Modulation of oxygen binding to insect hemoglobins: The structure of hemoglobin from the botfly Gasterophilus intestinalis

Protein Science

Volumn 14, Issue 12, 2005, Pages 3057-3063

  Pesce, Alessandra ^a   Nardini, Marco ^b   Dewilde, Sylvia ^c   Hoogewijs, David ^d   Ascenzi, Paolo ^e   Moens, Luc ^c   Bolognesi, Martino ^b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

^e ROMA TRE UNIVERSITY   (Italy)

Author keywords

Gasterophilus intestinalis hemoglobin; Heme hexa penta coordination; Insect hemoglobin; Oxygen recognition; Parasitic botfly hemoglobin; Protein structure

Indexed keywords

HEME; HEMOGLOBIN; OXYGEN;

ARTICLE; BINDING AFFINITY; CHIRONOMIDAE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEOXYGENATION; DROSOPHILA MELANOGASTER; FLY; GASTEROPHILUS INTESTINALIS; MOLECULAR MECHANICS; NONHUMAN; OXYGEN AFFINITY; OXYGENATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SPECIES COMPARISON;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DIPTERA; HEMOGLOBINS; MOLECULAR SEQUENCE DATA; OXYGEN; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

CHIRONOMIDAE; CHIRONOMUS THUMMI THUMMI; DROSOPHILA MELANOGASTER; GASTEROPHILUS INTESTINALIS; INSECTA;

EID: 28844471469     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051742605     Document Type: Article

References (48)

