Skip to main content

Advertisement

SpringerLink
Log in

Circadian rhythm disorder: a potential inducer of vascular calcification?

  • Review
  • Published:
Journal of Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Over the past decades, circadian rhythm has drawn a great attention in cardiovascular diseases. The expressions of rhythm genes fluctuate in accordance with the diurnal changes of vascular physiology, which highlights the pivotal effect of vascular clock. Recent researches show that the circadian clock can directly regulate the synthetic and secretory function of endothelial cells and phenotypic switch of vascular smooth muscle cells to adjust vascular relaxation and contraction. Importantly, dysfunction of vascular cells is involved in vascular calcification. Secretion of osteogenic cytokines and calcified vesicles in the vessel, osteogenic phenotype switch of vascular smooth muscle cells are all implicated in the calcification process. Moreover, circadian rhythm disorder can lead to abnormal hormone secretion, oxidative stress, inflammatory reaction, and autophagy, all of which should not be ignored in vascular calcification. Vascular senescence is another pathogenetic mechanism in vascular calcification. Accelerated vascular senescence may act as an important intermediate factor to promote vascular calcification in circadian rhythm disorders. In this review, we elaborate the potential effect of circadian rhythm disorder in vascular calcification and try to provide a new direction in the prevention of vascular calcification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AKT:

Protein kinase B

Ang II:

Angiotensin II

AT1/2:

Ang II type-1/2

BMAL1/2:

Brain and muscle ARNT-like 1/2

BMP:

Bone morphogenetic protein

CCL2:

Chemokine ligand 2

CLOCK:

Circadian locomotor output cycles kaput

CRY1/2:

Cryptochrome 1/2

ECs:

Endothelial cells

eNOS:

Endothelial nitric oxide synthase

ERK:

Extracellular signal-regulating kinase

IFN-γ:

Interferon-γ

IL-1β/6:

Interleukin-1β/6

MAPK:

Mitogen-activated protein kinase

MGP:

Matrix Gla protein

MMP:

Matrix metalloproteinase

mTOR:

Mammalian target of rapamycin

NF-κB:

Nuclear factor kappa B

NO:

Nitric oxide

Nox:

NADPH oxidase

PER1/2/3:

Period 1/2/3

PI3K:

Phosphatidylinositol 3-kinase

PPAR:

Peroxisome proliferator-activated receptor

RAAS:

Renin–angiotensin–aldosterone system

RANKL:

Receptor activator of NF-κB ligand

REV-ERBα/β (NR1D1/2):

Nuclear receptor subfamily 1, group D, member1/2

RORE:

ROR response element

RORα/β:

Retinoic acid receptor-related orphan receptor α/β

ROS:

Reactive oxygen species

RUNX2:

Runt-related transcription factor2

SIRT1:

Sirtuin1

Smad:

Small mothers against decapentaplegic

SOD:

Superoxide dismutase

TGF-β:

Transforming growth factor-β

TNF-α:

Tumor necrosis factor-α

VC:

Vascular calcification

VSMCs:

Vascular smooth muscle cells

References

  1. Al-Aly Z (2008) Arterial calcification: a tumor necrosis factor-alpha mediated vascular Wnt-opathy. Transl Res 151:233–239. https://doi.org/10.1016/j.trsl.2007.12.005

    Article  CAS  PubMed  Google Scholar 

  2. Anea CB, Ali MI, Osmond JM, Sullivan JC, Stepp DW, Merloiu AM, Rudic RD (2010) Matrix metalloproteinase 2 and 9 dysfunction underlie vascular stiffness in circadian clock mutant mice. Arterioscler Thromb Vasc Biol 30:2535–2543. https://doi.org/10.1161/atvbaha.110.214379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Anea CB, Cheng B, Sharma S, Kumar S, Caldwell RW, Yao L, Ali MI, Merloiu AM, Stepp DW, Black SM, Fulton DJ, Rudic RD (2012) Increased superoxide and endothelial NO synthase uncoupling in blood vessels of Bmal1-knockout mice. Circ Res 111:1157–1165. https://doi.org/10.1161/circresaha.111.261750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Anea CB, Zhang M, Chen F, Ali MI, Hart CM, Stepp DW, Kovalenkov YO, Merloiu AM, Pati P, Fulton D, Rudic RD (2013) Circadian clock control of Nox4 and reactive oxygen species in the vasculature. PLoS One 8:e78626. https://doi.org/10.1371/journal.pone.0078626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Anea CB, Zhang M, Stepp DW, Simkins GB, Reed G, Fulton DJ, Rudic RD (2009) Vascular disease in mice with a dysfunctional circadian clock. Circulation 119:1510–1517. https://doi.org/10.1161/circulationaha.108.827477

