Hell's Gate globin I: An acid and thermostable bacterial hemoglobin resembling mammalian neuroglobin

FEBS Letters

Volumn 585, Issue 20, 2011, Pages 3250-3258

  Teh, Aik Hong ^a   Saito, Jennifer A ^a   Baharuddin, Aida ^a,i   Tuckerman, Jason R ^b   Newhouse, James S ^c   Kanbe, Masaomi ^a   Newhouse, Elizabeth I ^c   Rahim, Rashidah Abdul ^a   Favier, Frédérique ^d   Didierjean, Claude ^d   Sousa, Eduardo H S ^e   Stott, Matthew B ^f   Dunfield, Peter F ^g   Gonzalez, Gonzalo ^b   Gilles Gonzalez, Marie Alda ^b   Najimudin, Nazalan ^a   Alam, Maqsudul ^a,h  

^a SCHOOL OF PHYSICS   (Malaysia)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c Maui High Performance Computing Center   (United States)

^d Nancy University CNRS   (France)

^e FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^f GNS SCIENCE   (New Zealand)

^g UNIVERSITY OF CALGARY   (Canada)

^h UNIVERSITY OF HAWAII   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crystal structure; Globin; Hell's Gate globin I; Molecular dynamics; Oxidation resistance; Oxygen binding

Indexed keywords

BACTERIAL PROTEIN; HELL GATE GLOBIN I; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; METHANOTROPHIC BACTERIUM; METHYLACIDIPHILUM INFERNORUM; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; THERMOACIDOPHILIC BACTERIUM; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; GLOBINS; GRAM-NEGATIVE BACTERIA; HEMOGLOBINS; HUMANS; HYDROGEN-ION CONCENTRATION; NERVE TISSUE PROTEINS; OXYGEN; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 80054076084     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.09.002     Document Type: Article

References (52)

