Enhanced oxidative stress and endocrine pancreas alterations are linked to a novel glucokinase missense mutation in ENU-derived Munich GckD217V mutants

Molecular and Cellular Endocrinology

Volumn 362, Issue 1-2, 2012, Pages 139-148

  van Buerck, L ^a,b   Schuster, M ^a   Rathkolb, B ^a,c   Sabrautzki, S ^c   Hrabe de Angelis M ^c,d   Wolf, E ^a   Aigner, B ^a   Wanke, R ^a   Herbach, N ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

cell dysfunction; ENU; Experimental genetics; Glucokinase; Maturity onset diabetes of the young

Indexed keywords

ETHYLNITROSOUREA; GLUCOKINASE; GLUCOSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL VOLUME; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE MODEL; DISEASE SEVERITY; ENZYME ACTIVITY; FEMALE; GCK GENE; GENE; GROWTH RETARDATION; HETEROZYGOSITY; HOMOZYGOSITY; HYPERGLYCEMIA; IMPAIRED GLUCOSE TOLERANCE; INSULIN RELEASE; MALE; MISSENSE MUTATION; MOUSE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN SIZE; OXIDATIVE STRESS; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PANCREAS ISLET SIZE; PATHOGENESIS; PRIORITY JOURNAL; SURVIVAL RATE;

ANIMALS; BASE SEQUENCE; BLOOD GLUCOSE; BODY WEIGHT; DNA MUTATIONAL ANALYSIS; EUKARYOTIC INITIATION FACTOR-2; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC LINKAGE; GENOTYPE; GLUCOKINASE; HEAT-SHOCK PROTEINS; HYPERGLYCEMIA; ISLETS OF LANGERHANS; LIPID PEROXIDATION; MALE; MALONDIALDEHYDE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MUTAGENESIS; MUTATION, MISSENSE; OXIDATIVE STRESS; TRANSCRIPTION FACTOR CHOP;

EID: 84865292350     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2012.06.001     Document Type: Article

References (69)