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bhatwadekar AD, Beli E, Diao Y, Chen J, Luo Q, Alex A, Caballero S, Dominguez JM 2nd, Salazar TE, Busik JV, Segal MS, Grant MB (2017) Conditional deletion of Bmal1 accentuates microvascular and macrovascular injury. Am J Pathol 187:1426–1435. https://doi.org/10.1016/j.ajpath.2017.02.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, Darley-Usmar VM, McDonald JM, Chen Y (2008) Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem 283:15319–15327. https://doi.org/10.1074/jbc.M800021200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Callegari A, Coons ML, Ricks JL, Rosenfeld ME, Scatena M (2014) Increased calcification in osteoprotegerin-deficient smooth muscle cells: dependence on receptor activator of NF-kappaB ligand and interleukin 6. J Vasc Res 51:118–131. https://doi.org/10.1159/000358920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cavadini G, Petrzilka S, Kohler P, Jud C, Tobler I, Birchler T, Fontana A (2007) TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc Natl Acad Sci U S A 104:12843–12848. https://doi.org/10.1073/pnas.0701466104

    Article  PubMed  PubMed Central  Google Scholar 

  10. Chen C, Zhou M, Ge Y, Wang X (2020) SIRT1 and aging related signaling pathways. Mech Ageing Dev 187:111215. https://doi.org/10.1016/j.mad.2020.111215

    Article  CAS  PubMed  Google Scholar 

  11. Chen WD, Wen MS, Shie SS, Lo YL, Wo HT, Wang CC, Hsieh IC, Lee TH, Wang CY (2014) The circadian rhythm controls telomeres and telomerase activity. Biochem Biophys Res Commun 451:408–414. https://doi.org/10.1016/j.bbrc.2014.07.138

    Article  CAS  PubMed  Google Scholar 

  12. Chen YQ, Zhao J, Jin CW, Li YH, Tang MX, Wang ZH, Zhang W, Zhang Y, Li L, Zhong M (2016) Testosterone delays vascular smooth muscle cell senescence and inhibits collagen synthesis via the Gas6/Axl signaling pathway. Age (Dordrecht, Netherlands) 38:60. https://doi.org/10.1007/s11357-016-9910-5

    Article  CAS  Google Scholar 

  13. Chen Z, Yoo SH, Takahashi JS (2013) Small molecule modifiers of circadian clocks. Cell Mol Life Sci 70:2985–2998. https://doi.org/10.1007/s00018-012-1207-y

    Article  CAS  PubMed  Google Scholar 

  14. Chi C, Li DJ, Jiang YJ, Tong J, Fu H, Wu YH, Shen FM (2019) Vascular smooth muscle cell senescence and age-related diseases: state of the art. Biochim Biophys Acta Mol Basis Dis 1865:1810–1821. https://doi.org/10.1016/j.bbadis.2018.08.015

    Article  CAS  PubMed  Google Scholar 

  15. Colafella KMM, Denton KM (2018) Sex-specific differences in hypertension and associated cardiovascular disease. Nat Rev Nephrol 14:185–201. https://doi.org/10.1038/nrneph.2017.189

    Article  PubMed  Google Scholar 

  16. Crnko S, Du Pre BC, Sluijter JPG, Van Laake LW (2019) Circadian rhythms and the molecular clock in cardiovascular biology and disease. Nat Rev Cardiol 16:437–447. https://doi.org/10.1038/s41569-019-0167-4

    Article  PubMed  Google Scholar 

  17. Demer LL, Tintut Y (2008) Vascular calcification: pathobiology of a multifaceted disease. Circulation 117:2938–2948. https://doi.org/10.1161/circulationaha.107.743161

    Article  PubMed  PubMed Central  Google Scholar 

  18. Deretic V, Saitoh T, Akira S (2013) Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13:722–737. https://doi.org/10.1038/nri3532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Deuell KA, Callegari A, Giachelli CM, Rosenfeld ME, Scatena M (2012) RANKL enhances macrophage paracrine pro-calcific activity in high phosphate-treated smooth muscle cells: dependence on IL-6 and TNF-alpha. J Vasc Res 49:510–521. https://doi.org/10.1159/000341216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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 GT, Okamura H (2010) Salt-sensitive hypertension in circadian clock-deficient cry-null mice involves dysregulated adrenal Hsd3b6. Nat Med 16:67–74. https://doi.org/10.1038/nm.2061

