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Current Neuropharmacology

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ISSN (Online): 1875-6190

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General Review Article

Inhibition of Caspase 3 and Caspase 9 Mediated Apoptosis: A Multimodal Therapeutic Target in Traumatic Brain Injury

Author(s): Aziz Unnisa, Nigel H. Greig and Mohammad Amjad Kamal*

Volume 21, Issue 4, 2023

Published on: 19 October, 2022

Page: [1001 - 1012] Pages: 12

DOI: 10.2174/1570159X20666220327222921

Price: $65

Abstract

Traumatic brain injury (TBI) is one of the significant causes of death and morbidity, and it is hence a focus of translational research. Apoptosis plays an essential part in the pathophysiology of TBI, and its inhibition may help overcome TBI's negative consequences and improve functional recovery. Although physiological neuronal death is necessary for appropriate embryologic development and adult cell turnover, it can also drive neurodegeneration. Caspases are principal mediators of cell death due to apoptosis and are critical for the required cleavage of intracellular proteins of cells committed to die. Caspase-3 is the major executioner Caspase of apoptosis and is regulated by a range of cellular components during physiological and pathological conditions. Activation of Caspase-3 causes proteolyzation of DNA repair proteins, cytoskeletal proteins, and the inhibitor of Caspase-activated DNase (ICAD) during programmed cell death, resulting in morphological alterations and DNA damage that define apoptosis. Caspase-9 is an additional crucial part of the intrinsic pathway, activated in response to several stimuli. Caspases can be altered post-translationally or by modulatory elements interacting with the zymogenic or active form of a Caspase, preventing their activation. The necessity of Caspase-9 and -3 in diverse apoptotic situations suggests that mammalian cells have at least four distinct apoptotic pathways. Continued investigation of these processes is anticipated to disclose new Caspase regulatory mechanisms with consequences far beyond apoptotic cell death control. The present review discusses various Caspase-dependent apoptotic pathways and the treatment strategies to inhibit the Caspases potentially.

Keywords: Traumatic brain injury, apoptosis, Caspase-3, Caspase-9, Caspase-dependent apoptosis, Caspase inhibitors

