Oxidized LDL (oxLDL) activates the angiotensin II type 1 receptor by binding to the lectin-like oxLDL receptor

FASEB Journal

Volumn 29, Issue 8, 2015, Pages 3342-3356

  Yamamoto, Koichi ^a   Kakino, Akemi ^b,c,d   Takeshita, Hikari ^a,d   Hayashi, Norihiro ^a   Li, Lei ^b   Nakano, Atsushi ^b   Hanasaki Yamamoto, Hiroko ^a   Fujita, Yoshiko ^b   Imaizumi, Yuki ^a   Toyama Yokoyama, Serina ^a   Nakama, Chikako ^a   Kawai, Tatsuo ^a   Takeda, Masao ^a   Hongyo, Kazuhiro ^a   Oguro, Ryosuke ^a   Maekawa, Yoshihiro ^a   Itoh, Norihisa ^a   Takami, Yoichi ^a   Onishi, Miyuki ^a   Takeya, Yasushi ^a   Sugimoto, Ken ^a   Kamide, Kei ^a   Nakagami, Hironori ^c   Ohishi, Mitsuru ^a   Kurtz, Theodore W ^e   Sawamura, Tatsuya ^b,c,d   Rakugi, Hiromi ^a   more..

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Allosteric activation; G protein coupled receptor; Receptor multimerization; Vascular dysfunction

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; LECTIN; OXIDIZED LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR;

ALLOSTERISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR DISEASE; CELL MEMBRANE; CELL SURFACE; CHO CELL LINE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOASSAY; IMMUNOPRECIPITATION; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROXIMITY LIGATION ASSAY; SIGNAL TRANSDUCTION; THORACIC AORTA; VASCULAR ENDOTHELIUM; VASCULAR RING; VASODILATATION; ANIMAL; CELL LINE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; CRICETULUS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CRICETULUS GRISEUS;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETULUS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; LECTINS; LIPOPROTEINS, LDL; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTORS, OXIDIZED LDL; SIGNAL TRANSDUCTION;

EID: 84940118205     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-271627     Document Type: Article

References (51)

