Pancreatic b cell enhancers regulate rhythmic transcription of genes controlling insulin secretion

Science

Volumn 350, Issue 6261, 2015, Pages

  Perelis, Mark ^a   Marcheva, Biliana ^a   Ramsey, Kathryn Moynihan ^a   Schipma, Matthew J ^b   Hutchison, Alan L ^c,d   Taguchi, Akihiko ^a   Peek, Clara Bien ^a   Hong, Heekyung ^a   Huang, Wenyu ^a   Omura, Chiaki ^a   Allred, Amanda L ^a   Bradfield, Christopher A ^e   Dinner, Aaron R ^c,d   Barish, Grant D ^a   Bass, Joseph ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CLOCK; ARNTL PROTEIN, MOUSE; CLOCK PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; INSULIN; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR ARNTL;

CELLS AND CELL COMPONENTS; DIABETES; ENVIRONMENTAL CUE; GENE EXPRESSION; HORMONE; METABOLISM; PHYSIOLOGICAL RESPONSE; RODENT;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE CONTROL; GENETIC TRANSCRIPTION; GLUCOSE METABOLISM; INSULIN RELEASE; LIVER CELL; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ANIMAL; C57BL MOUSE; ENHANCER REGION; EXOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE INTOLERANCE; HUMAN; LIVER; MALE; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PHYSIOLOGY; SECRETION (PROCESS);

MAMMALIA; MUS;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; CLOCK PROTEINS; DIABETES MELLITUS, TYPE 2; ENHANCER ELEMENTS, GENETIC; EXOCYTOSIS; GENE EXPRESSION REGULATION; GLUCOSE INTOLERANCE; HOMEODOMAIN PROTEINS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; LIVER; MALE; MICE; MICE, INBRED C57BL; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84947437372     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aac4250     Document Type: Article

References (54)

