Human acyl-coenzyme A:cholesterol acyltransferase expressed in Chinese hamster ovary cells: Membrane topology and active site location

Molecular Biology of the Cell

Volumn 14, Issue 6, 2003, Pages 2447-2460

  Lin, Song ^a   Lu, Xiaohui ^a   Chang, Catherine C Y ^a   Chang, Ta Yuan ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL ACYLTRANSFERASE; CHOLESTEROL ESTER; HEMAGGLUTININ; HISTIDINE; MONOCLONAL ANTIBODY; PROTEINASE; SERINE;

ACAT1 GENE; ACAT2 GENE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL MUTANT; CHO CELL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; GENE; GENE EXPRESSION; HYDROPHILICITY; HYDROPHOBICITY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ANIMALS; BINDING SITES; CELL MEMBRANE; CHO CELLS; CRICETINAE; DIGITONIN; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INDICATORS AND REAGENTS; SAPONINS; STEROL O-ACYLTRANSFERASE;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS;

EID: 0037632868     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-11-0725     Document Type: Article

References (42)

1. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J.D. (1994). Molecular Biology of the Cell, New York: Garland Publishing.
2. Anderson, R.A., Joyce, C., Davis, M., Reagan, J.W., Clark, M., Shelness, G.S., and Rudel, L.L. (1998). Identification of a form of acyl-CoA:cholesterol acyltransferase specific to liver and intestine in nonhuman primates. J. Biol. Chem. 273, 26747-26754.
3. Buhman, K.F., Accad, M., and Farese, R.V., Jr. (2000a). Mammalian acyl-CoA:cholesterol acyltransferases. Biochim. Biophys. Acta 1529, 142-154.
4. Buhman, K.K., Accad, M., Novak, S., Choi, R.S., Wong, J.S., Hamilton, R.L., Turley, S., and Farese, R.V., Jr. (2000b). Resistance to diet-induced hypercholesterolemia and gallstone formation in ACAT2-deficient mice. Nat. Med. 6, 1341-1347.
5. Buhman, K.K., Chen, H.C., and Farese, R.V., Jr. (2001). The enzymes of neutral lipid synthesis. J. Biol. Chem. 276, 40369-40372.
6. Cadigan, K.M., Heider, J.G., and Chang, T.Y. (1988). Isolation and characterization of Chinese hamster ovary cell mutants deficient in acyl-coenzyme A:cholesterol acyltransferase activity. J. Biol. Chem. 263, 274-282.
7. Cao, G., Goldstein, J.L., and Brown, M.S. (1996). Complementation of mutation in acyl-CoA:cholesterol acyltransferase (ACAT) fails to restore sterol regulation in ACAT-defective sterol-resistant hamster cells. J. Biol. Chem. 271, 14642-14648.
8. Cases, S., et al. (1998a). ACAT-2, a second mammalian acyl-CoA: cholesterol acyltransferase. Its cloning, expression, and characterization. J. Biol. Chem. 273, 26755-26764.
9. Cases, S., et al. (1998b). Identification of a gene encoding an acyl CoA:diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. Proc. Natl. Acad. Sci. USA 95, 13018-13023.
10. Chang, C.C.Y., et al. (2000). Immunological quantitation and localization of ACAT-1 and ACAT-2 in human liver and small intestines. J. Biol. Chem. 275, 28083-28092.
11. Chang, T.Y., Chang, C.C.Y., and Cheng, D. (1997). Acyl-coenzyme A:cholesterol acyltransferase. Annu. Rev. Biochem. 66, 613-638.
12. Chang, T.Y., Chang, C.C.Y., Lin, S., Yu, C., Li, B.L., and Miyazaki, A. (2001a). Roles of acyl-coenzyme A:cholesterol acyltransferase-1 and -2. Curr. Opin. Lipidol. 12, 289-296.
