PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2014 | 1 | 1 |
Tytuł artykułu

Approaches to imaging unfolded secretory protein stress in living cells

Treść / Zawartość
Warianty tytułu
Języki publikacji
EN
Abstrakty
EN
The endoplasmic reticulum (ER) is the point of entry of proteins into the secretory pathway. Nascent peptides interact with the ER quality control machinery that ensures correct folding of the nascent proteins. Failure to properly fold proteins can lead to loss of protein function and cytotoxic aggregation of misfolded proteins that can lead to cell death. To cope with increases in the ER unfolded secretory protein burden, cells have evolved the Unfolded Protein Response (UPR). The UPR is the primary signaling pathway that monitors the state of the ER folding environment. When the unfolded protein burden overwhelms the capacity of the ER quality control machinery, a state termed ER stress, sensor proteins detect accumulation of misfolded peptides and trigger the UPR transcriptional response. The UPR, which is conserved from yeast to mammals, consists of an ensemble of complex signaling pathways that aims at adapting the ER to the new misfolded protein load. To determine how different factors impact the ER folding environment, various tools and assays have been developed. In this review, we discuss recent advances in live cell imaging reporters and model systems that enable researchers to monitor changes in the unfolded secretory protein burden and activation of the UPR and its associated signaling pathways.
Wydawca

Rocznik
Tom
1
Numer
1
Opis fizyczny
Daty
wydano
2014-01-01
otrzymano
2014-03-08
zaakceptowano
2014-04-06
online
2014-05-17
Twórcy
  • Department of Anatomy and Cell Biology, University of Western Ontario, London, Ontario N6A 5C1, Canada, Phone: 519-661-2111 x88220, plajoie3@uwo.ca
  • Department of Anatomy and Cell Biology, University of Western Ontario, London, Ontario, Canada
  • Department of Anatomy and Structural Biology, AlbERt Einstein College of Medicine, Forchheimer 640, 1300 Morris Park Avenue, Bronx, NY 10461, USA, erik-lee.snapp@einstein.yu.edu
Bibliografia
  • [1] Walter, P. and D. Ron, The unfolded protein response: from stress pathway to homeostatic regulation. Science, 2011. 334(6059): p. 1081-6.
  • [2] Kozutsumi, Y., et al., The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucoseregulated proteins. Nature, 1988. 332(6163): p. 462-4.
  • [3] Pavitt, G.D. and D. Ron, New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb Perspect Biol, 2012. 4(6).
  • [4] Hetz, C., et al., Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science, 2006. 312(5773): p. 572-6.
  • [5] Tabas, I. and D. Ron, Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol, 2011. 13(3): p. 184-90.[Crossref]
  • [6] Upton, J.P., et al., IRE1alpha cleaves select microRNAs during ER stress to derepress translation of proapoptotic Caspase-2. Science, 2012. 338(6108): p. 818-22.
  • [7] Rutkowski, D.T. and R.J. Kaufman, That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci, 2007. 32(10): p. 469-76.[Crossref]
  • [8] Mori, K., Signalling pathways in the unfolded protein response: development from yeast to mammals. J Biochem, 2009. 146(6): p. 743-50.
  • [9] Cox, J.S. and P. Walter, A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell, 1996. 87(3): p. 391-404.[Crossref]
  • [10] Travers, K.J., et al., Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell, 2000. 101(3): p. 249-58.[Crossref]
  • [11] Chawla, A., et al., Attenuation of yeast UPR is essential for survival and is mediated by IRE1 kinase. J Cell Biol, 2011. 193(1): p. 41-50.
  • [12] Rubio, C., et al., Homeostatic adaptation to endoplasmic reticulum stress depends on Ire1 kinase activity. J Cell Biol, 2011. 193(1): p. 171-84.
  • [13] Bertolotti, A., et al., Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol, 2000. 2(6): p. 326-32.
  • [14] Okada, T., et al., Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J, 2002. 366(Pt 2): p. 585-94.
  • [15] Lee, A.H., N.N. Iwakoshi, and L.H. Glimcher, XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol, 2003. 23(21): p. 7448-59.
