Sequence and Structural Determinants of Strand Swapping in Cadherin Domains: Do All Cadherins Bind Through the Same Adhesive Interface?

Journal of Molecular Biology

Volumn 378, Issue 4, 2008, Pages 954-968

  Posy, Shoshana ^a   Shapiro, Lawrence ^a,b   Honig, Barry ^a  

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

^b New York Presbyterian Hospital   (United States)

Author keywords

adhesion; cadherins; cell surface receptors; domain swapping; strand swapping

Indexed keywords

CADHERIN; CELL SURFACE RECEPTOR; DESMOCOLLIN; DESMOGLEIN; DESMOSOMAL CADHERIN; RECOMBINANT GAMMA INTERFERON;

AMINO TERMINAL SEQUENCE; ARTICLE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

VERTEBRATA;

EID: 41949131198     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.02.063     Document Type: Article

References (69)

1. Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7 (1995) 619-627
2. Vleminckx K., and Kemler R. Cadherins and tissue formation: integrating adhesion and signaling. BioEssays 21 (1999) 211-220
3. Pla P., Moore R., Morali O.G., Grille S., Martinozzi S., Delmas V., and Larue L. Cadherins in neural crest cell development and transformation. J. Cell Physiol. 189 (2001) 121-132
4. Gooding J.M., Yap K.L., and Ikura M. The cadherin-catenin complex as a focal point of cell adhesion and signalling: new insights from three-dimensional structures. BioEssays 26 (2004) 497-511
5. Takeichi M. The cadherin superfamily in neuronal connections and interactions. Nature Rev. Neurosci. 8 (2007) 11-20
6. Oda H., Uemura T., Harada Y., Iwai Y., and Takeichi M. A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165 (1994) 716-726
7. Yonekura S., Ting C., Neves G., Hung K., Hsu S., Chiba A., et al. The variable transmembrane domain of Drosophila N-cadherin regulates adhesive activity. Mol. Cell Biol. 26 (2006) 6598-6608
8. Moeller M.J., Soofi A., Braun G.S., Li X., Watzl C., Kriz W., and Holzman L.B. Protocadherin FAT1 binds Ena/VASP proteins and is necessary for actin dynamics and cell polarization. EMBO J. 23 (2004) 3769-3779
9. Matakatsu H., and Blair S.S. Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 131 (2004) 3785-3794
10. Rock R., Schrauth S., and Gessler M. Expression of mouse dchs1, fjx1, and fat-j suggests conservation of the planar cell polarity pathway identified in Drosophila. Dev. Dyn. 234 (2005) 747-755
11. Matakatsu H., and Blair S. Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins. Development 133 (2006) 2315-2324
12. Casal J., Lawrence P., and Struhl G. Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity. Development 133 (2006) 4561-4572
13. Overduin M., Harvey T., Bagby S., Tong K., Yau P., Takeichi M., and Ikura M. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science 267 (1995) 386-389
14. Shapiro L., Fannon A., Kwong P., Thompson A., Lehmann M., Grubel G., et al. Structural basis of cell-cell adhesion by cadherins. Nature 374 (1995) 327-337
15. Nagar B., Overduin M., Ikura M., and Rini J.M. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380 (1996) 360-364
16. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 18 (1999) 1738-1747
17. Boggon T., Murray J., Chappuis-Flament S., Wong E., Gumbiner B., and Shapiro L. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296 (2002) 1308-1313
18. Haussinger D., Ahrens T., Sass H., Pertz O., Engel J., and Grzesiek S. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation and mapping of contact regions. J. Mol. Biol. 324 (2002) 823-839
19. Schubert W., Urbanke C., Ziehm T., Beier V., Machner M., Domann E., et al. Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111 (2002) 825-836
20. Koch A.W., Farooq A., Shan W., Zeng L., Colman D.R., and Zhou M.M. Structure of the neural (N-) cadherin prodomain reveals a cadherin extracellular domain-like fold without adhesive characteristics. Structure 12 (2004) 793-805
21. Haussinger D., Ahrens T., Aberle T., Engel J., Stetefeld J., and Grzesiek S. Proteolytic E-cadherin activation followed by solution NMR and X-ray crystallography. EMBO J. 23 (2004) 1699-1708
