Mutant proinsulin proteins associated with neonatal diabetes are retained in the endoplasmic reticulum and not efficiently secreted

Biochemical and Biophysical Research Communications

Volumn 391, Issue 3, 2010, Pages 1449-1454

  Park, Soo Young ^a   Ye, Honggang ^a   Steiner, Donald F ^a   Bell, Graeme I ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Diabetes; Insulin; Misfolded protein; Unfolded protein response

Indexed keywords

MUTANT PROTEIN; PROINSULIN;

ANIMAL CELL; ARTICLE; ATTENUATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; HYPERINSULINEMIA; INSULIN RELEASE; INSULIN SYNTHESIS; INSULINOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; SECRETORY GRANULE; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE, TUMOR; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; HUMANS; INFANT, NEWBORN; INFANT, NEWBORN, DISEASES; MUTATION; PROINSULIN; PROTEIN FOLDING; RATS;

RATTUS;

EID: 73949154312     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2009.12.090     Document Type: Article

References (33)

1. Støy J., Edghill E.L., Flanagan S.E., Ye H., Paz V.P., Pluzhnikov A., Below J.E., Hayes M.G., Cox N.J., Lipkind G.M., Lipton R.B., Greeley S.A., Patch A.M., Ellard S., Steiner D.F., Hattersley A.T., Philipson L.H., Bell G.I., and Neonatal Diabetes International Collaborative Group. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc. Natl. Acad. Sci. USA 104 (2007) 15040-15044
2. 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. Insulin mutation screening in 1044 patients with diabetes: mutations in the INS gene are a common cause of neonatal diabetes but a rare cause of diabetes diagnosed in childhood or adulthood. Diabetes 57 (2008) 1034-1042
3. Polak M., Dechaume A., Cavé H., Nimri R., Crosnier H., Sulmont V., de Kerdanet M., Scharfmann R., Lebenthal Y., Froguel P., and Vaxillaire M. Heterozygous missense mutations in the insulin gene are linked to permanent diabetes appearing in the neonatal period or in early infancy. A report from the French ND (neonatal diabetes) study group. Diabetes 57 (2008) 1115-1119
4. Molven A., Ringdal M., Nordbø A.M., Ræder H., Støy J., Lipkind G.M., Steiner D.F., Philipson L.H., Bergmann I., Aarskog D., Undlien D.E., Joner G., Søvik O., the Norwegian Childhood Diabetes Study Group, Bell G.I., and Njølstad P.R. Mutations in the insulin gene can cause MODY and autoantibody-negative type 1 diabetes. Diabetes 57 (2008) 1131-1135
5. Colombo C., Porzio O., Liu M., Massa O., Vasta M., Salardi S., Beccaria L., Monciotti C., Toni S., Pedersen O., Hansen T., Federici L., Pesavento R., Cadario F., Federici G., Ghirri P., Arvan P., Iafusco D., Barbetti F., and the Early Onset Diabetes Study Group of the Italian Society of Pediatric Endocrinology and Diabetes (SIEDP). Seven mutations in the human insulin gene linked to permanent neonatal/infancy-onset diabetes mellitus. J. Clin. Invest. 118 (2008) 2148-2156
6. Ahamed A., Unnikrishnan A.G., Pendsey S.S., Nampoothiri S., Bhavani V., Praveen V.P., Kumar H., Jayakumar R.V., Nair V., Ellard S., and Edghill E. Permanent neonatal diabetes mellitus due to a C96Y heterozygous mutation in the insulin gene: a case report. J. Pancreas 9 (2008) 715-718
7. Bonfanti R., Colombo C., Nocerino V., Massa O., Lampasona V., Iafusco D., Viscardi M., Chiumello G., Meschi F., and Barbetti F. Insulin gene mutations as cause of diabetes in children negative for five type 1 diabetes autoantibodies. Diabetes Care 32 (2009) 123-125
8. Rubio-Cabezas O., Edghill E., Argente J., and Hattersley A.T. Testing for monogenic diabetes among children with antibody-negative clinically defined type 1 diabetes. Diabet. Med. 26 (2009) 1070-1074
9. Wang J., Takeuchi T., Tanaka S., Kubo S.-K., Kayo T., Lu D., Takata K., Koizumi A., and Izumi T. A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J. Clin. Invest. 103 (1999) 27-37
10. C95S mutant mice. Diabetes 56 (2007) 1268-1276
