©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
Regulation of Murine Plasma Phospholipid Transfer Protein Activity and mRNA Levels by Lipopolysaccharide and High Cholesterol Diet (*)

(Received for publication, April 28, 1995; and in revised form, May 15, 1995 )

Xian-cheng Jiang (§) , Can Bruce

From the Division of Molecular Medicine, Department of Medicine, Columbia University, New York, New York 10032

ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
FOOTNOTES
ACKNOWLEDGEMENTS
REFERENCES

ABSTRACT

Plasma phospholipid transfer protein mediates the net movement of phospholipids between lipoproteins and between lipid bilayers and high density lipoprotein. In this study, the mouse phospholipid transfer protein cDNA was cloned by reverse transcription polymerase chain reactions based on the cDNA sequence of human phospholipid transfer protein. The predicted amino acid sequence of mouse phospholipid transfer protein shows the protein to be 476 amino acids long and to have a sequence identity of 83% with that of human phospholipid transfer protein. Mouse plasma phospholipid transfer protein activity is 1.5-2 times that of human plasma phospholipid transfer protein activity. As in humans, mouse peripheral tissues displayed a higher abundance of phospholipid transfer protein mRNA than observed in central organs. The order of phospholipid transfer protein mRNA expression was as follows: lung > adipose tissue, placenta, testis > brain > muscle, heart, liver. We examined the regulation of phospholipid transfer protein expression by dietary cholesterol and by bacterial lipopolysaccharide. A high fat, high cholesterol diet caused a significant increase (35%) in plasma phospholipid transfer protein activity and a significant increase (18%) in high density lipoprotein phospholipids. This increased activity was accompanied by 100% increase in phospholipid transfer protein mRNA in lung. After lipopolysaccharide injection, plasma phospholipid transfer protein activity was decreased by 66%. This decrease in activity was associated with a similar decrease in phospholipid transfer protein mRNA in lung, adipose tissue, and liver. The decrease in plasma phospholipid transfer protein activity was also associated with a significant increase (17%) in high density lipoprotein phospholipid concentration. The opposite changes in phospholipids levels with lipopolysaccharide treatment and dietary cholesterol despite similarly increased high density lipoprotein phospholipids levels indicate that high density lipoprotein phospholipids levels are likely determined both by phospholipid transfer protein levels and by gradients of phospholipids concentration between high density lipoprotein and other phospholipids sources.


INTRODUCTION

Plasma phospholipid transfer protein (PLTP)()transfers phospholipids among lipoprotein particles (1, 2, 3) and from lipid bilayers to high density lipoproteins (HDL)(1, 4) . There is accumulating evidence indicating that PLTP plays an important role in the remodeling of lipoproteins. In vitro experiments show that partially purified PLTP mediates both the transfer and exchange of phospholipids between triglyceride-rich lipoproteins and HDL during lipolysis(5) . PLTP can also cause conversion of HDL to larger (10.9 nm) and smaller (7.8 nm) particles in a time- and concentration-dependent fashion(6, 7) . PLTP activity also modulates the activities of lecithin cholesterol acyltransferase and cholesteryl ester transfer protein (CETP)(3, 9) . In in vivo experiments using partially purified PLTP injected into rats, the turnover rate of [C]phosphatidylcholine ether-labeled HDL increases by 50%. This suggests that PLTP can facilitate the transfer of radiolabeled phospholipid between HDL and tissues or that PLTP increases the rate of HDL uptake by these tissues(8) .

PLTP and CETP, a protein that transfers phospholipids as well as cholesteryl esters and triglycerides, each account for about 50% of the plasma phospholipid transfer activities(9) . Addition of PLTP to a cholesteryl ester transfer assay containing CETP results in a marked enhancement of CETP activity (3) by a mechanism that is most likely the enhanced binding of CETP to phospholipid-enriched HDL(9) . CETP activity plays a central role in HDL metabolism, and its transcription is up-regulated by dietary cholesterol(17) . These two proteins are evolutionarily related and are part of a gene family that also includes lipopolysaccharide binding protein (LBP) and bactericidal/permeability increasing protein(10, 11) . LBP and bactericidal/permeability increasing protein modulate the organism's response to bacterial infections by their ability to bind lipopolysaccharide(12, 13) . Recent studies suggest that CETP may also be involved in the acute phase response because it also binds lipopolysaccharide,()and its transcription is down-regulated by lipopolysaccharide treatment(15) . However, unlike CETP, LBP is markedly up-regulated by lipopolysaccharide treatment(14) .

