Temporal and spatial pattern of expression of the HDL receptor SR-BI during murine embryogenesis

Journal of Lipid Research

Volumn 39, Issue 3, 1998, Pages 495-508

  Hatzopoulos, Antonis K ^a   Rigotti, Attilio ^a,b   Rosenberg, Robert D ^a   Krieger, Monty ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Cholesterol transport system; Immunofluorescence microscopy; Maternal fetal lipoprotein; Placenta; Trophoblast cells; Yolk sac

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HIGH DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; CHOLESTEROL TRANSPORT; EMBRYO; EMBRYO DEVELOPMENT; FETOPLACENTAL UNIT; GENE EXPRESSION; HORMONE SYNTHESIS; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TROPHOBLAST; YOLK SAC;

ANIMALS; ANTIGENS, CD36; BIOLOGICAL TRANSPORT; CARBOCYANINES; CHOLESTEROL; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FLUORESCENT DYES; GENE EXPRESSION; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; PLACENTA; PLACENTATION; PREGNANCY; RECEPTORS, IMMUNOLOGIC; RECEPTORS, LIPOPROTEIN; RECEPTORS, SCAVENGER; SCAVENGER RECEPTORS, CLASS B; TIME FACTORS; YOLK SAC;

EID: 0031897629     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Albrecht, E. D., and G. J. Pepe. 1990. Placental steroid hormone biosynthesis in primate pregnancy. Endocrinol. Rev. 11: 124-150.
2. Cross, J. C., Z. Werb, and S. J. Fisher. 1994. Implantation and the placenta: key pieces of the developmental puzzle. Science. 266: 1508-1518.
3. Strauss III, J. F., F. Martinez, and M. Kiriakidou. 1996. Placental steroid hormone synthesis: unique features and unanswered questions. Biol. Reprod. 54: 303-311.
4. Roux, C., and M. Aubry. 1966. Action teratogene d'un inhibiteur de la synthese du cholesterol, le AY 9944. C. R. Soc. Biol. 160: 1353-1357.
5. 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.
6. Porter, J. A., K. E. Young, and P. A. Beachy. 1996. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 274: 255-259.
7. Carr, B. R., and E. R. Simpson. 1982. Cholesterol synthesis in human fetal tissues. J. Clin. Endocrinol. Metab. 55: 447-452.
8. 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.
9. Belknap, W. M., and J. M. Dietschy. 1988. Sterol synthesis and low density lipoprotein clearance in vivo in the pregnant rat, placenta, and fetus. J. Clin. Invest. 82: 2077-2085.
10. Haave, N. C., and S. M. Innis. 1991. Perinatal development of hepatic cholesterol synthesis in the rat. Biochim. Biophys. Acta. 1085: 35-44.
11. Yount, N. Y., and D. J. McNamara. 1991. Dietary regulation of maternal and fetal cholesterol metabolism in the guinea pig. Biochim. Biophys. Acta. 1085: 82-90.
12. Cavender, C. P., S. D. Turley, and J. M. Dietschy. 1995. Sterol metabolism in fetal, newborn, and suckled lambs and their response to cholesterol after weaning. Am. J. Physiol. 269: E331-E340.
13. 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.
14. Chevallier, F. 1964. Transferts et synthese du cholesterol chez le rat au cours de sa croissance. Biochim. Biophys. Acta. 84: 316-339.
15. 14C into rabbit and guinea pig fetus. J. Lipid Res. 8: 558-564.
16. Pitkin, R. M., W. E. Connor, and D. S. Lin. 1972. Cholesterol metabolism and placental transfer in the pregnant rhesus monkey. J. Clin. Invest. 51: 2584-2592.
17. 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.
18. 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.
19. 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.
20. Plotz, E. J., J. J. Kabara, M. E. Davis, G. V. LeRoy, and R. G. Gould. 1968. Studies on the synthesis of cholesterol in the brain of the human fetus. Am. J. Obstet. Gynecol. 101: 534-538.
21. 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.
22. Alsat, E., Y. Bouali, S. Goldstein, A. Malassine, M. Berthelier, F. Mondon, and L. Gedard. 1984. Low-density lipoprotein binding sites in the microvillous membranes of human placenta at different stages of gestation. Mol. Cell. Endocrinol. 38: 197-203.
