Home LiteratureArticle Details
PMID: 9050895 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage.

Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, Huang Z, Shimizu-Sasamata M, Yuan J, Moskowitz MA

Abstract

The interleukin 1beta converting enzyme (ICE) family plays a pivotal role in programmed cell death and has been implicated in stroke and neurodegenerative diseases. During reperfusion after filamentous middle cerebral artery occlusion, ICE-like cleavage products and tissue immunoreactive interleukin 1beta (IL-1beta) levels increased in ischemic mouse brain. Ischemic injury decreased after intracerebroventricular injections of ICE-like protease inhibitors, N-benzyloxycarbonyl-Val-Ala-Asp-fluoromethylketone (z-VAD.FMK), acetyl-Tyr-Val-Ala-Asp-chloromethylketone, or a relatively selective inhibitor of CPP32-like caspases, N-benzyloxycarbonyl-Asp-Glu-Val-Asp-fluoromethylketone, but not a cathepsin B inhibitor, N-benzyloxycarbonyl-Phe-Ala-fluoromethylketone. z-VAD.FMK decreased ICE-like cleavage products and tissue immunoreactive IL-1beta levels in ischemic mouse brain and reduced tissue damage when administered to rats as well. Only z-VAD.FMK and acetyl-Tyr-Val-Ala-Asp-chloromethylketone reduced brain swelling, and N-benzyloxycarbonyl-Asp-Glu-Val-Asp-fluoromethylketone did not attenuate the ischemia-induced increase in tissue IL-1beta levels. The three cysteine protease inhibitors significantly improved behavioral deficits, thereby showing that functional recovery of ischemic neuronal tissue can follow blockade of enzymes associated with apoptotic cell death. Finally, we examined the effect of z-VAD.FMK on excitotoxicity and found that it protected against alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate-induced or to a lesser extent N-methyl-D-aspartate-induced excitotoxic brain damage. Thus, ICE-like and CPP32-like caspases contribute to mechanisms of cell death in ischemic and excitotoxic brain injury and provide therapeutic targets for stroke and neurodegenerative brain damage.

