Bmal1 and β-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress- induced β-cell failure in mice

Molecular and Cellular Biology

Volumn 33, Issue 11, 2013, Pages 2327-2338

  Lee, Jeongkyung ^a   Moulik, Mousumi ^b   Fang, Zhe ^a   Saha, Pradip ^a   Zou, Fang ^a   Yong Xu, ^a   Nelson, David L ^a   Ma, Ke ^c   Moore, David D ^a   Yechoor, Vijay K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE CYSTEINE LIGASE; PEROXIREDOXIN 3; PROTEIN BMAL1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; UNCOUPLING PROTEIN 2;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; LOSS OF FUNCTION MUTATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIOXIDANTS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; DIABETES MELLITUS, EXPERIMENTAL; GENE EXPRESSION REGULATION; GLUCOSE; HYPERGLYCEMIA; INSULIN; INSULIN-SECRETING CELLS; ION CHANNELS; MALE; MICE; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

MUS;

EID: 84879001061     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01421-12     Document Type: Article

References (50)

1. Kroenke CH, Spiegelman D, Manson J, Schernhammer ES, Colditz GA, Kawachi I. 2007. Work characteristics and incidence of type 2 diabetes in women. Am. J. Epidemiol. 165:175-183.
2. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. 2009. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Natl. Acad. Sci. U. S. A. 106:4453-4458.
3. Pan A, Schernhammer ES, Sun Q, Hu FB. 2011. Rotating night shift work and risk of type 2 diabetes: two prospective cohort studies in women. PLoS Med. 8:e1001141. doi:10.1371/journal.pmed.1001141.
4. Kivimaki M, Batty GD, Hublin C. 2011. Shift work as a risk factor for future type 2 diabetes: evidence, mechanisms, implications, and future research directions. PLoS Med. 8:e1001138. doi:10.1371/journal.pmed .1001138.
5. Green CB, Takahashi JS, Bass J. 2008. The meter of metabolism. Cell 134:728-742.
6. Dibner C, Schibler U, Albrecht U. 2010. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72:517-549.
7. Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U. 2007. System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol. 5:e34. doi:10.1371 /journal.pbio.0050034.
8. Damiola F, Le MN, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. 2000. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 14:2950-2961.
9. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. 2001. Entrainment of the circadian clock in the liver by feeding. Science 291:490-493.
10. Bellet MM, Sassone-Corsi P. 2010. Mammalian circadian clock and metabolism- the epigenetic link. J. Cell Sci. 123:3837-3848.
11. Rudic RD, McNamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, FitzGerald GA. 2004. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2:e377. doi:10.1371/journal.pbio.0020377.
12. Lamia KA, Storch KF, Weitz CJ. 2008. Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. U. S. A. 105:15172-15177.
13. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH, Lopez JP, Philipson LH, Bradfield CA, Crosby SD, JeBailey L, Wang X, Takahashi JS, Bass J. 2010. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466:627-631.
14. Lee J, Kim MS, Li R, Liu VY, Fu L, Moore DD, Ma K, Yechoor VK. 2011. Loss of Bmal1 leads to uncoupling and impaired glucose-stimulated insulin secretion in beta cells. Islets 3:381-388.
15. Sadacca LA, Lamia KA, Delemos AS, Blum B, Weitz CJ. 2011. An intrinsic circadian clock of the pancreas is required for normal insulin release and glucose homeostasis in mice. Diabetologia 54:120-124.
16. Yechoor V, Liu V, Espiritu C, Paul A, Oka K, Kojima H, Chan L. 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.
17. Vandesompele J, De PK, Pattyn F, Poppe B, Van RN, De PA, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034.
18. Balsalobre A, Damiola F, Schibler U. 1998. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929-937.
19. Carlsson C, Borg LA, Welsh N. 1999. Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140:3422-3428.
20. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ. 2007. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130:730-741.
21. Wicksteed B, Brissova M, Yan W, Opland DM, Plank JL, Reinert RB, Dickson LM, Tamarina NA, Philipson LH, Shostak A, Bernal-Mizrachi E, Elghazi L, Roe MW, Labosky PA, Myers MG, Jr, Gannon M, Powers AC, Dempsey PJ. 2010. Conditional gene targeting in mouse pancreatic ss cells: analysis of ectopic Cre transgene expression in the brain. Diabetes 59:3090-3098.
22. Zhang CY, Parton LE, Ye CP, Krauss S, Shen R, Lin CT, Porco JA, Jr, Lowell BB. 2006. Genipin inhibits UCP2-mediated proton leak and acutely reverses obesity-and high glucose-induced beta cell dysfunction in isolated pancreatic islets. Cell Metab. 3:417-427.