13. Chang, T.Y., Chang, C.C.Y., Lu, X.H., and Lin, S. (2001b). ACAT catalysis may be completed within the plane of the membrane: a working hypothesis. J. Lipid Res. 42, 1933-1938.
14. Chang, C.C.Y., Chen, J., Thomas, M.A., Cheng, D., Del Priore, V.A., Newton, R.S., Pape, M.E., and Chang, T.Y. (1995). Regulation and immunolocalization of acyl-coenzyme A:cholesterol acyltransferase in mammalian cells as studied with specific antibodies. J. Biol. Chem. 270, 29532-29540.
15. Chang, C.C.Y., Doolittle, G.M., and Chang, T.Y. (1986). Cycloheximide sensitivity in regulation of acyl coenzyme A:cholesterol acyltransferase activity in Chinese hamster ovary cells. I. Effect of exogenous sterols. Biochemistry 25, 1693-1699.
16. Chang, C.C.Y., Huh, H.Y., Cadigan, K.M., and Chang, T.Y. (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.
17. Chang, C.C.Y., Lee, C.Y.G., Chang, E.T., Cruz, J.C., Levesque, M.C., and Chang, T.Y. (1998). Recombinant human acyl-CoA:cholesterol acyltransferase-1 (ACAT-1) purified to essential homogeneity utilizes cholesterol in mixed micelles or vesicles in a highly cooperative manner. J. Biol. Chem. 273, 35132-35141.
18. Fu, D., Libson, A., Miercke, L.J., Weitzman, C., Nollert, P., Krucinski, J., and Stroud, R.M. (2000). Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486.
19. Guo, Z., Cromley, D., Billheimer, J.T., and Sturley, S.L. (2001). Identification of potential binding sites in yeast and human acyl-CoA sterol acyltransferases by mutagenesis of conserved sequences. J. Lipid Res. 42, 1282-1291.
20. Hofmann, K. (2000). A superfamily of membrane-bound O-acyltransferases with implications for Wnt signaling. Trends Biochem. Sci. 25, 111-112.
21. Hofmann, K., and Stoffel, W. (1993). Tmbase: a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 347, 166
22. Joyce, C.W., Shelness, G.S., Davis, M.A., Lee, R.G., Skinner, K., Anderson, R.A., and Rudel, L.L. (2000). ACAT1 and ACAT2 membrane topology segregates a serine residue essential for activity to opposite sides of the endoplasmic reticulum membrane. Mol. Biol. Cell 11, 3675-3687.
23. Kolodziej, P.A., and Young, R.A. (1991). Epitope tagging and protein surveillance. Methods Enzymol. 194, 509-519.
24. Lee, O., Chang, C.C.Y., Lee, W., and Chang, T.Y. (1998). Immunodepletion experiments suggest that acyl-coenzyme A:cholesterol acyltransferase-1(ACAT-1) protein plays a major catalytic role in adult human liver, adrenal gland, macrophages, and kidney, but not in intestines. J. Lipid Res. 39, 1722-1727.
25. Lee, R.G., Willingham, M.C., Davis, M.A., Skinner, K.A., and Rudel, L.L. (2000). Differential expression of ACAT1 and ACAT2 among cells within liver, intestine, kidney, and adrenal of nonhuman primates. J. Lipid Res. 41, 1991-2001.
26. Lin, S., Cheng, D., Liu, M.S., Chen, J., and Chang, T.Y. (1999). Human acyl-CoA:cholesterol acyltransferase-1 in the endoplasmic reticulum contains seven transmembrane domains. J. Biol. Chem. 274, 23276-23285.
27. Lodish, H., Berk, A., Zipursky, S.L., Matsudaira, P., Baltimore, D., and Darnell, J. (1999). Molecular Cell Biology, 4th ed. Scientific American Books. New York, NY: W. H. Freeman and Co.
