A functional circadian clock is required for proper insulin secretion by human pancreatic islet cells

Diabetes, Obesity and Metabolism

Volumn 18, Issue 4, 2016, Pages 355-365

  Saini, C ^a,b   Petrenko, V ^a,b   Pulimeno, P ^a,c   Giovannoni, L ^a   Berney, T ^d   Hebrok, M ^c   Howald, C ^b,e,f   Dermitzakis, E T ^b,e,f   Dibner, C ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Institute of Genetics and Genomics in Geneva (IGE3)   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^f SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

Circadian bioluminescence; Circadian clock; Human pancreatic islet; Insulin secretion; RNA sequencing

Indexed keywords

GLUCOSE; INSULIN; REGULATOR PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ATP1A1 PROTEIN, HUMAN; CATION TRANSPORT PROTEIN; CELLUBREVIN; CLOCK PROTEIN, HUMAN; FORSKOLIN; GNAQ PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; SLC30A8 PROTEIN, HUMAN; STX6 PROTEIN, HUMAN; SYNTAXIN; VAMP3 PROTEIN, HUMAN;

ARTICLE; ATP1A1 GENE; ATP5G2 GENE; BIOLUMINESCENCE; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GNAQ GENE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; INSULIN RELEASE; KCNJ11 GENE; MONITORING; PANCREAS ISLET CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA SEQUENCE; SLC30A8 GENE; STX6 GENE; VAMP3 GENE; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HYPERGLYCEMIA; METABOLISM; PANCREAS ISLET; PANCREAS ISLET BETA CELL; REPORTER GENE; RNA INTERFERENCE; SECRETION (PROCESS);

CATION TRANSPORT PROTEINS; CELLS, CULTURED; CIRCADIAN CLOCKS; CLOCK PROTEINS; COLFORSIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, REPORTER; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; HYPERGLYCEMIA; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; QA-SNARE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SODIUM-POTASSIUM-EXCHANGING ATPASE; VESICLE-ASSOCIATED MEMBRANE PROTEIN 3;

EID: 84960130296     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12616     Document Type: Article

References (50)

