Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and “selective” pathway connection

Azhar, Salman

doi:10.2741/1165

Cited by 109Cholesterol and Lipid MetabolismSteroid Chemistry and BiochemistryLipid Membrane Structure and Behavior

Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and “selective” pathway connection

Azhar, Salman·2003·Frontiers in bioscience

DOI 10.2741/1165

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Abstract

A constant supply of cholesterol is needed as a substrate for steroid hormone synthesis in steroidogenic tissues. Although there are three potential sources, which could contribute to the 'cholesterol pool', needed for steroidogenesis (i.e., de novo synthesis, hydrolysis of stored cholesteryl esters and exogenous lipoproteins), current evidence suggests that plasma lipoproteins are the major source of cholesterol for steroid production in adrenal gland, ovary and, under certain conditions, testicular Leydig cells. In many species, steroid producing cells and tissues obtain this lipoprotein-cholesterol by a unique pathway in which circulating lipoproteins bind to the surface of the steroidogenic cells and contribute their cholesteryl esters to the cells by a 'selective' process. This is a process in which cholesterol is selectively absorbed while the lipoprotein remains at the cell surface. The discovery of a specific receptor for this process (scavenger receptor class B, type I, known as SR-BI) has revolutionized our knowledge about the selective uptake pathway. The present review summarizes the functional importance of the selective pathway as a bulk cholesterol delivery system for steroidogenesis, and attempts to detail the expression, regulation and characteristics of SR-BI as it is deployed in steroidogenic systems as a means of achieving cholesterol balance.

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Plasma lipoproteins are widely accepted as the principal source of cholesterol used for steroid biosynthesis.
“All three primary steroidogenic organs, namely the adrenal cortex, gonads and placenta, can biosynthesize cholesterol de novo under the regulation of tropic hormones and plasma lipoproteins are widely accepted as the principal source of cholesterol used for steroid biosynthesis [[5], [6], [7], [8]].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [7]
All three primary steroidogenic organs (adrenal cortex, gonads, placenta) can biosynthesize cholesterol de novo under regulation of tropic hormones.
“All three primary steroidogenic organs, namely the adrenal cortex, gonads and placenta, can biosynthesize cholesterol de novo under the regulation of tropic hormones and plasma lipoproteins are widely accepted as the principal source of cholesterol used for steroid biosynthesis [[5], [6], [7], [8]].”
From Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review (2019) · cites this paper as [7]

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Cellular and molecular mechanisms of asbestos-induced fibrosis
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Separate mechanisms for the uptake of high and low density lipoproteins by mouse adrenal gland in vivo.
Kovanen, P. T., Schneider, W. J., Hillman, G. M., Goldstein, J. L., & Brown, M. S. (1979) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)50623-2 · Cited by 136 · see citing works
Co-expression of scavenger receptor-BI and caveolin-1 is associated with enhanced selective cholesteryl ester uptake in THP-1 macrophages
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Elevated Triglyceride Content Diminishes the Capacity of High Density Lipoprotein to Deliver Cholesteryl Esters via the Scavenger Receptor Class B Type I (SR-BI)
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“According to this model, HDL docks with SR-BI, forming a hydrophobic channel in which neutral core lipids, CE and TG are translocated to the plasma membrane (250).”
BackgroundMethod
Scavenger Receptor Class B, Type I-mediated Uptake of Various Lipids into Cells
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Steroidogenic Acute Regulatory Protein and Peripheral-Type Benzodiazepine Receptor Associate at the Mitochondrial Membrane
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Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model
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Scavenger receptor class B type I (SR-BI) mediates adhesion of neonatal murine microglia to fibrillar β-amyloid
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Correlation of low and high density lipoprotein binding in vivo with rates of lipoprotein degradation in the rat. A comparison of lipoproteins of rat and human origin.
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Intracellular Events in the “Selective” Transport of Lipoprotein-derived Cholesteryl Esters
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Differentiation-dependent expression and localization of the class B type I scavenger receptor in intestine
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Regulation of low density lipoprotein receptors by adrenocorticotropin in the adrenal gland of mice and rats in vivo.
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A Carboxyl-terminal PDZ-interacting Domain of Scavenger Receptor B, Type I Is Essential for Cell Surface Expression in Liver
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Phosphatidylserine Binding of Class B Scavenger Receptor Type I, a Phagocytosis Receptor of Testicular Sertoli Cells*
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Scavenger receptor class B type I affects cholesterol homeostasis by magnifying cholesterol flux between cells and HDL
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Scavenger Receptor-BI Inhibits ATP-binding Cassette Transporter 1- mediated Cholesterol Efflux in Macrophages
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Scavenger Receptors that Recognize Advanced Glycation End Products
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Steroid Production from Plasma Cholesterol. I. Conversion of Plasma Cholesterol to Placental Progesterone in Humans1
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Morphological evidence that high density lipoproteins are not internalized by steroid-producing cells during in situ organ perfusion.