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Graphical Abstract

[1]
Khellaf, A.; Khan, D.Z.; Helmy, A. Recent advances in traumatic brain injury. J. Neurol., 2019, 266(11), 2878-2889.
[http://dx.doi.org/10.1007/s00415-019-09541-4] [PMID: 31563989]
[2]
Maas, A.I.R.; Menon, D.K.; Adelson, P.D.; Andelic, N.; Bell, M.J.; Belli, A.; Bragge, P.; Brazinova, A.; Büki, A.; Chesnut, R.M.; Citerio, G.; Coburn, M.; Cooper, D.J.; Crowder, A.T.; Czeiter, E.; Czosnyka, M.; Diaz-Arrastia, R.; Dreier, J.P.; Duhaime, A.C.; Ercole, A.; van Essen, T.A.; Feigin, V.L.; Gao, G.; Giacino, J.; Gonzalez-Lara, L.E.; Gruen, R.L.; Gupta, D.; Hartings, J.A.; Hill, S.; Jiang, J.Y.; Ketharanathan, N.; Kompanje, E.J.O.; Lanyon, L.; Laureys, S.; Lecky, F.; Levin, H.; Lingsma, H.F.; Maegele, M.; Majdan, M.; Manley, G.; Marsteller, J.; Mascia, L.; McFadyen, C.; Mondello, S.; Newcombe, V.; Palotie, A.; Parizel, P.M.; Peul, W.; Piercy, J.; Polinder, S.; Puybasset, L.; Rasmussen, T.E.; Rossaint, R.; Smielewski, P.; Söderberg, J.; Stanworth, S.J.; Stein, M.B.; von Steinbüchel, N.; Stewart, W.; Steyerberg, E.W.; Stocchetti, N.; Synnot, A.; Te Ao, B.; Tenovuo, O.; Theadom, A.; Tibboel, D.; Videtta, W.; Wang, K.K.W.; Williams, W.H.; Wilson, L.; Yaffe, K. Traumatic brain injury: Integrated approaches to improve prevention, clinical care, and research. Lancet Neurol., 2017, 16(12), 987-1048.
[http://dx.doi.org/10.1016/S1474-4422(17)30371-X] [PMID: 29122524]
[3]
Glushakov, A.V.; Glushakova, O.Y.; Doré, S.; Carney, P.R.; Hayes, R.L. Animal models of posttraumatic seizures and epilepsy. Methods Mol. Biol., 2016, 1462, 481-519.
[http://dx.doi.org/10.1007/978-1-4939-3816-2_27] [PMID: 27604735]
[4]
Lucke-Wold, B.P.; Nguyen, L.; Turner, R.C.; Logsdon, A.F.; Chen, Y.W.; Smith, K.E.; Huber, J.D.; Matsumoto, R.; Rosen, C.L.; Tucker, E.S.; Richter, E. Traumatic brain injury and epilepsy: Underlying mechanisms leading to seizure. Seizure, 2015, 33, 13-23.
[http://dx.doi.org/10.1016/j.seizure.2015.10.002] [PMID: 26519659]
[5]
Daneshvar, D.H.; Goldstein, L.E.; Kiernan, P.T.; Stein, T.D.; McKee, A.C. Post-traumatic neurodegeneration and chronic traumatic encephalopathy. Mol Cell Neurosci, 2015, 66(Pt B), 81-90.
[http://dx.doi.org/10.1016/j.mcn.2015.03.007]
[6]
Taylor, K.M.; Saint-Hilaire, M.H.; Sudarsky, L.; Simon, D.K.; Hersh, B.; Sparrow, D.; Hu, H.; Weisskopf, M.G. Head injury at early ages is associated with risk of Parkinson’s disease. Parkinsonism Relat. Disord., 2016, 23, 57-61.
[http://dx.doi.org/10.1016/j.parkreldis.2015.12.005] [PMID: 26725141]
[7]
Mendez, M.F.; Paholpak, P.; Lin, A.; Zhang, J.Y.; Teng, E. Prevalence of traumatic brain injury in early versus late-onset Alzheimer’s disease. J. Alzheimers Dis., 2015, 47(4), 985-993.
[http://dx.doi.org/10.3233/JAD-143207] [PMID: 26401777]
[8]
Dams-O’Connor, K.; Guetta, G.; Hahn-Ketter, A.E.; Fedor, A. Traumatic brain injury as a risk factor for Alzheimer’s disease: Current knowledge and future directions. Neurodegener. Dis. Manag., 2016, 6(5), 417-429.
[http://dx.doi.org/10.2217/nmt-2016-0017] [PMID: 27599555]
[9]
LoBue, C.; Wadsworth, H.; Wilmoth, K.; Clem, M.; Hart, J., Jr; Womack, K.B.; Didehbani, N.; Lacritz, L.H.; Rossetti, H.C.; Cullum, C.M. Traumatic brain injury history is associated with earlier age of onset of Alzheimer disease. Clin. Neuropsychol., 2017, 31(1), 85-98.
[http://dx.doi.org/10.1080/13854046.2016.1257069] [PMID: 27855547]
[10]
Akamatsu, Y.; Hanafy, K.A. Cell death and recovery in traumatic brain injury. Neurotherapeutics, 2020, 17(2), 446-456.
[http://dx.doi.org/10.1007/s13311-020-00840-7] [PMID: 32056100]
[11]
Ng, S.Y.; Lee, A.Y.W. Traumatic brain injuries: Pathophysiology and potential therapeutic targets. Front. Cell. Neurosci., 2019, 13, 528.
[http://dx.doi.org/10.3389/fncel.2019.00528] [PMID: 31827423]
[12]
Härter, L.; Keel, M.; Hentze, H.; Leist, M.; Ertel, W. Caspase-3 activity is present in cerebrospinal fluid from patients with traumatic brain injury. J. Neuroimmunol., 2001, 121(1-2), 76-78.
[http://dx.doi.org/10.1016/S0165-5728(01)00409-X] [PMID: 11730942]
[13]
Darwish, R.S.; Amiridze, N.S. Detectable levels of cytochrome C and activated caspase-9 in cerebrospinal fluid after human traumatic brain injury. Neurocrit. Care, 2010, 12(3), 337-341.
[http://dx.doi.org/10.1007/s12028-009-9328-3] [PMID: 20087688]
[14]
Jiang, W.; Jin, P.; Wei, W.; Jiang, W. Apoptosis in cerebrospinal fluid as outcome predictors in severe traumatic brain injury: An observational study. Medicine (Baltimore), 2020, 99(26), e20922.
