Oxidation increases the strength of the methionine-aromatic interaction

Nature Chemical Biology

Volumn 12, Issue 10, 2016, Pages 860-866

  Lewis, Andrew K ^a   Dunleavy, Katie M ^b   Senkow, Tiffany L ^a   Her, Cheng ^a   Horn, Benjamin T ^b   Jersett, Mark A ^b   Mahling, Ryan ^b   McCarthy, Megan R ^a   Perell, Gabriella T ^a   Valley, Christopher C ^a   Karim, Christine B ^a   Gao, Jiali ^a   Pomerantz, William C K ^a   Thomas, David D ^a   Cembran, Alessandro ^b   Hinderliter, Anne ^b   Sachs, Jonathan N ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA DULUTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC COMPOUND; BENZENE; CALMODULIN; DIMETHYL SULFOXIDE; INDOLE; LYMPHOTOXIN; METHIONINE; PEPTIDE; PHENOL; AROMATIC HYDROCARBON;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOLOGY; DATA BASE; ELECTRON SPIN RESONANCE; LIGAND BINDING; MODEL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DATA BANK; PROTEIN STRUCTURE; QUANTUM MECHANICS; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION; QUANTUM THEORY;

HYDROCARBONS, AROMATIC; METHIONINE; MODELS, MOLECULAR; OXIDATION-REDUCTION; QUANTUM THEORY;

EID: 84983268356     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2159     Document Type: Article

References (59)