1. Diagnosis and classification of diabetes mellitus. Diabetes Care 2009, 32:S62-S67. ADA.
2. Agius L., Aiston S., Mukhtar M., Iglesia N.d.l. GKRP/GK: Control of metabolic fluxes in hepatocytes. Glucokinase and Glycaemic Diseases: From Basics to Novel Therapeutics 2001, 208-221. Karger, Basel. F.M. Matschinsky, M.A. Magnuson (Eds.).
3. Aigner B., Rathkolb B., Herbach N., Hrabě de Angelis M., Wanke R., Wolf E. Diabetes models by screen for hyperglycaemia in phenotype-driven ENU mouse mutagenesis projects. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E232-E240.
4. Bakri D., Gershoni-Baruch R., Shehadeh N. Permanent neonatal diabetes. Isr. Med. Assoc. J. 2004, 6:290-291.
5. Bali D., Svetlanov A., Lee H.W., Fusco-DeMane D., Leiser M., Li B., Barzilai N., Surana M., Hou H., Fleischer N., et al. Animal model for maturity-onset diabetes of the young generated by disruption of the mouse glucokinase gene. J. Biol. Chem. 1995, 270:21464-21467.
6. Bell G.I., Polonsky K.S. Diabetes mellitus and genetically programmed defects in β-cell function. Nature 2001, 414:788-791.
7. Byrne M.M., Sturis J., Clement K., Vionnet N., Pueyo M.E., Stoffel M., Takeda J., Passa P., Cohen D., Bell G.I., et al. Insulin secretory abnormalities in subjects with hyperglycaemia due to glucokinase mutations. J. Clin. Invest. 1994, 93:1120-1130.
8. Cheng J.L., Randall A., Baldi P. Prediction of protein stability changes for single-site mutations using support vector machines. Proteins-Struct. Funct. Bioinf. 2006, 62:1125-1132.
9. Clement K., Pueyo M.E., Vaxillaire M., Rakotoambinina B., Thuillier F., Passa P., Froguel P., Robert J.J., Velho G. Assessment of insulin sensitivity in glucokinase-deficient subjects. Diabetologia 1996, 39:82-90.
10. Cnop M., Welsh N., Jonas J.C., Jorns A., Lenzen S., Eizirik D.L. Mechanisms of pancreatic β-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 2005, 54(Suppl 2):S97-S107.
11. Cohen C.D., Kretzler M. Gene expression analysis of microdissected renal biopsies. Renal Disease: Techniques and Protocols 2003, 285-293. Humana Press. M. Goligorsky, N. Totowa (Eds.).
12. Danial N.N., Gramm C.F., Scorrano L., Zhang C.Y., Krauss S., Ranger A.M., Datta S.R., Greenberg M.E., Licklider L.J., Lowell B.B., Gygi S.P., Korsmeyer S.J. BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 2003, 424:952-956.
13. Danial N.N., Walensky L.D., Zhang C.Y., Choi C.S., Fisher J.K., Molina A.J., Datta S.R., Pitter K.L., Bird G.H., Wikstrom J.D., Deeney J.T., Robertson K., Morash J., Kulkarni A., Neschen S., Kim S., Greenberg M.E., Corkey B.E., Shirihai O.S., Shulman G.I., Lowell B.B., Korsmeyer S.J. Dual role of proapoptotic BAD in insulin secretion and β-cell survival. Nat. Med. 2008, 14:144-153.
14. Donath M.Y., Ehses J.A., Maedler K., Schumann D.M., Ellingsgaard H., Eppler E., Reinecke M. Mechanisms of β-cell death in type 2 diabetes. Diabetes 2005, 54(Suppl 2):S108-S113.
15. Eizirik D.L., Cardozo A.K., Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 2008, 29:42-61.
16. Fajans S.S., Bell G.I., Polonsky K.S. Molecular mechanisms and clinical pathophysiology of maturity-onset diabetes of the young. N. Engl. J. Med. 2001, 345:971-980.
17. Fajans S.S., Bell G.I. Phenotypic heterogeneity between different mutations of MODY subtypes and within MODY pedigrees. Diabetologia 2006, 49:1106-1108.
18. Fenner D., Odili S., Takahashi J.S., Matschinsky F.M., Bass J. Insight into glucokinase diabetes from ENU mutagenesis. Diabetes 2009, 58(Suppl 1):A308.
19. Froguel P., Vaxillaire M., Sun F., Velho G., Zouali H., Butel M.O., Lesage S., Vionnet N., Clement K., Fougerousse F., et al. Close linkage of glucokinase locus on chromosome 7p to early-onset non-insulin-dependent diabetes mellitus. Nature 1992, 356:162-164.
