Artificial light at night suppresses the expression of sarco/endoplasmic reticulum Ca2+ -ATPase in the left ventricle of the heart in normotensive and hypertensive rats
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
34089548
DOI
10.1113/ep089594
Knihovny.cz E-zdroje
- Klíčová slova
- angiotensin II receptor type 1, artificial light at night, rats, sarco/endoplasmic reticulum Ca2+-ATPase, the left ventricle of the heart,
- MeSH
- endoplazmatické retikulum metabolismus MeSH
- hypertenze * MeSH
- krevní tlak MeSH
- krysa rodu Rattus MeSH
- potkani Wistar MeSH
- srdeční komory * MeSH
- světelné znečištění MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
NEW FINDINGS: What is the central question of this study? Artificial light at night decreases blood pressure and heart rate in rats. Are these changes in heart rate accompanied by changes in protein expression in the heart's left ventricle? What is the main finding and its importance? Five weeks of artificial light at night affected protein expression in the heart's left ventricle in normotensive and hypertensive rats. Artificial light at night decreased expression of the sarco/endoplasmic reticulum Ca2+ -ATPase, angiotensin II receptor type 1 and endothelin-1. ABSTRACT: Artificial light at night (ALAN) affects the circadian rhythm of the heart rate in normotensive Wistar rats (WT) and spontaneously hypertensive rats (SHR) through the autonomic nervous system, which regulates the heart's activity through calcium handling, an important regulator in heart contractility. We analysed the expression of the sarco/endoplasmic reticulum Ca2+ -ATPase (SERCA2) and other selected regulatory proteins involved in the regulation of heart contractility, angiotensin II receptor type 1 (AT1 R), endothelin-1 (ET-1) and tyrosine hydroxylase (TH), in the left ventricle of the heart in WT and SHR after 2 and 5 weeks of ALAN with intensity 1-2 lx. Expression of SERCA2 was decreased in WT (control: 0.53 ± 0.07; ALAN: 0.46 ± 0.10) and SHR (control: 0.72 ± 0.18; ALAN: 0.56 ± 0.21) after 5 weeks of ALAN (P = 0.067). Expression of AT1 R was significantly decreased in WT (control: 0.51 ± 0.27; ALAN: 0.34 ± 0.20) and SHR (control: 0.38 ± 0.07; ALAN: 0.23 ± 0.09) after 2 weeks of ALAN (P = 0.028) and in SHR after 5 weeks of ALAN. Expression of ET-1 was decreased in WT (control: 0.51 ± 0.27; ALAN: 0.28 ± 0.12) and SHR (control: 0.54 ± 0.10; ALAN: 0.35 ± 0.23) after 5 weeks of ALAN (P = 0.015). ALAN did not affect the expression of TH in WT or SHR. In conclusion, ALAN suppressed the expression of SERCA2, AT1 R and ET-1, which are important for the regulation of heart contractility, in a strain-dependent pattern in both WT and SHR.
Zobrazit více v PubMed
Alaasam, V. J., Liu, X., Niu, Y., Habibian, J. S., Pieraut, S., Ferguson, B. S., Zhang Y., & Ouyang, J. Q. (2021). Effects of dim artificial light at night on locomotor activity, cardiovascular physiology, and circadian clock genes in a diurnal songbird. Environmental Pollution, 282, 117036. https://doi.org/10.1016/j.envpol.2021.117036
Beesley, S., Noguchi, T., & Welsh, D. K. (2016). Cardiomyocyte circadian oscillations are cell-autonomous, amplified by β-adrenergic signaling, and synchronized in cardiac ventricle tissue. PLoS One, 11(7), e0159618. https://doi.org/10.1371/journal.pone.0159618
Black, N., D'Souza, A., Wang, Y., Piggins, H., Dobrzynski, H., Morris, G., & Boyett, M. R. (2019). Circadian rhythm of cardiac electrophysiology, arrhythmogenesis, and the underlying mechanisms. Heart Rhythm, 16(2), 298-307. https://doi.org/10.1016/j.hrthm.2018.08.026