1. Valley, C.C., et al. The methionine-aromatic motif plays a unique role in stabilizing protein structure. J. Biol. Chem. 287, 34979-34991 (2012
2. Zauhar, R.J., Colbert, C.L., Morgan, R.S., & Welsh, W.J. Evidence for a strong sulfur-aromatic interaction derived from crystallographic data. Biopolymers 53, 233-248 (2000
3. Reid, K.S.C., Lindley, P.F., & Thornton, J.M. Sulphur-aromatic interactions in proteins. FEBS Lett. 190, 209-213 (1985
4. Pranata, J. Sulfur-Aromatic Interactions: A Computational Study of the Dimethyl Sulfide-Benzene Complex. Bioorg. Chem. 25, 213-219 (1997
5. Morgan, R.S., & McAdon, J.M. Predictor for sulfur-aromatic interactions in globular proteins. Int. J. Pept. Protein Res. 15, 177-180 (1980
6. Morgan, R.S., Tatsch, C.E., Gushard, R.H., McAdon, J., & Warme, P.K. Chains of alternating sulfur and pi-bonded atoms in eight small proteins. Int. J. Pept. Protein Res. 11, 209-217 (1978
7. Viguera, A.R., & Serrano, L. Side-chain interactions between sulfur-containing amino acids and phenylalanine in α-helices. Biochemistry 34, 8771-8779 (1995
8. Shechter, Y., Burstein, Y., & Patchornik, A. Selective oxidation of methionine residues in proteins. Biochemistry 14, 4497-4503 (1975
9. Hoshi, T., & Heinemann, S. Regulation of cell function by methionine oxidation and reduction. J. Physiol. (Lond) 531, 1-11 (2001
10. Levine, R.L., Berlett, B.S., Moskovitz, J., Mosoni, L., & Stadtman, E.R. Methionine residues may protect proteins from critical oxidative damage. Mech. Ageing Dev. 107, 323-332 (1999
11. Kim, G., Weiss, S.J., & Levine, R.L. Methionine oxidation and reduction in proteins. Biochim. Biophys. Acta 1840, 901-905 (2014
12. Arakawa, T., Kita, Y., & Timasheff, S.N. Protein precipitation and denaturation by dimethyl sulfoxide. Biophys. Chem. 131, 62-70 (2007
13. Rose, G.D., Geselowitz, A.R., Lesser, G.J., Lee, R.H., & Zehfus, M.H. Hydrophobicity of amino acid residues in globular proteins. Science 229, 834-838 (1985
14. Dougherty, D.A. Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271, 163-168 (1996
15. Bogan, A.A., & Thorn, K.S. Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280, 1-9 (1998
16. Gottlieb, H.E., Kotlyar, V., & Nudelman, A. NMR chemical shifts of common laboratory solvents as trace impurities. J. Org. Chem. 62, 7512-7515 (1997
17. Butterfield, S.M., Patel, P.R., & Waters, M.L. Contribution of aromatic interactions to alpha-helix stability. J. Am. Chem. Soc. 124, 9751-9755 (2002
18. Greenfield, N.J. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1, 2527-2535 (2006
19. Marqusee, S., & Baldwin, R.L. Helix stabilization by Glu-Lys+ salt bridges in short peptides of de novo design. Proc. Natl. Acad. Sci. USA 84, 8898-8902 (1987
20. Pearson, K. LIII. On lines and planes of closest fit to systems of points in space. Phil. Mag. 2, 559-572 (1901
21. Yin, D., Kuczera, K., & Squier, T.C. The sensitivity of carboxyl-terminal methionines in calmodulin isoforms to oxidation by H(2)O(2) modulates the ability to activate the plasma membrane Ca-ATPase. Chem. Res. Toxicol. 13, 103-110 (2000
22. Sacksteder, C.A., et al. Tertiary structural rearrangements upon oxidation of Methionine145 in calmodulin promotes targeted proteasomal degradation. Biophys. J. 91, 1480-1493 (2006
23. Gao, J., Yao, Y., & Squier, T.C. Oxidatively modified calmodulin binds to the plasma membrane Ca-ATPase in a nonproductive and conformationally disordered complex. Biophys. J. 80, 1791-1801 (2001
24. Gao, J., et al. Loss of conformational stability in calmodulin upon methionine oxidation. Biophys. J. 74, 1115-1134 (1998
25. Boschek, C.B., Jones, T.E., Smallwood, H.S., Squier, T.C., & Bigelow, D.J. Loss of the calmodulin-dependent inhibition of the RyR1 calcium release channel upon oxidation of methionines in calmodulin. Biochemistry 47, 131-142 (2008
26. Bartlett, R.K., et al. Oxidation of Met144 and Met145 in calmodulin blocks calmodulin dependent activation of the plasma membrane Ca-ATPase. Biochemistry 42, 3231-3238 (2003
27. Babu, Y.S., Bugg, C.E., & Cook, W.J. Structure of calmodulin refined at 2.2 A resolution. J. Mol. Biol. 204, 191-204 (1988
28. Kuboniwa, H., et al. Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2, 768-776 (1995
29. Mukherjea, P., Maune, J.F., & Beckingham, K. Interlobe communication in multiple calcium-binding site mutants of Drosophila calmodulin. Protein Sci. 5, 468-477 (1996
