimone, D. W. (2008) Curr. Opin. Cell Biol. 20, 551-556
4. Carrión-Vázquez, M., Oberhauser, A. F., Díez, H., Hervás, R., Oroz, J., Fernández, J., and Martínez- Martín, D. (2006) in Advanced Techniques in Biophysics (Arrondo, J. L. R., and Alonso, L., eds) pp. 163-245, Springer-Verlag, Berlin
5. Takeichi, M. (1990) Annu. Rev. Biochem. 59, 237-252
6. Tepass, U., Truong, K., Godt, D., Ikura, M., and Peifer, M. (2000) Nat. Rev. Mol. Cell Biol. 1, 91-100
7. Conacci-Sorrell, M., Zhurinsky, J., and Ben-Ze'ev, A. (2002) J. Clin. Investig. 109, 987-991
8. Yagi, T., and Takeichi, M. (2000) Genes Dev. 14, 1169-1180
9. Pérez-Moreno, M., Jamora, C., and Fuchs, E. (2003) Cell 112, 535-548
10. Yamada, S., Pokutta, S., Drees, F., Weis, W. I., and Nelson, W. J. (2005) Cell 123, 889-901
11. Abe, K., and Takeichi, M. (2008) Proc. Natl. Acad. Sci. U.S.A. 105, 13-19
12. Kim, S. H., Li, Z., and Sacks, D. B. (2000) J. Biol. Chem. 275, 36999-37005
13. Noren, N. K., Niessen, C. M., Gumbiner, B. M., and Burridge, K. (2001) J. Biol. Chem. 276, 33305-33308
14. Kovacs, E. M., Goodwin, M., Ali, R. G., Paterson, A. D., and Yap, A. S. (2002) Curr. Biol. 12, 379-382
15. Braga, V. M. (2002) Curr. Opin. Cell Biol. 14, 546-556
16. Ko, K. S., Arora, P. D., and McCulloch, C. A. (2001) J. Biol. Chem. 276, 35967-35977
17. Chu, Y. S., Thomas, W. A., Eder, O., Pincet, F., Perez, E., Thiery, J. P., and Dufour, S. (2004) J. Cell Biol. 167, 1183-1194
18. Lamprecht, R., and LeDoux, J. (2004) Nat. Rev. Neurosci. 5, 45-54
19. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H., and Schwartz, M. A. (2005) Nature 437, 426-431
20. Müller, U. (2008) Curr. Opin. Cell Biol. 20, 557-566
21. Ganz, A., Lambert, M., Saez, A., Silberzan, P., Buguin, A., Mège, R. M., and Ladoux, B. (2006) Biol. Cell 98, 721-730
22. Brieher, W. M., Yap, A. S., and Gumbiner, B. M. (1996) J. Cell Biol. 135, 487-496
23. Boggon, T. J., Murray, J., Chappuis-Flament, S., Wong, E., Gumbiner, B. M., and Shapiro, L. (2002) Science 296, 1308-1313
24. He, W., Cowin, P., and Stokes, D. L. (2003) Science 302, 109-113
25. Hewat, E. A., Durmort, C., Jacquamet, L., Concord, E., and Gulino-Debrac, D. (2007) J. Mol. Biol. 365, 744-751
26. Zhang, Y., Sivasankar, S., Nelson, W. J., and Chu, S. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 109-114
27. Troyanovsky, R. B., Klingelhöfer, J., and Troyanovsky, S. (1999) J. Cell Sci. 112, 4379-4387
28. Chappuis-Flament, S., Wong, E., Hicks, L. D., Kay, C. M., and Gumbiner, B. M. (2001) J. Cell Biol. 154, 231-243
29. Baumgartner, W., Hinterdorfer, P., Ness, W., Raab, A., Vestweber, D., Schindler, H., and Drenckhahn, D. (2000) Proc. Natl. Acad. Sci. U.S.A. 97, 4005-4010
30. Baumgartner, W., Golenhofen, N., Grundhöfer, N., Wiegand, J., and Drenckhahn, D. (2003) J. Neurosci. 23, 11008-11014
31. Zhu, B., Chappuis-Flament, S., Wong, E., Jensen, I. E., Gumbiner, B. M., and Leckband, D. (2003) Biophys. J. 84, 4033-4042
32. Sivasankar, S., Zhang, Y., Nelson, W. J., and Chu, S. (2009) Structure 17, 1075-1081
33. Harrison, O. J., Bahna, F., Katsamba, P. S., Jin, X., Brasch, J., Vendome, J., Ahlsen, G., Carroll, K. J., Price, S. R., Honig, B., and Shapiro, L. (2010) Nat. Struct. Mol. Biol. 17, 348-357
