Increased Sensitivity of the Circadian System to Temporal Changes in the Feeding Regime of Spontaneously Hypertensive Rats - A Potential Role for Bmal2 in the Liver

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Polidarová, Lenka ^a   Sládek, Martin ^a   Nováková, Marta ^a   Parkanová, Daniela ^a   Sumová, Alena ^a  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BMAL1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICIPATION; ARTICLE; BMAL1 GENE; BMAL2 GENE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DIET RESTRICTION; FEEDING BEHAVIOR; FOOD ANTICIPATORY ACTIVITY; GENE; GENE EXPRESSION; LIVER; LOCOMOTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; SENSITIVITY ANALYSIS; SPONTANEOUSLY HYPERTENSIVE RAT; STRAIN DIFFERENCE; WISTAR RAT;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CLOCK PROTEINS; COLON; FEEDING BEHAVIOR; FOOD; GENE EXPRESSION; LIVER; MALE; MOTOR ACTIVITY; RATS; RATS, INBRED SHR; RATS, WISTAR;

EID: 84884554329     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075690     Document Type: Article

References (72)

1. Ralph MR, Foster RG, Davis FC, Menaker M, (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247: 975-978. doi:10.1126/science.2305266. PubMed: 2305266.
2. Drucker-Colín R, Aguilar-Roblero R, García-Hernández F, Fernández-Cancino F, Rattoni Bermudez F, (1984) Fetal suprachiasmatic nucleus transplants: diurnal rhythm recovery of lesioned rats. Brain Res 311: 353-357. doi:10.1016/0006-8993(84)90099-4. PubMed: 6541955.
3. Morin LP, Allen CN, (2006) The circadian visual system, 2005. Brain. Res Rev 51: 1-60. doi:10.1016/j.brainresrev.2005.08.003.
4. 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. doi:10.1146/annurev-physiol-021909-135821. PubMed: 20148687.
5. Takahashi JS, Hong HK, Ko CH, McDearmon EL, (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9: 764-775. doi:10.1038/nrg2430. PubMed: 18802415.
6. Ikeda M, Yu W, Hirai M, Ebisawa T, Honma S, et al. (2000) cDNA cloning of a novel bHLH-PAS transcription factor superfamily gene, BMAL2: its mRNA expression, subcellular distribution, and chromosomal localization. Biochem Biophys Res Commun 275: 493-502. doi:10.1006/bbrc.2000.3248. PubMed: 10964693.
7. Shi S, Hida A, McGuinness OP, Wasserman DH, Yamazaki S, et al. (2010) Circadian clock gene Bmal1 is not essential; functional replacement with its paralog, Bmal2. Curr Biol 20: 316-321. doi:10.1016/j.cub.2010.02.018. PubMed: 20153195.
8. Liu C, Li S, Liu T, Borjigin J, Lin JD, (2007) Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447: 477-481. doi:10.1038/nature05767. PubMed: 17476214.
9. Ohno T, Onishi Y, Ishida N, (2007) A novel E4BP4 element drives circadian expression of mPeriod2. Nucleic Acids Res 35: 648-655. PubMed: 17182630.
10. Ueda HR, Hayashi S, Chen W, Sano M, Machida M, et al. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37: 187-192. doi:10.1038/ng1504. PubMed: 15665827.
11. Masri S, Zocchi L, Katada S, Mora E, Sassone-Corsi P, (2012) The circadian clock transcriptional complex: metabolic feedback intersects with epigenetic control. Ann N Y Acad Sci 1264: 103-109. doi:10.1111/j.1749-6632.2012.06649.x. PubMed: 22834651.
12. Bozek K, Relógio A, Kielbasa SM, Heine M, Dame C, et al. (2009) Regulation of clock-controlled genes in mammals. PLOS ONE 4: e4882. doi:10.1371/journal.pone.0004882. PubMed: 19287494.