MeSH Terms
Animals Blotting, Western Brain/drug effects,metabolism Brain Ischemia/drug therapy,enzymology Caspase 1 Caspase 3 Caspases Cathepsin B/antagonists & inhibitors Cerebrovascular Disorders/drug therapy Cysteine Endopeptidases/metabolism Cysteine Proteinase Inhibitors/pharmacology Gene Expression/genetics Interleukin-1/metabolism Male Mice Neurons/drug effects,metabolism Neurotoxins/pharmacology Rats Rats, Sprague-Dawley Receptors, Glutamate/metabolism Reperfusion
Chemicals
Cysteine Proteinase Inhibitors Interleukin-1 Neurotoxins Receptors, Glutamate Casp3 protein, mouse Casp3 protein, rat Caspase 3 Caspases Cysteine Endopeptidases Cathepsin B Caspase 1
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Hara H
Department of Surgery and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown 02129, USA.
Friedlander R M
Gagliardini V
Ayata C
Fink K
Huang Z
Shimizu-Sasamata M
Yuan J
Moskowitz M A
References (50)
50 references, click to expand
  1. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme.
    Cell. 1993 Nov 19;75(4):641-52 PMID: 8242740
  2. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat.
    J Cereb Blood Flow Metab. 1995 May;15(3):389-97 PMID: 7713996
  3. ICE-LAP6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B.
    J Biol Chem. 1996 Jul 12;271(28):16720-4 PMID: 8663294
  4. Attenuation of p53 expression protects against focal ischemic damage in transgenic mice.
    J Cereb Blood Flow Metab. 1994 Nov;14(6):887-91 PMID: 7929653
  5. Functional role of interleukin 1 beta (IL-1 beta) in IL-1 beta-converting enzyme-mediated apoptosis.
    J Exp Med. 1996 Aug 1;184(2):717-24 PMID: 8760825
  6. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase.
    Science. 1994 Sep 23;265(5180):1883-5 PMID: 7522345
  7. Mch3, a novel human apoptotic cysteine protease highly related to CPP32.
    Cancer Res. 1995 Dec 15;55(24):6045-52 PMID: 8521391
  8. Prevention of vertebrate neuronal death by the crmA gene.
    Science. 1994 Feb 11;263(5148):826-8 PMID: 8303301
  9. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes.
    Nature. 1992 Apr 30;356(6372):768-74 PMID: 1574116
  10. Identification and characterization of Ich-3, a member of the interleukin-1beta converting enzyme (ICE)/Ced-3 family and an upstream regulator of ICE.
    J Biol Chem. 1996 Aug 23;271(34):20580-7 PMID: 8702803
  11. A novel human protease similar to the interleukin-1 beta converting enzyme induces apoptosis in transfected cells.
    EMBO J. 1995 May 1;14(9):1914-22 PMID: 7743998
  12. ICE-LAP3, a novel mammalian homologue of the Caenorhabditis elegans cell death protein Ced-3 is activated during Fas- and tumor necrosis factor-induced apoptosis.
    J Biol Chem. 1996 Jan 19;271(3):1621-5 PMID: 8576161
  13. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis.
    Nature. 1995 Jul 6;376(6535):37-43 PMID: 7596430
  14. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia.
    Neuron. 1994 Oct;13(4):1017-30 PMID: 7946326
  15. The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death.
    Dev Biol. 1990 Mar;138(1):33-41 PMID: 2307287
  16. Excitotoxic cell death.
    J Neurobiol. 1992 Nov;23(9):1261-76 PMID: 1361523
  17. Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat.
    Brain Res Bull. 1992 Aug;29(2):243-6 PMID: 1388088
  18. Both apoptosis and necrosis occur following intrastriatal administration of excitotoxins.
    Acta Neuropathol. 1995;90(5):504-10 PMID: 8560984
  19. Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1 beta-converting enzyme.
    Genes Dev. 1994 Jul 15;8(14):1613-26 PMID: 7958843
  20. Interleukin-1 beta mRNA expression in ischemic rat cortex.
    Stroke. 1993 Nov;24(11):1746-50; discussion 1750-1 PMID: 8236352
  21. Human ICE/CED-3 protease nomenclature.
    Cell. 1996 Oct 18;87(2):171 PMID: 8861900
  22. Neuronal apoptosis: current understanding of molecular mechanisms and potential role in ischemic brain injury.
    J Neurotrauma. 1995 Oct;12(5):843-52 PMID: 8594212
  23. A cleavage-site-directed inhibitor of interleukin-1 beta-converting enzyme-like proteases inhibits apoptosis in primary cultures of rat hepatocytes.
    Biochem J. 1996 Feb 15;314 ( Pt 1):27-32 PMID: 8660294
  24. Induction of interleukin-1 beta mRNA after focal cerebral ischaemia in the rat.
    Brain Res Mol Brain Res. 1994 Apr;23(1-2):126-34 PMID: 8028476
  25. Involvement of cytokines in acute neurodegeneration in the CNS.
    Neurosci Biobehav Rev. 1993 Summer;17(2):217-27 PMID: 8515904
  26. In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7464-9 PMID: 8755496
  27. Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion.
    J Cereb Blood Flow Metab. 1996 Jul;16(4):605-11 PMID: 8964799
  28. Increased expression of IL-1beta converting enzyme in hippocampus after ischemia: selective localization in microglia.
    J Neurosci. 1996 Jul 1;16(13):4146-54 PMID: 8753876
  29. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product.
    J Biol Chem. 1995 Feb 17;270(7):3255-60 PMID: 7531702
  30. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination.
    Stroke. 1986 May-Jun;17(3):472-6 PMID: 3715945
  31. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death--inducing signaling complex.
    Cell. 1996 Jun 14;85(6):817-27 PMID: 8681377
  32. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death.
    Cell. 1996 Jun 14;85(6):803-15 PMID: 8681376
  33. Prevention of apoptosis in CNTF-dependent neurons by a mutant ICE and by viral protein CrmA but not by proto-oncogene product Bcl-2.
    Cell Death Differ. 1996 Jan;3(1):105-12 PMID: 17180061
  34. Identification and characterization of CPP32/Mch2 homolog 1, a novel cysteine protease similar to CPP32.
    J Biol Chem. 1996 Jan 26;271(4):1825-8 PMID: 8567622
  35. Molecular cloning and pro-apoptotic activity of ICErelII and ICErelIII, members of the ICE/CED-3 family of cysteine proteases.
    J Biol Chem. 1995 Jun 30;270(26):15870-6 PMID: 7797592
  36. Mechanisms and functions of cell death.
    Annu Rev Cell Biol. 1991;7:663-98 PMID: 1809356
  37. Inactivation of interleukin-1 beta converting enzyme by peptide (acyloxy)methyl ketones.
    Biochemistry. 1994 Apr 5;33(13):3934-40 PMID: 8142397
  38. Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro.
    Neuron. 1995 Aug;15(2):385-93 PMID: 7646891
  39. 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. 1995 Aug 1;92(16):7162-6 PMID: 7638161
  40. Different interleukin-1 beta converting enzyme (ICE) family protease requirements for the apoptotic death of T lymphocytes triggered by diverse stimuli.
    J Exp Med. 1996 Dec 1;184(6):2445-50 PMID: 8976202
  41. Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death.
    Cell. 1994 Sep 9;78(5):739-50 PMID: 8087842
  42. Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats.
    Stroke. 1995 Apr;26(4):676-80; discussion 681 PMID: 7709417
  43. Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.FMK) inhibits apoptosis by blocking the processing of CPP32.
    Biochem J. 1996 Apr 1;315 ( Pt 1):21-4 PMID: 8670109
  44. Mch2, a new member of the apoptotic Ced-3/Ice cysteine protease gene family.
    Cancer Res. 1995 Jul 1;55(13):2737-42 PMID: 7796396
  45. An ICE inhibitor, z-VAD-DCB attenuates ischaemic brain damage in the rat.
    Neuroreport. 1996 Jun 17;7(9):1465-8 PMID: 8856699
  46. Induction of interleukin-1 beta mRNA in rat brain after transient forebrain ischemia.
    J Neurochem. 1992 Jan;58(1):390-2 PMID: 1727445
  47. Apoptosis and necrosis after reversible focal ischemia: an in situ DNA fragmentation analysis.
    J Cereb Blood Flow Metab. 1996 Mar;16(2):186-94 PMID: 8594049
  48. Identification and characterization of ICH-2, a novel member of the interleukin-1 beta-converting enzyme family of cysteine proteases.
    J Biol Chem. 1995 Jun 23;270(25):15250-6 PMID: 7797510
  49. Edema, cation content, and ATPase activity after middle cerebral artery occlusion in rats.
    Stroke. 1992 Sep;23(9):1331-6 PMID: 1325690
  50. A semiautomated method for measuring brain infarct volume.
    J Cereb Blood Flow Metab. 1990 Mar;10(2):290-3 PMID: 1689322
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-03-04
Pages
2007-12
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC20033
Subset
IM
Grants
NINDS NIH HHS · F32 NS010828 · United States
NINDS NIH HHS · P01 NS010828 · United States
NINDS NIH HHS · P50 NS010828 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com