Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Hippo: A New Hub for Atherosclerotic Disease

Author(s): Xi-Yan Liu, Kun Zhou, Kai-Jiang Tian, Bin-Jie Yan, Zhong Ren, Zhi-Xiang Zhou, Wen-Hao Xiong and Zhi-Sheng Jiang*

Volume 28, Issue 16, 2022

Published on: 02 June, 2022

Page: [1321 - 1328] Pages: 8

DOI: 10.2174/1381612828666220428090540

Price: $65

Abstract

Hippo, an evolutionarily conserved kinase cascade reaction in organisms, can respond to a set of signals, such as mechanical signals and cell metabolism, to maintain cell growth, differentiation, tissue/organ development, and homeostasis. In the past ten years, Hippo has controlled the development of tissues and organs by regulating the process of cell proliferation, especially in the field of cardiac regeneration after myocardial infarction. This suggests that Hippo signaling is closely linked to cardiovascular disease. Atherosclerosis is the most common disease of the cardiovascular system. It is characterised by chronic inflammation of the vascular wall, mainly involving dysfunction of endothelial cells, smooth muscle cells, and macrophages. Oxidized Low density lipoprotein (LDL) damages the barrier function of endothelial cells, which enter the middle membrane of the vascular wall, accelerate the formation of foam cells, and promote the occurrence and development of atherosclerosis. Autophagy is associated with the development of atherosclerosis. However, the mechanism of Hippo regulation of atherosclerosis has not meant to be clarified. In view of the pivotal role of this signaling pathway in maintaining cell growth, proliferation, and differentiation, the imbalance of Hippo is related to atherosclerosis and related diseases. In this review, we emphasized Hippo as a hub for regulating atherosclerosis and discussed its potential targets in pathophysiology, human diseases, and related pharmacology.

Keywords: Hippo, endothelial cell, macrophages, smooth muscle cells, lipid metabolism, autophagy.

