Structure of the Tandem Fibronectin Type 3 Domains of Neural Cell Adhesion Molecule

Journal of Molecular Biology

Volumn 377, Issue 2, 2008, Pages 524-534

  Carafoli, Federico ^a   Saffell, Jane L ^a   Hohenester, Erhard ^a  

^a Blackett Laboratory   (United Kingdom)

Author keywords

cell adhesion; crystal packing; domain linker; protein interaction; X ray crystallography

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR; FIBRONECTIN; NERVE CELL ADHESION MOLECULE;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; CONTROLLED STUDY; CRYSTAL STRUCTURE; GEL PERMEATION CHROMATOGRAPHY; MAMMAL CELL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SURFACE PLASMON RESONANCE; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

EID: 40049086554     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.01.030     Document Type: Article

References (52)

1. F.S. Walsh P. Doherty Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance Annu. Rev. Cell Dev. Biol. 13 1997 425 456
2. P.F. Maness M. Schachner Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration Nat. Neurosci. 10 2007 19 26
3. P.S. Walmod K. Kolkova V. Berezin E. Bock Zippers make signals: NCAM-mediated molecular interactions and signal transduction Neurochem. Res. 29 2004 2015 2035
4. K.L. Crossin L.A. Krushel Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily Dev. Dyn. 218 2000 260 279
5. H. Cremer R. Lange A. Christoph M. Plomann G. Vopper J. Roes Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning Nature 367 1994 455 459
6. D. Muller C. Wang G. Skibo N. Toni H. Cremer V. Calaora PSA-NCAM is required for activity-induced synaptic plasticity Neuron 17 1996 413 422
7. M. Schachner Neural recognition molecules and synaptic plasticity Curr. Opin. Cell Biol. 9 1997 627 634
8. G.C. Owens G.M. Edelman B.A. Cunningham Organization of the neural cell adhesion molecule (N-CAM) gene: alternative exon usage as the basis for different membrane-associated domains Proc. Natl Acad. Sci. USA 84 1987 294 298
9. G. Dickson H.J. Gower C.H. Barton H.M. Prentice V.L. Elsom S.E. Moore Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain Cell 50 1987 1119 1130
10. A.A. Reyes S.J. Small R. Akeson At least 27 alternatively spliced forms of the neural cell adhesion molecule mRNA are expressed during rat heart development Mol. Cell. Biol. 11 1991 1654 1661
11. S.J. Small R. Akeson Expression of the unique NCAM VASE exon is independently regulated in distinct tissues during development J. Cell Biol. 111 1990 2089 2096
12. M.J. Santoni D. Barthels G. Vopper A. Boned C. Goridis W. Wille Differential exon usage involving an unusual splicing mechanism generates at least eight types of NCAM cDNA in mouse brain EMBO J. 8 1989 385 392
13. E. Gascon L. Vutskits J.Z. Kiss Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res. Rev. 56 2007 101 118
14. A.R. Atkins W.J. Gallin G.C. Owens G.M. Edelman B.A. Cunningham Neural cell adhesion molecule (N-CAM) homophilic binding mediated by the two N-terminal Ig domains is influenced by intramolecular domain–domain interactions J. Biol. Chem. 279 2004 49633 49643
15. C.P. Johnson I. Fujimoto C. Perrin-Tricaud U. Rutishauser D. Leckband Mechanism of homophilic adhesion by the neural cell adhesion molecule: use of multiple domains and flexibility Proc. Natl Acad. Sci. USA 101 2004 6963 6968
16. V. Soroka K. Kolkova J.S. Kastrup K. Diederichs J. Breed V.V. Kiselyov Structure and interactions of NCAM Ig1–2–3 suggest a novel zipper mechanism for homophilic adhesion Structure 11 2003 1291 1301
17. J.A. Wieland A.A. Gewirth D.E. Leckband Single molecule adhesion measurements reveal two homophilic neural cell adhesion molecule bonds with mechanically distinct properties J. Biol. Chem. 280 2005 41037 41046
18. J.L. Saffell E.J. Williams I.J. Mason F.S. Walsh P. Doherty Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs Neuron 18 1997 231 242
19. E.J. Williams J. Furness F.S. Walsh P. Doherty Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin Neuron 13 1994 583 594
20. E. Sanchez-Heras F.V. Howell G. Williams P. Doherty The fibroblast growth factor receptor acid box is essential for interactions with N-cadherin and all of the major isoforms of neural cell adhesion molecule J. Biol. Chem. 281 2006 35208 35216
21. U. Cavallaro J. Niedermeyer M. Fuxa G. Christofori N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling Nat. Cell Biol. 3 2001 650 657
22. V.V. Kiselyov V. Soroka V. Berezin E. Bock Structural biology of NCAM homophilic binding and activation of FGFR J. Neurochem. 94 2005 1169 1179
23. L. Dailey D. Ambrosetti A. Mansukhani C. Basilico Mechanisms underlying differential responses to FGF signaling Cytokine Growth Factor Rev. 16 2005 233 247
24. V.P. Eswarakumar I. Lax J. Schlessinger Cellular signaling by fibroblast growth factor receptors Cytokine Growth Factor Rev. 16 2005 139 149
