Reduced IRE1 mediates apoptotic cell death by disrupting calcium homeostasis via the InsP3 receptor

Cell Death and Disease

Volumn 5, Issue 4, 2014, Pages

  Son, S M ^a   Byun, J ^a   Roh, S E ^a   Kim, S J ^a   Mook Jung, I ^a  

^a Seoul National University College of Medicine   (South Korea)

Author keywords

Cell death; InsP3R; IRE1 ; Mitochondrial dysfunction

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PROTEIN IRE1; PROTEIN IRE1ALPHA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; CALCIUM; CALCIUM BINDING PROTEIN; CIB1 PROTEIN, HUMAN; ERN1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL DEATH; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; BIOLOGICAL MODEL; ENDOPLASMIC RETICULUM; GENE SILENCING; HOMEOSTASIS; INTRACELLULAR SPACE; METABOLISM; MITOCHONDRION; ULTRASTRUCTURE; UPREGULATION;

APOPTOSIS; CALCIUM; CALCIUM-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; GENE KNOCKDOWN TECHNIQUES; HOMEOSTASIS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INTRACELLULAR SPACE; MAP KINASE KINASE KINASE 5; MITOCHONDRIA; MODELS, BIOLOGICAL; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; UP-REGULATION;

EID: 84901022639     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.129     Document Type: Article

References (56)

