• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Feb 28, 1995; 92(5): 1485–1489.
PMCID: PMC42544

The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily.

Abstract

Sequence comparisons of vitellogenins from a wide range of organisms have identified regions of similarity not only to each other but also to vertebrate apolipoproteins (e.g. apoB-100 and apoE). Furthermore, the chicken vitellogenin receptor, which also binds apolipoproteins receptor (LDLR) superfamily [Bujo, H., Hermann, M., Kaderli, M. O., Jacobsen, L., Sugawara, S., Nimpf, J., Yamamoto, T. & Schneider, W. J. (1994) EMBO J. 13, 5165-5175]. The yolk proteins of higher dipterans are exceptional, however, and instead show similarity to lipoprotein lipases. The molecular characterization of the putative Drosophila melanogaster vitellogenin receptor gene, yolkless (yl), described in this report reveals that the protein it encodes (Yl), is also a member of the LDLR superfamily. The ovary-specific 6.5-kb yl RNA codes for a protein of approximately 210 kDa which contains all three motifs common to the LDLR class of proteins. Within this superfamily, Yl may be related more to the LDLR-related proteins (LRPs), which bind both apolipoproteins and lipoprotein lipases. The similarity of Yl to the other LDLR proteins is restricted to the putative extracellular domain. Most noticeably, the cytoplasmic domain of Yl lacks the typical NPXY sequence which is involved in receptor internalization.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.3M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Gruenberg J, Howell KE. Membrane traffic in endocytosis: insights from cell-free assays. Annu Rev Cell Biol. 1989;5:453–481. [PubMed]
  • Pryer NK, Wuestehube LJ, Schekman R. Vesicle-mediated protein sorting. Annu Rev Biochem. 1992;61:471–516. [PubMed]
  • Schneider WJ. Lipoprotein receptors in oocyte growth. Clin Investig. 1992 May;70(5):385–390. [PubMed]
  • Raikhel AS, Dhadialla TS. Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol. 1992;37:217–251. [PubMed]
  • Postlethwait JH, Weiser K. Vitellogenesis induced by juvenile hormone in the female sterile mutant apterous-four in Drosophila melanogaster. Nat New Biol. 1973 Aug 29;244(139):284–285. [PubMed]
  • Stifani S, Barber DL, Nimpf J, Schneider WJ. A single chicken oocyte plasma membrane protein mediates uptake of very low density lipoprotein and vitellogenin. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1955–1959. [PMC free article] [PubMed]
  • Nimpf J, Radosavljevic MJ, Schneider WJ. 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]
  • Bujo H, Hermann M, Kaderli MO, Jacobsen L, Sugawara S, Nimpf J, Yamamoto T, Schneider WJ. Chicken oocyte growth is mediated by an eight ligand binding repeat member of the LDL receptor family. EMBO J. 1994 Nov 1;13(21):5165–5175. [PMC free article] [PubMed]
  • Stifani S, Nimpf J, Schneider WJ. Vitellogenesis in Xenopus laevis and chicken: cognate ligands and oocyte receptors. The binding site for vitellogenin is located on lipovitellin I. J Biol Chem. 1990 Jan 15;265(2):882–888. [PubMed]
  • Stifani S, Le Menn F, Rodriguez JN, Schneider WJ. Regulation of oogenesis: the piscine receptor for vitellogenin. Biochim Biophys Acta. 1990 Aug 6;1045(3):271–279. [PubMed]
  • Indrasith LS, Kindle H, Lanzrein B. Solubilization, identification, and localization of vitellogenin-binding sites in follicles of the cockroach, Nauphoeta cinerea. Arch Insect Biochem Physiol. 1990;15(4):213–228. [PubMed]
  • Waring GL, DiOrio JP, Hennen S. Isolation of germ line-dependent female-sterile mutation that affects yolk specific sequestration and chorion formation in Drosophila. Dev Biol. 1983 Dec;100(2):452–463. [PubMed]
  • Perrimon N, Mohler D, Engstrom L, Mahowald AP. X-linked female-sterile loci in Drosophila melanogaster. Genetics. 1986 Jul;113(3):695–712. [PMC free article] [PubMed]
  • DiMario PJ, Mahowald AP. Female sterile (1) yolkless: a recessive female sterile mutation in Drosophila melanogaster with depressed numbers of coated pits and coated vesicles within the developing oocytes. J Cell Biol. 1987 Jul;105(1):199–206. [PMC free article] [PubMed]
  • Tamkun JW, Deuring R, Scott MP, Kissinger M, Pattatucci AM, Kaufman TC, Kennison JA. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. [PubMed]
  • Schonbaum CP, Organ EL, Qu S, Cavener DR. The Drosophila melanogaster stranded at second (sas) gene encodes a putative epidermal cell surface receptor required for larval development. Dev Biol. 1992 Jun;151(2):431–445. [PubMed]
  • Rubin GM, Spradling AC. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. [PubMed]
  • Spradling AC, Rubin GM. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. [PubMed]
