HDL Cholesterol And Female Infertility: Lessons From Animal Models

Anastasia V. Poznyak; Igor A. Sobenin; Victor Y Glanz; Victoria A. Khotina; Vasily N. Sukhorukov; and Alexander N. Orekhov

doi:10.25163/angiotherapy.859558

Angiogenesis, Inflammation & Therapeutics | Online ISSN 2207-872X

REVIEWS (Open Access)

HDL Cholesterol And Female Infertility: Lessons From Animal Models

Anastasia V. Poznyak ^1*, Igor A. Sobenin ², Victor Y Glanz ², Victoria A. Khotina ², Vasily N. Sukhorukov ¹, and Alexander N. Orekhov ¹

+ Author Affiliations

Journal of Angiotherapy 8 (5) 1-10 https://doi.org/10.25163/angiotherapy.859558

Submitted: 05 March 2024 Revised: 01 May 2024 Published: 04 May 2024

Abstract

Cholesterol metabolism, particularly the role of high density lipoprotein (HDL), plays a critical role in female fertility. This review examines the implications of HDL metabolism on various aspects of female reproduction using animal models, including ABCA1 KO mice, SCARB1 KO mice, a restricted ovulator chicken mutant model, and liver X receptor KO mice. The paper highlights the importance of HDL in oocyte development, embryo quality, and overall reproductive outcomes. By summarizing the findings from these models, significant insights into the mechanisms behind dysfunctional HDL metabolism and its impact on female infertility are revealed. The methodology employed in this review includes a systematic analysis of literature and data from studies on animal models, providing a comprehensive understanding of the complex relationship between HDL cholesterol and female reproductive health.

Keywords: Cholesterol, Lipoproteins, HDL Metabolism, Animal Models, Female Infertility

References

Adorni MP, Ronda N, Bernini F, Zimetti F. High Density Lipoprotein Cholesterol Efflux Capacity and Atherosclerosis in Cardiovascular Disease: Pathophysiological Aspects and Pharmacological Perspectives. Cells. 2021 Mar 5;10(3):574. doi: 10.3390/cells10030574. PMID: 33807918; PMCID: PMC8002038.

Agarwala AP, Rodrigues A, Risman M, McCoy M, Trindade K, Qu L, Cuchel M, Billheimer J, Rader DJ. High-Density Lipoprotein (HDL) Phospholipid Content and Cholesterol Efflux Capacity Are Reduced in Patients With Very High HDL Cholesterol and Coronary Disease. Arterioscler Thromb Vasc Biol. 2015 Jun;35(6):1515-9. doi: 10.1161/ATVBAHA.115.305504. Epub 2015 Apr 2. PMID: 25838421; PMCID: PMC4560933.

Amin M, Simerman A, Cho M, Singh P, Briton-Jones C, Hill D, Grogan T, Elashoff D, Clarke NJ, Chazenbalk GD, Dumesic DA. 21-Hydroxylase-derived steroids in follicles of nonobese women undergoing ovarian stimulation for in vitro fertilization (IVF) positively correlate with lipid content of luteinized granulosa cells (LGCs) as a source of cholesterol for steroid synthesis. J Clin Endocrinol Metab. 2014 Apr;99(4):1299-306. doi: 10.1210/jc.2013-3204. Epub 2014 Jan 13. PMID: 24423334; PMCID: PMC3973780.

Arias A, Quiroz A, Santander N, Morselli E, Busso D. Implications of High-Density Cholesterol Metabolism for Oocyte Biology and Female Fertility. Front Cell Dev Biol. 2022 Sep 14;10:941539. doi: 10.3389/fcell.2022.941539. PMID: 36187480; PMCID: PMC9518216.

Bacchetti T, Morresi C, Vignini A, Tiano L, Orlando P, Montik N, Ciavattini A, Ferretti G. HDL functionality in follicular fluid in normal-weight and obese women undergoing assisted reproductive treatment. J Assist Reprod Genet. 2019 Aug;36(8):1657-1664. doi: 10.1007/s10815-019-01523-9. Epub 2019 Jul 23. PMID: 31338723; PMCID: PMC6708027.

Barber DL, Sanders EJ, Aebersold R, Schneider WJ. The receptor for yolk lipoprotein deposition in the chicken oocyte. J Biol Chem. 1991 Oct 5;266(28):18761-70. PMID: 1655760.

