The role of maternal-fetal cholesterol transport in early fetal life: Current insights

Biology of Reproduction

Volumn 88, Issue 1, 2013, Pages

  Baardman, Maria E ^a   Kerstjens Frederikse, Wilhelmina S ^a   Berger, Rolf M F ^b   Bakker, Marian K ^a   Hofstra, Robert M W ^a,d   Plösch, Torsten ^a,c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Cholesterol; Embryology; Placenta; Placental transport; Yolk sac

Indexed keywords

7 DEHYDROCHOLESTEROL; ABC TRANSPORTER A1; APOLIPOPROTEIN A1; APOLIPOPROTEIN B; APOLIPOPROTEIN E; CHOLESTEROL; CUBILIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIVER X RECEPTOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; SCAVENGER RECEPTOR B; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

BASOLATERAL MEMBRANE; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; EMBRYO DEVELOPMENT; EPIDEMIC; FETUS CIRCULATION; FETUS DEVELOPMENT; GENETIC SUSCEPTIBILITY; GENOTYPE PHENOTYPE CORRELATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MATERNAL DISEASE; MATERNAL OBESITY; METABOLIC SYNDROME X; MOTHER FETUS RELATIONSHIP; NONHUMAN; OXIDATIVE STRESS; PLACENTA; PREGNANCY DIABETES MELLITUS; PREVALENCE; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; SHORT SURVEY; SIGNAL TRANSDUCTION; TROPHOBLAST; YOLK SAC;

BIOLOGICAL TRANSPORT; CHOLESTEROL; FEMALE; FETAL DEVELOPMENT; HUMANS; MATERNAL-FETAL EXCHANGE; PREGNANCY;

EID: 84876888132     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.102442     Document Type: Short Survey

References (131)

1. Testaz S, Jarov A, Williams KP, Ling LE, Koteliansky VE, Fournier-Thibault C, Duband JL. Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the patched- smoothened-gli signaling pathway. Proc Natl Acad Sci U S A 2001; 98:12521-12526.
2. Washington Smoak I, Byrd NA, Abu-Issa R, Goddeeris MM, Anderson R, Morris J, Yamamura K, Klingensmith J, Meyers EN. Sonic hedgehog is required for cardiac outflow tract and neural crest cell development. Dev Biol 2005; 283:357-372.
3. Pare JF, Malenfant D, Courtemanche C, Jacob-Wagner M, Roy S, Allard D, Belanger L. The fetoprotein transcription factor (FTF) gene is essential to embryogenesis and cholesterol homeostasis and is regulated by a DR4 element. J Biol Chem 2004; 279:21206-21216.
4. Rausa FM, Galarneau L, Belanger L, Costa RH. The nuclear receptor fetoprotein transcription factor is coexpressed with its target gene HNF-3beta in the developing murine liver, intestine and pancreas. Mech Dev 1999; 89:185-188.
5. Jurevics HA, Kidwai FZ, Morell P. Sources of cholesterol during development of the rat fetus and fetal organs. J Lipid Res 1997; 38:723-733.
6. Baardman ME, Erwich JJ, Berger RM, Hofstra RM, Kerstjens-Frederikse WS, Lutjohann D, Plosch T. The origin of fetal sterols in secondtrimester amniotic fluid: endogenous synthesis or maternal-fetal transport? Am J Obstet Gynecol 2012; 207(202):e19-e25.
7. Christenson LK, Devoto L. Cholesterol transport and steroidogenesis by the corpus luteum. Reprod Biol Endocrinol 2003; 1:90.
8. Fujimoto VY, Kane JP, Ishida BY, Bloom MS, Browne RW. Highdensity lipoprotein metabolism and the human embryo. Hum Reprod Update 2010; 16:20-38.
9. Roy R, Belanger A. Elevated levels of endogenous pregnenolone fatty acid esters in follicular fluid high density lipoproteins supportprogesterone synthesis in porcine granulosa cells. Endocrinology 1992;131:1390-1396.
10. Ingham PW, McMahon AP. Hedgehog signaling in animal development. paradigms and principles. Genes Dev 2001; 15:3059-3087.
11. Villavicencio EH, Walterhouse DO, Iannaccone PM. The sonic hedgehog-patched-gli pathway in human development and disease. Am J Hum Genet 2000; 67:1047-1054.