Given the similarities among the members of the lipid transfer/lipopolysaccharide binding protein gene family, we investigated whether mouse PLTP is also regulated by dietary cholesterol and lipopolysaccharide. We chose the mouse as a model organism for two reasons. First, mouse plasma has no measurable CETP mass and so its plasma phospholipid transfer activity would be due solely to PLTP. This would simplify future studies on the phospholipid metabolism of this animal. Second, in order to lay the foundations of PLTP transgenesis and gene knock-out manipulations in mouse we need to characterize the structure, pattern of expression, and gene regulation of PLTP in the wild-type mouse. So, in this study we have isolated and characterized PLTP cDNA from C57BL/6 mouse and determined the tissue distribution of its mRNA. We indicate here that PLTP has a tissue distribution that is distinct from that of the other gene family member and that lipopolysaccharide and dietary cholesterol regulate its expression.


EXPERIMENTAL PROCEDURES

Mouse PLTP cDNA Cloning

First strand cDNA was synthesized from mouse lung mRNA using oligo(dT) as a primer. The mouse PLTP cDNA was amplified from total cDNA by primer extension and polymerase chain reactions (21) using rTth DNA polymerase (Perkin Elmer) and several degenerate primers based on the human PLTP cDNA sequence(10) . The amplified products were cloned into Bluescript KS- (Stratagene) and sequenced according to standard procedures.

RNA Isolation, Northern Blot Analysis, and RNase Protection Assay

Total RNA was isolated from various tissues using the lithium chloride/urea extraction method(18) . The integrity and quality of all RNA samples was determined by electrophoresis on agarose/borate gels before mRNA isolation. Polyadenylated RNA was isolated from total RNA by batch isolation using oligo(dT)-cellulose. Northern blot analysis of mRNA was performed as described previously(19) . A fragment of the human PLTP cDNA (112 base pairs, 1544-1655) was cloned into Bluescript SK+ (Stratagene) and used to prepare radiolabeled cRNA probes for the RNase protection assay, which was performed as described previously(17) .

PLTP Activity Measurement

Phospholipid transfer activity was measured with [H]dipalmitoylphosphatidylcholine (DPPC; DuPont NEN) -containing vesicles that were prepared as described previously(20) . Briefly, 10 µmol of egg phosphatidylcholine containing 10 nmol of [H]DPPC was dried under a stream of nitrogen, resuspended in 1 ml of a solution of 10 mM Tris, 150 mM NaCl, 1 mM EDTA, pH 7.4, was probe-sonicated, and then was centrifuged to remove lipid aggregates. Transfer of radiolabeled phospholipids was measured by incubating an aliquot of 100 µl of each sample with [H]DPPC vesicles (125 nmol of phosphatidylcholine) and HDL (250 µg of protein) in a final volume of 400 µl at 37 °C for 1 h. Vesicles were subsequently precipitated by the addition of 300 µl of a solution of 500 mM NaCl, 215 mM MnCl, 445 units/ml heparin, and the radioactivity of a 500-µl aliquot of the supernatant was measured.

Dietary Study

C57BL/6 mouse (males, 25-30 g, n = 6) had free access to food and water. They were fed either the high cholesterol, high fat diet (20% coconut oil, 1% cholesterol from Research Diets Inc. New Bruswick, NJ) or a standard laboratory diet (Purina Laboratory rodent chow 5001) for 1 week before being sacrificed.