Bovo, E., Huke, S., Blatter, L. A., & Zima, A. V. (2017). The effect of PKA-mediated phosphorylation of ryanodine receptor on SR Ca2+ leak in ventricular myocytes. Journal of Molecular and Cellular Cardiology, 104, 9-16. https://doi.org/10.1016/j.yjmcc.2017.01.015
Curtis, A. M., Cheng, Y., Kapoor, S., Reilly, D., Price, T. S., & FitzGerald, G. A. (2007). Circadian variation of blood pressure and the vascular response to asynchronous stress. Proceedings of the National Academy of Sciences, USA, 104(9), 3450-3455. https://doi.org/10.1073/pnas.0611680104
Doi, M., Takahashi, Y., Komatsu, R., Yamazaki, F., Yamada, H., Haraguchi, S., Emoto N., Okuno Y., Tsujimoto G., Kanematsu A., Ogawa O., Todo T., Tsutsui K., van der Horst G. T. J., & Okamura, H. (2010). Salt-sensitive hypertension in circadian clock-deficient Cry-null mice involves dysregulated adrenal Hsd3b6. Nature Medicine, 16(1), 67-74. https://doi.org/10.1038/nm.2061
Dupont, S., Maizel, J., Mentaverri, R., Chillon, J.-M., Six, I., Giummelly, P., Brazier M., Choukroun G., Tribouilloy C., Massy Z. A., & Slama, M. (2012). The onset of left ventricular diastolic dysfunction in SHR rats is not related to hypertrophy or hypertension. American Journal of Physiology. Heart and Circulatory Physiology, 302(7), H1524-H1532. https://doi.org/10.1152/ajpheart.00955.2010
El-Armouche, A., & Eschenhagen, T. (2009). β-Adrenergic stimulation and myocardial function in the failing heart. Heart Failure Reviews, 14(4), 225-241. https://doi.org/10.1007/s10741-008-9132-8
Engelhardt, S., Hein, L., Dyachenkow, V., Kranias, E. G., Isenberg, G., & Lohse, M. J. (2004). Altered calcium handling is critically involved in the cardiotoxic effects of chronic β-adrenergic stimulation. Circulation, 109(9), 1154-1160. https://doi.org/10.1161/01.CIR.0000117254.68497.39
Fisher, J. P., & Paton, J. F. R. (2012). The sympathetic nervous system and blood pressure in humans: Implications for hypertension. Journal of Human Hypertension, 26(8), 463-475. https://doi.org/10.1038/jhh.2011.66
Grundy, D. (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. Experimental Physiology, 100(7), 755-758. https://doi.org/10.1113/EP085299
Hahn, A. W., Resink, T. J., Scott-Burden, T., Powell, J., Dohi, Y., & Bühler, F. R. (1990). Stimulation of endothelin mRNA and secretion in rat vascular smooth muscle cells: A novel autocrine function. Cell Regulation, 1(9), 649-659. https://doi.org/10.1091/mbc.1.9.649
Hanai, S., Masuo, Y., Shirai, H., Oishi, K., Saida, K., & Ishida, N. (2005). Differential circadian expression of endothelin-1 mRNA in the rat suprachiasmatic nucleus and peripheral tissues. Neuroscience Letters, 377(1), 65-68. https://doi.org/10.1016/j.neulet.2004.11.082
Honma, S. (2018). The mammalian circadian system: A hierarchical multi-oscillator structure for generating circadian rhythm. Journal of Physiological Sciences, 68(3), 207-219. https://doi.org/10.1007/s12576-018-0597-5
Kalsbeek, A., van der Spek, R., Lei, J., Endert, E., Buijs, R. M., & Fliers, E. (2012). Circadian rhythms in the hypothalamo-pituitary-adrenal (HPA) axis. Molecular and Cellular Endocrinology, 349(1), 20-29. https://doi.org/10.1016/j.mce.2011.06.042
Khan, S., Duan, P., Yao, L., & Hou, H. (2018). Shiftwork-mediated disruptions of circadian rhythms and sleep homeostasis cause serious health problems. International Journal of Genomics, 2018, 8576890. https://doi.org/10.1155/2018/8576890
Kobayashi, T., Hamada, M., Okayama, H., Shigematsu, Y., Sumimoto, T., & Hiwada, K. (1995). Contractile properties of left ventricular myocytes isolated from spontaneously hypertensive rats: Effect of angiotensin II. Journal of Hypertension, 13(12 Pt 2), 1803-1807.
