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

Journal of Lipid Research

Volumn 39, Issue 3, 1998, Pages 518-530

  Wyne, Kathleen L ^a   Woollett, Laura A ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Cholesterol; gp330; LDL receptor; SR BI

Indexed keywords

APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IODINE 125; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; CHOLESTEROL TRANSPORT; FEMALE; FETOPLACENTAL UNIT; FETUS; GESTATIONAL AGE; IMMUNOCYTOCHEMISTRY; ISOTOPE LABELING; MALE; NONHUMAN; PLACENTA; PRIORITY JOURNAL; SYRIAN HAMSTER; YOLK SAC;

ANIMALS; ANTIGENS, CD36; APOLIPOPROTEIN A-I; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CHOLESTEROL; CRICETINAE; EXTRAEMBRYONIC MEMBRANES; FEMALE; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MALE; MEMBRANE PROTEINS; MESOCRICETUS; METABOLIC CLEARANCE RATE; PLACENTA; PREGNANCY; RECEPTORS, IMMUNOLOGIC; RECEPTORS, LDL; RECEPTORS, LIPOPROTEIN; RECEPTORS, SCAVENGER; RNA-BINDING PROTEINS; SCAVENGER RECEPTORS, CLASS B; YOLK SAC;

EID: 0031946343     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Dietschy, J. M., S. D. Turley, and D. K. Spady. 1993. Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J. Lipid Res. 34: 1637-1659.
2. Carr, B. R., and E. R. Simpson. 1982. Cholesterol synthesis in human fetal tissues. J. Clin. Endocrinol. Metab. 55: 447-452.
3. Dietschy, J. M., T. Kita, K. E. Suckling, J. L. Goldstein, and M. S. Brown. 1983. Cholesterol synthesis in vivo and in vitro in the WHHL rabbit, an animal with defective low density lipoprotein receptors. J. Lipid Res. 24: 469-480.
4. Haave, N. C., and S. M. Innis. 1991. Perinatal development of hepatic cholesterol synthesis in the rat. Biochim. Biophys. Acta. 1085: 35-44.
5. Smith, J. L., S. R. Lear, and S. K. Erickson. 1995. Developmental expression of elements of hepatic cholesterol metabolism in the rat. J. Lipid Res. 36: 641-652.
6. Belknap, W. M., and J. M. Dietschy. 1988. Sterol synthesis and low density lipoprotein clearance in vivo in the pregnant rat, placenta, and fetus. Sources for tissue cholesterol during fetal development. J. Clin. Invest. 82: 2077-2085.
7. Woollett, L. A. 1996. Origin of cholesterol in the fetal Golden Syrian hamster: contribution of de novo sterol synthesis and maternal-derived lipoprotein cholesterol. J. Lipid Res. 37: 1246-1257.
8. Jurevics, H. A., F. Z. Kidwai, and P. Morell. 1997. Sources of cholesterol during development of the rat fetus and fetal organs. J. Lipid Res. 38: 723-733.
9. Winkel, C. A., J. M. Snyder, P. C. MacDonald, and E. R. Simpson. 1980. Regulation of cholesterol and progesterone synthesis in human placental cells in culture by serum lipoproteins. Endocrinology. 106: 1054-1060.
10. Winkel, C. A., P. C. MacDonald, and E. R. Simpson. 1981. The role of receptor-mediated low-density lipoprotein up-take and degradation in the regulation of progesterone biosynthesis and cholesterol metabolism by human trophoblasts. Placenta. 3 (Suppl): 133-143.
11. Farese, R. V., Jr., S. Cases, S. L. Ruland, H. J. Kayden, J. S. Wong, S. G. Young, and R. L. Hamilton. 1996. A novel function for apolipoprotein B: lipoprotein synthesis in the yolk sac is critical for maternal-fetal lipid transport in mice. J. Lipid Res. 37: 347-360.
12. Lin, D. S., R. M. Pitkin, and W. E. Connor. 1977. Placental transfer of cholesterol into the human fetus. Am. J. Obstet. Gynecol. 128: 735-739.