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Scavenger Receptor, Class B, Type I-dependent Stimulation of Cholesterol Esterification by High Density Lipoproteins, Low Density Lipoproteins, and Nonlipoprotein Cholesterol
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Studies on the source of cholesterol used for steroid biosynthesis in cultured Leydig tumor cells.
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Effects of serum and lipoproteins on steroidogenesis in cultured bovine luteal cells
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Role of Scavenger Receptors SR-BI and CD36 in Selective Sterol Uptake in the Small Intestine
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Cholesterol esters selectively taken up from high-density lipoproteins are hydrolyzed extralysosomally
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Regulation of the selective uptake of high density lipoprotein-associated cholesteryl esters
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Human Granulosa Cells Use High Density Lipoprotein Cholesterol for Steroidogenesis1
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Structure and Function of the Peripheral-Type Benzodiazepine Receptor in Steroidogenic Cells
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Uptake of rat plasma HDL subfractions labeled with [3H]cholesteryl linoleyl ether or with 125I by cultured rat hepatocytes and adrenal cells
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Structure and function of membrane rafts
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Cholesterol and hepatic lipoprotein assembly and secretion
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Human Retinal Pigment Epithelial Cells Express Scavenger Receptors BI and BII
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Regulation of the selective uptake of high density lipoprotein-associated cholesteryl esters by human fibroblasts and Hep G2 hepatoma cells.
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Expression and Microvillar Localization of Scavenger Receptor, Class B, Type I (a High Density Lipoprotein Receptor) in Luteinized and Hormone-Desensitized Rat Ovarian Models
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The human breast carcinoma cell line HBL-100 acquires exogenous cholesterol from high-density lipoprotein via CLA-1 (CD-36 and LIMPII analogous 1)-mediated selective cholesteryl ester uptake
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Identification of the N-Linked Glycosylation Sites on the High Density Lipoprotein (HDL) Receptor SR-BI and Assessment of Their Effects on HDL Binding and Selective Lipid Uptake
Viñals, M., Xu, S., Vasile, E., & Krieger, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211073200 · Cited by 88 · see citing works
Distinctive properties of adrenal cortex mitochondria
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Blood Cholesterol and Hydrocortisone Production in Man: Quantitative Aspects of the Utilization of Circulating Cholesterol by the Adrenals at Rest and under Adrenocorticotropin Stimulation*
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Scavenger Receptor BI Transfers Major Lipoprotein-associated Phospholipids into the Cells
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Stimulation of Adrenal Cholesterol Uptake from Plasma by Adrenocorticotrophin
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Microvillar channels: a unique plasma membrane compartment for concentrating lipoproteins on the surface of rat adrenal cortical cells.
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Lipoprotein Lipase-mediated Selective Uptake from Low Density Lipoprotein Requires Cell Surface Proteoglycans and Is Independent of Scavenger Receptor Class B Type 1
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Plasma Lipoprotein Regulation of Progesterone Biosynthesis by Human Corpus Luteum Tissue in Organ Culture*
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Differential Regulation of Steroid Hormone Biosynthesis in R2C and MA-10 Leydig Tumor Cells: Role of SR-B1-Mediated Selective Cholesteryl Ester Transport1
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Cholesterogenesis: Derepression in Extrahepatic Tissues with 4-Aminopyrazolo [3,4- d ]pyrimidine
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Cellular and physiological roles of SR-BI, a lipoprotein receptor which mediates selective lipid uptake
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Down-regulation of intestinal scavenger receptor class B, type I (SR-BI) expression in rodents under conditions of deficient bile delivery to the intestine
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The Low Density Lipoprotein Receptor-related Protein Contributes to Selective Uptake of High Density Lipoprotein Cholesteryl Esters by SW872 Liposarcoma Cells and Primary Human Adipocytes
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Expression of scavenger receptor class B type 1 (SR-BI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system
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Regulation of scavenger receptor class B type I in hamster liver and Hep3B cells by endotoxin and cytokines
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The synthesis and metabolism of progesterone in the human and bovine ovary
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In SituHybridization 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 Steroidogenesis1
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Lipid Free Apolipoprotein E Binds to the Class B Type I Scavenger Receptor I (SR-BI) and Enhances Cholesteryl Ester Uptake from Lipoproteins
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Hepatic lipase facilitates the selective uptake of cholesteryl esters from remnant lipoproteins in apoE-deficient mice
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Chinese Hamster Ovary Cells Expressing a Cell Surface-anchored Form of Hepatic Lipase
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Caveolin-1 does not affect SR-BI-mediated cholesterol efflux or selective uptake of cholesteryl ester in two cell lines
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SERUM LIPOPROTEINS INCREASE TESTOSTERONE PRODUCTION IN hCG-DESENSITIZED LEYDIG CELLS
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Cholesteryl Ester Transfer Protein Mediates Selective Uptake of High Density Lipoprotein Cholesteryl Esters by Human Adipose Tissue
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Reconstituted Discoidal ApoE-Phospholipid Particles Are Ligands for the Scavenger Receptor BI
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Human Scavenger Receptor B1 Is Involved in Recognition of Apoptotic Thymocytes by Thymic Nurse Cells
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Receptor-mediated gonadotropin action in the ovary. Rat luteal cells preferentially utilize and are acutely dependent upon the plasma lipoprotein-supplied sterols in gonadotropin-stimulated steroid production.
