Targeting neonatal ischemic brain injury with a pentapeptide-based irreversible caspase inhibitor

Cell Death and Disease

Volumn 2, Issue 9, 2011, Pages

  Chauvier, D ^a,b   Renolleau, S ^c,d,e   Holifanjaniaina, S ^f,g   Ankri, S ^a,b   Bezault, M ^a,b   Schwendimann, L ^f,g   Rousset, C ^h,i   Casimir, R ^a,b,j   Hoebeke, J ^j   Smirnova, M ^a,b   Debret, G ^d,k   Trichet, A P ^b   Carlsson, Y ^i,l   Wang, X ⁱ   Bernard, E ^b   He Bert M ^b   Rauzier, J M ^m,n   Matecki, S ^o,p   Lacampagne, A ^n,p   Rustin, P ^f,g   Mariani, J ^c,d,q   Hagberg, H ^h,i,l   Gressens, P ^f,g,h   Charriaut Marlangue, C ^c,d   Jacotot, E ^a,b,f,g,h   more..

^a INSTITUT PASTEUR   (France)

^b Theraptosis SA   (France)

^c CNRS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e ARMAND TROUSSEAU HOSPITAL   (France)

^f HÔPITAL ROBERT DEBRÉ   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h HAMMERSMITH HOSPITAL   (United Kingdom)

ⁱ UNIVERSITY OF GOTHENBURG   (Sweden)

^j INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^k UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^l SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^m NÎMES UNIVERSITY HOSPITAL   (France)

ⁿ UNIVERSITY OF MONTPELLIER   (France)

^o MONTPELLIER UNIVERSITY HOSPITAL   (France)

^p UNIV MONTPELLIER   (France)

^q HÔPITAL CHARLES FOIX   (France)

more..

Author keywords

Caspase inhibitor; Ischemia; Neuroprotection; Perinatal brain damage

Indexed keywords

CASPASE INHIBITOR; CYTOCHROME C; PENTAPEPTIDE; TRP 601; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EXCITOTOXICITY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; STROKE;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BINDING SITES; CASPASES; CYSTEINE PROTEINASE INHIBITORS; CYTOCHROMES C; DISEASE MODELS, ANIMAL; HYPOXIA-ISCHEMIA, BRAIN; ISCHEMIA; MICE; NEUROPROTECTIVE AGENTS; OLIGOPEPTIDES; QUINOLINES; RATS;

RODENTIA;

EID: 80053425629     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.87     Document Type: Article

References (49)