« Previous Next »
[1]
Flinn MA, Link BA, O’Meara CC. Upstream regulation of the Hippo-YAP pathway in cardiomyocyte regeneration. Semin Cell Dev Biol 2020; 100: 11-9.
[http://dx.doi.org/10.1016/j.semcdb.2019.09.004] [PMID: 31606277]
[2]
Yu Y, Su X, Qin Q, et al. Yes-associated protein and transcriptional coactivator with PDZ-binding motif as new targets in cardiovascular diseases. Pharmacol Res 2020; 159: 105009.
[http://dx.doi.org/10.1016/j.phrs.2020.105009] [PMID: 32553712]
[3]
Liu D, Lv H, Liu Q, et al. Atheroprotective effects of methotrexate via the inhibition of YAP/TAZ under disturbed flow. J Transl Med 2019; 17(1): 378.
[http://dx.doi.org/10.1186/s12967-019-02135-8] [PMID: 31730006]
[4]
Wang KC, Yeh YT, Nguyen P, et al. Flow-dependent YAP/TAZ activities regulate endothelial phenotypes and atherosclerosis. Proc Natl Acad Sci USA 2016; 113: 11525-30.
[http://dx.doi.org/10.1073/pnas.1613121113]
[5]
Xu S, Xu Y, Liu P, et al. The novel coronary artery disease risk gene JCAD/KIAA1462 promotes endothelial dysfunction and atherosclerosis. Eur Heart J 2019; 40(29): 2398-408.
[http://dx.doi.org/10.1093/eurheartj/ehz303] [PMID: 31539914]
[6]
Mohajan S, Jaiswal PK, Vatanmakarian M, et al. Hippo pathway: Regulation, deregulation and potential therapeutic targets in cancer. Cancer Lett 2021; 507: 112-23.
[http://dx.doi.org/10.1016/j.canlet.2021.03.006] [PMID: 33737002]
[7]
Wu Z, Guan KL. Hippo signaling in embryogenesis and development. Trends Biochem Sci 2021; 46(1): 51-63.
[http://dx.doi.org/10.1016/j.tibs.2020.08.008] [PMID: 32928629]
[8]
Yin F, Dong J, Kang LI, Liu X. Hippo-YAP signaling in digestive system tumors. Am J Cancer Res 2021; 11(6): 2495-507.
[PMID: 34249412]
[9]
Cho YS, Jiang J. Hippo-independent regulation of YKI/YAP/TAZ: A non-canonical view. Front Cell Dev Biol 2021; 9: 658481.
[http://dx.doi.org/10.3389/fcell.2021.658481] [PMID: 33869224]
[10]
Ouyang T, Meng W, Li M, et al. Recent advances of the Hippo/YAP signaling pathway in brain development and glioma. Cell Mol Neurobiol 2020; 40(4): 495-510.
[11]
Truong HQ, Lieber S, Najera E, Alves-Belo JT, Gardner PA, Fernandez-Miranda JC. The medial wall of the cavernous sinus. Part 1: Surgical anatomy, ligaments, and surgical technique for its mobilization and/or resection. J Neurosurg 2018; 131(1): 122-30.
[http://dx.doi.org/10.3171/2018.3.JNS18596] [PMID: 30192192]
[12]
Kim W, Kim M, Jho EH. Wnt/β-catenin signalling: From plasma membrane to nucleus. Biochem J 2013; 450(1): 9-21.
[http://dx.doi.org/10.1042/BJ20121284] [PMID: 23343194]
[13]
Gong R, Hong AW, Plouffe SW, et al. Opposing roles of conventional and novel PKC isoforms in Hippo-YAP pathway regulation. Cell Res 2015; 25(8): 985-8.
[http://dx.doi.org/10.1038/cr.2015.88] [PMID: 26206313]
[14]
Wang W, Xiao ZD, Li X, et al. AMPK modulates Hippo pathway activity to regulate energy homeostasis. Nat Cell Biol 2015; 17(4): 490-9.
[http://dx.doi.org/10.1038/ncb3113] [PMID: 25751139]
[15]
Enzo E, Santinon G, Pocaterra A, et al. Aerobic glycolysis tunes YAP/TAZ transcriptional activity. EMBO J 2015; 34(10): 1349-70.
[http://dx.doi.org/10.15252/embj.201490379] [PMID: 25796446]
[16]
Mo JS, Meng Z, Kim YC, et al. Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat Cell Biol 2015; 17(4): 500-10.
[http://dx.doi.org/10.1038/ncb3111] [PMID: 25751140]
[17]
Koo JH, Guan KL. Interplay between YAP/TAZ and metabolism. Cell Metab 2018; 28(2): 196-206.
[http://dx.doi.org/10.1016/j.cmet.2018.07.010] [PMID: 30089241]
[18]
Nakajima H, Yamamoto K, Agarwala S, et al. Flow-dependent endothelial YAP regulation contributes to vessel maintenance. Dev Cell 2017; 40(6): 523-536.e6.
