Caspases and their role in inflammation and ischemic neuronal death. Focus on caspase-12

Apoptosis

Volumn 21, Issue 7, 2016, Pages 763-777

  García de la Cadena, Selene ^a   Massieu, Lourdes ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Apoptosis; Caspase 12; Caspase 4; Caspases; Cerebral ischemia; ER stress; Inflammation

Indexed keywords

APOPTOSOME; CASPASE; CASPASE 11; CASPASE 12; CASPASE 2; CASPASE 3; CASPASE 4; CASPASE 5; CASPASE 7; CASPASE 8; CASPASE 9; EFFECTOR CASPASE; GLUCOSE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; OXYGEN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

APOPTOSIS; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; CALCIUM CELL LEVEL; ENDOPLASMIC RETICULUM STRESS; HUMAN; HYPOXIA; INFLAMMATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PYROPTOSIS; REVIEW; SEPSIS; UPREGULATION; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; IMMUNOLOGY; NERVE CELL; PATHOPHYSIOLOGY;

ANIMALS; APOPTOSIS; BRAIN ISCHEMIA; CASPASE 12; CASPASES; HUMANS; INFLAMMATION; NEURONS;

EID: 84965049977     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-016-1247-0     Document Type: Review

References (127)

1. Parrish AB, Freel CD, Kornbluth S (2013) Cellular mechanisms controlling caspase activation and function. Cold Spring Harb Perspect Biol 5:1–24
2. Chowdhury I, Tharakan B, Bhat GK (2008) Caspases—an update. Comp Biochem Physiol B 151:10–27
3. Shalini S, Dorstyn L, Dawar S, Kumar S (2014) Old, new and emerging functions of caspases. Cell Death Differ 21:1–14
4. Lamkanfi M, Dixit VM (2014) Mechanisms and functions of inflammasomes. Cell 157:1013–1022
5. Park HH (2012) Structural features of caspase-activating complexes. Int J Mol Sci 13:4807–4818
6. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281:1312–1316
7. Mcllwain DR, Berger T, Mak TW (2013) Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 5:1–28
8. Creagh EM (2014) Caspase crosstalk: integration of apoptotic and innate immune signalling pathways. Trends Immunol 35:631–640
9. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1–16
10. Wang ZB, Liu YQ, Cui YF (2005) Pathways to caspase activation. Cell Biol Int 29:489–496
11. Hermel E, Klapstein K (2011) A possible mechanism for maintenance of the deleterious allele of human caspase-12. Med Hypotheses 77:803–806
12. Denault JB, Salvesen GS (2002) Caspases: keys in the ignition of cell death. Chem Rev 102:4489–4499
13. Park HH, Wu H (2006) Crystal structure of RAIDD death domain implicates potential mechanism of PIDDosome assembly. J Mol Biol 357:358–364
14. Kersse T, Vanden Berghe T, Lamkanfi M, Vandenabeele P (2007) A phylogenetic and functional overview of inflammatory caspases and caspase-1-related CARD-only proteins. Biochem Soc Trans 35:1508–1511
15. Sollberger G, Strittmatter GE, Kistowska M, French LE, Beer HD (2012) Caspase-4 is required for activation of inflammasomes. J Immunol 188:1992–2000
16. Kersse K, Vandenabeele P (2013) Caspase-12. In: Rawlings ND, Salvesen GS (eds) Handbook of proteolytic enzymes, 3rd edn. Academic Press, Oxford, pp 2274–2280
17. Jiménez D, Lamkanfi M (2015) Inflammatory caspases: key regulators of inflammation and cell death. Biol Chem 396:193–203
18. Schroder K, Tschopp J (2010) The inflammasomes. Cell 140:821–832
19. Chavarría-Smith J, Vance R (2014) The NLRP1 inflammasomes. Immunol Rev 265:22–34
20. Casson CN, Copenhaver AM, Zwack EE, Nguyen HT, Strowig T, Javdan B, Bradley WP, Fung TC, Flavell RA, Brodsky IE, Shin S (2013) Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog 9:1–16
21. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszynski A, Forsberg LS, Carlson RW, Dixit VM (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341:1246–1249
