T-cadherin structures reveal a novel adhesive binding mechanism

Nature Structural and Molecular Biology

Volumn 17, Issue 3, 2010, Pages 339-347

  Ciatto, Carlo ^a   Bahna, Fabiana ^a   Zampieri, Niccolò ^a   Vansteenhouse, Harper C ^b   Katsamba, Phini S ^a   Ahlsen, Goran ^a   Harrison, Oliver J ^a   Brasch, Julia ^a   Jin, Xiangshu ^a   Posy, Shoshana ^a   Vendome, Jeremie ^a   Ranscht, Barbara ^b   Jessell, Thomas M ^a   Honig, Barry ^a   Shapiro, Lawrence ^a,c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b BURNHAM INSTITUTE   (United States)

^c New York Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; DIMER; T CADHERIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BINDING SITE; CALCIUM BINDING; CHICKEN; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; EMBRYONIC STEM CELL; MOUSE; MUTATION; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; XENOPUS LAEVIS;

ANIMALS; CADHERINS; CALCIUM; CELLS, CULTURED; CHICKENS; CRYSTALLOGRAPHY, X-RAY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; NEURONS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY;

VERTEBRATA;

EID: 77949261544     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1781     Document Type: Article

References (57)

1. Gumbiner, B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634 (2005).
2. Takeichi, M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627 (1995).
3. Takeichi, M. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8, 11-20 (2007).
4. Nollet, F., Kools, P. & van Roy, F. Phylogenetic analysis of the cadherin superfamily allows identifcation of six major subfamilies besides several solitary members. J. Mol. Biol. 299, 551-572 (2000).
5. Posy, S., Shapiro, L. & Honig, B. Sequence and structural determinants of strand swapping in cadherin domains: do all cadherins bind through the same adhesive interface? J. Mol. Biol. 378, 954-968 (2008).
6. Bekirov, I.H., Needleman, L.A., Zhang, W. & Benson, D.L. Identifcation and localization of multiple classic cadherins in developing rat limbic system. Neuroscience 115, 213-227 (2002).
7. Nishimura, E.K., Yoshida, H., Kunisada, T. & Nishikawa, S.I. Regulation of E-and P-cadherin expression correlated with melanocyte migration and diversifcation. Dev. Biol. 215, 155-166 (1999).
8. Price, S.R., De Marco Garcia, N.V., Ranscht, B. & Jessell, T.M. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109, 205-216 (2002).
9. Wu, Q. & Maniatis, T. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790 (1999).
10. Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595 (1999).
11. Siemens, J. et al. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428, 950-955 (2004).
12. Patel, S.D., Chen, C.P., Bahna, F., Honig, B. & Shapiro, L. Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13, 690-698 (2003).
13. Boggon, T.J. et al. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296, 1308-1313 (2002).
14. Nagar, B., Overduin, M., Ikura, M. & Rini, J.M. Structural basis of calcium-induced E-cadherin rigidifcation and dimerization. Nature 380, 360-364 (1996).
15. Pokutta, S., Herrenknecht, K., Kemler, R. & Engel, J. Conformational changes of the recombinant extracellular domain of E-cadherin upon calcium binding. Eur. J. Biochem. 223, 1019-1026 (1994).
16. Goodwin, M. & Yap, A.S. Classical cadherin adhesion molecules: coordinating cell adhesion, signaling and the cytoskeleton. J. Mol. Histol. 35, 839-844 (2004).
17. Drees, F., Pokutta, S., Yamada, S., Nelson, W.J. & Weis, W.I. α-catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin-flament assembly. Cell 123, 903-915 (2005).
18. Haussinger, D. et al. Proteolytic E-cadherin activation followed by solution NMR and X-ray crystallography. EMBO J. 23, 1699-1708 (2004).
19. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18, 1738-1747 (1999).
20. Shapiro, L. et al. Structural basis of cell-cell adhesion by cadherins. Nature 374, 327-337 (1995).
21. Tamura, K., Shan, W.S., Hendrickson, W.A., Colman, D.R. & Shapiro, L. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20, 1153-1163 (1998).
22. Patel, S.D. et al. Type II cadherin ectodomain structures: implications for classical cadherin specifcity. Cell 124, 1255-1268 (2006).
23. Chen, C.P., Posy, S., Ben-Shaul, A., Shapiro, L. & Honig, B.H. Specifcity of cell-cell adhesion by classical cadherins: critical role for low-affnity dimerization through β-strand swapping. Proc. Natl. Acad. Sci. USA 102, 8531-8536 (2005).
24. Ranscht, B. & Dours-Zimmermann, M.T. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region. Neuron 7, 391-402 (1991).
25. Vestal, D.J. & Ranscht, B. Glycosyl phosphatidylinositol-anchored T-cadherin mediates calcium-dependent, homophilic cell adhesion. J. Cell Biol. 119, 451-461 (1992).
