Secretion of triacylglycerol-poor VLDL particles from McA-RH7777 cells expressing human hepatic lipase

Hepatic lipase (HL) plays a role in the catabolism of apolipoprotein (apo)B-containing lipoproteins through its lipolytic and ligand-binding properties. We describe a potential intracellular role of HL in the assembly and secretion of VLDL. Transient or stable expression of HL in McA-RH7777 cells resulted in decreased (by 40%) incorporation of [3H]glycerol into cell-associated and secreted triacylglycerol (TAG) relative to control cells. However, incorporation of [35S]methionine/cysteine into cell and medium apoB-100 was not decreased by HL expression. The decreased 3H-TAG synthesis/secretion in HL expressing cells was not attributable to decreased expression of genes involved in lipogenesis. Fractionation of medium revealed that the decreased [3H]TAG from HL expressing cells was mainly attributable to decreased VLDL. Expression of catalytically-inactive HL (HLSG) (Ser-145 at the catalytic site was substituted with Gly) in the cells also resulted in decreased secretion of VLDL-[3H]TAG. Examination of lumenal contents of microsomes showed a 40% decrease in [3H]TAG associated with lumenal lipid droplets in HL or HLSG expressing cells as compared with control. The microsomal membrane-associated [3H]TAG was decreased by 50% in HL expressing cells but not in HLSG expressing cells. Thus, expression of HL, irrespective of its lipolytic function, impairs formation of VLDL precursor [3H]TAG in the form of lumenal lipid droplets. These results suggest that HL expression in McA-RH7777 cells result in secretion of [3H]TAG-poor VLDL. Hepatic lipase (HL) plays a role in the catabolism of apolipoprotein (apo)B-containing lipoproteins through its lipolytic and ligand-binding properties. We describe a potential intracellular role of HL in the assembly and secretion of VLDL. Transient or stable expression of HL in McA-RH7777 cells resulted in decreased (by 40%) incorporation of [3H]glycerol into cell-associated and secreted triacylglycerol (TAG) relative to control cells. However, incorporation of [35S]methionine/cysteine into cell and medium apoB-100 was not decreased by HL expression. The decreased 3H-TAG synthesis/secretion in HL expressing cells was not attributable to decreased expression of genes involved in lipogenesis. Fractionation of medium revealed that the decreased [3H]TAG from HL expressing cells was mainly attributable to decreased VLDL. Expression of catalytically-inactive HL (HLSG) (Ser-145 at the catalytic site was substituted with Gly) in the cells also resulted in decreased secretion of VLDL-[3H]TAG. Examination of lumenal contents of microsomes showed a 40% decrease in [3H]TAG associated with lumenal lipid droplets in HL or HLSG expressing cells as compared with control. The microsomal membrane-associated [3H]TAG was decreased by 50% in HL expressing cells but not in HLSG expressing cells. Thus, expression of HL, irrespective of its lipolytic function, impairs formation of VLDL precursor [3H]TAG in the form of lumenal lipid droplets. These results suggest that HL expression in McA-RH7777 cells result in secretion of [3H]TAG-poor VLDL. HL is a 65 kDa glycoprotein that is synthesized and secreted primarily from parenchymal cells of the liver (1Martin G.A. Busch S.J. Meredith G.D. Cardin A.D. Blankenship D.T. Mao S.J. Rechtin A.E. Woods C.W. Racke M.M. Schafer M.P. Isolation and cDNA sequence of human postheparin plasma hepatic triglyceride lipase.J. Biol. Chem. 1988; 263: 10907-10914Abstract Full Text PDF PubMed Google Scholar). Once secreted, HL is bound, via heparan sulfate proteoglycans (HSPG), to the surfaces of hepatic sinusoids, the external surfaces of hepatocyte microvilli in the space of Disse and in interhepatocyte spaces (2Sanan D.A. Fan J. Bensadoun A. Taylor J.M. Hepatic lipase is abundant on both hepatocyte and endothelial cell surfaces in the liver.J. Lipid Res. 1997; 38: 1002-1013Abstract Full Text PDF PubMed Google Scholar). As a member of the triglyceride lipase gene family that includes LPL and endothelial lipase (EL), HL plays a central role in lipoprotein metabolism and atherosclerosis. Like LPL and EL, HL has a number of functional domains including the serine-aspartic acid-histidine catalytic triad, a lipid-binding surface loop shielding the catalytic pocket, and heparin binding domains (3Yu W. Hill J.S. Mapping the heparin-binding domain of human hepatic lipase.Biochem. Biophys. Res. Commun. 2006; 343: 659-665Crossref PubMed Scopus (13) Google Scholar, 4Stahnke G. Sprengel R. Augustin J. Will H. Human hepatic triglyceride lipase: cDNA cloning, amino acid sequence and expression in a cultured cell line.Differentiation. 1987; 35: 45-52Crossref PubMed Scopus (64) Google Scholar). 