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The Journal of Lipid Research, Vol. 39, 228-232, January 1998
Copyright © 1998 by Lipid Research, Inc.

Rapid Communication

Hepatic lipase activity is lower in African American men than in white American men: effects of 5' flanking polymorphism in the hepatic lipase gene (LIPC)

Gloria Lena Vegaa, Luther T. Clarkb, Aylmer Tangb, Santica Marcovinac, Scott M. Grundya, and Jonathan C. Cohena
a The Center for Human Nutrition, Departments of Clinical Nutrition and Internal Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75235-9052
b The State University of New York Health Science Center at Brooklyn, Brooklyn, NY 11203
c Department of Medicine and Northwest Lipid Research Laboratories, The University of Washington, Seattle, WA 98103

Correspondence to: Jonathan C. Cohen.


  ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES

Plasma high density lipoprotein cholesterol (HDL-C) concentrations are higher in African American men than in white men, but the mechanism(s) responsible for this ethnic difference has not been elucidated. This study examined the relationship between hepatic lipase activity, plasma HDL-C concentrations, and a hepatic lipase polymorphism (-514T) in African American and white American men. Consistent with previous reports, plasma HDL-C concentrations were significantly higher in African American men than in white American men. Mean post-heparin plasma hepatic lipase activity was significantly lower in African American than in white American men (27 ± 12 vs. 44 ± 17 mmol · h-1 · l-1, P < 0.001). The -514T hepatic lipase allele was associated with low hepatic lipase activity in both populations, and was 3-fold more common among African Americans than white Americans.

Taken together, these data suggest that genetic differences in hepatic lipase activity contribute to the differences in plasma HDL-C concentrations between African American men and white American men.—Vega, G. L., L. T. Clark, A. Tang, S. Marcovina, S. M. Grundy, and J. C. Cohen. Hepatic lipase activity is lower in African American men than in white American men: effects of 5' flanking polymorphism in the hepatic lipase gene (LIPC). J. Lipid Res. 1998. 39: 228–232.

Supplementary key words: high density lipoprotein cholesterol


  INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES

Epidemiological studies have shown that plasma high density lipoprotein cholesterol (HDL-C) concentrations are higher in African American men than in white American men (1) (2) (3) (4). This ethnic difference in plasma HDL-C concentrations cannot be accounted for by environmental factors, and is therefore likely to be of genetic origin (2). Interestingly, the difference is specific to men, and reflects differences in the magnitude of the pubertal decrease in plasma HDL-C concentrations that occurs during puberty in boys (1) (4). The pubertal decrease in plasma HDL-C concentrations appears to be due to an androgen-mediated increase in the activity of hepatic lipase, an enzyme that catalyzes the hydrolysis of HDL triglycerides and phospholipids (5). Androgen administration leads to a dose-dependent increase in hepatic lipase activity (6) (7) and decreases plasma HDL-C concentrations in men and women (8) (9) (10) (11). Differences in the responsiveness of hepatic lipase to androgens, therefore, could explain the sex-specific differences in plasma HDL-C concentrations between African Americans and white Americans.

Recently we identified a hepatic lipase allele that is associated with increased plasma HDL-C concentrations in men, but not in women (12). The allele (designated -514T) is defined by four linked polymorphisms in the 5' flanking region of the gene, and has a frequency of 0.15 in white Americans. Plasma HDL-C concentrations were slightly higher in white men who were heterozygotes for the -514T allele, and appreciably higher in men who were -514T homozygotes. As the -514T allele leads to increased plasma HDL-C concentrations in men only, an increased frequency of this allele in African Americans could explain the sex-specific increase in plasma HDL-C concentrations in this population. To test this hypothesis, we compared plasma HDL-C concentrations, post-heparin plasma hepatic lipase activities, and -514T allele frequencies in African American and white American men.


  METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES

The study was approved by the Internal Review Boards at the University of Texas Southwestern Medical Center and the State University of New York Health Science Center.

