Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Mar;87(5):1955–1959. doi: 10.1073/pnas.87.5.1955

A single chicken oocyte plasma membrane protein mediates uptake of very low density lipoprotein and vitellogenin.

S Stifani 1, D L Barber 1, J Nimpf 1, W J Schneider 1
PMCID: PMC53603  PMID: 2308956

Abstract

Specific cell-surface receptors mediate the uptake of plasma proteins into growing oocytes of oviparous species, thereby forming yolk. Quantitatively the most important yolk precursors are the lipoproteins, very low density lipoprotein, and vitellogenin. We show that a single major chicken oocyte plasma membrane protein with an apparent molecular mass of 95 kDa as determined by SDS/PAGE under nonreducing conditions is the receptor for both of these ligands. Binding activities for the two ligands copurified on ligand affinity matrices and were inhibited by the same antibody preparations, and the ligands competed with each other for binding to the 95-kDa protein. In addition to these biochemical and immunological lines of evidence for the identity of the vitellogenin receptor with the very low density lipoprotein receptor, genetic proof was obtained. We have previously shown that the mutant nonlaying "restricted-ovulator" hen carries a defect in the gene responsible for functional expression of the oocyte 95-kDa protein. Here we demonstrate that this single gene defect in the restricted-ovulator hen has detrimental consequences for the binding not only of very low density lipoprotein but also of vitellogenin to the 95-kDa receptor normally present in oocytes. The intriguing bifunctionality of this chicken oocyte membrane protein possibly relates to its crucial role in receptor-mediated control of oocyte growth.

Full text

PDF
1955

Images in this article

1956Image
on p.1956
1957Image
on p.1957
1957Image
on p.1957
1957Image
on p.1957
1958Image
on p.1958
1958Image
on p.1958

