Ursodeoxycholic acid (UDCA) exerts antiatherogenic effects by inhibiting endoplasmic reticulum (ER) stress induced by disturbed flow

Molecules and Cells

Volumn 38, Issue 10, 2015, Pages 851-858

  Chung, Jihwa ^a   Kim, Kyoung Hwa ^a   Lee, Seok Cheol ^a   An, Shung Hyun ^a   Kwon, Kihwan ^a  

^a Ewha Womans University School of Medicine   (South Korea)

Author keywords

Atherosclerosis; Disturbed flow; Endoplasmic reticulum stress; Endothelial cells; Ursodeoxycholic acid

Indexed keywords

CELL ADHESION MOLECULE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; URSODEOXYCHOLIC ACID; X BOX BINDING PROTEIN 1; DDIT3 PROTEIN, MOUSE; DNA BINDING PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; XBP1 PROTEIN, HUMAN; XBP1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIATHEROGENIC ACTIVITY; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BLOOD FLOW; CELL ADHESION; CONTROLLED STUDY; DRUG ACTIVITY; ENDOPLASMIC RETICULUM STRESS; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; INFLAMMATION; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; CELL CULTURE; CIRCULATION; COMMON CAROTID ARTERY; DISEASE MODEL; DOWN REGULATION; DRUG EFFECTS; ENDOPLASMIC RETICULUM; MALE; MECHANICAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PLAQUE, ATHEROSCLEROTIC; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; BLOOD CIRCULATION; CAROTID ARTERY, COMMON; CELL ADHESION; CELL ADHESION MOLECULES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DOWN-REGULATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; MALE; MICE; MONOCYTES; PLAQUE, ATHEROSCLEROTIC; REGULATORY FACTOR X TRANSCRIPTION FACTORS; STRESS, MECHANICAL; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; URSODEOXYCHOLIC ACID; X-BOX BINDING PROTEIN 1;

EID: 84949963906     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2015.0094     Document Type: Article

References (31)

