Inefficient translocation of preproinsulin contributes to pancreatic β cell failure and late-onset diabetes

Journal of Biological Chemistry

Volumn 289, Issue 23, 2014, Pages 16290-16302

  Guo, Huan ^a   Xiong, Yi ^a   Witkowski, Piotr ^b   Cui, Jingqing ^a,c   Wang, Ling Jia ^b   Sun, Jinhong ^a   Lara Lemus, Roberto ^a,d   Haataja, Leena ^a   Hutchison, Kathryn ^a   Shan, Shu Ou ^e   Arvan, Peter ^a   Liu, Ming ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^e California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CELL DEATH; CELL MEMBRANES; INSULIN; PROTEINS;

AUTOSOMAL DOMINANTS; ENDOPLASMIC RETICULUM STRESS; HEAT SHOCK PROTEIN 70; MOLECULAR PATHOGENESIS; POSITIVE CHARGES; POTENTIAL DEFECTS; SECRETORY PATHWAYS; SIGNAL SEQUENCE;

DEFECTS;

HEAT SHOCK PROTEIN 70; PREPROINSULIN; PROINSULIN; SIGNAL PEPTIDE;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIABETES MELLITUS; EMBRYO; ENDOPLASMIC RETICULUM; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; YOUNG ADULT;

CYTOSOLIC PROTEIN ACCUMULATION; DIABETES; INSULIN SYNTHESIS; MUTANT; PREPROINSULIN; PROINSULIN; PROTEIN TRANSLOCATION; Β CELL;

AMINO ACID SEQUENCE; ANIMALS; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; HUMANS; INSULIN; ISLETS OF LANGERHANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN PRECURSORS; PROTEIN TRANSPORT; RATS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84902188979     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.562355     Document Type: Article

References (62)