1. Partch CL, Green CB, Takahashi JS. Molecular architecture of the mammalian circadian clock. Trends Cell Biol 2014; 24: 90-99.
2. Dibner C, Schibler U. Circadian timing of metabolism in animal models and humans. J Intern Med 2015; 277: 513-527.
3. Marcheva B, Ramsey KM, Peek CB, Affinati A, Maury E, Bass J. Circadian clocks and metabolism. Handb Exp Pharmacol 2013; 217: 127-155.
4. Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 2010; 72: 517-549.
5. Dallmann R, Viola AU, Tarokh L, Cajochen C, Brown SA. The human circadian metabolome. Proc Natl Acad Sci U S A 2012; 109: 2625-2629.
6. Adamovich Y, Rousso-Noori L, Zwighaft Z et al. Circadian clocks and feeding time regulate the oscillations and levels of hepatic triglycerides. Cell Metab 2014; 19: 319-330.
7. Marcheva B, Ramsey KM, Buhr ED et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 2010; 466: 627-631.
8. Turek FW, Joshu C, Kohsaka A et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005; 308: 1043-1045.
9. Muhlbauer E, Wolgast S, Finckh U, Peschke D, Peschke E. Indication of circadian oscillations in the rat pancreas. FEBS Lett 2004; 564: 91-96.
10. Qian J, Block GD, Colwell CS, Matveyenko AV. Consequences of exposure to light at night on the pancreatic islet circadian clock and function in rats. Diabetes 2013; 62: 3469-3478.
11. Stamenkovic JA, Olsson AH, Nagorny CL et al. Regulation of core clock genes in human islets. Metabolism 2012; 61: 978-985.
12. Pulimeno P, Mannic T, Sage D et al. Autonomous and self-sustained circadian oscillators displayed in human islet cells. Diabetologia 2013; 56: 497-507.
13. Parnaud G, Bosco D, Berney T et al. Proliferation of sorted human and rat beta cells. Diabetologia 2008; 51: 91-100.
14. Liu AC, Tran HG, Zhang EE, Priest AA, Welsh DK, Kay SA. Redundant function of REV-ERBalpha and beta and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet 2008; 4: e1000023.
15. Saini C, Morf J, Stratmann M, Gos P, Schibler U. Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators. Genes Dev 2012; 26: 567-580.
16. Paget MB, Murray HE, Bailey CJ, Flatt PR, Downing R. Rotational co-culture of clonal beta-cells with endothelial cells: effect of PPAR-gamma agonism in vitro on insulin and VEGF secretion. Diabetes Obes Metab 2011; 13: 662-668.
17. Perrin L, Loizides-Mangold U, Skarupelova S et al. Human skeletal myotubes display a cell-autonomous circadian clock implicated in basal myokine secretion. Mol Metab 2015; 4: 834-845.
18. Hughes ME, Hogenesch JB, Kornacker K. JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 2010; 25: 372-380.
19. Lappalainen T, Sammeth M, Friedlander MR et al. Transcriptome and genome sequencing uncovers functional variation in humans. Nature 2013; 501: 506-511.
20. Mele M, Ferreira PG, Reverter F et al. Human genomics. The human transcriptome across tissues and individuals. Science 2015; 348: 660-665.
21. Cho H, Zhao X, Hatori M et al. Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 2012; 485: 123-127.
22. Takeda Y, Jothi R, Birault V, Jetten AM. RORgamma directly regulates the circadian expression of clock genes and downstream targets in vivo. Nucleic Acids Res 2012; 40: 8519-8535.
23. Honma S, Kawamoto T, Takagi Y et al. Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 2002; 419: 841-844.
24. Wuarin J, Schibler U. Expression of the liver-enriched transcriptional activator protein DBP follows a stringent circadian rhythm. Cell 1990; 63: 1257-1266.
25. Lee J, Kim MS, Li R et al. Loss of Bmal1 leads to uncoupling and impaired glucose-stimulated insulin secretion in beta-cells. Islets 2011; 3: 381-388.
26. Cerf ME. Transcription factors regulating beta-cell function. Eur J Endocrinol 2006; 155: 671-679.
27. Marcheva B, Ramsey KM, Bass J. Circadian genes and insulin exocytosis. Cell Logist 2011; 1: 32-36.
28. Sato M, Murakami M, Node K, Matsumura R, Akashi M. The role of the endocrine system in feeding-induced tissue-specific circadian entrainment. Cell Rep 2014; 8: 393-401.
29. Brown SA, Kunz D, Dumas A et al. Molecular insights into human daily behavior. Proc Natl Acad Sci U S A 2008; 105: 1602-1607.
30. Mannic T, Meyer P, Triponez F et al. Circadian clock characteristics are altered in human thyroid malignant nodules. J Clin Endocrinol Metab 2013; 98: 4446-4456.
31. Saini C, Brown SA, Dibner C. Human peripheral clocks: applications for studying circadian phenotypes in physiology and pathophysiology. Front Neurol 2015; 6: 95.
32. Akashi M, Soma H, Yamamoto T et al. Noninvasive method for assessing the human circadian clock using hair follicle cells. Proc Natl Acad Sci U S A 2010; 107: 15643-15648.
33. Chua EC, Shui G, Lee IT et al. Extensive diversity in circadian regulation of plasma lipids and evidence for different circadian metabolic phenotypes in humans. Proc Natl Acad Sci U S A 2013; 110: 14468-14473.
34. Gale JE, Cox HI, Qian J, Block GD, Colwell CS, Matveyenko AV. Disruption of circadian rhythms accelerates development of diabetes through pancreatic beta-cell loss and dysfunction. J Biol Rhythms 2011; 26: 423-433.
35. Qian J, Yeh B, Rakshit K, Colwell CS, Matveyenko AV. Circadian disruption and diet-induced obesity synergize to promote development of beta cell failure and diabetes in male rats. Endocrinology 2015; 156: en20151516.
36. Kalsbeek A, la Fleur S, Fliers E. Circadian control of glucose metabolism. Mol Metab 2014; 3: 372-383.
37. Perelis M, Marcheva B, Ramsey KM et al. Pancreatic beta cell enhancers regulate rhythmic transcription of genes controlling insulin secretion. Science 2015; 350: aac4250.
38. Morris CJ, Yang JN, Garcia JI et al. Endogenous circadian system and circadian misalignment impact glucose tolerance via separate mechanisms in humans. Proc Natl Acad Sci U S A 2015; 112: E2225-E2234.
39. Davidson HW, Wenzlau JM, O'Brien RM. Zinc transporter 8 (ZnT8) and beta cell function. Trends Endocrinol Metab 2014; 25: 415-424.
40. Nicolson TJ, Bellomo EA, Wijesekara N et al. Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 2009; 58: 2070-2083.
41. Kuliawat R, Kalinina E, Bock J et al. Syntaxin-6 SNARE involvement in secretory and endocytic pathways of cultured pancreatic beta-cells. Mol Biol Cell 2004; 15: 1690-1701.
42. Regazzi R, Wollheim CB, Lang J et al. VAMP-2 and cellubrevin are expressed in pancreatic beta-cells and are essential for Ca(2+)-but not for GTP gamma S-induced insulin secretion. EMBO J 1995; 14: 2723-2730.
43. Tarasov A, Dusonchet J, Ashcroft F. Metabolic regulation of the pancreatic beta-cell ATP-sensitive K+ channel: a pas de deux. Diabetes 2004; 53(Suppl. 3): S113-S122.
44. Gloyn AL, Siddiqui J, Ellard S. Mutations in the genes encoding the pancreatic beta-cell KATP channel subunits Kir6.2 (KCNJ11) and SUR1 (ABCC8) in diabetes mellitus and hyperinsulinism. Hum Mutat 2006; 27: 220-231.
45. Girard CA, Wunderlich FT, Shimomura K et al. Expression of an activating mutation in the gene encoding the KATP channel subunit Kir6.2 in mouse pancreatic beta cells recapitulates neonatal diabetes. J Clin Invest 2009; 119: 80-90.
46. Sassmann A, Gier B, Grone HJ, Drews G, Offermanns S, Wettschureck N. The Gq/G11-mediated signaling pathway is critical for autocrine potentiation of insulin secretion in mice. J Clin Invest 2010; 120: 2184-2193.
47. Balsalobre A, Brown SA, Marcacci L et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 2000; 289: 2344-2347.
48. Balsalobre A, Marcacci L, Schibler U. Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr Biol 2000; 10: 1291-1294.
49. Cnop M, Abdulkarim B, Bottu G et al. RNA sequencing identifies dysregulation of the human pancreatic islet transcriptome by the saturated fatty acid palmitate. Diabetes 2014; 63: 1978-1993.
50. Arvan P, Pietropaolo M, Ostrov D, Rhodes CJ. Islet autoantigens: structure, function, localization, and regulation. Cold Spring Harb Perspect Med 2012; 2: a007658.