Ligand migration and hexacoordination in type 1 non-symbiotic rice hemoglobin

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 8, 2011, Pages 1042-1053

  Bisht, Nitin Kumar ^a,b,c   Abbruzzetti, Stefania ^a,b   Uppal, Sheetal ^c   Bruno, Stefano ^a   Spyrakis, Francesca ^a,d   Mozzarelli, Andrea ^a,d   Viappiani, Cristiano ^a,e   Kundu, Suman ^c  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c UNIVERSITY OF DELHI   (India)

^d NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

^e CNR   (Italy)

Author keywords

Hexacoordination; Laser flash photolysis; Ligand migration; Non symbiotic plant hemoglobin; Silica gel

Indexed keywords

CARBON MONOXIDE; HEMOGLOBIN; HISTIDINE; RICE HEMOGLOBIN; SILICA GEL; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BINDING AFFINITY; ENCAPSULATION; LIGAND BINDING; LIGAND MIGRATION; MOLECULAR DOCKING; MUTATION; NONHUMAN; OXIDATION; PHOTOLYSIS; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; TEMPERATURE DEPENDENCE;

CARBON MONOXIDE; CHROMATOGRAPHY, GEL; HEMOGLOBINS; KINETICS; LIGANDS; MODELS, MOLECULAR; NITRIC OXIDE; ORYZA SATIVA; OXYGEN; RECOMBINANT PROTEINS;

EID: 79958775000     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.09.016     Document Type: Article

References (62)