[http://dx.doi.org/10.1016/j.devcel.2017.02.019] [PMID: 28350986]
[19]
Wang L, Luo JY, Li B, et al. Integrin-YAP/TAZ-JNK cascade mediates atheroprotective effect of unidirectional shear flow. Nature 2016; 540(7634): 579-82.
[http://dx.doi.org/10.1038/nature20602] [PMID: 27926730]
[20]
Komarova YA, Kruse K, Mehta D, Malik AB. Protein interactions at endothelial junctions and signaling mechanisms regulating endothelial permeability. Circ Res 2017; 120(1): 179-206.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.306534] [PMID: 28057793]
[21]
Fan X, Shan X, Jiang S, et al. YAP promotes endothelial barrier repair by repressing STAT3/VEGF signaling. Life Sci 2020; 256: 117884.
[http://dx.doi.org/10.1016/j.lfs.2020.117884] [PMID: 32502546]
[22]
Kim J, Kim YH, Kim J, et al. YAP/TAZ regulates sprouting angiogenesis and vascular barrier maturation. J Clin Invest 2017; 127(9): 3441-61.
[http://dx.doi.org/10.1172/JCI93825] [PMID: 28805663]
[23]
Choi H-J, Kim N-E, Kim BM, et al. TNF-α-induced YAP/TAZ activity mediates leukocyte-endothelial adhesion by regulating VCAM1 expression in endothelial cells. Int J Mol Sci 2018; 19(11): 3428.
[http://dx.doi.org/10.3390/ijms19113428]
[24]
Testai L, Brancaleone V, Flori L, Montanaro R, Calderone V. Modulation of EndMT by hydrogen sulfide in the prevention of cardiovascular fibrosis. Antioxidants 2021; 10(6): 910.
[http://dx.doi.org/10.3390/antiox10060910] [PMID: 34205197]
[25]
Zhao H, Liu M, Liu H, Suo R, Lu C. Naringin protects endothelial cells from apoptosis and inflammation by regulating the Hippo-YAP Pathway. Biosci Rep 2020; 40(3): BSR20193431.
[http://dx.doi.org/10.1042/BSR20193431] [PMID: 32091090]
[26]
Ling HH, Kuo CC, Lin BX, Huang YH, Lin CW. Elevation of YAP promotes the epithelial-mesenchymal transition and tumor aggressiveness in colorectal cancer. Exp Cell Res 2017; 350(1): 218-25.
[http://dx.doi.org/10.1016/j.yexcr.2016.11.024] [PMID: 27914787]
[27]
Chen H, Chen Q, Luo Q. Expression of netrin-1 by hypoxia contributes to the invasion and migration of prostate carcinoma cells by regulating YAP activity. Exp Cell Res 2016; 349(2): 302-9.
[http://dx.doi.org/10.1016/j.yexcr.2016.10.023] [PMID: 27815019]
[28]
Lv H, Ai D. Hippo/yes-associated protein signaling functions as a mechanotransducer in regulating vascular homeostasis. J Mol Cell Cardiol 2022; 162(162): 158-65.
[http://dx.doi.org/10.1016/j.yjmcc.2021.09.007] [PMID: 34547259]
[29]
Yuan P, Hu Q, He X, et al. Laminar flow inhibits the Hippo/YAP pathway via autophagy and SIRT1-mediated deacetylation against atherosclerosis. Cell Death Dis 2020; 11(2): 141.
[http://dx.doi.org/10.1038/s41419-020-2343-1] [PMID: 32081881]
[30]
Taniguchi K, Wu LW, Grivennikov SI, et al. A gp130-Src-YAP module links inflammation to epithelial regeneration. Nature 2015; 519(7541): 57-62.
[http://dx.doi.org/10.1038/nature14228] [PMID: 25731159]
[31]
Song K, Kwon H, Han C, et al. Yes-associated protein in kupffer cells enhances the production of proinflammatory cytokines and promotes the development of nonalcoholic steatohepatitis. Hepatology 2020; 72(1): 72-87.
[http://dx.doi.org/10.1002/hep.30990] [PMID: 31610032]
[32]
Jia J, Zhang H, He L, Zhang H, Shu M. Cutaneous neurofibroma cells with active YAP promotes proliferation of macrophages resulting in increased accumulation of macrophages by modulating CCL5 and TGF β1. Oncol Rep 2020; 43(4): 1319-30.
[http://dx.doi.org/10.3892/or.2020.7513] [PMID: 32323813]
[33]
Guo X, Zhao Y, Yan H, et al. Single tumor-initiating cells evade immune clearance by recruiting type II macrophages. Genes Dev 2017; 31(3): 247-59.
