The Role of Endoplasmic Reticulum Stress-Glycogen Synthase Kinase-3 Signaling in Atherogenesis
Abstract
1. Introduction
2. Atherosclerosis
3. Molecular Mechanisms that Promote Atherosclerosis
4. The Endoplasmic Reticulum (ER) and ER Stress
5. ER Stress and Atherosclerosis
6. Glycogen Synthase Kinase (GSK)-3
7. GSK3 and Atherosclerosis
8. ER Stress Signaling through GSK3α/β
9. Targeting the ER Stress-GSK3α/β Pathway
10. Conclusions
Author Contributions
Acknowledgments
Conflicts of Interest
Abbreviations
ApoE | Apolipoprotein E |
ATF6 | Activating transcription factor 6 |
CHOP | C/EBP homologous protein |
CVD | Cardiovascular disease |
EC | Endothelial cell |
ER | Endoplasmic reticulum |
ERAD | ER stress associated protein degradation |
GSK3α/β | Glycogen synthase kinase 3α/β |
HDL | High-density lipoprotein |
HFD | High fat diet |
IFN γ | Interferon γ |
IL | Interleukin |
IRE1 | Inositol-requiring enzyme-1 |
JAK | Janus kinase |
JNK | c-Jun N-terminal kinase |
LDL | Low-density lipoprotein |
LDLR | Low-density lipoprotein receptor |
MAPK | Mitogen-activated protein kinase |
MMP | Matrix metalloprotease |
NF κB | Nuclear factor κB |
4PBA | 4-phenylbutyrate |
PERK | Protein kinase RNA-like ER kinase |
SREBP | Sterol element binding protein |
STAT | Signal transducer and activator of transcription protein |
Th | T helper cell |
TNFα | Tumor necrosis factor α |
TUDCA | Tauroursodeoxycholic acid |
UPR | Unfolded protein response |
VCAM1 | Viral cell adhesion protein 1 |
VLDL | Very low-density lipoprotein |
VSMC | Vascular smooth muscle cell |
References
- Joseph, P.; Leong, D.; McKee, M.; Anand, S.S.; Schwalm, J.D.; Teo, K.; Mente, A.; Yusuf, S. Reducing the Global Burden of Cardiovascular Disease, Part 1: The Epidemiology and Risk Factors. Circ. Res. 2017, 121, 677–694. [Google Scholar] [CrossRef] [PubMed]
- Grundy, S.M.; Pasternak, R.; Greenland, P.; Smith, S.; Fuster, V. Assessment of Cardiovascular Risk by Use of Multiple-Risk-Factor Assessment Equations. Circulation 1999, 100, 1481–1492. [Google Scholar] [CrossRef] [PubMed]
- Lusis, A.J. Atherosclerosis. Nature 2000, 407, 233–241. [Google Scholar] [CrossRef] [PubMed]
- Zarins, C.K.; Giddens, D.P.; Bharadvaj, B.K.; Sottiurai, V.S.; Mabon, R.F.; Glagov, S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ. Res. 1983, 53, 502–514. [Google Scholar] [CrossRef] [PubMed]
- Cybulsky, M.I.; Iiyama, K.; Li, H.; Zhu, S.; Chen, M.; Iiyama, M.; Davis, V.; Gutierrez-Ramos, J.C.; Connelly, P.W.; Milstone, D.S. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J. Clin. Investig. 2001, 107, 1255–1262. [Google Scholar] [CrossRef] [PubMed]
- Johnson-Tidey, R.R.; McGregor, J.L.; Taylor, P.R.; Poston, R.N. Increase in the adhesion molecule P-selectin in endothelium overlying atherosclerotic plaques. Coexpression with intercellular adhesion molecule-1. Am. J. Pathol. 1994, 144, 952–961. [Google Scholar] [PubMed]
- Stary, H.C.; Chandler, A.B.; Glagov, S.; Guyton, J.R.; Insull, W., Jr.; Rosenfeld, M.E.; Schaffer, S.A.; Schwartz, C.J.; Wagner, W.D.; Wissler, R.W. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1994, 89, 2462–2478. [Google Scholar] [CrossRef] [PubMed]
