Ca2+-signaling, alternative splicing and endoplasmic reticulum stress responses

Neurochemical Research

Volumn 36, Issue 7, 2011, Pages 1198-1211

  Krebs, Joachim ^a   Groenendyk, Jody ^b   Michalak, Marek ^b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Alternative splicing; ATF6; BiP GRP78; Ca2+ signaling; IRE1; PERK; Stress response; UPR; XBP1

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CALCIUM ION; GLUCOSE REGULATED PROTEIN 78; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN IRE1; PROTEIN KINASE R; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; ATF6 PROTEIN, HUMAN; CALCIUM; ERN2 PROTEIN, MOUSE; HEAT SHOCK PROTEIN; ISOPROTEIN; MEMBRANE PROTEIN; MOLECULAR CHAPERONE GRP78; PERK KINASE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PROTEIN SERINE THREONINE KINASE;

ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA GENE; ALTERNATIVE RNA SPLICING; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DEPHOSPHORYLATION; DSRNA ACTIVATED PROTEIN KINASE LIKE ER KINASE GENE; ENDOPLASMIC RETICULUM STRESS; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GLUCOSE REGULATED PROTEIN 78 GENE; HUMAN; INOSITOL REQUIRING TRANSMEMBRANE KINASE ENDONUCLEASE 1 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; UNFOLDED PROTEIN RESPONSE; X BOX BINDING PROTEIN 1 GENE; ANIMAL; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETICS; HOMEOSTASIS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ACTIVATING TRANSCRIPTION FACTOR 6; ALTERNATIVE SPLICING; ANIMALS; CALCIUM; CALCIUM SIGNALING; EIF-2 KINASE; ENDOPLASMIC RETICULUM; HEAT-SHOCK PROTEINS; HOMEOSTASIS; HUMANS; MEMBRANE PROTEINS; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; PROTEIN ISOFORMS; PROTEIN-SERINE-THREONINE KINASES; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE;

EID: 79959876794     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-011-0431-4     Document Type: Review

References (165)

1. Costa FF (2010) Non-coding RNAs: meet thy masters. Bioessays 32(7):599-608
2. Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126(1):37-47
3. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291-336
4. Wang ET, Sandberg R, Luo S et al (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456(7221):470-476 (Pubitemid 352759009)
5. Pan Q, Shai O, Lee LJ et al (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40(12):1413-1415
6. Lynch KW (2007) Regulation of alternative splicing by signal transduction pathways. Adv Exp Med Biol 623:161-174
7. Shin C, Manley JL (2004) Cell signalling and the control of premRNA splicing. Nat Rev Mol Cell Biol 5(9):727-738 (Pubitemid 39208182)
8. Ip JY, Tong A, Pan Q et al (2007) Global analysis of alternative splicing during T-cell activation. RNA 13(4):563-572 (Pubitemid 46506939)
9. Faustino NA, Cooper TA (2003) Pre-mRNA splicing and human disease. Genes Dev 17(4):419-437 (Pubitemid 36258756)
10. Novoyatleva T, Tang Y, Rafalska I et al (2006) Pre-mRNA missplicing as a cause of human disease. Prog Mol Subcell Biol 44:27-46
11. Licatalosi DD, Darnell RB (2006) Splicing regulation in neurologic disease. Neuron 52(1):93-101 (Pubitemid 44466357)
12. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4(7):517-529 (Pubitemid 36773404)
13. Rao RV, Ellerby HM, Bredesen DE (2004) Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 11(4):372-380 (Pubitemid 38489415)
14. Kawasaki H, Nakayama S, Kretsinger RH (1998) Classification and evolution of EF-hand proteins. Biometals 11(4):277-295 (Pubitemid 29121537)
15. Krebs J, Heizmann CW (2007) Calcium-binding proteins and the EF-hand principle. In: Krebs J, Michalak M (eds) Calcium: a matter of life or death. Elsevier B.V, Amsterdam, The Netherlands, pp 51-93
16. Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4):1341-1378
17. Pedersen PL (2007) Transport ATPases into the year 2008: a brief overview related to types, structures, functions and roles in health and disease. J Bioenerg Biomembr 39(5-6):349-355
