Novel technique for generating macrophage foam cells for in vitro reverse cholesterol transport studies

Journal of Lipid Research

Volumn 54, Issue 12, 2013, Pages 3358-3372

  Sengupta, Bhaswati ^a   Narasimhulu, Chandrakala Aluganti ^a   Parthasarathy, Sampath ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

High density lipoprotein; Lysophosphatidylcholine; NBD cholesterol

Indexed keywords

CHOLESTEROL; CHOLESTEROL ESTER; HIGH DENSITY LIPOPROTEIN; LYSOPHOSPHATIDYLCHOLINE; OLEIC ACID; OXIDIZED DENSITY LIPOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; FLUORESCENCE; FOAM CELL; IN VITRO STUDY; ISOTOPE LABELING; LIPID SOLUBILITY; MICELLE; MICROSCOPY; MOLECULAR STABILITY; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; THIN LAYER CHROMATOGRAPHY;

HIGH DENSITY LIPOPROTEIN; LYSOPHOSPHATIDYLCHOLINE; NBD-CHOLESTEROL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CHOLESTEROL; DETERGENTS; FOAM CELLS; LIPOPROTEINS, HDL; LYSOPHOSPHATIDYLCHOLINES; MICE; MICELLES; SOLUBILITY; WATER;

EID: 84887912709     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M041327     Document Type: Article

References (56)