1. Dodson G, Steiner, D. (1998) The role of assembly in insulin's biosynthesis. Curr. Opin. Struct. Biol. 8, 189-194
2. Patzelt, C., Labrecque, A. D., Duguid, J. R., Carroll, R. J., Keim, P. S., Heinrikson, R. L., and Steiner, D. F. (1978) Detection and kinetic behavior of preproinsulin in pancreatic islets. Proc. Natl. Acad. Sci. U. S. A. 75, 1260-1264
3. Wolin, S. L., and Walter, P. (1993) Discrete nascent chain lengths are required for the insertion of presecretory proteins into microsomal membranes. J. Cell Biol. 121, 1211-1219
4. Okun, M. M., and Shields, D. (1992) Translocation of preproinsulin across the endoplasmic reticulum membrane. The relationship between nascent polypeptide size and extent of signal recognition particle-mediated inhibition of protein synthesis. J. Biol. Chem. 267, 11476-11482
5. 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
6. Zhang, B. Y., Liu, M., and Arvan, P. (2003) Behavior in the eukaryotic secretory pathway of insulin-containing fusion proteins and single-chain insulins bearing various B-chain mutations. J. Biol. Chem. 278, 3687-3693
7. Liu, M., Ramos-Castañeda, J., and Arvan, P. (2003) Role of the connecting peptide in insulin biosynthesis. J. Biol. Chem. 278, 14798-14805
8. Huang, X. F., and Arvan, P. (1995) Intracellular transport of proinsulin in pancreaticβ-cells. Structural maturation probed by disulfide accessibility. J. Biol. Chem. 270, 20417-20423
9. 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 dominantnegative inhibition on wild-type proinsulin transport. PLoS ONE 5, e13333
10. 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
11. Weiss, M. A. (2013) Diabetes mellitus due to the toxic misfolding of proinsulin variants. FEBS Lett. 587, 1942-1950
12. 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
13. 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
14. Meur, G., Simon, A., Harun, N., Virally, M., Dechaume, A., Bonnefond, A., Fetita, S., Tarasov, A. I., Guillausseau, P. J., Boesgaard, T. W., Pedersen, O., Hansen, T., Polak, M., Gautier, J. F., Froguel, P., Rutter, G. A., and Vaxillaire, M. (2010) Insulin gene mutations resulting in early-onset diabetes: marked differences in clinical presentation, metabolic status, and pathogenic effect through endoplasmic reticulum retention. Diabetes 59, 653-661
15. Boesgaard, T. W., Pruhova, S., Andersson, E. A., Cinek, O., Obermannova, B., Lauenborg, J., Damm, P., Bergholdt, R., Pociot, F., Pisinger, C., Barbetti, F., Lebl, J., Pedersen, O., and Hansen, T. (2010) Further evidence that mutations in INS can be a rare cause of maturity-onset diabetes of the young (MODY). BMC Medical Genetics 11, 42
16. Edghill, E. L., Flanagan, S. E., Patch, A.-M., Boustred, C., Parrish, A., Shields, B., Shepherd, M. H., Hussain, K., Kapoor, R. R., Malecki, M., MacDonald, M. J., Støy, J., Steiner, D. F., Philipson, L. H., Bell, G. I., Neonatal Diabetes International Collaborative Group, Hattersley, A. T., and Ellard, S. (2008) Insulin mutation screening in 1, 044 patients with diabetes. Diabetes 57, 1034-1042
17. Peterson, J. H., Woolhead, C. A., and Bernstein, H. D. (2003) Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J. Biol. Chem. 278, 46155-46162
18. Sasaki, S., Matsuyama, S., and Mizushima, S. (1990) In vitro kinetic analysis of the role of the positive charge at the amino-terminal region of signal peptides in translocation of secretory protein across the cytoplasmic membrane in Escherichia coli. J. Biol. Chem. 265, 4358-4363
19. Iino, T., Takahashi, M., and Sako, T. (1987) Role of amino-terminal positive charge on signal peptide in staphylokinase export across the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 262, 7412-7417
20. Powers, T., and Walter, P. (1997) Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J. 16, 4880-4886
21. Shan, S.-O., Chandrasekar, S., and Walter, P. (2007) Conformational changes in the GTPase modules of the signal reception particle and its receptor drive initiation of protein translocation. J. Cell Biol. 178, 611-620
