The Krüppel-like zinc finger protein GLIS3 transactivates neurogenin 3 for proper fetal pancreatic islet differentiation in mice

Diabetologia

Volumn 54, Issue 10, 2011, Pages 2595-2605

  Yang, Y ^a   Chang, B H J ^a   Yechoor, V ^a   Chen, W ^a   Li, L ^a   Tsai, M J ^a   Chan, L ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b ST LUKE S EPISCOPAL HOSPITAL   (United States)

Author keywords

GLIS3; Neonatal diabetes; Neurog3; Pancreatic islet differentiation

Indexed keywords

GLUCOSE; HEPATOCYTE NUCLEAR FACTOR 1BETA; HEPATOCYTE NUCLEAR FACTOR 3BETA; HEPATOCYTE NUCLEAR FACTOR 6; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR GLIS3; NEUROGENIN 3; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CELL CULTURE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE SEVERITY; DNA BINDING; DOWN REGULATION; EMBRYO DEVELOPMENT; EXON; FETUS; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSCRIPTION; GLUCOSE BLOOD LEVEL; GROWTH RETARDATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEWBORN DIABETES MELLITUS; NEWBORN DISEASE; NONHUMAN; ORGAN WEIGHT; PANCREAS; PANCREAS ISLET CELL; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; STOP CODON; TRANSACTIVATION; UPREGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FEMALE; ISLETS OF LANGERHANS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PREGNANCY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; RESPONSE ELEMENTS; TRANS-ACTIVATORS;

EID: 80054107636     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2255-9     Document Type: Article

References (41)