12. Wagner M, Siddiqui MA. Signal transduction in early heart development (I): cardiogenic induction and heart tube formation. Exp Biol Med (Maywood) 2007; 232:852-865.
13. Cooper MK, Porter JA, Young KE, Beachy PA. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 1998; 280:1603-1607.
14. Smith DW, Lemli L, Opitz JM. A newly recognized syndrome of multiple congenital anomalies. J Pediatr 1964; 64:210-217.
15. Waterham HR, Wijburg FA, Hennekam RC, Vreken P, Poll-The BT, Dorland L, Duran M, Jira PE, Smeitink JA, Wevers RA, Wanders RJ. Smith-Lemli-Opitz syndrome is caused by mutations in the 7-dehydrocholesterol reductase gene. Am J Hum Genet 1998; 63:329-338.
16. Cooper MK, Wassif CA, Krakowiak PA, Taipale J, Gong R, Kelley RI, Porter FD, Beachy PA. A defective response to Hedgehog signaling in disorders of cholesterol biosynthesis. Nat Genet 2003; 33:508-513.
17. Linck LM, Hayflick SJ, Lin DS, Battaile KP, Ginat S, Burlingame T, Gibson KM, Honda M, Honda A, Salen G, Tint GS, Connor WE, et al. Fetal demise with Smith-Lemli-Opitz syndrome confirmed by tissue sterol analysis and the absence of measurable 7-dehydrocholesterol Delta(7)-reductase activity in chorionic villi. Prenat Diagn 2000; 20:238-240.
18. Lin DS, Pitkin RM, Connor WE. Placental transfer of cholesterol into the human fetus. Am J Obstet Gynecol 1977; 128:735-739.
19. Yoshida S, Wada Y. Transfer of maternal cholesterol to embryo and fetus in pregnant mice. J Lipid Res 2005; 46:2168-2174.
20. Tint GS, Yu H, Shang Q, Xu G, Patel SB. The use of the Dhcr7 knockout mouse to accurately determine the origin of fetal sterols. J Lipid Res 2006; 47:1535-1541.
21. Vuorio AF, Miettinen TA, Turtola H, Oksanen H, Gylling H. Cholesterol metabolism in normal and heterozygous familial hypercholesterolemic newborns. J Lab Clin Med 2002; 140:35-42.
22. Jauniaux E, Cindrova-Davies T, Johns J, Dunster C, Hempstock J, Kelly FJ, Burton GJ. Distribution and transfer pathways of antioxidant molecules inside the first trimester human gestational sac. J Clin Endocrinol Metab 2004; 89:1452-1458.
23. Jones CJ, Jauniaux E. Ultrastructure of the materno-embryonic interface in the first trimester of pregnancy. Micron 1995; 26:145-173.
24. Jauniaux E, Gulbis B. Fluid compartments of the embryonic environment. Hum Reprod Update 2000; 6:268-278.
25. Lanford RE, Bronson DL, Estlack LE, Wians FH Jr. Plasma protein and apolipoprotein synthesis by human yolk sac carcinoma cells in vitro. In Vitro Cell Dev Biol 1991; 27A:205-210.
26. Raabe M, Flynn LM, Zlot CH, Wong JS, Veniant MM, Hamilton RL, Young SG. Knockout of the abetalipoproteinemia gene in mice: reduced lipoprotein secretion in heterozygotes and embryonic lethality in homozygotes. Proc Natl Acad Sci U S A 1998; 95:8686-8691.
27. Woollett LA. Review: transport of maternal cholesterol to the fetal circulation. Placenta 2011; 32(Suppl 2):S218-21.
28. Winkel CA, MacDonald PC, Simpson ER. The role of receptor-mediated low-density lipoprotein uptake and degradation in the regulation of progesterone biosynthesis and cholesterol metabolism by human trophoblasts. Placenta Suppl 1981; 3:133-143.
29. Wadsack C, Hammer A, Levak-Frank S, Desoye G, Kozarsky KF, Hirschmugl B, Sattler W, Malle E. Selective cholesteryl ester uptake from high density lipoprotein by human first trimester and term villous trophoblast cells. Placenta 2003; 24:131-143.