1. Beuers, U., Boyer, J.L., and Paumgartner, G (1998). Ursodeoxycholic acid in cholestasis: Potential mechanisms of action and therapeutic applications. Hepatology 28, 1449-1453.
2. Bucciarelli, L.G, Wendt, T., Qu, W., Lu, Y, Lalla, E., Rong, L.L., Goova, M.T., Moser, B., Kislinger, T., Lee, D.C., et al. (2002). RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation 106, 2827-2835.
3. Chien, S. (2007). Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am. J. Physiol-Heart C 292, H1209-H1224.
4. Chien, S. (2008). Effects of disturbed flow on endothelial cells. Ann. Biomed. Eng. 36, 554-562.
5. Civelek, M., Manduchi, E., Riley, R.J., Stoeckert, C.J., Jr., and Davies, PF. (2009). Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis. Circ. Res. 105, 453-461.
6. Cunningham, K.S., and Gotlieb, A.I. (2005). The role of shear stress in the pathogenesis of atherosclerosis. Lab. Invest. 85, 942-942.
7. Dai, GH., Kaazempur-Mofrad, M.R., Natarajan, S., Zhang, Y.Z., Vaughn, S., Blackman, B.R., Kamm, R.D., Garcia-Cardena, G, and Gimbrone, M.A. (2004). Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis- susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. USA 101, 14871-14876.
8. Feaver, R.E., Hastings, N.E., Pryor, A., and Blackman, B.R. (2008). GRP78 upregulation by atheroprone shear stress via p38-, alpha 2 beta 1-dependent mechanism in endothelial cells. Arterioscl. Throm. Vas. 28, 1534-1541.
9. Gambillara, V., Chambaz, C., Montorzi, G, Roy, S., Stergiopulos, N., and Silacci, P. (2006). Plaque-prone hemodynamics impair endothelial function in pig carotid arteries. Am. J. Physiol. Heart Circ. Physiol. 290, H2320-2328.
10. Gotoh, T., Endo, M., and Oike, Y. (2011). Endoplasmic reticulum stress-related inflammation and cardiovascular diseases. Int. J. Inflamm. 2011, 259462.
11. Ha, C.H., Wang, W., Jhun, B.S., Wong, C., Hausser, A., Pfizenmaier, K., McKinsey, T.A., Olson, E.N., and Jin, Z.G (2008). Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J. Biol. Chem. 283, 14590-14599.
12. Ha, C.H., Kim, S., Chung, J., An, S.H., and Kwon, K. (2013). Extracorporeal shock wave stimulates expression of the angiogenic genes via mechanosensory complex in endothelial cells: Mimetic effect of fluid shear stress in endothelial cells. Int. J. Cardiol. 168, 4168-4177.
13. Heo, K.S., Fujiwara, K., and Abe, J. (2014). Shear stress and atherosclerosis. Mol. Cells 37, 435-440.
14. Hotamisligil, GS. (2010). Endoplasmic reticulum stress and atherosclerosis. Nat. Med. 16, 396-399.
15. Kim, K.M., Pae, H.O., Zheng, M., Park, R., Kim, Y.M., and Chung, H.T. (2007). Carbon monoxide induces heme oxygenase-1 via activation of protein kinase R-like endoplasmic reticulum kinase and inhibits endothelial cell apoptosis triggered by endoplasmic reticulum stress. Circ. Res. 101, 919-927.
16. Kim, S.Y, Kwon, Y.W., Jung, I.L., Sung, J.H., and Park, S.G (2011). Tauroursodeoxycholate (TUDCA) inhibits neointimal hyperplasia by suppression of ERK via PKCalpha-mediated MKP-1 induction. Cardiovasc. Res. 92, 307-316.
17. Lin, J.H., Li, H., Yasumura, D., Cohen, H.R., Zhang, C., Panning, B., Shokat, K.M., LaVail, M.M., and Walter, P. (2007). IRE1 signaling affects cell fate during the unfolded protein response. Science 318, 944-949.
18. Lindor, K. (2007). Ursodeoxycholic acid for the treatment of primary biliary cirrhosis. New Engl. J. Med. 357, 1524-1529.
19. Ma, J., Iida, H., Jo, T., Takano, H., Oonuma, H., Morita, T., Toyo-Oka, T., Omata, M., Nagai, R., Okuda, Y., et al. (2004). Ursodeoxycholic acid inhibits endothelin-1 production in human vascular endothelial cells. Eur. J. Pharmacol. 505, 67-74.
20. Marciniak, S.J., Yun, C.Y., Oyadomari, S., Novoa, I., Zhang, Y.H., Jungreis, R., Nagata, K., Harding, H.P., and Ron, D. (2004). CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Gene Dev. 18, 3066-3077.
21. Nam, D., Ni, C.W., Rezvan, A., Suo, J., Budzyn, K., Llanos, A., Harrison, D., Giddens, D., and Jo, H. (2009). Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am. J. Physiol. Heart Circ. Physiol. 297, H1535-H1543.
22. Passerini, A.G, Polacek, D.C., Shi, C.Z., Francesco, N.M., Manduchi, E., Grant, G.R., Pritchard, W.F., Powell, S., Chang, GY., Stoeckert, C.J., et al. (2004). Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc. Natl. Acad. Sci. USA 101, 2482-2487.
23. Scull, C.M., and Tabas, I. (2011). Mechanisms of ER Stress- Induced Apoptosis in Atherosclerosis. Arterioscl. Throm. Vas. 31, 2792-2797.
24. Tabas, I. (2009). Macrophage apoptosis in atherosclerosis: consequences on plaque progression and the role of endoplasmic reticulum stress. Antioxid. Redox Signal. 11, 2333-2339.
25. Tabas, I. (2010). The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ. Res. 107, 839-850.
26. -/- mice lacking CHOP. Cell Metab. 9, 474-481.
27. Timmins, J.M., Ozcan, L., Seimon, T.A., Li, G, Malagelada, C., Backs, J., Backs, T., Bassel-Duby, R., Olson, E.N., Anderson, M.E., et al. (2009). Calcium/calmodulin-dependent protein kinase II links ER stress with Fas and mitochondrial apoptosis pathways. J. Clin. Invest. 119, 2925-2941.
28. Zeng, L., Zampetaki, A., Margariti, A., Pepe, A.E., Alam, S., Martin, D., Xiao, Q., Wang, W., Jin, Z.G., Cockerill, G., et al. (2009). Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proc. Natl. Acad. Sci. USA 106, 8326-8331.
29. Zhang, K.Z., and Kaufman, R.J. (2008). From endoplasmic- reticulum stress to the inflammatory response. Nature 454, 455-462.
30. Zhou, J., Lhotak, S., Hilditch, B.A., and Austin, R.C. (2005). Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E- deficient mice. Circulation 111, 1814-1821.
31. Zinszner, H., Kuroda, M., Wang, X.Z., Batchvarova, N., Lightfoot, R.T., Remotti, H., Stevens, J.L., and Ron, D. (1998). CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Gene Dev. 12, 982-995.