1. Steinberg, D. (1997) Low density lipoprotein oxidation and its pathobiological significance. J. Biol. Chem. 272, 20963-20966
2. Inoue, K., Arai, Y., Kurihara, H., Kita, T., and Sawamura, T. (2005) Overexpression of lectin-like oxidized low-density lipoprotein receptor-1 induces intramyocardial vasculopathy in apolipoprotein E-null mice. Circ. Res. 97, 176-184
3. Mehta, J. L., Chen, J., Hermonat, P. L., Romeo, F., and Novelli, G. (2006) Lectin-like, oxidized low-density lipoprotein receptor-1 (LOX-1): a critical player in the development of atherosclerosis and related disorders. Cardiovasc. Res. 69, 36-45
4. Mehta, J. L., Sanada, N., Hu, C. P., Chen, J., Dandapat, A., Sugawara, F., Satoh, H., Inoue, K., Kawase, Y., Jishage, K., Suzuki, H., Takeya, M., Schnackenberg, L., Beger, R., Hermonat, P. L., Thomas, M., and Sawamura, T. (2007) Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ. Res. 100, 1634-1642
5. Sawamura, T., Kume, N., Aoyama, T., Moriwaki, H., Hoshikawa, H., Aiba, Y., Tanaka, T., Miwa, S., Katsura, Y., Kita, T., and Masaki, T. (1997) An endothelial receptor for oxidized low-density lipoprotein. Nature 386, 73-77
6. Dunn, S., Vohra, R. S., Murphy, J. E., Homer-Vanniasinkam, S., Walker, J. H., and Ponnambalam, S. (2008) The lectin-like oxidized low-density-lipoprotein receptor: a pro-inflammatory factor in vascular disease. Biochem. J. 409, 349-355
7. Nickenig, G., and Harrison, D. G. (2002) The AT (1)-type angiotensin receptor in oxidative stress and atherogenesis: part I: oxidative stress and atherogenesis. Circulation 105, 393-396
8. Nickenig, G., and Harrison, D. G. (2002) The AT (1)-type angiotensin receptor in oxidative stress and atherogenesis: Part II: AT (1) receptor regulation. Circulation 105, 530-536
9. Morawietz, H., Rueckschloss, U., Niemann, B., Duerrschmidt, N., Galle, J., Hakim, K., Zerkowski, H. R., Sawamura, T., and Holtz, J. (1999) Angiotensin II induces LOX-1, the human endothelial receptor for oxidized low-density lipoprotein. Circulation 100, 899-902
10. Li, D., Saldeen, T., Romeo, F., and Mehta, J. L. (2000) Oxidized LDL upregulates angiotensin II type 1 receptor expression in cultured human coronary artery endothelial cells: the potential role of transcription factor NF-kappaB. Circulation 102, 1970-1976
11. Wang, X., Khaidakov, M., Guo, Z., Ding, Z., He, Q., and Mehta, J. L. (2014) LOX-1 deletion limits cardiac angiogenesis in mice given angiotensin II. Cardiovasc. Drugs Ther. 28, 441-446
12. Griendling, K. K., Minieri, C. A., Ollerenshaw, J. D., and Alexander, R. W. (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74, 1141-1148
13. Heinloth, A., Heermeier, K., Raff, U., Wanner, C., and Galle, J. (2000) Stimulation of NADPH oxidase by oxidized low-density lipoprotein induces proliferation of human vascular endothelial cells. J. Am. Soc. Nephrol. 11, 1819-1825
14. Nakano, A., Inoue, N., Sato, Y., Nishimichi, N., Takikawa, K., Fujita, Y., Kakino, A., Otsui, K., Yamaguchi, S., Matsuda, H., and Sawamura, T. (2010) LOX-1 mediates vascular lipid retention under hypertensive state. J. Hypertens. 28, 1273-1280
15. Fujita, Y., Kakino, A., Nishimichi, N., Yamaguchi, S., Sato, Y., Machida, S., Cominacini, L., Delneste, Y., Matsuda, H., and Sawamura, T. (2009) Oxidized LDL receptor LOX-1 binds to Creactive protein and mediates its vascular effects. Clin. Chem. 55, 285-294
16. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000
17. Iwamoto, S., Fujita, Y., Kakino, A., Yanagida, K., Matsuda, H., Yoshimoto, R., and Sawamura, T. (2011) An alternative protein standard to measure activity of LOX-1 ligand containing apoB (LAB)-utilization of anti-LOX-1 single-chain antibody fused to apoB fragment. J. Atheroscler. Thromb. 18, 818-828
18. Aoyama, T., Sawamura, T., Furutani, Y., Matsuoka, R., Yoshida, M. C., Fujiwara, H., and Masaki, T. (1999) Structure and chromosomal assignment of thehumanlectin-likeoxidized low-density-lipoprotein receptor-1 (LOX-1) gene. Biochem. J. 339, 177-184
19. Babnigg, G., Zagranichnaya, T., Wu, X., and Villereal, M. L. (2003) Differential tyrosine phosphorylation of plasma membrane Ca2+-ATPase and regulation of calcium pump activity by carbachol and bradykinin. J. Biol. Chem. 278, 14872-14882
