Impairment of the mitochondrial respiratory enzyme activity triggers sequential activation of apoptosis-inducing factordependent and caspase-dependent signaling pathways to induce apoptosis after spinal cord injury

Journal of Neurochemistry

Volumn 101, Issue 6, 2007, Pages 1552-1566

  Wu, Kay L H ^a,b   Hsu, Chin ^a   Chan, Julie Y H ^b  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Apoptosis; Apoptosis inducing factor; Caspase; Coenzyme Q10; Cytochrome c; Mitochondrial respiratory enzyme complex

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOPTOSIS INDUCING FACTOR; CASPASE; CASPASE 3; CASPASE 9; CYTOCHROME C; DNA FRAGMENT; MITOCHONDRIAL ENZYME; UBIDECARENONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BIOENERGY; CELL DEATH; CONTINUOUS INFUSION; CONTROLLED STUDY; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFECT; ENZYME ACTIVATION; GENE TRANSLOCATION; MALE; MICROGLIA; MITOCHONDRIAL RESPIRATION; MOLECULAR WEIGHT; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 9; COENZYMES; CYTOCHROMES C; DNA FRAGMENTATION; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; MALE; MITOCHONDRIA; NADH DEHYDROGENASE; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; SPECIFIC PATHOGEN-FREE ORGANISMS; SPINAL CORD; SPINAL CORD INJURIES; UBIQUINONE;

EID: 34249802899     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04445.x     Document Type: Article

References (74)

