Histidine orientation modulates the structure and dynamics of a de novo metalloenzyme active site

Journal of the American Chemical Society

Volumn 137, Issue 32, 2015, Pages 10164-10176

  Ross, Matthew R ^a   White, Aaron M ^a,b   Yu, Fangting ^a,c   King, John T ^a,d   Pecoraro, Vincent L ^a   Kubarych, Kevin J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COPPER COMPOUNDS; DIHEDRAL ANGLE; DISSOCIATION; DYNAMICS; ELECTROSTATICS; INFRARED SPECTROSCOPY; LIGANDS; POTENTIAL ENERGY; PROTEINS; QUANTUM CHEMISTRY;

ELECTROSTATIC ENVIRONMENTS; OPTIMIZED STRUCTURES; SELF ASSEMBLED COMPLEXES; STRUCTURAL REARRANGEMENT; STRUCTURE AND DYNAMICS; TWO-DIMENSIONAL INFRARED SPECTROSCOPY; VIBRATIONAL EXCITATION; VIBRATIONAL RELAXATION;

METALS;

COPPER; ENZYME; HISTIDINE; IMIDAZOLE; METALLOENZYME; UNCLASSIFIED DRUG; CARBON; CARBON MONOXIDE; METALLOPROTEIN; NITRITE REDUCTASE; NITRITE REDUCTASE, COPPER-CONTAINING; OXYGEN; PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL MODEL; DIELECTRIC CONSTANT; DIPOLE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; EXCITATION; HYDROGEN BOND; INFRARED SPECTROSCOPY; LIGAND BINDING; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; STATIC ELECTRICITY; SURFACE PROPERTY; ULTRAFAST TWO DIMENSIONAL INFRARED SPECTROSCOPY; VIBRATION; CHEMISTRY; INFRARED SPECTROPHOTOMETRY; METABOLISM; PROCEDURES;

CARBON; CARBON MONOXIDE; CATALYTIC DOMAIN; COPPER; ENZYMES; HISTIDINE; METALLOPROTEINS; MODELS, CHEMICAL; NITRITE REDUCTASES; OXYGEN; PEPTIDES; SPECTROPHOTOMETRY, INFRARED; STATIC ELECTRICITY;

EID: 84939826172     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.5b02840     Document Type: Article

References (105)