22. Shi J, Zhao Y, Wang Y, Gao W, Ding J, Li P, Hu L, Shao F (2014) Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514:187–192
23. Casson CN, Yu J, Reyes VM, Taschuk FO, Yadav A, Copenhaver AM, Nguyen HT, Collman RG, Shin S (2015) Human caspase-4 mediates noncanonical inflammasome activation against gram-negative bacterial pathogens. Proc Natl Acad Sci USA 112:6688–6693
24. Knodler LA, Crowley SM, Sham HP, Yang H, Wrande M, Ma C, Ernst RK, Steele-Mortimer O, Celli J, Vallance BA (2014) Non-canonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16:249–256
25. Baker PJ, Boucher D, Bierschenk D, Tebartz C, Whitney PG, D’Silva DB, Tanzer MC, Monteleone M, Robertson AA, Cooper MA, Alvarez-Diaz S, Herold MJ, Bedoui S, Schroder K, Masters SL (2015) NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. Eur J Immunol 45:2918–2926
26. Schmid-Burgk JL, Gaidt MM, Schmidt T, Ebert TS, Bartok E, Hornung V (2015) Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. Eur J Immunol 45:2911–2917
27. Kajiwara Y, Schiff T, Voloudakis G, Gama Sosa MA, Elder G, Bozdagi O, Buxbaum JD (2014) A critical role for human caspase-4 in endotoxin sensitivity. J Immunol 193:335–343
28. Lakshmanan U, Porter AG (2007) Caspase-4 interacts with TNF receptor-associated factor 6 and mediates lipopolysaccharide-induced NF-κB-dependent production of IL-8 and CC chemokine ligand 4 (macrophage-inflammatory protein-1β). J Immunol 179:8480–8490
29. Sanders MG, Parsons MJ, Howard AG, Liu J, Fassio SR, Martinez JA, Bouchier-Hayes L (2015) Single-cell imaging of inflammatory caspase dimerization reveals differential recruitment to inflammasomes. Cell Death Dis 6:1–11
30. Gringhuis S, Kaptein TM, Wevers BA, Theelen B, Van der Vlist M, Boekhout T, Geijtenbeek TBH (2012) Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1β via a noncanonical caspase-8 inflammasome. Nat Immunol 13:246–255
31. Philip NH, Dillon CP, Snyder AG, Fitzgerald P, Wynosky-Dolfi MA, Zwack EE, Hu B, Fitzgerald L, Mauldin EA, Copenhaver AM, Shin S, Wei L, Parker M, Zhang J, Oberst A, Green DR, Brodsky IE (2014) Caspase-8 mediates caspase-1 processing and innate immune defense in response to bacterial blockade of NF-κB and MAPK signaling. Proc Natl Acad Sci USA 111:7385–7390
32. Gurung P, Anand PK, Malireddi RK, Vande Walle L, Van Opdenbosch N, Dillon CP, Weinlich R, Green DR, Lamkanfi M, Kanneganti TD (2014) FADD and caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes. J Immunol 192:1835–1846
33. Fann DYW, Lee SY, Manzanero S, Chunduri P, Sobey C, Arumugam T (2013) Pathogenesis of acute stroke and the role of inflammasomes. Ageing Res Rev 12:941–966
34. Hotchkiss RS, Nicholson DW (2006) Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol 6:813–822
35. Kayagaki N, Stowe IB, Lee BL, O’Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX, Fitzgerald L, Zhang Y, Bertram EM, Goodnow CC, Dixit VM (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signaling. Nature 526:666–671
36. Nadiri A, Wolinski MK, Saleh M (2006) The inflammatory caspases: key players in the host response to pathogenic invasion and sepsis. J Immunol 77:4239–4245
37. Martinon F, Tschopp J (2007) Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 14:10–22
38. Scott AM, Saleh M (2007) The inflammatory caspases: guardians against infections and sepsis. Cell Death Differ 14:23–31
39. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J (2000) Caspase-12 mediates endoplasmic reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 403:98–103
40. Kalai M, Lamkanfi M, Denecker G, Boogmans M, Lippens S, Meeus A, Declercq W, Vandenabeele P (2003) Regulation of the expression and processing of caspase-12. J Cell Biol 162:457–467
