Preferences help
enabled [disable] Abstract
Number of results
2005 | 52 | 2 | 381-395
Article title

Endoplasmic reticulum quality control and apoptosis.

Title variants
Languages of publication
The ER is one of the most important folding compartments within the cell, as well as an intracellular Ca^(2+) storage organelle and it contains a number of Ca^(2+) regulated molecular chaperones responsible for the proper folding of glycosylated as well as non-glycosylated proteins. The luminal environment of the ER contains Ca^(2+) which is involved in regulating chaperones such as calnexin and calreticulin, as well as apoptotic proteins caspase-12 and Bap31, which may play an important role in determining cellular sensitivity to ER stress and apoptosis. The ER quality control system consists of several molecular chaperones, including calnexin, that assist in properly folding proteins and transporting them through the ER as well as sensing misfolded proteins, attempting to refold them and if this is not possible, targeting them for degradation. Accumulation of misfolded protein in the ER leads to activation of genes responsible for the expression of ER chaperones. The UPR mechanism involves transcriptional activation of chaperones by the membrane-localized transcription factor ATF6, in conjunction with the ER membrane kinase IRE1, as well as translational repression of protein synthesis by another ER membrane kinase PERK. When accumulation of misfolded protein becomes toxic, apoptosis is triggered, potentially with IRE1 involved in signaling via caspase-12. Both the extrinsic and intrinsic apoptotic pathways appear to culminate in the activation of caspases and this results in the recruitment of mitochondria in an essential amplifying manner. Bap31 may direct pro-apoptotic crosstalk between the ER and the mitochondria via Ca^(2+) in conjunction with caspase-12 and calnexin. Accordingly, ER stress and the resultant Ca^(2+) release must be very carefully regulated because of their effects in virtually all areas of cell function.
Physical description
  • Department of Biochemistry, University of Alberta, Edmonton, Alberta, Canada, T6G 2H7
  • Department of Biochemistry, University of Alberta, Edmonton, Alberta, Canada, T6G 2H7
  • Adams JM, Cory S (2002) Apoptosomes: engines for caspase activation. Curr Opin Cell Biol 14: 715-720.
  • Amaral MD (2004) CFTR and chaperones: processing and degradation. J Mol Neurosci 23: 41-48.
  • Amuthan G, Biswas G, Ananadatheerthavarada HK, Vijayasarathy C, Shephard HM, Avadhani NG (2002) Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells. Oncogene 21: 7839-7849.
  • Annis MG, Yethon JA, Leber B, Andrews DW (2004) There is more to life and death than mitochondria: Bcl-2 proteins at the endoplasmic reticulum. Biochim Biophys Acta 1644: 115-123.
  • Arnaudeau S, Frieden M, Nakamura K, Castelbou C, Michalak M, Demaurex N (2002) Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J Biol Chem 277: 46696-46705.
  • Arur S, Uche UE, Rezaul K, Fong M, Scranton V, Cowan AE, Mohler W, Han DK (2003) Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev Cell 4: 587-598.
  • Ashkenazi A (2002) Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2: 420-430.
  • Baffy G, Miyashita T, Williamson JR, Reed JC (1993) Apoptosis induced by withdrawal of interleukin-3 (IL-3) from an IL-3-dependent hematopoietic cell line is associated with repartitioning of intracellular calcium and is blocked by enforced Bcl-2 oncoprotein production. J Biol Chem 268: 6511-6519.
  • Balasubramanian K, Schroit AJ (2003) Aminophospholipid asymmetry: A matter of life and death. Annu Rev Physiol 65: 701-734.
  • Baumann O, Walz B (2001) Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205: 149-214.
  • Bergeron JJM, Brenner MB, Thomas DY, Williams DB (1994) Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem Sci 19: 124-128.
  • Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32: 235-249.
  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1: 11-21.
  • Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326-332.
  • Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM, Ricci JE, Edris WA, Sutherlin DP, Green DR, Salvesen GS (2003) A unified model for apical caspase activation. Mol Cell 11: 529-541.
  • Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH (2003) Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5: 1051-1061.
  • Borner C (2003) The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 39: 615-647.
  • Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC (2003a) Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22: 8608-8618.
  • Breckenridge DG, Stojanovic M, Marcellus RC, Shore GC (2003b) Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol 160: 1115-1127.