1. Yu, F.; Cangelosi, V. M.; Zastrow, M. L.; Tegoni, M.; Plegaria, J. S.; Tebo, A. G.; Mocny, C. S.; Ruckthong, L.; Qayyum, H.; Pecoraro, V. L. Chem. Rev. 2014, 114, 3495-3578 10.1021/cr400458x
2. Zastrow, M. L.; Peacock, A. F. A.; Stuckey, J. A.; Pecoraro, V. L. Nat. Chem. 2011, 4, 118-123 10.1038/nchem.1201
3. Tegoni, M.; Yu, F. T.; Bersellini, M.; Penner-Hahn, J. E.; Pecoraro, V. L. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 21234-21239 10.1073/pnas.1212893110
4. Yu, F. T.; Penner-Hahn, J. E.; Pecoraro, V. L. J. Am. Chem. Soc. 2013, 135, 18096-18107 10.1021/ja406648n
5. Warshel, A.; Sharma, P. K.; Kato, M.; Xiang, Y.; Liu, H.; Olsson, M. H. M. Chem. Rev. 2006, 106, 3210-3235 10.1021/cr0503106
6. Warshel, A. Proc. Natl. Acad. Sci. U. S. A. 1978, 75, 5250-5254 10.1073/pnas.75.11.5250
7. Warshel, A. Proc. Natl. Acad. Sci. U. S. A. 1984, 81, 444-448 10.1073/pnas.81.2.444
8. Brooks, C. L.; Karplus, M. J. Mol. Biol. 1989, 208, 159-181 10.1016/0022-2836(89)90093-4
9. Karplus, M.; Kuriyan, J. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 6679-6685 10.1073/pnas.0408930102
10. Hanggi, P.; Talkner, P.; Borkovec, M. Rev. Mod. Phys. 1990, 62, 251-341 10.1103/RevModPhys.62.251
11. Hynes, J. T. Annu. Rev. Phys. Chem. 1985, 36, 573-597 10.1146/annurev.pc.36.100185.003041
12. Berne, B. J.; Borkovec, M.; Straub, J. E. J. Phys. Chem. 1988, 92, 3711-3725 10.1021/j100324a007
13. Zwanzig, R. Acc. Chem. Res. 1990, 23, 148-152 10.1021/ar00173a005
14. Hanggi, P.; Talkner, P.; Borkovec, M. Rev. Mod. Phys. 1990, 62, 251-341 10.1103/RevModPhys.62.251
15. Karplus, M.; McCammon, J. A. Annu. Rev. Biochem. 1983, 52, 263-300 10.1146/annurev.bi.52.070183.001403
16. Olsson, M. H. M.; Parson, W. W.; Warshel, A. Chem. Rev. 2006, 106, 1737-1756 10.1021/cr040427e
17. Fried, S. D.; Bagchi, S.; Boxer, S. G. Science 2014, 346, 1510-1514 10.1126/science.1259802
18. Shurki, A.; Warshel, A. Protein Simulations 2003, 66, 249-313 10.1016/S0065-3233(03)66007-9
19. Solomon, E. I.; Szilagyi, R. K.; George, S. D.; Basumallick, L. Chem. Rev. 2004, 104, 419-458 10.1021/cr0206317
20. Zwanzig, R. J. Chem. Phys. 1992, 97, 3587-3589 10.1063/1.462993
21. Min, W.; English, B. P.; Luo, G. B.; Cherayil, B. J.; Kou, S. C.; Xie, X. S. Acc. Chem. Res. 2005, 38, 923-931 10.1021/ar040133f
22. Minton, A. P. J. Biol. Chem. 2001, 276, 10577-10580 10.1074/jbc.R100005200
23. Hamm, P.; Zanni, M. T. Concepts and Methods of 2D Infrared Spectroscopy; Cambridge University Press: New York, 2011.
24. Fager, L. Y.; Alben, J. O. Biochemistry 1972, 11, 4786-4792 10.1021/bi00775a023
25. Treuffet, J.; Kubarych, K. J.; Lambry, J. C.; Pilet, E.; Masson, J. B.; Martin, J. L.; Vos, M. H.; Joffre, M.; Alexandrou, A. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 15705-15710 10.1073/pnas.0703279104
26. Lemon, D. D.; Calhoun, M. W.; Gennis, R. B.; Woodruff, W. H. Biochemistry 1993, 32, 11953-11956 10.1021/bi00096a002
27. Lim, M. H.; Hamm, P.; Hochstrasser, R. M. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 15315-15320 10.1073/pnas.95.26.15315
