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Current Molecular Medicine

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ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

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Review Article

The Effects of Cholesterol Metabolism on Follicular Development and Ovarian Function

Author(s): Qin Huang, Yannan Liu, Zhen Yang, Yuanjie Xie and Zhongcheng Mo*

Volume 19, Issue 10, 2019

Page: [719 - 730] Pages: 12

DOI: 10.2174/1566524019666190916155004

Price: $65

Abstract

Cholesterol is an important substrate for the synthesis of ovarian sex hormones and has an important influence on follicular development. The cholesterol in follicular fluid is mainly derived from plasma. High-density lipoprotein (HDL) and lowdensity lipoprotein (LDL) play important roles in ovarian cholesterol transport. The knockout of related receptors in the mammalian HDL and LDL pathways results in the reduction or absence of fertility, leading us to support the importance of cholesterol homeostasis in the ovary. However, little is known about ovarian cholesterol metabolism and the complex regulation of its homeostasis. Here, we reviewed the cholesterol metabolism in the ovary and speculated that regardless of the functioning of cholesterol metabolism in the system or the ovarian microenvironment, an imbalance in cholesterol homeostasis is likely to have an adverse effect on ovarian structure and function.

Keywords: Ovarian follicles, lipoprotein, sterol carrier protein 2, steroidogenesis, cholesterol homeostasis, fertility.

