Home LiteratureArticle Details
PMID: 1757463 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

An endogenous MDCK lysosomal membrane glycoprotein is targeted basolaterally before delivery to lysosomes.

The Journal of cell biology ·Vol. 115 ·No. 6 ·1991-12-00 ·Pages 1573-84

Nabi IR, Le Bivic A, Fambrough D, Rodriguez-Boulan E

Abstract

Using surface immunoprecipitation at 37 degrees C to "catch" the transient apical or basolateral appearance of an endogenous MDCK lysosomal membrane glycoprotein, the AC17 antigen, we demonstrate that the bulk of newly synthesized AC17 antigen is polarly targeted from the Golgi apparatus to the basolateral plasma membrane or early endosomes and is then transported to lysosomes via the endocytic pathway. The AC17 antigen exhibits very similar properties to members of the family of lysosomal-associated membrane glycoproteins (LAMPs). Parallel studies of an avian LAMP, LEP100, transfected into MDCK cells revealed colocalization of the two proteins to lysosomes, identical biosynthetic and degradation rates, and similar low levels of steady-state expression on both the apical (0.8%) and basolateral (2.1%) membranes. After treatment of the cells with chloroquine, newly synthesized AC17 antigen, while still initially targeted basolaterally, appears stably in both the apical and basolateral domains, consistent with the depletion of the AC17 antigen from lysosomes and its recycling in a nonpolar fashion to the cell surface.