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In humans, HL deficiency is associated with increased plasma concentrations of HDL as well as TAG-rich apolipoprotein (apo)B-containing lipoproteins, and also an increased prevalence of premature atherosclerosis (7Breckenridge W.C. Little J.A. Alaupovic P. Wang C.S. Kuksis A. Kakis G. Lindgren F. Gardiner G. Lipoprotein abnormalities associated with a familial deficiency of hepatic lipase.Atherosclerosis. 1982; 45: 161-179Abstract Full Text PDF PubMed Scopus (232) Google Scholar, 8Hegele R.A. Little J.A. Vezina C. Maguire G.F. Tu L. Wolever T.S. Jenkins D.J. Connelly P.W. Hepatic lipase deficiency. Clinical, biochemical, and molecular genetic characteristics.Arterioscler. Thromb. 1993; 13: 720-728Crossref PubMed Scopus (216) Google Scholar, 9Ruel I.L. Couture P. Cohn J.S. Bensadoun A. Marcil M. Lamarche B. Evidence that hepatic lipase deficiency in humans is not associated with proatherogenic changes in HDL composition and metabolism.J. 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Metabolism of lipoproteins containing apolipoprotein B in hepatic lipase-deficient mice.J. Lipid Res. 1998; 39: 1661-1668Abstract Full Text Full Text PDF PubMed Google Scholar). Studies with genetically modified mice, either through overexpression or inactivation of the human HL gene (LIPC), have also provided evidence for HL action in apoB-containing lipoprotein metabolism. Introducing HL deficiency into apoE-null or LDL receptor (LDLR)-null background results in increased plasma concentrations of apoB-containing lipoproteins, TAG, PL, and cholesterol (14Mezdour H. Jones R. Dengremont C. Castro G. Maeda N. Hepatic lipase deficiency increases plasma cholesterol but reduces susceptibility to atherosclerosis in apolipoprotein E-deficient mice.J. Biol. Chem. 1997; 272: 13570-13575Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar, 15Barcat D. Amadio A. Palos-Pinto A. Daret D. Benlian P. Darmon M. Berard A.M. Combined hyperlipidemia/hyperalphalipoproteinemia associated with premature spontaneous atherosclerosis in mice lacking hepatic lipase and low density lipoprotein receptor.Atherosclerosis. 2006; 188: 347-355Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar). On the other hand, overexpression of human HL in HL-null/LDLR-null background results in ∼60–70% reduction of plasma VLDL-associated TAG, PL, and cholesterol under chow or Western diet (16Dichek H.L. Qian K. Agrawal N. Divergent effects of the catalytic and bridging functions of hepatic lipase on atherosclerosis.Arterioscler. Thromb. Vasc. Biol. 2004; 24: 1696-1702Crossref PubMed Scopus (17) Google Scholar, 17Freeman L. Amar M.J. Shamburek R. B. S. Gonzalez-Navarro H. and ligand-binding functions of hepatic lipase atherosclerosis in LDL mice.J. Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar). expression of human HL in mice also results in reduction in plasma of TAG, PL, and cholesterol H. Nong Z. Amar M.J. Shamburek J. S. The ligand-binding of hepatic lipase the of atherosclerosis in mice.J. Biol. Chem. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). These in have a role for HL in plasma apoB-containing the HL action increases or the of atherosclerosis S. Gonzalez-Navarro H. Freeman L. Wagner E. Nong Z. Hepatic lipase, lipoprotein metabolism, and atherogenesis.Arterioscler. Thromb. Vasc. Biol. 2004; 24: 1750-1754Crossref PubMed Scopus (159) Google Scholar). the of the the role of HL in the catabolism of circulating lipoproteins, have that HL lipolytic activity H. of hepatic lipase to the and is associated with a decrease in Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, of hepatic of functional in the is the in its Biol. Chem. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar, M. Mao D. M.J. K. in lipase deficiency and 39: PubMed Scopus Google Scholar). The intracellular activity of HL has been the in cells of hepatic of functional in the is the in its Biol. Chem. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). In the present the that expression of HL in hepatic cells the assembly and secretion of VLDL. The of VLDL assembly is and of apoB-100 the M. Z. in and lipid hepatic VLDL assembly and PubMed Scopus Google Scholar). The VLDL is in through a is to form VLDL. In McA-RH7777 of TAG-rich VLDL is in K. G. Z. J. L. Z. assembly of low density lipoproteins containing apolipoprotein in McA-RH7777 Biol. Chem. 2002; Full Text Full Text PDF PubMed Scopus Google and the for VLDL is present in the microsomal in the form of lipid droplets M. S. H. J. M.M. D. Wang of the associated with human Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar, M. S. J. M.M. R.J. Wang Z. Expression of apolipoprotein in McA-RH7777 cells VLDL assembly and secretion under Lipid Res. 