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[1]
Murase T, Iwase A, Komatsu K, et al. Follicle dynamics: visualization and analysis of follicle growth and maturation using murine ovarian tissue culture. J Assist Reprod Genet 2018; 35(2): 339-43.
[http://dx.doi.org/10.1007/s10815-017-1073-5] [PMID: 29080194]
[2]
Rimon-Dahari N, Yerushalmi-Heinemann L, Alyagor L, Dekel N. Ovarian Folliculogenesis. Results Probl Cell Differ 2016; 58: 167-90.
[http://dx.doi.org/10.1007/978-3-319-31973-5_7] [PMID: 27300179]
[3]
Chou CH, Chen MJ. The Effect of steroid hormones on ovarian follicle development. Vitam Horm 2018; 107: 155-75.
[http://dx.doi.org/10.1016/bs.vh.2018.01.013] [PMID: 29544629]
[4]
Hernandez-Medrano JH, Campbell BK, Webb R. Nutritional influences on folliculogenesis.Reproduction in domestic animals = Zuchthygiene. 2012; 47(Suppl 4): 274-82.
[http://dx.doi.org/10.1111/j.1439-0531.2012.02086.x]
[5]
Palma GA, Argañaraz ME, Barrera AD, Rodler D, Mutto AA, Sinowatz F. Biology and biotechnology of follicle development ScientificWorldJournal 2012; 2012.
[http://dx.doi.org/10.1100/2012/938138] [PMID: 22666170]
[6]
Komatsu K, Masubuchi S. Observation of the dynamics of follicular development in the ovary. Reprod Med Biol 2016; 16(1): 21-7.
[http://dx.doi.org/10.1002/rmb2.12010] [PMID: 29259446]
[7]
Rinaldi L, Selman H. Profile of follitropin alpha/lutropin alpha combination for the stimulation of follicular development in women with severe luteinizing hormone and follicle-stimulating hormone deficiency. Int J Womens Health 2016; 8: 169-79.
[http://dx.doi.org/10.2147/IJWH.S88904] [PMID: 27307766]
[8]
Stouffer RL, Xu F, Duffy DM. Molecular control of ovulation and luteinization in the primate follicle Frontiers in bioscience: a journal and virtual library, 2007; 12: 297-307.
[http://dx.doi.org/10.2741/2065]
[9]
Allinquant B, Clamagirand C, Potier MC. Role of cholesterol metabolism in the pathogenesis of Alzheimer’s disease. Curr Opin Clin Nutr Metab Care 2014; 17(4): 319-23.
[http://dx.doi.org/10.1097/MCO.0000000000000069] [PMID: 24839952]
[10]
Cortes VA, Busso D, Maiz A, Arteaga A, Nervi F, Rigotti A. Physiological and pathological implications of cholesterol. Front Biosci 2014; 19: 416-28.
[http://dx.doi.org/10.2741/4216] [PMID: 24389193]
[11]
Ofori-Asenso R, Zoungas S, Tonkin A, Liew D. LDL-cholesterol is the only clinically relevant biomarker for atherosclerotic cardiovascular disease (ASCVD) risk. Clin Pharmacol Ther 2018; 104(2): 235-8.
[http://dx.doi.org/10.1002/cpt.1125] [PMID: 30004113]
[12]
Favari E, Chroni A, Tietge UJ, Zanotti I, Escolà-Gil JC, Bernini F. Cholesterol efflux and reverse cholesterol transport. Handb Exp Pharmacol 2015; 224: 181-206.
[http://dx.doi.org/10.1007/978-3-319-09665-0_4] [PMID: 25522988]
[13]
Murao K, Yu X, Imachi H, et al. Hyperglycemia suppresses hepatic scavenger receptor class B type I expression. Am J Physiol Endocrinol Metab 2008; 294(1): E78-87.
[http://dx.doi.org/10.1152/ajpendo.00023.2007] [PMID: 17957039]
[14]
Davis HR Jr, Basso F, Hoos LM, Tetzloff G, Lally SM, Altmann SW. Cholesterol homeostasis by the intestine: lessons from Niemann-Pick C1 Like 1 [NPC1L1). Atheroscler Suppl 2008; 9(2): 77-81.
[http://dx.doi.org/10.1016/j.atherosclerosissup.2008.05.008] [PMID: 18585981]
[15]
Jiménez LM, Binelli M, Bertolin K, Pelletier RM, Murphy BD. Scavenger receptor-B1 and luteal function in mice. J Lipid Res 2010; 51(8): 2362-71.
[http://dx.doi.org/10.1194/jlr.M006973] [PMID: 20404351]
[16]
Zhang J, Liu Q. Cholesterol metabolism and homeostasis in the brain. Protein Cell 2015; 6(4): 254-64.
[http://dx.doi.org/10.1007/s13238-014-0131-3] [PMID: 25682154]
[17]
