Structural analysis in nonsymbiotic hemoglobins: What can we learn from inner cavities?

Plant Science

Volumn 181, Issue 1, 2011, Pages 8-13

  Spyrakis, Francesca ^a,b   Luque, F Javier ^c   Viappiani, Cristiano ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Docking sites; Ligand binding; Nonsymbiotic hemoglobins; Protein dynamics; Structure function relationship

Indexed keywords

AHB1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; HEMOGLOBIN; NITRIC OXIDE; NITRIC OXIDE DIOXYGENASE; OXYGENASE; VEGETABLE PROTEIN;

CHEMICAL PHENOMENA; CHEMISTRY; GENE EXPRESSION REGULATION; METABOLISM; PROTEIN TERTIARY STRUCTURE; REVIEW; X RAY CRYSTALLOGRAPHY;

ARABIDOPSIS PROTEINS; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION, PLANT; HEMOGLOBINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; NITRIC OXIDE; OXYGENASES; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS);

EID: 79956047307     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2011.03.021     Document Type: Review

References (65)

1. Appleby C.A. Leghemoglobin and rhizobium respiration. Annu. Rev. Plant Physiol. 1984, 35:443-478.
2. Bogusz D., Appleby C.A., Landsmann J., Dennis E.S., Trinick M.J., Peacock W.J. Functioning hemoglobin genes in non-nodulating plants. Nature 1988, 331:178-180.
3. Arredondo-Peter R., Hargrove M.S., Sarath C., Moran J.F., Lohrman J., Olson J.S., Klucas R.V. Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiol. 1997, 115:1259-1266.
4. Trevaskis B., Watts R.A., Andersson C.R., Llewellyn D.J., Hargrove M.S., Olson J.S., Dennis E.S., Peacock W.J. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:12230-12234.
5. Wang Y.H., Kochian L.V., Doyle J.J., Garvin D.F. Two tomato non-symbiotic haemoglobin genes are differentially expressed in response to diverse changes in mineral nutrient status. Plant Cell Environ. 2003, 26:673-680.
6. 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., Appleby C.A. Correlations between oxygen affinity and sequence classifications of plant hemoglobins. Biopolymers 2009, 91:1083-1096.
7. Hunt P.W., Watts R.A., Trevaskis B., Llewelyn D.J., Burnell J., Dennis E.S., Peacock W.J. Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Mol. Biol. 2001, 47:677-692.
8. Dordas C. Nonsymbiotic hemoglobins and stress tolerance in plants. Plant Sci. 2009, 176:433-440.
9. Taylor E.R., Nie X.Z., MacGregor A.W., Hill R.D. A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol. Biol. 1994, 24:853-862.
10. Lira-Ruan V., Sarath G., Klucas R.V., Arredondo-Peter R. Synthesis of hemoglobins in rice (Oryza sativa var. Jackson) plants growing in normal and stress conditions. Plant Sci. 2001, 161:279-287.
11. Qu Z.L., Wang H.Y., Xia G.X. GhHb1: a nonsymbiotic hemoglobin gene of cotton responsive to infection by Verticillium dahliae. Biochim. Biophys. Acta Gene Struct. Expr. 2005, 1730:103-113.
12. Wang R., Guegler K., LaBrie S.T., Crawford N.M. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 2000, 12:1491-1509.
13. Nie X., Hill R.D. Mitochondrial respiration and hemoglobin gene expression in barley aleurone tissue. Plant Physiol. 1997, 114:835-840.
14. Bruno S., Faggiano S., Spyrakis F., Mozzarelli A., Abbruzzetti S., Grandi E., Viappiani C., Feis A., Mackowiak S., Smulevich G., Cacciatori E., Dominici P. 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. 2007, 129:2880-2889.
15. Smagghe B.J., Trent J.T., Hargrove M.S. NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo. PLoS ONE 2008, 3:e2039.
16. Perazzolli M, Romero-Puertas M.C., Delledonne M. Modulation of nitric oxide bioactivity by plant haemoglobins. J. Exp. Bot. 2006, 57:479-488.
17. Perazzolli M., Dominici P., Puertas M.C.R., Zago E., Zeier J., Sonoda M., Lamb C., Delledonne M. Non-symbiotic hemoglobin AHb1 modulates nitric oxyde bioactivity in Arabidopsis thaliana. Plant Cell 2004, 16:2785-2794.
18. Hendriks T., Scheer I., Quillet M.C., Randoux B., Delbreil B., Vasseur J., Hilbert J.L. A nonsymbiotic hemoglobin gene is expressed during somatic embryogenesis in Cichorium. Biochim. Biophys. Acta Gene Struct. Expr. 1998, 1443:193-197.
19. Schotte F., Lim M., Jackson T.A., Smirnov A.V., Soman J., Olson J.S., G.N.P., Wulff M., Anfinrud P.A. Watching a protein as it functions with 150-ps time-resolved X-ray crystallography. Science 2003, 300:1944-1947.
