Thermodynamic effects of noncoded and coded methionine substitutions in calmodulin

Biophysical Journal

Volumn 96, Issue 4, 2009, Pages 1495-1507

  Yamniuk, Aaron P ^a   Ishida, Hiroaki ^a   Lippert, Dustin ^b   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APOCALMODULIN; APOPROTEIN; CALCIUM; CALMODULIN; LEUCINE; METHIONINE; NORLEUCINE; UNCLASSIFIED DRUG; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; MYOSIN LIGHT CHAIN KINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DIFFERENTIAL SCANNING CALORIMETRY; ENTHALPY; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; MELTING POINT; MOLECULAR STABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; SUBSTITUTION REACTION; THERMODYNAMICS; AMINO ACID SUBSTITUTION; CALORIMETRY; CHEMISTRY; GENETICS; MISSENSE MUTATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; SPECTROFLUOROMETRY; TEMPERATURE; TOBACCO;

AMINO ACID SUBSTITUTION; CALMODULIN; CALORIMETRY; LEUCINE; MAGNETIC RESONANCE SPECTROSCOPY; METHIONINE; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; MUTATION, MISSENSE; MYOSIN-LIGHT-CHAIN KINASE; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; THERMODYNAMICS; TOBACCO;

EID: 62649170281     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.10.060     Document Type: Article

References (61)