1. Parthasarathy, S., N. Santanam, S. Ramachandran, and O. Meilhac. 1999. Oxidants and antioxidants in atherogenesis. An appraisal. J. Lipid Res. 40:2143-2157.
2. Khoo, J. C., E. Miller, P. McLoughlin, and D. Steinberg. 1988. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis. 8:348-358.
3. Xu, X. X., and I. Tabas. 1991. Sphingomyelinase enhances low density lipoprotein uptake and ability to induce cholesteryl ester accumulation in macrophages. J. Biol. Chem. 266:24849-24858. (Pubitemid 21909018)
4. Basu, S. K., J. L. Goldstein, G. W. Anderson, and M. S. Brown. 1976. Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. USA. 73:3178-3182.
5. Lusis, A. J. 2000. Atherosclerosis. Nature. 407:233-241.
6. Collot-Teixeira, S., J. Martin, C. McDermott-Roe, R. Poston, and J. L. McGregor. 2007. CD36 and macrophages in atherosclerosis. Cardiovasc. Res. 75:468-477. (Pubitemid 47080960)
7. Stephen, S. L., K. Freestone, S. Dunn, M. W. Twigg, S. Homer-Vanniasinkam, J. H. Walker, S. B. Wheatcroft, and S. Ponnambalam. 2010. Scavenger receptors and their potential as therapeutic targets in the treatment of cardiovascular disease. Int. J. Hypertens. 2010:2010:646929.
8. Kruth, H. S. 2011. Receptor-independent fluid-phase pinocytosis mechanisms for induction of foam cell formation with native lowdensity lipoprotein particles. Curr. Opin. Lipidol. 22:386-393.
9. Lippi, G., M. Franchini, and G. Targher. 2011. Arterial thrombus formation in cardiovascular disease. Nat. Rev. Cardiol. 8:502-512.
10. Wei, C., M. Penumetcha, N. Santanam, Y. G. Liu, M. Garelnabi, and S. Parthasarathy. 2005. Exercise might favor reverse cholesterol transport and lipoprotein clearance: potential mechanism for its anti-atherosclerotic effects. Biochim. Biophys. Acta. 1723:124-127. (Pubitemid 40744679)
11. Rye, K-A., and P. J. Barter. 2004. Formation and metabolism of prebetamigrating, lipid-poor apolipoprotein A-I. Arterioscler. Thromb. Vasc. Biol. 24:421-428. (Pubitemid 38326133)
12. Rothblat, G. H., and M. C. Phillips. 2010. High-density lipoprotein heterogeneity and function in reverse cholesterol transport. Curr. Opin. Lipidol. 21:229-238.
13. Ohashi, R., H. Mu, X. Wang, Q. Yao, and C. Chen. 2005. Reverse cholesterol transport and cholesterol efflux in atherosclerosis. QJM. 98:845-856. (Pubitemid 43071450)
14. Khera, A. V., and D. J. Rader. 2013. Cholesterol efflux capacity: full steam ahead or a bump in the road? Arterioscler. Thromb. Vasc. Biol. 33:1449-1451.
15. Li, X. M., W. H. Tang, M. K. Mosior, Y. Huang, Y. Wu, W. Matter, V. Gao, D. Schmitt, J. A. Didonato, E. A. Fisher, et al. 2013. Paradoxical association of enhanced cholesterol efflux with increased incident cardiovascular risks. Arterioscler. Thromb. Vasc. Biol. 33:1696-1705.
16. Tall, A. R., P. Costet, and N. Wang. 2002. Regulation and mechanisms of macrophage cholesterol efflux. J. Clin. Invest. 110:899-904.
17. Cuchel, M., and D. J. Rader. 2006. Macrophage reverse cholesterol transport. Circulation. 113:2548-2555.
18. Feig, J. E., J. X. Rong, R. Shamir, M. Sanson, Y. Vengrenyuk, J. Liu, K. Rayner, K. Moore, M. Garabedian, and E. A. Fisher. 2011. HDL promotes rapid atherosclerosis regression in mice and alters inflammatory properties of plaque monocyte-derived cells. Proc. Natl. Acad. Sci. USA. 108:7166-7171.
19. Parthasarathy, S., J. Barnett, and L. G. Fong. 1990. High-density lipoprotein inhibits the oxidative modification of low-density lipoprotein. Biochim. Biophys. Acta. 22:275-283. (Pubitemid 20151285)
20. Rye, K-A., C. A. Bursill, G. Lambert, F. Tabet, and P. J. Barter. 2009. The metabolism and anti-atherogenic properties of HDL. J. Lipid Res. 50:S195 - S200.
21. Barter, P. J., S. Nicholls, K. A. Rye, G. M. Anantharamaiah, M. Navab, and A. M. Fogelman. 2004. Antiinflammatory properties of HDL. Circ. Res. 95:764-772. (Pubitemid 39390578)
22. Shao, B., M. N. Oda, J. F. Oram, and J. W. Heinecke. 2010. Myeloperoxidase: an oxidative pathway for generating dysfunctional high-density lipoprotein. Chem. Res. Toxicol. 23:447-454.
