New Views on the Misconstrued: Executioner Caspases and Their Diverse Non-apoptotic Roles

Neuron

Volumn 88, Issue 3, 2015, Pages 461-474

  Unsain, Nicolas ^a   Barker, Philip A ^b  

^a INSTITUTO DE INVESTIGACIÓN MÉDICA MERCEDES Y MARTÍN FERREYRA   (Argentina)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; CASPASE 7; CASPASE 9; EXECUTIONER CASPASE; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLULAR PARAMETERS; CELLULAR REMODELLING; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NERVE FIBER DEGENERATION; NERVE FIBER REGENERATION; NERVE GROWTH; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ANIMAL; DEGENERATIVE DISEASE; ENZYMOLOGY; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CASPASES; HUMANS; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY; NEURONS;

EID: 84946132951     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.08.029     Document Type: Review

References (201)

1. Adlard P.A., Parncutt J.M., Finkelstein D.I., Bush A.I. Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer's disease?. J. Neurosci. 2010, 30:1631-1636.
2. Ai H.W., Hazelwood K.L., Davidson M.W., Campbell R.E. Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat. Methods 2008, 5:401-403.
3. Albin R.L., Young A.B., Penney J.B., Handelin B., Balfour R., Anderson K.D., Markel D.S., Tourtellotte W.W., Reiner A. Abnormalities of striatal projection neurons and N-methyl-D-aspartate receptors in presymptomatic Huntington's disease. N. Engl. J. Med. 1990, 322:1293-1298.
4. 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, 5:647-654.
5. Arama E., Bader M., Srivastava M., Bergmann A., Steller H. The two Drosophila cytochrome C proteins can function in both respiration and caspase activation. EMBO J. 2006, 25:232-243.
6. Asselin E., Mills G.B., Tsang B.K. XIAP regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res. 2001, 61:1862-1868.
7. Beattie E.C., Carroll R.C., Yu X., Morishita W., Yasuda H., von Zastrow M., Malenka R.C. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 2000, 3:1291-1300.
8. Bergmann A., Steller H. Apoptosis, stem cells, and tissue regeneration. Sci. Signal. 2010, 3:re8.
9. Bilak A., Uyetake L., Su T.T. Dying cells protect survivors from radiation-induced cell death in Drosophila. PLoS Genet. 2014, 10:e1004220.
10. Bourne J.N., Harris K.M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 2011, 21:354-373.
11. 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, 25:10543-10555.
12. Bravarenko N.I., Onufriev M.V., Stepanichev M.Y., Ierusalimsky V.N., Balaban P.M., Gulyaeva N.V. Caspase-like activity is essential for long-term synaptic plasticity in the terrestrial snail Helix. Eur. J. Neurosci. 2006, 23:129-140.
13. Brusco J., Haas K. Interactions between mitochondria and the transcription factor myocyte enhancer factor 2 (MEF2) regulate neuronal structural and functional plasticity and metaplasticity. J. Physiol. 2015, 593:3471-3481.
14. Cajal R. Histologie du systeme nerveux 1911, Oxford University Press, New York, NY.
15. Campbell D.S., Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 2003, 37:939-952.
16. Campbell D.S., Okamoto H. Local caspase activation interacts with Slit-Robo signaling to restrict axonal arborization. J. Cell Biol. 2013, 203:657-672.
17. Cao Q., Wang X.J., Liu C.W., Liu D.F., Li L.F., Gao Y.Q., Su X.D. Inhibitory mechanism of caspase-6 phosphorylation revealed by crystal structures, molecular dynamics simulations, and biochemical assays. J. Biol. Chem. 2012, 287:15371-15379.
18. Carlile G.W., Smith D.H., Wiedmann M. Caspase-3 has a nonapoptotic function in erythroid maturation. Blood 2004, 103:4310-4316.
19. 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, 104:769-780.
20. Chan S.L., Griffin W.S., Mattson M.P. Evidence for caspase-mediated cleavage of AMPA receptor subunits in neuronal apoptosis and Alzheimer's disease. J. Neurosci. Res. 1999, 57:315-323.
21. Chen S.X., Cherry A., Tari P.K., Podgorski K., Kwong Y.K., Haas K. The transcription factor MEF2 directs developmental visually driven functional and structural metaplasticity. Cell 2012, 151:41-55.
22. Chen X., Lin R., Chang L., Xu S., Wei X., Zhang J., Wang C., Anwyl R., Wang Q. Enhancement of long-term depression by soluble amyloid β protein in rat hippocampus is mediated by metabotropic glutamate receptor and involves activation of p38MAPK, STEP and caspase-3. Neuroscience 2013, 253:435-443.
23. Cheng L., Yin W.J., Zhang J.F., Qi J.S. Amyloid beta-protein fragments 25-35 and 31-35 potentiate long-term depression in hippocampal CA1 region of rats in vivo. Synapse 2009, 63:206-214.
24. Chera S., Ghila L., Dobretz K., Wenger Y., Bauer C., Buzgariu W., Martinou J.C., Galliot B. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev. Cell 2009, 17:279-289.
25. Cho E., Hwang J.J., Han S.H., Chung S.J., Koh J.Y., Lee J.Y. Endogenous zinc mediates apoptotic programmed cell death in the developing brain. Neurotox. Res. 2010, 17:156-166.
