Neuroglobin upregulation induced by 17β-estradiol sequesters cytocrome c in the mitochondria preventing H2 O2 -induced apoptosis of neuroblastoma cells

Cell Death and Disease

Volumn 4, Issue 2, 2013, Pages

  De Marinis, E ^a   Fiocchetti, M ^a   Acconcia, F ^a   Ascenzi, P ^a   Marino, M ^a  

^a ROMA TRE UNIVERSITY   (Italy)

Author keywords

17 estradiol; Apoptosis; Cytochrome c; Estrogen receptor; Neuroblastoma cell lines; Neuroglobin

Indexed keywords

CASPASE 3; CYTOCHROME C; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HYDROGEN PEROXIDE; NEUROGLOBIN;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; MITOCHONDRION; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; TOXICITY; UPREGULATION;

APOPTOSIS; CASPASE 3; CELL LINE, TUMOR; CYTOCHROMES C; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLOBINS; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA; NERVE TISSUE PROTEINS; NEUROBLASTOMA; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION; UP-REGULATION;

EID: 84875968702     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.30     Document Type: Article

References (40)

1. Burmester T, Hankeln T. What is the function of neuroglobin? J Exp Biol 2009; 212: 1423-1428.
2. Burmester T, Weich B, Reinhardt S, Hankeln T. A vertebrate globin expressed in the brain. Nature 2000; 407: 520-523.
3. Emara M, Turner AR, Allalunis-Turner J. Hypoxic regulation of cytoglobin and neuroglobin expression in human normal and tumor tissues. Cancer Cell Int 2010; 10: 33.
4. Dewilde S, Kiger L, Burmester T, Hankeln T, Baudin-Creuza V, Aerts T et al. Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J Biol Chem 2001; 276: 38949-38955.
5. Trent JT 3rd, Watts RA, Hargrove MS. Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J Biol Chem 2001; 276: 30106-30110.
6. Fordel E, Thijs L, Martinet W, Schrijvers D, Moens L, Dewilde S. Anoxia or oxygen and glucose deprivation in SH-SY5Y cells: a step closer to the unraveling of neuroglobin and cytoglobin functions. Gene 2007; 398: 114-122.
7. Brunori M, Giuffre A, Nienhaus K, Nienhaus GU, Scandurra FM, B Vallone. Neuroglobin nitric oxide, and oxygen: functional pathways and conformational changes. Proc Natl Acad Sci USA 2005; 102: 8483-8488.
8. Jayaraman T, Tejero J, Chen BB, Blood AB, Frizzell S, Shapiro C et al. 14-3-3 binding and phosphorylation of neuroglobin during hypoxia modulate six-to-five heme pocket coordination and rate of nitrite reduction to nitric oxide. J Biol Chem 2011; 286: 42679-42689.
9. Greenberg DA, Jin K, Khan AA. Neuroglobin: an endogenous neuroprotectant. Curr Opin Pharmacol 2008; 8: 20-24.
10. Shao G, Gong KR, Li J, Xu XJ, Gao CY, Zeng XZ et al. Antihypoxic effects of neuroglobin in hypoxia-preconditioned mice and SH-SY5Y cells. Neurosignals 2009; 17: 196-202.
11. Khan AA, Wang Y, Sun Y, Mao XO, Xie L, Miles E et al. Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia. Proc Natl Acad Sci USA 2006; 103: 17944-17948.
12. 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.
13. 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.
14. Yu Z, Fan X, Lo EH, Wang X. Neuroprotective roles and mechanisms of neuroglobin. Neurol Res 2009; 31: 122-127.
15. Brittain T, Skommer J, Henty K, Birch N, Raychaudhuri S. A role for human neuroglobin in apoptosis. IUBMB Life 2010; 62: 878-885.
16. Brittain T, Skommer J, Raychaudhuri S, Birch N. An antiapoptotic neuroprotective role for neuroglobin. Int J Mol Sci 2010; 11: 2306-2321.
17. Fago A, Mathews AJ, Brittain T. A role for neuroglobin: resetting the trigger level for apoptosis in neuronal and retinal cells. IUBMB Life 2008; 60: 398-401.
18. Raychaudhuri S, Skommer J, Henty K, Birch N, Brittain T. Neuroglobin protects nerve cells from apoptosis by inhibiting the intrinsic pathway of cell death. Apoptosis 2010; 15: 401-411.