28. Lu, X., Lin, S., Chang, C. C. Y. and Chang, T. Y. (2002a). Mutagenesis studies on ACAT1 reveal several residues, but not S269, that may be essential for ACAT catalysis (Abstract). The 3rd AHA National Conference on Atherosclerosis, Thrombosis, and Vascular Biology, Salt Lake City, UT.
29. Lu, X., Lin, S., Chang, C.C.Y., and Chang, T.Y. (2002b). Mutant acyl-coenzyme A:cholesterol acyltransferase 1 (ACAT1) devoid of cysteine residues remains catalytically active. J. Biol. Chem. 276, 711-718.
30. Macri, J., and Adeli, K. (1997). Studies on intracellular translocation of apolipoprotein B in a permeabilized HepG2 system. J. Biol. Chem. 272, 7328-7337.
31. Meiner, V.L., et al. (1996). Disruption of the acyl-CoA:cholesterol acyltransferase gene in mice: evidence suggesting multiple cholesterol esterification enzymes in mammals. Proc. Natl. Acad. Sci. USA 93, 14041-14046.
32. Meiner, V.L., Tam, C., Gunn, M.D., Dong, L.M., Weisgraber, K.H., Novak, S., Myers, H.M., Erickson, S.K., and Farese, R.V., Jr. (1997). Tissue expression studies of mouse acyl CoA:cholesterol acyltransferase gene (Acact): findings supporting the existence of multiple cholesterol esterification enzymes in mice. J. Lipid Res. 38, 1928-1933.
33. Oelkers, P., Behari, A., Cromley, D., Billheimer, J.T., and Sturley, S.L. (1998). Characterization of two human genes encoding acyl coenzyme A:cholesterol acyltransferase-related enzymes. J. Biol. Chem. 273, 26765-26771.
34. Otto, J.C., and Smith, W.L. (1994). The orientation of prostaglandin endoperoxide synthases-1 and -2 in the endoplasmic reticulum. J. Biol. Chem. 269, 19868-19875.
35. Picot, D., Loll, P.J., and Garavito, R.M. (1994). The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1. Nature 367, 243-249.
36. Rost, B., Casadio, R., Fariselli, P., and Sander, C. (1995). Prediction of helical transmembrane segments at 95% accuracy. Protein Sci. 4, 521-533.
37. Rudel, L., Lee, R., and Cockman, T. (2001). Structure, function, and regulation of ACAT. Curr. Opin. Lipidol. 12, 121-127.
38. Sakashita, N., Miyazaki, A., Takeya, M., Horiuchi, S., Chang, C.C.Y., Chang, T.Y., and Takahashi, K. (2000). Localization of human acyl-coenzyme A:cholesterol acyltransferase-1 in macrophages and in various tissues. Am. J. Pathol. 156, 227-236.
39. Spady, D.K., Willard, M.N., and Meidell, R.S. (2000). Role of acyl-coenzyme A:cholesterol acyltransferase-1 in the control of hepatic very low density lipoprotein secretion and low density lipoprotein receptor expression in the mouse and hamster. J. Biol. Chem. 275, 27005-27012.
40. Yagyu, H., et al. (2000). Absence of ACAT-1 attenuates atherosclerosis but causes dry eye and cutaneous xanthomatosis in mice with congenital hyperlipidemia. J. Biol. Chem. 275, 21324-21330.
41. Yu, C., Chen, J., Lin, S., Liu, J., Chang, C.C.Y., and Chang, T.Y. (1999). Human acyl-CoA:cholesterol acyltransferase-1 is a homotetrameric enzyme in intact cells and in Vitro. J. Biol. Chem. 274, 36139-36145.
42. Yu, C., Zhang, Y., Lu, X., Chen, J., Chang, C.C.Y., and Chang, T.Y. (2002). The role of the N-terminal hydrophilic domain of acyl coenzyme A:cholesterol acyltransferase 1 on the enzyme's quaternary structure and catalytic efficiency. Biochemistry 41, 3762-3769.