Circadian profiles in the embryonic chick heart: L-type voltage-gated calcium channels and signaling pathways

Chronobiology International

Volumn 27, Issue 9-10, 2010, Pages 1673-1696

  Ko, Michael L ^a   Shi, Liheng ^a   Grushin, Kirill ^a   Nigussie, Fikru ^a   Ko, Gladys Y P ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Cardiomyocyte; Chick heart embryo; Circadian L type voltage gated calcium channel; Signal transduction

Indexed keywords

ACTIN; CALCIUM CHANNEL L TYPE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL; ARTICLE; BIOLOGICAL RHYTHM; CHICK EMBRYO; CHICKEN; CIRCADIAN RHYTHM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; HEART MUSCLE; HEART MUSCLE CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE;

ACTINS; ANIMALS; BIOLOGICAL CLOCKS; CALCIUM CHANNELS, L-TYPE; CHICK EMBRYO; CHICKENS; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION; HEART; MAP KINASE KINASE KINASES; MUSCLE, SMOOTH, VASCULAR; MYOCARDIUM; MYOCYTES, CARDIAC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA; SPONDIAS PURPUREA;

EID: 78049231452     PISSN: 07420528     EISSN: 15256073     Source Type: Journal    
DOI: 10.3109/07420528.2010.514631     Document Type: Article

References (93)

1. Acosta L, Haase H, Morano I, Moorman AF, Franco D. (2004). Regional expression of L-type calcium channel subunits during cardiac development. Dev. Dyn. 230:131-136.
2. 2+ current amplitude and open channel probability. Circ. Res. 101:590-597.
3. Ballard-Croft C, Locklar AC, Keith BJ, Mentzer RM, Jr., Lasley RD. (2008). Oxidative stress and adenosine A1 receptor activation differentially modulate subcellular cardiomyocyte MAPKs. Am. J. Physiol. Heart Circ. Physiol. 294:H263-H271.
4. Boixel C, Gonzalez W, Louedec L, Hatem SN. (2001). Mechanisms of L-type Ca(2+) current downregulation in rat atrial myocytes during heart failure. Circ. Res. 89:607-613.
5. Bray MS, Young ME. (2008). Diurnal variations in myocardial metabolism. Cardiovasc. Res. 79:228-237.
6. Bray MS, Shaw CA, Moore MW Garcia RA, Zanquetta MM, Durgan DJ, Jeong WJ, Tsai JY, Bugger H, Zhang D, Rohrwasser A, Rennison JH, Dyck JR, Litwin SE, Hardin PE, Chow CW, Chandler MP, Abel ED, Young ME. (2008). Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am. J. Physiol. Heart Circ. Physiol. 294:H1036-H1047.
7. Butcher GQ, Doner J, Dziema H, Collamore M, Burgoon PW, Obrietan K. (2002). The p42/44 mitogen-activated protein kinase pathway couples photic input to circadian clock entrainment. J. Biol. Chem. 277:29519-29525.
8. Butcher GQ, Lee B, Obrietan K. (2003). Temporal regulation of light-induced extracellular signalregulated kinase activation in the suprachiasmatic nucleus. J. Neurophysiol. 90:3854-3863.
9. Carroll SL, Horowits R. (2000). Myofibrillogenesis and formation of cell contacts mediate the localization of N-RAP in cultured chick cardiomyocytes. Cell. Motil. Cytoskeleton 47:63-76.
10. Collins HE, Rodrigo GC. (2010). Inotropic response of cardiac ventricular myocytes to beta-adrenergic stimulation with isoproterenol exhibits diurnal variation: involvement of nitric oxide. Circ. Res. 106:1244-1252.
11. Davidson AJ, Yamazaki S, Menaker M. (2003). SCN: ringmaster of the circadian circus or conductor of the circadian orchestra? Novartis Found. Symp. 253:110-121; discussion 121-115, 281-114.
