Exendin-4 increases histone acetylase activity and reverses epigenetic modifications that silence Pdx1 in the intrauterine growth retarded rat

Diabetologia

Volumn 54, Issue 10, 2011, Pages 2606-2614

  Pinney, S E ^a   Jaeckle Santos, L J ^a   Han, Y ^a   Stoffers, D A ^a   Simmons, R A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Beta cell; Epigenetics; Exendin 4; Histone; Intrauterine growth retardation; Pdx1

Indexed keywords

BETA ACTIN; DNA METHYLTRANSFERASE 1; EXENDIN 4; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE PCAF; HISTONE H3; HISTONE H3 LYSINE 4; MESSENGER RNA; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DIABETES MELLITUS; DNA METHYLATION; DNA MODIFICATION; ENZYME ACTIVITY; ENZYME BINDING; EPIGENETICS; FETUS; GENE SILENCING; HISTONE ACETYLATION; HISTONE MODIFICATION; INTRAUTERINE GROWTH RETARDATION; NONHUMAN; PANCREAS ISLET BETA CELL; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PYROSEQUENCING; RAT;

ANIMALS; ANIMALS, NEWBORN; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FETAL GROWTH RETARDATION; HISTONE ACETYLTRANSFERASES; HOMEODOMAIN PROTEINS; PEPTIDES; PROMOTER REGIONS, GENETIC; RATS; TRANS-ACTIVATORS; UPSTREAM STIMULATORY FACTORS; VENOMS;

EID: 80054098357     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2250-1     Document Type: Article

References (48)

