The structure of murine neuroglobin: Novel pathways for ligand migration and binding

Proteins: Structure, Function and Genetics

Volumn 56, Issue 1, 2004, Pages 85-92

  Vallone, Beatrice ^a   Nienhaus, Karin ^b   Brunori, Maurizio ^a   Nienhaus, G Ulrich ^b,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF ULM   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; FERROUS ION; HEME; HEMOGLOBIN; LIGAND; MYOGLOBIN; NEUROGLOBIN; POLYPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; BRAIN; CRYSTAL STRUCTURE; CRYSTALLIZATION; ESCHERICHIA COLI; HYDROGEN BOND; HYPOXIA; LIGAND BINDING; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; GLOBINS; HEME; HYDROPHOBICITY; LIGANDS; MICE; MODELS, MOLECULAR; MUTATION; NERVE TISSUE PROTEINS; PLIABILITY; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP;

MURINAE; VERTEBRATA;

EID: 2642521269     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20113     Document Type: Article

References (56)

1. Perutz MF. Stereochemistry of cooperative effects in haemoglobin. Nature 1970;228:726-739.
2. Antonini E, Brunori, M. Hemoglobin and myoglobin in their reactions with ligands. Amsterdam: North-Holland, 1971.
3. Perutz MF. Myoglobin and haemoglobin: role of distal residues in reactions with haem ligands. Trends Biochem Sci. 1989;14:42-44.
4. Frauenfelder H, McMahon BH, Austin RH, Chu K, Groves JT. The role of structure, energy landscape, dynamics, and allostery in the enzymatic function of myoglobin. Proc Natl Acad Sci USA 2001;98: 2370-2374.
5. Pesce A, Bolognesi M, Bocedi A, Ascenzi P, Dewilde S, Moens L, Hankeln T, Burmester T. Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep. 2002;3:1146-1151.
6. Couture M, Yeh SR, Wittenberg BA, Wittenberg JB, Ouellet Y, Rousseau DL, Guertin M. A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 1999;96:11223-11228.
7. Yeh SR, Couture M, Ouellet Y, Guertin M, Rousseau DL. A cooperative oxygen binding hemoglobin from Mycobacterium tuberculosis. Stabilization of heme ligands by a distal tyrosine residue. J Biol Chem 2000;275:1679-1684.
8. Hankeln T, Rozynek P, Schmidt ER. The nucleotide sequence and in situ localization of a gene for a dimeric haemoglobin from the midge Chironomus thummi piger. Gene 1988;64:297-304.
9. Gardner PR, Gardner AM, Martin LA, Salzman AL. Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc Natl Acad Sci USA 1998;95:10378-10383.
10. Potts M, Angeloni SV, Ebel RE, Bassam D. Myoglobin in a cyanobacterium. Science 1992;256:1690-1691.
11. Couture M, Das TK, Lee HC, Peisach J, Rousseau DL, Wittenberg BA, Wittenberg JB, Guertin M. Chlamydomonas chloroplast ferrous hemoglobin. Heme pocket structure and reactions with ligands. J Biol Chem 1999;274:6898-6910.
12. Burmester T, Weich B, Reinhardt S, Hankeln T. A vertebrate globin expressed in the brain. Nature 2000;407:520-523.
13. Dewilde S, Blaxter M, Van Hauwaert ML, Vanfleteren J, Esmans EL, Marden M, Griffon N, Moens L. Globin and globin gene structure of the nerve myoglobin of Aphrodite aculeata. J Biol Chem 1996;271:19865-19870.
14. Sun Y, Jin K, Peel A, Mao XO, Xie L, Greenberg DA. Neuroglobin protects the brain from experimental stroke in vivo. Proc Natl Acad Sci USA 2003;100:3497-3500.
15. Bashford D, Chothia C, Lesk AM. Determinants of a protein fold. Unique features of the globin amino acid sequences. J Mol Biol 1987;196:199-216.
16. Pesce A, Dewilde S, Nardini M, Moens L, Ascenzi P, Hankeln T, Burmester T, Bolognesi M. Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity. Structure (Camb) 2003;11:1087-1095.
17. Couture M, Burmester T, Hankeln T, Rousseau DL. The heme environment of mouse neuroglobin. Evidence for the presence of two conformations of the heme pocket. J Biol Chem 2001;276: 36377-36382.
18. Kriegl JM, Bhattacharyya AJ, Nienhaus K, Deng P, Minkow O, Nienhaus GU. Ligand binding and protein dynamics in neuroglobin. Proc Natl Acad Sci USA 2002;99:7992-7997.
19. Trent JT, Watts RA, Hargrove MS. Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J Biol Chem 2001;276:30106-30110.
20. Couture M, Das TK, Savard PY, Ouellet Y, Wittenberg JB, Wittenberg BA, Rousseau DL, Guertin M. Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket. Eur J Biochem 2000;267:4770-4780.
21. Scott NL, Falzone CJ, Vuletich DA, Zhao J, Bryant DA, Lecomte JT. Truncated hemoglobin from the cyanobacterium Synechococcus sp. PCC 7002: evidence for hexacoordination and covalent adduct formation in the ferric recombinant protein. Biochemistry 2002;41:6902-6910.
22. Goodman MD, Hargrove MS. Quaternary structure of rice nonsymbiotic hemoglobin. J Biol Chem 2001;276:6834-6839.
23. Hargrove MS, Brucker EA, Stec B, Sarath G, Arredondo-Peter R, Klucas RV, Olson JS, Phillips GN, Jr. Crystal structure of a nonsymbiotic plant hemoglobin. Structure Fold Des 2000;8:1005-1014.
24. Arrendondo-Peter R, Hargrove MS, Sarath G, Moran JF, Lohrman J, Olson JS, Klucas RV. Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiol 1997;115:1259-1266.