- Tabas, I.; Bornfeldt, K.E. Macrophage Phenotype and Function in Different Stages of Atherosclerosis. Circ. Res. 2016, 118, 653–667. [Google Scholar] [CrossRef] [PubMed]
- Robbins, C.S.; Hilgendorf, I.; Weber, G.F.; Theurl, I.; Iwamoto, Y.; Figueiredo, J.L.; Gorbatov, R.; Sukhova, G.K.; Gerhardt, L.M.; Smyth, D.; et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat. Med. 2013, 19, 1166–1172. [Google Scholar] [CrossRef] [PubMed]
- Allahverdian, S.; Chehroudi, A.C.; McManus, B.M.; Abraham, T.; Francis, G.A. Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation 2014, 129, 1551–1559. [Google Scholar] [CrossRef] [PubMed]
- Biswas, S.K.; Mantovani, A. Macrophage plasticity and interaction with lymphocyte subsets: Cancer as a paradigm. Nat. Immunol. 2010, 11, 889–896. [Google Scholar] [CrossRef] [PubMed]
- De Paoli, F.; Staels, B.; Chinetti-Gbaguidi, G. Macrophage Phenotypes and Their Modulation in Atherosclerosis. Circ. J. 2014, 78, 1775–1781. [Google Scholar] [CrossRef] [PubMed]
- Adorni, M.P.; Zimetti, F.; Billheimer, J.T.; Wang, N.; Rader, D.J.; Phillips, M.C.; Rothblat, G.H. The roles of different pathways in the release of cholesterol from macrophages. J. Lipid Res. 2007, 48, 2453–2462. [Google Scholar] [CrossRef] [PubMed]
- Van Gils, J.M.; Derby, M.C.; Fernandes, L.R.; Ramkhelawon, B.; Ray, T.D.; Rayner, K.J.; Parathath, S.; Distel, E.; Feig, J.L.; Alvarez-Leite, J.I.; et al. The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques. Nat. Immunol. 2012, 13, 136–143. [Google Scholar] [CrossRef] [PubMed]
- Yao, P.M.; Tabas, I. Free cholesterol loading of macrophages induces apoptosis involving the fas pathway. J. Biol. Chem. 2000, 275, 23807–23813. [Google Scholar] [CrossRef] [PubMed]
- To, K.; Agrotis, A.; Besra, G.; Bobik, A.; Toh, B. NKT Cell Subsets Mediate Differential Proatherogenic Effects in ApoE(−/−) Mice. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 671–677. [Google Scholar] [CrossRef] [PubMed]
- Amorino, G.; Hoover, R. Interactions of monocytic cells with human endothelial cells stimulate monocytic metalloproteinase production. Am. J. Pathol. 1998, 152, 199–207. [Google Scholar] [PubMed]
- Thim, T.; Hagensen, M.K.; Bentzon, J.F.; Falk, E. From vulnerable plaque to atherothrombosis. J. Intern. Med. 2008, 263, 506–516. [Google Scholar] [CrossRef] [PubMed]
- Tabas, I.; Ron, D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 2011, 13, 184–190. [Google Scholar] [CrossRef] [PubMed]
- Tabas, I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ. Res. 2010, 107, 839–850. [Google Scholar] [CrossRef] [PubMed]
- Ron, D.; Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8, 519–529. [Google Scholar] [CrossRef] [PubMed]
- Zinszner, H.; Kuroda, M.; Wang, X.; Batchvarova, N.; Lightfoot, R.T.; Remotti, H.; Stevens, J.L.; Ron, D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998, 12, 982–995. [Google Scholar] [CrossRef] [PubMed]
- Lindholm, D.; Korhonen, L.; Eriksson, O.; Kõks, S. Recent Insights into the Role of Unfolded Protein Response in ER Stress in Health and Disease. Front. Cell Dev. Biol. 2017, 5, 48. [Google Scholar] [CrossRef] [PubMed]
