Palmitoylation is the switch that assigns calnexin to quality control or ER Ca2+ signaling

Journal of Cell Science

Volumn 126, Issue 17, 2013, Pages 3893-3903

  Lynes, Emily M ^a   Raturi, Arun ^a   Shenkman, Marina ^b   Sandoval, Carolina Ortiz ^a   Yap, Megan C ^a   Wu, Jiahui ^a   Janowicz, Aleksandra ^a   Myhill, Nathan ^a   Benson, Matthew D ^a   Campbell, Robert E ^a   Berthiaume, Luc G ^a   Lederkremer, Gerardo Z ^b   Simmen, Thomas ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Ca2+ signaling; Endoplasmic reticulum; ERp57; Mitochondria; Quality control; SERCA2b

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ASIALOGLYCOPROTEIN RECEPTOR; CALNEXIN; CYCLIN DEPENDENT KINASE INHIBITOR 1C; LOW DENSITY LIPOPROTEIN RECEPTOR; OXIDOREDUCTASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CELL MEMBRANE; CELL STRAIN 3T3; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FEMALE; HELA CELL; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MITOCHONDRION; MOUSE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; QUALITY CONTROL; REGULATORY MECHANISM;

CA2+ SIGNALING; ENDOPLASMIC RETICULUM; ERP57; MITOCHONDRIA; QUALITY CONTROL; SERCA2B;

3T3 CELLS; ANIMALS; CALCIUM; CALCIUM SIGNALING; CALNEXIN; CELL LINE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HUMANS; LIPOYLATION; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PROTEIN DISULFIDE-ISOMERASES; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 84883283648     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.125856     Document Type: Article

References (47)

