Original Article
Increased High-Density Lipoprotein Levels Caused by a Common Cholesteryl-Ester Transfer Protein Gene Mutation
N Engl J Med 1990; 323:1234-1238November 1, 1990
- Abstract
- Abstract
Background and Methods.
The plasma cholesteryl-ester transfer protein (CETP) catalyzes the transfer of cholesteryl esters from high-density lipoprotein (HDL) to other lipoproteins. We recently described a Japanese family with increased HDL levels and CETP deficiency due to a splicing defect of the CETP gene. To assess the frequency and phenotype of this condition, we screened 11 additional families with high HDL levels by means of a radioimmunoassay for CETP and DNA analysis.
Results.
We found the same CETP gene mutation in four families from three different regions of Japan. Analysis of Restriction-Fragment Length polymorphisms of the mutant CETP allele showed that all probands were homozygous for the identical haplotype. Family members homozygous for CETP deficiency (n = 10) had moderate hypercholesterolemia (mean total cholesterol level [±SD], 7.01±0.83 mmol per liter), markedly increased levels of HDL cholesterol (4.24±1.01 mmol per liter) and apolipoprotein A-I, and decreased levels of low-density lipoprotein cholesterol (1.99±0.80 mmol per liter) and apolipoprotein B. Members heterozygous for the deficiency (n = 20), whose CETP levels were in the lower part of the normal range, had moderately increased levels of HDL cholesterol and apolipoprotein A-I and an increased ratio of HDL subclass 2 to HDL subclass 3, as compared with unaffected family members (1.5±0.8 vs. 0.7±0.4). CETP deficiency was not found in six unrelated subjects with elevated HDL cholesterol levels who were from different parts of the United States.
Conclusions.
CETP deficiency appears to be a frequent cause of increased HDL levels in the population of Japan, possibly because of a founder effect. The results that we observed in heterozygotes suggest that CETP normally plays a part in the regulation of levels of HDL subclass 2. There was no evidence of premature atherosclerosis in the families with CETP deficiency. In fact, the lipoprotein profile of persons with CETP deficiency is potentially antiatherogenic and may be associated with an increased life span. (N Engl J Med 1990; 323:1234–8.)
Article Activity
- Article
MOST prospective epidemiologic studies have found an inverse correlation between levels of high-density lipoprotein (HDL) and the incidence of atherosclerotic cardiovascular disease.1 , 2 Although HDL levels are known to be decreased by obesity, cigarette smoking, male sex, and diets high in polyunsaturated fat,1 , 3 the mechanisms of variation of HDL levels in populations are poorly understood. Studies in twins suggest that genetic factors play an important part in the determination of HDL cholesterol levels.4 In small populations, the levels of HDL have been found to correlate positively with lipoprotein lipase activity and negatively with hepatic lipase activity.4 , 5 Another factor that may regulate HDL levels is plasma cholesteryl-ester transfer protein (CETP).
The plasma CETP, a hydrophobic glycoprotein with a relative molecular mass of 74,000, facilitates the transfer of cholesteryl esters from their site of synthesis in HDL to lipoproteins containing apolipoprotein B.6 7 8 Recently, we described a family with increased HDL levels and CETP deficiency due to a point mutation (G→A) in the splice donor site (position +1) of intron 14 of the CETP gene — a mutation known to prevent normal processing of RNA and to yield a null phenotype.9
We now show that the identical CETP gene mutation is present in four additional Japanese families with increased HDL levels, including a previously identified family with unusual longevity and increased HDL levels.10 The lipoprotein phenotype of CETP deficiency, which is characterized by both increased levels of HDL and decreased levels of low-density lipoprotein (LDL), appears to have strong antiatherogenic potential.
Methods
Subjects
To identify additional families with CETP deficiency, we screened 11 unrelated families with increased HDL levels from various regions of Japan, as well as six subjects from different parts of the United States. These subjects were attending lipid clinics to which they had been referred for evaluation of increased plasma levels of total cholesterol or HDL cholesterol. The only criterion for inclusion in this study was that an individual subject or a family member should have a primary increase in the HDL cholesterol level (>2.6 mmol per liter).
