Insulin gene expression is regulated by DNA methylation

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Kuroda, Akio ^a,b   Rauch, Tibor A ^a,c   Todorov, Ivan ^a   Ku, Hsun Teresa ^a   Al Abdullah, Ismail H ^a   Kandeel, Fouad ^a   Mullen, Yoko ^a   Pfeifer, Gerd P ^a   Ferreri, Kevin ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; CPG OLIGODEOXYNUCLEOTIDE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FORSKOLIN; GENOMIC DNA; GLUCOSE; INSULIN; METHYL CPG BINDING PROTEIN 2; PRIMER DNA;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; GENE ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROMOTER REGION; PROTEIN BINDING; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CHEMISTRY; CPG ISLAND; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; METABOLISM; TRANSCRIPTION INITIATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; DNA PRIMERS; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MODELS, BIOLOGICAL; MODELS, GENETIC; PROMOTER REGIONS, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 70349138460     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006953     Document Type: Article

References (51)

1. Wentworth BM, Schaefer IM, Villa-Komaroff L, Chirgwin JM (1986) Characterization of the two nonallelic genes encoding mouse preproinsulin. Journal of Molecular Evolution 23: 305-312.
2. Palumbo MO, Levi D, Chentoufi AA, Polychronakos C (2006) Isolation and characterization of proinsulin-producing medullary thymic epithelial cell clones. Diabetes 55: 2595-2601.
3. Deltour L, Montagutelli X, Guenet JL, Jami J, Paldi A (1995) Tissue- and developmental stage-specific imprinting of the mouse proinsulin gene, Ins2. Dev Biol 168: 686-688.
4. Leighton PA, Saam JR, Ingram RS, Stewart CL, Tilghman SM (1995) An enhancer deletion affects both H19 and Igf2 expression. Genes Dev 9: 2079-2089.
5. Lamotte L, Jackerott M, Bucchini D, Jami J, Joshi RL, et al. (2004) Knock-in of diphteria toxin A chain gene at Ins2 locus: effects on islet development and localization of Ins2 expression in the brain. Transgenic Research 13: 463-473.
6. Moore GE, Abu-Amero SN, Bell G, Wakeling EL, Kingsnorth A, et al. (2001) Evidence that insulin is imprinted in the human yolk sac. Diabetes 50: 199-203.
7. Caspary T, Cleary MA, Baker CC, Guan XJ, Tilghman SM (1998) Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Molecular and cellular biology 18: 3466-3474.
8. Duvillié B, Bucchini D, Tang T, Jami J, Pàldi A (1998) Imprinting at the mouse Ins2 locus: evidence for cis- and trans-allelic interactions. Genomics 47: 52-57.
9. Bennett ST, Lucassen AM, Gough SCL, Powell EE, Undlien DE, et al. (1995) Susceptibility to human type 1 diabetes at IDDM2 is determined by tandem repeat variation at the insulin gene minisatellite locus. Nature Genetics 9: 284-292.
10. Feil R, Walter J, Allen ND, Reik W (1994) Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development 120: 2933-2943.
11. Vu TH, Li T, Nguyen D, Nguyen BT, Yao XM, et al. (2000) Symmetric and asymmetric DNA methylation in the human IGF2-H19 imprinted region. Genomics 64: 132-143.
12. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nature Reviews Cancer 6: 107-116.
13. Robertson KD (2005) DNA methylation and human disease. Nature Reviews Genetics 6: 597-610.
14. Jirtle RL, Skinner MK (2007) Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8: 253-262.
15. Turek-Plewa J, Jagodziński PP (2005) The role of mammalian DNA methyltransferases in the regulation of gene expression. Cellular & molecular biology letters 10: 631-647.
16. Hay CW, Docherty K (2006) Comparative analysis of insulin gene promoters: implications for diabetes research. Diabetes 55: 3201-3213.
17. Faideau B, Larger E, Lepault F, Carel JC, Boitard C (2005) Role of beta-cells in type 1 diabetes pathogenesis. Diabetes 54: S87-96.
18. Hamaguchi K, Gaskins HR, Leiter EH (1991) NIT-1, a pancreatic beta-cell line established from a transgenic NOD/Lt mouse. Diabetes 40: 842-849.
19. Lukowiak B, Vandewalle B, Riachy R, Kerr-Conte J, Gmyr V, et al. (2001) Identification and purification of functional human beta-cells by a new specific zinc-fluorescent probe. The journal of histochemistry and cytochemistry 49: 519-528.
20. Todorov I, Omori K, Pascual M, Rawson J, Nair I, et al. (2006) Generation of human islets through expansion and differentiation of non-islet pancreatic cells discarded (pancreatic discard) after islet isolation. Pancreas 32: 130-138.
21. Docherty K, Clark AR (1994) Nutrient regulation of insulin gene expression. The FASEB journal 8: 20-27.
22. Poitout V, Hagman D, Stein R, Artner I, Robertson RP, et al. (2006) Regulation of the insulin gene by glucose and fatty acids. The Journal of nutrition 136: 873-876.
23. German M, Ashcroft S, Docherty K, Edlund H, Edlund T, et al. (1995) The insulin gene promoter. A simplified nomenclature. Diabetes 44: 1002-1004.
24. Melloul D, Marshak S, Cerasi E (2002) Regulation of insulin gene transcription. Diabetologia 45: 309-326.
