Localization and regulation of the human very low density lipoprotein/apolipoprotein-E receptor: trophoblast expression predicts a role for the receptor in placental lipid transport.

Wittmaack, F M; Gåfvels, M E; Bronner, M; Matsuo, H; McCrae, K R; Tomaszewski, J E; Robinson, S L; Strickland, D K; Strauss, J F

doi:10.1210/endo.136.1.7828550

Cited by 133Cholesterol and Lipid MetabolismPregnancy and preeclampsia studiesLipid metabolism and disorders

Localization and regulation of the human very low density lipoprotein/apolipoprotein-E receptor: trophoblast expression predicts a role for the receptor in placental lipid transport.

Wittmaack, F M, Gåfvels, M E, Bronner, M, Matsuo, H, McCrae, K R, Tomaszewski, J E, Robinson, S L, Strickland, D K +1 more·1995·Endocrinology

DOI 10.1210/endo.136.1.7828550

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Abstract

The very low density lipoprotein/apolipoprotein-E receptor (VLDLR) is the newest member of the low density lipoprotein receptor (LDLR) family. Very little is known about VLDLR localization and regulation. Immunohistochemical analysis of human placenta with a specific polyclonal antibody detected VLDLR in syncytiotrophoblast and intermediate trophoblast cells. VLDLR transcripts were also localized in these cells by in situ hybridization histochemistry. In addition, VLDLR messenger RNA (mRNA) was detected in villous core endothelial cells and cells appearing to be Hofbauer cells. Northern blot analysis of placenta revealed a 2.6-fold increase in VLDLR mRNA at term compared to that in the first trimester. The regulation of VLDLR expression was studied in JEG-3 and BeWo choriocarcinoma cells, two trophoblast-derived cell lines. Treatment of these cells with 8-bromo-cAMP caused a profound suppression of VLDLR message, whereas LDLR transcripts were increased. Incubation of JEG-3 cells with 25-hydroxycholesterol did not lead to sterol negative feedback on VLDLR gene expression, unlike LDLR mRNA, which declined markedly. Insulin (200 mg/L) up-regulated VLDLR message in JEG-3 cells 2-fold, as did the fibrate hypolipidemic drug, clofibric acid. We conclude that 1) VLDLR is expressed in human placental trophoblast cells in a pattern consistent with a role in placental lipid transport; 2) VLDLR expression is high at term relative to that in the first trimester; and 3) the trophoblast VLDLR is subject to down-regulation by cAMP and up-regulation by insulin and fibrate hypolipidemic drugs.