20. Bourgeois D., Vallone B., Arcovito A., Sciara G., Schotte F., Anfinrud P.A., Brunori M. Extended subnanosecond structural dynamics of myoglobin revealed by Laue crystallography. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4924-4929.
21. Kriegl J.M., Bhattacharyya A.J., Nienhaus K., Deng P., Minkow O., Nienhaus G.U. Ligand binding and protein dynamics in neuroglobin. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:7992-7997.
22. Nienhaus K., Dominici P., Astegno A., Abbruzzetti S., Viappiani C., Nienhaus G.U. Ligand migration and binding in non-symbiotic hemoglobins of Arabidopsis thaliana. Biochemistry 2010, 49:7448-7458.
23. Abbruzzetti S., Bruno S., Faggiano S., Grandi E., Mozzarelli A., Viappiani C. Monitoring haem proteins at work with nanosecond laser flash photolysis. Photochem. Photobiol. Sci. 2006, 5:1109-1120.
24. Sottini S., Abbruzzetti S., Viappiani C., Ronda L., Mozzarelli A. Determination of microscopic rate constants for CO binding and migration in myoglobin encapsulated in silica gels. J. Phys. Chem. B 2005, 109:19523-19528.
25. Bruno S., Faggiano S., Spyrakis F., Mozzarelli A., Cacciatori E., Dominici P., Grandi E., Abbruzzetti S., Viappiani C. Different roles of protein dynamics and ligand migration in non-symbiotic hemoglobins AHb1 and AHb2 from Arabidopsis thaliana. Gene 2007, 398:224-233.
26. Abbruzzetti S., Grandi E., Bruno S., Faggiano S., Spyrakis F., Mozzarelli A., Dominici P., Viappiani C. Ligand migration in non symbiotic hemoglobin AHb1 from Arabidopsis thaliana. J. Phys. Chem. B 2007, 111:12582-12590.
27. Abbruzzetti S., Faggiano S., Bruno S., Spyrakis F., Mozzarelli A., Dewilde S., Moens L., Viappiani C. Ligand migration through the internal hydrophobic cavities in human neuroglobin. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18984-18989.
28. Smagghe B.J., Kundu S., Hoy J.A., Halder P., Weiland T.R., Savage A., Venugopal A., Goodman M., Premer S., Hargrove M.S. Role of phenylalanine B10 in plant nonsymbiotic hemoglobins. Biochemistry 2006, 45:9735-9745.
29. 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., Luque F.J. 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 2009, 113:16028-16038.
30. Smulevich G., Mauro J.M., Fishel L.A., English A.M., Kraut J., Spiro T.G. Cytochrome c peroxidase mutant active site structures probed by resonance raman and infrared signatures of the CO adducts. Biochemistry 1988, 27:5486-5492.
31. Spyrakis F., Faggiano S., Abbruzzetti S., Dominici P., Cacciatori E., Astegno A., Droghetti E., Feis A., Smulevich G., Bruno S., Mozzarelli A., Cozzini P., Viappiani C., Bidon-Chanal A., Luque F.J. Histidine E7 dynamics modulates ligand exchange between distal pocket and solvent in AHb1 from Arabidopsis thaliana. J. Phys. Chem. B 2011, 115:4138-4146.
32. Dewilde S., Kiger L., Burmester T., Hankeln T., Baudin-Creuza V., Aerts T., Marden M.C., Caubergs R., Moens L. Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J. Biol. Chem. 2001, 276:38949-38955.
33. Shikama K. The molecular mechanism of autoxidation for myoglobin and haemoglobin: a venerable puzzle. Chem. Rev. 1998, 98:1357-1373.
34. Kakar S., Hoffman F.G., Storz J.F., Fabian M., Hargrove M.S. Structure and reactivity of hexacoordinate hemoglobins. Biophys. Chem. 2010, 152:1-14.
35. Ioanitescu A.I., Dewilde S., Kiger L., Marden M.C., Moens L., VanDoorslaer S. Characterization of nonsymbiotic tomato hemoglobin. Biophys. J. 2005, 89:2628-2639.
36. Uzan J., Dewilde S., Burmester T., Hankeln T., Moens L., Hamdane D., Marden M.C., Kiger L. Neuroglobin and other hexacoordinated hemoglobins show a weak temperature dependence of oxygen binding. Biophys. J. 2004, 87:1196-1204.
37. Hamdane D., Kiger L., Hoa G.H.B., Dewilde S., Uzan J., Burmester T., Hankeln T., Moens L., Marden M.C. High pressure enhances hexacoordination in neuroglobin and other globins. J. Biol. Chem. 2005, 280:36809-36814.
38. Smagghe B.J., Sarath G., Ross E., Hilbert J.L., Hargrove M.S. Slow ligand binding kinetics dominate ferrous hexacoordinate hemoglobin reactivities and reveal differences between plants and other species. Biochemistry 2006, 45:561-570.
39. Brunori M. Nitric oxide, cytochrome-c oxidase, and myoglobin. TIBS 2001, 26:21-23.
40. Brunori M Nitric oxide moves myoglobin centre stage. TIBS 2001, 26:209-210.
41. Brunori M., Gibson Q.H. Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep. 2001, 2:674-679.