MeSH Terms
Animals Antigens, CD Antigens, Surface/metabolism Biological Transport Cell Line Chloroquine/pharmacology Endocytosis Immunoenzyme Techniques Lysosome-Associated Membrane Glycoproteins Lysosomes/metabolism,ultrastructure Membrane Glycoproteins/metabolism Microscopy, Immunoelectron Precipitin Tests
Chemicals
Antigens, CD Antigens, Surface Lysosome-Associated Membrane Glycoproteins Membrane Glycoproteins Chloroquine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Nabi I R
Department of Cell Biology and Anatomy, Cornell University Medical College, New York 10021.
Le Bivic A
Fambrough D
Rodriguez-Boulan E
References (66)
66 references, click to expand
  1. A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits.
    Cell. 1988 Jun 3;53(5):743-52 PMID: 2897244
  2. A sorting signal for the basolateral delivery of the vesicular stomatitis virus (VSV) G protein lies in its luminal domain: analysis of the targeting of VSV G-influenza hemagglutinin chimeras.
    Proc Natl Acad Sci U S A. 1989 Jun;86(11):4112-6 PMID: 2542964
  3. Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins.
    J Cell Biol. 1987 Sep;105(3):1227-40 PMID: 2821012
  4. Polarized expression of a chimeric protein in which the transmembrane and cytoplasmic domains of the influenza virus hemagglutinin have been replaced by those of the vesicular stomatitis virus G protein.
    Proc Natl Acad Sci U S A. 1986 Dec;83(24):9318-22 PMID: 3025835
  5. An internalized transmembrane protein resides in a fusion-competent endosome for less than 5 minutes.
    Proc Natl Acad Sci U S A. 1987 Aug;84(16):5758-62 PMID: 3039505
  6. Polarized apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line.
    Proc Natl Acad Sci U S A. 1988 Dec;85(24):9557-61 PMID: 2974157
  7. Polarized delivery of viral glycoproteins to the apical and basolateral plasma membranes of Madin-Darby canine kidney cells infected with temperature-sensitive viruses.
    J Cell Biol. 1985 Jan;100(1):136-51 PMID: 2981229
  8. Apical membrane marker is expressed early in colonic epithelial cells.
    Biol Cell. 1987;60(3):209-16 PMID: 2962680
  9. The isolation and nucleotide sequence of a cDNA encoding the T cell surface protein T4: a new member of the immunoglobulin gene family.
    Cell. 1985 Aug;42(1):93-104 PMID: 2990730
  10. Molecular cloning of cDNAs encoding lamp A, a human lysosomal membrane glycoprotein with apparent Mr approximately equal to 120,000.
    Proc Natl Acad Sci U S A. 1988 Jun;85(11):3743-7 PMID: 3131762
  11. The low density lipoprotein receptor. Identification of amino acids in cytoplasmic domain required for rapid endocytosis.
    J Biol Chem. 1987 Mar 25;262(9):4075-82 PMID: 3104336
  12. Cycling of the integral membrane glycoprotein, LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis.
    Cell. 1987 Jun 5;49(5):669-77 PMID: 3107839
  13. Human lysosomal acid phosphatase is transported as a transmembrane protein to lysosomes in transfected baby hamster kidney cells.
    EMBO J. 1988 Aug;7(8):2351-8 PMID: 3056714
  14. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells.
    J Cell Biol. 1989 Nov;109(5):2145-56 PMID: 2478564
  15. Expression of macrophage-lymphocyte Fc receptors in Madin-Darby canine kidney cells: polarity and transcytosis differ for isoforms with or without coated pit localization domains.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3291-302 PMID: 2574723
  16. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells.
    Science. 1989 Sep 29;245(4925):1499-501 PMID: 2571189
  17. The biogenesis of lysosomes.
    Annu Rev Cell Biol. 1989;5:483-525 PMID: 2557062
  18. Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9313-7 PMID: 2687880
  19. Endocytosis in filter-grown Madin-Darby canine kidney cells.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3243-58 PMID: 2689455
  20. Polarized endocytosis by Madin-Darby canine kidney cells transfected with functional chicken liver glycoprotein receptor.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2809-16 PMID: 2687287
  21. Fusion accessibility of endocytic compartments along the recycling and lysosomal endocytic pathways in intact cells.
    J Cell Biol. 1989 Nov;109(5):2097-104 PMID: 2681226
  22. Morphogenesis of the polarized epithelial cell phenotype.
    Science. 1989 Aug 18;245(4919):718-25 PMID: 2672330
  23. Biogenesis of endogenous plasma membrane proteins in epithelial cells.
    Annu Rev Physiol. 1989;51:755-70 PMID: 2653204
  24. Lysosomal acid phosphatase is transported to lysosomes via the cell surface.
    EMBO J. 1989 Dec 1;8(12):3633-40 PMID: 2583113
  25. A new technique for the assay of infectivity of human adenovirus 5 DNA.
    Virology. 1973 Apr;52(2):456-67 PMID: 4705382
  26. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  27. Transferrin receptor polarity and recycling accuracy in "tight" and "leaky" strains of Madin-Darby canine kidney cells.
    J Cell Biol. 1986 Nov;103(5):1767-79 PMID: 2877994
  28. Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein.
    J Cell Biol. 1986 May;102(5):1593-605 PMID: 2871029
  29. Intracellular sorting and basolateral appearance of the G protein of vesicular stomatitis virus in Madin-Darby canine kidney cells.
    J Cell Biol. 1985 Aug;101(2):470-6 PMID: 2991300
  30. Cloning of cDNAs encoding human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Comparison of their deduced amino acid sequences.
    J Biol Chem. 1988 Dec 15;263(35):18920-8 PMID: 3198605
  31. Isolation and sequencing of a cDNA clone encoding lysosomal membrane glycoprotein mouse LAMP-1. Sequence similarity to proteins bearing onco-differentiation antigens.
    J Biol Chem. 1988 Jun 25;263(18):8754-8 PMID: 3379044
