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PMID: 10769163 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin.

The Biochemical journal ·Vol. 347 Pt 3 ·2000-05-01 ·Pages 613-21

Oleinikov AV, Zhao J, Makker SP

Abstract

gp600/megalin, an endocytic receptor, belongs to the low-density lipoprotein receptor family. It is most abundant in the renal proximal tubular cells, where it is implicated in the reabsorption of a number of molecules filtered through the glomerulus. The cytoplasmic tail (CT) of gp600/megalin contains a number of sequence similarities, which indicate that gp600/megalin might be involved in signal transduction. To find intracellular proteins that would interact with the gp600/megalin CT, a human kidney cDNA library was screened by using the yeast two-hybrid system. The phosphotyrosine interaction domain (PID) of the Disabled protein 2 (Dab2), a mammalian structural analogue of Drosophila Disabled, was found to bind to the gp600/megalin CT in this system. The interaction between these two proteins was confirmed by a binding assay in vitro and by the co-immunoprecipitation of both proteins from renal cell lysates. The gp600/megalin CT contains three PsiXNPXY motifs (in which Psi represents a hydrophobic residue) that are potentially able to interact with PID. Analysis of the CT deletion and point-mutation variants of gp600/megalin by the two-hybrid system revealed that the third PsiXNPXY motif is most probably involved in this interaction. Dab2 is a mitogen-responsive phosphoprotein thought to be an adaptor molecule involved in signal transduction, and a suggested negative regulator of cell growth. Dab2 is the first intracellular ligand identified for gp600/megalin; gp600/megalin is the first known transmembrane receptor that interacts with the cytosolic protein Dab2. We speculate that their interaction might involve gp600/megalin in signal transduction pathways or might mediate the intracellular trafficking of this receptor.