25. Sun Y, Jin K, Mao XO, Zhu Y, Greenberg DA. Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury. Proc Natl Acad Sci USA 2001;98:15306-15311.
26. Otwinowski Z, Minor W. Processing X-ray diffraction data collected in oscillation mode. Methods Enzymol 1996;276:307-326.
27. Dauter Z, Dauter M, Dodson E. Jolly SAD. Acta Crystallogr D Biol Crystallogr 2002;58:494-506.
28. Terwilliger TC, Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 1999;55:849-861.
29. Terwilliger TC. Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 2000;56:965-972.
30. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. Procheck - a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
31. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994;50:760-763.
32. Laskowski RA. SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions. J Mol Graph 1995;13:323-330.
33. Holm L, Sander C. Protein folds and families: sequence and structure alignments. Nucleic Acids Res 1999;27:244-247.
34. Holm L, Ouzounis C, Sander C, Tuparev G, Vriend G. A database of protein structure families with common folding motifs. Protein Sci 1992;1:1691-1998.
35. Shindyalov IN, Bourne PE. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 1998;11:739-747.
36. Kachalova GS, Popov AN, Bartunik HD. A steric mechanism for inhibition of CO binding to heme proteins. Science 1999;284:473-476.
37. Du W, Syvitski R, Dewilde S, Moens L, La Mar GN. Solution (1)h NMR characterization of equilibrium heme orientational disorder with functional consequences in mouse neuroglobin. J Am Chem Soc 2003;125:8080-8081.
38. Ormos P, Szaraz S, Cupane A, Nienhaus GU. Structural factors controlling ligand binding to myoglobin: a kinetic hole-burning study. Proc Natl Acad Sci USA 1998;95:6762-6767.
39. Liong EC, Dou Y, Scott EE, Olson JS, Phillips GN, Jr. Waterproofing the heme pocket. Role of proximal amino acid side chains in preventing hemin loss from myoglobin. J Biol Chem 2001;276: 9093-9100.
40. Conti E, Moser C, Rizzi M, Mattevi A, Lionetti C, Coda A, Ascenzi P, Brunori M, Bolognesi M. X-ray crystal structure of ferric Aplysia limacina myoglobin in different liganded states. J Mol Biol 1993;233:498-508.
41. De Baere I, Perutz MF, Kiger L, Marden MC, Poyart C. Formation of two hydrogen bonds from the globin to the heme-linked oxygen molecule in Ascaris hemoglobin. Proc Natl Acad Sci USA 1994;91: 1594-1597.
42. Horovitz A, Serrano L, Avron B, Bycroft M, Fersht A R, Strength and cooperativity of contributions of surface salt bridges to protein stability. J Mol Biol 1990;216:1031-1044.
43. Takano K, Tsuchimori K, Yamagata Y, Yutani K, Contribution of salt bridges near the surface of a protein to the conformational stability. Biochemistry 2000;39:12375-12381.
44. Tilton RF, Jr., Kuntz ID, Jr., Petsko GA. Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 Å. Biochemistry 1984;23:2849-2857.
45. Nienhaus K, Deng P, Kriegl JM, Nienhaus GU. Structural dynamics of myoglobin: the effect of internal cavities on ligand migration and binding. Biochemistry 2003;42:9647-9658.
46. Nienhaus K, Deng P, Kriegl JM, Nienhaus GU. Structural dynamics of myoglobin: spectroscopic and structural characterization of ligand docking sites in myoglobin mutant L29W. Biochemistry 2003;42:9633-9646.
47. Scott EE, Gibson QH, Olson JS. Mapping the pathways for 02 entry into and exit from myoglobin. J Biol Chem 2001;276:5177-5188.
48. Brunori M, Gibson QH. Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep 2001;2:674-679.
49. Ostermann A, Waschipky R, Parak FG, Nienhaus GU. Ligand binding and conformational motions in myoglobin. Nature 2000; 404:205-208.
50. Bourgeois D, Vallone B, Schotte F, Arcovito A, Miele AE, Sciara G, Wulff M, Anfinrud P, Brunori M. Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography. Proc Natl Acad Sci USA 2003; 100:8704-8709.
51. Pesce A, Nardini M, Dewilde S, Ascenzi P, Riggs AF, Yamauchi K, Geuens E, Moens L, Bolognesi M. Crystallization and preliminary X-ray analysis of neural haemoglobin from the nemertean worm Cerebratulus lacteus. Acta Crystallogr D Biol Crystallogr 2001;57:1897-1899.
52. Milani M, Pesce A, Ouellet Y, Ascenzi P, Guertin M, Bolognesi M. Mycobacterium tuberculosis hemoglobin N displays a protein tunnel suited for O2 diffusion to the heme. EMBO J 2001;20:3902-3909.
53. Hargrove MS. A flash photolysis method to characterize hexacoordinate hemoglobin kinetics. Biophys J 2000;79:2733-2738.
54. Perutz MF, Mathews, F. S. An x-ray study of azide methaemoglobin. J Mol Biol 1966:21:199-202.
55. Van Doorslaer S, Dewilde S, Kiger L, Nistor SV, Goovaerts E, Marden MC, Moens L. Nitric oxide binding properties of neuroglobin. A characterization by EPR and flash photolysis. J Biol Chem 2003;278:4919-4925.
56. Lawson DM, Stevenson CE, Andrew CR, Eady RR. Unprecedented proximal binding of nitric oxide to heme: implications for guanylate cyclase. Embo J 2000;19:5661-5671.