  • Brini M, Bano D, Manni S, Rizzuto R, Carafoli E (2000) Effects of PMCA and SERCA pump overexpression on the kinetics of cell Ca(2+) signalling. EMBO J 19: 4926-4935.
  • Brooks DA (1997) Protein processing: a role in the pathophysiology of genetic disease. FEBS Lett 409: 115-120.
  • Brooks DA (1999) Introduction: molecular chaperones of the ER: their role in protein folding and genetic disease. Semin Cell Dev Biol 10: 441-442.
  • Brostrom CO, Prostko CR, Kaufman RJ, Brostrom MA (1996) Inhibition of translational initiation by activators of the glucose-regulated stress protein and heat shock protein stress response systems. Role of the interferon-inducible double-stranded RNA-activated eukaryotic initiation factor 2α kinase. J Biol Chem 271: 24995-25002.
  • Brunagel G, Shah U, Schoen RE, Getzenberg RH (2003) Identification of calreticulin as a nuclear matrix protein associated with human colon cancer. J Cell Biochem 89: 238-243.
  • Burlacu A (2003) Regulation of apoptosis by Bcl-2 family proteins. J Cell Mol Med 7: 249-257.
  • 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.
  • Camacho P, Lechleiter JD (1995) Calreticulin inhibits repetitive intracellular Ca2+ waves. Cell 82: 765-771.
  • Canzoniero LM, Babcock DJ, Gottron FJ, Grabb MC, Manzerra P, Snider BJ, Choi DW (2004) Raising intracellular calcium attenuates neuronal apoptosis triggered by staurosporine or oxygen-glucose deprivation in the presence of glutamate receptor blockade. Neurobiol Dis 15: 520-528.
  • Carlberg M, Dricu A, Blegen H, Kass GE, Orrenius S, Larsson O (1996) Short exposures to tunicamycin induce apoptosis in SV40-transformed but not in normal human fibroblasts. Carcinogenesis 17: 2589-2596.
  • Chami M, Ferrari D, Nicotera P, Paterlini-Brechot P, Rizzuto R (2003) Caspase-dependent alterations of Ca2+ signaling in the induction of apoptosis by hepatitis B virus X protein. J Biol Chem 278: 31745-31755.
  • Chevet E, Jakob CA, Thomas DY, Bergeron JJ (1999a) Calnexin family members as modulators of genetic diseases. Semin Cell Dev Biol 10: 473-480.
  • Chevet E, Wong HN, Gerber D, Cochet C, Fazel A, Cameron PH, Gushue JN, Thomas DY, Bergeron JJ (1999b) Phosphorylation by CK2 and MAPK enhances calnexin association with ribosomes. EMBO J 18: 3655-3666.
  • Choi YH, Lee SJ, Nguyen P, Jang JS, Lee J, Wu ML, Takano E, Maki M, Henkart PA, Trepel JB (1997) Regulation of cyclin D1 by calpain protease. J Biol Chem 272: 28479-28484.
  • Choi WS, Lee EH, Chung CW, Jung YK, Jin BK, Kim SU, Oh TH, Saido TC, Oh YJ (2001) Cleavage of Bax is mediated by caspase-dependent or -independent calpain activation in dopaminergic neuronal cells: protective role of Bcl-2. J Neurochem 77: 1531-1541.
  • Chou KJ, Fang HC, Chung HM, Cheng JS, Lee KC, Tseng LL, Tang KY, Jan CR (2000) Effect of betulinic acid on intracellular-free Ca2+ levels in Madin Darby canine kidney cells. Eur J Pharmacol 408: 99-106.
  • Corbett EF, Michalak M (2000) Calcium, a signaling molecule in the endoplasmic reticulum? Trends Biochem Sci 25: 307-311.
  • Corbett EF, Oikawa K, Francois P, Tessier DC, Kay C, Bergeron JJ, Thomas DY, Krause KH, Michalak M (1999) Ca2+ regulation of interactions between endoplasmic reticulum chaperones. J Biol Chem 274: 6203-6211.
  • Cory S, Huang DC, Adams JM (2003) The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22: 8590-8607.
  • Creagh EM, Conroy H, Martin SJ (2003) Caspase-activation pathways in apoptosis and immunity. Immunol Rev 193: 10-12.