22. Patel S., Ciatto C., Chen C., Bahna F., Rajebhosale M., Arkus N., et al. Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124 (2006) 1255-1268
23. Parisini E., Higgins J.M., Liu J.H., Brenner M.B., and 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 (2007) 401-411
24. Umitsu M., Morishita H., Murata Y., Udaka K., Akutsu H., Yagi T., and Ikegami T. 1H, 13C and 15N resonance assignments of the first cadherin domain of Cadherin-related neuronal receptor (CNR)/protocadherin alpha. J. Biomol. NMR 31 (2005) 365-366
25. Morishita H., Umitsu M., Murata Y., Shibata N., Udaka K., Higuchi Y., et al. Structure of the cadherin-related neuronal receptor/protocadherin-alpha first extracellular cadherin domain reveals diversity across cadherin families. J. Biol. Chem. 281 (2006) 33650-33663
26. Harrison O.J., Corps E.M., and Kilshaw P.J. Cadherin adhesion depends on a salt bridge at the N-terminus. J. Cell Sci. 118 (2005) 4123-4130
27. Tamura K., Shan W., Hendrickson W., Colman D., and Shapiro L. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20 (1998) 1153-1163
28. Troyanovsky R., Sokolov E., and Troyanovsky S. Adhesive and lateral E-cadherin dimers are mediated by the same interface. Mol. Cell Biol. 23 (2003) 7965-7972
29. Harrison O.J., Corps E.M., Berge T., and Kilshaw P.J. The mechanism of cell adhesion by classical cadherins: the role of domain 1. J. Cell Sci. 118 (2005) 711-721
30. He W., Cowin P., and Stokes D. Untangling desmosomal knots with electron tomography. Science 302 (2003) 109-113
31. Tomschy A., Fauser C., Landwehr R., and Engel J. Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N-terminal domains. EMBO J. 15 (1996) 3507-3514
32. Norvell S., and Green K. Contributions of extracellular and intracellular domains of full length and chimeric cadherin molecules to junction assembly in epithelial cells. J. Cell Sci. 111 (1998) 1305-1318
33. Takeda H., Shimoyama Y., Nagafuchi A., and Hirohashi S. E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nature Struct. Biol. 6 (1999) 310-312
34. Letunic I., Copley R., Pils B., Pinkert S., Schultz J., and Bork P. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res. 34 (2006) D257-D260
35. Finn R., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., et al. Pfam: clans, web tools and services. Nucleic Acids Res. 34 (2006) D247-D251
36. Wu C.H., Apweiler R., Bairoch A., Natale D.A., Barker W.C., and Boeckmann B. The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res. 34 (2006) D187-D191
37. Hatta K., Nose A., Nagafuchi A., and Takeichi M. Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J. Cell Biol. 106 (1988) 873-881
38. Shimoyama Y., Tsujimoto G., Kitajima M., and Natori M. Identification of three human type-II classic cadherins and frequent heterophilic interactions between different subclasses of type-II classic cadherins. Biochem. J. 349 (2000) 159-167
39. Noonan J., Grimwood J., Schmutz J., Dickson M., and Myers R. Gene conversion and the evolution of protocadherin gene cluster diversity. Genome Res. 14 (2004) 354-366
40. Li W., and Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22 (2006) 1658-1659
41. Notredame C., Higgins D., and Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302 (2000) 205-217
42. Eddy S.R. Hidden Markov models. Curr. Opin. Struct. Biol. 6 (1996) 361-365
43. Petrey D., and Honig B. GRASP2: visualization, surface properties, and electrostatics of macromolecular structures and sequences. Methods Enzymol. 374 (2003) 492-509
44. Al-Lazikani B., Sheinerman F., and Honig B. Combining multiple structure and sequence alignments to improve sequence detection and alignment: application to the SH2 domains of Janus kinases. Proc. Natl Acad. Sci. USA 98 (2001) 14796-14801
45. Tang C., Xie L., Koh I., Posy S., Alexov E., and Honig B. On the role of structural information in remote homology detection and sequence alignment: new methods using hybrid sequence profiles. J. Mol. Biol. 334 (2003) 1043-1062
46. Ptitsyn O., and Ting K. Non-functional conserved residues in globins and their possible role as a folding nucleus. J. Mol. Biol. 291 (1999) 671-682
