Ligand migration and binding in nonsymbiotic hemoglobins of arabidopsis thaliana

Biochemistry

Volumn 49, Issue 35, 2010, Pages 7448-7458

  Nienhaus, Karin ^a   Dominici, Paola ^b   Astegno, Alessandra ^b   Abbruzzetti, Stefania ^c   Viappiani, Cristiano ^c   Nienhaus, G Ulrich ^a,d  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF VERONA   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; CARBON MONOXIDE; CRYOGENICS; DOCKING; FOURIER TRANSFORMS; FREQUENCY BANDS; HEMOGLOBIN; LIGANDS; ORGANIC ACIDS; PHYSIOLOGY; PORPHYRINS;

ACTIVE SITE STRUCTURE; AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; BOUND LIGANDS; CO MOLECULE; CO STRETCHING FREQUENCIES; CRYOGENIC TEMPERATURES; DOCKING SITES; GEMINATE REBINDING; HIGH FREQUENCY HF; LIGAND BINDING PROPERTIES; LOW FREQUENCY BAND; NEAR-NEUTRAL PH; PHYSIOLOGICAL FUNCTIONS; PROTONATES; SIDE CHAINS; STRETCHING BANDS; TEMPERATURE DERIVATIVES;

CONFORMATIONS;

CARBON MONOXIDE; HEMOGLOBIN; AHB1 PROTEIN, ARABIDOPSIS; AHB2 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; LIGAND; NITRIC OXIDE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BINDING SITE; INFRARED SPECTROSCOPY; LIGAND BINDING; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; TEMPERATURE DEPENDENCE; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; METABOLISM;

ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CARBON MONOXIDE; HEMOGLOBINS; KINETICS; LIGANDS; MODELS, MOLECULAR; NITRIC OXIDE; PROTEIN CONFORMATION;

EID: 77956147343     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100768g     Document Type: Article

References (88)

1. Trevaskis, B., Watts, R. A., Andersson, C. R., Llewellyn, D. J., Hargrove, M. S., Olson, J. S., Dennis, E. S., and Peacock, W. J. (1997) Two hemoglobin genes in Arabidopsis thaliana: The evolutionary origins of leghemoglobins Proc. Natl. Acad. Sci. U.S.A. 94, 12230-12234
2. Duff, S. M., Wittenberg, J. B., and Hill, R. D. (1997) Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands J. Biol. Chem. 272, 16746-16752
3. 2-binding kinetics of a recombinant protein synthesized in Escherichia coli Plant Physiol. 115, 1259-1266
4. Hunt, P. W., Watts, R. A., Trevaskis, B., Llewelyn, D. J., Burnell, J., Dennis, E. S., and Peacock, W. J. (2001) Expression and evolution of functionally distinct haemoglobin genes in plants Plant Mol. Biol. 47, 677-692
5. Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A., and Guertin, M. (2002) Truncated hemoglobins: A new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants J. Biol. Chem. 277, 871-874
6. Perazzolli, M., Dominici, P., Romero-Puertas, M. C., Zago, E., Zeier, J., Sonoda, M., Lamb, C., and Delledonne, M. (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity Plant Cell 16, 2785-2794
7. Olson, J. S., Mathews, A. J., Rohlfs, R. J., Springer, B. A., Egeberg, K. D., Sligar, S. G., Tame, J., Renaud, J. P., and Nagai, K. (1988) The role of the distal histidine in myoglobin and haemoglobin Nature 336, 265-266
8. Olson, J. S. and Phillips, G. N., Jr. (1996) Kinetic pathways and barriers for ligand binding to myoglobin J. Biol. Chem. 271, 17593-17596