18. Strehler EE, Strehler-Page MA, Vogel G et al (1989) mRNAs for plasma membrane calcium pump isoforms differing in their regulatory domain are generated by alternative splicing that involves two internal donor sites in a single exon. Proc Natl Acad Sci USA 86(18):6908-6912 (Pubitemid 19240841)
19. Strehler EE, Zacharias DA (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 81(1):21-50 (Pubitemid 32096172)
20. Zacharias DA, Kappen C (1999) Developmental expression of the four plasma membrane calcium ATPase (Pmca) genes in the mouse. Biochim Biophys Acta 1428(2-3):397-405 (Pubitemid 29352289)
21. Stauffer TP, Guerini D, Carafoli E (1995) Tissue distribution of the four gene products of the plasma membrane Ca2+ pump. A study using specific antibodies. J Biol Chem 270(20):12184-12190
22. Stauffer TP, Hilfiker H, Carafoli E et al (1993) Quantitative analysis of alternative splicing options of human plasma membrane calcium pump genes. J Biol Chem 268(34):25993-26003 (Pubitemid 23358221)
23. 2+-ATPase by either self-association or interaction with calmodulin J. Biol Chem 263:18184-18189
24. Brodin P, Falchetto R, Vorherr T et al (1992) Identification of two domains which mediate the binding of activating phospholipids to the plasma-membrane Ca2+ pump. Eur J Biochem 204(2):939-946
25. James PH, Pruschy M, Vorherr TE et al (1989) Primary structure of the cAMP-dependent phosphorylation site of the plasma membrane calcium pump. Biochemistry 28(10):4253-4258 (Pubitemid 19141627)
26. James P, Maeda M, Fischer R et al (1988) Identification and primary structure of a calmodulin binding domain of the Ca2+ pump of human erythrocytes. J Biol Chem 263(6):2905-2910
27. Falchetto R, Vorherr T, Brunner J et al (1991) The plasma membrane Ca2+ pump contains a site that interacts with its calmodulin-binding domain. J Biol Chem 266(5):2930-2936 (Pubitemid 21909157)
28. Falchetto R, Vorherr T, Carafoli E (1992) The calmodulin-binding site of the plasma membrane Ca2+ pump interacts with the transduction domain of the enzyme. Protein Sci 1(12):1613-1621 (Pubitemid 23047477)
29. Guerini D, Krebs J, Carafoli E (1984) Stimulation of the purified erythrocyte Ca2+ -ATPase by tryptic fragments of calmodulin. J Biol Chem 259(24):15172-15177
30. Enyedi A, Verma AK, Heim R et al (1994) The Ca2+ affinity of the plasma membrane Ca2+ pump is controlled by alternative splicing. J Biol Chem 269(1):41-43
31. Elshorst B, Hennig M, Forsterling H et al (1999) NMR solution structure of a complex of calmodulin with a binding peptide of the Ca2+ pump. Biochemistry 38(38):12320-12332
32. Di Leva F, Domi T, Fedrizzi L et al (2008) The plasma membrane Ca2+ ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476(1):65-74
33. Verma AK, Filoteo AG, Stanford DR et al (1988) Complete primary structure of a human plasma membrane Ca2+ pump. J Biol Chem 263(28):14152-14159
34. Shull GE, Greeb J (1988) Molecular cloning of two isoforms of the plasma membrane Ca2+ -transporting ATPase from rat brain. Structural and functional domains exhibit similarity to Na +, K+ - and other cation transport ATPases. J Biol Chem 263(18):8646-8657
35. Guerini D, Garcia-Martin E, Gerber A et al (1999) The expression of plasma membrane Ca2+ pump isoforms in cerebellar granule neurons is modulated by Ca2+. J Biol Chem 274(3):1667-1676
36. Preiano BS, Guerini D, Carafoli E (1996) Expression and functional characterization of isoforms 4 of the plasma membrane calcium pump. Biochemistry 35(24):7946-7953 (Pubitemid 26202535)
37. Keeton TP, Burk SE, Shull GE (1993) Alternative splicing of exons encoding the calmodulin-binding domains and C termini of plasma membrane Ca(2 +)-ATPase isoforms 1, 2, 3, and 4. J Biol Chem 268(4):2740-2748 (Pubitemid 23057904)
38. Brandt P, Neve RL (1992) Expression of plasma membrane calcium-pumping ATPase mRNAs in developing rat brain and adult brain subregions: evidence for stage-specific expression. J Neurochem 59(4):1566-1569