13. 14C into rabbit and guinea pig fetus. J. Lipid Res. 8: 558-564.
14. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
15. Alsat, E., F. Mondon, R. Rebourcet, M. Berthelier, D. ErIich, L. Cedard, and S. Goldstein. 1985. Identification of specific binding sites for acetylated low density lipoprotein in microvillous membranes from human placenta. Mol. Cell. Endocrinol. 41: 229-235.
16. Goldstein, J. L., Y. K. Ho, S. K. Basu, and M. S. Brown. 1979. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, : producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA. 76: 333-337.
17. Gåfvels, M. E., L. G. Paavola, C. O. Boyd, P. M. Nolan, F. Wittmaack, A. Chawla, M. A. Lazar, M. Bucan, B. Angelin, and J. F. Strauss, III. 1994. 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. 135: 387-394.
18. Wittmaack, F. M., M. E. Gåfvels, M. Bronner, H. Matsuo, K. R. McCrae, J. E. Tomaszewski, S. L. Robinson, D. K. Strickland, and J. J. Strauss, III. 1995. 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. 136: 340-348.
19. Willnow, T. E., J. L. Goldstein, K. Orth, M. S. Brown, and J. Herz. 1992. 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. 267: 26172-26180.
20. Takahashi, S., Y. Kawarabayasi, T. Nakai, J. Sakai, and T. Yamamoto. 1992. Rabbit very low density lipoprotein receptor: a low density lipoprotein receptor-like protein with distinct ligand specificity. Proc. Natl. Acad. Sci. USA. 89: 9252-9257.
21. Zheng, G., D. R. Bachinsky, I. Stamenkovic, D. K. Strickland, D. Brown, G. Andres, and R. T. McCluskey. 1994. Organ distribution in rats of two members of the low-density lipoprotein receptor gene family, gp330 and LRP/α2MR, and the receptor-associated protein (RAP). J. Histochem. Cytochem. 42: 531-542.
22. Lundstrom, M., R. A. Orlando, M. S. Saedi, L. Woodward, H. Kurihara, and M. G. Farquhar. 1993. Immunocytochemical and biochemical characterization of the Heymann nephritis antigenic complex in rat L2 yolk sac cells. Am. J. Pathol. 143: 1423-1435.
23. Stefansson, S., D. A. Chappell, K. M. Argraves, D. K. Strickland, and W. S. Argraves. 1995. Glycoprotein 330/low density lipoprotein receptor-related protein-2 mediates enclocytosis of low density lipoproteins via interaction with apolipoprotein B-100. J. Biol. C.hem. 270: 19417-19421.
24. Frykman, P. K., M. S. Brown, T. Yamamoto, J. L. Goldstein, and J. Herz. 1995. Normal plasma lipoproteins and fertility in gene-targeted mice homozygous for a disruption in the gene encoding very low density lipoprotein receptor. Proc. Natl. Acad. Sci. USA. 92: 8453-8457.
25. Ishibashi, S., M. S. Brown, J. L. Goldstein, R. D. Gerard, R. E. Hammer, and J. Herz. 1993. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92: 883-893.
26. Cummings, S. W., W. Hatley, E. R. Simpson, and M. Ohashi. 1982. The binding of high and low density lipoproteins to human placental membrane fractions. J. Clin. Endocrinol. Metab. 54: 903-908.
27. 3 binding and biological action: high affinity binding is not necessary for stimulation of placental lactogen release from trophoblast cells. Endocrinology. 125: 2915-2921.
28. Rabe, T., H. Kalbfleisch, A. Haun, and B. Runnebaum. 1983. Influence of human lipoproteins on the progesterone synthesis of human term placenta in organ culture. Biol. Res. Preg. 4: 75-83.
29. Glass, C., R. C. Pittman, M. Civen, and D. Steinberg. 1985. Uptake of high-density lipoprotein-associated apoprotein A-I and cholesterol esters by 16 tissues of the rat in vivo and by adrenal cells and hepatocytes in vitro. J. Biol. Chem. 260: 744-750.
