A phylogenetic and structural analysis of truncated hemoglobins

Journal of Molecular Evolution

Volumn 62, Issue 2, 2006, Pages 196-210

  Vuletich, David A ^a   Lecomte, Juliette T J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Gene transfer; Globin gene evolution; Globin structure; trHbN; trHbO; trHbP; Truncated globin; Two on two hemoglobin

Indexed keywords

HEMOGLOBIN; LIGAND;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; GENETICS; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN QUATERNARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; HEMOGLOBINS; LIGANDS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 33646341657     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-005-0077-4     Document Type: Article

References (65)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
2. Aurora R, Rose GD (1998) Helix capping. Protein Sci 7:21-38 (Pubitemid 28133743)
3. Baldwin J, Chothia C (1979) Haemoglobin: the structural changes related to ligand binding and its allosteric mechanism. J Mol Biol 129:175-220 (Pubitemid 9168805)
4. Bashford D, Chothia C, Lesk AM (1987) Determinants of a protein fold. Unique features of the globin amino acid sequences. J Mol Biol 196:199-216 (Pubitemid 17102240)
5. Bolognesi M, Bordo D, Rizzi M, Tarricone C, Ascenzi P (1997) Nonvertebrate hemoglobins: structural bases for reactivity. Prog Biophys Mol Biol 68:29-68 (Pubitemid 28066408)
6. Brown JR (2003) Ancient horizontal gene transfer. Nat Rev Genet 4:121-132
7. Clamp M, Cuff J, Searle SM, Barton GJ (2004) The Jalview Java alignment editor. Bioinformatics 20:426-427 (Pubitemid 38262778)
8. Couture M, Das TK, Lee HC, Peisach J, Rousseau DL, Wittenberg BA, Wittenberg JB, Guertin M (1999a) Chlamydomonas chloroplast ferrous hemoglobin. Heme pocket structure and reactions with ligands. J Biol Chem 274:6898-6910
9. Couture M, Yeh SR, Wittenberg BA, Wittenberg JB, Ouellet Y, Rousseau DL, Guertin M (1999b) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 96:11223-11228 (Pubitemid 29487362)
10. Couture M, Das TK, Savard PY, Ouellet Y, Wittenberg JB, Wittenberg BA, Rousseau DL, Guertin M (2000) Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket. Eur J Biochem 267:4770-4780 (Pubitemid 30619468)
11. Creevey CJ, Fitzpatrick DA, Philip GK, Kinsella RJ, O'Connell MJ, Pentony MM, Travers SA, Wilkinson M, McInerney JO (2004) Does a tree-like phylogeny only exist at the tips in the prokaryotes? Proc R Soc Lond B Biol Sci 271:2551-2558
12. Das TK, Weber RE, Dewilde S, Wittenberg JB, Wittenberg BA, Yamauchi K, Van Hauwaert ML, Moens L, Rousseau DL (2000) Ligand binding in the ferric and ferrous states of Paramecium hemoglobin. Biochemistry 39:14330-14340
13. Das TK, Couture M, Ouellet Y, Guertin M, Rousseau DL (2001) Simultaneous observation of the O-O and Fe-O2 stretching modes in oxyhemoglobins. Proc Natl Acad Sci USA 98:479-484 (Pubitemid 32105067)
14. Egawa T, Yeh SR (2005) Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy. J Inorg Biochem 99:72-96 (Pubitemid 39646480)
15. Falzone CJ, Vu BC, Scott NL, Lecomte JTJ (2002) The solution structure of the recombinant hemoglobin from the cyanobacterium Synechocystis sp. PCC 6803 in its hemichrome state. J Mol Biol 324:1015-1029 (Pubitemid 41782990)
16. Freitas TA, Saito JA, Hou S, Alam M (2005) Globin-coupled sensors, protoglobins, and the last universal common ancestor. J Inorg Biochem 99:23-33 (Pubitemid 39642969)
17. Frey AD, Kallio PT (2003) Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiol Rev 27:525-545 (Pubitemid 37205168)
18. Giangiacomo L, Ilari A, Boffi A, Morea V, Chiancone E (2005) The truncated oxygen-avid hemoglobin from Bacillus subtilis. X-ray structure and ligand binding properties. J Biol Chem 280:9192-9202 (Pubitemid 40409609)
19. Hardison RC (1996) A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc Natl Acad Sci USA 93:5675-5679
20. Hedges SB (2002) The origin and evolution of model organisms. Nat Rev Genet 3:838-849