30. Burke KT, Colvin PL, Myatt L, Graf GA, Schroeder F, Woollett LA. Transport of maternal cholesterol to the fetus is affected by maternal plasma cholesterol concentrations in the golden Syrian hamster. J Lipid Res 2009; 50:1146-1155.
31. Madsen EM, Lindegaard ML, Andersen CB, Damm P, Nielsen LB. Human placenta secretes apolipoprotein B-100-containing lipoproteins. J Biol Chem 2004; 279:55271-55276.
32. Stefulj J, Panzenboeck U, Becker T, Hirschmugl B, Schweinzer C, Lang I, Marsche G, Sadjak A, Lang U, Desoye G, Wadsack C. Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ Res 2009; 104:600-608.
33. Aye IL, Waddell BJ, Mark PJ, Keelan JA. Placental ABCA1 and ABCG. transporters efflux cholesterol and protect trophoblasts from oxysterol induced toxicity. Biochim Biophys Acta 2010; 1801:1013-1024.
34. Bhattacharjee J, Ietta F, Giacomello E, Bechi N, Romagnoli R, Fava A, Paulesu L. Expression and localization of ATP binding cassette transporter A1 (ABCA1) in first trimester and term human placenta. Placenta 2010; 31:423-430.
35. Scholler M, Wadsack C, Lang I, Etschmaier K, Schweinzer C, Marsche G, Dieber-Rotheneder M, Desoye G, Panzenboeck U. Phospholipid transfer protein in the placental endothelium is affected by gestational diabetes mellitus. J Clin Endocrinol Metab 2012; 97:437-445.
36. Oram JF, Wolfbauer G, Vaughan AM, Tang C, Albers JJ. Phospholipid transfer protein interacts with and stabilizes ATP-binding cassette transporter A1 and enhances cholesterol efflux from cells. J Biol Chem 2003; 278:52379-52385.
37. Russell DW. Oxysterol biosynthetic enzymes. Biochim Biophys Acta 2000; 1529:126-135.
38. Iuliano L. Pathways of cholesterol oxidation via non-enzymatic mechanisms. Chem Phys Lipids 2011; 164:457-468.
39. Plosch T, van Straten EM, Kuipers F. Cholesterol transport by the placenta: placental liver X receptor activity as a modulator of fetal cholesterol metabolism? Placenta 2007; 28:604-610.
40. Lindegaard ML, Wassif CA, Vaisman B, Amar M, Wasmuth EV, Shamburek R, Nielsen LB, Remaley AT, Porter FD. Characterization of placental cholesterol transport: ABCA1 is a potential target for in utero therapy of Smith-Lemli-Opitz syndrome. Hum Mol Genet 2008; 17:3806-3813.
41. Chiang AN, Yang ML, Hung JH, Chou P, Shyn SK, Ng HT. Alterations of serum lipid levels and their biological relevances during and after pregnancy. Life Sci 1995; 56:2367-2375.
42. Martin U, Davies C, Hayavi S, Hartland A, Dunne F. Is normal pregnancy atherogenic? Clin Sci (Lond) 1999; 96:421-425.
43. Amundsen AL, Khoury J, Iversen PO, Bergei C, Ose L, Tonstad S, Retterstol K. Marked changes in plasma lipids and lipoproteins during pregnancy in women with familial hypercholesterolemia. Atherosclerosis 2006; 189:451-457.
44. Edison RJ, Berg K, Remaley A, Kelley R, Rotimi C, Stevenson RE, Muenke M. Adverse birth outcome among mothers with low serum cholesterol. Pediatrics 2007; 120:723-733.
45. Sattar N, Greer IA, Galloway PJ, Packard CJ, Shepherd J, Kelly T, Mathers A. Lipid and lipoprotein concentrations in pregnancies complicated by intrauterine growth restriction. J Clin Endocrinol Metab 1999; 84:128-130.
46. Pecks U, Brieger M, Schiessl B, Bauerschlag DO, Piroth D, Bruno B, Fitzner C, Orlikowsky T, Maass N, Rath W. Maternal and fetal cord blood lipids in intrauterine growth restriction. J Perinat Med 2012; 40:287-296.
47. Kusters DM, Lahsinoui HH, van de Post JA, Wiegman A, Wijburg FA, Kastelein JJ, Hutten BA. Statin use during pregnancy: a systematic review and meta-analysis. Expert Rev Cardiovasc Ther 2012; 10:363-378.