- Hofmann, M.A.; Lalla, E.; Lu, Y.; Gleason, M.R.; Wolf, B.M.; Tanji, N.; Ferran, L.J., Jr.; Kohl, B.; Rao, V.; Kisiel, W.; et al. Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J. Clin. Investig. 2001, 107, 675–683. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Lhotak, S.; Hilditch, B.A.; Austin, R.C. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2005, 111, 1814–1821. [Google Scholar] [CrossRef] [PubMed]
- Khan, M.I.; Pichna, B.A.; Shi, Y.; Bowes, A.J.; Werstuck, G.H. Evidence supporting a role for endoplasmic reticulum stress in the development of atherosclerosis in a hyperglycaemic mouse model. Antioxid. Redox Signal. 2009, 11, 2289–2298. [Google Scholar] [CrossRef] [PubMed]
- Beriault, D.R.; Sharma, S.; Shi, Y.; Khan, M.I.; Werstuck, G.H. Glucosamine-supplementation promotes endoplasmic reticulum stress, hepatic steatosis and accelerated atherogenesis in apoE−/− mice. Atherosclerosis 2011, 219, 134–140. [Google Scholar] [CrossRef] [PubMed]
- Werstuck, G.H.; Lentz, S.R.; Dayal, S.; Shi, Y.; Hossain, G.S.; Sood, S.K.; Krisans, S.K.; Austin, R.C. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J. Clin. Investig. 2001, 107, 1263–1273. [Google Scholar] [CrossRef] [PubMed]
- Ozcan, U.; Cao, Q.; Yilmaz, E.; Lee, A.H.; Iwakoshi, N.N.; Ozdelen, E.; Tuncman, G.; Görgün, C.; Glimcher, L.H.; Hotamisligil, G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306, 457–461. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Schwabe, R.F.; Devries-Seimon, T.; Yao, P.M.; Gerbod-Giannone, M.C.; Tall, A.R.; Davis, R.J.; Flavell, R.; Brenner, D.A.; Tabas, I. Free cholesterol-loaded macrophages are an abundant source of TNF-alpha and IL-6. Model of NF-kappa B- and MAP kinase-dependent inflammation in advanced atherosclerosis. J. Biol. Chem. 2005, 280, 21763–21772. [Google Scholar] [CrossRef] [PubMed]
- Karaskov, E.; Scott, C.; Zhang, L.; Teodoro, T.; Ravazzola, M.; Volchuk, A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 2006, 147, 3398–3407. [Google Scholar] [CrossRef] [PubMed]
- Young, C.N.; Cao, X.; Guruju, M.R.; Pierce, J.P.; Morgan, D.A.; Wang, G.; Iadecola, C.; Mark, A.L.; Davisson, R.L. ER stress in the brain subfornical organ mediates angiotensin-dependent hypertension. J. Clin. Investig. 2012, 122, 3960–3964. [Google Scholar] [CrossRef] [PubMed]
- Somborac-Bacura, A.; van der Toorn, M.; Franciosi, L.; Slebos, D.J.; Zanic-Grubisic, T.; Bischoff, R.; van Oosterhout, A.J. Cigarette smoke induces endoplasmic reticulum stress response and proteasomal dysfunction in human alveolar epithelial cells. Exp. Physiol. 2013, 98, 316–325. [Google Scholar] [CrossRef] [PubMed]
- Myoishi, M.; Hao, H.; Minamino, T.; Watanabe, K.; Nishihira, K.; Hatakeyama, K.; Asada, Y.; Okada, K.; Ishibashi-Ueda, H.; Gabbiani, G.; et al. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation 2007, 116, 1226–1233. [Google Scholar] [CrossRef] [PubMed]
- Thorp, E.; Li, G.; Seimon, T.A.; Kuriakose, G.; Ron, D.; Tabas, I. Reduced Apoptosis and Plaque Necrosis in Advanced Atherosclerotic Lesions of Apoe−/− and Ldlr−/− Mice Lacking CHOP. Cell Metab. 2009, 9, 474–481. [Google Scholar] [CrossRef] [PubMed]