21. Hill DR, Belbin TJ, Thorsteinsson MV, Bassam D, Brass S, Ernst A, Boger P, Paerl H, Mulligan ME, Potts M (1996) GlbN (cyanoglobin) is a peripheral membrane protein that is restricted to certain Nostoc spp. J Bacteriol 178:6587-6598 (Pubitemid 26374728)
22. Hiner AN, Raven EL, Thorneley RN, Garcia-Canovas F, Rodriguez-Lopez JN (2002) Mechanisms of compound I formation in heme peroxidases. J Inorg Biochem 91:27-34 (Pubitemid 34727758)
23. Hoy JA, Kundu S, Trent JT 3rd, Ramaswamy S, Hargrove MS (2004) The crystal structure of Synechocystis hemoglobin with a covalent heme linkage. J Biol Chem 279:16535-16542 (Pubitemid 38509353)
24. 10-helices and α-helices. Protein Sci 1:1333-1342
25. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, Phillips DC (1958) A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature 181:662-666
26. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17:1244-1245 (Pubitemid 33735359)
27. Kundu S, Trent JT 3rd, Hargrove MS (2003) Plants, humans and hemoglobins. Trends Plant Sci 8:387-393 (Pubitemid 37065225)
28. Lecomte JTJ, Scott NL, Vu BC, Falzone CJ (2001) Binding of ferric heme by the recombinant globin from the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 40:6541-6552 (Pubitemid 32472745)
29. Lecomte JTJ, Vuletich DA, Lesk AM (2005) Structural divergence and distant relationships in proteins: evolution of the globins. Curr Opin Struct Biol 15:290-301 (Pubitemid 40826448)
30. Lesk AM, Chothia C (1980) How different amino acid sequences determine similar protein structures: the structure and evolutionary dynamics of the globins. J Mol Biol 136:225-270
31. Milani M, Pesce A, Ouellet Y, Ascenzi P, Guertin M, Bolognesi M (2001) Mycobacterium tuberculosis hemoglobin N displays a protein tunnel suited for O2 diffusion to the heme. EMBO J 20:3902-3909 (Pubitemid 32751806)
32. Milani M, Savard PY, Ouellet H, Ascenzi P, Guertin M, Bolognesi M (2003) A TyrCD1/TrpG8 hydrogen bond network and a TyrB10TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O. Proc Natl Acad Sci USA 100:5766-5771 (Pubitemid 36576882)
33. Milani M, Ouellet Y, Ouellet H, Guertin M, Boffi A, Antonini G, Bocedi A, Mattu M, Bolognesi M, Ascenzi P (2004a) Cyanide binding to truncated hemoglobins: a crystallographic and kinetic study. Biochemistry 43:5213-5221 (Pubitemid 38620913)
34. Milani M, Pesce A, Ouellet Y, Dewilde S, Friedman JM, Ascenzi P, Guertin M, Bolognesi M (2004b) Heme-ligand tunneling in group I truncated hemoglobins. J Biol Chem 279:21520-21525 (Pubitemid 38656562)
35. Milani M, Pesce A, Nardini M, Ouellet H, Ouellet Y, Dewilde S, Bocedi A, Ascenzi P, Guertin M, Moens L, Friedman JM, Wittenberg JB, Bolognesi M (2005) Structural bases for heme binding and diatomic ligand recognition in truncated hemoglobins. J Inorg Biochem 99:97-109 (Pubitemid 39642973)
36. Moens L, Vanfleteren J, Van de Peer Y, Peeters K, Kapp O, Czeluzniak J, Goodman M, Blaxter M, Vinogradov S (1996) Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships. Mol Biol Evol 13:324-333 (Pubitemid 26035315)
37. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12:88-118
38. Nisbet RE, Kilian O, McFadden GI (2004) Diatom genomics: genetic acquisitions and mergers. Curr Biol 14:R1048-R1050 (Pubitemid 40042987)
39. Ouellet H, Ouellet Y, Richard C, Labarre M, Wittenberg B Wittenberg J, Guertin M (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc Natl Acad Sci USA 99:5902-5907 (Pubitemid 34493237)
40. Ouellet H, Juszczak L, Dantsker D, Samuni U, Ouellet YH, Savard PY, Wittenberg JB, Wittenberg BA, Friedman JM, Guertin M (2003) Reactions of Mycobacterium tuberculosis truncated hemoglobin O with ligands reveal a novel ligand-inclusive hydrogen bond network. Biochemistry 42:5764-5774 (Pubitemid 36582868)
41. Perutz MF (1979) Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annu Rev Biochem 48:327-386