Lipopolysaccharide Administration Study

C57BL/6 mouse (males, 25-30 g, n = 6) had free access to food and water. They were fed a standard laboratory diet (Chow 5001). Lipopolysaccharide (Escherichia coli 0127:B8, from Difco) was suspended in sterile saline. Stock lipopolysaccharide was sonicated and diluted just before use, at a dosage of 50 µg/animal. After 15 h, the animals were sacrificed.

Statistical Analysis

Differences between groups were tested by Student's t test. All analyses were performed with the Statworks® software. Significance levels given are those for the two-tailed test. Data are presented as mean ± S.D. Significant results were with p < 0.01 unless otherwise stated.


RESULTS

PLTP Gene Expression in Mouse

Although mice have negligible or no CETP activity, their PLTP activity is present. We measured PLTP activity in mice of three different strains. The PLTP activity in C57BL/6, C3H, and BALB/C mice were 220% (±15%), 205% (±10%), and 155% (±20%) of human plasma activity, respectively (n = 6 for each group).

The mouse PLTP cDNA was obtained by polymerase chain reaction amplification of lung cDNA using degenerate primers based on the human PLTP cDNA sequence(10) . The cDNA sequence and the predicted amino acid sequence of mouse PLTP are shown in Fig. 1. Both mouse and human PLTP leader sequences are 17 amino acids in length with 9 identical amino acids, conforming to the pattern of similarity among the signal sequences of PLTP, CETP, lipoprotein lipase, and apolipoproteins A-I, and A-IV that was described previously(10, 21) . Like human PLTP, the predicted mature mouse PLTP is 476 amino acids long with an 83% amino acid sequence identity (Fig. 1). At the nucleotide sequence level, the identity in the translated regions of the human and mouse genes is 86%, while the 3`-untranslated regions are divergent.


Figure 1: Alignment of mouse and human PLTP cDNA and mature protein. The amino acid sequence of the mature mouse PLTP derived from cDNA sequencing. m-DNA, mouse PLTP cDNA; h-DNA, human PLTP cDNA; m-aa, mouse PLTP amino acid sequence; h-aa, human PLTP amino acid sequence.



We determined the tissue distribution of PLTP mRNA in mouse (strain C57BL/6) by Northern blot analysis (Fig. 2). Hybridization of a PLTP probe to poly(A) mRNA isolated from various mouse tissues indicated the existence of a single transcript of approximately 1.8 kilobases, similar in length to that of human(10) . In another set of analyses, we used the RNase protection assay to measure PLTP mRNA concentration in lung, adipose tissue, and testis (Fig. 2C). The order of PLTP mRNA abundance is as follows: lung > adipose tissue, placenta > testis > brain > muscle > heart > kidney > liver > spleen.


Figure 2: Northern blot analysis of poly(A) RNA from various human tissues. Two µg/lane of poly(A) RNA from various mouse tissues was probed with a 749-base pair fragment (nucleotides 50-798 in Fig. 3) that was random primer-labeled. A and B, two set of Northern blot experiments; C, RNase protection assay for three tissues (30 µg of total RNA was used) using mouse 3`-PLTP cRNA as probe. For details see ``Experimental Procedures.''




Figure 3: RNase protection analysis of total RNA from human adipose tissue and heart. Fifty µg of total RNA from tissues was used for the RNase protection assay. See ``Experimental Procedures'' for details.



Because of the striking levels of PLTP mRNA expression in mouse adipose tissue, we investigated whether PLTP was also expressed in human adipose tissue. Human adipose tissue (from the heart) shows approximately 5 times as much PLTP mRNA expression as that seen in the heart (Fig. 3).