Subjects
Two independent groups of men were recruited for this study. Plasma HDL-C concentrations, post-heparin plasma hepatic lipase activities, and LIPC genotypes were assayed in 43 African Americans and 45 white Americans aged 20 to 40 years who were medical students and staff of the State University of New York Health Science Center (Group 1). LIPC genotypes were determined in 54 African Americans and 60 white Americans recruited at a health fair sponsored by the Dallas Firefighters Association (Group 2).

Assay of plasma lipoproteins
Plasma concentrations of cholesterol and triglyceride were measured enzymatically using commercial reagents. Plasma HDL-C concentrations were measured by sodium phosphotungstate (0.55 mM) precipitation.

Assay of post-heparin plasma hepatic lipase activity
Hepatic lipase activity was measured in post-heparin plasma as described previously (13).

Assay of LIPC genotypes
The LIPC polymorphisms located at -250, -514, and -763 were assayed by PCR amplification and restriction digestion as described previously (12).

Statistical analysis
Median plasma HDL-C concentrations and hepatic lipase activities of African American and white men were compared using the Wilcoxon rank test. The correlation between plasma HDL-C concentrations and hepatic lipase activity was calculated using Pearson's method. The frequency of -514T homozygotes was compared in the two populations using Fisher's exact test. The observed frequencies of the -514C and -514T alleles were compared with the frequencies expected under Hardy-Weinberg equilibrium by {chi}2 tests.


  RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES

Plasma HDL-C concentrations and hepatic lipase activities in African American and white American men
Mean plasma HDL-C concentrations were significantly higher in African American than in white American men ( Table 1). Mean post-heparin plasma hepatic lipase activity was markedly lower in African American men than in white men (Table 1). Hepatic lipase activity was less than 20 mmol·h-1·l-1 in 12 of the 43 African Americans studied (28%). and less than 40 mmol·h-1 · l-1 in 39 (91%). Only 1 African American man (2%) had a hepatic lipase activity greater than 50 mmol·h-1 · l-1. In contrast, none of the 45 whites in the study had hepatic lipase activities below 20 mmol·h-1 · l-1; 20 (44%) had activities below 40 mmol·h-1 · l-1; and 16 (35%) had hepatic lipase activities exceeding 50 mmol·h-1 · l-1. Plasma HDL-C concentrations and hepatic lipase activities were inversely correlated both in African Americans (r = -0.32, P < 0.036) and whites (r = -0.42, P < 0.004). Mean plasma HDL-C concentrations were similar in the 27 African Americans and 20 whites whose hepatic lipase activities were between 20 and 40 mmol·h-1 · l-1 (46 ± 11 vs. 45 ± 9, P > 0.8).


 
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  		Table 1. Plasma lipids and HDL-C concentrations in African American and white American men

Frequency of the -514T allele in African Americans and white Americans
DNA samples were obtained from 42 of the African American and 41 of the white men recruited in New York. In this group, the frequency of the -514T allele was significantly higher in African Americans (0.52) than in white Americans (0.17, P < 0.0001). Essentially identical results were observed among firefighters recruited in Dallas (Group 2), where the frequency of the -514T allele was 0.53 in African Americans and 0.18 in white Americans (P < 0.0001). In both groups of African Americans and white Americans, the relative frequencies of the -514C and -514T alleles were consistent with Hardy-Weinberg equilibrium ( Table 2). In the 40 African American alleles examined, complete linkage disequilibrium was observed between the polymorphisms at -250, -514, and -763.


 
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  		Table 2. LIPC allele frequencies in African American and white American men

Effects of LIPC genotype on hepatic lipase activities in African American and white American men
In both African Americans and whites, hepatic lipase activity was significantly higher in CC homozygotes than in CT heterozygotes ( Table 3). Only 1 white American was homozygous for the -514T allele. In African Americans, mean hepatic lipase activity was slightly lower in TT homozygotes than in CT heterozygotes, but this difference did not reach significance at the 0.05 confidence level. When individuals were grouped by race and LIPC genotype, African Americans with the CC or CT genotype had significantly lower hepatic lipase activity than did white Americans with the corresponding genotypes. The sample size precluded a comparison of the TT genotype in the two ethnic groups.