1. P.F. Dunfield, A. Yuryev, P. Senin, A.V. Smirnova, M.B. Stott, S. Hou, B. Ly, J.H. Saw, Z. Zhou, Y. Ren, J. Wang, B.W. Mountain, M.A. Crowe, T.M. Weatherby, P.L. Bodelier, W. Liesack, L. Feng, L. Wang, and M. Alam Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia Nature 450 2007 879 882 (Pubitemid 350231335)
2. S. Hou, K.S. Makarova, J.H. Saw, P. Senin, B.V. Ly, Z. Zhou, Y. Ren, J. Wang, M.Y. Galperin, M.V. Omelchenko, Y.I. Wolf, N. Yutin, E.V. Koonin, M.B. Stott, B.W. Mountain, M.A. Crowe, A.V. Smirnova, P.F. Dunfield, L. Feng, L. Wang, and M. Alam Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia Biol. Direct 3 2008 26
3. V. Garrocho-Villegas, S.K. Gopalasubramaniam, and R. Arredondo-Peter Plant hemoglobins: what we know six decades after their discovery Gene 398 2007 78 85 (Pubitemid 47082417)
4. H. Iwaasa, T. Takagi, and K. Shikama Amino acid sequence of yeast hemoglobin. A two-domain structure J. Mol. Biol. 227 1992 948 954
5. S.G. Vasudevan, W.L. Armarego, D.C. Shaw, P.E. Lilley, N.E. Dixon, and R.K. Poole Isolation and nucleotide sequence of the hmp gene that encodes a haemoglobin-like protein in Escherichia coli K-12 Mol. Gen. Genet. 226 1991 49 58
6. R.E. Weber, and S.N. Vinogradov Nonvertebrate hemoglobins: functions and molecular adaptations Physiol. Rev. 81 2001 569 628 (Pubitemid 32267074)
7. J.B. Wittenberg, M. Bolognesi, B.A. Wittenberg, and M. Guertin Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants J. Biol. Chem. 277 2002 871 874 (Pubitemid 34968827)
8. T. Burmester, B. Weich, S. Reinhardt, and T. Hankeln A vertebrate globin expressed in the brain Nature 407 2000 520 523
9. T. Burmester, B. Ebner, B. Weich, and T. Hankeln Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues Mol. Biol. Evol. 19 2002 416 421 (Pubitemid 34289416)
10. S. Hou, T. Freitas, R.W. Larsen, M. Piatibratov, V. Sivozhelezov, A. Yamamoto, E.A. Meleshkevitch, M. Zimmer, G.W. Ordal, and M. Alam Globin-coupled sensors: a class of heme-containing sensors in Archaea and Bacteria Proc. Natl. Acad. Sci. USA 98 2001 9353 9358 (Pubitemid 32743920)
11. T.A. Freitas, S. Hou, E.M. Dioum, J.A. Saito, J. Newhouse, G. Gonzalez, M.A. Gilles-Gonzalez, and M. Alam Ancestral hemoglobins in Archaea Proc. Natl. Acad. Sci. USA 101 2004 6675 6680 (Pubitemid 38586033)
12. J.J. Miranda, D.H. Maillett, J. Soman, and J.S. Olson Thermoglobin, oxygen-avid hemoglobin in a bacterial hyperthermophile J. Biol. Chem. 280 2005 36754 36761 (Pubitemid 41587755)
13. L. Holm, and C. Sander Structural alignment of globins, phycocyanins and colicin A FEBS Lett. 315 1993 301 306 (Pubitemid 23025028)
14. A. Pesce, M. Couture, S. Dewilde, M. Guertin, K. Yamauchi, P. Ascenzi, L. Moens, and M. Bolognesi A novel two-over-two α-helical sandwich fold is characteristic of the truncated hemoglobin family EMBO J. 19 2000 2424 2434 (Pubitemid 30323532)
15. M.D. Goodman, and M.S. Hargrove Quaternary structure of rice nonsymbiotic hemoglobin J. Biol. Chem. 276 2001 6834 6839
16. W. Kabsch Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants J. Appl. Cryst. 26 1993 795 800
17. T.C. Terwilliger, and J. Berendzen Automated MAD and MIR structure solution Acta Crystallogr. D55 1999 849 861 (Pubitemid 29194533)
18. T.C. Terwilliger Maximum-likelihood density modification Acta Crystallogr. D56 2000 965 972 (Pubitemid 30622779)
19. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D60 2004 2126 2132 (Pubitemid 41742764)
20. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53 1997 240 255 (Pubitemid 27235885)
21. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P. Zwart PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66 2010 213 221
22. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948 (Pubitemid 350162903)
23. L. Holm, and P. Rosenström Dali server: conservation mapping in 3D Nucleic Acids Res. 38 2010 W545 W549
24. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308 (Pubitemid 29213756)
25. R.A. Laskowski SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions J. Mol. Graph. 13 1995 323 330
26. J. Damborský, M. Petrek, P. Banás, and M. Otyepka Identification of tunnels in proteins, nucleic acids, inorganic materials and molecular ensembles Biotechnol. J. 2 2007 62 67 (Pubitemid 46744756)
27. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
28. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kalé, and K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
29. G. Kaminski, R.A. Friesner, J. Tirado-Rives, and W.L. Jorgensen Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides J. Phys. Chem. B 105 2001 6474 6487 (Pubitemid 35339015)
30. I. De Baere, M.F. Perutz, L. Kiger, M.C. Marden, and C. Poyart Formation of two hydrogen bonds from the globin to the heme-linked oxygen molecule in Ascaris hemoglobin Proc. Natl. Acad. Sci. USA 91 1994 1594 1597 (Pubitemid 24059059)