  • [16] Oda, Y., et al., Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J Cell Biol, 2006. 172(3): p. 383-93.
  • [17] Hebert, D.N. and M. Molinari, In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol Rev, 2007. 87(4): p. 1377-408.[Crossref]
  • [18] Ron, D. and P. Walter, Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol, 2007. 8(7): p. 519-29.[Crossref]
  • [19] Bernales, S., F.R. Papa, and P. Walter, Intracellular signaling by the unfolded protein response. Annu Rev Cell Dev Biol, 2006. 22: p. 487-508.[Crossref]
  • [20] Malhotra, J.D. and R.J. Kaufman, The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol, 2007. 18(6): p. 716-31.[Crossref]
  • [21] Yoshida, H., ER stress and diseases. Febs J, 2007. 274(3): p. 630-58.
  • [22] Credle, J.J., et al., On the mechanism of sensing unfolded protein in the endoplasmic reticulum. Proc Natl Acad Sci U S A, 2005. 102(52): p. 18773-84.[Crossref]
  • [23] Gardner, B.M. and P. Walter, Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science, 2011. 333(6051): p. 1891-4.
  • [24] Pincus, D., et al., BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biol, 2010. 8(7): p. e1000415.[Crossref]
  • [25] Promlek, T., et al., Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways. Mol Biol Cell, 2011. 22(18): p. 3520-32.[Crossref]
  • [26] Harding, H.P., et al., Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell, 2000. 6(5): p. 1099-108.[Crossref]
  • [27] Harding, H.P., Y. Zhang, and D. Ron, Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature, 1999. 397(6716): p. 271-4.
  • [28] Shen, J., et al., ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell, 2002. 3(1): p. 99-111.
  • [29] Rutkowski, D.T. and R.J. Kaufman, A trip to the ER: coping with stress. Trends Cell Biol, 2004. 14(1): p. 20-8.[Crossref]
  • [30] Hetz, C. and L.H. Glimcher, Protein homeostasis networks in physiology and disease. Curr Opin Cell Biol, 2011. 23(2): p. 123-5.[Crossref]
  • [31] Vidal, R., et al., Converging pathways in the occurrence of endoplasmic reticulum (ER) stress in Huntington’s disease. Curr Mol Med, 2011. 11(1): p. 1-12.[Crossref]
  • [32] Imrie, D. and K.C. Sadler, Stress management: How the unfolded protein response impacts fatty liver disease. J Hepatol, 2012. 57(5): p. 1147-51.[Crossref]
  • [33] Wang, W.A., J. Groenendyk, and M. Michalak, Endoplasmic reticulum stress associated responses in cancer. Biochim Biophys Acta, 2014.
  • [34] Cawley, K., et al., Assays for detecting the unfolded protein response. Methods Enzymol, 2011. 490: p. 31-51.
  • [35] Back, S.H., et al., ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods, 2005. 35(4): p. 395-416.
  • [36] Shang, J., Quantitative measurement of events in the mammalian unfolded protein response. Methods, 2005. 35(4): p. 390-4.[Crossref]
  • [37] Qi, L., L. Yang, and H. Chen, Detecting and quantitating physiological endoplasmic reticulum stress. Methods Enzymol, 2011. 490: p. 137-46.
  • [38] Oslowski, C.M. and F. Urano, Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods Enzymol, 2011. 490: p. 71-92.
  • [39] Niepel, M., S.L. Spencer, and P.K. Sorger, Non-genetic cell-to-cell variability and the consequences for pharmacology. Curr Opin Chem Biol, 2009. 13(5-6): p. 556-61.[Crossref]
  • [40] Lippincott-Schwartz, J., E. Snapp, and A. Kenworthy, Studying protein dynamics in living cells. Nat Rev Mol Cell Biol, 2001. 2(6): p. 444-56.[Crossref]
  • [41] Miyawaki, A., Development of probes for cellular functions using fluorescent proteins and fluorescence resonance energy transfer. Annu Rev Biochem, 2011. 80: p. 357-73.[Crossref]
  • [42] Costantini, L.M. and E.L. Snapp, Fluorescent proteins in cellular organelles: serious pitfalls and some solutions. DNA and cell biology, 2013. 32(11): p. 622-7.[Crossref]
  • [43] Tsien, R.Y. and A. Miyawaki, Seeing the machinery of live cells. Science, 1998. 280(5371): p. 1954-5.