1. Alano C. C., Ying W. Swanson R. A. (2004) Poly (ADP-ribose) polymerase-1-mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition. J. Biol. Chem. 279, 18895 18902.
2. Bagci E. Z., Vodovotz Y., Billiar T. R., Ermentrout G. B. Bahar I. (2006) Bistability in apoptosis: roles of bax, bcl-2, and mitochondrial permeability transition pores. Biophys. J. 90, 1546 1559.
3. Bahi N., Zhang J., Llovera M., Ballester M., Comella J. X. Sanchis D. (2006) Switch from caspase-dependent to caspase-independent death during heart development: essential role of endonuclease G in ischemia-induced DNA processing of differentiated cardiomyocytes. J. Biol. Chem. 281, 22943 22952.
4. Baud O., Li J., Zhang Y., Neve R. L., Volpe J. J. Rosenberg P. A. (2004) Nitric oxide-induced cell death in developing oligodendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eu. J. Neurosci. 20, 1713 1726.
5. Beattie M. S. (2004) Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol. Med. 10, 580 583.
6. Beattie M. S., Hermann G. E., Rogers R. C. Bresnahan J. C. (2002) Cell death in models of spinal cord injury. Prog. Brain Res. 137, 37 47.
7. Bidere N. Senik A. (2001) Caspase-independent apoptotic pathways in T lymphocytes: a minireview. Apoptosis 6, 371 375.
8. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P. Lipton S. A. (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. U.S.A. 92, 7162 7166.
9. Cande C., Vahsen N., Garrido C. Kroemer G. (2004) Apoptosis-inducing factor (AIF): caspase-independent after all. Cell Death Differ. 11, 591 595.
10. Carlson G. D. Gorden C. (2002) Current developments in spinal cord injury research. Spine J. 2, 116 128.
11. Chan P. H. (2004) Mitochondria and neuronal death/survival signaling pathways in cerebral ischemia. Neurochem. Res. 29, 1943 1949.
12. Chan S. H. H., Wu K. L. H., Wang L. L. Chan J. Y. (2005) Nitric oxide- and superoxide-dependent mitochondrial signaling in endotoxin-induced apoptosis in the rostral ventrolateral medulla of rats. Free Radic. Biol. Med. 39, 603 618.
13. Chandra D., Liu J. W. Tang D. G. (2002) Early mitochondrial activation and cytochrome c up-regulation during apoptosis. J. Biol. Chem. 277, 50842 50854.
14. Chauvin C., De Oliveira F., Ronot X., Mousseau M., Leverve X. Fontaine E. (2001) Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J. Biol. Chem. 276, 41394 41398.
15. Cheng H., Cao Y. Olson L. (1996) Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273, 510 513.
16. Chuang Y. C., Tsai J. L., Chang A. Y., Chan J. Y., Liou C. W. Chan S. H. H. (2002) Dysfunction of the mitochondrial respiratory chain in the rostral ventrolateral medulla during experimental endotoxemia in the rat. J Biomed. Sci. 9, 542 548.
17. Chuang Y. C., Chan J. Y. H., Chang A. Y. W., Sidorska M., Borowy-Borowski H., Liou C. W. Chan S. H. H. (2003) Neuroprotective effects of coenzyme Q10 at rostral ventrolateral medulla against fatality during experimental endotoxemia in the rat. Shock 19, 427 432.
18. Clarke P. G. (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181, 195 213.
19. Cregan S. P., Fortin A., MacLaurin J. G. et al. (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J. Cell Biol. 158, 507 517.
20. Cregan S. P., Dawson V. L. Slack R. S. (2004) Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 23, 2785 2796.
21. De Giorgi F., Lartigue L., Bauer M. K., Schubert A., Grimm S., Hanson G. T., Remington S. J., Youle R. J. Ichas F. (2002) The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J. 16, 607 609.
22. Dumont R. J., Okonkwo D. O., Verma S., Hurlbert R. J., Boulos P. T., Ellegala D. B. Dumont A. S. (2001) Acute spinal cord injury, part I: pathophysiologic mechanisms. Clin. Neuropharmacol. 24, 254 264.
23. Eldadah B. A. Faden A. I. (2000) Caspase pathways, neuronal apoptosis, and CNS injury. J. Neurotrauma 17, 811 829.
24. Ernster L. Dallner G. (1995) Biochemical, physiological and medical aspects of ubiquinone function. Biochim. Biophys. Acta 1271, 195 204.
25. Gomes-Leal W., Corkill D. J., Freire M. A., Picanço-Diniz C. W. Perry V. H. (2004) Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp. Neurol. 190, 456 467.
26. Guo Y., Srinivasula S. M., Druilhe A., Fernandes-Alnemri T. Alnemri E. S. (2002) Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J. Biol. Chem. 277, 1343013 1343017.