28. Lim, M.; Jackson, T. A.; Anfinrud, P. A. Science 1995, 269, 962-966 10.1126/science.7638619
29. Ray, G. B.; Li, X. Y.; Ibers, J. A.; Sessler, J. L.; Spiro, T. G. J. Am. Chem. Soc. 1994, 116, 162-176 10.1021/ja00080a019
30. Li, T. S.; Quillin, M. L.; Phillips, G. N.; Olson, J. S. Biochemistry 1994, 33, 1433-1446 10.1021/bi00172a021
31. Spiro, T. G.; Wasbotten, I. H. J. Inorg. Biochem. 2005, 99, 34-44 10.1016/j.jinorgbio.2004.09.026
32. Ghosh, D.; Pecoraro, V. L. Inorg. Chem. 2004, 43, 7902-7915 10.1021/ic048939z
33. Dill, K. A.; Bromberg, S.; Yue, K. Z.; Fiebig, K. M.; Yee, D. P.; Thomas, P. D.; Chan, H. S. Protein Sci. 1995, 4, 561-602 10.1002/pro.5560040401
34. Berne, B. J.; Weeks, J. D.; Zhou, R. H. Annu. Rev. Phys. Chem. 2009, 60, 85-103 10.1146/annurev.physchem.58.032806.104445
35. Agashe, V. R.; Shastry, M. C. R.; Udgaonkar, J. B. Nature 1995, 377, 754-757 10.1038/377754a0
36. Gutin, A. M.; Abkevich, V. I.; Shakhnovich, E. I. Biochemistry 1995, 34, 3066-3076 10.1021/bi00009a038
37. Dieckmann, G. R.; McRorie, D. K.; Tierney, D. L.; Utschig, L. M.; Singer, C. P.; OHalloran, T. V.; PennerHahn, J. E.; DeGrado, W. F.; Pecoraro, V. L. J. Am. Chem. Soc. 1997, 119, 6195-6196 10.1021/ja964351i
38. Dieckmann, G. R.; McRorie, D. K.; Lear, J. D.; Sharp, K. A.; DeGrado, W. F.; Pecoraro, V. L. J. Mol. Biol. 1998, 280, 897-912 10.1006/jmbi.1998.1891
39. FMOC Solid Phase Peptide Synthesis, A Practical Approach; Chang, W. C.; White, P. D., Eds.; Oxford University Press Inc.: New York, 2000; Vol. 222.
40. Farrer, B. T.; Harris, N. P.; Balchus, K. E.; Pecoraro, V. L. Biochemistry 2001, 40, 14696-14705 10.1021/bi015649a
41. Zastrow, M. L.; Pecoraro, V. L. J. Am. Chem. Soc. 2013, 135, 5895-5903 10.1021/ja401537t
42. Baiz, C. R.; Mcrobbie, P. L.; Anna, J. M.; Geva, E.; Kubarych, K. J. Acc. Chem. Res. 2009, 42, 1395-1404 10.1021/ar9000263
43. Christen, D.; Griffiths, J. H.; Sheridan, J. Z. Naturforsch., A: Phys. Sci. 1981, 36, 1378-1385 10.1515/zna-1981-1220
44. Aqvist, J.; Luecke, H.; Quiocho, F. A.; Warshel, A. Proc. Natl. Acad. Sci. U. S. A. 1991, 88, 2026-2030 10.1073/pnas.88.5.2026
45. Kwak, K.; Rosenfeld, D.; Fayer, M. J. Chem. Phys. 2008, 128, 204505 10.1063/1.2927906
46. Lazonder, K.; Pshenichnikov, M.; Wiersma, D. Opt. Lett. 2006, 31, 3354-3356 10.1364/OL.31.003354
47. Roberts, S.; Loparo, J.; Tokmakoff, A. J. Chem. Phys. 2006, 125, 084502 10.1063/1.2232271
48. Hybl, J.; Christophe, Y.; Jonas, D. Chem. Phys. 2001, 266, 295-309 10.1016/S0301-0104(01)00233-6
49. King, J. T.; Arthur, E. J.; Brooks, C. L.; Kubarych, K. J. J. Am. Chem. Soc. 2014, 136, 188-194 10.1021/ja407858c
50. King, J. T.; Kubarych, K. J. J. Am. Chem. Soc. 2012, 134, 18705-18712 10.1021/ja307401r
51. Bagchi, S.; Nebgen, B. T.; Loring, R. F.; Fayer, M. D. J. Am. Chem. Soc. 2010, 132, 18367-18376 10.1021/ja108491t
52. Dixon, N. A.; McQuarters, A. B.; Kraus, J. S.; Soffer, J. B.; Lehnert, N.; Schweitzer-Stenner, R.; Papish, E. T. Chem. Commun. 2013, 49, 5571-5573 10.1039/c3cc00036b
53. Faeder, S.; Jonas, D. J. Phys. Chem. A 1999, 103, 10489-10505 10.1021/jp9925738