30. Anbanandam, A., et al. Mediating molecular recognition by methionine oxidation: conformational switching by oxidation of methionine in the carboxyl-terminal domain of calmodulin. Biochemistry 44, 9486-9496 (2005
31. Jeschke, G. DEER distance measurements on proteins. Annu. Rev. Phys. Chem. 63, 419-446 (2012
32. Ilardi, E.A., Vitaku, E., & Njardarson, J.T. Data-mining for sulfur and fluorine: an evaluation of pharmaceuticals to reveal opportunities for drug design and discovery. J. Med. Chem. 57, 2832-2842 (2014
33. Scott, J., Asami, M., & Tanaka, K. Novel chromogenic, guest-sensitive host compounds. New J. Chem. 26, 1822-1826 (2002
34. Jiménez, M.A., Muñoz, V., Rico, M., & Serrano, L. Helix stop and start signals in peptides and proteins. The capping box does not necessarily prevent helix elongation. J. Mol. Biol. 242, 487-496 (1994
35. Vasquez, M., Pincus, M.R., & Scheraga, H.A. Helix-coil transition theory including long-range electrostatic interactions: application to globular proteins. Biopolymers 26, 351-371 (1987
36. Fealey, M.E., et al. Negative coupling as a mechanism for signal propagation between C2 domains of synaptotagmin I. PLoS One 7, e46748 (2012
37. Horovitz, A. Double-mutant cycles: a powerful tool for analyzing protein structure and function. Fold. Des. 1, R121-R126 (1996
38. Horovitz, A., Serrano, L., Avron, B., Bycroft, M., & Fersht, A.R. Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216, 1031-1044 (1990
39. Serrano, L., Bycroft, M., & Fersht, A.R. Aromatic-aromatic interactions and protein stability. Investigation by double-mutant cycles. J. Mol. Biol. 218, 465-475 (1991
40. Balog, E.M., Lockamy, E.L., Thomas, D.D., & Ferrington, D.A. Site-specific methionine oxidation initiates calmodulin degradation by the 20S proteasome. Biochemistry 48, 3005-3016 (2009
41. Klein, J.C., et al. Actin-binding cleft closure in myosin II probed by site-directed spin labeling and pulsed EPR. Proc. Natl. Acad. Sci. USA 105, 12867-12872 (2008
42. Etemadi, N., et al. Lymphotoxin α induces apoptosis, necroptosis and inflammatory signals with the same potency as tumour necrosis factor. FEBS J. 280, 5283-5297 (2013
43. Frisch, M.J., et al. Gaussian 09, Revision D.01. (Gaussian, Inc., 2009
44. Boys, S.F., & Bernardi, F. The calculation of small molecular interactions by the differences of separate total energies. Some procedures with reduced errors. Mol. Phys. 19, 553-566 (1970
45. Zhao, Y., & Truhlar, D.G. A new local density functional for main-group thermochemistry, transition metal bonding, thermochemical kinetics, and noncovalent interactions. J. Chem. Phys. 125, 194101 (2006
46. Reed, A.E., Curtiss, L.A., & Weinhold, F. Intermolecular interactions from a natural bond orbital, donor-acceptor viewpoint. Chem. Rev. 88, 899-926 (1988
47. Mulliken, R.S. Electronic population analysis on LCAO-MO molecular wave functions. I. J. Chem. Phys. 23, 1833-1840 (1955
48. Cramer, C.J. Essentials of Computational Chemistry: Theories and Models (John Wiley, & Sons, 2013
49. Phillips, J.C., et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005
50. Banner, D.W., et al. Crystal structure of the soluble human 55 kd TNF receptor-human TNF beta complex: implications for TNF receptor activation. Cell 73, 431-445 (1993
51. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., & Klein, M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935 (1983
52. MacKerell, A.D., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616 (1998
53. MacKerell, A.D. Jr., Feig, M., & Brooks, C.L. III. Improved treatment of the protein backbone in empirical force fields. J. Am. Chem. Soc. 126, 698-699 (2004
54. Best, R.B., et al. Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, ψ and side-chain χ(1) and χ(2) dihedral angles. J. Chem. Theory Comput. 8, 3257-3273 (2012
55. Martyna, G.J., Tobias, D.J., & Klein, M.L. Constant-pressure molecular-dynamics algorithms. J. Chem. Phys. 101, 4177-4189 (1994
56. Jas, G.S., & Kuczera, K. Free-energy simulations of the oxidation of c-terminal methionines in calmodulin. Proteins 48, 257-268 (2002
57. Darden, T., Perera, L., Li, L., & Pedersen, L. New tricks for modelers from the crystallography toolkit: the particle mesh Ewald algorithm and its use in nucleic acid simulations. Structure 7, R55-R60 (1999
58. Tuckerman, M., Berne, B.J., & Martyna, G.J. Reversible multiple time scale molecular dynamics. J. Chem. Phys. 97, 1990-2001 (1992
59. Andersen, H.C. Rattle: a velocity version of the shake algorithm for molecular-dynamics calculations. J. Comput. Phys. 52, 24-34 (1983