30. Glass, C., R. C. Pittman, D. B. Weinstein, and D. Steinberg. 1983. Dissociation of tissue uptake of cholesterol ester from that of apoprotein A-I of rat plasma high density lipoprotein: selective delivery of cholesterol ester to liver, adrenal, and gonad. Proc. Natl. Acad. Sci. USA. 80: 5435-5439.
31. Acton, S., A. Rigotti, K. T. Landschultz, S. Xu, H. H. Hobbs, and M. Krieger. 1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 271: 518-520.
32. Landschulz, K. T., R. K. Pathak, A. Rigotti, M. Krieger, and H. H. Hobbs. 1996. Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J. Clin. Invest. 98: 984-995.
33. Andersen, J. M., and J. M. Dietschy. 1978. Relative importance of high and low density lipoproteins in the regulation of cholesterol synthesis in the adrenal gland, ovary and testes of the rat. J. Biol. Chem. 253: 9024-9032.
34. Mazurkiewicz, J. C., G. F. Watts, F. G. Warburton, B. M. Slavin, C. Lowy, and E. Konkkou. 1994. Serum lipids, lipoproteins and apolipoproteins in pregnant non-diabetic patients. J. Clin. Pathol. 47: 728-731.
35. Potter, J. M., and P. J. Nestel. 1979. The hyperlipidemia of pregnancy in normal and complicated pregnancies. Am. J. Obstet. Gynecol. 133: 165-170.
36. Reichen, J., G. Karlaganis, and F. Kern, Jr. 1987. Cholesterol synthesis in the perfused liver of pregnant hamsters. J. Lipid Res. 28: 1046-1052.
37. Turley, S. D., M. W. Herndon, and J. M. Dietschy. 1994. Reevaluation and application of the dual-isotope plasma ratio method for the measurement of intestinal cholesterol absorption in the hamster. J. Lipid Res. 35: 328-339.
38. Pittman, R. C., T. E. Carew, G. K. Glass, S. R. Green, G. A. Taylor, Jr., and A. D. Attie. 1983. A radioiodinated, intracellularly trapped ligand for determining the sites of plasma protein degradation in vivo. Biochem. J. 212: 791-800.
39. Bilheimer, D. W., S. Eisenberg, and R. I. Levy. 1972. The metabolism of very low density lipoprotein proteins. I. Preliminary in vitro and in vivo observations. Biochim. Biophys. Acta. 260:212-221.
40. Weisgraber, K. H., T. L. Innerarity, and R. W. Mahley. 1978. Role of the lysine residues of plasma lipoprotein in high affinity binding to cell surface receptors on human fibroblasts. J. Biol. Chem. 253: 9053-9062.
41. Woollett, L. A., and D. K. Spady. 1997. Kinetic parameters for HDL apoprotein A-I and cholesteryl ester transport in the hamster. J. Clin. Invest. 99: 1704-1713.
42. Spady, D. K., D. W. Bilheimer, and J. M. Dietschy. 1983. Rates of receptor-dependent and -independent low density lipoprotein uptake in the hamster. Proc. Natl. Acad. Sci. USA. 80: 3499-3503.
43. Woollett, L. A., D. K. Spady, and J. M. Dietschy. 1989. Mechanisms by which saturated triacylglycerols elevate the plasma low density lipoprotein-cholesterol concentration in hamsters. Differential effects of fatty acid chain length. J. Clin. Invest. 84: 119-128.
44. Woollett, L. A., D. K. Spady, and J. M. Dietschy. 1992. Regulatory effects of the saturated fatty' acids 6:0 through 18:0 on hepatic low density lipoprotein receptor activity in the hamster. J. Clin. Invest. 89: 1133-1141.
45. Russell, D. W., W. J. Schneider, T. Yamamoto, K. Luskey, M. S. Brown, and J. L. Goldstein. 1984. Domain map of the LDL receptor: sequence homology with the epidermal growth factor precursor. Cell. 37: 577-585.
