Caveolin-1 and regulation of cellular cholesterol homeostasis

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 291, Issue 2, 2006, Pages

  Frank, Philippe G ^a,b   Cheung, Michelle W C ^a   Pavlides, Stephanos ^a,b   Llaverias, Gemma ^a,b   Park, David S ^a   Lisanti, Michael P ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Atherosclerosis; High density lipoprotein; Lipoproteins; Macrophages

Indexed keywords

ABC TRANSPORTER A1; ACYL COENZYME A; CAVEOLIN 1; CHOLESTEROL; CHOLESTEROL ACYLTRANSFERASE; GLIBENCLAMIDE; HIGH DENSITY LIPOPROTEIN; METHYL BETA CYCLODEXTRIN; SPHINGOLIPID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL SURFACE; CHOLESTEROL ESTERIFICATION; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; EXPERIMENTAL MODEL; FIBROBLAST; HEART MUSCLE; HOMEOSTASIS; IMMUNOFLUORESCENCE MICROSCOPY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SKELETAL MUSCLE; STATISTICAL ANALYSIS; WESTERN BLOTTING;

ANIMALS; APOLIPOPROTEINS A; BLOTTING, WESTERN; CAVEOLIN 1; CHOLESTEROL; CHOLESTEROL ESTERS; CHOLESTEROL, HDL; CHOLESTEROL, LDL; FIBROBLASTS; HOMEOSTASIS; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 33746855808     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01092.2005     Document Type: Article

References (55)

