Prolyl hydroxylase inhibitors delay neuronal cell death caused by trophic factor deprivation

Journal of Neurochemistry

Volumn 103, Issue 5, 2007, Pages 1897-1906

  Lomb, David J ^a   Straub, Jennifer A ^a,b   Freeman, Robert S ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; EGLN; Hypoxia inducible factor; JNK; Nerve growth factor; Sympathetic neuron

Indexed keywords

BENZOIC ACID; BH3 PROTEIN; CYTOCHROME C; DIMETHYLOXALYLGLYCINE; ENZYME INHIBITOR; ETHYL 3,4 DIHYDROXYBENZOIC ACID; GENE PRODUCT; GLYCINE DERIVATIVE; HEXOKINASE 2 PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 2ALPHA; NERVE GROWTH FACTOR; PROLYL HYDROXYLASE INHIBITOR; PROTEIN BCL 2; PROTOCATECHUIC ACID; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; MITOCHONDRION; NERVE CELL; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RAT; UPREGULATION;

AMINO ACIDS, DICARBOXYLIC; ANIMALS; ANIMALS, NEWBORN; CELL DEATH; CELLS, CULTURED; CYTOCHROMES C; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HYDROXYBENZOIC ACIDS; MITOCHONDRIA; NERVE GROWTH FACTOR; NEURONS; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTO-ONCOGENE PROTEINS C-JUN; RATS; SUPERIOR CERVICAL GANGLION;

EID: 36248945117     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04873.x     Document Type: Article

References (54)