9. Gardner, P. R., Gardner, A. M., Martin, L. A., and Salzman, A. L. (1998) Nitric oxide dioxygenase: An enzymic function for flavohemoglobin Proc. Natl. Acad. Sci. U.S.A. 95, 10378-10383
10. Arredondo-Peter, R., Hargrove, M. S., Moran, J. F., Sarath, G., and Klucas, R. V. (1998) Plant hemoglobins Plant Physiol. 118, 1121-1125
11. Arcovito, A., Benfatto, M., Cianci, M., Hasnain, S. S., Nienhaus, K., Nienhaus, G. U., Savino, C., Strange, R. W., Vallone, B., and Della Longa, S. (2007) X-ray structure analysis of a metalloprotein with enhanced active-site resolution using in situ X-ray absorption near edge structure spectroscopy Proc. Natl. Acad. Sci. U.S.A. 104, 6211-6216
12. Ormos, P., Szaraz, S., Cupane, A., and Nienhaus, G. U. (1998) Structural factors controlling ligand binding to myoglobin: A kinetic hole-burning study Proc. Natl. Acad. Sci. U.S.A. 95, 6762-6767
13. Li, T., Quillin, M. L., Phillips, G. N., Jr., and Olson, J. S. (1994) Structural determinants of the stretching frequency of CO bound to myoglobin Biochemistry 33, 1433-1446
14. Nienhaus, K., Olson, J. S., Franzen, S., and Nienhaus, G. U. (2005) The Origin of Stark splitting in the initial photoproduct state of MbCO J. Am. Chem. Soc. 127, 40-41
15. Ray, G. B., Li, X.-Y., Ibers, J. A., Sessler, J. L., and Spiro, G. S. (1994) How far can proteins bend the FeCO unit J. Am. Chem. Soc. 116, 162-176
16. Meuwly, M. (2006) On the influence of the local environment on the CO stretching frequencies in native myoglobin: Assignment of the B-states in MbCO ChemPhysChem 7, 2061-2063
17. Nutt, D. R. and Meuwly, M. (2004) CO migration in native and mutant myoglobin: Atomistic simulations for the understanding of protein function Proc. Natl. Acad. Sci. U.S.A. 101, 5998-6002
18. Plattner, N. and Meuwly, M. (2008) The role of higher CO-multipole moments in understanding the dynamics of photodissociated carbonmonoxide in myoglobin Biophys. J. 94, 2505-2515
19. 17O isotropic chemical shifts, and nuclear quadrupole coupling constants Biophys. J. 72, 899-912
20. Kaposi, A. D., Vanderkooi, J. M., Wright, W. W., Fidy, J., and Stavrov, S. S. (2001) Influence of static and dynamic disorder on the visible and infrared absorption spectra of carbonmonoxy horseradish peroxidase Biophys. J. 81, 3472-3482
21. Elber, R. and Karplus, M. (1987) Multiple conformational states of proteins: A molecular dynamics analysis of myoglobin Science 235, 318-321
22. Dalosto, S. D., Vanderkooi, J. M., and Sharp, K. A. (2004) Vibrational Stark Effects on Carbonyl, Nitrile, and Nitrosyl Compounds Including Heme Ligands, CO, CN, and NO, Studied with Density Functional Theory J. Phys. Chem. B 108, 6450-6457
23. Nienhaus, G. U., Chu, K., and Jesse, K. (1998) Structural heterogeneity and ligand binding in carbonmonoxy myoglobin crystals at cryogenic temperatures Biochemistry 37, 6819-6823
24. Nienhaus, K., Deng, P., Kriegl, J. M., and Nienhaus, G. U. (2003) Structural Dynamics of Myoglobin: The Effect of Internal Cavities on Ligand Migration and Binding Biochemistry 42, 9647-9658
25. Nienhaus, K., Deng, P., Kriegl, J. M., and Nienhaus, G. U. (2003) Structural Dynamics of Myoglobin: Spectroscopic and Structural Characterization of Ligand Docking Sites in Myoglobin Mutant L29W Biochemistry 42, 9633-9646
