Retarded PDI diffusion and a reductive shift in poise of the calcium depleted endoplasmic reticulum

BMC Biology

Volumn 13, Issue 1, 2015, Pages

  Avezov, Edward ^a   Konno, Tasuku ^a   Zyryanova, Alisa ^a   Chen, Weiyue ^b   Laine, Romain ^b   Crespillo Casado, Ana ^a   Melo, Pinho ^c   Ushioda, Ryo ^d   Nagata, Kazuhiro ^d   Kaminski, Clemens F ^b   Harding, Heather P ^a   Ron, David ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF ALGARVE   (Portugal)

^d KYOTO SANGYO UNIVERSITY   (Japan)

Author keywords

Calcium; Calreticulin; Endoplasmic reticulum; Fluorescence lifetime imaging; Protein disulfide isomerase; Redox

Indexed keywords

CALCIUM; CALRETICULIN; CHAPERONE; DISULFIDE; DNAJC10 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 40; PROTEIN BINDING; PROTEIN DISULFIDE ISOMERASE;

ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; DEFICIENCY; DIFFUSION; ENDOPLASMIC RETICULUM; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION;

ANIMALS; CALCIUM; CALRETICULIN; CERCOPITHECUS AETHIOPS; COS CELLS; DIFFUSION; DISULFIDES; ENDOPLASMIC RETICULUM; HEK293 CELLS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MICE; MOLECULAR CHAPERONES; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES;

EID: 84924613166     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-014-0112-2     Document Type: Article

References (33)