19. Ascenzi P, Polticelli F, Marino M, Santucci R, Coletta M. Cardiolipin drives cytochrome c proapoptotic and antiapoptotic actions. IUBMB Life 2011; 63: 160-165.
20. De Marinis E, Ascenzi P, Pellegrini M, Galluzzo P, Bulzomi P, Arevalo MA et al. 17Betaestradiol- a new modulator of neuroglobin levels in neurons: role in neuroprotection against HO-induced toxicity. Neurosignals 2010; 18: 223-235.
21. De Marinis E, Marino M, P Ascenzi. Neuroglobin estrogens, and neuroprotection. IUBMB Life 2011; 63: 140-145.
22. Arnold S, Beyer C. Neuroprotection by estrogen in the brain: the mitochondrial compartment as presumed therapeutic target. J Neurochem 2009; 110: 1-11.
23. Simpkins JW, Yang SH, Sarkar SN, Pearce V. Estrogen actions on mitochondriaphysiological and pathological implications. Mol Cell Endocrinol 2008; 290: 51-59.
24. Ow YP, Green DR, Hao Z, Mak TW. Cytochrome c: functions beyond respiration. Nat Rev Mol Cell Biol 2008; 9: 532-542.
25. Purring-Koch C, McLendon G. Cytochrome c binding to Apaf-1: the effects of dATP and ionic strength. Proc Natl Acad Sci USA 2000; 97: 11928-11931.
26. Hankeln T,Wystub S, Laufs T, Schmidt M, Gerlach F, Saaler-Reinhardt S et al. The cellular and subcellular localization of neuroglobin and cytoglobin - a clue to their function? IUBMB Life 2004; 56: 671-679.
27. Brittain T, Skommer J. Does a redox cycle provide a mechanism for setting the capacity of neuroglobin to protect cells from apoptosis? IUBMB Life 2012; 64: 419-422.
28. Hundahl CA, Allen GC, Hannibal J, Kjaer K, Rehfeld JF, Dewilde S et al. Anatomical characterization of cytoglobin and neuroglobin mRNA and protein expression in the mouse brain. Brain Res 2010; 1331: 58-73.
29. Hundahl CA, Luuk H, Ilmjarv S, Falktoft B, Raida Z, Vikesaa J et al. Neuroglobin-deficiency exacerbates Hif1A and c-FOS response, but does not affect neuronal survival during severe hypoxia in vivo. PLoS One 2011; 6: e28160.
30. Haines B, Demaria M, Mao X, Xie L, Campisi J, Jin K et al. Hypoxia-inducible factor-1 and neuroglobin expression. Neurosci Lett 2012; 51: 137-1340.
31. Yu Z, Liu N, Wang Y, Li X, Wang X. Identification of neuroglobin- interacting proteins using yeast two-hybrid screening. Neuroscience 2012; 200: 99-105.
32. Arnold S, Victor MB, Beyer C. Estrogen and the regulation of mitochondrial structure and function in the brain. J Steroid Biochem Mol Biol 2012; 131: 2-9.
33. Okoh V, Deoraj A, Roy D. Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta 2011; 1815: 115-133.
34. Borras C, Gambini J, Lopez-Grueso R, Pallardo FV, Vina J. Direct antioxidant and protective effect of estradiol on isolated mitochondria. Biochim Biophys Acta 2010; 1802: 205-211.
35. Bonding SH, Henty K, Dingley AJ, Brittain T. The binding of cytochrome c to neuroglobin: a docking and surface plasmon resonance study. Int J Biol Macromol 2008; 43: 295-299.
36. Fago A, Mathews AJ, Dewilde S, Moens L, Brittain T. The reactions of neuroglobin with CO: evidence for two forms of the ferrous protein. J Inorg Biochem 2006; 100: 1339-1343.
37. Nadal-Serrano M, Sastre-Serra J, Pons DG, Miro AM, Oliver J, Roca P. The ERalpha/ ERbeta ratio determines oxidative stress in breast cancer cell lines in response to 17betaestradiol. J Cell Biochem 2012; 113: 3178-3185.
38. Flynn JM, Dimitrijevich SD, Younes M, Skliris G, Murphy LC, Cammarata PR. Role of wild-type estrogen receptor-beta in mitochondrial cytoprotection of cultured normal male and female human lens epithelial cells. Am J Physiol Endocrinol Metab 2008; 295: E637-E647.
39. Yang SH, Sarkar SN, Liu R, Perez EJ, Wang X, Wen Y et al. Estrogen receptor beta as a mitochondrial vulnerability factor. J Biol Chem 2009; 284: 9540-9548.
40. Fordel E, Thijs L, Martinet W, Lenjou M, Laufs T, Van Bockstaele D et al. Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells against oxidative stress-induced cell death. Neurosci Lett 2006; 410: 146-151.