  32. Biogenesis of epithelial cell polarity: intracellular sorting and vectorial exocytosis of an apical plasma membrane glycoprotein.
    Cell. 1984 Dec;39(3 Pt 2):537-46 PMID: 6509551
  33. Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA.
    Cell. 1986 Aug 15;46(4):613-21 PMID: 3524859
  34. Sorting of an apical plasma membrane glycoprotein occurs before it reaches the cell surface in cultured epithelial cells.
    J Cell Biol. 1984 Dec;99(6):2131-9 PMID: 6501415
  35. Biogenesis of the rat hepatocyte plasma membrane in vivo: comparison of the pathways taken by apical and basolateral proteins using subcellular fractionation.
    J Cell Biol. 1987 Sep;105(3):1241-51 PMID: 3654750
  36. Accumulation of membrane glycoproteins in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail.
    J Cell Biol. 1990 Sep;111(3):955-66 PMID: 2391371
  37. Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization.
    J Cell Biol. 1990 Feb;110(2):283-94 PMID: 2298808
  38. Surface distribution of the mannose 6-phosphate receptors in epithelial Madin-Darby canine kidney cells.
    J Biol Chem. 1990 Jul 25;265(21):12629-35 PMID: 1973688
  39. Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells.
    J Cell Biol. 1990 Sep;111(3):987-1000 PMID: 2202740
  40. Polarity of endogenous and exogenous glycosyl-phosphatidylinositol-anchored membrane proteins in Madin-Darby canine kidney cells.
    J Cell Sci. 1990 May;96 ( Pt 1):143-9 PMID: 1973690
  41. Characterization and cloning of lgp110, a lysosomal membrane glycoprotein from mouse and rat cells.
    J Biol Chem. 1990 Jul 15;265(20):12036-43 PMID: 2142158
  42. Polarized sorting in epithelia.
    Cell. 1990 Jul 27;62(2):207-10 PMID: 2196994
  43. Polarized expression of functional rat liver asialoglycoprotein receptor in transfected Madin-Darby canine kidney cells.
    J Biol Chem. 1990 Jan 15;265(2):1216-24 PMID: 2404008
  44. Vectorial targeting of an endogenous apical membrane sialoglycoprotein and uvomorulin in MDCK cells.
    J Cell Biol. 1990 May;110(5):1533-9 PMID: 2335561
  45. The cDNA sequence of mouse LAMP-2. Evidence for two classes of lysosomal membrane glycoproteins.
    J Biol Chem. 1990 Mar 25;265(9):5008-13 PMID: 2318880
  46. Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2).
    Cell. 1990 Feb 9;60(3):429-37 PMID: 2302734
  47. Polarized assembly of enveloped viruses from cultured epithelial cells.
    Methods Enzymol. 1983;98:486-501 PMID: 6321907
  48. Phase separation of integral membrane proteins in Triton X-114 solution.
    J Biol Chem. 1981 Feb 25;256(4):1604-7 PMID: 6257680
  49. Intracellular transport of influenza virus hemagglutinin to the apical surface of Madin-Darby canine kidney cells.
    J Cell Biol. 1984 Jan;98(1):308-19 PMID: 6707094
  50. Iodination of proteins, glycoproteins, and peptides using a solid-phase oxidizing agent, 1,3,4,6-tetrachloro-3 alpha,6 alpha-diphenyl glycoluril (Iodogen).
    Anal Biochem. 1981 Oct;117(1):136-46 PMID: 7316186
  51. 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):4350-4 PMID: 388439
  52. Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate.
    Anal Biochem. 1979 Sep 15;98(1):132-5 PMID: 543547
  53. A technique for ultracryotomy of cell suspensions and tissues.
    J Cell Biol. 1973 May;57(2):551-65 PMID: 4121290
  54. Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line.
    J Cell Biol. 1990 Oct;111(4):1351-61 PMID: 1976637
  55. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin.
    J Cell Biol. 1991 Aug;114(3):413-21 PMID: 1860878
  56. An internal deletion in the cytoplasmic tail reverses the apical localization of human NGF receptor in transfected MDCK cells.
    J Cell Biol. 1991 Nov;115(3):607-18 PMID: 1655809
  57. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor.
    Cell. 1991 Jul 12;66(1):65-75 PMID: 2070419
  58. Targeting of a lysosomal membrane protein: a tyrosine-containing endocytosis signal in the cytoplasmic tail of lysosomal acid phosphatase is necessary and sufficient for targeting to lysosomes.
    EMBO J. 1990 Nov;9(11):3497-506 PMID: 2209556
  59. Derived protein sequence, oligosaccharides, and membrane insertion of the 120-kDa lysosomal membrane glycoprotein (lgp120): identification of a highly conserved family of lysosomal membrane glycoproteins.
    Proc Natl Acad Sci U S A. 1988 Oct;85(20):7577-81 PMID: 3174652
  60. Steady-state distribution and biogenesis of endogenous Madin-Darby canine kidney glycoproteins: evidence for intracellular sorting and polarized cell surface delivery.
    J Cell Biol. 1989 Nov;109(5):2117-27 PMID: 2808522
  61. Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3259-72 PMID: 2557351
  62. Intracellular movement of two mannose 6-phosphate receptors: return to the Golgi apparatus.
    J Cell Biol. 1988 Mar;106(3):617-28 PMID: 2964450
  63. The mannose 6-phosphate receptor and the biogenesis of lysosomes.
    Cell. 1988 Feb 12;52(3):329-41 PMID: 2964276
  64. Lysosomal enzymes and their receptors.
    Annu Rev Biochem. 1986;55:167-93 PMID: 2943218
  65. Structure of LEP100, a glycoprotein that shuttles between lysosomes and the plasma membrane, deduced from the nucleotide sequence of the encoding cDNA.
    J Cell Biol. 1988 Jan;106(1):61-7 PMID: 3339090
  66. The large external domain is sufficient for the correct sorting of secreted or chimeric influenza virus hemagglutinins in polarized monkey kidney cells.
    J Cell Biol. 1987 Mar;104(3):769-82 PMID: 3546337
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.115.6.1573
Published
1991-12-00
Pages
1573-84
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289220
Subset
IM
Grants
NIGMS NIH HHS · R01-GM34107 · United States
NINDS NIH HHS · R01-NS23241 · United States
External Links
PubMed source DOI: 10.1083/jcb.115.6.1573 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2