Induction of transcription factor CEBP homology protein mediates hypoglycaemia-induced necrotic cell death in human neuroblastoma cells

Journal of Neurochemistry

Volumn 99, Issue 3, 2006, Pages 952-964

  Kögel, Donat ^a   Svensson, Birte ^b   Copanaki, Ekaterini ^a   Anguissola, Sergio ^c   Bonner, Caroline ^c   Thurow, Nadia ^a   Gudorf, Daniel ^b   Hetschko, Holger ^a   Müller, Thorsten ^b   Peters, Marion ^b   König, Hans Georg ^a,c   Prehn, Jochen H M ^c  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Metabolic stress; Necrosis; Neuroprotection; Oxygen; Transcriptome analysis

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CEBP HOMOLOGY PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; CANCER CELL CULTURE; CELL HYPOXIA; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOGLYCEMIA; MICROARRAY ANALYSIS; NERVE CELL NECROSIS; NEUROBLASTOMA CELL; NEUROPROTECTION; PRIORITY JOURNAL; PROTEIN INDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

ANOXIA; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CASPASE 3; CCAAT-ENHANCER-BINDING PROTEINS; CELL DEATH; CELL LINE, TUMOR; FLUORESCENT DYES; GLUCOSE; HUMANS; HYPOGLYCEMIA; NECROSIS; NEUROBLASTOMA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33750078076     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04135.x     Document Type: Article

References (58)

1. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A. and Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
2. Baehrecke E. H. (2005) Autophagy: dual roles in life and death? Nat. Rev. Mol. Cell Biol. 6, 505-510.
3. Bernaudin M., Nedelec A. S., Divoux D., MacKenzie E. T., Petit E. and Schumann-Bard P. (2002) Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J. Cereb. Blood Flow Metab 22, 393-403.
4. Brusselmans K., Bono F., Collen D., Herbert J. M., Carmeliet P. and Dewerchin M. (2005) A novel role for vascular endothelial growth factor as an autocrine survival factor for embryonic stem cells during hypoxia. J. Biol. Chem. 280, 3493-3499.
5. Bursch W., Ellinger A., Kienzl H., Torok L., Pandey S., Sikorska M., Walker R. and Hermann R. S. (1996) Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 17, 1595-1607.
6. Carlson S. G., Fawcett T. W., Bartlett J. D., Bernier M. and Holbrook N. J. (1993) Regulation of the C/EBP-related gene gadd153 by glucose deprivation. Mol. Cell Biol. 13, 4736-4744.
7. Carmeliet P. and Jain R. K. (2000) Angiogenesis in cancer and other diseases. Nature 407, 249-257.
8. Carmeliet P. and Storkebaum E. (2002) Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin. Cell Dev. Biol. 13, 39-53.
9. Dirnagl U., Simon R. P. and Hallenbeck J. M. (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 26, 248-254.
10. Eisen M. B., Spellman P. T., Brown P. O. and Botstein D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA 95, 14 863-14 868.
11. Fern R., Davis P., Waxman S. G. and Ransom B. R. (1998) Axon conduction and survival in CNS white matter during energy deprivation: a developmental study. J. Neurophysiol. 79, 95-105.
12. Ferrara N., Gerber H. P. and LeCouter J. (2003) The biology of VEGF and its receptors. Nat. Med. 9, 669-676.
13. Gatenby R. A. and Gillies R. J. (2004) Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4, 891-899.
14. Golstein P. and Kroemer G. (2005) Redundant cell death mechanisms as relics and backups. Cell Death Differ. 12, 1490-1496.
15. Gottron F. J., Ying H. S. and Choi D. W. (1997) Caspase inhibition selectively reduces the apoptotic component of oxygen-glucose deprivation-induced cortical neuronal cell death. Mol. Cell Neurosci. 9, 159-169.
16. Harmey J. H. and Bouchier-Hayes D. (2002) Vascular endothelial growth factor (VEGF), a survival factor for tumour cells: implications for anti-angiogenic therapy. Bioessays 24, 280-283.
17. Harris A. L. (2002) Hypoxia - a key regulatory factor in tumour growth. Nat. Rev. Cancer 2, 38-47.
18. Jin K. L., Mao X. O. and Greenberg D. A. (2000) Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc. Natl Acad. Sci. USA 97, 10 242-10 247.
19. Jin K., Mao X. O., Eshoo M. W., Nagayama T., Minami M., Simon R. P. and Greenberg D. A. (2001) Microarray analysis of hippocampal gene expression in global cerebral ischemia. Ann. Neurol. 50, 93-103.
20. Jones N. M. and Bergeron M. (2001) Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J. Cereb. Blood Flow Metab. 21, 1105-1114.
21. Jones R. G., Plas D. R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M. J. and Thompson C. B. (2005) AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 18, 283-293.
22. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y. and Yoshimori T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
23. Kaufman R. J., Scheuner D., Schroder M., Shen X., Lee K., Liu C. Y. and Arnold S. M. (2002) The unfolded protein response in nutrient sensing and differentiation. Nat. Rev. Mol. Cell Biol. 3, 411-421.
24. Kögel D., Reimertz C., Mech P., Poppe M., Frühwald M. C., Engemann H., Scheidtmann K. H. and Prehn J. H. (2001) Dlk/ZIP kinase-induced apoptosis in human medulloblastoma cells: requirement of the mitochondrial apoptosis pathway. Br. J. Cancer 85, 1801-1808.
25. Kögel D., Reimertz C., Düßmann H., Mech P., Scheidtmann K. H. and Prehn J. H. (2003) The death associated protein (DAP) kinase homologue Dlk/ZIP kinase induces p19ARF- and p53-independent apoptosis. Eur. J. Cancer 39, 249-256.
26. Kuwana T. and Newmeyer D. D. (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr. Opin. Cell Biol. 15, 691-699.
27. Lambrechts D., Storkebaum E., Morimoto M. et al. (2003) VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet 34, 383-394.
28. Lee J. M., Grabb M. C., Zipfel G. J. and Choi D. W. (2000) Brain tissue responses to ischemia. J. Clin. Invest. 106, 723-731.
29. Li C. and Wong W. H. (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl Acad. Sci. USA 98, 31-36.
30. Liu Y. and Downey J. M. (1992) Ischemic preconditioning protects against infarction in rat heart. Am. J. Physiol. 263, H1107-H1112.
31. Loike J. D., Cao L., Brett J., Ogawa S., Silverstein S. C. and Stern D. (1992) Hypoxia induces glucose transporter expression in endothelial cells. Am. J. Physiol. 263, C326-C333.