Five Japanese families, including the family originally described,9 , 11 were found to have inherited CETP deficiency as determined by a radioimmunoassay for the protein.9 The first family was from Kanazawa, located in the middle of the main island of Japan (Honshu). Data on some members of this family had been reported previously.9 Further analysis revealed that the proband's parents were first cousins. We obtained data on 14 other family members. In tracing back three generations of the family, we identified two obligate heterozygotes who had had long lives (87 and 97 years). The second family found to have CETP deficiency was from Morioka, in the northeast of the main Japanese island. The dead members of this family were previously reported to have a mean 10-year prolongation of the life span, as compared with an appropriate control population.10 The proband's mother, who is heterozygous for the G→A mutation, is now 100 years old and healthy. The other three families have not previously been described. The third and fourth families were from Hiroshima, located in the southeast of the main island. The members of the third family had a high incidence of cerebral vascular attacks in the sixth or seventh decade of life. The proband had a cerebral infarction at the age of 50. In view of the presence of a small low-density area in his right internal capsule on CT scanning, he probably had a lacunar stroke, which can occur without cerebral atherosclerosis. On coronary angiography, he had only mild coronary ectasia without any stenotic lesions. Mild hypertension (150/90 mm Hg) and a moderately increased lipoprotein(a) level (23.8 mg per deciliter) were apparent risk factors for the cerebral vascular attack. The fifth family was from a rural district near Kanazawa. A marriage between first cousins had also occurred in this family. The probands of the fourth and fifth families were healthy.
Ten healthy subjects with normal lipid levels (five men and five women) were selected from among patients at Kanazawa University. To determine haplotype frequency in Japan, we obtained DNA from 15 unrelated Japanese subjects who came from different regions of Japan.
Analysis of Lipids and Apolipoproteins
Cholesterol and triglyceride concentrations were determined enzymatically in plasma obtained after a 12-hour fast.12 , 13 Plasma levels of apolipoprotein A-I and apolipoprotein B were determined by immunologic methods.14 , 15 HDL cholesterol was measured after heparin—calcium chloride precipitation of the apolipoprotein B—containing lipoproteins from 100 μl of plasma (final concentration, 47.6 mg per deciliter and 23.8 mM, respectively) with a commercial kit (Nihon-Syoji, Osaka, Japan).16 , 17 This method was validated by comparison of values for HDL cholesterol determined by both precipitation and analytic ultracentrifugation (range for HDL cholesterol, 0.78 to 2.07 mmol per liter)17 or by precipitation and agarose-gel chromatography (HDL cholesterol, >2.07 mmol per liter).11 To determine the ratio of HDL2 to HDL3, native (non—sodium dodecyl sulfate) gradient polyacrylamide-gel electrophoresis on a 4 to 30 percent gel (Pharmacia, Piscataway, N.J.) was carried out with plasma prestained with Sudan black, and the result was analyzed by densitometric scanning.9 To quantitate CETP mass, plasma samples were analyzed by a radioimmunoassay using 125I-labeled monoclonal antibodies (TP2) in a competitive-displacement assay18 and by immunoaffinity purification and analysis with Western immunoblotting.9
DNA Analysis
Genomic DNA was extracted from white cells according to a modified method of Triton X-100 lysis.19 The G→A mutation in the first position of intron 14 of the CETP gene was revealed by in vitro amplification of genomic DNA by the polymerase chain reaction and direct sequencing of the amplified product by means of an internal primer, exactly as described elsewhere.9
The haplotype of the CETP gene in each subject homozygous for CETP deficiency was determined by analysis of restriction-fragmentlength polymorphisms (RFLPs). DNA (10 μg) was digested independently with TaqI or StuI and then analyzed by Southern blotting and probed with the CETP complementary DNA (cDNA). The full-length cDNA (1581 bp [base pairs]) was used to detect TaqI polymorphism,20 21 22 and a PstI—PvuII 732-bp fragment of the CETP cDNA was used to detect the StuI polymorphism.23 We also identified a new polymorphism of the CETP gene. This BamHI polymorphism in intron 9 (29 nucleotides downstream of the exon 9—intron 9 boundary) was evaluated after polymerase-chain-reaction amplification. Polymerase-chain-reaction assays were carried out with intron 8 primer P1 (5′-TTGTTGAATGAGTGAAAGCC-3′) and intron 9 primer P2 (5′-CACCAAGTTTCCGAGTTTCC-3′).24 The amplified DNA was digested with BamHI and analyzed by 2.0 percent agarose-gel electrophoresis. The polymorphic site generated either 390-bp or 460-bp fragments.
