Abstract
Context: Exogenous estrogens have been shown to affect the lipid profile, leading to the hypothesis that endogenous estrogens may have similar effects.
Objective: The objective of the study was to evaluate the association between endogenous estrogen and serum lipoproteins across the menstrual cycle.
Design: This was a prospective cohort study.
Setting: The study was conducted at the University at Buffalo, 2005–2007.
Participants: Participants included 259 healthy, regularly menstruating women aged 18–44 yr.
Main Outcome Measures: Serum levels of total, high-density lipoprotein (HDL) and low-density lipoprotein (LDL) cholesterol, and triglycerides measured up to eight times per cycle for up to two cycles were measured.
Results: Total and LDL cholesterol were lower during the luteal phase as compared with the follicular phase (P < 0.001), and HDL levels were highest around ovulation (P < 0.001). More women were classified above the desirable range (LDL ≥130 mg/dl or total cholesterol ≥200 mg/dl) when measured during the follicular phase. Estradiol was positively associated with HDL in acute effects models [beta = 0.019, 95% confidence interval (CI) 0.015, 0.022] and inversely associated with total (beta = −0.017, 95% CI −0.020, −0.014) and LDL cholesterol (beta = −0.023, 95% CI −0.027, −0.018) and triglycerides (beta = −0.041, 95% CI −0.054, −0.029) in persistent effects models.
Conclusions: Endogenous estrogen, like exogenous estrogen, appears to have beneficial effects on the lipid profile. Because lipoprotein cholesterol levels vary across the menstrual cycle, cyclic variations in lipoprotein levels may need to be considered in the design and interpretation of studies in reproductive-age women and in the clinical management of women’s cholesterol.
Cholesterol levels vary and are associated with endogenous estrogen levels across the cycle; lipoprotein cholesterol measurements should be appropriately timed to menstrual cycle phase.
Exogenous estrogens have been shown to affect the lipid profile, leading to the hypothesis that endogenous estrogens may have similar effects. In particular, results from randomized trials found that hormone therapy improved lipoprotein profiles, even though they were associated with increased rates of cardiovascular disease (1,2). Studies on the effect of exogenous hormones in the form of oral contraceptives, which contain higher doses of estrogens and progestins, however, have shown increased levels of triglycerides and total cholesterol (TC) (3).
Exogenous estrogen is thought to exert a favorable effect on lipoprotein metabolism by increasing very low-density lipoprotein (VLDL) synthesis, inhibiting hepatic lipase and lipoprotein lipase activity, and up-regulating the low-density lipoprotein (LDL) receptors (4,5,6). The association between endogenous sex hormones and lipoprotein levels in healthy premenopausal women as well as whether these effects are chronic vs. acute, however, remains uncertain. The objective of this study was to evaluate the association between endogenous serum estradiol and lipoprotein cholesterol levels during the normal menstrual cycle in a prospective study of menstrual cycle function.
Materials and Methods
The BioCycle study was a prospective cohort of 259 healthy, premenopausal women, aged 18–44 yr, recruited from western New York and followed up for up to two cycles (7). Exclusion criteria included current use of oral contraceptives or other medications. Further details on exclusion criteria have been reported (7). The University at Buffalo Institutional Review Board approved the study. All participants provided written informed consent.
The study involved up to eight clinic visits per cycle for two cycles with visits timed using fertility monitors (Clearblue Easy fertility monitor; Inverness Medical, Waltham, MA). Participants were highly compliant with the study protocol, with 94% of all women completing at least seven visits per cycle. Fasting serum samples were collected at each visit along with information on demographics, lifestyle, physical activity, reproductive history, and dietary intake.
Estradiol, progesterone, LH, and FSH were measured at each clinic visit. Estradiol was measured using a RIA. Progesterone, LH, and FSH were measured using solid-phase competitive chemiluminescent enzymatic immunoassay by Specialty Laboratories, Inc. (Valencia, CA) on the DPC Immulite2000 analyzer (Siemens Medical Solutions Diagnostics, Deerfield, IL). Across the study period, the coefficient of variation for these tests was less than 10% for estradiol, less than 5% for LH and FSH, and less than 14% for progesterone.