  • Csordas G, Madesh M, Antonsson B, Hajnoczky G (2002) tcBid promotes Ca2+ signal propagation to the mitochondria: control of Ca2+ permeation through the outer mitochondrial membrane. EMBO J 21: 2198-2206.
  • Dachary-Prigent J, Pasquet JM, Freyssinet JM, Nurden AT (1995) Calcium involvement in aminophospholipid exposure and microparticle formation during platelet activation: a study using Ca2+-ATPase inhibitors. Biochemistry 34: 11625-11634.
  • Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116: 205-219.
  • Darios F, Lambeng N, Troadec JD, Michel PP, Ruberg M (2003) Ceramide increases mitochondrial free calcium levels via caspase 8 and Bid: role in initiation of cell death. J Neurochem 84: 643-654.
  • Denault JB, Salvesen GS (2002) Caspases: keys in the ignition of cell death. Chem Rev 102: 4489-4500.
  • Diaz-Horta O, Kamagate A, Herchuelz A, Van Eylen F (2002) Na/Ca exchanger overexpression induces endoplasmic reticulum-related apoptosis and caspase-12 activation in insulin-releasing BRIN-BD11 cells. Diabetes 51: 1815-1824.
  • Dissemond J, Busch M, Kothen T, Mors J, Weimann TK, Lindeke A, Goos M, Wagner SN (2004) Differential downregulation of endoplasmic reticulum-residing chaperones calnexin and calreticulin in human metastatic melanoma. Cancer Lett 203: 225-231.
  • Distelhorst CW, McCormick TS (1996) Bcl-2 acts subsequent to and independent of Ca2+ fluxes to inhibit apoptosis in thapsigargin- and glucocorticoid-treated mouse lymphoma cells. Cell Calcium 19: 473-483.
  • Distelhorst CW, Shore GC (2004) Bcl-2 and calcium: controversy beneath the surface. Oncogene 23: 2875-2880.
  • Donepudi M, Mac Sweeney A, Briand C, Grutter MG (2003) Insights into the regulatory mechanism for caspase-8 activation. Mol Cell 11: 543-549.
  • Draper DW, Harris VG, Culver CA, Laster SM (2004) Calcium and its role in the nuclear translocation and activation of cytosolic phospholipase A(2) in cells rendered sensitive to TNF-induced apoptosis by cycloheximide. J Immunol 172: 2416-2423.
  • Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol 529: 57-68.
  • Dussmann H, Rehm M, Kogel D, Prehn JH (2003) Outer mitochondrial membrane permeabilization during apoptosis triggers caspase-independent mitochondrial and caspase-dependent plasma membrane potential depolarization: a single-cell analysis. J Cell Sci 116: 525-536.
  • Earnshaw WC, Martins LM, Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383-424.
  • Ellgaard L, Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191.
  • Ellgaard L, Riek R, Herrmann T, Guntert P, Braun D, Helenius A, Wuthrich K (2001) NMR structure of the calreticulin P-domain. Proc Natl Acad Sci USA 98: 3133-3138.
  • Ermak G, Davies KJ (2002) Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 38: 713-721.
  • Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405: 85-90.
  • Ferrari D, Pinton P, Szabadkai G, Chami M, Campanella M, Pozzan T, Rizzuto R (2002) Endoplasmic reticulum, Bcl-2 and Ca2+ handling in apoptosis. Cell Calcium 32: 413-420.
  • Ferraro E, Corvaro M, Cecconi F (2003) Physiological and pathological roles of Apaf1 and the apoptosome. J Cell Mol Med 7: 21-34.
  • Frickel EM, Riek R, Jelesarov I, Helenius A, Wuthrich K, Ellgaard L (2002) TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc Natl Acad Sci USA 99: 1954-1959.
  • Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355: 33-45.
  • Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
  • Gong Y, Blok LJ, Perry JE, Lindzey JK, Tindall DJ (1995) Calcium regulation of androgen receptor expression in the human prostate cancer cell line LNCaP. Endocrinology 136: 2172-2178.
  • Goping IS, Gross A, Lavoie JN, Nguyen M, Jemmerson R, Roth K, Korsmeyer SJ, Shore GC (1998) Regulated targeting of BAX to mitochondria. J Cell Biol 143: 207-215.