1. C.A. Appleby, Leghemoglobin and rhizobium respiration, Annu. Rev. Plant Physiol. 35 (1984) 443-478.
2. D. Bogusz, C.A. Appleby, J. Landsmann, E.S. Dennis, M.J. Trinick, W.J. Peacock, Functioning hemoglobin genes in non-nodulating plants, Nature 331 (1988) 178-180.
3. R. Arredondo-Peter, M.S. Hargrove, C. 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.
4. 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. U. S. A. 94 (1997) 12230-12234. (Pubitemid 27467871)
5. Y.H. Wang, L.V. Kochian, J.J. Doyle, D.F. Garvin, Two tomato non-symbiotic haemoglobin genes are differentially expressed in response to diverse changes in mineral nutrient status, Plant Cell Environ. 26 (2003) 673-680. (Pubitemid 36631984)
6. 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.
7. C. Dordas, Nonsymbiotic hemoglobins and stress tolerance in plants, Plant Sci. 176 (2009) 433-440.
8. B.J. Smagghe, J.A. Hoy, R. Percifield, S. Kundu, M.S. Hargrove, G. Sarath, J.L. Hilbert, R.A. Watts, E.S. Dennis, W.J. Peacock, S. Dewilde, L. Moens, G.C. Blouin, J.S. Olson, C.A. Appleby, Correlations between oxygen affinity and sequence classifications of plant hemoglobins, Biopolymers (2009) 1083-1096.
9. R. Wang, K. Guegler, S.T. LaBrie, N.M. Crawford, Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate, Plant Cell 12 (2000) 1491-1509.
10. X. Nie, R.D. Hill, Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue, Plant Physiol. 114 (1997) 835-840. (Pubitemid 28382330)
11. B.J. Smagghe, J.T. Trent III, M.S. Hargrove, NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo, PLoS ONE 3 (2008) e2039.
12. M. Perazzolli, P. Dominici, M.C.R. Puertas, E. Zago, J. Zeier, M. Sonoda, C. Lamb, M. Delledonne, Non-symbiotic hemoglobin AHb1 modulates nitric oxyde bioactivity in Arabidopsis thaliana, Plant Cell 16 (2004) 2785-2794. (Pubitemid 41071362)
13. M. Perazzolli, M.C. Romero-Puertas, M. Delledonne, Modulation of nitric oxide bioactivity by plant haemoglobins, J. Exp. Bot. 57 (2006) 479-488.
14. A.U. Igamberdiev, N.V. Bykova, R.D. Hill, Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin, Planta 223 (2006) 1033-1040.
15. 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 reactivity with CO of AHb1 and AHb2 from Arabidopsis thaliana is controlled by the distal His E7 and internal hydrophobic cavities, J. Am. Chem. Soc. 129 (2007) 2880-2889. (Pubitemid 46417964)
16. B.J. Smagghe, S. Kundu, J.A. Hoy, P. Halder, T.R. Weiland, A. Savage, A. Venugopal, M. Goodman, S. Premer, M.S. Hargrove, Role of phenylalanine B10 in plant nonsymbiotic hemoglobins, Biochemistry 45 (2006) 9735-9745. (Pubitemid 44257421)
17. F. Spyrakis, S. Faggiano, S.Abbruzzetti, P.Dominici, E. Cacciatori,A.Astegno, E.Droghetti, A. Feis, G. Smulevich, S. Bruno, A. Mozzarelli, P. Cozzini, C. Viappiani, A. Bidon-Chanal, F.J. Luque,Histidine E7 dynamicsmodulates ligand exchange between distal pocket and solvent in AHb1 from Arabidopsis thaliana, J. Phys. Chem. B (in preparation).
18. M. Brunori, A. Giuffrè, K. Nienhaus, G.U. Nienhaus, F.M. Scandurra, B. Vallone, Neuroglobin, nitric oxide, and oxygen: functional pathways and conformational changes, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 8483-8488.
19. B. Vallone, K. Nienhaus, K. Matthes, M. Brunori, G.U. Nienhaus, The structure of murine neuroglobin: novel pathways for ligand migration and binding, Proteins 56 (2004) 85.
20. 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 from Arabidopsis thaliana, J. Phys. Chem. B 113 (2009) 16028-16038.
21. S. Bruno, S. Faggiano, F. Spyrakis, A. Mozzarelli, E. Cacciatori, P. Dominici, E. Grandi, S. Abbruzzetti, C. Viappiani, Different roles of protein dynamics and ligand migration in non-symbiotic hemoglobins AHb1 and AHb2 from Arabidopsis thaliana, Gene 398 (2007) 224-233. (Pubitemid 47068896)
22. S. Abbruzzetti, S. Bruno, S. Faggiano, E. Grandi, A. Mozzarelli, C. Viappiani, Monitoring haem proteins at work with nanosecond laser flash photolysis, Photochem. Photobiol. Sci. 5 (2006) 1109-1120.
23. S. Abbruzzetti, E. Grandi, S. Bruno, S. Faggiano, F. Spyrakis, A.Mozzarelli, P. Dominici, C. Viappiani, Ligand migration in non symbiotic hemoglobin AHb1 from Arabidopsis thaliana, J. Phys. Chem. B 111 (2007) 12582-12590.