26. Choi Y.E., Butterworth M., Malladi S., Duckett C.S., Cohen G.M., Bratton S.B. The E3 ubiquitin ligase cIAP1 binds and ubiquitinates caspase-3 and -7 via unique mechanisms at distinct steps in their processing. J. Biol. Chem. 2009, 284:12772-12782.
27. Chowdhury I., Tharakan B., Bhat G.K. Caspases - an update. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2008, 151:10-27.
28. Costa-Mattioli M., Gobert D., Stern E., Gamache K., Colina R., Cuello C., Sossin W., Kaufman R., Pelletier J., Rosenblum K., et al. eIF2alpha phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory. Cell 2007, 129:195-206.
29. Cowan C.M., Roskams A.J. Caspase-3 and caspase-9 mediate developmental apoptosis in the mouse olfactory system. J. Comp. Neurol. 2004, 474:136-148.
30. Cowan C.M., Thai J., Krajewski S., Reed J.C., Nicholson D.W., Kaufmann S.H., Roskams A.J. Caspases 3 and 9 send a pro-apoptotic signal from synapse to cell body in olfactory receptor neurons. J. Neurosci. 2001, 21:7099-7109.
31. Cusack C.L., Swahari V., Hampton Henley W., Michael Ramsey J., Deshmukh M. Distinct pathways mediate axon degeneration during apoptosis and axon-specific pruning. Nat. Commun. 2013, 4:1876.
32. D'Amelio M., Cavallucci V., Middei S., Marchetti C., Pacioni S., Ferri A., Diamantini A., De Zio D., Carrara P., Battistini L., et al. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat. Neurosci. 2011, 14:69-76.
33. D'Brot A., Chen P., Vaishnav M., Yuan S., Akey C.W., Abrams J.M. Tango7 directs cellular remodeling by the Drosophila apoptosome. Genes Dev. 2013, 27:1650-1655.
34. Dash P.K., Blum S., Moore A.N. Caspase activity plays an essential role in long-term memory. Neuroreport 2000, 11:2811-2816.
35. De Botton S., Sabri S., Daugas E., Zermati Y., Guidotti J.E., Hermine O., Kroemer G., Vainchenker W., Debili N. Platelet formation is the consequence of caspase activation within megakaryocytes. Blood 2002, 100:1310-1317.
36. Dorstyn L., Read S., Cakouros D., Huh J.R., Hay B.A., Kumar S. The role of cytochrome c in caspase activation in Drosophila melanogaster cells. J. Cell Biol. 2002, 156:1089-1098.
37. Dunfield D., Haas K. Metaplasticity governs natural experience-driven plasticity of nascent embryonic brain circuits. Neuron 2009, 64:240-250.
38. Durie D., Lewis S.M., Liwak U., Kisilewicz M., Gorospe M., Holcik M. RNA-binding protein HuR mediates cytoprotection through stimulation of XIAP translation. Oncogene 2011, 30:1460-1469.
39. Ernsberger U. Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Res. 2009, 336:349-384.
40. Ertürk A., Wang Y., Sheng M. Local pruning of dendrites and spines by caspase-3-dependent and proteasome-limited mechanisms. J. Neurosci. 2014, 34:1672-1688.
41. Esteban J.A., Shi S.H., Wilson C., Nuriya M., Huganir R.L., Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 2003, 6:136-143.
42. Fernando P., Kelly J.F., Balazsi K., Slack R.S., Megeney L.A. Caspase 3 activity is required for skeletal muscle differentiation. Proc. Natl. Acad. Sci. USA 2002, 99:11025-11030.
43. Fernando P., Brunette S., Megeney L.A. Neural stem cell differentiation is dependent upon endogenous caspase 3 activity. FASEB J. 2005, 19:1671-1673.
44. Ferrer I., Guionnet N., Cruz-Sánchez F., Tuñón T. Neuronal alterations in patients with dementia: a Golgi study on biopsy samples. Neurosci. Lett. 1990, 114:11-16.
45. Figueroa R.A., Ramberg V., Gatsinzi T., Samuelsson M., Zhang M., Iverfeldt K., Hallberg E. Anchored FRET sensors detect local caspase activation prior to neuronal degeneration. Mol. Neurodegener. 2011, 6:35.
46. Finn J.T., Weil M., Archer F., Siman R., Srinivasan A., Raff M.C. Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases. J. Neurosci. 2000, 20:1333-1341.
47. Fuchs Y., Brown S., Gorenc T., Rodriguez J., Fuchs E., Steller H. Sept4/ARTS regulates stem cell apoptosis and skin regeneration. Science 2013, 341:286-289.
48. Fuentes-Prior P., Salvesen G.S. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem. J. 2004, 384:201-232.
49. Fujita J., Crane A.M., Souza M.K., Dejosez M., Kyba M., Flavell R.A., Thomson J.A., Zwaka T.P. Caspase activity mediates the differentiation of embryonic stem cells. Cell Stem Cell 2008, 2:595-601.
50. Fulda S., Vucic D. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 2012, 11:109-124.
51. Gafni J., Hermel E., Young J.E., Wellington C.L., Hayden M.R., Ellerby L.M. Inhibition of calpain cleavage of huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J. Biol. Chem. 2004, 279:20211-20220.