    Article  CAS  PubMed  Google Scholar 

  21. Dominguez-Rodriguez A, Abreu-Gonzalez P, Sanchez-Sanchez JJ, Kaski JC, Reiter RJ (2010) Melatonin and circadian biology in human cardiovascular disease. J Pineal Res 49:14–22. https://doi.org/10.1111/j.1600-079X.2010.00773.x

    Article  CAS  PubMed  Google Scholar 

  22. Durham AL, Speer MY, Scatena M, Giachelli CM, Shanahan CM (2018) Role of smooth muscle cells in vascular calcification: implications in atherosclerosis and arterial stiffness. Cardiovasc Res 114:590–600. https://doi.org/10.1093/cvr/cvy010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Feng W, Zhang K, Liu Y, Chen J, Cai Q, Zhang Y, Wang M, Wang J, Huang H (2016) Apocynin attenuates angiotensin II-induced vascular smooth muscle cells osteogenic switching via suppressing extracellular signal-regulated kinase 1/2. Oncotarget 7:83588–83600. https://doi.org/10.18632/oncotarget.13193

    Article  PubMed  PubMed Central  Google Scholar 

  24. Forrester SJ, Booz GW, Sigmund CD, Coffman TM, Kawai T, Rizzo V, Scalia R, Eguchi S (2018) Angiotensin II signal transduction: an update on mechanisms of physiology and pathophysiology. Physiol Rev 98:1627–1738. https://doi.org/10.1152/physrev.00038.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Gao J, Zhang K, Chen J, Wang MH, Wang J, Liu P, Huang H (2016) Roles of aldosterone in vascular calcification: an update. Eur J Pharmacol 786:186–193. https://doi.org/10.1016/j.ejphar.2016.05.030

    Article  CAS  PubMed  Google Scholar 

  26. Ghosh HS, McBurney M, Robbins PD (2010) SIRT1 negatively regulates the mammalian target of rapamycin. PLoS One 5:e9199. https://doi.org/10.1371/journal.pone.0009199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Haberzettl P, Hill BG (2013) Oxidized lipids activate autophagy in a JNK-dependent manner by stimulating the endoplasmic reticulum stress response. Redox Biol 1:56–64. https://doi.org/10.1016/j.redox.2012.10.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hardeland R (2019) Aging, melatonin, and the pro- and anti-inflammatory networks. Int J Mol Sci 20. https://doi.org/10.3390/ijms20051223

  29. Harvey A, Montezano AC, Touyz RM (2015) Vascular biology of ageing-implications in hypertension. J Mol Cell Cardiol 83:112–121. https://doi.org/10.1016/j.yjmcc.2015.04.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5:e1000442. https://doi.org/10.1371/journal.pgen.1000442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Inokawa H, Umemura Y, Shimba A, Kawakami E, Koike N, Tsuchiya Y, Ohashi M, Minami Y, Cui G, Asahi T, Ono R, Sasawaki Y, Konishi E, Yoo SH, Chen Z, Teramukai S, Ikuta K, Yagita K (2020) Chronic circadian misalignment accelerates immune senescence and abbreviates lifespan in mice. Sci Rep 10:2569. https://doi.org/10.1038/s41598-020-59541-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jenwitheesuk A, Nopparat C, Mukda S, Wongchitrat P, Govitrapong P (2014) Melatonin regulates aging and neurodegeneration through energy metabolism, epigenetics, autophagy and circadian rhythm pathways. Int J Mol Sci 15:16848–16884. https://doi.org/10.3390/ijms150916848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Jia G, Aroor AR, Jia C, Sowers JR (2019) Endothelial cell senescence in aging-related vascular dysfunction. Biochim Biophys Acta Mol Basis Dis 1865:1802–1809. https://doi.org/10.1016/j.bbadis.2018.08.008

    Article  CAS  PubMed  Google Scholar 

  34. Jia G, Stormont RM, Gangahar DM, Agrawal DK (2012) Role of matrix Gla protein in angiotensin II-induced exacerbation of vascular calcification. Am J Phys Heart Circ Phys 303:H523–H532. https://doi.org/10.1152/ajpheart.00826.2011

