Elasticity and rupture of a multi-domain neural cell adhesion molecule complex

Biophysical Journal

Volumn 96, Issue 8, 2009, Pages 3005-3014

  Maruthamuthu, Venkat ^a   Schulten, Klaus ^a,b   Leckband, Deborah ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b United States of America   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN FRAGMENT; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; NERVE CELL ADHESION MOLECULE; SOLVENT; MULTIPROTEIN COMPLEX;

ARTICLE; CELL MOTILITY; CRYSTAL STRUCTURE; ELASTICITY; FORCE; HUMAN; MOLECULAR DYNAMICS; MOLECULAR MODEL; NERVE CELL; NERVE CELL MEMBRANE; NERVOUS SYSTEM DEVELOPMENT; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TENSION; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; HYDROGEN BOND; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

COMPUTER SIMULATION; ELASTICITY; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MULTIPROTEIN COMPLEXES; NEURAL CELL ADHESION MOLECULES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 67649394763     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.12.3936     Document Type: Article

References (60)

1. Leckband, D. 2004. Nanomechanics of adhesion proteins. Curr. Opin. Struct. Biol. 14:524-530.
2. Bustamante, C., Y. R. Chemla, N. R. Forde, and D. Izhaky. 2004. Mechanical processes in biochemistry. Annu. Rev. Biochem. 73:705-748.
3. Johnson, C. P., H. Y. Tang, C. Carag, D. W. Speicher, and D. E. Discher. 2007. Forced unfolding of proteins within cells. Science. 317:663-666.
4. Vogel, V. 2006. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35:459-488.
5. Rief, M., M. Gautel, F. Oesterhelt, J. M. Fernandez, and H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112.
6. Erickson, H. P. 1994. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl. Acad. Sci. USA. 91:10114-10118.
7. Sotomayor, M., and K. Schulten. 2007. Single-molecule experiments in vitro and in silico. Science. 316:1144-1148.
8. Sotomayor, M., D. P. Corey, and K. Schulten. 2005. In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure. 13:669-682.
9. Lee, G., K. Abdi, Y. Jiang, P. Michaely, V. Bennett, et al. 2006. Nanospring behaviour of ankyrin repeats. Nature. 440:246-249.
10. Lee, E. H., J. Hsin, O. Mayans, and K. Schulten. 2007. Secondary and tertiary structure elasticity of titin Z1Z2 and a titin chain model. Biophys. J. 93:1719-1735.
11. Sotomayor, M., and K. Schulten. 2008. The allosteric role of the Ca++ switch in adhesion and elasticity of C cadherin. Biophys. J. 94:4621-4633.
12. Choudhuri, K., D. Wiseman, M. H. Brown, K. Gould, and P. A. van der Merwe. 2005. T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature. 436:578-582.
13. Aricescu, A. R., C. Siebold, K. Choudhuri, V. T. Chang, W. Lu, et al. 2007. Structure of a tyrosine phosphatase adhesive interaction reveals a spacer-clamp mechanism. Science. 317:1217-1220.
14. Aricescu, A. R., and E. Y. Jones. 2007. Immunoglobulin superfamily cell adhesion molecules: zippers and signals. Curr. Opin. Cell Biol. 19:543-550.
15. Evans, E. A., and D. A. Calderwood. 2007. Forces and bond dynamics in cell adhesion. Science. 316:1148-1153.
16. Alon, R., D. A. Hammer, and T. A. Springer. 1995. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature. 374:539-542.
17. Benoit, M., D. Gabriel, G. Gerisch, and H. E. Gaub. 2000. Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat. Cell Biol. 2:313-317.
18. Balaban, N. Q., U. S. Schwarz, D. Riveline, P. Goichberg, G. Tzur, et al. 2001. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3:466-472.