47. Kister A., Roytberg M., Chothia C., Vasiliev J., and Gelfand I. The sequence determinants of cadherin molecules. Protein Sci. 10 (2001) 1801-1810
48. Chothia C., Gelfand I., and Kister A. Structural determinants in the sequences of immunoglobulin variable domain. J. Mol. Biol. 278 (1998) 457-479
49. Prasad A., Housley N., and Pedigo S. Thermodynamic stability of domain 2 of epithelial cadherin. Biochemistry 43 (2004) 8055-8066
50. Green S., Gittis A., Meeker A., and Lattman E. One-step evolution of a dimer from a monomeric protein. Nature Struct. Biol. 2 (1995) 746-751
51. Murray A., Lewis S., Barclay A., and Brady R. One sequence, two folds: a metastable structure of CD2. Proc. Natl Acad. Sci. USA 92 (1995) 7337-7341
52. Kelley B., Chang L., and Bewley C. Engineering an obligate domain-swapped dimer of cyanovirin-N with enhanced anti-HIV activity. J. Am. Chem. Soc. 124 (2002) 3210-3211
53. Gevaert K., Goethals M., Martens L., Van D.J., Staes A., Thomas G., and Vandekerckhove J. Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted N terminal peptides. Nature Biotechnol. 21 (2003) 566-569
54. Hill E., Broadbent I., Chothia C., and Pettitt J. Cadherin superfamily proteins in Caenorhabditis elegans and Drosophila melanogaster. J. Mol. Biol. 305 (2001) 1011-1024
55. Iwai Y., Usui T., Hirano S., Steward R., Takeichi M., and Uemura T. Axon patterning requires DN cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19 (1997) 77-89
56. Kitagawa M., Natori M., Murase S., Hirano S., Taketani S., and Suzuki S. Mutation analysis of cadherin 4 reveals amino acid residues of EC1 important for the structure and function. Biochem. Biophys. Res. Commun. 271 (2000) 358-363
57. Bennett M.J., Schlunegger M.P., and Eisenberg D. 3D domain swapping: a mechanism for oligomer assembly. Protein Sci. 4 (1995) 2455-2468
58. Newlove T., Atkinson K., Van D.L., and Cordes M. A trade between similar but nonequivalent intrasubunit and intersubunit contacts in Cro dimer evolution. Biochemistry 45 (2006) 6379-6391
59. Chen C., Posy S., Ben Shaul A., Shapiro L., and Honig B. Specificity of cell cell adhesion by classical cadherins: Critical role for low affinity dimerization through beta strand swapping. Proc. Natl Acad. Sci. USA 102 (2005) 8531-8536
60. Murray A.J., Head J.G., Barker J.J., and Brady R.L. Engineering an intertwined form of CD2 for stability and assembly. Nature Struct. Biol. 5 (1998) 778-782
61. Simeoni F., Masotti L., and Neyroz P. Structural role of the proline residues of the beta hinge region of p13suc1 as revealed by site directed mutagenesis and fluorescence studies. Biochemistry 40 (2001) 8030-8042
62. Barrientos L.G., Louis J.M., Botos I., Mori T., Han Z., O'Keefe B.R., et al. The domain swapped dimer of cyanovirin N is in a metastable folded state: reconciliation of X ray and NMR structures. Structure 10 (2002) 673-686
63. Harpaz Y., and Chothia C. Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J. Mol. Biol. 238 (1994) 528-539
64. Wiesmann C., Ultsch M., Bass S., and de Vos A.M. Crystal structure of nerve growth factor in complex with the ligand binding domain of the TrkA receptor. Nature 401 (1999) 184-188
65. Ultsch M., Wiesmann C., Simmons L., Henrich J., Yang M., Reilly D., et al. Crystal structures of the neurotrophin binding domain of TrkA, TrkB and TrkC. J. Mol. Biol. 290 (1999) 149-159
66. Wolfenden R., and Radzicka A. How hydrophilic is tryptophan?. Trends Biochem. Sci. 11 (1986) 69-70
67. Ting C., Yonekura S., Chung P., Hsu S., Robertson H., Chiba A., and Lee C. Drosophila N cadherin functions in the first stage of the two stage layer selection process of R7 photoreceptor afferents. Development 132 (2005) 953-963
68. Klingelhofer J., Laur O.Y., Troyanovsky R.B., and Troyanovsky S.M. Dynamic interplay between adhesive and lateral E cadherin dimers. Mol. Cell Biol. 22 (2002) 7449-7458
69. Pokutta S., Herrenknecht K., Kemler R., and Engel J. Conformational changes of the recombinant extracellular domain of E-cadherin upon calcium binding. Eur. J. Biochem. 223 (1994) 1019-1026