    Article  CAS  Google Scholar 

  35. Kagawa Y (2012) From clock genes to telomeres in the regulation of the healthspan. Nutr Rev 70:459–471. https://doi.org/10.1111/j.1753-4887.2012.00504.x

    Article  PubMed  Google Scholar 

  36. Kanno Y, Into T, Lowenstein CJ, Matsushita K (2008) Nitric oxide regulates vascular calcification by interfering with TGF-β signalling. Cardiovasc Res 77:221–230. https://doi.org/10.1093/cvr/cvm049

    Article  CAS  PubMed  Google Scholar 

  37. Kida Y, Goligorsky MS (2016) Sirtuins, cell senescence, and vascular aging. Can J Cardiol 32:634–641. https://doi.org/10.1016/j.cjca.2015.11.022

    Article  PubMed  Google Scholar 

  38. Knowlton AA, Lee AR (2012) Estrogen and the cardiovascular system. Pharmacol Ther 135:54–70. https://doi.org/10.1016/j.pharmthera.2012.03.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ko CH, Takahashi JS (2006) Molecular components of the mammalian circadian clock. Hum Mol Genet 15:Spec No 2:R271-277. https://doi.org/10.1093/hmg/ddl207

    Article  CAS  Google Scholar 

  40. Kondratov RV, Vykhovanets O, Kondratova AA, Antoch MP (2009) Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging 1:979–987. https://doi.org/10.18632/aging.100113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kruger-Genge A, Blocki A, Franke RP, Jung F (2019) Vascular endothelial cell biology: an update. Int J Mol Sci 20. https://doi.org/10.3390/ijms20184411

  42. Lang F, Ritz E, Alesutan I, Voelkl J (2014) Impact of aldosterone on osteoinductive signaling and vascular calcification. Nephron Physiol 128:40–45. https://doi.org/10.1159/000368268

    Article  CAS  PubMed  Google Scholar 

  43. Lee J, Ma K, Moulik M, Yechoor V (2018) Untimely oxidative stress in beta-cells leads to diabetes - role of circadian clock in beta-cell function. Free Radic Biol Med 119:69–74. https://doi.org/10.1016/j.freeradbiomed.2018.02.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lee SJ, Lee IK, Jeon JH (2020) Vascular calcification-new insights into its mechanism. Int J Mol Sci 21. https://doi.org/10.3390/ijms21082685

  45. Liu J, Malkani G, Shi X, Meyer M, Cunningham-Runddles S, Ma X, Sun ZS (2006) The circadian clock period 2 gene regulates gamma interferon production of NK cells in host response to lipopolysaccharide-induced endotoxic shock. Infect Immun 74:4750–4756. https://doi.org/10.1128/iai.00287-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lopez M, Meier D, Muller A, Franken P, Fujita J, Fontana A (2014) Tumor necrosis factor and transforming growth factor beta regulate clock genes by controlling the expression of the cold inducible RNA-binding protein (CIRBP). J Biol Chem 289:2736–2744. https://doi.org/10.1074/jbc.M113.508200

    Article  CAS  PubMed  Google Scholar 

  47. Lu CL, Liao MT, Hou YC, Fang YW, Zheng CM, Liu WC, Chao CT, Lu KC, Ng YY (2020) Sirtuin-1 and its relevance in vascular calcification. Int J Mol Sci 21. https://doi.org/10.3390/ijms21051593

  48. Lucas-Herald AK, Alves-Lopes R, Montezano AC, Ahmed SF, Touyz RM (2017) Genomic and non-genomic effects of androgens in the cardiovascular system: clinical implications. Clin Sci (London, England : 1979) 131:1405–1418. https://doi.org/10.1042/cs20170090

    Article  CAS  Google Scholar 

  49. Luciano AK, Santana JM, Velazquez H, Sessa WC (2017) Akt1 controls the timing and amplitude of vascular circadian gene expression. J Biol Rhythm 32:212–221. https://doi.org/10.1177/0748730417704534

    Article  CAS  Google Scholar 

  50. Luo Z, Xu W, Ma S, Qiao H, Gao L, Zhang R, Yang B, Qiu Y, Chen J, Zhang M, Tao B, Cao F, Wang Y (2017) Moderate autophagy inhibits vascular smooth muscle cell senescence to stabilize progressed atherosclerotic plaque via the mTORC1/ULK1/ATG13 signal pathway. Oxidative Med Cell Longev 2017:3018190–3018199. https://doi.org/10.1155/2017/3018190