Ben Aissa M, Lewandowski CT, Ratia KM, Lee SH, Layden BT, LaDu MJ, Thatcher GRJ. Discovery of Nonlipogenic ABCA1 Inducing Compounds with Potential in Alzheimer's Disease and Type 2 Diabetes. ACS Pharmacol Transl Sci. 2021 Jan 5;4(1):143-154. doi: 10.1021/acsptsci.0c00149. PMID: 33615168; PMCID: PMC7887740.

Bergh C, Olsson JH, Selleskog U, Hillensjö T. Steroid production in cultured thecal cells obtained from human ovarian follicles. Hum Reprod. 1993 Apr;8(4):519-24. doi: 10.1093/oxfordjournals.humrep.a138087. PMID: 8501177.

Beyea MM, Heslop CL, Sawyez CG, Edwards JY, Markle JG, Hegele RA, Huff MW. Selective up-regulation of LXR-regulated genes ABCA1, ABCG1, and APOE in macrophages through increased endogenous synthesis of 24(S),25-epoxycholesterol. J Biol Chem. 2007 Feb 23;282(8):5207-16. doi: 10.1074/jbc.M611063200. Epub 2006 Dec 23. PMID: 17186944.

Bisgaier CL, Chanderbhan R, Hinds RW, Vahouny GV. Adrenal cholesterol esters as substrate source for steroidogenesis. J Steroid Biochem. 1985 Dec;23(6A):967-74. doi: 10.1016/0022-4731(85)90054-8. PMID: 3005771.

Burchall GF, Pouniotis DS, Teede HJ, Ranasinha S, Walters KA, Piva TJ. Expression of the plasminogen system in the physiological mouse ovary and in the pathological polycystic ovary syndrome (PCOS) state. Reprod Biol Endocrinol. 2019 Mar 16;17(1):33. doi: 10.1186/s12958-019-0472-0. PMID: 30878040; PMCID: PMC6420749.

Catalano G, Duchene E, Julia Z, Le Goff W, Bruckert E, Chapman MJ, Guerin M. Cellular SR-BI and ABCA1-mediated cholesterol efflux are gender-specific in healthy subjects. J Lipid Res. 2008 Mar;49(3):635-43. doi: 10.1194/jlr.M700510-JLR200. Epub 2007 Dec 5. PMID: 18057374.

Cedó L, Metso J, Santos D, García-León A, Plana N, Sabate-Soler S, Rotllan N, Rivas-Urbina A, Méndez-Lara KA, Tondo M, Girona J, Julve J, Pallarès V, Benitez-Amaro A, Llorente-Cortes V, Pérez A, Gómez-Coronado D, Ruotsalainen AK, Levonen AL, Sanchez-Quesada JL, Masana L, Kovanen PT, Jauhiainen M, Lee-Rueckert M, Blanco-Vaca F, Escolà-Gil JC. LDL Receptor Regulates the Reverse Transport of Macrophage-Derived Unesterified Cholesterol via Concerted Action of the HDL-LDL Axis: Insight From Mouse Models. Circ Res. 2020 Aug 28;127(6):778-792. doi: 10.1161/CIRCRESAHA.119.316424. Epub 2020 Jun 4. PMID: 32495699.

Chadwick AC, Sahoo D. Functional genomics of the human high-density lipoprotein receptor scavenger receptor BI: an old dog with new tricks. Curr Opin Endocrinol Diabetes Obes. 2013 Apr;20(2):124-31. doi: 10.1097/MED.0b013e32835ed575. PMID: 23403740; PMCID: PMC3967407.

Chang XL, Liu L, Wang N, Chen ZJ, Zhang C. The function of high-density lipoprotein and low-density lipoprotein in the maintenance of mouse ovarian steroid balance. Biol Reprod. 2017 Jan 1;97(6):862-872. doi: 10.1093/biolre/iox134. PMID: 29092018.

Christianson MS, Yates M. Scavenger receptor class B type 1 gene polymorphisms and female fertility. Curr Opin Endocrinol Diabetes Obes. 2012 Apr;19(2):115-20. doi: 10.1097/MED.0b013e3283505771. PMID: 22261999.

