TNF-α decreases ABCA1 expression and attenuates HDL cholesterol efflux in the human intestinal cell line Caco-2

Journal of Lipid Research

Volumn 51, Issue 6, 2010, Pages 1407-1415

  Field, F Jeffrey ^a   Watt, Kim ^a   Mathur, Satya N ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A1; ABC TRANSPORTER G1; ABC TRANSPORTER G8; APOLIPOPROTEIN A1; APOLIPOPROTEIN C1; FAS ANTIGEN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; SCAVENGER RECEPTOR BI; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN CACO 2; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CROHN DISEASE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; INTESTINE CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CACO-2 CELLS; CHOLESTEROL, HDL; GENE EXPRESSION REGULATION; HUMANS; INTESTINES; NF-KAPPA B; ORPHAN NUCLEAR RECEPTORS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77952739913     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M002410     Document Type: Article

References (58)

1. Rhoads, G. G., C. L. Gulbrandsen, and A. Kagan. 1976. Serum lipoproteins and coronary heart disease in a population study of Hawaii Japanese men. N. Engl. J. Med. 294: 293-298.
2. Gordon, T., W. P. Castelli, M. C. Hjortland, W. B. Kannel, and T. R. Dawber. 1977. High density lipoprotein as a protective factor against coronary heart disease. The Framingham Study. Am. J. Med. 62: 707-714. (Pubitemid 8110784)
3. Sharrett, A. R., C. M. Ballantyne, S. A. Coady, G. Heiss, P. D. Sorlie, D. Catellier, and W. Patsch. 2001. Coronary heart disease prediction from lipoprotein cholesterol levels, triglycerides, lipoprotein(a), apolipoproteins A-I and B, and HDL density subfractions: the Atherosclerosis Risk in Communities (ARIC) Study. Circulation. 104: 1108-1113.
4. Wang, N., and A. R. Tall. 2003. Regulation and mechanisms of ATP-binding cassette transporter A1-mediated cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23: 1178-1184. (Pubitemid 36871270)
5. Brewer, H. B., Jr., A. T. Remaley, E. B. Neufeld, F. Basso, and C. Joyce. 2004. Regulation of plasma high-density lipoprotein levels by the ABCA1 transporter and the emerging role of high-density lipoprotein in the treatment of cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 24: 1755-1760.
6. Francis, G. A., R. H. Knopp, and J. F. Oram. 1995. Defective removal of cellular cholesterol and phospholipids by apolipoprotein A-I in Tangier disease. J. Clin. Invest. 96: 78-87.
7. Asztalos, B. F. 2004. High-density lipoprotein metabolism and progression of atherosclerosis: new insights from the HDL Atherosclerosis Treatment Study. Curr. Opin. Cardiol. 19: 385-391.
8. Yokoyama, S. 2006. Assembly of high-density lipoprotein. Arterioscler. Thromb. Vasc. Biol. 26: 20-27.
9. Bodzioch, M., E. Orso, J. Klucken, T. Langmann, A. Bottcher, W. Diederich, W. Drobnik, S. Barlage, C. Buchler, M. Porsch-Ozcurumez, et al. 1999. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22: 347-351. (Pubitemid 29369524)
10. Rust, S., M. Rosier, H. Funke, J. Real, Z. Amoura, J. C. Piette, J. F. Deleuze, H. B. Brewer, N. Duverger, P. Denefle, et al. 1999. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22: 352-355. (Pubitemid 29369525)
11. Schaefer, E. J., L. A. Zech, D. E. Schwartz, and H. B. Brewer, Jr. 1980. Coronary heart disease prevalence and other clinical features in familial high-density lipoprotein deficiency (Tangier disease). Ann. Intern. Med. 93: 261-266.
12. Clee, S. M., J. J. Kastelein, M. van Dam, M. Marcil, K. Roomp, K. Y. Zwarts, J. A. Collins, R. Roelants, N. Tamasawa, T. Stulc, et al. 2000. Age and residual cholesterol efflux affect HDL cholesterol levels and coronary artery disease in ABCA1 heterozygotes. J. Clin. Invest. 106: 1263-1270.
13. Berge, K. E., H. Tian, G. A. Graf, L. Yu, N. V. Grishin, J. Schultz, P. Kwiterovich, B. Shan, R. Barnes, and H. H. Hobbs. 2000. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science. 290: 1771-1775.
14. Repa, J. J., S. D. Turley, J. 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.
15. Venkateswaran, A., B. A. Laffitte, S. B. Joseph, P. A. Mak, D. C. Wilpitz, P. A. Edwards, and P. Tontonoz. 2000. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXR alpha. Proc. Natl. Acad. Sci. USA. 97: 12097-12102.
16. 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.