12. Davidson AJ, London B, Block GD, Menaker M. (2005). Cardiovascular tissues contain independent circadian clocks. Clin. Exp. Hypertens. 27:307-311.
13. Dhingra S, Sharma AK, Singla DK, Singal PK. (2007). p38 and ERK1/2 MAPKs mediate the interplay of TNF-alpha and IL-10 in regulating oxidative stress and cardiac myocyte apoptosis. Am. J. Physiol Heart Circ. Physiol. 293:H3524-H3531.
14. Duguay D, Cermakina N. (2009). Crosstalk between physiology and circadian clock proteins. Chronobiol. Int, 26:1479-1513.
15. Durgan DJ, Hotze MA, Tomlin TM, Egbejimi O, Graveleau C, Abel ED, Shaw CA, Bray MS, Hardin PE, Young ME. (2005). The intrinsic circadian clock within the cardiomyocyte. Am. J. Physiol Heart. Circ. Physiol. 289:H1530-H1541.
16. Durgan DJ, Smith JK, Hotze MA, Egbejimi O, Cuthbert KD, Zaha VG, Dyck JR, Abel ED, Young ME. (2006a). Distinct transcriptional regulation of long-chain acyl-CoA synthetase isoforms and cytosolic thioesterase 1 in the rodent heart by fatty acids and insulin. Am. J. Physiol. Heart Circ. Physiol. 290:H2480-H2497.
17. Durgan DJ, Trexler NA, Egbejimi O, McElfresh TA, Suk HY, Petterson LE, Shaw CA, Hardin PE, Bray MS, Chandler MP, Chow CW, Young ME. (2006b). The circadian clock within the cardiomyocyte is essential for responsiveness of the heart to fatty acids. J. Biol. Chem 281:24254-24269.
18. Durgan DJ, Moore MW, Ha NP, Egbejimi O, Fields A, Mbawuike U, Egbejimi A, Shaw CA, Bray MS, Nannegari V, Hickson-Bick DL, Heird WC, Dyck JR, Chandler MP, Young ME. (2007). Circadian rhythms in myocardial metabolism and contractile function: influence of workload and oleate. Am. J. Physiol. Heart Circ. Physiol. 293:H2385-H2393.
19. Durgan DJ, Pulinilkunnil T, Villegas-Montoya C, Garvey ME, Frangogiannis NG, Michael LH, Chow CW, Dyck JR, Young ME. (2010). Short communication: ischemia/reperfusion tolerance is timeof- day-dependent: mediation by the cardiomyocyte circadian clock. Circ. Res. 106:546-550.
20. Dziema H, Oatis B, Butcher GQ, Yates R, Hoyt KR, Obrietan K. (2003). The ERK/MAP kinase pathway couples light to immediate-early gene expression in the suprachiasmatic nucleus. Eur. J. Neurosci. 17:1617-1627.
21. Fan JS, Palade P. (1998). Perforated patch recording with beta-escin. Pflugers Arch. 436:1021-1023.
22. 2+ current-mediated regulation of action potential by pacing rate in rat ventricular myocytes. Cardiovasc. Res. 57:670-680.
23. Fayard E, Tintignac LA, Baudry A, Hemmings BA. (2005). Protein kinase B/Akt at a glance. J. Cell Sci. 118:5675-5678.
24. Gaborit N, Le Bouter S, Szuts V, Varro A, Escande D, Nattel S, Demolombe S. (2007). Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J. Physiol. 582:675-693.
25. Gonzalez A, Ravassa S, Loperena I, Lopez B, Beaumont J, Querejeta R, Larman M, Diez J. (2007). Association of depressed cardiac gp130-mediated antiapoptotic pathways with stimulated cardiomyocyte apoptosis in hypertensive patients with heart failure. J. Hypertens. 25:2148-2157.
26. 2+ current kinetics and cardiac wave stability. Am. J. Physiol. Heart Circ. Physiol. 293:H1805-H1815.