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Cloning, Characterization, and Cellular Distribution of Rat Scavenger Receptor Class B Type I (SRBI) in the Ovary
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Angiotensin II Promotes Selective Uptake of High Density Lipoprotein Cholesterol Esters in Bovine Adrenal Glomerulosa and Human Adrenocortical Carcinoma Cells Through Induction of Scavenger Receptor Class B Type I
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Selective uptake of cholesteryl esters from low density lipoproteins in vitro and in vivo
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The role of apolipoproteins of HDL in the selective uptake of cholesteryl linoleyl ether by cultured rat and bovine adrenal cells
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The Inhibition of Low Density Lipoprotein Metabolism by Transforming Growth Factor-β Mediates Its Effects on Steroidogenesis in Bovine Adrenocortical Cellsin Vitro*
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Trophoblast‐like human choriocarcinoma cells serve as a suitable in vitro model for selective cholesteryl ester uptake from high density lipoproteins
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Apolipoprotein AII Enrichment of HDL Enhances Their Affinity for Class B Type I Scavenger Receptor but Inhibits Specific Cholesteryl Ester Uptake
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Metabolism of high density lipoproteins by the perfused rabbit liver.
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Experimental Glomerulopathy Alters Renal Cortical Cholesterol, SR-B1, ABCA1, and HMG CoA Reductase Expression
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Characterization and Chromosomal Localization of Rat Scavenger Receptor Class B Type I, a High Density Lipoprotein Receptor with a Putative Leucine Zipper Domain and Peroxisomal Targeting Sequence
Johnson, M. S. C., Svensson, P., Helou, K., Billig, H., Levan, G., Carlsson, L. M. S., & Carlsson, B. (1998) · Endocrinology · doi:10.1210/endo.139.1.5666 · Cited by 47 · see citing works
Role of Cholesterol in thein VivoBiosynthesis of Adrenal Steroids by the Dog
KRUM, A. A., Morris, M. D., & Bennett, L. L. (1964) · Endocrinology · doi:10.1210/endo-74-4-543 · Cited by 45 · see citing works
The kinetics of steroidogenesis activator polypeptide in the rat adrenal cortex
Mertz, L. M., & Pedersen, R. C. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84821-4 · Cited by 44 · see citing works
Interaction of lipoproteins with isolated ovary plasma membranes.
REAVEN, E. P., Shi, X. Y., & Azhar, S. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)30630-0 · Cited by 44 · see citing works
Scavenger Receptor Class B Type I in the Rat Ovary: Possible Role in High Density Lipoprotein Cholesterol Uptake and in the Recognition of Apoptotic Granulosa Cells
Svensson, P., Johnson, M. S. C., Ling, C., Carlsson, L. M. S., Billig, H., & Carlsson, B. (1999) · Endocrinology · doi:10.1210/endo.140.6.6693 · Cited by 42 · see citing works
Regulation of human fetal testicular secretion of testosterone: Low-density lipoprotein-cholesterol and cholesterol synthesized de novo as steroid precursor
Carr, B. R., Parker, C. R., Ōhashi, M., MacDonald, P. C., & Simpson, E. R. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90743-3 · Cited by 41 · see citing works
Studies on Lipoprotein and Adrenal Steroidogenesis: I. Roles of Low Density Lipoprotein- and High Density Lipoprotein- Cholesterol in Steroid Production in Cultured Human Adrenocortical Cells.
HIGASHIJIMA, M., Nawata, H., KATO, K.-I., & Ibayashi, H. (1987) · Endocrinologia Japonica · doi:10.1507/endocrj1954.34.635 · Cited by 40 · see citing works
Overexpression of SR-BI by adenoviral vector promotes clearance of apoA-I, but not apoB, in human apoB transgenic mice
Webb, N. R., de Beer, M. C., Yu, J., Kindy, M. S., Daugherty, A., van der Westhuyzen, D. R., & de Beer, F. C. (2002) · Journal of Lipid Research · doi:10.1194/jlr.m200026-jlr200 · Cited by 40 · see citing works
Estrogen Regulates Low Density Lipoprotein Metabolism by Cultured Swine Granulosa Cells*
Veldhuis, J. D., Gwynne, J. T., Azimi, P., Garmey, J. C., & JUCHTER, D. (1985) · Endocrinology · doi:10.1210/endo-117-4-1321 · Cited by 34 · see citing works
Influence of adrenocorticotropin on transport of a cholesteryl linoleate-low density lipoprotein complex into adrenal tumor cells.