17. Lehmann, J. M., S. A. Kliewer, L. B. Moore, T. A. Smith-Oliver, B. B. Oliver, J. L. Su, S. S. Sundseth, D. A. Winegar, D. E. Blanchard, T. A. Spencer, et al. 1997. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J. Biol. Chem. 272: 3137-3140.
18. Luo, Y., and A. R. Tall. 2000. Sterol upregulation of human CETP expression in vitro and in transgenic mice by an LXR element. J. Clin. Invest. 105: 513-520. (Pubitemid 30127252)
19. Venkateswaran, A., J. J. Repa, J. M. Lobaccaro, A. Bronson, D. J. Mangelsdorf, and P. A. Edwards. 2000. Human white/murine ABC8 mRNA levels are highly induced in lipid-loaded macrophages. A transcriptional role for specific oxysterols. J. Biol. Chem. 275: 14700-14707. (Pubitemid 30339762)
20. Repa, J. J., G. Liang, J. Ou, Y. Bashmakov, J. M. Lobaccaro, I. Shimomura, B. Shan, M. S. Brown, J. L. Goldstein, and D. J. Mangelsdorf. 2000. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 14: 2819-2830.
21. Attie, A. D., J. P. Kastelein, and M. R. Hayden. 2001. Pivotal role of ABCA1 in reverse cholesterol transport influencing HDL levels and susceptibility to atherosclerosis. J. Lipid Res. 42: 1717-1726.
22. Haghpassand, M., P. A. Bourassa, O. L. Francone, and R. J. Aiello. 2001. Monocyte/macrophage expression of ABCA1 has minimal contribution to plasma HDL levels. J. Clin. Invest. 108: 1315-1320. (Pubitemid 33107759)
23. Brunham, L. R., J. K. Kruit, J. Iqbal, C. Fievet, J. M. Timmins, T. D. Pape, B. A. Coburn, N. Bissada, B. Staels, A. K. Groen, et al. 2006. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J. Clin. Invest. 116: 1052-1062.
24. van Leuven, S. I., R. Hezemans, J. H. Levels, S. Snoek, P. C. Stokkers, G. K. Hovingh, J. J. Kastelein, E. S. Stroes, E. de Groot, and D. W. Hommes. 2007. Enhanced atherogenesis and altered high density lipoprotein in patients with Crohn's disease. J. Lipid Res. 48: 2640-2646.
25. Popa, C., M. G. Netea, P. L. van Riel, J. W. van der Meer, and A. F. Stalenhoef. 2007. The role of TNF-alpha in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J. Lipid Res. 48: 751-762. (Pubitemid 46557880)
26. Braegger, C. P., S. Nicholls, S. H. Murch, S. Stephens, and T. T. MacDonald. 1992. Tumour necrosis factor alpha in stool as a marker of intestinal inflammation. Lancet. 339: 89-91.
27. Murch, S. H., C. P. Braegger, J. A. Walker-Smith, and T. T. MacDonald. 1993. Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease. Gut. 34: 1705-1709.
28. Van Deventer, S. J. 1997. Tumour necrosis factor and Crohn's disease. Gut. 40: 443-448. (Pubitemid 27204920)
29. Hattori, Y., K. Suzuki, S. Hattori, and K. Kasai. 2006. Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells. Hypertension. 47: 1183-1188. (Pubitemid 44289177)
30. Field, F. J., K. Watt, and S. N. Mathur. 2008. Origins of intestinal ABCA1-mediated HDL-cholesterol. J. Lipid Res. 49: 2605-2619.
31. Mathur, S. N., K. R. Watt, and F. J. Field. 2007. Regulation of intestinal NPC1L1 expression by dietary fish oil and docosahexaenoic acid. J. Lipid Res. 48: 395-404.
32. Wong, M. L., and J. F. Medrano. 2005. Real-time PCR for mRNA quantitation. Biotechniques. 39: 75-85.
33. Field, F. J., E. Albright, and S. N. Mathur. 1988. Regulation of triglyceride-rich lipoprotein secretion by fatty acids in CaCo-2 cells. J. Lipid Res. 29: 1427-1437.
34. Bowden, K., and N. D. Ridgway. 2008. OSBP negatively regulates ABCA1 protein stability. J. Biol. Chem. 283: 18210-18217.
35. Agassandian, M., O. L. Miakotina, M. Andrews, S. N. Mathur, and R. K. Mallampalli. 2007. Pseudomonas aeruginosa and sPLA2 IB stimulate ABCA1-mediated phospholipid efflux via ERK-activation of PPARalpha-RXR. Biochem. J. 403: 409-420. (Pubitemid 46710927)
36. Murthy, S., E. Born, S. N. Mathur, and F. J. Field. 2002. LXR/RXR activation enhances basolateral efflux of cholesterol in CaCo-2 cells. J. Lipid Res. 43: 1054-1064. (Pubitemid 34760876)
37. Zhang, J. R., T. Coleman, S. J. Langmade, D. E. Scherrer, L. Lane, M. H. Lanier, C. Feng, M. S. Sands, J. E. Schaffer, C. F. Semenkovich, et al. 2008. Niemann-Pick C1 protects against atherosclerosis in mice via regulation of macrophage intracellular cholesterol traffi cking. J. Clin. Invest. 118: 2281-2290.
38. 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.