1. Aminova L. R., Chavez J. C., Lee J., Ryu H., Kung A., LaManna J. C. Ratan R. R. (2005) Prosurvival and prodeath effects of hypoxia-inducible factor-1alpha stabilization in a murine hippocampal cell line. J. Biol. Chem. 280, 3996 4003.
2. Aprelikova O., Chandramouli G. V., Wood M., Vasselli J. R., Riss J., Maranchie J. K., Linehan W. M. Barrett J. C. (2004) Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J. Cell. Biochem. 92, 491 501.
3. Bruckner S. R., Tammariello S. P., Kuan C. Y., Flavell R. A., Rakic P. Estus S. (2001) JNK3 contributes to c-Jun activation and apoptosis but not oxidative stress in nerve growth factor-deprived sympathetic neurons. J. Neurochem. 78, 298 303.
4. Bruick R. K. McKnight S. L. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337 1340.
5. Deckwerth T. L., Elliott J. L., Knudson C. M., Johnson E. M., Snider W. D. Korsmeyer S. J. (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17, 401 411.
6. Deshmukh M. Johnson E. M., Jr. (1998) Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 21, 695 705.
7. Edwards S. N., Buckmaster A. E. Tolkovsky A. M. (1991) The death programme in cultured sympathetic neurones can be suppressed at the posttranslational level by nerve growth factor, cyclic AMP, and depolarization. J. Neurochem. 57, 2140 2143.
8. Eilers A., Whitfield J., Shah B., Spadoni C., Desmond H. Ham J. (2001) Direct inhibition of c-Jun N-terminal kinase in sympathetic neurones prevents c-jun promoter activation and NGF withdrawal-induced death. J. Neurochem. 76, 1439 1454.
9. Epstein A. C., Gleadle J. M., McNeill L. A. et al. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43 54.
10. Estus S., Zaks W. J., Freeman R. S., Gruda M., Bravo R. Johnson E. M. (1994) Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127, 1717 1727.
11. Farinelli S. E. Greene L. A. (1996) Cell cycle blockers mimosine, ciclopirox, and deferoxamine prevent the death of PC12 cells and postmitotic sympathetic neurons after removal of trophic support. J. Neurosci. 16, 1150 1162.
12. Ferrari G., Yan C. Y. Greene L. A. (1995) N-acetylcysteine (D- and L-stereoisomers) prevents apoptotic death of neuronal cells. J. Neurosci. 15, 2857 2866.
13. Freeman R. S., Estus S. Johnson E. M. (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12, 343 355.
14. Freeman R. S., Burch R. L., Crowder R. J., Lomb D. J., Schoell M. C., Straub J. A. Xie L. (2004) NGF deprivation-induced gene expression: after ten years, where do we stand? Prog. Brain Res. 146, 111 126.
15. Ham J., Babij C., Whitfield J., Pfarr C. M., Lallemand D., Yaniv M. Rubin L. L. (1995) A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14, 927 939.
16. Ham J., Towers E., Gilley J., Terzano S. Randall R. (2005) BH3-only proteins: key regulators of neuronal apoptosis. Cell Death Differ. 12, 1015 1020.
17. Harding T. C., Xue L., Bienemann A., Haywood D., Dickens M., Tolkovsky A. M. Uney J. B. (2001) Inhibition of JNK by overexpression of the JNK binding domain of JIP-1 prevents apoptosis in sympathetic neurons. J. Biol. Chem. 276, 4531 4534.
18. Harris C. A. Johnson E. M. (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J. Biol. Chem. 276, 37754 37760.
19. Harris C. A., Deshmukh M., Tsui-Pierchala B., Maroney A. C. Johnson E. M. (2002) Inhibition of the c-Jun N-terminal kinase signaling pathway by the mixed lineage kinase inhibitor CEP-1347 (KT7515) preserves metabolism and growth of trophic factor-deprived neurons. J. Neurosci. 22, 103 113.
20. Hewitson K. S. Schofield C. J. (2004) The HIF pathway as a therapeutic target. Drug Discov Today 9, 704 711.
21. Hirsilä M., Koivunen P., Günzler V., Kivirikko K. I. Myllyharju J. (2003) Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J. Biol. Chem. 278, 30772 30780.
22. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J. M., Lane W. S. Kaelin W. G., Jr. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292, 464 468.
23. Ivan M., Haberberger T., Gervasi D. C. et al. (2002) Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc. Natl Acad. Sci. USA 99, 13459 13464.
24. Jaakkola P., Mole D. R., Tian Y. M. et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292, 468 472.
25. Kim J. W., Tchernyshyov I., Semenza G. L. Dang C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3, 177 185.
26. Lee S., Nakamura E., Yang H. et al. (2005) Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 8, 155 167.
27. Lipscomb E. A., Sarmiere P. D., Crowder R. J. Freeman R. S. (1999) Expression of the SM-20 gene promotes death in nerve growth factor-dependent sympathetic neurons. J. Neurochem. 73, 429 432.
28. Lipscomb E. A., Sarmiere P. D. Freeman R. S. (2001) SM-20 is a novel mitochondrial protein that causes caspase-dependent cell death in nerve growth factor-dependent neurons. J. Biol. Chem. 276, 5085 5092.
