Ligand dynamics in heme proteins observed by Fourier transform infrared-temperature derivative spectroscopy

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 8, 2011, Pages 1030-1041

  Nienhaus, Karin ^a   Nienhaus, G Ulrich ^a,b  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

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

Author keywords

Fourier transform infrared spectroscopy; Heme protein; Ligand binding; Ligand migration; Photolysis difference spectroscopy; Temperature derivative spectroscopy

Indexed keywords

CARBON MONOXIDE; DEHALOPEROXIDASE; HEMOGLOBIN; HEMOGLOBIN I; HEMOPROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; MYOGLOBIN; NEUROGLOBIN; NITRIC OXIDE; NITROPHORIN 4; OXYGEN; UNCLASSIFIED DRUG;

ARABIDOPSIS; CEREBRATULUS LACTEUS; ELECTRIC FIELD; ENZYME SUBSTRATE COMPLEX; HUMAN; INFRARED SPECTROSCOPY; LIGAND BINDING; MOLECULAR DOCKING; NEMERTEA; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; REVIEW; SCAPHARCA; SPECTROSCOPY; TEMPERATURE DERIVATIVE SPECTROSCOPY;

CATALYTIC DOMAIN; COLD TEMPERATURE; HEMEPROTEINS; LIGANDS; MODELS, MOLECULAR; REPRODUCIBILITY OF RESULTS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 79958775057     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.07.018     Document Type: Review

References (122)

1. J.C. Kendrew, R.E. Dickerson, B.E. Strandberg, R.G. Hart, D.R. Davies, D.R. Phillips, D.C. Phillips, V.C. Shore, Structure of myoglobin: a three-dimensional Fourier synthesis at 2 A resolution, Nature 185 (1960) 422-427.
2. Q.H. Gibson, S. Ainsworth, Photosensitivity of haem compounds, Nature 180 (1957) 1416-1417.
3. M. Brunori, J. Bonaventura, C. Bonaventura, E. Antonini, J. Wyman, Carbon monoxide binding by hemoglobin and myoglobin under photodissociating conditions, Proc. Natl Acad. Sci. USA 69 (1972) 868-871.
4. R.H. Austin, K.W. Beeson, L. Eisenstein, H. Frauenfelder, I.C. Gunsalus, Dynamics of ligand binding to myoglobin, Biochemistry 14 (1975) 5355-5373.
5. B.H. McMahon, B.P. Stojkovic, P.J. Hay, R.L. Martin, A.E. García, Microscopic model of carbon monoxide binding to myoglobin, J. Chem. Phys. 113 (2000) 6831-6850.
6. J.M. Kriegl, A.J. Bhattacharyya, K. Nienhaus, P. Deng, O. Minkow, G.U. Nienhaus, Ligand binding and protein dynamics in neuroglobin, Proc. Natl Acad. Sci. USA 99 (2002) 7992-7997. (Pubitemid 34650993)
7. 2 affinity in cerebratulus lacteus mini-hemoglobin, J. Biol. Chem. 279 (2004) 33662-33672.
8. K. Nienhaus, P. Deng, J. Belyea, S. Franzen, G.U. Nienhaus, Spectroscopic study of substrate binding to the carbonmonoxy form of dehaloperoxidase from Amphitrite ornata, J. Phys. Chem. B 110 (2006) 13264-13276.
9. D. Ehrenstein, G.U. Nienhaus, Conformational substates in azurin, Proc. Natl Acad. Sci. USA 89 (1992) 9681-9685.
10. B.H. McMahon, J.D. Muller, C.A. Wraight, G.U. Nienhaus, Electron transfer and protein dynamics in the photosynthetic reaction center, Biophys. J. 74 (1998) 2567-2587. (Pubitemid 28225252)
11. F. Parak, J. Heidemeier, G.U. Nienhaus, Protein structural dynamics as determined by Mössbauer spectroscopy, Hyperfine Interact. 40 (1988) 147-158.