Kokubo, M., Uemura, A., Matsubara, T., & Murohara, T. (2005). Noninvasive evaluation of the time course of change in cardiac function in spontaneously hypertensive rats by echocardiography. Hypertension Research, 28(7), 601-609. https://doi.org/10.1291/hypres.28.601
Kranias, E. G., & Hajjar, R. J. (2012). Modulation of cardiac contractility by the phopholamban/SERCA2a regulatome. Circulation Research, 110(12), 1646-1660. https://doi.org/10.1161/CIRCRESAHA.111.259754
Larivière, R., Sventek, P., & Schiffrin, E. L. (1995). Expression of endothelin-1 gene in blood vessels of adult spontaneously hypertensive rats. Life Sciences, 56(22), 1889-1896. https://doi.org/10.1016/0024-3205(95)00163-Z
Larivière, R., Thibault, G., & Schiffrin, E. L. (1993). Increased endothelin-1 content in blood vessels of deoxycorticosterone acetate-salt hypertensive but not in spontaneously hypertensive rats. Hypertension, 21(3), 294-300. https://doi.org/10.1161/01.HYP.21.3.294
Lefta, M., Campbell, K. S., Feng, H.-Z., Jin, J.-P., & Esser, K. A. (2012). Development of dilated cardiomyopathy in Bmal1-deficient mice. American Journal of Physiology. Heart and Circulatory Physiology, 303(4), H475-H485. https://doi.org/10.1152/ajpheart.00238.2012
Martino, T., Arab, S., Straume, M., Belsham, D. D., Tata, N., Cai, F., Liu P., Trivieri M., Ralph M., & Sole, M. J. (2004). Day/night rhythms in gene expression of the normal murine heart. Journal of Molecular Medicine, 82(4), 256-264. https://doi.org/10.1007/s00109-003-0520-1
Molcan, L., Sutovska, H., Okuliarova, M., Senko, T., Krskova, L., & Zeman, M. (2019). Dim light at night attenuates circadian rhythms in the cardiovascular system and suppresses melatonin in rats. Life Sciences, 231, 116568. https://doi.org/10.1016/j.lfs.2019.116568
Molcan, L., Vesela, A., & Zeman, M. (2016). Influences of phase delay shifts of light and food restriction on blood pressure and heart rate in telemetry monitored rats. Biological Rhythm Research, 47(2), 233-246. https://doi.org/10.1080/09291016.2015.1103945
Moura, E., Pinho Costa, P. M., Moura, D., Guimarães, S., & Vieira-Coelho, M. A. (2005). Decreased tyrosine hydroxylase activity in the adrenals of spontaneously hypertensive rats. Life Sciences, 76(25), 2953-2964. https://doi.org/10.1016/j.lfs.2004.11.017
Naito, Y., Tsujino, T., Fujioka, Y., Ohyanagi, M., & Iwasaki, T. (2002). Augmented diurnal variations of the cardiac renin-angiotensin system in hypertensive rats. Hypertension, 40(6), 827-833. https://doi.org/10.1161/01.HYP.0000039960.66987.89
Nonaka, H., Emoto, N., Ikeda, K., Fukuya, H., Rohman, M. S., Raharjo, S. B., Yagita K., Okamura H., & Yokoyama, M. (2001). Angiotensin II induces circadian gene expression of clock genes in cultured vascular smooth muscle cells. Circulation, 104(15), 1746-1748. https://doi.org/10.1161/hc4001.098048
Obayashi, K., Saeki, K., Iwamoto, J., Ikada, Y., & Kurumatani, N. (2014). Association between light exposure at night and nighttime blood pressure in the elderly independent of nocturnal urinary melatonin excretion. Chronobiology International, 31(6), 779-786. https://doi.org/10.3109/07420528.2014.900501
Obayashi, K., Yamagami, Y., Tatsumi, S., Kurumatani, N., & Saeki, K. (2019). Indoor light pollution and progression of carotid atherosclerosis: A longitudinal study of the HEIJO-KYO cohort. Environment International, 133, 105184. https://doi.org/10.1016/j.envint.2019.105184
Oh, S., Kim, K.-B., Ahn, H., Cho, H.-J., & Choi, Y.-S. (2010). Remodeling of ion channel expression in patients with chronic atrial fibrillation and mitral valvular heart disease. Korean Journal of Internal Medicine, 25(4), 377. https://doi.org/10.3904/kjim.2010.25.4.377