27. Hirai K., Sugawara T., Chan P. H., Basus V. J., James T. L. Litt L. (2002) Cytochrome c associated apoptosis during ATP recovery after hypoxia in neonatal rat cerebrocortical slices. J. Neurochem. 83, 309 319.
28. Ishihara Y. Shimamoto N. (2006) Involvement of endonuclease G in nucleosomal DNA fragmentation under sustained endogenous oxidative stress. J. Biol. Chem. 281, 6726 6733.
29. Joseph T. W. Moll U. M. (2003) Analysis of nuclear and cytoplasmic degradation of p53 in cells after stress. Methods Mol. Biol. 234, 211 217.
30. Kantrow S. P., Taylor D. E., Carraway M. S. Piantadosi C. A. (1997) Oxidative metabolism in rat hepatocytes and mitochondria during sepsis. Arch. Biochem. Biophys. 345, 278 288.
31. Keane R. W., Kraydieh S., Lotocki G., Bethea J. R., Krajewski S., Reed J. C. Dietrich W. D. (2001) Apoptotic and anti-apoptotic mechanisms following spinal cord injury. J. Neuropathol. Exp. Neurol. 60, 422 429.
32. Knoblach S. M., Huang X., VanGelderen J., Calva-Cerqueira D. Faden A. I. (2005) Selective caspase activation may contribute to neurological dysfunction after experimental spinal cord trauma. J. Neurosci. Res. 80, 369 380.
33. Kroemer G. Martin S. J. (2005) Caspase-independent cell death. Nat. Med. 11, 725 730.
34. Kroemer G. Reed J. C. (2000) Mitochondrial control of cell death. Nat. Med. 6, 513 519.
35. Kudin A. P., Bimpong-Buta N. Y., Vielhaber S., Elger C. E. Kunz W. S. (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 279, 4127 4135.
36. Lang-Rollin I. C., Rideout H. J., Noticewala M. Stefanis L. (2003) Mechanisms of caspase-independent neuronal death: energy depletion and free radical generation. J. Neurosci. 23, 11015 11025.
37. Lenaz G., Fato R., Castelluccio C., Genova M. L., Bovina C., Estornell E., Valls V., Pallotti F. Parenti C. G. (1993) The function of coenzyme Q in mitochondria. Clin. Invest. 71, 66 70.
38. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J. A. Robinson J. P. (2003) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278, 8516 8525.
39. Luetjens C. M., Bui N. T., Sengpiel B., Munstermann G., Poppe M., Krohn A. J., Bauerbach E., Krieglstein J. Prehn J. H. (2000) Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci. 20, 5715 5723.
40. Matsumori Y., Hong S. M., Aoyama K., Fan Y., Kayama T., Sheldon R. A., Vexler Z. S., Ferriero D. M., Weinstein P. R. Liu J. (2005) Hsp70 overexpression sequesters AIF and reduces neonatal hypoxic/ischemic brain injury. J. Cereb. Blood Flow Metab. 25, 899 910.
41. McCarthy S., Somayajulu M., Sikorska M., Borowy-Borowsk H. Pandey S. (2004) Paraquat induces oxidative stress and neuronal cell death; neuroprotection by water-soluble Coenzyme Q10. Toxicol. Appl. Pharmacol. 201, 21 31.
42. Naithani S., Saracco S. A., Butler C. A. Fox T. D. (2003) Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol. Biol. Cell. 14, 324 333.
43. Otake Y., Mims A. Fernandes D. J. (2006) Merbarone induces activation of caspase-activated DNase and excision of chromosomal DNA loops from the nuclear matrix. Mol. Pharmacol. 69, 1477 1485.
44. Papucci L., Schiavone N., Witort E. et al. (2003) Coenzyme Q10 prevents apoptosis by inhibiting mitochondrial depolarization independently of its free radical scavenging property. J. Biol. Chem. 278, 28220 28228.
45. Patel T., Gores G. J. Kaufmann S. H. (1996) The role of proteases during apoptosis. FASEB J. 10, 587 597.
46. Pelicano H., Feng L., Zhou Y., Carew J. S., Hileman E. O., Plunkett W., Keating M. J. Huang P. (2003) Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Biol. Chem. 278, 37832 37839.
47. Polster B. M. Fiskum G. (2004) Mitochondrial mechanisms of neural cell apoptosis. J. Neurochem. 90, 1281 1289.
48. Saito N., Yamamoto T., Watanabe T., Abe Y. Kumagai T. (2000) Implication of p53 protein expression in experimental spinal cord injury. J. Neurotrauma 17, 173 182.
49. Springer J. E., Azbill R. D. Knapp P. E. (1999) Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat. Med. 5, 943 946.
50. Stefanis L. (2005) Caspase-dependent and -independent neuronal death: two distinct pathways to neuronal injury. Neuroscientist 11, 50 62.
51. Stirling D. P., Khodarahmi K., Liu J., McPhail L. T., McBride C. B., Steeves J. D., Ramer M. S. Tetzlaff W. (2004) Miocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J. Neurosci. 24, 2182 2190.