12. H. Frauenfelder, G.U. Nienhaus, J.B. Johnson, Rate processes in proteins, Ber. Bunsenges. Phys. Chem. 95 (1991) 272-278.
13. G.U. Nienhaus, J. Heinzl, E. Huenges, F. Parak, Protein crystal dynamics studied by time-resolved analysis of X-ray diffuse scattering, Nature 338 (1989) 665-666.
14. E.R. Henry, J.H. Sommer, J. Hofrichter, W.A. Eaton, Geminate recombination of carbon monoxide to myoglobin, J. Mol. Biol. 166 (1983) 443-451.
15. N. Agmon, J.J. Hopfield, CO binding to heme proteins: a model for barrier height distributions and slow conformational changes, J. Chem. Phys. 79 (1983) 2042-2053.
16. L. Powers, J.L. Sessler, G.L. Woolery, B. Chance, CO bond angle changes in photolysis of carboxymyoglobin, Biochemistry 23 (1984) 5519.
17. B. Chance, L. Powers, Y.-H. Zhou, A. Naqui, Bull. Am. Phys. Soc. 31 (1986) 386.
18. A. Ansari, J. Berendzen, D. Braunstein, B.R. Cowen, H. Frauenfelder, M.K. Hong, I.E. Iben, J.B. Johnson, P. Ormos, T.B. Sauke, et al., Rebinding and relaxation in the myoglobin pocket, Biophys. Chem. 26 (1987) 337-355.
19. V. Srajer, L. Reinisch, P.M. Champion, Investigation of laser-induced long-lived states of photolyzed MbCO, Biochemistry 30 (1991) 4886-4895.
20. P.J. Steinbach, A. Ansari, J. Berendzen, D. Braunstein, K. Chu, B.R. Cowen, D. Ehrenstein, H. Frauenfelder, J.B. Johnson, D.C. Lamb, S. Luck, J.R. Mourant, G.U. Nienhaus, P. Ormos, R. Philipp, A. Xie, R.D. Young, Ligand binding to heme proteins: connection between dynamics and function, Biochemistry 30 (1991) 3988-4001.
21. G.U. Nienhaus, J.R. Mourant, H. Frauenfelder, Spectroscopic evidence for conformational relaxation in myoglobin, Proc. Natl Acad. Sci. USA 89 (1992) 2902-2906.
22. G.U. Nienhaus, J.R. Mourant, K. Chu, H. Frauenfelder, Ligand binding to heme proteins: the effect of light on ligand binding in myoglobin, Biochemistry 33 (1994) 13413-13430. (Pubitemid 24373258)
23. H. Hartmann, S. Zinser, P. Komninos, R.T. Schneider, G.U. Nienhaus, F. Parak, X-ray structure determination of a metastable state of carbonmonoxy myoglobin after photodissociation, Proc. Natl Acad. Sci. USA 93 (1996) 7013-7016. (Pubitemid 26243492)
24. T.Y. Teng, V. Srajer, K. Moffat, Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K, Nat. Struct. Biol. 1 (1994) 701-705.
25. I. Schlichting, J. Berendzen, G.N. Phillips Jr., R.M. Sweet, Crystal structure of photolysed carbonmonoxy-myoglobin, Nature 371 (1994) 808-812. (Pubitemid 24333871)
26. V. Srajer, T. Teng, T. Ursby, C. Pradervand, Z. Ren, S. Adachi, W. Schildkamp, D. Bourgeois, M. Wulff, K. Moffat, Photolysis of the carbon monoxide complex of myoglobin: nanosecond time-resolved crystallography, Science 274 (1996) 1726-1729. (Pubitemid 26414908)
27. D.P. Braunstein, K. Chu, K.D. Egeberg, H. Frauenfelder, J.R. Mourant, G.U. Nienhaus, P. Ormos, S.G. Sligar, B.A. Springer, R.D. Young, Ligand binding to heme proteins: III. FTIR studies of His-E7 and Val-E11 mutants of carbonmonoxymyoglobin, Biophys. J. 65 (1993) 2447-2454.
