Clock genes in hypertension: Novel insights from rodent models

Blood Pressure Monitoring

Volumn 19, Issue 5, 2014, Pages 249-254

  Richards, Jacob ^a,b   Diaz, Alexander N ^a   Gumz, Michelle L ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Blood pressure; Circadian; Heart; Kidney; Vasculature

Indexed keywords

ALDOSTERONE; CRYPTOCHROME; NITRIC OXIDE; PER1 PROTEIN; PER2 PROTEIN; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK; CIRCADIAN RHYTHM SIGNALING PROTEIN; SODIUM INTAKE; TRANSCRIPTION FACTOR ARNTL;

BLOOD PRESSURE REGULATION; CIRCADIAN RHYTHM; DIASTOLIC BLOOD PRESSURE; HEART; HYPERTENSION; KIDNEY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SODIUM ABSORPTION; VASCULARIZATION; ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; BLOOD VESSEL; DIABETES MELLITUS; EXPERIMENTAL DIABETES MELLITUS; FEEDBACK SYSTEM; FEEDING BEHAVIOR; GENETIC PREDISPOSITION; GENETICS; HUMAN; KNOCKOUT MOUSE; LIGHT; METABOLIC SYNDROME X; MOUSE; NATRIURESIS; PATHOPHYSIOLOGY; PHARMACOKINETICS; PHYSIOLOGY; RADIATION RESPONSE; RODENT; SODIUM INTAKE; TOXICITY;

ALDOSTERONE; ANIMALS; ARNTL TRANSCRIPTION FACTORS; BLOOD VESSELS; CIRCADIAN RHYTHM; CLOCK PROTEINS; CRYPTOCHROMES; DIABETES MELLITUS; DIABETES MELLITUS, EXPERIMENTAL; FEEDBACK, PHYSIOLOGICAL; FEEDING BEHAVIOR; GENETIC PREDISPOSITION TO DISEASE; HEART; HUMANS; HYPERTENSION; KIDNEY; LIGHT; METABOLIC SYNDROME X; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; MODELS, BIOLOGICAL; NATRIURESIS; PERIOD CIRCADIAN PROTEINS; RODENTIA; SODIUM, DIETARY;

EID: 84925845810     PISSN: 13595237     EISSN: 14735725     Source Type: Journal    
DOI: 10.1097/MBP.0000000000000060     Document Type: Review

References (59)