41. Kachapati K, O’brien TR, Bergeron J, Zhang M, Dean M (2006) Population distribution of the functional caspase-12 allele. Hum Mutat 27:975–980
42. Fischer H, Koenig U, Eckhart L, Tschachler E (2002) Human caspase 12 has acquired deleterious mutations. Biochem Biophys Res Commun 293:722–726
43. Saleh M, Mathison JC, Wolinski MK, Bensinger SJ, Fitzgerald P, Droin N, Ulevitch RJ, Green DR, Nicholson DW (2006) Enhanced bacterial clearance and sepsis resistance in caspase-12-deficient mice. Nature 440:1064–1068
44. Xue Y, Daly A, Yngvadottir B, Liu M, Coop G, Kim Y, Sabeti P, Chen Y, Stalker J, Huckle E, Burton J, Leonard S, Rogers J, Tyler-Smith C (2006) Spread of an inactive form of caspase-12 in humans is due to recent positive selection. Am J Hum Genet 78:659–670
45. Saleh M, Vaillancourt JP, Graham RK, Huyck M, Srinivasula SM, Alnemri ES, Steinberg MH, Nolan V, Baldwin CT, Hotchkiss RS, Buchman TG, Zehnbauer BA, Hayden MR, Farrer LA, Roy S, Nicholson DW (2004) Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 429:75–79
46. Rosentul D, Plantinga T, Scott W, Alexander B, Van de Geer N, Perfect J, Kullberg B, Johnson M, Netea M (2012) The impact of caspase-12 on susceptibility to candidemia. Eur J Clin Microbiol Infect Dis 31:277–280
47. Roy S, Sharom JR, Houde C, Loisel TP, Vaillancourt JP, Shao W, Saleh M, Nicholson DW (2008) Confinement of caspase-12 proteolytic activity to autoprocessing. Proc Natl Acad Sci USA 105:4133–4138
48. LeBlanc PM, Yeretssian G, Rutherford N, Doiron K, Nadiri A, Zhu L, Green DR, Gruenheid S, Saleh M (2008) Caspase-12 modulates NOD signaling and regulates antimicrobial peptide production and mucosal immunity. Cell Host Microbe 3:146–157
49. Labbé K, Miu J, Yeretssian G, Serghides L, Tam M, Finney C, Erdman L, Goulet ML, Kain K, Stevenson M, Saleh M (2010) Caspase-12 dampens the immune response to malaria independently of the inflammasome by targeting NF-κB signaling. J Immunol 185:5495–5502
50. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, Zhang J, Lee WP, Roose-Girma M, Dixit VM (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479:117–121
51. Galluzzi López-Soto A, Kumar S, Kroemer G (2016) Caspases connect cell-death signaling to organismal homeostasis. Immunity 44:221–231
52. Wang P, Arjona A, Zhang Y, Sultana H, Dai J, Yang L, LeBlanc PM, Doiron K, Saleh M, Fikrig E (2010) Caspase-12 controls West Nile virus infection via the viral RNA receptor RIG-I. Nat Immunol 11:912–919
53. Skeldon AM, Morizot A, Douglas T, Santoro N, Kursawe R, Kozlitina J, Caprio S, Mehal WZ, Saleh M (2016) Caspase-12, but not caspase-11, inhibits obesity and insulin resistance. J Immunol 196:437–447
54. Trendelenburg G (2014) Molecular regulation of cell fate in cerebral ischemia: role of the inflammasome and connected pathways. J Cereb Blood Flow Metab 34:1857–1867
55. Guo H, Callaway JB, Ting JP (2015) Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 21:677–687
56. Peng S, Kuang Z, Zhang Y, Xu H, Cheng Q (2011) The protective effects and potential mechanism of calpain inhibitor calpeptin against focal cerebral ischemia–reperfusion injury in rats. Mol Biol Rep 38:905–912
57. Espinosa-García C, Vigueras-Villaseñor RM, Rojas-Castañeda JC, Aguilar-Hernández A, Monfil T, Cervantes M, Moralí G (2013) Post-ischemic administration of progesterone reduces caspase-3 activation and DNA fragmentation in the hippocampus following global cerebral ischemia. Neurosci Lett 550:98–103
58. Wen XR, Fu YY, Liu HZ, Wu J, Shao XP, Zhang XB, Tang M, Shi Y, Ma K, Zhang F, Wang YW, Tang H, Han D, Zhang P, Wang SL, Xu Z, Song YJ (2015) Neuroprotection of sevoflurane against ischemia/reperfusion-induced brain injury through inhibiting JNK3/Caspase-3 by enhancing Akt signaling pathway. Mol Neurobiol 51:1–11