1. Budisa, N. 2004. Prolegomena to future experimental efforts on genetic code engineering by expanding its amino acid repertoire. Angew. Chem. Int. Ed. Engl. 43:6426-6463. (Pubitemid 40029495)
2. Hendrickson, T. L., V. Crecy-Lagard, and P. Schimmel. 2004. Incorporation of nonnatural amino acids into proteins. Annu. Rev. Biochem. 73:147-176. (Pubitemid 39050366)
3. Link, A. J., M. L. Mock, and D. A. Tirrell. 2003. Non-canonical amino acids in protein engineering. Curr. Opin. Biotechnol. 14:603-609. (Pubitemid 37518438)
4. Hendrickson, W. A., J. R. Horton, and D. M. LeMaster. 1990. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9:1665-1672.
5. Bann, J. G., J. Pinkner, S. J. Hultgren, and C. Frieden. 2002. Real-time and equilibrium (19)F-NMR studies reveal the role of domain-domain interactions in the folding of the chaperone PapD. Proc. Natl. Acad. Sci. USA. 99:709-714.
6. Budisa, N., C. Minks, F. J. Medrano, J. Lutz, R. Huber, et al. 1998. Residue-specific bioincorporation of non-natural, biologically active amino acids into proteins as possible drug carriers: structure and stability of the per-thiaproline mutant of annexin V. Proc. Natl. Acad. Sci. USA. 95:455-459.
7. Budisa, N., R. Huber, R. Golbik, C. Minks, E. Weyher, et al. 1998. Atomic mutations in annexin V-thermodynamic studies of isomorphous protein variants. Eur. J. Biochem. 253:1-9.
8. Ratnaparkhi, G. S., and R. Varadarajan. 2000. Thermodynamic and structural studies of cavity formation in proteins suggest that loss of packing interactions rather than the hydrophobic effect dominates the observed energetics. Biochemistry. 39:12365-12374.
9. Ishida, H., and H. J. Vogel. 2006. Protein-peptide interaction studies demonstrate the versatility of calmodulin target protein binding. Protein Pept. Lett. 13:455-465.
10. Yamniuk, A. P., and H. J. Vogel. 2004. Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol. Biotechnol. 27:33-57.
11. Yuan, T., H. Ouyang, and H. J. Vogel. 1999. Surface exposure of the methionine side chains of calmodulin in solution. A nitroxide spin label and two-dimensional NMR study. J. Biol. Chem. 274:8411-8420.
12. Ikura, M., and J. B. Ames. 2006. Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality. Proc. Natl. Acad. Sci. USA. 103:1159-1164.
13. Chin, D., and A. R. Means. 2000. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10:322-328.
14. Jurado, L. A., P. S. Chockalingam, and H. W. Jarrett. 1999. Apocalmodulin. Physiol. Rev. 79:661-682.
15. Ishida, H., M. A. Borman, J. Ostrander, H. J. Vogel, and J. A. Macdonald. 2008. Solution structure of the calponin homology (CH)-domain from the smoothelin-like 1 protein: a unique Apo-calmodulin binding mode and the possible role of the C-terminal type 2 CH-domain in smooth muscle relaxation. J. Biol. Chem. 283:20569-20578.
16. Edwards, R. A., M. P. Walsh, C. Sutherland, and H. J. Vogel. 1998. Activation of calcineurin and smooth muscle myosin light chain kinase by Met-to-Leu mutants of calmodulin. Biochem. J. 331:149-152. (Pubitemid 28163968)
17. Weljie, A. M., and H. J. Vogel. 2000. Tryptophan fluorescence of calmodulin binding domain peptides interacting with calmodulin containing unnatural methionine analogues. Protein Eng. 13:59-66. (Pubitemid 30105579)
18. Yuan, T., A. M. Weljie, and H. J. Vogel. 1998. Tryptophan fluorescence quenching by methionine and selenomethionine residues of calmodulin: orientation of peptide and protein binding. Biochemistry. 37:3187-3195.
19. Yuan, T., and H. J. Vogel. 1999. Substitution of the methionine residues of calmodulin with the unnatural amino acid analogs ethionine and norleucine: biochemical and spectroscopic studies. Protein Sci. 8:113-121.
20. Zhang, M., M. Li, J. H. Wang, and H. J. Vogel. 1994. The effect of Met→Leu mutations on calmodulin's ability to activate cyclic nucleotide phosphodiesterase. J. Biol. Chem. 269:15546-15552. (Pubitemid 2090686)
21. Zhang, M., and H. J. Vogel. 1994. Two-dimensional NMR studies of selenomethionyl calmodulin. J. Mol. Biol. 239:545-554. (Pubitemid 24210423)
22. Gellman, S. H. 1991. On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry. 30:6633-6636.
23. Protasevich, I., B. Ranjbar, V. Lobachov, A. Makarov, R. Gilli, et al. 1997. Conformation and thermal denaturation of apocalmodulin: role of electrostatic mutations. Biochemistry. 36:2017-2024.
24. Tsalkova, T. N., and P. L. Privalov. 1985. Thermodynamic study of domain organization in troponin C and calmodulin. J. Mol. Biol. 181:533-544.
25. Tjandra, N., H. Kuboniwa, H. Ren, and A. Bax. 1995. Rotational dynamics of calcium-free calmodulin studied by 15N-NMR relaxation measurements. Eur. J. Biochem. 230:1014-1024.
26. Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, et al. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6:277-293.
27. Johnson, B. A., and R. A. Blevins. 1994. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR. 4:603-614.
28. Lafitte, D., P. O. Tsvetkov, F. Devred, R. Toci, F. Barras, et al. 2002. Cation binding mode of fully oxidised calmodulin explained by the unfolding of the apostate. Biochim. Biophys. Acta. 1600:105-110.
29. Tsvetkov, P. O., I. I. Protasevich, R. Gilli, D. Lafitte, V. M. Lobachov, et al. 1999. Apocalmodulin binds to the myosin light chain kinase calmodulin target site. J. Biol. Chem. 274:18161-18164.
30. Zhang, M., T. Tanaka, and M. Ikura. 1995. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2:758-767.
31. Wang, C., and A. G. Palmer. 2003. Solution NMR methods for quantitative identification of chemical exchange in 15N-labeled proteins. Magn. Reson. Chem. 41:866-876. (Pubitemid 37352340)