Contreras-Duarte S, Santander N, Birner-Gruenberger R, Wadsack C, Rigotti A, Busso D. High density lipoprotein cholesterol and proteome in SR-B1 KO mice: lost in precipitation. J Transl Med. 2018 Nov 12;16(1):309. doi: 10.1186/s12967-018-1683-4. PMID: 30419936; PMCID: PMC6233513.

Craig M, Yarrarapu SNS, Dimri M. Biochemistry, Cholesterol. [Updated 2022 Aug 15]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK513326/

Da Broi MG, Giorgi VSI, Wang F, Keefe DL, Albertini D, Navarro PA. Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications. J Assist Reprod Genet. 2018 May;35(5):735-751. doi: 10.1007/s10815-018-1143-3. Epub 2018 Mar 2. PMID: 29497954; PMCID: PMC5984887.

Dag ZÖ, Dilbaz B. Impact of obesity on infertility in women. J Turk Ger Gynecol Assoc. 2015 Jun 1;16(2):111-7. doi: 10.5152/jtgga.2015.15232. PMID: 26097395; PMCID: PMC4456969.

DeAngelis AM, Roy-O'Reilly M, Rodriguez A. Genetic alterations affecting cholesterol metabolism and human fertility. Biol Reprod. 2014 Nov;91(5):117. doi: 10.1095/biolreprod.114.119883. Epub 2014 Aug 13. PMID: 25122065; PMCID: PMC4434926.

Elkin RG, Bauer R, Schneider WJ. The restricted ovulator chicken strain: an oviparous vertebrate model of reproductive dysfunction caused by a gene defect affecting an oocyte-specific receptor. Anim Reprod Sci. 2012 Dec;136(1-2):1-13. doi: 10.1016/j.anireprosci.2012.10.002. Epub 2012 Oct 18. PMID: 23123285; PMCID: PMC3521959.

Favari E, Calabresi L, Adorni MP, Jessup W, Simonelli S, Franceschini G, Bernini F. Small discoidal pre-beta1 HDL particles are efficient acceptors of cell cholesterol via ABCA1 and ABCG1. Biochemistry. 2009 Nov 24;48(46):11067-74. doi: 10.1021/bi901564g. PMID: 19839639.

Feingold KR. Introduction to Lipids and Lipoproteins. [Updated 2021 Jan 19]. In: Feingold KR, Anawalt B, Blackman MR, et al., editors. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.; 2000-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK305896/

Futamata R, Kinoshita M, Ogiwara K, Kioka N, Ueda K. Cholesterol accumulation in ovarian follicles causes ovulation defects in Abca1a-/-Japanese medaka (Oryzias latipes). Heliyon. 2023 Jan 31;9(2):e13291. doi: 10.1016/j.heliyon.2023.e13291. PMID: 36816300; PMCID: PMC9932449.

Gao M, Liu D. The liver X receptor agonist T0901317 protects mice from high fat diet-induced obesity and insulin resistance. AAPS J. 2013 Jan;15(1):258-66. doi: 10.1208/s12248-012-9429-3. Epub 2012 Nov 22. PMID: 23180161; PMCID: PMC3535091.

Hildebrand RB, Lammers B, Meurs I, Korporaal SJ, De Haan W, Zhao Y, Kruijt JK, Praticò D, Schimmel AW, Holleboom AG, Hoekstra M, Kuivenhoven JA, Van Berkel TJ, Rensen PC, Van Eck M. Restoration of high-density lipoprotein levels by cholesteryl ester transfer protein expression in scavenger receptor class B type I (SR-BI) knockout mice does not normalize pathologies associated with SR-BI deficiency. Arterioscler Thromb Vasc Biol. 2010 Jul;30(7):1439-45. doi: 10.1161/ATVBAHA.110.205153. Epub 2010 Apr 29. PMID: 20431066.

Ji A, Wroblewski JM, Cai L, de Beer MC, Webb NR, van der Westhuyzen DR. Nascent HDL formation in hepatocytes and role of ABCA1, ABCG1, and SR-BI. J Lipid Res. 2012 Mar;53(3):446-455. doi: 10.1194/jlr.M017079. Epub 2011 Dec 20. PMID: 22190590; PMCID: PMC3276468.

