Limitation of individual folding resources in the ER leads to outcomes distinct from the unfolded protein response

Journal of Cell Science

Volumn 125, Issue 20, 2012, Pages 4865-4875

  Eletto, Davide ^a   Maganty, Avinash ^a,g   Eletto, Daniela ^a,b   Dersh, Devin ^a,c   Makarewich, Catherine ^a,h   Biswas, Chhanda ^a,d   Paton, James C ^e   Paton, Adrienne W ^e   Doroudgar, Shirin ^f   Glembotski, Christopher C ^f   Argon, Yair ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF SALERNO   (Italy)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF ADELAIDE   (Australia)

^f SAN DIEGO STATE UNIVERSITY   (United States)

^g WEILL CORNELL MEDICAL COLLEGE   (United States)

^h TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALRETICULIN; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; HEAT SHOCK PROTEIN 47; MESSENGER RNA; PROTEIN DISULFIDE ISOMERASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHEMICAL STRESS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GENE SILENCING; GENE TARGETING; GENETIC CODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; NIH 3T3 CELLS; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84872194587     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.108928     Document Type: Article

References (53)

1. Bagatell, R., Paine-Murrieta, G. D., Taylor, C. W., Pulcini, E. J., Akinaga, S., Benjamin, I. J. and Whitesell, L. (2000). Induction of a heat shock factor 1-dependent stress response alters the cytotoxic activity of hsp90-binding agents. Clin. Cancer Res. 6, 3312-3318.
2. Balch, W. E., Morimoto, R. I., Dillin, A. and Kelly, J. W. (2008). Adapting proteostasis for disease intervention. Science 319, 916-919.
3. Bartke, A. (2009). The somatotropic axis and aging: mechanisms and persistent questions about practical implications. Exp. Gerontol. 44, 372-374.
4. Barton, E. R., DeMeo, J. and Lei, H. (2010). The insulin-like growth factor (IGF)-I Epeptides are required for isoform-specific gene expression and muscle hypertrophy after local IGF-I production. J. Appl. Physiol. 108, 1069-1076.
5. Barton, E. R., Park, S., James, J. K., Makarewich, C. A., Philippou, A., Eletto, D., Lei, H., Brisson, B., Ostrovsky, O., Li, Z. and Argon, Y. (2012). Deletion of muscle GRP94 impairs both muscle and body growth by inhibiting local IGF production. FASEB J. 26, 3691-3702.
6. Biswas, C., Ostrovsky, O., Makarewich, C. A., Wanderling, S., Gidalevitz, T. and Argon, Y. (2007). The peptide-binding activity of GRP94 is regulated by calcium. Biochem. J. 405, 233-241.
7. Burnett, H. F., Audas, T. E., Liang, G. and Lu, R. R. (2012). Herpes simplex virus-1 disarms the unfolded protein response in the early stages of infection. Cell Stress Chaperones 17, 473-483.
8. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G. and Ron, D. (2002). IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
9. Chang, S. C., Erwin, A. E. and Lee, A. S. (1989). Glucose-regulated protein (GRP94 and GRP78) genes share common regulatory domains and are coordinately regulated by common trans-acting factors. Mol. Cell. Biol. 9, 2153-2162.
10. Christianson, J. C., Shaler, T. A., Tyler, R. E. and Kopito, R. R. (2008). OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10, 272-282.
11. Dorner, A. J., Wasley, L. C. and Kaufman, R. J. (1992). Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO J. 11, 1563-1571.
12. Doroudgar, S., Thuerauf, D. J., Marcinko, M. C., Belmont, P. J. and Glembotski, C. C. (2009). Ischemia activates the ATF6 branch of the endoplasmic reticulum stress response. J. Biol. Chem. 284, 29735-29745.
13. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H. and Ron, D. (2000). Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904.
14. Hartley, T., Siva, M., Lai, E., Teodoro, T., Zhang, L. and Volchuk, A. (2010). Endoplasmic reticulum stress response in an INS-1 pancreatic beta-cell line with inducible expression of a folding-deficient proinsulin. BMC Cell Biol. 11, 59.
15. Haze, K., Yoshida, H., Yanagi, H., Yura, T. and Mori, K. (1999). Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10, 3787-3799.
16. Hayano, T. and Kikuchi, M. (1995). Cloning and sequencing of the cDNA encoding human P5. Gene. 164, 377-378.
17. Iwawaki, T. and Akai, R. (2006). Analysis of the XBP1 splicing mechanism using endoplasmic reticulum stress-indicators. Biochem. Biophys. Res. Commun. 350, 709-715.
18. Jessop, C. E., Watkins, R. H., Simmons, J. J., Tasab, M. and Bulleid, N. J. (2009). Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J. Cell Sci. 122, 4287-4295.
19. Kabani, M., Beckerich, J. M. and Brodsky, J. L. (2002). Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol. Cell. Biol. 22, 4677-4689.
20. Kamauchi, S., Nakatani, H., Nakano, C. and Urade, R. (2005). Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 272, 3461-3476.
21. Kapulkin, W. J., Hiester, B. G. and Link, C. D. (2005). Compensatory regulation among ER chaperones in C. elegans. FEBS Lett. 579, 3063-3068.
22. Kondo, S., Murakami, T., Tatsumi, K., Ogata, M., Kanemoto, S., Otori, K., Iseki, K., Wanaka, A. and Imaizumi, K. (2005). OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat. Cell Biol. 7, 186-194.
23. Kropp, L. E., Garg, M. and Binder, R. J. (2010). Ovalbumin-derived precursor peptides are transferred sequentially from gp96 and calreticulin to MHC class I in the endoplasmic reticulum. J. Immunol. 184, 5619-5627.
24. Lee, A. H., Iwakoshi, N. N. and Glimcher, L. H. (2003). XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459.
25. Li, M., Baumeister, P., Roy, B., Phan, T., Foti, D., Luo, S. and Lee, A. S. (2000). ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol. Cell. Biol. 20, 5096-5106.
26. Lie'vremont, J. P., Rizzuto, R., Hendershot, L. and Meldolesi, J. (1997). BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+. J. Biol. Chem. 272, 30873-30879.
27. Ma, Y. and Hendershot, L. M. (2004). ER chaperone functions during normal and stress conditions. J. Chem. Neuroanat. 28, 51-65.
28. Mao, C., Wang, M., Luo, B., Wey, S., Dong, D., Wesselschmidt, R., Rawlings, S. and Lee, A. S. (2010). Targeted mutation of the mouse Grp94 gene disrupts development and perturbs endoplasmic reticulum stress signaling. PLoS ONE 5, e10852.
29. Melnick, J., Aviel, S. and Argon, Y. (1992). The endoplasmic reticulum stress protein GRP94, in addition to BiP, associates with unassembled immunoglobulin chains. J. Biol. Chem. 267, 21303-21306.
30. Melnick, J., Dul, J. L. and Argon, Y. (1994). Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 370, 373-375.
31. Meunier, L., Usherwood, Y. K., Chung, K. T. and Hendershot, L. M. (2002). A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13, 4456-4469.
32. Morinaga, N., Yahiro, K., Matsuura, G., Moss, J. and Noda, M. (2008). Subtilase cytotoxin, produced by Shiga-toxigenic Escherichia coli, transiently inhibits protein synthesis of Vero cells via degradation of BiP and induces cell cycle arrest at G1 by downregulation of cyclin D1. Cell. Microbiol. 10, 921-929.
33. Muresan, Z. and Arvan, P. (1997). Thyroglobulin transport along the secretory pathway. Investigation of the role of molecular chaperone, GRP94, in protein export from the endoplasmic reticulum. (published erratum appears in J. Biol. Chem. 272, 30590. J. Biol. Chem. 272, 26095-26102.