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Expression of the mRNAs encoding the VLDL-R and LDL-R increases across gestation, but is suppressed at term in pregnancies complicated by pre-eclampsia and severe growth restriction.
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Hatzopoulos, A. K., Rigotti, A., ROSENBERG, R. D., & Krieger, M. (1998) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)33289-2 · Cited by 87 · see citing works
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Acuff, R. V., Dunworth, R., Webb, L., et al. (1998) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/67.3.459 · Cited by 83 · see citing works
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Background
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Self-citation
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Self-citation
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Background
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Background
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Schmehl, K., Beninde, J., Finckh, B., Florian, S., Dudenhausen, J. W., Brigelius‐Flohé, R., & Schuelke, M. (2004) · Free Radical Research · doi:10.1080/10715760310001659611 · Cited by 51 · see citing works
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Descamps, O. S., Bruniaux, M., Guilmot, P.-F., Tonglet, R., & Heller, F. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500223-jlr200 · Cited by 42 · see citing works
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Background
Enhanced APOE2 transmission rates in families with autistic probands
Persico, A. M., D’Agruma, L., Zelante, L., Militerni, R., Bravaccio, C., Schneider, C., Melmed, R. D., Trillo, S., Montecchi, F., Elia, M., et al. (2004) · Psychiatric Genetics · doi:10.1097/01.ypg.0000128768.37838.17 · Cited by 34 · see citing works
“Patterns of VLDLR gene expression in human placental trophoblast, for example, are consistent with VLDLR involvement in placental lipid transport (Wittmaack et al., 1995).”
Background
Breast Carcinoma Epithelial Cells Express a Very Low‐Density Lipoprotein Receptor Variant Lacking the O‐Linked Glycosylation Domain Encoded by Exon 16, But with Full Binding Activity for Serine Proteinase/Serpin Complexes and Mr‐40000 Receptor‐Associated Protein
Martensen, P. M., Oka, K., Christensen, L., Rettenberger, P. M., Petersen, H. H., Christensen, A., Chan, L., Heegaard, C. W., & Andreasen, P. A. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.00583.x · Cited by 34 · see citing works
Maternal-Fetal Transfer of Lipid Metabolites
Herrera, E., & Lasunción, M. A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-35214-7.00034-2 · Cited by 32 · see citing works
Identification of novel genes regulated by LH in the primate corpus luteum: insight into their regulation during the late luteal phase
Yadav, V. K. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah089 · Cited by 30 · see citing works
“Two transcripts, 5.3 and 3.7 kb for LDLr in the primate CL and choriocarcinoma cells, have been reported by others (Benyo et al., 1993; Wittmaack et al., 1995).”
Influential
Expression of Scavenger Receptor-BI and Low-Density Lipoprotein Receptor and Differential Use of Lipoproteins to Support Early Steroidogenesis in Luteinizing Macaque Granulosa Cells
Cherian‐Shaw, M., Puttabyatappa, M., Greason, E., Rodríguez, A., VandeVoort, C. A., & Chaffin, C. L. (2008) · Endocrinology · doi:10.1210/en.2008-0619 · Cited by 29 · see citing works
Nutrient transporter expression in both the placenta and fetal liver are affected by maternal smoking
Walker, N., Filis, P., O’Shaughnessy, P. J., Bellingham, M., & Fowler, P. (2019) · Placenta · doi:10.1016/j.placenta.2019.02.010 · Cited by 28 · see citing works
“VLDLR age ↑ 1st vs term 11 [47] Small n, term placentas were laboured smoking No relevant study found”
Background
Modulation of placental protein expression of OLR1: implication in pregnancy-related disorders or pathologies
Ethier-Chiasson, M., Forest, J., Giguère, Y., Masse, A., Marseille‐Tremblay, C., Levy, E. H., & Lafond, J. (2008) · Reproduction · doi:10.1530/rep-08-0082 · Cited by 27 · see citing works
“1992), the very low density lipoprotein receptor (VLDL receptor) (Wittmaack et al. 1995), the scavenger receptors (Bonet et al.”
Background
Fetal High-Density Lipoproteins: Current Knowledge on Particle Metabolism, Composition and Function in Health and Disease
Stadler, J. T., Wadsack, C., & Marsche, G. (2021) · Biomedicines · doi:10.3390/biomedicines9040349 · Cited by 26 · see citing works
Role of Lectin-Like Oxidized Low Density Lipoprotein-1 in Fetoplacental Vascular Dysfunction in Preeclampsia
Zuñiga, F. A., Ormazábal, V., Gutiérrez, N., Aguilera, V., Radojkovic, C., Veas, C., Escudero, C., Lamperti, L., & Aguayo, C. R. (2014) · BioMed Research International · doi:10.1155/2014/353616 · Cited by 26 · see citing works
“Human placental cells express many lipoprotein receptors such as the LDL receptor (LDLR; [136]), the LDL receptor-related protein (LRP; [137]), the VLDL receptor (VLDL receptor; [138]), the scavenger receptors [139–141], and the LOX-1 [142].”
Background
Effects of gemfibrozil on insulin resistance to fat metabolism in subjects with type 2 diabetes and hypertriglyceridaemia
Whitelaw, D. C., Smith, J. M., & Nattrass, M. (2002) · Diabetes Obesity and Metabolism · doi:10.1046/j.1463-1326.2002.00199.x · Cited by 26 · see citing works
Interplay between β-carotene and lipoprotein metabolism at the maternal-fetal barrier
Quadro, L., Giordano, E., Costabile, B. K., Nargis, T., Iqbal, J., Kim, Y., Wassef, L., & Hussain, M. M. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2019.158591 · Cited by 29 · see citing works
