Neuroglobin, seven years after

Cellular and Molecular Life Sciences

Volumn 64, Issue 10, 2007, Pages 1259-1268

  Brunori, M ^a   Vallone, B ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Crystallography; Evolution; Globins; Ligand binding; Neuroprotection; Radical scavenging

Indexed keywords

HEME; NEUROGLOBIN; OXYGEN;

AUTOOXIDATION; BIOSYNTHESIS; CONFORMATIONAL TRANSITION; GENE MUTATION; GENE OVEREXPRESSION; GENE STRUCTURE; HUMAN; HYPOXIA; LIGAND BINDING; MUTAGENESIS; NEUROPROTECTION; NONHUMAN; OXYGEN AFFINITY; PROTEIN STRUCTURE; REVIEW;

ANIMALS; CARBON DIOXIDE; EVOLUTION, MOLECULAR; GLOBINS; HUMANS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; OXYGEN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

VERTEBRATA;

EID: 34249031561     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-7090-2     Document Type: Review

References (57)

1. Burmester, T., Weich, B., Reinhardt, S. and Hankeln, T. (2000) Avertebrate globin expressed in the brain. Nature 407, 520-523.
2. Trent, J. T. 3rd and Hargrove, M. S. (2002) A ubiquitously expressed human hexacoordinate hemoglobin. J. Biol. Chem. 277, 19538-19545.
3. Burmester, T. and Hankeln, T. (2004) Neuroglobin: A respiratory protein of the nervous system. News Physiol. Sci. 19, 110-113.
4. Sun, Y., Jin, K., Mao, X. O., Zhu, Y. and Greenberg, D. A. (2001) Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury. Proc. Natl. Acad. Sci. USA 98, 15306-15311.
5. Sun, Y., Jin, K., Peel, A., Mao, X. O. and Greenberg, D. A. (2003) Neuroglobin protects the brain from experimental stroke in vivo. Proc. Natl. Acad. Sci. USA 100, 3497-3500.
6. Lane, N. (2002) Oxygen: The Molecule That Made The World. Oxford University Press, New York.
7. Hardison, R. C. (1996) A brief history of hemoglobins: Plant, animal, protist, and bacteria. Proc. Natl. Acad. Sci. USA 93, 5675-5679.
8. Weber, R. and Vinogradov, S. N. (2001) Nonvertebrate hemoglobins: Functions and molecular adaptations. Physiol. Rev. 81, 569-628.
9. Freitas, T. A., Hou, S., Dioum, E. M., Saito, J. A., Newhouse, J., Gonzalez, G., Gilles-Gonzalez, M. A. and Alam, M. (2004) Ancestral hemoglobins in Archaea. Proc. Natl. Acad. Sci. USA 101, 6675-6680.
10. Minning, D. M., Gow, A. J., Bonaventura, J., Braun, R., Dewhirst, M., Goldberg, D. E. and Stamler, J. S. (1999) Ascaris haemoglobin is a nitric oxide-activated "deoxygenase". Nature 401, 497-502.
11. Zal, F., Leize, E., Lallier, F. H., Toulmond, A., Van Dorsselaer, A. and Childress, J. J. (1998) S-Sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. Proc. Natl. Acad. Sci. USA 95, 8997-9002.
12. Poole, R. K. and Hughes, M. N. (2000) New functions for the ancient globin family: Bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36, 775-783.
13. Ascenzi, P., Bocedi, A., Bolognesi, M., Fabozzi, G., Milani, M. and Visca, P. (2006) Nitric oxide scavenging by Mycobacterium leprae GlbO involves the formation of the ferric heme-bound peroxynitrite intermediate. Biochem. Biophys. Res. Commun. 339, 450-456.
14. Gow, A. J., Luchsinger, B. P., Pawloski, J. R., Singel, D. J. and Stamler, J. S. (1999) The oxyhemoglobin reaction of nitric oxide. Proc. Natl. Acad. Sci. USA. 96, 9027-9032.
15. Pawloski, J. R., Hess, D. T. and Stamler, J. S. (2001) Export by red blood cells of nitric oxide bioactivity. Nature 409, 622-626.
16. Brunori, M. (2001) Nitric oxide moves myoglobin centre stage. Trends Biochem. Sci. 26, 209-210.
17. Wittenberg, J. B. and Wittenberg, B. A. (2003) Myoglobin function reassessed. J. Exp. Biol. 206, 2011-2020.
18. Angelo, M., Singel, D. J. and Stamler, J. S. (2006) An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc. Natl. Acad. Sci. USA 103, 8366-8371.
