Neuroglobins, pivotal proteins associated with emerging neural systems and precursors of metazoan globin diversity

Journal of Biological Chemistry

Volumn 288, Issue 10, 2013, Pages 6957-6967

  Lechauve, Christophe ^a   Jager, Muriel ^b   Laguerre, Laurent ^c   Kiger, Laurent ^a   Correc, Gaëlle ^d   Leroux, Cédric ^c   Vinogradov, Serge ^e   Czjzek, Mirjam ^c,d   Marden, Michael C ^a   Bailly, Xavier ^c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d STATION BIOLOGIQUE DE ROSCOFF   (France)

^e WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD SYSTEM; NEURAL CELLS; NEURAL SYSTEMS; NEUROGLOBIN; TRANSCRIPTOMES;

HEMOGLOBIN;

PROTEINS;

GLOBIN; MESSENGER RNA; NEUROGLOBIN; NEUROGLOBIN 1; NEUROGLOBIN 2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CLYTIA HEMISPHAERICA; CNIDARIA; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; GENE; GENE LOCATION; HUMAN; HYDROGEN BOND; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LIGAND BINDING; MOLECULAR PHYLOGENY; NEUROGLOBIN 1 GENE; NEUROGLOBIN 2 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PLATYHELMINTH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TERTIARY STRUCTURE; STRUCTURE ANALYSIS; SYMSAGITTIFERA ROSCOFFENSIS;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENETIC VARIATION; GLOBINS; HYDROZOA; IN SITU HYBRIDIZATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; OXYGEN; PHYLOGENY; PLATYHELMINTHS; PROTEIN BINDING; PROTEIN PRECURSORS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84874927587     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.407601     Document Type: Article

References (64)