54. Kwak, K.; Park, S.; Finkelstein, I.; Fayer, M. J. Chem. Phys. 2007, 127, 124503 10.1063/1.2772269
55. Gaffney, K.; Davis, P.; Piletic, I.; Levinger, N.; Fayer, M. J. Phys. Chem. A 2002, 106, 12012-12023 10.1021/jp021696g
56. Huse, N.; Bruner, B. D.; Cowan, M. L.; Dreyer, J.; Nibbering, E. T. J.; Miller, R. J. D.; Elsaesser, T. Phys. Rev. Lett. 2005, 95, 147402 10.1103/PhysRevLett.95.147402
57. Samanta, A. J. Phys. Chem. B 2006, 110, 13704-13716 10.1021/jp060441q
58. Castner, E.; Maroncelli, M. J. Mol. Liq. 1998, 77, 1-36 10.1016/S0167-7322(98)00066-X
59. Stratt, R.; Maroncelli, M. J. Phys. Chem. 1996, 100, 12981-12996 10.1021/jp9608483
60. Maroncelli, M. J. Mol. Liq. 1993, 57, 1-37 10.1016/0167-7322(93)80045-W
61. Baiz, C. R.; Kubarych, K. J.; Geva, E.; Sibert, E. L. J. Phys. Chem. A 2011, 115, 5354-5363 10.1021/jp201641h
62. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M. J.; Heyd, J.; Brothers, E. N.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A. P.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N. J.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09; Gaussian, Inc.: Wallingford, CT, 2009.
63. Dapprich, S.; Komaromi, I.; Byun, K. S.; Morokuma, K.; Frisch, M. J. J. Mol. Struct.: THEOCHEM 1999, 461, 1-21 10.1016/S0166-1280(98)00475-8
64. Vreven, T.; Morokuma, K.; Farkas, O.; Schlegel, H. B.; Frisch, M. J. J. Comput. Chem. 2003, 24, 760-769 10.1002/jcc.10156
65. Vreven, T.; Byun, K. S.; Komaromi, I.; Dapprich, S.; Montgomery, J. A.; Morokuma, K.; Frisch, M. J. J. Chem. Theory Comput. 2006, 2, 815-826 10.1021/ct050289g
66. Finkelstein, I.; Goj, A.; McClain, B.; Massari, A.; Merchant, K.; Loring, R.; Fayer, M. J. Phys. Chem. B 2005, 109, 16959-16966 10.1021/jp0517201
67. McClain, B.; Finkelstein, I.; Fayer, M. J. Am. Chem. Soc. 2004, 126, 15702-15710 10.1021/ja0454790
68. McClain, B.; Finkelstein, I.; Fayer, M. Chem. Phys. Lett. 2004, 392, 324-329 10.1016/j.cplett.2004.05.080
69. Merchant, K.; Noid, W.; Akiyama, R.; Finkelstein, I.; Goun, A.; McClain, B.; Loring, R.; Fayer, M. J. Am. Chem. Soc. 2003, 125, 13804-13818 10.1021/ja035654x
70. Merchant, K.; Thompson, D.; Xu, Q.; Williams, R.; Loring, R.; Fayer, M. Biophys. J. 2002, 82, 3277-3288 10.1016/S0006-3495(02)75669-5
71. Falvo, C.; Daniault, L.; Vieille, T.; Kemlin, V.; Lambry, J.-C.; Meier, C.; Vos, M. H.; Bonvalet, A.; Joffre, M. J. Phys. Chem. Lett. 2015, 6, 2216-2222 10.1021/acs.jpclett.5b00811
72. Choi, J.-H.; Kwak, K.-W.; Cho, M. J. Phys. Chem. B 2013, 117, 15462-15478 10.1021/jp405210s
73. Ishikawa, H.; Kwak, K.; Chung, J.; Kim, S.; Fayer, M. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 8619-8624 10.1073/pnas.0803764105
74. Auer, B. M.; Skinner, J. L. J. Chem. Phys. 2008, 128, 224511 10.1063/1.2925258
75. Hayashi, T.; Jansen, T. L.; Zhuang, W.; Mukamel, S. J. Phys. Chem. A 2005, 109, 64-82 10.1021/jp046685x
76. Hayashi, T.; Zhuang, W.; Mukamel, S. J. Phys. Chem. A 2005, 109, 9747-9759 10.1021/jp052324l
77. Lin, Y. S.; Shorb, J. M.; Mukherjee, P.; Zanni, M. T.; Skinner, J. L. J. Phys. Chem. B 2009, 113, 592-602 10.1021/jp807528q
