Glucose-regulated protein 78 inhibits scavenger receptor A-mediated internalization of acetylated low density lipoprotein

Journal of Molecular and Cellular Cardiology

Volumn 47, Issue 5, 2009, Pages 646-655

  Ben, Jingjing ^a   Gao, Song ^a   Zhu, Xudong ^a   Zheng, Yuan ^a   Zhuang, Yan ^a   Bai, Hui ^a   Xu, Yong ^a   Ji, Yong ^a   Sha, Jiahao ^a   He, Zhigang ^b   Chen, Qi ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

6 Aminonicotinamide; Class A scavenger receptor; Fluvastatin; Foam cell formation; Glucose regulated protein 78; Internalization of acetylated LDL; JNK signaling pathway; Macrophages

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; CHOLESTEROL ESTER; FLUINDOSTATIN; GLUCOSE REGULATED PROTEIN 78; SCAVENGER RECEPTOR A; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; BINDING ASSAY; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; FOAM CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LIPID STORAGE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; ANTHRACENES; BIOLOGICAL TRANSPORT; CELL LINE; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPRECIPITATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPROTEINS, LDL; MICE; PROTEIN BINDING; RECEPTORS, SCAVENGER; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 70349728787     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.08.011     Document Type: Article

References (46)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362 (1993) 801-809
2. Hansson G.K., Seifert P.S., Olsson G., and Bondjers G. Immunohistochemical detection of macrophages and T lymphocytes in atherosclerotic lesions of cholesterol-fed rabbits. Arterioscler. Thromb. 11 (1991) 745-750
3. Li A.C., and Glass C.K. The macrophage foam cell as a target for therapeutic intervention. Nat. Med. 8 (2002) 1235-1242
4. Kunjathoor V.V., Febbraio M., Podrez E.A., Moore K.J., Andersson L., Koehn S., et al. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J. Biol. Chem. 277 (2002) 49982-49988
5. Goldstein J.L., Ho Y.K., Basu S.K., and Brown M.S. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 333-337
6. Greaves D.R., and Gordon S. Thematic review series: the immune system and atherogenesis. Recent insights into the biology of macrophage scavenger receptors. J. Lipid Res. 46 (2005) 11-20
7. Mori T., Takahashi K., Naito M., Kodama T., Hakamata H., Sakai M., et al. Endocytic pathway of scavenger receptors via trans-Golgi system in bovine alveolar macrophages. Lab. Invest. 71 (1994) 409-416
8. Chen Y., Wang X., Ben J., Yue S., Bai H., Guan X., et al. The di-leucine motif contributes to class a scavenger receptor-mediated internalization of acetylated lipoproteins. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 1317-1322
9. Fong L.G., and Le D. The processing of ligands by the class A scavenger receptor is dependent on signal information located in the cytoplasmic domain. J. Biol. Chem. 274 (1999) 36808-36816
10. Morimoto K., Wada Y., Hinagata J., Imanishi T., Kodama T., and Doi T. VXFD in the cytoplasmic domain of macrophage scavenger receptors mediates their efficient internalization and cell-surface expression. Biol. Pharm. Bull. 22 (1999) 1022-1026
11. Kosswig N., Rice S., Daugherty A., and Post S.R. Class A scavenger receptor-mediated adhesion and internalization require distinct cytoplasmic domains. J. Biol. Chem. 278 (2003) 34219-34225
12. Sano H., Ishino M., Kramer H., Shimizu T., Mitsuzawa H., Nishitani C., et al. The microtubule-binding protein Hook3 interacts with a cytoplasmic domain of scavenger receptor A. J. Biol. Chem. 282 (2007) 7973-7981
13. Wang X., Zheng Y., Xu Y., Ben J., Gao S., Zhu X., et al. A novel peptide binding to the cytoplasmic domain of class A scavenger receptor reduces lipid uptake in THP-1 macrophages. Biochim. Biophys. Acta 1791 (2009) 76-83
14. Tian G., Wilcockson D., Perry V.H., Rudd P.M., Dwek R.A., Platt F.M., et al. Inhibition of alpha-glucosidases I and II increases the cell surface expression of functional class A macrophage scavenger receptor (SR-A) by extending its half-life. J. Biol. Chem. 279 (2004) 39303-39309
15. Hsu H.Y., Hajjar D.P., Khan K.M., and Falcone D.J. Ligand binding to macrophage scavenger receptor-A induces urokinase-type plasminogen activator expression by a protein kinase-dependent signaling pathway. J. Biol. Chem. 273 (1998) 1240-1246
16. Whitman S.C., Daugherty A., and Post S.R. Regulation of acetylated low density lipoprotein uptake in macrophages by pertussis toxin-sensitive G proteins. J. Lipid Res. 41 (2000) 807-813
17. Hsu H.Y., Chiu S.L., Wen M.H., Chen K.Y., and Hua K.F. Ligands of macrophage scavenger receptor induce cytokine expression via differential modulation of protein kinase signaling pathways. J. Biol. Chem. 276 (2001) 28719-28730
18. Post S.R., Gass C., Rice S., Nikolic D., Crump H., and Post G.R. Class A scavenger receptors mediate cell adhesion via activation of G(i/o) and formation of focal adhesion complexes. J. Lipid Res. 43 (2002) 1829-1836
19. Nakamura T., Suzuki H., Wada Y., Kodama T., and Doi T. Fucoidan induces nitric oxide production via p38 mitogen-activated protein kinase and NF-kappaB-dependent signaling pathways through macrophage scavenger receptors. Biochem. Biophys. Res. Commun. 343 (2006) 286-294