22. Wang, H., Kouri, G., and Wollheim, C. B. (2005) ER stress and SREBP-1 activation are implicated in β-cell glucolipotoxicity. J. Cell Sci. 118, 3905-3915
23. Feng, Y., Jadhav, A. P., Rodighiero, C., Fujinaga, Y., Kirchhausen, T., and Lencer, W. I. (2004) Retrograde transport of cholera toxin from the plasma membrane to the endoplasmic reticulum requires the trans-Golgi network but not the Golgi apparatus in Exo2-treated cells. EMBO Rep. 5, 596-601
24. Fujita, H., Kida, Y., Hagiwara, M., Morimoto, F., and Sakaguchi, M. (2010) Positive charges of translocating polypeptide chain retrieve an upstream marginal hydrophobic segment from the endoplasmic reticulum lumen to the translocon. Mol. Biol. Cell 21, 2045-2056
25. Parks, G. D., and Lamb, R. A. (1991) Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain. Cell 64, 777-787
26. Goder, V., and Spiess, M. (2001) Topogenesis of membrane proteins: determinants and dynamics. FEBS Lett. 504, 87-93
27. Sakaguchi, M., Tomiyoshi, R., Kuroiwa, T., Mihara, K., and Omura, T. (1992) Functions of signal and signal-anchor sequences are determined by the balance between the hydrophobic segment and the N-terminal charge. Proc. Natl. Acad. Sci. U. S. A. 89, 16-19
28. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
29. von Heijne, G. (1986) Net N-C charge imbalance may be important for signal sequence function in bacteria. J. Mol. Biol. 192, 287-290
30. 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
31. Garin, I., Edghill, E. L., Akerman, I., Rubio-Cabezas, O., Rica, I., Locke, J. M., Maestro, M. A., Alshaikh, A., Bundak, R., del Castillo, G., Deeb, A., Deiss, D., Fernandez, J. M., Godbole, K., Hussain, K., O'Connell, M., Klupa, T., Kolouskova, S., Mohsin, F., Perlman, K., Sumnik, Z., Rial, J. M., Ugarte, E., Vasanthi, T., Neonatal Diabetes International Group, Johnstone, K., Flanagan, S. E., Martínez, R., Castaño, C., Patch, A. M., Fernández-Rebollo, E., Raile, K., Morgan, N., Harries, L. W., Castaño, L., Ellard, S., Ferrer, J., Perez de Nanclares, G., and Hattersley AT. (2010) Recessive mutations in the INS gene result in neonatal diabetes through reduced insulin biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 107, 3105-3110
32. Lakkaraju, A. K., Thankappan, R., Mary, C., Garrison, J. L., Taunton, J., and Strub, K. (2012) Efficient secretion of small proteins in mammalian cells relies on Sec62-dependent posttranslational translocation. Mol. Biol. Cell 23, 2712-2722
33. Johnson, N., Vilardi, F., Lang, S., Leznicki, P., Zimmermann, R., and High, S. (2012) TRC40 can deliver short secretory proteins to the Sec61 translocon. J. Cell Sci. 125, 3612-3620
34. Shao, S., and Hegde, R. S. (2011) A calmodulin-dependent translocation pathway for small secretory proteins. Cell 147, 1576-1588
35. Kaganovich, D., Kopito, R., and Frydman, J. (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095
36. Kocik, L., Junne, T., and Spiess, M. (2012) Orientation of internal signalanchor sequences at the Sec61 translocon. J. Mol. Biol. 424, 368-378
37. Debure, L., Vayssiere, J.-L., Rincheval, V., Loison, F., Le Drean, Y., and Michel, D. (2003) Intracellular clusterin causes juxtanuclear aggregate formation and mitochondrial alteration. J. Cell Sci. 116, 3109-3121
38. Viswanathan, J., Haapasalo, A., Böttcher, C., Miettinen, R., Kurkinen, K. M., Lu, A., Thomas, A., Maynard, C. J., Romano, D., Hyman, B. T., Berezovska, O., Bertram, L., Soininen, H., Dantuma, N. P., Tanzi, R. E., and Hiltunen, M. (2011) Alzheimer's disease-associated ubiquilin-1 regulates presenilin-1 accumulation and aggresome formation. Traffic 12, 330-348
39. Alarcón, C., Leahy, J. L., Schuppin, G. T., and Rhodes, C. J. (1995) Increased secretory demand rather than a defect in the proinsulin conversion mechanism causes hyperproinsulinemia in a glucose-infusion rat model of non-insulin-dependent diabetes mellitus. J. Clin. Invest. 95, 1032-1039