1. N. Preitner et al., The orphan nuclear receptor REV-ERBa controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260 (2002). doi: 10.1016/S0092-8674(02)00825-5; pmid: 12150932
2. I. Zamir et al., A nuclear hormone receptor corepressor mediates transcriptional silencing by receptors with distinct repression domains. Mol. Cell. Biol. 16, 5458-5465 (1996). doi: 10.1128/MCB.16.10.5458; pmid: 8816459
3. A. Balsalobre, F. Damiola, U. Schibler, A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93, 929-937 (1998). doi: 10.1016/S0092-8674(00)81199-X; pmid: 9635423
4. F. W. Turek et al., Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308, 1043-1045 (2005). doi: 10.1126/science.1108750; pmid: 15845877
5. K. A. Lamia, K. F. Storch, C. J. Weitz, Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. U.S.A. 105, 15172-15177 (2008). doi: 10.1073/pnas.0806717105 pmid: 18779586
6. B. Marcheva et al., Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466, 627-631 (2010). doi: 10.1038/nature09253 pmid: 20562852
7. L. A. Sadacca, K. A. Lamia, A. S. deLemos, B. Blum, C. J. Weitz, An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 54, 120-124 (2011). doi: 10.1007/s00125-010-1920-8 pmid: 20890745
8. C. B. Peek et al., Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice. Science 342, 1243417 (2013). doi: 10.1126/science.1243417; pmid: 24051248
9. N. Koike et al., Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338, 349-354 (2012). doi: 10.1126/science.1226339 pmid: 22936566
10. B. Fang et al., Circadian enhancers coordinate multiple phases of rhythmic gene transcription in vivo. Cell 159, 1140-1152 (2014). doi: 10.1016/j.cell.2014.10.022; pmid: 25416951
11. J. S. Menet, J. Rodriguez, K. C. Abruzzi, M. Rosbash, Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. eLife 1, e00011 (2012). pmid: 23150795
12. S. H. Yoo et al., PERIOD2:LUCIFERASE real-Time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. U.S.A. 101, 5339-5346 (2004). pmid: 14963227
13. J. S. O'Neill, E. S. Maywood, J. E. Chesham, J. S. Takahashi, M. H. Hastings, cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320, 949-953 (2008). doi: 10.1126/science.1152506 pmid: 18487196
14. A. L. Hutchison et al., Improved statistical methods enable greater sensitivity in rhythm detection for genome-wide data. PLOS Comput. Biol. 11, e1004094 (2015). doi: 10.1371/journal. pcbi.1004094; pmid: 25793520
15. H. R. Ueda et al., System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet. 37, 187-192 (2005). doi: 10.1038/ng1504; pmid: 15665827
16. X. W. Chen et al., SEC24A deficiency lowers plasma cholesterol through reduced PCSK9 secretion. eLife 2, e00444 (2013). doi: 10.7554/eLife.00444; pmid: 23580231
17. A. J. Noble et al., A pseudoatomic model of the COPII cage obtained from cryo-electron microscopy and mass spectrometry. Nat. Struct. Mol. Biol. 20, 167-173 (2013). doi: 10.1038/nsmb.2467; pmid: 23262493
18. Z. Wang, D. C. Thurmond, Mechanisms of biphasic insulingranule exocytosis-roles of the cytoskeleton, small GTPases and SNARE proteins. J. Cell Sci. 122, 893-903 (2009). doi: 10.1242/jcs.034355; pmid: 19295123
19. Y. Liu, Y. Sugiura, W. Lin, The role of synaptobrevin1/VAMP1 in Ca2+-Triggered neurotransmitter release at the mouse neuromuscular junction. J. Physiol. 589, 1603-1618 (2011). doi: 10.1113/jphysiol.2010.201939; pmid: 21282288
20. M. Ohara-Imaizumi et al., Correlation of syntaxin-1 and SNAP-25 clusters with docking and fusion of insulin granules analysed by total internal reflection fluorescence microscopy. Diabetologia 47, 2200-2207 (2004). doi: 10.1007/s00125-004-1579-0; pmid: 15647897
21. K. Fujimoto et al., Piccolo, a Ca2+ sensor in pancreatic betacells. Involvement of cAMP-GEFII.Rim2. Piccolo complex in cAMP-dependent exocytosis. J. Biol. Chem. 277, 50497-50502 (2002). doi: 10.1074/jbc.M210146200; pmid: 12401793
22. H. Takahashi et al., Role of Epac2A/Rap1 signaling in interplay between incretin and sulfonylurea in insulin secretion. Diabetes 64, 1262-1272 (2015). pmid: 25315008
23. M. Fukuda, Molecular cloning, expression, and characterization of a novel class of synaptotagmin (Syt XIV) conserved from Drosophila to humans. J. Biochem. 133, 641-649 (2003). doi: 10.1093/jb/mvg082; pmid: 12801916
24. A. Milochau et al., Synaptotagmin 11 interacts with components of the RNA-induced silencing complex RISC in clonal pancreatic b-cells. FEBS Lett. 588, 2217-2222 (2014). pmid: 24882364
25. R. A. Easom, CaM kinase II: A protein kinase with extraordinary talents germane to insulin exocytosis. Diabetes 48, 675-684 (1999). doi: 10.2337/diabetes.48.4.675; pmid: 10102681
26. T. J. Biden et al., The diverse roles of protein kinase C in pancreatic beta-cell function. Biochem. Soc. Trans. 36, 916-919 (2008). doi: 10.1042/BST0360916; pmid: 18793161