MeSH Terms
Adaptor Proteins, Signal Transducing Adaptor Proteins, Vesicular Transport Amino Acid Motifs Amino Acid Sequence Animals Apoptosis Regulatory Proteins Binding Sites Cell Line Genes, Tumor Suppressor Heymann Nephritis Antigenic Complex Humans Kidney/cytology,metabolism Ligands Membrane Glycoproteins/chemistry,genetics,metabolism Molecular Sequence Data Phosphoproteins/chemistry,metabolism Point Mutation/genetics Precipitin Tests Protein Binding Protein Structure, Tertiary Proteins Rats Receptors, LDL/chemistry,genetics,metabolism Sequence Deletion/genetics Signal Transduction Tumor Cells, Cultured Tumor Suppressor Proteins Two-Hybrid System Techniques
Chemicals
Adaptor Proteins, Signal Transducing Adaptor Proteins, Vesicular Transport Apoptosis Regulatory Proteins DAB2 protein, human Heymann Nephritis Antigenic Complex Ligands Membrane Glycoproteins Phosphoproteins Proteins Receptors, LDL Tumor Suppressor Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Oleinikov A V
Department of Pediatrics, Division of Nephrology, School of Medicine, University of California, Davis, CA 95616, USA. avoleinikov@ucdavis.edu
Zhao J
Makker S P
References (49)
49 references, click to expand
  1. DOC-2, a candidate tumor suppressor gene in human epithelial ovarian cancer.
    Oncogene. 1998 May 7;16(18):2381-7 PMID: 9620555
  2. Chromosomal localization of human genes for the LDL receptor family member glycoprotein 330 (LRP2) and its associated protein RAP (LRPAP1).
    Genomics. 1994 Jul 1;22(1):88-93 PMID: 7959795
  3. The 39-kDa receptor-associated protein interacts with two members of the low density lipoprotein receptor family, alpha 2-macroglobulin receptor and glycoprotein 330.
    J Biol Chem. 1992 Oct 15;267(29):21162-6 PMID: 1400426
  4. Characterization of the antigen (gp600) of Heymann nephritis.
    Lab Invest. 1984 Mar;50(3):287-93 PMID: 6199583
  5. Cloning of a novel phosphoprotein regulated by colony-stimulating factor 1 shares a domain with the Drosophila disabled gene product.
    J Biol Chem. 1995 Jun 9;270(23):14184-91 PMID: 7775479
  6. PTB domains of IRS-1 and Shc have distinct but overlapping binding specificities.
    J Biol Chem. 1995 Nov 17;270(46):27407-10 PMID: 7499194
  7. Immortalized rat proximal tubule cells produce membrane bound and soluble megalin.
    Kidney Int. 1998 Feb;53(2):358-66 PMID: 9461095
  8. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3.
    Cell. 1999 Feb 19;96(4):507-15 PMID: 10052453
  9. Glycoprotein 330/megalin: probable role in receptor-mediated transport of apolipoprotein J alone and in a complex with Alzheimer disease amyloid beta at the blood-brain and blood-cerebrospinal fluid barriers.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4229-34 PMID: 8633046
  10. Immortalized rat proximal tubule cell lines expressing components of the renin-angiotensin system.
    Exp Nephrol. 1994 Mar-Apr;2(2):127 PMID: 8082004
  11. DOC-2/hDab2, a candidate tumor suppressor gene involved in the development of gestational trophoblastic diseases.
    Oncogene. 1998 Jul 30;17(4):419-24 PMID: 9696034
  12. 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):4572-6 PMID: 8506301
  13. Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein.
    J Biol Chem. 1998 Dec 11;273(50):33556-60 PMID: 9837937
  14. Complexity in biological signaling systems.
    Science. 1999 Apr 2;284(5411):92-6 PMID: 10102825
  15. Megalin/gp330 mediates uptake of albumin in renal proximal tubule.
    Am J Physiol. 1996 Oct;271(4 Pt 2):F900-7 PMID: 8898021
  16. Specificity of the PTB domain of Shc for beta turn-forming pentapeptide motifs amino-terminal to phosphotyrosine.
    J Biol Chem. 1995 Aug 4;270(31):18205-8 PMID: 7543098
  17. Sequence, genomic structure, and chromosomal assignment of human DOC-2.
    Genomics. 1996 Apr 15;33(2):207-13 PMID: 8660969
  18. The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids.
    Mol Cell Biol. 1999 Jul;19(7):5179-88 PMID: 10373567
  19. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development.
    EMBO J. 1997 Jan 2;16(1):121-32 PMID: 9009273
  20. Identification of a cell line that expresses a cell surface and a soluble form of the gp330/receptor-associated protein (RAP) Heymann nephritis antigenic complex.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4082-6 PMID: 8483924
  21. The role of DOC-2/DAB2 protein phosphorylation in the inhibition of AP-1 activity. An underlying mechanism of its tumor-suppressive function in prostate cancer.
    J Biol Chem. 1999 Nov 5;274(45):31981-6 PMID: 10542228
  22. Heymann antigen GP330 demonstrates affinity for fibronectin, laminin, and type I collagen and mediates rat proximal tubule epithelial cell adherence to such matrices in vitro.
    Exp Cell Res. 1990 May;188(1):23-35 PMID: 1691715
  23. Production of nephrotic syndrome in rats by Freund's adjuvants and rat kidney suspensions.
    Proc Soc Exp Biol Med. 1959 Apr;100(4):660-4 PMID: 13645677
  24. Characterization of a rat yolk sac carcinoma cell line.
    Dev Biol. 1982 Oct;93(2):416-21 PMID: 7141105
  25. Molecular cloning of differentially expressed genes in human epithelial ovarian cancer.
    Gynecol Oncol. 1994 Feb;52(2):247-52 PMID: 8314147
  26. YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis.
    J Biol Chem. 1993 Oct 15;268(29):21686-92 PMID: 8408022
  27. Detection of two forms of GP330. Their role in Heymann nephritis.
    Am J Pathol. 1993 Aug;143(2):598-611 PMID: 8342605
  28. 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):9725-9 PMID: 7937880
  29. Cloning and sequencing of human gp330, a Ca(2+)-binding receptor with potential intracellular signaling properties.
    Eur J Biochem. 1996 Jul 1;239(1):132-7 PMID: 8706697
  30. Disabled-2 (Dab2) is an SH3 domain-binding partner of Grb2.
    Oncogene. 1998 Mar 26;16(12):1561-9 PMID: 9569023
  31. Defective forebrain development in mice lacking gp330/megalin.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8460-4 PMID: 8710893
  32. Functional expression of low density lipoprotein receptor-related protein is controlled by receptor-associated protein in vivo.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4537-41 PMID: 7538675
  33. beta2-glycoprotein-I (apolipoprotein H) and beta2-glycoprotein-I-phospholipid complex harbor a recognition site for the endocytic receptor megalin.
    J Clin Invest. 1998 Sep 1;102(5):902-9 PMID: 9727058
  34. 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):3116-23 PMID: 1968060
  35. 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein.
    EMBO J. 1995 May 15;14(10):2269-80 PMID: 7774585
  36. Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation.
    Cell. 1998 Dec 11;95(6):793-803 PMID: 9865697
  37. Transcription and translation of gp600 and receptor-associated protein (RAP) in active Heymann nephritis.
    Am J Pathol. 1995 Jun;146(6):1481-7 PMID: 7778686
  38. Grb2 interaction with MEK-kinase 1 is involved in regulation of Jun-kinase activities in response to epidermal growth factor.
    J Biol Chem. 1998 Sep 18;273(38):24301-4 PMID: 9733714
  39. Neuronal position in the developing brain is regulated by mouse disabled-1.
    Nature. 1997 Oct 16;389(6652):733-7 PMID: 9338785
  40. Experimental autoimmune nephrosis in rats. Morphogenesis of the glomerular lesion: immunohistochemical and electron microscopic studies.
    Am J Pathol. 1969 Jan;54(1):47-71 PMID: 4178552
  41. 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):26172-80 PMID: 1464627
  42. Autoimmune target in Heymann nephritis is a glycoprotein with homology to the LDL receptor.
    Science. 1989 Jun 9;244(4909):1163-5 PMID: 2786251
  43. Regulation of rat DOC-2 gene during castration-induced rat ventral prostate degeneration and its growth inhibitory function in human prostatic carcinoma cells.
    Endocrinology. 1998 Aug;139(8):3542-53 PMID: 9681506
  44. Epithelial glycoprotein-330 mediates endocytosis of plasminogen activator-plasminogen activator inhibitor type-1 complexes.
    J Biol Chem. 1993 Aug 5;268(22):16564-70 PMID: 8344937
  45. Evidence for an essential role of megalin in transepithelial transport of retinol.
    J Am Soc Nephrol. 1999 Apr;10(4):685-95 PMID: 10203351
  46. Identification of the rat Heymann nephritis autoantigen (GP330) as a receptor site for plasminogen.
    J Biol Chem. 1991 Jun 15;266(17):10825-9 PMID: 1645711
  47. The pathogenic antigen of Heymann nephritis is a membrane glycoprotein of the renal proximal tubule brush border.
    Proc Natl Acad Sci U S A. 1982 Sep;79(18):5557-61 PMID: 6752952
  48. Megalin-mediated endocytosis of transcobalamin-vitamin-B12 complexes suggests a role of the receptor in vitamin-B12 homeostasis.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8612-7 PMID: 8710919
  49. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction.
    Cell. 1992 Jul 10;70(1):93-104 PMID: 1623525
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2000-05-01
Pages
613-21
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1220996
Subset
IM
Grants
NIDDK NIH HHS · DK 33941 · United States
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