Hall, P. F., & Nakamura, M. (1979) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)86349-4 · Cited by 33 · see citing works
Lipoprotein lipase mediates an increase in selective uptake of HDL-associated cholesteryl esters by cells in culture independent of scavenger receptor BI
Rinninger, F., Brundert, M., Brosch, I., Donarski, N., Budzinski, R., & Greten, H. (2001) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)31500-5 · Cited by 33 · see citing works
Effect of Low Density and High Density Lipoproteins on Progesterone Secretion by Dispersed Corpora Luteal Cells from Rats Treated with Aminopyrazolo-(3,4-d)pyrimidine*
Bruot, B. C., Wiest, W. G., & Collins, D. C. (1982) · Endocrinology · doi:10.1210/endo-110-5-1572 · Cited by 33 · see citing works
Receptor mediated gonadotropin action in gonadal tissues: Relationship between blood cholesterol levels and gonadotropin stimulated steroidogenesis in isolated rat leydig and luteal cells
Azhar, S., & Menon, K. M. J. (1982) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(82)90165-0 · Cited by 32 · see citing works
Expression and Hormonal Regulation of the High-Density Lipoprotein (HDL) Receptor Scavenger Receptor Class B Type I Messenger Ribonucleic Acid in the Rat Ovary
McLean, M. P., & Sandhoff, T. W. (1998) · Endocrine · doi:10.1385/endo:9:3:243 · Cited by 31 · see citing works
Bile Salt Stimulated Cholesterol Esterase Increases Uptake of High Density Lipoprotein-Associated Cholesteryl Esters by HepG2 Cells
Li, F., Huang, Y., & Hui, D. Y. (1996) · Biochemistry · doi:10.1021/bi952313q · Cited by 29 · see citing works
Angiotensin II stimulates receptor-mediated uptake of LDL by bovine adrenal cortical cells in primary culture
Leitersdorf, E., Stein, O. T., & Stein, Y. (1985) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(85)90272-3 · Cited by 28 · see citing works
Evidence for extralysosomal hydrolysis of high‐density lipoprotein cholesteryl esters in rat hepatoma cells (Fu5AH): A model for delivery of high‐density lipoprotein cholesterol
Delamatre, J. G., Carter, R. M., & Hornick, C. A. (1991) · Journal of Cellular Physiology · doi:10.1002/jcp.1041460104 · Cited by 27 · see citing works
Effect of apolipoprotein E-free high density lipoproteins on cholesterol metabolism in cultured pig hepatocytes.
Bachorik, P. S., Virgil, D. G., & Kwiterovich, P. O. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)76475-8 · Cited by 25 · see citing works
Delivery of high-density lipoprotein free and esterified cholesterol to bile by the perfused monkey liver
Scobey, M., Johnson, F. L., & Rudel, L. L. (1989) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1989.257.4.g644 · Cited by 25 · see citing works
Signal Transduction Pathways Combining Peptide Hormones and Steroidogenesis
Waterman, M. R., & Keeney, D. S. (1996) · Vitamins and hormones · doi:10.1016/s0083-6729(08)60409-4 · Cited by 24 · see citing works
Uptake and metabolism of high-density lipoproteins by cultured rabbit hepatocytes
Wishart, R., & Mackinnon, M. (1990) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(90)90083-a · Cited by 23 · see citing works
Enhanced expression of granulosa cell low density lipoprotein receptor activity in response to in vitro culture conditions
REAVEN, E. P., Tsai, L., Spicher, M., Shilo, L., Philip, M., Cooper, A. D., & Azhar, S. (1994) · Journal of Cellular Physiology · doi:10.1002/jcp.1041610308 · Cited by 22 · see citing works
Lipoprotein Requirements for Secretion of Ultraviolet-Absorbing Corticosteroids by Guinea Pig Adrenocortical Cellsin Vitro: InnerVersusOuter Cortices; Zona GlomerulosaVersusZona Fasciculata*
Black, V. H. (1987) · Endocrinology · doi:10.1210/endo-120-2-640 · Cited by 22 · see citing works
Selective uptake of HDL cholesteryl esters is active in transgenic mice expressing human apolipoprotein A-I.
Khoo, J. C., Pittman, R. C., & Rubin, E. M. (1995) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)39893-x · Cited by 22 · see citing works
Selective Uptake from LDL Is Stimulated by Unsaturated Fatty Acids and Modulated by Cholesterol Content in the Plasma Membrane: Role of Plasma Membrane Composition in Regulating Non-SR-BI-Mediated Selective Lipid Transfer
Seo, T., Velez‐Carrasco, W., Qi, K., Hall, M., Worgall, T. S., Johnson, R. A., & Deckelbaum, R. J. (2002) · Biochemistry · doi:10.1021/bi011949g · Cited by 21 · see citing works
Cytochromes P450 in synthesis of steroid hormones, bile acids, vitamin D3 and cholesterol.
