ABCA1 promotes the efflux of bacterial LPS from macrophages and accelerates recovery from LPS-induced tolerance

Journal of Lipid Research

Volumn 51, Issue 9, 2010, Pages 2672-2685

  Thompson, Patricia A ^a   Gauthier, Karine C ^a,b,c   Varley, Alan W ^a   Kitchens, Richard L ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

Apolipoprotein; ATP binding cassette transporter A1; Cytokine; Endotoxin; Gene reprogramming; Immunosuppression; Inflammation; Lipopolysaccharide; Signaling

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN E; BACTERIUM LIPOPOLYSACCHARIDE;

ANIMAL CELL; ARTICLE; CARBOHYDRATE TRANSPORT; CELL SURFACE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; LIPOGENESIS; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; WILD TYPE;

EID: 77956811488     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M007435     Document Type: Article

References (56)

1. Tang, C., and J. F. Oram. 2009. The cell cholesterol exporter ABCA1 as a protector from cardiovascular disease and diabetes. Biochim. Biophys. Acta. 1791: 563-572.
2. Yvan-Charvet, L., N. Wang, and A. R. Tall. 2010. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 30: 139-143.
3. Francone, O. L., L. Royer, G. Boucher, M. Haghpassand, A. Freeman, D. Brees, and R. J. Aiello. 2005. Increased cholesterol deposition, expression of scavenger receptors, and response to chemotactic factors in Abca1-deficient macrophages. Arterioscler. Thromb. Vasc. Biol. 25: 1198-1205.
4. Koseki, M., K. I. Hirano, D. Masuda, C. Ikegami, M. Tanaka, A. Ota, J. C. Sandoval, Y. Nakagawa-Toyama, S. B. Sato, T. Kobayashi et al. 2007. Increased lipid rafts and accelerated lipopolysaccharide-induced tumor necrosis factor-{alpha} secretion in Abca1-deficient macrophages. J. Lipid Res. 48: 299-306.
5. Yvan-Charvet, L., C. Welch, T. A. Pagler, M. Ranalletta, M. Lamkanfi, S. Han, M. Ishibashi, R. Li, N. Wang, and A. R. Tall. 2008. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation. 118: 1837-1847.
6. Zhu, X., J-Y. Lee, J. M. Timmins, J. M. Brown, E. Boudyguina, A. Mulya, A. K. Gebre, M. C. Willingham, E. M. Hiltbold, N. Mishra, et al. 2008. Increased cellular free cholesterol in macrophagespecific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283: 22930-22941.
7. Baldan, A., A. V. Gomes, P. Ping, and P. A. Edwards. 2008. Loss of ABCG1 results in chronic pulmonary inflammation. J. Immunol. 180: 3560-3568.
8. Repa, J. J., S. D. Turley, J-M. A. Lobaccaro, J. Medina, L. Li, K. Lustig, B. Shan, R. A. Heyman, J. M. Dietschy, and D. J. Mangelsdorf. 2000. Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science. 289: 1524-1529.
9. Laffitte, B. A., J. J. Repa, S. B. Joseph, D. C. Wilpitz, H. R. Kast, D. J. Mangelsdorf, and P. Tontonoz. 2001. LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl. Acad. Sci. USA. 98: 507-512.
10. Oram, J. F., R. M. Lawn, M. R. Garvin, and D. P. Wade. 2000. ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J. Biol. Chem. 275: 34508-34511.
11. Rubic, T., and R. L. Lorenz. 2006. Downregulated CD36 and ox- LDL uptake and stimulated ABCA1/G1 and cholesterol efflux as anti-atherosclerotic mechanisms of interleukin-10. Cardiovasc. Res. 69: 527-535.
