This Article Full Text Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Reaven, E. Articles by Azhar, S. Search for Related Content PubMed PubMed Citation Articles by Reaven, E. Articles by Azhar, S. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Hazardous Substances DB CHOLESTEROL CHORIONIC GONADOTROPIN

Expression and Microvillar Localization of Scavenger Receptor, Class B, Type I (a High Density Lipoprotein Receptor) in Luteinized and Hormone-Desensitized Rat Ovarian Models¹

Geriatric Research, Education and Clinical Center, Veterans Administration Palo Alto Health Care System (E.R., A.N., S.L.-S., S.A.), Palo Alto, California 94304; and the Department of Pharmacological Sciences, University Medical Center, State University of New York (R.T., D.L.W.), Stony Brook, New York 11794

Address all correspondence and requests for reprints to: Eve Reaven, Ph.D., Veterans Administration Palo Alto Health Care System (GRECC, 182B), 3801 Miranda Avenue, Palo Alto, California 94304. E-mail: eve{at}icon.palo-alto.med.va.gov

Steroidogenic cells in rats and mice obtain most of their cholesterol for steroid production and cholesteryl ester (CE) storage via the selective uptake pathway in which high density lipoprotein CE (HDL-CE) is taken into the cell without the uptake and degradation of the HDL particle. A number of recent studies show that the scavenger receptor, class B, type I (SR-BI) can mediate HDL-CE selective uptake in cultured cells and suggest that this receptor may be responsible for HDL-CE selective uptake in steroidogenic cells in vivo. In the current study we examine the relationship between SR-BI expression and HDL-CE selective uptake in the gonadotropin-primed, luteinized rat ovary and in the ovary that is desensitized by multiple gonadotropin treatments. Results from this study demonstrate a tight association between expression of SR-BI and measurements of HDL-CE selective uptake regardless of the steroidogenic state of the ovary. Thus, in the luteinized ovary (which is actively producing progestins), HDL-CE selective uptake is high, as is the expression of SR-BI. In the desensitized ovary (where CE content is reduced by 90% and progestin production is virtually absent), HDL-CE selective uptake and SR-BI are induced 2- to 3-fold compared with those in the luteinized ovary. These data argue that SR-BI can be regulated by the cholesterol status of the luteal cell independently of gonadotropic stimulation. Immunostaining at the light microscopic level showed strong expression of SR-BI specifically on the surface of luteal cells in the luteinized and desensitized ovary. Immunolocalization at the electron microscopic level showed that SR-BI was associated with microvilli and microvillar channels of the luteal cell surface. This result supports the hypothesis that microvilli and microvillar channels represent a cell surface compartment that is specialized for the selective uptake of lipoprotein cholesterol into steroidogenic cells.

This article has been cited by other articles:

				S. Parathath, Y. F. Darlington, M. de la Llera Moya, D. Drazul-Schrader, D. L. Williams, M. C. Phillips, G. H. Rothblat, and M. A. Connelly Effects of amino acid substitutions at glycine 420 on SR-BI cholesterol transport function J. Lipid Res., June 1, 2007; 48(6): 1386 - 1395. [Abstract] [Full Text] [PDF]

				L. Cocquerel, C. Voisset, and J. Dubuisson Hepatitis C virus entry: potential receptors and their biological functions. J. Gen. Virol., May 1, 2006; 87(Pt 5): 1075 - 1084. [Abstract] [Full Text] [PDF]

				A. Yesilaltay, M. G. Morales, L. Amigo, S. Zanlungo, A. Rigotti, S. L. Karackattu, M. H. Donahee, K. F. Kozarsky, and M. Krieger Effects of Hepatic Expression of the High-Density Lipoprotein Receptor SR-BI on Lipoprotein Metabolism and Female Fertility Endocrinology, April 1, 2006; 147(4): 1577 - 1588. [Abstract] [Full Text] [PDF]

				B Lohrke, T Viergutz, and B Kruger Polar phospholipids from bovine endogenously oxidized low density lipoprotein interfere with follicular thecal function J. Mol. Endocrinol., December 1, 2005; 35(3): 531 - 545. [Abstract] [Full Text] [PDF]

				A.-L. Tondu, C. Robichon, L. Yvan-Charvet, N. Donne, X. Le Liepvre, E. Hajduch, P. Ferre, I. Dugail, and G. Dagher Insulin and Angiotensin II Induce the Translocation of Scavenger Receptor Class B, Type I from Intracellular Sites to the Plasma Membrane of Adipocytes J. Biol. Chem., September 30, 2005; 280(39): 33536 - 33540. [Abstract] [Full Text] [PDF]