32. Wiseman, T., S. Williston, J. F. Brandts, and L. N. Lin. 1989. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 179:131-137. (Pubitemid 19149635)
33. Meador, W. E., A. R. Means, and F. A. Quiocho. 1992. Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex. Science. 257:1251-1255.
34. Wintrode, P. L., and P. L. Privalov. 1997. Energetics of target peptide recognition by calmodulin: a calorimetric study. J. Mol. Biol. 266:1050-1062.
35. Brokx, R. D., M. M. Lopez, H. J. Vogel, and G. I. Makhatadze. 2001. Energetics of target peptide binding by calmodulin reveals different modes of binding. J. Biol. Chem. 276:14083-14091. (Pubitemid 37391793)
36. Yamniuk, A. P., and H. J. Vogel. 2005. Structural investigation into the differential target enzyme regulation displayed by plant calmodulin isoforms. Biochemistry. 44:3101-3111. (Pubitemid 40293685)
37. Rainaldi, M., A. P. Yamniuk, T. Murase, and H. J. Vogel. 2007. Calcium-dependent and -independent binding of soybean calmodulin isoforms to the calmodulin binding domain of tobacco MAPK phosphatase-1. J. Biol. Chem. 282:6031-6042. (Pubitemid 47100831)
38. Schumacher, M. A., M. Crum, and M. C. Miller. 2004. Crystal structures of apocalmodulin and an apocalmodulin/SK potassium channel gating domain complex. Structure. 12:849-860. (Pubitemid 38595773)
39. Budisa, N., B. Steipe, P. Demange, C. Eckerskorn, J. Kellermann, et al. 1995. High-level biosynthetic substitution of methionine in proteins by its analogs 2-aminohexanoic acid, selenomethionine, telluromethionine and ethionine in Escherichia coli. Eur. J. Biochem. 230:788-796.
40. Gassner, N. C., W. A. Baase, A. C. Hausrath, and B. W. Matthews. 1999. Substitution with selenomethionine can enhance the stability of methionine-rich proteins. J. Mol. Biol. 294:17-20.
41. Holder, J. B., A. F. Bennett, J. Chen, D. S. Spencer, M. P. Byrne, et al. 2001. Energetics of side chain packing in staphylococcal nuclease assessed by exchange of valines, isoleucines, and leucines. Biochemistry. 40:13998-14003.
42. Lipscomb, L. A., N. C. Gassner, S. D. Snow, A. M. Eldridge, W. A. Baase, et al. 1998. Context-dependent protein stabilization by methionine-to-leucine substitution shown in T4 lysozyme. Protein Sci. 7:765-773.
43. Ohmura, T., T. Ueda, Y. Hashimoto, and T. Imoto. 2001. Tolerance of point substitution of methionine for isoleucine in hen egg white lysozyme. Protein Eng. 14:421-425. (Pubitemid 32762379)
44. Karpusas, M., W. A. Baase, M. Matsumura, and B. W. Matthews. 1989. Hydrophobic packing in T4 lysozyme probed by cavity-filling mutants. Proc. Natl. Acad. Sci. USA. 86:8237-8241. (Pubitemid 19286034)
45. Sandberg, W. S., and T. C. Terwilliger. 1989. Influence of interior packing and hydrophobicity on the stability of a protein. Science. 245:54-57. (Pubitemid 19180245)
46. Skene, R. J. 2001. Crystallographic Studies of Calcium-Binding Proteins: Aeromonas salmonicida Surface Array Protein and Calmodulin. University of Calgary, Calgary, Alberta, Canada.
47. Chin, D., and A. R. Means. 1996. Methionine to glutamine substitutions in the C-terminal domain of calmodulin impair the activation of three protein kinases. J. Biol. Chem. 271:30465-30471. (Pubitemid 26404052)
48. Lee, A. L., S. A. Kinnear, and A. J. Wand. 2000. Redistribution and loss of side chain entropy upon formation of a calmodulin-peptide complex. Nat. Struct. Biol. 7:72-77. (Pubitemid 30043252)
49. Biekofsky, R. R., S. R. Martin, J. E. McCormick, L. Masino, S. Fefeu, et al. 2002. Thermal stability of calmodulin and mutants studied by (1)H-(15)N HSQC NMR measurements of selectively labeled [(15)N]Ile proteins. Biochemistry. 41:6850-6859.
50. Masino, L., S. R. Martin, and P. M. Bayley. 2000. Ligand binding and thermodynamic stability of a multidomain protein, calmodulin. Protein Sci. 9:1519-1529.
51. Yap, K. L., J. Kim, K. Truong, M. Sherman, T. Yuan, et al. 2000. Calmodulin target database. J. Struct. Funct. Genomics. 1:8-14.
52. Dunitz, J. D. 1995. Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions. Chem. Biol. 2:709-712.
53. Cooper, A., C. M. Johnson, J. H. Lakey, and M. Nollmann. 2001. Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys. Chem. 93:215-230.
54. Lumry, R., and S. Rajender. 1970. Enthalpy-entropy compensation phenomena in water solutions of proteins and small molecules: a ubiquitous property of water. Biopolymers. 9:1125-1227.
55. Whitesides, G. M., and V. M. Krishnamurthy. 2005. Designing ligands to bind proteins. Q. Rev. Biophys. 38:385-395. (Pubitemid 44366939)
56. Steiner, R. F. 1984. Location of a binding site for 1-anilinonaphthalene- 8-sulfonate on calmodulin. Arch. Biochem. Biophys. 228:105-112.
57. Ferrington, D. A., H. Sun, K. K. Murray, J. Costa, T. D. Williams, et al. 2001. Selective degradation of oxidized calmodulin by the 20 S proteasome. J. Biol. Chem. 276:937-943.
58. Tsvetkov, P. O., B. Ezraty, J. K. Mitchell, F. Devred, V. Peyrot, et al. 2005. Calorimetry and mass spectrometry study of oxidized calmodulin interaction with target and differential repair by methionine sulfoxide reductases. Biochimie. 87:473-480.
59. Gifford, J. L., M. P. Walsh, and H. J. Vogel. 2007. Structures and metalion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 405:199-221. (Pubitemid 47075156)
60. Miyawaki, A., J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, et al. 1997. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature. 388:882-887.
61. Berggard, T., G. Arrigoni, O. Olsson, M. Fex, S. Linse, et al. 2006. 140 mouse brain proteins identified by Ca2+-calmodulin affinity chromatography and tandem mass spectrometry. J. Proteome Res. 5:669-687.