Failure to complete apoptosis following neonatal hypoxia-ischemia manifests as "continuum" phenotype of cell death and occurs with multiple manifestations of mitochondrial dysfunction in rodent forebrain

Neuroscience

Volumn 149, Issue 4, 2007, Pages 822-833

  Northington, F J ^a   Zelaya, M E ^a   O'Riordan, D P ^a   Blomgren, K ^b,d   Flock, D L ^a   Hagberg, H ^b   Ferriero, D M ^c   Martin, L J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

Author keywords

continuum cell death; mitochondria; neonatal brain injury; neurodegeneration; ultrastructure

Indexed keywords

APOPTOSOME; CALPAIN; CASPASE 3; CASPASE 9; CYTOCHROME C OXIDASE; KINESIN; SPECTRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; FOREBRAIN; NECROSIS; NERVE DEGENERATION; NEWBORN HYPOXIA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYPOXIA-ISCHEMIA, BRAIN; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEURONS; PROSENCEPHALON; RATS; TIME FACTORS;

EID: 36248945038     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.06.060     Document Type: Article

References (43)

1. Al-Abdulla N.A., and Martin L.J. Apoptosis of retrograde degeneration neurons occurs in association with the accumulation of perikaryal mitochondria and oxidative damage to the nucleus. Am J Pathol 153 (1998) 447-456
2. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., and Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15 (1995) 961-973
3. Blomgren K., and Hagberg H. Free radicals, mitochondria, and hypoxia-ischemia in the developing brain. Free Radic Biol Med 40 (2006) 388-397
4. Blomgren K., Leist M., and Groc L. Pathological apoptosis in the developing brain. Apoptosis 12 (2007) 993-1010
5. Blomgren K., Zhu C., Wang X., Karlsson J.O., Leverin A.L., Bahr B.A., Mallard C., and Hagberg H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"?. J Biol Chem 276 (2001) 10191-10198
6. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S.A. 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 (1995) 7162-7166
7. Eguchi Y., Shimizu S., and Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57 (1997) 1835-1840
8. Ferriero D.M. Neonatal brain injury. N Engl J Med 351 (2004) 1985-1995
9. Fujikawa D.G. Confusion between neuronal apoptosis and activation of programmed cell death mechanisms in acute necrotic insults. Trends Neurosci 23 (2000) 410-411
10. Geddes R., Vannucci R.C., and Vannucci S.J. Delayed cerebral atrophy following moderate hypoxia-ischemia in the immature rat. Dev Neurosci 23 (2001) 180-185
11. Graham E.M., Sheldon R.A., Flock D.L., Ferriero D.M., Martin L.J., O'Riordan D.P., and Northington F.J. Neonatal mice lacking functional Fas death receptors are resistant to hypoxic-ischemic brain injury. Neurobiol Dis 17 (2004) 89-98
12. Han B.H., DeMattos R.B., Dugan L.L., Kim-Han J.S., Brendza R.P., Fryer J.D., Kierson M., Cirrito J., Quick K., Harmony J.A., Aronow B.J., and Holtzman D.M. Clusterin contributes to caspase-3-independent brain injury following neonatal hypoxia-ischemia. Nat Med 7 (2001) 338-343
13. Hentze H., Schwoebel F., Lund S., Keel M., Ertel W., Wendel A., Jaattela M., and Leist M. In vivo and in vitro evidence for extracellular caspase activity released from apoptotic cells. Biochem Biophys Res Commun 283 (2001) 1111-1117
14. Ishimaru M.J., Ikonomidou C., Tenkova T.I., Der T.C., Dikranian K., Sesma M.A., and Olney J.W. Distinguishing excitotoxic from apoptotic neurodegeneration in the developing rat brain. J Comp Neurol 408 (1999) 461-476
15. Kuida K., Haydar T.F., Kuan C.Y., Gu Y., Taya C., Karasuyama H., Su M.S., Rakic P., and Flavell R.A. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94 (1998) 325-337
16. Kuida K., Zheng T.S., Na S., Kuan C., Yang D., Karasuyama H., Rakic P., and Flavell R.A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384 (1996) 368-372
17. Leist M., Single B., Castoldi A.F., Kuhnle S., and Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185 (1997) 1481-1486
18. Leist M., Single B., Naumann H., Fava E., Simon B., Kuhnle S., and Nicotera P. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 249 (1999) 396-403
19. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., and Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91 (1997) 479-489
20. Martin L.J., Brambrink A.M., Price A.C., Kaiser A., Agnew D.M., Ichord R.N., and Traystman R.J. Neuronal death in newborn striatum after hypoxia-ischemia is necrosis and evolves with oxidative stress. Neurobiol Dis 7 (2000) 169-191
21. Martin L.J., Liu Z., Chen K., Price A.C., Pan Y., Swaby J.A., and Golden W.C. Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanisms of mitochondriopathy and cell death. J Comp Neurol 500 (2007) 20-46
22. Nakajima W., Ishida A., Lange M.S., Gabrielson K.L., Wilson M.A., Martin L.J., Blue M.E., and Johnston M.V. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci 20 (2000) 7994-8004
23. Nicotera P., Leist M., and Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett 102- 103 (1998) 139-142
24. Nicotera P., Leist M., and Ferrando-May E. Apoptosis and necrosis: different execution of the same death. Biochem Soc Symp 66 (1999) 69-73
25. Nicotera P., Leist M., and Manzo L. Neuronal cell death: a demise with different shapes. Trends Pharmacol Sci 20 (1999) 46-51
26. Nicotera P., and Lipton S.A. Excitotoxins in neuronal apoptosis and necrosis. J Cereb Blood Flow Metab 19 (1999) 583-591
27. Northington F.J., Ferriero D.M., Flock D.L., and Martin L.J. Delayed neurodegeneration in neonatal rat thalamus after hypoxia-ischemia is apoptosis. J Neurosci 21 (2001) 1931-1938
28. Northington F.J., Ferriero D.M., Graham E.M., Traystman R.J., and Martin L.J. Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis 8 (2001) 207-219
29. Northington F.J., Koehler R.C., Traystman R.J., and Martin L.J. Nitric oxide synthase 1 and nitric oxide synthase 3 protein expression is regionally and temporally regulated in fetal brain. Dev Brain Res 95 (1996) 1-14
30. Peeters-Scholte C., van den Tweel E., Groenendaal F., and van Bel F. Redox state of near infrared spectroscopy-measured cytochrome aa(3) correlates with delayed cerebral energy failure following perinatal hypoxia-ischaemia in the newborn pig. Exp Brain Res 156 (2004) 20-26
31. Poon S., Easterbrook-Smith S.B., Rybchyn M.S., Carver J.A., and Wilson M.R. Clusterin is an ATP-independent chaperone with very broad substrate specificity that stabilizes stressed proteins in a folding-competent state. Biochemistry 39 (2000) 15953-15960
32. Portera-Cailliau C., Price D.L., and Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 378 (1997) 70-87
33. Portera-Cailliau C., Price D.L., and Martin L.J. Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J Comp Neurol 378 (1997) 88-104
34. Rice J.E., Vannucci R.C., and Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 9 (1981) 131-141
35. Sheldon R.A., Hall J.J., Noble L.J., and Ferriero D.M. Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neurosci Lett 304 (2001) 165-168
36. Shimohama S., Fujimoto S., Sumida Y., and Tanino H. Differential expression of rat brain bcl-2 family proteins in development and aging. Biochem Biophys Res Commun 252 (1998) 92-96
37. Towfighi J., Zec N., Yager J., Housman C., and Vannucci R.C. Temporal evolution of neuropathologic changes in an immature rat model of cerebral hypoxia: a light microscopic study. Acta Neuropathol 90 (1995) 375-386
38. Vallee R.B., and Bloom G.S. Mechanisms of fast and slow axonal transport. Annu Rev Neurosci 14 (1991) 59-92
39. Wilson M.R., and Easterbrook-Smith S.B. Clusterin is a secreted mammalian chaperone. Trends Biochem Sci 25 (2000) 95-98
40. Wong-Riley M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12 (1989) 94-101
41. Zamzami N., Susin S.A., Marchetti P., Hirsch T., Gomez-Monterrey I., Castedo M., and Kroemer G. Mitochondrial control of nuclear apoptosis. J Exp Med 183 (1996) 1533-1544
42. Zhu C., Wang X., Huang Z., Qiu L., Xu F., Vahsen N., Nilsson M., Eriksson P.S., Hagberg H., Culmsee C., Plesnila N., Kroemer G., and Blomgren K. Apoptosis-inducing factor is a major contributor to neuronal loss induced by neonatal cerebral hypoxia-ischemia. Cell Death Differ 14 (2007) 775-784
43. Zhu C., Wang X., Xu F., Bahr B.A., Shibata M., Uchiyama Y., Hagberg H., and Blomgren K. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 12 (2005) 162-176