1. Kraft M, Martin RJ. Chronobiology and chronotherapy in medicine. Dis Mon 1995; 41: 506-575.
2. Loudon AS Circadian biology: a 2.5 billion year old clock. Curr Biol 2012; 22:R570-R571.
3. Richards J, Gumz ML. Mechanism of the circadian clock in physiology. Am J Physiol Regul Integr Comp Physiol 2013; 304:R1053-R1064.
4. Richards J, Gumz ML. Advances in understanding the peripheral circadian clocks. FASEB J 2012; 26: 3602-3613.
5. Hermida RC, Ayala DE, Smolensky MH, Mojón A, Fernández JR, Crespo JJ, et al. Chronotherapy improves blood pressure control and reduces vascular risk in CKD. Nat Rev Nephrol 2013; 9: 358-368.
6. Albrecht U, Eichele G. The mammalian circadian clock. Curr Opin Genet Dev 2003; 13: 271-277.
7. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science 1998; 280: 1564-1569.
8. Zhang EE, Kay SA. Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol 2010; 11: 764-776.
9. Curtis AM, Cheng Y, Kapoor S, Reilly D, Price TS, Fitzgerald GA. Circadian variation of blood pressure and the vascular response to asynchronous stress. Proc Natl Acad Sci USA 2007; 104: 3450-3455.
10. Anea CB, Cheng B, Sharma S, Kumar S, Caldwell RW, Yao L, et al. Increased superoxide and endothelial NO synthase uncoupling in blood vessels of Bmal1-knockout mice. Circ Res 2012; 111: 1157-1165.
11. Anea CB, Zhang M, Chen F, Ali MI, Hart CM, Stepp DW, et al. Circadian clock control of nox4 and reactive oxygen species in the vasculature. PLoS One 2013; 8:e78626.
12. Cheng B, Anea CB, Yao L, Chen F, Patel V, Merloiu A, et al. Tissue-intrinsic dysfunction of circadian clock confers transplant arteriosclerosis. Proc Natl Acad Sci USA 2011; 108: 17147-17152.
13. Lefta M, Campbell KS, Feng HZ, Jin JP, Esser KA. Development of dilated cardiomyopathy in Bmal1 deficient mice. Am J Physiol Heart Circ Physiol 2012; 303:H475-H485.
14. Oster H, Baeriswyl S, Van Der Horst GT, Albrecht U. Loss of circadian rhythmicity in aging mPer1-/-mCry2-/- mutant mice. Genes Dev 2003; 17: 1366-1379.
15. Kunieda T, Minamino T, Miura K, Katsuno T, Tateno K, Miyauchi H, et al. Reduced nitric oxide causes age-associated impairment of circadian rhythmicity. Circ Res 2008; 102: 607-614.
16. Kaneko M, Zechman FW, Smith RE. Circadian variation in human peripheral blood flow levels and exercise responses. J Appl Physiol 1968; 25: 109-114.
17. Panza JA, Epstein SE, Quyyumi AA. Circadian variation in vascular tone and its relation to alpha-sympathetic vasoconstrictor activity. N Engl J Med 1991; 325: 986-990.
18. Hossmann V, Fitzgerald GA, Dollery CT. Circadian rhythm of baroreflex reactivity and adrenergic vascular response. Cardiovasc Res 1980; 14: 125-129.
19. Takeda N, Maemura K. Circadian clock and cardiovascular disease. J Cardiol 2011; 57: 249-256.
20. Naito Y, Tsujino T, Kawasaki D, Okumura T, Morimoto S, Masai M, Sakoda T, et al. Circadian gene expression of clock genes and plasminogen activator inhibitor-1 in heart and aorta of spontaneously hypertensive and Wistar-Kyoto rats. J Hypertens 2003; 21: 1107-1115.
21. Schoenhard JA, Smith LH, Painter CA, Eren M, Johnson CH, Vaughan DE. Regulation of the PAI-1 promoter by circadian clock components: differential activation by BMAL1 and BMAL2. J Mol Cell Cardiol 2003; 35: 473-481.
22. Huang J, Sabater-Lleal M, Asselbergs FW, Tregouet D, Shin SY, Ding J, et al. Genome-wide association study for circulating levels of PAI-1 provides novel insights into its regulation. Blood 2012; 120: 4873-4881.
23. Guo B, Chatterjee S, Li L, Kim JM, Lee J, Yechoor VK, et al. The clock gene, brain and muscle Arnt-like 1, regulates adipogenesis via Wnt signaling pathway. FASEB J 2012; 26: 3453-3463.
24. 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.
25. Lee J, Kim MS, Li R, Liu VY, Fu L, Moore DD, et al. Loss of Bmal1 leads to uncoupling and impaired glucose-stimulated insulin secretion in beta-cells. Islets 2011; 3: 381-388.
26. Pappa KI, Gazouli M, Anastasiou E, Iliodromiti Z, Antsaklis A, Anagnou NP. The major circadian pacemaker ARNT-like protein-1 (BMAL1) is associated with susceptibility to gestational diabetes mellitus. Diabetes Res Clin Pract 2013; 99: 151-157.
27. Durgan DJ, Trexler NA, Egbejimi O, McElfresh TA, Suk HY, Petterson LE, et al. The circadian clock within the cardiomyocyte is essential for responsiveness of the heart to fatty acids. J Biol Chem 2006; 281: 24254-24269.
28. Durgan DJ, Young ME. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 2010; 106: 647-658.
29. Jeyaraj D, Haldar SM, Wan X, McCauley MD, Ripperger JA, Hu K, et al. Circadian rhythms govern cardiac repolarization and arrhythmogenesis. Nature 2012; 483: 96-99.
30. Zuber AM, Centeno G, Pradervand S, Nikolaeva S, Maquelin L, Cardinaux L, et al. Molecular clock is involved in predictive circadian adjustment of renal function. Proc Natl Acad Sci USA 2009; 106: 16523-16528.
31. Nikolaeva S, Pradervand S, Centeno G, Zavadova V, Tokonami N, Maillard M, et al. The circadian clock modulates renal sodium handling. J Am Soc Nephrol 2012; 23: 1019-1026.
32. 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.
33. Bandin C, Martinez-Nicolas A, Ordovás JM, Ros Lucas JA, Castell P, Silvente T, et al. Differences in circadian rhythmicity in CLOCK 3111T/C genetic variants in moderate obese women as assessed by thermometry, actimetry and body position. Int J Obes (Lond) 2012; 37: 1044-1050.