25. Seamon KB, Padgett W, Daly JW (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proceedings of the National Academy of Sciences of the United States of America 78: 3363-3367.
26. Hay CW, Ferguson LA, Docherty K (2007) ATF-2 stimulates the human insulin promoter through the conserved CRE2 sequence. Biochimica et biophysica acta 1769: 79-91.
27. Iannello RC, Gould JA, Young JC, Giudice A, Medcalf R, et al. (2000) Methylation-dependent silencing of the testis-specific Pdha-2 basal promoter occurs through selective targeting of an activating transcription factor/cAMP-responsive element-binding site. The Journal of biological chemistry 275: 19603-19608.
28. Iguchi-Ariga SM, Schaffner W (1989) CpG methylation of the cAMP-responsive enhancer/promoter sequence TGACGTCA abolishes specific factor binding as well as transcriptional activation. Genes & development 3: 612-619.
29. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, et al. (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proceedings of the National Academy of Sciences of the United States of America 102: 4459-4464.
30. Meehan RR, Lewis JD, Bird AP (1992) Characterization of MeCP2, a vertebrate DNA binding protein with affinity for methylated DNA. Nucleic Acids Research 20: 5085-5092.
31. Sharma RP, Grayson DR, Guidotti A, Costa E (2005) Chromatin, DNA methylation and neuron gene regulation - the purpose of the package. Journal of psychiatry & neuroscience 30: 257-263.
32. Evans-Molina C, Garmey JC, Ketchum R, Brayman KL, Deng S, et al. (2007) Glucose regulation of insulin gene transcription and pre-mRNA processing in human islets. Diabetes 56: 827-835.
33. D'Amour KA, Bang AG, E S, Kelly O, Agulnick AD, et al. (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nature Biotechnology 24: 1392-1401.
34. Ku HT, Chai J, Kim YJ, White P, Purohit-Ghelani S, et al. (2007) Insulin-expressing colonies developed from murine embryonic stem cell-derived progenitors. Diabetes 56: 921-929.
35. Lee CS, Perreault N, Brestelli JE, Kaestner KH (2002) Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev 16: 1488-1497.
36. Gasa R, Mrejen C, Leachman N, Otten M, Barnes M, et al. (2004) Proendocrine genes coordinate the pancreatic islet differentiation program in vitro. Proceedings of the National Academy of Sciences of the United States of America 101: 13245-13250.
37. Gu G, Dubauskaite J, Melton DA (2002) Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129: 2447-2457.
38. Goodge KA, Hutton JC (2000) Translational regulation of proinsulin biosynthesis and proinsulin conversion in the pancreatic beta-cell. Semin Cell Dev Biol 11: 235-242.
39. Wicksteed B, Alarcon C, Briaud I, Lingohr MK, Rhodes CJ (2003) Glucose-induced translational control of proinsulin biosynthesis is proportional to preproinsulin mRNA levels in islet beta-cells but not regulated via a positive feedback of secreted insulin. J Biol Chem 278: 42080-42090.
40. Uchizono Y, Alarcon C, Wicksteed BL, Marsh BJ, Rhodes CJ (2007) The balance between proinsulin biosynthesis and insulin secretion: where can imbalance lead? Diabetes Obes Metab 9 Suppl 2: 56-66.
41. Lorenzo M, Fernandez-Veledo S, Vila-Bedmar R, Garcia-Guerra L, De Alvaro C, et al. (2008) Insulin resistance induced by tumor necrosis factor-alpha in myocytes and brown adipocytes. J Anim Sci 86: E94-104.
42. Youngren JF (2007) Regulation of insulin receptor function. Cell Mol Life Sci 64: 873-891.
43. Wu C, Gilbert W (1981) Tissue-specific exposure of chromatin structure at the 5′ terminus of the rat preproinsulin II gene. Proceedings of the National Academy of Sciences of the United States of America 78: 1577-1580.
44. Francis J, Babu DA, Deering TG, Chakrabarti SK, Garmey JC, et al. (2006) Role of chromatin accessibility in the occupancy and transcription of the insulin gene by the pancreatic and duodenal homeobox factor 1. Molecular endocrinology (Baltimore, Md) 20: 3133-3145.
45. Francis J, Chakrabarti SK, Garmey JC, Mirmira RG (2005) Pdx-1 links histone H3-Lys-4 methylation to RNA polymerase II elongation during activation of insulin transcription. The Journal of biological chemistry 280: 36244-36253.
46. Abu M, Waters TR (2003) The main role of human thymine-DNA glycosylase is removal of thymine produced by deamination of 5-methylcytosine and not removal of ethenocytosine. J Biol Chem 278: 8739-8744.
47. Morgan HD, Dean W, Coker HA, Reik W, Petersen-Mahrt SK (2004) Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J Biol Chem 279: 52353-52360.
48. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein expression and purification 41: 207-234.
49. Dell G, Charalambous M, Ward A (2001) In vitro methylation of specific regions in recombinant DNA constructs by excision and religation. Methods in molecular biology 181: 251-258.
50. Martinowich K, Hattori D, Wu H, Fouse S, He F, et al. (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302: 890-893.
51. Schreiber E, Matthias P, Müller MM, Schaffner W (1989) Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Research 17: 6419.