19. 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.
20. Kugelstadt, D., Haberkamp, M., Hankeln, T. and Burmester, T. (2004) Neuroglobin, cytoglobin, and a novel, eye-specific globin from chicken. Biochem. Biophys. Res. Commun. 325, 719-725.
21. Roesner, A., Fuchs, C., Hankeln, T. and Burmester, T. (2005) A globin gene of ancient evolutionary origin in lower vertebrates: Evidence for two distinct globin families in animals. Mol. Biol. Evol. 22, 12-20.
22. Dixon, B., Walker, B., Kimmins, W. and Pohajdak, B. (1992) A nematode hemoglobin gene contains an intron previously thought to be unique to plants. J. Mol. Evol. 35, 131-136.
23. Stoltzfus, A., Spencer, D. F., Zuker, M., Logsdon, J. M. Jr and Doolittle, W. F. (1994) Testing the exon theory of genes: the evidence from protein structure. Science 265, 202-207.
24. Andersson, C. R., Jensen, E. O., Llewellyn, D. J., Dennis, E. S. and Peacock, W. J. (1996) A new hemoglobin gene from soybean: a role for hemoglobin in all plants. Proc. Natl. Acad. Sci. USA 93, 5682-5687.
25. Rogozin, I. B., Lyons-Weiler, J. and Koonin, E. V. (2000) Intron sliding in conserved gene families. Trends Genet. 16, 430-432.
26. Burmester, T., Haberkamp, M., Mitz, S., Roesner, A., Schmidt, M., Ebner, B., Gerlach, F., Fuchs, C. and Hankeln, T. (2004) Neuroglobin and cytoglobin: genes, proteins and evolution. IUBMB Life 56, 703-707.
27. 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.
28. Vallone, B., Nienhaus, K., Brunori, M. and Nienhaus, G. U. (2004) The structure of murine neuroglobin: Novel pathways for ligand migration and binding. Proteins 56, 85-92.
29. Trent, J. T. 3rd, Watts, R. A. and Hargrove MS. (2001) Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J. Biol. Chem. 276, 30106-30110.
30. Dewilde, S., Kiger, L., Burmester, T., Hankeln, T., Baudin-Creuza V., Aerts, T., Marden, M. C., Caubergs, R. and Moens, L. (2001) Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J. Biol. Chem. 276, 38949-38955.
31. Fago, A., Hundahl, C., Dewilde, S., Gilany, K., Moens, L. and Weber, R. E. (2004) Allosteric regulation and temperature dependence of oxygen binding in human neuroglobin and cytoglobin: molecular mechanisms and physiological significance. J. Biol. Chem. 279, 44417-44426.
32. Couture, M., Burmester, T., Hankeln, T. and Rousseau, D. L. (2001)The heme environment of mouse neuroglobin: evidence for the presence of two conformations of the heme pocket. J. Biol. Chem. 276, 36377-36382.
33. Hamdane, D., Kiger, L., Dewilde, S., Green, B. N., Pesce, A., Uzan, J., Burmester, T., Hankeln, T., Bolognesi, M., Moens, L. and Marden, M. C. (2003) The redox state of the cell regulates the ligand binding affinity of human neuroglobin and cytoglobin. J. Biol. Chem. 278, 51713-51721.
34. 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. USA 102, 8483-8488.
35. Smagghe, B. J. , Sarath, G., Ross, E., Hilbert, J. L. and Hargrove, M. S. (2006) Slow ligand binding kinetics dominate ferrous hexacoordinate hemoglobin reactivities and reveal differences between plants and other species. Biochemistry 45, 561-570.
36. Van Doorslaer, S. , Dewilde, S. , Kiger, L. , Nistor, S. V. , Goovaerts, E. , Marden, M. C. and Moens, L. (2003) Nitric oxide binding properties of neuroglobin: A characterization by EPR and flash photolysis. J. Biol. Chem. 278 , 4919-4925.
37. Kriegl, J. M., Bhattacharyya, A. J., Nienhaus, K., Deng, P., Minkow, O. and Nienhaus, G. U. (2002) Ligand binding and protein dynamics in neuroglobin. Proc. Natl. Acad. Sci. USA 99, 7992-7997.