Statistical Analysis
Haplotype categories were combined to calculate chi-square values for the two-by-two contingency table (i.e., either positive or negative status for haplotype II). The exact probability of the occurrence of the observed frequencies was computed with Fisher's exact test (two-tailed). Analysis of variance with eight quantitative variables for lipids and apolipoproteins was performed by one-way analysis. Comparisons between the four study groups (homozygotes, heterozygotes, unaffected family members, and controls) were done with the use of t-tests. Linear regression analysis was done with Slide-Write Plus (Advanced Graphics Software, Sunnyvale, Calif.). All calculated P values are two-tailed. Group data are reported as means ±SD.
Results
CETP was found to be absent in at least one member of the second through the fifth families with increased HDL levels (hyperalphalipoproteinemia). The same G→A mutation at the 5′ splice donor of intron 14 (position +1) of the CETP gene was found in each case. When the members of these four families and the additional members of the first family9 were included in the analysis, 10 subjects were found to be homozygous for the deficiency, 20 were heterozygous, and 16 were unaffected. Although this small screening effort revealed CETP deficiency in 4 of 11 Japanese families with elevated HDL cholesterol levels, no evidence of CETP deficiency (in terms of mass or activity) was found in the 6 unrelated subjects with increased HDL cholesterol levels (3.10 to 5.28 mmol per liter) from different parts of the United States.
These findings suggest that CETP deficiency may be a common cause of increased HDL levels in the Japanese population. To determine whether these features were due to a single progenitor or represented independent origins of the mutation, we performed CETP-gene haplotype analysis in each subject homozygous for CETP deficiency. Table 1Table 1
Results of CETP-Gene Haplotype Analysis in Family Members Homozygous for CETP Deficiency and Controls. summarizes the haplotypes based on four different RFLPs in subjects with CETP deficiency and in controls from different regions of Japan. The frequencies of TaqI RFLPs in the Japanese controls were not significantly different from the frequencies previously observed in U.S. and Norwegian populations.21 , 22 In contrast to the findings in the control subjects, all five homozygotes in five unrelated families were homozygous for haplotype II, representing 10 alleles with haplotype II. There was a strong association (i.e., linkage disequilibrium) between the mutant allele and haplotype II (P = 0.0068), a finding consistent with the existence of a common progenitor with a single mutation.Lipoprotein and apolipoprotein levels in the five families with CETP deficiency are shown in Table 2Table 2
Lipid, Apolipoprotein, and CETP Levels in Five Families with CETP Deficiency and Japanese Normolipidemic Controls.*. In subjects homozygous for CETP deficiency (n = 10), there was a marked increase in HDL cholesterol and apolipoprotein A-I levels. The HDL cholesterol levels were three to four times higher than in unaffected family members and the unrelated Japanese controls, and the apolipoprotein A-I levels were approximately twice as high. Also, there was a pronounced decrease in LDL cholesterol and apolipoprotein B levels in the homozygotes. Four of 10 homozygotes had mild hypertriglyceridemia (triglycerides >1.69 mmol per liter). CETP was not detected in any of the homozygotes on either radioimmunoassay or immunoaffinity purification and Western blotting using an anti-CETP monoclonal antibody.The mean HDL cholesterol and apolipoprotein A-I levels in the heterozygous group (n = 20) were significantly higher than those in the Japanese controls (Table 2). CETP levels in the heterozygotes were significantly lower than those in the unaffected family members (1.4±0.3 vs. 2.3±0.6 mg per liter; P<0.001). However, all but one of the heterozygotes had CETP levels that overlapped the normal range (1.0 to 3.4 mg per liter [mean ±2 SD]). As compared with values in the unaffected family members, the mean CETP mass of the heterozygotes was decreased by 39 percent, their HDL cholesterol level was increased by 0.34 mmol per liter, and their apolipoprotein A-I level was increased by 0.25 g per liter. Furthermore, the HDL2/HDL3 ratio was increased in the heterozygotes as compared with the unaffected family members (1.5±0.8 vs. 0.7±0.4; P = 0.017). These results imply that HDL2 levels are increased twofold to threefold in heterozygotes.