Jiménez LM, Binelli M, Bertolin K, Pelletier RM, Murphy BD. Scavenger receptor-B1 and luteal function in mice. J Lipid Res. 2010 Aug;51(8):2362-71. doi: 10.1194/jlr.M006973. Epub 2010 Apr 19. PMID: 20404351; PMCID: PMC2903804.

Kim K, Bloom MS, Browne RW, Bell EM, Yucel RM, Fujimoto VY. Associations between follicular fluid high density lipoprotein particle components and embryo quality among in vitro fertilization patients. J Assist Reprod Genet. 2017 Jan;34(1):1-10. doi: 10.1007/s10815-016-0826-x. Epub 2016 Nov 29. PMID: 27900613; PMCID: PMC5237431.

Klees S, Schlüter JS, Schellhorn J, Bertram H, Kurzweg AC, Ramzan F, Schmitt AO, Gültas M. Comparative Investigation of Gene Regulatory Processes Underlying Avian Influenza Viruses in Chicken and Duck. Biology (Basel). 2022 Jan 29;11(2):219. doi: 10.3390/biology11020219. PMID: 35205087; PMCID: PMC8868632.

Krieger M, Kozarsky K. Influence of the HDL receptor SR-BI on atherosclerosis. Curr Opin Lipidol. 1999 Dec;10(6):491-7. doi: 10.1097/00041433-199912000-00003. PMID: 10680042.

Le Goff W, Guerin M, Chapman MJ. Pharmacological modulation of cholesteryl ester transfer protein, a new therapeutic target in atherogenic dyslipidemia. Pharmacol Ther. 2004 Jan;101(1):17-38. doi: 10.1016/j.pharmthera.2003.10.001. PMID: 14729390.

Liu T, Qu J, Tian M, Yang R, Song X, Li R, Yan J, Qiao J. Lipid Metabolic Process Involved in Oocyte Maturation During Folliculogenesis. Front Cell Dev Biol. 2022 Mar 31;10:806890. doi: 10.3389/fcell.2022.806890. PMID: 35433675; PMCID: PMC9009531.

Marques LR, Diniz TA, Antunes BM, Rossi FE, Caperuto EC, Lira FS, Gonçalves DC. Reverse Cholesterol Transport: Molecular Mechanisms and the Non-medical Approach to Enhance HDL Cholesterol. Front Physiol. 2018 May 15;9:526. doi: 10.3389/fphys.2018.00526. PMID: 29867567; PMCID: PMC5962737.

Miettinen HE, Rayburn H, Krieger M. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J Clin Invest. 2001 Dec;108(11):1717-22. doi: 10.1172/JCI13288. PMID: 11733567; PMCID: PMC200987.

Miller WL, Auchus RJ. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev. 2011 Feb;32(1):81-151. doi: 10.1210/er.2010-0013. Epub 2010 Nov 4. Erratum in: Endocr Rev. 2011 Aug;32(4):579. PMID: 21051590; PMCID: PMC3365799.

Miranda-Jiménez L, Murphy BD. Lipoprotein receptor expression during luteinization of the ovarian follicle. Am J Physiol Endocrinol Metab. 2007 Oct;293(4):E1053-61. doi: 10.1152/ajpendo.00554.2006. Epub 2007 Aug 14. PMID: 17698983.

Nagy RA, van Montfoort APA, Groen H, Homminga I, Andrei D, Mistry RH, Anderson JLC, Hoek A, Tietge UJF. Anti-oxidative function of follicular fluid HDL and outcomes of modified natural cycle-IVF. Sci Rep. 2019 Sep 6;9(1):12817. doi: 10.1038/s41598-019-49091-3. PMID: 31492916; PMCID: PMC6731220.

Nandi S, Ma L, Denis M, Karwatsky J, Li Z, Jiang XC, Zha X. ABCA1-mediated cholesterol efflux generates microparticles in addition to HDL through processes governed by membrane rigidity. J Lipid Res. 2009 Mar;50(3):456-466. doi: 10.1194/jlr.M800345-JLR200. Epub 2008 Oct 21. PMID: 18941142.