[http://dx.doi.org/10.1101/gad.294348.116] [PMID: 28223311]
[34]
Yang K, Xu J, Fan M, et al. Lactate suppresses macrophage pro-inflammatory response to lps stimulation by inhibition of YAP and NF-κB activation via GPR81-mediated signaling. Front Immunol 2020; 11: 587913.
[http://dx.doi.org/10.3389/fimmu.2020.587913] [PMID: 33123172]
[35]
Liu M, Yan M, Lv H, et al. Macrophage K63-linked ubiquitination of YAP promotes its nuclear localization and exacerbates atherosclerosis. Cell Rep 2020; 32(5): 107990.
[http://dx.doi.org/10.1016/j.celrep.2020.107990] [PMID: 32755583]
[36]
Mia MM, Cibi DM, Ghani ASAB, et al. YAP/TAZ deficiency reprograms macrophage phenotype and improves infarct healing and cardiac function after myocardial infarction. PLoS Biol 2020; 18(12): e3000941.
[http://dx.doi.org/10.1371/journal.pbio.3000941] [PMID: 33264286]
[37]
Xin Zhou X, Li W, Wang S, et al. YAP aggravates IBD via regulating M1/M2 macrophage polarization and gut microbial homeostasis. Cell Rep 2019; 27(4): 1176-89.e5.
[38]
Li C, Jin Y, Zei S, et al. Hippo signaling controls NLRP3 Activation and governs immunoregulation of mesenchymal stem cells in mouse liver injury. Hepatology 2019; 70(5): 1714-31.
[http://dx.doi.org/10.1002/hep.30700] [PMID: 31063235]
[39]
Kimura TE, Duggirala A, Smith MC, et al. The Hippo pathway mediates inhibition of vascular smooth muscle cell proliferation by cAMP. J Mol Cell Cardiol 2016; 90: 1-10.
[http://dx.doi.org/10.1016/j.yjmcc.2015.11.024] [PMID: 26625714]
[40]
Xiao J, Jin K, Wang J, et al. Conditional knockout of TFPI-1 in VSMCs of mice accelerates atherosclerosis by enhancing AMOT/YAP pathway. Int J Cardiol 2017; 228: 605-14.
[http://dx.doi.org/10.1016/j.ijcard.2016.11.195] [PMID: 27875740]
[41]
Liu M, Yu T, Li M, et al. Apoptosis repressor with caspase recruitment domain promotes cell proliferation and phenotypic modulation through 14-3-3ε/YAP signaling in vascular smooth muscle cells. J Mol Cell Cardiol 2020; 147: 35-48.
[42]
Wang L, Qiu P, Jiao J, et al. Yes-associated protein inhibits transcription of myocardin and attenuates differentiation of vascular smooth muscle cell from cardiovascular progenitor cell lineage. Stem Cells 2017; 35(2): 351-61.
[http://dx.doi.org/10.1002/stem.2484] [PMID: 27571517]
[43]
Wang Y, Cao W, Cui J, et al. Arterial wall stress induces phenotypic switching of arterial smooth muscle cells in vascular remodeling by activating the YAP/TAZ signaling pathway. Cell Physiol Biochem 2018; 51(2): 842-53.
[http://dx.doi.org/10.1159/000495376] [PMID: 30466081]
[44]
Huang C, Zhao J, Zhu Y. Drug-eluting stent targeting Sp-1-attenuated restenosis by engaging YAP-mediated vascular smooth muscle cell phenotypic modulation. J Am Heart Assoc 2020; 9(1): e014103.
[http://dx.doi.org/10.1161/JAHA.119.014103] [PMID: 31880978]
[45]
Li H, Jiang W, Ren W, et al. Downregulation of the yes-associated protein is associated with extracellular matrix disorders in ascending aortic aneurysms. Stem Cells Int 2016; 2016: 6786184.
[http://dx.doi.org/10.1155/2016/6786184] [PMID: 26904131]
[46]
Liu T, Xu J, Guo JL, et al. YAP1 up-regulation inhibits apoptosis of aortic dissection vascular smooth muscle cells. Eur Rev Med Pharmacol Sci 2017; 21(20): 4632-9.
[PMID: 29131252]
[47]
Shi Y, Liu B, Wang CS, et al. MST1 down-regulation in decreasing apoptosis of aortic dissection smooth muscle cell apoptosis. Eur Rev Med Pharmacol Sci 2018; 22(7): 2044-51.
[48]
Wang P, Gong Y, Guo T, et al. Activation of aurora A kinase increases YAP stability via blockage of autophagy. Cell Death Dis 2019; 10(6): 432.
