LOX-1 augments oxLDL uptake by lysoPC-stimulated murine macrophages but is not required for oxLDL clearance from plasma

Journal of Lipid Research

Volumn 50, Issue 8, 2009, Pages 1676-1684

  Schaeffer, David F ^a   Riazy, Maziar ^a   Parhas, Kuljit S ^a   Chen, Johnny H ^a   Duronio, Vincent ^a   Sawamura, Tatsuya ^b   Steinbrecher, Urs P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

Apoptosis; Lysophosphatidycholine; Macrophage; Oxidized low density lipoprotein; Scavenger receptor

Indexed keywords

CYTOKINE; LYSOPHOSPHATIDYLCHOLINE; OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PROTEIN KINASE B; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; OLR1 PROTEIN, MOUSE; STEAROYL ALPHA LYSOLECITHIN; STEAROYL ALPHA-LYSOLECITHIN;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CELL ISOLATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; IMMUNOBLOTTING; KNOCKOUT MOUSE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN MODIFICATION; RECEPTOR INTRINSIC ACTIVITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOUSE MUTANT; OXIDATION REDUCTION REACTION; PERITONEUM MACROPHAGE; PHENOTYPE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION REGULATION; LIPOPROTEINS, LDL; LYSOPHOSPHATIDYLCHOLINES; MACROPHAGES; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDATION-REDUCTION; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SCAVENGER RECEPTORS, CLASS E;

EID: 69449088984     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M900167-JLR200     Document Type: Article

References (53)