39. Carafoli E, Stauffer T (1994) The plasma membrane calcium pump: functional domains, regulation of the activity, and tissue specificity of isoform expression. J Neurobiol 25(3):312-324 (Pubitemid 24072913)
40. Talarico EF Jr, Mangini NJ (2007) Alternative splice variants of plasma membrane calcium-ATPases in human corneal epithelium. Exp Eye Res 85(6):869-879
41. Xiong Y, Antalffy G, Enyedi A et al (2009) Apical localization of PMCA2w/b is lipid raft-dependent. Biochem Biophys Res Commun 384(1):32-36
42. Blencowe BJ (2000) Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem Sci 25(3):106-110
43. Fairbrother WG, Yeh RF, Sharp PA et al (2002) Predictive identification of exonic splicing enhancers in human genes. Science 297(5583):1007-1013 (Pubitemid 34856033)
44. Andreadis A, Gallego ME, Nadal-Ginard B (1987) Generation of protein isoform diversity by alternative splicing: mechanistic and biological implications. Annu Rev Cell Biol 3:207-242
45. Smith CW, Nadal-Ginard B (1989) Mutually exclusive splicing of alpha-tropomyosin exons enforced by an unusual lariat branch point location: implications for constitutive splicing. Cell 56(5):749-758 (Pubitemid 19082509)
46. Sheng M, McFadden G, Greenberg ME (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4(4):571-582 (Pubitemid 20160846)
47. Matthews RP, Guthrie CR, Wailes LM et al (1994) Calcium/calmodulin- dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol Cell Biol 14(9):6107-6116 (Pubitemid 24264440)
48. Enslen H, Sun P, Brickey D et al (1994) Characterization of Ca2+/calmodulin-dependent protein kinase IV. Role in transcriptional regulation. J Biol Chem 269(22):15520-15527
49. Sheng M, Thompson MA, Greenberg ME (1991) CREB: a Ca(2 +)-regulated transcription factor phosphorylated by calmodulin- dependent kinases. Science 252(5011):1427-1430 (Pubitemid 21917061)
50. Sun Z, Sassone-Corsi P, Means AR (1995) Calspermin gene transcription is regulated by two cyclic AMP response elements contained in an alternative promoter in the calmodulin kinase IV gene. Mol Cell Biol 15(1):561-571 (Pubitemid 24379955)
51. Sun P, Lou L, Maurer RA (1996) Regulation of activating transcription factor-1 and the cAMP response element-binding protein by Ca2+/calmodulin- dependent protein kinases type I, II, and IV. J Biol Chem 271(6):3066-3073
52. Pognonec P, Boulukos KE, Gesquiere JC et al (1988) Mitogenic stimulation of thymocytes results in the calcium-dependent phosphorylation of c-ets-1 proteins. EMBO J 7(4):977-983
53. Fisher CL, Ghysdael J, Cambier JC (1991) Ligation of membrane Ig leads to calcium-mediated phosphorylation of the proto-oncogene product, Ets-1. J Immunol 146(6):1743-1749
54. Krebs J (1998) Calmodulin-dependent protein kinase IV: regulation of function and expression. Biochim Biophys Acta 1448(2):183-189
55. Krebs J, Means RL, Honegger P (1996) Induction of calmodulin kinase IV by the thyroid hormone during the development of rat brain. J Biol Chem 271(19):11055-11058 (Pubitemid 26155930)
56. Liu YY, Brent GA (2002) A complex deoxyribonucleic acid response element in the rat Ca(2 +)/calmodulin-dependent protein kinase IV gene 5′-flanking region mediates thyroid hormone induction and chicken ovalbumin upstream promoter transcription factor 1 repression. Mol Endocrinol 16(11):2439-2451
57. Xie J, Black DL (2001) A CaMK IV responsive RNA element mediates depolarization-induced alternative splicing of ion channels. Nature 410(6831):936-939 (Pubitemid 32335839)
58. Xie J, Jan C, Stoilov P et al (2005) A consensus CaMK IV-responsive RNA sequence mediates regulation of alternative exons in neurons. RNA 11(12):1825-1834 (Pubitemid 41720032)
59. Lee JA, Xing Y, Nguyen D et al (2007) Depolarization and CaM kinase IV modulate NMDA receptor splicing through two essential RNA elements. PLoS Biol 5(2):e40
60. Krebs J (2009) The influence of calcium signaling on the regulation of alternative splicing. Biochim Biophys Acta 1793(6):979-984
61. Xie J (2008) Control of alternative pre-mRNA splicing by Ca(++) signals. Biochim Biophys Acta 1779(8):438-452