Regulations of PLTP Activity and mRNA Levels

Lipopolysaccharide Regulation

In order to evaluate the effects of lipopolysaccharide on PLTP gene expression, lipopolysaccharide was injected into mice at 50 µg/animal. This resulted in a marked decrease in plasma PLTP activity and profound reductions of PLTP mRNA in lung, adipose tissue, and liver (Fig. 4). In order to evaluate the effects of altered PLTP gene expression on the plasma lipoprotein response to lipopolysaccharide, we measured plasma lipid and lipoprotein concentrations. Lipopolysaccharide-treated animals had significantly higher HDL phospholipids and HDL cholesterol than controls (Table 1). Analysis by fast protein liquid chromatograph gel filtration of pooled mouse (n = 6) plasmas confirmed these observations (data not shown). By nondenaturing gradient gel electrophoresis, the HDL particles isolated by ultracentrifugation were increased in size (from 10.2 to 10.9 nm). However, apoA-I levels in such HDL from lipopolysaccharide-treated and control animals were unchanged while apoE was increased, as determined by SDS-polyacrylamide gel electrophoresis (data not shown). Although there was an increase of plasma triglyceride concentration, this did not reach statistical significance probably because of the low lipopolysaccharide dose used. The effect of lipopolysaccharide on PLTP plasma activity was not due to an interaction of lipopolysaccharide with PLTP because in an in vitro assay with mouse plasma there was no direct inhibition of transfer activity at lipopolysaccharide concentrations up to 0.3 µg/µl. We also verified that the amount of lipopolysaccharide used in the assay system did not influence the lipoprotein precipitability by heparin-Mn.


Figure 4: Regulations of PLTP activity and mRNA levels by lipopolysacchride administration. Three µl of mouse plasma was used for PLTP activity assay. Fifty µg of total RNA was used for RNase protection assay. PLTP activity assay, p < 0.001; RNase protection assay for liver, adipose tissue, and lung total RNA, p < 0.001, p < 0.01, p < 0.01, respectively.





Dietary Regulation

In order to determine whether there are alterations in PLTP activity and mRNA levels in response to dietary fat and cholesterol, mice were fed for 1 week a diet containing 20% coconut oil and 1% cholesterol, which has previously been shown to significantly increase CETP activity and mRNA in CETP transgenic mice (17) . In this study, plasma PLTP activity was significantly increased (35%) in response to the high fat and cholesterol diet (Fig. 5), but the increase of PLTP mRNA was observed only in lung, not in liver and adipose tissue (Fig. 5). The HDL-phospholipids and HDL-cholesterol were increased 18 and 50% respectively, while the cholesterol and phospholipid levels of the very low density and low density lipoprotein fraction was increased 300 and 60%, respectively (Table 1).


Figure 5: Regulations of PLTP activity and mRNA levels by high fat and high cholesterol diet. The PLTP activity assay and RNase protection assay were same as Fig. 4. PLTP activity assay, p < 0.02; RNase protection assay for liver RNA; RNase protection assay for adipose tissue RNA, p = 0.09; RNase protection assay for lung RNA, p < 0.01.




DISCUSSION

We have shown in this study that mouse and human PLTP have similar sequence and similar tissue distribution of mRNA production. The plasma activity is 1.5-2 times human levels. These findings suggest that the mouse will have utility as a model organism to study the role of PLTP in lipid metabolism. In mouse, as in human, extrahepatic tissues contribute to a large fraction of total PLTP mRNA production. It is likely that production of PLTP in these tissues is important in regulating phospholipid transfer to and from these tissues. Lung, adipose tissue, and testis were the tissues with the highest levels of PLTP expression. Although its PLTP expression ranks low among the tissues studied here, the large mass of liver means that this organ produces an appreciable amount of PLTP mRNA. Thus liver, adipose tissue and lung likely contribute to most of the total circulating PLTP mass.

PLTP belongs to LBP gene family(10) , but it has its own distinct structure, function, and regulatory patterns. Although evolutionarily PLTP is more similar to LBP and bactericidal/permeability increasing protein than to CETP(10) , functionally it is more similar to CETP in that both transfer phospholipids between lipoproteins(9, 16) . In its regulation by lipopolysaccharide, PLTP is also more similar to CETP than to LBP and bactericidal/permeability increasing protein since this agent down-regulates expression of both proteins. PLTP mRNA levels are responsive to dietary cholesterol, but the -fold increase and tissue-specific up-regulation are different from CETP (see below). Unlike CETP, whose cholestyl ester transfer activity is inhibitable by lipopolysaccharide(15) , PLTP activity is not inhibited by lipopolysaccharide. The regulatory mechanisms of PLTP appear to have differentiated during evolution from those of its family members so as to adapt to this protein's unique function.

