Insulin gene mutations resulting in early-onset diabetes: Marked differences in clinical presentation, metabolic status, and pathogenic effect through endoplasmic reticulum retention

Diabetes

Volumn 59, Issue 3, 2010, Pages 653-661

  Meur, Gargi ^a   Simon, Albane ^b   Harun, Nasret ^a   Virally, Marie ^c   Dechaume, Aurélie ^d   Bonnefond, Amélie ^d   Fetita, Sabrina ^e   Tarasov, Andrei I ^a   Guillausseau, Pierre Jean ^c   Boesgaard, Trine Welløv ^f   Pedersen, Oluf ^f,g,h   Hansen, Torben ^f,i   Polak, Michel ^b   Gautier, Jean François ^e   Froguel, Philippe ^d,j   Rutter, Guy A ^a   Vaxillaire, Martine ^d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL LARIBOISIÈRE   (France)

^d UNIV LILLE   (France)

^e SAINT LOUIS HOSPITAL   (France)

^f STENO DIABETES CENTER   (Denmark)

^g AARHUS UNIVERSITY   (Denmark)

^h UNIVERSITY OF COPENHAGEN   (Denmark)

ⁱ UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^j HAMMERSMITH HOSPITAL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; INSULIN; PROINSULIN; X BOX BINDING PROTEIN 1; MESSENGER RNA;

ADULT; ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE MUTATION; GENE SEQUENCE; HORMONE RELEASE; HUMAN; IMMUNOCYTOCHEMISTRY; JUVENILE DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; MATURITY ONSET DIABETES MELLITUS; PATHOGENESIS; PRIORITY JOURNAL; RADIOIMMUNOASSAY; REAL TIME POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; ADOLESCENT; CHEMISTRY; FAMILY HEALTH; FRANCE; GENETICS; HETEROZYGOTE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; ONSET AGE; PANCREAS ISLET BETA CELL; PEDIGREE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POINT MUTATION; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ADOLESCENT; ADULT; AGE OF ONSET; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM; FAMILY HEALTH; FEMALE; FRANCE; GREEN FLUORESCENT PROTEINS; HETEROZYGOTE; HUMANS; INSULIN-SECRETING CELLS; MALE; MUTAGENESIS, SITE-DIRECTED; PEDIGREE; POINT MUTATION; PROINSULIN; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; YOUNG ADULT;

EID: 77950348445     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-1091     Document Type: Article

References (30)