23. Li LX, Skorpen F, Egeberg K, Jorgensen IH, Grill V. 2001. Uncoupling protein-2 participates in cellular defense against oxidative stress in clonal beta cells. Biochem. Biophys. Res. Commun. 282:273-277.
24. Pi J, Collins S. 2010. Reactive oxygen species and uncoupling protein 2 in pancreatic beta-cell function. Diabetes Obes. Metab. 12(Suppl. 2):141-148.
25. Mailloux RJ, Harper ME. 2011. Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic. Biol. Med. 51:1106-1115.
26. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP. 2006. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20:1868-1873.
27. Asher G, Schibler U. 2011. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 13:125-137.
28. Allaman-Pillet N, Roduit R, Oberson A, Abdelli S, Ruiz J, Beckmann JS, Schorderet DF, Bonny C. 2004. Circadian regulation of islet genes involved in insulin production and secretion. Mol. Cell. Endocrinol. 226: 59-66.
29. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA. 2000. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103:1009-1017.
30. Kawai K, Yokota C, Ohashi S, Watanabe Y, Yamashita K. 1995. Evidence that glucagon stimulates insulin secretion through its own receptor in rats. Diabetologia 38:274-276.
31. Daunt M, Dale O, Smith PA. 2006. Somatostatin inhibits oxidative respiration in pancreatic beta cells. Endocrinology 147:1527-1535.
32. Atiya AW, Moldovan S, Adrian TE, Coy D, Walsh J, Brunicardi FC. 1997. Intraislet somatostatin inhibits insulin (via a subtype-2 somatostatin receptor) but not islet amyloid polypeptide secretion in the isolated perfused human pancreas. J. Gastrointest. Surg. 1:251-256.
33. Chan CB, Kashemsant N. 2006. Regulation of insulin secretion by uncoupling protein. Biochem. Soc. Trans. 34:802-805.
34. Poitout V, Robertson RP. 2008. Glucolipotoxicity: fuel excess and betacell dysfunction. Endocr. Rev. 29:351-366.
35. Chan CB, MacDonald PE, Saleh MC, Johns DC, Marban E, WheelerMB. 1999. Overexpression of uncoupling protein 2 inhibits glucosestimulated insulin secretion from rat islets. Diabetes 48:1482-1486.
36. Chan CB, De LD, Joseph JW, McQuaid TS, Ha XF, Xu F, Tsushima RG, Pennefather PS, Salapatek AM, Wheeler MB. 2001. Increased uncoupling protein-2 levels in beta cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes 50:1302-1310.
37. Joseph JW, Koshkin V, Saleh MC, Sivitz WI, Zhang CY, Lowell BB, Chan CB, Wheeler MB. 2004. Free fatty acid-induced beta-cell defects are dependent on uncoupling protein 2 expression. J. Biol. Chem. 279:51049-51056.
38. Joseph JW, Koshkin V, Zhang CY, Wang J, Lowell BB, Chan CB, Wheeler MB. 2002. Uncoupling protein 2 knockout mice have enhanced insulin secretory capacity after a high-fat diet. Diabetes 51:3211-3219.
39. Zhang CY, Baffy G, Perret P, Krauss S, Peroni O, Grujic D, Hagen T, Vidal-Puig AJ, Boss O, Kim YB, Zheng XX, Wheeler MB, Shulman GI, Chan CB, Lowell BB. 2001. Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105:745-755.
40. Acharya JD, Ghaskadbi SS. 2010. Islets and their antioxidant defense. Islets 2:225-235.
41. Robertson RP. 2006. Oxidative stress and impaired insulin secretion in type 2 diabetes. Curr. Opin. Pharmacol. 6:615-619.
42. Kaneto H, Kawamori D, Matsuoka TA, Kajimoto Y, Yamasaki Y. 2005. Oxidative stress and pancreatic beta-cell dysfunction. Am. J. Ther. 12: 529-533.
43. Lenzen S, Drinkgern J, Tiedge M. 1996. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic. Biol. Med. 20:463-466.
44. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB. 2002. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307-320.
45. Xu YQ, Zhang D, Jin T, Cai DJ, Wu Q, Lu Y, Liu J, Klaassen CD. 2012. Diurnal variation of hepatic antioxidant gene expression in mice. PLoS One 7:e44237. doi:10.1371/journal.pone.0044237.
46. Wolf G, Aumann N, Michalska M, Bast A, Sonnemann J, Beck JF, Lendeckel U, Newsholme P, Walther R. 2010. Peroxiredoxin III protects pancreatic ss cells from apoptosis. J. Endocrinol. 207:163-175.
47. Tran PO, Parker SM, LeRoy E, Franklin CC, Kavanagh TJ, Zhang T, Zhou H, Vliet P, Oseid E, Harmon JS, Robertson RP. 2004. Adenoviral overexpression of the glutamylcysteine ligase catalytic subunit protects pancreatic islets against oxidative stress. J. Biol. Chem. 279: 53988-53993.
48. Kondratov RV, Vykhovanets O, Kondratova AA, Antoch MP. 2009. Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging (Albany NY) 1:979-987.
49. Buxton OM, Cain SW, O'Connor SP, Porter JH, Duffy JF, Wang W, Czeisler CA, Shea SA. 2012. Adverse metabolic consequences in humans of prolonged sleep restriction combined with circadian disruption. Sci. Transl. Med. 4:129ra43.
50. Gale JE, Cox HI, Qian J, Block GD, Colwell CS, Matveyenko AV. 2011. Disruption of circadian rhythms accelerates development of diabetes through pancreatic beta-cell loss and dysfunction. J. Biol. Rhythms 26: 423-433.