26. Nienhaus, K., Deng, P., Olson, J. S., Warren, J. J., and Nienhaus, G. U. (2003) Structural Dynamics of Myoglobin: Ligand Migration and Binding in Valine 68 Mutants J. Biol. Chem. 278, 42532-42544
27. Kriegl, J. M., Nienhaus, K., Deng, P., Fuchs, J., and Nienhaus, G. U. (2003) Ligand dynamics in a protein internal cavity Proc. Natl. Acad. Sci. U.S.A. 100, 7069-7074
28. Park, E. S., Andrews, S. S., Hu, R. B., and Boxer, S. G. (1999) Vibrational stark spectroscopy in proteins: A probe and calibration for electrostatic fields J. Phys. Chem. B 103, 9813-9817
29. Hush, N. S. and Reimers, J. R. (1995) Vibrational stark spectroscopy. 1. Basic theory and application to the CO stretch J. Phys. Chem. 99, 15798-15805
30. Park, E. S. and Boxer, S. G. (2002) Origins of the sensitivity of molecular vibrations on electric fields: Carbonyl and Nitrosyl Stretches in Model Compounds and Proteins J. Phys. Chem. B 106, 5800-5806
31. Alben, J. O., Beece, D., Bowne, S. F., Doster, W., Eisenstein, L., Frauenfelder, H., Good, D., McDonald, J. D., Marden, M. C., Moh, P. P., Reinisch, L., Reynolds, A. H., Shyamsunder, E., and Yue, K. T. (1982) Infrared spectroscopy of photodissociated carboxymyoglobin at low temperatures Proc. Natl. Acad. Sci. U.S.A. 79, 3744-3748
32. Yang, F. and Phillips, G. N., Jr. (1996) Crystal structures of CO-, deoxy- and met-myoglobins at various pH values J. Mol. Biol. 256, 762-774
33. Vojtechovsky, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution Biophys. J. 77, 2153-2174
34. Müller, J. D., McMahon, B. H., Chien, E. Y., Sligar, S. G., and Nienhaus, G. U. (1999) Connection between the taxonomic substates and protonation of histidines 64 and 97 in carbonmonoxy myoglobin Biophys. J. 77, 1036-1051
35. Braunstein, D. P., Chu, K., Egeberg, K. D., Frauenfelder, H., Mourant, J. R., Nienhaus, G. U., Ormos, P., Sligar, S. G., Springer, B. A., and Young, R. D. (1993) Ligand binding to heme proteins: III. FTIR studies of His-E7 and Val-E11 mutants of carbonmonoxymyoglobin Biophys. J. 65, 2447-2454
36. Nienhaus, K. and Nienhaus, G. U. (2007) Influence of Distal Residue B10 on the CO Dynamics in Myoglobin and Neuroglobin J. Biol. Phys. 33, 357-379
37. Lamb, D. C., Nienhaus, K., Arcovito, A., Draghi, F., Miele, A. E., Brunori, M., and Nienhaus, G. U. (2002) Structural dynamics of myoglobin: Ligand migration among protein cavities studied by Fourier transform infrared/temperature derivative spectroscopy J. Biol. Chem. 277, 11636-11644
38. Gibson, Q. H. and Ainsworth, S. (1957) Photosensitivity of haem compounds Nature 180, 1416-1417
39. Frauenfelder, H., Nienhaus, G. U., and Johnson, J. B. (1991) Rate Processes in Proteins Phys. Chem. Chem. Phys. 95, 272-278
40. Parak, F. G. and Nienhaus, G. U. (2002) Myoglobin, a Paradigm in the Study of Protein Dynamics ChemPhysChem 3, 249-254
41. Lim, M., Jackson, T. A., and Anfinrud, P. A. (1997) Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin Nat. Struct. Biol. 4, 209-214
42. Lehle, H., Kriegl, J. M., Nienhaus, K., Deng, P., Fengler, S., and Nienhaus, G. U. (2005) Probing electric fields in protein cavities by using the vibrational Stark effect of carbon monoxide Biophys. J. 88, 1978-1990