 
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  		Table 3. Postheparin plasma hepatic lipase activities and LIPC genotypes in African American and white American men


  DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES

There is considerable evidence that hepatic lipase activity is an important determinant of plasma HDL-C concentrations. Clinical studies have consistently found an inverse relationship between hepatic lipase activity measured in post-heparin plasma and plasma HDL-C concentrations (13) (14) (15) (16) (17), and genetic studies have indicated linkage between the gene encoding hepatic lipase and plasma HDL-C concentrations in white Americans (12) (18). In the present study, we have evaluated the relationship between hepatic lipase activity, plasma HDL-C concentrations, and hepatic lipase genotypes in African American and white American men. Consistent with previous reports (1) (2) (3) (4), plasma HDL-C concentrations were significantly higher in African American men than in white American men in this study. In addition, two novel observations were made. First, hepatic lipase activity is significantly lower in African American than in white American men. Second, the -514T hepatic lipase allele, which is associated with low hepatic lipase activity and increased plasma HDL-C concentrations, is far more common among African Americans than among white Americans. Taken together, these data suggest that genetic differences in hepatic lipase activity contribute to the differences in plasma HDL-C concentrations between African American and white Americans.

Although the difference in plasma HDL-C concentrations between African American and white American men has been well established, the mechanism(s) responsible for this difference has not been elucidated. Hepatic lipase activities in African American men have not been reported previously. The present data indicate that hepatic lipase activity is markedly lower in African American men than in white American men. In both groups, plasma HDL-C concentrations were inversely related to post-heparin plasma hepatic lipase activities. Among men with post-heparin plasma hepatic lipase activities between 20 and 40 mmol·h-1·l-1, no ethnic difference in plasma HDL-C concentrations was observed. This finding suggests that the difference in plasma HDL-C concentrations between African American and white men can be accounted for in large part by differences in hepatic lipase activity.

Recently, we have identified an allele of hepatic lipase (defined by a T 514 bases upstream of the transcription start site) that is associated with increased plasma HDL-C concentrations and low hepatic lipase activity in white men (12). In the current study, we sought to determine whether the low hepatic lipase activities in African American men are due to an increased frequency of this allele. LIPC genotypes were assayed in two independent groups of African American and white men. In both groups, the -514T allele of LIPC was 3-fold more common in African Americans than in whites. As we observed previously in white Americans (12), the polymorphism at -514 was in complete linkage disequilibrium with two other polymorphisms in the 5' flanking region of LIPC, indicating that this allele arose early in human evolution. In African Americans and in whites, hepatic lipase activities were highest in men who were homozygous for the C allele, lower in CT heterozygotes, and lowest in TT homozygotes. This finding indicates that the increased frequency of the -514T allele contributes to low post-heparin plasma hepatic lipase activities observed in African American men. Interestingly, however, post-heparin plasma hepatic lipase activities were lower in African American men than in white men, even among individuals of the same LIPC genotype. Therefore, the increased frequency of the -514T allele in African American men does not fully account for the ethnic frequency of the ethnic difference in post-heparin plasma hepatic lipase activity. This difference may be due to other, as yet unidentified polymorphisms in LIPC, or to factors that influence the synthesis or secretion of the hepatic lipase protein.

Although our data indicate that the difference in plasma HDL-C concentrations between African American and white men reflects ethnic differences in hepatic lipase activity, it is possible that HDL-C concentrations and hepatic lipase activities are jointly influenced by a third factor that affects both of these parameters independently, and that the two are not causally related. Several lines of evidence support a direct effect of hepatic lipase on plasma HDL-C concentrations, however. Genetic deficiency of hepatic lipase is associated with increased plasma HDL-C concentrations (19), whereas administration of pharmacological doses of androgens leads to reciprocal changes in hepatic lipase activity and plasma HDL-C concentrations (6) (7). In vitro studies indicate that HDL is a substrate for hepatic lipase (20) (21). Finally, overexpression of human hepatic lipase in transgenic animals leads to decreased plasma HDL-C concentrations (22) (23). Therefore, while we cannot formally exclude the possibility that the low hepatic lipase activity observed in African American men is not directly related to their increased plasma HDL-C concentrations, a causal relationship between the two parameters seems more likely. Accordingly, we conclude that low hepatic lipase activity leads to increased plasma HDL-C concentrations in African American men. The low hepatic lipase activities in African American men are likely to be genetically determined, and are due in part to the high frequency of the -514T allele in this population.