Siu MK, Cheng CY. The blood-follicle barrier (BFB) in disease and in ovarian function. Adv Exp Med Biol 2012; 763: 186-92.
[http://dx.doi.org/10.1007/978-1-4614-4711-5_9] [PMID: 23397625]
[18]
Kenigsberg S, Wyse BA, Librach CL, da Silveira JC. Protocol for exosome isolation from small volume of ovarian follicular fluid: Evaluation of ultracentrifugation and commercial kits. Methods Mol Biol 2017; 1660: 321-41.
[http://dx.doi.org/10.1007/978-1-4939-7253-1_26] [PMID: 28828668]
[19]
Kraemer FB. Adrenal cholesterol utilization. Mol Cell Endocrinol 2007; 265-266: 42-5.
[http://dx.doi.org/10.1016/j.mce.2006.12.001] [PMID: 17208360]
[20]
Bloom MS, Kim K, Fujimoto VY, Browne RW. Variability in the components of high-density lipoprotein particles measured in human ovarian follicular fluid: a cross-sectional analysis. Fertil Steril 2014; 101(5): 1431-40.
[http://dx.doi.org/10.1016/j.fertnstert.2014.01.028] [PMID: 24581578]
[21]
Grummer RR, Carroll DJ. A review of lipoprotein cholesterol metabolism: importance to ovarian function. J Anim Sci 1988; 66(12): 3160-73.
[http://dx.doi.org/10.2527/jas1988.66123160x] [PMID: 3068221]
[22]
Yamada S, Fujiwara H, Kataoka N, et al. Stage-specific uptake of apolipoprotein-B in ovarian follicles and corpora lutea of the menstrual cycle and early pregnancy. Hum Reprod 1998; 13(4): 944-52.
[http://dx.doi.org/10.1093/humrep/13.4.944] [PMID: 9619552]
[23]
Murata M, Tamura A, Kodama H, Hirano H, Takahashi O, Tanaka T. Possible involvement of very low density lipoproteins in steroidogenesis in the human ovary. Mol Hum Reprod 1998; 4(8): 797-801.
[http://dx.doi.org/10.1093/molehr/4.8.797] [PMID: 9733438]
[24]
Zerbinatti CV, Dyer CA. Apolipoprotein E peptide stimulation of rat ovarian theca cell androgen synthesis is mediated by members of the low density lipoprotein receptor superfamily. Biol Reprod 1999; 61(3): 665-72.
[http://dx.doi.org/10.1095/biolreprod61.3.665] [PMID: 10456843]
[25]
Argov N, Sklan D. Expression of mRNA of lipoprotein receptor related protein 8, low density lipoprotein receptor, and very low density lipoprotein receptor in bovine ovarian cells during follicular development and corpus luteum formation and regression. Mol Reprod Dev 2004; 68(2): 169-75.
[http://dx.doi.org/10.1002/mrd.20072] [PMID: 15095337]
[26]
Argov N, Moallem U, Sklan D. Lipid transport in the developing bovine follicle: messenger RNA expression increases for selective uptake receptors and decreases for endocytosis receptors. Biol Reprod 2004; 71(2): 479-85.
[http://dx.doi.org/10.1095/biolreprod.104.028092] [PMID: 15056566]
[27]
Valckx SD, De Pauw I, De Neubourg D, et al. BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality. Hum Reprod 2012; 27(12): 3531-9.
[http://dx.doi.org/10.1093/humrep/des350] [PMID: 23019302]
[28]
Gautier T, Becker S, Drouineaud V, et al. Human luteinized granulosa cells secrete apoB100-containing lipoproteins. J Lipid Res 2010; 51(8): 2245-52.
[http://dx.doi.org/10.1194/jlr.M005181] [PMID: 20407020]
[29]
Hu S, Liu H, Pan Z, et al. Molecular cloning, expression profile and transcriptional modulation of two splice variants of very low density lipoprotein receptor during ovarian follicle development in geese (Anser cygnoide). Anim Reprod Sci 2014; 149(3-4): 281-96.
[http://dx.doi.org/10.1016/j.anireprosci.2014.06.024] [PMID: 25018046]
[30]
Fayad T, Lefebvre R, Nimpf J, Silversides DW, Lussier JG. Low-density lipoprotein receptor-related protein 8 (LRP8) is upregulated in granulosa cells of bovine dominant follicle: molecular characterization and spatio-temporal expression studies. Biol Reprod 2007; 76(3): 466-75.
[http://dx.doi.org/10.1095/biolreprod.106.057216] [PMID: 17108332]
[31]