				L. Wang and K. M. J. Menon Regulation of Luteinizing Hormone/Chorionic Gonadotropin Receptor Messenger Ribonucleic Acid Expression in the Rat Ovary: Relationship to Cholesterol Metabolism Endocrinology, January 1, 2005; 146(1): 423 - 431. [Abstract] [Full Text] [PDF]

				N. Argov, U. Moallem, and D. Sklan Lipid Transport in the Developing Bovine Follicle: Messenger RNA Expression Increases for Selective Uptake Receptors and Decreases for Endocytosis Receptors Biol Reprod, August 1, 2004; 71(2): 479 - 485. [Abstract] [Full Text] [PDF]

				E. Reaven, Y. Cortez, S. Leers-Sucheta, A. Nomoto, and S. Azhar Dimerization of the scavenger receptor class B type I: formation, function, and localization in diverse cells and tissues J. Lipid Res., March 1, 2004; 45(3): 513 - 528. [Abstract] [Full Text] [PDF]

				F. B. Kraemer, W.-J. Shen, K. Harada, S. Patel, J.-i. Osuga, S. Ishibashi, and S. Azhar Hormone-Sensitive Lipase Is Required for High-Density Lipoprotein Cholesteryl Ester-Supported Adrenal Steroidogenesis Mol. Endocrinol., March 1, 2004; 18(3): 549 - 557. [Abstract] [Full Text] [PDF]

				Y. Peng, W. Akmentin, M. A. Connelly, S. Lund-Katz, M. C. Phillips, and D. L. Williams Scavenger Receptor BI (SR-BI) Clustered on Microvillar Extensions Suggests that This Plasma Membrane Domain Is a Way Station for Cholesterol Trafficking between Cells and High-Density Lipoprotein Mol. Biol. Cell, January 1, 2004; 15(1): 384 - 396. [Abstract] [Full Text] [PDF]

				A. Rigotti, H. E. Miettinen, and M. Krieger The Role of the High-Density Lipoprotein Receptor SR-BI in the Lipid Metabolism of Endocrine and Other Tissues Endocr. Rev., June 1, 2003; 24(3): 357 - 387. [Abstract] [Full Text] [PDF]

				Q. Wu, S. Sucheta, S. Azhar, and K. M. J. Menon 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, June 1, 2003; 144(6): 2437 - 2445. [Abstract] [Full Text] [PDF]

				R. M. Rao, Y. Jo, S. Leers-Sucheta, H. S. Bose, W. L. Miller, S. Azhar, and D. M. Stocco Differential Regulation of Steroid Hormone Biosynthesis in R2C and MA-10 Leydig Tumor Cells: Role of SR-B1-Mediated Selective Cholesteryl Ester Transport Biol Reprod, January 1, 2003; 68(1): 114 - 121. [Abstract] [Full Text] [PDF]

				K. Nagaosa, A. Shiratsuchi, and Y. Nakanishi Determination of Cell Type Specificity and Estrous Cycle Dependency of Monocyte Chemoattractant Protein-1 Expression in Corpora Lutea of Normally Cycling Rats in Relation to Apoptosis and Monocyte/Macrophage Accumulation Biol Reprod, November 1, 2002; 67(5): 1502 - 1508. [Abstract] [Full Text] [PDF]

				B. Liu and M. Krieger Highly Purified Scavenger Receptor Class B, Type I Reconstituted into Phosphatidylcholine/Cholesterol Liposomes Mediates High Affinity High Density Lipoprotein Binding and Selective Lipid Uptake J. Biol. Chem., September 6, 2002; 277(37): 34125 - 34135. [Abstract] [Full Text] [PDF]

				R. E. Temel, R. L. Walzem, C. L. Banka, and D. L. Williams Apolipoprotein A-I Is Necessary for the in Vivo Formation of High Density Lipoprotein Competent for Scavenger Receptor BI-mediated Cholesteryl Ester-selective Uptake J. Biol. Chem., July 12, 2002; 277(29): 26565 - 26572. [Abstract] [Full Text] [PDF]

				S. Azhar, A. Nomoto, and E. Reaven Hormonal regulation of adrenal microvillar channel formation J. Lipid Res., June 1, 2002; 43(6): 861 - 871. [Abstract] [Full Text] [PDF]

				D. L. Williams, J. S. Wong, and R. L. Hamilton SR-BI is required for microvillar channel formation and the localization of HDL particles to the surface of adrenocortical cells in vivo J. Lipid Res., April 1, 2002; 43(4): 544 - 549. [Abstract] [Full Text] [PDF]