12. Panousis, C. G., G. Evans, and S. H. Zuckerman. 2001. TGF-{beta} increases cholesterol efflux and ABC-1 expression in macrophagederived foam cells: opposing the effects of IFN-{{gamma}}. J. Lipid Res. 42: 856-863.
13. Gerbod-Giannone, M. C., Y. Li, A. Holleboom, S. Han, L. C. Hsu, I. Tabas, and A. R. Tall. 2006. TNF{alpha} induces ABCA1 through NF-{kappa}B in macrophages and in phagocytes ingesting apoptotic cells. Proc. Natl. Acad. Sci. USA. 103: 3112-3117.
14. Kaplan, R., X. Gan, J. G. Menke, S. D. Wright, and T. Q. Cai. 2002. Bacterial lipopolysaccharide induces expression of ABCA1 but not ABCG1 via an LXR-independent pathway. J. Lipid Res. 43: 952-959.
15. Baranova, I., T. Vishnyakova, A. Bocharov, C. Zhigang, A. T. Remaley, J. Stonick, T. L. Eggerman, and A. P. Patterson. 2002. Lipopolysaccharide down regulates both scavenger receptor B1 and ATP binding cassette transporter A1 in RAW cells. Infect. Immun. 70: 2995-3003.
16. Khovidhunkit, W., A. H. Moser, J. K. Shigenaga, C. Grunfeld, and K. R. Feingold. 2003. Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J. Lipid Res. 44: 1728-1736.
17. Castrillo, A., S. B. Joseph, S. A. Vaidya, M. Haberland, A. M. Fogelman, G. Cheng, and P. Tontonoz. 2003. Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol. Cell. 12: 805-816.
18. Maitra, U., J. S. Parks, and L. Li. 2009. An innate immunity signaling process suppresses macrophage ABCA1 expression through IRAK-1-mediated downregulation of retinoic acid receptor {alpha} and NFATc2. Mol. Cell. Biol. 29: 5989-5997.
19. Schumann, R. R., S. R. Leong, G. W. Flaggs, P. W. Gray, S. D. Wright, J. C. Mathison, P. S. Tobias, and R. J. Ulevitch. 1990. Structure and function of lipopolysaccharide-binding protein. Science. 249: 1429-1431.
20. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 249: 1431-1433.
21. Haziot, A., E. Ferrero, F. Köntgen, N. Hijiya, S. Yamamoto, J. Silver, C. L. Stewart, and S. M. Goyert. 1997. Resistance to endotoxin shock and reduced dissemination of gram-negative bacteria in CD14-deficient mice. Immunity. 4: 407-414.
22. Poltorak, A., X. He, I. Smirnova, M-Y. H. C. Liu, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, M. Freudenberg, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 282: 2085-2088.
23. Nagai, Y., S. Akashi, M. Nagafuku, M. Ogata, Y. Iwakura, S. Akira, T. Kitamura, A. Kosugi, M. Kimoto, and K. Miyake. 2002. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat. Immunol. 3: 667-672.
24. Foster, S. L., and R. Medzhitov. 2009. Gene-specific control of the TLR-induced inflammatory response. Clin. Immunol. 130: 7-15.
25. Biswas, S. K., and E. Lopez-Collazo. 2009. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30: 475-487.
26. Foster, S. L., D. C. Hargreaves, and R. Medzhitov. 2007. Genespecifi c control of inflammation by TLR-induced chromatin modi- fications. Nature. 447: 972-978.
27. Lu, M., M. Zhang, R. L. Kitchens, S. Fosmire, A. Takashima, and R. S. Munford. 2003. Stimulus-dependent deacylation of bacterial lipopolysaccharide by dendritic cells. J. Exp. Med. 197: 1745-1754.
28. Lu, M., A. W. Varley, S. Ohta, J. Hardwick, and R. S. Munford. 2008. Host inactivation of bacterial lipopolysaccharide prevents prolonged tolerance following gram-negative bacterial infection. Cell Host Microbe. 4: 293-302.