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baker M. E. Is vitellogenin an ancestor of apolipoprotein B-100 of human low-density lipoprotein and human lipoprotein lipase? Biochem J. 1988 Nov 1;255(3):1057–1060. doi: 10.1042/bj2551057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beisiegel U., Schneider W. J., Brown M. S., Goldstein J. L. Immunoblot analysis of low density lipoprotein receptors in fibroblasts from subjects with familial hypercholesterolemia. J Biol Chem. 1982 Nov 10;257(21):13150–13156. [PubMed] [Google Scholar]
  3. Daniel T. O., Schneider W. J., Goldstein J. L., Brown M. S. Visualization of lipoprotein receptors by ligand blotting. J Biol Chem. 1983 Apr 10;258(7):4606–4611. [PubMed] [Google Scholar]
  4. Esser V., Limbird L. E., Brown M. S., Goldstein J. L., Russell D. W. Mutational analysis of the ligand binding domain of the low density lipoprotein receptor. J Biol Chem. 1988 Sep 15;263(26):13282–13290. [PubMed] [Google Scholar]
  5. George R., Barber D. L., Schneider W. J. Characterization of the chicken oocyte receptor for low and very low density lipoproteins. J Biol Chem. 1987 Dec 15;262(35):16838–16847. [PubMed] [Google Scholar]
  6. Goldstein J. L., Brown M. S., Anderson R. G., Russell D. W., Schneider W. J. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu Rev Cell Biol. 1985;1:1–39. doi: 10.1146/annurev.cb.01.110185.000245. [DOI] [PubMed] [Google Scholar]
  7. Hayashi K., Nimpf J., Schneider W. J. Chicken oocytes and fibroblasts express different apolipoproteins-B-specific receptors. J Biol Chem. 1989 Feb 25;264(6):3131–3139. [PubMed] [Google Scholar]
  8. Hermier D., Forgez P., Chapman M. J. A density gradient study of the lipoprotein and apolipoprotein distribution in the chicken, Gallus domesticus. Biochim Biophys Acta. 1985 Aug 22;836(1):105–118. doi: 10.1016/0005-2760(85)90226-7. [DOI] [PubMed] [Google Scholar]
  9. Ho K. J., Lawrence W. D., Lewis L. A., Liu L. B., Taylor C. B. Hereditary hyperlipidemia in nonlaying chickens. Arch Pathol. 1974 Sep;98(3):161–172. [PubMed] [Google Scholar]
  10. Innerarity T. L., Arnold K. S., Weisgraber K. H., Mahley R. W. Apolipoprotein E is the determinant that mediates the receptor uptake of beta-very low density lipoproteins by mouse macrophages. Arteriosclerosis. 1986 Jan-Feb;6(1):114–122. doi: 10.1161/01.atv.6.1.114. [DOI] [PubMed] [Google Scholar]
  11. Kirchgessner T. G., Heinzmann C., Svenson K. L., Gordon D. A., Nicosia M., Lebherz H. G., Lusis A. J., Williams D. L. Regulation of chicken apolipoprotein B: cloning, tissue distribution, and estrogen induction of mRNA. Gene. 1987;59(2-3):241–251. doi: 10.1016/0378-1119(87)90332-5. [DOI] [PubMed] [Google Scholar]
  12. Kita T., Brown M. S., Watanabe Y., Goldstein J. L. Deficiency of low density lipoprotein receptors in liver and adrenal gland of the WHHL rabbit, an animal model of familial hypercholesterolemia. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2268–2272. doi: 10.1073/pnas.78.4.2268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Knott T. J., Pease R. J., Powell L. M., Wallis S. C., Rall S. C., Jr, Innerarity T. L., Blackhart B., Taylor W. H., Marcel Y., Milne R. Complete protein sequence and identification of structural domains of human apolipoprotein B. Nature. 1986 Oct 23;323(6090):734–738. doi: 10.1038/323734a0. [DOI] [PubMed] [Google Scholar]
  14. Knott T. J., Rall S. C., Jr, Innerarity T. L., Jacobson S. F., Urdea M. S., Levy-Wilson B., Powell L. M., Pease R. J., Eddy R., Nakai H. Human apolipoprotein B: structure of carboxyl-terminal domains, sites of gene expression, and chromosomal localization. Science. 1985 Oct 4;230(4721):37–43. doi: 10.1126/science.2994225. [DOI] [PubMed] [Google Scholar]
  15. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  16. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  17. Nimpf J., Radosavljevic M. J., Schneider W. J. Oocytes from the mutant restricted ovulator hen lack receptor for very low density lipoprotein. J Biol Chem. 1989 Jan 25;264(3):1393–1398. [PubMed] [Google Scholar]
  18. Nimpf J., Radosavljevic M., Schneider W. J. Specific postendocytic proteolysis of apolipoprotein B in oocytes does not abolish receptor recognition. Proc Natl Acad Sci U S A. 1989 Feb;86(3):906–910. doi: 10.1073/pnas.86.3.906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Persson B., Bengtsson-Olivecrona G., Enerbäck S., Olivecrona T., Jörnvall H. Structural features of lipoprotein lipase. Lipase family relationships, binding interactions, non-equivalence of lipase cofactors, vitellogenin similarities and functional subdivision of lipoprotein lipase. Eur J Biochem. 1989 Jan 15;179(1):39–45. doi: 10.1111/j.1432-1033.1989.tb14518.x. [DOI] [PubMed] [Google Scholar]
  20. Pitas R. E., Innerarity T. L., Arnold K. S., Mahley R. W. Rate and equilibrium constants for binding of apo-E HDLc (a cholesterol-induced lipoprotein) and low density lipoproteins to human fibroblasts: evidence for multiple receptor binding of apo-E HDLc. Proc Natl Acad Sci U S A. 1979 May;76(5):2311–2315. doi: 10.1073/pnas.76.5.2311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schneider W. J., Basu S. K., McPhaul M. J., Goldstein J. L., Brown M. S. Solubilization of the low density lipoprotein receptor. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5577–5581. doi: 10.1073/pnas.76.11.5577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schneider W. J., Beisiegel U., Goldstein J. L., Brown M. S. Purification of the low density lipoprotein receptor, an acidic glycoprotein of 164,000 molecular weight. J Biol Chem. 1982 Mar 10;257(5):2664–2673. [PubMed] [Google Scholar]
  23. Schneider W. J., Goldstein J. L., Brown M. S. Partial purification and characterization of the low density lipoprotein receptor from bovine adrenal cortex. J Biol Chem. 1980 Dec 10;255(23):11442–11447. [PubMed] [Google Scholar]
  24. Schneider W. J. The low density lipoprotein receptor. Biochim Biophys Acta. 1989 May 9;988(2):303–317. doi: 10.1016/0304-4157(89)90023-3. [DOI] [PubMed] [Google Scholar]
  25. Stifani S., George R., Schneider W. J. Solubilization and characterization of the chicken oocyte vitellogenin receptor. Biochem J. 1988 Mar 1;250(2):467–475. doi: 10.1042/bj2500467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Weisgraber K. H., Innerarity T. L., Mahley R. W. Role of lysine residues of plasma lipoproteins in high affinity binding to cell surface receptors on human fibroblasts. J Biol Chem. 1978 Dec 25;253(24):9053–9062. [PubMed] [Google Scholar]
  27. van Driel I. R., Davis C. G., Goldstein J. L., Brown M. S. Self-association of the low density lipoprotein receptor mediated by the cytoplasmic domain. J Biol Chem. 1987 Nov 25;262(33):16127–16134. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES