Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury

Journal of Clinical Investigation

Volumn 101, Issue 9, 1998, Pages 1992-1999

  Cheng, Yu ^a   Deshmukh, Mohanish ^a   D'Costa, Anselm ^a   Demaro, Joseph A ^a   Gidday, Jeffrey M ^a   Shah, Aarti ^a   Sun, Yuling ^a   Jacquin, Mark F ^a   Johnson Jr , Eugene M ^a   Holtzman, David M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Caspase; Cell death; Cerebral palsy; Hypoxia; Ischemia

Indexed keywords

ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN PROTECTION; CEREBRAL PALSY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0032080673     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI2169     Document Type: Article

References (48)

1. Oppenheim, R.W. 1991. Cell death during the development of the nervous system. Annu. Rev. Neurosci. 14:453-501.
2. Raff, M.C., B.A. Barres, J.F. Burne, H.S. Coles, Y. Ishizaki, and M.D. Jacobson. 1993. Programmed cell death and the control of cell survival: lessons from the nervous system. Science. 262:695-700.
3. Wyllie, A.H., J.F. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306.
4. Schwartzman, R.A., and J.A. Cidlowski. 1993. Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr. Rev. 14:133-151.
5. Sloviter, R.S., E. Dean, and S. Neubort. 1993. Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system. J. Comp. Neurol. 33:337-351.
6. Rink, A., K.M. Fung, J.Q. Trojanowski, V.M. Lee, E. Neugebauer, and T.K. McIntosh. 1995. Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am. J. Pathol. 147:1575-1583.
7. Goto, K., A. Ishige, K. Sekiguchi, S. Iizuka, A. Sugimoto, M. Yuzurihara, M. Aburada, E. Hosoya, and K. Kogure. 1990. Effects of cycloheximide on delayed neuronal death in rat hippocampus. Brain Res. 534:299-302.
8. Tominaga, T., S. Kure, K. Narisawa, and T. Yoshimoto. 1993. Endonuclease activation following focal cerebral ischemic injury in the rat brain. Brain Res. 608:21-26.
9. Nitatori, T., N. Sato, S. Waguri, Y. Karasawa, H. Araki, K. Shibanai, E. Kominami, and Y. Uchiyama. 1995. Delayed neuronal death in the CA1 pyramidal layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15:1001-1011.
10. Brown, A.W., and J.B. Brierley. 1972. Anoxic-ischeamic cell change in rat brain: light microscopic and fine-structural observations. J. Neurol. Sci. 16: 59-84.
11. Deshpande, J., K. Bergstedt, T. Linden, H. Kalimo, and T. Wieloch. 1992. Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: evidence against programmed cell death. Exp. Brain Res. 88:91-105.
12. Rothman, S.M., and J.W. Olney. 1986. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19:105-111.
13. Ferrer, I., A. Tortosa, A. Macaya, A. Sierra, D. Moreno, F. Munell, R. Bianco, and W. Squier. 1994. Evidence of nuclear DNA fragmentation following hypoxia-ischemia in the infant rat brain, and transient forebrain ischemia in the adult gerbil. Brain Path. 4:115-122.
14. Hill, I.E., J.P. MacManus, I. Rasquinha, and U.I. Tuor. 1995. DNA fragmentation indicative of apoptosis following unilateral cerebral hypoxia-ischemia in the neonatal rat. Brain Res. 676:398-403.
15. Sidhu, S., U.I. Tuor, and M.R. Del Bigio. 1997. Nuclear condensation and fragmentation following cerebral hypoxia-ischemia occurs more frequently in immaturre than older rats. Neurosci. Lett. 223:129-132.
16. Portera-Cailliau, C., D.L. Price, and L.J. Martin. 1997. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J. Comp. Neurol. 378:70-87.
17. Deckwerth, T.L., and E.M. Johnson, Jr. 1993. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell. Biol. 123:1207-1222.
18. Kumar, S., and M.F. Lavin. 1996. The ICE family of cysteine proteases as effectors of cell death. Cell Death Differ. 3:255-267.
19. Schwartz, L.M., and C.E. Milligan. 1996. Cold thoughts of death: the role of ICE proteases in neuronal death. Trends Neurosci. 19:555-562.
20. Deshmukh, M., and E.M.J. Johnson. 1997. Programmed cell death in neurons: focus on the pathway of nerve growth factor deprivation-induced death of sympathetic neurons. Mol. Pharmacol. 51:897-906.
21. Holtzman, D.M., and M. Deshmukh. 1997. Caspases: a treatment target for neurodegenerative diseases? Nature Med. 3:954-955.
22. Deshmukh, M., J. Vasilakos, T.L. Deckwerth, P.A. Lampe, B.D. Shivers, and E.M. Johnson, Jr. 1996. Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE family proteases. J. Cell Biol. 135:1341-1345.