34. Gumz ML, Stow LR, Lynch IJ, Greenlee MM, Rudin A, Cain BD, et al. The circadian clock protein period 1 regulates expression of the renal epithelial sodium channel in mice. J Clin Invest 2009; 119: 2423-2434.
35. Gumz ML, Cheng KY, Lynch IJ, Stow LR, Greenlee MM, Cain BD, Wingo CS. Regulation of alphaENaC expression by the circadian clock protein period 1 in mpkCCD(c14) cells. Biochim Biophys Acta 2010; 1799: 622-629.
36. Richards J, Greenlee MM, Jeffers LA, Cheng KY, Guo L, Eaton DC, Gumz ML. Inhibition of alphaENaC expression and ENaC activity following blockade of the circadian clock-regulatory kinases CKIδ/ε. Am J Physiol Renal Physiol 2012; 303:F918-F927.
37. Richards J, Jeffers LA, All SC, Cheng KY, Gumz ML. Role of Per1 and the mineralocorticoid receptor in the coordinate regulation of alphaENaC in renal cortical collecting duct cells. Front Physiol 2013; 4: 253.
38. Stow LR, Richards J, Cheng KY, Lynch IJ, Jeffers LA, Greenlee MM, et al. The circadian protein period 1 contributes to blood pressure control and coordinately regulates renal sodium transport genes. Hypertension 2012; 59: 1151-1156.
39. Lubarski I, Pihakaski-Maunsbach K, Karlish SJ, Maunsbach AB, Garty H. Interaction with the Na,K-ATPase and tissue distribution of FXYD5 (related to ion channel). J Biol Chem 2005; 280: 37717-37724.
40. Debonneville C, Staub O. Participation of the ubiquitin-conjugating enzyme UBE2E3 in Nedd4-2-dependent regulation of the epithelial Na + channel. Mol Cell Biol 2004; 24: 2397-2409.
41. Lee IH, Campbell CR, Song SH, Day ML, Kumar S, Cook DI, Dinudom A. The activity of the epithelial sodium channels is regulated by caveolin-1 via a Nedd4-2-dependent mechanism. J Biol Chem 2009; 284: 12663-12669.
42. Bugaj V, Mironova E, Kohan DE, Stockand JD. Collecting duct-specific endothelin B receptor knockout increases ENaC activity. Am J Physiol Cell Physiol 2012; 302:C188-C194.
43. Bose S, Boockfor FR. Episodes of prolactin gene expression in GH3 cells are dependent on selective promoter binding of multiple circadian elements. Endocrinology 2010; 151: 2287-2296.
44. Oster H, van der Horst GT, Albrecht U. Daily variation of clock output gene activation in behaviorally arrhythmic mPer/mCry triple mutant mice. Chronobiol Int 2003; 20: 683-695.
45. Richards J, All S, Skopis G, Cheng KY, Compton B, Srialluri N, et al. Opposing actions of Per1 and Cry2 in the regulation of Per1 target gene expression in the liver and kidney. Am J Physiol Regul Integr Comp Physiol 2013; 305:R735-747.
46. Marques FZ, Campain AE, Tomaszewski M, Zukowska-Szczechowska E, Yang YH, Charchar FJ, Morris BJ. Gene expression profiling reveals renin mRNA overexpression in human hypertensive kidneys and a role for microRNAs. Hypertension 2011; 58: 1093-1098.
47. Chen R, Schirmer A, Lee Y, Lee H, Kumar V, Yoo SH, et al. Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol Cell 2009; 36: 417-430.
48. Vukolic A, Antic V, Van Vliet BN, Yang Z, Albrecht U, Montani JP. Role of mutation of the circadian clock gene Per2 in cardiovascular circadian rhythms. Am J Physiol Regul Integr Comp Physiol 2010; 298: R627-R634.
49. Viswambharan H, Carvas JM, Antic V, Marecic A, Jud C, Zaugg CE, et al. Mutation of the circadian clock gene Per2 alters vascular endothelial function. Circulation 2007; 115: 2188-2195.
50. Eckle T, Hartmann K, Bonney S, Reithel S, Mittelbronn M, Walker LA, et al. Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch crucial for myocardial adaptation to ischemia. Nat Med 2012; 18: 774-782.
51. Bonney S, Kominsky D, Brodsky K, Eltzschig H, Walker L, Eckle T. Cardiac Per2 functions as novel link between fatty acid metabolism and myocardial inflammation during ischemia and reperfusion injury of the heart. PLoS One 2013; 8:e71493.
52. Dallmann R, Weaver DR. Altered body mass regulation in male mPeriod mutant mice on high-fat diet. Chronobiol Int 2010; 27: 1317-1328.
53. Englund A, Kovanen L, Saarikoski ST, Haukka J, Reunanen A, Aromaa A, et al. NPAS2 and PER2 are linked to risk factors of the metabolic syndrome. J Circadian Rhythms 2009; 7: 5.
54. Garcia-Rios A, Perez-Martinez P, Delgado-Lista J, Phillips CM, Gjelstad IM, Wright JW, et al. A Period 2 genetic variant interacts with plasma SFA to modify plasma lipid concentrations in adults with metabolic syndrome. J Nutr 2012; 142: 1213-1218.
55. Doi M, Takahashi Y, Komatsu R, Yamazaki F, Yamada H, Haraguchi S, et al. Salt-sensitive hypertension in circadian clock-deficient Cry-null mice involves dysregulated adrenal Hsd3b6. Nat Med 2010; 16: 67-74.
56. Nugrahaningsih DA, Emoto N, Vignon-Zellweger N, Purnomo E, Yagi K, Nakayama K, et al. Chronic hyperaldosteronism in cryptochrome-null mice induces high-salt- and blood pressure-independent kidney damage in mice. Hypertens Res 2013; 37: 202-209.
57. Tanida M, Yamatodani A, Niijima A, Shen J, Todo T, Nagai K. Autonomic and cardiovascular responses to scent stimulation are altered in cry KO mice. Neurosci Lett 2007; 413: 177-182.
58. Zhang EE, Liu Y, Dentin R, Pongsawakul PY, Liu AC, Hirota T. Cryptochrome mediates circadian regulation of cAMP signaling and hepatic gluconeogenesis. Nat Med 2010; 16: 1152-1156.
59. Hirota T, Lee JW, St John PC, Sawa M, Iwaisako K, Noguchi T, et al. Identification of small molecule activators of cryptochrome. Science 2012; 337: 1094-1097.