48. Edison RJ, Muenke M. Mechanistic and epidemiologic considerations in the evaluation of adverse birth outcomes following gestational exposure to statins. Am J Med Genet A 2004; 131:287-298.
49. Manson JM, Freyssinges C, Ducrocq MB, Stephenson WP. Postmarketing surveillance of lovastatin and simvastatin exposure during pregnancy. Reprod Toxicol 1996; 10:439-446.
50. Taguchi N, Rubin ET, Hosokawa A, Choi J, Ying AY, Moretti ME, Koren G, Ito S. Prenatal exposure to HMG-CoA reductase inhibitors. effects on fetal and neonatal outcomes. Reprod Toxicol 2008; 26:175-177.
51. Witsch-Baumgartner M, Gruber M, Kraft HG, Rossi M, Clayton P, Giros M, Haas D, Kelley RI, Krajewska-Walasek M, Utermann G. Maternal apo E genotype is a modifier of the Smith-Lemli-Opitz syndrome. J Med Genet 2004; 41:577-584.
52. Lanthaler B, Steichen-Gersdorf E, Kollerits B, Zschocke J, Witsch-Baumgartner M. Maternal ABCA1 genotype is associated with severity of Smith-Lemli-Opitz syndrome and with viability of patients homozygous for null mutations. Eur J Hum Genet 2013; (in press). Published online ahead of print 29 August 2012; DOI: 10.1038/ejhg.2012.169.
53. Toleikyte I, Retterstol K, Leren TP, Iversen PO. Pregnancy outcomes in familial hypercholesterolemia: a registry-based study. Circulation 2011;124:1606-1614.
54. Trigatti B, Rayburn H, Vinals M, Braun A, Miettinen H, Penman M, Hertz M, Schrenzel M, Amigo L, Rigotti A, Krieger M. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A 1999; 96:9322-9327.
55. Vergeer M, Korporaal SJ, Franssen R, Meurs I, Out R, Hovingh GK, Hoekstra M, Sierts JA, Dallinga-Thie GM, Motazacker MM, Holleboom AG, Van Berkel TJ, et al. Genetic variant of the scavenger receptor BI in humans. N Engl J Med 2011; 364:136-145.
56. Hoekstra M, Van Eck M, Korporaal SJ. Genetic studies in mice and humans reveal new physiological roles for the high-density lipoprotein receptor scavenger receptor class B type I. Curr Opin Lipidol 2012; 23:127-132.
57. Smith BT, Mussell JC, Fleming PA, Barth JL, Spyropoulos DD, Cooley MA, Drake CJ, Argraves WS. Targeted disruption of cubilin reveals essential developmental roles in the structure and function of endoderm and in somite formation. BMC Dev Biol 2006; 6:30.
58. Hammad SM, Barth JL, Knaak C, Argraves WS. Megalin acts in concert with cubilin to mediate endocytosis of high density lipoproteins. J Biol Chem 2000; 275:12003-12008.
59. Willnow TE, Goldstein JL, Orth K, Brown MS, Herz J. Low density lipoprotein receptor-related protein and gp330 bind similar ligands, including plasminogen activator-inhibitor complexes and lactoferrin, an inhibitor of chylomicron remnant clearance. J Biol Chem 1992; 267:26172-26180.
60. Stefansson S, Chappell DA, Argraves KM, Strickland DK, Argraves WS. Glycoprotein 330/low density lipoprotein receptor-related protein-. mediates endocytosis of low density lipoproteins via interaction with apolipoprotein B100. J Biol Chem 1995; 270:19417-19421.
61. Assemat E, Chatelet F, Chandellier J, Commo F, Cases O, Verroust P, Kozyraki R. Overlapping expression patterns of the multiligand endocytic receptors cubilin and megalin in the CNS, sensory organs and developing epithelia of the rodent embryo. Gene Expr Patterns 2005;6:69-78.
62. Willnow TE, Hilpert J, Armstrong SA, Rohlmann A, Hammer RE, Burns DK, Herz J. Defective forebrain development in mice lacking gp330. megalin. Proc Natl Acad Sci U S A 1996; 93:8460-8464.
63. Spoelgen R, Hammes A, Anzenberger U, Zechner D, Andersen OM, Jerchow B, Willnow TE. LRP2/megalin is required for patterning of the ventral telencephalon. Development 2005; 132:405-414.
