Structural and energetic determinants of adhesive binding specificity in type i cadherins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 40, 2014, Pages E4175-E4184

  Vendome, Jeremie ^a,b,c   Felsovalyi, Klara ^a,b,c   Song, Hang ^a,b,c   Yang, Zhongyu ^d   Jin, Xiangshu ^a,b,c   Brasch, Julia ^a,b   Harrison, Oliver J ^a,b,c   Ahlsen, Goran ^a,b,c   Bahna, Fabiana ^a,b,c   Kaczynska, Anna ^a,b   Katsamba, Phinikoula S ^a,b,c   Edmond, Darwin ^e   Hubbell, Wayne L ^d,f   Shapiro, Lawrence ^a,b   Honig, Barry ^a,b,c  

^a Department of Biochemistry and Molecular Biophysics ^*  (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c Department of Systems Biology ^*  (United States)

^d JULES STEIN EYE INSTITUTE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cadherin dimerization; Entropy contribution; Protein family design

Indexed keywords

CADHERIN; PROTEIN BINDING; XENOPUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; BINDING COMPETITION; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON SPIN RESONANCE; GENETICS; HEK293 CELL LINE; HUMAN; KINETICS; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; STATIC ELECTRICITY; X RAY CRYSTALLOGRAPHY; XENOPUS;

AMINO ACID SEQUENCE; ANIMALS; BINDING, COMPETITIVE; CADHERINS; CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEK293 CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; XENOPUS; XENOPUS PROTEINS;

EID: 84907834099     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416737111     Document Type: Article

References (45)