A lipid profile was performed at each cycle visit, including analysis of TC, high-density lipoprotein (HDL), and triglycerides, using a LX20 automated chemistry analyzer (Beckman, Brea, CA). LDL was determined indirectly using the Friedewald formula (8). The coefficients of variation for all lipid and lipoprotein assays were less than 5%.
Median and interquartile range levels of hormones and lipoprotein cholesterol as well as the percentage of women with cholesterol levels above the desirable ranges, as identified by the National Cholesterol Education Program (NCEP), were calculated for each clinic visit (9). Linear mixed models were used to compute the P values for comparisons between the mean log values of hormones and lipoproteins across the cycle.
Weighted linear mixed-effects models were used to model the association between lipoprotein cholesterol and estrogen levels measured on the same day (acute effects) or with estrogen levels at one visit predicting lipoprotein cholesterol levels at the next visit (persistent effects). Persistent-effects models represent prolonged exposure to estrogen (approximately 2 d) and were used to demonstrate temporality of effects. Lipoprotein cholesterol and hormone levels were allowed to vary over time, and all models included hormone and lipoprotein cholesterol concentrations throughout the cycle, including up to eight measurements per cycle.
Inverse probability of exposure weights were used to appropriately adjust for time-dependent confounding (10). The choice of covariates in the weight models was determined by a review of the literature and included age, body mass index, progesterone, LH, and FSH. Additional measures of dietary intake, physical activity, smoking, alcohol use, and race were considered as potential covariates but did not appreciably alter the estimates.
Results
The women in the BioCycle study were on average 27.3 yr of age (range 18–44 yr) and consisted mainly of single, nulliparous, normal-weight, highly physical active, white women with some postsecondary education (Supplemental Table 1, published on The Endocrine Society’s Journals Online web site at http://jcem.endojournals.org.). Both hormones and lipoprotein cholesterol levels varied across the menstrual cycle (Table 1). TC, LDL, and triglycerides were highest during the follicular phase and declined during the luteal phase. Median TC declined by 3.0% (P < 0.0001) and LDL by 4.9% (P < 0.0001) from the midfollicular phase to the midluteal phase. HDL levels were highest during ovulation but did not change across other phases. Absolute changes in median lipoprotein cholesterol levels between women across the cycle were modest (TC, −3.0%; HDL, +2.0%; LDL, −4.9%); however, the mean change within a woman over the cycle was much greater [TC, 19%, mean change (sd) 27.7 (11.1) mg/dl].
Table 1.
Serum hormone and lipoprotein cholesterol concentrations and percentage above desirable ranges of total, HDL, and LDL cholesterol and triglycerides as defined by the NCEP (9) among women in the BioCycle study (n = 259) by menstrual cycle phase