1. Babitt J, Trigatti B, Rigotti A, Smart EJ, Anderson RG, Xu S, and Krieger M. Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acylated and colocalizes with plasma membrane caveolae. J Biol Chem 272: 13242-13249, 1997.
2. Baorto DM, Gao Z, Malaviya R, Dustin ML, van der Merwe A, Lublin DM, and Abraham SN. Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature 389: 636-639, 1997.
3. Bist A, Fielding PE, and Fielding CJ. Two sterol regulatory element-like sequences mediate up-regulation of caveolin gene transcription in response to low density lipoprotein free cholesterol. Proc Natl Acad Sci USA 94: 10693-10698, 1997.
4. Bligh EG and Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem 37: 911-917, 1959.
5. Breuza L, Corby S, Arsanto JP, Delgrossi MH, Scheiffele P, and Le Bivic A. The scaffolding domain of caveolin 2 is responsible for its Golgi localization in Caco-2 cells. J Cell Sci 115: 4457-4467, 2002.
6. Brown MS and Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340, 1997.
7. Chawla A, Boisvert WA, Lee C, Laffitte BA, Barak Y, Joseph SB, Liao D, Nagy L, Edwards PA, Curtiss LK, Evans RM, and Tontonoz P. A PPARgamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol Cell 7: 161-171, 2001.
8. Everson WV and Smart EJ. Caveolae and the regulation of cellular cholesterol homeostasis. In: Caveolae and Lipid Rafts: Roles in Signal Transduction and the Pathogenesis of Human Diseases, edited by Lisanti MP and Frank PG: Elsevier, 2005, p. 37-55.
9. Fielding CJ, Bist A, and Fielding PE. Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers. Proc Natl Acad Sci USA 94: 3753-3758, 1997.
10. Fielding PE and Fielding CJ. Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae. Biochemistry 35: 14932-14938, 1996.
11. Fielding PE and Fielding CJ. Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry 34: 14288-14292, 1995.
12. Francis GA, Knopp RH, and Oram JF. Defective removal of cellular cholesterol and phospholipids by apolipoprotein A-I in Tangier disease. J Clin Invest 96: 78-87, 1995.
13. Frank PG, Galbiati F, Volonte D, Razani B, Cohen DE, Marcel YL, and Lisanti MP. Influence of caveolin-1 on cellular cholesterol efflux mediated by high-density lipoproteins. Am J Physiol Cell Physiol 280: C1204-C1214, 2001.
14. Frank PG, Lee H, Park DS, Tandon NN, Scherer PE, and Lisanti MP. Genetic ablation of caveolin-1 confers protection against atherosclerosis. Arterioscler Thromb Vasc Biol 24: 98-105, 2004.
15. Frank PG and Lisanti MP. Caveolin-1 and caveolae in atherosclerosis: differential roles in fatty streak formation and neointimal hyperplasia. Curr Opin Lipidol 15: 523-529, 2004.
16. Frank PG, Marcel YL, Connelly MA, Lublin DM, Franklin V, Williams DL, and Lisanti MP. Stabilization of caveolin-1 by cellular cholesterol and scavenger receptor class B type I. Biochemistry 41: 11931-11940, 2002.
17. Fujimoto T, Kogo H, Ishiguro K, Tauchi K, and Nomura R. Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J Cell Biol 152: 1079-1086, 2001.
18. Gargalovic P and Dory L. Caveolin-1 and caveolin-2 expression in mouse macrophages. High density lipoprotein 3-stimulated secretion and a lack of significant subcellular co-localization. J Biol Chem 276: 26164-26170, 2001.
19. Gargalovic P and Dory L. Caveolins and macrophage lipid metabolism. J Lipid Res 44: 11-21, 2003.
20. Gocze PM and Freeman DA. Factors underlying the variability of lipid droplet fluorescence in MA-10 Leydig tumor cells. Cytometry 17: 151-158, 1994.
21. Graf GA, Connell PM, Van der Westhuyzen DR, and Smart EJ. The class B, type I scavenger receptor promotes the selective uptake of high density lipoprotein cholesterol ethers into caveolae. J Biol Chem 274: 12043-12048, 1999.
22. Hailstones D, Sleer LS, Parton RG, and Stanley KK. Regulation of caveolin and caveolae by cholesterol in MDCK cells. J Lipid Res 39: 369-379, 1998.
23. Handel Fernandez ME and Lopez DM. Isolation of macrophages from tissues, fluids, and immune response sites. In: Manual of Macrophages Methodology, edited by Paulnock DM. Oxford, UK: Oxford Univ. Press, 2000, p. 1-30. [Practical Approach Series]
24. Horton JD. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis. Biochem Soc Trans 30: 1091-1095, 2002.
25. Ji Y, Jian B, Wang N, Sun Y, Moya MD, Phillips MC, Rothblat GH, Swaney JB, and Tall AR. Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux. J Biol Chem 272: 20982-20985, 1997.
26. Kiss AL, Turi A, Mullner N, and Timar J. Caveolin isoforms in resident and elicited rat peritoneal macrophages. Eur J Cell Biol 79: 343-349, 2000.
27. Klucken J, Buchler C, Orso E, Kaminski WE, Porsch-Ozcurumez M, Liebisch G, Kapinsky M, Diederich W, Drobnik W, Dean M, Allikmets R, and Schmitz G. ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc Natl Acad Sci USA 97: 817-822, 2000.
28. Langmann T, Klucken J, Reil M, Liebisch G, Luciani MF, Chimini G, Kaminski WE, and Schmitz G. Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem Biophys Res Commun 257: 29-33, 1999.
29. Llaverias G, Vazquez-Carrera M, Sanchez RM, Noe V, Ciudad CJ, Laguna JC, and Alegret M. Rosiglitazone upregulates caveolin-1 expression in THP-1 cells through a PPAR-dependent mechanism. J Lipid Res 45: 2015-2024, 2004.