42. Perutz MF (1990) Mechanisms of cooperativity and allosteric regulation in proteins. Cambridge University Press, Cambridge,
43. Pesce A, Couture M, Dewilde S, Guertin M, Yamauchi K, Ascenzi P, Moens L, Bolognesi M (2000) A novel two-over-two α-helical sandwich fold is characteristic of the truncated hemoglobin family. EMBO J 19:2424-2434 (Pubitemid 30323532)
44. Phillips SEV, Schoenborn BP (1981) Neutron diffraction reveals oxygen-histidine hydrogen bond in oxymyoglobin. Nature 292:81-82 (Pubitemid 11048554)
45. Porter RD (1986) Transformation in cyanobacteria. Crit Rev Microbiol 13:111-132
46. Presta LG, Rose GD (1988) Helix signals in proteins. Science 240:1632-1641
47. Ptitsyn OB, Ting KL (1999) Non-functional conserved residues in globins and their possible role as a folding nucleus. J Mol Biol 291:671-682 (Pubitemid 29392642)
48. Scala S, Carels N, Falciatore A, Chiusano ML, Bowler C (2002) Genome properties of the diatom Phaeodactylum tricornutum. Plant Physiol 129:993-1002 (Pubitemid 34801073)
49. Schloss PD, Handelsman J (2004) Status of the microbial census. Microbiol Mol Biol Rev 68:686-691 (Pubitemid 39628533)
50. Scott NL, Falzone CJ, Vuletich DA, Zhao J, Bryant DA, Lecomte JTJ (2002) Truncated hemoglobin from the cyanobacterium Synechococcus sp. PCC 7002: evidence for hexacoordination and covalent adduct formation in the ferric recombinant protein. Biochemistry 41:6902-6910 (Pubitemid 34575661)
51. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631-637 (Pubitemid 27464953)
52. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882 (Pubitemid 28022245)
53. Thorsteinsson MV, Bevan DR, Ebel RE, Weber RE, Potts M (1996) Spectroscopical and functional characterization of the hemoglobin of Nostoc commune UTEX 584 (Cyanobacteria). Biochim Biophys Acta 1292:133-139 (Pubitemid 26015433)
54. Trent JT 3rd, Kundu S, Hoy JA, Hargrove MS (2004) Crystallographic analysis of synechocystis cyanoglobin reveals the structural changes accompanying ligand binding in a hexacoordinate hemoglobin. J Mol Biol 341:1097-1108 (Pubitemid 39037366)
55. Vinogradov SN (1985) The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins). Comp Biochem Physiol B 82:1-15
56. Vinogradov SN, Walz DA, Pohajdak B, Moens L, Kapp OH, Suzuki T, Trotman CN (1993) Adventitious variability? The amino acid sequences of nonvertebrate globins. Comp Biochem Physiol B 106:1-26 (Pubitemid 23225864)
57. Visca P, Fabozzi G, Petrucca A, Ciaccio C, Coletta M, De Sanctis G, Bolognesi M, Milani M, Ascenzi P (2002) The truncated hemoglobin from Mycobacterium leprae. Biochem Biophys Res Commun 294:1064-1070
58. Vu BC, Jones AD, Lecomte JTJ (2002) Novel histidine-heme covalent linkage in a hemoglobin. J Am Chem Soc 124:8544-8545 (Pubitemid 34791020)
59. Vu BC, Nothnagel HJ, Vuletich DA, Falzone CJ, Lecomte JTJ (2004a) Cyanide binding to hexacoordinate cyanobacterial hemoglobins: hydrogen-bonding network and heme pocket rearrangement in ferric H117A Synechocystis hemoglobin. Biochemistry 43:12622-12633 (Pubitemid 39314724)
60. Vu BC, Vuletich DA, Kuriakose SA, Falzone CJ, Lecomte JTJ (2004b) Characterization of the heme-histidine cross-link in cyanobacterial hemoglobins from Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002. J Biol Inorg Chem 9:183-194 (Pubitemid 38327314)
61. Weber RE, Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81:569-628 (Pubitemid 32267074)
62. Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277:871-874 (Pubitemid 34968827)
63. Wu G, Wainwright LM, Poole RK (2003) Microbial globins. Adv Microb Physiol 47:255-310 (Pubitemid 37214152)
64. Yeh SR (2004) A novel intersubunit communication mechanism in a truncated hemoglobin from Mycobacterium tuberculosis. J Phys Chem B 108:1478-1484
65. Yeh SR, Couture M, Ouellet Y, Guertin M, Rousseau DL (2000) A cooperative oxygen binding hemoglobin from Mycobacterium tuberculosis. Stabilization of heme ligands by a distal tyrosine residue. J Biol Chem 275:1679-1684 (Pubitemid 30060786)