1. DJ Barker 1999 The fetal origins of type 2 diabetes mellitus Ann Intern Med 16 322 324 (Pubitemid 29091862)
2. RA Simmons L Templeton S Gertz H Niu 2001 Intrauterine growth retardation leads to type II diabetes in adulthood in the rat Diabetes 50 2279 2286 11574409 10.2337/diabetes.50.10.2279 1:CAS:528:DC%2BD3MXntlGhurc%3D (Pubitemid 33641912)
3. RA Simmons I Suponitsky-Kroyter MA Selak 2005 Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to beta-cell failure J Biol Chem 280 28785 28791 15946949 10.1074/jbc.M505695200 1:CAS:528:DC%2BD2MXmvFSnt7o%3D (Pubitemid 41105780)
4. DA Stoffers BM Desai DD Ng RA Simmons 2003 Neonatal exendin-4 prevents the development of diabetes mellitus in the intrauterine growth retarded rat Diabetes 52 734 740 12606515 10.2337/diabetes.52.3.734 1:CAS:528: DC%2BD3sXitFajtrY%3D (Pubitemid 36323581)
5. RA Simmons 2007 Developmental origins of diabetes: the role of epigenetic mechanisms Curr Opin Endocrinol Diabetes Obes 14 13 16 17940413 10.1097/MED.0b013e328013da5b 1:CAS:528:DC%2BD2sXitVenu78%3D (Pubitemid 46375382)
6. M Brissova M Blaha C Spear, et al. 2005 Reduced PDX-1 expression impairs islet response to insulin resistance and worsens glucose homeostasis Am J Physiol Endocrinol Metab 288 E707 E714 15562255 10.1152/ajpendo.00252.2004 1:CAS:528:DC%2BD2MXjtlyjsrs%3D (Pubitemid 40397205)
7. RN Kulkarni US Jhala JN Winnay S Krajewski M Montminy CR Kahn 2004 PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance J Clin Invest 114 828 836 15372107 1:CAS:528:DC%2BD2cXnslWiurc%3D (Pubitemid 39578742)
8. AM Holland LJ Gonez G Naselli RJ MacDonald LC Harrison 2005 Conditional expression demonstrates the role of the homeodomain transcription factor Pdx1 in maintenance and regeneration of beta-cells in the adult pancreas Diabetes 54 2586 2595 16123346 10.2337/diabetes.54.9.2586 1:CAS:528:DC%2BD2MXhtVSjs7rO (Pubitemid 41233579)
9. J Jonsson LJ Gonez G Naselli RJ MacDonald LC Harrison 1994 Insulin-promoter-factor 1 is required for pancreas development in mice Nature 371 606 609 7935793 10.1038/371606a0 1:CAS:528:DyaK2cXmsFahsbg%3D (Pubitemid 24315741)
10. MF Offield TL Jetton PA Labosky, et al. 1996 PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum Development 122 983 995 8631275 1:CAS:528:DyaK28XhvVOruro%3D (Pubitemid 26096002)
11. H Hui R Perfetti 2002 Pancreas duodenum homeobox-1 regulates pancreas development during embryogenesis and islet cell function in adulthood Eur J Endocrinol 146 129 141 11834421 10.1530/eje.0.1460129 1:CAS:528: DC%2BD38XhvVenurk%3D (Pubitemid 34162905)
12. U Ahlgren J Jonsson L Jonsson K Simu H Edlund 1998 Beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes Genes Dev 12 1763 1768 9637677 10.1101/gad.12.12.1763 1:CAS:528:DyaK1cXktl2isbw%3D (Pubitemid 28304328)
13. DA Stoffers NT Zinkin V Stanojevic WL Clarke JF Habener 1997 Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence Nat Genet 15 106 110 8988180 10.1038/ng0197-106 1:CAS:528:DyaK2sXjsFKitA%3D%3D (Pubitemid 27014961)
14. JH Park DA Stoffers RD Nicholls RA Simmons 2008 Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1 J Clin Invest 118 2316 2324 18464933 10.1172/JCI32011 1:CAS:528:DC%2BD1cXntVClsrY%3D (Pubitemid 351872348)
15. DA Stoffers TJ Kieffer DJ Drucker S Bonner-Weir JF Habener JM Egan 2000 Insulinotropic glucagon-like peptide 1 agonists stimulate expression of homeodomain protein IDX-1 and increase islet size in mouse pancreas Diabetes 49 741 748 10905482 10.2337/diabetes.49.5.741 1:CAS:528:DC%2BD3cXjsF2msrc%3D (Pubitemid 30339989)
16. WJ Song WE Schreiber E Zhong, et al. 2008 Exendin-4 stimulation of cyclin A2 in beta-cell proliferation Diabetes 57 2371 2381 18544709 10.2337/db07-1541 1:CAS:528:DC%2BD1cXhtFSrtrjP