| Menses (n = 257) | Midfollicular (n = 258) | Late follicular (n = 259) | LH/FSH surge (n = 258) | Ovulation (n = 257) | Early luteal (n = 252) | Midluteal (n = 244) | Late luteal (n = 191) | |
|---|---|---|---|---|---|---|---|---|
| Serum hormone and lipoprotein concentrations: median (IQR) | ||||||||
| Estrogena | ||||||||
| pg/ml | 33.0 (20.0) | 48.0 (37.0) | 121.0 (155.0) | 116.0 (153.0) | 96.0 (111.0) | 117.0 (93.0) | 122.0 (91.5) | 75.0 (79.0) |
| pmol/liter | 121.1 (73.4) | 176.2 (135.8) | 444.1 (568.9) | 425.7 (561.5) | 352.3 (407.4) | 429.4 (341.3) | 447.7 (335.8) | 275.3 (289.9) |
| Progesteronea | ||||||||
| ng/ml | 0.5 (0.3) | 0.4 (0.3) | 0.6 (0.6) | 0.9 (1.2) | 1.7 (3.0) | 7.4 (10.0) | 8.9 (7.4) | 4.0 (6.3) |
| nmol/liter | 1.6 (1.0) | 1.3 (1.0) | 1.9 (1.9) | 2.9 (3.8) | 5.4 (9.5) | 23.5 (31.8) | 28.3 (23.5) | 12.7 (20.0) |
| LHa | ||||||||
| ng/ml | 3.9 (2.4) | 4.7 (3.0) | 7.6 (10.6) | 10.3 (14.6) | 8.5 (10.9) | 6.4 (6.2) | 4.3 (4.6) | 4.0 (3.4) |
| FSHa | ||||||||
| mIU/ml | 6.3 (2.5) | 6.4 (2.5) | 6.2 (4.0) | 6.8 (5.3) | 6.3 (5.3) | 4.4 (3.8) | 3.1 (2.5) | 3.4 (2.3) |
| TCa | ||||||||
| mg/dl | 160.0 (36.0) | 166.0 (39.0) | 164.0 (38.0) | 164.0 (34.0) | 162.0 (34.0) | 161.0 (35.0) | 161.0 (36.0) | 157.0 (40.5) |
| mmol/liter | 4.1 (0.9) | 4.3 (1.0) | 4.2 (1.0) | 4.2 (0.9) | 4.2 (0.9) | 4.2 (0.9) | 4. (0.9) | 4.1 (1.0) |
| HDL cholesterola | ||||||||
| mg/dl | 48.0 (17.0) | 50.0 (17.0) | 52.0 (17.0) | 52.0 (16.0) | 52.0 (16.0) | 52.0 (16.0) | 51.0 (16.0) | 50.0 (17.0) |
| mmol/liter | 1.2 (0.4) | 1.3 (0.4) | 1.3 (0.4) | 1.3 (0.4) | 1.3 (0.4) | 1.3 (0.4) | 1.3 (0.4) | 1.3 (0.4) |
| LDL cholesterola | ||||||||
| mg/dl | 98.0 (32.0) | 102.0 (33.0) | 100.0 (32.0) | 98.5 (32.0) | 98.0 (30.0) | 96.0 (31.0) | 97.0 (34.0) | 96.0 (34.5) |
| mmol/liter | 2.5 (0.8) | 2.6 (0.9) | 2.6 (0.8) | 2.6 (0.8) | 2.5 (0.8) | 2.5 (0.8) | 2.5 (0.9) | 2.5 (0.9) |
| Triglyceridesb | ||||||||
| mg/dl | 51.5 (32.0) | 56.0 (33.0) | 55.0 (30.0) | 51.0 (28.0) | 53.0 (27.0) | 53.0 (31.0) | 51.0 (28.0) | 49.0 (28.0) |
| mmol/liter | 0.6 (0.4) | 0.6 (0.4) | 0.6 (0.3) | 0.6 (0.3) | 0.6 (0.3) | 0.6 (0.4) | 0.6 (0.3) | 0.6 (0.3) |
| TC to HDL ratioc | 3.3 (1.0) | 3.3 (1.2) | 3.2 (1.1) | 3.1 (1.0) | 3.1 (1.0) | 3.1 (0.9) | 3.1 (1.0) | 3.2 (1.1) |
| Above desirable ranges during cycle 1 as defined by NCEP: n (%) | ||||||||
| TC ≥200 mg/dl | 26 (10.1) | 37 (14.3) | 29 (11.2) | 28 (10.9) | 27 (10.5) | 23 (9.1) | 23 (9.4) | 15 (7.9) |
| TC ≥240 mg/dl | 5 (1.9) | 4 (1.6) | 6 (2.3) | 6 (2.3) | 5 (1.9) | 5 (2.0) | 4 (1.6) | 4 (2.1) |
| LDL cholesterol ≥130 mg/dl | 34 (13.2) | 46 (17.8) | 36 (13.9) | 27 (10.5) | 29 (11.3) | 28 (11.1) | 27 (11.1) | 20 (10.5) |
| LDL cholesterol ≥160 mg/dl | 5 (1.9) | 5 (1.9) | 5 (1.9) | 5 (1.9) | 6 (2.3) | 4 (1.6) | 4 (1.6) | 5 (2.6) |
| HDL cholesterol <40 mg/dl | 43 (16.7) | 42 (16.3) | 32 (12.4) | 34 (13.2) | 32 (12.5) | 36 (14.3) | 38 (15.6) | 39 (20.4) |
| Triglycerides ≥150 mg/dL | 4 (1.6) | 9 (3.5) | 3 (1.2) | 3 (1.2) | 5 (2.0) | 7 (2.8) | 6 (2.5) | 4 (2.1) |
IQR, Interquartile range.