  • [44] Smith, M.H., H.L. Ploegh, and J.S. Weissman, Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science, 2011. 334(6059): p. 1086-90.
  • [45] Bernasconi, R. and M. Molinari, ERAD and ERAD tuning: disposal of cargo and of ERAD regulators from the mammalian ER. Curr Opin Cell Biol, 2011. 23(2): p. 176-83.[Crossref]
  • [46] Costantini, L.M. and E.L. Snapp, Fluorescent proteins in cellular organelles: serious pitfalls and some solutions. DNA Cell Biol, 2013. 32(11): p. 622-7. [Crossref]
  • [47] Costantini, L.M., et al., Cysteineless non-glycosylated monomeric blue fluorescent protein, secBFP2, for studies in the eukaryotic secretory pathway. Biochem Biophys Res Commun, 2013. 430(3): p. 1114-9.
  • [48] Suzuki, T., et al., Development of cysteine-free fluorescent proteins for the oxidative environment. PLoS One, 2012. 7(5): p. e37551.[Crossref]
  • [49] Snapp, E., N. Altan-Bonnet, and J. Lippincott-Schwartz, Measuring protein mobility by photobleaching GFP-chimeras in living cells., in Current Protocols in Cell Biology, J.S. Bonafacino, et al., Editors. 2003, John Wiley&Sons, Inc.: New York. p. Unit 21.1.
  • [50] Zacharias, D.A., Sticky caveats in an otherwise glowing report: oligomerizing fluorescent proteins and their use in cell biology. Sci STKE, 2002. 2002(131): p. pe23.
  • [51] Hink, M.A., et al., Structural dynamics of green fluorescent protein alone and fused with a single chain Fv protein. J Biol Chem, 2000. 275(23): p. 17556-60.
  • [52] Snapp, E.L., et al., The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells. J Cell Biol, 2004. 164(7): p. 997-1007.
  • [53] Shaner, N.C., G.H. Patterson, and M.W. Davidson, Advances in fluorescent protein technology. J Cell Sci, 2007. 120(Pt 24): p. 4247-60.
  • [54] Moir, R.D., et al., SCS3 and YFT2 link transcription of phospholipid biosynthetic genes to ER stress and the UPR. PLoS Genet, 2012. 8(8): p. e1002890.[Crossref]
  • [55] Jonikas, M.C., et al., Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science, 2009. 323(5922): p. 1693-7.
  • [56] Pedelacq, J.D., et al., Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol, 2006. 24(1): p. 79-88.[Crossref]
  • [57] Aronson, D.E., L.M. Costantini, and E.L. Snapp, Superfolder GFP is fluorescent in oxidizing environments when targeted via the Sec translocon. Traffic, 2011. 12(5): p. 543-8.[Crossref]
  • [58] Shemiakina, II, et al., A monomeric red fluorescent protein with low cytotoxicity. Nat Commun, 2012. 3: p. 1204.[Crossref]
  • [59] Shaner, N.C., et al., A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nat Methods, 2013. 10(5): p. 407-9.[Crossref]
  • [60] Merzlyak, E.M., et al., Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods, 2007. 4(7): p. 555-7.[Crossref]
  • [61] Merksamer, P.I., A. Trusina, and F.R. Papa, Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell, 2008. 135(5): p. 933-47.
  • [62] Lajoie, P., et al., Kar2p availability defines distinct forms of endoplasmic reticulum stress in living cells. Mol Biol Cell, 2012. 23(5): p. 955-64.[Crossref]
  • [63] Young, C.L., D.L. Raden, and A.S. Robinson, Analysis of ER resident proteins in Saccharomyces cerevisiae: implementation of H/KDEL retrieval sequences. Traffic, 2013. 14(4): p. 365-81.[Crossref]
  • [64] Calfon, M., et al., IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature, 2002. 415(6867): p. 92-6.