28. J.O. Alben, D. Beece, S.F. Bowne, W. Doster, L. Eisenstein, H. Frauenfelder, D. Good, J.D. McDonald, M.C. Marden, P.P. Moh, L. Reinisch, A.H. Reynolds, E. Shyamsunder, K.T. Yue, Infrared spectroscopy of photodissociated carboxymyoglobin at low temperatures, Proc. Natl Acad. Sci. USA 79 (1982) 3744-3748. (Pubitemid 12013542)
29. M. Lim, T.A. Jackson, P.A. Anfinrud, Binding of CO to myoglobin froma heme pocket docking site to form nearly linear Fe-C-O, Science 269 (1995) 962-966.
30. M. Lim, T.A. Jackson, P.A. Anfinrud, Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin, Nat. Struct. Biol. 4 (1997) 209-214. (Pubitemid 27111167)
31. E.E. Scott, Q.H. Gibson, Ligand migration in sperm whale myoglobin, Biochemistry 36 (1997) 11909-11917. (Pubitemid 27424119)
32. R.F. Tilton Jr., I.D. Kuntz Jr., G.A. Petsko, Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 Å, Biochemistry 23 (1984) 2849-2857.
33. G.U. Nienhaus, K. Chu, K. Jesse, Structural heterogeneity and ligand binding in carbonmonoxy myoglobin crystals at cryogenic temperatures, Biochemistry 37 (1998) 6819-6823. (Pubitemid 28228117)
34. A. Ostermann, R. Waschipky, F.G. Parak, G.U. Nienhaus, Ligand binding and conformational motions in myoglobin, Nature 404 (2000) 205-208. (Pubitemid 30154491)
35. K. Chu, J. Vojtechovsky, B.H. McMahon, R.M. Sweet, J. Berendzen, I. Schlichting, Structure of a ligand-binding intermediate in wild-type carbonmonoxy myoglobin, Nature 403 (2000) 921-923. (Pubitemid 30130998)
36. M. Brunori, Structural dynamics ofmyoglobin, Biophys. Chem. 86 (2000) 221-230.
37. M. Brunori, B. Vallone, F. Cutruzzola, C. Travaglini-Allocatelli, J. Berendzen, K. Chu, R.M. Sweet, I. Schlichting, The role of cavities in protein dynamics: crystal structure of a photolytic intermediate of a mutant myoglobin, Proc. Natl Acad. Sci. USA 97 (2000) 2058-2063. (Pubitemid 30134021)
38. G.U. Nienhaus, K. Nienhaus, Infrared study of carbon monoxide migration among internal cavities of myoglobin mutant L29W, J. Biol. Phys. 28 (2002) 163-172.
39. M. Schmidt, K. Nienhaus, R. Pahl, A. Krasselt, S. Anderson, F. Parak, G.U. Nienhaus, V. Srajer, Ligand migration pathway and protein dynamics in myoglobin: a time-resolved crystallographic study on L29W MbCO, Proc. Natl Acad. Sci. USA 102 (2005) 11704-11709. (Pubitemid 41170790)
40. F. Schotte, M. Lim, T.A. Jackson, A.V. Smirnov, J. Soman, J.S. Olson, G.N. Phillips Jr., M. Wulff, P.A. Anfinrud, Watching a protein as it functions with 150-ps time-resolved x-ray crystallography, Science 300 (2003) 1944-1947. (Pubitemid 36734600)
41. G. Hummer, F. Schotte, P.A. Anfinrud, Unveiling functional protein motions with picosecond x-ray crystallography and molecular dynamics simulations, Proc. Natl Acad. Sci. USA 101 (2004) 15330-15334. (Pubitemid 39441541)
42. D. Bourgeois, B. Vallone, F. Schotte, A. Arcovito, A.E. Miele, G. Sciara, M. Wulff, P. Anfinrud, M. Brunori, Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography, Proc. Natl Acad. Sci. USA 100 (2003) 8704-8709. (Pubitemid 36899162)
43. V. Srajer, Z. Ren, T.Y. Teng, M. Schmidt, T. Ursby, D. Bourgeois, C. Pradervand, W. Schildkamp, M. Wulff, K. Moffat, Protein conformational relaxation and ligand migration in myoglobin: a nanosecond to millisecond molecular movie from time-resolved Laue x-ray diffraction, Biochemistry 40 (2001) 13802-13815. (Pubitemid 33078849)
44. X. Huang, S.G. Boxer, Discovery of new ligand binding pathways in myoglobin by random mutagenesis, Nat. Struct. Biol. 1 (1994) 226-229.