[http://dx.doi.org/10.1097/MD.0000000000020922] [PMID: 32590803]
[15]
Lorente, L.; Martín, M.M.; González-Rivero, A.F.; Argueso, M.; Ramos, L.; Solé-Violán, J.; Cáceres, J.J.; Jiménez, A.; Borreguero-León, J.M. Serum levels of caspase-cleaved cytokeratin-18 in patients with severe traumatic brain injury are associated with mortality: A pilot study. PLoS One, 2015, 10(3), e0121739.
[http://dx.doi.org/10.1371/journal.pone.0121739] [PMID: 25822281]
[16]
Brophy, G.M.; Pineda, J.A.; Papa, L.; Lewis, S.B.; Valadka, A.B.; Hannay, H.J.; Heaton, S.C.; Demery, J.A.; Liu, M.C.; Tepas, J.J., III; Gabrielli, A.; Robicsek, S.; Wang, K.K.; Robertson, C.S.; Hayes, R.L. alphaII-Spectrin breakdown product cerebrospinal fluid exposure metrics suggest differences in cellular injury mechanisms after severe traumatic brain injury. J. Neurotrauma, 2009, 26(4), 471-479.
[http://dx.doi.org/10.1089/neu.2008.0657] [PMID: 19206997]
[17]
Dash, P.K.; Zhao, J.; Hergenroeder, G.; Moore, A.N. Biomarkers for the diagnosis, prognosis, and evaluation of treatment efficacy for traumatic brain injury. Neurotherapeutics, 2010, 7(1), 100-114.
[http://dx.doi.org/10.1016/j.nurt.2009.10.019] [PMID: 20129502]
[18]
Yokobori, S.; Hosein, K.; Burks, S.; Sharma, I.; Gajavelli, S.; Bullock, R. Biomarkers for the clinical differential diagnosis in traumatic brain injury--a systematic review. CNS Neurosci. Ther., 2013, 19(8), 556-565.
[http://dx.doi.org/10.1111/cns.12127] [PMID: 23710877]
[19]
Wang, K.K. Calpain and caspase: Can you tell the difference? Trends Neurosci., 2000, 23(1), 20-26.
[http://dx.doi.org/10.1016/S0166-2236(99)01479-4] [PMID: 10631785]
[20]
Rohn, T.T.; Rissman, R.A.; Davis, M.C.; Kim, Y.E.; Cotman, C.W.; Head, E. Caspase-9 activation and caspase cleavage of tau in the Alzheimer’s disease brain. Neurobiol. Dis., 2002, 11(2), 341-354.
[http://dx.doi.org/10.1006/nbdi.2002.0549] [PMID: 12505426]
[21]
Kanaan, N.M.; Cox, K.; Alvarez, V.E.; Stein, T.D.; Poncil, S.; McKee, A.C. Characterization of early pathological tau conformations and phosphorylation in chronic traumatic encephalopathy. J. Neuropathol. Exp. Neurol., 2016, 75(1), 19-34.
[http://dx.doi.org/10.1093/jnen/nlv001] [PMID: 26671985]
[22]
Shahim, P.; Linemann, T.; Inekci, D.; Karsdal, M.A.; Blennow, K.; Tegner, Y.; Zetterberg, H.; Henriksen, K. Serum tau fragments predict return to play in concussed professional ice hockey players. J. Neurotrauma, 2016, 33(22), 1995-1999.
[http://dx.doi.org/10.1089/neu.2014.3741] [PMID: 25621407]
[23]
Henriksen, K.; Byrjalsen, I.; Christiansen, C.; Karsdal, M.A. Relationship between serum levels of tau fragments and clinical progression of Alzheimer’s disease. J. Alzheimers Dis., 2015, 43(4), 1331-1341.
[http://dx.doi.org/10.3233/JAD-140984] [PMID: 25171717]
[24]
Avrutsky, M.I.; Troy, C.M. Caspase-9: A multimodal therapeutic target with diverse cellular expression in human disease. Front. Pharmacol., 2021, 12, 701301.
[http://dx.doi.org/10.3389/fphar.2021.701301] [PMID: 34305609]
[25]
Logsdon, A.F.; Lucke-Wold, B.P.; Turner, R.C.; Huber, J.D.; Rosen, C.L.; Simpkins, J.W. Role of microvascular disruption in brain damage from traumatic brain injury. Compr. Physiol., 2015, 5(3), 1147-1160.
[http://dx.doi.org/10.1002/cphy.c140057] [PMID: 26140712]
[26]
Zhang, X.; Chen, J.; Graham, S.H.; Du, L.; Kochanek, P.M.; Draviam, R.; Guo, F.; Nathaniel, P.D.; Szabó, C.; Watkins, S.C.; Clark, R.S. 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., 2002, 82(1), 181-191.
[http://dx.doi.org/10.1046/j.1471-4159.2002.00975.x] [PMID: 12091479]
[27]
Molla, M.D.; Akalu, Y.; Geto, Z.; Dagnew, B.; Ayelign, B.; Shibabaw, T. Role of caspase-1 in the pathogenesis of inflammatory-associated chronic noncommunicable diseases. J. Inflamm. Res., 2020, 13, 749-764.
[http://dx.doi.org/10.2147/JIR.S277457] [PMID: 33116753]
[28]
Baptiste-Okoh, N.; Barsotti, A.M.; Prives, C. A role for caspase 2 and PIDD in the process of p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA, 2008, 105(6), 1937-1942.
[http://dx.doi.org/10.1073/pnas.0711800105] [PMID: 18238895]
[29]
Porter, A.G.; Jänicke, R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ., 1999, 6(2), 99-104.
[http://dx.doi.org/10.1038/sj.cdd.4400476] [PMID: 10200555]
[30]
Sollberger, G.; Strittmatter, G.E.; Kistowska, M.; French, L.E.; Beer, H.D. Caspase-4 is required for activation of inflammasomes. J. Immunol., 2012, 188(4), 1992-2000.
[http://dx.doi.org/10.4049/jimmunol.1101620] [PMID: 22246630]
[31]