17. J Movassat GM Beattie AD Lopez A Hayek 2002 Exendin 4 up-regulates expression of PDX 1 and hastens differentiation and maturation of human fetal pancreatic cells J Clin Endocrinol Metab 87 4775 4781 12364473 10.1210/jc.2002-020137 1:CAS:528:DC%2BD38XnvFCrtro%3D (Pubitemid 35247075)
18. R Perfetti J Zhou ME Doyle JM Egan 2000 Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats Endocrinology 141 4600 4605 11108273 10.1210/en.141.12.4600 1:CAS:528: DC%2BD3cXosVSqsbo%3D (Pubitemid 32055138)
19. E Cheung P Mayr F Coda-Zabetta PG Woodman DS Boam 1999 DNA-binding activity of the transcription factor upstream stimulatory factor 1 (USF1) is regulated by cyclin-dependent phosphorylation Biochem J 344 145 152 10548544 10.1042/0264-6021:3440145 1:CAS:528:DyaK1MXns1yjt7w%3D
20. MD Galibert S Carreira CR Goding 2001 The USF1 transcription factor is a novel target for the stress-responsive p38 kinase and mediates UV-induced tyrosinase expression EMBO J 20 5022 5031 11532965 10.1093/emboj/20.17.5022 1:CAS:528:DC%2BD3MXnt1Cmurk%3D (Pubitemid 32851035)
21. Q Xiao A Kenessey K Ojamaa 2002 Role of USF1 phosphorylation on cardiac alpha-myosin heavy chain promoter activity Am J Physiol 283 H213 H219 1:CAS:528:DC%2BD38XlsVCksr0%3D
22. S Corre A Primot Y Baron J Le Seyec C Goding MD Galibert 2009 Target gene specificity of USF1 is directed via p38 mediated phosphorylation dependent acetylation J Biol Chem 284 18851 18862 19389701 10.1074/jbc.M808605200 1:CAS:528:DC%2BD1MXotVKnsbs%3D
23. K Sayasith JG Lussier J Sirois 2005 Role of upstream stimulatory factor phosphorylation in the regulation of the prostaglandin G/H synthase-2 promoter in granulosa cells J Biol Chem 280 28885 28893 15927963 10.1074/jbc.M413434200 1:CAS:528:DC%2BD2MXntVehu78%3D (Pubitemid 41161333)
24. M Haring S Offermann T Danker 2007 Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization Plant Methods 3 1 16 10.1186/1746-4811-3-11 (Pubitemid 350125929)
25. M Jaskelioff CL Peterson 2003 Chromatin and transcription: histones continue to make their marks Nat Cell Biol 5 395 399 12724776 10.1038/ncb0503-395 1:CAS:528:DC%2BD3sXjtlamu78%3D (Pubitemid 36592261)
26. G Liang JC Lin V Wei, et al. 2004 Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome Proc Natl Acad Sci USA 101 7357 7362 15123803 10.1073/pnas.0401866101 1:CAS:528:DC%2BD2cXksFaksLk%3D (Pubitemid 38638037)
27. KP Nightingale S Gendreizig DA White C Bradbury F Hollfelder BM Turner 2007 Cross talk between histone modifications in response to HDAC inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation J Biol Chem 282 4408 4416 17166833 10.1074/jbc.M606773200 1:CAS:528:DC%2BD2sXhsFKhu7s%3D (Pubitemid 47100929)
28. CR Vakoc MM Sachdeva H Wang GA Blobel 2006 Profile of histone lysine methylation across transcribed mammalian chromatin Mol Cell Biol 26 9185 9195 17030614 10.1128/MCB.01529-06 1:CAS:528:DC%2BD28XhtlemsLvN (Pubitemid 44904415)
29. J Qian EN Kaytor HC Towle LK Olson 1999 Upstream stimulatory factor regulates Pdx-1 gene expression in differentiated pancreatic -cells Biochem J 341 315 322 10393088 10.1042/0264-6021:3410315 1:CAS:528:DyaK1MXltFCksL4%3D (Pubitemid 29373655)
30. S Sharma J Leonard S Lee HD Chapman EH Leiter MR Montminy 1996 Pancreatic islet expression of the homeobox factor STF-1 (Pdx-1) relies on an E-box motif that binds USF J Biol Chem 271 2294 2299 8567692 10.1074/jbc.271.4.2294 1:CAS:528:DyaK28Xns1SisA%3D%3D (Pubitemid 26047822)
31. K Gerrish JC van Velkinburgh R Stein 2004 Conserved transcriptional regulatory domains of the pdx-1 gene Mol Endo 18 533 548 10.1210/me.2003-0371 1:CAS:528:DC%2BD2cXivFCqsbg%3D (Pubitemid 38328201)
32. M Gannon LW Gamer CV Wright 2001 Regulatory regions driving developmental and tissue-specific expression of the essential pancreatic gene pdx1 Dev Biol 238 185 201 11784003 10.1006/dbio.2001.0359 1:CAS:528:DC%2BD3MXmvFGks74%3D (Pubitemid 32939295)
