Abstract
Caveolae form the terminus for a major pathway of intracellular free cholesterol (FC) transport. Caveolin mRNA levels in confluent human skin fibroblasts were up-regulated following increased uptake of low density lipoprotein (LDL) FC. The increase induced by FC was not associated with detectable change in mRNA stability, indicating that caveolin mRNA levels were mediated at the level of gene transcription. A total of 924 bp of 5' flanking region of the caveolin gene were cloned and sequenced. The promoter sequence included three G+C-rich potential sterol regulatory elements (SREs), a CAAT sequence and a Sp1 consensus sequence. Deletional mutagenesis of individual SRE-like sequences indicated that of these two (at -646 and -395 bp) were essential for the increased transcription rates mediated by LDL-FC, whereas the third was inconsequential. Gel shift analysis of protein binding from nuclear extracts to these caveolin promoter DNA sequences, together with DNase I footprinting, confirmed nucleoprotein binding to the SRE-like elements as part of the transcriptional response to LDL-FC. A supershift obtained with antibody to SRE-binding protein 1 (SPEBP-1) indicated that this protein binds at -395 bp. There was no reaction at -395 bp with anti-Sp1 antibody nor with either antibody at -646 bp. The cysteine protease inhibitor N-acetyl-leu-leu-norleucinal (ALLN), which inhibits SREBP catabolism, superinhibited caveolin mRNA levels regardless of LDL-FC. This finding suggests that SREBP inhibits caveolin gene transcription in contrast to its stimulating effect on other promoters. The findings of this study are consistent with the postulated role for caveolin as a regulator of cellular FC homeostasis in quiescent peripheral cells, and the coordinate regulation by SREBP of FC influx and efflux.
MeSH Terms
Base Sequence
CCAAT-Enhancer-Binding Proteins
Caveolin 1
Caveolins
Cells, Cultured
Cholesterol, LDL/physiology
DNA
DNA Footprinting
DNA-Binding Proteins/genetics
Helix-Loop-Helix Motifs
Humans
Membrane Proteins/genetics
Molecular Sequence Data
Mutagenesis
Nuclear Proteins/genetics
Promoter Regions, Genetic
Sequence Deletion
Sterol Regulatory Element Binding Protein 1
Transcription Factors
Transcription, Genetic
Up-Regulation
Chemicals
CAV1 protein, human
CCAAT-Enhancer-Binding Proteins
Caveolin 1
Caveolins
Cholesterol, LDL
DNA-Binding Proteins
Membrane Proteins
Nuclear Proteins
SREBF1 protein, human
Sterol Regulatory Element Binding Protein 1
Transcription Factors
DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bist A
Cardiovascular Research Institute, University of California, San Francisco, CA 94143, USA.
Fielding P E
Fielding C J
References (27)
27 references, click to expand
-
Letter: Enzymatic determination of cholesterol in high-density lipoprotein fractions prepared by polyanion precipitation.
Clin Chem. 1976 May;22(5):695
PMID: 177229
-
Intracellular cholesterol transport.
J Lipid Res. 1997 Aug;38(8):1503-21
PMID: 9300773
-
An apo-E-free very low density lipoprotein enriched in phosphatidylethanolamine in human plasma.
J Biol Chem. 1986 Apr 25;261(12):5233-6
PMID: 3957923
-
Sterol-dependent repression of low density lipoprotein receptor promoter mediated by 16-base pair sequence adjacent to binding site for transcription factor Sp1.
J Biol Chem. 1988 Mar 5;263(7):3372-9
PMID: 3277969
-
Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells.
Nucleic Acids Res. 1989 Aug 11;17(15):6419
PMID: 2771659
-
Regulation of the mevalonate pathway.
Nature. 1990 Feb 1;343(6257):425-30
PMID: 1967820
-
Minimally modified low density lipoprotein stimulates monocyte endothelial interactions.
J Clin Invest. 1990 Apr;85(4):1260-6
PMID: 2318980
-
Mechanism of transfer of LDL-derived free cholesterol to HDL subfractions in human plasma.
Biochemistry. 1990 Nov 20;29(46):10469-74
PMID: 2271659
-
The sequence of human caveolin reveals identity with VIP21, a component of transport vesicles.
FEBS Lett. 1992 Dec 7;314(1):45-8
PMID: 1360410
-
ADD1: a novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation.
Mol Cell Biol. 1993 Aug;13(8):4753-9
PMID: 8336713
-
SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis.
Cell. 1994 Apr 8;77(1):53-62
PMID: 8156598
-
Identification of a 6-base pair element involved in the sterol-mediated transcriptional regulation of farnesyl diphosphate synthase.
J Biol Chem. 1994 Oct 7;269(40):25212-8
PMID: 7929210
-
Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation.
J Cell Biol. 1994 Dec;127(5):1185-97
PMID: 7962084
-
Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae.
J Biol Chem. 1994 Dec 9;269(49):30745-8
PMID: 7982998
-
Independent regulation of sterol regulatory element-binding proteins 1 and 2 in hamster liver.
Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):935-8
PMID: 7862668
-
Reduction of caveolin and caveolae in oncogenically transformed cells.
Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1381-5
PMID: 7877987
-
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. 1995 Jul 7;270(27):16395-401
PMID: 7608210
-
Digging into caveolae.
Science. 1995 Sep 8;269(5229):1398-9
PMID: 7660120
-
Molecular cloning and functional analysis of the promoter of the human squalene synthase gene.
J Biol Chem. 1995 Sep 15;270(37):21958-65
PMID: 7665618
-
De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin.
Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8655-9
PMID: 7567992
-
Plasma membrane caveolae mediate the efflux of cellular free cholesterol.
Biochemistry. 1995 Nov 7;34(44):14288-92
PMID: 7578031
-
Oxysterols present in atherosclerotic tissue decrease the expression of lipoprotein lipase messenger RNA in human monocyte-derived macrophages.
J Clin Invest. 1996 Jan 15;97(2):461-8
PMID: 8567968
-
A direct role for sterol regulatory element binding protein in activation of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene.
J Biol Chem. 1996 May 24;271(21):12247-53
PMID: 8647822
-
Sterol-regulated release of SREBP-2 from cell membranes requires two sequential cleavages, one within a transmembrane segment.
Cell. 1996 Jun 28;85(7):1037-46
PMID: 8674110
-
Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae.
Biochemistry. 1996 Nov 26;35(47):14932-8
PMID: 8942658
-
Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers.
Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3753-8
PMID: 9108050
-
DNA sequencing with chain-terminating inhibitors.
Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7
PMID: 271968