1. Kendrew, J. C., Bodo, G., Dintzis, H. M., Parrish, R. G., Wyckoff, H., and Phillips, D. C. (1958) A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature 181, 662-666
2. Perutz, M. F., Rossmann, M. G., Cullis, A. F., Muirhead, H., Will, G., and North, A. C. (1960) Structure of haemoglobin: A three-dimensional Fourier synthesis at 5.5-Å resolution, obtained by x-ray analysis. Nature 185, 416-422
3. Zuckerkandl, E., and Pauling, L. (1965) Molecules as documents of evolutionary history. J. Theor. Biol. 8, 357-366
4. Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Guertin, M., Gough, J., Dewilde, S., Moens, L., and Vanfleteren, J. R. (2005) Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc. Natl. Acad. Sci. U.S.A. 102, 11385-11389 (Pubitemid 41153829)
5. Burmester, T., Weich, B., Reinhardt, S., and Hankeln, T. (2000) A vertebrate globin expressed in the brain. Nature 407, 520-523
6. Burmester, T., Gerlach, F., and Hankeln, T. (2007) Regulation and role of neuroglobin and cytoglobin under hypoxia. Adv. Exp. Med. Biol. 618, 169-180
7. Li, W., Wu, Y., Ren, C., Lu, Y., Gao, Y., Zheng, X., and Zhang, C. (2011) The activity of recombinant human neuroglobin as an antioxidant and free radical scavenger. Proteins 79, 115-125
8. Brittain, T., Skommer, J., Henty, K., Birch, N., and Raychaudhuri, S. (2010) A role for human neuroglobin in apoptosis. IUBMB Life 62, 878-885
9. Tiso, M., Tejero, J., Basu, S., Azarov, I., Wang, X., Simplaceanu, V., Frizzell, S., Jayaraman, T., Geary, L., Shapiro, C., Ho, C., Shiva, S., Kim-Shapiro, D. B., and Gladwin, M. T. (2011) Human neuroglobin functions as a redoxregulated nitrite reductase. J. Biol. Chem. 286, 18277-18289
10. Lechauve, C., Augustin, S., Cwerman-Thibault, H., Bouaita, A., Forster, V., Célier, C., Rustin, P., Marden, M. C., Sahel, J. A., and Corral-Debrinski, M. (2012) Neuroglobin involvement in respiratory chain function and retinal ganglion cell integrity. Biochim. Biophys. Acta 1823, 2261-2273
11. DellaValle, B., Hempel, C., Kurtzhals, J. A., and Penkowa, M. (2010) In vivo expression of neuroglobin in reactive astrocytes during neuropathology in murine models of traumatic brain injury, cerebral malaria, and autoimmune encephalitis. Glia 58, 1220-1227
12. Wittenberg, B. A., Briehl, R. W., and Wittenberg, J. B. (1965) Haemoglobins of invertebrate tissues: Nerve haemoglobins of Aphrodite, Aplysia and Halosydna. Biochem. J. 96, 363-371
13. Geuens, E., Dewilde, S., Hoogewijs, D., Pesce, A., Nienhaus, K., Nienhaus, G. U., Olson, J., Vanfleteren, J., Bolognesi, M., and Moens, L. (2004) Nerve globins in invertebrates. IUBMB Life 56, 653-656 (Pubitemid 40515809)
14. Hundahl, C., Fago, A., Dewilde, S., Moens, L., Hankeln, T., Burmester, T., and Weber, R. E. (2006) Oxygen binding properties of non-mammalian nerve globins. FEBS J. 273, 1323-1329 (Pubitemid 43345050)
15. Hoffmann, F. G., Opazo, J. C., and Storz, J. F. (2010) Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates. Proc. Natl. Acad. Sci. U.S.A. 107, 14274-14279
16. Storz, J. F., Opazo, J. C., and Hoffmann, F. G. (2011) Phylogenetic diversification of the globin gene superfamily in chordates. IUBMB Life 63, 313-322
17. Hoffmann, F. G., Opazo, J. C., and Storz, J. F. (2012) Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates. Mol. Biol. Evol. 29, 303-312
18. Hoffmann, F. G., Opazo, J. C., Hoogewijs, D., Hankeln, T., Ebner, B., Vinogradov, S. N., Bailly, X., and Storz, J. F. (2012) Evolution of the globin gene family in deuterostomes: Lineage-specific patterns of diversification and attrition. Mol. Biol. Evol. 29, 1735-1745
19. Blank, M., Wollberg, J., Gerlach, F., Reimann, K., Roesner, A., Hankeln, T., Fago, A., Weber, R. E., and Burmester, T. (2011) A membrane-bound vertebrate globin. PloS One 6, e25292
20. 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 (Pubitemid 39628539)
21. Dröge, J., and Makalowski, W. (2011) Phylogenetic analysis reveals wide distribution of globin X. Biol. Direct. 6, 54
22. Bailly, X., and Vinogradov, S. N. (2008) in Dioxygen Binding and Sensing Proteins: A Tribute to Beatrice and Jonathan Wittenberg (Bolognesi, M., di Prisco, G., and Verde, C., eds) pp. 191-201, Springer, New York
23. Bailly, X. (2009) Focus on S. roscoffensis. Cahiers Biol. Marine 50, 106-107
24. Lowe, C. J., and Pani, A. M. (2011) Animal evolution: A soap opera of unremarkable worms. Curr. Biol. 21, R151-153
25. Bery, A., Cardona, A., Martinez, P., and Hartenstein, V. (2010) Structure of the central nervous system of a juvenile acoel, Symsagittifera roscoffensis. Dev. Genes Evol. 220, 61-76
26. Houliston, E., Momose, T., and Manuel, M. (2010) Clytia hemisphaerica: A jellyfish cousin joins the laboratory. Trends Genet. 26, 159-167
27. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
28. Uzan, J., Dewilde, S., Burmester, T., Hankeln, T., Moens, L., Hamdane, D., Marden, M. C., and Kiger, L. (2004) Neuroglobin and other hexacoordinated hemoglobins show a weak temperature dependence of oxygen binding. Biophys. J. 87, 1196-1204 (Pubitemid 39095096)
29. Chevalier, S., Martin, A., Leclère, L., Amiel, A., and Houliston, E. (2006) Polarised expression of FoxB and FoxQ2 genes during development of the hydrozoan Clytia hemisphaerica. Dev. Genes Evol. 216, 709-720 (Pubitemid 44644643)
30. Jager, M., Quéinnec, E., Le Guyader, H., and Manuel, M. (2011) Multiple Sox genes are expressed in stem cells or in differentiating neuro-sensory cells in the hydrozoan Clytia hemisphaerica. Evodevo 2, 12
31. Chiori, R., Jager, M., Denker, E., Wincker, P., Da Silva, C., Le Guyader, H., Manuel, M., and Quéinnec, E. (2009) Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PloS One 4, e4231