“analysis of human placenta also localized the very low-density lipoprotein/apolipoprotein E receptor (VLDLR) in the syncytiotrophoblast and intermediate trophoblast cells [78].”
BackgroundInfluential
Transduction of human trophoblastic cells by replication-deficient recombinant viral vectors. Promoting cellular differentiation affects virus entry.
Parry, S. I., Holder, J. E., Halterman, M. W., Weitzman, M. D., Davis, A. R., Federoff, H. J., & Strauss, J. F. (1998) · Europe PMC (PubMed Central) · Cited by 25 · see citing works
Self-citation
Oxidatively modified LDL particles in the human placenta in early and late onset intrauterine growth restriction
Pecks, U., Rath, W. H., Caspers, R., Sosnowsky, K., Ziems, B., Thiesen, H.-J., Maass, N., & Huppertz, B. (2013) · Placenta · doi:10.1016/j.placenta.2013.10.006 · Cited by 23 · see citing works
Decreased very-low-density lipoprotein and low-density lipoprotein receptor messenger ribonucleic acid expression in placentas from preeclamptic pregnancies
Murata, M., Kodama, H., Goto, K., Hirano, H., & Tanaka, T. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70105-9 · Cited by 23 · see citing works
Fetal Nutrition: How We Become What We Are
McClellan, R., & Novak, D. (2001) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200109000-00002 · Cited by 23 · see citing works
Estrogen-enhanced apical and basolateral secretion of apolipoprotein B-100 by polarized trophoblast-derived BeWo cells
Kamper, M., Mittermayer, F., Cabuk, R., Gelles, K., Ellinger, I., & Hermann, M. (2017) · Biochimie · doi:10.1016/j.biochi.2017.05.006 · Cited by 20 · see citing works
Transcription factors CCAAT/enhancer-binding protein β and nuclear factor-Y bind to discrete regulatory elements in the very low density lipoprotein receptor promoter
Kreuter, R., Soutar, A. K., & Wade, D. P. (1999) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)32441-x · Cited by 19 · see citing works
Pathophysiology of placenta and fetus in diabetes mellitus
Kapustin, R. V., Onopriychuk, A. R., Arzhanova, O. N., Polyakova, V. O., & Николаевна, А. Е. (2018) · Journal of obstetrics and women s diseases · doi:10.17816/jowd67679-92 · Cited by 18 · see citing works
Placental Transfer
Atkinson, D. E., BOYD, R., & Sibley, C. P. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50057-9 · Cited by 36 · see citing works
Placental Endocrine Function and Hormone Action
Albrecht, E. D., & Pepe, G. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00040-5 · Cited by 20 · see citing works
Association of early maternal hypertriglyceridemia with pregnancy-induced hypertension
Chandi, A., Sirohiwal, D., & Malik, R. (2015) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-015-3706-1 · Cited by 17 · see citing works
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)
Hu, S., Liu, H., Pan, Z., et al. (2014) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2014.06.024 · Cited by 16 · see citing works
Osteopontin and LDLR Are Upregulated in Hearts of Sudden Cardiac Death Victims With Heart Failure With Preserved Ejection Fraction and Diabetes Mellitus
Patel, M. J., Rodriguez, D., Yousefi, K., et al. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.610282 · Cited by 13 · see citing works
“Conversely, the LDLR is downregulated by sterol negative feedback, but the VLDLR is not affected by sterols (32).”
Background
Increased Fetal Cardiovascular Disease Risk: Potential Synergy Between Gestational Diabetes Mellitus and Maternal Hypercholesterolemia
Espinoza, C., Fuenzalida, B., & Leiva, A. (2021) · Current Vascular Pharmacology · doi:10.2174/1570161119666210423085407 · Cited by 13 · see citing works
The impact of ionizing radiation on placental trophoblasts
Kanter, D. J., O'Brien, M. B., Shi, X., et al. (2014) · Placenta · doi:10.1016/j.placenta.2013.12.011 · Cited by 13 · see citing works
“The VLDL receptor (VLDLR) probably plays a role in placental cholesterol metabolism, which may be disrupted as a consequence of cell injury [43].”
Background
Effects of gemfibrozil administration on very low density lipoprotein receptor mRNA levels in rabbits
Matsuoka, N., Jingami, H., Masuzaki, H., et al. (1996) · Atherosclerosis · doi:10.1016/0021-9150(96)05910-2 · Cited by 13 · see citing works
Regulation of the Ligand Binding Activity of the Human Very Low Density Lipoprotein Receptor by Protein Kinase C-dependent Phosphorylation
Sakthivel, R., Zhang, J.-C., Strickland, D. K., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m003953200 · Cited by 12 · see citing works
Self-citation
Maternal-Fetal Transfer of Lipid Metabolites
Herrera, E., & Lasunción, M. A. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-3479-7.10041-2 · Cited by 12 · see citing works
Dietary Phospholipid-Bound Conjugated Linoleic Acid and Docosahexaenoic Acid Incorporation Into Fetal Liver and Brain Modulates Fatty Acid and N-Acylethanolamine Profiles
Murru, E., Carta, G., Manca, C., Sæbø, A., Santoni, M., Mostallino, R., Pistis, M., & Banni, S. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.834066 · Cited by 10 · see citing works
Analysis of Expression of Genes Involved in Apolipoprotein E-Based Lipoprotein Metabolism in Pregnant Mice Deficient in the Receptor-Associated Protein, the Low Density Lipoprotein Receptor, or Apolipoprotein E1
Umans, L., Overbergh, L., Serneels, L., et al. (1999) · Biology of Reproduction · doi:10.1095/biolreprod61.5.1216 · Cited by 10 · see citing works
“Expression of VLDLR is essentially absent in liver, while high levels are observed in various tissues including the placenta, suggesting a role in placental lipid metabolism [6, 40].”
Background