38. Nienhaus, K., Kriegl, J. M. and Nienhaus, G. U. (2004) Structural dynamics in the active site of murine neuroglobin and its effects on ligand binding. J. Biol. Chem. 279, 22944-22952.
39. Sawai, H., Makino, M., Mizutani, Y., Ohta, T., Sugimoto, H., Uno, T., Kawada, N., Yoshizato, K., Kitagawa, T. and Shiro, Y. (2005) Structural characterization of the proximal and distal histidine environment of cytoglobin and neuroglobin. Biochemistry 44, 13257-13265.
40. 1HNMR characterization of equilibrium heme orientational disorder with functional consequences in mouse neuroglobin. J. Am. Chem. Soc. 125, 8080-8081.
41. Weiland, T. R., Kundu, S., Trent, J. T. 3rd, Hoy, J. A. and Hargrove, M. S. (2004) Bis-histidyl hexacoordination in hemoglobins facilitates heme reduction kinetics. J. Am. Chem. Soc. 126, 11930-11935.
42. Esplugues, J. V. (2002) NO as a signalling molecule in the nervous system. Br. J. Pharmacol. 135, 1079-1095.
43. Herold, S., Fago, A., Weber, R. E., Dewilde, S. and Moens, L. (2004) Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress. J. Biol. Chem. 279, 22841-22847.
44. Herold, S. and Fago, A. (2005) Reactions of peroxynitrite with globin proteins and their possible physiological role. Comp. Biochem. Physiol. 142, 124-129.
45. Vallone, B., Nienhaus, K., Matthes, A., Brunori, M. and Nienhaus, G. U. (2004) The structure of carbomonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity. Proc. Natl. Acad. Sci. USA 101, 17351-17356.
46. Hargrove, M. S., Brucker, E. A., Stec, B., Sarath, G., Arredondo-Peter, R., Klucas, R. V., Olson, J. S. and Phillips, G. N. Jr. (2000) Crystal structure of a nonsymbiotic plant hemoglobin. Structure Fold Des. 8, 1005-1014.
47. Tilton, R. F. Jr., Kuntz, I. D. Jr. and Petsko, G. A. (1984) Cavities in proteins: Structure of a metmyoglobin-xenon complex solved to 1.9 Å. Biochemistry 23, 2849-2857.
48. La Mar, G. N., Budd, D. L., Viscio, D. B., Smith, K. M. and Langry, K. C. (1978) Proton nuclear magnetic resonance characterization of heme disorder in hemoproteins. Proc. Natl. Acad. Sci. USA 75, 5755-5759.
49. Walker, F. A. (2006) The heme environment of mouse neuroglobin: histidine imidazole plane orientations obtained from solution NMR and EPR spectroscopy as compared with X-ray crystallography. J. Biol. Inorg. Chem. 11, 391-397.
50. Vinck, E., Van Doorslaer, S., Dewilde, S., Mitrikas, G., Schweiger, A. and Moens, L. (2006) Analyzing heme proteins using EPR techniques, the heme pocket structure of ferric mouse neuroglobin. J. Biol. Inorg. Chem. 11, 391-397.
51. Wakasugi, K., Nakano, T. and Morishima, I. (2003) Identification of residues in human neuroglobin crucial for guanine nucleotide dissociation inhibitor activity. J. Biol. Chem. 278, 36505-36512.
52. Lipton, P. (1999) Ischemic cell death in brain neurons. Physiol. Rev. 79, 1431-1568.
53. Antonini, E. and Brunori, M. (1971) Hemoglobin and Myoglobin in their Reactions with Ligands, North Holland Publishing Co, Amsterdam.
54. Springer, B. A., Sligar, S. G., Olson, J. S. and Phillips, G. N. Jr. (1994) Mechanisms of ligand recognition in myoglobin. Chem. Rev. 94, 699-714.
55. Moore, E. G. and Gibson, Q. H. (1976) Cooperativity in dissociation of nitric oxide from hemoglobin. J. Biol. Chem. 251, 2788-2794.
56. Cassoly, R. and Gibson, Q. H. (1975) Conformation, cooperativity and ligand binding in human hemoglobin. J. Mol. Biol. 91, 301-313.
57. Azizi, F., Kielbasa, J. E., Adeyiga, A. M., Maree, R. D., Frazier, M., Yakubu, M., Shields, H., King, S. B. and Kim-Shapiro, D. B. (2005) Rates of nitric oxide dissociation from hemoglobin. Free Radic. Biol. Med. 39, 145-151.