45. M.F. Perutz, F.S. Mathews, An x-ray study of azide methaemoglobin, J. Mol. Biol. (1966) 199-202.
46. R.F. Tilton Jr., U.C. Singh, I.D. Kuntz Jr., P.A. Kollman, Protein-ligand dynamics. A 96 picosecond simulation of a myoglobin-xenon complex, J. Mol. Biol. 199 (1988) 195-211.
47. R. Elber, M. Karplus, Enhanced sampling in molecular dynamics: use of the time-dependent Hartree approximation for a simulation of carbon monoxide diffusion through myoglobin, J. Am. Chem. Soc. 112 (1990) 9161-9175.
48. 2 entry into and exit from myoglobin, J. Biol. Chem. 276 (2001) 5177-5188.
49. A. Dong, W.S. Caughey, Infrared methods for study of hemoglobin reactions and structures, Methods. Enzymol. 232 (1994) 139-175.
50. K. Gerwert, Molecular recognition mechanisms of proteins as monitored by time-resolved FTIR spectroscopy, Curr. Opin. Struct. Biol. 3 (1993) 769-773. (Pubitemid 23295586)
51. W. Mäntele, Reaction-induced infrared difference spectroscopy for the study of protein function and reaction mechanisms, Trends Biochem. Sci. 18 (1993) 197-202.
52. J.B. Johnson, D.C. Lamb, H. Frauenfelder, J.D. Müller, B. McMahon, G.U. Nienhaus, R.D. Young, Ligand binding to heme proteins. VI. Interconversion of taxonomic substates in carbonmonoxymyoglobin, Biophys. J. 71 (1996) 1563-1573. (Pubitemid 26299794)
53. J. Bredenbeck, J. Helbing, K. Nienhaus, G.U. Nienhaus, P. Hamm, Protein ligand migration mapped by nonequilibrium 2D-IR exchange spectroscopy, Proc. Natl Acad. Sci. USA 104 (2007) 14243-14248. (Pubitemid 350003247)
54. J. Helbing, K. Nienhaus, G.U. Nienhaus, P. Hamm, Restricted rotational motion of CO in a protein internal cavity: evidence for nonseparating correlation functions from IR pump-probe spectroscopy, J. Chem. Phys. 122 (2005) 124505.
55. N. Alberding, R.H. Austin, K.W. Beeson, S.S. Chan, L. Eisenstein, H. Frauenfelder, T. M. Nordlund, Tunneling in ligand binding to heme proteins, Science 192 (1976) 1002-1004.
56. J.O. Alben, D. Beece, S.F. Bowne, L. Eisenstein, H. Frauenfelder, D. Good, M. Marden, P.P. Moh, L. Reinisch, A.H. Reynolds, K.T. Yue, Isotope effect in molecular tunneling, Phys. Rev. Lett. 44 (1980) 1157-1160.
57. K. Nienhaus, P. Deng, J.M. Kriegl, G.U. Nienhaus, Structural dynamics of myoglobin: the effect of internal cavities on ligand migration and binding, Biochemistry 42 (2003) 9647-9658. (Pubitemid 36993137)
58. K. Nienhaus, P. Deng, J.M. Kriegl, G.U. Nienhaus, Structural dynamics of myoglobin: spectroscopic and structural characterization of ligand docking sites in myoglobin mutant L29W, Biochemistry 42 (2003) 9633-9646. (Pubitemid 36993136)
59. K. Nienhaus, P. Deng, J.S. Olson, J.J. Warren, G.U. Nienhaus, Structural dynamics of myoglobin: ligand migration and binding in valine 68 mutants, J. Biol. Chem. 278 (2003) 42532-42544.