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However, is into the VLDL precursor is not is lipid or that the formation of from the present that or stable expression of HL, of its catalytic a on the formation of the assembly and secretion of TAG-rich lipoproteins under and from and from [35S]methionine/cysteine was from and from and from human HL and from and The apoB-100 or was in The and the from and The expression human HL was as R.J. Hill J.S. Z. The amino acid of the of human and hepatic lipase cell surface Lipid Res. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). The the catalytic HLSG in the site was into was by the The for was The HL was the to McA-RH7777 cells from the and cultured in containing and cell by with with either or or expression for human apolipoprotein in a cell Biol. Chem. Full Text PDF PubMed Google The stable with for HL the stable in HL cells with in a of for the cells cultured in for an to cell expressing HL or HLSG cultured for with with heparin The medium was as the to HL activity as a to K. N. S. plasma hepatic triacylglycerol hydrolysis of of lipid Biophys. PubMed Scopus (20) Google Scholar). The of into the was by The cells with medium heparin for The cells in and and the secreted HL as D. Isolation and of lipoproteins secreted by liver Biophys. PubMed Scopus Google and in The cell and medium on cell and to for with HL and lipid cells for the with [3H]glycerol in containing and and either with or lipids from cells and and by as K. Wang Z. Z. The assembly of low density lipoproteins in McA-RH7777 cells is by Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The associated with [3H]TAG and was by cells with for to with [35S]methionine/cysteine in the for Both and with and In heparin was in the The from the cells and and by for for and associated with the was by with [3H]glycerol for the and as K. G. Z. J. L. Z. assembly of low density lipoproteins containing apolipoprotein in McA-RH7777 Biol. Chem. 2002; Full Text Full Text PDF PubMed Scopus Google Scholar). The was to for to the microsomal The and lumenal of the as K. G. Z. J. L. Z. assembly of low density lipoproteins containing apolipoprotein in McA-RH7777 Biol. Chem. 2002; Full Text Full Text PDF PubMed Scopus Google Scholar). from the and by as with [3H]glycerol or [35S]methionine/cysteine for the as either present in the or the microsomal from cells into and other lipoproteins as K. Z. The activity of microsomal triglyceride is for of triglyceride microsomes in McA-RH7777 cells. for the assembly of low density Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). from and by as was following the was to was on the following The to of the in as The of control and HL expressing cells or control and HLSG expressing cells In the the potential role of HL on hepatic TAG-rich lipoprotein assembly and secretion was by or stable expression of wild-type or the catalytically-inactive form of HL in McA-RH7777 cells. stable that of HL the hydrolysis activity as a was in that the was low of HL was in the containing heparin not that the HL, as was mainly to R.J. Hill J.S. Z. The amino acid of the of human and hepatic lipase cell surface Lipid Res. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). of HL expression in the stable the and secretion of as by incorporation of [3H]glycerol under in the of and decreased On the other hand, or secretion of was not by HL expression that the [3H]TAG in HL cells was not to [3H]glycerol cells with [3H]glycerol for as as and also showed a decrease in [3H]glycerol incorporation into cell and medium [3H]TAG in HL expressing cells the decreased medium [3H]TAG not The decreased incorporation of [3H]glycerol into cell and medium [3H]TAG was also in McA-RH7777 cells with HL that the decrease in [3H]TAG in stable HL was not to an of HL expression. These evidence that expression of HL resulted in decreased and secretion of [3H]TAG in that of expression of HL not result in decreased or secretion of showed that incorporation of into cell-associated or medium apoB-100 was not was increased in HL expressing the in not or secretion of hepatic as a was by HL expression The decreased [3H]TAG secretion decrease in secretion the for secretion of VLDL HL of HL not decrease or secretion of with [35S]methionine/cysteine for and in the of and apoB-100 and from the cells and by by and by The of was by as the of cell of the We or not the decreased [3H]TAG secretion HL expression was attributable to the catalytic activity of the stable cell expressing a HL in at the catalytic site was substituted with As the HLSG secreted from the cells its hydrolysis activity However, showed that expression of the HLSG also resulted in decreased [3H]TAG secretion (by the to that of wild-type HL Fractionation of lipoproteins showed that the decreased [3H]TAG secretion from HL and HLSG cells was mainly attributable to decreased and (by and relative to control cells These results that expression of HL, of its catalytic decreased of as or from HL or HLSG cells was as compared with control cells has been A.D. and hepatic lipase the uptake of Biol. Chem. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, S.J. S. Bensadoun A. Taylor J.M. binding and uptake of lipoproteins by hepatic cells in Biol. Chem. Full Text PDF PubMed Google Scholar, role for proteoglycans in and PubMed Scopus Google that HL the secreted TAG-rich lipoproteins on the cell or not the decreased from HL or HLSG cells was attributable to HL, in the of heparin to HL cell surface the of [3H]TAG from the HL or HLSG was increased as compared with result that a of secreted VLDL was on the surface of cells expressing either HL or However, as compared with the [3H]TAG from HL or HLSG cells was decreased Fractionation of lipoproteins secreted under also secretion of (by from HL or HLSG cells as compared with control of from HL or HLSG cells under heparin was as compared with control cells The of heparin in the not have an on incorporation of [3H]glycerol into cell-associated or not These that the secretion of HL expression in McA-RH7777 cells cultured under was of the catalytic activity of HL, and that the of secreted TAG-rich by cell HL not for the of in the the secretion of from HL expressing cells was also under in the of incorporation of [3H]glycerol into and was low and a 50% decrease in secretion from HL expression cells was with changes in secretion Thus, HL expression impairs secretion from McA-RH7777 cells under both and The of HL expression on VLDL secretion was also by of As in of lipoproteins was HL expressing cells and lipoprotein of secreted from HLSG cells was to that from and the lipoprotein of secreted from HL, and control cells also These in with was in that HL expression on secretion the secretion of was The suggest that HL expression have an on VLDL assembly and an into the HL action the of HL expression on the formation of that for TAG-rich VLDL the M. S. H. J. M.M. D. Wang of the associated with human Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar, M. S. J. M.M. R.J. Wang Z. Expression of apolipoprotein in McA-RH7777 cells VLDL assembly and secretion under Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar). showed that with the of [3H]TAG with with density that of density lipoprotein was in control cells However, of [3H]TAG in was (by in cells expressing HL or These results that the expression of HL, of its catalytic resulted in formation of in On the other hand, of in was by HLSG expression and increased by HL expression As cells expressing HL decrease in incorporation of [3H]glycerol into cell-associated We or not expression of HLSG and HL and HLSG cells. As in HL expression decreased the of [3H]TAG in cells as compared with that in expression of the HLSG on [3H]glycerol incorporation into These in with the of formation of in HLSG suggest that i) the catalytic activity of HL was for the decreased incorporation of [3H]glycerol into cell and ii) of synthesized [3H]TAG into microsomal was HL irrespective of catalytic activity of the that HL expression results in of [3H]TAG into of synthesized [3H]TAG and microsomes as well as microsomal and microsomal the of of [3H]TAG into microsomes in HL expressing cells was decreased (by as compared with [3H]TAG was The decreased microsomal [3H]TAG in HL expressing cells in both microsomal and microsomal In HLSG expressing the decrease in [3H]TAG in the microsomal changes in [3H]TAG associated with microsomes or microsomal not The decreased lumenal [3H]TAG the decrease in [3H]TAG in HL and HLSG expressing cells These suggest that the formation of is to expression of the HL not the HL of synthesized microsomal and microsomal was by expressing of either HL or HLSG not The decrease in lumenal [3H]TAG in cells expressing HL or HLSG that HL a role in microsomes and the relative of [3H]TAG showed in and with microsomes in HL or HLSG expressing cells relative to expression of genes involved in VLDL and and and in cells expressing HL or As in expression of HL or HLSG not but the and These results in with the and secretion in cells expressing HL or HLSG The of was and increased in HL or HLSG expressing cells as compared with that in The relative expression of the gene involved in was also increased as compared with Thus, expression of HL or HLSG in McA-RH7777 cells not the and The present results in evidence that expression of the HL not the HL results in the secretion of VLDL with on apoB-100 of the VLDL from cells expressing HL of the catalytic is the of of VLDL results from the formation of in the form of M. S. H. J. M.M. D. Wang of the associated with human Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar, M. S. J. M.M. R.J. Wang Z. Expression of apolipoprotein in McA-RH7777 cells VLDL assembly and secretion under Lipid Res. Full Text Full Text PDF PubMed Scopus Google The decreased precursor the microsomal in HL expressing cells is not attributable to expression of HL of catalytic