FRET conformational analysis of calmodulin binding to nitric oxide synthase peptides and enzymes

Biochemistry

Volumn 47, Issue 46, 2008, Pages 12006-12017

  Spratt, Donald E ^a   Taiakina, Valentina ^a   Palmer, Michael ^a   Guillemette, J Guy ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; BINDING ENERGY; CALCIUM; CATALYSTS; CONCENTRATION (PROCESS); CRYSTAL STRUCTURE; ENERGY TRANSFER; ENZYMES; FLUORESCENCE; NITRIC OXIDE; OXIDES; PEPTIDES; PORPHYRINS; PROTEINS;

BINDING DOMAINS; CALMODULIN BINDINGS; CONFORMATIONAL ANALYSES; CONFORMATIONAL TRANSITIONS; DO-MAINS; FLUORESCENCE RESONANCE ENERGY TRANSFERS; SOLVED CRYSTAL STRUCTURES; SYNTHASE;

CAMS;

CALMODULIN; NITRIC OXIDE SYNTHASE;

ARTICLE; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

AMINO ACID SUBSTITUTION; ANIMALS; CALCIUM; CALMODULIN; CATTLE; FLUORESCENCE RESONANCE ENERGY TRANSFER; ISOENZYMES; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS;

EID: 56249146311     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801418s     Document Type: Article

References (49)