64. McCarthy RA, Barth JL, Chintalapudi MR, Knaak C, Argraves WS. Megalin functions as an endocytic sonic hedgehog receptor. J Biol Chem 2002; 277:25660-25667.
65. Ovunc B, Otto EA, Vega-Warner V, Saisawat P, Ashraf S, Ramaswami G, Fathy HM, Schoeb D, Chernin G, Lyons RH, Yilmaz E, Hildebrandt F. Exome sequencing reveals cubilin mutation as a single-gene cause of proteinuria. J Am Soc Nephrol 2011; 22:1815-1820.
66. Donnai D, Barrow M. Diaphragmatic hernia, exomphalos, absent corpus callosum, hypertelorism, myopia, and sensorineural deafness: a newly recognized autosomal recessive disorder? Am J Med Genet 1993; 47:679-682.
67. Kantarci S, Al-Gazali L, Hill RS, Donnai D, Black GC, Bieth E, Chassaing N, Lacombe D, Devriendt K, Teebi A, Loscertales M, Robson C, et al. Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat Genet 2007; 39:957-959.
68. Christiansen-Weber TA, Voland JR, Wu Y, Ngo K, Roland BL, Nguyen S, Peterson PA, Fung-Leung WP. Functional loss of ABCA1 in mice causes severe placental malformation, aberrant lipid distribution, and kidney glomerulonephritis as well as high-density lipoprotein cholesterol deficiency. Am J Pathol 2000; 157:1017-1029.
69. Bodzioch M, Orso E, Klucken J, Langmann T, Bottcher A, Diederich W, Drobnik W, Barlage S, Buchler C, Porsch-Ozcurumez M, Kaminski WE, Hahmann HW, et al. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 1999; 22:347-351.
70. Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, Yu L, Brewer C, Collins JA, Molhuizen HO, Loubser O, Ouelette BF, et al. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 1999; 22:336-345.
71. Rust S, Rosier M, Funke H, Real J, Amoura Z, Piette JC, Deleuze JF, Brewer HB, Duverger N, Denefle P, Assmann G. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet 1999; 22:352-355.
72. Homanics GE, Maeda N, Traber MG, Kayden HJ, Dehart DB, Sulik KK. Exencephaly and hydrocephaly in mice with targeted modification of the apolipoprotein B (Apob) gene. Teratology 1995; 51:1-10.
73. Homanics GE, Smith TJ, Zhang SH, Lee D, Young SG, Maeda N. Targeted modification of the apolipoprotein B gene results in hypobetalipoproteinemia and developmental abnormalities in mice. Proc Natl Acad Sci U S A 1993; 90:2389-2393.
74. Farese RV Jr, Ruland SL, Flynn LM, Stokowski RP, Young SG. Knockout of the mouse apolipoprotein B gene results in embryonic lethality in homozygotes and protection against diet-induced hypercholesterolemia in heterozygotes. Proc Natl Acad Sci U S A 1995; 92:1774-1778.
75. Huang LS, Voyiaziakis E, Markenson DF, Sokol KA, Hayek T. Breslow JL. apo B gene knockout in mice results in embryonic lethality in homozygotes and neural tube defects, male infertility, and reduced HDL cholesterol ester and apo A-I transport rates in heterozygotes.J Clin Invest 1995; 96:2152-2161.
76. Linton MF, Farese RV, Jr, Young SG. Familial hypobetalipoproteinemia. J Lipid Res 1993; 34:521-541.
77. Wetterau JR, Aggerbeck LP, Bouma ME, Eisenberg C, Munck A, Hermier M, Schmitz J, Gay G, Rader DJ, Gregg RE. Absence of microsomal triglyceride transfer protein in individuals with abetalipoproteinemia. Science 1992; 258:999-1001.
78. Jauniaux E, Jurkovic D, Henriet Y, Rodesch F, Hustin J. Development of the secondary human yolk sac: correlation of sonographic and anatomical features. Hum Reprod 1991; 6:1160-1166.
79. Heslehurst N, Rankin J, Wilkinson JR, Summerbell CD. A nationally representative study of maternal obesity in England, UK: trends in incidence and demographic inequalities in 619 323 births, 1989-2007. Int J Obes (Lond) 2010; 34:420-428.