27. Haq S, Choukroun G, Lim H, Tymitz KM, del Monte F, Gwathmey J, Grazette L, Michael A, Hajjar R, Force T, Molkentin JD. (2001). Differential activation of signal transduction pathways in human hearts with hypertrophy versus advanced heart failure. Circulation 103:670-677.
28. Hasegawa M, Cahill GM. (2004). Regulation of the circadian oscillator in Xenopus retinal photoreceptors by protein kinases sensitive to the stress-activated protein kinase inhibitor, SB 203580. J. Biol. Chem. 279:22738-22746.
29. Hu Y, Chen X, Pan TT, Neo KL, Lee SW, Khin ES, Moore PK, Bian JS. (2008). Cardioprotection induced by hydrogen sulfide preconditioning involves activation of ERK and PI3K/Akt pathways. Pflugers Arch. 455:607-616.
30. Hull C, Studholme K, Yazulla S, von Gersdorff H. (2006). Diurnal changes in exocytosis and the number of synaptic ribbons at active zones of an ON-type bipolar cell terminal. J. Neurophysiol. 96:2025-2033.
31. Hullin R, Khan IF, Wirtz S, Mohacsi P, Varadi G, Schwartz A, Herzig S. (2003). Cardiac L-type calcium channel beta-subunits expressed in human heart have differential effects on single channel characteristics. J. Biol. Chem. 278:21623-21630.
32. Iuvone PM. (1990). Development of melatonin synthesis in chicken retina: regulation of serotonin Nacetyltransferase activity by light, circadian oscillators, and cyclic AMP. J. Neurochem. 54:1562-1568.
33. Iuvone PM, Avendano G, Butler BJ, Adler R. (1990). Cyclic AMP-dependent induction of serotonin N-acetyltransferase activity in photoreceptor-enriched chick retinal cell cultures: characterization and inhibition by dopamine. J. Neurochem. 55:673-682.
34. Karaganis SP, Kumar V, Beremand PD, Bailey MJ, Thomas TL, Cassone VM. (2008). Circadian genomics of the chick pineal gland in vitro. BMC Genomics 9:206.
35. Kawano H, Ashizawa N, Toda G, Seto S, Yano K. (2003). Administration of nifedipine CR immediately after awakening prevents a morning surge in hypertensive patients. Case report of three cases. Blood Press. (Suppl.) 1:44-48.
36. Kitahara Y, Saito F, Akao M, Fujita H, Takahashi A, Taguchi H, Hino T, Otsuka Y, Kushiro T, Kanmatsuse K. (2004). Effect of morning and bedtime dosing with cilnidipine on blood pressure, heart rate, and sympathetic nervous activity in essential hypertensive patients. J. Cardiovasc. Pharmacol. 43:68-73.
37. 2+/calmodulin-dependent protein kinase II. Neuron 29:255-266.
38. Ko GY, Ko ML, Dryer SE. (2004). Circadian regulation of cGMP-gated channels of vertebrate cone photoreceptors: role of cAMP and Ras. J. Neurosci. 24:1296-1304.
39. Ko ML, Liu Y, Dryer SE, Ko GY. (2007). The expression of L-type voltage-gated calcium channels in retinal photoreceptors is under circadian control. J. Neurochem. 103:784-792.
40. Korhonen T, Rapila R, Tavi P. (2008). Mathematical model of mouse embryonic cardiomyocyte excitation- contraction coupling. J. Gen. Physiol. 132:407-419.
41. Kranias EG, Bers DM. (2007). Calcium and cardiomyopathies. Subcell. Biochem. 45:523-537.
42. Kubalova Z. (2003). Inactivation of L-type calcium channels in cardiomyocytes. Experimental and theoretical approaches. Gen. Physiol. Biophys. 22:441-454.
43. 2+ channels by phosphatidylinositol 3,4,5-trisphosphate. Circ. Res. 95:300-307.