62. Lagrutta A, Shen KZ, North RA et al (1994) Functional differences among alternatively spliced variants of Slowpoke, a Drosophila calcium-activated potassium channel. J Biol Chem 269(32):20347-20351 (Pubitemid 24260433)
63. Tseng-Crank J, Foster CD, Krause JD et al (1994) Cloning, expression, and distribution of functionally distinct Ca(2 +)-activated K+ channel isoforms from human brain. Neuron 13(6):1315-1330
64. Colomer J, Means AR (2007) Physiological roles of the Ca2+/CaM-dependent protein kinase cascade in health and disease. Subcell Biochem 45:169-214
65. Shepard PJ, Hertel KJ (2008) Conserved RNA secondary structures promote alternative splicing. RNA 14(8):1463-1469
66. Yu J, Hai Y, Liu G et al (2009) The heterogeneous nuclear ribonucleoprotein L is an essential component in the Ca2+/calmodulin-dependent protein kinase IV-regulated alternative splicing through cytidine-adenosine repeats. J Biol Chem 284(3):1505-1513
67. Hui J, Hung LH, Heiner M et al (2005) Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J 24(11):1988-1998 (Pubitemid 40896170)
68. Kessler F, Falchetto R, Heim R et al (1992) Study of calmodulin binding to the alternatively spliced C-terminal domain of the plasma membrane Ca2+ pump. Biochemistry 31(47):11785-11792
69. Bland CS, Wang ET, Vu A et al. (2010) Global regulation of alternative splicing during myogenic differentiation. Nucleic Acids Res 38:7651-7664
70. Guerini D, Wang X, Li L et al (2000) Calcineurin controls the expression of isoform 4CII of the plasma membrane Ca(2 +) pump in neurons. J Biol Chem 275(5):3706-3712 (Pubitemid 30083084)
71. Mikoshiba K (2007) IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J Neurochem 102(5):1426-1446
72. Nakagawa T, Okano H, Furuichi T et al (1991) The subtypes of the mouse inositol 1, 4, 5-trisphosphate receptor are expressed in a tissue-specific and developmentally specific manner. Proc Natl Acad Sci USA 88(14):6244-6248 (Pubitemid 21914923)
73. Nucifora FC Jr, Li SH, Danoff S et al (1995) Molecular cloning of a cDNA for the human inositol 1, 4, 5-trisphosphate receptor type 1, and the identification of a third alternatively spliced variant. Brain Res Mol Brain Res 32(2):291-296
74. Choi JY, Beaman-Hall CM, Vallano ML (2004) Granule neurons in cerebellum express distinct splice variants of the inositol trisphosphate receptor that are modulated by calcium. Am J Physiol Cell Physiol 287(4):C971-C980 (Pubitemid 39238321)
75. Rossi D, Simeoni I, Micheli M et al (2002) RyR1 and RyR3 isoforms provide distinct intracellular Ca2+ signals in HEK 293 cells. J Cell Sci 115(Pt 12):2497-2504 (Pubitemid 34778067)
76. Futatsugi A, Kuwajima G, Mikoshiba K (1995) Tissue-specific and developmentally regulated alternative splicing in mouse skeletal muscle ryanodine receptor mRNA. Biochem J 305(Pt 2):373-378
77. Takasawa S, Kuroki M, Nata K et al. (2010) A novel ryanodine receptor expressed in pancreatic islets by alternative splicing from type 2 ryanodine receptor gene. Biochem Biophys Res Commun 397(2):140-145
78. Leeb T, Brenig B (1998) cDNA cloning and sequencing of the human ryanodine receptor type 3 (RYR3) reveals a novel alternative splice site in the RYR3 gene. FEBS Lett 423(3):367-370 (Pubitemid 28129367)
79. Schroder M (2008) Endoplasmic reticulum stress responses. Cell Mol Life Sci 65(6):862-894
80. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569(1-2):29-63 (Pubitemid 39643256)
81. Rao RV, Poksay KS, Castro-Obregon S et al (2004) Molecular components of a cell death pathway activated by endoplasmic reticulum stress. J Biol Chem 279(1):177-187 (Pubitemid 38044813)
82. 2+ store: a view from the lumen. Trends Biochem Sci 23:10-14
83. Corbett EF, Michalak M (2000) Calcium, a signaling molecule in the endoplasmic reticulum? Trends Biochem Sci 25(7):307-311
84. Corbett EF, Michalak KM, Oikawa K et al (2000) The conformation of calreticulin is influenced by the endoplasmic reticulum lumenal environment. J Biol Chem 275:27177-27185
85. Booth C, Koch GEL (1989) Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell 59:729-737 (Pubitemid 19282880)