P < 0.0001; P values from repeated-measures ANOVA based on log-transformed values.
P < 0.10.
P < 0.01.
In this study, only 13 women (5%) had TC levels above 200 mg/dl at all eight visits, whereas 51 women (19.7%) had levels above 200 mg/dl on at least one cycle visit. When measured during the late luteal phase, the smallest percentage of women would be classified as having high cholesterol (TC, 7.9%; LDL, 10.5%), whereas the largest percentage are above the desirable levels during the follicular phase (TC, 14.3%; LDL, 17.8%) (Table 1).
In acute-effects models, estradiol was positively associated with levels of TC (P = 0.03) and HDL (P < 0.0001) and inversely associated with LDL (P = 0.009) and the TC to HDL ratio (P < 0.0001) (Table 2). In persistent-effects models, estradiol was inversely associated with TC (P < 0.0001), LDL (P < 0.0001), TC to HDL ratio (P < 0.0001), and triglycerides (P = 0.01).
Table 2.
Association between log(estrogen) and log(lipoprotein cholesterol, milligrams per deciliter) levels among women participating in the BioCycle study (n = 259) based on marginal structural models with inverse probability of exposure weights
| Effectsa | Betab | 95% CI | P value |
|---|---|---|---|
| TC | |||
| Acute | 0.0032 | (0.0003, 0.0060) | 0.03 |
| Persistent | −0.0173 | (−0.0203, −0.0144) | <0.0001 |
| HDL cholesterol | |||
| Acute | 0.0186 | (0.0151, 0.0221) | <0.0001 |
| Persistent | 0.0005 | (−0.0033, 0.0043) | 0.8 |
| LDL cholesterol | |||
| Acute | −0.0058 | (−0.0101, −0.0014) | 0.009 |
| Persistent | −0.0228 | (−0.0274, −0.0182) | <0.0001 |
| Triglycerides | |||
| Acute | 0.0037 | (−0.0079, 0.0154) | 0.5 |
| Persistent | −0.0410 | (−0.0535, −0.0285) | <0.0001 |
| TC to HDL ratio | |||
| Acute | −0.0173 | (−0.0205, −0.0140) | <0.0001 |
| Persistent | −0.0178 | (−0.0213, −0.0143) | <0.0001 |
CI, Confidence interval.
Acute-effects models model the association between estrogen and lipoproteins measured on the same day. Persistent-effects models model the association between estrogen measured at one visit and lipoprotein cholesterol levels at the next visit.
Weight models adjusted for age, body mass index, and hormone levels on previous days of the cycle.
Discussion
We observed that TC and LDL were highest during the follicular phase and declined during the luteal phase, whereas HDL was highest at ovulation. In fact, more women would be classified above the desirable TC and LDL ranges when tested during the follicular phase. We also observed that increased levels of endogenous estrogen were associated with an improved lipid profile. It appears that estrogen has a rapid effect on increasing HDL levels, but effects on TC and LDL do not appear to be acute.
Although the TC and LDL changes observed were modest (only 5–8% on average), women did cross between clinical boundaries of acceptable levels. Although treatment decisions regarding the lipid profile may still require repeated samples above the recommended level, standardizing the timing of lipid measurements may improve the interpretability of results and consequently reduce the overall number of tests. The changes in classification above clinical boundaries and variability across the cycle that we observed occurred even among healthy women. Among obese women older than 40 yr of age, we observed increased variability (data not presented), further emphasizing the importance of standardization of measurement.
The results of this study are consistent with past research and help to reconcile some of the apparent contradictions in the evidence. In particular, the acute effects we observed are in line with results from a cross-sectional study that measured estrogen and lipoprotein cholesterol on the same day during the midfollicular phase and observed a similar positive association between estrogen and HDL and no accompanying effects on TC and LDL (11). Our evaluation of persistent effects are in line with studies that have compared lipid levels between phases of the cycle because the effect of estrogen can be considered as being accumulated over the first half of the cycle. These studies tended to observe lower TC and LDL levels during the luteal phase (similar in magnitude to our study) and no cyclic variations in HDL levels (12,13,14,15,16,17). Measurements compared between phases tend to miss the peak levels of HDL that we observed around ovulation (13,14,15,17).