33. ME Doyle JM Egan 2007 Mechanisms of action of GLP-1 in the pancreas Pharmocol Ther 113 546 593 10.1016/j.pharmthera.2006.11.007 1:CAS:528: DC%2BD2sXislKjsb4%3D (Pubitemid 46365961)
34. AJ Bannister T Kouzarides 1996 The CBP co-activator is a histone acetyltransferase Nature 384 641 643 8967953 10.1038/384641a0 1:CAS:528:DyaK2sXlsVen (Pubitemid 27021517)
35. A Rodolosse ML Campos I Rooman M Lichtenstein FX Reak 2009 p/CAF modulates the activity of the transcription factor p48/Ptf1a involved in pancreatic acinar differentiation Biochem J 418 463 473 18834332 10.1042/BJ20080293 1:CAS:528:DC%2BD1MXhs1Ons7w%3D
36. AP Bird AP Wolffe 1999 Methylation-induced repression-belts, braces, and chromatin Cell 99 451 454 10589672 10.1016/S0092-8674(00)81532-9 1:CAS:528:DyaK1MXnvVSis7s%3D (Pubitemid 129746827)
37. H Li T Rauch ZX Chen PE Szabo AD Riggs GP Pfeifer 2006 The histone methyltransferase SETDB1 and the DNA methyltransferase DNMT3A interact directly and localize to promoters silenced in cancer cells J Biol Chem 281 19489 19500 16682412 10.1074/jbc.M513249200 1:CAS:528:DC%2BD28Xms1GqsL8%3D (Pubitemid 44035453)
38. S Huang X Li TM Yusufzai Y Qiu G Felsenfeld 2007 USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier Mol Cell Biol 22 7991 8002 10.1128/MCB.01326-07 (Pubitemid 350086431)
39. MJ Pikaart F Recillas-Targa G Felsenfeld 1998 Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators Genes Dev 12 2852 2862 9744862 10.1101/gad.12.18.2852 1:CAS:528:DyaK1cXmtFCku7o%3D (Pubitemid 28440144)
40. J Buteau R Roduit S Susini M Prentki 1999 Glucagon-like peptide-1 promotes DNA synthesis, activates phosphatidylinositol 3-kinase and increases transcription factor pancreatic and duodenal homeobox gene 1 (PDX-1) DNA binding activity in beta (INS-1)-cells Diabetologia 42 856 864 10440129 10.1007/s001250051238 1:CAS:528:DyaK1MXktF2lsbs%3D (Pubitemid 29325077)
41. RHF Wong I Chang CSS Hudak S Hyun H Kwan HS Sul 2009 A role of DNA-PK for metabolic gene regulation in response to insulin Cell 136 1056 1072 19303849 10.1016/j.cell.2008.12.040 1:CAS:528:DC%2BD1MXltFSntrY%3D
42. MD Litt M Simpson M Gaszner CD Allis G Felsenfeld 2001 Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus Science 293 2453 2455 11498546 10.1126/science.1064413 1:CAS:528:DC%2BD3MXntlKjs7k%3D (Pubitemid 32917326)
43. K Noma SI Grewal 2002 Histone H3 lysine 4 methylation is mediated by Set1 and promotes maintenance of active chromatin states in fission yeast Proc Natl Acad Sci USA 99 16438 16445 12193658 10.1073/pnas.182436399 1:CAS:528: DC%2BD38Xps12ht7w%3D (Pubitemid 35470991)
44. L Scaglia CJ Cahill DT Finegood S Bonner-Weir 1997 Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat Endocrinology 138 1736 1741 9075738 10.1210/en.138.4.1736 1:CAS:528:DyaK2sXitVKgtb8%3D (Pubitemid 27137129)
45. S Bonner-Weir 2000 Perspective: postnatal pancreatic beta cell growth Endocrinology 141 1926 1929 10830272 10.1210/en.141.6.1926 1:CAS:528: DC%2BD3cXlt1Wnurk%3D (Pubitemid 32274338)
46. HL Kaung 1994 Growth dynamics of pancreatic islet cell populations during fetal and neonatal development of the rat Dev Dyn 200 163 175 7919502 10.1002/aja.1002000208 1:STN:280:DyaK2M%2FgtlWmug%3D%3D
47. KE Bachman BH Park I Rhee, et al. 2003 Histone modifications and silencing prior to DNA methylation of a tumor suppressor gene Cancer Cell 3 89 95 12559178 10.1016/S1535-6108(02)00234-9 1:CAS:528:DC%2BD3sXhtFamtL8%3D (Pubitemid 37443893)
48. T Kouzarides 2002 Histone methylation in transcriptional control Curr Opin Genet Dev 12 198 209 11893494 10.1016/S0959-437X(02)00287-3 1:CAS:528:DC%2BD38XhvVCnsbY%3D (Pubitemid 34219493)