1. Hatahet F, Ruddock LW. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal. 2009;11:2807-50.
2. Givol D, Delorenzo F, Goldberger RF, Anfinsen CB. Disulfide interchange and the three-dimensional structure of proteins. Proc Natl Acad Sci U S A. 1965;53:676-84.
3. Bulleid NJ, Ellgaard L. Multiple ways to make disulfides. Trends Biochem Sci. 2011;36:485-92.
4. Ushioda R, Hoseki J, Araki K, Jansen G, Thomas DY, Nagata K. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science. 2008;321:569-72.
5. Oka OB, Pringle MA, Schopp IM, Braakman I, Bulleid NJ. ERdj5 is the ER reductase that catalyzes the removal of non-native disulfides and correct folding of the LDL receptor. Mol Cell. 2013;50:793-804.
6. Lohman JR, Remington SJ. Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments. Biochemistry. 2008;47:8678-88.
7. Birk J, Ramming T, Odermatt A, Appenzeller-Herzog C. Green fluorescent protein-based monitoring of endoplasmic reticulum redox poise. Front Genet. 2013;4:108.
8. van Lith M, Tiwari S, Pediani J, Milligan G, Bulleid NJ. Real-time monitoring of redox changes in the mammalian endoplasmic reticulum. J Cell Sci. 2011;124:2349-56.
9. Avezov E, Cross BC, Kaminski Schierle GS, Winters M, Harding HP, Melo EP, et al. Lifetime imaging of a fluorescent protein sensor reveals surprising stability of ER thiol redox. J Cell Biol. 2013;201:337-49.
10. Enyedi B, Varnai P, Geiszt M. Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid Redox Signal. 2010;13:721-9.
11. Mehmeti I, Lortz S, Lenzen S. The H2O2-sensitive HyPer protein targeted to the endoplasmic reticulum as a mirror of the oxidizing thiol-disulfide milieu. Free Radic Biol Med. 2012;53:1451-8.
12. Birk J, Meyer M, Aller I, Hansen HG, Odermatt A, Dick TP, et al. Endoplasmic reticulum: reduced and oxidized glutathione revisited. J Cell Sci. 2013;126:1604-17.
13. Corbett EF, Oikawa K, Francois P, Tessier DC, Kay C, Bergeron JJ, et al. Ca2+ regulation of interactions between endoplasmic reticulum chaperones. J Biol Chem. 1999;274:6203-11.
14. Wijeyesakere SJ, Gafni AA, Raghavan M. Calreticulin is a thermostable protein with distinct structural responses to different divalent cation environments. J Biol Chem. 2011;286:8771-85.
15. Berezin MY, Achilefu S. Fluorescence lifetime measurements and biological imaging. Chem Rev. 2010;110:2641-84.
16. Palmer AE, Jin C, Reed JC, Tsien RY. Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci U S A. 2004;101:17404-9.
17. Wang C, Yu J, Huo L, Wang L, Feng W, Wang CC. Human protein-disulfide isomerase is a redox-regulated chaperone activated by oxidation of domain a'. J Biol Chem. 2012;287:1139-49.
18. Hagiwara M, Maegawa K, Suzuki M, Ushioda R, Araki K, Matsumoto Y, et al. Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol Cell. 2011;41:432-44.
19. Kubisch CH, Logsdon CD. Secretagogues differentially activate endoplasmic reticulum stress responses in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1804-12.
20. Harding H, Zhang Y, Ron D. Translation and protein folding are coupled by an endoplasmic reticulum resident kinase. Nature. 1999;397:271-4.
21. Ashcroft SJ, Weerasinghe LC, Randle PJ. Interrelationship of islet metabolism, adenosine triphosphate content and insulin release. Biochem J. 1973;132:223-31.
22. Chin KT, Kang G, Qu J, Gardner LB, Coetzee WA, Zito E, et al. The sarcoplasmic reticulum luminal thiol oxidase ERO1 regulates cardiomyocyte excitation-coupled calcium release and response to hemodynamic load. FASEB J. 2011;25:2583-91.
23. Anelli T, Bergamelli L, Margittai E, Rimessi A, Fagioli C, Malgaroli A, et al. Ero1alpha regulates Ca(2+) fluxes at the endoplasmic reticulum-mitochondria interface (MAM). Antioxid Redox Signal. 2012;16:1077-87.
24. Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T, Mikoshiba K. Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell. 2005;120:85-98.
25. Li Y, Camacho P. Ca2 + -dependent redox modulation of SERCA 2b by ERp57. J Cell Biol. 2004;164:35-46.
26. Araki K, Iemura S, Kamiya Y, Ron D, Kato K, Natsume T, et al. Ero1-alpha and PDIs constitute a hierarchical electron transfer network of endoplasmic reticulum oxidoreductases. J Cell Biol. 2013;202:861-74.
27. Blais JD, Chin KT, Zito E, Zhang Y, Heldman N, Harding HP, et al. A small molecule inhibitor of endoplasmic reticulum oxidation 1 (ERO1) with selectively reversible thiol reactivity. J Biol Chem. 2010;285:20993-1003.
28. Tsunoda S, Avezov E, Zyryanova A, Konno T, Mendes-Silva L, Pinho Melo E, et al. Intact protein folding in the glutathione-depleted endoplasmic reticulum implicates alternative protein thiol reductants. Elife. 2014;3:e03421.
29. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, et al. Calreticulin is essential for cardiac development. J Cell Biol. 1999;144:857-68.
30. Ron D, Habener JF. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant negative inhibitor of gene transcription. Gene Dev. 1992;6:439-53.
31. Frank JH, Elder AD, Swartling J, Venkitaraman AR, Jeyasekharan AD, Kaminski CF. A white light confocal microscope for spectrally resolved multidimensional imaging. J Microsc. 2007;227:203-15.
32. Lleres D, Swift S, Lamond AI. Detecting protein-protein interactions in vivo with FRET using multiphoton fluorescence lifetime imaging microscopy (FLIM). Curr Protoc Cytom. 2007;Chapter 12:Unit12 10.
33. Esfandiarei M, Fameli N, Choi YY, Tehrani AY, Hoskins JG, van Breemen C. Waves of calcium depletion in the sarcoplasmic reticulum of vascular smooth muscle cells: an inside view of spatiotemporal Ca2+ regulation. PLoS One. 2013;8:e55333.