23. Kontush, A., and M. J. Chapman. 2006. Functionally defective highdensity lipoprotein: a new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol. Rev. 58:342-374. (Pubitemid 44394906)
24. Garner, B., P. K. Witting, A. R. Waldeck, J. K. Christison, M. Raftery, and R. Stocker. 1998. Oxidation of high density lipoproteins: I. Formation of methionine sulfoxide in apolipoproteins AI and AII is an early event that accompanies lipid peroxidation and can be enhanced by α-tocopherol. J. Biol. Chem. 273:6080-6087. (Pubitemid 28144687)
25. Asztalos, B. F., M. De La Llera-Moya, G. E. Dallal, K. V. Horvath, E. J. Schaefer, and G. H. Rothblat. 2005. Differential effects of HDL subpopulations on cellular ABCA1- and SR-BI-mediated cholesterol efflux. J. Lipid Res. 46:2246-2253. (Pubitemid 41377476)
26. De La Llera-Moya, M., D. Drazul-Schrader, B. F. Asztalos, M. Cuchel, D. J. Rader, and G. H. Rothblat. 2010. The ability to promote efflux via ABCA1 determines the capacity of serum specimens with similar high-density lipoprotein cholesterol to remove cholesterol from macrophages. Arterioscler. Thromb. Vasc. Biol. 30:796-801.
27. Zhang, J., S. Cai, B. R. Peterson, P. M. Kris-Etherton, and J. P. Heuvel. 2011. Development of a cell-based, high-throughput screening assay for cholesterol efflux using a fluorescent mimic of cholesterol. Assay Drug Dev. Technol. 9:136-146.
28. Khera, A. V., M. Cuchel, M. De La Llera-Moya, A. Rodrigues, M. F. Burke, K. Jafri, B. C. French, J. A. Phillips, M. L. Mucksavage, R. L. Wilensky, et al. 2011. Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N. Engl. J. Med. 364:127-135.
29. Frolov, A., A. Petrescu, B. P. Atshaves, P. T. So, E. Gratton, G. Serrero, and F. Schroeder. 2000. High density lipoprotein-mediated cholesterol uptake and targeting to lipid droplets in intact L-cell fi-broblasts. A single- and multiphoton fluorescence approach. J. Biol. Chem. 275:12769-12780. (Pubitemid 30241431)
30. Weibel, G. L., S. Hayes, A. Wilson, M. C. Phillips, J. Billheimer, D. J. Rader, and G. H. Rothblat. 2011. Novel in vivo method for measuring cholesterol mass flux in peripheral macrophages. Arterioscler. Thromb. Vasc. Biol. 31:2865-2871.
31. Sparrow, C. P., S. Patel, J. Baffic, Y. S. Chao, M. Hernandez, M. H. Lam, J. Montenegro, S. D. Wright, and P. A. Detmers. 1999. A fluorescent cholesterol analog traces cholesterol absorption in hamsters and is esterified in vivo and in vitro. J. Lipid Res. 40:1747-1757. (Pubitemid 29477245)
32. Auge, N., N. Santanam, and S. Parthasarathy. 1998. An efficient method for solubilizing β-carotene in aqueous solutions. J. Med. Food. 1:39-43.
33. Marinetti, G. V., J. Erbland, R. F. Witter, J. Petix, and E. Stotz. 1958. Metabolic pathways of lysolecithin in a soluble rat-liver system. Biochim. Biophys. Acta. 30:223.
34. Portman, O. W., P. Soltys, M. Alexander, and T. Osuga. 1970. Metabolism of lysolecithin in vivo: effects of hyperlipemia and atherosclerosis in squirrel monkeys. J. Lipid Res. 11:596-604.
35. Brown, M. S., and J. L. Goldstein. 1983. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu. Rev. Biochem. 52:223-261. (Pubitemid 13030685)
36. Quinn, M. T., S. Parthasarathy, and D. Steinberg. 1988. Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis. Proc. Natl. Acad. Sci. USA. 85:2805-2809.
37. Portman, O. W., and M. Alexander. 1969. Lysophosphatidylcholine concentrations and metabolism in aortic intima plus inner media: effect of nutritionally induced atherosclerosis. J. Lipid Res. 10:158-165.
38. Storey, S. M., B. P. Atshaves, A. L. McIntosh, K. K. Landrock, G. G. Martin, H. Huang, H. Ross Payne, J. D. Johnson, R. D. Macfarlane, A. B. Kier, et al. 2010. Effect of sterol carrier protein-2 gene ablation on HDL-mediated cholesterol efflux from cultured primary mouse hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 299:G244 - G254.