86. Lodish HF, Kong N (1990) Perturbation of cellular calcium blocks exit of secretory proteins from the rough endoplasmic reticulum. J Biol Chem 265:10893-10899
87. Lodish HF, Kong N, Wikstrom L (1992) Calcium is required for folding of newly made subunits of the asialoglycoprotein receptor within the endoplasmic reticulum. J Biol Chem 267:12753-12760
88. Molinari M, Helenius A (2000) Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288(5464):331-333 (Pubitemid 30226193)
89. Meunier L, Usherwood YK, Chung KT et al (2002) A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 13(12):4456-4469 (Pubitemid 35471198)
90. Argon Y, Simen BB (1999) GRP94, an ER chaperone with protein and peptide binding properties. Semin Cell Dev Biol 10(5):495-505 (Pubitemid 129513640)
91. Mengesdorf T, Althausen S, Oberndorfer I et al (2001) Response of neurons to an irreversible inhibition of endoplasmic reticulum Ca(2 +)-ATPase: relationship between global protein synthesis and expression and translation of individual genes. Biochem J 356(Pt 3):805-812
92. 2+-calmodulin-regulated actin-binding protein. J Biol Chem 264(25):15083-15087
93. Mao C, Wang M, Luo B et al. (2010) Targeted mutation of the mouse Grp94 gene disrupts development and perturbs endoplasmic reticulum stress signaling. PLoS One 5(5):e10852
94. 2+-ATPase inhibitor thapsigargin. J Biol Chem 268(16):12003-12009
95. Csermely P, Miyata Y, Schnaider T et al. (1995) Autophosphorylation of grp94 (endoplasmin). J Biol Chem 270(11):6381-6388
96. Edman JC, Ellis L, Blacher RW et al (1985) Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature 317(6034):267-270 (Pubitemid 16246506)
97. Noiva R (1999) Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Sem Cell Dev Biol 10(5):481-493
98. Oliver JD, van der Wal FJ, Bulleid NJ et al (1997) Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 275:86-88 (Pubitemid 27020314)
99. Molinari M, Helenius A (1999) Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402:90-93
100. Corbett EF, Oikawa K, Francois P et al (1999) Ca2+ regulation of interactions between endoplasmic reticulum chaperones. J Biol Chem 274(10):6203-6211 (Pubitemid 29111029)
101. Nakamura K, Zuppini A, Arnaudeau S et al (2001) Functional specialization of calreticulin domains. J Cell Biol 154(5):961-972 (Pubitemid 34286176)
102. Mesaeli N, Nakamura K, Zvaritch E et al (1999) Calreticulin is essential for cardiac development. J Cell Biol 144(5):857-868 (Pubitemid 29238963)
103. Martin V, Groenendyk J, Steiner SS et al (2006) Identification by mutational analysis of amino acid residues essential in the chaperone function of calreticulin. J Biol Chem 281(4):2338-2346 (Pubitemid 43845825)
104. Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14(1):20-28 (Pubitemid 38076857)
105. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33-45
106. Prostko CR, Dholakia JN, Brostrom MA et al (1995) Activation of the double-stranded RNA-regulated protein kinase by depletion of endoplasmic reticular calcium stores. J Biol Chem 270(11):6211-6215
107. Brostrom CO, Prostko CR, Kaufman RJ et al (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 2alpha kinase. J Biol Chem 271(40):24995-25002 (Pubitemid 26333258)
108. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum- resident kinase. Nature 397(6716):271-274 (Pubitemid 29051178)
109. Jeffery J, Kendall JM, Campbell AK (2000) Apoaequorin monitors degradation of endoplasmic reticulum (ER) proteins initiated by loss of ER Ca(2 +). Biochem Biophys Res Commun 268(3):711-715
110. Ma Y, Hendershot LM (2004) ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28(1-2):51-65 (Pubitemid 39195252)
111. Bertolotti A, Zhang Y, Hendershot LM et al (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2(6):326-332
112. DuRose JB, Scheuner D, Kaufman RJ et al (2009) Phosphorylation of eukaryotic translation initiation factor 2alpha coordinates rRNA transcription and translation inhibition during endoplasmic reticulum stress. Mol Cell Biol 29(15):4295-4307