The 35% increase in plasma PLTP activity in response to dietary cholesterol and fat is not comparable to the 5-10-fold increase observed with CETP in CETP transgenic mice(17) , but it is statistically significant (p < 0.02). A similar up-regulation is seen in rabbits in which, after administration of a cholesterol (0.15%) diet, PLTP activity is increased 12 and 50% depending on whether they are hyporesponsive and hyperresponsive to cholesterol, respectively(22) . Also different from CETP regulation by cholesterol that occurs in most tissues(17, 23) , PLTP mRNA level is up-regulated by cholesterol diet in lung but not in adipose tissue and liver. This would suggest that cholesterol up-regulatory transcription factors must have different interactions with tissue-specific factors for these two genes.

In this study, we found the HDL cholesterol and HDL phospholipid levels in mice treated with lipopolysaccharide were significantly elevated. These changes were due to an increase in HDL surface area rather than HDL particle number, because HDL size was increased while apoA-I content was not altered. HDL has been shown to be protective against endotoxic shock by binding lipopolysaccharide(24) . This is likely an adaptive response for the lipopolysaccharide-treated animal since larger HDL surface area would have greater lipopolysaccharide binding capacity/HDL particle(25) . Lipopolysaccharide treatment causes complex changes in lipoprotein metabolism resulting in large changes in lipoprotein profile. Many enzymes involved in HDL metabolism are influenced by lipopolysaccharide treatment; there are increases in serum amyloid protein (26) and probably hepatic lipase (27, 28) and decreases in lipoprotein lipase(29) , lecithin cholesterol acyltransferase(27) , CETP (in animals with CETP activity(15) ) and, as shown in this study, PLTP. Of these changes, none of them except that of PLTP could possibly increase HDL phospholipid. Thus, the increased HDL phospholipid that we observe here is likely due to decreased phospholipid transfer by PLTP from HDL. The decreased PLTP levels appear to play an important role in the altered quantities, sizes, and lipid distribution of lipoproteins during acute phase.

It is interesting to note that a dietary cholesterol and lipopolysaccharide treatment similarly regulate PLTP in mice and CETP in CETP transgenic mice(15, 17) . Similarly, these two proteins are induced in obese people by 15 and 35%, respectively, relative to nonobese people(30) . Also, it has been reported that cigarette smoking increases CETP and PLTP activities by 18 and 8%, respectively(31) . The correlation in CETP and PLTP activities may be due to the fact that removal of either cholesterol or phospholipid from a lipid membrane would disrupt an optimal phospholipid/cholesterol ratio. This disruption caused by removal of phospholipid by PLTP can be corrected either by a concomitant removal of cholesterol (which would result in decreased surface area) or an influx of phospholipid from another source. One mechanism by which cholesterol removal could accompany phospholipid transfer is the coordinate action of lecithin cholesterol acyltransferase and CETP. Another possible reason for the correlation of PLTP and CETP activities may be that processes that lead to a change in the surface area of lipoproteins would need to be coupled to mechanisms that change the core volume, either by neutral lipid transfer by CETP or by lipolysis. Whichever of these mechanisms is operating, phospholipid transfer can be expected to be interrelated with phospholipid and cholesterol metabolism. Since mice and rats do not have significant CETP activity it should be of interest to determine what alternative mechanisms of cholesterol removal are coupled to PLTP activity in these animals.