60. J. Berendzen, D. Braunstein, Temperature-derivative spectroscopy: a tool for protein dynamics, Proc. Natl Acad. Sci. USA 87 (1990) 1-5.
61. K. Chu, R.M. Ernst, H. Frauenfelder, J.R. Mourant, G.U. Nienhaus, R. Philipp, Light-induced and thermal relaxation in a protein, Phys. Rev. Lett. 74 (1995) 2607-2610.
62. J.M. Kriegl, K. Nienhaus, P. Deng, J. Fuchs, G.U. Nienhaus, Ligand dynamics in a protein internal cavity, Proc. Natl Acad. Sci. USA 100 (2003) 7069-7074. (Pubitemid 36706394)
63. S. McCoy, W. Caughey, Infrared studies of azido, cyano, and other derivatives of metmyoglobin, methemoglobin, and hemins, Biochemistry 9 (1970) 2387-2393.
64. M.W. Makinen, R.A. Houtchens, W.S. Caughey, Structure of carboxymyoglobin in crystals and in solution, Proc. Natl Acad. Sci. USA 76 (1979) 6042-6046.
65. H. Frauenfelder, S.G. Sligar, P.G. Wolynes, The energy landscapes and motions of proteins, Science 254 (1991) 1598-1603. (Pubitemid 21917496)
66. T. Li,M.L. Quillin, G.N. Phillips Jr., J.S. Olson, Structural determinants of the stretching frequency of CO bound to myoglobin, Biochemistry 33 (1994) 1433-1446. (Pubitemid 24093691)
67. J.D. Müller, B.H. McMahon, E.Y. Chien, S.G. Sligar, G.U. Nienhaus, Connection between the taxonomic substates and protonation of histidines 64 and 97 in carbonmonoxy myoglobin, Biophys. J. 77 (1999) 1036-1051. (Pubitemid 29362474)
68. B. Kushkuley, S.S. Stavrov, Theoretical study of the distal-side steric and electrostatic effects on the vibrational characteristics of the FeCO unit of the carbonylheme proteins and their models, Biophys. J. 70 (1996) 1214-1229. (Pubitemid 26073036)
69. B. Kushkuley, S.S. Stavrov, Theoretical study of the electrostatic and steric effects on the spectroscopic characteristics of the metal-ligand unit of heme proteins. 2. C-O vibrational frequencies, 17O isotropic chemical shifts, and nuclear quadrupole coupling constants, Biophys. J. 72 (1997) 899-912.
70. F. Yang, G.N. Phillips Jr., Crystal structures of CO-, deoxy- and met-myoglobins at various pH values, J. Mol. Biol. 256 (1996) 762-774. (Pubitemid 26108816)
71. M.L. Quillin, R.M. Arduini, J.S. Olson, G.N. Phillips Jr., High-resolution crystal structures of distal histidine mutants of sperm whale myoglobin, J. Mol. Biol. 234 (1993) 140-155.
72. J. Vojtechovsky, K. Chu, J. Berendzen, R.M. Sweet, I. Schlichting, Crystal structures of myoglobin-ligand complexes at near-atomic resolution, Biophys. J. 77 (1999) 2153-2174. (Pubitemid 29463176)
73. C. Tetreau, E. Novikov, M. Tourbez, D. Lavalette, Kinetic evidence for three photolyzable taxonomic conformational substates in oxymyoglobin, Biophys. J. 82 (2002) 2148-2155. (Pubitemid 34280827)
74. K. Nienhaus, P. Palladino, G.U. Nienhaus, Structural dynamics of myoglobin: FTIR-TDS study of NO migration and binding, Biochemistry 47 (2008) 935-948. (Pubitemid 351147799)
75. K. Nienhaus, G.U. Nienhaus, Ligand dynamics in heme proteins observed by Fourier transform infrared spectroscopy at cryogenic temperatures, Methods Enzymol. 437 (2008) 347-378.
76. 2O to ferrous sperm whale myoglobin, J. Am. Chem. Soc. 120 (1998) 2981-2982.