40. Pilon, M., Römisch, K., Quach, D., and Schekman, R. (1998) Sec61p serves multiple roles in secretory precursor binding and translocation into the endoplasmic reticulum membrane. Mol. Biol. Cell 9, 3455-3473
41. Plath, K., Mothes, W., Wilkinson, B. M., Stirling, C. J., and Rapoport, T. A. (1998) Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 94, 795-807
42. Goder, V., Junne, T., and Spiess, M. (2004) Sec61p contributes to signal sequence orientation according to the positive-inside rule. Mol. Biol. Cell 15, 1470-1478
43. von Heijne, G., and Gavel, Y. (1988) Topogenic signals in integral membrane proteins. Eur. J. Biochem. 174, 671-678
44. + on the translocation of charged residues explain the "positive inside" rule. EMBO J. 13, 2267-2272
45. Bionda, T., Tillmann, B., Simm, S., Beilstein, K., Ruprecht, M., and Schleiff, E. (2010) Chloroplast import signals: the length requirement for translocation in vitro and in vivo. J. Mol. Biol. 402, 510-523
46. Frith, M. C., Forrest, A. R., Nourbakhsh, E., Pang, K. C., Kai, C., Kawai, J., Carninci, P., Hayashizaki, Y., Bailey, T. L., and Grimmond, S. M. (2006) The abundance of short proteins in the mammalian proteome. PLoS Genet. 2, e52
47. Johnson, N., Powis, K., and High, S. (2013) Post-translational translocation into the endoplasmic reticulum. Biochim. Biophys. Acta 1833, 2403-2409
48. Izumi, T., Yokota-Hashimoto, H., Zhao, S., Wang, J., Halban, P. A., and Takeuchi, T. (2003) Dominant negative pathogenesis by mutant proinsulin in the Akita diabetic mouse. Diabetes 52, 409-416
49. 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
50. Schaffar, G., Breuer, P., Boteva, R., Behrends, C., Tzvetkov, N., Strippel, N., Sakahira, H., Siegers, K., Hayer-Hartl, M., and Hartl, F. U. (2004) Cellular toxicity of polyglutamine expansion proteins: mechanism of transcription factor deactivation. Mol. Cell 15, 95-105
51. Rubinsztein, D. C. (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780-786
52. Rane, N. S., Chakrabarti, O., Feigenbaum, L., and Hegde, R. S. (2010) Signal sequence insufficiency contributes to neurodegeneration caused by transmembrane prion protein. J. Cell Biol. 188, 515-526
53. Miesbauer, M., Rambold, A. S., Winklhofer, K. F., and Tatzelt, J. (2010) Targeting of the prion protein to the cytosol: mechanisms and consequences. Curr. Issues Mol. Biol. 12, 109-118
54. Strom, A., Wang, G.-S., Reimer, R., Finegood, D. T., and Scott, F. W. (2007) Pronounced cytosolic aggregation of cellular prion protein in pancreatic β-cells in response to hyperglycemia. Lab. Invest. 87, 139-149
55. Reiner, T., Thurber, G., Gaglia, J., Vinegoni, C., Liew, C. W., Upadhyay, R., Kohler, R. H., Li, L., Kulkarni, R. N., Benoist, C., Mathis, D., and Weissleder, R. (2011) Accurate measurement of pancreatic islet β-cell mass using a second-generation fluorescent exendin-4 analog. Proc. Natl. Acad. Sci. U. S. A. 108, 12815-12820
56. Rane, N. S., Kang, S.-W., Chakrabarti, O., Feigenbaum, L., and Hegde, R. S. (2008) Reduced translocation of nascent prion protein during ER stress contributes to neurodegeneration. Dev. Cell 15, 359-370
57. Hegde, R. S., and Ploegh, H. L. (2010) Quality and quantity control at the endoplasmic reticulum. Curr. Opin. Cell Biol. 22, 437-446
58. Hegde, R. S., and Kang, S.-W. (2008) The concept of translocational regulation. J. Cell Biol. 182, 225-232
59. Schuit, F. C., In't Veld, P. A., and Pipeleers, D. G. (1988) Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic β cells. Proc. Natl. Acad. Sci. U. S. A. 85, 3865-3869
60. Scheuner, D., and Kaufman, R. J. (2008) The unfolded protein response: a pathway that links insulin demand withβ-cell failure and diabetes. Endocr. Rev. 29, 317-333
61. Tersey, S. A., Nishiki, Y., Templin, A. T., Cabrera, S. M., Stull, N. D., Colvin, S. C., Evans-Molina, C., Rickus, J. L., Maier, B., and Mirmira, R. G. (2012) Islet B-cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes 61, 818-827
62. Kaufman, R. J. (2011) β-Cell failure, stress, and type 2 diabetes. N. Engl. J. Med. 365, 1931-1933