rapid communication


  ACKNOWLEDGMENTS

We thank Ahn Nguyen, Sijing Niu, Liangcais Nie, Biman Pramanik, Hanh Nguyen, Han Tron, and Sharon Haynes, R. N. This work was supported in part by National Institutes of Health grants HL-53917 and M-01-RR-00633 Department of Veterans Affairs, the Southwestern Medical Foundation, and the Moss Heart Foundation, Dallas, TX.

Manuscript received October 30, 1997.

Abbreviations: HDL-C, high density lipoprotein cholesterol


  REFERENCES
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 ABSTRACT
 INTRODUCTION
 METHODS
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 DISCUSSION
 REFERENCES

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  2. Sprafka, J. M., Norsted, S. W., Folsom, A. R., Burke, G. L., Luepker, R. V. 1992. Life-style factors do not explain racial differences in high-density lipoprotein cholesterol: the Minnesota Heart Survey. Epidemiology. 3:156-163[Medline].

  3. Webber, L. S., Srinivasan, S. R., Wattigney, W. A., Berenson, G. S. 1991. Tracking of serum lipids and lipoproteins from childhood to adulthood. The Bogalusa Heart Study. Am. J. Epidemiol. 133:884-899[Abstract/Free Full Text].

  4. Brown, S. A., Hutchinson, R., Morrisett, J., Boerwinkle, E., Davis, C. E., Gotto, A. M., Jr., Patsch, W. 1993. Plasma lipid, lipoprotein cholesterol, and apoprotein distributions in selected US communities. The Atherosclerosis Risk in Communities (ARIC) Study. Arterioscler. Thromb. 13:1139-1158[Abstract/Free Full Text].

  5. Tikkanen, M. J., Nikkila, E. A. 1987. Regulation of hepatic lipase and serum lipoproteins by sex steroids. [Review]. Am. Heart J. 113:562-567[Medline].

  6. Kantor, M. A., Bianchini, A., Bernier, D., Sady, S. P., Thompson, P. D. 1985. Androgens reduce HDL2-cholesterol and increase hepatic triglyceride lipase activity. Med. Sci. Sports Exercise. 17:462-465[Medline].

  7. Applebaum-Bowden, D., Haffner, S. M., Hazzard, W. R. 1987. The dyslipoproteinemia of anabolic steroid therapy: increase in hepatic triglyceride lipase precedes the decrease in high density lipoprotein2 cholesterol. Metabolism. 36:949-952[Medline].

  8. Masarei, J. R., Lynch, W. J. 1977. Lowering of HDL-cholesterol by androgens [letter]. Lancet. 2:827-828[Medline].

  9. Cohen, J. C., Faber, W. M., Benade, A. J., Noakes, T. D. 1986. Altered serum lipoprotein profiles in male and female powerlifters ingesting anabolic steroids. Phys. Sportsmed. 14:131-136.

  10. Alen, M., Rahkila, P., Marniemi, J. 1985. Serum lipids in power athletes self-administering testosterone and anabolic steroids. Int. J. Sports Med. 6:139-144[Medline].

  11. Hurley, B. F., Seals, D. R., Hagberg, J. M., Goldberg, A. C., Ostrove, S. M., Holloszy, J. O., Wiest, W. G., Goldberg, A. P. 1984. High-density-lipoprotein cholesterol in bodybuilders vs. powerlifters. Negative effects of androgen use. J. Am. Med. Assoc. 252:507-513[Abstract].

  12. Guerra, R., Wang, J. P., Grundy, S. M., Cohen, J. C. 1997. A hepatic lipase (LIPC) allele associated with high plasma concentrations of high density lipoprotein cholesterol. Proc. Natl. Acad. Sci. USA. 94:4532-4537[Abstract/Free Full Text].