113. Shen J, Chen X, Hendershot L et al (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3(1):99-111 (Pubitemid 34778399)
114. Cox JS, Shamu CE, Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197-1206 (Pubitemid 23180493)
115. Munro S, Pelham HR (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46(2):291-300
116. Kassenbrock CK, Kelly RB (1989) Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides. EMBO J 8(5):1461-1467 (Pubitemid 19274372)
117. Gaut JR, Hendershot LM (1993) Mutations within the nucleotide binding site of immunoglobulin-binding protein inhibit ATPase activity and interfere with release of immunoglobulin heavy chain. J Biol Chem 268(10):7248-7255 (Pubitemid 23105615)
118. 2+. J Biol Chem 272:30873-33089
119. Gething MJ (1999) Role and regulation of the ER chaperone BiP. Sem Cell Dev Biol 10(5):465-472
120. Suzuki CK, Bonifacino JS, Lin AY et al (1991) Regulating the retention of T-cell receptor alpha chain variants within the endoplasmic reticulum: Ca2+-dependent association with BiP. J Cell Biol 114(2):189-205 (Pubitemid 21909790)
121. Kozutsumi Y, Segal M, Normington K et al (1988) The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins.Nature 332(6163):462-464
122. Ni M, Zhou H, Wey S et al (2009) Regulation of PERK signaling and leukemic cell survival by a novel cytosolic isoform of the UPR regulator GRP78/BiP. PLoS One 4(8):e6868
123. Yoshida H, Haze K, Yanagi H et al (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273(50):33741-33749
124. Mori K, Kawahara T, Yoshida H et al (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 (Pubitemid 126670790)
125. Hong M, Luo S, Baumeister P et al (2004) Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J Biol Chem 279(12):11354-11363 (Pubitemid 38401633)
126. Yamamoto K, Sato T, Matsui T et al (2007) Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 13(3):365-376 (Pubitemid 47308680)
127. Thuerauf DJ, Morrison L, Glembotski CC (2004) Opposing roles for ATF6alpha and ATF6beta in endoplasmic reticulum stress response gene induction. J Biol Chem 279(20):21078-21084 (Pubitemid 38656510)
128. Hetz C, Glimcher LH (2009) Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome. Mol Cell 35(5):551-561
129. Schroder M, Kaufman RJ (2006)Divergent roles of IRE1alpha and PERK in the unfolded protein response. Curr Mol Med 6(1):5-36
130. Tirasophon W, Welihinda AA, Kaufman RJ (1998) A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 12:1812-1824 (Pubitemid 28304334)
131. Yoshida H, Matsui T, Yamamoto A et al (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(7):881-891 (Pubitemid 34084979)
132. Niwa M, Patil CK, DeRisi J et al (2005) Genome-scale approaches for discovering novel nonconventional splicing substrates of the Ire1 nuclease. Gen Biol 6(1):R3
133. Calfon M, Zeng H, Urano F et al (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415(6867):92-96 (Pubitemid 34062456)
134. Uemura A, Oku M, Mori K et al (2009) Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response. J Cell Sci 122(Pt 16):2877-2886
135. Lee KP, Dey M, Neculai D et al (2008) Structure of the dual enzyme Ire1 reveals the basis for catalysis and regulation in nonconventional RNA splicing. Cell 132(1):89-100
136. Yamamoto K, Yoshida H, Kokame K et al (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 136(3):343-350 (Pubitemid 39545794)
137. Lee K, Tirasophon W, Shen X et al (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev 16(4):452-466 (Pubitemid 34165102)
138. Rotin D and Staub O (2011) Role of the ubiquitin system in regulating ion transport. Pflugers Arch 461:1-21
139. Reimold AM, Etkin A, Clauss I et al (2000) An essential role in liver development for transcription factor XBP-1. Genes Dev 14(2):152-157 (Pubitemid 30070980)
140. Chen H, Qi L (2010) SUMO modification regulates transcriptional activity of XBP1. Biochem J 429:95-102