- Ishimura, S.; Furuhashi, M.; Mita, T.; Fuseya, T.; Watanabe, Y.; Hoshina, K.; Kokubu, N.; Inoue, K.; Yoshida, H.; Miura, T. Reduction of endoplasmic reticulum stress inhibits neointima formation after vascular injury. Sci. Rep. 2014, 4, 6943. [Google Scholar] [CrossRef] [PubMed]
- Dong, Y.; Zhang, M.; Liang, B.; Xie, Z.; Zhao, Z.; Asfa, S.; Choi, H.C.; Zou, M.H. Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation 2010, 121, 792–803. [Google Scholar] [CrossRef] [PubMed]
- Huang, A.; Young, T.L.; Dang, V.T.; Shi, Y.; McAlpine, C.S.; Werstuck, G.H. 4-phenylbutyrate and valproate treatment attenuates the progression of atherosclerosis and stabilizes existing plaques. Atherosclerosis 2017, 266, 103–112. [Google Scholar] [CrossRef] [PubMed]
- Dang, V.T.; Beriault, D.R.; Deng, A.; Shi, Y.; Werstuck, G.H. Glucosamine-induced ER stress accelerates atherogenesis: A potential link between diabetes and cardiovascular disease. J. Mol. Genet. Med. 2016, 9, 197. [Google Scholar] [CrossRef]
- Zeng, L.; Lu, M.; Mori, K.; Luo, S.; Lee, A.S.; Zhu, Y.; Shyy, J.Y. ATF6 modulates SREBP2-mediated lipogenesis. EMBO J. 2004, 23, 950–958. [Google Scholar] [CrossRef] [PubMed]
- Colgan, S.M.; Tang, D.; Werstuck, G.H.; Austin, R.C. Endoplasmic reticulum stress activation of sterol regulatory element binding protein-2. Int. J. Biochem. Cell Biol. 2007, 39, 1843–1851. [Google Scholar] [CrossRef] [PubMed]
- Pahl, H.L.; Baeuerle, P.A. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by the transcription factor NF-kappaB. EMBO J. 1995, 14, 2580–2588. [Google Scholar] [PubMed]
- Jiang, H.Y.; Wek, S.A.; McGrath, B.C.; Scheumer, D.; Kaufman, R.J.; Cavener, D.R.; Wek, R.C. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol. Cell Biol. 2003, 23, 5651–5663. [Google Scholar] [CrossRef] [PubMed]
- DeVries-Seimon, T.; Li, Y.; Yao, P.M.; Stone, E.; Wang, Y.; Davis, R.S.; Flavell, R.; Tabas, I. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J. Cell Biol. 2005, 171, 61–73. [Google Scholar] [CrossRef] [PubMed]
- Hossain, G.S.; van Thienen, J.V.; Werstuck, G.H.; Zhou, J.; Sood, S.K.; Dickhout, J.G.; de Koning, A.B.; Tang, D.; Wu, D.; Falk, E.; et al. TDAG51 is induced by homocysteine, promotes detachment-mediated programmed cell death and contributes to the development of atherosclerosis in hyperhomocysteinemia. J. Biol. Chem. 2003, 278, 30317–30327. [Google Scholar] [CrossRef] [PubMed]
- Seimon, T.A.; Obstfeld, A.; Moore, K.J.; Golenbock, D.T.; Tabas, I. Combinatorial pattern recognition receptor signaling alters the balance of life and death in macrophages. Proc. Natl. Acad. Sci. USA 2006, 103, 19794–19799. [Google Scholar] [CrossRef] [PubMed]
- Bowes, A.J.; Khan, M.I.; Shi, Y.Y.; Robertson, L.; Werstuck, G.H. A role for glycogen synthase kinase–3 in endoplasmic reticulum stress-associated lipid accumulation and accelerated atherogenesis in hyperglycemic ApoE-deficient mice. Am. J. Pathol. 2009, 174, 330–342. [Google Scholar] [CrossRef] [PubMed]
- McAlpine, C.S.; Bowes, A.J.; Khan, M.I.; Shi, Y.Y.; Werstuck, G.H. Endoplasmic reticulum stress and glycogen synthase kinase-3β activation in apolipoprotein E-deficient mouse models of accelerated atherosclerosis. Arterioscler. Throm. Vasc. Biol. 2012, 32, 82–91. [Google Scholar] [CrossRef] [PubMed]