    Article  CAS  Google Scholar 

  51. Ma D, Li S, Molusky MM, Lin JD (2012) Circadian autophagy rhythm: a link between clock and metabolism? Trends Endocrinol Metab 23:319–325. https://doi.org/10.1016/j.tem.2012.03.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ma H, Zhong W, Jiang Y, Fontaine C, Li S, Fu J, Olkkonen VM, Staels B, Yan D (2013) Increased atherosclerotic lesions in LDL receptor deficient mice with hematopoietic nuclear receptor rev-erbalpha knock-down. J Am Heart Assoc 2:e000235. https://doi.org/10.1161/jaha.113.000235

    Article  PubMed  PubMed Central  Google Scholar 

  53. McAlpine CS, Swirski FK (2016) Circadian influence on metabolism and inflammation in atherosclerosis. Circ Res 119:131–141. https://doi.org/10.1161/circresaha.116.308034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Migita H, Morser J, Kawai K (2004) Rev-erbalpha upregulates NF-kappaB-responsive genes in vascular smooth muscle cells. FEBS Lett 561:69–74. https://doi.org/10.1016/s0014-5793(04)00118-8

    Article  CAS  PubMed  Google Scholar 

  55. Min LJ, Mogi M, Iwai M, Horiuchi M (2009) Signaling mechanisms of angiotensin II in regulating vascular senescence. Ageing Res Rev 8:113–121. https://doi.org/10.1016/j.arr.2008.12.002

    Article  CAS  PubMed  Google Scholar 

  56. Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451:1069–1075. https://doi.org/10.1038/nature06639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Morris CJ, Purvis TE, Hu K, Scheer FA (2016) Circadian misalignment increases cardiovascular disease risk factors in humans. Proc Natl Acad Sci U S A 113:E1402–E1411. https://doi.org/10.1073/pnas.1516953113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Nakano-Kurimoto R, Ikeda K, Uraoka M, Nakagawa Y, Yutaka K, Koide M, Takahashi T, Matoba S, Yamada H, Okigaki M, Matsubara H (2009) Replicative senescence of vascular smooth muscle cells enhances the calcification through initiating the osteoblastic transition. Am J Phys Heart Circ Phys 297:H1673–H1684. https://doi.org/10.1152/ajpheart.00455.2009

    Article  CAS  Google Scholar 

  59. Neves MF, Cunha AR, Cunha MR, Gismondi RA, Oigman W (2018) The role of renin-angiotensin-aldosterone system and its new components in arterial stiffness and vascular aging. High Blood Press Cardiovasc Prev 25:137–145. https://doi.org/10.1007/s40292-018-0252-5

    Article  CAS  PubMed  Google Scholar 

  60. Okamura H, Doi M, Goto K, Kojima R (2016) Clock genes and salt-sensitive hypertension: a new type of aldosterone-synthesizing enzyme controlled by the circadian clock and angiotensin II. Hypertens Res 39:681–687. https://doi.org/10.1038/hr.2016.91

    Article  CAS  PubMed  Google Scholar 

  61. Osako MK, Nakagami H, Koibuchi N, Shimizu H, Nakagami F, Koriyama H, Shimamura M, Miyake T, Rakugi H, Morishita R (2010) Estrogen inhibits vascular calcification via vascular RANKL system: common mechanism of osteoporosis and vascular calcification. Circ Res 107:466–475. https://doi.org/10.1161/circresaha.110.216846

    Article  CAS  PubMed  Google Scholar 

  62. Osako MK, Nakagami H, Shimamura M, Koriyama H, Nakagami F, Shimizu H, Miyake T, Yoshizumi M, Rakugi H, Morishita R (2013) Cross-talk of receptor activator of nuclear factor-kappaB ligand signaling with renin-angiotensin system in vascular calcification. Arterioscler Thromb Vasc Biol 33:1287–1296. https://doi.org/10.1161/atvbaha.112.301099

    Article  CAS  PubMed  Google Scholar 

  63. Ota T, Fustin JM, Yamada H, Doi M, Okamura H (2012) Circadian clock signals in the adrenal cortex. Mol Cell Endocrinol 349:30–37. https://doi.org/10.1016/j.mce.2011.08.010

    Article  CAS  PubMed  Google Scholar 

  64. Ou H, Liu C, Feng W, Xiao X, Tang S, Mo Z (2018) Role of AMPK in atherosclerosis via autophagy regulation. Sci China Life Sci 61:1212–1221. https://doi.org/10.1007/s11427-017-9240-2