13. Challet E, Pévet P, Vivien-Roels B, Malan A, (1997) Phase-advanced daily rhythms of melatonin, body temperature, and locomotor activity in food-restricted rats fed during daytime. J Biol Rhythms 12: 65-79. doi:10.1177/074873049701200108. PubMed: 9104691.
14. Honma K, von Goetz C, Aschoff J, (1983) Effects of restricted daily feeding on freerunning circadian rhythms in rats. Physiol Behav 30: 905-913. doi:10.1016/0031-9384(83)90256-1. PubMed: 6611695.
15. Escobar C, Díaz-Muñoz M, Encinas F, Aguilar-Roblero R, (1998) Persistence of metabolic rhythmicity during fasting and its entrainment by restricted feeding schedules in rats. Am J Physiol 274: R1309-R1316. PubMed: 9644044.
16. Stephan FK, Swann JM, Sisk CL, (1979) Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behav Neural Biol 25: 346-363. doi:10.1016/S0163-1047(79)90415-1. PubMed: 464979.
17. Davidson AJ, (2009) Lesion studies targeting food-anticipatory activity. Eur J Neurosci 30: 1658-1664. doi:10.1111/j.1460-9568.2009.06961.x. PubMed: 19863659.
18. Storch KF, Weitz CJ, (2009) Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock. Proc Natl Acad Sci U S A 106: 6808-6813. doi:10.1073/pnas.0902063106. PubMed: 19366674.
19. Pendergast JS, Nakamura W, Friday RC, Hatanaka F, Takumi T, et al. (2009) Robust food anticipatory activity in BMAL1-deficient mice. PLOS ONE 4: e4860. doi:10.1371/journal.pone.0004860. PubMed: 19300505.
20. Coleman GJ, Harper S, Clarke JD, Armstrong S, (1982) Evidence for a separate meal-associated oscillator in the rat. Physiol Behav 29: 107-115. doi:10.1016/0031-9384(82)90373-0. PubMed: 7122716.
21. Bolles RC, De Lorge J, (1962) The rat's adjustment to a-diurnal feeding cycles. J Comp Physiol Psychol 55: 760-762. doi:10.1037/h0046716. PubMed: 13968622.
22. Stephan FK, (1989) Forced dissociation of activity entrained to T cycles of food access in rats with suprachiasmatic lesions. J Biol Rhythms 4: 467-479. doi:10.1177/074873048900400406. PubMed: 2519607.
23. Mistlberger RE, Marchant EG, (1995) Computational and entrainment models of circadian food-anticipatory activity: evidence from non-24-hr feeding schedules. Behav Neurosci 109: 790-798. doi:10.1037/0735-7044.109.4.790. PubMed: 7576223.
24. Takasu NN, Kurosawa G, Tokuda IT, Mochizuki A, Todo T, et al. (2012) Circadian regulation of food-anticipatory activity in molecular clock-deficient mice. PLOS ONE 7: e48892. doi:10.1371/journal.pone.0048892. PubMed: 23145013.
25. Mistlberger RE, (2009) Food-anticipatory circadian rhythms: concepts and methods. Eur J Neurosci 30: 1718-1729. doi:10.1111/j.1460-9568.2009.06965.x. PubMed: 19878279.
26. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, et al. (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14: 2950-2961. doi:10.1101/gad.183500. PubMed: 11114885.
27. 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. doi:10.1126/science.291.5503.490. PubMed: 11161204.
28. Hara R, Wan K, Wakamatsu H, Aida R, Moriya T, et al. (2001) Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells 6: 269-278. doi:10.1046/j.1365-2443.2001.00419.x. PubMed: 11260270.
29. Sládek M, Rybová M, Jindráková Z, Zemanová Z, Polidarová L, et al. (2007) Insight into the circadian clock within rat colonic epithelial cells. Gastroenterology 133: 1240-1249. doi:10.1053/j.gastro.2007.05.053. PubMed: 17675004.