Nicosia M, Moger WH, Dyer CA, Prack MM, Williams DL. Apolipoprotein-E messenger RNA in rat ovary is expressed in theca and interstitial cells and presumptive macrophage, but not in granulosa cells. Mol Endocrinol 1992; 6(6): 978-88.
[PMID: 1495495]
[32]
Azhar S, Leers-Sucheta S, Reaven E. Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and ‘selective’ pathway connection. Front Biosci 2003; 8: s998-s1029.
[http://dx.doi.org/10.2741/1165]
[33]
Reaven E, Lua Y, Nomoto A, et al. The selective pathway and a high-density lipoprotein receptor (SR-BI) in ovarian granulosa cells of the mouse. Biochim Biophys Acta 1999; 1436(3): 565-76.
[http://dx.doi.org/10.1016/S0005-2760(98)00169-6] [PMID: 9989286]
[34]
Li X, Peegel H, Menon KM. In situ hybridization of high density lipoprotein (scavenger, type 1) receptor messenger ribonucleic acid (mRNA) during folliculogenesis and luteinization: evidence for mRNA expression and induction by human chorionic gonadotropin specifically in cell types that use cholesterol for steroidogenesis. Endocrinology 1998; 139(7): 3043-9.
[http://dx.doi.org/10.1210/endo.139.7.6108] [PMID: 9645674]
[35]
Nandi S, Kumar VG, Manjunatha BM, Gupta PS. Biochemical composition of ovine follicular fluid in relation to follicle size. Dev Growth Differ 2007; 49(1): 61-6.
[http://dx.doi.org/10.1111/j.1440-169X.2007.00901.x] [PMID: 17227345]
[36]
Endresen MJ, Haug E, Abyholm T, Henriksen T. The source of cholesterol for progesterone synthesis in cultured preovulatory human granulosa cells. Acta Endocrinol (Copenh) 1990; 123(3): 359-64.
[http://dx.doi.org/10.1530/acta.0.1230359] [PMID: 2239084]
[37]
Oon VJ, Johnson MR. The regulation of the human corpus luteum steroidogenesis: a hypothesis? Hum Reprod Update 2000; 6(5): 519-29.
[http://dx.doi.org/10.1093/humupd/6.5.519] [PMID: 11045882]
[38]
Miranda-Jiménez L, Murphy BD. Lipoprotein receptor expression during luteinization of the ovarian follicle. Am J Physiol Endocrinol Metab 2007; 293(4): E1053-61.
[http://dx.doi.org/10.1152/ajpendo.00554.2006] [PMID: 17698983]
[39]
Murphy BD, Silavin SL. Luteotrophic agents and steroid substrate utilization. Oxf Rev Reprod Biol 1989; 11: 179-223.
[PMID: 2560824]
[40]
Fujimoto VY, Kane JP, Ishida BY, Bloom MS, Browne RW. High-density lipoprotein metabolism and the human embryo. Hum Reprod Update 2010; 16(1): 20-38.
[http://dx.doi.org/10.1093/humupd/dmp029] [PMID: 19700490]
[41]
Tong MH, Christenson LK, Song WC. Aberrant cholesterol transport and impaired steroidogenesis in Leydig cells lacking estrogen sulfotransferase. Endocrinology 2004; 145(5): 2487-97.
[http://dx.doi.org/10.1210/en.2003-1237] [PMID: 14749355]
[42]
Liu CC, Kanekiyo T, Roth B, Bu G. Tyrosine-based signal mediates LRP6 receptor endocytosis and desensitization of Wnt/β-catenin pathway signaling. J Biol Chem 2014; 289(40): 27562-70.
[http://dx.doi.org/10.1074/jbc.M113.533927] [PMID: 25143377]
[43]
Azhar S, Tsai L, Medicherla S, Chandrasekher Y, Giudice L, Reaven E. Human granulosa cells use high density lipoprotein cholesterol for steroidogenesis. J Clin Endocrinol Metab 1998; 83(3): 983-91.
[http://dx.doi.org/10.1210/jc.83.3.983] [PMID: 9506760]
[44]
Wang Y, Meng C, Wei Q, Shi F, Mao D. Expression and regulation of scavenger receptor class B type 1 in the rat ovary and uterus during the estrous cycle. Acta Histochem 2015; 117(3): 297-304.
[http://dx.doi.org/10.1016/j.acthis.2015.03.007] [PMID: 25817199]
[45]
Magoffin DA. Ovarian theca cell. Int J Biochem Cell Biol 2005; 37(7): 1344-9.
[http://dx.doi.org/10.1016/j.biocel.2005.01.016] [PMID: 15833266]
[46]
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; 97(6): 862-72.
[http://dx.doi.org/10.1093/biolre/iox134] [PMID: 29092018]
[47]