20. Froguel P., Zouali H., Vionnet N., Velho G., Vaxillaire M., Sun F., Lesage S., Stoffel M., Takeda J., Passa P., et al. Familial hyperglycaemia due to mutations in glucokinase. Definition of a subtype of diabetes mellitus. N. Engl. J. Med. 1993, 328:697-702.
21. Gloyn A.L. Glucokinase (GCK) mutations in hyper- and hypoglycaemia: maturity-onset diabetes of the young, permanent neonatal diabetes, and hyperinsulinaemia of infancy. Hum. Mutat. 2003, 22:353-362.
22. Grupe A., Hultgren B., Ryan A., Ma Y.H., Bauer M., Stewart T.A. Transgenic knockouts reveal a critical requirement for pancreatic β-cell glucokinase in maintaining glucose homeostasis. Cell 1995, 83:69-78.
23. Gundersen H.J., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988, 96:379-394.
24. Hattersley A.T., Turner R.C., Patel P., O'Rahilly S., Wainscoat J.S., Permutt M.A., Tanazawa Y., Chin K.C., Watkins P. Linkage of type 2 diabetes to the glucokinase gene. The Lancet 1992, 339:1307-1310.
25. Hattersley A.T., Pearson E.R. Minireview: pharmacogenetics and beyond: the interaction of therapeutic response, β-cell physiology, and genetics in diabetes. Endocrinology 2006, 147:2657-2663.
26. Herbach N., Goeke B., Schneider M., Hermanns W., Wolf E., Wanke R. Overexpression of a dominant negative GIP receptor in transgenic mice results in disturbed postnatal pancreatic islet and β-cell development. Regul. Pept. 2005, 125:103-117.
27. C95S mutant mice. Diabetes 2007, 56:1268-1276.
28. Herbach N., Schairer I., Blutke A., Kautz S., Siebert A., Goke B., Wolf E., Wanke R. Diabetic kidney lesions of GIPRdn transgenic mice. podocyte hypertrophy and thickening of the GBM precede glomerular hypertrophy and glomerulosclerosis. Am. J. Physiol. Renal Physiol. 2009, 296:F819-F829.
29. Hrabě de Angelis M., Flaswinkel H., Fuchs H., Rathkolb B., Soewarto D., Marschall S., Heffner S., Pargent W., Wuensch K., Jung M., Reis A., Richter T., Alessandrini F., Jakob T., Fuchs E., Kolb H., Kremmer E., Schaeble K., Rollinski B., Roscher A., Peters C., Meitinger T., Strom T., Steckler T., Holsboer F., Klopstock T., Gekeler F., Schindewolf C., Jung T., Avraham K., Behrendt H., Ring J., Zimmer A., Schughart K., Pfeffer K., Wolf E., Balling R. Genome-wide, large-scale production of mutant mice by ENU mutagenesis. Nat. Genet. 2000, 25:444-447.
30. Inoue M., Sakuraba Y., Motegi H., Kubota N., Toki H., Matsui J., Toyoda Y., Miwa I., Terauchi Y., Kadowaki T., Shigeyama Y., Kasuga M., Adachi T., Fujimoto N., Matsumoto R., Tsuchihashi K., Kagami T., Inoue A., Kaneda H., Ishijima J., Masuya H., Suzuki T., Wakana S., Gondo Y., Minowa O., Shiroishi T., Noda T. A series of maturity-onset diabetes of the young, type 2 (MODY2) mouse models generated by a large-scale ENU mutagenesis program. Hum. Mol. Genet. 2004, 13:1147-1157.
31. Johnson J. Pancreatic β-cell apoptosis in maturity-onset diabetes of the young. Can. J. Diabetes 2007, 31:67-74.
32. Justice M.J., Noveroske J.K., Weber J.S., Zheng B., Bradley A. Mouse ENU mutagenesis. Hum. Mol. Genet. 1999, 8:1955-1963.
33. Kauri L.M., Wang G.S., Patrick C., Bareggi M., Hill D.J., Scott F.W. Increased islet neogenesis without increased islet mass precedes autoimmune attack in diabetes-prone rats. Lab. Invest. 2007, 87:1240-1251.
34. Keays D.A., Clark T.G., Flint J. Estimating the number of coding mutations in genotypic- and phenotypic-driven N-ethyl-N-nitrosourea (ENU) screens. Mamm. Genome 2006, 17:230-238.
35. Kim W.H., Lee J.W., Suh Y.H., Hong S.H., Choi J.S., Lim J.H., Song J.H., Gao B., Jung M.H. Exposure to chronic high glucose induces β-cell apoptosis through decreased interaction of glucokinase with mitochondria: downregulation of glucokinase in pancreatic β-cells. Diabetes 2005, 54:2602-2611.