52. Gafni J., Papanikolaou T., Degiacomo F., Holcomb J., Chen S., Menalled L., Kudwa A., Fitzpatrick J., Miller S., Ramboz S., et al. Caspase-6 activity in a BACHD mouse modulates steady-state levels of mutant huntingtin protein but is not necessary for production of a 586 amino acid proteolytic fragment. J. Neurosci. 2012, 32:7454-7465.
53. Galbán S., Duckett C.S. XIAP as a ubiquitin ligase in cellular signaling. Cell Death Differ. 2010, 17:54-60.
54. Gillies L.A., Kuwana T. Apoptosis regulation at the mitochondrial outer membrane. J. Cell. Biochem. 2014, 115:632-640.
55. Gottfried Y., Rotem A., Lotan R., Steller H., Larisch S. The mitochondrial ARTS protein promotes apoptosis through targeting XIAP. EMBO J. 2004, 23:1627-1635.
56. Goyal L., McCall K., Agapite J., Hartwieg E., Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 2000, 19:589-597.
57. Graham R.K., Deng Y., Slow E.J., Haigh B., Bissada N., Lu G., Pearson J., Shehadeh J., Bertram L., Murphy Z., et al. Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 2006, 125:1179-1191.
58. Graham R.K., Deng Y., Carroll J., Vaid K., Cowan C., Pouladi M.A., Metzler M., Bissada N., Wang L., Faull R.L., et al. Cleavage at the 586 amino acid caspase-6 site in mutant huntingtin influences caspase-6 activation in vivo. J. Neurosci. 2010, 30:15019-15029.
59. Graham R.K., Deng Y., Pouladi M.A., Vaid K., Ehrnhoefer D., Southwell A.L., Bissada N., Franciosi S., Hayden M.R. Caspase-6-Resistant Mutant Huntingtin Does not Rescue the Toxic Effects of Caspase-Cleavable Mutant Huntingtin in vivo. J. Huntingtons Dis. 2012, 1:243-260.
60. Gray C.W., Ward R.V., Karran E., Turconi S., Rowles A., Viglienghi D., Southan C., Barton A., Fantom K.G., West A., et al. Characterization of human HtrA2, a novel serine protease involved in the mammalian cellular stress response. Eur. J. Biochem. 2000, 267:5699-5710.
61. Gulyaeva N.V., Kudryashov I.E., Kudryashova I.V. Caspase activity is essential for long-term potentiation. J. Neurosci. Res. 2003, 73:853-864.
62. Gurley K.A., Elliott S.A., Simakov O., Schmidt H.A., Holstein T.W., Sánchez Alvarado A. Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev. Biol. 2010, 347:24-39.
63. Gyrd-Hansen M., Darding M., Miasari M., Santoro M.M., Zender L., Xue W., Tenev T., da Fonseca P.C., Zvelebil M., Bujnicki J.M., et al. IAPs contain an evolutionarily conserved ubiquitin-binding domain that regulates NF-kappaB as well as cell survival and oncogenesis. Nat. Cell Biol. 2008, 10:1309-1317.
64. Han M.H., Jiao S., Jia J.M., Chen Y., Chen C.Y., Gucek M., Markey S.P., Li Z. The novel caspase-3 substrate Gap43 is involved in AMPA receptor endocytosis and long-term depression. Mol. Cell. Proteomics 2013, 12:3719-3731.
65. Happo L., Strasser A., Cory S. BH3-only proteins in apoptosis at a glance. J. Cell Sci. 2012, 125:1081-1087.
66. Hawkins C.J., Wang S.L., Hay B.A. A cloning method to identify caspases and their regulators in yeast: identification of Drosophila IAP1 as an inhibitor of the Drosophila caspase DCP-1. Proc. Natl. Acad. Sci. USA 1999, 96:2885-2890.
67. Hsieh H., Boehm J., Sato C., Iwatsubo T., Tomita T., Sisodia S., Malinow R. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 2006, 52:831-843.
68. Huang Y.Y., Colino A., Selig D.K., Malenka R.C. The influence of prior synaptic activity on the induction of long-term potentiation. Science 1992, 255:730-733.
69. 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, 275:26661-26664.
70. Huber K.L., Hardy J.A. Mechanism of zinc-mediated inhibition of caspase-9. Protein Sci. 2012, 21:1056-1065.
71. Huesmann G.R., Clayton D.F. Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron 2006, 52:1061-1072.
72. Huh J.R., Vernooy S.Y., Yu H., Yan N., Shi Y., Guo M., Hay B.A. Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol. 2004, 2:E15.
73. Hunter A.L., Zhang J., Chen S.C., Si X., Wong B., Ekhterae D., Luo H., Granville D.J. Apoptosis repressor with caspase recruitment domain (ARC) inhibits myogenic differentiation. FEBS Lett. 2007, 581:879-884.
74. Ingelsson M., Fukumoto H., Newell K.L., Growdon J.H., Hedley-Whyte E.T., Frosch M.P., Albert M.S., Hyman B.T., Irizarry M.C. Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004, 62:925-931.
75. Ishizaki Y., Jacobson M.D., Raff M.C. A role for caspases in lens fiber differentiation. J. Cell Biol. 1998, 140:153-158.
76. Janzen V., Fleming H.E., Riedt T., Karlsson G., Riese M.J., Lo Celso C., Reynolds G., Milne C.D., Paige C.J., Karlsson S., et al. Hematopoietic stem cell responsiveness to exogenous signals is limited by caspase-3. Cell Stem Cell 2008, 2:584-594.