19. Cunningham, B. A., J. J. Hemperly, B. A. Murray, E. A. Prediger, R. Brackenbury, et al. 1987. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 236:799-806.
20. Ditlevsen, D. K., G. K. Povlsen, V. Berezin, and E. Bock. 2007. NCAM-induced intracellular signaling revisited. J. Neurosci. Res. 86:727-743.
21. Rutishauser, U., A. Acheson, A. K. Hall, D. M. Mann, and J. Sunshine. 1988. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science. 240:53-57.
22. Walsh, F. S., and P. Doherty. 1997. Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. Annu. Rev. Cell Dev. Biol. 13:425-456.
23. Maness, P. F., and M. Schachner. 2007. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10:19-26.
24. El Maarouf, A., and U. Rutishauser. 2008. Use of PSA-NCAM in repair of the central nervous system. Neurochem. Res. doi:10.1007/s11064-008-9635- 7.
25. Ranheim, T. S., G. M. Edelman, and B. A. Cunningham. 1996. Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. Proc. Natl. Acad. Sci. USA. 93:4071-4075.
26. Atkins, A. R., M. J. Osborne, H. A. Lashuel, G. M. Edelman, P. E. Wright, et al. 1999. Association between the first two immunoglobulin-like domains of the neural cell adhesion molecule N-CAM. FEBS Lett. 451:162-168.
27. Atkins, A. R., J. Chung, S. Deechongkit, E. B. Little, G. M. Edelman, et al. 2001. Solution structure of the third immunoglobulin domain of the neural cell adhesion molecule N-CAM: can solution studies define the mechanism of homophilic binding? J. Mol. Biol. 311:161-172.
28. Kiselyov, V. V., V. Berezin, T. E. Maar, V. Soroka, K. Edvardsen, et al. 1997. The first immunoglobulin-like neural cell adhesion molecule (NCAM) domain is involved in double-reciprocal interaction with the second immunoglobulin-like NCAM domain and in heparin binding. J. Biol. Chem. 271:10125-10134.
29. Johnson, C. P., I. Fujimoto, C. Perrin-Tricaud, U. Rutishauser, and D. Leckband. 2004. Mechanism of homophilic adhesion by the neural cell adhesion molecule: use of multiple domains and flexibility. Proc. Natl. Acad. Sci. USA. 101:6963-6968.
30. Wieland, J. A., A. A. Gewirth, and D. E. Leckband. 2005. Single molecule adhesion measurements reveal two homophilic neural cell adhesion molecule bonds with mechanically distinct properties. J. Biol. Chem. 280:41037-41046.
31. Atkins, A. R., W. J. Gallin, G. C. Owens, G. M. Edelman, and B. A. Cunningham. 2004. N-CAM homophilic binding mediated by the two N-terminal Ig domains is influenced by intramolecular domain: domain interactions. J. Biol. Chem. 279:49633-49643.
32. Soroka, V., K. Kolkova, J. S. Kastrup, K. Diederichs, J. Breed, et al. 2003. Structure and interactions of NCAM Ig1-2-3 suggest a novel zipper mechanism for homophilic adhesion. Structure. 11:1291-1301.
33. Jensen, P. H., V. Soroka, N. K. Thomsen, I. Ralets, V. Berezin, et al. 1999. Structure and interactions of NCAM modules 1 and 2, basic elements in neural cell adhesion. Nat. Struct. Biol. 6:486-493.
34. Johnson, C. P., I. Fujimoto, U. Rutishauser, and D. E. Leckband. 2005. Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem. 280:137-145.
35. Kiss, J. Z., and D. Muller. 2001. Contribution of the neural cell adhesion molecule to neuronal and synaptic plasticity. Rev. Neurosci. 12:297-310.
36. van den Pol, A. N., U. di Porzio, and U. Rutishauser. 1986. Growth cone localization of neural cell adhesion molecule on central nervous system neurons in vitro. J. Cell Biol. 102:2281-2294.