Pikuleva, I. A., & Waterman, M. R. (1999) · PubMed · Cited by 21 · see citing works
Follicle-Stimulating Hormone Regulates Low Density Lipoprotein Metabolism By Swine Granulosa Cells*
Veldhuis, J. D., Garmey, J. C., & JUCHTER, D. (1988) · Endocrinology · doi:10.1210/endo-123-3-1660 · Cited by 18 · see citing works
Antibody against low density lipoprotein receptor blocks uptake of low density lipoprotein (but not high density lipoprotein) by the adrenal gland of the mouse in vivo.
Kita, T., Beisiegel†, U., Goldstein, J. L., Schneider, W. J., & Brown, M. S. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69305-1 · Cited by 17 · see citing works
Characterisation of heterologous and homologous low-density lipoprotein binding to apolipoprotein B,E receptors on porcine adrenal cortex membranes: enhanced binding of trypsin-modified human low-density lipoprotein
Chapman, M. J., Loisay, F. Y. M., Forgez, P., & Cadman, H. F. (1985) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(85)90281-4 · Cited by 17 · see citing works
The Effect of Human Chorionic Gonadotropin, Dibutyryl Cyclic Adenosine 3′,5′-Monophosphate, Prostaglandins, and 25-Hydroxycholesterol on Acute Progesterone Secretion by Dissociated Rabbit Luteal Cells in Vitro: Evidence for Independent Effect of Human Chorionic Gonadotropins and Lipoproteins1
McLean, M. P., Derick, R. J., & Miller, J. B. (1987) · Biology of Reproduction · doi:10.1095/biolreprod36.4.854 · Cited by 17 · see citing works
Selective uptake of HDL cholesterol ester by human fat cells
Després, J., Fong, B. S., Jimenez, J., Julien, P., & Ángel, A. (1988) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1988.254.5.e667 · Cited by 17 · see citing works
Low Density Lipoprotein Receptor Activity in the Guinea Pig Adrenal Cortex. I. Zonal Characterization and Response to Adrenocorticotropin
Nonomura, K., Obara, T., & Strott, C. A. (1986) · Endocrinology · doi:10.1210/endo-118-2-653 · Cited by 16 · see citing works
Short-term effects of ACTH on the low-density lipoprotein receptor mRNA level in rat and hamster adrenals
Lehoux, J., & Lefebvre, A. (1991) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0060223 · Cited by 16 · see citing works
The influence of plasma lipoproteins on steroidogenesis of cultured ovine fetal and neonatal adrenal cells
Durand, P., Cathiard, A. M., Naaman, E., Brieu, V., & Saez, J. (1987) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(87)90051-3 · Cited by 15 · see citing works
HDL and Vitamin E in Plasma and the Expression of SR-BI on Lung Cells during Rat Perinatal Development
Kolleck, I., Witt, W., Wissel, H., Sinha, P. K., & Rüstow, B. (2000) · Lung · doi:10.1007/s004080000023 · Cited by 13 · see citing works
Differences in the Control of Sterol Metabolism between Mouse and Rat Leydig Cells*
Quinn, P. G., Georgiou, M., & Payne, A. H. (1985) · Endocrinology · doi:10.1210/endo-116-6-2300 · Cited by 13 · see citing works
Effect of rat plasma high density lipoprotein with or without apolipoprotein E on the cholesterol uptake and on the induction of the corticosteroid biosynthetic pathway in newborn rat adrenocortical cell cultures
Hammami, M., Meunier, S., Maume, G., Gambert, P., & Maume, B. F. (1991) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(91)90003-g · Cited by 12 · see citing works

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Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones
Hu, J., Zhang, Z., Shen, W., & Azhar, S. (2010) · Nutrition & Metabolism · doi:10.1186/1743-7075-7-47 · Cited by 538 · see citing works
Human steroid biosynthesis, metabolism and excretion are differentially reflected by serum and urine steroid metabolomes: a comprehensive review
Schiffer, L., Barnard, L., Baranowski, E. S., Gilligan, L. C., Taylor, A. E., Arlt, W., Shackleton, C. H. L., & Storbeck, K.-H. (2019) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2019.105439 · Cited by 450 · see citing works
Building the mammalian testis: origins, differentiation, and assembly of the component cell populationsPreprint
Svingen, T., & Koopman, P. A. (2013) · Genes & Development · doi:10.1101/gad.228080.113 · Cited by 387 · see citing works
Gene Expression Profiling Following In Utero Exposure to Phthalate Esters Reveals New Gene Targets in the Etiology of Testicular Dysgenesis1
