Cholesterol esterification by ACAT2 is essential for efficient intestinal cholesterol absorption: Evidence from thoracic lymph duct cannulation

Journal of Lipid Research

Volumn 53, Issue 1, 2012, Pages 95-104

  Nguyen, Tam M ^a,b   Sawyer, Janet K ^a   Kelley, Kathryn L ^a   Davis, Matthew A ^a   Rudel, Lawrence L ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Cholesterol transport; Chylomicron; Lipoprotein metabolism

Indexed keywords

CARBON 14; CHOLESTEROL ACYLTRANSFERASE; CHOLESTEROL ESTER; CHYLOMICRON; HISTONE H3; ISOTOPE; MESSENGER RNA; PALM OIL; PROTEIN ACAT2; SITOSTEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CANNULATION; CHOLESTEROL ABSORPTION; CHOLESTEROL ESTERIFICATION; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DOSAGE; INTESTINE ABSORPTION; LIPID ABSORPTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; THORACIC LYMPH DUCT CANNULATION;

ANIMALS; CHOLESTEROL; CHOLESTEROL ESTERS; CHYLOMICRONS; ESTERIFICATION; INTESTINAL ABSORPTION; MALE; MICE; PARTICLE SIZE; STEROL O-ACYLTRANSFERASE; THORACIC DUCT;

EID: 84455161546     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M018820     Document Type: Article

References (47)

