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PMID: 7512501 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Release of GPI-anchored membrane proteins by a cell-associated GPI-specific phospholipase D.

The EMBO journal ·Vol. 13 ·No. 7 ·1994-04-01 ·Pages 1741-51

Metz CN, Brunner G, Choi-Muira NH, Nguyen H, Gabrilove J, Caras IW, Altszuler N, Rifkin DB, Wilson EL, Davitz MA

Abstract

Although many glycosylphosphatidylinositol (GPI)-anchored proteins have been observed as soluble forms, the mechanisms by which they are released from the cell surface have not been demonstrated. We show here that a cell-associated GPI-specific phospholipase D (GPI-PLD) releases the GPI-anchored, complement regulatory protein decay-accelerating factor (DAF) from HeLa cells, as well as the basic fibroblast growth factor-binding heparan sulfate proteoglycan from bone marrow stromal cells. DAF found in the HeLa cell culture supernatants contained both [3H]ethanolamine and [3H]inositol, but not [3H]palmitic acid, whereas the soluble heparan sulfate proteoglycan present in bone marrow stromal cell culture supernatants contained [3H]ethanolamine. 125I-labeled GPI-DAF incorporated into the plasma membranes of these two cell types was released in a soluble form lacking the fatty acid GPI-anchor component. GPI-PLD activity was detected in lysates of both HeLa and bone marrow stromal cells. Treatment of HeLa cells with 1,10-phenanthroline, an inhibitor of GPI-PLD, reduced the release of [3H]ethanolamine-DAF by 70%. The hydrolysis of these GPI-anchored molecules is likely to be mediated by an endogenous GPI-PLD because [3H]ethanolamine DAF is constitutively released from HeLa cells maintained in serum-free medium. Furthermore, using PCR, a GPI-PLD mRNA has been identified in cDNA libraries prepared from both cell types. These studies are the first demonstration of the physiologically relevant release of GPI-anchored proteins from cells by a GPI-PLD.