Liu, K., Lehmann, K. P., Sar, M., Young, S. S., & Gaido, K. W. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.104.039404 · Cited by 219 · see citing works
Autophagy regulates testosterone synthesis by facilitating cholesterol uptake in Leydig cells
Gao, F., Li, G., Liu, C., Gao, H., Wang, H., Liu, W., Chen, M., Shang, Y., Wang, L., Shi, J., et al. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201710078 · Cited by 216 · see citing works
Scavenger receptor BI: A scavenger receptor with a mission to transport high density lipoprotein lipids
Connelly, M. A., & Williams, D. L. (2004) · Current Opinion in Lipidology · doi:10.1097/00041433-200406000-00008 · Cited by 162 · see citing works
Thematic Review Series: Lipid Transfer Proteins Scavenger receptor B type 1: expression, molecular regulation, and cholesterol transport function
Shen, W., Asthana, S., Kraemer, F. B., & Azhar, S. (2018) · Journal of Lipid Research · doi:10.1194/jlr.r083121 · Cited by 148 · see citing works
Multiple roles for lipids in the Hedgehog signalling pathway
Eaton, S. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2414 · Cited by 135 · see citing works
MicroRNAs 125a and 455 Repress Lipoprotein-Supported Steroidogenesis by Targeting Scavenger Receptor Class B Type I in Steroidogenic Cells
Hu, Z., Shen, W., Kraemer, F. B., & Azhar, S. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.01002-12 · Cited by 108 · see citing works
Scavenger Receptor class B type I (SR-BI): A versatile receptor with multiple functions and actions
Shen, W., Hu, J., Hu, Z., Kraemer, F. B., & Azhar, S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.03.011 · Cited by 97 · see citing works
Autophagy in male reproduction
Zhu, Y., Yin, Q., Wei, D., Yang, Z., Du, Y., & Ma, Y. (2019) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2019.1606361 · Cited by 94 · see citing works
Role of PCSK9 in lipid metabolic disorders and ovarian dysfunction in polycystic ovary syndrome
Wang, M., Zhao, D. Y., Xu, L., Guo, W., Nie, L., Lei, Y., Long, Y., Liu, M., Wang, Y., Zhang, X., et al. (2019) · Metabolism · doi:10.1016/j.metabol.2019.02.002 · Cited by 89 · see citing works
Dimerization of the scavenger receptor class B type I
REAVEN, E. P., Cortez, Y., Leers‐Sucheta, S., Nomoto, A. M., & Azhar, S. (2004) · Journal of Lipid Research · doi:10.1194/jlr.m300370-jlr200 · Cited by 83 · see citing works
The HDL receptor SR-BI is associated with human prostate cancer progression and plays a possible role in establishing androgen independence
Schörghofer, D., Kinslechner, K., Preitschopf, A., Schütz, B., Röhrl, C., Hengstschläger, M., Stangl, H., & Mikula, M. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0087-z · Cited by 82 · see citing works
The Expanding Role of Mitochondria, Autophagy and Lipophagy in Steroidogenesis
Bassi, G., Sidhu, S. K., & Mishra, S. (2021) · Cells · doi:10.3390/cells10081851 · Cited by 83 · see citing works
SR-BI: Linking Cholesterol and Lipoprotein Metabolism with Breast and Prostate Cancer
Gutiérrez-Pajares, J. L., Hassen, C. B., Chevalier, S., & Frank, P. G. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2016.00338 · Cited by 80 · see citing works
Regulation of Steroid Hormone Biosynthesis by the Cytoskeleton
Sewer, M. B., & Li, D. (2008) · Lipids · doi:10.1007/s11745-008-3221-2 · Cited by 74 · see citing works
Evidence for multiple complementary pathways for efficient cholesterol absorption in mice
Iqbal, J., & Hussain, M. M. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500023-jlr200 · Cited by 73 · see citing works
Corpus Luteum Development: Lessons from Genetic Models in Mice
Bachelot, A., & Binart, N. (2005) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(05)68003-9 · Cited by 65 · see citing works
Deregulation of sertoli and leydig cells function in patients with klinefelter syndrome as evidenced by testis transcriptome analysis
D’Aurora, M., Ferlin, A., Nicola, M. D., Garolla, A., Toni, L. D., Franchi, S., Palka, G., Foresta, C., Stuppia, L., & Gatta, V. (2015) · BMC Genomics · doi:10.1186/s12864-015-1356-0 · Cited by 63 · see citing works
Apolipoprotein E ( ApoE ) polymorphism is related to differences in potential fertility in women: a case of antagonistic pleiotropy?