44. Macrez N, Mironneau C, Carricaburu V, Quignard JF, Babich A, Czupalla C, Nurnberg B, Mironneau J. (2001). Phosphoinositide 3-kinase isoforms selectively couple receptors to vascular L-type Ca(2+) channels. Circ. Res. 89:692-699.
45. 2+ channels in cardiac pacemaker activity. Proc. Natl. Acad. Sci. U. S. A. 100:5543-5548.
46. Matsuda T, Zhai P, Maejima Y, Hong C, Gao S, Tian B, Goto K, Takagi H, Tamamori-Adachi M, Kitajima S, Sadoshima J. (2008). Distinct roles of GSK-3alpha and GSK-3beta phosphorylation in the heart under pressure overload. Proc. Natl. Acad. Sci. U. S. A. 105:20900-20905.
47. McDowell SA, McCall E, Matter WF, Estridge TB, Vlahos CJ. (2004). Phosphoinositide 3-kinase regulates excitation-contraction coupling in neonatal cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 286:H796-H805.
48. McNamara P, Seo SP, Rudic RD, Sehgal A, Chakravarti D, FitzGerald GA. (2001). Regulation of CLOCK and MOP4 by nuclear hormone receptors in the vasculature: a humoral mechanism to reset a peripheral clock. Cell 105:877-889.
49. Mudalagiri NR, Mocanu MM, Di Salvo C, Kolvekar S, Hayward M, Yap J, Keogh B, Yellon DM. (2008). Erythropoietin protects the human myocardium against hypoxia/reoxygenation injury via phosphatidylinositol-3 kinase and ERK1/2 activation. Br. J. Pharmacol. 153:50-56.
50. Nagy AD, Kommedal S, Seomangal K, Csernus VJ. (2009). Circadian expression of clock genes clock and Cry1 in the embryonic chicken pineal gland. Ann. N. Y. Acad. Sci. 1163:484-487.
51. Ohta H, Xu S, Moriya T, Iigo M, Watanabe T, Nakahata N, Chisaka H, Hanita T, Matsuda T, Ohura T, Kimura Y, Yaegashi N, Tsuchiya S, Tei H, Okamura K. (2008). Maternal feeding controls fetal biological clock. PLoS One 3:pe2601.
52. Olson EN, Molkentin JD. (1999). Prevention of cardiac hypertrophy by calcineurin inhibition: hope or hype? Circ. Res. 84:623-632.
53. Parraguez VH, Valenzuela GJ, Vergara M, Ducsay CA, Yellon SM, Seron-Ferre M. (1996). Effect of constant light on fetal and maternal prolactin rhythms in sheep. Endocrinology 137:2355-2361.
54. Pennartz CM, de Jeu MT, Bos NP, Schaap J, Geurtsen AM. (2002). Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 416:286-290.
55. Pierce ME, Sheshberadaran H, Zhang Z, Fox LE, Applebury ML, Takahashi JS. (1993). Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron 10:579-584.
56. Potraluppi F, Touitou Y, Smolensky MH. (2008). Ethical and methological standards for laboratory and medical biological rhythm research. Chronobiol. Int. 25:999-1016.
57. Qiu YG, Chen JZ, Zhu JH, Yao XY. (2003). Differential effects of morning or evening dosing of amlodipine on circadian blood pressure and heart rate. Cardiovasc. Drugs Ther. 17:335-341.
58. Qu Y, Baroudi G, Yue Y, Boutjdir M. (2005a). Novel molecular mechanism involving alpha1D (Cav1.3) L-type calcium channel in autoimmune-associated sinus bradycardia. Circulation 111:3034-3041.
59. Qu Y, Baroudi G, Yue Y, El-Sherif N, Boutjdir M. (2005b). Localization and modulation of {alpha}1D (Cav1.3) L-type Ca channel by protein kinase A. Am. J. Physiol. Heart Circ. Physiol. 288:H2123-H2130.
