Hepatic circadian-clock system altered by insulin resistance, diabetes and insulin sensitizer in mice

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Tseng, Huey Ling ^a   Yang, Shu Chuan ^b   Yang, Shih Hsien ^a,c   Shieh, Kun Ruey ^a  

^a TZU CHI UNIVERSITY   (Taiwan)

^b TZU CHI COLLEGE OF TECHNOLOGY   (Taiwan)

^c BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME 1; GLUCOSE; INSULIN; INSULIN SENSITIZING AGENT; MESSENGER RNA; PER2 PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN BMAL1; ROSIGLITAZONE; STREPTOZOCIN; 2,4 THIAZOLIDINEDIONE DERIVATIVE; GLUCOSE BLOOD LEVEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE SEVERITY; ENERGY METABOLISM; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE TEST; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; LIVER; LOW DRUG DOSE; MALE; MOUSE; NEWBORN; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; BLOOD; BODY WEIGHT; C57BL MOUSE; DIET RESTRICTION; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY;

MUS;

ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CIRCADIAN CLOCKS; DIABETES MELLITUS, EXPERIMENTAL; FASTING; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE TOLERANCE TEST; INSULIN; INSULIN RESISTANCE; LIVER; MALE; MICE; MICE, INBRED C57BL; PREGNANCY; THIAZOLIDINEDIONES;

EID: 84925873106     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120380     Document Type: Article

References (61)