  • Graf GA, Cohen JC, Hobbs HH (2004) Missense mutations in ABCG5 and ABCG8 disrupt heterodimerization and trafficking. J Biol Chem 279: 24881-24888.
  • Green DR, Evan GI (2002) A matter of life and death. Cancer Cell 1: 19-30.
  • Griffiths GJ, Dubrez L, Morgan CP, Jones NA, Whitehouse J, Corfe BM, Dive C, Hickman JA (1999) Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J Cell Biol 144: 903-914.
  • Gross A, McDonnell JM, Korsmeyer SJ (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13: 1899-1911.
  • Hajnoczky G, Davies E, Madesh M (2003) Calcium signaling and apoptosis. Biochem Biophys Res Commun 304: 445-454.
  • Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum- resident kinase. Nature 397: 271-274.
  • Helenius A, Aebi M (2001) Intracellular functions of N-linked glycans. Science 291: 2364-2369.
  • Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049.
  • Hirsch C, Jarosch E, Sommer T, Wolf DH (2004) Endoplasmic reticulum-associated protein degradation - one model fits all? Biochim Biophys Acta 1695: 215-223.
  • Hirschberg CB, Snider MD (1987) Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus. Annu Rev Biochem 56: 63-87.
  • Hosokawa N, Wada I, Hasegawa K, Yorihuzi T, Tremblay LO, Herscovics A, Nagata K (2001) A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep 2: 415-422.
  • Hsu YT, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94: 3668-3672.
  • Jackson MR, Nilsson T, Peterson PA (1990) Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J 9: 3153-3162.
  • Jakob CA, Bodmer D, Spirig U, Battig P, Marcil A, Dignard D, Bergeron JJ, Thomas DY, Aebi M (2001a) Htm1p, a mannosidase-like protein, is involved in glycoprotein degradation in yeast. EMBO Rep 2: 423-430.
  • Jakob CA, Chevet E, Thomas DY, Bergeron JJ (2001b) Lectins of the ER quality control machinery. Results Probl Cell Differ 33: 1-17.
  • Jayaraman T, Marks AR (1997) T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol Cell Biol 17: 3005-3012.
  • Jeffery J, Kendall JM, Campbell AK (2000) Apoaequorin monitors degradation of endoplasmic reticulum (ER) proteins initiated by loss of ER Ca2+. Biochem Biophys Res Commun 268: 711-715.
  • Johnson S, Michalak M, Opas M, Eggleton P (2001) The ins and outs of calreticulin: from the ER lumen to the extracellular space. Trends Cell Biol 11: 122-129.
  • Joseph SK, Boehning D, Bokkala S, Watkins R, Widjaja J (1999) Biosynthesis of inositol trisphosphate receptors: selective association with the molecular chaperone calnexin. Biochem J 342: 153-161.
  • Kam PC, Ferch NI (2000) Apoptosis: mechanisms and clinical implications. Anaesthesia 55: 1081-1093.
  • Katoh I, Tomimori Y, Ikawa Y, Kurata S (2004) Dimerization and processing of procaspase-9 by redox stress in mitochondria. J Biol Chem 279: 15515-15523.
  • Kehlenbach RH, Gerace L (2000) Phosphorylation of the nuclear transport machinery down-regulates nuclear protein import in vitro. J Biol Chem 275: 17848-17856.
  • Kim MJ, Jo DG, Hong GS, Kim BJ, Lai M, Cho DH, Kim KW, Bandyopadhyay A, Hong YM, Kim do H, et al. (2002) Calpain-dependent cleavage of cain/cabin1 activates calcineurin to mediate calcium-triggered cell death. Proc Natl Acad Sci USA 99: 9870-9875.
  • Kleizen B, Braakman I (2004) Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 16: 343-349.
  • Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136.
  • Kudo T, Katayama T, Imaizumi K, Yasuda Y, Yatera M, Okochi M, Tohyama M, Takeda M (2002) The unfolded protein response is involved in the pathology of Alzheimer’s disease. Ann NY Acad Sci 977: 349-355.
  • Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384: 368-372.
  • Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P, Flavell RA (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94: 325-337.
  • Kusakawa G, Saito T, Onuki R, Ishiguro K, Kishimoto T, Hisanaga S (2000) Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J Biol Chem 275: 17166-17172.