25. R. Grose C. Dickson Fibroblast growth factor signaling in tumorigenesis Cytokine Growth Factor Rev. 16 2005 179 186
26. M. Presta P. Dell'Era S. Mitola E. Moroni R. Ronca M. Rusnati Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis Cytokine Growth Factor Rev. 16 2005 159 178
27. P. Doherty F.S. Walsh CAM–FGF receptor interactions: a model for axonal growth Mol. Cell. Neurosci. 8 1996 99 111
28. V.V. Kiselyov G. Skladchikova A.M. Hinsby P.H. Jensen N. Kulahin V. Soroka Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP Structure 11 2003 691 701
29. C. Christensen J.B. Lauridsen V. Berezin E. Bock V.V. Kiselyov The neural cell adhesion molecule binds to fibroblast growth factor receptor 2 FEBS Lett. 580 2006 3386 3390
30. A.A. Anderson C.E. Kendal M. Garcia-Maya A.V. Kenny S.A. Morris-Triggs T. Wu A peptide from the first fibronectin domain of NCAM acts as an inverse agonist and stimulates FGF receptor activation, neurite outgrowth and survival J. Neurochem. 95 2005 570 583
31. S.S. Mendiratta N. Sekulic F.G. Hernandez-Guzman B.E. Close A. Lavie K.J. Colley A novel alpha-helix in the first fibronectin type III repeat of the neural cell adhesion molecule is critical for N-glycan polysialylation J. Biol. Chem. 281 2006 36052 36059
32. R.A. Laskowski M.W. MacArthur D.A. Moss J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1996 283 291
33. D. Chow X. He A.L. Snow S. Rose-John K.C. Garcia Structure of an extracellular gp130 cytokine receptor signaling complex Science 291 2001 2150 2155
34. M. Mrosek D. Labeit S. Witt H. Heerklotz E. von Castelmur S. Labeit O. Mayans Molecular determinants for the recruitment of the ubiquitin-ligase MuRF-1 onto M-line titin FASEB J. 21 2007 1383 1392
35. J.W. Becker H.P. Erickson S. Hoffman B.A. Cunningham G.M. Edelman Topology of cell adhesion molecules Proc. Natl Acad. Sci. USA 86 1989 1088 1092
36. A.K. Hall U. Rutishauser Visualization of neural cell adhesion molecule by electron microscopy J. Cell Biol. 104 1987 1579 1586
37. A.H. Huber Y.M. Wang A.J. Bieber P.J. Bjorkman Crystal structure of tandem type III fibronectin domains from Drosophila neuroglian at 2.0 Å Neuron 12 1994 717 731
38. D.J. Leahy I. Aukhil H.P. Erickson 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region Cell 84 1996 155 164
39. A. Sharma J.A. Askari M.J. Humphries E.Y. Jones D.I. Stuart Crystal structure of a heparin- and integrin-binding segment of human fibronectin EMBO J. 18 1999 1468 1479
40. A. Lundell A.I. Olin M. Morgelin S. al-Karadaghi A. Aspberg D.T. Logan Structural basis for interactions between tenascins and lectican C-type lectin domains: evidence for a cross-linking role for tenascins Structure 12 2004 1495 1506
41. A.H. Merry R.J. Gilbert D.A. Shore L. Royle O. Miroshnychenko M. Vuong O -glycan sialylation and the structure of the stalk-like region of the T cell co-receptor CD8 J. Biol. Chem. 278 2003 27119 27128
42. C. Kasper M. Stahlhut V. Berezin T.E. Maar K. Edvardsen V.V. Kiselyov Functional characterization of NCAM fibronectin type III domains: demonstration of modulatory effects of the proline-rich sequence encoded by alternatively spliced exons a and AAG J. Neurosci. Res. 46 1996 173 186
43. M. Stahlhut V. Berezin E. Bock J.P. Ternaux NCAM-fibronectin-type-III-domain substrata with and without a six-amino-acid-long proline-rich insert increase the dendritic and axonal arborization of spinal motoneurons J. Neurosci. Res. 48 1997 112 121
44. D. Peck F.S. Walsh Differential effects of over-expressed neural cell adhesion molecule isoforms on myoblast fusion J. Cell Biol. 123 1993 1587 1595
45. A. Santuccione V. Sytnyk I. Leshchyns'ka M. Schachner Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth J. Cell Biol. 169 2005 341 354
46. L. Duchesne B. Tissot T.R. Rudd A. Dell D.G. Fernig N-glycosylation of fibroblast growth factor receptor 1 regulates ligand and heparan sulfate co-receptor binding J. Biol. Chem. 281 2006 27178 27189
47. E. Kohfeldt P. Maurer C. Vannahme R. Timpl Properties of the extracellular calcium binding module of the proteoglycan testican FEBS Lett. 414 1997 557 561
48. The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
49. T.A. Jones J.Y. Zou S.W. Cowan M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr., Sect. A: Found. Crystallogr. 47 1991 110 119
50. A.T. Brunger P.D. Adams G.M. Clore W.L. DeLano P. Gros R.W. Grosse-Kunstleve Crystallography & NMR System: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 1998 905 921
51. A.J. McCoy R.W. Grosse-Kunstleve L.C. Storoni R.J. Read Likelihood-enhanced fast translation functions Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 2005 458 464
52. L.C. Storoni A.J. McCoy R.J. Read Likelihood-enhanced fast rotation functions Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 432 438