resulted in of synthesized into the into the microsomal These of to the HL in hepatic lipoprotein metabolism. Thus, in to the role of HL in hydrolysis and lipoprotein clearance through or HL also an intracellular role in the assembly and secretion of TAG-rich VLDL. The by HL, a that through the metabolism VLDL assembly and secretion to However, have been that a role in and of for VLDL assembly and secretion R. and expression of a cDNA a hepatic microsomal lipase that J. PubMed Scopus Google Scholar, V. B. M. R. R. triacylglycerol in Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar, B. R. triacylglycerol in Biophys. PubMed Scopus Google Scholar). Expression of has been to on the metabolism of hepatic and apoB-100 associated with VLDL. cells expressing triacylglycerol hydrolase increased of on [3H]TAG and in secreted and apoB-100 R. and expression of a cDNA a hepatic microsomal lipase that J. PubMed Scopus Google Scholar). Thus, expression of triacylglycerol hydrolase TAG-rich VLDL secretion through increased is via the evidence has been for namely expression resulted in decreased [3H]TAG in the cell and an decrease in [3H]TAG and apoB-100 secretion V. B. M. R. R. triacylglycerol in Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar). On the other hand, expression of on [3H]TAG or apoB-100 was B. R. triacylglycerol in Biophys. PubMed Scopus Google Scholar). The present is the that HL, a lipase, also TAG-rich VLDL by the of apoB-100 secretion of with decrease in apoB-100 has also been in in as liver inactivation of the in mice of hepatic by the PubMed Scopus Google Scholar). have that HL catalytic activity in the of hepatic of functional in the is the in its Biol. Chem. 2004; Full Text Full Text PDF PubMed Scopus Google and H. of hepatic lipase to the and is associated with a decrease in Biol. Chem. Full Text Full Text PDF PubMed Scopus Google the intracellular activity was that of the secreted of HL of into to secretion of hepatic of functional in the is the in its Biol. Chem. 2004; Full Text Full Text PDF PubMed Scopus Google a that in the and to S. M. Wong H. Hepatic lipase a of Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar). The of HL the a on of into microsomal for VLDL The by the HL the into microsomes is However, the present that the catalytic activity of HL is not for of have been that a role in intracellular HL of to involved in lipid binding or S. M. Wong H. Hepatic lipase a of Lipid Res. Full Text Full Text PDF PubMed Scopus Google Scholar). Lipid binding present HL site in lipoprotein lipase for and Lipid Res. Full Text Full Text PDF PubMed Google Scholar). has been that the functional of HL is associated with a microsomal M. of lipase PubMed Scopus Google Scholar). Thus, is to that microsomal HL with the or other lumenal of synthesized have that of into microsomal for VLDL the activity of M. M.M. J. Wong J.S. of the role of microsomal triglyceride in the liver of mice.J. PubMed Scopus Google Scholar). is or not HL the of the that its was not in HL expressing cells. hepatic including and HL, have been to a role in the that the of apoB-containing lipoproteins from the liver role for proteoglycans in and PubMed Scopus Google Scholar). The present that the HL in McA-RH7777 was to the cell surface in a the and lipoprotein of [3H]TAG and in the or of have that the HL synthesized lipoprotein on the cells and that of the secreted lipoproteins by HL is of its catalytic Thus, was to the that the reduction in from HL expressing cells was attributable to cell surface However, of [3H]TAG in cells and revealed that the cell surface binding of secreted VLDL not for the decrease in [3H]TAG in the the decreased [3H]TAG in the was the result of assembly and secretion of TAG-rich VLDL of of the is decreased of cell-associated but not in cells with HL, either or to the low cell [3H]TAG was attributable to decreased or incorporation of [3H]glycerol into cell was as as or a for reduction in cell-associated However, a decrease in cell [3H]TAG was not in cells expressing the a role that HL activity in cell [3H]TAG On the other hand, that expression of genes involved in was other expression of suggest a role for but HL expression to is to is the intracellular catalytic activity of HL by other potential of HL activity by a family of secreted has been L. S.J. Bensadoun A. M. S. cholesterol in liver via of and hepatic cholesterol Thromb. Vasc. Biol. PubMed Scopus Google Scholar). In the present cell have revealed an intracellular role of HL expression in the assembly and secretion of TAG-rich lipoproteins, and the of action of HL is of its The Wang for the for on and and for with apolipoprotein endothelial lipase catalytically-inactive HL heparin sulfate low density lipoprotein receptor lumenal lipid microsomal triglyceride triacylglycerol

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