29. Maroney A. C., Finn J. P., Bozyczko-Coyne D., O'Kane T. M., Neff N. T., Tolkovsky A. M., Park D. S., Yan C. Y., Troy C. M. Greene L. A. (1999) CEP-1347 (KT7515), an inhibitor of JNK activation, rescues sympathetic neurons and neuronally differentiated PC12 cells from death evoked by three distinct insults. J. Neurochem. 73, 1901 1912.
30. Martin D. P., Schmidt R. E., DiStefano P. S., Lowry O. H., Carter J. G. Johnson E. M. Jr. (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106, 829 844.
31. Martin D. P., Ito A., Horigome K., Lampe P. A. Johnson E. M. (1992) Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol. 23, 1205 1220.
32. Mathupala S. P., Rempel A. Pedersen P. L. (2001) Glucose catabolism in cancer cells: identification and characterization of a marked activation response of the type II hexokinase gene to hypoxic conditions. J. Biol. Chem. 276, 43407 43412.
33. Naranjo-Suarez S., Castellanos M. C., Alvarez-Tejado M., Vara A., Landazuri M. O. del Peso L. (2003) Down-regulation of hypoxia-inducible factor-2 in PC12 cells by nerve growth factor stimulation. J. Biol. Chem. 278, 31895 31901.
34. Ockaili R., Natarajan R., Salloum F., Fisher B. J., Jones D., Fowler A. A. III. Kukreja R. C. (2005) HIF-1 activation attenuates postischemic myocardial injury: role for heme oxygenase-1 in modulating microvascular chemokine generation. Am. J. Physiol. Heart Circ. Physiol. 289, H542 H548.
35. Oppenheim R. W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453 501.
36. Palmada M., Kanwal S., Rutkoski N. J., Gufstafson-Brown C., Johnson R. S., Wisdom R. Carter B. D. (2002) c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J. Cell Biol. 158, 453 461.
37. Papandreou I., Cairns R. A., Fontana L., Lim A. L. Denko N. C. (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 3, 187 197.
38. Park D. S., Stefanis L., Yan C. Y., Farinelli S. E. Greene L. A. (1996) Ordering the cell death pathway. Differential effects of BCL2, an interleukin-1-converting enzyme family protease inhibitor, and other survival agents on JNK activation in serum/nerve growth factor-deprived PC12 cells. J. Biol. Chem. 271, 21898 21905.
39. Putcha G. V., Moulder K. L., Golden J. P., Bouillet P., Adams J. A., Strasser A. Johnson E. M. (2001) Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron 29, 615 628.
40. Putcha G. V., Le S., Frank S. et al. (2003) JNK-Mediated BIM Phosphorylation Potentiates BAX-Dependent Apoptosis. Neuron 38, 899 914.
41. Robey R. B. Hay N. (2006) Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene 25, 4683 4696.
42. Semenza G. L. (2000) HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474 1480.
43. Shi G. F., An L. J., Jiang B., Guan S. Bao Y. M. (2006) Alpinia protocatechuic acid protects against oxidative damage in vitro and reduces oxidative stress in vivo. Neurosci. Lett. 403, 206 210.
44. Siddiq A., Ayoub I. A., Chavez J. C. et al. (2005) Hypoxia-inducible factor prolyl 4-hydroxylase inhibition. A target for neuroprotection in the central nervous system. J. Biol. Chem. 280, 41732 41743.
45. Soucek T., Cumming R., Dargusch R., Maher P. Schubert D. (2003) The regulation of glucose metabolism by HIF-1 mediates a neuroprotective response to amyloid beta peptide. Neuron 39, 43 56.
46. Straub J. A., Lipscomb E. A., Yoshida E. S. Freeman R. S. (2003) Induction of SM-20 in PC12 cells leads to increased cytochrome c levels, accumulation of cytochrome c in the cytosol, and caspase-dependent cell death. J. Neurochem. 85, 318 328.
47. Takeda K., Ho V. C., Takeda H., Duan L. J., Nagy A. Fong G. H. (2006) Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol. Cell. Biol. 26, 8336 8346.
48. Taylor M. S. (2001) Characterization and comparative analysis of the EGLN gene family. Gene 275, 125 132.
49. Tsui-Pierchala B. A., Putcha G. V. Johnson E. M. Jr. (2000) Phosphatidylinositol 3-kinase is required for the trophic, but not the survival-promoting, actions of NGF on sympathetic neurons. J. Neurosci. 20, 7228 7237.
50. Ueda J., Saito N., Shimazu Y. Ozawa T. (1996) A comparison of scavenging abilities of antioxidants against hydroxyl radicals. Arch. Biochem. Biophys. 333, 377 384.
51. Wang J., Buss J. L., Chen G., Ponka P. Pantopoulos K. (2002) The prolyl 4-hydroxylase inhibitor ethyl-3,4-dihydroxybenzoate generates effective iron deficiency in cultured cells. FEBS Lett. 529, 309 312.
52. Whitfield J., Neame S. J., Paquet L., Bernard O. Ham J. (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29, 629 643.
53. Wright G., Higgin J. J., Raines R. T., Steenbergen C. Murphy E. (2003) Activation of the prolyl hydroxylase oxygen-sensor results in induction of GLUT1, HO-1, NOS-2 proteins, and confers protection from metabolic inhibition to cardiomyocytes. J. Biol. Chem. 278, 20235 20239.
54. Xie L., Johnson R. S. Freeman R. S. (2005) Inhibition of NGF deprivation-induced death by low oxygen involves suppression of BIM(EL) and activation of HIF-1. J. Cell Biol. 168, 911 920.