1. 2+] in the endoplasmic reticulum with aequorin. Cell Calcium 32, 251-260.
2. Arnaudeau, S., Kelley, W. L., Walsh, J. V., Jr and Demaurex, N. (2001). Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J. Biol. Chem. 276, 29430-29439.
3. Avezov, E., Frenkel, Z., Ehrlich, M., Herscovics, A. and Lederkremer, G. Z. (2008). Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for Nglycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Mol. Biol. Cell 19, 216-225.
4. Baekkeskov, S. and Kanaani, J. (2009). Palmitoylation cycles and regulation of protein function (Review). Mol. Membr. Biol. 26, 42-54.
5. Baldwin, A. C., Green, C. D., Olson, L. K., Moxley, M. A. and Corbett, J. A. (2012). A role for aberrant protein palmitoylation in FFA-induced ER stress and b-cell death. Am. J. Physiol. 302, E1390-E1398.
6. Bravo, R., Vicencio, J. M., Parra, V., Troncoso, R., Munoz, J. P., Bui, M., Quiroga, C., Rodriguez, A. E., Verdejo, H. E., Ferreira, J. et al. (2011). Increased ERmitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J. Cell Sci. 124, 2143-2152.
7. 2+ transfer to mitochondria. Cell 142, 270-283.
8. Chevet, E., Wong, H. N., Gerber, D., Cochet, C., Fazel, A., Cameron, P. H., Gushue, J. N., Thomas, D. Y. and Bergeron, J. J. (1999). Phosphorylation by CK2 and MAPK enhances calnexin association with ribosomes. EMBO J. 18, 3655-3666.
9. Coe, H. and Michalak, M. (2010). ERp57, a multifunctional endoplasmic reticulum resident oxidoreductase. Int. J. Biochem. Cell Biol. 42, 796-799.
10. Coe, H., Bedard, K., Groenendyk, J., Jung, J. and Michalak, M. (2008). Endoplasmic reticulum stress in the absence of calnexin. Cell Stress Chaperones 13, 497-507.
11. Csordá s, G., Renken, C., Várnai, P., Walter, L., Weaver, D., Buttle, K. F., Balla, T., Mannella, C. A. and Hajnóczky, G. (2006). Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915-921.
12. de Brito, O. M. and Scorrano, L. (2008). Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610.
13. Delom, F., Fessart, D. and Chevet, E. (2007). Regulation of calnexin sub-cellular localization modulates endoplasmic reticulum stress-induced apoptosis in MCF-7 cells. Apoptosis 12, 293-305.
14. Dowal, L., Yang, W., Freeman, M. R., Steen, H. and Flaumenhaft, R. (2011). Proteomic analysis of palmitoylated platelet proteins. Blood 118, e62-e73.
15. Ferrera, D., Panigada, M., Porcellini, S. and Grassi, F. (2008). Recombinasedeficient T cell development by selective accumulation of CD3 into lipid rafts. Eur. J. Immunol. 38, 1148-1156.
16. Frenkel, Z., Shenkman, M., Kondratyev, M. and Lederkremer, G. Z. (2004). Separate roles and different routing of calnexin and ERp57 in endoplasmic reticulum quality control revealed by interactions with asialoglycoprotein receptor chains. Mol. Biol. Cell 15, 2133-2142.
17. Gilady, S. Y., Bui, M., Lynes, E. M., Benson, M. D., Watts, R., Vance, J. E. and Simmen, T. (2010). Ero1alpha requires oxidizing and normoxic conditions to localize to the mitochondria-associated membrane (MAM). Cell Stress Chaperones 15, 619- 629.
18. 2+ in the regulation of cellular energetics. Biochemistry 51, 2959-2973.
19. Hayashi, T. and Su, T. P. (2007). Sigma-1 receptor chaperones at the ERmitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131, 596- 610.
20. Higo, T., Hattori, M., Nakamura, T., Natsume, T., Michikawa, T. and Mikoshiba, K. (2005). Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 120, 85-98.
21. Jessop, C. E., Chakravarthi, S., Garbi, N., Hämmerling, G. J., Lovell, S. and Bulleid, N. J. (2007). ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J. 26, 28-40.
22. Kamhi-Nesher, S., Shenkman, M., Tolchinsky, S., Fromm, S. V., Ehrlich, R. and Lederkremer, G. Z. (2001). A novel quality control compartment derived from the endoplasmic reticulum. Mol. Biol. Cell 12, 1711-1723.
23. Kang, R., Wan, J., Arstikaitis, P., Takahashi, H., Huang, K., Bailey, A. O., Thompson, J. X., Roth, A. F., Drisdel, R. C., Mastro, R. et al. (2008). Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456, 904-909.
24. Kondratyev, M., Avezov, E., Shenkman, M., Groisman, B. and Lederkremer, G. Z. (2007). PERK-dependent compartmentalization of ERAD and unfolded protein response machineries during ER stress. Exp. Cell Res. 313, 3395-3407.