1. Takeichi M (1990) Cadherins: A molecular family important in selective cell-cell adhesion. Annu Rev Biochem 59:237-252.
2. Takeichi M (1995) Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 7(5): 619-627.
3. Halbleib JM, Nelson WJ (2006) Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20(23):3199-3214.
4. Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6(8):622-634.
5. Suzuki SC, Takeichi M (2008) Cadherins in neuronal morphogenesis and function. Dev Growth Differ 50(Suppl 1):S119-S130.
6. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109(2): 205-216.
7. Duguay D, Foty RA, Steinberg MS (2003) Cadherin-mediated cell adhesion and tissue segregation: Qualitative and quantitative determinants. Dev Biol 253(2): 309-323.
8. Foty RA, Steinberg MS (2005) The differential adhesion hypothesis: A direct evaluation. Dev Biol 278(1):255-263.
9. Katsamba P, et al. (2009) Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc Natl Acad Sci USA 106(28): 11594-11599.
10. Boggon TJ, et al. (2002) C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296(5571):1308-1313.
11. Patel SD, et al. (2006) Type II cadherin ectodomain structures: Implications for classical cadherin specificity. Cell 124(6):1255-1268.
12. Parisini E, Higgins JM, Liu JH, Brenner MB, Wang JH (2007) 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(2):401-411.
13. Harrison OJ, et al. (2011) The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19(2):244-256.
14. Nagar B, Overduin M, Ikura M, Rini JM (1996) Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380(6572):360-364.
15. Pertz O, et al. (1999) A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J 18(7): 1738-1747.
16. Harrison OJ, et al. (2010) Two-step adhesive binding by classical cadherins. Nat Struct Mol Biol 17(3):348-357.
17. Li Y, et al. (2013) Mechanism of E-cadherin dimerization probed by NMR relaxation dispersion. Proc Nati Acad Sci USA 110(41):16462-16467.
18. Hong S, Troyanovsky RB, Troyanovsky SM (2010) Spontaneous assembly and active disassembly balance adherens junction homeostasis. Proc Natl Acad Sci USA 107(8): 3528-3533.
19. Harrison OJ, Corps EM, Kilshaw PJ (2005) Cadherin adhesion depends on a salt bridge at the N-terminus. J Cell Si 118(Pt 18):4123-4130.
20. Tamura K, Shan WS, Hendrickson WA, Colman DR, Shapiro L (1998) Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 20(6): 1153-1163.
21. Troyanovsky RB, Sokolov E, Troyanovsky SM (2003) Adhesive and lateral E-cadherin dimers are mediated by the same interface. Mol Cell Biol 23(22):7965-7972.
22. Shan WS, Koch A, Murray J, Colman DR, Shapiro L (1999) The adhesive binding site of cadherins revisited. Biophys Chem 82(2-3):157-163.
23. Niessen CM, Gumbiner BM (2002) Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J Cell Biol 156(2):389-399.
24. Shan WS, et al. (2000) Functional cis-heterodimers of N- and R-cadherins. J Cell Biol 148(3):579-590.
25. Chen CP, Posy S, Ben-Shaul A, Shapiro L, Honig BH (2005) Specificity of cell-cell adhesion by classical cadherins: Critical role for low-affinity dimerization through beta-strand swapping. Proc Nati Acad Sci USA 102(24):8531-8536.
26. Vendome J, et al. (2011) Molecular design principles underlying β-strand swapping in the adhesive dimerization of cadherins. Nat Struct Mol Biol 18(6):693-700.
27. Vunnam N, Pedigo S (2011) Calcium-induced strain in the monomer promotes dimerization in neural cadherin. Biochemistry 50(39):8437-8444.
28. Hulpiau P, van Roy F (2009) Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 41 (2):349-369.
29. Ciatto C, et al. (2010) T-cadherin structures reveal a novel adhesive binding mechanism. Nat Struct Mol Biol 17(3):339-347.
30. Jeschke G (2012) DEER distance measurements on proteins. Annu Rev Phys Chem 63: 419-446.
31. Fleissner MR, et al. (2011) Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy. Proc Natl Acad Sci USA 108(39):16241-16246.
32. Fleissner MR, Cascio D, Hubbell WL (2009) Structural origin of weakly ordered nitroxide motion in spin-labeled proteins. Protein Sci 18(5):893-908.
33. Wright PE, Dyson HJ (2009) Linking folding and binding. Curr Opin Struct Biol 19(1) :31-38.
34. Wu Y, Vendome J, Shapiro L, Ben-Shaul A, Honig B (2011) Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 475(7357):510-513.
35. Harrison OJ, et al. (2012) Nectin ectodomain structures reveal a canonical adhesive interface. Nat Struct Mol Biol 19(9):906-915.
36. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
37. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online-A web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33(Web Server issue):W557-559.
38. Sridharan S, Nicholls A, Honig B (1992) A new vertex algorithm to calculate solvent accessible surface-areas. FASEB J 6(1):A174-A174.
39. Foote J, Raman A (2000) A relation between the principal axes of inertia and ligand binding. Proc Nati Acad Sci USA 97(3):978-983.
40. Brooks BR, et al. (2009) CHARMM: The biomolecular simulation program. J Comput Chem 30(10):1545-1614.
41. Petrey D, et al. (2003) Using multiple structure alignments, fast model building, and energetic analysis in fold recognition and homology modeling. Proteins 53(Suppl 6): 430-435.
42. Grassetti DR, Murray JF, Jr (1967) Determination of sulfhydryl groups with 2,2 - or 4,4'-dithiodipyridine. Arch Biochem Biophys 119(1):41-49.
43. Hatmal MM, et al. (2012) Computer modeling of nitroxide spin labels on proteins. Biopolymers 97(1):35-44.
44. Altenbach C, Kusnetzow AK, Ernst OP, Hofmann KP, Hubbell WL (2008) High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation. Proc Nati Acad Sci USA 105(21):7439-7444.
45. López CJ, Yang Z, Altenbach C, Hubbell WL (2013) Conformational selection and adaptation to ligand binding in T4 lysozyme cavity mutants. Proc Natl Acad Sci USA 110(46):E4306-E4315.