Velasco M, Alexander C, King J, Zhao Y, Garcia J, Rodriguez A. Association of lower plasma estradiol levels and low expression of scavenger receptor class B, type I in infertile women. Fertil Steril 2006; 85(5): 1391-7.
[http://dx.doi.org/10.1016/j.fertnstert.2005.10.046] [PMID: 16600224]
[48]
Kolmakova A, Wang J, Brogan R, Chaffin C, Rodriguez A. Deficiency of scavenger receptor class B type I negatively affects progesterone secretion in human granulosa cells. Endocrinology 2010; 151(11): 5519-27.
[http://dx.doi.org/10.1210/en.2010-0347] [PMID: 20844007]
[49]
Sato N, Kawamura K, Fukuda J, et al. Expression of LDL receptor and uptake of LDL in mouse preimplantation embryos. Mol Cell Endocrinol 2003; 202(1-2): 191-4.
[http://dx.doi.org/10.1016/S0303-7207(03)00082-0] [PMID: 12770750]
[50]
Xie C, Richardson JA, Turley SD, Dietschy JM. Cholesterol substrate pools and steroid hormone levels are normal in the face of mutational inactivation of NPC1 protein. J Lipid Res 2006; 47(5): 953-63.
[http://dx.doi.org/10.1194/jlr.M500534-JLR200] [PMID: 16461760]
[51]
Milligan S, Martin GG, Landrock D, et al. Ablating both Fabp1 and Scp2/Scpx (TKO) induces hepatic phospholipid and cholesterol accumulation in high fat-fed mice. Biochim Biophys Acta Mol Cell Biol Lipids 2018; 1863(3): 323-38.
[http://dx.doi.org/10.1016/j.bbalip.2017.12.013] [PMID: 29307784]
[52]
He H, Wang J, Yannie PJ, Kakiyama G, Korzun WJ, Ghosh S. Sterol carrier protein-2 deficiency attenuates diet-induced dyslipidemia and atherosclerosis in mice. J Biol Chem 2018; 293(24): 9223-31.
[http://dx.doi.org/10.1074/jbc.RA118.002290] [PMID: 29700117]
[53]
Petrescu AD, Gallegos AM, Okamura Y, Strauss JF III, Schroeder F. Steroidogenic acute regulatory protein binds cholesterol and modulates mitochondrial membrane sterol domain dynamics. J Biol Chem 2001; 276(40): 36970-82.
[http://dx.doi.org/10.1074/jbc.M101939200] [PMID: 11489878]
[54]
McLean MP, Puryear TK, Khan I, et al. Estradiol regulation of sterol carrier protein-2 independent of cytochrome P450 side-chain cleavage expression in the rat corpus luteum. Endocrinology 1989; 125(3): 1337-44.
[http://dx.doi.org/10.1210/endo-125-3-1337] [PMID: 2474437]
[55]
McLean MP, Nelson SE, Billheimer JT, Gibori G. Differential capacity for cholesterol transport and processing in large and small rat luteal cells. Endocrinology 1992; 131(5): 2203-12.
[http://dx.doi.org/10.1210/endo.131.5.1425418] [PMID: 1425418]
[56]
Rone MB, Fan J, Papadopoulos V. Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim Biophys Acta 2009; 1791(7): 646-58.
[http://dx.doi.org/10.1016/j.bbalip.2009.03.001] [PMID: 19286473]
[57]
LaVoie HA, Benoit AM, Garmey JC, Dailey RA, Wright DJ, Veldhuis JD. Coordinate developmental expression of genes regulating sterol economy and cholesterol side-chain cleavage in the porcine ovary. Biol Reprod 1997; 57(2): 402-7.
[http://dx.doi.org/10.1095/biolreprod57.2.402] [PMID: 9241056]
[58]
Azhar S, Nomoto A, Leers-Sucheta S, Reaven E. Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model. J Lipid Res 1998; 39(8): 1616-28.
[PMID: 9717722]
[59]
Wu Q, Sucheta S, Azhar S, Menon KM. Lipoprotein enhancement of ovarian theca-interstitial cell steroidogenesis: relative contribution of scavenger receptor class B (type I) and adenosine 5′-triphosphate- binding cassette (type A1) transporter in high-density lipoprotein-cholesterol transport and androgen synthesis. Endocrinology 2003; 144(6): 2437-45.
[http://dx.doi.org/10.1210/en.2002-221110] [PMID: 12746305]
[60]
Christianson MS, Yates M. Scavenger receptor class B type 1 gene polymorphisms and female fertility. Curr Opin Endocrinol Diabetes Obes 2012; 19(2): 115-20.
[http://dx.doi.org/10.1097/MED.0b013e3283505771] [PMID: 22261999]