Grazyna Jasienska, A., Ellison, P. T., Galbarczyk, A., Jasieński, M., Kalemba-Drożdż, M., Kapiszewska, M., Nenko, I., Thune, I., & Ziomkiewicz, A. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2395 · Cited by 62 · see citing works
Cyclic AMP-Stimulated Interaction between Steroidogenic Factor 1 and Diacylglycerol Kinase θ Facilitates Induction of CYP17
Li, D., Urs, A. N., Allegood, J., Leon, A., Merrill, A. H., & Sewer, M. B. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00355-07 · Cited by 58 · see citing works
Liver X receptor-α mediates cholesterol efflux in glomerular mesangial cells
Wu, J., Zhang, Y.-H., Wang, N.-P., Davis, L., Yang, G.-R., Wang, X., Zhu, Y., Breyer, M., & Guan, Y. (2004) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00123.2004 · Cited by 58 · see citing works
Low-density lipoprotein receptor affects the fertility of female mice
Guo, T., Zhang, L., Cheng, D., Liu, T., An, L., Li, W., & Zhang, C. (2014) · Reproduction Fertility and Development · doi:10.1071/rd13436 · Cited by 57 · see citing works
High density lipoprotein as a source of cholesterol for adrenal steroidogenesis: a study in individuals with low plasma HDL-C
Bochem, A. E., Holleboom, A. G., Romijn, J. A., Hoekstra, M., Dallinga-Thie, G. M., Motazacker, M. M., Hovingh, G. K., Kuivenhoven, J. A., & Stroes, E. S. G. (2013) · Journal of Lipid Research · doi:10.1194/jlr.p033449 · Cited by 56 · see citing works
Transcriptional Regulation of Adrenocortical Steroidogenic Gene Expression
Sewer, M. B., Dammer, E. B., & Jagarlapudi, S. (2007) · Drug Metabolism Reviews · doi:10.1080/03602530701498828 · Cited by 55 · see citing works
Autophagy: A Double-Edged Sword in Male Reproduction
Yan, Q., Zhang, Y., Wang, Q., & Yuan, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315273 · Cited by 54 · see citing works
Mendelian Disorders of High-Density Lipoprotein Metabolism
Oldoni, F., Sinke, R. J., & Kuivenhoven, J. A. (2014) · Circulation Research · doi:10.1161/circresaha.113.300634 · Cited by 48 · see citing works
SR‐BI and HDL Cholesteryl Ester Metabolism
Connelly, M. A., & Williams, D. L. (2004) · Endocrine Research · doi:10.1081/erc-200043979 · Cited by 49 · see citing works
SR-BI-mediated HDL cholesteryl ester delivery in the adrenal gland
Connelly, M. A. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.09.011 · Cited by 47 · see citing works
The Effects of Cholesterol Metabolism on Follicular Development and Ovarian Function
Huang, Q., Liu, Y., Yang, Z. L., Xie, Y., & Mo, Z. (2019) · Current Molecular Medicine · doi:10.2174/1566524019666190916155004 · Cited by 42 · see citing works
Regulation of Expression and Function of Scavenger Receptor Class B, Type I (SR-BI) by Na+/H+ Exchanger Regulatory Factors (NHERFs)
Hu, Z., Hu, J., Zhang, Z., Shen, W., Yun, C. C., Berlot, C. H., Kraemer, F. B., & Azhar, S. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.437368 · Cited by 40 · see citing works
Acid Ceramidase (ASAH1) Is a Global Regulator of Steroidogenic Capacity and Adrenocortical Gene Expression
Lucki, N. C., Bandyopadhyay, S., Wang, E. L., Merrill, A. H., & Sewer, M. B. (2012) · Molecular Endocrinology · doi:10.1210/me.2011-1150 · Cited by 40 · see citing works
Steroids - From Physiology to Clinical Medicine
Ostojić, S. M. (2012) · InTech eBooks · doi:10.5772/46119 · Cited by 39 · see citing works
Physiology of Testicular Steroidogenesis
Stocco, D. M., & McPhaul, M. J. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50025-7 · Cited by 38 · see citing works
The Game Plan
Wainwright, E. N., & Wilhelm, D. (2010) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(10)90006-9 · Cited by 38 · see citing works
Estrogen regulation of the scavenger receptor class B gene: Anti-atherogenic or steroidogenic, is there a priority?