Aberrations of Early Trophoblast Differentiation Predispose to Pregnancy Failure: Lessons from the Anti-phospholipid Syndrome
Bose, P., Kadyrov, M., Goldin, R. D., Hahn, S., Backos, M., Regan, L., & Huppertz, B. (2005) · Placenta · doi:10.1016/j.placenta.2005.09.007 · Cited by 69 · see citing works
Biochemical and Immunological Aspects of the Human Trophoblast Cell Surface
Webb, P. D., Hole, N., McLaughlin, P., et al. (1987) · Springer eBooks · doi:10.1007/978-1-4757-1936-9_1 · Cited by 6 · see citing works
IFPA Award in Placentology Lecture: Biology of the placental syncytiotrophoblast – Myths and facts
Huppertz, B. (2009) · Placenta · doi:10.1016/j.placenta.2009.12.001 · Cited by 77 · see citing works
Hydatidiform Moles
Baergen, R. N. (2010) · Springer eBooks · doi:10.1007/978-1-4419-7494-5_23 · Cited by 1 · see citing works
Molahidatidosa from Pathophysiology to Clinical: Literature Review
Hidayat, R., & Sastradinata, I. (2021) · Biomedical Journal of Indonesia · doi:10.32539/bji.v7i1.260

Authors: Wittmaack, F. M., Gåfvels, M. E., Bronner, M., Matsuo, H., McCrae, K. R., Tomaszewski, J. E., Robinson, S. L., Strickland, D. K., & Strauss, J. F.
Affiliations: University of Pennsylvania (US)
ORCID: Bronner, M
Matsuo, H
McCrae, K R
Tomaszewski, J E
Strickland, D K
Strauss, J F
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 1995-01
Volume: 136
Issue: 1
Pages: 340-348
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/endo.136.1.7828550
OpenAlex: W2041398886
Cited by: 133
References: 0
Citations by year: 2026: 2 · 2025: 2 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 5 · 2018: 2 · 2017: 3 · 2016: 4 · 2015: 2 · 2014: 7 · 2013: 1 · 2012: 3
FWCI: 10.76
Type: journal article
Language: en
Open access: closed
Locations: Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01gm042581-09, 5r01hd029946-04)
National Institute of General Medical Sciences (GM-42581)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-29946)
Topics: Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
Keywords: VLDLR, low-density lipoprotein receptor family, placenta, trophoblast, syncytiotrophoblast, gene expression regulation, cyclic AMP, insulin, clofibric acid, fibrates, 25-hydroxycholesterol, JEG-3 cells, BeWo cells, Hofbauer cells
MeSH terms: Apolipoproteins, Biological Transport, Endothelium, Vascular, Forecasting, Humans, Placenta, Receptors, LDL, RNA, Messenger, Tissue Distribution, Trophoblasts, Tumor Cells, Cultured, Receptors, Lipoprotein, Low Density Lipoprotein Receptor-Related Protein-1, Lipid Metabolism

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Localization and regulation of the human very low density lipoprotein/apolipoprotein-E receptor: trophoblast expression predicts a role for the receptor in placental lipid transport.

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