Endogenous estrogen appears to increase VLDL synthesis leading to subsequent decreases in LDL and increases in HDL (4,5,6). Estrogens appear to up-regulate the LDL receptors (18); up-regulate ATP-binding cassette transporter A1 and apolipoprotein-A1, which increases HDL synthesis (19); and suppress hepatic SR-BI expression leading to decreased hepatic cholesterol uptake from HDL (20). Although these changes would also tend to increase triglyceride levels, estrogen appears to primarily increase the light subtype of VLDL that lacks atherogenicity, thus leading to overall beneficial effects (5).
In studies of exogenous hormones, progestins are usually considered to oppose the stimulatory effects of estrogen on lipoprotein metabolism (5). In our study, progesterone levels were taken into account when evaluating the associations between estradiol and lipoprotein cholesterol levels; endogenous progesterone did not appear to reduce the effects of estrogen during the luteal phase. In fact, TC, LDL, and triglyceride levels were lowest during the luteal phase, the phase that corresponds to a natural state of opposed estrogen, suggesting that endogenous progesterone may not exhibit the same opposing effects as exogenous progesterone. However, HDL levels also declined during the luteal phase, suggesting that the beneficial effects of estrogen on HDL may be observed only when progesterone levels are low.
Intensive monitoring throughout two cycles on a relatively large number of women, with multiple clinic visits timed using fertility monitors, are unique strengths of our study. Multiple measurements of both hormones and lipoproteins enabled us to more precisely model the association between estradiol and lipoprotein cholesterol levels and evaluate both acute and persistent effects. Standardized assessment of a wide variety of participant and dietary characteristics increased the ability to adjust for potential confounding factors.
There are several limitations worth noting. Residual confounding is a possibility because it can be difficult to capture effects of diet and exercise. Although our sample population was restricted to normally menstruating women to exclude potential confounders by design, such restrictions could also limit generalizability. The increase in TC observed during the follicular phase could be due, at least in part, to reductions in plasma volume observed during this phase, which we were unable to evaluate (12). The observed changes in HDL around ovulation, however, appear to be independent from the expected increase in plasma volume. Also, we cannot completely account for temporality of the effects of hormones and lipoproteins.
In conclusion, cholesterol levels varied and were associated with endogenous estrogen levels across the cycle. This study confirms the hypothesized beneficial effects of endogenous estrogen on lipoprotein cholesterol levels and suggests that the effects of estrogen are not acute. This study is the first to evaluate the association between endogenous estrogen and lipoproteins using multiple and longitudinal serum measures of estrogen and lipoproteins and to comprehensively consider potential impacts from other reproductive hormones. Cyclic variations in lipoprotein cholesterol levels observed in the present study may have clinical implications regarding the appropriate timing of lipoprotein cholesterol measurement during the cycle and may need to be accounted for in the design and interpretation of studies in women of reproductive age.
Supplementary Material
Acknowledgments
We are indebted to all the investigators and staff at the Epidemiology Branch, Eunice Kennedy Shriver National Institute of Child Health and Human Development, and the University at Buffalo as well as the BioCycle participants for their commitment to the study. We thank Andy Olshan, Mary Hediger, and the BioCycle Working Group for their helpful suggestions and Steve Cole and Aijun Ye for their assistance with the marginal structural models.
Footnotes
This work was supported by the Intramural Research Program of the Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health.
Disclosure Summary: The authors have nothing to disclose.
First Published Online June 9, 2010
Abbreviations: HDL, High-density lipoprotein; LDL, low-density lipoprotein; NCEP, National Cholesterol Education Program; TC, total cholesterol; VLDL, very low-density lipoprotein.