				D. Lopez, W. Shea-Eaton, M. D. Sanchez, and M. P. McLean DAX-1 Represses the High-Density Lipoprotein Receptor Through Interaction with Positive Regulators Sterol Regulatory Element-Binding Protein-1a and Steroidogenic Factor-1 Endocrinology, December 1, 2001; 142(12): 5097 - 5106. [Abstract] [Full Text] [PDF]

				N. Cherradi, M. Bideau, S. Arnaudeau, N. Demaurex, R. W. James, S. Azhar, and A. M. Capponi 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 Endocrinology, October 1, 2001; 142(10): 4540 - 4549. [Abstract] [Full Text] [PDF]

				G. A. Graf, K. L. Roswell, and E. J. Smart 17{beta}-Estradiol promotes the up-regulation of SR-BII in HepG2 cells and in rat livers J. Lipid Res., September 1, 2001; 42(9): 1444 - 1449. [Abstract] [Full Text] [PDF]

				S. F. Cai, R. J. Kirby, P. N. Howles, and D. Y. Hui Differentiation-dependent expression and localization of the class B type I scavenger receptor in intestine J. Lipid Res., June 1, 2001; 42(6): 902 - 909. [Abstract] [Full Text]

				E. Reaven, S. Leers-Sucheta, A. Nomoto, and S. Azhar Expression of scavenger receptor class B type 1 (SR-BI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system PNAS, February 13, 2001; 98(4): 1613 - 1618. [Abstract] [Full Text] [PDF]

				W. Witt, I. Kolleck, H. Fechner, P. Sinha, and B. Rüstow Regulation by vitamin E of the scavenger receptor BI in rat liver and HepG2 cells J. Lipid Res., December 1, 2000; 41(12): 2009 - 2016. [Abstract] [Full Text]

				E. Reaven, L. Zhan, A. Nomoto, S. Leers-Sucheta, and S. Azhar Expression and microvillar localization of scavenger receptor class B, type I (SR-BI) and selective cholesteryl ester uptake in Leydig cells from rat testis J. Lipid Res., March 1, 2000; 41(3): 343 - 356. [Abstract] [Full Text]

				D. Lopez and M. P. McLean Sterol Regulatory Element-Binding Protein-1a Binds to cis Elements in the Promoter of the Rat High Density Lipoprotein Receptor SR-BI Gene Endocrinology, December 1, 1999; 140(12): 5669 - 5681. [Abstract] [Full Text]

				X. Buton, Z. Mamdouh, R. Ghosh, H. Du, G. Kuriakose, N. Beatini, G. A. Grabowski, F. R. Maxfield, and I. Tabas Unique Cellular Events Occurring during the Initial Interaction of Macrophages with Matrix-retained or Methylated Aggregated Low Density Lipoprotein (LDL). PROLONGED CELL-SURFACE CONTACT DURING WHICH LDL-CHOLESTERYL ESTER HYDROLYSIS EXCEEDS LDL PROTEIN DEGRADATION J. Biol. Chem., November 5, 1999; 274(45): 32112 - 32121. [Abstract] [Full Text] [PDF]

				G. Cao, L. Zhao, H. Stangl, T. Hasegawa, J. A. Richardson, K. L. Parker, and H. H. Hobbs Developmental and Hormonal Regulation of Murine Scavenger Receptor, Class B, Type 1 Mol. Endocrinol., September 1, 1999; 13(9): 1460 - 1473. [Abstract] [Full Text]

				B. Trigatti, H. Rayburn, M. Vinals, A. Braun, H. Miettinen, M. Penman, M. Hertz, M. Schrenzel, L. Amigo, A. Rigotti, et al. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology PNAS, August 3, 1999; 96(16): 9322 - 9327. [Abstract] [Full Text] [PDF]

				G. A. Graf, P. M. Connell, D. R. van der Westhuyzen, and E. J. Smart The Class B, Type I Scavenger Receptor Promotes the Selective Uptake of High Density Lipoprotein Cholesterol Ethers into Caveolae J. Biol. Chem., April 23, 1999; 274(17): 12043 - 12048. [Abstract] [Full Text] [PDF]

				D. L. Williams, M. de la Llera-Moya, S. T. Thuahnai, S. Lund-Katz, M. A. Connelly, S. Azhar, G. M. Anantharamaiah, and M. C. Phillips Binding and Cross-linking Studies Show That Scavenger Receptor BI Interacts with Multiple Sites in Apolipoprotein A-I and Identify the Class A Amphipathic alpha -Helix as a Recognition Motif J. Biol. Chem., June 16, 2000; 275(25): 18897 - 18904. [Abstract] [Full Text] [PDF]