24. S. Abbruzzetti, C. Viappiani, S. Bruno, A. Mozzarelli, Enhanced geminate ligand rebinding upon photo-dissociation of silica gel-embedded myoglobin-CO, Chem. Phys. Lett. 346 (2001) 430-436. (Pubitemid 33628503)
25. S. Abbruzzetti, C. Viappiani, S. Bruno, S. Bettati, M. Bonaccio, A. Mozzarelli, Functional characterization of heme proteins encapsulated in wet nanoporous silica gels, J. Nanosci. Nanotech. 1 (2001) 407-415.
26. S. Sottini, C. Viappiani, L. Ronda, S. Bettati, A.Mozzarelli, CO rebinding kinetics to myoglobin- and R state hemoglobin-doped silica gels in the presence of glycerol, J. Phys. Chem. B 108 (2004) 8475-8484.
27. S. Sottini, S. Abbruzzetti, C. Viappiani, S. Bettati, L. Ronda, A.Mozzarelli, Evidence for two geminate rebinding states following laser photolysis of R state hemoglobin encapsulated in wet silica gels, J. Phys. Chem. B 109 (2005) 11411-11413.
28. S. Sottini, S. Abbruzzetti, C. Viappiani, L. Ronda, A. Mozzarelli, Determination of microscopic rate constants for CO binding and migration in myoglobin encapsulated in silica gels, J. Phys. Chem. B 109 (2005) 19523-19528.
29. S. Sottini, S. Abbruzzetti, F. Spyrakis, S. Bettati, L. Ronda, A. Mozzarelli, C. Viappiani, Geminate rebinding in R state hemoglobin: kinetic and computational evidence for multiple hydrophobic pockets, J. Am. Chem. Soc. 127 (2005) 17427-17432. (Pubitemid 41791062)
30. I. Khan, C.F. Shannon, D. Dantsker, A.J. Friedman, J. Perez-Gonzales-de-Apodaca, J.M. Friedman, Sol-gel trapping of functional intermediates of hemoglobin: geminate and bimolecular recombination studies, Biochemistry 39 (2000) 16099-16109.
31. U. Samuni, D. Dantsker, I. Khan, A.J. Friedman, E. Peterson, J.M. Friedman, Spectroscopically and kinetically distinct conformational populations of sol-gel-encapsulated carbonmonoxy myoglobin, J. Biol. Chem. 277 (2002) 25783-25790.
32. U. Samuni, D. Dantsker, A. Ray, J.B. Wittenberg, B.A. Wittenberg, S. Dewilde, L. Moens, Y. Ouellet, M. Guertin, J.M. Friedman, Kinetic modulation in carbonmonoxy derivatives of truncated hemoglobins. The role of distal heme pocket residues and extended apolar tunnel, J. Biol. Chem. 278 (2003) 27241-27250. (Pubitemid 36876881)
33. D. Dantsker, C. Roche, U. Samuni, G. Blouin, J.S. Olson, J.M. Friedman, The position 68(E11) side chain in myoglobin regulates ligand capture, bond formation with heme iron, and internal movement into the Xe cavities, J. Biol. Chem. 280 (2005) 38740-38755.
34. U. Samuni, C.J. Roche, D. Dantsker, L.J. Juszczak, J.M. Friedman, Modulation of reactivity and conformation within the t-quaternary state of human hemoglobin: the combined use of mutagenesis and sol-gel encapsulation, Biochemistry 45 (2006) 2820-2835. (Pubitemid 43334531)
35. S. Bettati, A. Mozzarelli, T state hemoglobin binds oxygen noncooperatively with allosteric effects of protons, inositol hexaphosphate and chloride, J. Biol. Chem. 272 (1997) 32050-32055. (Pubitemid 28011873)
36. P.J. Steinbach, Inferring lifetime distributions from kinetics by maximizing entropy using a bootstrapped model, J. Chem. Inf. Comput. Sci. 42 (2002) 1476-1478. (Pubitemid 35468337)
37. P.J. Steinbach, R. Ionescu, C.R. Matthews, Analysis of kinetics using a hybrid maximum-entropy/nonlinear-least-squares method: application to protein folding, Biophys. J. 82 (2002) 2244-2255. (Pubitemid 34280835)
38. S. Abbruzzetti, S. Bruno, S. Faggiano, L. Ronda, E. Grandi, A. Mozzarelli, C. Viappiani, Characterization of Ligand Migration Mechanisms Inside Haemoglobins from the Analysis of Geminate Rebinding Kinetics, Methods in Enzymology - Globins and Other NO-Reactive Proteins in Microbes, Plants and Invertebrates, 437, 2008, pp. 329-345.
39. J.A.Hoy,H. Robinson, J.T. Trent, S. Kakar, B.J. Smagge,M.S.Hargrove, Plant hemoglobins: a molecular fossil record for the evolution of oxygen transport, J. Mol. Biol. 371 (2007) 168-179.
40. M. Keil, T.E. Exner, J. Brickmann, Pattern recognition strategies for molecular surfaces: III. Binding site prediction with a neural network, J. Comput. Chem. 25 (2003) 779-789.