27. X. Zhang et al., Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180, 145-158 (2008). doi: 10.1083/jcb.200704128 pmid: 18195105
28. G. Jedd, J. Mulholland, N. Segev, Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J. Cell Biol. 137, 563-580 (1997). doi: 10.1083/jcb.137.3.563; pmid: 9151665
29. P. Pulimeno et al., Autonomous and self-sustained circadian oscillators displayed in human islet cells. Diabetologia 56, 497-507 (2013). doi: 10.1007/s00125-012-2779-7; pmid: 23242133
30. C. Benner et al., The transcriptional landscape of mouse beta cells compared to human beta cells reveals notable species differences in long non-coding RNA and protein-coding gene expression. BMC Genomics 15, 620 (2014). doi: 10.1186/1471-2164-15-620; pmid: 25051960
31. L. Pasquali et al., Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-Associated variants. Nat. Genet. 46, 136-143 (2014). doi: 10.1038/ng.2870; pmid: 24413736
32. M. P. Creyghton et al., Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U.S.A. 107, 21931-21936 (2010). doi: 10.1073/pnas.1016071107; pmid: 21106759
33. H. H. He et al., Nucleosome dynamics define transcriptional enhancers. Nat. Genet. 42, 343-347 (2010). doi: 10.1038/ng.545; pmid: 20208536
34. G. Rey et al., Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLOS Biol. 9, e1000595 (2011). doi: 10.1371/journal. pbio.1000595; pmid: 21364973
35. N. D. Heintzman et al., Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39, 311-318 (2007). doi: 10.1038/ng1966; pmid: 17277777
36. S. J. Cooper, N. D. Trinklein, E. D. Anton, L. Nguyen, R. M. Myers, Comprehensive analysis of transcriptional promoter structure and function in 1% of the human genome. Genome Res. 16, 1-10 (2006). doi: 10.1101/gr.4222606 pmid: 16344566
37. P. Carninci et al., Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 38, 626-635 (2006). doi: 10.1038/ng1789; pmid: 16645617
38. C. Vollmers et al., Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab. 16, 833-845 (2012). doi: 10.1016/j.cmet.2012.11.004; pmid: 23217262
39. D. A. Stoffers, N. T. Zinkin, V. Stanojevic, W. L. Clarke, J. F. Habener, Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat. Genet. 15, 106-110 (1997). doi: 10.1038/ng0197-106; pmid: 8988180
40. B. G. Hoffman et al., Locus co-occupancy, nucleosome positioning, and H3K4me1 regulate the functionality of FOXA2-, HNF4A-, and PDX1-bound loci in islets and liver. Genome Res. 20, 1037-1051 (2010). doi: 10.1101/gr.104356.109 pmid: 20551221
41. C. Gu et al., Pancreatic beta cells require NeuroD to achieve and maintain functional maturity. Cell Metab. 11, 298-310 (2010). doi: 10.1016/j.cmet.2010.03.006; pmid: 20374962
42. L. Kang et al., Munc13-1 is required for the sustained release of insulin from pancreatic beta cells. Cell Metab. 3, 463-468 (2006). doi: 10.1016/j.cmet.2006.04.012; pmid: 16697276
43. O. Genç O. Kochubey, R. F. Toonen, M. Verhage, R. Schneggenburger, Munc18-1 is a dynamically regulated PKC target during short-Term enhancement of transmitter release. eLife 3, e01715 (2014). doi: 10.7554/eLife.01715 pmid: 24520164
44. C. J. Morris et al., Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proc. Natl. Acad. Sci. U.S.A. 112, E2225-E2234 (2015). doi: 10.1073/pnas.1418955112 pmid: 25870289
45. O. M. Buxton et al., Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci. Transl. Med. 4, 129ra43 (2012). pmid: 22496545
46. A. Bonnefond et al., Rare MTNR1B variants impairing melatonin receptor 1B function contribute to type 2 diabetes. Nat. Genet. 44, 297-301 (2012). doi: 10.1038/ng.1053; pmid: 22286214
47. B. P. Johnson et al., The hepatocyte circadian clock controls acetaminophen bioactivation through NADPH-cytochrome P450 oxidoreductase. Proc. Natl. Acad. Sci. U.S.A. 111, 18757-18762 (2014). doi: 10.1073/pnas.1421708111; pmid: 25512522
48. G. Gu, J. Dubauskaite, D. A. Melton, Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129, 2447-2457 (2002). pmid: 11973276
49. A. Dobin et al., STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013). doi: 10.1093/bioinformatics/bts635; pmid: 23104886
50. M. I. Love, W. Huber, S. Anders, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014). doi: 10.1186/s13059-014-0550-8 pmid: 25516281
51. M. Kanehisa et al., Data, information, knowledge and principle: Back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205 (2014). doi: 10.1093/nar/gkt1076; pmid: 24214961
52. H. Ogata et al., KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27, 29-34 (1999). doi: 10.1093/nar/27.1.29; pmid: 9847135
53. S. Heinz et al., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010). doi: 10.1016/j.molcel.2010.05.004; pmid: 20513432
54. B. Langmead, C. Trapnell, M. Pop, S. L. Salzberg, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009). doi: 10.1186/gb-2009-10-3-r25; pmid: 19261174