1. Lawn JE, Lee AC, Kinney M, Sibley L, Carlo WA, Paul VK et al. Two million intrapartumrelated stillbirths and neonatal deaths: where, why, and what can be done? Int J Gynaecol Obstet 2009; 107: S5.
2. du Plessis AJ, Volpe JJ. Perinatal brain injury in the preterm and term newborn. Curr Opin Neurol 2002; 15: 151-157. (Pubitemid 34286899)
3. Ferriero DM. Neonatal brain injury. N Engl J Med 2004; 351: 1985-1995.
4. Lawn JE, Bahl R, Bergstrom S, Bhutta ZA, Darmstadt GL, Ellis M et al. Setting research priorities to reduce almost one million deaths from birth asphyxia by 2015. PLoS Med 2011; 8: e1000389.
5. Azzopardi DV, Strohm B, Edwards AD, Dyet L, Halliday HL, Juszczak E et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med 2009; 361: 1349-1358.
6. Gonzalez FF, Ferriero DM. Neuroprotection in the newborn infant. Clin Perinatol 2009; 36: 859-880.
7. Northington FJ, Zelaya ME, O'Riordan DP, Blomgren K, Flock DL, Hagberg H et al. 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 2007; 149: 822-833. (Pubitemid 350130287)
8. Kaindl AM, Favrais G, Gressens P. Molecular mechanisms involved in injury to the preterm brain. J Child Neurol 2009; 24: 1112-1118.
9. Gill R, Soriano M, Blomgren K, Hagberg H, Wybrecht R, Miss MT et al. Role of caspase-3 activation in cerebral ischemia-induced neurodegeneration in adult and neonatal brain. J Cereb Blood Flow Metab 2002; 22: 420-430. (Pubitemid 34273598)
10. Renolleau S, Fau S, Goyenvalle C, Joly LM, Chauvier D, Jacotot E et al. Specific caspase inhibitor Q-VD-OPh prevents neonatal stroke in P7 rat: a role for gender. J Neurochem 2007; 100: 1062-1071. (Pubitemid 46213929)
11. Wang X, Carlsson Y, Basso E, Zhu C, Rousset CI, Rasola A et al. Developmental shift of cyclophilin D contribution to hypoxic-ischemic brain injury. J Neurosci 2009; 29: 2588-2596.
12. Edwards AD, Yue X, Cox P, Hope PL, Azzopardi DV, Squier MV et al. Apoptosis in the brains of infants suffering intrauterine cerebral injury. Pediatr Res 1997; 42: 684-689. (Pubitemid 27459479)
13. Hagberg H, Mallard C, Rousset CI, Wang X. Apoptotic mechanisms in the immature brain: involvement of mitochondria. J Child Neurol 2009; 24: 1141-1146.
14. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y et al. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2005; 12: 162-176. (Pubitemid 40220647)
15. Wang X, Han W, Du X, Zhu C, Carlsson Y, Mallard C et al. Neuroprotective effect of Bax-inhibiting peptide on neonatal brain injury. Stroke 2010; 41: 2050-2055.
16. Zhu C, Wang X, Huang Z, Qiu L, Xu F, Vahsen N et al. Apoptosis-inducing factor is a major contributor to neuronal loss induced by neonatal cerebral hypoxia-ischemia. Cell Death Differ 2007; 14: 775-784. (Pubitemid 46444515)
17. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998; 281: 1312-1316. (Pubitemid 28406817)
18. Talanian RV, Brady KD, Cryns VL. Caspases as targets for anti-inflammatory and anti-apoptotic drug discovery. J Med Chem 2000; 43: 3351-3371.
19. Yuan J, Yankner BA. Apoptosis in the nervous system. Nature 2000; 407: 802-809.
20. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D et al. Substrate specificities of caspase family proteases. J Biol Chem 1997; 272: 9677-9682. (Pubitemid 27171628)
21. Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, Thornberry NA et al. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 1998; 273: 32608-32613. (Pubitemid 28557641)
22. Garcia-Calvo M, Peterson EP, Rasper DM, Vaillancourt JP, Zamboni R, Nicholson DW et al. Purification and catalytic properties of human caspase family members. Cell Death Differ 1999; 6: 362-369. (Pubitemid 29186880)
23. Cheng Y, Deshmukh M, D'Costa A, Demaro JA, Gidday JM, Shah A et al. Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury. J Clin Invest 1998; 101: 1992-1999. (Pubitemid 28226119)
24. Han BH, Xu D, Choi J, Han Y, Xanthoudakis S, Roy S et al. Selective, reversible caspase-3 inhibitor is neuroprotective and reveals distinct pathways of cell death after neonatal hypoxic-ischemic brain injury. J Biol Chem 2002; 277: 30128-30136.
25. Joly LM, Mucignat V, Mariani J, Plotkine M, Charriaut-Marlangue C. Caspase inhibition after neonatal ischemia in the rat brain. J Cereb Blood Flow Metab 2004; 24: 124-131. (Pubitemid 38021276)