  • Lai MM, Burnett PE, Wolosker H, Blackshaw S, Snyder SH (1998) Cain, a novel physiologic protein inhibitor of calcineurin. J Biol Chem 273: 18325-18331.
  • Lai MM, Luo HR, Burnett PE, Hong JJ, Snyder SH (2000) The calcineurin-binding protein cain is a negative regulator of synaptic vesicle endocytosis. J Biol Chem 275: 34017-34020.
  • Leach MR, Cohen-Doyle MF, Thomas DY, Williams DB (2002) Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J Biol Chem 277: 29686-29697.
  • Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, Okada T, Yoshida H, Mori K, Kaufman RJ (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.
  • Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405: 360-364.
  • Li F, Mandal M, Barnes CJ, Vadlamudi RK, Kumar R (2001) Growth factor regulation of the molecular chaperone calnexin. Biochem Biophys Res Commun 289: 725-732.
  • Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157.
  • Ma TS, Mann DL, Lee JH, Gallinghouse GJ (1999) SR compartment calcium and cell apoptosis in SERCA overexpression. Cell Calcium 26: 25-36.
  • Mandic A, Viktorsson K, Strandberg L, Heiden T, Hansson J, Linder S, Shoshan MC (2002) Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Mol Cell Biol 22: 3003-3013.
  • Mann CL, Bortner CD, Jewell CM, Cidlowski JA (2001) Glucocorticoid-induced plasma membrane depolarization during thymocyte apoptosis: association with cell shrinkage and degradation of the Na+/K+-adenosine triphosphatase. Endocrinology 142: 5059-5068.
  • Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC, Kroemer G (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031.
  • Mattson MP (2000) Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1: 120-129.
  • Mattson MP, Chan SL (2003) Calcium orchestrates apoptosis. Nat Cell Biol 5: 1041-1043.
  • McClintock DS, Santore MT, Lee VY, Brunelle J, Budinger GR, Zong WX, Thompson CB, Hay N, Chandel NS (2002) Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol Cell Biol 22: 94-104.
  • Meier P, Finch A, Evan G (2000) Apoptosis in development. Nature 407: 796-801.
  • Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause K-H, Opas M, MacLennan DH, Michalak M (1999) Calreticulin is essential for cardiac development. J Cell Biol 144: 857-868.
  • Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M (1999) Calreticulin: one protein, one gene, many functions. Biochem J 344: 281-292.
  • Michalak M, Robert Parker JM, Opas M (2002) Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32: 269-278.
  • Molinari M, Helenius A (2000) Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288: 331-333.
  • Molinari M, Calanca V, Galli C, Lucca P, Paganetti P (2003) Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299: 1397-1400.
  • Molinari M, Eriksson KK, Calanca V, Galli C, Cresswell P, Michalak M, Helenius A (2004) Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol Cell 13: 125-135.
  • Mori K, Kawahara T, Yoshida H, Yanagi H, Yura T (1996) Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1: 803-817.
  • 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.
  • Munch G, Bolck B, Karczewski P, Schwinger RH (2002) Evidence for calcineurin-mediated regulation of SERCA 2a activity in human myocardium. J Mol Cell Cardiol 34: 321-334.
  • Naismith JH, Sprang SR (1998) Modularity in the TNF-receptor family. Trends Biochem Sci 23: 74-79.
  • 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.
  • 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.
  • Nakamura K, Bossy-Wetzel E, Burns K, Fadel M, Lozyk M, Goping IS, Opas M, Bleackley RC, Green DR, Michalak M (2000) Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J Cell Biol 150: 731-740.
  • Nakamura K, Zuppini A, Arnaudeau S, Lynch J, Ahsan I, Krause R, Papp S, De Smedt H, Parys JB, Müller-Esterl W, et al. (2001) Functional specialization of calreticulin domains. J Cell Biol 154: 961-972.
  • Nakayama T, Hattori M, Uchida K, Nakamura T, Tateishi Y, Bannai H, Iwai M, Michikawa T, Inoue T, Mikoshiba K (2004) The regulatory domain of the inositol 1,4,5-trisphosphate receptor is necessary to keep the channel domain closed: possible physiological significance of specific cleavage by caspase 3. Biochem J 377: 299-307.
  • Nath R, Raser KJ, McGinnis K, Nadimpalli R, Stafford D, Wang KK (1996) Effects of ICE-like protease and calpain inhibitors on neuronal apoptosis. Neuroreport 8: 249-255.