Correlational analysis of lipoprotein and CETP levels revealed a strong inverse relation between CETP levels and the ratio of the HDL2 level to the sum of HDL2 and HDL3 levels (Fig. 1Figure 1
CETP Level Plotted against the Ratio of HDL2 to the Sum of HDL2 and HDL3.). When homozygotes, heterozygotes, unaffected family members, and unrelated controls were included in the analysis, the correlation coefficient (r) was −0.790 (P<0.001). The correlation was also observed when homozygotes were excluded from the analysis (r = −0.539, P<0.001). A positive correlation was found between CETP and LDL cholesterol levels (r = 0.517, P<0.001) (Fig. 2Figure 2
CETP Level Plotted against the Plasma LDL Cholesterol Level.) and was also observed when homozygotes were excluded from the analysis (r = 0.428, P<0.02). Similarly, a significant correlation was found between the CETP and apolipoprotein B levels (r = 0.445, P<0.01).An inverse correlation between plasma levels of triglycerides and of HDL cholesterol has usually been observed in different populations. This correlation was found in an analysis of the heterozygotes and unaffected family members in the present study (r = −0.560, P<0.001). However, there was no inverse relation between plasma triglyceride and HDL cholesterol levels in the homozygotes, even though their plasma triglyceride levels encompassed a wide range (0.71 to 4.85 mmol per liter).
Discussion
In this report, we describe five families with increased HDL levels due to an identical mutation of the CETP gene. There was complete concordance between the homozygous G→A mutation, the absence of CETP, and the marked increase in HDL levels in these families, proving that the G→A mutation of the first position of intron 14 of the CETP gene is the cause of CETP deficiency and increased HDL levels. The findings also indicate that this mutation is a common cause of increased HDL levels among the Japanese, possibly due to a founder effect (the principle that when a small group establishes itself as a separate and isolated entity, it carries only a fraction of the genetic variability of the parent population). The lipoprotein profile of a person with CETP deficiency is potentially antiatherogenic, and a striking number of members of the families we have studied have had an increased life span. Like familial hypobetalipoproteinemia,25 CETP deficiency may represent an antiatherogenic mutation.
The pronounced increase in HDL cholesterol levels in persons homozygous for the CETP deficiency indicates that CETP is required for the normal catabolism of HDL cholesteryl esters. The increase in apolipoprotein A-I is probably secondary to the increase in HDL cholesterol and could be due to delayed catabolism of enlarged HDL particles. Comparison of the lipoprotein values in heterozygotes and controls gives some potential insights into the role of CETP in the normal physiology of lipoproteins. In the heterozygotes whom we studied, mean HDL cholesterol levels were moderately increased as compared with those in the controls. More impressive were the more-than-twofold increase in the HDL2/HDL3 ratio in heterozygotes as compared with controls and the strong inverse correlation between the CETP level and the ratio of HDL2 to the sum of HDL2 and HDL3 (Fig. 1). These findings imply that CETP has a major effect on the determination of HDL2 levels. The increased levels of apolipoprotein A-I but not apolipoprotein A-II in heterozygotes10 , 11 are also consistent with this suggestion, since HDL2 contains a much higher ratio of apolipoprotein A-I to apolipoprotein A-II than does HDL3.