37. Cremer, H., G. Chazal, C. Goridis, and A. Represa. 1997. NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol. Cell. Neurosci. 8:323-335.
38. Baker, M. W., and E. R. Macagno. 2007. In vivo imaging of growth cone and filopodial dynamics: evidence for contact-mediated retraction of filopodia leading to the tiling of sibling processes. J. Comp. Neurol. 500:850-862.
39. Karplus, M., and J. A. McCammon. 2002. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9:646-652.
40. Lu, H., B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:662-671.
41. Craig, D., M. Gao, K. Schulten, and V. Vogel. 2004. Tuning the mechanical stability of fibronectin type III modules through sequence variations. Structure. 12:21-30.
42. Ortiz, V., S. O. Nielsen, M. L. Klein, and D. E. Discher. 2005. Unfolding a linker between helical repeats. J. Mol. Biol. 349:638-647.
43. Marszalek, P. E., H. Lu, H. Li, M. Carrion-Vazquez, A. F. Oberhauser, et al. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
44. Oberhauser, A. F., C. Badilla-Fernandez, M. Carrion-Vazquez, and J. M. Fernandez. 2002. The mechanical hierarchies of fibronectin observed with single-molecule AFM. J. Mol. Biol. 319:433-447.
45. Johnson, C. P., M. Gaetani, V. Ortiz, N. Bhasin, S. Harper, et al. 2007. Pathogenic proline mutation in the linker between spectrin repeats: disease caused by spectrin unfolding. Blood. 109:3538-3543.
46. Bayas, M. V., A. Kearney, A. Avramovic, P. A. van der Merwe, and D. E. Leckband. 2007. Impact of salt bridges on the equilibrium binding and adhesion of human CD2 and CD58. J. Biol. Chem. 282:5589-5596.
47. Bayas, M. V., K. Schulten, and D. Leckband. 2003. Forced detachment of the CD2-CD58 complex. Biophys. J. 84:2223-2233.
48. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, et al. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
49. MacKerell, A. D., D. Bashford, M. Bellott, R. L. Dunbrack, J. D. Evanseck, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
50. Buck, M., S. Bouguet-Bonnet, R. W. Pastor, and A. D. MacKerell Jr. 2006. Importance of the CMAP correction to the CHARMM22 protein force field: dynamics of hen lysozyme. Biophys. J. 90:L36-L38.
51. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.
52. Gao, M., M. Sotomayor, E. Villa, E. H. Lee, and K. Schulten. 2006. Molecular mechanisms of cellular mechanics. Phys. Chem. Chem. Phys. 8:3692-3706.
53. Altmann, S. M., R. G. Grunberg, P. F. Lenne, J. Ylanne, A. Raae, et al. 2002. Pathways and intermediates in forced unfolding of spectrin repeats. Structure. 10:1085-1096.
54. Lee, E. H., M. Gao, N. Pinotsis, M. Wilmanns, and K. Schulten. 2006. Mechanical strength of the titin Z1Z2-telethonin complex. Structure. 14:497-509.
55. Schwaiger, I., C. Sattler, D. R. Hostetter, and M. Rief. 2002. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 1:232-235.
56. Paramore, S., G. S. Ayton, D. T. Mirijanian, and G. A. Voth. 2006. Extending a spectrin repeat unit. I: linear force-extension response. Biophys. J. 90:92-100.
57. Evans, E. 2001. Probing the relation between force - lifetime - and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:105-128.
58. Itsuo, H., H. Tomoaki, and K. Satoyuki. 2008. The antigen-antibody unbinding process through steered molecular dynamics of a complex of an Fv fragment and lysozyme. J. Phys. Condens. Matter. 20:255238-1-255238-10.
59. 3 receptor. Biophys. J. 90:1979-1991.
60. Kim, T., A. Rhee, and C. M. Yip. 2006. Force-induced insulin dimer dissociation: a molecular dynamics study. J. Am. Chem. Soc. 128:5330-5331.