77. Jiao S., Li Z. Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 2011, 70:758-772.
78. Jo J., Whitcomb D.J., Olsen K.M., Kerrigan T.L., Lo S.C., Bru-Mercier G., Dickinson B., Scullion S., Sheng M., Collingridge G., Cho K. Aβ(1-42) inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3β. Nat. Neurosci. 2011, 14:545-547.
79. Jones J.M., Datta P., Srinivasula S.M., Ji W., Gupta S., Zhang Z., Davies E., Hajnóczky G., Saunders T.L., Van Keuren M.L., et al. Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice. Nature 2003, 425:721-727.
80. Kallop D.Y., Meilandt W.J., Gogineni A., Easley-Neal C., Wu T., Jubb A.M., Yaylaoglu M., Shamloo M., Tessier-Lavigne M., Scearce-Levie K., Weimer R.M. A death receptor 6-amyloid precursor protein pathway regulates synapse density in the mature CNS but does not contribute to Alzheimer's disease-related pathophysiology in murine models. J. Neurosci. 2014, 34:6425-6437.
81. Kanuka H., Kuranaga E., Takemoto K., Hiratou T., Okano H., Miura M. Drosophila caspase transduces Shaggy/GSK-3beta kinase activity in neural precursor development. EMBO J. 2005, 24:3793-3806.
82. Khalil H., Peltzer N., Walicki J., Yang J.Y., Dubuis G., Gardiol N., Held W., Bigliardi P., Marsland B., Liaudet L., Widmann C. Caspase-3 protects stressed organs against cell death. Mol. Cell. Biol. 2012, 32:4523-4533.
83. Kim J.H., Anwyl R., Suh Y.H., Djamgoz M.B., Rowan M.J. Use-dependent effects of amyloidogenic fragments of (beta)-amyloid precursor protein on synaptic plasticity in rat hippocampus in vivo. J. Neurosci. 2001, 21:1327-1333.
84. King R.S., Newmark P.A. The cell biology of regeneration. J. Cell Biol. 2012, 196:553-562.
85. Kissel H., Georgescu M.M., Larisch S., Manova K., Hunnicutt G.R., Steller H. The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev. Cell 2005, 8:353-364.
86. Kozyrev S.A., Nikitin V.P., Sherstnev V.V. Synapse-specific plasticity in command neurons during learning of edible snails under the action of caspase inhibitors. Bull. Exp. Biol. Med. 2007, 144:755-759.
87. Kuo C.T., Zhu S., Younger S., Jan L.Y., Jan Y.N. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 2006, 51:283-290.
88. Kuranaga E., Kanuka H., Tonoki A., Takemoto K., Tomioka T., Kobayashi M., Hayashi S., Miura M. Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 2006, 126:583-596.
89. Landles C., Weiss A., Franklin S., Howland D., Bates G. Caspase-6 does not contribute to the proteolysis of mutant huntingtin in the HdhQ150 knock-in mouse model of Huntington's disease. PLoS Curr. 2012, 4. e4fd085bfc9973.
90. Lanz T.A., Carter D.B., Merchant K.M. Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiol. Dis. 2003, 13:246-253.
91. Larisch S., Yi Y., Lotan R., Kerner H., Eimerl S., Tony Parks W., Gottfried Y., Birkey Reffey S., de Caestecker M.P., Danielpour D., et al. A novel mitochondrial septin-like protein, ARTS, mediates apoptosis dependent on its P-loop motif. Nat. Cell Biol. 2000, 2:915-921.
92. Larsen B.D., Megeney L.A. Parole terms for a killer: directing caspase3/CAD induced DNA strand breaks to coordinate changes in gene expression. Cell Cycle 2010, 9:2940-2945.
93. Larsen B.D., Rampalli S., Burns L.E., Brunette S., Dilworth F.J., Megeney L.A. Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNA strand breaks. Proc. Natl. Acad. Sci. USA 2010, 107:4230-4235.
94. Lee K.J., Park I.S., Kim H., Greenough W.T., Pak D.T., Rhyu I.J. Motor skill training induces coordinated strengthening and weakening between neighboring synapses. J. Neurosci. 2013, 33:9794-9799.
95. Li J., Yuan J. Caspases in apoptosis and beyond. Oncogene 2008, 27:6194-6206.
96. Li F., He Z., Shen J., Huang Q., Li W., Liu X., He Y., Wolf F., Li C.Y. Apoptotic caspases regulate induction of iPSCs from human fibroblasts. Cell Stem Cell 2010, 7:508-520.
97. Li F., Huang Q., Chen J., Peng Y., Roop D.R., Bedford J.S., Li C.Y. Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci. Signal. 2010, 3:ra13.
98. Li Z., Jo J., Jia J.M., Lo S.C., Whitcomb D.J., Jiao S., Cho K., Sheng M. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 2010, 141:859-871.
99. Lippens S., Kockx M., Knaapen M., Mortier L., Polakowska R., Verheyen A., Garmyn M., Zwijsen A., Formstecher P., Huylebroeck D., et al. Epidermal differentiation does not involve the pro-apoptotic executioner caspases, but is associated with caspase-14 induction and processing. Cell Death Differ. 2000, 7:1218-1224.