Martinon, F.; Tschopp, J. Inflammatory caspases and inflammasomes: Master switches of inflammation. Cell Death Differ., 2007, 14(1), 10-22.
[http://dx.doi.org/10.1038/sj.cdd.4402038] [PMID: 16977329]
[32]
Bian, Z.M.; Elner, S.G.; Khanna, H.; Murga-Zamalloa, C.A.; Patil, S.; Elner, V.M. Expression and functional roles of caspase-5 in inflammatory responses of human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci., 2011, 52(12), 8646-8656.
[http://dx.doi.org/10.1167/iovs.11-7570] [PMID: 21969293]
[33]
Chen, H.; Ning, X.; Jiang, Z. Caspases control antiviral innate immunity. Cell. Mol. Immunol., 2017, 14(9), 736-747.
[http://dx.doi.org/10.1038/cmi.2017.44] [PMID: 28690332]
[34]
Wang, X.J.; Cao, Q.; Zhang, Y.; Su, X.D. Activation and regulation of caspase-6 and its role in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol., 2015, 55, 553-572.
[http://dx.doi.org/10.1146/annurev-pharmtox-010814-124414] [PMID: 25340928]
[35]
LeBlanc, A.; Liu, H.; Goodyer, C.; Bergeron, C.; Hammond, J. Caspase-6 role in apoptosis of human neurons, amyloidogenesis, and Alzheimer’s disease. J. Biol. Chem., 1999, 274(33), 23426-23436.
[http://dx.doi.org/10.1074/jbc.274.33.23426] [PMID: 10438520]
[36]
Zheng, M.; Karki, R.; Vogel, P.; Kanneganti, T.D. Caspase-6 is a key regulator of innate immunity, inflammasome activation, and host defense. Cell, 2020, 181(3), 674-687.e13.
[http://dx.doi.org/10.1016/j.cell.2020.03.040] [PMID: 32298652]
[37]
Mahib, M.R.; Hosojima, S.; Kushiyama, H.; Kinoshita, T.; Shiroishi, T.; Suda, T.; Tsuchiya, K. Caspase-7 mediates caspase-1-induced apoptosis independently of Bid. Microbiol. Immunol., 2020, 64(2), 143-152.
[http://dx.doi.org/10.1111/1348-0421.12756] [PMID: 31687791]
[38]
Lamkanfi, M.; Kanneganti, T.D. Caspase-7: A protease involved in apoptosis and inflammation. Int. J. Biochem. Cell Biol., 2010, 42(1), 21-24.
[http://dx.doi.org/10.1016/j.biocel.2009.09.013] [PMID: 19782763]
[39]
Salmena, L.; Lemmers, B.; Hakem, A.; Matysiak-Zablocki, E.; Murakami, K.; Au, P.Y.; Berry, D.M.; Tamblyn, L.; Shehabeldin, A.; Migon, E.; Wakeham, A.; Bouchard, D.; Yeh, W.C.; McGlade, J.C.; Ohashi, P.S.; Hakem, R. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev., 2003, 17(7), 883-895.
[http://dx.doi.org/10.1101/gad.1063703] [PMID: 12654726]
[40]
Kruidering, M.; Evan, G.I. Caspase-8 in apoptosis: The beginning of “the end”? IUBMB Life, 2000, 50(2), 85-90.
[http://dx.doi.org/10.1080/713803693] [PMID: 11185963]
[41]
Salvesen, G.S.; Walsh, C.M. Functions of caspase 8: The identified and the mysterious. Semin. Immunol., 2014, 26(3), 246-252.
[http://dx.doi.org/10.1016/j.smim.2014.03.005] [PMID: 24856110]
[42]
Brentnall, M.; Rodriguez-Menocal, L.; De Guevara, R.L.; Cepero, E.; Boise, L.H. Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis. BMC Cell Biol., 2013, 14, 32.
[http://dx.doi.org/10.1186/1471-2121-14-32] [PMID: 23834359]
[43]
Wachmann, K.; Pop, C.; van Raam, B.J.; Drag, M.; Mace, P.D.; Snipas, S.J.; Zmasek, C.; Schwarzenbacher, R.; Salvesen, G.S.; Riedl, S.J. Activation and specificity of human caspase-10. Biochemistry, 2010, 49(38), 8307-8315.
[http://dx.doi.org/10.1021/bi100968m] [PMID: 20795673]
[44]
Wang, J.; Chun, H.J.; Wong, W.; Spencer, D.M.; Lenardo, M.J. Caspase-10 is an initiator caspase in death receptor signaling. Proc. Natl. Acad. Sci. USA, 2001, 98(24), 13884-13888.
[http://dx.doi.org/10.1073/pnas.241358198] [PMID: 11717445]
[45]
Huang, X.; Feng, Y.; Xiong, G.; Whyte, S.; Duan, J.; Yang, Y.; Wang, K.; Yang, S.; Geng, Y.; Ou, Y.; Chen, D. Caspase-11, a specific sensor for intracellular lipopolysaccharide recognition, mediates the non-canonical inflammatory pathway of pyroptosis. Cell Biosci., 2019, 9, 31.
[http://dx.doi.org/10.1186/s13578-019-0292-0] [PMID: 30962873]
[46]
Man, S.M.; Karki, R.; Briard, B.; Burton, A.; Gingras, S.; Pelletier, S.; Kanneganti, T.D. Differential roles of caspase-1 and caspase-11 in infection and inflammation. Sci. Rep., 2017, 7, 45126.
[http://dx.doi.org/10.1038/srep45126] [PMID: 28345580]
[47]
Oh, C.; Verma, A.; Aachoui, Y. Caspase-11 Non-canonical Inflammasomes in the Lung. Front. Immunol., 2020, 11, 1895.
[http://dx.doi.org/10.3389/fimmu.2020.01895] [PMID: 32973786]
[48]
García de la Cadena, S.; Massieu, L. Caspases and their role in inflammation and ischemic neuronal death. Focus on caspase-12. Apoptosis, 2016, 21(7), 763-777.
[http://dx.doi.org/10.1007/s10495-016-1247-0] [PMID: 27142195]
[49]
Szegezdi, E.; Fitzgerald, U.; Samali, A. Caspase-12 and ER-stress-mediated apoptosis: The story so far. Ann. N. Y. Acad. Sci., 2003, 1010, 186-194.