80. Sanchez-Vera I, Bonet B, Viana M, Quintanar A, Martin MD, Blanco P, Donnay S, Albi M. Changes in plasma lipids and increased low-density lipoprotein susceptibility to oxidation in pregnancies complicated by gestational diabetes: consequences of obesity. Metabolism 2007; 56:1527-1533.
81. Merzouk H, Madani S, Prost J, Loukidi B, Meghelli-Bouchenak M, Belleville J. Changes in serum lipid and lipoprotein concentrations and compositions at birth and after 1 month of life in macrosomic infants of insulin-dependent diabetic mothers. Eur J Pediatr 1999; 158:750-756.
82. Sheffield JS, Butler-Koster EL, Casey BM, McIntire DD, Leveno KJ. Maternal diabetes mellitus and infant malformations. Obstet Gynecol 2002; 100:925-930.
83. Stothard KJ, Tennant PW, Bell R, Rankin J. Maternal overweight and obesity and the risk of congenital anomalies: a systematic review and meta-analysis. JAMA 2009; 301:636-650.
84. Baardman ME, Kerstjens-Frederikse WS, Corpeleijn E, de Walle HE, Hofstra RM, Berger RM, Bakker MK. Combined adverse effects of maternal smoking and high body mass index on heart development in offspring: evidence for interaction? Heart 2012; 98:474-479.
85. Reece EA, Homko CJ, Wu YK, Wiznitzer A. The role of free radicals and membrane lipids in diabetes-induced congenital malformations. J Soc Gynecol Investig 1998; 5:178-187.
86. Bodzek P, Olejek A, Zamlynski J. Concentration of the oxygenated derivates of cholesterol in pregnant women suffering from diabetes type I. [Article in Polish.] Wiad Lek 2002; 55(suppl 1):S50-S53.
87. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114:1752-1761.
88. Pettersen KS, Boberg KM, Stabursvik A, Prydz H. Toxicity of oxygenated cholesterol derivatives toward cultured human umbilical vein endothelial cells. Arterioscler Thromb 1991; 11:423-428.
89. Berliner JA, Heinecke JW. The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med 1996; 20:707-727.
90. Lizard G, Deckert V, Dubrez L, Moisant M, Gambert P, Lagrost L. Induction of apoptosis in endothelial cells treated with cholesterol oxides. Am J Pathol 1996; 148:1625-1638.
91. Valencia A, Kochevar IE. Ultraviolet A induces apoptosis via reactive oxygen species in a model for Smith-Lemli-Opitz syndrome. Free Radic Biol Med 2006; 40:641-650.
92. Pavan L, Hermouet A, Tsatsaris V, Therond P, Sawamura T, Evain-Brion D, Fournier T. Lipids from oxidized low-density lipoprotein modulate human trophoblast invasion: involvement of nuclear liver X receptors. Endocrinology 2004; 145:4583-4591.
93. Fournier T, Handschuh K, Tsatsaris V, Guibourdenche J, Evain-Brion D. Role of nuclear receptors and their ligands in human trophoblast invasion. J Reprod Immunol 2008; 77:161-170.
94. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 1996; 271:518-520.
95. Hatzopoulos AK, Rigotti A, Rosenberg RD, Krieger M. Temporal and spatial pattern of expression of the HDL receptor SR-BI during murine embryogenesis. J Lipid Res 1998; 39:495-508.
96. Miettinen HE, Rayburn H, Krieger M. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J Clin Invest 2001; 108:1717-1722.
97. Kozyraki R, Fyfe J, Kristiansen M, Gerdes C, Jacobsen C, Cui S, Christensen EI, Aminoff M, de la Chapelle A, Krahe R, Verroust PJ, Moestrup SK. The intrinsic factor-vitamin B12 receptor, cubilin, is a high-affinity apolipoprotein A-I receptor facilitating endocytosis of highdensity lipoprotein. Nat Med 1999; 5:656-661.
98. Sahali D, Mulliez N, Chatelet F, Dupuis R, Ronco P, Verroust P. Characterization of a 280-kD protein restricted to the coated pits of the renal brush border and the epithelial cells of the yolk sac. Teratogenic effect of the specific monoclonal antibodies. J Exp Med 1988; 167:213-218.