60. Quignard JF, Mironneau J, Carricaburu V, Fournier B, Babich A, Nurnberg B, Mironneau C, Macrez N. (2001). Phosphoinositide 3-kinase gamma mediates angiotensin II-induced stimulation of L-type calcium channels in vascular myocytes. J. Biol. Chem. 276:32545-32551.
61. Rapila R, Korhonen T, Tavi P. (2008). Excitation-contraction coupling of the mouse embryonic cardiomyocyte. J. Gen. Physiol. 132:397-405.
62. Reppert SM, Schwartz WJ. (1983). Maternal coordination of the fetal biological clock in utero. Science 220:969-971.
63. 2+ oscillations, a potential pacemaking mechanism in early embryonic heart cells. J. Gen. Physiol. 130:133-144.
64. Sauer H, Theben T, Hescheler J, Lindner M, Brandt MC, Wartenberg M. (2001). Characteristics of calcium sparks in cardiomyocytes derived from embryonic stem cells. Am. J. Physiol. Heart Circ. Physiol. 281:H411-H421.
65. Seisenberger C, Specht V, Welling A, Platzer J, Pfeifer A, K äbandner S, Striessnig J, Klugbauer N, Feil R, Hofmann F. (2000). Functional embryonic cardiomyocytes after disruption of the L-type alpha1C (Cav1.2) calcium channel gene in the mouse. J. Biol. Chem. 275:39193-39199.
66. Sharma AK, Dhingra S, Khaper N, Singal PK. (2007). Activation of apoptotic processes during transition from hypertrophy to heart failure in guinea pigs. Am. J. Physiol. Heart Circ. Physiol. 293:H1384-H1390.
67. Shioi T, Kang PM, Douglas PS, Hampe J, Yballe CM, Lawitts J, Cantley LC, Izumo S. (2000). The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J. 19:2537-2548.
68. Splawski I, Timothy KW, Sharpe LM, Decher N, Kumar P, Bloise R, Napolitano C, Schwartz PJ, Joseph RM, Condouris K, Tager-Flusberg H, Priori SG, Sanguinetti MC, Keating MT. (2004). Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119:19-31.
69. Splawski I, Timothy KW, Decher N, Kumar P, Sachse FB, Beggs AH, Sanguinetti MC, Keating MT. (2005). Severe arrhythmia disorder caused by cardiac L-type calcium channel mutations. Proc. Natl. Acad. Sci. U. S. A. 102:8089-8096; discussion 8086-8088.
70. Stavinoha MA, RaySpellicy JW, Essop MF, Graveleau C, Abel ED, Hart-Sailors ML, Mersmann HJ, Bray MS, Young ME. (2004a). Evidence for mitochondrial thioesterase 1 as a peroxisome proliferator- activated receptor-alpha-regulated gene in cardiac and skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 287:E888-E895.
71. Stavinoha MA, Rayspellicy JW, Hart-Sailors ML, Mersmann HJ, Bray MS, Young ME. (2004b). Diurnal variations in the responsiveness of cardiac and skeletal muscle to fatty acids. Am. J. Physiol. Endocrinol. Metab. 287:E878-E887.
72. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ. (2002). Extensive and divergent circadian gene expression in liver and heart. Nature 417:78-83.
73. Sugden PH. (1999). Signaling in myocardial hypertrophy: life after calcineurin? Circ. Res. 84:633-646.
74. Sun H, Xu B, Inoue H, Chen QM. (2008). P38 MAPK mediates COX-2 gene expression by corticosterone in cardiomyocytes. Cell Signal. 20:1952-1959.
75. Szokodi I, Kerkela R, Kubin AM, Sármán B, Pikkarainen S, Kònyi A, Horváth IG, Papp L, Tòth M, Skoumal R, Ruskoaho H. (2008). Functionally opposing roles of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase in the regulation of cardiac contractility. Circulation 118:1651-1658.