29. Lu, M., M. Zhang, A. Takashima, J. Weiss, M. A. Apicella, X. H. Li, D. Yuan, and R. S. Munford. 2005. Lipopolysaccharide deacylation by an endogenous lipase controls innate antibody responses to Gram-negative bacteria. Nat. Immunol. 6: 989-994.
30. Shao, B., M. Lu, S. C. Katz, A. W. Varley, J. Hardwick, T. E. Rogers, N. Ojogun, D. C. Rockey, R. P. DeMatteo, and R. S. Munford. 2007. A host lipase detoxifies bacterial lipopolysaccharides in the liver and spleen. J. Biol. Chem. 282: 13726-13735.
31. Kitchens, R. L., G. Wolfbauer, J. J. Albers, and R. S. Munford. 1999. Plasma lipoproteins promote the release of bacterial lipopolysaccharide from the monocyte cell surface. J. Biol. Chem. 274: 34116-34122.
32. Kitchens, R. L., P. A. Thompson, S. Viriyakosol, G. E. O'Keefe, and R. S. Munford. 2001. Plasma CD14 decreases monocyte responses to LPS by transferring cell-bound LPS to plasma lipoproteins. J. Clin. Invest. 108: 485-493.
33. Thompson, P. A., P. S. Tobias, S. Viriyakosol, T. N. Kirkland, and R. L. Kitchens. 2003. Lipopolysaccharide (LPS)-binding protein inhibits responses to cell-bound LPS. J. Biol. Chem. 278: 28367-28371.
34. Basu, S. K., Y. K. Ho, M. S. Brown, D. W. Bilheimer, R. G. Anderson, and J. L. Goldstein. 1982. Biochemical and genetic studies of the apoprotein E secreted by mouse macrophages and human monocytes. J. Biol. Chem. 257: 9788-9795.
35. Hashimoto, S., T. Suzuki, H-Y. Dong, N. Yamazaki, and K. Matsushima. 1999. Serial analysis of gene expression in human monocytes and macrophages. Blood. 94: 837-844. (Pubitemid 29361813)
36. Mahley, R. W., and S. C. Jr. Rall. 2000. Apolipoprotein E: far more than a lipid transport protein. Annu. Rev. Genomics Hum. Genet. 1: 507-537.
37. Zhang, W. Y., P. M. Gaynor, and H. S. Kruth. 1996. Apolipoprotein E produced by human monocyte-derived macrophages mediates cholesterol efflux that occurs in the absence of added cholesterol acceptors. J. Biol. Chem. 271: 28641-28646.
38. Huang, Z. H., M. L. Fitzgerald, and T. Mazzone. 2006. Distinct cellular loci for the ABCA1-dependent and ABCA1-independent lipid efflux mediated by endogenous apolipoprotein E expression. Arterioscler. Thromb. Vasc. Biol. 26: 157-162.
39. Rensen, P. C. N., M. Van Oosten, E. Van de Bilt, M. Van Eck, J. Kuiper, and T. J. C. Van Berkel. 1997. Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats in vivo. J. Clin. Invest. 99: 2438-2445.
40. Fitzgerald, M. L., A. L. Morris, A. Chroni, A. J. Mendez, V. I. Zannis, and M. W. Freeman. 2004. ABCA1 and amphipathic apolipoproteins form high-affinity molecular complexes required for cholesterol efflux. J. Lipid Res. 45: 287-294.
41. Vedhachalam, C., A. B. Ghering, W. S. Davidson, S. Lund-Katz, G. H. Rothblat, and M. C. Phillips. 2007. ABCA1-induced cell surface binding sites for ApoA-I. Arterioscler. Thromb. Vasc. Biol. 27: 1603-1609.
42. Peet, D. J., S. D. Turley, W. Ma, B. A. Janowski, J. M. Lobaccaro, R. E. Hammer, and D. J. Mangelsdorf. 1998. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell. 93: 693-704.