    Article  CAS  PubMed  Google Scholar 

  65. Pandi-Perumal SR, Trakht I, Srinivasan V, Spence DW, Maestroni GJ, Zisapel N, Cardinali DP (2008) Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog Neurobiol 85:335–353. https://doi.org/10.1016/j.pneurobio.2008.04.001

    Article  CAS  PubMed  Google Scholar 

  66. Patel SA, Velingkaar NS, Kondratov RV (2014) Transcriptional control of antioxidant defense by the circadian clock. Antioxid Redox Signal 20:2997–3006. https://doi.org/10.1089/ars.2013.5671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Pati P, Fulton DJ, Bagi Z, Chen F, Wang Y, Kitchens J, Cassis LA, Stepp DW, Rudic RD (2016) Low-salt diet and circadian dysfunction synergize to induce angiotensin II-dependent hypertension in mice. Hypertension 67:661–668. https://doi.org/10.1161/HYPERTENSIONAHA.115.06194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Peng YQ, Xiong D, Lin X, Cui RR, Xu F, Zhong JY, Zhu T, Wu F, Mao MZ, Liao XB, Yuan LQ (2017) Oestrogen inhibits arterial calcification by promoting autophagy. Sci Rep 7:3549. https://doi.org/10.1038/s41598-017-03801-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Perez-Cremades D, Mompeon A, Vidal-Gomez X, Hermenegildo C, Novella S (2018) Role of miRNA in the regulatory mechanisms of estrogens in cardiovascular ageing. Oxidative Med Cell Longev 2018:6082387–6082316. https://doi.org/10.1155/2018/6082387

    Article  CAS  Google Scholar 

  70. Pescatore LA, Gamarra LF, Liberman M (2019) Multifaceted mechanisms of vascular calcification in aging. Arterioscler Thromb Vasc Biol 39:1307–1316. https://doi.org/10.1161/ATVBAHA.118.311576

    Article  CAS  PubMed  Google Scholar 

  71. Qian M, Fang X, Wang X (2017) Autophagy and inflammation. Clin Transl Med 6:24. https://doi.org/10.1186/s40169-017-0154-5

    Article  PubMed  PubMed Central  Google Scholar 

  72. Rana S, Prabhu SD, Young ME (2020) Chronobiological influence over cardiovascular function: the good, the bad, and the ugly. Circ Res 126:258–279. https://doi.org/10.1161/CIRCRESAHA.119.313349

    Article  CAS  PubMed  Google Scholar 

  73. Richards J, Cheng KY, All S, Skopis G, Jeffers L, Lynch IJ, Wingo CS, Gumz ML (2013) A role for the circadian clock protein Per1 in the regulation of aldosterone levels and renal Na+ retention. Am J Physiol Renal Physiol 305:F1697–F1704. https://doi.org/10.1152/ajprenal.00472.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Rodrigo GC, Herbert KE (2018) Regulation of vascular function and blood pressure by circadian variation in redox signalling. Free Radic Biol Med 119:115–120. https://doi.org/10.1016/j.freeradbiomed.2017.10.381

    Article  CAS  PubMed  Google Scholar 

  75. Rossetti S, Corlazzoli F, Gregorski A, Azmi NH, Sacchi N (2012) Identification of an estrogen-regulated circadian mechanism necessary for breast acinar morphogenesis. Cell Cycle (Georgetown, Tex) 11:3691–3700. https://doi.org/10.4161/cc.21946

    Article  CAS  Google Scholar 

  76. Rzewuska-Lech E, Jayachandran M, Fitzpatrick LA, Miller VM (2005) Differential effects of 17beta-estradiol and raloxifene on VSMC phenotype and expression of osteoblast-associated proteins. Am J Phys Endocrinol Metab 289:E105–E112. https://doi.org/10.1152/ajpendo.00366.2004

    Article  CAS  Google Scholar 

  77. Sachdeva UM, Thompson CB (2008) Diurnal rhythms of autophagy: implications for cell biology and human disease. Autophagy 4:581–589. https://doi.org/10.4161/auto.6141

    Article  CAS  PubMed  Google Scholar 

  78. Sato S, Sakurai T, Ogasawara J, Takahashi M, Izawa T, Imaizumi K, Taniguchi N, Ohno H, Kizaki T (2014) A circadian clock gene, rev-erbalpha, modulates the inflammatory function of macrophages through the negative regulation of Ccl2 expression. J Immunol (Baltimore, Md : 1950) 192:407–417. https://doi.org/10.4049/jimmunol.1301982