Lopez, D., & McLean, M. P. (2005) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.10.005 · Cited by 37 · see citing works
Gonadal Sex Steroids: Production, Action and Interactions in Mammals
Tatiana, Z. (2012) · InTech eBooks · doi:10.5772/52994 · Cited by 33 · see citing works
Cholesterol metabolism is decreased in patients with diminished ovarian reserve
Yang, X., Zhao, Z., Fan, Q., Li, H., Zhao, L., Liu, C., & Liang, X. (2021) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2021.09.013 · Cited by 28 · see citing works
Effect of nutrition on plasma lipid profile and mRNA levels of ovarian genes involved in steroid hormone synthesis in Hu sheep during luteal phase1
Ying, S. J., Xiao, S., Wang, C. L., Zhong, B., Zhang, G., Wang, Z., He, D. Y., Ding, X. L., Xing, H. J., & Wang, F. (2013) · Journal of Animal Science · doi:10.2527/jas.2013-6450 · Cited by 27 · see citing works
Effects of different dietary DHA:EPA ratios on gonadal steroidogenesis in the marine teleost, tongue sole (Cynoglossus semilaevis)
Xu, H., Cao, L., Wei, Y., Zhang, Y., & Liang, M. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114517001891 · Cited by 27 · see citing works
Lipoprotein receptor expression during luteinization of the ovarian follicle
Jiménez, L. M., & Murphy, B. D. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00554.2006 · Cited by 25 · see citing works
Differential Roles of Cysteine Residues in the Cellular Trafficking, Dimerization, and Function of the High-Density Lipoprotein Receptor, SR-BI
Hu, J., Zhang, Z., Shen, W., Nomoto, A. M., & Azhar, S. (2011) · Biochemistry · doi:10.1021/bi201264y · Cited by 24 · see citing works
MicroRNAs and High-Density Lipoprotein Cholesterol Metabolism
Ono, K., Horie, T., Nishino, T., Baba, O., Kuwabara, Y., & Kimura, T. (2015) · International Heart Journal · doi:10.1536/ihj.15-019 · Cited by 23 · see citing works
Characterisation of scavenger receptor class B type 1 in rare minnow (Gobiocypris rarus)
Ou, M., Huang, R., Luo, Q., Xiong, L., Chen, K., & Wang, Y. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.04.031 · Cited by 23 · see citing works
A Novel Role of Salt-Inducible Kinase 1 (SIK1) in the Post-Translational Regulation of Scavenger Receptor Class B Type 1 Activity
Hu, Z., Hu, J., Shen, W., Kraemer, F. B., & Azhar, S. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b00147 · Cited by 23 · see citing works
Contribution of high-fat diet-induced PCSK9 upregulation to a mouse model of PCOS is mediated partly by SREBP2
Guo, W., Wang, Y., Ma, Y.-D., Cui, Z., Zhang, L.-X., Nie, L., Zhang, X., Wang, M., Zhang, J., Yuan, D., et al. (2021) · Reproduction · doi:10.1530/rep-21-0164 · Cited by 22 · see citing works
Biochemical and cellular characterization of lipophorin–midgut interaction in the hematophagous Panstrongylus megistus (Hemiptera: Reduviidae)
Fruttero, L. L., Rubiolo, E. R., & Canavoso, L. E. (2009) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2009.01.009 · Cited by 22 · see citing works
Impact of Aging on Steroid Hormone Biosynthesis and Secretion
Zaidi, S. K. (2012) · Open Longevity Science · doi:10.2174/1876326x01206010001 · Cited by 23 · see citing works
Regulation of Leydig Cell Cholesterol Metabolism
Azhar, S., & REAVEN, E. P. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-453-7_8 · Cited by 22 · see citing works
Consequences of over-expression of rat Scavenger Receptor, SR-BI, in an adrenal cell model
REAVEN, E. P., Nomoto, A. M., Cortez, Y., & Azhar, S. (2006) · Nutrition & Metabolism · doi:10.1186/1743-7075-3-43 · Cited by 22 · see citing works
Scavenger Receptor Class B type 1 (SR-B1) and the modifiable risk factors of stroke
Lenahan, C., Huang, L., Travis, Z. D., & Zhang, J. H. (2019) · Chinese Neurosurgical Journal · doi:10.1186/s41016-019-0178-3 · Cited by 21 · see citing works
Initiation of Steroidogenesis Precedes Expression of Cholesterologenic Enzymes in the Fetal Mouse Testes
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Authors: Azhar, S.
Affiliations: VA Palo Alto Health Care System (US)
Corresponding author: Azhar, Salman
ORCID: Azhar, Salman
Venue: Frontiers in bioscience
Publisher: IMR Press
Published: 2003
Volume: 8
Issue: 6
Pages: s998-1029
ISSN: 1093-4715 (ISSN-L)
1093-9946
DOI: 10.2741/1165
OpenAlex: W1974711948
Cited by: 109
References: 205
Citations by year: 2026: 2 · 2025: 6 · 2024: 3 · 2023: 6 · 2022: 4 · 2021: 5 · 2020: 1 · 2019: 8 · 2018: 2 · 2017: 1 · 2016: 2 · 2015: 6 · 2014: 7 · 2013: 7 · 2012: 10
FWCI: 4.47
Type: journal article
Language: en
Open access: closed
Locations: Frontiers in bioscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Heart, Lung, and Blood Institute (HL 33881)
National Institute of Diabetes and Digestive and Kidney Diseases (DK-56339, P30DK056339)
Topics: Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Steroid Chemistry and Biochemistry
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Keywords: cholesterol absorption, scavenger receptor class B type I, steroidogenesis, adrenal gland, ovary, serum lipoproteins, cholesterol esters, steroidogenic tissues
MeSH terms: Adrenal Glands, Animals, Gonads, Humans, Cholesterol, HDL, Membrane Proteins, Organ Specificity, Receptors, Immunologic, Signal Transduction, Receptors, Lipoprotein, CD36 Antigens, Receptors, Scavenger, Scavenger Receptors, Class B

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Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and “selective” pathway connection

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