Palme N, Becher AC, Merkl M, Glösmann M, Aurich C, Schäfer-Somi S. Immunolocalization of the cholesterol transporters ABCA1 and ABCG1 in canine reproductive tract tissues and spermatozoa. Reprod Domest Anim. 2014 Jun;49(3):441-7. doi: 10.1111/rda.12294. Epub 2014 Mar 11. Erratum in: Reprod Domest Anim. 2015 Aug;50(4):704. PMID: 24612239.

Patel MB, Oza NA, Anand IS, Deshpande SS, Patel CN. Liver x receptor: a novel therapeutic target. Indian J Pharm Sci. 2008 Mar-Apr;70(2):135-44. doi: 10.4103/0250-474X.41445. PMID: 20046702; PMCID: PMC2792482.

Pervaiz MA, Gau G, Jaffe AS, Saenger AK, Baudhuin L, Ellison J. A Non-classical Presentation of Tangier Disease with Three ABCA1 Mutations. JIMD Rep. 2012;4:109-11. doi: 10.1007/8904_2011_81. Epub 2011 Sep 28. PMID: 23430904; PMCID: PMC3509900.

Poznyak AV, Nikiforov NG, Markin AM, Kashirskikh DA, Myasoedova VA, Gerasimova EV, Orekhov AN. Overview of OxLDL and Its Impact on Cardiovascular Health: Focus on Atherosclerosis. Front Pharmacol. 2021 Jan 11;11:613780. doi: 10.3389/fphar.2020.613780. PMID: 33510639; PMCID: PMC7836017.

Quiroz A, Molina P, Santander N, Gallardo D, Rigotti A, Busso D. Ovarian cholesterol efflux: ATP-binding cassette transporters and follicular fluid HDL regulate cholesterol content in mouse oocytes†. Biol Reprod. 2020 Feb 14;102(2):348-361. doi: 10.1093/biolre/ioz159. PMID: 31423535.

Robker RL, Hennebold JD, Russell DL. Coordination of Ovulation and Oocyte Maturation: A Good Egg at the Right Time. Endocrinology. 2018 Sep 1;159(9):3209-3218. doi: 10.1210/en.2018-00485. PMID: 30010832; PMCID: PMC6456964.

Rodriguez A. High HDL-Cholesterol Paradox: SCARB1-LAG3-HDL Axis. Curr Atheroscler Rep. 2021 Jan 5;23(1):5. doi: 10.1007/s11883-020-00902-3. PMID: 33398433; PMCID: PMC7782461.

Rosales C, Yelamanchili D, Gillard BK, Liu J, Gotto AM Jr, Pownall HJ. Serum opacity factor rescues fertility among female Scarb1-/- mice by reducing HDL-free cholesterol bioavailability. J Lipid Res. 2023 Feb;64(2):100327. doi: 10.1016/j.jlr.2022.100327. Epub 2022 Dec 31. PMID: 36596339; PMCID: PMC9932678.

Schomberg DW, Couse JF, Mukherjee A, Lubahn DB, Sar M, Mayo KE, Korach KS. Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology. 1999 Jun;140(6):2733-44. doi: 10.1210/endo.140.6.6823. PMID: 10342864.

Shen WJ, Asthana S, Kraemer FB, Azhar S. Scavenger receptor B type 1: expression, molecular regulation, and cholesterol transport function. J Lipid Res. 2018 Jul;59(7):1114-1131. doi: 10.1194/jlr.R083121. Epub 2018 May 2. PMID: 29720388; PMCID: PMC6027903.

Sorci-Thomas MG, Zabalawi M, Bharadwaj MS, Wilhelm AJ, Owen JS, Asztalos BF, Bhat S, Thomas MJ. Dysfunctional HDL containing L159R ApoA-I leads to exacerbation of atherosclerosis in hyperlipidemic mice. Biochim Biophys Acta. 2012 Mar;1821(3):502-12. doi: 10.1016/j.bbalip.2011.08.019. Epub 2011 Sep 14. PMID: 21944998; PMCID: PMC3690280.

Tolani S, Pagler TA, Murphy AJ, Bochem AE, Abramowicz S, Welch C, Nagareddy PR, Holleran S, Hovingh GK, Kuivenhoven JA, Tall AR. Hypercholesterolemia and reduced HDL-C promote hematopoietic stem cell proliferation and monocytosis: studies in mice and FH children. Atherosclerosis. 2013 Jul;229(1):79-85. doi: 10.1016/j.atherosclerosis.2013.03.031. Epub 2013 Apr 19. PMID: 23684512; PMCID: PMC3691284.