23. 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.
24. Jollie, W. P. 1990. Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology. 41: 361-381.
25. 2-macroglobulin- and pregnancy zone protein-proteinase complexes in the human placental syncytiotrophoblast. Placenta. 9: 463-477.
26. Furuhashi, M., H. Seo, S. Mizutani, O. Narita, Y. Tomoda, and N. Matsui. 1989. Expression of low density lipoprotein receptor gene in human placenta during pregnancy. Mol. Endocrinol. 3: 1252-1256.
27. 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Differentiation and cAMP modulate protein and mRNA levels. J. Biol. Chem. 267: 21230-21234.
28. 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 LPR/α2MR, and the receptor-associated protein (RAP). J. Histochem. Cytochem. 42: 531-542.
29. Gafvels, M. E., L. G. Paavola, C. O. Boyd, P. M. Nolan, F. Wittmaack, A. Chawla, M. A. Lazar, M. Bucan, B. O. 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.
30. Wittmaack, F. M., M. E. Gafvels, M. Bronner, H. Matsuo, K. R. McCrae, J. E. Tomaszewski, S. L. Robinson, D. K. Strickland, and J. F. 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.
31. Overbergh, L., K. Lorent, S. Torrekens, F. Van Leuven, and H. Van den Berghe. 1995. Expression of mouse alpha-macroglobulins, lipoprotein receptor-related protein, LDL receptor, apolipoprotein E, and lipoprotein lipase in pregnancy. J. Lipid Res. 36: 1774-1786.
32. Winkel, C. A., P. C. MacDonald, and E. R. Simpson. 1981. The role of receptor-mediated low-density lipoprotein uptake and degradation in the regulation of progesterone biosynthesis and cholesterol metabolism by human trophoblasts. Placenta. 3 (Suppl): 133-143.
33. Shi, W-K., and J. K. Heath. 1984. Apolipoprotein expression by murine visceral yolk sac endoderm. J. Embryol. Exp. Morphol. 81: 143-152.
34. 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 sac and other foetal organs. J. Embryol. Exp. Morphol. 85: 191-206.
35. Hopkins, B., A. L. Brice, P. N. Schofield, F. E. Baralle, and C. F. Graham. 1987. Identity of cells containing apolipoprotein B messenger RNA in 6- to 12-week postfertihzation human embryos. Development. 100: 83-93.
36. Lanford, R. E., D. L. Bronson, L. E. Estlack, and F. H. Wians, Jr. 1991. Plasma protein and apolipoprotein synthesis by human yolk sac carcinoma cells in vitro. In Vitro Cell. Dev. Biol. 27A: 205-210.
37. Plonne, D., L. Winkler, H. Franke, and R. Dargel. 1992. The visceral yolk sac: an important site of synthesis and secretion of apolipoprotein B-containing lipoproteins in the feto-placental unit of the rat. Biochem. Biophys. Acta. 1127: 174-185.
38. Franke, H., D. Plonne, 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.
39. Homanics, G. E., T. J. Smith, S. H. Zhang, D. Lee, S. G. Young, and N. Maeda. 1993. Targeted modification of the apolipoprotein B gene results in hypobetalipoproteinemia and developmental abnormalities in mice. Proc. Natl. Acad. Sci. USA. 90: 2389-2393.
40. 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 heteroxygotes. Proc. Natl. Acad. Sci. USA. 92: 1774-1778.
41. Huang, L. S., E. Voyiaziakis, D. F. Markenson, K. A. Sokol, T. Hayek, and J. L. Breslow. 1995. ApoB gene knockout in mice results in embryonic lethality in homozygotes and neural tube defects, male infertility, and reduced HDL cholesteryl ester and apoA-I transport rates in heterozygotes. J. Clin. Invest. 96: 2152-2161.
42. Willnow, T. E., J. Hilpert, S. A. Amstrong, 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.
43. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
44. Pieters, M. N., D. Schouten, and T. J. C. van Berkel. 1994. In vitro and in vivo evidence for the role of HDL in reverse cholesterol transport. Biochim. Biophys. Acta. 1225: 125-134.