99. Moestrup SK, Kozyraki R, Kristiansen M, Kaysen JH, Rasmussen HH, Brault D, Pontillon F, Goda FO, Christensen EI, Hammond TG, Verroust PJ. The intrinsic factor-vitamin B12 receptor and target of teratogenic antibodies is a megalin-binding peripheral membrane protein with homology to developmental proteins. J Biol Chem 1998; 273:5235-5242.
100. Sahali D, Mulliez N, Chatelet F, Laurent-Winter C, Citadelle D, Roux C, Ronco P, Verroust P. Coexpression in humans by kidney and fetal envelopes of a 280 kDa-coated pit-restricted protein. Similarity with the murine target of teratogenic antibodies. Am J Pathol 1992; 140:33-44.
101. Aminoff M, Tahvanainen E, Grasbeck R, Weissenbach J, Broch H, de la Chapelle A. Selective intestinal malabsorption of vitamin B12 displays recessive mendelian inheritance: assignment of a locus to chromosome 10by linkage. Am J Hum Genet 1995; 57:824-831.
102. Kounnas MZ, Moir RD, Rebeck GW, Bush AI, Argraves WS, Tanzi RE, Hyman BT, Strickland DK. LDL receptor-related protein, a multifunctional ApoE receptor, binds secreted beta-amyloid precursor protein and mediates its degradation. Cell 1995; 82:331-340.
103. Gueth-Hallonet C, Santa-Maria A, Verroust P, Maro B. Gp330 is specifically expressed in outer cells during epithelial differentiation in the preimplantation mouse embryo. Development 1994; 120:3289-3299.
104. Lambot N, Lybaert P, Boom A, Delogne-Desnoeck J, Vanbellinghen AM, Graff G, Lebrun P, Meuris S. Evidence for a clathrin-mediated recycling of albumin in human term placenta. Biol Reprod 2006; 75:90-97.
105. Buc-Caron MH, Condamine H, Kerjaschki D. Rat Heymann nephritis antigen is closely related to brushin, a glycoprotein present in early mouse embryo epithelia. Ann Inst Pasteur Immunol 1987; 138:707-722.
106. Brown MS, Goldstein JL. Expression of the familial hypercholesterolemia gene in heterozygotes: mechanism for a dominant disorder in man. Science 1974; 185:61-63.
107. Bradley WA, Gianturco SH. ApoE is necessary and sufficient for the binding of large triglyceride-rich lipoproteins to the LDL receptor; apoB is unnecessary. J Lipid Res 1986; 27:40-8.
108. Wyne KL, Woollett LA. Transport of maternal LDL and HDL to the fetal membranes and placenta of the Golden Syrian hamster is mediated by receptor-dependent and receptor-independent processes. J Lipid Res 1998; 39:518-530.
109. Winkel CA, Gilmore J, MacDonald PC, Simpson ER. Uptake and degradation of lipoproteins by human trophoblastic cells in primary culture. Endocrinology 1980; 107:1892-1898.
110. 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; 92:883-893.
111. Lehrman MA, Schneider WJ, Sudhof TC, Brown MS, Goldstein JL, Russell DW. Mutation in LDL receptor: Alu-Alu recombination deletes exons encoding transmembrane and cytoplasmic domains. Science 1985;227:140-146.
112. Hobbs HH, Brown MS, Goldstein JL, Russell DW. Deletion of exon encoding cysteine-rich repeat of low density lipoprotein receptor alters its binding specificity in a subject with familial hypercholesterolemia. J Biol Chem 1986; 261:13114-13120.
113. Kim DH, Iijima H, Goto K, Sakai J, Ishii H, Kim HJ, Suzuki H, Kondo H, Saeki S, Yamamoto T. Human apolipoprotein E receptor 2. A novel lipoprotein receptor of the low density lipoprotein receptor family predominantly expressed in brain. J Biol Chem 1996; 271:8373-8380.
114. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992; 258:468-471.
115. Shen GQ, Li L, Girelli D, Seidelmann SB, Rao S, Fan C, Park JE, Xi Q, Li J, Hu Y, Olivieri O, Marchant K, et al. An LRP8 variant is associated with familial and premature coronary artery disease and myocardial infarction. Am J Hum Genet 2007; 81:780-791.
116. Malassine A, Alsat E, Besse C, Rebourcet R, Cedard L. Acetylated low density lipoprotein endocytosis by human syncytiotrophoblast in culture. Placenta 1990; 11:191-204.