34. Ciatto, C., Bahna, F., Zampieri, N., VanSteenhouse, H. C., Katsamba, P. S., Ahlsen, G., Harrison, O. J., Brasch, J., Jin, X., Posy, S., Vendome, J., Ranscht, B., Jessell, T. M., Honig, B., and Shapiro, L. (2010) Nat. Struct. Mol. Biol. 17, 339-347
35. Sotomayor, M., Weihofen, W. A., Gaudet, R., and Corey, D. P. (2010) Neuron 66, 85-100
36. Elledge, H. M., Kazmierczak, P., Clark, P., Joseph, J. S., Kolatkar, A., Kuhn, P., and Müller, U. (2010) Proc. Natl. Acad. Sci. U.S.A. 107, 10708-10712
37. Giannone, G., Mège, R. M., and Thoumine, O. (2009) Trends Cell Biol. 19, 475-486
38. Ladoux, B., Anon, E., Lambert, M., Rabodzey, A., Hersen, P., Buguin, A., Silberzan, P., and Mège, R. M. (2010) Biophys. J. 98, 534-542
39. Wiest, M. C., Eagleman, D. M., King, R. D., and Montague, P. R. (2000) J. Neurophysiol. 83, 1329-1337
40. Pokutta, S., Herrenknecht, K., Kemler, R., and Engel, J. (1994) Eur. J. Biochem. 223, 1019-1026
41. Alattia, J. R., Ames, J. B., Porumb, T., Tong, K. I., Heng, Y. M., Ottensmeyer, P., Kay, C. M., and Ikura, M. (1997) FEBS Lett. 417, 405-408
42. Koch, A. W., Pokutta, S., Lustig, A., and Engel, J. (1997) Biochemistry 36, 7697-7705
43. Pertz, O., Bozic, D., Koch, A. W., Fauser, C., Brancaccio, A., and Engel, J. (1999) EMBO J. 18, 1738-1747
44. Häussinger, D., Ahrens, T., Sass, H. J., Pertz, O., Engel, J., and Grzesiek, S. (2002) J. Mol. Biol. 324, 823-839
45. Choi, Y. S., Sehgal, R., McCrea, P., and Gumbiner, B. M. (1990) J. Cell Biol. 110, 1575-1582
46. Ginsberg, D., DeSimone, D., and Geiger, B. (1991) Development 111, 315-325
47. Sotomayor, M., and Schulten, K. (2008) Biophys. J. 94, 4621-4633
48. Tai, C. Y., Kim, S. A., and Schuman, E. M. (2008) Curr. Opin. Cell Biol. 20, 567-575
49. Rader, C., and Sonderegger, P. (1999) in Ig Superfamily Molecules in the Nervous System (Sonderegger, P., ed) pp. 1-22, Harwood Academic Publishers, Amsterdam
50. Harpaz, Y., and Chothia, C. (1994) J. Mol. Biol. 238, 528-539
51. Shapiro, L., Kwong, P. D., Fannon, A. M., Colman, D. R., and Hendrickson, W. A. (1995) Proc. Natl. Acad. Sci. U.S.A. 92, 6793-6797
52. Li, H., Oberhauser, A. F., Redick, S. D., Carrión-Vázquez, M., Erickson, H. P., and Fernández, J. M. (2001) Proc. Natl. Acad. Sci. U.S.A. 98, 10682-10686
53. Steward, A., Toca-Herrera, J. L., and Clarke, J. (2002) Protein Sci. 11, 2179-2183
54. Miroux, B., and Walker, J. E. (1996) J. Mol. Biol. 260, 289-298
55. Sambrook, J., and Russell, D. (1989) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
56. Bers, D. M., Patton, C. W., and Nuccitelli, R. (1994) Methods Cell Biol. 40, 3-29
57. Valbuena, A., Oroz, J., Hervás, R., Vera, A. M., Rodríguez, D., Menéndez, M., Sulkowska, J. I., Cieplak, M., and Carrión-Vázquez, M. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 13791-13796
58. Florin, E. L., Rief, M., Lehmann, H., Ludwig, M., Dornmair, C., Moy, V. T., and Gaub, H. E. (1995) Biosens. Bioelectron. 10, 895-901
59. Bustamante, C., Marko, J. F., Siggia, E. D., and Smith, S. (1994) Science 265, 1599-1600
60. Marko, J. F., and Siggia, E. D. (1995) Macromolecules 28, 8759-8770
61. Case, D. A., Pearlman, D. A., Caldwell, J. W., Cheatham, T. E., III, Wang, J., Ross, W. S., Simmerling, C. L., Darden, T. A., Merz, K. M., Stanton, R. V., Cheng, A. L., Vincent, J. J., Crowley, M., Tsui, V., Gohlke, H., Radmer, R. J., Duan, Y., Pitera, J., Massova, I., Seibel, G. L., Singh, U. C., Weiner, P. K., and Kollman, P. A. (2002) AMBER7, University of California, San Francisco