    Article  CAS  Google Scholar 

  79. Shanahan CM (2013) Autophagy and matrix vesicles: new partners in vascular calcification. Kidney Int 83:984–986. https://doi.org/10.1038/ki.2013.75

    Article  CAS  PubMed  Google Scholar 

  80. Shao J, Wu P, Wu J, Li M (2016) Mechanism of losartan suppressing vascular calcification in rat aortic artery. Chinese Journal of Cellular and Molecular Immunology 32:1060–1064

    PubMed  Google Scholar 

  81. Simko F, Paulis L (2007) Melatonin as a potential antihypertensive treatment. J Pineal Res 42:319–322. https://doi.org/10.1111/j.1600-079X.2007.00436.x

    Article  CAS  PubMed  Google Scholar 

  82. Smolensky MH, Hermida RC, Portaluppi F (2017) Circadian mechanisms of 24-hour blood pressure regulation and patterning. Sleep Med Rev 33:4–16. https://doi.org/10.1016/j.smrv.2016.02.003

    Article  PubMed  Google Scholar 

  83. Son BK, Akishita M, Iijima K, Ogawa S, Maemura K, Yu J, Takeyama K, Kato S, Eto M, Ouchi Y (2010) Androgen receptor-dependent transactivation of growth arrest-specific gene 6 mediates inhibitory effects of testosterone on vascular calcification. J Biol Chem 285:7537–7544. https://doi.org/10.1074/jbc.M109.055087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Strohmaier S, Devore EE, Zhang Y, Schernhammer ES (2018) A review of data of findings on night shift work and the development of DM and CVD events: a synthesis of the proposed molecular mechanisms. Current Diabetes Reports 18:132. https://doi.org/10.1007/s11892-018-1102-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Sturtzel C (2017) Endothelial cells. Adv Exp Med Biol 1003:71–91. https://doi.org/10.1007/978-3-319-57613-8_4

    Article  CAS  PubMed  Google Scholar 

  86. Sutra T, Morena M, Bargnoux AS, Caporiccio B, Canaud B, Cristol JP (2008) Superoxide production: a procalcifying cell signalling event in osteoblastic differentiation of vascular smooth muscle cells exposed to calcification media. Free Radic Res 42:789–797. https://doi.org/10.1080/10715760802400766

    Article  CAS  PubMed  Google Scholar 

  87. Tesauro M, Mauriello A, Rovella V, Annicchiarico-Petruzzelli M, Cardillo C, Melino G, Di Daniele N (2017) Arterial ageing: from endothelial dysfunction to vascular calcification. J Intern Med 281:471–482. https://doi.org/10.1111/joim.12605

    Article  CAS  PubMed  Google Scholar 

  88. Thosar SS, Butler MP, Shea SA (2018) Role of the circadian system in cardiovascular disease. J Clin Invest 128:2157–2167. https://doi.org/10.1172/JCI80590

    Article  PubMed  PubMed Central  Google Scholar 

  89. Traish AM, Kypreos KE (2011) Testosterone and cardiovascular disease: an old idea with modern clinical implications. Atherosclerosis 214:244–248. https://doi.org/10.1016/j.atherosclerosis.2010.08.078

    Article  CAS  PubMed  Google Scholar 

  90. Viswambharan H, Carvas JM, Antic V, Marecic A, Jud C, Zaugg CE, Ming XF, Montani JP, Albrecht U, Yang Z (2007) Mutation of the circadian clock gene Per2 alters vascular endothelial function. Circulation 115:2188–2195. https://doi.org/10.1161/circulationaha.106.653303

    Article  CAS  PubMed  Google Scholar 

  91. Voloshyna I, Littlefield MJ, Reiss AB (2014) Atherosclerosis and interferon-gamma: new insights and therapeutic targets. Trends Cardiovasc Med 24:45–51. https://doi.org/10.1016/j.tcm.2013.06.003