100. Lisi S., Mazzon I., White K. Diverse domains of THREAD/DIAP1 are required to inhibit apoptosis induced by REAPER and HID in Drosophila. Genetics 2000, 154:669-678.
101. Liu L., Stamler J.S. NO: an inhibitor of cell death. Cell Death Differ. 1999, 6:937-942.
102. Lo Y.J., Poo M.M. Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science 1991, 254:1019-1022.
103. Lopez J., Meier P. To fight or die - inhibitor of apoptosis proteins at the crossroad of innate immunity and death. Curr. Opin. Cell Biol. 2010, 22:872-881.
104. Lopez J., John S.W., Tenev T., Rautureau G.J., Hinds M.G., Francalanci F., Wilson R., Broemer M., Santoro M.M., Day C.L., Meier P. CARD-mediated autoinhibition of cIAP1's E3 ligase activity suppresses cell proliferation and migration. Mol. Cell 2011, 42:569-583.
105. Lu C., Fu W., Salvesen G.S., Mattson M.P. Direct cleavage of AMPA receptor subunit GluR1 and suppression of AMPA currents by caspase-3: implications for synaptic plasticity and excitotoxic neuronal death. Neuromolecular Med. 2002, 1:69-79.
106. Lu C., Wang Y., Furukawa K., Fu W., Ouyang X., Mattson M.P. Evidence that caspase-1 is a negative regulator of AMPA receptor-mediated long-term potentiation at hippocampal synapses. J. Neurochem. 2006, 97:1104-1110.
107. Mannick J.B., Hausladen A., Liu L., Hess D.T., Zeng M., Miao Q.X., Kane L.S., Gow A.J., Stamler J.S. Fas-induced caspase denitrosylation. Science 1999, 284:651-654.
108. Marik S.A., Olsen O., Tessier-Lavigne M., Gilbert C.D. Death receptor 6 regulates adult experience-dependent cortical plasticity. J. Neurosci. 2013, 33:14998-15003.
109. 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, 280:15449-15455.
110. Martin M.C., Allan L.A., Mancini E.J., Clarke P.R. The docking interaction of caspase-9 with ERK2 provides a mechanism for the selective inhibitory phosphorylation of caspase-9 at threonine 125. J. Biol. Chem. 2008, 283:3854-3865.
111. Martins L.M., Morrison A., Klupsch K., Fedele V., Moisoi N., Teismann P., Abuin A., Grau E., Geppert M., Livi G.P., et al. Neuroprotective role of the Reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Mol. Cell. Biol. 2004, 24:9848-9862.
112. Masliah E., Mallory M., Hansen L., DeTeresa R., Alford M., Terry R. Synaptic and neuritic alterations during the progression of Alzheimer's disease. Neurosci. Lett. 1994, 174:67-72.
113. McIlwain D.R., Berger T., Mak T.W. Caspase functions in cell death and disease. Cold Spring Harb. Perspect. Biol. 2013, 5:a008656.
114. McLaughlin B., Hartnett K.A., Erhardt J.A., Legos J.J., White R.F., Barone F.C., Aizenman E. Caspase 3 activation is essential for neuroprotection in preconditioning. Proc. Natl. Acad. Sci. USA 2003, 100:715-720.
115. Mendes C.S., Arama E., Brown S., Scherr H., Srivastava M., Bergmann A., Steller H., Mollereau B. Cytochrome c-d regulates developmental apoptosis in the Drosophila retina. EMBO Rep. 2006, 7:933-939.
116. Metzler M., Gan L., Mazarei G., Graham R.K., Liu L., Bissada N., Lu G., Leavitt B.R., Hayden M.R. Phosphorylation of huntingtin at Ser421 in YAC128 neurons is associated with protection of YAC128 neurons from NMDA-mediated excitotoxicity and is modulated by PP1 and PP2A. J. Neurosci. 2010, 30:14318-14329.
117. Milnerwood A.J., Gladding C.M., Pouladi M.A., Kaufman A.M., Hines R.M., Boyd J.D., Ko R.W., Vasuta O.C., Graham R.K., Hayden M.R., et al. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
118. Mollereau B., Perez-Garijo A., Bergmann A., Miura M., Gerlitz O., Ryoo H.D., Steller H., Morata G. Compensatory proliferation and apoptosis-induced proliferation: a need for clarification. Cell Death Differ. 2013, 20:181.
119. Moody-Corbett F. Formation of the vertebrate neuromuscular junction. Dev. Biol. (N. Y.) 1986, 2:605-635.
120. Mukerjee N., McGinnis K.M., Park Y.H., Gnegy M.E., Wang K.K. Caspase-mediated proteolytic activation of calcineurin in thapsigargin-mediated apoptosis in SH-SY5Y neuroblastoma cells. Arch. Biochem. Biophys. 2000, 379:337-343.
121. Murray T.V., McMahon J.M., Howley B.A., Stanley A., Ritter T., Mohr A., Zwacka R., Fearnhead H.O. A non-apoptotic role for caspase-9 in muscle differentiation. J. Cell Sci. 2008, 121:3786-3793.
122. Nägerl U.V., Eberhorn N., Cambridge S.B., Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 2004, 44:759-767.
123. Nakamura T., Wang L., Wong C.C., Scott F.L., Eckelman B.P., Han X., Tzitzilonis C., Meng F., Gu Z., Holland E.A., et al. Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Mol. Cell 2010, 39:184-195.