34. Murray, J. I., Whitfield, M. L., Trinklein, N. D., Myers, R. M., Brown, P. O. and Botstein, D. (2004). Diverse and specific gene expression responses to stresses in cultured human cells. Mol. Biol. Cell 15, 2361-2374.
35. Musaro', A., McCullagh, K., Paul, A., Houghton, L., Dobrowolny, G., Molinaro, M., Barton, E. R., Sweeney, H. L. and Rosenthal, N. (2001). Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 27, 195-200.
36. Ostrovsky, O., Ahmed, N. T. and Argon, Y. (2009). The chaperone activity of GRP94 toward insulin-like growth factor II is necessary for the stress response to serum deprivation. Mol. Biol. Cell 20, 1855-1864.
37. Ostrovsky, O., Eletto, D., Makarewich, C., Barton, E. R. and Argon, Y. (2010). Glucose regulated protein 94 is required for muscle differentiation through its control of the autocrine production of insulin-like growth factors. Biochim. Biophys. Acta 1803, 333-341.
38. Paton, A. W., Beddoe, T., Thorpe, C. M., Whisstock, J. C., Wilce, M. C., Rossjohn, J., Talbot, U. M. and Paton, J. C. (2006). AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 443, 548-552.
39. Ron, D. (2002). Proteotoxicity in the endoplasmic reticulum: lessons from the Akita diabetic mouse. J. Clin. Invest. 109, 443-445.
40. Ron, D. and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.
41. Shiu, R. P., Pouyssegur, J. and Pastan, I. (1977). Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc. Natl. Acad. Sci. USA 74, 3840-3844.
42. Thibault, G., Ismail, N. and Ng, D. T. (2011). The unfolded protein response supports cellular robustness as a broad-spectrum compensatory pathway. Proc. Natl. Acad. Sci. USA 108, 20597-20602.
43. Travers, K. J., Patil, C. K., Wodicka, L., Lockhart, D. J., Weissman, J. S. and Walter, P. (2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
44. van Anken, E., Romijn, E. P., Maggioni, C., Mezghrani, A., Sitia, R., Braakman, I. and Heck, A. J. (2003). Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion. Immunity 18, 243-253.
45. Walter, P. and Ron, D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086.
46. Wanderling, S., Simen, B. B., Ostrovsky, O., Ahmed, N. T., Vogen, S., Gidalevitz, T. and Argon, Y. (2007). GRP94 is essential for mesoderm induction and muscle development because it regulates insulin-like growth factor secretion. Mol. Biol. Cell 18, 3764-3775.
47. Wang, Y., Shen, J., Arenzana, N., Tirasophon, W., Kaufman, R. J. and Prywes, R. (2000). Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275, 27013-27020.
48. Wiest, D. L., Burkhardt, J. K., Hester, S., Hortsch, M., Meyer, D. I. and Argon, Y. (1990). Membrane biogenesis during B cell differentiation: most endoplasmic reticulum proteins are expressed coordinately. J. Cell Biol. 110, 1501-1511.
49. Wolfson, J. J., May, K. L., Thorpe, C. M., Jandhyala, D. M., Paton, J. C. and Paton, A. W. (2008). Subtilase cytotoxin activates PERK, IRE1 and ATF6 endoplasmic reticulum stress-signalling pathways. Cell. Microbiol. 10, 1775-1786.
50. Yang, Y., Liu, B., Dai, J., Srivastava, P. K., Zammit, D. J., Lefrançois, L. and Li, Z. (2007). Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26, 215-226.
51. Ye, R., Jung, D. Y., Jun, J. Y., Li, J., Luo, S., Ko, H. J., Kim, J. K. and Lee, A. S. (2010). Grp78 heterozygosity promotes adaptive unfolded protein response and attenuates diet-induced obesity and insulin resistance. Diabetes 59, 6-16.
52. Yoshida, H., Haze, K., Yanagi, H., Yura, T. and Mori, K. (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, 33741-33749.
53. Zou, J., Guo, Y., Guettouche, T., Smith, D. F. and Voellmy, R. (1998). Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471-480.