59. Benchoua A, Couriaud C, Guégan C, Tartier L, Couvert P, Friocourt G, Chelly J, Ménissier-de Murcia J, Onténiente B (2002) Active caspase-8 translocates into the nucleus of apoptotic cells to inactivate poly(ADP-ribose) polymerase-2. J Biol Chem 277:34217–34222
60. Shabanzadeh AP, D’Onofrio PM, Monnier PP, Koeberle PD (2015) Targeting caspase-6 and caspase-8 to promote neuronal survival following ischemic stroke. Cell Death Dis 6:1–13
61. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391–397
62. Leker RR, Shohami E (2002) Cerebral ischemia and trauma-different etiologies yet similar mechanisms: neuroprotective opportunities Brain. Res Rev 39:55–73
63. Bramlett H, Dietrich WD (2004) Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J Cereb Blood Flow Metab 24:133–150
64. Fann DYW, Lee SY, Manzanero S, Tang SC, Gelderblom M, Chunduri P, Bernreuther C, Glatzel M, Cheng YL, Thundyil J, Widiapradja A, Lok KZ, Foo SL, Wang YC, Li YI, Drummond GR, Basta M, Magnus T, Jo DG, Mattson MP, Sobey SG, Arumugam TV (2013) Intravenous immunoglobulin suppresses NLRP1 and NLRP3 inflammasome-mediated neuronal death in ischemic stroke. Cell Death Dis 4:1–10
65. Fann DYW, Santro T, Manzanero S, Widiapradja A, Cheng YL, Lee SY, Chunduri P, Jo DG, Stranahand AM, Mattson MP, Arumugam TV (2014) Intermittent fasting attenuates inflammasome activity in ischemic stroke. Exp Neurol 257:114–119
66. Yang F, Wang Z, Wei X, Han H, Meng X, Zhang Y, Shi W, Li F, Xin T, Pang Q, Yi F (2014) NLRP3 deficiency ameliorates neurovascular damage in experimental ischemic stroke. J Cereb Blood Flow Metab 34:660–667
67. Zhang WH, Wang X, Narayanan M, Zhang Y, Huo C, Reed JC, Friedlander RM (2003) Fundamental role of the Rip2/caspase-1 pathway in hypoxia and ischemia-induced neuronal cell death. Proc Natl Acad Sci USA 100:16012–16017
68. Mergenthaler P, Ulrich D, Meisel A (2004) Pathophysiology of stroke: lessons from animal models. Metab Brain Dis 19:151–167
69. Schielke GP, Yang GY, Shivers BD, Betz AL (1998) Reduced ischemic brain injury in interleukin-lβ converting enzyme-deficient mice. J Cereb Blood Flow Metab 18:180–185
70. Ross J, Brough D, Gibson RM, Loddick SA, Rothwell NJ (2007) A selective, non-peptide caspase-1 inhibitor, VRT-018858, markedly reduces brain damage induced by transient ischemia in the rat. Neuropharmacology 53:638–642
71. Aoyama K, Burns DM, Suh SW, Garnier P, Matsumori Y, Shiina H, Swanson RA (2005) Acidosis causes endoplasmic reticulum stress and caspase-12-mediated astrocyte death. J Cereb Blood Flow Metab 25:358–370
72. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381–389
73. Chen L, Gao X (2002) Neuronal apoptosis induced by endoplasmic reticulum stress. Neurochem Res 27:891–898
74. Cao SS, Kaufman RJ (2012) Unfolded protein response. Curr Biol 22:622–626
75. Schröder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569:29–63
76. Wang S, Kaufman RJ (2012) The impact of the unfolded protein response on human disease. J Cell Biol 197:857–867
77. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinasa. Nature 397:271–274
78. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5:897–904
79. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619–633
80. Zinszner H, Kuroda M, Wang XZ, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982–995
81. McCullough KD, Martindale JL, Klotz L, Aw T, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249–1259
82. Reimertz C, Kögel D, Rami A, Chittenden T, Prehn JHM (2003) Gene expression during ER stress–induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 162:587–597
