A role for human neuroglobin in apoptosis

IUBMB Life

Volumn 62, Issue 12, 2010, Pages 878-885

  Brittain, Thomas ^a   Skommer, Joanna ^a   Henty, Kristen ^a   Birch, Nigel ^a   Raychaudhuri, Subhadip ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b University of California   (United States)

Author keywords

apoptosis; binding; cytochrome c; neuroglobin

Indexed keywords

NEUROGLOBIN;

APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL DEATH; CELL FUNCTION; HUMAN; OXIDATION REDUCTION REACTION;

ANIMALS; APOPTOSIS; CYTOCHROMES C; GLOBINS; HUMANS; MICE; MITOCHONDRIA; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; NEURONS; NITRIC OXIDE; OXIDATION-REDUCTION; OXYGEN; RATS; REACTIVE OXYGEN SPECIES; RETINA; SIGNAL TRANSDUCTION;

EID: 79952035765     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.405     Document Type: Article

References (67)

1. Burmester, T., Weich, B., Reinhardt, S., and, Hankeln, T., (2000) A vertebrate globin expressed in the brain. Nature 407, 520-523.
2. Lankester, E. R., (1872) A contribution to the knowledge of haemoglobion. Proc. R. Soc. 21, 70-81.
3. Vallone, B., Nienhaus, K., Matthes, A., Brunori, M., and, Nienhaus, G. U., (2004) The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand binding. Proc. Natl. Acad. Sci. USA 101, 17351-17356. (Pubitemid 39657407)
4. Pesce, A., Dewide, 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. (Pubitemid 37103070)
5. 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)
6. Fago, A., Mathews, A. J., Dewilde, S., Moens, L., and, Brittain. T,. (2006) The reactions of neuroglobin with CO: evidence for two forms of the ferrous protein. J. Inorg. Biochem. 100, 1339-1343.
7. Dewilde, S., Kiger, L., Burmester, T., Hankeln, T., Baudin-Creuzal, V., Aerts, T., Marden, M. C., Caubergs, R., and, Moens, L., (2001) Biochemical characterisation and ligand binding properties of neuroglobin, a novel member of the globin family. J. Biol. Chem. 276, 38949-38955.
8. Brunori, M., Giuffre, 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. (Pubitemid 40862762)
9. Brittain, T., Yosaatmadja. Y., and, Henty, K., (2008) The interaction of human neuroglobin with hydrogen sulphide. IUBMB Life 60, 135-138.
10. 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)
11. Arcovito, A., Moschetti, T., D'Angelo, P., Mancini, G., Vallone, B., Brunori, M., and, Della Longa, S., (2008) An X-ray diffraction and X-ray absorption spectroscopy joint study of neuroglobin. Arch. Biochem. Biophys. 475, 7-13.
12. Hamdane, D., Kiger, L., Dewilde, S., Uzan, J., Burmester, T., Hankeln, T., Moens, L, and, Marden, M. C., (2005) Hyperthermal stability of neuroglobin and cytoglobin. FEBS J. 272, 2076-2084. (Pubitemid 40547260)
13. Picotti, P., Dewilde, S., Fago, A., Hundahl, C., De Filippis, V., Moens, L, and, Fontana, A., (2009) Unusual stability of human neuroglobin at low pH-molecular mechanisms and biological significance. FEBS J. 276, 7027-7039.
14. Hankeln, T., Ebner, B., Fuchs, C., Gerlach, F., Haberkamp, M., Laufs, T.L, Roesner, A., Schmidt, M., Weich, B., Wystub, S., Saaler-Reinhardt, S., Reuss, S., Bolognesi, M., De Sanctis, D., Marden, M. C., Kiger, L., Moens, L., Dewilde, S., Nevo, E., Avivi, A., Weber, R. E., Fago, A., and, Burmester, T., (2005) Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J. Inorg. Biochem. 99, 110-119. (Pubitemid 39642974)
15. 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