77. K. Nienhaus, J.S. Olson, S. Franzen, G.U. Nienhaus The, Origin of Stark splitting in the initial photoproduct state of MbCO, J. Am. Chem. Soc. 127 (2005) 40-41. (Pubitemid 40094354)
78. J.R. Mourant, D.P. Braunstein, K. Chu, H. Frauenfelder, G.U. Nienhaus, P. Ormos, R. D. Young, Ligand binding to heme proteins: II. Transitions in the heme pocket of myoglobin, Biophys. J. 65 (1993) 1496-1507.
79. B.F. Campbell, M.R. Chance, J.M. Friedman, Linkage of functional and structural heterogeneity in proteins: dynamic hole burning in carboxymyoglobin, Science 238 (1987) 373-376. (Pubitemid 17151731)
80. P. Ormos, S. Szaraz, A. Cupane, G.U. Nienhaus, Structural factors controlling ligand binding to myoglobin: a kinetic hole-burning study, Proc. Natl Acad. Sci. USA 95 (1998) 6762-6767. (Pubitemid 28278054)
81. D.C. Lamb, K. Nienhaus, A. Arcovito, F. Draghi, A.E. Miele,M. Brunori, G.U. Nienhaus, Structural dynamics ofmyoglobin: ligandmigration among protein cavities studied by Fourier transform infrared/temperature derivative spectroscopy, J. Biol. Chem. 277 (2002) 11636-11644.
82. D.C. Lamb, A. Arcovito, K. Nienhaus, O. Minkow, F. Draghi, M. Brunori, G.U. Nienhaus, Structural dynamics of myoglobin: an infrared kinetic study of ligand migration in mutants YQR and YQRF, Biophys. Chem. 109 (2004) 41-58.
83. H. Lehle, J.M. Kriegl, K. Nienhaus, P. Deng, S. Fengler, G.U. Nienhaus, Probing electric fields in protein cavities by using the vibrational Stark effect of carbon monoxide, Biophys. J. 88 (2005) 1978-1990. (Pubitemid 40976208)
84. K. Nienhaus, E.M. Maes, A. Weichsel, W.R. Montfort, G.U. Nienhaus, Structural dynamics controls nitric oxide affinity in nitrophorin 4, J. Biol. Chem. 279 (2004) 39401-39407.
85. K. Nienhaus, J.E. Knapp, P. Palladino, W.E. Royer Jr., G.U. Nienhaus, Ligand migration and binding in the dimeric hemoglobin of Scapharca inaequivalvis, Biochemistry 46 (2007) 14018-14031. (Pubitemid 350253073)
86. A. Pesce, M. Nardini, S. Dewilde, E. Geuens, K. Yamauchi, P. Ascenzi, A.F. Riggs, L. Moens, M. Bolognesi, The 109 residue nerve tissue minihemoglobin from Cerebratulus lacteus highlights striking structural plasticity of the alpha-helical globin fold, Structure (Camb) 10 (2002) 725-735. (Pubitemid 34518713)
87. 2 entry and exit, J. Biol. Chem. 283 (2008) 35689-35702.
88. J.M.C. Ribeiro, J.M.H. Hazzard, R.H. Nussenzveig, D.E. Champagne, F.A. Walker, Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect, Science 260 (1993) 539-541. (Pubitemid 23161618)
89. W.R. Montfort, A. Weichsel, J.F. Andersen, Nitrophorins and related antihemostatic lipocalins from Rhodnius prolixus and other blood-sucking arthropods, Biochim. Biophys. Acta 1482 (2000) 110-118.
90. D.E. Champagne, R.H. Nussenzveig, J.M. Ribeiro, Purification, partial characterization, and cloning of nitric oxide-carrying heme proteins (nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus, J. Biol. Chem. 270 (1995) 8691-8695.
91. A. Weichsel, J.F. Andersen, S.A. Roberts, W.R. Montfort, Nitric oxide binding to nitrophorin 4 induces complete distal pocket burial, Nat. Struct. Biol. 7 (2000) 551-554. (Pubitemid 30445910)
92. T. Burmester, B. Weich, S. Reinhardt, T. Hankeln, A vertebrate globin expressed in the brain, Nature 407 (2000) 520-523.