  • [65] Luo, S., et al., Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J Biol Chem, 2003. 278(39): p. 37375-85.
  • [66] Lajoie, P. and E.L. Snapp, Changes in BiP availability reveal hypersensitivity to acute endoplasmic reticulum stress in cells expressing mutant huntingtin. J Cell Sci, 2011. 124(Pt 19): p. 3332-43.[Crossref]
  • [67] Rutkowski, D.T., et al., Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol, 2006. 4(11): p. e374.[Crossref]
  • [68] Novoa, I., et al., Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol, 2001. 153(5): p. 1011-22.
  • [69] Lu, P.D., H.P. Harding, and D. Ron, Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol, 2004. 167(1): p. 27-33.
  • [70] Shamu, C.E. and P. Walter, Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO, 1996. 15(12): p. 3028-3039.
  • [71] Aragon, T., et al., Messenger RNA targeting to endoplasmic reticulum stress signalling sites. Nature, 2009. 457(7230): p. 736-40.
  • [72] Ishiwata-Kimata, Y., et al., F-actin and a type-II myosin are required for efficient clustering of the ER stress sensor Ire1. Cell Struct Funct, 2013. 38(2): p. 135-43.[Crossref]
  • [73] Li, H., et al., Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc Natl Acad Sci U S A, 2010. 107(37): p. 16113-8.[Crossref]
  • [74] Bunt, G. and F.S. Wouters, Visualization of molecular activities inside living cells with fluorescent labels. Int Rev Cytol, 2004. 237: p. 205-77.
  • [75] Wallrabe, H. and A. Periasamy, Imaging protein molecules using FRET and FLIM microscopy. Curr Opin Biotechnol, 2005. 16(1): p. 19-27.[Crossref]
  • [76] Shim, J., et al., The unfolded protein response regulates glutamate receptor export from the endoplasmic reticulum. Mol Biol Cell, 2004. 15(11): p. 4818-28.[Crossref]
  • [77] Ryoo, H.D., et al., Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J, 2007. 26(1): p. 242-52.[Crossref]
  • [78] Back, S.H., et al., Cytoplasmic IRE1alpha-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress. J Biol Chem, 2006. 281(27): p. 18691-706.
  • [79] Iwawaki, T., et al., A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med, 2004. 10(1): p. 98-102.[Crossref]
  • [80] Kimata, Y., et al., A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J Cell Biol, 2004. 167(3): p. 445-56.
  • [81] Lai, C.W., D.E. Aronson, and E.L. Snapp, BiP availability distinguishes states of homeostasis and stress in the endoplasmic reticulum of living cells. Mol Biol Cell, 2010. 21(12): p. 1909-21.[Crossref]
  • [82] Siggia, E.D., J. Lippincott-Schwartz, and S. Bekiranov, Diffusion in inhomogeneous media: theory and simulations applied to whole cell photobleach recovery. Biophys J, 2000. 79(4): p. 1761-70.[Crossref]
  • [83] Volmer, R., K. van der Ploeg, and D. Ron, Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci U S A, 2013. 110(12): p. 4628-33. [Crossref]
  • [84] McCombs, J.E. and A.E. Palmer, Measuring calcium dynamics in living cells with genetically encodable calcium indicators. Methods, 2008. 46(3): p. 152-9.[Crossref]
  • [85] Palmer, A.E., et al., Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci U S A, 2004. 101(50): p. 17404-9.[Crossref]
  • [86] Avezov, E., et al., Lifetime imaging of a fluorescent protein sensor reveals surprising stability of ER thiol redox. J Cell Biol, 2013. 201(2): p. 337-49.
  • [87] Palmer, A.E. and R.Y. Tsien, Measuring calcium signaling using genetically targetable fluorescent indicators. Nat Protoc, 2006. 1(3): p. 1057-65.
  • [88] Brini, M., et al., A calcium signaling defect in the pathogenesis of a mitochondrial DNA inherited oxidative phosphorylation deficiency. Nat Med, 1999. 5(8): p. 951-4.