45. Fielding, C. J., and P. E. Fielding. 1995. Molecular physiology of reverse cholesterol transport. J. Lipid Res. 36: 211-228.
46. Rigotti, A., B. Trigatti, J. Babitt, M. Penman, S. Xu, and M. Krieger. 1997. SR-BI, a cell surface receptor for HDL. Curr. Opin. Lipidol. 8: 181-188.
47. Acton, S., A. Rigotti, K. T. Landschulz, 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.
48. 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.
49. Rigotti, A., E. R. Edelman, P. Seifert, S. N. Iqbal, R. B. DeMattos, 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. Wang, N., W. Weng, J. L. Breslow, and A. R. Tall. 1996. Scavenger receptor BI (SR-BI) is up-regulated in adrenal gland in apolipoprotein A-I and hepatic lipase knock-out mice as a response to depletion of cholesterol stores. In vivo evidence that SR-BI is a functional high density lipoprotein receptor under feedback control. J. Biol. Chem. 271: 21001-21004.
51. Kozarsky, K. F., M. H. Donahee, A. Rigotti, S. N. Iqbal, E. R. Edelman, and M. Krieger. 1997. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature. 387: 414-417.
52. 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.
53. Pitas, R. E., T. L. Innerarity, J. N. Weinstein, and R. W. Mahley. 1981. Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis. 1: 177-185.
54. Theiler, K. 1989. The House Mouse: Atlas of Embryonic Development. Springer-Verlag, New York, Berlin, Heidelberg. 29-33.
55. Hogan, B. L. M., D. P. Parlow, and M. Kurkinen. 1984. Reichert's membrane as a model for biosynthesis of basement membrane components. CIBA Found. Symp. 108: 60-69.
56. Esmon, C. T., and W. G. Owen. 1981. Identification of an endothelial cell cofactor for thrombin catalyzed activation of protein C. Proc. Natl. Acad. Sci. USA. 78: 2249-2252.
57. Maruyama, I., C. E. Bell, and P. W. Majerus. 1985. Thrombomodulin is found on endothelium of arteries, veins, capillaries, and lymphatics, and on syncytiotrophoblast of human placenta. J. Cell Biol. 101: 363-371.
58. Weiler-Guettler, H., W. C. Aird, H. Rayburn, M. Husain, and R. D. Rosenberg. 1996. Developmentally regulated gene expression of thrombomodulin in postimplantation mouse embryos. Development. 122: 2271-2281.
59. Wagner, D. D., and V. J. Marder. 1984. Biosynthesis of von Willebrand protein by human endothelial cells: processing steps and their intracellular localization. J. Cell Biol. 99: 2123-2130.
60. Theiler, K. 1989. The House Mouse: Atlas of Embryonic Development. Springer-Verlag, New York, Berlin, Heidelberg. 73-77.
61. Krieger, M., and J. Herz. 1994. Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LPR). Annu. Rev. Biochem. 63: 601-637.
62. Voyta, J. C., D. P. Via, C. E. Butterfield, and B. R. Zetter. 1984. Identification and isolation of endothelial cells based on their increased uptake of acetylated low density lipoprotein. J. Cell Biol. 99: 2034-2040.
63. Rugh, R. 1990. The Mouse: Its Reproduction and Developinent, Oxford University Press, Oxford, New York, Tokyo. 262.
64. Keeney, D. S., Y. Ikeda, M. R. Waterman, and K. L. Parker. 1995. Cholesterol side-chain cleavage cytochrome P450 gene expression in the primitive gut of the mouse embryo does not require steroidogenic factor I. Mol. Endocrinol. 9: 1091-1098.
65. Breier, G., F., Brevario, L. Caveda, R. Berthier, H. Schnuerch, U. Gotsch, D. Vestweber, W. Risau, and E. Dejana. 1996. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood. 87: 630-641.
66. Breier, G., M. Clauss, and W. Risau. 1995. Coordinate expression of vascular endothelial growth factor receptor-1 (flt-1) and its ligand suggest a paracrine regulation of the murine vascular development. Dev Dyn. 204: 228-239.
67. Dumont, D. J., G. H. Fong, M. C. Puri, G. Gradwohl, K. Alitalo, and M. L. Breitman. 1995. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev. Dyn. 203:80-92.