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PMID: 7490295 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A transferrin-like GPI-linked iron-binding protein in detergent-insoluble noncaveolar microdomains at the apical surface of fetal intestinal epithelial cells.

The Journal of cell biology ·Vol. 131 ·No. 4 ·1995-11-00 ·Pages 939-50

Danielsen EM, van Deurs B

Abstract

A GPI-anchored 80-kD protein was found to be the major component of detergent-insoluble complexes, prepared from fetal porcine small intestine, constituting about 25% of the total amount of protein. An antibody was raised to the 80-kD protein, and by immunogold electron microscopy of ultracryosections of mucosal tissue, the protein was localized to the apical surface of the enterocytes, whereas it was absent from the basolateral plasma membrane. Interestingly, it was mainly found in patches of flat or invaginated apical membrane domains rather than at the surface of microvilli. Caveolae were not found in association with these labeled microdomains. In addition, the 80-kD protein was seen in apical endocytic vacuoles and in tubulo-vesicular structures, suggesting that the apical microdomains are involved in endocytosis of the 80-kD protein. By its NH2-terminal amino acid sequence, iron-binding capacity and partial immunological cross-reactivity with serum transferrin, the 80-kD protein was shown to belong to the transferrin family, and it is probably homologous to melanotransferrin, a human melanoma-associated antigen. The 80-kD iron-binding protein was fully detergent-soluble immediately after synthesis and only became insoluble after gaining resistance to endo H, supporting a mechanism for exocytic delivery to the apical cell surface by way of detergent-insoluble glycolipid "rafts" that fuse with the plasmalemma at restricted sites devoid of microvilli.