16. 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. (Pubitemid 34014010)
17. Fordel, E., Thijs, L., Martinet, W., Lenjou, M., Laufs, T., Van Bockstaele, D., Moens, L., and, Dewilde, S., (2006) Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells against oxidative stress-induced cell death. Neurosci. Lett. 410, 146-151. (Pubitemid 44709414)
18. Li, R. C., Pouranfar, F., Lee, S. K., Morris, M. W., Wang, Y., and, Gozal. D,. (2008) Neuroglobin protects PC12 cells against beta-amyloid-induced cell injury. Neurobiol. Aging 29, 1815-1822.
19. Li, R. C., Morris, M. W., Lee, S. K., Pouranfar, F., Wang, Y., and, Gozal, D., (2008) Neuroglobin protects PC12 cells against oxidative stress. Brain Res. 1190, 159-166.
20. Raychaudhuri, S., Skommer, J., Henty, K., Birch, N., and, Brittain, T., (2010) Neuroglobin protects nerve cells from apoptosis by inhibiting the intrinsic pathway of cell death. Apoptosis 15, 401-411.
21. Antao, S. T., Duong, T. T., Aran, R., and, Witting, P. K., (2010) Neuroglobin over-expression in cultured human neuronal cells protects against hydrogen peroxide insult via activating phosphoinositide-3 kinase and opening the mitochondrial K ATP channel. Antioxid. Redox. Signal 13, 769-781.
22. 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 down-regulating 14-3-3gamma. Acta Pharmacol. Sin. 30, 913-918.
23. Khan, A. A., Wang, Y., Sun, Y., Mao, X. O., Xie, L., Miles, E., Graboski, J., Chen. S., Ellerby, L. M., Jin, K., and, Greenberg, D. A., (2006) Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia. Proc. Natl. Acad. Sci. USA 103, 17944-17948. (Pubitemid 44852265)
24. Wang, X., Liu, J., Zhu, H., Tejima, E., Tsuji, K., Murata, Y., Atochin, D. N., Huang, P. L., Zhang, C., and, Lo, E. H., (2008) Effects of neuroglobin overexpression on acute brain injury and long-term outcomes after focal cerebral ischemia. Stroke 39, 1869-1874.
25. Sun, Y., Jin. K., Peel, A., Mao, X. O., Xie, L., and, Greenberg, D. A., (2003) Neuroglobin protects the brain from experimental stroke in vivo. Proc. Natl. Acad. Sci. USA 100, 3497-3500. (Pubitemid 36356612)
26. Szymanski, M., Wang, R., Fallin, M. D., Bassett, S. S., and, Avramopoulos, D., (2008) Neuroglobin and Alzheimer's dementia: genetic association and gene expression changes. Neurobiol. Aging 31, 1835-1842.
27. Chuang, P.Y., Conley, Y.P., Poloyac, S.M., Okonkwo, D.O., Ren, D., Sherwood, P.R., Hravnak, M., and, Alexander, S.A., (2010) Neuroglobin genetic polymorphisms and their relationship to functional outcomes following traumatic brain injury. J. Neurotrauma 27, 999-1006.
28. Lin, Y., Fang, L., Xue, X.H., Murong, S.X., Wang, N., and, Wu, Z.Y., (2008) Association between Ngb polymorphisms and ischemic stroke in the Southern Chinese Han population. BMC Med. Genet. 9, 110-120.
29. Schmidt, M., Giess, A., Laufs, T., Hankeln, T., Wolfrum, U., and, Burmester, T., (2002) How does the eye breathe? J. Biol. Chem. 276, 1932-1935.
30. Dewilde, S., Kiger, L., Burmester, T., Hankeln, T., Baudin-Creuzal, V., Aerts, T., Marden, M. C., Caubergs, R., and, Moens, L., (2001) Biochemical characterisation 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. J. Biol. Chem. 279, 44417-444426.
32. Kim, P. K. M., Zamora, R., Petrosko, P., and, Billiar, T. R., (2001) The regulatory role of nitric oxide in apoptosis. Int. Immunopharm. 1, 1421-1441. (Pubitemid 32622788)