83. Logue SE, Cleary P, Saveljeva S, Samali A (2013) New directions in ER stress-induced cell death. Apoptosis 18:537–546
84. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P (2013) Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5:1–15
85. Ye J, Rawson RB, Komuro R, Chen X, Davé UP, Prywes R, Brown MS, Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355–1364
86. Shen J, Prywes R (2005) ER stress signaling by regulated proteolysis of ATF6. Methods 35:382–389
87. Chakrabarti A, Chen AW, Varner JD (2011) A review of the mammalian unfolded protein response. Biotechnol Bioeng 108:2777–2793
88. Carrara M, Prischi F, Ali MU (2013) UPR signal activation by luminal sensor domains. Int J Mol Sci 14:6454–6466
89. Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89–102
90. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891
91. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92–96
92. Lee K, Tirasophon W, Shen X (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 16:452–466
93. Parmar VM, Schröder M (2012) Sensing endoplasmic reticulum stress. Adv Exp Med Biol 738:153–168
94. Yk Oh, Shin KS, Yuan J, Kang SJ (2008) Superoxide dismutase 1 mutants related to amyotrophic lateral sclerosis induce endoplasmic stress in neuro2a cells. J Neurochem 104:993–1005
95. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M (2001) Activation of Caspase-12, an endoplasmic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 276:13935–13940
96. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y (2002) An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 277:34287–34294
97. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE, Ellerby HM (2002) Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 277:21836–21842
98. Fujita E, Kouroku Y, Jimbo A, Isoai A, Maruyama K, Momoi T (2002) Caspase-12 processing and fragment translocation into nuclei of tunicamycin-treated cells. Cell Death Differ 9:1108–1114
99. Nakagawa T, Yuan J (2000) Cross-talk between two cysteine protease families: activation of caspase-12 by calpain in apoptosis. J Cell Biol 150:887–894
100. de la Cadena SG, Hernández-Fonseca K, Camacho-Arroyo I, Massieu L (2014) Glucose deprivation induces reticulum stress by the PERK pathway and caspase-7- and calpain-mediated caspase-12 activation. Apoptosis 19:414–427
101. Martinez JA, Zhang Z, Svetlov SI, Hayes RL, Wang KK, Larner SF (2010) Calpain and caspase processing of caspase-12 contribute to the ER stress-induced cell death pathway in differentiated PC12 cells. Apoptosis 15:1480–1493
102. Rao RV, Hermel E, Castro-Obregon S, Del Rio G, Ellerby LM, Ellerby HM, Bredesen DE (2001) Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 276:33869–33874
103. Heath-Engel HM, Chang NC, Shore GC (2008) The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene 27:6419–6433
104. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS (2003) Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors. J Biol Chem 278:20915–20924
105. Kikuchi S, Shinpo K, Tsuji S, Yabe I, Niino M, Tashiro K (2003) Brefeldin A-induced neurotoxicity in cultured spinal cord neurons. J Neurosci Res 71:591–599
106. Obeng EA, Boise LH (2005) Caspase-12 and caspase-4 are not required for caspase-dependent endoplasmic reticulum stress-induced apoptosis. J Biol Chem 280:29578–29587
107. Di Sano F, Ferraro E, Tufi R, Achsel T, Piacentini M, Cecconi F (2006) Endoplasmic reticulum stress induces apoptosis by an apoptosome-dependent but caspase 12-independent mechanism. J Biol Chem 281:2693–2700
108. 2+ homeostasis under the ER stress. Neurochem Int 56:352–356