- Banko, N.; McAlpine, C.S.; Raja, P.; Shi, Y.; Khan, M.I.; Venegas-Pino, D.E.; Werstuck, G.H. Glycogen Synthase Kinase 3 alpha deficiency protects LDLR knockout mice from high fat diet induced accelerated atherosclerosis. Am. J. Pathol. 2014, 184, 3394–3404. [Google Scholar] [CrossRef] [PubMed]
- Woodgett, J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 1990, 9, 2431–2438. [Google Scholar] [PubMed]
- Phiel, C.J.; Wilson, C.A.; Lee, V.M.-Y.; Klein, P.S. GSK-3α regulates production of Alzheimer’s disease amyloid-β peptides. Nature 2003, 423, 435–439. [Google Scholar] [CrossRef] [PubMed]
- Nikoulina, S.E.; Ciaraldi, T.P.; Mudaliar, S.; Mohideen, P.; Carter, L.; Henry, R.R. Potential role of glycogen synthase kinase-3 in skeletal muscle insulin resistance of type 2 diabetes. Diabetes 2000, 49, 263–271. [Google Scholar] [CrossRef] [PubMed]
- Klein, P.S.; Melton, D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 1996, 93, 8455–8459. [Google Scholar] [CrossRef] [PubMed]
- Sutherland, C. What are the bona fide GSK3 Substrates? Int. J. Alzheimers Dis. 2011, 2011, 505607. [Google Scholar] [PubMed]
- MacAulay, K.; Doble, B.W.; Patel, S.; Hansotia, T.; Sinclair, E.M.; Drucker, D.J.; Nagy, A.; Woodgett, J.R. Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism. Cell Metab. 2007, 6, 329–337. [Google Scholar] [CrossRef] [PubMed]
- Patel, S.; Macaulay, K.; Woodgett, J.R. Tissue-specific analysis of glycogen synthase kinase-3α (GSK-3α) in glucose metabolism: Effect of strain variation. PLoS ONE 2011, 6, e15845. [Google Scholar] [CrossRef] [PubMed]
- Hoeflich, K.P.; Luo, J.; Rubie, E.A.; Tsao, M.S.; Jin, O.; Woodgett, J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000, 406, 86–90. [Google Scholar] [CrossRef] [PubMed]
- Demarchi, F.; Bertoli, C.; Sandy, P.; Schneider, C. Glycogen synthase kinase-3 beta regulates NF-kappa B1/p105 stability. J. Biol. Chem. 2003, 278, 39583–39590. [Google Scholar] [CrossRef] [PubMed]
- Song, L.; De Sarno, P.; Jope, R.S. Central role of glycogen synthase kinase-3beta in endoplasmic reticulum stress-induced caspase-3 activation. J. Biol. Chem. 2002, 277, 44701–44708. [Google Scholar] [CrossRef] [PubMed]
- Baltzis, D.; Pluquet, O.; Papadakis, A.I.; Kazemi, S.; Qu, L.K.; Koromilas, A.E. The eIF2alpha kinases PERK and PKR activate glycogen synthase kinase 3 to promote the proteasomal degradation of p53. J. Biol. Chem. 2007, 282, 31675–31687. [Google Scholar] [CrossRef] [PubMed]
- Qu, L.; Huang, S.; Baltzis, D.; Rivas-Estilla, A.M.; Pluquet, O.; Hatzoglou, M.; Koumenis, C.; Taya, Y.; Yoshimura, A.; Koromilas, A.E. Endoplasmic reticulum stress induces p53 cytoplasmic localization and prevents p53-dependent apoptosis by a pathway involving glycogen synthase kinase-3beta. Genes Dev. 2004, 18, 261–277. [Google Scholar] [CrossRef] [PubMed]
- Ali, A.; Hoeflich, K.P.; Woodgett, J.R. Glycogen Synthase Kinase-3: Properties, Functions, and Regulation. Chem. Rev. 2001, 101, 2527–2540. [Google Scholar] [CrossRef] [PubMed]
- McAlpine, C.S.; Huang, A.; Emdin, A.; Banko, N.S.; Beriault, D.R.; Shi, Y.; Werstuck, G.H. Deletion of myeloid GSK3α attenuates atherosclerosis and promotes an M2 macrophage phenotype. Arterioscler. Thromb. Vasc. Biol. 2015, 35, 1113–1122. [Google Scholar] [CrossRef] [PubMed]