33. Lee, V. Y., Mclintock, D. S., Santore, M. T., Budinger, G. R. S., and, Chandel, N. S., (2002) Hypoxia sensitizes cells to nitric oxide induced apoptosis. J. Biol. Chem. 277, 16067-16074. (Pubitemid 34967891)
34. 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. (Pubitemid 38685596)
35. Brunori, M., Giuffre, 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. (Pubitemid 40862762)
36. Brunori, M., Vallone, B., (2006) A globin for the brain. FASEB J. 20, 2192-2197. (Pubitemid 44953848)
37. Giuffre, A., Moschetti, T., Vallone, B., and, Brunori, M., (2008) Neuroglobin: enzymic reduction and oxygen affinity. Biochem. Biophys. Res. Com. 367, 893-898.
38. Moschetti, T., Giuffre, A., Ardiccioni, C., Vallone, B., Modjtahedi, N., Kroemer, G., and, Brunori, M., (2009) Failure of apoptosis inducing factor to act as neuroglobin reductase. Biochem. Biophys. Res. Com. 390, 121-124.
39. Smagghe, B. J., Trent, J. T., and, Hargrove, M. S., (2008) NO dioxygenase activity is ubiquitous in vitro but limited by reduction in vivo. Plos One 3, e2039. doi: 10.1371/journal.pone.0002039, p 1-10.
40. Petersen, M. G., Dewilde, S., and, Fago, A., (2008) Reactions of ferrous neuroglobin and cytoglobin with nitrite under anaerobic conditions. J. Inorg. Biochem. 102, 1777-1782.
41. 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. (Pubitemid 38685584)
42. Lipton, P., (1999) Ischemic cell death in brain neurons. Physiol. Rev. 79, 1431-1568. (Pubitemid 29473320)
43. 5 and cytochrome c. FEBS Lett. 580, 4884-4888. (Pubitemid 44308330)
44. Bonding, S. H., Henty, K., Dingley, A., and, Brittain, T., (2008) The binding of cytochrome c to neuroglobin: a docking and Surface Plasmon Resonance study. Int. J. Biol. Macromol. 43, 295-299.
45. Kitatsuji, C., Kurogochi, M., Nishimura, S., Ishimori, K., and, Wakasugi, K., (2007) Molecular basis of guanine nucleotide dissociation inhibitor activity of human neuroglobin by chemical cross-linking and mass spectrometry. J. Mol. Biol. 368, 150-160. (Pubitemid 46441221)
46. Yu, T., Wang, X., Purring-Koch, C., Weil, Y., and, McLendon, G. L., (2001) A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 276, 13034-13038.
47. Abdullaev, Z. K., Bodrova, M. E., Chernyak, B. V., Dolgihk, D. A., Kluck, R. M., Pereverzev, M. O., Aseniev, A. S., Efremov, R. G., Kirpichnikov, M. P., Mokhova, E. N., Newmeyer, D. D., Roder, H., and, Skulachev, V. P., (2002) A cytochrome c mutant with high electron transfer and antioxidant activities but devoid of apoptogenic effect. Biochem. J. 362, 749-754. (Pubitemid 34242328)
48. Kluck, R. M., Ellerby, L. M., Ellerby, H. M., Naiem, S., Yaffe, M. P., Margoliash, E., Bredesen, D., Mauk, A. G., Sherman, F., and, Newmaeyer, D. D., (2000) Determinants of cytochrome c pro-apoptotic activity. J. Biol. Chem. 275, 16127-16133.
49. Chertkova, R. V., Sharanov, G. V., Feofanov, A. V., Bocharova, O. V., Latypov, R. F., Chernyak, B. V., Arseniev, A. S., Dolgikh, D. A., and, Kirpichnikov, M. P., (2008) Proapototic activity of cytochrome c in living cells: effect of K72 substitution and species differences. Mol. Cell. Biochem. 314, 85-93.
50. Hampton, M. B., Zhivotovsky, B., Slater, A. F., Burgess, D. H., and, Orrenius, S., (1998) Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem. J. 329, 95-99. (Pubitemid 28022295)
51. Pan, Z., Voehringer, D. W., and, Meyn, R. E., (1999) Analysis of redox regulation of cytochrome c-induced apoptosis in a cell free system. Cell Death Differ. 6, 683-688. (Pubitemid 29366658)