1. Moriwaki, H., N. Kume, T. Sawamura, T. Aoyama, H. Hoshikawa, H. Ochi, E. Nishi, T. Masaki, and T. Kita. 1998. Ligand specificity of LOX-1, a novel endothelial receptor for oxidized low density lipoprotein. Arterioscler. Thromb. Vasc. Biol. 18: 1541-1547.
2. Chen, M., T. Masaki, and T. Sawamura. 2002. LOX-1, the receptor for oxidized low-density lipoprotein identified from endothelial cells: implications in endothelial dysfunction and atherosclerosis. Pharmacol. Ther. 95: 89-100.
3. Sawamura, T., N. Kume, T. Aoyama, H. Moriwaki, H. Hoshikawa, Y. Aiba, T. Tanaka, S. Miwa, Y. Katsura, T. Kita, et al. 1997. An endothelial receptor for oxidized low-density lipoprotein. Nature. 386: 73-77.
4. Cominacini, L., A. F. Pasini, U. Garbin, A. Davoli, M. L. Tosetti, M. Campagnola, A. Rigoni, A. M. Pastorino, V. Lo Cascio, and T. Sawamura. 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.
5. Cominacini, L., A. Rigoni, A. F. Pasini, U. Garbin, A. Davoli, M. Campagnola, A. M. Pastorino, V. Lo Cascio, and T. Sawamura. 2001. The binding of oxidized low density lipoprotein (ox-LDL) to ox-LDL receptor-1 reduces the intracellular concentration of nitric oxide in endothelial cells through an increased production of superoxide. J. Biol. Chem. 276: 13750-13755.
6. Li, D., and J. Mehta. 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.
7. Kataoka, H., N. Kume, S. Miyamoto, M. Minami, H. Moriwaki, T. Murase, T. Sawamura, T. Masaki, N. Hashimoto, and T. Kita. 1999. Expression of lectinlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation. 99: 3110-3117.
8. Chen, C. H., W. Jiang, D. P. Via, S. Luo, T. R. Li, Y. T. Lee, and P. D. Henry. 2000. Oxidized low-density lipoproteins inhibit endothelial cell proliferation by suppressing basic fibroblast growth factor expression. Circulation. 101: 171-177.
9. Mehta, J. L., N. Sanada, C. P. Hu, J. Chen, A. Dandapat, F. Sugawara, H. Satoh, K. Inoue, Y. Kawase, K. Jishage, et al. 2007. Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ. Res. 100: 1634-1642.
10. Kataoka, H., N. Kume, S. Miyamoto, M. Minami, M. Morimoto, K. Hayashida, N. Hashimoto, and T. Kita. 2001. Oxidized LDL modulates Bax/Bcl-2 through the lectinlike Ox-LDL receptor-1 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 21: 955-960.
11. Greaves, D. R., and S. Gordon. 2005. Thematic review series: The immune system and atherogenesis. Recent insights into the biology of macrophage scavenger receptors. J. Lipid Res. 46: 11-20.
12. Lougheed, M., C. Ming Lum, W. Ling, H. Suzuki, T. Kodama, and U. P. Steinbrecher. 1997. 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: 12938-12944.
13. Kunjathoor, V. V., M. Febbraio, E. A. Podrez, K. J. Moore, L. Andersson, S. Koehn, J. S. Rhee, R. Silverstein, H. F. Hoff, and M. W. Freeman. 2002. 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: 49982-49988.
14. Yoshida, H., N. Kondratenko, S. Green, D. Steinberg, and O. Quehenberger. 1998. Identification of the lectin-like receptor for oxidized low-density lipoprotein in human macrophages and its potential role as a scavenger receptor. Biochem. J. 334: 9-13.
15. Hundal, R., B. Salh, J. Schrader, A. Gómez-Muñoz, V. Duronio, and U. Steinbrecher. 2001. Oxidized low density lipoprotein inhibits macrophage apoptosis through activation of the PI 3-kinase/PKB pathway. J. Lipid Res. 42: 1483-1491.
16. Hundal, R., A. Gómez-Muñoz, J. Kong, B. Salh, A. Marotta, V. Duronio, and U. Steinbrecher. 2003. Oxidized low density lipoprotein inhibits macrophage apoptosis by blocking ceramide generation, thereby maintaining PKB activation and Bcl-XL levels. J. Biol. Chem. 278: 24399-24408.
17. Martens, J., M. Lougheed, A. Gomez-Muñoz, and U. Steinbrecher. 1999. A modification of apolipoprotein B accounts for most of the induction of macrophage growth by oxidized low density lipoprotein. J. Biol. Chem. 274: 10903-10910.
18. Matsunaga, T., S. Hokari, I. Koyama, T. Harada, and T. Komoda. 2003. NF-kappa B activation in endothelial cells treated with oxidized high-density lipoprotein. Biochem. Biophys. Res. Commun. 303: 313-319.
19. Havel, R. J., H. A. Eder, and J. H. Bragdon. 1955. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 43: 1345-1353.
20. Bilheimer, D. W., S. Eisenberg, and R. I. Levy. 1972. The metabolism of very low density lipoproteins. Biochim. Biophys. Acta. 260: 212-221.
21. Steinbrecher, U. P. 1987. Oxidation of human low density lipoproteins results in derivatization of lysine residues of apolipoprotein B by lipid peroxide decomposition products. J. Biol. Chem. 262: 3603-3608.
22. Zhang, H., Y. Yang, and U. P. Steinbrecher. 1993. Structural requirements for the binding of modified proteins to the scavenger receptor of macrophages. J. Biol. Chem. 268: 5535-5542.
23. Hamilton, J. A., D. Myers, W. Jessup, F. Cochrane, R. Byrne, G. Whitty, and S. Moss. 1999. Oxidized LDL can induce macrophage survival, DNA synthesis, and enhanced proliferative response to CSF-1 and GM-CSF. Arterioscler. Thromb. Vasc. Biol. 19: 98-105.
24. Pitas, R. E., T. L. Innerarity, J. N. Weinstein, and R. W. Mahley. 1981. Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis. 1: 177-185.
25. Ling, W., M. Lougheed, H. Suzuki, A. Buchan, T. Kodama, and U. Steinbrecher. 1997. Oxidized or acetylated low density lipoprotein are rapidly cleared by the liver in mice with disruption of the scavenger receptor class A type I/type II gene. J. Clin. Invest. 100: 244-252.
26. Martens, J., N. Reiner, P. Herrera-Velit, and U. Steinbrecher. 1998. Phosphatidylinositol 3-kinase is involved in the induction of macrophage growth by oxidized low density lipoprotein. J. Biol. Chem. 273: 4915-4920.
27. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
28. Stephan, Z., and E. Yurachek. 1993. Rapid fluorometric assay of LDL receptor activity by DiI-labelled LDL. J. Lipid Res. 34: 325-330.
29. Aoyama, T., H. Fujiwara, T. Masaki, and T. Sawamura. 1999. Induction of lectin-like oxidized LDL receptor by oxidized LDL and lysophosphatidylcholine in cultured endothelial cells. J. Mol. Cell. Cardiol. 31: 2101-2114.
30. Aoyama, T., M. Chen, H. Fujiwara, T. Masaki, and T. Sawamura. 2000. LOX-1 mediates lysophosphatidylcholine-induced oxidized LDL uptake in smooth muscle cells. FEBS Lett. 467: 217-220.
31. Kakutani, M., M. Ueda, T. Naruko, T. Masaki, and T. Sawamura. 2001. Accumulation of LOX-1 ligand in plasma and atherosclerotic lesions of Watanabe heritable hyperlipidemic rabbits: identification by a novel enzyme immunoassay. Biochem. Biophys. Res. Commun. 282: 180-185.
32. Smirnova, I. V., M. Kajstura, T. Sawamura, and M. S. Goligorsky. 2004. Asymmetric dimethylarginine upregulates LOX-1 in activated macrophages: role in foam cell formation. Am. J. Physiol. Heart Circ. Physiol. 287: H782-H790.
33. Lougheed, M., and U. P. Steinbrecher. 1996. Mechanism of uptake of copper-oxidized low density lipoprotein in macrophages is dependent on its extent of oxidation. J. Biol. Chem. 271: 11798-11805.
34. Kume, N., H. Moriwaki, H. Kataoka, M. Minami, T. Murase, T. Sawamura, T. Masaki, and T. Kita. 2000. Inducible expression of LOX-1, a novel receptor for oxidized LDL, in macrophages and vascular smooth muscle cells. Ann. N. Y. Acad. Sci. 902: 323-327.
35. Draude, G., and R. L. Lorenz. 2000. TGF-beta1 downregulates CD36 and scavenger receptor A but upregulates LOX-1 in human macrophages. Am. J. Physiol. Heart Circ. Physiol. 278: H1042-H1048.
36. Tabas, I. 2005. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler. Thromb. Vasc. Biol. 25: 2255-2264.
37. Salomonsson, L., S. Pettersson, M. C. Englund, O. Wiklund, and B. G. Ohlsson. 2002. Post-transcriptional regulation of VEGF expression by oxidised LDL in human macrophages. Eur. J. Clin. Invest. 32: 767-774.
38. Claus, R., B. Fyrnys, H. P. Deigner, and G. Wolf. 1996. Oxidized low-density lipoprotein stimulates protein kinase C (PKC) and induces expression of PKC-isotypes via prostaglandin-H-synthase in P388D1 macrophage-like cells. Biochemistry. 35: 4911-4922.
39. Li, D., L. Liu, H. Chen, T. Sawamura, and J. L. Mehta. 2003. LOX-1, an oxidized LDL endothelial receptor, induces CD40/CD40L signaling in human coronary artery endothelial cells. Arterioscler. Thromb. Vasc. Biol. 23: 816-821.
40. Li, D., L. Liu, H. Chen, T. Sawamura, S. Ranganathan, and J. L. Mehta. 2003. LOX-1 mediates oxidized low-density lipoprotein-induced expression of matrix metalloproteinases in human coronary artery endothelial cells. Circulation. 107: 612-617.
41. Iwai-Kanai, E., K. Hasegawa, T. Sawamura, M. Fujita, T. Yanazume, S. Toyokuni, S. Adachi, Y. Kihara, and S. Sasayama. 2001. Activation of lectin-like oxidized low-density lipoprotein receptor-1 induces apoptosis in cultured neonatal rat cardiac myocytes. Circulation. 104: 2948-2954.
42. Li, D., and J. L. Mehta. 2000. Antisense to LOX-1 inhibits oxidized LDL-mediated upregulation of monocyte chemoattractant protein-1 and monocyte adhesion to human coronary artery endothelial cells. Circulation. 101: 2889-2895.
43. Imanishi, T., T. Hano, T. Sawamura, S. Takarada, and I. Nishio. 2002. Oxidized low density lipoprotein potentiation of Fas-induced apoptosis through lectin-like oxidized-low density lipoprotein receptor-1 in human umbilical vascular endothelial cells. Circ. J. 66: 1060-1064.
44. Nakagawa, T., T. Yasuda, H. Hoshikawa, M. Shimizu, T. Kakinuma, M. Chen, T. Masaki, T. Nakamura, and T. Sawamura. 2002. LOX-1 expressed in cultured rat chondrocytes mediates oxidized LDL-induced cell death-possible role of dephosphorylation of Akt. Biochem. Biophys. Res. Commun. 299: 91-97.
45. Steinbrecher, U. P., A. Gomez-Munoz, and V. Duronio. 2004. Acid sphingomyelinase in macrophage apoptosis. Curr. Opin. Lipidol. 15: 531-537.
46. Fadok, V. A., D. Xue, and P. Henson. 2001. If phosphatidylserine is the death knell, a new phosphatidylserine-specific receptor is the bellringer. Cell Death Differ. 8: 582-587.
47. Delerive, P., C. Furman, E. Teissier, J. Fruchart, P. Duriez, and B. Staels. 2000. Oxidized phospholipids activate PPARalpha in a phospholipase A2-dependent manner. FEBS Lett. 471: 34-38.
48. Lee, H., W. Shi, P. Tontonoz, S. Wang, G. Subbanagounder, C. C. Hedrick, S. Hama, C. Borromeo, R. M. Evans, J. A. Berliner, et al. 2000. Role for peroxisome proliferator-activated receptor alpha in oxidized phospholipid-induced synthesis of monocyte chemotactic protein-1 and interleukin-8 by endothelial cells. Circ. Res. 87: 516-521.
49. Nagy, L., P. Tontonoz, J. Alvarez, H. Chen, and R. Evans. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARg. Cell. 93: 229-240.
50. Davies, S. S., A. V. Pontsler, G. K. Marathe, K. A. Harrison, R. C. Murphy, J. C. Hinshaw, G. D. Prestwich, A. S. Hilaire, S. M. Prescott, G. A. Zimmerman, et al. 2001. Oxidized alkyl phospholipids are specific, high affinity peroxisome proliferator-activated receptor gamma ligands and agonists. J. Biol. Chem. 276: 16015-16023.
51. Pontsler, A. V., A. St Hilaire, G. K. Marathe, G. A. Zimmerman, and T. M. McIntyre. 2002. Cyclooxygenase-2 is induced in monocytes by peroxisome proliferator activated receptor gamma and oxidized alkyl phospholipids from oxidized low density lipoprotein. J. Biol. Chem. 277: 13029-13036.
52. Miller, Y. I., S. Viriyakosol, C. J. Binder, J. R. Feramisco, T. N. Kirkland, and J. L. Witztum. 2003. Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J. Biol. Chem. 278: 1561-1568.
53. Stanton, L. W., R. T. White, C. M. Bryant, A. A. Protter, and G. Endemann. 1992. A macrophage Fc receptor for IgG is also a receptor for oxidized low density lipoprotein. J. Biol. Chem. 267: 22446-22451.