43. Nienhaus, G. U., Mourant, J. R., Chu, K., and Frauenfelder, H. (1994) Ligand binding to heme proteins: The effect of light on ligand binding in myoglobin Biochemistry 33, 13413-13430
44. Nienhaus, G. U., Mourant, J. R., and Frauenfelder, H. (1992) Spectroscopic evidence for conformational relaxation in myoglobin Proc. Natl. Acad. Sci. U.S.A. 89, 2902-2906
45. Chu, K., Ernst, R. M., Frauenfelder, H., Mourant, J. R., Nienhaus, G. U., and Philipp, R. (1995) Light-induced and thermal relaxation in a protein Phys. Rev. Lett. 74, 2607-2610
46. Bruno, S., Faggiano, S., Spyrakis, F., Mozzarelli, A., Abbruzzetti, S., Grandi, E., Viappiani, C., Feis, A., Mackowiak, S., Smulevich, G., Cacciatori, E., and Dominici, P. (2007) The reactivity with CO of AHb1 and AHb2 from Arabidopsis thaliana is controlled by the distal HisE7 and internal hydrophobic cavities J. Am. Chem. Soc. 129, 2880-2889
47. Berendzen, J. and Braunstein, D. (1990) Temperature-derivative spectroscopy: A tool for protein dynamics Proc. Natl. Acad. Sci. U.S.A. 87, 1-5
48. Mourant, J. R., Braunstein, D. P., Chu, K., Frauenfelder, H., Nienhaus, G. U., Ormos, P., and Young, R. D. (1993) Ligand binding to heme proteins: II. Transitions in the heme pocket of myoglobin Biophys. J. 65, 1496-1507
49. Bredenbeck, J., Helbing, J., Nienhaus, K., Nienhaus, G. U., and Hamm, P. (2007) Protein ligand migration mapped by nonequilibrium 2D-IR exchange spectroscopy Proc. Natl. Acad. Sci. U.S.A. 104, 14243-14248
50. Nienhaus, K., Maes, E. M., Weichsel, A., Montfort, W. R., and Nienhaus, G. U. (2004) Structural dynamics controls nitric oxide affinity in nitrophorin 4 J. Biol. Chem. 279, 39401-39407
51. Vogel, K. M., Kozlowski, P. M., Zgierski, M. Z., and Spiro, T. G. (1999) Determinants of the FeXO (X = C, N, O) vibrational frequencies in heme adducts from experiment and density functional theory J. Am. Chem. Soc. 121, 9915-9921
52. Hoy, J. A., Robinson, H., Trent, J. T., III, Kakar, S., Smagghe, B. J., and Hargrove, M. S. (2007) Plant hemoglobins: A molecular fossil record for the evolution of oxygen transport J. Mol. Biol. 371, 168-179
53. Spiro, T. G. and Wasbotten, I. H. (2005) CO as a vibrational probe of heme protein active sites J. Inorg. Biochem. 99, 34-44
54. Faggiano, S., Abbruzzetti, S., Spyrakis, F., Grandi, E., Viappiani, C., Bruno, S., Mozzarelli, A., Cozzini, P., Astegno, A., Dominici, P., Brogioni, S., Feis, A., Smulevich, G., Carrillo, O., Schmidtke, P., Bidon-Chanal, A., and Luque, F. J. (2009) Structural Plasticity and Functional Implications of Internal Cavities in Distal Mutants of Type 1 Non-Symbiotic Hemoglobin AHb1 from Arabidopsis thaliana J. Phys. Chem. B 113, 16028-16038
55. Young, R. D., Frauenfelder, H., Johnson, J. B., Lamb, D. C., Nienhaus, G. U., Phillip, R., and Scholl, R. (1991) Time- and temperature dependence of large-scale conformational transitions in myoglobin Chem. Phys. 158, 315-328
56. 13CO-labeled species Biochemistry 30, 2333-2347
57. Smagghe, B. J., Kundu, S., Hoy, J. A., Halder, P., Weiland, T. R., Savage, A., Venugopal, A., Goodman, M., Premer, S., and Hargrove, M. S. (2006) Role of phenylalanine B10 in plant nonsymbiotic hemoglobins Biochemistry 45, 9735-9745