[http://dx.doi.org/10.1196/annals.1299.032] [PMID: 15033718]
[50]
Scott, A.M.; Saleh, M. The inflammatory caspases: Guardians against infections and sepsis. Cell Death Differ., 2007, 14(1), 23-31.
[http://dx.doi.org/10.1038/sj.cdd.4402026] [PMID: 16977333]
[51]
Markiewicz, A.; Sigorski, D.; Markiewicz, M.; Owczarczyk-Saczonek, A.; Placek, W. Caspase-14-from biomolecular basics to clinical approach. A review of available data. Int. J. Mol. Sci., 2021, 22(11), 5575.
[http://dx.doi.org/10.3390/ijms22115575] [PMID: 34070382]
[52]
Zhang, X.; Graham, S.H.; Kochanek, P.M.; Marion, D.W.; Nathaniel, P.D.; Watkins, S.C.; Clark, R.S. Caspase-8 expression and proteolysis in human brain after severe head injury. FASEB J., 2003, 17(10), 1367-1369.
[http://dx.doi.org/10.1096/fj.02-1067fje] [PMID: 12738800]
[53]
Knoblach, S.M.; Nikolaeva, M.; Huang, X.; Fan, L.; Krajewski, S.; Reed, J.C.; Faden, A.I. Multiple caspases are activated after traumatic brain injury: Evidence for involvement in functional outcome. J. Neurotrauma, 2002, 19(10), 1155-1170.
[http://dx.doi.org/10.1089/08977150260337967] [PMID: 12427325]
[54]
Robertson, G.S.; Crocker, S.J.; Nicholson, D.W.; Schulz, J.B. Neuroprotection by the inhibition of apoptosis. Brain Pathol., 2000, 10(2), 283-292.
[http://dx.doi.org/10.1111/j.1750-3639.2000.tb00262.x] [PMID: 10764048]
[55]
Qiu, J.; Whalen, M.J.; Lowenstein, P.; Fiskum, G.; Fahy, B.; Darwish, R.; Aarabi, B.; Yuan, J.; Moskowitz, M.A. Upregulation of the Fas receptor death-inducing signaling complex after traumatic brain injury in mice and humans. J. Neurosci., 2002, 22(9), 3504-3511.
[http://dx.doi.org/10.1523/JNEUROSCI.22-09-03504.2002] [PMID: 11978827]
[56]
Kischkel, F.C.; Lawrence, D.A.; Tinel, A.; LeBlanc, H.; Virmani, A.; Schow, P.; Gazdar, A.; Blenis, J.; Arnott, D.; Ashkenazi, A. Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J. Biol. Chem., 2001, 276(49), 46639-46646.
[http://dx.doi.org/10.1074/jbc.M105102200] [PMID: 11583996]
[57]
Renatus, M.; Stennicke, H.R.; Scott, F.L.; Liddington, R.C.; Salvesen, G.S. Dimer formation drives the activation of the cell death protease caspase 9. Proc. Natl. Acad. Sci. USA, 2001, 98(25), 14250-14255.
[http://dx.doi.org/10.1073/pnas.231465798] [PMID: 11734640]
[58]
Boatright, K.M.; Renatus, M.; Scott, F.L.; Sperandio, S.; Shin, H.; Pedersen, I.M.; Ricci, J.E.; Edris, W.A.; Sutherlin, D.P.; Green, D.R.; Salvesen, G.S. A unified model for apical caspase activation. Mol. Cell, 2003, 11(2), 529-541.
[http://dx.doi.org/10.1016/S1097-2765(03)00051-0] [PMID: 12620239]
[59]
Sakahira, H.; Enari, M.; Nagata, S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature, 1998, 391(6662), 96-99.
[http://dx.doi.org/10.1038/34214] [PMID: 9422513]
[60]
Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516.
[http://dx.doi.org/10.1080/01926230701320337] [PMID: 17562483]
[61]
Parrish, A.B.; Freel, C.D.; Kornbluth, S. Cellular mechanisms controlling caspase activation and function. Cold Spring Harb. Perspect. Biol., 2013, 5(6), a008672.
[http://dx.doi.org/10.1101/cshperspect.a008672] [PMID: 23732469]
[62]
Bratton, S.B.; Salvesen, G.S. Regulation of the Apaf-1-caspase-9 apoptosome. J. Cell Sci., 2010, 123(Pt 19), 3209-3214.
[http://dx.doi.org/10.1242/jcs.073643] [PMID: 20844150]
[63]
Würstle, M.L.; Laussmann, M.A.; Rehm, M. The central role of initiator caspase-9 in apoptosis signal transduction and the regulation of its activation and activity on the apoptosome. Exp. Cell Res., 2012, 318(11), 1213-1220.
[http://dx.doi.org/10.1016/j.yexcr.2012.02.013] [PMID: 22406265]
[64]
Pistritto, G.; Papaleo, V.; Sanchez, P.; Ceci, C.; Barbaccia, M.L. Divergent modulation of neuronal differentiation by caspase-2 and -9. PLoS One, 2012, 7(5), e36002.
[http://dx.doi.org/10.1371/journal.pone.0036002] [PMID: 22629307]
[65]
McIlwain, D.R.; Berger, T.; Mak, T.W. Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol., 2013, 5(4), a008656.
[http://dx.doi.org/10.1101/cshperspect.a008656]
[66]
Hu, Y.; Benedict, M.A.; Wu, D.; Inohara, N.; Núñez, G. Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Natl. Acad. Sci. USA, 1998, 95(8), 4386-4391.
[http://dx.doi.org/10.1073/pnas.95.8.4386] [PMID: 9539746]
[67]
Hakem, R.; Hakem, A.; Duncan, G.S.; Henderson, J.T.; Woo, M.; Soengas, M.S.; Elia, A.; de la Pompa, J.L.; Kagi, D.; Khoo, W.; Potter, J.; Yoshida, R.; Kaufman, S.A.; Lowe, S.W.; Penninger, J.M.; Mak, T.W. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell, 1998, 94(3), 339-352.
