Endoplasmic reticulum oxidoreductin-1α(Ero1α) improves folding and secretion of mutant proinsulin and limits mutant proinsulin-induced endoplasmic reticulum stress

Journal of Biological Chemistry

Volumn 288, Issue 43, 2013, Pages 31010-31018

  Wright, Jordan ^a   Birk, Julia ^b   Haataja, Leena ^a   Liu, Ming ^a   Ramming, Thomas ^b   Weiss, Michael A ^c   Appenzeller Herzog, Christian ^b   Arvan, Peter ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENEFICIAL EFFECTS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; OXIDATIVE FOLDING; OXIDIZING ENVIRONMENTS; PROTEIN DISULFIDE ISOMERASES; THERAPEUTIC STRATEGY; TYPE 2 DIABETES MELLITUS;

CELL DEATH; CELL MEMBRANES;

INSULIN;

CELL PROTEIN; OXIDOREDUCTIN 1ALPHA; PROINSULIN; UNCLASSIFIED DRUG;

ARTICLE; DIMERIZATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; MUTATION; OXIDATION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; UPREGULATION;

Β-CELL; DIABETES; DISULFIDE; ENDOPLASMIC RETICULUM (ER); INSULIN SYNTHESIS; MUTANT INS-GENE-INDUCED DIABETES OF YOUTH; OXIDATIVE FOLDING;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; INSULIN-SECRETING CELLS; MEMBRANE GLYCOPROTEINS; MICE; MUTATION, MISSENSE; OXIDATION-REDUCTION; OXIDOREDUCTASES; PROINSULIN; PROTEIN FOLDING;

EID: 84886672340     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.510065     Document Type: Article

References (45)