39. Heeren, J., T. Grewal, A. Laatsch, D. Rottke, F. Rinninger, C. Enrich, and U. Beisiegel. 2003. Recycling of apoprotein E is associated with cholesterol efflux and high density lipoprotein internalization. J. Biol. Chem. 278:14370-14378. (Pubitemid 36799988)
40. Atshaves, B. P., O. Starodub, A. McIntosh, A. Petrescu, J. B. Roths, A. B. Kier, and F. Schroeder. 2000. Sterol carrier protein-2 alters high density lipoprotein-mediated cholesterol efflux. J. Biol. Chem. 275:36852-36861. (Pubitemid 32002097)
41. Sripada, P. K. 1988. Synthesis of single- and double-13C-labeled cholesterol oleate. Chem. Phys. Lipids. 48:147-151.
42. Chung, B. H., T. Wilkinson, J. C. Geer, and J. P. Segrest. 1980. Preparative and quantitative isolation of plasma lipoproteins: rapid, single discontinuous density gradient ultracentrifugation in a vertical rotor. J. Lipid Res. 21:284-291. (Pubitemid 10055505)
43. Chandrakala, A. N., D. Sukul, K. Selvarajan, C. Sai-Sudhakar, B. Sun, and S. Parthasarathy. 2012. Induction of brain natriuretic peptide and monocyte chemotactic protein-1 gene expression by oxidized low-density lipoprotein: relevance to ischemic heart failure. Am. J. Physiol. Cell Physiol. 302:C165 - C177.
44. Santanam, N., and S. Parthasarathy. 1995. Paradoxical actions of antioxidants in the oxidation of low density lipoprotein by peroxidases. J. Clin. Invest. 95:2594-2600.
45. Kritharides, L., A. Christian, G. Stoudt, D. Morel, and G. H. Rothblat. 1998. Cholesterol metabolism and efflux in human THP-1 macrophages. Arterioscler. Thromb. Vasc. Biol. 18:1589-1599. (Pubitemid 28465411)
46. Mahlberg, F. H., A. Rodriguez-Oquendo, D. W. Bernard, J. M. Glick, and G. H. Rothblat. 1990. Potential problems in the use of commercial preparations of radiolabeled cholesterol. Atherosclerosis. 84:95-100. (Pubitemid 20360852)
47. Zhou, H., W. Mak, Y. Zheng, C. R. Dunstan, and M. J. Seibel. 2008. Osteoblasts directly control lineage commitment of mesenchymal progenitor cells through Wnt signaling. J. Biol. Chem. 283:1936-1945.
48. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
49. Raghavamenon, A., M. Garelnabi, S. Babu, A. Aldrich, D. Litvinov, and S. Parthasarathy. 2009. Alpha-tocopherol is ineffective in preventing the decomposition of preformed lipid peroxides and may promote the accumulation of toxic aldehydes: a potential explanation for the failure of antioxidants to affect human atherosclerosis. Antioxid. Redox Signal. 11:1237-1248.
50. Erbland, J. F., and G. V. Marinetti. 1965. The enzymatic acylation and hydrolysis of lysolecithin. Biochim. Biophys. Acta. 106:128-138.
51. Elsbach, P. 1966. Phospholipid metabolism by phagocytic cells. I. A comparison of conversion of [32P]lysolecithin to lecithin and glycerylphosphorylcholine by homogenates of rabbit polymorphonuclear leukocytes and alveolar macrophages. Biochim. Biophys. Acta. 125:510-524.
52. Terpstra, V., N. Kondratenko, and D. Steinberg. 1997. Macrophages lacking scavenger receptor A show a decrease in binding and uptake of acetylated low-density lipoprotein and of apoptotic thymocytes, but not of oxidatively damaged red blood cells. Proc. Natl. Acad. Sci. USA. 94:8127-8131. (Pubitemid 27343788)
53. Palkama, T. 1991. Induction of interleukin-1 production by ligands binding to the scavenger receptor in human monocytes and the THP-1 cell line. Immunology. 74:432-438.
54. Rand, R. P., W. A. Pangborn, A. D. Purdon, and D. O. Tinker. 1975. Lysolecithin and cholesterol interact stoichiometrically forming bimolecular lamellar structures in the presence of excess water, of lysolecithin or cholesterol. Can. J. Biochem. 53:189-195.
55. Hsieh, C. C., M. H. Yen, H. W. Liu, and Y. T. Lau. 2000. Lysophosphatidylcholine induces apoptotic and non-apoptotic death in vascular smooth muscle cells: in comparison with oxidized LDL. Atherosclerosis. 151:481-491.
56. Weltzien, H. U., B. Arnold, and R. Reuther. 1977. Quantitative studies on lysolecithin-mediated hemolysis. Use of ether-deoxy lysolecithin analogs with varying aliphatic chain-lengths. Biochim. Biophys. Acta. 466:411-421. (Pubitemid 8074965)