[http://dx.doi.org/10.1016/S0092-8674(00)81477-4] [PMID: 9708736]
[68]
Kuida, K.; Zheng, T.S.; Na, S.; Kuan, C.; Yang, D.; Karasuyama, H.; Rakic, P.; Flavell, R.A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature, 1996, 384(6607), 368-372.
[http://dx.doi.org/10.1038/384368a0] [PMID: 8934524]
[69]
Cui, Q.; Yu, J.H.; Wu, J.N.; Tashiro, S.; Onodera, S.; Minami, M.; Ikejima, T. P53-mediated cell cycle arrest and apoptosis through a caspase-3- independent, but caspase-9-dependent pathway in oridonin-treated MCF-7 human breast cancer cells. Acta Pharmacol. Sin., 2007, 28(7), 1057-1066.
[http://dx.doi.org/10.1111/j.1745-7254.2007.00588.x] [PMID: 17588343]
[70]
Lee, D.; Long, S.A.; Adams, J.L.; Chan, G.; Vaidya, K.S.; Francis, T.A.; Kikly, K.; Winkler, J.D.; Sung, C.M.; Debouck, C.; Richardson, S.; Levy, M.A.; DeWolf, W.E., Jr; Keller, P.M.; Tomaszek, T.; Head, M.S.; Ryan, M.D.; Haltiwanger, R.C.; Liang, P.H.; Janson, C.A.; McDevitt, P.J.; Johanson, K.; Concha, N.O.; Chan, W.; Abdel-Meguid, S.S.; Badger, A.M.; Lark, M.W.; Nadeau, D.P.; Suva, L.J.; Gowen, M.; Nuttall, M.E. Potent and selective nonpeptide inhibitors of caspases 3 and 7 inhibit apoptosis and maintain cell functionality. J. Biol. Chem., 2000, 275(21), 16007-16014.
[http://dx.doi.org/10.1074/jbc.275.21.16007] [PMID: 10821855]
[71]
Bilsland, J.; Harper, S. Caspases and neuroprotection. Curr. Opin. Investig. Drugs, 2002, 3(12), 1745-1752.
[PMID: 12528311]
[72]
Concha, N.O.; Abdel-Meguid, S.S. Controlling apoptosis by inhibition of caspases. Curr. Med. Chem., 2002, 9(6), 713-726.
[http://dx.doi.org/10.2174/0929867023370761] [PMID: 11945133]
[73]
Clark, R.S.; Kochanek, P.M.; Watkins, S.C.; Chen, M.; Dixon, C.E.; Seidberg, N.A.; Melick, J.; Loeffert, J.E.; Nathaniel, P.D.; Jin, K.L.; Graham, S.H. Caspase-3 mediated neuronal death after traumatic brain injury in rats. J. Neurochem., 2000, 74(2), 740-753.
[http://dx.doi.org/10.1046/j.1471-4159.2000.740740.x] [PMID: 10646526]
[74]
Felderhoff-Mueser, U.; Sifringer, M.; Pesditschek, S.; Kuckuck, H.; Moysich, A.; Bittigau, P.; Ikonomidou, C. Pathways leading to apoptotic neurodegeneration following trauma to the developing rat brain. Neurobiol. Dis., 2002, 11(2), 231-245.
[http://dx.doi.org/10.1006/nbdi.2002.0521] [PMID: 12505417]
[75]
Yemişci, M.; Gürsoy-Özdemir, Y.; Caban, S.; Bodur, E.; Capan, Y.; Dalkara, T. Transport of a caspase inhibitor across the blood-brain barrier by chitosan nanoparticles. Methods Enzymol., 2012, 508, 253-269.
[http://dx.doi.org/10.1016/B978-0-12-391860-4.00013-6] [PMID: 22449930]
[76]
Clark, R.S.; Nathaniel, P.D.; Zhang, X.; Dixon, C.E.; Alber, S.M.; Watkins, S.C.; Melick, J.A.; Kochanek, P.M.; Graham, S.H. boc-Aspartyl(OMe)-fluoromethylketone attenuates mitochondrial release of cytochrome c and delays brain tissue loss after traumatic brain injury in rats. J. Cereb. Blood Flow Metab., 2007, 27(2), 316-326.
[http://dx.doi.org/10.1038/sj.jcbfm.9600338] [PMID: 16736044]
[77]
Los, M.; Mozoluk, M.; Ferrari, D.; Stepczynska, A.; Stroh, C.; Renz, A.; Herceg, Z.; Wang, Z.Q.; Schulze-Osthoff, K. Activation and caspase-mediated inhibition of PARP: A molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol. Biol. Cell, 2002, 13(3), 978-988.
[http://dx.doi.org/10.1091/mbc.01-05-0272] [PMID: 11907276]
[78]
Dash, P.K.; Blum, S.; Moore, A.N. Caspase activity plays an essential role in long-term memory. Neuroreport, 2000, 11(12), 2811-2816.
[http://dx.doi.org/10.1097/00001756-200008210-00040] [PMID: 10976968]
[79]
Alvarado-Kristensson, M.; Melander, F.; Leandersson, K.; Rönnstrand, L.; Wernstedt, C.; Andersson, T. p38-MAPK signals survival by phosphorylation of caspase-8 and caspase-3 in human neutrophils. J. Exp. Med., 2004, 199(4), 449-458.
[http://dx.doi.org/10.1084/jem.20031771] [PMID: 14970175]
[80]
Huang, Hk.; Joazeiro, C.A.; Bonfoco, E.; Kamada, S.; Leverson, J.D.; Hunter, T. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J. Biol. Chem., 2000, 275(35), 26661-26664.
[http://dx.doi.org/10.1016/S0021-9258(19)61427-4] [PMID: 10862606]
[81]
Choi, W.Y.; Jin, C.Y.; Han, M.H.; Kim, G.Y.; Kim, N.D.; Lee, W.H.; Kim, S.K.; Choi, Y.H. Sanguinarine sensitizes human gastric adenocarcinoma AGS cells to TRAIL-mediated apoptosis via down-regulation of AKT and activation of caspase-3. Anticancer Res., 2009, 29(11), 4457-4465.
[PMID: 20032392]
[82]
Scott, F.L.; Denault, J.B.; Riedl, S.J.; Shin, H.; Renatus, M.; Salvesen, G.S. XIAP inhibits caspase-3 and -7 using two binding sites: Evolutionarily conserved mechanism of IAPs. EMBO J., 2005, 24(3), 645-655.