MeSH Terms
Age Factors Amino Acid Sequence Animals Carrier Proteins/analysis,chemistry,physiology Cell Compartmentation/physiology Detergents Endosomes/chemistry Epithelial Cells Epithelium/chemistry,embryology Fetus/physiology Gene Expression Regulation, Developmental/physiology Glycosylphosphatidylinositols/analysis,chemistry,physiology Immunoelectrophoresis Intestine, Small/chemistry,cytology,embryology Iron/metabolism Iron-Binding Proteins Membrane Proteins/analysis,genetics Microscopy, Electron Microvilli/chemistry Molecular Sequence Data Molecular Weight Solubility Swine Transferrin/analysis,chemistry,physiology Transferrin-Binding Proteins
Chemicals
Carrier Proteins Detergents Glycosylphosphatidylinositols Iron-Binding Proteins Membrane Proteins Transferrin Transferrin-Binding Proteins Iron
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Danielsen E M
Department of Medical Biochemistry and Genetics, Panum Institute, University of Copenhagen, Denmark.
van Deurs B
References (46)
46 references, click to expand
  1. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles.
    J Cell Biol. 1992 Sep;118(5):1003-14 PMID: 1512286
  2. Guilty by insolubility--does a protein's detergent insolubility reflect a caveolar location?
    Trends Cell Biol. 1995 May;5(5):187-9 PMID: 14731445
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels.
    Eur J Biochem. 1974 Jul 1;46(1):83-8 PMID: 4850204
  5. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment.
    Mol Biol Cell. 1995 Jul;6(7):929-44 PMID: 7579703
  6. Human melanoma-associated antigen p97 is structurally and functionally related to transferrin.
    Nature. 1982 Mar 11;296(5853):171-3 PMID: 7063021
  7. Interactions between GPI-anchored proteins and membrane lipids.
    Trends Cell Biol. 1992 Nov;2(11):338-43 PMID: 14731512
  8. Quantitative analysis of melanoma-associated antigen p97 in normal and neoplastic tissues.
    Proc Natl Acad Sci U S A. 1981 Jan;78(1):539-43 PMID: 6165996
  9. The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures.
    Annu Rev Cell Biol. 1992;8:157-95 PMID: 1476799
  10. The membrane form of variant surface glycoproteins of Trypanosoma brucei.
    Nature. 1983 Mar 24-30;302(5906):349-52 PMID: 6188057
  11. The urokinase-type plasminogen activator receptor, a GPI-linked protein, is localized in caveolae.
    J Cell Biol. 1995 Apr;129(2):335-44 PMID: 7721938
  12. Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin.
    J Cell Biol. 1995 May;129(3):619-27 PMID: 7537273
  13. Potocytosis: sequestration and transport of small molecules by caveolae.
    Science. 1992 Jan 24;255(5043):410-1 PMID: 1310359
  14. Determination of amino acid compositions and NH2-terminal sequences of peptides electroblotted onto PVDF membranes from tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis: application to peptide mapping of human complement component C3.
    Anal Biochem. 1989 Aug 15;181(1):33-9 PMID: 2817381
  15. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae.
    J Biol Chem. 1994 Dec 9;269(49):30745-8 PMID: 7982998
  16. Nucleotide sequence of porcine liver transferrin.
    Nucleic Acids Res. 1988 Sep 12;16(17):8720 PMID: 3419934
  17. Selective antibody transport in the proximal small intestine of the neonatal rat.
    J Cell Biol. 1970 Jun;45(3):635-40 PMID: 5459946
  18. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface.
    Cell. 1992 Feb 7;68(3):533-44 PMID: 1531449
  19. Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells.
    J Cell Biol. 1993 Jan;120(2):353-8 PMID: 8380601
  20. Are caveolae involved in clathrin-independent endocytosis?
    Trends Cell Biol. 1993 Aug;3(8):249-51 PMID: 14731741
  21. Lactoferrin, lactoferrin receptors and iron metabolism.
    Eur J Clin Nutr. 1993 Apr;47(4):232-41 PMID: 8491159
  22. Uptake of maternal immunoglobulins in the enterocytes of suckling piglets: improved detection with a streptavidin-biotin bridge gold technique.
    J Histochem Cytochem. 1992 Nov;40(11):1637-46 PMID: 1431052
  23. Purification and characterization of smooth muscle cell caveolae.
    J Cell Biol. 1994 Jul;126(1):127-38 PMID: 8027172
  24. Primary structure of the human melanoma-associated antigen p97 (melanotransferrin) deduced from the mRNA sequence.
    Proc Natl Acad Sci U S A. 1986 Mar;83(5):1261-5 PMID: 2419904
  25. Comparison of transferrin sequences from different species.
    Comp Biochem Physiol B. 1993 Sep;106(1):203-18 PMID: 8403849
  26. Early stages of intestinal absorption of specific antibiodies in the newborn. An ultrastructural, cytochemical, and immunological study in the pig, rat, and rabbit.
    J Cell Biol. 1969 Aug;42(2):345-65 PMID: 5815502
  27. Molecules internalized by clathrin-independent endocytosis are delivered to endosomes containing transferrin receptors.
    J Cell Biol. 1993 Oct;123(1):89-97 PMID: 8408209
  28. Caveolae and sorting in the trans-Golgi network of epithelial cells.
    EMBO J. 1993 Apr;12(4):1597-605 PMID: 8385608
  29. Biosynthesis of intestinal microvillar proteins. Characterization of intestinal explants in organ culture and evidence for the existence of pro-forms of the microvillar enzymes.
    Biochem J. 1982 Mar 15;202(3):647-54 PMID: 7092836
  30. Sphingolipid trafficking--sorted out?
    Trends Cell Biol. 1992 Nov;2(11):332-7 PMID: 14731511
  31. Transport and expression in human melanomas of a transferrin-like glycosylphosphatidylinositol-anchored protein.
    J Biol Chem. 1994 Jan 28;269(4):3034-40 PMID: 8300636
  32. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells.
    EMBO J. 1994 Jan 1;13(1):42-53 PMID: 8306971
  33. Involvement of detergent-insoluble complexes in the intracellular transport of intestinal brush border enzymes.
    Biochemistry. 1995 Feb 7;34(5):1596-605 PMID: 7849019
  34. Human melanotransferrin (p97) has only one functional iron-binding site.
    FEBS Lett. 1992 Feb 24;298(2-3):215-8 PMID: 1544447
  35. Regulated internalization of caveolae.
    J Cell Biol. 1994 Dec;127(5):1199-215 PMID: 7962085
  36. Caveolin, a protein component of caveolae membrane coats.
    Cell. 1992 Feb 21;68(4):673-82 PMID: 1739974
  37. Biosynthesis of intestinal microvillar proteins. Pulse-chase labelling studies on aminopeptidase N and sucrase-isomaltase.
    Biochem J. 1982 Jun 15;204(3):639-45 PMID: 6127070
  38. The effect of dexamethasone on the development of rat intestinal brush border enzymes in organ culture.
    Dev Biol. 1980 Jan;74(1):9-21 PMID: 6765934
  39. Microvillus membrane vesicles from pig small intestine. Purity and lipid composition.
    Biochim Biophys Acta. 1981 Oct 2;647(2):188-95 PMID: 6170331
  40. Identification of a cell surface protein, p97, in human melanomas and certain other neoplasms.
    Proc Natl Acad Sci U S A. 1980 Apr;77(4):2183-7 PMID: 6929544
  41. Purification of the human intestinal brush border membrane.
    Biochim Biophys Acta. 1973 Sep 27;323(1):98-112 PMID: 4356391
  42. Characterization of the cross-reacting determinant (CRD) of the glycosyl-phosphatidylinositol membrane anchor of Trypanosoma brucei variant surface glycoprotein.
    Eur J Biochem. 1988 Oct 1;176(3):527-34 PMID: 2458923
  43. Biogenesis of the apical endosome-lysosome complex during differentiation of absorptive epithelial cells in rat ileum.
    J Cell Sci. 1991 Sep;100 ( Pt 1):133-43 PMID: 1795021
  44. A rapid method for the preparation of microvilli from rabbit kidney.
    Biochem J. 1974 Sep;142(3):575-81 PMID: 4464842
  45. Nucleotide and primary amino acid sequence of porcine lactoferrin.
    Biochim Biophys Acta. 1992 Aug 17;1132(1):97-9 PMID: 1511016
  46. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells.
    J Cell Biol. 1993 Aug;122(4):789-807 PMID: 8349730
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1995-11-00
Pages
939-50
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2199996
Subset
IM
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