11. Steiner D.F., Tager H.S., Nanjo K., Chan S.J., and Rubenstein A.H. Familial syndromes of hyperproinsulinemia and hyperinsulinemia with mild diabetes. In: Scriver C., Beaudet A., Sly W., and Valle D. (Eds). The Metabolic Basis of Inherited Disease. seventh ed. (1995), McGraw-Hill, New York 897-904
12. Bell G.I., Swain W.F., Pictet R., Cordell B., Goodman H.M., and Rutter W.J. Nucleotide sequence of a cDNA clone encoding human preproinsulin. Nature 282 (1979) 525-527
13. Snapp E.L., Sharma A., Lippincott-Schwartz J., and Hegde R.S. Monitoring chaperone engagement of substrates in the endoplasmic reticulum of live cells. Proc. Natl. Acad. Sci. USA 103 (2006) 6536-6541
14. Bolte S., and Cordelières F.P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224 (2006) 213-232
15. Oyadomari S., Koizumi A., Takeda K., Gotoh T., Akira S., Araki E., and Mori M. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109 (2002) 525-532
16. +/Akita pancreatic beta cells. Genes Cells 9 (2004) 261-270
17. Carroll R.J., Hammer R.E., Chan S.J., Swift H.N., Rubenstein A.H., and Steiner D.F. A mutant human proinsulin is secreted from islets of Langerhans in increased amounts via an unregulated pathway. Proc. Natl. Acad. Sci. USA 85 (1988) 8943-8947
18. Steiner D.F., Tager H.S., Chan S.J., Nanjo K., Sanke T., and Rubenstein A.H. Lessons learned from molecular biology of insulin-gene mutations. Diabetes Care 13 (1990) 600-609
19. Izumi T., Yokota-Hashimoto H., Zhao S., Wang J., Halban P.A., and Takeuchi T. Dominant negative pathogenesis by mutant proinsulin in the Akita diabetic mouse. Diabetes 52 (2003) 409-416
20. Scheuner D., and Kaufman R.J. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr. Rev. 29 (2008) 317-333
21. Liu M., Hodish I., Rhodes C.J., and Arvan P. Proinsulin maturation, misfolding, and proteotoxicity. Proc Natl Acad Sci USA 104 (2007) 15841-15846
22. Moore H.P., Walker M.D., Lee F., and Kelly R.B. Expressing a human proinsulin cDNA in a mouse ACTH-secreting cell. Intracellular storage, proteolytic processing, and secretion on stimulation. Cell 35 (1983) 531-538
23. Gross D.J., Halban P.A., Kahn C.R., Weir G.C., and Villa-Komaroff L. Partial diversion of a mutant proinsulin (B10 aspartic acid) from the regulated to the constitutive secretory pathway in transfected AtT-20 cells. Proc. Natl. Acad. Sci. USA 86 (1989) 4107-4111
24. B10]insulin in AtT20 cells. Mol. Endocrinol. 5 (1991) 319-326
25. Zhu Y.L., Abdo A., Gesmonde J.F., Zawalich K.C., Zawalich W., and Dannies P.S. Aggregation and lack of secretion of most newly synthesized proinsulin in non-beta-cell lines. Endocrinology 145 (2004) 3840-3849
26. Liu M., Li Y., Cavener D., and Arvan P. Proinsulin disulfide maturation and misfolding in the endoplasmic reticulum. J. Biol. Chem. 280 (2005) 13209-13212
27. Hua Q.X., Liu M., Hu S.Q., Jia W., Arvan P., and Weiss M.A. A conserved histidine in insulin is required for the foldability of human proinsulin: structure and function of an ALAB5 analog. J. Biol. Chem. 281 (2006) 24889-24899
28. C96Y results in enhanced tubule formation causing enlargement of pre-Golgi intermediates in CHO cells. Histochem. Cell Biol. 128 (2007) 161-173
29. Ohara-Imaizumi M., Nakamichi Y., Tanaka T., Ishida H., and Nagamatsu S. Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J. Biol. Chem. 277 (2002) 3805-3808
30. Shibasaki T., Takahashi H., Miki T., Sunaga Y., Matsumura K., Yamanaka M., Zhang C., Tamamoto A., Satoh T., Miyazaki J., and Seino S. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by camp. Proc. Natl. Acad. Sci. USA 104 (2007) 19333-19338
31. Waldo G.S., Standish B.M., Berendzen J., and Terwilliger T.C. Rapid protein-folding assay using green fluorescent protein. Nat. Biotechnol. 17 (1999) 691-695
32. Rajan S., Eames S.C., Park S.Y., Labno C., Bell G.I., Prince V., and Philipson L.H. In vitro processing and secretion of mutant insulin proteins that cause permanent neonatal diabetes. Am. J. Physiol. Endocrinol. Metab. (2009) (Epub ahead of print)
33. Weiss M.A. Proinsulin and the genetics of diabetes mellitus. J. Biol. Chem. 284 (2009) 19159-19163