[http://dx.doi.org/10.1038/sj.emboj.7600544] [PMID: 15650747]
[83]
Chai, J.; Shiozaki, E.; Srinivasula, S.M.; Wu, Q.; Datta, P.; Alnemri, E.S.; Shi, Y. Structural basis of caspase-7 inhibition by XIAP. Cell, 2001, 104(5), 769-780.
[http://dx.doi.org/10.1016/S0092-8674(01)00272-0] [PMID: 11257230]
[84]
Riedl, S.J.; Fuentes-Prior, P.; Renatus, M.; Kairies, N.; Krapp, S.; Huber, R.; Salvesen, G.S.; Bode, W. Structural basis for the activation of human procaspase-7. Proc. Natl. Acad. Sci. USA, 2001, 98(26), 14790-14795.
[http://dx.doi.org/10.1073/pnas.221580098] [PMID: 11752425]
[85]
Eckelman, B.P.; Salvesen, G.S. The human anti-apoptotic proteins cIAP1 and cIAP2 bind but do not inhibit caspases. J. Biol. Chem., 2006, 281(6), 3254-3260.
[http://dx.doi.org/10.1074/jbc.M510863200] [PMID: 16339151]
[86]
Tenev, T.; Zachariou, A.; Wilson, R.; Ditzel, M.; Meier, P. IAPs are functionally non-equivalent and regulate effector caspases through distinct mechanisms. Nat. Cell Biol., 2005, 7(1), 70-77.
[http://dx.doi.org/10.1038/ncb1204] [PMID: 15580265]
[87]
Schile, A.J.; García-Fernández, M.; Steller, H. Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev., 2008, 22(16), 2256-2266.
[http://dx.doi.org/10.1101/gad.1663108] [PMID: 18708583]
[88]
Mannick, J.B.; Schonhoff, C.; Papeta, N.; Ghafourifar, P.; Szibor, M.; Fang, K.; Gaston, B. S-Nitrosylation of mitochondrial caspases. J. Cell Biol., 2001, 154(6), 1111-1116.
[http://dx.doi.org/10.1083/jcb.200104008] [PMID: 11551979]
[89]
Jiang, Z.L.; Fletcher, N.M.; Diamond, M.P.; Abu-Soud, H.M.; Saed, G.M. S-nitrosylation of caspase-3 is the mechanism by which adhesion fibroblasts manifest lower apoptosis. Wound Repair Regen., 2009, 17(2), 224-229.
[http://dx.doi.org/10.1111/j.1524-475X.2009.00459.x] [PMID: 19320891]
[90]
Maejima, Y.; Adachi, S.; Morikawa, K.; Ito, H.; Isobe, M. Nitric oxide inhibits myocardial apoptosis by preventing caspase-3 activity via S-nitrosylation. J. Mol. Cell. Cardiol., 2005, 38(1), 163-174.
[http://dx.doi.org/10.1016/j.yjmcc.2004.10.012] [PMID: 15623433]
[91]
Ueta, E.; Kamatani, T.; Yamamoto, T.; Osaki, T. Tyrosine-nitration of caspase 3 and cytochrome c does not suppress apoptosis induction in squamous cell carcinoma cells. Int. J. Cancer, 2003, 103(6), 717-722.
[http://dx.doi.org/10.1002/ijc.10832] [PMID: 12516089]
[92]
Lau, A.; Arundine, M.; Sun, H.S.; Jones, M.; Tymianski, M. Inhibition of caspase-mediated apoptosis by peroxynitrite in traumatic brain injury. J. Neurosci., 2006, 26(45), 11540-11553.
[http://dx.doi.org/10.1523/JNEUROSCI.3507-06.2006] [PMID: 17093075]
[93]
Tsuda, T.; Ohmori, Y.; Muramatsu, H.; Hosaka, Y.; Takiguchi, K.; Saitoh, F.; Kato, K.; Nakayama, K.; Nakamura, N.; Nagata, S.; Mochizuki, H. Inhibitory effect of M50054, a novel inhibitor of apoptosis, on anti-Fas-antibody-induced hepatitis and chemotherapy-induced alopecia. Eur. J. Pharmacol., 2001, 433(1), 37-45.
[http://dx.doi.org/10.1016/S0014-2999(01)01489-3] [PMID: 11755132]
[94]
Tseng, A.S.; Adams, D.S.; Qiu, D.; Koustubhan, P.; Levin, M. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev. Biol., 2007, 301(1), 62-69.
[http://dx.doi.org/10.1016/j.ydbio.2006.10.048] [PMID: 17150209]
[95]
Shi, Y.; Zhao, S.; Li, J.; Mao, B. Islet-1 is required for ventral neuron survival in Xenopus. Biochem. Biophys. Res. Commun., 2009, 388(3), 506-510.
[http://dx.doi.org/10.1016/j.bbrc.2009.08.017] [PMID: 19666005]
[96]
Knoblach, S.M.; Alroy, D.A.; Nikolaeva, M.; Cernak, I.; Stoica, B.A.; Faden, A.I. Caspase inhibitor z-DEVD-fmk attenuates calpain and necrotic cell death in vitro and after traumatic brain injury. J. Cereb. Blood Flow Metab., 2004, 24(10), 1119-1132.
[http://dx.doi.org/10.1097/01.WCB.0000138664.17682.32] [PMID: 15529012]
[97]
Kaptanoglu, E.; Caner, H.; Solaroglu, I.; Kilinc, K. Mexiletine treatment-induced inhibition of caspase-3 activation and improvement of behavioral recovery after spinal cord injury. J. Neurosurg. Spine, 2005, 3(1), 53-56.
[http://dx.doi.org/10.3171/spi.2005.3.1.0053] [PMID: 16122023]
[98]
Perry, D.K.; Smyth, M.J.; Stennicke, H.R.; Salvesen, G.S.; Duriez, P.; Poirier, G.G.; Hannun, Y.A. Zinc is a potent inhibitor of the apoptotic protease, caspase-3. A novel target for zinc in the inhibition of apoptosis. J. Biol. Chem., 1997, 272(30), 18530-18533.
[http://dx.doi.org/10.1074/jbc.272.30.18530] [PMID: 9228015]
[99]
Allan, L.A.; Clarke, P.R. Apoptosis and autophagy: Regulation of caspase-9 by phosphorylation. FEBS J., 2009, 276(21), 6063-6073.