- Beurel, E.; Kaidanovich-Beilin, O.; Yeh, W.I.; Song, L.; Palomo, V.; Michalek, S.M.; Woodgett, J.R.; Harrington, L.E.; Eldar-Finkelman, H.; Martinez, A.; et al. Regulation of Th1 Cells and Experimental Autoimmune Encephalomyelitis by Glycogen Synthase Kinase-3. J. Immunol. 2013, 190, 5000–5011. [Google Scholar] [CrossRef] [PubMed]
- Babaev, V.R.; Yancey, P.G.; Ryzhov, S.V.; Kon, V.; Breyer, M.D.; Magnuson, M.A.; Fazio, S.; Linton, M.F. Conditional Knockout of Macrophage PPAR Increases Atherosclerosis in C57BL/6 and Low-Density Lipoprotein Receptor-Deficient Mice. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 1647–1653. [Google Scholar] [CrossRef] [PubMed]
- Matsuda, T.; Zhai, P.; Maejima, Y.; Hong, C.; Gao, S.; Tian, B.; Goto, K.; Takagi, H.; Tamamori-Adachi, M.; Kitajima, S.; et al. Distinct roles of GSK-3alpha and GSK-3beta phosphorylation in the heart under pressure overload. Proc. Natl. Acad. Sci. USA 2008, 105, 20900–20905. [Google Scholar] [CrossRef] [PubMed]
- Hardt, S.E.; Tomita, H.; Katus, H.A.; Sadoshima, J. Phosphorylation of eukaryotic initiation factor 2Bepsilon by glycogen synthase kinase-3beta regulates beta-adrenergic cardiac myocyte hypertrophy. Circ. Res. 2004, 94, 926–935. [Google Scholar] [CrossRef] [PubMed]
- Badorff, C.; Seeger, F.H.; Zeiher, A.M.; Dimmeler, S. Glycogen synthase kinase 3beta inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation. Circ. Res. 2005, 97, 645–654. [Google Scholar] [CrossRef] [PubMed]
- Kerkela, R.; Kockeritz, L.; Macaulay, K.; Zhou, J.; Doble, B.W.; Beahm, C.; Greytak, S.; Woulfe, K.; Trivedi, C.M.; Woodgett, J.R.; et al. Deletion of GSK-3beta in mice leads to hypertrophic cardiomyopathy secondary to cardiomyoblast hyperproliferation. J. Clin. Investig. 2008, 118, 3609–3618. [Google Scholar] [CrossRef] [PubMed]
- Juhaszova, M.; Zorov, D.B.; Kim, S.H.; Pepe, S.; Fu, Q.; Fishbein, K.W.; Ziman, B.D.; Wang, S.; Ytrehus, K.; Antos, C.L.; et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Investig. 2004, 113, 1535–1549. [Google Scholar] [CrossRef] [PubMed]
- Martin, M.; Rehani, K.; Jope, R.S.; Michalek, S.M. Toll-like receptor–mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 2005, 6, 777–784. [Google Scholar] [CrossRef] [PubMed]
- Beurel, E.; Jope, R.S. Glycogen synthase kinase-3 promotes the synergistic action of interferon-gamma on lipopolysaccharide-induced IL-6 production in RAW264.7 cells. Cell Signal. 2009, 21, 978–985. [Google Scholar] [CrossRef] [PubMed]
- Beurel, E.; Jope, R.S. Differential regulation of STAT family members by glycogen synthase kinase-3. J. Biol. Chem. 2008, 283, 21934–21944. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Devgan, G.; Darnell, J.; Bromberg, J. Constitutively activated Stat3 protects fibroblasts from serum withdrawal and UV-induced apoptosis and antagonizes the proapoptotic effects of activated Stat1. Proc. Natl. Acad. Sci. USA 2001, 98, 1543–1548. [Google Scholar] [CrossRef] [PubMed]