1. JP Hamilton-Shield 2007 Overview of neonatal diabetes Endocr Dev 12 12 23 17923765 10.1159/000109601 1:CAS:528:DC%2BD1MXltlSnsrk%3D
2. F Barbetti 2007 Diagnosis of neonatal and infancy-onset diabetes Endocr Dev 11 83 93 17986829 10.1159/000111060
3. SA Greeley SE Tucker RN Naylor GI Bell LH Philipson 2010 Neonatal diabetes mellitus: a model for personalized medicine Trends Endocrinol. Metab 21 464 472 20434356 10.1016/j.tem.2010.03.004 1:CAS:528:DC%2BC3cXpsFKhs7Y%3D
4. D Taha M Barbar H Kanaan BJ Williamson 2003 Neonatal diabetes mellitus, congenital hypothyroidism, hepatic fibrosis, polycystic kidneys, and congenital glaucoma: a new autosomal recessive syndrome? Am J Med Genet A 122A 269 273 12966531 10.1002/ajmg.a.20267 (Pubitemid 37152876)
5. YS Kim G Nakanishi M Lewandoski AM Jetten 2003 GLIS3, a novel member of the GLIS subfamily of Kruppel-like zinc finger proteins with repressor and activation functions Nucleic Acids Res 31 5513 5525 14500813 10.1093/nar/gkg776 1:CAS:528:DC%2BD3sXns1CntbY%3D (Pubitemid 37441921)
6. V Senee C Chelala S Duchatelet D Feng H Blanc JC Cossec, et al. 2006 Mutations in GLIS3 are responsible for a rare syndrome with neonatal diabetes mellitus and congenital hypothyroidism Nat Genet 38 682 687 16715098 10.1038/ng1802 1:CAS:528:DC%2BD28XltVOhurw%3D (Pubitemid 43927311)
7. Y Yang BH Chang SL Samson MV Li L Chan 2009 The Kruppel-like zinc finger protein Glis3 directly and indirectly activates insulin gene transcription Nucleic Acids Res 37 2529 2538 19264802 10.1093/nar/gkp122 1:CAS:528: DC%2BD1MXlslertbo%3D
8. N Watanabe K Hiramatsu R Miyamoto, et al. 2009 A murine model of neonatal diabetes mellitus in Glis3-deficient mice FEBS Lett 583 2108 2113 19481545 10.1016/j.febslet.2009.05.039 1:CAS:528:DC%2BD1MXnt1Oku70%3D
9. HS Kang YS Kim G ZeRuth, et al. 2009 Transcription factor Glis3, a novel critical player in the regulation of pancreatic beta-cell development and insulin gene expression Mol Cell Biol 29 6366 6379 19805515 10.1128/MCB.01259-09 1:CAS:528:DC%2BC3cXisVKgtr4%3D
10. G Gu J Dubauskaite DA Melton 2002 Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors Development 129 2447 2457 11973276 1:CAS:528:DC%2BD38XksFWnur0%3D (Pubitemid 34863851)
11. A Apelqvist H Li L Sommer, et al. 1999 Notch signalling controls pancreatic cell differentiation Nature 400 877 881 10476967 10.1038/23716 1:CAS:528:DyaK1MXlslGksbw%3D (Pubitemid 29406724)
12. VM Schwitzgebel DW Scheel JR Conners, et al. 2000 Expression of neurogenin3 reveals an islet cell precursor population in the pancreas Development 127 3533 3542 10903178 1:CAS:528:DC%2BD3cXmsFKitLY%3D
13. J Jensen RS Heller T Funder-Nielsen, et al. 2000 Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: a role for the notch pathway in repression of premature differentiation Diabetes 49 163 176 10868931 10.2337/diabetes.49.2.163 1:CAS:528:DC%2BD3cXpsl2lug%3D%3D (Pubitemid 30070993)
14. EC Lee D Yu DV Martinez, et al. 2001 A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA Genomics 73 56 65 11352566 10.1006/geno.2000.6451 1:CAS:528:DC%2BD3MXisVykurg%3D (Pubitemid 32382387)
15. A Nagy J Rossant R Nagy W Bramow-Newerly JC Roder 1993 Derivation of completely cell culture-derived mice from early-passage embryonic stem cells Proc Natl Acad Sci USA 90 8424 8428 8378314 10.1073/pnas.90.18.8424 1:STN:280:DyaK3szptFeltA%3D%3D (Pubitemid 23277681)
16. S O'Gorman NA Dagenais M Qian Y Marchuk 1997 Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells Proc Natl Acad Sci USA 94 14602 14607 9405659 10.1073/pnas.94.26.14602 (Pubitemid 28041420)
17. FS Schreiber TB Deramaudt TB Brunner, et al. 2004 Successful growth and characterization of mouse pancreatic ductal cells: functional properties of the Ki-RAS(G12V) oncogene Gastroenterology 127 250 260 15236190 10.1053/j.gastro. 2004.03.058 1:CAS:528:DC%2BD2cXmsVShs7Y%3D (Pubitemid 38962292)
18. S Mizushima S Nagata 1990 pEF-BOS, a powerful mammalian expression vector Nucleic Acids Res 18 5322 1698283 10.1093/nar/18.17.5322 1:CAS:528: DyaK3cXmt1GksrY%3D (Pubitemid 20270119)
19. M Sander L Sussel J Conners, et al. 2000 Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas Development 127 5533 5540 11076772 1:CAS:528:DC%2BD3MXltFWkuw%3D%3D (Pubitemid 32049205)
20. SB Nelson AE Schaffer M Sander 2007 The transcription factors Nkx6.1 and Nkx6.2 possess equivalent activities in promoting beta-cell fate specification in Pdx1+ pancreatic progenitor cells Development 134 2491 2500 17537793 10.1242/dev.002691 1:CAS:528:DC%2BD2sXosVKrtLk%3D (Pubitemid 47074143)
21. JM Oliver-Krasinski DA Stoffers 2008 On the origin of the beta cell Genes Dev 22 1998 2021 18676806 10.1101/gad.1670808 1:CAS:528:DC%2BD1cXpslKqsLc%3D