The marked increase in HDL2 in CETP deficiency suggests that this lipoprotein subclass is the preferred donor in the cholesteryl-ester transfer process. Normally, CETP exchanges HDL2 cholesteryl esters with triglycerides from other lipoproteins, particularly when plasma triglyceride levels rise, as in the postprandial state. The triglyceride-rich HDL2 may then be converted into the smaller HDL3 as a result of the activity of hepatic lipase — e.g., during fasting. The interconversion of HDL2 to HDL3 can be mediated in vitro by the sequential activities of CETP and hepatic lipase.5 The present results suggest that CETP has a physiologically important role in the conversion of HDL2 into HDL3.
In homozygous CETP deficiency the usual inverse relation between triglyceride and HDL cholesterol levels is disrupted. This indicates that the well-known inverse relation of high plasma levels of triglycerides and low levels of HDL cholesterol26 , 27 is due to neutral lipid transfer (triglyceride—cholesteryl ester exchange) between very-low-density lipoprotein and HDL mediated by CETP.
Another striking finding was the decreased level of LDL cholesterol and apolipoprotein B in homozygotes. The mean levels of apolipoprotein B and LDL cholesterol in subjects homozygous for CETP deficiency were similar to those in subjects heterozygous for hypobetalipoproteinemia caused by mutations in the apolipoprotein B gene.25 Furthermore, the CETP level had a significant positive correlation with LDL cholesterol and apolipoprotein B levels in all groups studied (r = 0.517 and r = 0.445, respectively). There are several potential explanations for an effect of CETP on LDL. The rate of transfer of cholesteryl esters from HDL to precursor lipoproteins that eventually form LDL could influence the steady-state level of LDL cholesterol. An increased movement of apolipoprotein E from HDL to triglyceride-rich particles has been observed when CETP activity is inhibited.28 Low CETP levels could allow the precursor particles to become enriched with apolipoprotein E, increasing their clearance through hepatic LDL receptors and reducing LDL formation. Also, in CETP deficiency there could be enhanced clearance of LDL due to increased activity of LDL receptors, caused by reduced return to the liver of cholesteryl ester in chylomicron and very-low-density lipoprotein remnants.
The 10 subjects homozygous for CETP deficiency had no evidence of premature atherosclerosis although they had hypercholesterolemia. Indeed, a trend toward longevity was found in two families with CETP deficiency, including the documentation of the deficiency in a 100-year-old heterozygote. These anecdotal findings suggesting a protective effect of CETP deficiency against atherosclerosis will need to be confirmed. In contrast to the findings in CETP deficiency, the increase in HDL due to hepatic lipase deficiency causes an increase in triglyceride-enriched HDL2 and is associated with premature atherosclerosis that is possibly due to accumulation of intermediate-density lipoproteins.29 Thus, not all of the factors increasing HDL levels are associated with protection against atherosclerosis.
Supported by grants (HL-22682 and HL-21006) from the National Institutes of Health, the Scientific Research Grants (No. 63480187) of the Education Ministry of Japan, and a grant from Kanae Foundation of Research for New Medicine.
We are indebted to Kikuo Yasuda, M.D., and Yasuhiko Hirata, M.D., for providing clinical information and blood samples for the third and fifth families, respectively.
Source Information
From the Division of Molecular Medicine, Department of Medicine, Columbia University, College of Physicians and Surgeons, New York (A.I., M.L.B., C.B.H., L.B.A., A.R.T.); the Second Department of Internal Medicine, Kanazawa University School of Medicine, Kanazawa, Japan (A.I., J.K., H.M.); the Department of Internal Medicine, Hiroshima Railway Hospital, Hiroshima, Japan (K.T.); and the First Department of Internal Medicine, Iwate Medical University, Morioka, Japan (Y.M.). Address reprint requests to Dr. Tall at the Division of Molecular Medicine, Department of Medicine, Columbia University College of Physicians and Surgeons, 630 W. 168th St., New York, NY 10032.
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