76. Takahashi M, Seagar MJ, Jones JF, Reber BF, Catterall WA. (1987). Subunit structure of dihydropyridine- sensitive calcium channels from skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 84:5478-5482.
77. 2+ release in rat ventricular myocytes. J. Physiol. 552:415-424.
78. Teos LY, Zhao A, Alvin Z, Laurence GG, Li C, Haddad GE. (2008). Basal and IGF-I-dependent regulation of potassium channels by MAP kinases and PI3-kinase during eccentric cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 295:H1834-H1845.
79. 2+ channels in embryonic chick heart cells. Circ. Res. 71:376-384.
80. Viard P, Butcher AJ, Halet G, Davies A, Nurnberg B, Heblich F, Dolphin AC. (2004). PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nat. Neurosci. 7:939-946.
81. Vitalini MW, de Paula RM, Goldsmith CS, Jones CA, Borkovich KA, Bell-Pedersen D. (2007). Circadian rhythmicity mediated by temporal regulation of the activity of p38 MAPK. Proc. Natl. Acad. Sci. U. S. A. 104:18223-18228.
82. Wang MC, Collins RF, Ford RC, Berrow NS, Dolphin AC, Kitmitto A. (2004). The three-dimensional structure of the cardiac L-type voltage-gated calcium channel: comparison with the skeletal muscle form reveals a common architectural motif. J. Biol. Chem. 279:7159-7168.
83. Yamashita T, Sekiguchi A, Iwasaki YK, Sagara K, Iinuma H, Hatano S, Fu LT, Watanabe H. (2003). Circadian variation of cardiac K+ channel gene expression. Circulation 107:1917-1922.
84. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682-685.
85. Yan L, Tang Q, Shen D, Peng S, Zheng Q, Guo H, Jiang M, Deng W. (2008). SOCS-1 inhibits TNFalpha- induced cardiomyocyte apoptosis via ERK1/2 pathway activation. Inflammation 31:180-188.
86. Yang M, Wu J, Martin CM, Kvietys PR, Rui T. (2008). Important role of p38 MAP kinase/NFkappaB signaling pathway in the sepsis-induced conversion of cardiac myocytes to a proinflammatory phenotype. Am. J. Physiol. Heart Circ. Physiol. 294:H994-H1001.
87. Young ME. (2003). Circadian rhythms in cardiac gene expression. Curr. Hypertens. Rep. 5:445-453.
88. Young ME. (2006). The circadian clock within the heart: potential influence on myocardial gene expression, metabolism, and function. Am. J. Physiol. Heart Circ. Physiol. 290:H1-H16.
89. Young ME, Bray MS. (2007). Potential role for peripheral circadian clock dyssynchrony in the pathogenesis of cardiovascular dysfunction. Sleep Med. 8:656-667.
90. Young ME, Razeghi P, Cedars AM, Guthrie PH, Taegtmeyer H. (2001a). Intrinsic diurnal variations in cardiac metabolism and contractile function. Circ. Res. 89:1199-1208.
91. Young ME, Razeghi P, Taegtmeyer H. (2001b). Clock genes in the heart: characterization and attenuation with hypertrophy. Circ. Res. 88:1142-1150.
92. Zhang Z, Xu Y, Song H, Rodriguez J, Tuteja D, Namkung Y, Shin HS, Chiamvimonvat N. (2002). Functional Roles of Ca(v)1.3 (alpha(1D)) calcium channel in sinoatrial nodes: insight gained using gene-targeted null mutant mice. Circ. Res. 90:981-987.
93. Zhang Z, He Y, Tuteja D, Xu D, Timofeyev V, Zhang Q, Glatter KA, Xu Y, Shin HS, Low R. (2005). Functional roles of Cav1.3(alpha1D) calcium channels in atria: insights gained from gene-targeted null mutant mice. Circulation 112:1936-1944.