93. M. Brunori, B. Vallone, Neuroglobin, seven years after, Cell. Mol. Life Sci. 64 (2007) 1259-1268.
94. K. Nienhaus, G.U. Nienhaus, Searching for neuroglobin's role in the brain, IUBMB Life 59 (2007) 490-497. (Pubitemid 47265847)
95. S. Dewilde, L. Kiger, T. Burmester, T. Hankeln, V. Baudin-Creuza, T. Aerts, M.C. Marden, R. Caubergs, L. Moens, Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family, J. Biol. Chem. 276 (2001) 38949-38955.
96. J.T. Trent, A.N. Hvitved, M.S. Hargrove, A model for ligand binding to hexacoordinate hemoglobins, Biochemistry 40 (2001) 6155-6163. (Pubitemid 32466320)
97. B. Vallone, K. Nienhaus, M. Brunori, G.U. Nienhaus, The structure of murine neuroglobin: novel pathways for ligand migration and binding, Proteins 56 (2004) 85-92. (Pubitemid 38720840)
98. M. Anselmi, M. Brunori, B. Vallone, A. Di Nola, Molecular dynamics simulation of deoxy and carboxy murine neuroglobin in water, Biophys. J. 93 (2007) 434-441. (Pubitemid 47057810)
99. B. Vallone, K. Nienhaus, A. Matthes, M. Brunori, G.U. Nienhaus, The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity, Proc. Natl Acad. Sci. USA 101 (2004) 17351-17356. (Pubitemid 39657407)
100. K. Nienhaus, G.U. Nienhaus, Influence of distal residue B10 on the CO dynamics in myoglobin and neuroglobin, J. Biol. Phys. 33 (2008) 357-379.
101. S. Lutz, K. Nienhaus, G.U. Nienhaus, M. Meuwly, Ligand migration between internal docking sites in photodissociated carbonmonoxy neuroglobin, J. Phys. Chem. B 113 (2009) 15334-15343.
102. K. Nienhaus, S. Lutz, M. Meuwly, G.U. Nienhaus, Structural identification of spectroscopic substates in neuroglobin, Chemphyschem 11 (2010) 119-129.
103. S. Abbruzzetti, S. Faggiano, S. Bruno, F. Spyrakis, A.Mozzarelli, S. Dewilde, L.Moens, C. Viappiani, Ligand migration through the internal hydrophobic cavities in human neuroglobin, Proc. Natl Acad. Sci. USA 106 (2009) 18984-18989.
104. B. Trevaskis, R.A. Watts, C.R. Andersson, D.J. Llewellyn, M.S. Hargrove, J.S. Olson, E.S. Dennis, W.J. Peacock, Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins, Proc. Natl Acad. Sci. USA 94 (1997) 12230-12234. (Pubitemid 27467871)
105. S.M. Duff, J.B. Wittenberg, R.D. Hill, Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands, J. Biol. Chem. 272 (1997) 16746-16752.
106. R. Arredondo-Peter, M.S. Hargrove, G. Sarath, J.F. Moran, J. Lohrman, J.S. Olson, R.V. Klucas, Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli, Plant Physiol. 115 (1997) 1259-1266.
107. P.W. Hunt, R.A. Watts, B. Trevaskis, D.J. Llewelyn, J. Burnell, E.S. Dennis, W.J. Peacock, Expression and evolution of functionally distinct haemoglobin genes in plants, Plant Mol. Biol. 47 (2001) 677-692.