25. Kraus, A., Groenendyk, J., Bedard, K., Baldwin, T. A., Krause, K. H., Dubois-Dauphin, M., Dyck, J., Rosenbaum, E. E., Korngut, L., Colley, N. J. et al. (2010). Calnexin deficiency leads to dysmyelination. J. Biol. Chem. 285, 18928-18938.
26. Lakkaraju, A. K., Abrami, L., Lemmin, T., Blaskovic, S., Kunz, B., Kihara, A., Dal Peraro, M. and van der Goot, F. G. (2012). Palmitoylated calnexin is a key component of the ribosome-translocon complex. EMBO J. 31, 1823-1835.
27. Lederkremer, G. Z. (2009). Glycoprotein folding, quality control and ER-associated degradation. Curr. Opin. Struct. Biol. 19, 515-523.
28. Leitman, J., Ron, E., Ogen-Shtern, N. and Lederkremer, G. Z. (2013). Compartmentalization of endoplasmic reticulum quality control and er-associated degradation factors. DNA Cell Biol. 32, 2-7.
29. Li, G., Mongillo, M., Chin, K. T., Harding, H., Ron, D., Marks, A. R. and Tabas, I. (2009). Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J. Cell Biol. 186, 783-792.
30. Lynes, E. M., Bui, M., Yap, M. C., Benson, M. D., Schneider, B., Ellgaard, L., Berthiaume, L. G. and Simmen, T. (2012). Palmitoylated TMX and calnexin target to the mitochondria-associated membrane. EMBO J. 31, 457-470.
31. Myhill, N., Lynes, E. M., Nanji, J. A., Blagoveshchenskaya, A. D., Fei, H., Carmine Simmen, K., Cooper, T. J., Thomas, G. and Simmen, T. (2008). The subcellular distribution of calnexin is mediated by PACS-2. Mol. Biol. Cell 19, 2777-2788.
32. Oliver, J. D., van der Wal, F. J., Bulleid, N. J. and High, S. (1997). Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 275, 86-88.
33. Raturi, A. and Simmen, T. (2013). Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim. Biophys. Acta. 1833, 213-224.
34. Rizzuto, R., Marchi, S., Bonora, M., Aguiari, P., Bononi, A., De Stefani, D., Giorgi, C., Leo, S., Rimessi, A., Siviero, R. et al. (2009). Ca(2+) transfer from the ER to mitochondria: when, how and why. Biochim. Biophys. Acta 1787, 1342-1351.
35. Roderick, H. L., Lechleiter, J. D. and Camacho, P. (2000). Cytosolic phosphorylation of calnexin controls intracellular Ca(2+) oscillations via an interaction with SERCA2b. J. Cell Biol. 149, 1235-1248.
36. Ruddock, L. W. and Molinari, M. (2006). N-glycan processing in ER quality control. J. Cell Sci. 119, 4373-4380.
37. Rusch, M., Zimmermann, T. J., Bürger, M., Dekker, F. J., Görmer, K., Triola, G., Brockmeyer, A., Janning, P., Böttcher, T., Sieber, S. A. et al. (2011). Identification of acyl protein thioesterases 1 and 2 as the cellular targets of the Ras-signaling modulators palmostatin B and M. Angew. Chem. Int. Ed. Engl. 50, 9838-9842.
38. Rutkevich, L. A. and Williams, D. B. (2011). Participation of lectin chaperones and thiol oxidoreductases in protein folding within the endoplasmic reticulum. Curr. Opin. Cell Biol. 23, 157-166.
39. Shenkman, M., Ayalon, M. and Lederkremer, G. Z. (1997). Endoplasmic reticulum quality control of asialoglycoprotein receptor H2a involves a determinant for retention and not retrieval. Proc. Natl. Acad. Sci. USA 94, 11363-11368.
40. Simmen, T., Lynes, E. M., Gesson, K. and Thomas, G. (2010). Oxidative protein folding in the endoplasmic reticulum: tight links to the mitochondria-associated membrane (MAM). Biochim. Biophys. Acta 1798, 1465-1473.
41. Tolchinsky, S., Yuk, M. H., Ayalon, M., Lodish, H. F. and Lederkremer, G. Z. (1996). Membrane-bound versus secreted forms of human asialoglycoprotein receptor subunits. Role of a juxtamembrane pentapeptide. J. Biol. Chem. 271, 14496-14503.
42. Wang, S. and Kaufman, R. J. (2012). The impact of the unfolded protein response on human disease. J. Cell Biol. 197, 857-867.
43. Wieckowski, M. R., Giorgi, C., Lebiedzinska, M., Duszynski, J. and Pinton, P. (2009). Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat. Protoc. 4, 1582-1590.
44. Zapun, A., Darby, N. J., Tessier, D. C., Michalak, M., Bergeron, J. J. and Thomas, D. Y. (1998). Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J. Biol. Chem. 273, 6009-6012.
45. 2+ indicators. Science 333, 1888-1891.
46. Zhivotovsky, B. and Orrenius, S. (2011). Calcium and cell death mechanisms: a perspective from the cell death community. Cell Calcium 50, 211-221.
47. Zuppini, A., Groenendyk, J., Cormack, L. A., Shore, G., Opas, M., Bleackley, R. C. and Michalak, M. (2002). Calnexin deficiency and endoplasmic reticulum stressinduced apoptosis. Biochemistry 41, 2850-2858.