  • Ng FW, Nguyen M, Kwan T, Branton PE, Nicholson DW, Cromlish JA, Shore GC (1997) p28 Bap31, a Bcl-2/Bcl-XL- and procaspase-8-associated protein in the endoplasmic reticulum. J Cell Biol 139: 327-338.
  • Nguyen M, Breckenridge DG, Ducret A, Shore GC (2000) Caspase-resistant BAP31 inhibits Fas-mediated apoptotic membrane fragmentation and release of cytochrome c from mitochondria. Mol Cell Biol 20: 6731-6740.
  • Nicholson DW, Thornberry NA (1997) Caspases: killer proteases. Trends Biochem Sci 22: 299-306.
  • Nicolls MR, D’Antonio JM, Hutton JC, Gill RG, Czwornog JL, Duncan MW (2003) Proteomics as a tool for discovery: proteins implicated in Alzheimer’s disease are highly expressed in normal pancreatic islets. J Proteome Res 2: 199-205.
  • Norbury CJ, Zhivotovsky B (2004) DNA damage-induced apoptosis. Oncogene 23: 2797-2808.
  • Oakes SA, Opferman JT, Pozzan T, Korsmeyer SJ, Scorrano L (2003) Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem Pharmacol 66: 1335-1340.
  • Oda Y, Hosokawa N, Wada I, Nagata K (2003) EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299: 1394-1397.
  • Ogino T, Bandoh N, Hayashi T, Miyokawa N, Harabuchi Y, Ferrone S (2003) Association of tapasin and HLA class I antigen down-regulation in primary maxillary sinus squamous cell carcinoma lesions with reduced survival of patients. Clin Cancer Res 9: 4043-4051.
  • Ohsako S, Hayashi Y, Bunick D (1994) Molecular cloning and sequencing of calnexin-t. An abundant male germ cell-specific calcium-binding protein of the endoplasmic reticulum. J Biol Chem 269: 14140-14148.
  • Pan Z, Damron D, Nieminen AL, Bhat MB, Ma J (2000) Depletion of intracellular Ca2+ by caffeine and ryanodine induces apoptosis of chinese hamster ovary cells transfected with ryanodine receptor. J Biol Chem 275: 19978-19984.
  • Pariat M, Carillo S, Molinari M, Salvat C, Debussche L, Bracco L, Milner J, Piechaczyk M (1997) Proteolysis by calpains: a possible contribution to degradation of p53. Mol Cell Biol 17: 2806-2815.
  • Parodi AJ (2000) Protein glucosylation and its role in protein folding. Annu Rev Biochem 69: 69-93.
  • Pinton P, Ferrari D, Rapizzi E, Di Virgilio F, Pozzan T, Rizzuto R (2002) A role for calcium in Bcl-2 action? Biochimie 84: 195-201.
  • Pollock S, Kozlov G, Pelletier MF, Trempe JF, Jansen G, Sitnikov D, Bergeron JJ, Gehring K, Ekiel I, Thomas DY (2004) Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. EMBO J 23: 1020-1029.
  • Porn-Ares MI, Samali A, Orrenius S (1998) Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death Differ 5: 1028-1033.
  • Potter DA, Tirnauer JS, Janssen R, Croall DE, Hughes CN, Fiacco KA, Mier JW, Maki M, Herman IM (1998) Calpain regulates actin remodeling during cell spreading. J Cell Biol 141: 647-662.
  • Prostko CR, Dholakia JN, Brostrom MA, Brostrom CO (1995) Activation of the double-stranded RNA-regulated protein kinase by depletion of endoplasmic reticular calcium stores. J Biol Chem 270: 6211-6215.
  • Rajagopalan S, Xu Y, Brenner MB (1994) Retention of unassembled components of integral membrane proteins by calnexin. Science 263: 387-390.
  • 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.
  • Rao RV, Ellerby HM, Bredesen DE (2004) Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 11: 372-380.
  • Reddy RK, Lu J, Lee AS (1999) The endoplasmic reticulum chaperone glycoprotein GRP94 with Ca2+-binding and antiapoptotic properties is a novel proteolytic target of calpain during etoposide-induced apoptosis. J Biol Chem 274: 28476-28483.