1. Rosamond, W., K. Flegal, K. Furie, A. Go, K. Greenlund, N. Haase, S. M. Hailpern, M. Ho, V. Howard, B. Kissela, et al. 2008. Heart disease and stroke statistics--2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 117: e25-e146.
2. Kannel, W. B., W. P. Castelli, T. Gordon, and P. M. McNamara. 1971. Serum cholesterol, lipoproteins, and the risk of coronary heart disease. The Framingham study. Ann. Intern. Med. 74: 1-12.
3. Wang, D. Q. 2007. Regulation of intestinal cholesterol absorption. Annu. Rev. Physiol. 69: 221-248. (Pubitemid 46457642)
4. McMurry, M. P., W. E. Connor, D. S. Lin, M. T. Cerqueira, and S. L. Connor. 1985. The absorption of cholesterol and the sterol balance in the Tarahumara Indians of Mexico fed cholesterol-free and high cholesterol diets. Am. J. Clin. Nutr. 41: 1289-1298. (Pubitemid 15031374)
5. Iqbal, J., and M. M. Hussain. 2009. Intestinal lipid absorption. Am. J. Physiol. Endocrinol. Metab. 296: E1183-E1194.
6. McGill, H. C. J. 1979. The relationship of dietary cholesterol to serum cholesterol concentration and to atherosclerosis in man. Am. J. Clin. Nutr. 32: 2664-2702.
7. Dietschy, J. M., S. D. Turley, and D. K. Spady. 1993. Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J. Lipid Res. 34: 1637-1659. (Pubitemid 23298709)
8. Klein, R. L., and L. L. Rudel. 1983. Cholesterol absorption and transport in thoracic duct lymph lipoproteins of nonhuman primates. Effect of dietary cholesterol level. J. Lipid Res. 24: 343-356. (Pubitemid 13094280)
9. Rudel, L. L., T. Mitamura, and J. M. Felts. 1973. Characterization of rabbit lymph chylomicra and very low density lipoproteins. Circulation. 252: 47-48.
10. Hellman, L., E. L. Frazell, and R. S. Rosenfeld. 1960. Direct measurement of cholesterol absorption via the thoracic duct in man. J. Clin. Invest. 39: 1288-1294.
11. Rudel, L. L., M. D. Morris, and J. M. Felts. 1972. The transport of exogenous cholesterol in the rabbit. I. Role of cholesterol ester of lymph chylomicra and lymph very low density lipoproteins in absorption. J. Clin. Invest. 51: 2686-2692.
12. Hillyard, L. A., C. Entenman, I. L. Chaikoff, and W. O. Reinhardt. 1958. Composition and concentration of lymph and serum lipoproteins during fat and cholesterol absorption in the dog. J. Biol. Chem. 233: 838-842.
13. Imaizumi, K., M. Fainaru, and R. J. Havel. 1978. Composition of proteins of mesenteric lymph chylomicrons in the rat and alterations produced upon exposure of chylomicrons to blood serum and serum proteins. J. Lipid Res. 19: 712-722. (Pubitemid 9006234)
14. Chang, C. C., H. Y. Huh, K. M. Cadigan, and T. Y. Chang. 1993. Molecular cloning and functional expression of human acyl-coenzyme A:cholesterol acyltransferase cDNA in mutant Chinese hamster ovary cells. J. Biol. Chem. 268: 20747-20755. (Pubitemid 23292243)
15. Cases, S., S. Novak, Y. W. Zheng, H. M. Myers, S. R. Lear, E. Sande, C. B. Welch, A. J. Lusis, T. A. Spencer, B. R. Krause, et al. 1998. ACAT-2, a second mammalian acyl-CoA:cholesterol acyltransferase. Its cloning, expression, and characterization. J. Biol. Chem. 273: 26755-26764. (Pubitemid 28471692)
16. Lee, R. G., M. C. Willingham, M. A. Davis, K. A. Skinner, and L. L. Rudel. 2000. Differential expression of ACAT1 and ACAT2 among cells within liver, intestine, kidney, and adrenal of nonhuman primates. J. Lipid Res. 41: 1991-2001. (Pubitemid 32038994)
17. Anderson, R. A., C. Joyce, M. Davis, J. W. Reagan, M. Clark, G. S. Shelness, and L. L. Rudel. 1998. Identification of a form of acyl-CoA:cholesterol acyltransferase specific to liver and intestine in nonhuman primates. J. Biol. Chem. 273: 26747-26754. (Pubitemid 28471691)
18. Dreon, D. M., H. A. Fernstrom, H. Campos, P. Blanche, P. T. Williams, and R. M. Krauss. 1998. Change in dietary saturated fat intake is correlated with change in mass of large low-density-lipoprotein particles in men. Am. J. Clin. Nutr. 67: 828-836. (Pubitemid 28196655)
19. Rudel, L. L., J. Haines, J. K. Sawyer, R. Shah, M. S. Wilson, and T. P. Carr. 1997. Hepatic origin of cholesteryl oleate in coronary artery atherosclerosis in African green monkeys. Enrichment by dietary monounsaturated fat. J. Clin. Invest. 100: 74-83. (Pubitemid 27311245)
20. Rudel, L. L., J. S. Parks, L. Hedrick, M. Thomas, and K. Williford. 1998. Lipoprotein and cholesterol metabolism in diet-induced coronary artery atherosclerosis in primates. Role of cholesterol and fatty acids. Prog. Lipid Res. 37: 353-370. (Pubitemid 28475001)
21. Klein, R. L., and L. L. Rudel. 1983. Effect of dietary cholesterol level on the composition of thoracic duct lymph lipoproteins isolated from nonhuman primates. J. Lipid Res. 24: 357-367. (Pubitemid 13094281)
22. Dawson, P. A., and L. L. Rudel. 1999. Intestinal cholesterol absorption. Curr. Opin. Lipidol. 10: 315-320. (Pubitemid 29419688)
23. Goodman, D. S. 1962. The metabolism of chylomicron cholesterol ester in the rat. J. Clin. Invest. 41: 1886-1896.
24. Gage, S. H., and P. A. Fish. 1924. Fat digestion, absorption, and assimulation in man and animals as determined by the dark-field microscope, and a fat-soluble dye. Am. J. Anat. 34: 1-85.
25. Buhman, K. K., M. Accad, S. Novak, R. S. Choi, J. S. Wong, R. L. Hamilton, S. Turley, and R. V. Farese, Jr. 2000. Resistance to diet-induced hypercholesterolemia and gallstone formation in ACAT2-deficient mice. Nat. Med. 6: 1341-1347. (Pubitemid 32001017)