1. Ikura, M., and Ames, J. B. (2006) Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality. Proc. Natl. Acad. Sci. U.S.A. 103, 1159-1164.
2. Ishida, H., and Vogel, H. J. (2006) Protein-pepfide interaction studies demonstrate the versatility of calmodulin target protein binding. Protein Pept. Lett. 13, 455-465.
3. Alderton, W. K., Cooper, C. E., and Knowles, R. G. (2001) Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357, 593-615.
4. Ghosh, D. K., and Salerno, J. C. (2003) Nitric oxide synthases: domain structure and alignment in enzyme function and control. Front. Biosci. 8, d193-209.
5. Roman, L. J., Martasek, P., and Masters, B. S. (2002) Intrinsic and extrinsic modulation of nitric oxide synthase activity. Chem. Rev. 102, 1179-1190.
6. Aoyagi, M., Arvai, A. S., Tainer, J. A., and Getzoff, E. D. (2003) Structural basis for endothelial nitric oxide synthase binding to calmodulin. EMBO J. 22, 766-775.
7. Spratt, D. E., Taiakina, V., Palmer, M., and Guillemette, J. G. (2007) Differential binding of calmodulin domains to constitutive and inducible nitric oxide synthase enzymes. Biochemistry 46, 8288-8300.
8. Zhang, M., Yuan, T., Aramini, J. M., and Vogel, H. J. (1995) Interaction of calmodulin with its binding domain of rat cerebellar nitric oxide synthase. A multinuclear NMR study. J. Biol. Chem. 270, 20901-20907.
9. Garcin, E. D., Bruns, C. M., Lloyd, S. J., Hosfield, D. J., Tiso, M., Gachhui, R., Stuehr, D. J., Tainer, J. A., and Getzoff, E. D. (2004) Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J. Biol. Chem. 279, 37918-37927.
10. Ruan, J., Xie, Q., Hutchinson, N., Cho, H., Wolfe, G. C., and Nathan, C. (1996) Inducible nitric oxide synthase requires both the canonical calmodulin-binding domain and additional sequences in order to bind calmodulin and produce nitric oxide in the absence of free Ca2+. J. Biol. Chem. 271, 22679-22686.
11. Roman, L. J., and Masters, B. S. (2006) Electron transfer by neuronal nitric-oxide synthase is regulated by concerted interaction of calmodulin and two intrinsic regulatory elements. J. Biol. Chem. 281, 23111-23118.
12. Heyduk, T. (2002) Measuring protein conformational changes by FRET/LRET. Curr. Opin. Biotechnol. 13, 292-296.
13. Ikura, M., Clore, G. M., Gronenborn, A. M., Zhu, G., Klee, C. B., and Bax, A. (1992) Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638.
14. Drum, C. L., Yan, S. Z., Sarac, R., Mabuchi, Y., Beckingham, K., Bohm, A., Grabarek, Z., and Tang, W. J. (2000) An extended conformation of calmodulin induces interactions between the structural domains of adenylyl cyclase from Bacillus anthracis to promote catalysis. J. Biol. Chem. 275, 36334-36340.
15. Drum, C. L., Yan, S. Z., Bard, J., Shen, Y. Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A., and Tang, W. J. (2002) Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415, 396-402.
16. Maximciuc, A. A., Putkey, J. A., Shamoo, Y., and Mackenzie, K. R. (2006) Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode. Structure 14, 1547-1556.
17. Torok, K., Tzortzopoulos, A., Grabarek, Z., Best, S. L., and Thorogate, R. (2001) Dual effect of ATP in the activation mechanism of brain Ca(2+)/calmodulin-dependent protein kinase II by Ca(2+)/calmodulin. Biochemistry 40, 14878-14890.
18. Xiong, L., Kleerekoper, Q. K., He, R., Putkey, J. A., and Hamilton, S. L. (2005) Sites on calmodulin that interact with the C-terminal tail of Cav1.2 channel. J. Biol. Chem. 280, 7070-7079.
19. Slaughter, B. D., Unruh, J. R., Allen, M. W., Bieber Urbauer, R. J., and Johnson, C. K. (2005) Conformational substates of calmodulin revealed by single-pair fluorescence resonance energy transfer: influence of solution conditions and oxidative modification. Biochemistry 44, 3694-3707.
20. Slaughter, B. D., Unruh, J. R., Price, E. S., Huynh, J. L., Bieber Urbauer, R. J., and Johnson, C. K. (2005) Sampling unfolding intermediates in calmodulin by single-molecule spectroscopy. J. Am. Chem. Soc. 127, 12107-12114.
21. Newman, E., Spratt, D. E., Mosher, J., Cheyne, B., Montgomery, H. J., Wilson, D. L., Weinberg, J. B., Smith, S. M., Salerno, J. C., Ghosh, D. K., and Guillemette, J. G. (2004) Differential activation of nitric-oxide synthase isozymes by calmodulin-troponin C chimeras. J. Biol. Chem. 279, 33547-33557.
22. Spratt, D. E., Taiakina, V., and Guillemette, J. G. (2007) Calcium-deficient calmodulin binding and activation of neuronal and inducible nitric oxide synthases. Biochim. Biophys. Acta 1774, 1351-1358.
23. Spratt, D. E., Newman, E., Mosher, J., Ghosh, D. K., Salerno, J. C., and Guillemette, J. G. (2006) Binding and activation of nitric oxide synthase isozymes by calmodulin EF hand pairs. FEBS J. 273, 1759-1771.