It is interesting to find that adipose tissue express PLTP mRNA at high levels in mice and humans. Adipose tissue also is a major site for CETP synthesis(32) . In hamster, a strong inverse correlation of adipose tissue CETP mRNA levels with the concentration of HDL cholesteryl esters suggests a role for locally synthesized CETP in the metabolism of HDL cholesteryl esters(32) . Locally synthesized PLTP in adipose tissue may also be involved in HDL metabolism, since CETP and PLTP activities are correlated in obese humans(30) . Adipose tissue is also a major site for lipoprotein lipase synthesis(33) . In vitro studies showed that PLTP mediates the transfer and exchange of phospholipids between triglyceride-rich lipoproteins and HDL during lipolysis(5) , suggesting a possible coordinated action of lipoprotein lipase and PLTP. Since PLTP, CETP, and lipoprotein lipase are highly expressed in the same tissues and together they play important roles in lipoprotein remodeling, their coordinated action in adipose tissue deserves further study.

In mice and humans, lung is a major tissue expressing PLTP mRNA. This suggests an important function of PLTP in the lung, most likely in surfactant production and metabolism. It was recently reported that HDL and LDL could stimulate primary cultures of type II pneumocytes to secrete phospholipids(34) . PLTP may facilitate uptake of secreted phospholipid by HDL in the interstitial fluid of the lung, as well as subsequent deposition of phospholipid into the alveolar membrane. Because lung was the only tissue among those examined that increased PLTP expression (100%) in response to a high fat and cholesterol diet and this was accompanied by a significant increase (30%) in plasma PLTP activity, this organ must be contributing significant amounts of plasma PLTP.

It has been suggested that PLTP is involved in the provision of substrate for lecithin cholesterol acyltransferase and/or transferring phospholipid-rich surface fragments from triglyceride-rich lipoproteins to HDL during catalyzed lipolysis(5) , i.e. that PLTP promotes HDL formation or increases HDL-phospholipid concentration. On the other hand, there is evidence from rats suggesting that PLTP enables either an increased uptake of HDL-phospholipid by tissues or an increased clearance of HDL particles(8) . Thus, whether PLTP activity leads to a net transfer into or out of HDL seems to depend on the physiological context. Our findings in this study also suggest the same, because although HDL phospholipid and HDL cholesterol increased in both lipopolysaccharide-treated animals and animals on a cholesterol diet, we find that the levels of PLTP under these two treatments change in opposite directions. Since the phospholipid contents of LDL+VLDL were essentially unchanged, the changes in PLTP levels must have influenced primarily the phospholipid fluxes to and from tissues. In a high fat and cholesterol diet, it may be advantageous for the animal to increase the phospholipid flow into tissues by increasing PLTP levels. Conversely, with lipopolysaccharide treatment, it may be more advantageous to limit phospholipid flow between HDL and tissues by decreasing PLTP concentrations. Because lipopolysaccharide treatment and dietary fat and cholesterol have complex effects, the understanding of the role that PLTP plays in lipid metabolism will have to await the study of animals whose PLTP expression is specifically altered. However, it appears likely that HDL-phospholipid levels are determined both by PLTP levels and by gradients of phospholipid concentration between HDL and other phospholipid sources.


FOOTNOTES

*
This work was supported by Grants HL54591 and HL43165 from the National Institutes of Health. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore by hereby marked ``advertisement'' in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank®/EMBL Data Bank with accession number(s) U28960[GenBank® Link].

§
To whom correspondence should be addressed: Div. of Molecular Medicine, Dept. of Medicine, Columbia University, 630 W. 168th St., New York, NY 10032. Tel.: 212-305-7720; Fax: 212-305-5052.

The abbreviations used are: PLTP, phospholipid transfer protein; HDL, high density lipoprotein; CETP, cholesteryl ester transfer protein; LBP, lipopolysaccharide binding protein; DPPC, dipalmitoylphosphatidylcholine; LDL, low density lipoprotein; VLDL, very low density lipoprotein.

P. S. Tobias, R. J. Ulevitch, P. Kussie, and A. Tall, unpublished observations.


ACKNOWLEDGEMENTS

We thank Dr. Alan Tall for his invaluable guidance and discussions which have made this work possible. The human heart and human adipose tissue samples were generous gifts from Dr. Jie Wang.


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