  13. Blades, B., Vega, G. L., Grundy, S. M. 1993. Activities of lipoprotein lipase and hepatic triglyceride lipase in postheparin plasma of patients with low concentrations of HDL choleslerol. Arterioscler. Thromb. 13:1227-1235[Abstract/Free Full Text].

  14. Applebaum-Bowden, D., Haffner, S. M., Wahl, P. W., Hoover, J. J., Warnick, G. R., Albers, J. J., Hazzard, W. R. 1985. Postheparin plasma triglyceride lipases. Relationships with very low density lipoprotein triglyceride and high density lipoprotein2 cholesterol. Arteriosclerosis. 5:273-282[Abstract/Free Full Text].

  15. Kuusi, T., Saarinen, P., Nikkila, E. A. 1980. Evidence for the role of hepatic endothelial lipase in the metabolism of plasma high density lipoprotein2 in man. Atherosclerosis. 36:589-593[Medline].

  16. Jackson, R. L., Yates, M. T., McNerney, C. A., Kashyap, M. L. 1990. Relationship between post-heparin plasma lipases, triglycerides and high density lipoproteins in normal subjects. Hormone Metabol. Res. 22:289-294[Medline].

  17. Kuusi, T., Ehnholm, C., Viikari, J., Harkonen, R., Vartiainen, E., Puska, P., Taskinen, M. R. 1989. Postheparin plasma lipoprotein and hepatic lipase are determinants of hypo- and hyperalphalipoproteinemia. J. Lipid Res. 30:1117-1126[Abstract].

  18. Cohen, J. C., Wang, Z., Grundy, S. M., Stoesz, M. R., Guerra, R. 1994. Variation at the hepatic lipase and apolipoprotein AI/CIII/AIV loci is a major cause of genetically determined variation in plasma HDL cholesterol levels. J. Clin. Invest. 94:2377-2384.

  19. Hegele, R. A., Little, J. A., Vezina, A., Maguire, C. F., Tu, L., Wolever, T. S., Jenkins, D. J., Connelly, P. W. 1993. Hepatic lipase deficiency. Clinical, biochemical, and molecular genetic characteristics. Arterioscler. Thromb. 13:720-728[Abstract/Free Full Text].

  20. Shirai, K., Barnhart, R. L., Jackson, R. L. 1981. Hydrolysis of human plasma high density lipoprotein 2-phospholipids and triglycerides by hepatic lipase. Biochem. Biophys. Res.Commun. 100:591-599[Medline].

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P. J. Talmud, L. Berglund, E. M. Hawe, D. M. Waterworth, C. R. Isasi, R. E. Deckelbaum, T. Starc, H. N. Ginsberg, S. E. Humphries, and S. Shea
Age-Related Effects of Genetic Variation on Lipid Levels: The Columbia University BioMarkers Study
Pediatrics, September 1, 2001; 108(3): e50 - 50.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
M. C. Carr, J. E. Hokanson, A. Zambon, S. S. Deeb, P. H. R. Barrett, J. Q. Purnell, and J. D. Brunzell
The Contribution of Intraabdominal Fat to Gender Differences in Hepatic Lipase Activity and Low/High Density Lipoprotein Heterogeneity
J. Clin. Endocrinol. Metab., June 1, 2001; 86(6): 2831 - 2837.
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 CirculationHome page
A. Zambon, S. S. Deeb, B. G. Brown, J. E. Hokanson, and J. D. Brunzell
Common Hepatic Lipase Gene Promoter Variant Determines Clinical Response to Intensive Lipid-Lowering Treatment
Circulation, February 13, 2001; 103(6): 792 - 798.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
S.-H. H. Juo, Z. Han, J. D. Smith, L. Colangelo, and K. Liu
romoter polymorphisms of hepatic lipase gene influence HDL2 but not HDL3 in African American men: CARDIA study
J. Lipid Res., February 1, 2001; 42(2): 258 - 264.
[Abstract] [Full Text]