32. Luetjens C. M., Lankiewicz S., Bui N. T., Krohn A. J., Poppe M. and Prehn J. H. (2001) Up-regulation of Bcl-xL in response to subtoxic β-amyloid: role in neuronal resistance against apoptotic and oxidative injury. Neuroscience 102, 139-150.
33. Machein M. R. and Plate K. H. (2000) VEGF in brain tumors. J. Neurooncol. 50, 109-120.
34. Marciniak S. J., Yun C. Y., Oyadomari S., Novoa I., Zhang Y., Jungreis R., Nagata K., Harding H. P. and Ron D. (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18, 3066-3077.
35. McCullough K. D., Martindale J. L., Klotz L. O., Aw T. Y. and Holbrook N. J. (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell Biol. 21, 1249-1259.
36. Michiels C. (2004) Physiological and pathological responses to hypoxia. Am. J. Pathol. 164, 1875-1882.
37. Murry C. E., Jennings R. B. and Reimer K. A. (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74, 1124-1136.
38. Nicholson D. W. (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 6, 1028-1042.
39. Ogunshola O. O., Antic A., Donoghue M. J., Fan S. Y., Kim H., Stewart W. B., Madri J. A. and Ment L. R. (2002) Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 277, 11 410-11 415.
40. Onoue S., Kumon Y., Igase K., Ohnishi T. and Sakanaka M. (2005) Growth arrest and DNA damage-inducible gene 153 increases transiently in the thalamus following focal cerebral infarction. Brain Res. Mol. Brain Res. 134, 189-197.
41. Papandreou I., Krishna C., Kaper F., Cai D., Giaccia A. J. and Denko N. C. (2005) Anoxia is necessary for tumor cell toxicity caused by a low-oxygen environment. Cancer Res. 65, 3171-3178.
42. Peralta C., Hotter G., Closa D., Gelpi E., Bulbena O. and Rosello-Catafau J. (1997) Protective effect of preconditioning on the injury associated to hepatic ischemia-reperfusion in the rat: role of nitric oxide and adenosine. Hepatology 25, 934-937.
43. Piret J. P., Lecocq C., Toffoli S., Ninane N., Raes M. and Michiels C. (2004) Hypoxia and CoCl2 protect HepG2 cells against serum deprivation- and t-BHP-induced apoptosis: a possible anti-apoptotic role for HIF-1. Exp. Cell Res. 295, 340-349.
44. Semenza G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732.
45. Sharp F. R. and Bernaudin M. (2004) HIF1 and oxygen sensing in the brain. Nat. Rev. Neurosci. 5, 437-448.
46. Silverman H. S., Wei S., Haigney M. C., Ocampo C. J. and Stern M. D. (1997) Myocyte adaptation to chronic hypoxia and development of tolerance to subsequent acute severe hypoxia. Circ. Res. 80, 699-707.
47. Stys P. K., Ransom B. R., Waxman S. G. and Davis P. K. (1990) Role of extracellular calcium in anoxic injury of mammalian central white matter. Proc. Natl Acad. Sci. USA 87, 4212-4216.
48. Svensson B., Peters M., König H. G., Poppe M., Levkau B., Rothermundt M., Arolt V., Kögel D. and Prehn J. H. (2002) Vascular endothelial growth factor protects cultured rat hippocampal neurons against hypoxic injury via an anti-excitotoxic, caspase-independent mechanism. J. Cereb. Blood Flow Metab. 22, 1170-1175.
49. Tajiri S., Oyadomari S., Yano S., Morioka M., Gotoh T., Hamada J. I., Ushio Y. and Mori M. (2004) Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ. 11, 403-415.
50. Tang J. R., Nakamura M., Okura T., Takata Y., Watanabe S., Yang Z. H., Liu J., Kitami Y. and Hiwada K. (2002) Mechanism of oxidative stress-induced GADD153 gene expression in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 290, 1255-1259.
51. Tsujimoto Y. and Shimizu S. (2005) Another way to die: autophagic programmed cell death. Cell Death Differ. 12, 1528-1534.
52. Unno N., Menconi M. J., Salzman A. L., Smith M., Hagen S., Ge Y., Ezzell R. M. and Fink M. P. (1996) Hyperpermeability and ATP depletion induced by chronic hypoxia or glycolytic inhibition in Caco-2BBe monolayers. Am. J. Physiol. 270, G1010-G1021.
53. Wang C., Nguyen H. N., Maguire J. L. and Perry D. C. (2002) Role of intracellular calcium stores in cell death from oxygen-glucose deprivation in a neuronal cell line. J. Cereb. Blood Flow Metab. 22, 206-214.
54. Yamaguchi H. and Wang H. G. (2004) CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J. Biol. Chem. 279, 45 495-45 502.
55. Yancopoulos G. D., Davis S., Gale N. W., Rudge J. S., Wiegand S. J. and Holash J. (2000) Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248.
56. Yoshioka A., Ikegaki N., Williams M. and Pleasure D. (1996) Expression of N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor genes in neuroblastoma, medulloblastoma, and other cells lines. J. Neurosci. Res. 46, 164-178.
57. Zaulyanov L. L., Green P. S. and Simpkins J. W. (1999) Glutamate receptor requirement for neuronal death from anoxia-reoxygenation: an in vitro model for assessment of the neuroprotective effects of estrogens. Cell Mol. Neurobiol. 19, 705-718.
58. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R. T., Remotti H., Stevens J. L. and Ron D. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995.