1. Antonini, E. and Brunori, M. 1971. Hemoglobin and myoglobin in their reactions with ligands. North Holland Publishing, Amsterdam.
2. Bergstrom, G. 1999. Chironomus. In The encyclopedia of molecular biology (ed. T. Creighton), pp. 420-426. Wiley, New York.
3. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., and Bourne, P.E. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235-242.
4. Bolognesi, M., Cannillo, E., Ascenzi, P., Giacometti, G.M., Merli, A., and Brunori, M. 1982. Reactivity of ferric Aplysia and sperm whale myoglobins towards imidazole. X-ray and binding study. J. Mol. Biol. 158: 305-315.
5. Bolognesi, M., Bordo, D., Rizzi, M., Tarricone, C., and Ascenzi, P. 1997. Nonvertebrate hemoglobins: Structural bases for reactivity. Prog. Biophys. Molec. Biol. 68: 29-68.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.-S., Kuszewski, J., Nilges, N., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
7. Brunori, M., Giuffrè, A., Nienhaus, K., Nienhaus, G.U., Scandurra, F.M., and Vallone, B. 2005. Neuroglobin, nitric oxide, and oxygen: Functional pathways and conformational changes. Proc. Natl. Acad. Sci. 102: 8483-8488.
8. Brusca, R.C. and Brusca, G.J. 1990. Invertebrates. Sinauer Associates, Sunderland, MS.
9. Burmester, T. and Hankeln, T. 1999. A globin gene of Drosophila melanogaster. Mol. Biol. Evol. 16: 1809-1811.
10. -. 2004. Neuroglobin: A respiratory protein of the nervous system. News Physiol. Sci. 19: 1010-1113.
11. Burmester, T., Ebner, B., Weich, B., and Hankeln, T. 2002. Cytoglobin: A novel globin type ubiquitously expressed in vertebrate tissues. Mol. Biol. Evol. 19: 416-421.
12. Collaborative Computational Project, Number 4 (CCP4). 1994. The CCP4 suite. Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50: 760-763.
13. de Sanctis, D., Pesce, A., Nardini, M., Bolognesi, M., Bocedi, A., and Ascenzi, P. 2004a. Structure-function relationships in the growing hexa-coordinate hemoglobin sub-family. IUBMB Life 56: 643-651.
14. de Sanctis, D., Dewilde, S., Pesce, A., Moens, L., Ascenzi, P., Hankel, T., Burmester, T., and Bolognesi, M. 2004b. Crystal structure of cytoglobin: The fourth globin type discovered in man displays heme hexacoordination. J. Mol. Biol. 336: 917-927.
15. de Sanctis, D., Dewilde, S., Vonrheim, C., Pesce, A., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., Ponassi, M., Nardini, M., et al. 2005. Bishistidyl heme hexacoordination, a key structural property in Drosophila melanogaster hemoglobin. J. Biol. Chem. 280: 27222-27229.
16. Dewilde, S., Blaxter, M., Van Hauwaert, ML., Van Houte, K., Pesce, A., Griffon, N., Kiger, L., Marden, M.C., Vermeire, S., Vanfleteren, J., et al. 1998. Structural, functional, and genetic characterization of Gastrophilus hemoglobin. J. Biol. Chem. 273: 32467-32474.
17. Duff, S.M.G., Wittenberg, J.B., and Hill, R.D. 1997. Expression, purification and properties of recombinant barley (Hordeum sp.) hemoglobin. J. Biol. Chem. 272: 16746-16752.
18. Engh, R.A. and Huber, R. 1991. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr. A 47: 392-400.
19. Goodman, M., Braunitzer, G., Kleinschmidt, T., and Aschauer, H. 1983. The analysis of a protein-polymorphism. Evolution of monomeric and homodimeric haemoglobins (erythrocruorins) of Chironomus thummi thummi (Insecta, Diptera). Hoppe-Seyler's Z. Physiol. Chem. 364: 205-217.
20. Green, B.N., Kuchumov, A.R., Hankeln, T., Schmidt, E.R., Bergström, G., and Vinogradov, S.N. 1998. An electrospray ionization mass spectrometric study of the extracellular hemoglobins from Chironomus thummi thummi. Biochem. Biophys. Acta 1383: 143-150.
21. Hankeln, T., Jaenicke, V., Kiger, L., Dewilde, S., Ungerechts, G., Schmidt, M., Urban, J., Marden, M.C., Moens, L., and Burmester, T. 2002. Characterization of Drosophila hemoglobin. Evidence for hemoglobinmediated respiration in insects. J. Biol. Chem. 277: 29012-29017.
22. Hankeln, T., Ebner, B., Fuchs, C., Gerlach, F., Haberkamp, M., Laufs, T.L., Roesner, A., Schmidt, M., Weich, B., Wystub, S., et al. 2005. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J. Inorg. Biochem. 99: 110-119.
23. Hargrove, M.S., Brucker, E.A., Stec, B., Sarath, G., Arredondo-Peter, R., Klucas, R.V., Olson, J.S., and Phillips Jr., G.N. 2000. Crystal structure of a nonsymbiotic plant hemoglobin. Structure Fold. Des. 8: 1005-1014.
24. Hoy, J.A., Kundu, S., Trent III, J.T., Ramaswamy, S., and Hargrove, M.S. 2004. The crystal structure of Synechocystis hemoglobin with a covalent heme linkage. J. Biol. Chem. 279: 16535-16542.
25. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. D Biol. Crystallogr. 47: 110-119.
26. Keilin, D. 1944. Respiratory systems and respiratory adaptations in larvae and pupae of Diptera. Parasitology 36: 1-66.
27. Keilin, D. and Wang, Y.L. 1946. Haemoglobin of Gastrophilus larvae. Purification and properties. Biochem. J. 40: 855-866.
28. Kraulis, P.J. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
29. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK, a program to check the stereochemical quality of protein structure. J. Appl. Crystallogr. 26: 283-291.
30. Leslie, A.G.W. 1992. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EACBM Newsletter 26.
31. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53: 240-255.
32. Perutz, M.F. 1989. Myoglobin and haemoglobin: Role of distal residues in reactions with haem ligands. Trends Biochem. Sci. 14: 42-44.
33. Pesce, A., Bolognesi, M., Bocedi, A., Ascenzi, P., Dewilde, S., Moens, L., Hankeln, T., and Burmester, T. 2002. Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep. 3: 1146-1151.
34. Pesce, A., Dewilde, S., Nardini, M., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., and Bolognesi, M. 2003. Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity. Structure 11: 1087-1095.
35. Pesce, A., De Sanctis, D., Nardini, M., Dewilde, S., Moens, L., Hankeln, T., Burmester, T., Ascenzi, P., and Bolognesi, M. 2004. Reversible hexa- to penta-coordination of the heme Fe atom modulates ligand binding properties of neuroglobin and cytoglobin. IUBMB Life 56: 657-664.
36. Phelps, C.F., Antonini, E., Brunori, M., and Kelett, G. 1972. The kinetics of binding of oxygen and carbon monoxide to Gastrophilus haemoglobin. Biochem. J. 129: 891-896.
37. Scott, N.L. and Lecomte, J.T.J. 2000. Cloning, expression, purification, and preliminary characterization of a putative hemoglobin from the cyanobacterium Synechocystis sp. PCC 6803. Protein Sci. 9: 587-597.
38. Springer, B.A., Sligar, S.G., Olson, J.S., and Phillips Jr., G.N. 1994. Mechanisms of ligand recognition in myoglobin. Chem. Rev. 94: 699-714.
39. Steigemann, W. and Weber, E. 1979. Structure of erythrocruorin in different ligand states refined at 1.4 Å resolution. J. Mol. Biol. 127: 309-338.
40. Tarricone, C., Galizzi, A., Coda, A., Ascenzi, P., and Bolognesi, M. 1997. Unusual structure of the oxygen-binding site in the dimeric bacterial hemoglobin from Vitreoscilla sp. Structure 5: 497-507.
41. Vagin, A. and Teplyakov, A. 1997. MOLREP: An automated program for molecular replacement. J. Appl. Crystallogr. 30: 1022-1025.
42. Vallone, B., Nienhaus, K., Brunori, M., and Nienhaus, G.U. 2004a. The structure of murine neuroglobin: Novel pathways for ligand migration and binding. Proteins 56: 85-92.
43. Vallone, B., Nienhaus, K., Matthes, A., Brunori, M., and Nienhaus, G.U. 2004b. The structure of carbonmonoxy neuroglobin reveals a hemesliding mechanism for control of ligand affinity. Proc. Natl. Acad. Sci. 101: 17351-17356.
44. Weber, R. and Fago, A. 2004. Functional adaptation and its molecular basis in vertebrate hemoglobins, neuroglobins and cytoglobins. Respir. Physiol. Neurobiol. 144: 141-159.
45. Weiland, T.R., Kundu, S., Trent III, J.T., Hoy, J.A., and Hargrove, M.S. 2004. Bis-histidyl hexacoordination in hemoglobins facilitates heme reduction kinetics. J. Am. Chem. Soc. 126: 11930-11935.
46. Wittenberg, J.B. 1992. Functions of cytoplasmatic hemoglobins and myohemerythrin. Adv. Comp. Environm. Physiol. 13: 59-85.
47. 1H-NMR study of dynamics and thermodynamics of Cl- binding to ferric hemoglobin of a midge larva (Tokunagayusurika akamusi). Biochem. Biophys. Acta 1652: 136-143.
48. Yang, F. and Phillips Jr., G.N. 1996. Crystal structures of CO-, deoxyand met-myoglobins at various pH values. J. Mol. Biol. 256: 762-774.