24. Gribovskaja, I., Brownlow, K. C., Dennis, S. J., Rosko, A. J., Marietta, M. A., and Stevens-Truss, R. (2005) Calcium-binding sites of calmodulin and electron transfer by inducible nitric oxide synthase. Biochemistry 44, 7593-7601.
25. Stevens-Truss, R., Beckingham, K., and Marietta, M. A. (1997) Calcium binding sites of calmodulin and electron transfer by neuronal nitric oxide synthase. Biochemistry 36, 12337-12345.
26. Wang, W., and Malcolm, B. A. (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange Site-Directed Mutagenesis. Biotechniques 26, 680-682.
27. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
28. Lang, S., Spratt, D. E., Guillemette, J. G., and Palmer, M. (2005) Dual-targeted labeling of proteins using cysteine and seleno-methionine residues. Anal. Biochem. 342, 271-279.
29. Richards, M. K., Clague, M. J., and Marietta, M. A. (1996) Characterization of C415 mutants of neuronal nitric oxide synthase. Biochemistry 35, 7772-7780.
30. Munro, A. W., and Noble, M. A. (1999) Fluorescence analysis of flavoproteins. Methods Mol. Biol. 131, 25-48.
31. Chen, P. F., Tsai, A. L., and Wu, K. K. (1994) Cysteine 184 of endothelial nitric oxide synthase is involved in heme coordination and catalytic activity. J. Biol. Chem. 269, 25062-25066.
32. Roman, L. J., Sheta, E. A., Martasek, P., Gross, S. S., Liu, Q., and Masters, B. S. (1995) High-level expression of functional rat neuronal nitric oxide synthase in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 8428-8432.
33. Martasek, P., Liu, Q., Liu, J., Roman, L. J., Gross, S. S., Sessa, W. C., and Masters, B. S. (1996) Characterization of bovine endothelial nitric oxide synthase expressed in E. coli. Biochem. Biophys. Res. Commun. 219, 359-365.
34. Newton, D. C., Montgomery, H. J., and Guillemette, J. G. (1998) The reductase domain of the human inducible nitric oxide synthase is fully active in the absence of bound calmodulin. Arch. Biochem. Biophys. 359, 249-257.
35. Tsien, R., and Pozzan, T. (1989) Measurement of cytosolic free Ca2+ with quin2. Methods Enzymol. 172, 230-262.
36. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd ed., Springer, New York, NY.
37. Van der Meer, B. W., Coker, G., and Chen, S. Y. S. (1994) Resonance Energy Transfer: Theory and Data, VCH, New York, NY.
38. Allen, M. W., Urbauer, R. J., Zaidi, A., Williams, T. D., Urbauer, J. L., and Johnson, C. K. (2004) Fluorescence labeling, purification, and immobilization of a double cysteine mutant calmodulin fusion protein for single-molecule experiments. Anal. Biochem. 325, 273-284.
39. Chattopadhyaya, R., Meador, W. E., Means, A. R., and Quiocho, F. A. (1992) Calmodulin structure refined at 1.7 A resolution. J. Mol. Biol. 228, 1177-1192.
40. 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.
41. Fallon, J. L., and Quiocho, F. A. (2003) A closed compact structure of native Ca(2+)-calmodulin. Structure 11, 1303-1307.
42. Persechini, A., McMillan, K., and Leakey, P. (1994) Activation of myosin light chain kinase and nitric oxide synthase activities by calmodulin fragments. J. Biol. Chem. 269, 16148-16154.
43. Sun, H., and Squier, T. C. (2000) Ordered and cooperative binding of opposing globular domains of calmodulin to the plasma membrane Ca-ATPase. J. Biol. Chem. 275, 1731-1738.
44. Weissman, B. A., Jones, C. L., Liu, Q., and Gross, S. S. (2002) Activation and inactivation of neuronal nitric oxide synthase: characterization of Ca(2+)-dependent [125I]Calmodulin binding. Eur. J. Pharmacol. 435, 9-18.
45. Olwin, B. B., and Storm, D. R. (1985) Calcium binding to complexes of calmodulin and calmodulin binding proteins. Biochemistry 24, 8081-8086.
46. Nishida, C. R., and Ortiz de Montellano, P. R. (1999) Autoinhibition of endothelial nitric-oxide synthase. Identification of an electron transfer control element. J. Biol. Chem. 274, 14692-14698.
47. Montgomery, H. J., Romanov, V., and Guillemette, J. G. (2000) Removal of a putative inhibitory element reduces the calcium-dependent calmodulin activation of neuronal nitric-oxide synthase. J. Biol. Chem. 275, 5052-5058.
48. Nishida, C. R., and de Montellano, P. R. (2001) Control of electron transfer in nitric-oxide synthases. Swapping of autoinhibitory elements among nitric-oxide synthase isoforms. J. Biol. Chem. 276, 20116-20124.
49. Venema, R. C., Sayegh, H. S., Kent, J. D., and Harrison, D. G. (1996) Identification, characterization, and comparison of the calmodulin-binding domains of the endothelial and inducible nitric oxide synthases. J. Biol. Chem. 271, 6435-6440.