42. Ouellet H., Ouellet Y., Richard C., Labarre M., Wittenberg B.W., Guertin M. Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:5902-5907.
43. Brunori M., Giuffre' A., Nienhaus K., Nienhaus G.U., Scandurra F.M., Vallone B. Neuroglobin, nitric oxide, and oxygen: functional pathways and conformational changes. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8483-8488.
44. Tilton R.F.J., Kuntz I.D.J., Petsko G.A. Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 A. Biochemistry 1984, 23:2849-2857.
45. Milani M., Pesce A., Ouellet Y., Dewilde S., Friedman J., Ascenzi P., Guertin M., Bolognesi M. Heme-ligand tunneling in group I truncated hemoglobins. J. Biol. Chem. 2004, 279:21520-21525.
46. Pesce A., Dewilde S., Nardini M., Moens L., Ascenzi P., Hankeln T., Bolognesi T.B. Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity. Structure 2003, 11:1087-1095.
47. Vallone B., Nienhaus K., Matthes A., Brunori M., Nienhaus G.U. The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17351-17356.
48. Moschetti T., Mueller U., Schulze J., Brunori M., Vallone B. The structure of neuroglobin at high Xe and Kr pressure reveals partial conservation of globin internal cavities. Biophys. J. 2009, 97:1700-1708.
49. Bidon-Chanal A., Martí M.A., Crespo A., Milani M., Orozco M., Bolognesi M., Luque F.J., Estrin D.A. Ligand-induced dynamical regulation of NO conversion in Mycobacterium tuberculosis truncated-hemoglobin-N. Proteins 2006, 64:457-464.
50. Marti M.A., Bidon-Chanal A., Crespo A., Yeh S.R., Guallar V., Luque F.J., Estrin D.A. Mechanism of product release in NO detoxification from Mycobacterium tuberculosis truncated hemoglobin N. J. Am. Chem. Soc. 2008, 130:1688-1693.
51. Cohen J., Schulten K. O2 migration pathways are not conserved across proteins of a similar fold. Biophys. J. 2007, 93:3591-3600.
52. Hargrove M.S., Brucker E.A., Stec B., Sarath G., Arredondo-Peter R., Klucas R.V., Olson J.S., G.N.P. Crystal structure of a nonsymbiotic plant hemoglobin. Structure 2000, 8:1005-1014.
53. Hoy J.A., Robinson H., Trent J.T., Kakar S., Smagge B.J., Hargrove M.S. Plant hemoglobins: a molecular fossil record for the evolution of oxygen transport. J. Mol. Biol. 2007, 371:168-179.
54. LeGuilloux V., Schmidtke P., Tuffery P. Fpocket: an open source platform for ligand pocket detection. BMC Bioinformatics 2009, 10:168.
55. Belenghi B., Romero-Puertas M.C., Vercammen D., Brackenier A., Inze D., Delledonne M., Breusegem F.V. Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J. Biol. Chem. 2007, 282:1352-1358.
56. Nadra A., Marti M.A., Pesce A., Bolognesi M., Estrin D.A. Exploring the molecular basis of heme coordination in human neuroglobin. Proteins 2007, 71:695-705.
57. Maragliano L., Cottone G., Ciccotti G., Vanden-Eijnden E. Mapping the network of pathways of CO diffusion in myoglobin. J. Am. Chem. Soc. 2009, 132:1010-1017.
58. Orlowski S., Nowak W. Locally enhanced sampling molecular dynamics study of the dioxygen transport in human cytoglobin. J. Mol. Model. 2007, 13:715-723.
59. Droghetti E., Nicoletti F.P., Bonamore A., Boechi L., Manez P.A., Estrin D.A., Boffi A., Smulevich G., Feis A. Heme pocket structural properties of a bacterial truncated hemoglobin from Thermobifida fusca. Biochemistry 2010, 49:10394-10402.
60. Bidon-Chanal A., Marti M.A., Estrin D.A., Luque F.J. Dynamical regulation of ligand migration by a gate-opening molecular switch in truncated hemoglobin-N from Mycobacterium tuberculosi. J. Am. Chem. Soc. 2007, 129:6782-6788.
61. Knapp J.E., Pahl R., Cohen J., Nichols J.C., Schulten K., Gibson Q.H., Šrajer V., Royer W.E. Ligand migration and cavities within Scapharca dimeric HbI: studies by time-resolved crystallography, Xe binding, and computational analysis. Structure 2009, 17:1494-1504.
62. Carlson M.L, Regan R.M., Gibson Q.H. Biochemistry 1996, 35:1125-1136.
63. Nelson D.L., Lehninger A.L., Cox M.M. Lehninger Principles of Biochemistry 2008, WH Freeman, New York. fifth ed.
64. Mattevi A., Gatti G., Coda A., Rizzi M., Ascenzi P., Brunori M., Bolognesi M. Binding mode of azide to ferric Aplysia limacina myoglobin. Crystallographic analysis at 1.9 resolution. J. Mol. Recog. 1991, 4:1-6.
65. Smith L.J., Kahraman A., Thornton J.M. Heme proteins-Diversity in structural characteristics, function, and folding. Proteins 2010, 78:2349-2368.