[http://dx.doi.org/10.1111/j.1742-4658.2009.07330.x] [PMID: 19788417]
[100]
Allan, L.A.; Morrice, N.; Brady, S.; Magee, G.; Pathak, S.; Clarke, P.R. Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK. Nat. Cell Biol., 2003, 5(7), 647-654.
[http://dx.doi.org/10.1038/ncb1005] [PMID: 12792650]
[101]
Allan, L.A.; Clarke, P.R. Phosphorylation of caspase-9 by CDK1/cyclin B1 protects mitotic cells against apoptosis. Mol. Cell, 2007, 26(2), 301-310.
[http://dx.doi.org/10.1016/j.molcel.2007.03.019] [PMID: 17466630]
[102]
Laguna, A.; Aranda, S.; Barallobre, M.J.; Barhoum, R.; Fernández, E.; Fotaki, V.; Delabar, J.M.; de la Luna, S.; de la Villa, P.; Arbonés, M.L. The protein kinase DYRK1A regulates caspase-9-mediated apoptosis during retina development. Dev. Cell, 2008, 15(6), 841-853.
[http://dx.doi.org/10.1016/j.devcel.2008.10.014] [PMID: 19081073]
[103]
Seifert, A.; Allan, L.A.; Clarke, P.R. DYRK1A phosphorylates caspase 9 at an inhibitory site and is potently inhibited in human cells by harmine. FEBS J., 2008, 275(24), 6268-6280.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06751.x] [PMID: 19016842]
[104]
Seifert, A.; Clarke, P.R. p38alpha- and DYRK1A-dependent phosphorylation of caspase-9 at an inhibitory site in response to hyperosmotic stress. Cell. Signal., 2009, 21(11), 1626-1633.
[http://dx.doi.org/10.1016/j.cellsig.2009.06.009] [PMID: 19586613]
[105]
Dessauge, F.; Cayla, X.; Albar, J.P.; Fleischer, A.; Ghadiri, A.; Duhamel, M.; Rebollo, A. Identification of PP1alpha as a caspase-9 regulator in IL-2 deprivation-induced apoptosis. J. Immunol., 2006, 177(4), 2441-2451.
[http://dx.doi.org/10.4049/jimmunol.177.4.2441] [PMID: 16888006]
[106]
Brady, S.C.; Allan, L.A.; Clarke, P.R. Regulation of caspase 9 through phosphorylation by protein kinase C zeta in response to hyperosmotic stress. Mol. Cell. Biol., 2005, 25(23), 10543-10555.
[http://dx.doi.org/10.1128/MCB.25.23.10543-10555.2005] [PMID: 16287866]
[107]
Martin, M.C.; Allan, L.A.; Lickrish, M.; Sampson, C.; Morrice, N.; Clarke, P.R. Protein kinase A regulates caspase-9 activation by Apaf-1 downstream of cytochrome c. J. Biol. Chem., 2005, 280(15), 15449-15455.
[http://dx.doi.org/10.1074/jbc.M414325200] [PMID: 15703181]
[108]
McDonnell, M.A.; Abedin, M.J.; Melendez, M.; Platikanova, T.N.; Ecklund, J.R.; Ahmed, K.; Kelekar, A. Phosphorylation of murine caspase-9 by the protein kinase casein kinase 2 regulates its cleavage by caspase-8. J. Biol. Chem., 2008, 283(29), 20149-20158.
[http://dx.doi.org/10.1074/jbc.M802846200] [PMID: 18467326]
[109]
Török, N.J.; Higuchi, H.; Bronk, S.; Gores, G.J. Nitric oxide inhibits apoptosis downstream of cytochrome C release by nitrosylating caspase 9. Cancer Res., 2002, 62(6), 1648-1653.
[PMID: 11912135]
[110]
Silke, J.; Meier, P. Inhibitor of apoptosis (IAP) proteins-modulators of cell death and inflammation. Cold Spring Harb. Perspect. Biol., 2013, 5(2), a008730.
[http://dx.doi.org/10.1101/cshperspect.a008730] [PMID: 23378585]
[111]
Joazeiro, C.A.; Weissman, A.M. RING finger proteins: Mediators of ubiquitin ligase activity. Cell, 2000, 102(5), 549-552.
[http://dx.doi.org/10.1016/S0092-8674(00)00077-5] [PMID: 11007473]
[112]
Morizane, Y.; Honda, R.; Fukami, K.; Yasuda, H. X-linked inhibitor of apoptosis functions as ubiquitin ligase toward mature caspase-9 and cytosolic Smac/DIABLO. J. Biochem., 2005, 137(2), 125-132.
[http://dx.doi.org/10.1093/jb/mvi029] [PMID: 15749826]
[113]
Srinivasula, S.M.; Hegde, R.; Saleh, A.; Datta, P.; Shiozaki, E.; Chai, J.; Lee, R.A.; Robbins, P.D.; Fernandes-Alnemri, T.; Shi, Y.; Alnemri, E.S. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature, 2001, 410(6824), 112-116.
[http://dx.doi.org/10.1038/35065125] [PMID: 11242052]
[114]
Bratton, S.B.; Walker, G.; Srinivasula, S.M.; Sun, X.M.; Butterworth, M.; Alnemri, E.S.; Cohen, G.M. Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J., 2001, 20(5), 998-1009.
[http://dx.doi.org/10.1093/emboj/20.5.998] [PMID: 11230124]
[115]
Eckelman, B.P.; Salvesen, G.S.; Scott, F.L. Human inhibitor of apoptosis proteins: Why XIAP is the black sheep of the family. EMBO Rep., 2006, 7(10), 988-994.
[http://dx.doi.org/10.1038/sj.embor.7400795] [PMID: 17016456]
[116]
Shiozaki, E.N.; Chai, J.; Rigotti, D.J.; Riedl, S.J.; Li, P.; Srinivasula, S.M.; Alnemri, E.S.; Fairman, R.; Shi, Y. Mechanism of XIAP-mediated inhibition of caspase-9. Mol. Cell, 2003, 11(2), 519-527.
[http://dx.doi.org/10.1016/S1097-2765(03)00054-6] [PMID: 12620238]

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