52. Sullivan P. G., Rabchevsky A. G., Waldmeier P. C. Springer J. E. (2005) Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death J. Neurosci. Res. 79, 231 239.
53. Susin S. A., Lorenzo H. K., Zamzami N. et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441 446.
54. Tafani M., Karpinich N. O., Hurster K. A., Pastorino J. G., Schneider T., Russo M. A. Farber J. L. (2002) Cytochrome c release upon Fas receptor activation depends on translocation of full-length bid and the induction of the mitochondrial permeability transition. J. Biol. Chem. 277, 10073 10082.
55. Tai C. J., Chang S. J., Chien L. Y., Leung P. C. Tzeng C. R. (2005) Adenosine triphosphate induces activation of caspase-3 in apoptosis of human granulosa-luteal cells. Endocr. J. 52, 327 335.
56. Takahashi A. Earnshaw W. C. (1996) ICE-related proteases in apoptosis. Curr. Opin. Genet. Dev. 6, 50 55.
57. Tsai E. C., Krassioukow A. V. Tator C. H. (2005) Corticospinal regeneration into lumbar grey matter correlates with locomotor recovery after complete spinal cord transection and repair with peripheral nerve grafts, fibroblast growth factor 1, fibrin glue, and spinal fusion. J. Neuropathol. Exp. Neurol. 64, 230 244.
58. Tsujimoto Y. (2003) Cell death regulation by the Bcl-2 protein family in the mitochondria. J. Cell Physiol. 195, 158 167.
59. Tsukahara Y., Wakatsuki A. Okatani Y. (1999) Antioxidant role of endogenous coenzyme Q against the ischemia and reperfusion-induced lipid peroxidation in fetal rat brain. Acta Obste. Gynecol. Scand. 78, 669 674.
60. Ueda H. Fujita R. (2004) Cell death mode switches from necrosis to apoptosis in brain. Bio. Pharm. Bull. 27, 950 955.
61. Wang H., Yu S. W., Koh D. W., Lew J., Coombs C., Bowers W., Federoff H. J., Poirier G. G., Dawson T. M. Dawson V. L. (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J. Neurosci. 24, 10963 10973.
62. Wingrave J. M., Schaecher K. E., Sribnick E. A., Wilford G. G., Ray S. K., Hazen-Martin D. J., Hogan E. L. Banik N. L. (2003) Early induction of secondary injury factors causing activation of calpain and mitochondria-mediated neuronal apoptosis following spinal cord injury in rats. J. Neurosci. Res. 73, 95 104.
63. Wu K. L. H., Chan S. H. H., Chao Y. M. Chan J. Y. (2003) Expression of pro-inflammatory cytokine and caspase genes promotes neuronal apoptosis in pontine reticular formation after spinal cord transection. Neurobiol. Dis. 14, 19 31.
64. Xiang S., Pan W. Kastin A. J. (2005) Strategies to create a regenerating environment for the injured spinal cord. Curr. Pharm. Des. 11, 1267 1277.
65. Xie Q., Lin T., Zhang Y., Zheng J. Bonanno J. A. (2005) Molecular cloning and characterization of a human AIF-like gene with ability to induce apoptosis. J. Biol. Chem. 280, 19673 19681.
66. Yakovlev A. G. Faden A. I. (2001) Caspase-dependent apoptotic pathways in CNS injury. Mol. Neurobiol. 24, 131 144.
67. Yen D. H. T., Chan J. Y. H., Huang C. I., Lee C. H., Chan S. H. H. Chang A. Y. W. (2005) Coenzyme Q10 confers cardiovascular protection against acute mevinphos intoxication by ameliorating bioenergetic failure and hypoxia in the rostral ventrolateral medulla of the rat. Shock 23, 353 359.
68. Yong C., Arnold P. M., Zoubine M. N., Citron B. A., Watanabe I., Berman N. E. Festoff B. W. (1998) Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J. Neurotrauma 15, 459 472.
69. Yoshida H., Kong Y. Y., Yoshida R., Elia A. J., Hakem A., Hakem R., Penninger J. M. Mak T. W. (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739 750.
70. Zamzami N. Kroemer G. (2001) The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2, 67 71.
71. Zhang X., Chen J., Graham S. H. et al. (2002) Intranuclear localization of apoptosis-inducing factor (AIF) and large scale DNA fragmentation after traumatic brain injury in rats and in neuronal cultures exposed to peroxynitrite. J. Neurochem. 82, 181 191.
72. Zhu C., Qiu L., Wang X., Hallin U., Cande C., Kroemer G., Hagberg H. Blomgren K. (2003) Involvement of apoptosis-inducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain. J. Neurochem. 86, 306 317.
73. Zou H., Henzel W. J., Liu X., Lutschg A. Wang X. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405 413.
74. Zurita M., Vaquero J., Oya S. Morales C. (2002) Effects of dexamethasone on apoptosis-related cell death after spinal cord injury. J. Neurosurg. 96, 83 89.