1. Liu, M., Hodish, I., Haataja, L., Lara-Lemus, R., Rajpal, G., Wright, J., and Arvan, P. (2010) Proinsulin misfolding and diabetes. Mutant INS geneinduced diabetes of youth. Trends Endocrinol. Metab. 21, 652-659
2. Rajpal, G., Schuiki, I., Liu, M., Volchuk, A., and Arvan, P. (2012) Action of protein disulfide isomerase on proinsulin exit from endoplasmic reticulum of pancreatic β-cells. J. Biol. Chem. 287, 43-47
3. Liu, M., Li, Y., Cavener, D., and Arvan, P. (2005) Proinsulin disulfide maturation and misfolding in the endoplasmic reticulum. J. Biol. Chem. 280, 13209-13212
4. Harding, H. P., Zyryanova, A. F., and Ron, D. (2012) Uncoupling proteostasis and development in vitro with a small molecule inhibitor of the pancreatic endoplasmic reticulum kinase, PERK. J. Biol. Chem. 287, 44338-44344
5. Han, J., Back, S. H., Hur, J., Lin, Y. H., Gildersleeve, R., Shan, J., Yuan, C. L., Krokowski, D., Wang, S., Hatzoglou, M., Kilberg, M. S., Sartor, M. A., and Kaufman, R. J. (2013) ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15, 481-490
6. Hodish, I., Liu, M., Rajpal, G., Larkin, D., Holz, R. W., Adams, A., Liu, L., and Arvan, P. (2010) Misfolded proinsulin affects bystander proinsulin in neonatal diabetes. J. Biol. Chem. 285, 685-694
7. Back, S. H., and Kaufman, R. J. (2012) Endoplasmic reticulum stress and type 2 diabetes. Annu. Rev. Biochem. 81, 767-793
8. Liu, M., Haataja, L., Wright, J., Wickramasinghe, N. P., Hua, Q. X., Phillips, N. F., Barbetti, F., Weiss, M. A., and Arvan, P. (2010) Mutant INS-gene induced diabetes of youth. Proinsulin cysteine residues impose dominant-negative inhibition on wild-type proinsulin transport. PLoS ONE 5, e13333
9. Park, S. Y., Ye, H., Steiner, D. F., and Bell, G. I. (2010) Mutant proinsulin proteins associated with neonatal diabetes are retained in the endoplasmic reticulum and not efficiently secreted. Biochem. Biophys. Res. Commun. 391, 1449-1454
10. Liu, M., Hodish, I., Rhodes, C. J., and Arvan, P. (2007) Proinsulin maturation, misfolding, and proteotoxicity. Proc. Natl. Acad. Sci. U. S. A. 104, 15841-15846
11. Rajan, S., Eames, S. C., Park, S. Y., Labno, C., Bell, G. I., Prince, V. E., and Philipson, L. H. (2010) In vitro processing and secretion of mutant insulin proteins that cause permanent neonatal diabetes. Am. J. Physiol. Endocrinol. Metab. 298, E403-E410
12. Oyadomari, S., Koizumi, A., Takeda, K., Gotoh, T., Akira, S., Araki, E., and Mori, M. (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109, 525-532
13. Zito, E., Chin, K. T., Blais, J., Harding, H. P., and Ron, D. (2010) ERO1β, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis. J. Cell Biol. 188, 821-832
14. Khoo, C., Yang, J., Rajpal, G., Wang, Y., Liu, J., Arvan, P., and Stoffers, D. A. (2011) Endoplasmic reticulum oxidoreductin-1-like β (ERO1lβ) regulates susceptibility to endoplasmic reticulum stress and is induced by insulin flux in β-cells. Endocrinology 152, 2599-2608
15. Ramming, T., and Appenzeller-Herzog, C. (2012) The physiological functions of mammalian endoplasmic oxidoreductin 1. On disulfides and more. Antioxid. Redox Signal. 16, 1109-1118
16. Tu, B. P., Ho-Schleyer, S. C., Travers, K. J., and Weissman, J. S. (2000) Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290, 1571-1574
17. Sevier, C. S., and Kaiser, C. A. (2002) Formation and transfer of disulphide bonds in living cells. Nat. Rev. Mol. Cell Biol. 3, 836-847
18. Bulleid, N. J., and Ellgaard, L. (2011) Multiple ways to make disulfides. Trends Biochem. Sci. 36, 485-492
19. Liu, M., Lara-Lemus, R., Shan, S. O., Wright, J., Haataja, L., Barbetti, F., Guo, H., Larkin, D., and Arvan, P. (2012) Impaired cleavage of preproinsulin signal peptide linked to autosomal-dominant diabetes. Diabetes 61, 828-837
20. Appenzeller-Herzog, C., Riemer, J., Christensen, B., Sørensen, E. S., and Ellgaard, L. (2008) A novel disulphide switch mechanism in Ero1α balances ER oxidation in human cells. EMBO J. 27, 2977-2987
21. Liu, M., Ramos-Castañeda, J., and Arvan, P. (2003) Role of the connecting peptide in insulin biosynthesis. J. Biol. Chem. 278, 14798-14805
22. Birk, J., Meyer, M., Aller, I., Hansen, H. G., Odermatt, A., Dick, T. P., Meyer, A. J., and Appenzeller-Herzog, C. (2013) Endoplasmic reticulum. Reduced and oxidized glutathione revisited. J. Cell Sci. 126, 1604-1617
23. Birk, J., Ramming, T., Odermatt, A., and Appenzeller-Herzog, C. (2013) Green fluorescent protein-based monitoring of endoplasmic reticulum redox poise. Front. Genet. 4, 108