30. Matveev S, Uittenbogaard A, van Der Westhuyzen D, and Smart EJ. Caveolin-1 negatively regulates SR-BI mediated selective uptake of high-density lipoprotein-derived cholesteryl ester. Eur J Biochem 268: 5609-5616, 2001.
31. Matveev S, van der Westhuyzen DR, and Smart EJ. Co-expression of scavenger receptor-BI and caveolin-1 is associated with enhanced selective cholesteryl ester uptake in THP-1 macrophages. J Lipid Res 40: 1647-1654, 1999.
32. McNeish J, Aiello RJ, Guyot D, Turi T, Gabel C, Aldinger C, Hoppe KL, Roach ML, Royer LJ, de Wet J, Broccardo C, Chimini G, and Francone OL. High density lipoprotein deficiency and foam cell accumulation in mice with targeted disruption of ATP-binding cassette transporter-1. Proc Natl Acad Sci USA 97: 4245-4250, 2000.
33. Mora R, Bonilha VL, Marmorstein A, Scherer PE, Brown D, Lisanti MP, and Rodriguez-Boulan E. Caveolin-2 localizes to the Golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J Biol Chem 274: 25708-25717, 1999.
34. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, and Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92: 10339-10343, 1995.
35. Nakamura K, Kennedy MA, Baldan A, Bojanic DD, Lyons K, and Edwards PA. Expression and regulation of multiple murine ATP-binding cassette transporter G1 mRNAs/isoforms that stimulate cellular cholesterol efflux to high density lipoprotein. J Biol Chem 279: 45980-45989, 2004.
36. Oram JF and Lawn RM. ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J Lipid Res 42: 1173-1179, 2001.
37. Orso E, Broccardo C, Kaminski WE, Bottcher A, Liebisch G, Drobnik W, Gotz A, Chambenoit O, Diederich W, Langmann T, Spruss T, Luciani MF, Rothe G, Lackner KJ, Chimini G, and Schmitz G. Transport of lipids from golgi to plasma membrane is defective in tangier disease patients and Abc1-deficient mice. Nat Genet 24: 192-196, 2000.
38. Ostermeyer AG, Paci JM, Zeng Y, Lublin DM, Munro S, and Brown DA. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J Cell Biol 152: 1071-1078, 2001.
39. Parolini I, Sargiacomo M, Galbiati F, Rizzo G, Grignani F, Engelman JA, Okamoto T, Ikezu T, Scherer PE, Mora R, Rodriguez-Boulan E, Peschle C, and Lisanti MP. Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the Golgi complex. J Biol Chem 274: 25718 -25725, 1999.
40. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, and Parton RG. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J Cell Biol 152: 1057-1070, 2001.
41. Puglielli L, Rigotti A, Greco AV, Santos MJ, and Nervi F. Sterol carrier protein-2 is involved in cholesterol transfer from the endoplasmic reticulum to the plasma membrane in human fibroblasts. J Biol Chem 270: 18723-18726, 1995.
42. Razani B, Combs TP, Wang XB, Frank PG, Park DS, Russell RG, Li M, Tang B, Jelicks LA, Scherer PE, and Lisanti MP. Caveolin-1 deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem 277: 8635-8647, 2001.
43. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, and Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138, 2001.
44. Oram JF, Trumbach B, Klima B, Lackner KJ, and Schmitz G. HDL-mediated efflux of intracellular cholesterol is impaired in fibroblasts from Tangier disease patients. Arterioscler Thromb Vasc Biol 15: 683-690, 1995.
45. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, and Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682, 1992.
46. Scherer PE, Lewis RY, Volonte D, Engelman JA, Galbiati F, Couet J, Kohtz DS, van Donselaar E, Peters P, and Lisanti MP. Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 272: 29337-29346, 1997.
47. Scherer PE, Tang Z, Chun M, Sargiacomo M, Lodish HF, and Lisanti MP. Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution. Identification and epitope mapping of an isoform-specific monoclonal antibody probe. J Biol Chem 270: 16395-16401, 1995.
48. Smart EJ, Ying Ys Donzell WC, and Anderson RGW. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271: 29427-29435, 1996.
49. Uittenbogaard A, Ying Y, and Smart EJ. Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J Biol Chem 273: 6525-6532, 1998.
50. Walter M, Gerdes U, Seedorf U, and Assmann G. The high density lipoprotein- and apolipoprotein A-I-induced mobilization of cellular cholesterol is impaired in fibroblasts from Tangier disease subjects. Biochem Biophys Res Commun 205: 850-856, 1994.
51. Wang L, Connelly MA, Ostermeyer AG, Chen HH, Williams DL, and Brown DA. Caveolin-1 does not affect SR-BI-mediated cholesterol efflux or selective uptake of cholesteryl ester in two cell lines. J Lipid Res 44: 807-815, 2003.
52. Wang N, Lan D, Chen W, Matsuura F, and Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc Natl Acad Sci USA 101: 9774-9779, 2004.
53. Wang N, Silver DL, Thiele C, and Tall AR. ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein. J Biol Chem 276: 23742-23747, 2001.
54. Williams TM and Lisanti MP. The caveolin proteins. Genome Biol 5: 214, 2004.
55. Zhou M, Parr RD, Petrescu AD, Payne HR, Atshaves BP, Kier AB, Ball JM, and Schroeder F. Sterol carrier protein-2 directly interacts with caveolin-1 in vitro and in vivo. Biochemistry 43: 7288-7306, 2004.