References
- Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J 2002 Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial. JAMA 288:321–333 [DOI] [PubMed] [Google Scholar]
- Hulley S, Grady D, Bush T, Furberg C, Herrington D, Riggs B, Vittinghoff E 1998 Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA 280:605–613 [DOI] [PubMed] [Google Scholar]
- Krauss RM, Burkman Jr RT 1992 The metabolic impact of oral contraceptives. Am J Obstet Gynecol 167:1177–1184 [DOI] [PubMed] [Google Scholar]
- Knopp RH, Paramsothy P, Retzlaff BM, Fish B, Walden C, Dowdy A, Tsunehara C, Aikawa K, Cheung MC 2006 Sex differences in lipoprotein metabolism and dietary response: basis in hormonal differences and implications for cardiovascular disease. Curr Cardiol Rep 8:452–459 [DOI] [PubMed] [Google Scholar]
- Knopp RH, Zhu X 1997 Multiple beneficial effects of estrogen on lipoprotein metabolism. J Clin Endocrinol Metab 82:3952–3954 [DOI] [PubMed] [Google Scholar]
- Campos H, Walsh BW, Judge H, Sacks FM 1997 Effect of estrogen on very low density lipoprotein and low density lipoprotein subclass metabolism in postmenopausal women. J Clin Endocrinol Metab 82:3955–3963 [DOI] [PubMed] [Google Scholar]
- Wactawski-Wende J, Schisterman EF, Hovey KM, Howards PP, Browne RW, Hediger M, Liu A, Trevisan M 2009 BioCycle study: design of the longitudinal study of the oxidative stress and hormone variation during the menstrual cycle. Paediatr Perinat Epidemiol 23:171–184 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedewald WT, Levy RI, Fredrickson DS 1972 Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502 [PubMed] [Google Scholar]
- Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults 2001 Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 285:2486–2497 [DOI] [PubMed] [Google Scholar]
- Robins JM, Hernán MA, Brumback B 2000 Marginal structural models and causal inference in epidemiology. Epidemiology 11:550–560 [DOI] [PubMed] [Google Scholar]
- Lamon-Fava S, Fisher EC, Nelson ME, Evans WJ, Millar JS, Ordovas JM, Schaefer EJ 1989 Effect of exercise and menstrual cycle status on plasma lipids, low density lipoprotein particle size, and apolipoproteins. J Clin Endocrinol Metab 68:17–21 [DOI] [PubMed] [Google Scholar]
- Cullinane EM, Yurgalevitch SM, Saritelli AL, Herbert PN, Thompson PD 1995 Variations in plasma volume affect total and low-density lipoprotein cholesterol concentrations during the menstrual cycle. Metabolism 44:965–971 [DOI] [PubMed] [Google Scholar]
- Jones DY, Judd JT, Taylor PR, Campbell WS, Nair PP 1988 Menstrual cycle effect on plasma lipids. Metabolism 37:1–2 [DOI] [PubMed] [Google Scholar]
- De Leon RG, Austin KL, Richards L, Guerrero F 1992 Lipid and hormonal profile of Panamanian women during the menstrual cycle. Int J Gynecol Obstet 39:219–226 [DOI] [PubMed] [Google Scholar]
- Kim HJ, Kalkhoff RK 1979 Changes in lipoprotein composition during the menstrual cycle. Metabolism 28:663–668 [DOI] [PubMed] [Google Scholar]
- Larsen LF, Andersen HR, Hansen AB, Andersen O 1996 Variation in risk indicators of cardiovascular disease during the menstrual cycle: an investigation of within-subject variations in glutathione peroxidase, haemostatic variables, lipids and lipoproteins in healthy young women. Scand J Clin Lab Invest 56:241–249 [DOI] [PubMed] [Google Scholar]
- Schijf CP, van der Mooren MJ, Doesburg WH, Thomas CM, Rolland R 1993 Differences in serum lipids, lipoproteins, sex hormone binding globulin and testosterone between the follicular and the luteal phase of the menstrual cycle. Acta Endocrinol (Copenhagen) 129:130–133 [DOI] [PubMed] [Google Scholar]
- Srivastava RA, Baumann D, Schonfeld G 1993 In vivo regulation of low-density lipoprotein receptors by estrogen differs at the post-transcriptional level in rat and mouse. Eur J Biochem 216:527–538 [DOI] [PubMed] [Google Scholar]
- Zannis VI, Chroni A, Krieger M 2006 Role of apoA-I, ABCA1, LCAT, and SR-BI in the biogenesis of HDL. J Mol Med 84:276–294 [DOI] [PubMed] [Google Scholar]
- Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M 1996 Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271:518–520 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.