Magnesium promotes structural integrity and conformational switching action of a calcium sensor protein

Biochemistry

Volumn 46, Issue 12, 2007, Pages 3835-3845

  Mukherjee, Sulakshana ^a   Mohan, P M Krishna ^a   Chary, Kandala V R ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICS; CALCIUM; MAGNESIUM; NUCLEAR MAGNETIC RESONANCE; PROTEINS; SIGNAL TRANSDUCTION;

CALCIUM BINDING; CALCIUM SENSOR; GAINS STABILITY;

BIOSENSORS;

CALCIUM; CALCIUM BINDING PROTEIN; MAGNESIUM; MONOMER;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; ENTAMOEBA HISTOLYTICA; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; ENTAMOEBA HISTOLYTICA; MAGNESIUM; PROTEIN CONFORMATION; PROTOZOAN PROTEINS;

ENTAMOEBA HISTOLYTICA;

EID: 33947622613     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0621260     Document Type: Article

References (46)

1. Ikura, M. (1996) Calcium binding and conformational response in EF-hand proteins, Trends Biochem. Sci. 21, 14-17.
2. Kretsinger, R. H., and Nockolds, C. E. (1973) Carp muscle calcium-binding protein. II. Structure determination and general description, J. Biol. Chem. 248, 3313-3326.
3. Nelson, M. R., and Chazin, W. J. (1998) Structures of EF-hand Ca(2+)-binding proteins: diversity in the organization, packing and response to Ca2+ binding, Biometals 11, 297-318.
4. Strynadka, N. C., and James, M. N. (1989) Crystal structures of the helix-loop-helix calcium-binding proteins, Annu. Rev. Biochem. 58, 951-998.
5. Wang, Z., Gergely, J., and Tao, T. (1992) Characterization of the Ca(2+)-triggered conformational transition in troponin C, Proc. Natl. Acad. Sci. U.S.A. 89, 11814-11817.
6. Trave, G., Lacombe, P. J., Pfuhl, M., Saraste, M., and Pastore, A. (1995) Molecular mechanism of the calcium-induced conformational change in the spectrin EF-hands, EMBO J. 14, 4922-4931.
7. Zhang, M., Tanaka, T., and Ikura, M. (1995) Calcium-induced conformational transition revealed by the solution structure of apo calmodulin, Nat. Struct. Biol. 2, 758-767.
8. Houdusse, A., Love, M. L., Dominguez, R., Grabarek, Z., and Cohen, C. (1997) Structures of four Ca2+-bound troponin C at 2.0 A resolution: further insights into the Ca2+-switch in the calmodulin superfamily, Structure 5, 1695-1711.
9. Falke, J. J., Drake, S. K., Hazard, A. L., and Peersen, O. B. (1994) Molecular tuning of ion binding to calcium signaling proteins, Q. Rev. Biophys. 27, 219-290.
10. Cates, M. S., Teodoro, M. L., and Phillips, G. N., Jr. (2002) Molecular mechanisms of calcium and magnesium binding to parvalbumin, Biophys. J. 82, 1133-1146.
11. Linse, S., and Forsen, S. (1995) Calcium Regulation of Cellular Function (Means, A. R., Ed.) pp 89-152, Raven Press, New York.
12. da Silva, A. C., Kendrick-Jones, J., and Reinach, F. C. (1995) Determinants of ion specificity on EF-hands sites. Conversion of the Ca2+/Mg2+ site of smooth muscle myosin regulatory light chain into a Ca(2+)-specific site, J. Biol. Chem. 270, 6773-6778.
13. Ohki, S., Ikura, M., and Zhang, M. (1997) Identification of Mg2+-binding sites and the role of Mg2+ on target recognition by calmodulin, Biochemistry 36, 4309-4316.
14. Wingard, J. N., Chan, J., Bosanac, I., Haeseleer, F., Palczewski, K., Ikura, M., and Ames, J. B. (2005) Structural analysis of Mg2+ and Ca2+ binding to CaBP1, a neuron-specific regulator of calcium channels, J. Biol. Chem. 280, 37461-37470.
15. Berggard, T., Miron, S., Onnerfjord, P., Thulin, E., Akerfeldt, K. S., Enghild, J. J., Akke, M., and Linse, S. (2002) Calbindin D28k exhibits properties characteristic of a Ca2+ sensor, J. Biol. Chem. 277, 16662-16672.
16. Yamniuk, A. P., Nguyen, L. T., Hoang, T. T., and Vogel, H. J. (2004) Metal ion binding properties and conformational states of calcium- and integrin-binding protein, Biochemistry 43, 2558-2568.
17. Mukherjee, S., Kuchroo, K., and Chary, K. V. (2005) Structural characterization of the apo form of a calcium binding protein from Entamoeba histolytica by hydrogen exchange and its folding to the holo state, Biochemistry 44, 11636-11645.
18. Combos, Z., Durussel, I., Ikura, M., Rose, D. R., Cox, J. A., and Chakrabartty, A. (2003) Conformational coupling of Mg2+ and Ca2+ on the three-state folding of calexcitin B, Biochemistry 42, 5531-5539.
19. Atreya, H. S., Sahu, S. C., Bhattacharya, A., Chary, K. V., and Govil, G. (2001) NMR derived solution structure of an EF-hand calcium-binding protein from Entamoeba Histolytica, Biochemistry 40, 14392-14403.
20. Sahu, S. C., Bhattacharya, A., Chary, K. V., and Govil, G. (1999) Secondary structure of a calcium binding protein (CaBP) from Entamoeba histolytica, FEBS Lett. 459, 51-56.
21. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants, Biochemistry 27, 8063-8068.
22. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
23. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
24. Christova, P., Cox, J. A., and Craescu, C. T. (2000) Ion-induced conformational and stability changes in Nereis sarcoplasmic calcium binding protein: evidence that the APO state is a molten globule, Proteins 40, 177-184.
25. Rao, B. D. (1989) Nuclear magnetic resonance line-shape analysis and determination of exchange rates, Methods Enzymol. 176, 279-311.
26. Linse, S., and Chazin, W. J. (1995) Quantitative measurements of the cooperativity in an EF-hand protein with sequential calcium binding, Protein Sci. 4, 1038-1044.
27. Mohan, P. M., Barve, M., Chatterjee, A., and Hosur, R. V. (2006) pH driven conformational dynamics and dimer-to-monomer transition in DLC8, Protein Sci. 15, 335-342.
28. Baum, J., Dobson, C. M., Evans, P. A., and Hanley, C. (1989) Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig alpha-lactalbumin, Biochemistry 28, 7-13.
29. Schulman, B. A., Kim, P. S., Dobson, C. M., and Redfield, C. (1997) A residue-specific NMR view of the non-cooperative unfolding of a molten globule, Nat. Struct. Biol. 4, 630-634.
30. Zuleeg, T., Hartmann, R. K., Kreutzer, R., and Limmer, S. (2001) NMR spectroscopic evidence for Mn(2+)(Mg(2+)) binding to a precursor-tRNA microhelix near the potential RNase P cleavage site, J. Mol. Biol. 305, 181-189.
31. Bock, C. W., Katz, A. K., Markham, G. D., and Glusker, J. P. (1999) Manganese as a Replacement for Magnesium and Zinc: Functional Comparison of the Divalent Ions, J. Am. Chem. Soc. 121, 7360-7372.
32. Henzl, M. T., Larson, J. D., and Agah, S. (2003) Estimation of parvalbumin Ca(2+)- and Mg(2+)-binding constants by global least-squares analysis of isothermal titration calorimetry data, Anal. Biochem. 319, 216-233.
33. Gilli, R., Lafitte, D., Lopez, C., Kilhoffer, M., Makarov, A., Briand, C., and Haiech, J. (1998) Thermodynamic analysis of calcium and magnesium binding to calmodulin, Biochemistry 37, 5450-5456.
34. Linse, S., Helmersson, A., and Forsen, S. (1991) Calcium binding to calmodulin and its globular domains, J. Biol. Chem. 266, 8050-8054.
35. Shaw, G. S., Hodges, R. S., and Sykes, B. D. (1990) Calcium-induced peptide association to form an intact protein domain: 1H NMR structural evidence, Science 249, 280-283.
36. Malmendal, A., Evenas, J., Thulin, E., Gippert, G. P., Drakenberg, T., and Forsen, S. (1998) When size is important. Accommodation of magnesium in a calcium binding regulatory domain, J. Biol. Chem. 273, 28994-29001.
37. Martin, S. R., Lu, A. Q., Xiao, J., Kleinjung, J., Beckingham, K., and Bayley, P. M. (1999) Conformational and metal-binding properties of androcam, a testis-specific, calmodulin-related protein from Drosophila, Protein Sci. 8, 2444-2454.
38. Finley, N. L., Howarth, J. W., and Rosevear, P. R. (2004) Structure of the Mg2+-loaded C-lobe of cardiac troponin C bound to the N-domain of cardiac troponin I: comparison with the Ca2+-loaded structure, Biochemistry 43, 11371-11379.
39. Andersson, M., Malmendal, A., Linse, S., Ivarsson, I., Forsen, S., and Svensson, L. A. (1997) Structural basis for the negative allostery between Ca(2+)- and Mg(2+)-binding in the intracellular Ca(2+)-receptor calbindin D9k, Protein Sci. 6, 1139-1147.
40. Malmendal, A., Linse, S., Evenas, J., Forsen, S., and Drakenberg, T. (1999) Battle for the EF-hands: magnesium-calcium interference in calmodulin, Biochemistry 38, 11844-11850.
41. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C. B., and Bax, A. (1995) Solution structure of calcium-free calmodulin, Nat. Struct. Biol. 2, 768-776.
42. Grabarek, Z. (2006) Structural basis for diversity of the EF-hand calcium-binding proteins, J. Mol. Biol. 359, 509-525.
43. Williams, D. H., Stephens, E., Zhou, M., and Zerella, R. (2004) Contributions to the catalytic efficiency of enzymes, and the binding of ligands to receptors, from improvements in packing within enzymes and receptors, Methods Enzymol. 380, 3-19.
44. Precheur, B., Cox, J. A., Petrova, T., Mispelter, J., and Craescu, C. T. (1996) Nereis sarcoplasmic Ca2+-binding protein has a highly unstructured apo state which is switched to the native state upon binding of the first Ca2+ ion, FEBS Lett. 395, 89-94.
45. Lytle, B. L., Volkman, B. F., Westler, W. M., and Wu, J. H. (2000) Secondary structure and calcium-induced folding of the Clostridium thermocellum dockerin domain determined by NMR spectroscopy, Arch. Biochem. Biophys. 379, 237-244.
46. Jeromin, A., Muralidhar, D., Parameswaran, M. N., Roder, J., Fairwell, T., Scarlata, S., Dowal, L., Mustafi, S. M., Chary, K. V., and Sharma, Y. (2004) N-terminal myristoylation regulates calcium-induced conformational changes in neuronal calcium sensor-1, J. Biol. Chem. 279, 27158-27167.