Structure-dynamic determinants governing a mode of regulatory response and propagation of allosteric signal in splice variants of Na+/Ca2+ exchange (NCX) proteins

Biochemical Journal

Volumn 465, Issue , 2015, Pages 489-501

  Giladi, Moshe ^a   Lee, Su Youn ^b   Hiller, Reuben ^a   Chung, Ka Young ^b   Khananshvili, Daniel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b Sungkyunkwan University   (South Korea)

Author keywords

Allosteric regulation; Calcium binding domain (CBD); Hydrogen deuterium exchange mass spectrometry (HDX MS); Na+ Ca2+ exchange (NCX); Small angle X ray scattering (SAXS); Structure dynamic coupling

Indexed keywords

CALCIUM 45; DEUTERIUM; PHENYLALANINE; SODIUM CALCIUM EXCHANGE PROTEIN; CALCIUM; ISOPROTEIN; PROTEIN BINDING;

ALLOSTERISM; ALTERNATIVE RNA SPLICING; ARTICLE; BINDING ASSAY; BINDING SITE; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; DISSOCIATION; DYNAMICS; GEL PERMEATION CHROMATOGRAPHY; GENE CONTROL; GENE STRUCTURE; GENETIC VARIABILITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DOG; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; STRUCTURE ACTIVITY RELATION; X RAY DIFFRACTION;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; ANIMALS; CALCIUM; DEUTERIUM EXCHANGE MEASUREMENT; DOGS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; SIGNAL TRANSDUCTION; SODIUM-CALCIUM EXCHANGER; STRUCTURE-ACTIVITY RELATIONSHIP; X-RAY DIFFRACTION;

EID: 84921753975     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20141036     Document Type: Article

References (39)

1. Philipson, K. D. and Nicoll, D. A. (2000) Sodium-calcium exchange: a molecular perspective. Annu. Rev. Physiol. 62, 111-133 CrossRef PubMed
2. Khananshvili, D. (2013) The SLC8 gene family of sodium-calcium exchangers (NCX): structure, function, and regulation in health and disease. Mol. Aspects Med. 34, 220-235 CrossRef PubMed
3. Khananshvili, D. (2014) Sodium-calcium exchangers (NCX): molecular hallmarks underlying the tissue-specific and systemic functions. Pflugers Arch. 466, 43-60 CrossRef PubMed
4. 2+ exchanger is essential for regulation: crystal structures and mutational analysis. Proc. Natl. Acad. Sci. U.S.A. 104, 18467-18472 CrossRef PubMed
5. 2+ sensors. Mol. Cell 22, 15-25 CrossRef PubMed
6. 2+ binding motif. J. Biol. Chem. 281, 21577-21581 CrossRef PubMed
7. Boyman, L., Mikhasenko, H., Hiller, R. and Khananshvili, D. (2009) Kinetic and equilibrium properties of regulatory calcium sensors of NCX1 protein. J. Biol. Chem. 284, 6185-6193 CrossRef PubMed
8. 2+ exchanger. J. Biol. Chem. 284, 14688-14692 CrossRef PubMed
9. 2+ exchanger and secondary regulation. Channels 4, 159-162 CrossRef PubMed
10. 2+ exchanger. J. Biol. Chem. 284, 32735-32741 CrossRef PubMed
11. 2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21, 1692-1703 CrossRef PubMed
12. 2+ sensor in tissue-specific NCX variants. Cell Calcium 51, 478-485 CrossRef PubMed
13. 2+-driven interdomain module governs eukaryotic NCX regulation. PLoS ONE 7, e39985 CrossRef PubMed
14. 2+ exchanger features a dual electrostatic switch mechanism. Proc. Natl. Acad. Sci. U.S.A. 106, 14333-14338 CrossRef PubMed
15. 2+ from the regulatory two-domain tandem of NCX1. J. Biol. Chem. 285, 28117-28125 CrossRef PubMed
16. Hilgemann, D. W., Matsuoka, S., Nagel, G. A. and Collins, A. (1992) Steady-state and dynamic properties of cardiac sodium-calcium exchange: sodium-dependent inactivation. J. Gen. Physiol. 100, 905-932 CrossRef PubMed
17. 2+ exchanger (NCX1) isoforms. J. Biol. Chem. 277, 33957-33962 CrossRef PubMed
18. 2+ exchanger CALX and its modification by alternative splicing. Structure 19, 1509-1517 CrossRef PubMed
19. 2+ exchanger. J. Gen. Physiol. 114, 701-711 CrossRef PubMed
20. 2+ exchanger from Drosophila melanogaster. J. Gen. Physiol. 111, 691-702 CrossRef PubMed
21. 2+-induced regulatory transitions in the sodium-calcium exchanger (NCX). J. Biol. Chem. 288, 23141-23149 CrossRef PubMed
22. 2+ exchanger dimers. Proc. Natl. Acad. Sci. U.S.A. 108, 1699-1704 CrossRef PubMed
23. 2+ exchanger. J. Biol. Chem. 286, 32123-32131 CrossRef PubMed
24. Giladi, M., Friedberg, I., Fang, X., Hiller, R., Wang, Y. X. and Khananshvili, D. (2012) G503 is obligatory for coupling of regulatory domains in NCX proteins. Biochemistry 51, 7313-7320 CrossRef PubMed
25. Koch, M. H., Vachette, P. and Svergun, D. I. (2003) Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q. Rev. Biophys. 36, 147-227 CrossRef PubMed
26. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Cryst. 36, 1277-1282 CrossRef
27. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40 CrossRef PubMed
28. Bernado, P., Mylonas, E., Petoukhov, M. V., Blackledge, M. and Svergun, D. I. (2007) Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc. 129, 5656-5664 CrossRef PubMed
29. Breukels, V. and Vuister, G. W. (2010) Binding of calcium is sensed structurally and dynamically throughout the second calcium-binding domain of the sodium/calcium exchanger. Proteins 78, 1813-1824 CrossRef PubMed
30. 2+ exchanger. J. Biol. Chem. 286, 28811-28820 CrossRef PubMed
31. Beckett, D. (2012) Hydrogen-deuterium exchange study of an allosteric energy cycle. Methods Mol. Biol. 796, 261-278 CrossRef PubMed
32. Konermann, L., Pan, J. and Liu, Y. H. (2011) Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem. Soc. Rev. 40, 1224-1234 CrossRef PubMed
33. Mo, J., Tymiak, A. A. and Chen, G. (2012) Structural mass spectrometry in biologics discovery: advances and future trends. Drug Discov. Today 17, 1323-1330 CrossRef PubMed
34. Goodey, N. M. and Benkovic, S. J. (2008) Allosteric regulation and catalysis emerge via a common route. Nat. Chem. Biol. 4, 474-482 CrossRef PubMed
35. Ma, B., Tsai, C. J., Haliloglu, T. and Nussinov, R. (2011) Dynamic allostery: linkers are not merely flexible. Structure 19, 907-917 CrossRef PubMed
36. Smock, R. G. and Gierasch, L. M. (2009) Sending signals dynamically. Science 324, 198-203 CrossRef PubMed
37. Tsai, C. J., del Sol, A. and Nussinov, R. (2008) Allostery: absence of a change in shape does not imply that allostery is not at play. J. Mol. Biol. 378, 1-11 CrossRef PubMed
38. 2+-binding domain. J. Gen. Physiol. 105, 403-420 CrossRef PubMed
39. 2+ exchanger. Proc. Natl. Acad. Sci. U.S.A. 90, 3870-3874 CrossRef PubMed