141. Urano F, Wang X, Bertolotti A et al (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287(5453):664-666 (Pubitemid 30070916)
142. Yoneda T, Imaizumi K, Oono K et al (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(17):13935-13940
143. Wanderling S, Simen BB, Ostrovsky O et al (2007) GRP94 is essential for mesoderm induction and muscle development because it regulates insulin-like growth factor secretion. Mol Biol Cell 18(10):3764-3775 (Pubitemid 47519471)
144. Yang Y, Liu B, Dai J et al (2007) Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26(2):215-226 (Pubitemid 46329432)
145. Martinon F, Chen X, Lee AH et al. (2010) TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol 11(5):411-418
146. Liu CY, Schroder M, Kaufman RJ (2000) Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J Biol Chem 275(32):24881-24885 (Pubitemid 30626593)
147. Harding HP, Novoa I, Zhang Y et al (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6(5):1099-1108
148. Scheuner D, Song B, McEwen E et al (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7(6):1165-1176 (Pubitemid 32607351)
149. Toth A, Nickson P, Mandl A et al (2007) Endoplasmic reticulum stress as a novel therapeutic target in heart diseases. Cardiovasc Hematol Disord Drug Targets 7(3):205-218 (Pubitemid 47496578)
150. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11(4):381-389 (Pubitemid 38489416)
151. Oyadomari S, Takeda K, Takiguchi M et al (2001) Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA 98(19):10845-10850 (Pubitemid 32878707)
152. Harding HP, Zeng H, Zhang Y et al (2001) Diabetes mellitus and exocrine pancreatic dysfunction in perk -/- mice reveals a role for translational control in secretory cell survival. Mol Cell 7(6):1153-1163 (Pubitemid 32607350)
153. Biamonti G, Caceres JF (2009) Cellular stress and RNA splicing. Trends Biochem Sci 34(3):146-153
154. Xie J, Lee JA, Kress TL et al (2003) Protein kinase A phosphorylation modulates transport of the polypyrimidine tractbinding protein. Proc Natl Acad Sci USA 100(15):8776-8781 (Pubitemid 36899175)
155. Daoud R, Mies G, Smialowska A et al (2002) Ischemia induces a translocation of the splicing factor tra2-beta 1 and changes alternative splicing patterns in the brain. J Neurosci 22(14):5889-5899 (Pubitemid 35387633)
156. Allemand E, Guil S, Myers M et al (2005) Regulation of heterogenous nuclear ribonucleoprotein A1 transport by phosphorylation in cells stressed by osmotic shock. Proc Natl Acad Sci USA 102(10):3605-3610 (Pubitemid 40354658)
157. van Oordt W, Diaz-Meco MT, Lozano J et al (2000) The MKK(3/6)-p38- signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J Cell Biol 149(2):307-316 (Pubitemid 30227149)
158. Lin JC, Hsu M, Tarn WY (2007) Cell stress modulates the function of splicing regulatory protein RBM4 in translation control. Proc Natl Acad Sci USA 104(7):2235-2240 (Pubitemid 46391381)
159. Shomron N, Alberstein M, Reznik M et al (2005) Stress alters the subcellular distribution of hSlu7 and thus modulates alternative splicing. J Cell Sci 118(Pt 6):1151-1159 (Pubitemid 40528686)
160. Hastings ML, Krainer AR (2001) Functions of SR proteins in the U12-dependent AT-AC pre-mRNA splicing pathway. RNA 7(3):471-482 (Pubitemid 32381920)
161. Shin C, Manley JL (2002) The SR protein SRp38 represses splicing in M phase cells. Cell 111(3):407-417 (Pubitemid 35341393)
162. Shin C, Feng Y, Manley JL (2004) Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 427(6974):553-558 (Pubitemid 38209114)
163. Montaville P, Dai Y, Cheung CY et al (2006) Nuclear translocation of the calcium-binding protein ALG-2 induced by the RNA-binding protein RBM22. Biochim Biophys Acta 1763(11):1335-1343 (Pubitemid 44779864)
164. Xu D, Friesen JD (2001) Splicing factor slt11p and its involvement in formation of U2/U6 helix II in activation of the yeast spliceosome. Mol Cell Biol 21(4):1011-1023 (Pubitemid 32114951)
165. Janowicz A, Michalak M, Krebs J (2010) Stress induced subcellular distribution of ALG-2, RMB22 and hSLU7. Biochem Biophys Acta, doi:10.1016/j.bbamcr.2010.11.010