  • Remillard CV, Yuan JX (2004) Activation of K+ channels: an essential pathway in programmed cell death. Am J Physiol Lung Cell Mol Physiol 286: L49-67.
  • Rizzuto R, Pinton P, Ferrari D, Chami M, Szabadkai G, Magalhaes PJ, Di Virgilio F, Pozzan T (2003) Calcium and apoptosis: facts and hypotheses. Oncogene 22: 8619-8627.
  • Rizzuto R, Duchen MR, Pozzan T (2004) Flirting in little space: the ER/mitochondria Ca2+ liaison. Sci STKE 2004, re1.
  • Roderick HL, Lechleiter JD, Camacho P (2000) Cytosolic phosphorylation of calnexin controls intracellular Ca2+ oscillations via an interaction with SERCA2b. J Cell Biol 149: 1235-1248.
  • Ruiz-Vela A, Gonzalez de Buitrago G, Martinez AC (1999) Implication of calpain in caspase activation during B cell clonal deletion. EMBO J 18: 4988-4998.
  • Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14: 20-28.
  • Saido TC, Nagao S, Shiramine M, Tsukaguchi M, Yoshizawa T, Sorimachi H, Ito H, Tsuchiya T, Kawashima S, Suzuki K (1994) Distinct kinetics of subunit autolysis in mammalian m-calpain activation. FEBS Lett 346: 263-267.
  • Saito Y, Ihara Y, Leach MR, Cohen-Doyle MF, Williams DB (1999) Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. EMBO J 18: 6718-6729.
  • Sakahira H, Enari M, Nagata S (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391: 96-99.
  • Salvesen GS, Renatus M (2002) Apoptosome: the seven-spoked death machine. Dev Cell 2: 256-257.
  • Sanchez D, Tuckova L, Sebo P, Michalak M, Whelan A, Sterzl I, Jelinkova L, Havrdova E, Imramovska M, Benes Z, et al. (2000) Occurrence of IgA and IgG autoantibodies to calreticulin in coeliac disease and various autoimmune diseases. J Autoimmun 15: 441-449.
  • Sanchez D, Tuckova L, Mothes T, Kreisel W, Benes Z, Tlaskalova-Hogenova H (2003) Epitopes of calreticulin recognised by IgA autoantibodies from patients with hepatic and coeliac disease. J Autoimmun 21: 383-392.
  • Saraste A, Pulkki K (2000) Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45: 528-537.
  • Sartorius U, Schmitz I, Krammer PH (2001) Molecular mechanisms of death-receptor-mediated apoptosis. Chembiochem 2: 20-29.
  • Savill J, Fadok V (2000) Corpse clearance defines the meaning of cell death. Nature 407: 784-788.
  • Schinzel A, Kaufmann T, Borner C (2004) Bcl-2 family members: intracellular targeting, membrane-insertion, and changes in subcellular localization. Biochim Biophys Acta 1644: 95-105.
  • Schrag JD, Bergeron JJM, Li Y, Borisova S, Hahn M, Thomas DY, Cygler M (2001) The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell 8: 633-644.
  • Shames I, Fraser A, Colby J, Orfali W, Snipes GJ (2003) Phenotypic differences between peripheral myelin protein-22 (PMP22) and myelin protein zero (P0) mutations associated with Charcot-Marie-Tooth-related diseases. J Neuropathol Exp Neurol 62: 751-764.
  • Shchepina LA, Pletjushkina OY, Avetisyan AV, Bakeeva LE, Fetisova EK, Izyumov DS, Saprunova VB, Vyssokikh MY, Chernyak BV, Skulachev VP (2002) Oligomycin, inhibitor of the F0 part of H+-ATP-synthase, suppresses the TNF-induced apoptosis. Oncogene 21: 8149-8157.
  • Sherman MY, Goldberg AL (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29: 15-32.
  • Shi Y (2004) Caspase activation: revisiting the induced proximity model. Cell 117: 855-858.
  • Siegel RM, Muppidi J, Roberts M, Porter M, Wu Z (2003) Death receptor signaling and autoimmunity. Immunol Res 27: 499-512.
  • Sitia R, Braakman I (2003) Quality control in the endoplasmic reticulum protein factory. Nature 426: 891-894.
  • Slee EA, Adrain C, Martin SJ (1999) Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 6: 1067-1074.