30. Hoogerwerf WA, Hellmich HL, Cornélissen G, Halberg F, Shahinian VB, et al. (2007) Clock gene expression in the murine gastrointestinal tract: endogenous rhythmicity and effects of a feeding regimen. Gastroenterology 133: 1250-1260. doi:10.1053/j.gastro.2007.07.009. PubMed: 17919497.
31. Sládek M, Polidarová L, Nováková M, Parkanová D, Sumová A, (2012) Early chronotype and tissue-specific alterations of circadian clock function in spontaneously hypertensive rats. PLOS ONE 7: e46951. doi:10.1371/journal.pone.0046951. PubMed: 23056539.
32. Swislocki A, Tsuzuki A, (1993) Insulin resistance and hypertension: glucose intolerance, hyperinsulinemia, and elevated free fatty acids in the lean spontaneously hypertensive rat. Am J Med Sci 306: 282-286. doi:10.1097/00000441-199311000-00002. PubMed: 8238081.
33. Pravenec M, Kazdova L, Landa V, Zidek V, Mlejnek P, et al. (2008) Identification of mutated Srebf1 as a QTL influencing risk for hepatic steatosis in the spontaneously hypertensive rat. Hypertension 51: 148-153. doi:10.1161/HYPERTENSIONAHA.107.100743. PubMed: 18071061.
34. Woon PY, Kaisaki PJ, Bragança J, Bihoreau MT, Levy JC, et al. (2007) Aryl hydrocarbon receptor nuclear translocator-like (BMAL1) is associated with susceptibility to hypertension and type 2 diabetes. Proc Natl Acad Sci U S A 104: 14412-14417. doi:10.1073/pnas.0703247104. PubMed: 17728404.
35. Cui H, Kohsaka A, Waki H, Bhuiyan ME, Gouraud SS, et al. (2011) Metabolic cycles are linked to the cardiovascular diurnal rhythm in rats with essential hypertension. PLOS ONE 6: e17339. doi:10.1371/journal.pone.0017339. PubMed: 21364960.
36. Dolinsky VW, Morton JS, Oka T, Robillard-Frayne I, Bagdan M, et al. (2010) Calorie restriction prevents hypertension and cardiac hypertrophy in the spontaneously hypertensive rat. Hypertension 56: 412-421. doi:10.1161/HYPERTENSIONAHA.110.154732. PubMed: 20696994.
37. Sládek M, Sumová A, Kováciková Z, Bendová Z, Laurinová K, et al. (2004) Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proc Natl Acad Sci U S A 101: 6231-6236. doi:10.1073/pnas.0401149101. PubMed: 15069203.
38. Sládek M, Jindráková Z, Bendová Z, Sumová A, (2007) Postnatal ontogenesis of the circadian clock within the rat liver. Am J Physiol Regul Integr Comp Physiol 292: R1224-R1229. PubMed: 17095653.
39. Nagai K, Nishio T, Nakagawa H, Nakamura S, Fukuda Y, (1978) Effect of Bilateral Lesions of Suprachiasmatic Nuclei on Circadian-Rhythm of Food-Intake. Brain Res 142: 384-389. doi:10.1016/0006-8993(78)90648-0. PubMed: 630395.
40. Carneiro BS, Araujo JF, (2012) Food entrainment: major and recent findings. Front Behav Neuroscience 6.
41. Silver R, Balsam P, (2010) Oscillators entrained by food and the emergence of anticipatory timing behaviors. Sleep Biol Rhythms 8: 120-136. doi:10.1111/j.1479-8425.2010.00438.x. PubMed: 21544255.
42. Li ZF, Guo ZF, Cao J, Hu JQ, Zhao XX, et al. (2010) Plasma ghrelin and obestatin levels are increased in spontaneously hypertensive rats. Peptides 31: 297-300. doi:10.1016/j.peptides.2009.11.018. PubMed: 19944125.