39. Zarubica, A., D. Trompier, and G. Chimini. 2007. ABCA1, from pathology to membrane function. Pflugers Arch. 453: 569-579.
40. Murthy, S., E. Born, S. N. Mathur, and F. J. Field. 2004. Liver-X-receptor-mediated increase in ATP-binding cassette transporter A1 expression is attenuated by fatty acids in CaCo-2 cells: effect on cholesterol efflux to high-density lipoprotein. Biochem. J. 377: 545-552. (Pubitemid 38221826)
41. 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. (Pubitemid 37185884)
42. 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. (Pubitemid 37352775)
43. Gerbod-Giannone, M. C., Y. Li, A. Holleboom, S. Han, L. C. Hsu, I. Tabas, and A. R. Tall. 2006. TNFalpha induces ABCA1 through NF-kappaB in macrophages and in phagocytes ingesting apoptotic cells. Proc. Natl. Acad. Sci. USA. 103: 3112-3117.
44. Wellington, C. L., E. K. Walker, A. Suarez, A. Kwok, N. Bissada, R. Singaraja, Y. Z. Yang, L. H. Zhang, E. James, J. E. Wilson, et al. 2002. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab. Invest. 82: 273-283.
45. 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.
46. Wang, N., W. Chen, P. Linsel-Nitschke, L. O. Martinez, B. Agerholm-Larsen, D. L. Silver, and A. R. Tall. 2003. A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J. Clin. Invest. 111: 99-107. (Pubitemid 36134853)
47. Wang, Y., and J. F. Oram. 2002. Unsaturated fatty acids inhibit cholesterol efflux from macrophages by increasing degradation of ATPbinding cassette transporter A1. J. Biol. Chem. 277: 5692-5697. (Pubitemid 34968625)
48. Arakawa, R., and S. Yokoyama. 2002. Helical apolipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiol protease-mediated degradation. J. Biol. Chem. 277: 22426-22429. (Pubitemid 34967213)
49. Ohama, T., K. Hirano, Z. Zhang, R. Aoki, K. Tsujii, Y. Nakagawa-Toyama, K. Tsukamoto, C. Ikegami, A. Matsuyama, M. Ishigami, et al. 2002. Dominant expression of ATP-binding cassette transporter-1 on basolateral surface of Caco-2 cells stimulated by LXR/RXR ligands. Biochem. Biophys. Res. Commun. 296: 625-630.
50. Tall, A. R. 2008. Cholesterol efflux pathways and other potential mechanisms involved in the athero-protective effect of high density lipoproteins. J. Intern. Med. 263: 256-273.
51. Neufeld, E. B., A. T. Remaley, S. J. Demosky, J. A. Stonik, A. M. Cooney, M. Comly, N. K. Dwyer, M. Zhang, J. Blanchette-Mackie, S. Santamarina-Fojo, et al. 2001. Cellular localization and trafficking of the human abca1 transporter. J. Biol. Chem. 276: 27584-27590. (Pubitemid 37410679)
52. Orso, E., C. Broccardo, W. E. Kaminski, A. Bottcher, G. Liebisch, W. Drobnik, A. Gotz, O. Chambenoit, W. Diederich, T. Langmann, et al. 2000. Transport of lipids from golgi to plasma membrane is defective in tangier disease patients and Abc1-deficient mice. Nat. Genet. 24: 192-196. (Pubitemid 30094724)
53. Yancey, P. G., A. E. Bortnick, G. Kellner-Weibel, M. de la Llera-Moya, M. C. Phillips, and G. H. Rothblat. 2003. Importance of different pathways of cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23: 712-719.
54. Field, F. J., E. Born, and S. N. Mathur. 2004. Stanol esters decrease plasma cholesterol independently of intestinal ABC sterol transporters and Niemann-Pick C1-like 1 protein gene expression. J. Lipid Res. 45: 2252-2259.
55. Koutroubakis, I. E., P. Oustamanolakis, N. Malliaraki, K. Karmiris, I. Chalkiadakis, E. Ganotakis, N. Karkavitsas, and E. A. Kouroumalis. 2009. Effects of tumor necrosis factor alpha inhibition with infliximab on lipid levels and insulin resistance in patients with inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 21: 283-288.
56. Seriolo, B., S. Paolino, A. Sulli, D. Fasciolo, and M. Cutolo. 2006. Effects of anti-TNF-alpha treatment on lipid profile in patients with active rheumatoid arthritis. Ann. N. Y. Acad. Sci. 1069: 414-419. (Pubitemid 43989884)
57. Karrasch, T., and C. Jobin. 2008. NF-kappaB and the intestine: friend or foe? Inflamm. Bowel Dis. 14: 114-124.
58. Santamarina-Fojo, S., K. Peterson, C. Knapper, Y. Qiu, L. Freeman, J. F. Cheng, J. Osorio, A. Remaley, X. P. Yang, C. Haudenschild, et al. 2000. Complete genomic sequence of the human ABCA1 gene: analysis of the human and mouse ATP-binding cassette A promoter. Proc. Natl. Acad. Sci. USA. 97: 7987-7992. (Pubitemid 30460760)