1. Meldolesi J, Pozzan T. The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem Sci 1998; 23: 10-14.
2. Ma Y, Hendershot LM. The unfolding tale of the unfolded protein response. Cell 2001; 107: 827-830.
3. Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J Clin Invest 2002; 110: 1389-1398.
4. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529.
5. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74: 739-789.
6. Shamu CE, Walter P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J 1996; 15: 3028-3039.
7. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001; 107: 881-891.
8. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000; 287: 664-666.
9. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002; 16: 1345-1355.
10. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999; 397: 271-274.
11. Rutkowski DT, Kaufman RJ. All roads lead to ATF4. Dev Cell 2003; 4: 442-444.
12. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 2000; 6: 1355-1364.
13. Carafoli E. Calcium signaling: a tale for all seasons. Proc Natl Acad Sci USA 2002; 99: 1115-1122.
14. Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 2006; 8: 1391-1418.
15. Bezprozvanny I. The inositol 1,4,5-trisphosphate receptors. Cell Calcium 2005; 38: 261-272.
16. Rossi D, Sorrentino V. Molecular genetics of ryanodine receptors Ca2+-release channels. Cell Calcium 2002; 32: 307-319.
17. East JM. Sarco(endo)plasmic reticulum calcium pumps: recent advances in our understanding of structure/function and biology (review). Mol Membr Biol 2000; 17: 189-200.
18. Squier MK, Sehnert AJ, Sellins KS, Malkinson AM, Takano E, Cohen JJ. Calpain and calpastatin regulate neutrophil apoptosis. J Cell Physiol 1999; 178: 311-319.
19. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F et al. Ca2+ -induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999; 284: 339-343.
20. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403: 98-103.
21. Kim I, XuW, Reed JC. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008; 7: 1013-1030.
22. Hennigs JK, Burhenne N, Stahler F, Winnig M, Walter B, Meyerhof W et al. Sweet taste receptor interacting protein CIB1 is a general inhibitor of InsP3-dependent Ca2+ release in vivo. J Neurochem 2008; 106: 2249-2262.
23. Rao RV, Hermel E, Castro-Obregon S, del Rio G, Ellerby LM, Ellerby HM et al. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 2001; 276: 33869-33874.
24. Tirasophon W, Welihinda AA, Kaufman RJ. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/ endoribonuclease (Ire1p) in mammalian cells. Genes Dev 1998; 12: 1812-1824.
25. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004; 11: 381-389.
26. Cox JS, Shamu CE, Walter P. Transcriptional induction of genes encoding endoplasmic reticulumresident proteins requires a transmembrane protein kinase. Cell 1993; 73: 1197-1206.
27. Bommiasamy H, Back SH, Fagone P, Lee K, Meshinchi S, Vink E et al. ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum. J Cell Sci 2009; 122(Pt 10): 1626-1636.
28. Pineau L, Colas J, Dupont S, Beney L, Fleurat-Lessard P, Berjeaud JM et al. Lipid-induced ER stress: synergistic effects of sterols and saturated fatty acids. Traffic 2009; 10: 673-690.
29. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE et al. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology 2002; 36: 592-601.
30. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH. Gene expression during ER stressinduced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 2003; 162: 587-597.
31. Thastrup O. Role of Ca2(+)-ATPases in regulation of cellular Ca2+ signalling, as studied with the selective microsomal Ca2(+)-ATPase inhibitor, thapsigargin. Agents Actions 1990; 29: 8-15.
32. Berridge MJ. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002; 32: 235-249.
33. Supattapone S, Worley PF, Baraban JM, Snyder SH. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem 1988; 263: 1530-1534.
34. Ellisman MH, Deerinck TJ, Ouyang Y, Beck CF, Tanksley SJ, Walton PD et al. Identification and localization of ryanodine binding proteins in the avian central nervous system. Neuron 1990; 5: 135-146.
35. Gunteski-Hamblin AM, Greeb J, Shull GE. A novel Ca2+ pump expressed in brain, kidney, and stomach is encoded by an alternative transcript of the slow-twitch muscle sarcoplasmic reticulum Ca-ATPase gene. Identification of cDNAs encoding Ca2+ and other cation-transporting ATPases using an oligonucleotide probe derived from the ATP-binding site. J Biol Chem 1988; 263: 15032-15040.
36. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 1999; 144: 281-292.
37. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998; 281: 1312-1316.
38. Sadowski-Debbing K, Coy JF, Mier W, Hug H, Los M. Caspases-their role in apoptosis and other physiological processes as revealed by knock-out studies. Arch Immunol Ther Exp (Warsz) 2002; 50: 19-34.
39. Gafni J, Munsch JA, Lam TH, Catlin MC, Costa LG, Molinski TF et al. Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron 1997; 19: 723-733.
40. Han D, Upton JP, Hagen A, Callahan J, Oakes SA, Papa FR. A kinase inhibitor activates the IRE1alpha RNase to confer cytoprotection against ER stress. Biochem Biophys Res Commun 2008; 365: 777-783.
41. Yoon KW, Cho JH, Lee JK, Kang YH, Chae JS, Kim YM et al. CIB1 functions as a Ca(2+)- sensitive modulator of stress-induced signaling by targeting ASK1. Proc Natl Acad Sci USA 2009; 106: 17389-17394.
42. Szalai G, Krishnamurthy R, Hajnoczky G. Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 1999; 18: 6349-6361.
43. Hajnoczky G, Csordas G, Das S, Garcia-Perez C, Saotome M, Sinha Roy S et al. Mitochondrial calcium signalling and cell death: approaches for assessing the role of mitochondrial Ca2+ uptake in apoptosis. Cell Calcium 2006; 40: 553-560.
44. Lee I, Bender E, Kadenbach B. Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. Mol Cell Biochem 2002; 234-235: 63-70.
45. Hansson MJ, Mansson R, Mattiasson G, Ohlsson J, Karlsson J, Keep MF et al. Brainderived respiring mitochondria exhibit homogeneous, complete and cyclosporin-sensitive permeability transition. J Neurochem 2004; 89: 715-729.
46. Lee H, Noh JY, Oh Y, Kim Y, Chang JW, Chung CW et al. IRE1 plays an essential role in ER stress-mediated aggregation of mutant huntingtin via the inhibition of autophagy flux. Hum Mol Genet 2012; 21: 101-114.
47. De Simoni S, Linard D, Hermans E, Knoops B, Goemaere J. Mitochondrial peroxiredoxin-5 as potential modulator of mitochondria-ER crosstalk in MPP(+) -induced cell death. J Neurochem 2012; 125: 473-485.
48. Jayaraman T, Marks AR. T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol Cell Biol 1997; 17: 3005-3012.
49. Jayaraman T, Marks AR. Calcineurin is downstream of the inositol 1,4,5-trisphosphate receptor in the apoptotic and cell growth pathways. J Biol Chem 2000; 275: 6417-6420.
50. Rizzuto R, De Stefani D, Raffaello A, Mammucari C. Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 2012; 13: 566-578.
51. Kirichok Y, Krapivinsky G, Clapham DE. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 2004; 427: 360-364.
52. He P, Wang AG, Xia T, Gao P, Niu Q, Guo LJ et al. Mechanism of the neurotoxic effect of PBDE-47 and interaction of PBDE-47 and PCB153 in enhancing toxicity in SH-SY5Y cells. Neurotoxicology 2009; 30: 10-15.
53. Son SM, Jung ES, Shin HJ, Byun J, Mook-Jung I. Abeta-induced formation of autophagosomes is mediated by RAGE-CaMKKbeta-AMPK signaling. Neurobiol Aging 2012; 33: 1006 e1011-1006 e1023.
54. Cha MY, Han SH, Son SM, Hong HS, Choi YJ, Byun J et al. Mitochondria-specific accumulation of amyloid beta induces mitochondrial dysfunction leading to apoptotic cell death. PLoS One 2012; 7: e34929.
55. Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T. Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr Biol 1995; 5: 635-642.
56. Son SM, Song H, Byun J, Park KS, Jang HC, Park YJ et al. Altered APP processing in insulin-resistant conditions is mediated by autophagosome accumulation via the inhibition of mammalian target of rapamycin pathway. Diabetes 2012; 61: 3126-3138.