58. Teng, T. Y., Srajer, V., and Moffat, K. (1994) Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K Nat. Struct. Biol. 1, 701-705
59. Hartmann, H., Zinser, S., Komninos, P., Schneider, R. T., Nienhaus, G. U., and Parak, F. (1996) X-ray structure determination of a metastable state of carbonmonoxy myoglobin after photodissociation Proc. Natl. Acad. Sci. U.S.A. 93, 7013-7016
60. Schlichting, I., Berendzen, J., Phillips, G. N., Jr., and Sweet, R. M. (1994) Crystal structure of photolysed carbonmonoxy-myoglobin Nature 371, 808-812
61. Lutz, S., Nienhaus, K., Nienhaus, G. U., and Meuwly, M. (2009) Ligand migration between internal docking sites in photodissociated carbonmonoxy neuroglobin J. Phys. Chem. B 113, 15334-15343
62. Nienhaus, K., Lutz, S., Meuwly, M., and Nienhaus, G. U. (2010) Structural identification of spectroscopic substates in neuroglobin ChemPhysChem 11, 119-129
63. Johnson, J. B., Lamb, D. C., Frauenfelder, H., Müller, J. D., McMahon, B., Nienhaus, G. U., and Young, R. D. (1996) Ligand binding to heme proteins. VI. Interconversion of taxonomic substates in carbonmonoxymyoglobin Biophys. J. 71, 1563-1573
64. Steinbach, P. J., Ansari, A., Berendzen, J., Braunstein, D., Chu, K., Cowen, B. R., Ehrenstein, D., Frauenfelder, H., Johnson, J. B., Lamb, D. C., Luck, S., Mourant, J. R., Nienhaus, G. U., Ormos, P., Philipp, R., Xie, A., and Young, R. D. (1991) Ligand binding to heme proteins: Connection between dynamics and function Biochemistry 30, 3988-4001
65. McMahon, B. H., Stojkovic, B. P., Hay, P. J., Martin, R. L., and García, A. E. (2000) Microscopic model of carbon monoxide binding to myoglobin J. Chem. Phys. 113, 6831-6850
66. Lamb, D. C., Arcovito, A., Nienhaus, K., Minkow, O., Draghi, F., Brunori, M., and Nienhaus, G. U. (2004) Structural dynamics of myoglobin: An infrared kinetic study of ligand migration in mutants YQR and YQRF Biophys. Chem. 109, 41-58
67. 2 affinity in Cerebratulus lacteus mini-hemoglobin J. Biol. Chem. 279, 33662-33672
68. Ostermann, A., Waschipky, R., Parak, F. G., and Nienhaus, G. U. (2000) Ligand binding and conformational motions in myoglobin Nature 404, 205-208
69. Abbruzzetti, S., Grandi, E., Bruno, S., Faggiano, S., Spyrakis, F., Mozzarelli, A., Cacciatori, E., Dominici, P., and Viappiani, C. (2007) Ligand migration in nonsymbiotic hemoglobin AHb1 from Arabidopsis thaliana J. Phys. Chem. B 111, 12582-12590
70. Nienhaus, K., Palladino, P., and Nienhaus, G. U. (2008) Structural dynamics of myoglobin: FTIR-TDS study of NO migration and binding Biochemistry 47, 935-948
71. Bruno, S., Faggiano, S., Spyrakis, F., Mozzarelli, A., Cacciatori, E., Dominici, P., Grandi, E., Abbruzzetti, S., and Viappiani, C. (2007) Different roles of protein dynamics and ligand migration in non-symbiotic hemoglobins AHb1 and AHb2 from Arabidopsis thaliana Gene 398, 224-233
72. Brunori, M., Vallone, B., Cutruzzola, F., Travaglini-Allocatelli, C., Berendzen, J., Chu, K., Sweet, R. M., and Schlichting, I. (2000) The role of cavities in protein dynamics: Crystal structure of a photolytic intermediate of a mutant myoglobin Proc. Natl. Acad. Sci. U.S.A. 97, 2058-2063