78. Wang, L.; Middleton, C. T.; Zanni, M. T.; Skinner, J. L. J. Phys. Chem. B 2011, 115, 3713-3724 10.1021/jp200745r
79. Zhuang, W.; Abramavicius, D.; Hayashi, T.; Mukamel, S. J. Phys. Chem. B 2006, 110, 3362-3374 10.1021/jp055813u
80. Falvo, C.; Meier, C. J. Chem. Phys. 2011, 134, 214106 10.1063/1.3592707
81. Asbury, J.; Steinel, T.; Fayer, M. J. Lumin. 2004, 107, 271-286 10.1016/j.jlumin.2003.12.035
82. Gaffney, K.; Piletic, I.; Fayer, M. J. Chem. Phys. 2003, 118, 2270-2278 10.1063/1.1534580
83. Levinger, N.; Davis, P.; Fayer, M. J. Chem. Phys. 2001, 115, 9352-9360 10.1063/1.1415447
84. Piletic, I.; Gaffney, K.; Fayer, M. J. Chem. Phys. 2003, 119, 423-434 10.1063/1.1578058
85. Kwac, K.; Geva, E. J. Phys. Chem. B 2011, 115, 9184-9194 10.1021/jp204245z
86. Kwac, K.; Geva, E. J. Phys. Chem. B 2012, 116, 2856-2866 10.1021/jp211792j
87. Dwyer, J.; Dreyer, J.; Nibbering, E.; Elsaesser, T. Chem. Phys. Lett. 2006, 432, 146-151 10.1016/j.cplett.2006.10.084
88. Elsaesser, T.; Huse, N.; Dreyer, J.; Dwyer, J.; Heyne, K.; Nibbering, E. Chem. Phys. 2007, 341, 175-188 10.1016/j.chemphys.2007.06.036
89. Heyne, K.; Huse, N.; Dreyer, J.; Nibbering, E.; Elsaesser, T.; Mukamel, S. J. Chem. Phys. 2004, 121, 902-913 10.1063/1.1762873
90. Heyne, K.; Huse, N.; Nibbering, E.; Elsaesser, T. Chem. Phys. Lett. 2003, 369, 591-596 10.1016/S0009-2614(03)00023-X
91. Heyne, K.; Huse, N.; Nibbering, E.; Elsaesser, T. J. Phys.: Condens. Matter 2003, 15, S129-S136 10.1088/0953-8984/15/1/316
92. Heyne, K.; Huse, N.; Nibbering, E.; Elsaesser, T. Chem. Phys. Lett. 2003, 382, 19-25 10.1016/j.cplett.2003.09.145
93. Baker, N. A.; Sept, D.; Joseph, S.; Holst, M. J.; McCammon, J. A. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 10037-10041 10.1073/pnas.181342398
94. Sundberg, R. J.; Martin, R. B. Chem. Rev. 1974, 74, 471-517 10.1021/cr60290a003
95. Tipmanee, V.; Blumberger, J. J. Phys. Chem. B 2012, 116, 1876-1883 10.1021/jp209175j
96. Schmiedekamp, A.; Nanda, V. J. Inorg. Biochem. 2009, 103, 1054-1060 10.1016/j.jinorgbio.2009.04.017
97. Horowitz, S.; Trievel, R. C. J. Biol. Chem. 2012, 287, 41576-41582 10.1074/jbc.R112.418574
98. Karlin, K. D.; Dahlstrom, P. L.; Dipierro, L. T.; Simon, R. A.; Zubieta, J. J. Coord. Chem. 1981, 11, 61-63 10.1080/00958978108080668
99. Moore, J. N.; Hansen, P. A.; Hochstrasser, R. M. Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 5062-5066 10.1073/pnas.85.14.5062
100. Spiro, T. G.; Kozlowski, P. M. Acc. Chem. Res. 2001, 34, 137-144 10.1021/ar000108j
101. Spiro, T. G.; Kozlowski, P. M. J. Am. Chem. Soc. 1998, 120, 4524-4525 10.1021/ja9732946
102. Gordon, R. G. Adv. Magn. Reson. 1968, 3, 1-42
103. Morse, P. M. Phys. Rev. 1929, 34, 57-64 10.1103/PhysRev.34.57
104. Sage, J. T.; Zhang, Y.; McGeehan, J.; Ravelli, R. B. G.; Weik, M.; van Thor, J. J. Biochim. Biophys. Acta, Proteins Proteomics 2011, 1814, 760-777 10.1016/j.bbapap.2011.02.012
105. Kraack, J. P.; Lotti, D.; Hamm, P. J. Phys. Chem. Lett. 2014, 5, 2325-2329 10.1021/jz500978z