26. Puyal J, Vaslin A, Mottier V, Clarke PG. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 2009; 66: 378-389.
27. Karatas H, Aktas Y, Gursoy-Ozdemir Y, Bodur E, Yemisci M, Caban S et al. A nanomedicine transports a peptide caspase-3 inhibitor across the blood-brain barrier and provide1neuroprotection. J Neurosci 2009; 29: 13761-13769.
28. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 1996; 384: 368-372. (Pubitemid 26408520)
29. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 1998; 94: 325-337. (Pubitemid 28376077)
30. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A et al. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 1998; 12: 1304-1314. (Pubitemid 28213406)
31. West T, Atzeva M, Holtzman DM. Caspase-3 deficiency during development increases vulnerability to hypoxic-ischemic injury through caspase-3-independent pathways. Neurobiol Dis 2006; 22: 523-537. (Pubitemid 43832124)
32. Carlsson Y, Schwendimann L, Vontell R, Rousset CI, Wang X, Lebon S et al. Genetic inhibition of caspase-2 reduces hypoxic-ischemic and excitotoxic neonatal brain injury. Ann Neurol 2011; e-pub ahead of print 28 March 2011; doi:10.1002/ana.22431.
33. Chauvier D, Ankri S, Charriaut-Marlangue C, Casimir R, Jacotot E. Broad-spectrum caspase inhibitors: from myth to reality? Cell Death Differ 2007; 14: 387-391. (Pubitemid 46092244)
34. Zhu C, Qiu L, Wang X, Hallin U, Candé C, Kroemer G et al. Involvement of apoptosisinducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain. J Neurochem 2003; 86: 306-317. (Pubitemid 36842430)
35. Linton SD, Aja T, Armstrong RA, Bai X, Chen LS, Chen N et al. First-in-class pan caspase inhibitor developed for the treatment of liver disease. J Med Chem 2005; 48: 6779-6782. (Pubitemid 41533098)
36. Leung-Toung R, Zhao Y, Li W, Tam TF, Karimian K, Spino M et al. Thiol proteases: inhibitors and potential therapeutic targets. Curr Med Chem 2006; 13: 547-581.
37. McStay GP, Salvesen GS, Green DR. Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ 2008; 15: 322-331.
38. Schweizer A, Briand C, Grutter MG. Crystal structure of caspase-2, apical initiator of the intrinsic apoptotic pathway. J Biol Chem 2003; 278: 42441-42447. (Pubitemid 37310516)
39. Chauvier D, Lecoeur H, Langonné A, Borgne-Sanchez A, Mariani J, Martinou JC et al. Upstream control of apoptosis by caspase-2 in serum-deprived primary neurons. Apoptosis 2005; 10: 1243-1259. (Pubitemid 43117673)
40. Dzietko M, Boos V, Sifringer M, Polley O, Gerstner B, Genz K et al. A critical role for Fas/CD-95 dependent signaling pathways in the pathogenesis of hyperoxia-induced brain injury. Ann Neurol 2008; 64: 664-673.
41. Renolleau S, Aggoun-Zouaoui D, Ben-Ari Y, Charriaut-Marlangue C. A model of transient unilateral focal ischemia with reperfusion in the P7 neonatal rat: morphological changes indicative of apoptosis. Stroke 1998; 29: 1454-1461. (Pubitemid 28300086)
42. Villapol S, Bonnin P, Fau S, Baud O, Renolleau S, Charriault-Marlangue C. Unilateral blood flow decrease induces bilateral and symmetric responses in the immature brain. Am J Pathol 2009; 175: 2111-2120.
43. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES. Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 2002; 277: 13430-13437. (Pubitemid 34967937)
44. Robertson JD, Enoksson M, Suomela M, Zhivotovsky B, Orrenius S. Caspase-2 acts upstream of mitochondria to promote cytochrome c release during etoposide-induced apoptosis. J Biol Chem 2002; 277: 29803-29809.
45. AndinéP, Thordstein M, Kjellmer I, Nordborg C, Thiringer K, Wennberg E et al. Evaluation of brain damage in a rat model of neonatal hypoxic-ischemia. J Neurosci Methods 1990; 35: 253-260.
46. Hunter AJ, Green AR, Cross AJ. Animal models of acute ischaemic stroke: can they predict clinically successful neuroprotective drugs? Trends Pharmacol Sci 1995; 16: 123-128.
47. Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A et al. Caspase signalling controls microglia activation and neurotoxicity. Nature 2011; 472: 319-324.
48. Gonzalez FF, Ferriero DM. Therapeutics for neonatal brain injury. Pharmacol Ther 2008; 120: 43-53.
49. Wu JC, Fritz LC. Irreversible caspase inhibitors: tools for studying apoptosis. Methods 1999; 17: 320-328. (Pubitemid 29440607)