43. Lee YH, Dai YW, Huang SC, Li TL, Hwang LL, (2013) Blockade of Central Orexin 2 Receptors Reduces Arterial Pressure in Spontaneously Hypertensive Rats. Exp Physiol, 98: 1145-55. PubMed: 23525245.
44. Sasaki M, Yoshitane H, Du NH, Okano T, Fukada Y, (2009) Preferential inhibition of BMAL2-CLOCK activity by PER2 reemphasizes its negative role and a positive role of BMAL2 in the circadian transcription. J Biol Chem 284: 25149-25159. doi:10.1074/jbc.M109.040758. PubMed: 19605937.
45. Dardente H, Fortier EE, Martineau V, Cermakian N, (2007) Cryptochromes impair phosphorylation of transcriptional activators in the clock: a general mechanism for circadian repression. Biochem J 402: 525-536. doi:10.1042/BJ20060827. PubMed: 17115977.
46. Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, et al. (2000) Interacting molecular loops in the mammalian circadian clock. Science 288: 1013-1019. doi:10.1126/science.288.5468.1013. PubMed: 10807566.
47. Shi SQ, Ansari TS, McGuinness OP, Wasserman DH, Johnson CH, (2013) Circadian disruption leads to insulin resistance and obesity. Curr Biol 23: 372-381. doi:10.1016/j.cub.2013.01.048. PubMed: 23434278.
48. Hung MS, Avner P, Rogner UC, (2006) Identification of the transcription factor ARNTL2 as a candidate gene for the type 1 diabetes locus Idd6. Hum Mol Genet 15: 2732-2742. doi:10.1093/hmg/ddl209. PubMed: 16893914.
49. Schoenhard JA, Eren M, Johnson CA, Vaughan DE, (2002) Alternative splicing yields novel BMAL2 variants: tissue distribution and functional characterization. Am J Physiol Cell Physiol 283: C103-C114. doi:10.1152/ajpcell.00541.2001. PubMed: 12055078.
50. Maemura K, de la Monte SM, Chin MT, Layne MD, Hsieh CM, et al. (2000) CLIF, a novel cycle-like factor, regulates the circadian oscillation of plasminogen activator inhibitor-1 gene expression. J Biol Chem 275: 36847-36851. doi:10.1074/jbc.C000629200. PubMed: 11018023.
51. Alessi MC, Juhan-Vague I, (2006) PAI-1 and the metabolic syndrome: links, causes, and consequences. Arterioscler Thromb Vasc Biol 26: 2200-2207. doi:10.1161/01.ATV.0000242905.41404.68. PubMed: 16931789.
52. Svoboda DS, Kawaja MD, (2012) Changes in hepatic protein expression in spontaneously hypertensive rats suggest early stages of non-alcoholic fatty liver disease. J Proteomics 75: 1752-1763. doi:10.1016/j.jprot.2011.12.011. PubMed: 22240297.
53. Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, et al. (2003) Control mechanism of the circadian clock for timing of cell division in vivo. Science 302: 255-259. doi:10.1126/science.1086271. PubMed: 12934012.
54. Ripperger JA, Schibler U, (2006) Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat Genet 38: 369-374. doi:10.1038/ng1738. PubMed: 16474407.
55. Gachon F, Olela FF, Schaad O, Descombes P, Schibler U, (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4: 25-36. doi:10.1016/j.cmet.2006.04.015. PubMed: 16814730.
56. Murakami Y, Higashi Y, Matsunaga N, Koyanagi S, Ohdo S, (2008) Circadian clock-controlled intestinal expression of the multidrug-resistance gene mdr1a in mice. Gastroenterology 135: 1636-1644. doi:10.1053/j.gastro.2008.07.073. PubMed: 18773899.