1. Tsatsoulis A, Mantzaris MD, Bellou S, Andrikoula M. Insulin resistance: an adaptive mechanism becomes maladaptive in the current environment-an evolutionary perspective. Metabolism. 2013; 62: 622-633. doi: 10.1016/j.metabol.2012.11.004 PMID: 23260798
2. Bugianesi E, McCullough AJ, Marchesini G. Insulin resistance: a metabolic pathway to chronic liver disease. Hepatology. 2005; 42: 987-1000. PMID: 16250043
3. Das S, Bhoi SK, Baliarsinha AK, Baig MA. Autoimmunity, insulin resistance and Beta cell function in subjects with low body weight type 2 diabetes mellitus. Metab Syndr Relat Disord. 2007; 5:136-141. doi: 10.1089/met.2006.0024 PMID: 18370822
4. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, et al. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell. 2000; 6: 87-97. PMID: 10949030
5. Lauro D, Kido Y, Castle AL, Zarnowski MJ, Hayashi H, Ebina Y, et al. Impaired glucose tolerance in mice with a targeted impairment of insulin action in muscle and adipose tissue. Nat Genet. 1998; 20: 294-298. PMID: 9806552
6. Green CB, Takahashi JS, Bass J. The meter of metabolism. Cell. 2008; 134: 728-742. doi: 10.1016/j.cell.2008.08.022 PMID: 18775307
7. Ramsey KM, Marcheva B, Kohsaka A, Bass J. The clockwork of metabolism. Annu Rev Nutr. 2007; 27: 219-240. PMID: 17430084
8. Zhang EE, Liu Y, Dentin R, Pongsawakul PY, Liu AC, Hirota T, et al. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat Med. 2010; 16:1152-1156. doi: 10.1038/nm.2214 PMID: 20852621
9. Bass J, Takahashi JS. Circadian integration of metabolism and energetics. Science. 2010; 330:1349-1354. doi: 10.1126/science.1195027 PMID: 21127246
10. Dunlap JC. Molecular bases for circadian clocks. Cell. 1999; 96: 271-290. PMID: 9988221
11. Hsieh MC, Yang SC, Tseng HL, Hwang LL, Chen CT, Shieh KR. Abnormal expressions of circadian-clock and circadian clock-controlled genes in the livers and kidneys of long-term, high-fat-diet-treated mice. Int J Obes. 2010; 34: 227-239. doi: 10.1038/ijo.2009.228 PMID: 19901953
12. Oishi K, Sakamoto K, Okada T, Nagase T, Ishida N. Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats. Biochem Biophys Res Commun. 1998; 253:199-203. PMID: 9878515
13. Shieh KR, Yang SC, Lu XY, Akil H, Watson SJ. Diurnal rhythmic expression of the rhythm-related genes, rPeriod1, rPeriod2, and rClock, in the rat brain. J BiomedSci. 2005; 12: 209-217. PMID: 15864751
14. Lamia KA, Storch KF, Weitz CJ. Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA. 2008; 105:15172-15177. doi: 10.1073/pnas.0806717105 PMID: 18779586
15. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature. 2010; 466: 627-631. doi: 10.1038/nature09253 PMID: 20562852
16. Rudic RD, McNamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, et al. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biology. 2004; 2: e377. PMID: 15523558
17. Wu P, Peters JM, Harris RA. Adaptive increase in pyruvate dehydrogenase kinase 4 during starvation is mediated by peroxisome proliferator-activated receptor alpha. Biochem Biophys Res Commun. 2001; 287: 391-396. PMID: 11554740
18. Gavrilova O, Haluzik M, Matsusue K, Cutson JJ, Johnson L, Dietz KR, et al. Liver peroxisome proliferator-activated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J Biol Chem. 2003; 278: 34268-34276. PMID: 12805374
19. Attia RR, Connnaughton S, Boone LR, Wang F, Elam MB, Ness GC, et al. Regulation of pyruvate dehydrogenase kinase 4 (PDK4) by thyroid hormone: role of the peroxisome proliferator-activated receptor gamma coactivator (PGC-1 alpha). J Biol Chem. 2010; 285: 2375-2385. doi: 10.1074/jbc.M109.039081 PMID: 19948729
20. Oishi K, Uchida D, Itoh N. Low-carbohydrate, high-protein diet affects rhythmic expression of gluconeogenic regulatory and circadian clock genes in mouse peripheral tissues. Chronobiol Int. 2012; 29: 799-809. doi: 10.3109/07420528.2012.699127 PMID: 22823864
21. Yang SC, Tseng HL, Shieh KR. Circadian-clock system in mouse liver affected by insulin resistance. Chronobiol Int. 2013; 30: 796-810. doi: 10.3109/07420528.2013.766204 PMID: 23738904
22. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005; 1: 361-370. PMID: 16054085
23. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science. 2005; 308:1043-1045. PMID: 15845877
24. Candela S, Hernandez RE, Gagliardino JJ. Circadian variation of the streptozotocin-diabetogenic effect in mice. Experientia. 1979; 35:1256-1257. PMID: 158539
25. Nelson W, Tong YL, Lee JK, Halberg F. Methods for cosinor-rhythmometry. Chronobiologia. 1979; 6: 305-323. PMID: 548245
26. La Fleur SE, Kalsbeek A, Wortel J, Buijs RM. A suprachiasmatic nucleus generated rhythm in basal glucose concentrations. J Neuroendocrinol. 1999; 11: 643-652. PMID: 10447803
27. Ruiter M, La Fleur SE, van Heijningen C, van der Vliet J, Kalsbeek A, Buijs RM. The daily rhythm in plasma glucagon concentrations in the rat is modulated by the biological clock and by feeding behavior. Diabetes. 2003; 52:1709-1715. PMID: 12829637
28. De Boer SF, Van derGugten J. Daily variations in plasma noradrenaline, adrenaline and corticosterone concentrations in rats. Physiol Behav. 1987; 40: 323-328. PMID: 3659148
29. Bodosi B, Gardi J, Hajdu I, Szentirmai E, Obal F Jr., Krueger JM. Rhythms of ghrelin, leptin, and sleep in rats: effects of the normal diurnal cycle, restricted feeding, and sleep deprivation. Am J Physiol Regul IntegrComp Physiol. 2004; 287: R1071-1079. PMID: 15475503
30. Froy O. Metabolism and circadian rhythms-implications for obesity. Endocr Rev. 2010; 31:1-24. doi: 10.1210/er.2009-0014 PMID: 19854863
31. Bunger MK, Walisser JA, Sullivan R, Manley PA, Moran SM, Kalscheur VL, et al. Progressive arthropathy in mice with a targeted disruption of the Mop3/Bmal-1 locus. Genesis. 2005; 41:122-132. PMID: 15739187
32. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 2006; 20:1868-1873. PMID: 16847346
33. Kohsaka A, Laposky AD, Ramsey KM, Estrada C, Joshu C, Kobayashi Y, et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 2007; 6: 414-421. PMID: 17983587