  • [89] Zhang, L.Y., et al., Bioluminescence Assisted Switching and Fluorescence Imaging (BASFI). Journal of Physical Chemistry Letters, 2013. 4(22): p. 3897-3902.[Crossref]
  • [90] Menendez-Benito, V., et al., Endoplasmic reticulum stress compromises the ubiquitin-proteasome system. Hum Mol Genet, 2005. 14(19): p. 2787-99.[Crossref]
  • [91] Cabantous, S., T.C. Terwilliger, and G.S. Waldo, Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat Biotechnol, 2005. 23(1): p. 102-7.[Crossref]
  • [92] Zhong, Y. and S. Fang, Live cell imaging of protein dislocation from the endoplasmic reticulum. J Biol Chem, 2012. 287(33): p. 28057-66.
  • [93] Grotzke, J.E., Q. Lu, and P. Cresswell, Deglycosylation-dependent fluorescent proteins provide unique tools for the study of ER-associated degradation. Proc Natl Acad Sci U S A, 2013. 110(9): p. 3393-8.[Crossref]
  • [94] Frand, A.R. and C.A. Kaiser, The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell, 1998. 1(2): p. 161-70.[Crossref]
  • [95] Tu, B.P., et al., Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science, 2000. 290(5496): p. 1571-4.
  • [96] Zito, E., et al., ERO1-beta, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis. J Cell Biol, 2010. 188(6): p. 821-32.
  • [97] Zito, E., et al., Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin. Mol Cell, 2010. 40(5): p. 787-97.[Crossref]
  • [98] Jessop, C.E., et al., Oxidative protein folding in the mammalian endoplasmic reticulum. Biochem Soc Trans, 2004. 32(Pt 5): p. 655-8.
  • [99] Bjornberg, O., H. Ostergaard, and J.R. Winther, Measuring intracellular redox conditions using GFP-based sensors. Antioxid Redox Signal, 2006. 8(3-4): p. 354-61.[Crossref]
  • [100] Hanson, G.T., et al., Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem, 2004. 279(13): p. 13044-53.
  • [101] van Lith, M., et al., Real-time monitoring of redox changes in the mammalian endoplasmic reticulum. J Cell Sci, 2011. 124(Pt 14): p. 2349-56.[Crossref]
  • [102] Mao, C., et al., In vivo regulation of Grp78/BiP transcription in the embryonic heart: role of the endoplasmic reticulum stress response element and GATA-4. J Biol Chem, 2006. 281(13): p. 8877-87.
  • [103] Mali, P., K.M. Esvelt, and G.M. Church, Cas9 as a versatile tool for engineering biology. Nat Methods, 2013. 10(10): p. 957-63.[Crossref]
  • [104] Pennisi, E., The CRISPR craze. Science, 2013. 341(6148): p. 833-6.
  • [105] Dickinson, D.J., et al., Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods, 2013. 10(10): p. 1028-34.[Crossref]
  • [106] Niswender, K.D., et al., Quantitative imaging of green fluorescent protein in cultured cells: comparison of microscopic techniques, use in fusion proteins and detection limits. J Microsc, 1995. 180(Pt 2): p. 109-16.
  • [107] Johnson, E.S., et al., A proteolytic pathway that recognizes ubiquitin as a degradation signal. J Biol Chem, 1995. 270(29): p. 17442-56.
  • [108] Li, X., et al., Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem, 1998. 273(52): p. 34970-5.
  • [109] Subach, F.V., et al., Monomeric fluorescent timers that change color from blue to red report on cellular trafficking. Nat Chem Biol, 2009. 5(2): p. 118-26.[Crossref]
  • [110] Gaietta, G., et al., Multicolor and electron microscopic imaging of connexin trafficking. Science, 2002. 296(5567): p. 503-7.
  • [111] Martin, B.R., et al., Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity. Nat Biotechnol, 2005. 23(10): p. 1308-14.[Crossref]
  • [112] Gaietta, G.M., et al., Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc Natl Acad Sci U S A, 2006. 103(47): p. 17777-82. [Crossref]
Typ dokumentu
Bibliografia
Identyfikatory
Identyfikator YADDA
bwmeta1.element.-psjd-doi-10_2478_ersc-2014-0002
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.