- Ho, H.; Ivashkiv, L. Role of STAT3 in type I interferon responses—Negative regulation of STAT1-dependent inflammatory gene activation. J. Biol. Chem. 2006, 281, 14111–14118. [Google Scholar] [CrossRef] [PubMed]
- McAlpine, C.S.; Werstuck, G.H. Protein kinase R-like endoplasmic reticulum kinase and glycogen synthase kinase-3α/β regulate foam cell formation. J. Lipid Res. 2014, 55, 2320–2333. [Google Scholar] [CrossRef] [PubMed]
- Petri, S.; Kiaei, M.; Kipiani, K.; Chen, J.; Calingasan, N.Y.; Crow, J.P.; Beal, M.F. Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 2006, 22, 40–49. [Google Scholar] [CrossRef] [PubMed]
- Akerfeldt, M.C.; Howes, J.; Chan, J.Y.; Stevens, V.A.; Boubenna, N.; McGuire, H.M.; King, C.; Biden, T.J.; Laybutt, D.R. Cytokine-induced beta-cell death is independent of endoplasmic reticulum stress signaling. Diabetes 2008, 57, 3034–3044. [Google Scholar] [CrossRef] [PubMed]
- Özcan, L.; Ergin, A.S.; Lu, A.; Chung, J.; Sarkar, S.; Nie, D.; Myers, M.G.Jr.; Özcan, U. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 2009, 9, 35–51. [Google Scholar] [CrossRef] [PubMed]
- Özcan, U.; Yilmaz, E.; Özcan, L.; Furuhashi, M.; Vaillancourt, E.; Smith, R.O.; Görgün, C.Z.; Hotamisligil, G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313, 1137–1140. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.; Bowes, R.C., 3rd; van de Water, B.; Sillence, C.; Nagelkerke, J.F.; Stevens, J.L. Endoplasmic reticulum chaperones GRP78 and calreticulin prevent oxidative stress, Ca2+ disturbances, and cell death in renal epithelial cells. J. Biol. Chem. 2007, 272, 21751–21759. [Google Scholar] [CrossRef]
- Kudo, T.; Kanemoto, S.; Hara, H.; Morimoto, N.; Morihara, T.; Kimura, R.; Tabira, T.; Imaizumi, K.; Takeda, M. A molecular chaperone inducer protects neurons from ER stress. Cell Death Differ. 2008, 15, 364–375. [Google Scholar] [CrossRef] [PubMed]
- Choi, S.E.; Jang, H.J.; Kang, Y.; Jung, J.G.; Han, S.J.; Kim, H.J.; Kim, D.J.; Lee, K.W. Atherosclerosis induced by a high-fat diet is alleviated by lithium chloride via reduction of VCAM expression in ApoE-deficient mice. Vascul. Pharmacol. 2010, 53, 264–272. [Google Scholar] [CrossRef] [PubMed]
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Huang, A.; Patel, S.; McAlpine, C.S.; Werstuck, G.H. The Role of Endoplasmic Reticulum Stress-Glycogen Synthase Kinase-3 Signaling in Atherogenesis. Int. J. Mol. Sci. 2018, 19, 1607. https://doi.org/10.3390/ijms19061607
Huang A, Patel S, McAlpine CS, Werstuck GH. The Role of Endoplasmic Reticulum Stress-Glycogen Synthase Kinase-3 Signaling in Atherogenesis. International Journal of Molecular Sciences. 2018; 19(6):1607. https://doi.org/10.3390/ijms19061607
Chicago/Turabian StyleHuang, Aric, Sarvatit Patel, Cameron S. McAlpine, and Geoff H. Werstuck. 2018. "The Role of Endoplasmic Reticulum Stress-Glycogen Synthase Kinase-3 Signaling in Atherogenesis" International Journal of Molecular Sciences 19, no. 6: 1607. https://doi.org/10.3390/ijms19061607
APA StyleHuang, A., Patel, S., McAlpine, C. S., & Werstuck, G. H. (2018). The Role of Endoplasmic Reticulum Stress-Glycogen Synthase Kinase-3 Signaling in Atherogenesis. International Journal of Molecular Sciences, 19(6), 1607. https://doi.org/10.3390/ijms19061607