[http://dx.doi.org/10.1038/s41419-019-1664-4] [PMID: 31160567]
[49]
Lin J, Zhang L, Zhang M, et al. Mst1 inhibits CMECs autophagy and participates in the development of diabetic coronary microvascular dysfunction. Sci Rep 2016; 6: 34199.
[http://dx.doi.org/10.1038/srep34199] [PMID: 27680548]
[50]
Wang D, He J, Huang B, Liu S, Zhu H, Xu T. Emerging role of the Hippo pathway in autophagy. Cell Death Dis 2020; 11(10): 880.
[http://dx.doi.org/10.1038/s41419-020-03069-6] [PMID: 33082313]
[51]
Pavel M, Renna M, Park SJ, et al. Contact inhibition controls cell survival and proliferation via YAP/TAZ-autophagy axis. Nat Commun 2018; 9(1): 2961.
[http://dx.doi.org/10.1038/s41467-018-05388-x] [PMID: 30054475]
[52]
Fitzgibbons TP, Czech MP. Emerging evidence for beneficial macrophage functions in atherosclerosis and obesity-induced insulin resistance. J Mol Med (Berl) 2016; 94(3): 267-75.
[http://dx.doi.org/10.1007/s00109-016-1385-4] [PMID: 26847458]
[53]
Hu J, Liu T, Zhang Z, et al. Oxidized low‐density lipoprotein promotes vascular endothelial cell dysfunction by stimulating miR‐496 expression and inhibiting the Hippo pathway effector YAP. Cell Biol Int 43(5): 528-38.
[http://dx.doi.org/10.1002/cbin.11120]
[54]
Xu K, Zhao H, Qiu X, Liu X, Zhao F, Zhao Y. VGLL4 protects against oxidized-LDL-induced endothelial cell dysfunction and inflammation by activating Hippo-YAP/TEAD1 signaling pathway. Mediators Inflamm 2020; 2020(1): 8292173.
[http://dx.doi.org/10.1155/2020/8292173] [PMID: 33456372]
[55]
Chan P, Han X, Zheng B, et al. Autopalmitoylation of TEAD proteins regulates transcriptional output of the Hippo pathway. Nat Chem Biol 2016; 12(4): 282-9.
[http://dx.doi.org/10.1038/nchembio.2036] [PMID: 26900866]
[56]
Yuan L, Mao Y, Luo W, et al. Palmitic acid dysregulates the Hippo-YAP pathway and inhibits angiogenesis by inducing mitochondrial damage and activating the cytosolic DNA sensor cGAS-STING-IRF3 signaling mechanism. J Biol Chem 2017; 292(36): 15002-15.
[http://dx.doi.org/10.1074/jbc.M117.804005] [PMID: 28698384]
[57]
Jones PD, Kaiser MA, Maryam GN, et al. JCAD gene at the 10p11 coronary artery disease locus regulates Hippo signaling in endothelial cells. Arter Thromb Vasc Biol 2018; 38: 8.
[58]
Choi HJ, Zhang H, Park H, et al. Yes-associated protein regulates endothelial cell contact-mediated expression of angiopoietin-2. Nat Commun 2015; 6: 6943.
[http://dx.doi.org/10.1038/ncomms7943] [PMID: 25962877]
[59]
Shao D, Zhai P, Del Re DP, et al. A functional interaction between Hippo-YAP signalling and FoxO1 mediates the oxidative stress response. Nat Commun 2014; 5: 3315.
[http://dx.doi.org/10.1038/ncomms4315] [PMID: 24525530]
[60]
Matsuda T, Zhai P, Sciarretta S, et al. NF2 activates Hippo signaling and promotes ischemia/reperfusion injury in the heart. Circ Res 2016; 119(5): 596-606.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.308586] [PMID: 27402866]
[61]
Noland CL, Gierke S, Schnier PD, et al. Palmitoylation of TEAD transcription factors is required for their stability and function in Hippo pathway signaling. Structure 2016; 24(1): 179-86.
[http://dx.doi.org/10.1016/j.str.2015.11.005] [PMID: 26724994]
[62]
Wu P, Liu Z, Zhao T, et al. Lovastatin attenuates angiotensin II induced cardiovascular fibrosis through the suppression of YAP/TAZ signaling. Biochem Biophys Res Commun 2019; 512(4): 736-41.
[http://dx.doi.org/10.1016/j.bbrc.2019.03.158] [PMID: 30926167]

Rights & Permissions Print Cite
Article Metrics
21
1
© 2024 Bentham Science Publishers | Privacy Policy