36. Klaften M., Hrabě de Angelis M. ARTS: a web-based tool for the set-up of high-throughput genome-wide mapping panels for the SNP genotyping of mouse mutants. Nucleic Acids Res. 2005, 33:W496-W500.
37. Leiter E.H., Gerling I.C., Flinn J.C. Spontaneous insulin-dependent diabetes in non-obese diabetic mice. comparisons with experimentially induced IDDM. Experimental Models of Diabetes 1999, CRC Press, Florida, USA. J.H. McNeill (Ed.).
38. Louvi A., Accili D., Efstratiadis A. Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev. Biol. 1997, 189:33-48.
39. Matschinsky F., Liang Y., Kesavan P., Wang L.Q., Froguel P., Velho G., Cohen D., Permutt M.A., Tanizawa Y., Jetton T.L., Niswender K., Magnuson M.A. Glucokinase as pancreatic β-cell glucose sensor and diabetes gene. J. Clin. Invest. 1993, 92:2092-2098.
40. Matschinsky F.M., Glaser B., Magnuson M.A. Pancreatic β-cell glucokinase: closing the gap between theoretical concepts and experimental realities. Diabetes 1998, 47:307-315.
41. Matschinsky F.M. Regulation of pancreatic b-cell glucokinase: from basics to therapeutics. Diabetes 2002, 51(Suppl 3):S394-S404.
42. Matschinsky F.M. Assessing the potential of glucokinase activators in diabetes therapy. Nat. Rev. Drug Discov. 2009, 8:399-416.
43. Murphy R., Ellard S., Hattersley A.T. Clinical implications of a molecular genetic classification of monogenic b-cell diabetes. Nat. Clin. Pract. Endocrinol. Metab. 2008, 4:200-213.
44. Newton C.R., Graham A., Heptinstall L.E., Powell S.J., Summers C., Kalsheker N., Smith J.C., Markham A.F. Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res. 1989, 17:2503-2516.
45. Niswender K.D., Postic C., Jetton T.L., Bennett B.D., Piston D.W., Efrat S., Magnuson M.A. Cell-specific expression and regulation of a glucokinase gene locus transgene. J. Biol. Chem. 1997, 272:22564-22569.
46. Njolstad P.R., Sovik O., Cuesta-Munoz A., Bjorkhaug L., Massa O., Barbetti F., Undlien D.E., Shiota C., Magnuson M.A., Molven A., Matschinsky F.M., Bell G.I. Neonatal diabetes mellitus due to complete glucokinase deficiency. N. Engl. J. Med. 2001, 344:1588-1592.
47. Onishi T., Okawa R., Ogawa T., Shintani S., Ooshima T. Phex mutation causes the reduction of npt2b mRNA in teeth. J. Dent. Res. 2007, 86:158-162.
48. Osbak K.K., Colclough K., Saint-Martin C., Beer N.L., Bellanne-Chantelot C., Ellard S., Gloyn A.L. Update on mutations in glucokinase (GCK), which cause maturity-onset diabetes of the young, permanent neonatal diabetes, and hyperinsulinaemic hypoglycaemia. Hum. Mutat. 2009, 30:1512-1526.
49. Parthiban V., Gromiha M.M., Schomburg D. CUPSAT: prediction of protein stability upon point mutations. Nucleic Acids Res. 2006, 34:W239-W242.
50. Pedelini L., Garcia-Gimeno M.A., Marina A., Gomez-Zumaquero J.M., Rodriguez-Bada P., Lopez-Enriquez S., Soriguer F.C., Cuesta-Munoz A.L., Sanz P. Structure-function analysis of the alpha 5 and the alpha 13 helices of human glucokinase: Description of two novel activating mutations. Protein Sci. 2005, 14:2080-2086.
51. Porter J.R., Barrett T.G. Monogenic syndromes of abnormal glucose homeostasis: clinical review and relevance to the understanding of the pathology of insulin resistance and β-cell failure. J. Med. Genet. 2005, 42:893-902.
52. Postic C., Shiota M., Niswender K.D., Jetton T.L., Chen Y., Moates J.M., Shelton K.D., Lindner J., Cherrington A.D., Magnuson M.A. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic β-cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 1999, 274:305-315.
53. Postic C., Shiota M., Magnuson M.A. Cell-specific roles of glucokinase in glucose homeostasis. Recent Prog. Horm. Res. 2001, 56:195-217.