24. Enyedi, B., Várnai, P., and Geiszt, M. (2010) Redox state of the endoplasmic reticulum is controlled by Ero1Lα and intraluminal calcium. Antioxid. Redox Signal. 13, 721-729
25. Haataja, L., Snapp, E., Wright, J., Liu, M., Hardy, A. B., Wheeler, M. B., Markwardt, M. L., Rizzo, M., and Arvan, P. (2013) Proinsulin intermolecular interactions during secretory trafficking in pancreatic βcells. J. Biol. Chem. 288, 1896-1906
26. Wright, J., Wang, X., Haataja, L., Kellogg, A. P., Lee, J., Liu, M., and Arvan, P. (2013) Dominant protein interactions that influence the pathogenesis of conformational diseases. J. Clin. Invest. 123, 3124-3134
27. Hansen, H. G., Schmidt, J. D., Søltoft, C. L., Ramming, T., Geertz-Hansen, H. M., Christensen, B., Sørensen, E. S., Juncker, A. S., Appenzeller-Herzog, C., and Ellgaard, L. (2012) Hyperactivity of the Ero1α oxidase elicits endoplasmic reticulum stress but no broad antioxidant response. J. Biol. Chem. 287, 39513-39523
28. Baker, K. M., Chakravarthi, S., Langton, K. P., Sheppard, A. M., Lu, H., and Bulleid, N. J. (2008) Low reduction potential of Ero1αregulatory disulphides ensures tight control of substrate oxidation. EMBO J. 27, 2988-2997
29. Frand, A. R., and Kaiser, C. A. (1999) Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol. Cell 4, 469-477
30. Zhang, L., Lai, E., Teodoro, T., and Volchuk, A. (2009) GRP78, but not protein-disulfide isomerase, partially reverses hyperglycemia-induced inhibition of insulin synthesis and secretion in pancreatic β-cells. J. Biol. Chem. 284, 5289-5298
31. Wang, L., Li, S. J., Sidhu, A., Zhu, L., Liang, Y., Freedman, R. B., and Wang, C. C. (2009) Reconstitution of human Ero1-Lα/protein-disulfide isomerase oxidative folding pathway in vitro. Position-dependent differences in role between the a and a' domains of protein-disulfide isomerase. J. Biol. Chem. 284, 199-206
32. Ferris, S. P., Jaber, N. S., Molinari, M., Arvan, P., and Kaufman, R. J. (2013) UDP-glucose: glycoprotein glucosyltransferase (UGGT1) promotes substrate solubility in the endoplasmic reticulum. Mol. Biol. Cell 24, 2597-2608
33. Scheuner, D., and Kaufman, R. J. (2008) The unfolded protein response. A pathway that links insulin demand with beta-cell failure and diabetes. Endocr. Rev. 29, 317-333
34. Weiss, M. A. (2009) Proinsulin and the genetics of diabetes mellitus. J. Biol. Chem. 284, 19159-19163
35. Volchuk, A., and Ron, D. (2010) The endoplasmic reticulum stress response in the pancreatic β-cell. Diabetes Obes. Metab. 12, 48-57
36. Thomas, S. E., Dalton, L., Malzer, E., and Marciniak, S. J. (2011) Unravelling the story of protein misfolding in diabetes mellitus. World J. Diabetes 2, 114-118
37. Ron, D., and Harding, H. P. (2012) Protein-folding homeostasis in the endoplasmic reticulum and nutritional regulation. Cold Spring Harb. Perspect. Biol. 4, a013177
38. Karunakaran, U., and Park, K. G. (2013) Structural modifications in the arterial wall during physiological aging and as a result of diabetes mellitus in a mouse model. Are the changes comparable? Diabetes Metab. J. 37, 106-112
39. Blais, J. D., Chin, K. T., Zito, E., Zhang, Y., Heldman, N., Harding, H. P., Fass, D., Thorpe, C., and Ron, D. (2010) A small molecule inhibitor of endoplasmic reticulum oxidation 1 (ERO1) with selectively reversible thiol reactivity. J. Biol. Chem. 285, 20993-21003
40. Back, S. H., Scheuner, D., Han, J., Song, B., Ribick, M., Wang, J., Gildersleeve, R. D., Pennathur, S., and Kaufman, R. J. (2009) Translation attenuation through eIF2α phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells. Cell Metab. 10, 13-26
41. Appenzeller-Herzog, C. (2011) Glutathione- and non-glutathione-based oxidant control in the endoplasmic reticulum. J. Cell Sci. 124, 847-855
42. Qiao, Z. S., Min, C. Y., Hua, Q. X., Weiss, M. A., and Feng, Y. M. (2003) In vitro refolding of human proinsulin. Kinetic intermediates, putative disulfideforming pathway folding initiation site, and potential role of C-peptide in folding process. J. Biol. Chem. 278, 17800-17809
43. Weiss, M. A. (2013) Diabetes mellitus due to the toxic misfolding of proinsulin variants. FEBS Lett. 587, 1942-1950
44. Zito, E., Melo, E. P., Yang, Y., Wahlander, Å., Neubert, T. A., and Ron, D. (2010) Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin. Mol. Cell 40, 787-797
45. 2 produced during disulphide formation. J. Cell Sci. 123, 2672-2679