26. Miskevich, F., Zhu, Y., Ranscht, B. & Sanes, J.R. Expression of multiple cadherins and catenins in the chick optic tectum. Mol. Cell. Neurosci. 12, 240-255 (1998).
27. Doyle, D.D. et al. T-cadherin is a major glycophosphoinositol-anchored protein associated with noncaveolar detergent-insoluble domains of the cardiac sarcolemma. J. Biol. Chem. 273, 6937-6943 (1998).
28. Koller, E. & Ranscht, B. Differential targeting of T-and N-cadherin in polarized epithelial cells. J. Biol. Chem. 271, 30061-30067 (1996).
29. Sacristan, M.P., Vestal, D.J., Dours-Zimmermann, M.T. & Ranscht, B. T-cadherin 2: molecular characterization, function in cell adhesion, and coexpression with T-cadherin and N-cadherin. J. Neurosci. Res. 34, 664-680 (1993).
30. Dames, S.A. et al. Insights into the low adhesive capacity of human T-cadherin from the NMR structure of its N-terminal extracellular domain. J. Biol. Chem. 283, 23485-23495 (2008).
31. Fredette, B.J. & Ranscht, B. T-cadherin expression delineates specifc regions of the developing motor axon-hindlimb projection pathway. J. Neurosci. 14, 7331-7346 (1994).
32. Fredette, B.J., Miller, J. & Ranscht, B. Inhibition of motor axon growth by T-cadherin substrata. Development 122, 3163-3171 (1996).
33. Ivanov, D. et al. Expression of cell adhesion molecule T-cadherin in the human vasculature. Histochem. Cell Biol. 115, 231-242 (2001).
34. Hebbard, L.W. et al. T-cadherin supports angiogenesis and adiponectin association with the vasculature in a mouse mammary tumor model. Cancer Res. 68, 1407-1416 (2008).
35. Hug, C. et al. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl. Acad. Sci. USA 101, 10308-10313 (2004).
36. Harrison, O. et al. Two-step adhesive binding by classical cadherins. Nat. Struct. Mol. Biol. advance online publication, doi:10:1038/nsmb.1784 (28 February 2010).
37. Harrison, O.J., Corps, E.M. & Kilshaw, P.J. Cadherin adhesion depends on a salt bridge at the N-terminus. J. Cell Sci. 118, 4123-4130 (2005).
38. Haussinger, D. et al. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation and mapping of contact regions. J. Mol. Biol. 324, 823-839 (2002).
39. Chappuis-Flament, S., Wong, E., Hicks, L.D., Kay, C.M. & Gumbiner, B.M. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 154, 231-243 (2001).
40. Koch, A.W., Pokutta, S., Lustig, A. & Engel, J. Calcium binding and homoassociation of E-cadherin domains. Biochemistry 36, 7697-7705 (1997).
41. Bai, S., Datta, J., Jacob, S.T. & Ghoshal, K. Treatment of PC12 cells with nerve growth factor induces proteasomal degradation of T-cadherin that requires tyrosine phosphorylation of its cadherin domain. J. Biol. Chem. 282, 27171-27180 (2007).
42. Bai, S., Ghoshal, K. & Jacob, S.T. Identifcation of T-cadherin as a novel target of DNA methyltransferase 3B and its role in the suppression of nerve growth factor-mediated neurite outgrowth in PC12 cells. J. Biol. Chem. 281, 13604-13611 (2006).
43. Wichterle, H., Lieberam, I., Porter, J.A. & Jessell, T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 110, 385-397 (2002).
44. Parisini, E., Higgins, J.M., Liu, J.H., Brenner, M.B. & Wang, J.H. The crystal structure of human E-cadherin domains 1 and 2, and comparison with other cadherins in the context of adhesion mechanism. J. Mol. Biol. 373, 401-411 (2007).
45. Alattia, J.R. et al. Lateral self-assembly of E-cadherin directed by cooperative calcium binding. FEBS Lett. 417, 405-408 (1997).
46. Katsamba, P. et al. Linking molecular affnity and cellular specifcity in cadherin-mediated adhesion. Proc. Natl. Acad. Sci. USA 106, 11594-11599 (2009).
47. Otwinowski, Z. & Minor, W. Processing of X-ray data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
48. Leslie, A.G.W. Recent changes to the MOSFLM package for processing flm and image plate data. Joint CCP4 and ESF-EACBM Newsletters on Protein Crystallography 26 (1992).
49. Collaborative Computation Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
50. Terwilliger, T.C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861 (1999).
51. Bricogne, G., Vonrhein, C., Flensburg, C., Schiltz, M. & Paciorek, W. Generation, representation and fow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr. 59, 2023-2030 (2003).
52. Terwilliger, T. SOLVE and RESOLVE: automated structure solution, density modifcation and model building. J. Synchrotron Radiat. 11, 49-52 (2004).
53. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
54. Brunger, A.T. et al. Crystallography and NMR system (CNS): A new software system for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
55. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refnement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
56. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
57. Domeniconi, M. et al. MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849-855 (2005).