[61]
Lai WA, Yeh YT, Lee MT, Wu LS, Ke FC, Hwang JJ. Ovarian granulosa cells utilize scavenger receptor SR-BI to evade cellular cholesterol homeostatic control for steroid synthesis. J Lipid Res 2013; 54(2): 365-78.
[http://dx.doi.org/10.1194/jlr.M030239] [PMID: 23197320]
[62]
Cui H, Zhao G, Wen J, Tong W. Follicle-stimulating hormone promotes the transformation of cholesterol to estrogen in mouse adipose tissue. Biochem Biophys Res Commun 2018; 495(3): 2331-7.
[http://dx.doi.org/10.1016/j.bbrc.2017.12.120] [PMID: 29274780]
[63]
Donaubauer EM, Law NC, Hunzicker-Dunn ME. Follicle-Stimulating Hormone (FSH)-dependent Regulation of Extracellular Regulated Kinase (ERK) Phosphorylation by the Mitogen-activated Protein (MAP) Kinase Phosphatase MKP3. J Biol Chem 2016; 291(37): 19701-12.
[http://dx.doi.org/10.1074/jbc.M116.733972] [PMID: 27422819]
[64]
Guo T, Zhang L, Cheng D, et al. Low-density lipoprotein receptor affects the fertility of female mice. Reprod Fertil Dev 2015; 27(8): 1222-32.
[http://dx.doi.org/10.1071/RD13436] [PMID: 25023761]
[65]
Kruit JK, Wijesekara N, Westwell-Roper C, et al. Loss of both ABCA1 and ABCG1 results in increased disturbances in islet sterol homeostasis, inflammation, and impaired β-cell function. Diabetes 2012; 61(3): 659-64.
[http://dx.doi.org/10.2337/db11-1341] [PMID: 22315310]
[66]
Ikonen E. Mechanisms for cellular cholesterol transport: defects and human disease. Physiol Rev 2006; 86(4): 1237-61.
[http://dx.doi.org/10.1152/physrev.00022.2005] [PMID: 17015489]
[67]
Di Renzo GC, Giardina I, Clerici G, Brillo E, Gerli S. Progesterone in normal and pathological pregnancy. Horm Mol Biol Clin Investig 2016; 27(1): 35-48.
[http://dx.doi.org/10.1515/hmbci-2016-0038] [PMID: 27662646]
[68]
Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest 1993; 92(2): 883-93.
[http://dx.doi.org/10.1172/JCI116663] [PMID: 8349823]
[69]
DeAngelis AM, Roy-O’Reilly M, Rodriguez A. Genetic alterations affecting cholesterol metabolism and human fertility. Biol Reprod 2014; 91(5): 117.
[http://dx.doi.org/10.1095/biolreprod.114.119883] [PMID: 25122065]
[70]
Miettinen HE, Rayburn H, Krieger M. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J Clin Invest 2001; 108(11): 1717-22.
[http://dx.doi.org/10.1172/JCI13288] [PMID: 11733567]
[71]
Yates M, Kolmakova A, Zhao Y, Rodriguez A. Clinical impact of scavenger receptor class B type I gene polymorphisms on human female fertility. Hum Reprod 2011; 26(7): 1910-6.
[http://dx.doi.org/10.1093/humrep/der124] [PMID: 21531995]
[72]
Schroeder F, Huang H, McIntosh AL, Atshaves BP, Martin GG, Kier AB. Caveolin, sterol carrier protein-2, membrane cholesterol-rich microdomains and intracellular cholesterol trafficking. Subcell Biochem 2010; 51: 279-318.
[http://dx.doi.org/10.1007/978-90-481-8622-8_10] [PMID: 20213548]
[73]
Wang J, Bie J, Ghosh S. Intracellular cholesterol transport proteins enhance hydrolysis of HDL-CEs and facilitate elimination of cholesterol into bile. J Lipid Res 2016; 57(9): 1712-9.
[http://dx.doi.org/10.1194/jlr.M069682] [PMID: 27381048]
[74]
Samardzija D, Pogrmic-Majkic K, Fa S, Stanic B, Jasnic J, Andric N. Bisphenol A decreases progesterone synthesis by disrupting cholesterol homeostasis in rat granulosa cells. Mol Cell Endocrinol 2018; 461: 55-63.
[http://dx.doi.org/10.1016/j.mce.2017.08.013] [PMID: 28859904]
[75]
Cannon MV, van Gilst WH, de Boer RA. Emerging role of liver X receptors in cardiac pathophysiology and heart failure. Basic Res Cardiol 2016; 111(1): 3.
[http://dx.doi.org/10.1007/s00395-015-0520-7] [PMID: 26611207]
[76]
Mouzat K, Chudinova A, Polge A, et al. Regulation of Brain Cholesterol: What Role Do Liver X Receptors Play in Neurodegenerative Diseases? Int J Mol Sci 2019; 20(16)E3858