22. MC Jorgensen J Ahnfelt-Ronne J Hald OD Madsen P Serup J Hecksher-Sorensen 2007 An illustrated review of early pancreas development in the mouse Endocr Rev 28 685 705 17881611 10.1210/er.2007-0016 (Pubitemid 47606652)
23. G Gradwohl A Dierich M LeMeur F Guillemot 2000 Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas Proc Natl Acad Sci USA 97 1607 1611 10677506 10.1073/pnas.97.4.1607 1:CAS:528:DC%2BD3cXhsFCrsLk%3D (Pubitemid 30118489)
24. LC Murtaugh 2007 Pancreas and beta-cell development: from the actual to the possible Development 134 427 438 17185316 10.1242/dev.02770 1:CAS:528:DC%2BD2sXjtlWgs74%3D (Pubitemid 46332480)
25. HP Huang M Liu HM El-Hodiri K Chu M Jamrich MJ Tsai 2000 Regulation of the pancreatic islet-specific gene BETA2 (neuroD) by neurogenin 3 Mol Cell Biol 20 3292 3307 10757813 10.1128/MCB.20.9.3292-3307.2000 1:CAS:528: DC%2BD3cXivFSrtrs%3D (Pubitemid 30215041)
26. R Gasa C Mrejen N Leachman, et al. 2004 Proendocrine genes coordinate the pancreatic islet differentiation program in vitro Proc Natl Acad Sci USA 101 13245 13250 15340143 10.1073/pnas.0405301101 1:CAS:528:DC%2BD2cXnvFemsrw%3D (Pubitemid 39209650)
27. Y Heremans M van de Casteele P In't Veld, et al. 2002 Recapitulation of embryonic neuroendocrine differentiation in adult human pancreatic duct cells expressing neurogenin 3 J Cell Biol 159 303 312 12403815 10.1083/jcb.200203074 1:CAS:528:DC%2BD38XosVaksrY%3D (Pubitemid 35283399)
28. JM Oliver-Krasinski MT Kasner J Yang, et al. 2009 The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice J Clin Invest 119 1888 1898 19487809 10.1172/JCI37028 1:CAS:528:DC%2BD1MXosVCrsr4%3D
29. J Jiang M Au K Lu, et al. 2007 Generation of insulin-producing islet-like clusters from human embryonic stem cells Stem Cells 25 1940 1953 17510217 10.1634/stemcells.2006-0761 1:CAS:528:DC%2BD2sXhtVSqsbbI (Pubitemid 47258172)
30. S Miyazaki E Yamato J Miyazaki 2004 Regulated expression of pdx-1 promotes in vitro differentiation of insulin-producing cells from embryonic stem cells Diabetes 53 1030 1037 15047618 10.2337/diabetes.53.4.1030 1:CAS:528:DC%2BD2cXivFyqsbw%3D (Pubitemid 38436615)
31. P Jacquemin SM Durviaux J Jensen, et al. 2000 Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3 Mol Cell Biol 20 4445 4454 10825208 10.1128/MCB.20.12.4445-4454.2000 1:CAS:528:DC%2BD3cXjvFWrsb0%3D (Pubitemid 30346639)
32. FC Lynn SB Smith ME Wilson KY Yang N Nekrep MS German 2007 Sox9 coordinates a transcriptional network in pancreatic progenitor cells Proc Natl Acad Sci USA 104 10500 10505 17563382 10.1073/pnas.0704054104 1:CAS:528:DC%2BD2sXnt1Kkt7c%3D (Pubitemid 47185694)
33. JC Lee SB Smith H Watada, et al. 2001 Regulation of the pancreatic pro-endocrine gene neurogenin3 Diabetes 50 928 936 11334435 10.2337/diabetes.50. 5.928 1:CAS:528:DC%2BD3MXkvFSgtbw%3D (Pubitemid 32374521)
34. MA Maestro SF Boj RF Luco, et al. 2003 Hnf6 and Tcf2 (MODY5) are linked in a gene network operating in a precursor cell domain of the embryonic pancreas Hum Mol Genet 12 3307 3314 14570708 10.1093/hmg/ddg355 1:CAS:528: DC%2BD3sXpsl2mtLs%3D (Pubitemid 37541076)
35. J Hald JP Hjorth MS German OD Madsen P Serup J Jensen 2003 Activated Notch1 prevents differentiation of pancreatic acinar cells and attenuate endocrine development Dev Biol 260 426 437 12921743 10.1016/S0012-1606(03)00326- 9 1:CAS:528:DC%2BD3sXmt1WqtLs%3D (Pubitemid 36966084)
36. LC Murtaugh BZ Stanger KM Kwan DA Melton 2003 Notch signaling controls multiple steps of pancreatic differentiation Proc Natl Acad Sci USA 100 14920 14925 14657333 10.1073/pnas.2436557100 1:CAS:528:DC%2BD3sXpvFaqtrc%3D (Pubitemid 37517992)
37. DS Dichmann H Yassin P Serup 2006 Analysis of pancreatic endocrine development in GDF11-deficient mice Dev Dyn 235 3016 3025 16964608 10.1002/dvdy.20953 1:CAS:528:DC%2BD28Xht12mt7jJ (Pubitemid 44749690)
38. EB Harmon AA Apelqvist NG Smart X Gu DH Osborne SK Kim 2004 GDF11 modulates NGN3+ islet progenitor cell number and promotes beta-cell differentiation in pancreas development Development 131 6163 6174 15548585 10.1242/dev.01535 1:CAS:528:DC%2BD2MXnslajuw%3D%3D (Pubitemid 40123929)
39. A Grapin-Botton AR Majithia DA Melton 2001 Key events of pancreas formation are triggered in gut endoderm by ectopic expression of pancreatic regulatory genes Genes Dev 15 444 454 11230152 10.1101/gad.846001 1:CAS:528:DC%2BD3MXhvVOju7c%3D (Pubitemid 32187005)
40. KA Johansson U Dursun N Jordan, et al. 2007 Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types Dev Cell 12 457 465 17336910 10.1016/j.devcel.2007.02.010 1:CAS:528:DC%2BD2sXjtlWjtr0%3D
41. V Yechoor V Liu C Espiritu, et al. 2009 Neurogenin3 is sufficient for transdetermination of hepatic progenitor cells into neo-islets in vivo but not transdifferentiation of hepatocytes Dev Cell 16 358 373 19289082 10.1016/j.devcel.2009.01.012 1:CAS:528:DC%2BD1MXjs1ygu7c%3D