46. Willnow, T. E., J. Hilpert, S. A. Armstrong, A. Rohlmann, R. E. Hammer, D. K. Burns, and J. Herz. 1996. Defective forebrain development in mice lacking gp330/megalin. Proc. Natl. Acad. Sci. USA. 93: 8460-8464.
47. Cao, G., C. K. Garcia, K. L. Wyne, R. A. Shultz, K. L. Parker, and H. H. Hobbs. 1997. Human SR-BI/CLA-1 gene structure and localization. Evidence for transcriptional control by steroidogenic factor-1. J. Biol. Chem. In press.
48. Wyne, K. L., R. K. Pathak, M. C. Seabra, and H. H. Hobbs. 1996. Expression of the VLDL receptor in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 16: 407-415.
49. Rigotti, A., E. R. Edelman, P. Seifert, S. N. Iqbal, R. B. De-Mattos, R. E. Temel, M. Krieger, and D. L. Williams. 1996. Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogenic cells of the murine adrenal gland. J. Biol. Chem. 271: 33545-33549.
50. Langman, J. 1975. Medical Embryology. Human Development - Normal and Abnormal. The Williams & Wilkins Company, Baltimore, MD. 89-107.
51. Tropper, P. J., and R. H. Petrie. 1987. Placental exchange. In The Human Placenta. Clinical Perspectives. J. P. La-very, editor. Aspen Publishers, Inc., Rockville, MD. 199-205.
52. Ahokas, R. A., and G. D. Anderson. 1987. The placenta as an organ of nutrition. In The Human Placenta. Clinical Perspectives. J. P. Lavery, editor. Aspen Publishers, Inc., Rockville, MD. 207-220.
53. Franke, H., D. Pionné, L. Winkler, and R. Dargel. 1992. Synthesis, secretion and immunoelectron microscopic demonstration of apolipoprotein B-containing lipoprotein particles in the visceral rat yolk sac. Histochemistry. 97: 283-292.
54. Shi, W-K., B. Hopkins, S. Thompson, J. K. Heath, B. M. Luke, and C. F. Graham. 1985. Synthesis of apolipoproteins, alphafoetoprotein, albumin, and transferrin by the human foetal yolk sack and other foetal organs. J. Embryol. Exp. Morphol. 85: 191-206.
55. Rigotti, A., B. L. Trigatti, M. Penman, H. Rayburn, J. Herz, and M. Krieger. 1997. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc. Natl. Acad. Sci. USA. 94:12610-12615.
56. Jollie, W. P. 1990. Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology. 41:361-381.
57. Irons, M., E. R. Elias, G. Salen, G. S. Tint, and A. K. Batta. 1993. Defective cholesterol biosynthesis in Smith-Lemli-Opitz syndrome. Lancet. 341: 1414.
58. 7-reductase activity in liver microsomes from Smith-Lemli-Opitz homozygotes. J. Clin. Invest. 96: 1779-1785.
59. Smith, D. W., L. Lemli, and J. M. Opitz. 1964. A newly recognized syndrome of multiple congenital anomalies. J. Pediatr. 64:210-217.
60. Ingham, P. W. 1995. Signalling by hedgehog family proteins in Drosophila and vertebrate development. Curr. Opin. Genet. Dev. 5: 492-498.
61. Porter, J. A., K. E. Young, and P. A. Beachy. 1996. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 274: 255-259.
62. Chiang, G., Y. Litingtung, E. Lee, K. E. Young, J. L. Corden, H. Westphal, and P. A. Beachy. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgeAog-gene function. Nature. 383: 407-413.
63. Homanics, G. E., N. Maedo, M. G. Traber, H. J. Kayden, D. B. Dehart, and K. K. Sulik. 1995. Exencephaly and hydrocephaly in mice with targeted modification of the apolipoprotein B (Apob) gene. Teratology. 51: 1-10.
64. Farese, R. V., Jr., S. L. Ruland, L. M. Flynn, R. P. Stokowski, and S. G. Young. 1995. 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. USA. 92: 1774-1778.