57. Tong X, Muchnik M, Chen Z, Patel M, Wu N, et al. (2010) Transcriptional repressor E4-binding protein 4 (E4BP4) regulates metabolic hormone fibroblast growth factor 21 (FGF21) during circadian cycles and feeding. J Biol Chem 285: 36401-36409. doi:10.1074/jbc.M110.172866. PubMed: 20851878.
58. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, et al. (2009) Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324: 651-654. doi:10.1126/science.1171641. PubMed: 19299583.
59. Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P, (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324: 654-657. doi:10.1126/science.1170803. PubMed: 19286518.
60. Lamia KA, Sachdeva UM, DiTacchio L, Williams EC, Alvarez JG, et al. (2009) AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 326: 437-440. doi:10.1126/science.1172156. PubMed: 19833968.
61. Gachon F, Leuenberger N, Claudel T, Gos P, Jouffe C, et al. (2011) Proline- and acidic amino acid-rich basic leucine zipper proteins modulate peroxisome proliferator-activated receptor alpha (PPARalpha) activity. Proc Natl Acad Sci U S A 108: 4794-4799. doi:10.1073/pnas.1002862108. PubMed: 21383142.
62. Kawai M, Green CB, Lecka-Czernik B, Douris N, Gilbert MR, et al. (2010) A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-gamma nuclear translocation. Proc Natl Acad Sci U S A 107: 10508-10513. doi:10.1073/pnas.1000788107. PubMed: 20498072.
63. Kawai M, Rosen CJ, (2010) PPARgamma: a circadian transcription factor in adipogenesis and osteogenesis. Nat Rev Endocrinol 6: 629-636. doi:10.1038/nrendo.2010.155. PubMed: 20820194.
64. Alenghat T, Meyers K, Mullican SE, Leitner K, Adeniji-Adele A, et al. (2008) Nuclear receptor corepressor and histone deacetylase 3 govern circadian metabolic physiology. Nature 456: 997-1000. doi:10.1038/nature07541. PubMed: 19037247.
65. Feng D, Liu T, Sun Z, Bugge A, Mullican SE, et al. (2011) A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 331: 1315-1319. doi:10.1126/science.1198125. PubMed: 21393543.
66. Denko NC, (2008) Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 8: 705-713. doi:10.1038/nrc2468. PubMed: 19143055.
67. Lee HM, Chen R, Kim H, Etchegaray JP, Weaver DR, et al. (2011) The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc Natl Acad Sci U S A 108: 16451-16456. doi:10.1073/pnas.1107178108. PubMed: 21930935.
68. Schmutz I, Wendt S, Schnell A, Kramer A, Mansuy IM, et al. (2011) Protein phosphatase 1 (PP1) is a post-translational regulator of the mammalian circadian clock. PLOS ONE 6: e21325. doi:10.1371/journal.pone.0021325. PubMed: 21712997.
69. Reddy AB, Maywood ES, Karp NA, King VM, Inoue Y, et al. (2007) Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45: 1478-1488. doi:10.1002/hep.21571. PubMed: 17538967.
70. Le Minh N, Damiola F, Tronche F, Schütz G, Schibler U, (2001) Glucocorticoid hormones inhibit food-induced phase-shifting of peripheral circadian oscillators. EMBO J 20: 7128-7136. doi:10.1093/emboj/20.24.7128. PubMed: 11742989.
71. Imaki T, Naruse M, Harada S, Chikada N, Nakajima K, et al. (1998) Stress-induced changes of gene expression in the paraventricular nucleus are enhanced in spontaneously hypertensive rats. J Neuroendocrinol 10: 635-643. PubMed: 9725716.
72. Djordjevic J, Vuckovic T, Jasnic N, Cvijic G, (2007) Effect of various stressors on the blood ACTH and corticosterone concentration in normotensive Wistar and spontaneously hypertensive Wistar-Kyoto rats. Gen Comp Endocrinol 153: 217-220. doi:10.1016/j.ygcen.2007.02.004. PubMed: 17383653.