1. Wang J, Takeuchi T, Tanaka S, Kubo SK, Kayo T, Lu D, Takata K, Koizumi A, Izumi T. A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J Clin Invest 1999;103: 27-37
2. Ron D. Translational control in the endoplasmic reticulum stress response. J Clin Invest 2002;110:1383-1388 (Pubitemid 35396906)
3. Herbach N, Rathkolb B, Kemter E, Pichl L, Klaften M, de Angelis MH, Halban PA, Wolf E, Aigner B, Wanke R. Dominant-negative effects of a novel mutated Ins2 allele causes early-onset diabetes and severe beta-cell loss in Munich Ins2C95S mutant mice. Diabetes 2007;56:1268-1276
4. Shoelson S, Fickova M, Haneda M, Nahum A, Musso G, Kaiser ET, Rubenstein AH, Tager H. Identification of a mutant human insulin predicted to contain a serine-for-phenylalanine substitution. Proc Natl Acad Sci U S A 1983;80:7390-7394 (Pubitemid 14178008)
5. Shoelson S, Haneda M, Blix P, Nanjo A, Sanke T, Inouye K, Steiner D, Rubenstein A, Tager H. Three mutant insulins in man. Nature 1983;302:540-543
6. Shibasaki Y, Kawakami T, Kanazawa Y, Akanuma Y, Takaku F. Posttranslational cleavage of proinsulin is blocked by a point mutation in familial hyperproinsulinemia. J Clin Invest 1985;76:378-380 (Pubitemid 15243468)
7. Yano H, Kitano N, Morimoto M, Polonsky KS, Imura H, Seino Y. A novel point mutation in the human insulin gene giving rise to hyperproinsulinemia (proinsulin Kyoto). J Clin Invest 1992;89:1902-1907
8. Støy J, Edghill EL, Flanagan SE, Ye H, Paz VP, Pluzhnikov A, Below JE, Hayes MG, Cox NJ, Lipkind GM, Lipton RB, Greeley SA, Patch AM, Ellard S, Steiner DF, Hattersley AT, Philipson LH, Bell GI, Neonatal Diabetes International Collaborative Group. Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci U S A 2007;104:15040-15044
9. Edghill EL, Flanagan SE, Patch AM, Boustred C, Parrish A, Shields B, Shepherd MH, Hussain K, Kapoor RR, Malecki M, MacDonald MJ, Støy J, Steiner DF, Philipson LH, Bell GI, Neonatal Diabetes International Collaborative Group, Hattersley AT, Ellard S. Insulin mutation screening in 1,044 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 2008;57:1034-1042
10. Polak M, Dechaume A, Cavé H, Nimri R, Crosnier H, Sulmont V, de Kerdanet M, Scharfmann R, Lebenthal Y, Froguel P, Vaxillaire M, French ND (Neonatal Diabetes) Study Group. 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 2008;57:1115-1119
11. Molven A, Ringdal M, Nordbø AM, Raeder H, Støy J, Lipkind GM, Steiner DF, Philipson LH, Bergmann I, Aarskog D, Undlien DE, Joner G, Søvik O, Norwegian Childhood Diabetes Study Group, Bell GI, Njølstad PR. Mutations in the insulin gene can cause MODY and autoantibody-negative type 1 diabetes. Diabetes 2008;57:1131-1135
12. 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, 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 2008; 118:2148-2156
13. Bonfanti R, Colombo C, Nocerino V, Massa O, Lampasona V, Iafusco D, Viscardi M, Chiumello G, Meschi F, Barbetti F. Insulin gene mutations as cause of diabetes in children negative for five type 1 diabetes autoantibodies. Diabetes Care 2009;32:123-125
14. Tarasov AI, Nicolson TJ, Riveline JP, Taneja TK, Baldwin SA, Baldwin JM, Charpentier G, Gautier JF, Froguel P, Vaxillaire M, Rutter GA. A rare mutation in ABCC8/SUR1 leading to altered ATP-sensitive K+ channel activity and beta-cell glucose sensing is associated with type 2 diabetes in adults. Diabetes 2008;57:1595-1604
15. Liu M, Hodish I, Rhodes CJ, Arvan P. Proinsulin maturation, misfolding, and proteotoxicity. Proc Natl Acad Sci U S A 2007;104:15841-15846
16. Chèvre JC, Hani EH, Boutin P, Vaxillaire M, Blanché H, Vionnet N, Pardini VC, Timsit J, Larger E, Charpentier G, Beckers D, Maes M, Bellanné-Chantelot C, Velho G, Froguel P. Mutation screening in 18 Caucasian families suggest the existence of other MODY genes. Diabetologia 1998;41:1017-1023
17. Miyazaki J, Araki K, Yamato E, Ikegami H, Asano T, Shibasaki Y, Oka Y, Yamamura K. Establishment of a pancreatic beta cell line that retains glucose inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 1990;127:126-132
18. Tsuboi T, Rutter GA. Multiple forms of "kiss-and-run" exocytosis revealed by evanescent wave microscopy. Curr Biol 2003;13:563-567
19. Varadi A, Cirulli V, Rutter GA. Mitochondrial localization as a determinant of capacitative Ca2+ entry in HeLa cells. Cell Calcium 2004;36:499-508 (Pubitemid 39366138)
20. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529 (Pubitemid 46985379)
21. Cnop M, Welsh N, Jonas JC, Jorns A, Lenzen S, Eizirik DL. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 2005;54(Suppl. 2):S97-S107
22. Cunha DA, Hekerman P, Ladrière L, Bazarra-Castro A, Ortis F, Wakeham MC, Moore F, Rasschaert J, Cardozo AK, Bellomo E, Overbergh L, Mathieu C, Lupi R, Hai T, Herchuelz A, Marchetti P, Rutter GA, Eizirik DL, Cnop M. Initiation and execution of lipotoxic ER stress in pancreatic beta cells. J Cell Sci 2008;121:2308-2318
23. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004;11:381-389 (Pubitemid 38489416)
24. Lai E, Bikopoulos G, Wheeler MB, Rozakis-Adcock M, Volchuk A. Differential activation of ER stress and apoptosis in response to chronically elevated free fatty acids in pancreatic beta-cells. Am J Physiol Endocrinol Metab 2008;294:E540-E550
25. Glaser B. Insulin mutations in diabetes: the clinical spectrum. Diabetes 2008;57:799-800
26. von Heijne G. Signal sequences: the limits of variation. J Mol Biol 1985;184:99-105
27. von Heijne G. Analysis of the distribution of charged residues in the N-terminal region of signal sequences: implications for protein export in prokaryotic and eukaryotic cells. EMBO J 1984;3:2315-2318
28. Scheuner D, Kaufman RJ. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 2008;29:317-333 (Pubitemid 351679702)
29. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008;118:3378-3389
30. Smith GD, Pangborn WA, Blessing RH. The structure of T6 human insulin at 1.0 A resolution. Acta Crystallogr D Biol Crystallogr 2003;59:474-482