    Article  CAS  PubMed  Google Scholar 

  92. Wang CY, Wen MS, Wang HW, Hsieh IC, Li Y, Liu PY, Lin FC, Liao JK (2008) Increased vascular senescence and impaired endothelial progenitor cell function mediated by mutation of circadian gene Per2. Circulation 118:2166–2173. https://doi.org/10.1161/circulationaha.108.790469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Wende AR, Young ME, Chatham J, Zhang J, Rajasekaran NS, Darley-Usmar VM (2016) Redox biology and the interface between bioenergetics, autophagy and circadian control of metabolism. Free Radic Biol Med 100:94–107. https://doi.org/10.1016/j.freeradbiomed.2016.05.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Wittert G (2014) The relationship between sleep disorders and testosterone in men. Asian J Androl 16:262–265. https://doi.org/10.4103/1008-682x.122586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wolf G, Wenzel U, Burns KD, Harris RC, Stahl RA, Thaiss F (2002) Angiotensin II activates nuclear transcription factor-kappaB through AT1 and AT2 receptors. Kidney Int 61:1986–1995. https://doi.org/10.1046/j.1523-1755.2002.00365.x

    Article  CAS  PubMed  Google Scholar 

  96. Wu M, Chen G, Li YP (2016) TGF-beta and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res 4:16009. https://doi.org/10.1038/boneres.2016.9

    Article  PubMed  PubMed Central  Google Scholar 

  97. Wu M, Rementer C, Giachelli CM (2013) Vascular calcification: an update on mechanisms and challenges in treatment. Calcif Tissue Int 93:365–373. https://doi.org/10.1007/s00223-013-9712-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Xing D, Nozell S, Chen YF, Hage F, Oparil S (2009) Estrogen and mechanisms of vascular protection. Arterioscler Thromb Vasc Biol 29:289–295. https://doi.org/10.1161/ATVBAHA.108.182279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Xu X, Wang B, Ren C, Hu J, Greenberg DA, Chen T, Xie L, Jin K (2017) Recent progress in vascular aging: mechanisms and its role in age-related diseases. Aging Dis 8:486–505. https://doi.org/10.14336/ad.2017.0507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Zhu M, Tang H, Tang X, Ma X, Guo D, Chen F (2018) BMAL1 suppresses ROS-induced endothelial-to-mesenchymal transition and atherosclerosis plaque progression via BMP signaling. Am J Transl Res 10:3150–3161

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Data and material availability

Not applicable.

Code availability

Not applicable.

Funding

This work was supported by the National Natural Science Foundation of China [81870506, 81670676, and 81422011], Project of Traditional Chinese Medicine in Guangdong Province [20201062], Basic Research Project of Shenzhen Science and Technology Innovation Committee [JCYJ20180306174648342 and JCYJ20190808102005602], Shenzhen Futian District Public Health Research Project [FTWS2019003], and Shenzhen Key Medical Discipline Construction Fund (SZXK002).

Author information

Author notes

  1. Haoran Huang and Zhaohuai Li contributed equally to this work.

Authors and Affiliations

  1. Department of Cardiology, The Eighth Affiliated Hospital, Sun Yat-sen University, No. 3025, Shennan Middle Road, Futian District, Shenzhen, 518000, China

    Haoran Huang, Zhaohuai Li, Yuyi Ruan, Xiaoxue Li, Liu Ouyang & Hui Huang

  2. Department of Pediatric Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China

    Haoran Huang

  3. State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou, China

    Zhaohuai Li

  4. Department of Nephrology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China

    Yuyi Ruan

  5. Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Department of Cardiology, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou, China

    Weijing Feng, Jie Chen & Liu Ouyang

  6. Department of Cardiology, Laboratory of Heart Center, Zhujiang Hospital, Southern Medical University, Guangzhou, Guangdong, China

    Weijing Feng

Authors
  1. Haoran Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhaohuai Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuyi Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weijing Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoxue Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Liu Ouyang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hui Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. The first draft of the manuscript was written by Haoran Huang and Zhaohuai Li. All authors commented on previous versions of the manuscript and participated in the revision. Hui Huang reviewed the manuscript and made final changes. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hui Huang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Key Points

• The circadian clock can directly regulate the synthetic and secretory function and phenotypic switch of endothelial cells and vascular smooth muscle cells.

• Circadian rhythm disorder is associated with abnormal hormone secretion, oxidative stress, inflammatory reaction, and autophagy.

• Accelerated vascular senescence and abnormal hormone secretion may act as important intermediate factors to promote vascular calcification in circadian rhythm disorders.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, H., Li, Z., Ruan, Y. et al. Circadian rhythm disorder: a potential inducer of vascular calcification?. J Physiol Biochem 76, 513–524 (2020). https://doi.org/10.1007/s13105-020-00767-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13105-020-00767-9

Keywords

Search

Navigation