[http://dx.doi.org/10.3390/ijms20163858] [PMID: 31398791]
[77]
Xu Y, Hernández-Ledezma JJ, Hutchison SM, Bogan RL. The liver X receptors and sterol regulatory element binding proteins alter progesterone secretion and are regulated by human chorionic gonadotropin in human luteinized granulosa cells. Mol Cell Endocrinol 2018; 473: 124-35.
[http://dx.doi.org/10.1016/j.mce.2018.01.011] [PMID: 29366778]
[78]
Guerreiro DD, de Lima LF, Mbemya GT, et al. ATP-binding cassette (ABC) transporters in caprine preantral follicles: gene and protein expression. Cell Tissue Res 2018; 372(3): 611-20.
[http://dx.doi.org/10.1007/s00441-018-2804-3] [PMID: 29488001]
[79]
Cordier AG, Léveillé P, Dupont C, et al. Dietary lipid and cholesterol induce ovarian dysfunction and abnormal LH response to stimulation in rabbits. PLoS One 2013; 8(5)e63101
[http://dx.doi.org/10.1371/journal.pone.0063101] [PMID: 23690983]
[80]
El-Sayyad HIH, El-Shershaby EMF, El-Mansi AA, El-Ashry NE. Anti-hypercholesterolemic impacts of barley and date palm fruits on the ovary of Wistar albino rats and their offspring. Reprod Biol 2018; 18(3): 236-51.
[http://dx.doi.org/10.1016/j.repbio.2018.07.003] [PMID: 30005909]
[81]
Robker RL, Akison LK, Bennett BD, et al. Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J Clin Endocrinol Metab 2009; 94(5): 1533-40.
[http://dx.doi.org/10.1210/jc.2008-2648] [PMID: 19223519]
[82]
Hallajzadeh J, Khoramdad M, Karamzad N, et al. Metabolic syndrome and its components among women with polycystic ovary syndrome: a systematic review and meta-analysis. J Cardiovasc Thorac Res 2018; 10(2): 56-69.
[http://dx.doi.org/10.15171/jcvtr.2018.10] [PMID: 30116503]
[83]
Prentice P, Viner RM. Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes 2013; 37(8): 1036-43.
[http://dx.doi.org/10.1038/ijo.2012.177] [PMID: 23164700]
[84]
Kajihara T, Uchino S, Suzuki M, Itakura A, Brosens JJ, Ishihara O. Increased ovarian follicle atresia in obese Zucker rats is associated with enhanced expression of the forkhead transcription factor FOXO1. Med Mol Morphol 2009; 42(4): 216-21.
[http://dx.doi.org/10.1007/s00795-009-0466-7] [PMID: 20033367]
[85]
Sagae SC, Menezes EF, Bonfleur ML, et al. Early onset of obesity induces reproductive deficits in female rats. Physiol Behav 2012; 105(5): 1104-11.
[http://dx.doi.org/10.1016/j.physbeh.2011.12.002] [PMID: 22178647]
[86]
Newell-Fugate AE, Taibl JN, Clark SG, Alloosh M, Sturek M, Krisher RL. Effects of diet-induced obesity on metabolic parameters and reproductive function in female Ossabaw minipigs. Comp Med 2014; 64(1): 44-9.
[PMID: 24512960]
[87]
Broughton DE, Moley KH. Obesity and female infertility: potential mediators of obesity’s impact. Fertil Steril 2017; 107(4): 840-7.
[http://dx.doi.org/10.1016/j.fertnstert.2017.01.017] [PMID: 28292619]
[88]
Wise LA, Rothman KJ, Mikkelsen EM, Sørensen HT, Riis A, Hatch EE. An internet-based prospective study of body size and time-to-pregnancy. Hum Reprod 2010; 25(1): 253-64.
[http://dx.doi.org/10.1093/humrep/dep360] [PMID: 19828554]
[89]
Chavarro JE, Rich-Edwards JW, Rosner BA, Willett WC. Diet and lifestyle in the prevention of ovulatory disorder infertility. Obstet Gynecol 2007; 110(5): 1050-8.
[http://dx.doi.org/10.1097/01.AOG.0000287293.25465.e1] [PMID: 17978119]
[90]
Seyam E, Al Gelany S, Abd Al Ghaney A, et al. Evaluation of prolonged use of statins on the clinical and biochemical abnormalities and ovulation dysfunction in single young women with polycystic ovary syndrome. Gynecol Endocrinol 2018; 34(7): 589-96.
[http://dx.doi.org/10.1080/09513590.2017.1418853] [PMID: 29258367]

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