Okayama, H., Hamada, M., Kawakami, H., Ikeda, S., Hashida, H., Shigematsu, Y., & Hiwada, K. (1998). Increased contraction of myocytes isolated from the young spontaneously hypertensive rat: Relationship between systolic and diastolic function. American Journal of Hypertension, 11(3 Pt 1), 349-356. https://doi.org/10.1016/S0895-7061(97)00465-2
Okuliarova, M., Mazgutova, N., Majzunova, M., Rumanova, V. S., & Zeman, M. (2021). Dim light at night impairs daily variation of circulating immune cells and renal immune homeostasis. Frontiers in Immunology, 11, 614960. https://doi.org/10.3389/fimmu.2020.614960
Okumura, S., Fujita, T., Cai, W., Jin, M., Namekata, I., Mototani, Y., Jin H., Ohnuki Y., Tsuneoka Y., Kurotani R., Suita K., Kawakami Y., Hamaguchi S., Abe T., Kiyonari H., Tsunematsu T., Bai Y., Suzuki S., Hidaka Y., …, & Ishikawa, Y. (2014). Epac1-dependent phospholamban phosphorylation mediates the cardiac response to stresses. Journal of Clinical Investigation, 124(6), 2785-2801. https://doi.org/10.1172/JCI64784
Pati, P., Fulton, D. J. R., Bagi, Z., Chen, F., Wang, Y., Kitchens, J., Cassis L. A., Stepp D. W., & Rudic, R. D. (2016). Low-salt diet and circadian dysfunction synergize to induce angiotensin II-dependent hypertension in mice. Hypertension, 67(3), 661-668. https://doi.org/10.1161/HYPERTENSIONAHA.115.06194
Pfeffer, M., Muller, C. M., Mordel, J., Meissl, H., Ansari, N., Deller, T., Korf H.-W., & von Gall, C. (2009). The mammalian molecular clockwork controls rhythmic expression of its own input pathway components. Journal of Neuroscience, 29(19), 6114-6123. https://doi.org/10.1523/JNEUROSCI.0275-09.2009
R Core Team (2020). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Reid, K. J., & Abbott, S. M. (2015). Jet lag and shift work disorder. Sleep Medicine Clinics, 10(4), 523-535. https://doi.org/10.1016/j.jsmc.2015.08.006
Ren, X.-S., Ling, L., Zhou, B., Han, Y., Zhou, Y.-B., Chen, Q., Li Y.-H., Kang Y.-M., & Zhu, G.-Q. (2017). Silencing salusin-β attenuates cardiovascular remodeling and hypertension in spontaneously hypertensive rats. Scientific Reports, 7(1), 43259. https://doi.org/10.1038/srep43259
Rumanova, V. S., Okuliarova, M., Molcan, L., Sutovska, H., & Zeman, M. (2019). Consequences of low-intensity light at night on cardiovascular and metabolic parameters in spontaneously hypertensive rats. Canadian Journal of Physiology and Pharmacology, 97(9), 863-871. https://doi.org/10.1139/cjpp-2019-0043
Sallinen, P., Mänttäri, S., Leskinen, H., Ilves, M., Ruskoaho, H., & Saarela, S. (2007). Time course of changes in the expression of DHPR, RyR2, and SERCA2 after myocardial infarction in the rat left ventricle. Molecular and Cellular Biochemistry, 303(1-2), 97-103. https://doi.org/10.1007/s11010-007-9460-3
Schiffrin, E. L., Larivière, R., Li, J. S., Sventek, P., & Touyz, R. M. (1995). Deoxycorticosterone acetate plus salt induces overexpression of vascular endothelin-1 and severe vascular hypertrophy in spontaneously hypertensive rats. Hypertension, 25(4), 769-773. https://doi.org/10.1161/01.HYP.25.4.769
Schiffrin, E. (2001). Role of endothelin-1 in hypertension and vascular disease. American Journal of Hypertension, 14(11), S83-S89. https://doi.org/10.1016/S0895-7061(01)02074-X
Schlaich, M. P., Socratous, F., Hennebry, S., Eikelis, N., Lambert, E. A., Straznicky, N., Esler M. D., & Lambert, G. W. (2009). Sympathetic activation in chronic renal failure. Journal of the American Society of Nephrology, 20(5), 933-939. https://doi.org/10.1681/ASN.2008040402
Silva-Cutini, M. A., Almeida, S. A., Nascimento, A. M., Abreu, G. R., Bissoli, N. S., Lenz, D., CEndringer D., Brasil G. A., Lima E. M., Biancardi V. C., & Andrade, T. U. (2019). Long-term treatment with kefir probiotics ameliorates cardiac function in spontaneously hypertensive rats. Journal of Nutritional Biochemistry, 66, 79-85. https://doi.org/10.1016/j.jnutbio.2019.01.006