117. Shi W, Swan KF, Henson MC. Expression of placental low-density lipoprotein receptor-related protein and scavenger receptors AI/AII transcripts in the baboon. Am J Obstet Gynecol 2003; 188:1211-1212.
118. Kamada N, Kodama T, Suzuki H. Macrophage scavenger receptor (SR-A I/II) deficiency reduced diet-induced atherosclerosis in C57BL/6J mice. J Atheroscler Thromb 2001; 8:1-6.
119. Xu J, Zheng SL, Komiya A, Mychaleckyj JC, Isaacs SD, Chang B, Turner AR, Ewing CM, Wiley KE, Hawkins GA, Bleecker ER, Walsh PC, et al. Common sequence variants of the macrophage scavenger receptor 1 gene are associated with prostate cancer risk. Am J Hum Genet 2003; 72:208-212.
120. Takahashi S, Kawarabayasi Y, Nakai T, Sakai J, Yamamoto T. Rabbit very low density lipoprotein receptor: a low density lipoprotein receptorlike protein with distinct ligand specificity. Proc Natl Acad Sci U S A 1992; 89:9252-9256.
121. Sakai J, Hoshino A, Takahashi S, Miura Y, Ishii H, Suzuki H, Kawarabayasi Y, Yamamoto T. Structure, chromosome location, and expression of the human very low density lipoprotein receptor gene. J Biol Chem 1994; 269:2173-2182.
122. Wittmaack FM, Gafvels ME, Bronner M, Matsuo H, McCrae KR, Tomaszewski JE, Robinson SL, Strickland DK, Strauss JF, 3rd. 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. Endocrinology 1995; 136:340-348.
123. Murata M, Kodama H, Goto K, Hirano H, Tanaka T. Decreased verylow-density lipoprotein and low-density lipoprotein receptor messenger ribonucleic acid expression in placentas from preeclamptic pregnancies. Am J Obstet Gynecol 1996; 175:1551-1556.
124. Gafvels ME, Paavola LG, Boyd CO, Nolan PM, Wittmaack F, Chawla A, Lazar MA, Bucan M, Angelin B, Strauss JF III. Cloning of a complementary deoxyribonucleic acid encoding the murine homolog of the very low density lipoprotein/apolipoprotein-E receptor: expression pattern and assignment of the gene to mouse chromosome 19". Endocrinology 1995; 136:795.
125. Li C, Huang Z, Kingsley R, Zhou X, Li F, Parke DW, 2nd, Cao W. Biochemical alterations in the retinas of very low-density lipoprotein receptor knockout mice: an animal model of retinal angiomatous proliferation. Arch Ophthalmol 2007; 125:795-803.
126. Boycott KM, Flavelle S, Bureau A, Glass HC, Fujiwara TM, Wirrell E, Davey K, Chudley AE, Scott JN, McLeod DR, Parboosingh JS. Homozygous deletion of the very low density lipoprotein receptor gene causes autosomal recessive cerebellar hypoplasia with cerebral gyral simplification. Am J Hum Genet 2005; 77:477-483.
127. Beisiegel U, Weber W, Ihrke G, Herz J, Stanley KK. The LDL-receptorrelated protein, LRP, is an apolipoprotein E-binding protein. Nature 1989; 341:162-164.
128. Coukos G, Gafvels ME, Wisel S, Ruelaz EA, Strickland DK, Strauss JF III, Coutifaris C. Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein and the 39-kd receptorassociated protein in human trophoblasts. Am J Pathol 1994; 144:383-392.
129. Overbergh L, Lorent K, Torrekens S, Van Leuven F, Van den Berghe H. Expression of mouse alpha-macroglobulins, lipoprotein receptor-related protein, LDL receptor, apolipoprotein E, and lipoprotein lipase in pregnancy. J Lipid Res 1995; 36:1774-1786.
130. Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J. LRP: role in vascular wall integrity and protection from atherosclerosis. Science 2003;300:329-332.
131. Lendon CL, Talbot CJ, Craddock NJ, Han SW, Wragg M, Morris JC, Goate AM. Genetic association studies between dementia of the Alzheimer's type and three receptors for apolipoprotein E in a Caucasian population. Neurosci Lett 1997; 222:187-190.