124. Nakhaei P., Sun Q., Solis M., Mesplede T., Bonneil E., Paz S., Lin R., Hiscott J. IκB kinase ε-dependent phosphorylation and degradation of X-linked inhibitor of apoptosis sensitizes cells to virus-induced apoptosis. J. Virol. 2012, 86:726-737.
125. Nelson C.D., Kim M.J., Hsin H., Chen Y., Sheng M. Phosphorylation of threonine-19 of PSD-95 by GSK-3β is required for PSD-95 mobilization and long-term depression. J. Neurosci. 2013, 33:12122-12135.
126. Nguyen A.W., Daugherty P.S. Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 2005, 23:355-360.
127. Nicholls S.B., Chu J., Abbruzzese G., Tremblay K.D., Hardy J.A. Mechanism of a genetically encoded dark-to-bright reporter for caspase activity. J. Biol. Chem. 2011, 286:24977-24986.
128. Nikolaev A., McLaughlin T., O'Leary D.D., Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
129. O'Riordan M.X., Bauler L.D., Scott F.L., Duckett C.S. Inhibitor of apoptosis proteins in eukaryotic evolution and development: a model of thematic conservation. Dev. Cell 2008, 15:497-508.
130. Oh W.C., Hill T.C., Zito K. Synapse-specific and size-dependent mechanisms of spine structural plasticity accompanying synaptic weakening. Proc. Natl. Acad. Sci. USA 2013, 110:E305-E312.
131. Oh W.C., Parajuli L.K., Zito K. Heterosynaptic structural plasticity on local dendritic segments of hippocampal CA1 neurons. Cell Rep. 2015, 10:162-169.
132. Ohsawa S., Hamada S., Kuida K., Yoshida H., Igaki T., Miura M. Maturation of the olfactory sensory neurons by Apaf-1/caspase-9-mediated caspase activity. Proc. Natl. Acad. Sci. USA 2010, 107:13366-13371.
133. Okada H., Suh W.K., Jin J., Woo M., Du C., Elia A., Duncan G.S., Wakeham A., Itie A., Lowe S.W., et al. Generation and characterization of Smac/DIABLO-deficient mice. Mol. Cell. Biol. 2002, 22:3509-3517.
134. Olsen K.M., Sheng M. NMDA receptors and BAX are essential for Aβ impairment of LTP. Sci. Rep. 2012, 2:225.
135. Olsen O., Kallop D.Y., McLaughlin T., Huntwork-Rodriguez S., Wu Z., Duggan C.D., Simon D.J., Lu Y., Easley-Neal C., Takeda K., et al. Genetic analysis reveals that amyloid precursor protein and death receptor 6 function in the same pathway to control axonal pruning independent of β-secretase. J. Neurosci. 2014, 34:6438-6447.
136. Oshima K., Takeda M., Kuranaga E., Ueda R., Aigaki T., Miura M., Hayashi S. IKK epsilon regulates F actin assembly and interacts with Drosophila IAP1 in cellular morphogenesis. Curr. Biol. 2006, 16:1531-1537.
137. Öztürk G., Cengiz N., Erdoğan E., Him A., Oğuz E.K., Yenidünya E., Ayşit N. Two distinct types of dying back axonal degeneration in vitro. Neuropathol. Appl. Neurobiol. 2013, 39:362-376.
138. Peineau S., Bradley C., Taghibiglou C., Doherty A., Bortolotto Z.A., Wang Y.T., Collingridge G.L. The role of GSK-3 in synaptic plasticity. Br. J. Pharmacol. 2008, 153(Suppl 1):S428-S437.
139. Pellettieri J., Fitzgerald P., Watanabe S., Mancuso J., Green D.R., Sánchez Alvarado A. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 2010, 338:76-85.
140. Pinan-Lucarre B., Gabel C.V., Reina C.P., Hulme S.E., Shevkoplyas S.S., Slone R.D., Xue J., Qiao Y., Weisberg S., Roodhouse K., et al. The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS Biol. 2012, 10:e1001331.
141. Pouladi M.A., Graham R.K., Karasinska J.M., Xie Y., Santos R.D., Petersen A., Hayden M.R. Prevention of depressive behaviour in the YAC128 mouse model of Huntington disease by mutation at residue 586 of huntingtin. Brain 2009, 132:919-932.
142. Putcha G.V., Johnson E.M. Men are but worms: neuronal cell death in C elegans and vertebrates. Cell Death Differ. 2004, 11:38-48.
143. Raff M.C., Whitmore A.V., Finn J.T. Axonal self-destruction and neurodegeneration. Science 2002, 296:868-871.
144. Riedl S.J., Renatus M., Schwarzenbacher R., Zhou Q., Sun C., Fesik S.W., Liddington R.C., Salvesen G.S. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001, 104:791-800.
145. Rodriguez A., Oliver H., Zou H., Chen P., Wang X., Abrams J.M. Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat. Cell Biol. 1999, 1:272-279.
146. Rowan M.J., Klyubin I., Wang Q., Anwyl R. Synaptic plasticity disruption by amyloid beta protein: modulation by potential Alzheimer's disease modifying therapies. Biochem. Soc. Trans. 2005, 33:563-567.
147. Ryoo H.D., Bergmann A. The role of apoptosis-induced proliferation for regeneration and cancer. Cold Spring Harb. Perspect. Biol. 2012, 4:a008797.
148. Salvesen G.S., Duckett C.S. IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell Biol. 2002, 3:401-410.
149. Scanziani M., Malenka R.C., Nicoll R.A. Role of intercellular interactions in heterosynaptic long-term depression. Nature 1996, 380:446-450.
150. 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, 24:645-655.
151. 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, 275:6268-6280.
152. Sensi S.L., Paoletti P., Bush A.I., Sekler I. Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 2009, 10:780-791.
153. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842.
154. Shapiro P.J., Hsu H.H., Jung H., Robbins E.S., Ryoo H.D. Regulation of the Drosophila apoptosome through feedback inhibition. Nat. Cell Biol. 2008, 10:1440-1446.
155. 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, 11:519-527.
156. Simon D.J., Weimer R.M., McLaughlin T., Kallop D., Stanger K., Yang J., O'Leary D.D., Hannoush R.N., Tessier-Lavigne M. A caspase cascade regulating developmental axon degeneration. J. Neurosci. 2012, 32:17540-17553.
157. Sjakste N., Sjakste T. Possible involvement of DNA strand breaks in regulation of cell differentiation. Eur. J. Histochem. 2007, 51:81-94.
158. Srinivasula S.M., Gupta S., Datta P., Zhang Z., Hegde R., Cheong N., Fernandes-Alnemri T., Alnemri E.S. Inhibitor of apoptosis proteins are substrates for the mitochondrial serine protease Omi/HtrA2. J. Biol. Chem. 2003, 278:31469-31472.
159. Steller H. Regulation of apoptosis in Drosophila. Cell Death Differ. 2008, 15:1132-1138.
160. Suberbielle E., Sanchez P.E., Kravitz A.V., Wang X., Ho K., Eilertson K., Devidze N., Kreitzer A.C., Mucke L. Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-β. Nat. Neurosci. 2013, 16:613-621.
161. Sun C., Cai M., Gunasekera A.H., Meadows R.P., Wang H., Chen J., Zhang H., Wu W., Xu N., Ng S.C., Fesik S.W. NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature 1999, 401:818-822.
162. Sun C., Cai M., Meadows R.P., Xu N., Gunasekera A.H., Herrmann J., Wu J.C., Fesik S.W. NMR structure and mutagenesis of the third Bir domain of the inhibitor of apoptosis protein XIAP. J. Biol. Chem. 2000, 275:33777-33781.
163. Suzuki Y., Imai Y., Nakayama H., Takahashi K., Takio K., Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell 2001, 8:613-621.
164. Suzuki Y., Nakabayashi Y., Takahashi R. Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc. Natl. Acad. Sci. USA 2001, 98:8662-8667.
165. Suzuki A., Kusakai G., Kishimoto A., Shimojo Y., Miyamoto S., Ogura T., Ochiai A., Esumi H. Regulation of caspase-6 and FLIP by the AMPK family member ARK5. Oncogene 2004, 23:7067-7075.
166. Takemoto K., Nagai T., Miyawaki A., Miura M. Spatio-temporal activation of caspase revealed by indicator that is insensitive to environmental effects. J. Cell Biol. 2003, 160:235-243.
167. Tamayev R., D'Adamio L. Inhibition of γ-secretase worsens memory deficits in a genetically congruous mouse model of Danish dementia. Mol. Neurodegener. 2012, 7:19.
168. Tamayev R., Akpan N., Arancio O., Troy C.M., D'Adamio L. Caspase-9 mediates synaptic plasticity and memory deficits of Danish dementia knock-in mice: caspase-9 inhibition provides therapeutic protection. Mol. Neurodegener. 2012, 7:60.
169. Tamayev R., Matsuda S., Arancio O., D'Adamio L. β- but not γ-secretase proteolysis of APP causes synaptic and memory deficits in a mouse model of dementia. EMBO Mol. Med. 2012, 4:171-179.
170. Tenneti L., D'Emilia D.M., Lipton S.A. Suppression of neuronal apoptosis by S-nitrosylation of caspases. Neurosci. Lett. 1997, 236:139-142.
171. Thakor N., Holcik M. IRES-mediated translation of cellular messenger RNA operates in eIF2α- independent manner during stress. Nucleic Acids Res. 2012, 40:541-552.
172. Truman J.W. Metamorphosis of the central nervous system of Drosophila. J. Neurobiol. 1990, 21:1072-1084.
173. Tsang A.H., Lee Y.I., Ko H.S., Savitt J.M., Pletnikova O., Troncoso J.C., Dawson V.L., Dawson T.M., Chung K.K. S-nitrosylation of XIAP compromises neuronal survival in Parkinson's disease. Proc. Natl. Acad. Sci. USA 2009, 106:4900-4905.
174. Unsain N., Higgins J.M., Parker K.N., Johnstone A.D., Barker P.A. XIAP regulates caspase activity in degenerating axons. Cell Rep. 2013, 4:751-763.
175. Unsain N., Heard K.N., Higgins J.M., Barker P.A. Production and isolation of axons from sensory neurons for biochemical analysis using porous filters. J. Vis. Exp. 2014, Published online July 8, 2014. 10.3791/51795.