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 Arterioscler. Thromb. Vasc. Bio.Home page
P. W. F. Wilson
Lipids, Lipases, and Obesity : Does Race Matter?
Arterioscler. Thromb. Vasc. Biol., August 1, 2000; 20(8): 1854 - 1856.
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 Arterioscler. Thromb. Vasc. Bio.Home page
J.-P. Despres, C. Couillard, J. Gagnon, J. Bergeron, A. S. Leon, D. C. Rao, J. S. Skinner, J. H. Wilmore, and C. Bouchard
Race, Visceral Adipose Tissue, Plasma Lipids, and Lipoprotein Lipase Activity in Men and Women : The Health, Risk Factors, Exercise Training, and Genetics (HERITAGE) Family Study
Arterioscler. Thromb. Vasc. Biol., August 1, 2000; 20(8): 1932 - 1938.
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 Arterioscler. Thromb. Vasc. Bio.Home page
J. Pihlajamaki, L. Karjalainen, P. Karhapaa, I. Vauhkonen, M.-R. Taskinen, S. S. Deeb, and M. Laakso
G-250A Substitution in Promoter of Hepatic Lipase Gene Is Associated With Dyslipidemia and Insulin Resistance in Healthy Control Subjects and in Members of Families With Familial Combined Hyperlipidemia
Arterioscler. Thromb. Vasc. Biol., July 1, 2000; 20(7): 1789 - 1795.
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 Arterioscler. Thromb. Vasc. Bio.Home page
F. M. van 't Hooft, B. Lundahl, F. Ragogna, F. Karpe, G. Olivecrona, and A. Hamsten
Functional Characterization of 4 Polymorphisms in Promoter Region of Hepatic Lipase Gene
Arterioscler. Thromb. Vasc. Biol., May 1, 2000; 20(5): 1335 - 1339.
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 Arterioscler. Thromb. Vasc. Bio.Home page
P. Couture, J. D. Otvos, L. A. Cupples, C. Lahoz, P. W. F. Wilson, E. J. Schaefer, and J. M. Ordovas
Association of the C-514T Polymorphism in the Hepatic Lipase Gene With Variations in Lipoprotein Subclass Profiles : The Framingham Offspring Study
Arterioscler. Thromb. Vasc. Biol., March 1, 2000; 20(3): 815 - 822.
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 J. Lipid Res.Home page
H. Allayee, K. M. Dominguez, B. E. Aouizerat, R. M. Krauss, J. I. Rotter, J. Lu, R. M. Cantor, T. W. A. de Bruin, and A. J. Lusis
Contribution of the hepatic lipase gene to the atherogenic lipoprotein phenotype in familial combined hyperlipidemia
J. Lipid Res., February 1, 2000; 41(2): 245 - 252.
[Abstract] [Full Text]

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 J. Lipid Res.Home page
S. S. Deeb and R. Peng
The C-514T polymorphism in the human hepatic lipase gene promoter diminishes its activity
J. Lipid Res., January 1, 2000; 41(1): 155 - 158.
[Abstract] [Full Text]

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 Arterioscler. Thromb. Vasc. Bio.Home page
M. C. Carr, J. E. Hokanson, S. S. Deeb, J. Q. Purnell, E. S. Mitchell, and J. D. Brunzell
A Hepatic Lipase Gene Promoter Polymorphism Attenuates the Increase in Hepatic Lipase Activity With Increasing Intra-abdominal Fat in Women
Arterioscler. Thromb. Vasc. Biol., November 1, 1999; 19(11): 2701 - 2707.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
S. M. Haffner, R. D'Agostino Jr, D. Goff, B. Howard, A. Festa, M. F. Saad, and L. Mykkanen
LDL Size in African Americans, Hispanics, and Non-Hispanic Whites : The Insulin Resistance Atherosclerosis Study
Arterioscler. Thromb. Vasc. Biol., September 1, 1999; 19(9): 2234 - 2240.
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 Arterioscler. Thromb. Vasc. Bio.Home page
R. V. Shohet, G. L. Vega, A. Anwar, J. E. Cigarroa, S. M. Grundy, and J. C. Cohen
Hepatic Lipase (LIPC) Promoter Polymorphism in Men With Coronary Artery Dis