  • Steller H, Pirrotta V. P transposons controlled by the heat shock promoter. Mol Cell Biol. 1986 May;6(5):1640–1649. [PMC free article] [PubMed]
  • Steinhauer WR, Walsh RC, Kalfayan LJ. Sequence and structure of the Drosophila melanogaster ovarian tumor gene and generation of an antibody specific for the ovarian tumor protein. Mol Cell Biol. 1989 Dec;9(12):5726–5732. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Koerner TJ, Hill JE, Myers AM, Tzagoloff A. High-expression vectors with multiple cloning sites for construction of trpE fusion genes: pATH vectors. Methods Enzymol. 1991;194:477–490. [PubMed]
  • Kleid DG, Yansura D, Small B, Dowbenko D, Moore DM, Grubman MJ, McKercher PD, Morgan DO, Robertson BH, Bachrach HL. Cloned viral protein vaccine for foot-and-mouth disease: responses in cattle and swine. Science. 1981 Dec 4;214(4525):1125–1129. [PubMed]
  • Hager DA, Burgess RR. Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity: results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes. Anal Biochem. 1980 Nov 15;109(1):76–86. [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. [PMC free article] [PubMed]
  • Russell DW, Schneider WJ, Yamamoto T, Luskey KL, Brown MS, Goldstein JL. Domain map of the LDL receptor: sequence homology with the epidermal growth factor precursor. Cell. 1984 Jun;37(2):577–585. [PubMed]
  • Yamamoto T, Davis CG, Brown MS, Schneider WJ, Casey ML, Goldstein JL, Russell DW. The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell. 1984 Nov;39(1):27–38. [PubMed]
  • Esser V, Limbird LE, Brown MS, Goldstein JL, Russell DW. Mutational analysis of the ligand binding domain of the low density lipoprotein receptor. J Biol Chem. 1988 Sep 15;263(26):13282–13290. [PubMed]
  • Herz J, Hamann U, Rogne S, Myklebost O, Gausepohl H, Stanley KK. Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J. 1988 Dec 20;7(13):4119–4127. [PMC free article] [PubMed]
  • Chen WJ, Goldstein JL, Brown MS. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem. 1990 Feb 25;265(6):3116–3123. [PubMed]
  • Bansal A, Gierasch LM. The NPXY internalization signal of the LDL receptor adopts a reverse-turn conformation. Cell. 1991 Dec 20;67(6):1195–1201. [PubMed]
  • Collawn JF, Kuhn LA, Liu LF, Tainer JA, Trowbridge IS. Transplanted LDL and mannose-6-phosphate receptor internalization signals promote high-efficiency endocytosis of the transferrin receptor. EMBO J. 1991 Nov;10(11):3247–3253. [PMC free article] [PubMed]
  • Steyrer E, Barber DL, Schneider WJ. Evolution of lipoprotein receptors. The chicken oocyte receptor for very low density lipoprotein and vitellogenin binds the mammalian ligand apolipoprotein E. J Biol Chem. 1990 Nov 15;265(32):19575–19581. [PubMed]
  • Saito A, Pietromonaco S, Loo AK, Farquhar MG. Complete cloning and sequencing of rat gp330/"megalin," a distinctive member of the low density lipoprotein receptor gene family. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9725–9729. [PMC free article] [PubMed]
  • Strickland DK, Ashcom JD, Williams S, Burgess WH, Migliorini M, Argraves WS. Sequence identity between the alpha 2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem. 1990 Oct 15;265(29):17401–17404. [PubMed]
  • Beisiegel U, Weber W, Ihrke G, Herz J, Stanley KK. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature. 1989 Sep 14;341(6238):162–164. [PubMed]
  • 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 Dec 25;267(36):26172–26180. [PubMed]
  • Yochem J, Greenwald I. A gene for a low density lipoprotein receptor-related protein in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4572–4576. [PMC free article] [PubMed]
  • Stifani S, Barber DL, Aebersold R, Steyrer E, Shen X, Nimpf J, Schneider WJ. The laying hen expresses two different low density lipoprotein receptor-related proteins. J Biol Chem. 1991 Oct 5;266(28):19079–19087. [PubMed]
  • Martinez A, Bownes M. The specificity of yolk protein uptake in cyclorrhaphan diptera is conserved through evolution. J Mol Evol. 1992 Nov;35(5):444–453. [PubMed]
  • Chen JS, Cho WL, Raikhel AS. Analysis of mosquito vitellogenin cDNA. Similarity with vertebrate phosvitins and arthropod serum proteins. J Mol Biol. 1994 Apr 15;237(5):641–647. [PubMed]
  • Yano K, Sakurai MT, Watabe S, Izumi S, Tomino S. Structure and expression of mRNA for vitellogenin in Bombyx mori. Biochim Biophys Acta. 1994 May 17;1218(1):1–10. [PubMed]
  • Trewitt PM, Heilmann LJ, Degrugillier SS, Kumaran AK. The boll weevil vitellogenin gene: nucleotide sequence, structure, and evolutionary relationship to nematode and vertebrate vitellogenin genes. J Mol Evol. 1992 Jun;34(6):478–492. [PubMed]

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

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links