43. Christiansen-Weber, T. A., J. R. Voland, Y. Wu, K. Ngo, B. L. Roland, S. Nguyen, P. A. Peterson, and W. P. Fung-Leung. 2000. Functional loss of ABCA1 in mice causes severe placental malformation, aberrant lipid distribution, and kidney glomerulonephritis as well as high-density lipoprotein cholesterol deficiency. Am. J. Pathol. 157: 1017-1029.
44. Xie, C., S. D. Turley, and J. M. Dietschy. 2009. ABCA1 plays no role in the centripetal movement of cholesterol from peripheral tissues to the liver and intestine in the mouse. J. Lipid Res. 50: 1316-1329.
45. Li, L., P. A. Thompson, and R. L. Kitchens. 2008. Infection induces a positive acute phase apolipoprotein E response from a negative acute phase gene: role of hepatic LDL receptors. J. Lipid Res. 49: 1782-1793.
46. Munford, R. S., L. C. DeVeaux, J. E. Cronan, Jr., and P. D. Rick. 1992. Biosynthetic radiolabeling of bacterial lipopolysaccharide to high specific activity. J. Immunol. Methods. 148: 115-120.
47. Kitchens, R. L., and R. S. Munford. 1998. CD14-dependent internalization of lipopolysaccharide (LPS) is strongly influenced by LPS aggregation but not by cellular responses to LPS. J. Immunol. 160: 1920-1928.
48. Schultz, J. R., H. Tu, A. Luk, J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, et al. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14: 2831-2838.
49. Larrede, S., C. M. Quinn, W. Jessup, E. Frisdal, M. Olivier, V. Hsieh, M. J. Kim, M. van Eck, P. Couvert, A. Carrie, et al. 2009. Stimulation of cholesterol efflux by LXR agonists in cholesterol-loaded human macrophages is ABCA1-dependent but ABCG1-independent. Arterioscler. Thromb. Vasc. Biol. 29: 1930-1936.
50. Yancey, P. G., H. Yu, M. F. Linton, and S. Fazio. 2007. A pathway-dependent on ApoE, ApoAI, and ABCA1 determines formation of buoyant high-density lipoprotein by macrophage foam cells. Arterioscler. Thromb. Vasc. Biol. 27: 1123-1131.
51. Pradel, L. C., A. J. Mitchell, A. Zarubica, L. Dufort, L. Chansson, P. Naquet, C. Broccardo, and G. Chimini. 2009. ATP-binding cassette transporter hallmarks tissue macrophages and modulates cytokine-triggered polarization programs. Eur. J. Immunol. 39: 2270-2280.
52. Gegner, J. A., R. J. Ulevitch, and P. S. Tobias. 1995. Lipopolysaccharide (LPS) signal transduction and clearance. Dual roles for LPS binding protein and membrane CD14. J. Biol. Chem. 270: 5320-5326.
53. Chen, H., M. J. Cowan, J. D. Hasday, S. N. Vogel, and A. E. Medvedev. 2007. Tobacco smoking inhibits expression of proinflammatory cytokines and activation of IL-1R-associated kinase, p38, and NF-kappaB in alveolar macrophages stimulated with TLR2 and TLR4 agonists. J. Immunol. 179: 6097-6106.
54. Von Baehr, V., W. D. Döcke, M. Plauth, C. Liebenthal, S. Küpferling, H. Lochs, R. Baumgarten, and H. D. Volk. 2000. Mechanisms of endotoxin tolerance in patients with alcoholic liver cirrhosis: role of interleukin 10, interleukin 1 receptor antagonist, and soluble tumour necrosis factor receptors as well as effector cell desensitisation. Gut. 47: 281-287.
55. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, D. Altmann, et al. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12: 1365-1371.
56. Gao, L., Y. J. Tsai, D. N. Grigoryev, and K. C. Barnes. 2007. Host defense genes in asthma and sepsis and the role of the environment. Curr. Opin. Allergy Clin. Immunol. 7: 459-467.