  • Soti C, Csermely P (2002) Chaperones and aging: role in neurodegeneration and in other civilizational diseases. Neurochem Int 41: 383-389.
  • Strasser A, O’Connor L, Dixit VM (2000) Apoptosis signaling. Annu Rev Biochem 69: 217-245.
  • Sun L, Youn HD, Loh C, Stolow M, He W, Liu JO (1998) Cabin 1, a negative regulator for calcineurin signaling in T lymphocytes. Immunity 8: 703-711.
  • Tantral L, Malathi K, Kohyama S, Silane M, Berenstein A, Jayaraman T (2004) Intracellular calcium release is required for caspase-3 and -9 activation. Cell Biochem Funct 22: 35-40.
  • Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281: 1312-1316.
  • Tjoelker LW, Seyfried CE, Eddy RL Jr, Byers MG, Shows TB, Calderon J, Gray PW (1994) Human, mouse, and rat calnexin cDNA cloning: identification of potential calcium binding motifs and gene localization to human chromosome 5. Biochemistry 33: 3229-3236.
  • Tsai B, Ye Y, Rapoport TA (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat Rev Mol Cell Biol 3: 246-255.
  • Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
  • Vanden Abeele F, Skryma R, Shuba Y, Van Coppenolle F, Slomianny C, Roudbaraki M, Mauroy B, Wuytack F, Prevarskaya N (2002) Bcl-2-dependent modulation of Ca2+ homeostasis and store-operated channels in prostate cancer cells. Cancer Cell 1: 169-179.
  • Varfolomeev EE, Schuchmann M, Luria V, Chiannilkulchai N, Beckmann JS, Mett IL, Rebrikov D, Brodianski VM, Kemper OC, Kollet O, et al. (1998) Targeted disruption of the mouse caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9: 267-276.
  • Wang KK (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23: 20-26.
  • Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15: 2922-2933.
  • Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F, McKeon F, Bobo T, Franke TF, Reed JC (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284: 339-343.
  • Waterhouse NJ, Finucane DM, Green DR, Elce JS, Kumar S, Alnemri ES, Litwack G, Khanna K, Lavin MF, Watters DJ (1998) Calpain activation is upstream of caspases in radiation-induced apoptosis. Cell Death Differ 5: 1051-1061.
  • Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139: 1281-1292.
  • Wong HN, Ward MA, Bell AW, Chevet E, Bains S, Blackstock WP, Solari R, Thomas DY, Bergeron JJM (1998) Conserved in vivo phosphorylation of calnexin at casein kinase II sites as well as a protein kinase C/proline-directed kinase site. J Biol Chem 273: 17227-17235.
  • Wood DE, Newcomb EW (1999) Caspase-dependent activation of calpain during drug-induced apoptosis. J Biol Chem 274: 8309-8315.
  • Wood DE, Thomas A, Devi LA, Berman Y, Beavis RC, Reed JC, Newcomb EW (1998) Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17: 1069-1078.
  • Yamamoto K, Yoshida H, Kokame K, Kaufman RJ, Mori K (2004) Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem (Tokyo) 136: 343-350.
  • Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132.
  • Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M (2001) Activation of caspase-12, an endoplastic 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.
  • Yoshida Y (2003) A novel role for N-glycans in the ERAD system. J Biochem (Tokyo) 134: 183-190.
  • Yoshida H, Matsui T, Hosokawa N, Kaufman RJ, Nagata K, Mori K (2003) A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 4: 265-271.
  • 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.
  • Zaidi NF, Thomson EE, Choi EK, Buxbaum JD, Wasco W (2004) Intracellular calcium modulates the nuclear translocation of calsenilin. J Neurochem 89: 593-601.
  • Zhu N, Pewitt EB, Cai XY, Cohn EB, Lang S, Chen R, Wang Z (1998) Calreticulin: An intracellular Ca++-binding protein abundantly expressed and regulated by androgen in prostatic epithelial cells. Endocrinology 139: 4337-4344.
  • Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB (2003) Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 162: 59-69.
  • Zuppini A, Groenendyk J, Cormack LA, Shore G, Opas M, Bleackley RC, Michalak M (2002) Calnexin deficiency and endoplasmic reticulum stress-induced apoptosis. Biochemistry 41: 2850-2858.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.