Simko, F., Baka, T., Paulis, L., & Reiter, R. J. (2016). Elevated heart rate and nondipping heart rate as potential targets for melatonin: A review. Journal of Pineal Research, 61(2), 127-137. https://doi.org/10.1111/jpi.12348
Smyrnias, I., Goodwin, N., Wachten, D., Skogestad, J., Aronsen, J. M., Robinson, E. L., Demydenko K., Segonds-Pichon A., Oxley D., Sadayappan S., Sipido K., Bootman M. D., & Roderick, H. L. (2018). Contractile responses to endothelin-1 are regulated by PKC phosphorylation of cardiac myosin binding protein-C in rat ventricular myocytes. Journal of Molecular and Cellular Cardiology, 117, 1-18. https://doi.org/10.1016/j.yjmcc.2018.02.012
Sutovska, H., Molcan, L., Koprdova, R., Piesova, M., Mach, M., & Zeman, M. (2020). Prenatal hypoxia increases blood pressure in male rat offspring and affects their response to artificial light at night. Journal of Developmental Origins of Health and Disease (in press). https://doi.org/10.1017/S2040174420000963
Vavřínová, A., Behuliak, M., Bencze, M., Vaněčková, I., & Zicha, J. (2019). Which sympathoadrenal abnormalities of adult spontaneously hypertensive rats can be traced to a prehypertensive stage? Hypertension Research, 42(7), 949-959. https://doi.org/10.1038/s41440-018-0198-y
Wang, Z., Tapa, S., Francis Stuart, S. D., Wang, L., Bossuyt, J., Delisle, B. P., & Ripplinger, C. M. (2020). Aging disrupts normal time-of-day variation in cardiac electrophysiology. Circulation: Arrhythmia and Electrophysiology, 13(9), e008093. https://doi.org/10.1161/CIRCEP.119.008093
Weisser-Thomas, J., Nguyen, Q., Schuettel, M., Thomas, D., Dreiner, U., Grohé, C., & Meyer, R. (2007). Age and hypertrophy related changes in contractile post-rest behavior and action potential properties in isolated rat myocytes. AGE, 29(4), 205-217. https://doi.org/10.1007/s11357-007-9040-1
West, A. C., Smith, L., Ray, D. W., Loudon, A. S., Brown, T. M., & Bechtold, D. A. (2017). Misalignment with the external light environment drives metabolic and cardiac dysfunction. Nature Communications, 8(1), 417. https://doi.org/10.1038/s41467-017-00462-2
Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag. https://ggplot2.tidyverse.org
Witte, K., Grebmer, W., Scalbert, E., Delagrange, P., Guardiola-Lemaître, B., & Lemmer, B. (1998a). Effects of melatoninergic agonists on light-suppressed circadian rhythms in rats. Physiology & Behavior, 65(2), 219-224.
Witte, K., Schnecko, A., Buijs, R. M., van der Vliet, J., Scalbert, E., Delagrange, P., Guardiola-Lemaître B., & Lemmer, B. (1998b). Effects of SCN lesions on circadian blood pressure rhythm in normotensive and transgenic hypertensive rats. Chronobiology International, 15(2), 135-145. https://doi.org/10.3109/07420529808998678
Young, M. E. (2006). The circadian clock within the heart: Potential influence on myocardial gene expression, metabolism, and function. American Journal of Physiology. Heart and Circulatory Physiology, 290(1), H1-H16. https://doi.org/10.1152/ajpheart.00582.2005
Zeng, Q., Li, X., Zhong, G., Zhang, W., & Sun, C. (2009). Endothelin-1 induces intracellular [Ca2+] increase via Ca2+ influx through the L-type Ca2+ channel, Ca2+-induced Ca2+ release and a pathway involving ETA receptors, PKC, PKA and AT1 receptors in cardiomyocytes. Science in China Series C: Life Sciences, 52(4), 360-370. https://doi.org/10.1007/s11427-009-0046-z
Zhang, M., Prosser, B. L., Bamboye, M. A., Gondim, A. N. S., Santos, C. X., Martin, D., Ghigo A., Perino A., Brewer A. C., Ward C. W., Hirsch E., Lederer W. J., & Shah, A. M. (2015). Contractile function during angiotensin-II activation. Journal of the American College of Cardiology, 66(3), 261-272. https://doi.org/10.1016/j.jacc.2015.05.020