20. Nikolic D.M., Cholewa J., Gass C., Gong M.C., and Post S.R. Class A scavenger receptor-mediated cell adhesion requires the sequential activation of Lyn and PI3-kinase. Am. J. Physiol., Cell Physiol. 292 (2007) C1450-C1458
21. Bonifacino J.S., and Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72 (2003) 395-447
22. Hendershot L.M. The ER function BiP is a master regulator of ER function. Mt. Sinai J. Med. 71 (2004) 289-297
23. Cho D.Y., Yang G.H., Ryu C.J., and Hong H.J. Molecular chaperone GRP78/BiP interacts with the large surface protein of hepatitis B virus in vitro and in vivo. J. Virol. 77 (2003) 2784-2788
24. Basu S.K., Goldstein J.L., Anderson G.W., and Brown M.S. Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 3178-3182
25. Lougheed M., Lum C.M., Ling W., Suzuki H., Kodama T., and Steinbrecher U. High affinity saturable uptake of oxidized low density lipoprotein by macrophages from mice lacking the scavenger receptor class A type I/II. J. Biol. Chem. 272 (1997) 12938-12944
26. Ricci R., Sumara G., Sumara I., Rozenberg I., Kurrer M., Akhmedov A., et al. Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science 306 (2004) 1558-1561
27. Kawano T., Hakamata H., Ohta T., Ding Y., Yoshida M., Ueda S., et al. Inhibitory effects of HepG2 cell-derived apolipoprotein A-I-containing lipoproteins on cholesteryl ester accumulation in macrophages. Biochemistry 36 (1997) 9816-9825
28. Munro S., and Pelham H.R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46 (1986) 291-300
29. Jorgensen M.M., Jensen O.N., Holst H.U., Hansen J.J., Corydon T.J., Bross P., et al. Grp78 is involved in retention of mutant low density lipoprotein receptor protein in the endoplasmic reticulum. J. Biol. Chem. 275 (2000) 33861-33868
30. Chen J.C., Wu M.L., Huang K.C., and Lin W.W. HMG-CoA reductase inhibitors activate the unfolded protein response and induce cytoprotective GRP78 expression. Cardiovasc. Res. 80 (2008) 138-150
31. Luo S., Mao C., Lee B., and Lee A.S. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol. 26 (2006) 5688-5697
32. Dong D., Ni M., Li J., Xiong S., Ye W., Virrey J.J., et al. Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res. 68 (2008) 498-505
33. Dong D., Ko B., Baumeister P., Swenson S., Costa F., Markland F., et al. Vascular targeting and antiangiogenesis agents induce drug resistance effector GRP78 within the tumor microenvironment. Cancer Res. 65 (2005) 5785-5791
34. Misra U.K., Deedwania R., and Pizzo S.V. Binding of activated alpha2-macroglobulin to its cell surface receptor GRP78 in 1-LN prostate cancer cells regulates PAK-2-dependent activation of LIMK. J. Biol. Chem. 280 (2005) 26278-26286
35. Misra U.K., Gonzalez-Gronow M., Gawdi G., Hart J.P., Johnson C.E., and Pizzo S.V. The role of Grp 78 in alpha 2-macroglobulin-induced signal transduction. Evidence from RNA interference that the low density lipoprotein receptor-related protein is associated with, but not necessary for, GRP 78-mediated signal transduction. J. Biol. Chem. 277 (2002) 42082-42087
36. Triantafilou K., Fradelizi D., Wilson K., and Triantafilou M. GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J. Virol. 76 (2002) 633-643
37. Rao R.V., Peel A., Logvinova A., del Rio G., Hermel E., Yokota T., et al. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett. 514 (2002) 122-128
38. Reddy R.K., Mao C., Baumeister P., Austin R.C., Kaufman R.J., and Lee A.S. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J. Biol. Chem. 278 (2003) 20915-20924
39. Qian Y., Zheng Y., Weber D., and Tiffany-Castiglioni E. A 78-kDa glucose-regulated protein is involved in the decrease of interleukin-6 secretion by lead treatment from astrocytes. Am. J. Physiol., Cell. Physiol. 293 (2007) C897-C905
40. Bhattacharjee G., Ahamed J., Pedersen B., El-Sheikh A., Mackman N., Ruf W., et al. Regulation of tissue factor-mediated initiation of the coagulation cascade by cell surface grp78. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1737-1743
41. Shani G., Fischer W.H., Justice N.J., Kelber J.A., Vale W., and Gray P.C. GRP78 and Cripto form a complex at the cell surface and collaborate to inhibit transforming growth factor beta signaling and enhance cell growth. Mol. Cell. Biol. 28 (2008) 666-677
42. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., and Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2 (2000) 326-332
43. Feaver R.E., Hastings N.E., Pryor A., and Blackman B.R. GRP78 upregulation by atheroprone shear stress via p38-, alpha2beta1-dependent mechanism in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1534-1541
44. Liao HS, Kodama T, Geng YJ. Expression of class A scavenger receptor inhibits apoptosis of macrophages triggered by oxidized low density lipoprotein and oxysterol. Arterioscler Thromb Vasc Biol.; 20: 1968-75.
45. Devries-Seimon T., Li Y., Yao P.M., Stone E., Wang Y., Davis R.J., et al. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J. Cell Biol. 171 (2005) 61-73
46. Zhou J., Lhotak S., Hilditch B.A., and Austin R.C. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 111 (2005) 1814-1821