32. Denker, E., Manuel, M., Leclère, L., Le Guyader, H., and Rabet, N. (2008) Ordered progression of nematogenesis from stem cells through differentiation stages in the tentacle bulb of Clytia hemisphaerica (Hydrozoa, Cnidaria). Dev. Biol. 315, 99-113
33. Kabsch, W. (1988) Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J. Appl. Crystallogr. 21, 916-924
34. Navaza, J. (2001) Implementation of molecular replacement in AMoRe. Acta Crystallogr. D Biol. Crystallogr. 57, 1367-1372 (Pubitemid 36117184)
35. Schneider, T. R., and Sheldrick, G. M. (2002) Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (Pubitemid 35169744)
36. Pape, T., and Schneider, T. R. (2004) HKL2MAP: A graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844
37. Potterton, L., McNicholas, S., Krissinel, E., Gruber, J., Cowtan, K., Emsley, P., Murshudov, G. N., Cohen, S., Perrakis, A., and Noble, M. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60, 2288-2294 (Pubitemid 41742782)
38. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr. D Biol. Crystallogr. 59, 1131-1137 (Pubitemid 36872348)
39. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E. L., Studholme, D. J., Yeats, C., and Eddy, S. R. (2004) The Pfam protein families database. Nucleic Acids Res. 32, D138-141 (Pubitemid 38081623)
40. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010) New algorithms and methods to estimate maximumlikelihood phylogenies: Assessing the performance of PhyMl 3.0. Syst. Biol. 59, 307-321
41. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739
42. Semmler, H., Chiodin, M., Bailly, X., Martinez, P., and Wanninger, A. (2010) Steps towards a centralized nervous system in basal bilaterians: Insights from neurogenesis of the acoel Symsagittifera roscoffensis. Dev. Growth Differ. 52, 701-713
43. Brunori, M., and Vallone, B. (2007) Neuroglobin, seven years after. Cell Mol. Life Sci. 64, 1259-1268 (Pubitemid 46791063)
44. Bashford, D., Chothia, C., and Lesk, A. M. (1987) Determinants of a protein fold: Unique features of the globin amino acid sequences. J. Mol. Biol. 196, 199-216 (Pubitemid 17102240)
45. 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 (Pubitemid 38720840)
46. 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 (Pubitemid 38020417)
47. Holm, L., and Rosenström, P. (2010) Dali server: Conservation mapping in 3D. Nucleic Acids Res. 38, W545-549
48. Galliot, B., Quiquand, M., Ghila, L., de Rosa, R., Miljkovic-Licina, M., and Chera, S. (2009) Origins of neurogenesis, a cnidarian view. Dev. Biol. 332, 2-24
49. Burmester, T., and Hankeln, T. (2009) What is the function of neuroglobin? J. Exp. Biol. 212, 1423-1428
50. Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D., and Martindale, M. Q. (2009) Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev. Neurobiol. 69, 235-254
51. Galliot, B. (2010) in Key Transitions in Animal Evolution (Schierwater, B., and De Salle, R., eds) pp. 127-161, Science Publishers & CRC Press, New York
52. Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E., Da Silva, C., Wincker, P., Le Guyader, H., Leys, S., Jackson, D. J., Schreiber, F., Erpenbeck, D., Morgenstern, B., Wörheide, G., and Manuel, M. (2009) Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706-712
53. Miljkovic-Licina, M., Gauchat, D., and Galliot, B. (2004) Neuronal evolution: Analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system. BioSystems 76, 75-87 (Pubitemid 39207438)
54. Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., Larroux, C., Putnam, N. H., Stanke, M., Adamska, M., Darling, A., Degnan, S. M., Oakley, T. H., Plachetzki, D. C., Zhai, Y., Adamski, M., Calcino, A., Cummins, S. F., Goodstein, D. M., Harris, C., Jackson, D. J., Leys, S. P., Shu, S., Woodcroft, B. J., Vervoort, M., Kosik, K. S., Manning, G., Degnan, B. M., and Rokhsar, D. S. (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720-726
55. Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., Signorovitch, A. Y., Moreno, M. A., Kamm, K., Grimwood, J., Schmutz, J., Shapiro, H., Grigoriev, I. V., Buss, L. W., Schierwater, B., Dellaporta, S. L., and Rokhsar, D. S. (2008) The Trichoplax genome and the nature of placozoans. Nature 454, 955-960
56. Ye, S. Q., Zhou, X. Y., Lai, X. J., Zheng, L., and Chen, X. Q. (2009) Silencing neuroglobin enhances neuronal vulnerability to oxidative injury by downregulating 14-3-3γ. Acta Pharmacol. Sin. 30, 913-918
57. Hundahl, C. A., Allen, G. C., Hannibal, J., Kjaer, K., Rehfeld, J. F., Dewilde, S., Nyengaard, J. R., Kelsen, J., and Hay-Schmidt, A. (2010) Anatomical characterization of cytoglobin and neuroglobin mRNA and protein expression in the mouse brain. Brain Res. 1331, 58-73
58. Ertas, B., Kiger, L., Blank, M., Marden, M. C., and Burmester, T. (2011) A membrane-bound hemoglobin from gills of the green shore crab Carcinus maenas. J. Biol. Chem. 286, 3185-3193
59. Fago, A., Mathews, A. J., Moens, L., Dewilde, S., and Brittain, T. (2006) The reaction of neuroglobin with potential redox protein partners cytochrome b5 and cytochrome c. FEBS Lett. 580, 4884-4888 (Pubitemid 44308330)
60. Kraus, D. W., and Colacino, J. M. (1986) Extended oxygen delivery from the nerve hemoglobin of Tellina alternata (Bivalvia). Science 232, 90-92 (Pubitemid 16037986)
61. Doeller, J. E., and Kraus, D. W. (1988) A physiological comparison of bivalve mollusc cerebro-visceral connectives with and without neurohemoglobin. II. Neurohemoglobin characteristics. Biol. Bull. 174, 67-76
62. Cheng, C. H., di Prisco, G., and Verde, C. (2009) The "icefish paradox": Which is the task of neuroglobin in Antarctic hemoglobin-less icefish? IUBMB Life 61, 184-188
63. Ganfornina, M. D., and Sánchez, D. (1999) Generation of evolutionary novelty by functional shift. Bioessays. 21, 432-439 (Pubitemid 29223315)
64. Nosengo, N. (2011) Marine biology network launches into choppy waters. Nature 470, 444-445