34. Gomez-Abellan P, Hernandez-Morante JJ, Lujan JA, Madrid JA, Garaulet M. Clock genes are implicated in the human metabolic syndrome. Int J Obes. 2008; 32:121-128. PMID: 17653067
35. Scott EM, Carter AM, Grant PJ. Association between polymorphisms in the Clock gene, obesity and the metabolic syndrome in man. Int J Obes. 2008; 32: 658-662. PMID: 18071340
36. Rutter J, Reick M, Wu LC, McKnight SL. Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science. 2001; 293: 510-514. PMID: 11441146
37. Diano S, Liu ZW, Jeong JK, Dietrich MO, Ruan HB, Kim E, et al. Peroxisome proliferation-associated control of reactive oxygen species sets melanocortin tone and feeding in diet-induced obesity. Nat Med. 2011; 17:1121-1127. doi: 10.1038/nm.2421 PMID: 21873987
38. Kuriyama K, Sasahara K, Kudo T, Shibata S. Daily injection of insulin attenuated impairment of liver circadian clock oscillation in the streptozotocin-treated diabetic mouse. FEBS Letters. 2004; 572: 206-210. PMID: 15304349
39. Herichova I, Zeman M, Stebelova K, Ravingerova T. Effect of streptozotocin-induced diabetes on daily expression of per2 and dbp in the heart and liver and melatonin rhythm in the pineal gland of Wistar rat. Mol Cell Biochem. 2005; 270: 223-229. PMID: 15792371
40. Hofmann K, Schonerstedt U, Muhlbauer E, Wedekind D, Peschke E. Clock gene expression in the liver of streptozotocin-induced and spontaneous type 1 diabetic rats. Horm Metab Res. 2013; 45: 629-639. doi: 10.1055/s-0033-1343462 PMID: 23632905
41. Lahouaoui H, Coutanson C, Cooper HM, Bennis M, Dkhissi-Benyahya O. Clock genes and behavioral responses to light are altered in a mouse model of diabetic retinopathy. PLoS One. 2014; 9: e101584. doi: 10.1371/journal.pone.0101584 PMID: 25006976
42. Bonner-Weir S, Trent DF, Honey RN, Weir GC. Responses of neonatal rat islets to streptozotocin: limited B-cell regeneration and hyperglycemia. Diabetes. 1981; 30: 64-69. PMID: 6112177
43. Kataoka M, Kawamuro Y, Shiraki N, Miki R, Sakano D, Yoshida T, et al. Recovery from diabetes in neonatal mice after a low-dose streptozotocin treatment. Biochem Biophys Res Commun. 2013; 430: 1103-1108. doi: 10.1016/j.bbrc.2012.12.030 PMID: 23257160
44. Burcelin R. Leptin and resistin: master enemy adipokines unified in brain to control glucose homeostasis. Endocrinology. 2008; 149: 443-444. doi: 10.1210/en.2007-1507 PMID: 18209210
45. Pittas AG, Joseph NA, Greenberg AS. Adipocytokines and insulin resistance. J Clin Endocrinol Metab. 2004; 89: 447-452. PMID: 14764746
46. Yang G, Jia Z, Aoyagi T, McClain D, Mortensen RM, Yang T. Systemic PPARgamma deletion impairs circadian rhythms of behavior and metabolism. PLoS One. 2012; 7: e38117. doi: 10.1371/journal.pone.0038117 PMID: 22899986
47. Herzig S, Hedrick S, Morantte I, Koo SH, Galimi F, Montminy M. CREB controls hepatic lipid metabolism through nuclear hormone receptor PPAR-gamma. Nature. 2003; 426:190-193. PMID: 14614508
48. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, et al. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature. 2001; 413:179-183. PMID: 11557984
49. Yang SJ, Choi JM, Chae SW, Kim WJ, Park SE, Rhee EJ, et al. Activation of peroxisome proliferator-activated receptor gamma by rosiglitazone increases sirt6 expression and ameliorates hepatic steatosis in rats. PLoS One. 2011; 6: e17057. doi: 10.1371/journal.pone.0017057 PMID: 21373642
50. Eckel-Mahan KL, Patel VR, de Mateo S, Orozco-Solis R, Ceglia NJ, Sahar S, et al. Reprogramming of the circadian clock by nutritional challenge. Cell. 2013; 155:1464-1478. doi: 10.1016/j.cell.2013.11.034 PMID: 24360271
51. Canaple L, Rambaud J, Dkhissi-Benyahya O, Rayet B, Tan NS, Michalik L, et al. Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferator-activated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock. Mol Endocrinol. 2006; 20:1715-1727. PMID: 16556735
52. Oishi K, Kasamatsu M, Ishida N. Gene-and tissue-specific alterations of circadian clock gene expression in streptozotocin-induced diabetic mice under restricted feeding. Biochem Biophys Res Commun. 2004; 317: 330-334. PMID: 15063761
53. Vu-Dac N, Chopin-Delannoy S, Gervois P, Bonnelye E, Martin G, Fruchart JC, et al. The nuclear receptors peroxisome proliferator-activated receptor alpha and Rev-erbalpha mediate the species-specific regulation of apolipoprotein A-I expression by fibrates. J Biol Chem. 1998; 273: 25713-25720. PMID: 9748239
54. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, et al. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 2002; 109: 307-320. PMID: 12015981
55. Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, et al. A transcription factor response element forgene expression during circadian night. Nature. 2002; 418: 534-539. PMID: 12152080
56. Lemberger T, Saladin R, Vazquez M, Assimacopoulos F, Staels B, Desvergne B, et al. Expression of the peroxisome proliferator-activated receptor alpha gene is stimulated by stress and follows a diurnal rhythm. J Biol Chem. 1996; 271:1764-1769. PMID: 8576180
57. Jin J, Albertz J, Guo Z, Peng Q, Rudow G, Troncoso JC, et al. Neuroprotective effects of PPAR-gamma agonist rosiglitazone in N171-82Q mouse model of Huntington's disease. J Neurochem. 2013; 125: 410-419. doi: 10.1111/jnc.12190 PMID: 23373812
58. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000; 14: 2950-2961. PMID: 11114885
59. 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. doi: 10.1016/j.celrep.2014.06.015 PMID: 25017062
60. Yamajuku D, Inagaki T, Haruma T, Okubo S, Kataoka Y, Kobayashi S, et al. Real-time monitoring in three-dimensional hepatocytes reveals that insulin acts as a synchronizer for liver clock. Sci Rep. 2012; 2: 439. doi: 10.1038/srep00439 PMID: 22666542
61. Coomans CP, vanden Berg SA, Lucassen EA, Houben T, Pronk AC, van der Spek RD, et al. The suprachiasmatic nucleus controls circadian energy metabolism and hepatic insulin sensitivity. Diabetes. 2013; 62:1102-1108. doi: 10.2337/db12-0507 PMID: 23274903