20. Tanigawa, H., Miura, S., Zhang, B., Uehara, Y., Matsuo, Y., Fujino, M., Sawamura, T., and Saku, K. (2006) Low-density lipoprotein oxidized to various degrees activates ERK1/2 through Lox-1. Atherosclerosis 188, 245-250
21. Suc, I., Meilhac, O., Lajoie-Mazenc, I., Vandaele, J., Jürgens, G., Salvayre, R., and Nègre-Salvayre, A. (1998) Activation of EGF receptor by oxidized LDL. FASEB J. 12, 665-671
22. Li, D., and Mehta, J. L. (2000) Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of human coronary artery endothelial cells: evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arterioscler. Thromb. Vasc. Biol. 20, 1116-1122
23. Eguchi, S., Dempsey, P. J., Frank, G. D., Motley, E. D., and Inagami, T. (2001) Activation of MAPKs by angiotensin II in vascular smooth muscle cells. Metalloprotease-dependent EGF receptor activation is required for activation of ERKand p38MAPKbut not for JNK. J. Biol. Chem. 276, 7957-7962
24. Lanctot, P. M., Leclerc, P. C., Clément, M., Auger-Messier, M., Escher, E., Leduc, R., and Guillemette, G. (2005) Importance of Nglycosylation positioning for cell-surface expression, targeting, affinity and quality control of the human AT1 receptor. Biochem. J. 390, 367-376
25. Li, D., Liu, L., Chen, H., Sawamura, T., Ranganathan, S., and Mehta, J. L. (2003) LOX-1 mediates oxidized low-density lipoproteininduced expression of matrix metalloproteinases in human coronary artery endothelial cells. Circulation 107, 612-617
26. Weisser, B., Locher, R., Mengden, T., and Vetter, W. (1992) Oxidation of low density lipoprotein enhances its potential to increase intracellular free calciumconcentration in vascular smooth muscle cells. Arterioscler. Thromb. 12, 231-236
27. Wettschureck, N., and Offermanns, S. (2005) Mammalian G proteins and their cell type specific functions. Physiol. Rev. 85, 1159-1204
28. Ohki, I., Ishigaki, T., Oyama, T., Matsunaga, S., Xie, Q., Ohnishi-Kameyama, M., Murata, T., Tsuchiya, D., Machida, S., Morikawa, K., and Tate, S. (2005) Crystal structure of human lectinlike, oxidized low-density lipoprotein receptor 1 ligand binding domain and its ligand recognition mode to OxLDL. Structure 13, 905-917
29. Greenberg, J. I., Shields, D. J., Barillas, S. G., Acevedo, L. M., Murphy, E., Huang, J., Scheppke, L., Stockmann, C., Johnson, R. S., Angle, N., and Cheresh, D. A. (2008) A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 456, 809-813
30. Hermanz-Falcón, P., Arce, I., Roda-Navarro, P., and Fernández-Ruiz, E. (2001) Cloning of human DECTIN-1, a novel C-type lectin-like receptor gene expressed on dendritic cells. Immunogenetics 53, 288-295
31. Brown, G. D. (2006) Dectin-1: a signalling non-TLR patternrecognition receptor. Nat. Rev. Immunol. 6, 33-43
32. Haendeler, J., Ishida, M., Hunyady, L., and Berk, B. C. (2000) The third cytoplasmic loop of the angiotensin II type 1 receptor exerts differential effects on extracellular signal-regulated kinase (ERK1/ERK2) and apoptosis via Ras- and Rap1-dependent pathways. Circ. Res. 86, 729-736
33. Zhang, M., Zhao, X., Chen, H. C., Catt, K. J., and Hunyady, L. (2000) Activation of the AT1 angiotensin receptor is dependent on adjacent apolar residues in the carboxyl terminus of the third cytoplasmic loop. J. Biol. Chem. 275, 15782-15788
34. Cominacini, L., Pasini, A. F., Garbin, U., Davoli, A., Tosetti, M. L., Campagnola, M., Rigoni, A., Pastorino, A. M., Lo Cascio, V., and Sawamura, T. (2000) Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cells induces the activation of NF-kappaB through an increased production of intracellular reactive oxygen species. J. Biol. Chem. 275, 12633-12638
35. Jing, Q., Xin, S. M., Cheng, Z. J., Zhang, W. B., Zhang, R., Qin, Y. W., and Pei, G. (1999) Activation of p38 mitogen-activated proteinkinase by oxidized LDL in vascular smooth muscle cells: mediation via pertussis toxin-sensitive G proteins and association with oxidized LDL-induced cytotoxicity. Circ. Res. 84, 831-839
36. Kusuhara, M., Chait, A., Cader, A., and Berk, B. C. (1997) Oxidized LDL stimulates mitogen-activated protein kinases in smooth muscle cells and macrophages. Arterioscler. Thromb. Vasc. Biol. 17, 141-148
37. Mazière, C., Alimardani, G., Dantin, F., Dubois, F., Conte, M. A., and Mazière, J. C. (1999) Oxidized LDL activates STAT1 and STAT3 transcription factors: possible involvement of reactive oxygen species. FEBS Lett. 448, 49-52
38. Auge, N., Garcia, V., Maupas-Schwalm, F., Levade, T., Salvayre, R., and Negre-Salvayre, A. (2002) Oxidized LDL-induced smooth muscle cell proliferation involves the EGF receptor/PI-3 kinase/Akt and the sphingolipid signaling pathways. Arterioscler. Thromb. Vasc. Biol. 22, 1990-1995
39. Besler, C., Heinrich, K., Rohrer, L., Doerries, C., Riwanto, M., Shih, D. M., Chroni, A., Yonekawa, K., Stein, S., Schaefer, N., Mueller, M., Akhmedov, A., Daniil, G., Manes, C., Templin, C., Wyss, C., Maier, W., Tanner, F. C., Matter, C. M., Corti, R., Furlong, C., Lusis, A. J., von Eckardstein, A., Fogelman, A. M., Lüscher, T. F., and Landmesser, U. (2011) Mechanisms underlying adverse effects of HDL on eNOS-activating pathways in patients with coronary artery disease. J. Clin. Invest. 121, 2693-2708
40. Daugherty, A., Rateri, D. L., Lu, H., Inagami, T., and Cassis, L. A. (2004) Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the AT1A receptor. Circulation 110, 3849-3857
41. Wassmann, S., Czech, T., van Eickels, M., Fleming, I., Böhm, M., and Nickenig, G. (2004) Inhibition of diet-induced atherosclerosis and endothelial dysfunction in apolipoprotein E/angiotensin II type 1A receptor double-knockout mice. Circulation 110, 3062-3067
42. Patel, T. B. (2004) Single transmembrane spanning heterotrimeric Gprotein-coupled receptors and their signaling cascades. Pharmacol. Rev. 56, 371-385
43. Erb, L., Liu, J., Ockerhausen, J., Kong, Q., Garrad, R. C., Griffin, K., Neal, C., Krugh, B., Santiago-Pérez, L. I., González, F. A., Gresham, H. D., Turner, J. T., and Weisman, G. A. (2001) An RGD sequence in the P2Y (2) receptor interacts with alpha (V) beta (3) integrins and is required for G (o)-mediated signal transduction. J. Cell Biol. 153, 491-501
44. Kumar, A., Humphreys, T. D., Kremer, K. N., Bramati, P. S., Bradfield, L., Edgar, C. E., and Hedin, K. E. (2006) CXCR4physically associates with the T cell receptor to signal in T cells. Immunity 25, 213-224
45. McLatchie, L. M., Fraser, N. J., Main, M. J., Wise, A., Brown, J., Thompson, N., Solari, R., Lee, M. G., and Foord, S. M. (1998) RAMPs regulate the transport and ligand specificity of the calciton in receptor like receptor. Nature 393, 333-339
46. Rozenfeld, R., and Devi, L. A. (2010) Recept or heteromerization and drug discovery. Trends Pharmacol. Sci. 31, 124-130
47. Oliveira, L., Costa-Neto, C. M., Nakaie, C. R., Schreier, S., Shimuta, S. I., and Paiva, A. C. (2007) The angiotensin II AT1 receptor structure-activity correlations in the light of rhodopsin structure. Physiol. Rev. 87, 565-592
48. Miura, S., Kiya, Y., Kanazawa, T., Imaizumi, S., Fujino, M., Matsuo, Y., Karnik, S. S., and Saku, K. (2008) Differential bonding interactions of inverse agonists of angiotensin II type 1 receptor in stabilizing the inactive state. Mol. Endocrinol. 22, 139-146
49. Zou, Y., Akazawa, H., Qin, Y., Sano, M., Takano, H., Minamino, T., Makita, N., Iwanaga, K., Zhu, W., Kudoh, S., Toko, H., Tamura, K., Kihara, M., Nagai, T., Fukamizu, A., Umemura, S., Iiri, T., Fujita, T., and Komuro, I. (2004) Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat. Cell Biol. 6, 499-506
50. Miura, S., Fujino, M., Hanzawa, H., Kiya, Y., Imaizumi, S., Matsuo, Y., Tomita, S., Uehara, Y., Karnik, S. S., Yanagisawa, H., Koike, H., Komuro, I., and Saku, K. (2006) Molecular mechanism underlying inverse agonist of angiotensin II type 1 receptor. J. Biol. Chem. 281, 19288-19295
51. Tanigawa, H., Miura, S., Matsuo, Y., Fujino, M., Sawamura, T., and Saku, K. (2006) Dominant-negative lox-1 blocks homodimerization of wild-type lox-1-induced cell proliferation through extracellular signal regulated kinase 1/2 activation. Hypertension 48, 294-300