52. Suto, D., Sato, K., Ohba, Y., Yoshimura, T., and, Fujii, J., (2005) Supression of the pro-aptotic function of cytochrome c by singlet oxygen via a haem redox state dependent mechanism. Biochem. J. 392, 399-406. (Pubitemid 41796529)
53. Borutaite, V., and, Brown, G. C., (2007) Mitochondrial regulation of caspase activation by cytochrome oxidase and tetra-methylphenylenediamine via cytosolic cytochrome c redox state. J. Biol. Chem. 282, 31124-31130. (Pubitemid 350044866)
54. Fago, A., Mathews, A. J., and, Brittain. T,. (2008) A role for neuroglobin: resetting the trigger level for apoptosis in neuronal and retinal cells. IUBMB Life 60, 398-401.
55. Raychaudhuri, S., Skommer, J., Henty, K., Birch, N., and, Brittain, T., (2010) Neuroglobin protects nerve cells from apoptosis by inhibiting the intrinsic pathway of cell death. Apoptosis 15, 401-411.
56. Raychaudhuri, S., Willgohs, E., Nguyen, T. N., Khan, E. M., and, Goldkorn, T., (2008) Monte Carlo simulation of cell death signaling predicts large cell-to-cell stochastic fluctuations through the type 2 pathway of apoptosis. Biophys. J. 295, 3559-3562
57. Hyrc, K., Handran, S. D., Rothman, S. M., and, Goldberg, M. P., (1997) Ionized intracellular calcium concentration predicts excitotoxic neuronal cell death: observations with low affinity fluorescent calcium indicators. J. Neurosci. 17, 6669-6677. (Pubitemid 27366619)
58. Duchen, M. R., (2000) Mitochondria and calcium: from cell signaling to cell death. J. Physiol. 529, 57-68.
59. Garrido, C., Galluzzi, L., Brunet, M., Puig, P. E., Didelot, C., and, Kroemer, G., (2006) Mechanism of cytochrome c release from mitochondria. Cell Death Diff. 13, 1423-1433.
60. Mattson, M. P., and, Chan, S. L., (2003) Calcium orchestrates apoptosis. Nature Cell Biol. 12, 1041-1043. (Pubitemid 37509106)
61. Pinton, P., Giorgi, C., Siviero, R., Zecchini, E., and, Rizzuto, R., (2008) Calcium and apoptosis: ER mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27, 6407-6418.
62. Crompton, M., (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341, 233-249. (Pubitemid 29373645)
63. Duong, T. T. H., Witting, P. K., Antao, S. T., Parry, S. N., Kennerson, M., Lai, B., Vogt, S., Lay, P. A., and, Harris, H. M., (2009) Multiple protective activities of neuroglobin in cultured neuronal cells exposed to hypoxia re-oxygenation injury. J. Neurochem. 108, 1143-1154.
64. Liu, J., Yu, Z., Guo, S., Lee, S., Xing, C., Zhang, C., Gao, Y., Nicholls, D. G., Lo, E. H., and, Wang, X., (2009) Effects of neuroglobin over-expression on mitochondrial function and oxidative stress following hypoxia/reoxygenation in cultured neurons. J. Neurosci. Res. 87, 164-170.
65. Boehning, D., Patterson, R. L., Sedaghat, L., Glebova, N. O., Kurosaki, T., and, Snyder, S. H., (2003) Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell. Biol. 5, 1051-1061. (Pubitemid 37509111)
66. Wakasugi, K., Nakano, T., and, Morishima, I., (2003) Oxidised human neuroglobin acts as a heterotrimeric Gα protein guanine nucleotide dissocation inhibitor J. Biol. Chem. 278, 36505-36512. (Pubitemid 37139980)
67. Khan, A. A., Mao, X. O., Banwait, S., DerMardirossian, C. M., Bokoch, G. M., Jin, K., and, Greenberg, D. A., (2008) Regulation of hypoxic neuronal death signaling by neuroglobin. FASEB J. 22, 1737-1747. (Pubitemid 351811451)