23. Troy, C.M., L. Stefanis, A. Prochiantz, L.A. Greene, and M.L. Shelanski. 1996. The contrasting roles of ICE family proteases and interleukin-1β in apoptosis induced by trophic factor withdrawal and by copper/zinc superoxide dismutase down-regulation. Proc. Natl. Acad. Sci. USA. 93:5635-5640.
24. Volpe, J.J. 1993. Neurology of the Newborn. W.B. Saunders, Philadelphia, PA. 876 pp.
25. Vanucci, R.C. 1990. Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage. Pediatr. Res. 27:317-326.
26. Rice, J.E., R.C. Vannucci, and J.B. Brierley. 1981. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9:131-141.
27. Johnston, M.V. 1983. Neurotransmitter alterations in a model of perinatal hypoxic-ischemic brain injury. Ann. Neurol. 13:511-518.
28. Silverstein, F., and M.V. Johnson. 1984. Effects of hypoxia-ischemia on monoamine metabolism in the immature brain. Ann. Neurol. 15:342-347.
29. Ferriero, D.M., L.J. Arcavi, S.M. Sagar, T.K. McIntosh, and R.P. Simon. 1988. Selective sparing of NADPH-diaphorase neurons in neonatal hypoxia-ischemia. Ann. Neurol. 24:670-676.
30. Cheng, Y., J.M. Gidday, Q. Yan, A.R. Shah, and D.M. Holtzman. 1997. Marked age-dependent neuroprotection by BDNF against neonatal hypoxic-ischemic brain injury. Ann. Neurol. 41:521-529.
31. Palmer, C., and R.C. Vanucci. 1993. Potential new therapies for perinatal cerebral hypoxia-ischemia. Clin. Perinatol. 20:411-432.
32. Gidday, J.M., J.C. Fitzgibbons, A.R. Shah, and T.S. Park. 1994. Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci. Lett. 168:221-224.
33. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
34. Golden, J.P., J.Z. Rana, J. Davis, D.S. Zahm, and M.F. Jacquin. 1993. Organization of the proximal, orbital segment of the infraorbital nerve at multiple intervals after axotomy at birth: a quantitative electron microscopic study in rat. J. Comp. Neurol. 338:159-174.
35. Mobley, W.C., J.L. Rutkowski, G.I. Tennekoon, J. Gemski, K. Buchanan, and M.V. Johnston. 1986. Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Mol. Brain Res. 387: 53-62.
36. Holtzman, D.M., R.A. Sheldon, W. Jaffe, Y. Cheng, and D.F. Ferriero. 1996. NGF protects the neonatal brain against hypoxic-ischemic injury. Ann. Neurol. 39:114-122.
37. Paxinos, G., and C. Watson. 1986. The Rat Brain in Stereotaxic Coordinates. Academic Press, Australia. 237 pp.
38. Holtzman, D.M., R.M. Bayney, Y. Li, H. Khosrovi, C.N. Berger, C.J. Epstein, and W.C. Mobley. 1992. Dysregulation of gene expression in mouse trisomy 16, an animal model of Down syndrome. EMBO (Eur. Mol. Biol. Organ.) J. 11:619-627.
39. Armstrong, R.C., T. Aja, K.D. Hoang, S. Gaur, X. Bai, E.S. Alnemri, G. Litwack, D.S. Karanewsky, L.C. Fritz, and K.J. Tomaselli. 1997. Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J. Neurosci. 17:553-562.
40. Ferriero, D.M., D.M. Holtzman, S.M. Black, and R.A. Sheldon. 1996. Mice without neuronal nitric oxide synthase have less injury after perinatal hypoxia-ischemia. Neurobiol. Dis. 3:64-71.
41. Wijsman, J.H., R.R. Jonker, R. Keijser, C.J. van de Velde, C.J. Cornelisse, and J.H. van Dierendonck. 1993. A new method to detect apoptosis in paraffin sections: in situ end-labeling of fragmented DNA. J. Histochem. Cytochem. 41:7-12.
42. Collins, R.J., B.V. Harmon, G.C. Gobe, and J.F.R. Kerr. 1992. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int. J. Radiat. Biol. 61:451-453.
43. Ellis, R.E., J. Yuan, and H.R. Horvitz. 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7:663-698.
44. Ni, B., X. Wu, Y. Du, Y. Su, E. Hamilton-Byrd, P.K. Rockey, P.J. Rosteck, G.G. Poirer, and S.M. Paul. 1997. Cloning and expression of a rat brain interleukin-1beta-converting enzyme (ICE)-related protein (IRP) and its possible role in apoptosis of cultured cerebellar granule neurons. J. Neurosci. 17: 1561-1569.
45. Loddick, S.A., A. MacKenzie, and N.J. Rothwell. 1996. An ICE inhibitor, z-VAD-DCB attenuates ischaemic brain damage in the rat. Neuroreport. 7: 1465-1468.
46. Hara, H., R.M. Friedlander, V. Gagliardini, C. Ayata, K. Fink, Z. Huang, M. Shimizu-Sasamata, J. Yuan, and M. Moskowitz. 1997. Inhibition of interleukin 1β converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl. Acad. Sci. USA. 94:2007-2012.
47. Hagan, P., J.D. Barks, M. Yabut, B.L. Davidson, B. Roessler, and F.S. Silverstein. 1996. Adenovirus-mediated over-expression of interleukin-1 receptor antagonist reduces susceptibility to excitotoxic brain injury in perinatal rats. Neurosciences. 75:1033-1045.
48. Silverstein, F.S., J.D. Barks, P. Hagan, X.H. Liu, J. Ivacko, and J. Szaflarski. 1997. Cytokines and perinatal brain injury. Neurochem. Int. 30:375-383.