31. M.L. Quillin, R.M. Arduini, J.S. Olson, and G.N.Jr. Philips High-resolution crystal structures of distal histidine mutants of sperm whale myoglobin J. Mol. Biol. 234 1993 140 155 (Pubitemid 23337970)
32. M.S. Hargrove, J.K. Barry, E.A. Brucker, M.B. Berry, G.N.Jr. Phillips, J.S. Olson, R. Arredondo-Peter, J.M. Dean, R.V. Klucas, and G. Sarath Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants J. Mol. Biol. 266 1997 1032 1042 (Pubitemid 27122607)
33. A. Pesce, S. Dewilde, M. Nardini, L. Moens, P. Ascenzi, T. Hankeln, T. Burmester, and M. Bolognesi Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity Structure 11 2003 1087 1095 (Pubitemid 37103070)
34. B. Vallone, K. Nienhaus, A. Matthes, M. Brunori, and 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)
35. M. Shepherd, V. Barynin, C. Lu, P.V. Bernhardt, G. Wu, S.R. Yeh, T. Egawa, S.E. Sedelnikova, D.W. Rice, J.L. Wilson, and R.K. Poole The single-domain globin from the pathogenic bacterium Campylobacter jejuni: novel D-helix conformation, proximal hydrogen bonding that influences ligand binding, and peroxidase-like redox properties J. Biol. Chem. 285 2010 12747 12754
36. C. Tarricone, A. Galizzi, A. Coda, P. Ascenzi, and M. Bolognesi Unusual structure of the oxygen-binding site in the dimeric bacterial hemoglobin from Vitreoscilla sp. Structure 5 1997 497 507 (Pubitemid 27191226)
37. U. Ermler, R.A. Siddiqui, R. Cramm, and B. Friedrich Crystal structure of the flavohemoglobin from Alcaligenes eutrophus at 1.75 resolution EMBO J. 14 1995 6067 6077
38. A. Ilari, A. Bonamore, A. Farina, K.A. Johnson, and A. Boffi The X-ray structure of ferric Escherichia coli flavohemoglobin reveals an unexpected geometry of the distal heme pocket J. Biol. Chem. 277 2002 23725 23732 (Pubitemid 34952213)
39. J. Vojtechovský, K. Chu, J. Berendzen, R.M. Sweet, and I. Schlichting Crystal structures of myoglobin-ligand complexes at near-atomic resolution Biophys. J. 77 1999 2153 2174 (Pubitemid 29463176)
40. D. de Sanctis, S. Dewilde, A. Pesce, L. Moens, P. Ascenzi, T. Hankeln, T. Burmester, and M. Bolognesi Crystal structure of cytoglobin: the fourth globin type discovered in man displays heme hexa-coordination J. Mol. Biol. 336 2004 917 927 (Pubitemid 38202333)
41. H. Sugimoto, M. Makino, H. Sawai, N. Kawada, K. Yoshizato, and Y. Shiro Structural basis of human cytoglobin for ligand binding J. Mol. Biol. 339 2004 873 885 (Pubitemid 38686350)
42. J. Yang, A.P. Kloek, D.E. Goldberg, and F.S. Mathews The structure of Ascaris hemoglobin domain I at 2.2 resolution: molecular features of oxygen avidity Proc. Natl. Acad. Sci. USA 92 1995 4224 4228
43. A. Pesce, M. Nardini, S. Dewilde, E. Geuens, K. Yamauchi, P. Ascenzi, A.F. Riggs, L. Moens, and M. Bolognesi The 109 residue nerve tissue minihemoglobin from Cerebratulus lacteus highlights striking structural plasticity of the alpha-helical globin fold Structure 10 2002 725 735 (Pubitemid 34518713)
44. B. Vallone, K. Nienhaus, M. Brunori, and G.U. Nienhaus The structure of murine neuroglobin: novel pathways for ligand migration and binding Proteins 56 2004 85 92 (Pubitemid 38720840)
45. 2 affinity in Cerebratulus lacteus mini-hemoglobin J. Biol. Chem. 279 2004 33662 33672 (Pubitemid 39063016)
46. A. Bonamore, A. Ilari, L. Giangiacomo, A. Bellelli, V. Morea, and A. Boffi A novel thermostable hemoglobin from the actinobacterium Thermobifida fusca FEBS J. 272 2005 4189 4201 (Pubitemid 41160925)
47. A. Ilari, P. Kjelgaard, C. von Wachenfeldt, B. Catacchio, E. Chiancone, and A. Boffi Crystal structure and ligand binding properties of the truncated hemoglobin from Geobacillus stearothermophilus Arch. Biochem. Biophys. 457 2007 85 94 (Pubitemid 44969279)
48. A. Pesce, M. Nardini, S. Dewilde, L. Capece, M.A. Martí, S. Congia, M.D. Salter, G.C. Blouin, D.A. Estrin, P. Ascenzi, L. Moens, M. Bolognesi, and J.S. Olson Ligand migration in the apolar tunnel of Cerebratulus lacteus mini-hemoglobin J. Biol. Chem. 286 2011 5347 5358
49. 2 entry and exit J. Biol. Chem. 283 2008 35689 35702
50. S.N. Vinogradov, D. Hoogewijs, X. Bailly, R. Arredondo-Peter, M. Guertin, J. Gough, S. Dewilde, L. Moens, and J.R. Vanfleteren Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life Proc. Natl. Acad. Sci. USA 102 2005 11385 11389 (Pubitemid 41153829)
51. S.N. Vinogradov, D. Hoogewijs, X. Bailly, R. Arredondo-Peter, J. Gough, S. Dewilde, L. Moens, and J.R. Vanfleteren A phylogenomic profile of globins BMC Evol. Biol. 6 2006 31
52. S.N. Vinogradov, D. Hoogewijs, X. Bailly, K. Mizuguchi, S. Dewilde, L. Moens, and J.R. Vanfleteren A model of globin evolution Gene 398 2007 132 142 (Pubitemid 47068897)