41. T.A. Binkowski, S.Naghibzadeh, J. Liang, CASTp: computed atlas of surface topography of proteins, Nucleic Acids Res. 31 (2003) 3352-3355. (Pubitemid 37442157)
42. A. Nicholls, K. Sharp, B. Honig, Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons, Proteins 11 (1991) 281-296.
43. P.J. Goodford, A computational procedure for determining energetically favourable binding sites on biologically important macromolecules, J. Med. Chem. 28 (1985) 849-857.
44. M.S. Hargrove, E.A. Brucker, B. Stec, G. Sarath, R. Arredondo-Peter, R.V. Klucas, J.S. Olson, G.N. Phillips Jr., Crystal structure of a nonsymbiotic plant hemoglobin, Structure 8 (2000) 1005-1014.
45. E.E. Scott, Q.H. Gibson, J.S. Olson, Mapping the pathways for O2 entry into and exit from myoglobin, J. Biol. Chem. 276 (2001) 5177-5188.
46. J.S. Olson, J. Soman, G.N. Phillips Jr., Ligand pathways in myoglobin: a review of Trp cavity mutations, IUBMB Life 59 (2007) 552-562. (Pubitemid 47265857)
47. H.E. Harutyunyan, T.N. Safonova, I.P. Kuranova, A.N. Popov, A.V. Teplyakov, G.V. Obmolova, A.A. Rusakov, B.K. Vainshtein, G.G. Dodson, J.C. Wilson, M.F. Perutz, The structure of deoxy- and oxy-leghaemoglobin fromlupin, J.Mol. Biol. 251 (1995) 104.
48. A. Pesce, S. Dewilde, M. Nardini, L. Moens, P. Ascenzi, T. Hankeln, T.B. Bolognesi, Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity, Structure 11 (2003) 1087-1095. (Pubitemid 37103070)
49. M. Brunori, Q.H. Gibson, Cavities and packing defects in the structural dynamics of myoglobin, EMBO Rep. 2 (2001) 674-679. (Pubitemid 32798709)
50. D. deSanctis, S. Dewilde, A. Pesce, L. Moens, P. Ascenzi, T. Hankeln, T. Burmester, M. Bolognesi, Crystal structure of cytoglobin: the fourth globin type discovered in man displays heme hexa-coordination, J. Mol. Biol. 336 (2004) 917-927.
51. M. Lim, T.A. Jackson, P.A. Anfinrud, Nonexponential protein relaxation: dynamics of conformational change in myoglobin, Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 5801-5804. (Pubitemid 23176250)
52. L.P.Murray, J.Hofrichter, E.R.Henry,M. Ikeda-Saito,K.Kitagishi, T. Yonetani,W.A. Eaton, The effect of quaternary structure on the kinetics of conformational changes and nanosecond rebinding of carbonmonoxide to hemoglobin, Proc. Natl.Acad. Sci. U. S. A. 85 (1988) 2151-2155.
53. T. Hankeln, B. Ebner, C. Fuchs, F. Gerlach, M. Haberkamp, T.L. Laufs, A. Roesner, M. Schmidt, B. Weich, S. Wystub, S. Saaler-Reinhardt, S. Reuss,M. Bolognesi, D. DeSanctis, M.C. Marden, L. Kiger, L. Moens, S. Dewilde, E. Nevo, A. Avivi, R.E.Weber, A. Fago, T. Burmester, Neuroglobin and cytoglobin in search of their role in the vertebrate globin family, J. Inorg. Biochem. 99 (2005) 110-119.
54. J.S. Olson, G.N.J. Phillips, Kinetic pathways and barriers for ligand binding to myoglobin, J. Biol. Chem. 271 (1996) 17593-17596.
55. K. Nienhaus, P. Palladino, G.U. Nienhaus, Structural dynamics of myoglobin: FTIRTDS study of NO migration and binding, Biochemistry 47 (2008) 935-948. (Pubitemid 351147799)
56. R.E.J. Brantley, S.J. Smerdon, A.J. Wilkinson, E.W. Singleton, J.S. Olson, The mechanism of autoxidation of myoglobin, J. Biol. Chem. 268 (1993) 6995-7010.
57. E. Liong, Y. Dou, E. Scott, J. Olson, G. Phillips Jr., Waterproofing the heme pocket. Role of proximal amino acid side chains in preventing hemin loss from myoglobin, J. Biol. Chem. 276 (2001) 9093-9100.
58. M. Brunori, Nitric oxide, cytochrome-c oxidase, and myoglobin, TIBS 26 (2001) 21-23.
59. M. Brunori, Nitric oxide moves myoglobin centre stage, TIBS 26 (2001) 209-210. (Pubitemid 32289229)
60. A. Bidon-Chanal,M.A.Martí, A. Crespo, M. Milani,M. Orozco,M. Bolognesi, F.J. Luque, D.A. Estrin, Ligand-induced dynamical regulation ofNOconversion inMycobacterium tuberculosis truncated-hemoglobin-N, Proteins 64 (2006) 457-464. (Pubitemid 43993653)
61. M.A. Marti, A. Bidon-Chanal, A. Crespo, S.R. Yeh, V. Guallar, F.J. Luque, D.A. Estrin, Mechanismof product release in NO detoxification fromMycobacteriumtuberculosis truncated hemoglobin N, J. Am. Chem. Soc. 130 (2008) 1688-1693. (Pubitemid 351214088)
62. 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. U. S. A. 106 (2009) 18984-18989.