109. Yukioka F, Matsuzaki S, Kawamoto K, Koyama Y, Hitomi J, Katayama T, Tohyama M (2008) Presenilin-1 mutation activates the signaling pathway of caspase-4 in endoplasmic reticulum stress-induced apoptosis. Neurochem Int 52:683–687
110. Hitomi J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, Koyama Y, Manabe T, Yamagishi S, Bando Y, Imaizumi K, Tsujimoto Y, Tohyama M (2004) Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Aβ-induced cell death. J Cell Biol 165:347–356
111. Binet F, Chiasson S, Girard D (2010) Evidence that endoplasmic reticulum (ER) stress and caspase-4 activation occur in human neutrophils. Biochem Biophys Res Commun 391:18–23
112. Bian ZM, Elner SG, Elner VM (2009) Dual involvement of caspase-4 in inflammatory and ER stress-induced apoptotic responses in human retinal pigment epithelial cells. Investig Ophthalmol Vis Sci 50:6006–6014
113. Mouw G, Zechel JL, Gamboa J, Lust WD, Selman WR, Ratcheson RA (2003) Activation of caspase-12, an endoplasmic reticulum resident caspase, after permanent focal ischemia in rat. Neuroreport 14:183–186
114. Nakka VP, Gusain A, Raghubir R (2010) Endoplasmic reticulum stress plays critical role in brain damage after cerebral ischemia/reperfusion in rats. Neurotox Res 17:189–202
115. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J (2005) A Selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science 307:935–939
116. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, Belluardo N, Lindholm D, Korhonen L (2007) Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci 27:901–908
117. Shibata M, Hattori H, Sasaki T, Gotoh J, Hamada J, Fukuuchi Y (2003) Activation of caspase-12 by endoplasmic reticulum stress induced by transient middle cerebral artery occlusion in mice. Neuroscience 118:491–499
118. Liu HJ, Yang JP, Wang CH, Liu RC, Li Y, Li CY (2009) Endoplasmic reticulum in the penumbra following middle cerebral artery occlusion in the rabbit. Neurol Sci 30:227–232
119. Zhu H, Zhu H, Xiao S, Sun H, Xie C, Ma Y (2012) Activation and crosstalk between the endoplasmic reticulum road and JNK pathway in ischemia-reperfusion brain injury. Acta Neurochir 154:1197–1203
120. Larner SF, Hayes RL, McKinsey DM, Pike BR, Wang KKW (2004) Increased expression and processing of caspase-12 after traumatic brain injury in rats. J Neurochem 88:78–90
121. Badiola N, Penas C, Miñano-Molina A, Barneda-Zahonero B, Fadó R, Sánchez-Opazo G, Comella JX, Sabriá J, Zhu C, Blomgren K, Casas C, Rodríguez-Alvarez J (2011) Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12. Cell Death Dis 2:1–8
122. − cotransporter. J Neurochem 106:1563–1576
123. Zhang A, Zhang J, Sun P, Yao C, Su C, Sui T, Huang H, Cao X, Ge Y (2010) EIF2α and caspase-12 activation are involved in oxygen–glucose–serum deprivation/restoration-induced apoptosis of spinal cord astrocytes. Neurosci Lett 478:32–36
124. D’Osualdo AD, Anania VG, Yu K, Lill JR, Kaufman RJ, Matsuzawa S, Reed JC (2015) Transcription factor ATF4 induces NLRP1 inflammasome expression during endoplasmic reticulum stress. PLoS One 10:1–16
125. Lerner AG, Upton JP, Praveen PV, Ghosh R, Nakagawa Y, Igbaria A, Shen S, Nguyen V, Backes BJ, Heiman M, Heintz N, Greengard P, Hui S, Tang Q, Trusina A, Oakes SA, Papa FR (2012) IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab 16:250–264
126. Bronner DN, Abuaita BH, Chen X, Fitzgerald KA, Nuñez G, He Y, Yin XM, O’Riordan MX (2015) Endoplasmic reticulum stress activates the inflammasome via NLRP3-and caspase-2-driven mitochondrial damage. Immunity 43:451–462
127. Lu M, Sun XL, Qiao C, Liu Y, Ding JH, Hu G (2014) Uncoupling protein 2 deficiency aggravates astrocytic endoplasmic reticulum stress and nod-like receptor protein 3 inflammasome activation. Neurobiol Aging 35:421–430