26. Rudel, L. L., K. Kelley, J. K. Sawyer, R. Shah, and M. D. Wilson. 1998. Dietary monounsaturated fatty acids promote aortic atherosclerosis in LDL receptor null, human apoB100 overexpressing transgenic mice. Arterioscler. Thromb. Vasc. Biol. 18: 1818-1827. (Pubitemid 28521074)
27. Kieft, K. A., T. M. A. Bocan, and B. R. Krause. 1991. Rapid on-line determination of cholesterol distribution among plasma lipoproteins after high-performance gel filtration chromatography. J. Lipid Res. 32: 859-866.
28. Temel, R. E., L. Hou, L. L. Rudel, and G. S. Shelness. 2007. ACAT2 stimulates cholesteryl ester secretion in apoB-containing lipoproteins. J. Lipid Res. 48: 1618-1627. (Pubitemid 47312023)
29. Temel, R. E., R. G. Lee, K. L. Kelley, M. A. Davis, R. Shah, J. K. Sawyer, M. D. Wilson, and L. L. Rudel. 2005. Intestinal cholesterol absorption is substantially reduced in mice deficient in both ABCA1 and ACAT2. J. Lipid Res. 46: 2423-2431. (Pubitemid 41532530)
30. Wang, D. Q-H., and M. C. Carey. 2003. Measurement of intestinal cholesterol absorption by plasma and fecal dual-isotope ratio, mass balance, and lymph fistula methods in the mouse: an analysis of direct versus indirect methodologies. J. Lipid Res. 44: 1042-1059. (Pubitemid 37279664)
31. Ionac, M. 2003. One technique, two approaches, and results: thoracic duct cannulation in small laboratory animals. Microsurgery. 23: 239-245. (Pubitemid 36835591)
32. 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.
33. Iverson, S. J., S. L. Lang, and M. H. Cooper. 2001. Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids. 36: 1283-1287. (Pubitemid 34007983)
34. Fiske, C. H., and Y. Subbarow. 1925. The colorimetric determination of phosphorus. J. Biol. Chem. 66: 375-400.
35. Fidge, N. H., and P. J. McCullagh. 1981. Studies on the apoproteins of rat lymph chylomicrons: characterization and metabolism of a new chylomicron-associated apoprotein. J. Lipid Res. 22: 138-146. (Pubitemid 11144713)
36. Lee, R. G., R. Shah, J. K. Sawyer, R. L. Hamilton, J. S. Parks, and L. L. Rudel. 2005. ACAT2 contributes cholesteryl esters to newly secreted VLDL, whereas LCAT adds cholesteryl ester to LDL in mice. J. Lipid Res. 46: 1205-1212. (Pubitemid 43109835)
37. Lee, R. G., K. L. Kelley, J. K. Sawyer, R. V. Farese, Jr., J. S. Parks, and L. L. Rudel. 2004. Plasma cholesterol esters provided by lecithin:cholesterol acyltransferase and acyl-coenzyme A:cholesterol acyltransferase 2 have opposite atherosclerotic potential. Circ. Res. 95: 998-1004. (Pubitemid 39532330)
38. Alger, H. M., J. M. Brown, J. K. Sawyer, K. L. Kelley, R. Shah, M. D. Wilson, M. C. Willingham, and L. L. Rudel. 2010. Inhibition of acyl-coenzyme A:cholesterol acyltransferase 2 (ACAT2) prevents dietary cholesterol-associated steatosis by enhancing hepatic triglyceride mobilization. J. Biol. Chem. 285: 14267-14274.
39. Repa, J. J., K. K. Buhman, R. B. Farese, Jr., J. M. Dietschy, and S. D. Turley. 2004. ACAT2 deficiency limits cholesterol absorption in the cholesterol-fed mouse: impact on hepatic cholesteol homeostasis. Hepatology. 40: 1088-1097. (Pubitemid 39425564)
40. 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.
41. Turley, S. D., M. A. Valasek, J. J. Repa, and J. M. Dietschy. 2010. Multiple mechanisms limit the accumulation of unesterifi ed cholesterol in the small intestine of mice deficient in both ACAT2 and ABCA1. Am. J. Physiol. Gastrointest. Liver Physiol. 299: G1012-G1022.
42. Turkish, A. R., A. L. Henneberry, D. Cromley, M. Padamsee, P. Oelkers, H. Bazzi, A. M. Christiano, J. T. Billheimer, and S. L. Sturley. 2005. Identification of two novel human acyl-CoA wax alcohol acyltransferases: members of the diacylglycerol acyltransferase 2 (DGAT2) gene superfamily. J. Biol. Chem. 280: 14755-14764. (Pubitemid 40562823)
43. Temel, R. E., A. K. Gebre, J. S. Parks, and L. L. Rudel. 2003. Compared with acyl-CoA:cholesterol O-acyltransferase (ACAT)1 and lecithin:cholesterol acyltransferase, ACAT2 displays the greatest capacity to differentiate cholesterol from sitosterol. J. Biol. Chem. 278: 47594-47601. (Pubitemid 37523203)
44. Davis, H. R., Jr., L. J. Zhu, L. M. Hoos, G. Tetzloff, M. Maguire, J. Liu, X. Yao, S. P. Iyer, M. H. Lam, E. G. Lund, et al. 2004. Niemann-Pick C1 Like 1 (NPC1L1) is the intestinal phytosterol and cholesterol transporter and a key modulator of whole-body cholesterol homeostasis. J. Biol. Chem. 279: 33586-33592. (Pubitemid 39063007)
45. Bell 3rd, T. A., J. M. Brown, M. J. Graham, K. M. Lemonidis, R. M. Crooke, and L. L. Rudel. 2006. Liver-specific inhibition of acyl-coenzyme a:cholesterol acyltransferase 2 with antisense oligonucleotides limits atherosclerosis development in apolipoprotein B100-only low-density lipoprotein receptor-/- mice. Arterioscler. Thromb. Vasc. Biol. 26: 1814-1820. (Pubitemid 44305335)
46. Field, F. J., K. Watt, and S. N. Mathur. 2008. Origins of intestinal ABCA1-mediated HDL-cholesterol. J. Lipid Res. 49: 2605-2619.
47. Field, F. J., and S. N. Mathur. 1983. beta-sitosterol: esterification by intestinal acylcoenzyme A:cholesterol acyltransferase (ACAT) and its effect on cholesterol esterification. J. Lipid Res. 24: 409-417 (Pubitemid 13094286)