62. Bradbrook, G. M., Gleichmann, T., Harrop, S. J., Habash, J., Raftery, J., Kalb (Gilboa), A. J., Yariv, J., Hillier, I. H., and Helliwell, J. R. (1998) J. Chem. Soc. Faraday Trans. 94, 1603-1611
63. Tsui, V., and Case, D. A. (2000) Biopolymers 56, 275-291
64. Weiser, J., Shenkin, P. S., and Still, W. C. (1999) J. Comput. Chem. 20, 217-230
65. Humphrey, W., Dalke, A., and Schulten, K. (1996) J. Mol. Graph. 14, 33-38, 27-28
66. Ainavarapu, S. R., Brujic, J., Huang, H. H., Wiita, A. P., Lu, H., Li, L., Walther, K. A., Carrión-Vázquez, M., Li, H., and Fernández, J. M. (2007) Biophys. J. 92, 225-233
67. Prasad, A., and Pedigo, S. (2005) Biochemistry 44, 13692-13701
68. Prasad, A., Zhao, H., Rutherford, J. M., Housley, N., Nichols, C., and Pedigo, S. (2006) Proteins 62, 111-121
69. Ainavarapu, S. R., Li, L., Badilla, C. L., and Fernández, J. M. (2005) Biophys. J. 89, 3337-3344
70. Cao, Y., Yoo, T., and Li, H. (2008) Proc. Natl. Acad. Sci. U.S.A. 105, 11152-11157
71. Junker, J. P., Ziegler, F., and Rief, M. (2009) Science 323, 633-637
72. Arias-Moreno, X., Cuesta-Lopez, S., Millet, O., Sancho, J., and Velázquez-Campoy, A. (2010) Proteins 78, 950-961
73. Ozawa, M., Engel, J., and Kemler, R. (1990) Cell 63, 1033-1038
74. Bayas, M. V., Schulten, K., and Leckband, D. (2004) Mech. Chem. Biosyst. 1, 101-111
75. Cailliez, F., and Lavery, R. (2006) Biophys. J. 91, 3964-3971
76. Lu, H., and Schulten, K. (1999) Proteins 35, 453-463
77. Sotomayor, M., Corey, D. P., and Schulten, K. (2005) Structure 13, 669-682
78. Lee, E. H., Hsin, J., Sotomayor, M., Comellas, G., and Schulten, K. (2009) Structure 17, 1295-1306
79. Salt, A. N., Inamura, N., Thalmann, R., and Vora, A. (1989) Am. J. Otolaryngol. 10, 371-375
80. Brown, E. M., Vassilev, P. M., and Hebert, S. C. (1995) Cell 83, 679-682
81. Maurer, P., and Hohenester, E. (1997) Matrix Biol. 15, 569-581
82. Breitwieser, G. E. (2008) Int. J. Biochem. Cell Biol. 40, 1467-1480
83. Rusakov, D. A., Kullmann, D. M., and Stewart, M. G. (1999) Trends Neurosci. 22, 382-388
84. Brusés, J. L. (2006) Mol. Neurobiol. 33, 237-252
85. Oberhauser, A. F., Marszalek, P. E., Erickson, H. P., and Fernández, J. M. (1998) Nature 393, 181-185
86. Evans, E., and Ritchie, K. (1999) Biophys. J. 76, 2439-2447
87. Panorchan, P., Thompson, M. S., Davis, K. J., Tseng, Y., Konstantopoulos, K., and Wirtz, D. (2006) J. Cell Sci. 119, 66-74
88. Bajpai, S., Feng, Y., Krishnamurthy, R., Longmore, G. D., and Wirtz, D. (2009) J. Biol. Chem. 284, 18252-18259
89. le Duc, Q., Shi, Q., Blonk, I., Sonnenberg, A., Wang, N., Leckband, D., and de Rooij, J. (2010) J. Cell Biol. 189, 1107-1115
90. del Río, A., Pérez-Jiménez, R., Liu, R., Roca-Cusachs, P., Fernández, J. M., and Sheetz, M. P. (2009) Science 323, 638-641
91. Kazmierczak, P., Sakaguchi, H., Tokita, J., Wilson-Kubalek, E. M., Milligan, R. A., Müller, U., and Kachar, B. (2007) Nature 449, 87-91
92. Schwander, M., Xiong, W., Tokita, J., Lelli, A., Elledge, H. M., Kazmierczak, P., Sczaniecka, A., Kolatkar, A., Wiltshire, T., Kuhn, P., Holt, J. R., Kachar, B., Tarantino, L., and Müller, U. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 5252-5257
93. Shin, J. B., and Gillespie, P. G. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 4959-4960