176. Vaux D.L., Silke J. IAPs, RINGs and ubiquitylation. Nat. Rev. Mol. Cell Biol. 2005, 6:287-297.
177. Velázquez-Delgado E.M., Hardy J.A. Phosphorylation regulates assembly of the caspase-6 substrate-binding groove. Structure 2012, 20:742-751.
178. Velázquez-Delgado E.M., Hardy J.A. Zinc-mediated allosteric inhibition of caspase-6. J. Biol. Chem. 2012, 287:36000-36011.
179. Verma P., Chierzi S., Codd A.M., Campbell D.S., Meyer R.L., Holt C.E., Fawcett J.W. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 2005, 25:331-342.
180. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., Richardson E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 1985, 44:559-577.
181. Wang H.G., Pathan N., Ethell I.M., Krajewski S., Yamaguchi Y., Shibasaki F., McKeon F., Bobo T., Franke T.F., Reed J.C. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999, 284:339-343.
182. Wang J.Y., Chen F., Fu X.Q., Ding C.S., Zhou L., Zhang X.H., Luo Z.G. Caspase-3 cleavage of dishevelled induces elimination of postsynaptic structures. Dev. Cell 2014, 28:670-684.
183. Westphal D., Sytnyk V., Schachner M., Leshchyns'ka I. Clustering of the neural cell adhesion molecule (NCAM) at the neuronal cell surface induces caspase-8- and -3-dependent changes of the spectrin meshwork required for NCAM-mediated neurite outgrowth. J. Biol. Chem. 2010, 285:42046-42057.
184. Westphal D., Kluck R.M., Dewson G. Building blocks of the apoptotic pore: how Bax and Bak are activated and oligomerize during apoptosis. Cell Death Differ. 2014, 21:196-205.
185. Williams D.W., Kondo S., Krzyzanowska A., Hiromi Y., Truman J.W. Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 2006, 9:1234-1236.
186. Wilson R., Goyal L., Ditzel M., Zachariou A., Baker D.A., Agapite J., Steller H., Meier P. The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat. Cell Biol. 2002, 4:445-450.
187. Wong B.K., Ehrnhoefer D.E., Graham R.K., Martin D.D., Ladha S., Uribe V., Stanek L.M., Franciosi S., Qiu X., Deng Y., et al. Partial rescue of some features of Huntington Disease in the genetic absence of caspase-6 in YAC128 mice. Neurobiol. Dis. 2015, 76:24-36.
188. Wu H.Y., Hudry E., Hashimoto T., Kuchibhotla K., Rozkalne A., Fan Z., Spires-Jones T., Xie H., Arbel-Ornath M., Grosskreutz C.L., et al. Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. J. Neurosci. 2010, 30:2636-2649.
189. Wu H.Y., Hudry E., Hashimoto T., Uemura K., Fan Z.Y., Berezovska O., Grosskreutz C.L., Bacskai B.J., Hyman B.T. Distinct dendritic spine and nuclear phases of calcineurin activation after exposure to amyloid-β revealed by a novel fluorescence resonance energy transfer assay. J. Neurosci. 2012, 32:5298-5309.
190. Xu X., Gerard A.L., Huang B.C., Anderson D.C., Payan D.G., Luo Y. Detection of programmed cell death using fluorescence energy transfer. Nucleic Acids Res. 1998, 26:2034-2035.
191. Yamaguchi Y., Shinotsuka N., Nonomura K., Takemoto K., Kuida K., Yosida H., Miura M. Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure. J. Cell Biol. 2011, 195:1047-1060.
192. Yamamoto-Tanaka M., Makino T., Motoyama A., Miyai M., Tsuboi R., Hibino T. Multiple pathways are involved in DNA degradation during keratinocyte terminal differentiation. Cell Death Dis. 2014, 5:e1181.
193. Yan N., Wu J.W., Chai J., Li W., Shi Y. Molecular mechanisms of DrICE inhibition by DIAP1 and removal of inhibition by Reaper, Hid and Grim. Nat. Struct. Mol. Biol. 2004, 11:420-428.
194. Yang Q.H., Du C. Smac/DIABLO selectively reduces the levels of c-IAP1 and c-IAP2 but not that of XIAP and livin in HeLa cells. J. Biol. Chem. 2004, 279:16963-16970.
195. Yang Y., Fang S., Jensen J.P., Weissman A.M., Ashwell J.D. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 2000, 288:874-877.
196. Yang Q.H., Church-Hajduk R., Ren J., Newton M.L., Du C. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev. 2003, 17:1487-1496.
197. Yuan J., Shaham S., Ledoux S., Ellis H.M., Horvitz H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993, 75:641-652.
198. Zhao W.Q., Santini F., Breese R., Ross D., Zhang X.D., Stone D.J., Ferrer M., Townsend M., Wolfe A.L., Seager M.A., et al. Inhibition of calcineurin-mediated endocytosis and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors prevents amyloid beta oligomer-induced synaptic disruption. J. Biol. Chem. 2010, 285:7619-7632.
199. Zheng T.S., Hunot S., Kuida K., Flavell R.A. Caspase knockouts: matters of life and death. Cell Death Differ. 1999, 6:1043-1053.
200. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44:749-757.
201. Zhou F., Xing D., Wu S., Chen W.R. Intravital imaging of tumor apoptosis with FRET probes during tumor therapy. Mol. Imaging Biol. 2010, 12:63-70.