Trigatti B, Rayburn H, Viñals M, Braun A, Miettinen H, Penman M, Hertz M, Schrenzel M, Amigo L, Rigotti A, Krieger M. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9322-7. doi: 10.1073/pnas.96.16.9322. PMID: 10430941; PMCID: PMC17781.

Vaisman BL, Vishnyakova TG, Freeman LA, Amar MJ, Demosky SJ, Liu C, Stonik JA, Sampson ML, Pryor M, Bocharov AV, Eggerman TL, Patterson AP, Remaley AT. Endothelial Expression of Scavenger Receptor Class B, Type I Protects against Development of Atherosclerosis in Mice. Biomed Res Int. 2015;2015:607120. doi: 10.1155/2015/607120. Epub 2015 Oct 4. PMID: 26504816; PMCID: PMC4609362.

Wang L, Zhou C, Sun J, Zhang Q, Lai D. Glutamine and norepinephrine in follicular fluid synergistically enhance the antioxidant capacity of human granulosa cells and the outcome of IVF-ET. Sci Rep. 2022 Jun 15;12(1):9936. doi: 10.1038/s41598-022-14201-1. PMID: 35705692; PMCID: PMC9200745.

Yesilaltay A, Dokshin GA, Busso D, Wang L, Galiani D, Chavarria T, Vasile E, Quilaqueo L, Orellana JA, Walzer D, Shalgi R, Dekel N, Albertini DF, Rigotti A, Page DC, Krieger M. Excess cholesterol induces mouse egg activation and may cause female infertility. Proc Natl Acad Sci U S A. 2014 Nov 18;111(46):E4972-80. doi: 10.1073/pnas.1418954111. Epub 2014 Nov 3. PMID: 25368174; PMCID: PMC4246315.

Yuan B, Yang J, Dubeau L, Hu Y, Li R. A Phosphotyrosine Switch in Estrogen Receptor β Is Required for Mouse Ovarian Function. Front Cell Dev Biol. 2021 Apr 9;9:649087. doi: 10.3389/fcell.2021.649087. PMID: 33898441; PMCID: PMC8063698.

Yvan-Charvet L, Wang N, Tall AR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler Thromb Vasc Biol. 2010 Feb;30(2):139-43. doi: 10.1161/ATVBAHA.108.179283. Epub 2009 Oct 1. PMID: 19797709; PMCID: PMC2812788.

Zanoni P, Khetarpal SA, Larach DB, Hancock-Cerutti WF, Millar JS, Cuchel M, DerOhannessian S, Kontush A, Surendran P, Saleheen D, Trompet S, Jukema JW, De Craen A, Deloukas P, Sattar N, Ford I, Packard C, Majumder Aa, Alam DS, Di Angelantonio E, Abecasis G, Chowdhury R, Erdmann J, Nordestgaard BG, Nielsen SF, Tybjærg-Hansen A, Schmidt RF, Kuulasmaa K, Liu DJ, Perola M, Blankenberg S, Salomaa V, Männistö S, Amouyel P, Arveiler D, Ferrieres J, Müller-Nurasyid M, Ferrario M, Kee F, Willer CJ, Samani N, Schunkert H, Butterworth AS, Howson JM, Peloso GM, Stitziel NO, Danesh J, Kathiresan S, Rader DJ; CHD Exome+ Consortium; CARDIoGRAM Exome Consortium; Global Lipids Genetics Consortium. Rare variant in scavenger receptor BI raises HDL cholesterol and increases risk of coronary heart disease. Science. 2016 Mar 11;351(6278):1166-71. doi: 10.1126/science.aad3517. PMID: 26965621; PMCID: PMC4889017.

Zeng TT, Tang DJ, Ye YX, Su J, Jiang H. Influence of SCARB1 gene SNPs on serum lipid levels and susceptibility to coronary heart disease and cerebral infarction in a Chinese population. Gene. 2017 Aug 30;626:319-325. doi: 10.1016/j.gene.2017.05.020. Epub 2017 May 24. PMID: 28552715.

PDF
Abstract
Export Citation

View Dimensions

View Plumx

View Altmetric

Save

0
Citation

440
View

Share