73. Schotte, F., Lim, M., Jackson, T. A., Smirnov, A. V., Soman, J., Olson, J. S., Phillips, G. N., Jr., Wulff, M., and Anfinrud, P. A. (2003) Watching a protein as it functions with 150-ps time-resolved X-ray crystallography Science 300, 1944-1947
74. Abbruzzetti, S., Bruno, S., Faggiano, S., Grandi, E., Mozzarelli, A., and Viappiani, C. (2006) Time-resolved methods in biophysics. 2. Monitoring haem proteins at work with nanosecond laser flash photolysis Photochem. Photobiol. Sci. 5, 1109-1120
75. 2 entry into and exit from myoglobin J. Biol. Chem. 276, 5177-5188
76. Young, R. D. and Bowne, S. F. (1984) Conformational substates and barrier height distributions in ligand binding to heme proteins J. Chem. Phys. 81, 3730-3737
77. Brunori, M. (2001) Nitric oxide moves myoglobin centre stage Trends Biochem. Sci. 26, 209-210
78. Frauenfelder, H., McMahon, B. H., Austin, R. H., Chu, K., and Groves, J. T. (2001) The role of structure, energy landscape, dynamics, and allostery in the enzymatic function of myoglobin Proc. Natl. Acad. Sci. U.S.A. 98, 2370-2374
79. Smagghe, B. J., Hoy, J. A., Percifield, R., Kundu, S., Hargrove, M. S., Sarath, G., Hilbert, J. L., Watts, R. A., Dennis, E. S., Peacock, W. J., Dewilde, S., Moens, L., Blouin, G. C., Olson, J. S., and Appleby, C. A. (2009) Review: Correlations between oxygen affinity and sequence classifications of plant hemoglobins Biopolymers 91, 1083-1096
80. Hoy, J. A. and Hargrove, M. S. (2008) The structure and function of plant hemoglobins Plant Physiol. Biochem. 46, 371-379
81. Parak, F., Heidemeier, J., and Nienhaus, G. U. (1988) Protein structural dynamics as determined by Mössbauer spectroscopy Hyperfine Interact. 40, 147-158
82. Doster, W., Cusack, S., and Petry, W. (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering Nature 337, 754-756
83. Austin, R. H., Beeson, K. W., Eisenstein, L., Frauenfelder, H., and Gunsalus, I. C. (1975) Dynamics of ligand binding to myoglobin Biochemistry 14, 5355-5373
84. Lim, M., Jackson, T. A., and Anfinrud, P. A. (1995) Binding of CO to myoglobin from a heme pocket docking site to form nearly linear Fe-C-O Science 269, 962-966
85. Bourgeois, D., Vallone, B., Schotte, F., Arcovito, A., Miele, A. E., Sciara, G., Wulff, M., Anfinrud, P., and Brunori, M. (2003) Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography Proc. Natl. Acad. Sci. U.S.A. 100, 8704-8709
86. Hummer, G., Schotte, F., and Anfinrud, P. A. (2004) Unveiling functional protein motions with picosecond X-ray crystallography and molecular dynamics simulations Proc. Natl. Acad. Sci. U.S.A. 101, 15330-15334
87. Schmidt, M., Nienhaus, K., Pahl, R., Krasselt, A., Anderson, S., Parak, F., Nienhaus, G. U., and Srajer, V. (2005) Ligand migration pathway and protein dynamics in myoglobin: a time-resolved crystallographic study on L29W MbCO Proc. Natl. Acad. Sci. U.S.A. 102, 11704-11709
88. Srajer, V., Teng, T., Ursby, T., Pradervand, C., Ren, Z., Adachi, S., Schildkamp, W., Bourgeois, D., Wulff, M., and Moffat, K. (1996) Photolysis of the carbon monoxide complex of myoglobin: Nanosecond time-resolved crystallography Science 274, 1726-1729