54. Rathkolb B., Decker T., Fuchs E., Soewarto D., Fella C., Heffner S., Pargent W., Wanke R., Balling R., Hrabě de Angelis M., Kolb H.J., Wolf E. The clinical-chemical screen in the Munich ENU Mouse Mutagenesis Project: screening for clinically relevant phenotypes. Mamm. Genome 2000, 11:543-546.
55. Rathkolb B., Fuchs E., Kolb H.J., Renner-Muller I., Krebs O., Balling R., Hrabě de Angelis M., Wolf E. Large-scale N-ethyl-N-nitrosourea mutagenesis of mice-from phenotypes to genes. Exp. Physiol. 2000, 85:635-644.
56. Terauchi Y., Sakura H., Yasuda K., Iwamoto K., Takahashi N., Ito K., Kasai H., Suzuki H., Ueda O., Kamada N., et al. Pancreatic b-cell-specific targeted disruption of glucokinase gene. Diabetes mellitus due to defective insulin secretion to glucose. J. Biol. Chem. 1995, 270:30253-30256.
57. Toye A.A., Moir L., Hugill A., Bentley L., Quarterman J., Mijat V., Hough T., Goldsworthy M., Haynes A., Hunter A.J., Browne M., Spurr N., Cox R.D. A new mouse model of type 2 diabetes, produced by N-ethyl-nitrosourea mutagenesis, is the result of a missense mutation in the glucokinase gene. Diabetes 2004, 53:1577-1583.
58. van Buerck L., Blutke A., Kautz S., Rathkolb B., Klaften M., Wagner S., Kemter E., Hrabě de Angelis M., Wolf E., Aigner B., Wanke R., Herbach N. Phenotypic and pathomorphological characteristics of a novel mutant mouse model for maturity-onset diabetes of the young type 2 (MODY 2). Am. J. Physiol. Endocrinol. Metab. 2010, 298:E512-E523.
59. van de Bunt M., Gloyn A.L. Monogenic disorders of the pancreatic β-cell: personalising treatment for rare forms of diabetes and hypoglycaemia. Personalized Med. 2007, 4:247-259.
60. van Haeften T.W., van Maarschalkerweerd W.W., Gerich J.E., van der Veen E.A. Decreased insulin secretory capacity and normal pancreatic b-cell glucose sensitivity in non-obese patients with NIDDM. Eur. J. Clin. Invest. 1991, 21:168-174.
61. Velho G., Froguel P., Clement K., Pueyo M.E., Rakotoambinina B., Zouali H., Passa P., Cohen D., Robert J.J. Primary pancreatic b-cell secretory defect caused by mutations in glucokinase gene in kindreds of maturity-onset diabetes of the young. Lancet 1992, 340:444-448.
62. Velho G., Vaxillaire M., Boccio V., Charpentier G., Froguel P. Diabetes complications in NIDDM kindreds linked to the MODY3 locus on chromosome 12q. Diabetes Care 1996, 19:915-919.
63. Velho G., Froguel P. Genetic, metabolic and clinical characteristics of maturity-onset diabetes of the young. Eur. J. Endocrinol. 1998, 138:233-239.
64. Venselaar H., te Beek T.A.H., Kuipers R.K.P., Hekkelman M.L., Vriend G. Protein structure analysis of mutations causing inheritable diseases. An e-Science approach with life scientist friendly interfaces. BMC Bioinformatics 2010, 11.
65. Vionnet N., Stoffel M., Takeda J., Yasuda K., Bell G.I., Zouali H., Lesage S., Velho G., Iris F., Passa P., Froguel P., Cohen D. Nonsense mutation in the glucokinase gene causes early-onset non-insulin-dependent diabetes-mellitus. Nature 1992, 356:721-722.
66. Wanke R., Weis S., Kluge D., Kahnt E., Schenck E., Brem G., Herrmanns W. Morphometric evaluation of the pancreas of growth hormone-transgenic mice. Acta Stereologica 1994, 4:3-8.
67. Waterfield T., Gloyn A.L. Monogenic β-cell dysfunction in children: clinical phenotypes, genetic etiology and mutational pathways. Pediatr. Health 2008, 2:517-532.
68. Winter W.E. Newly defined genetic diabetes syndromes: maturity-onset diabetes of the young. Rev. Endocr. Metab. Disord. 2003, 4:43-51.
69. Zinovieva N., Vasicek D., Aigner B., Müller M., Brem G. Short communication: single tube allele specific (STAS) PCR for direct determination of the mutation in the porcine ryanodine receptor gene associated with malignant hyperthermia. Anim. Biotechnol. 1996, 7:173-177.