108. M. Perazzolli, P. Dominici, M.C. Romero-Puertas, E. Zago, J. Zeier, M. Sonoda, C. Lamb, M. Delledonne, Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity, Plant Cell 16 (2004) 2785-2794. (Pubitemid 41071362)
109. S. Bruno, S. Faggiano, F. Spyrakis, A.Mozzarelli, S.Abbruzzetti, E.Grandi, C.Viappiani, A. Feis, S.Mackowiak, G. Smulevich, E. Cacciatori, P. Dominici, The reactivitywith CO of AHb1 and AHb2 from Arabidopsis thaliana is controlled by the distal HisE7 and internal hydrophobic cavities, J. Am. Chem. Soc. 129 (2007) 2880-2889. (Pubitemid 46417964)
110. S. Faggiano, S. Abbruzzetti, F. Spyrakis, E. Grandi, C. Viappiani, S. Bruno, A. Mozzarelli, P. Cozzini, A. Astegno, P. Dominici, S. Brogioni, A. Feis, G. Smulevich, O. Carrillo, P. Schmidtke, A. Bidon-Chanal, F.J. Luque, Structural plasticity and functional implications of internal cavities in distal mutants of type 1 nonsymbiotic hemoglobin AHb1 fromArabidopsis thaliana, J. Phys. Chem. B 113 (2009) 16028-16038.
111. S. Abbruzzetti, E. Grandi, S. Bruno, S. Faggiano, F. Spyrakis, A. Mozzarelli, E. Cacciatori, P. Dominici, C. Viappiani, Ligand migration in nonsymbiotic hemoglobin AHb1 from Arabidopsis thaliana, J. Phys. Chem. B 111 (2007) 12582-12590.
112. Y.P. Chen, S.A. Woodin, D.E. Lincoln, C.R. Lovell, An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata, J. Biol. Chem. 271 (1996) 4609-4612.
113. M.W. LaCount, E. Zhang, Y.P. Chen, K. Han, M.M. Whitton, D.E. Lincoln, S.A. Woodin, L. Lebioda, The crystal structure and amino acid sequence of dehaloperoxidase from Amphitrite ornata indicate common ancestry with globins, J. Biol. Chem. 275 (2000) 18712-18716.
114. T.L. Poulos, J. Kraut, The stereochemistry of peroxidase catalysis, J. Biol. Chem. 255 (1980) 8199-8205.
115. K. Nienhaus, E. Nickel, M.F. Davis, S. Franzen, G.U. Nienhaus, Determinants of substrate internalization in the distal pocket of dehaloperoxidase hemoglobin of Amphitrite ornata, Biochemistry 47 (2008) 12985-12994.
116. M. Sono, M.P. Roach, E.D. Coulter, J.H. Dawson, Heme-containing oxygenases, Chem. Rev. 96 (1996) 2841-2888.
117. O. Takikawa, Biochemical and medical aspects of the indoleamine 2, 3-dioxygenase-initiated L-tryptophan metabolism, Biochem. Biophys. Res. Commun. 338 (2005) 12-19.
118. E. Nickel, K. Nienhaus, C. Lu, S.R. Yeh, G.U. Nienhaus, Ligand and substrate migration in human indoleamine 2, 3-dioxygenase, J. Biol. Chem. 284 (2009) 31548-31554.
119. N. Strickland, J.N. Harvey, Spin-forbidden ligand binding to the ferrous-heme group: ab initio and DFT studies, J. Phys. Chem. B 111 (2007) 841-852.
120. G.U. Nienhaus, K. Chu, B. McMahon, J.D. Müller, Conformational relaxation and ligand binding in heme proteins, in: R.H. Sarma, M.H. Sarma (Eds.), Biological Structure and Dynamics, vol. 1, Adenine Press, Albany NY, 1996, pp. 281-296.
121. M. Weik, X. Vernede, A. Royant, D. Bourgeois, Temperature derivative fluorescence spectroscopy as a tool to study dynamical changes in protein crystals, Biophys. J. 86 (2004) 3176-3185. (Pubitemid 38552717)
122. A. Arcovito, D.C. Lamb, G.U. Nienhaus, J.L. Hazemann, M. Benfatto, S. Della Longa, Light-induced relaxation of photolyzed carbonmonoxy myoglobin: a temperature-dependent x-ray absorption near-edge structure (XANES) study, Biophys. J. 88 (2005) 2954-2964. (Pubitemid 40976159)