MeSH Terms
Antigens, CD/metabolism Bone Marrow/enzymology Bone Marrow Cells CD55 Antigens DNA, Complementary/genetics Ethanolamine Ethanolamines/metabolism Gene Library Glycosylphosphatidylinositols/metabolism HeLa Cells/enzymology Heparan Sulfate Proteoglycans Heparitin Sulfate/metabolism Humans Inositol/metabolism Membrane Glycoproteins/metabolism Phenanthrolines/pharmacology Phospholipase D/antagonists & inhibitors,genetics,metabolism Proteoglycans/metabolism RNA, Messenger/genetics
Chemicals
Antigens, CD CD55 Antigens DNA, Complementary Ethanolamines Glycosylphosphatidylinositols Heparan Sulfate Proteoglycans Membrane Glycoproteins Phenanthrolines Proteoglycans RNA, Messenger Inositol Ethanolamine Heparitin Sulfate Phospholipase D glycoprotein phospholipase D 1,10-phenanthroline
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Metz C N
Department of Pathology, New York University Medical Center, NY 10016.
Brunner G
Choi-Muira N H
Nguyen H
Gabrilove J
Caras I W
Altszuler N
Rifkin D B
Wilson E L
Davitz M A
References (57)
57 references, click to expand
  1. A phospholipase C from Trypanosoma brucei which selectively cleaves the glycolipid on the variant surface glycoprotein.
    J Biol Chem. 1986 Oct 15;261(29):13813-9 PMID: 3759991
  2. Growth factor-like action of phosphatidic acid.
    Nature. 1986 Sep 11-17;323(6084):171-3 PMID: 3748188
  3. Conversion of human placental alkaline phosphatase from a high Mr form to a low Mr form during butanol extraction. An investigation of the role of endogenous phosphoinositide-specific phospholipases.
    Biochem J. 1986 Dec 1;240(2):519-27 PMID: 3028377
  4. Isolation of decay accelerating factor (DAF) by a two-step procedure and determination of its N-terminal sequence.
    J Immunol Methods. 1987 Feb 26;97(1):71-6 PMID: 2434569
  5. Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids.
    J Exp Med. 1987 Mar 1;165(3):848-64 PMID: 2434600
  6. Decay-accelerating factor (DAF): a review of its function and structure.
    Acta Med Scand Suppl. 1987;715:111-21 PMID: 2438906
  7. A glycan-phosphatidylinositol-specific phospholipase D in human serum.
    Science. 1987 Oct 2;238(4823):81-4 PMID: 2443973
  8. Biosynthesis, membrane association, and release of N-CAM-120, a phosphatidylinositol-linked form of the neural cell adhesion molecule.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2489-500 PMID: 3693391
  9. A phospholipase D specific for the phosphatidylinositol anchor of cell-surface proteins is abundant in plasma.
    Proc Natl Acad Sci U S A. 1988 Feb;85(4):980-4 PMID: 3422494
  10. Partial characterization of the cross-reacting determinant, a carbohydrate epitope shared by decay accelerating factor and the variant surface glycoprotein of the African Trypanosoma brucei.
    J Immunol. 1988 Mar 15;140(6):2046-50 PMID: 2450138
  11. Characterization of a hydrophilic form of Thy-1 purified from human cerebrospinal fluid.
    J Biol Chem. 1988 Sep 5;263(25):12709-15 PMID: 2900838
  12. Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation.
    J Cell Biol. 1988 Aug;107(2):743-51 PMID: 2971068
  13. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures.
    Annu Rev Biochem. 1988;57:285-320 PMID: 3052274
  14. Decay-accelerating factor: biochemistry, molecular biology, and function.
    Annu Rev Immunol. 1989;7:35-58 PMID: 2469439
  15. Purification of a glycosyl-phosphatidylinositol-specific phospholipase D from human plasma.
    J Biol Chem. 1989 Aug 15;264(23):13760-4 PMID: 2760042
  16. Endocytosis and shedding of the decay accelerating factor on human polymorphonuclear cells.
    J Immunol. 1989 Nov 15;143(10):3295-302 PMID: 2478622
  17. The glycosyl-phosphatidylinositol anchor of membrane proteins.
    Biochim Biophys Acta. 1989 Dec 6;988(3):427-54 PMID: 2531614
  18. Release of basic fibroblast growth factor-heparan sulfate complexes from endothelial cells by plasminogen activator-mediated proteolytic activity.
    J Cell Biol. 1990 Mar;110(3):767-75 PMID: 2137829
  19. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity.
    Cell. 1990 Apr 6;61(1):157-70 PMID: 2317872
  20. Detection of a phosphatidylinositol-specific phospholipase C at the surface of Swiss 3T3 cells and its potential role in the regulation of cell growth.
    J Biol Chem. 1990 Apr 5;265(10):5337-40 PMID: 2156813
  21. Dynamics and longevity of the glycolipid-anchored membrane protein, Thy-1.
    J Cell Biol. 1990 May;110(5):1525-31 PMID: 1970823
  22. Fatty acid remodeling: a novel reaction sequence in the biosynthesis of trypanosome glycosyl phosphatidylinositol membrane anchors.
    Cell. 1990 Jul 13;62(1):73-80 PMID: 1694728
  23. Drosophila fasciclin I, a neural cell adhesion molecule, has a phosphatidylinositol lipid membrane anchor that is developmentally regulated.
    J Biol Chem. 1990 Sep 5;265(25):15104-9 PMID: 2394715
  24. Purification and characterization of glycosyl-phosphatidylinositol-specific phospholipase D.
    J Biol Chem. 1990 Oct 15;265(29):17738-45 PMID: 2170394
  25. "Pure" human hematopoietic progenitors: permissive action of basic fibroblast growth factor.
    Science. 1990 Sep 28;249(4976):1561-4 PMID: 2218497
  26. Characterization of soluble vs membrane-bound human placental 5'-nucleotidase.
    Biochem Biophys Res Commun. 1990 Nov 15;172(3):1371-7 PMID: 2173922
  27. Glycophospholipid membrane anchor attachment. Molecular analysis of the cleavage/attachment site.
    J Biol Chem. 1991 Jan 15;266(2):1250-7 PMID: 1824699
  28. Glycolipid anchoring of plasma membrane proteins.
    Annu Rev Cell Biol. 1990;6:1-39 PMID: 2148872
  29. The conversion of the human membrane-associated folate binding protein (folate receptor) to the soluble folate binding protein by a membrane-associated metalloprotease.
    J Biol Chem. 1991 Feb 5;266(4):2346-53 PMID: 1846624
  30. Basic fibroblast growth factor stimulates myelopoiesis in long-term human bone marrow cultures.
    Blood. 1991 Mar 1;77(5):954-60 PMID: 1995102
  31. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor.
    Cell. 1991 Feb 22;64(4):841-8 PMID: 1847668
  32. Primary structure and functional activity of a phosphatidylinositol-glycan-specific phospholipase D.
    Science. 1991 Apr 19;252(5004):446-8 PMID: 2017684
  33. Basic fibroblast growth factor (B-FGF) induces early- (CFU-s) and late-stage hematopoietic progenitor cell colony formation (CFU-gm, CFU-meg, and BFU-e) by synergizing with GM-CSF, Meg-CSF, and erythropoietin, and is a radioprotective agent in vitro.
    Int J Cell Cloning. 1991 May;9(3):220-32 PMID: 2061622
  34. Shedding as a mechanism of down-modulation of CD14 on stimulated human monocytes.
    J Immunol. 1991 Sep 1;147(5):1567-74 PMID: 1880416
  35. Phospholipase C release of basic fibroblast growth factor from human bone marrow cultures as a biologically active complex with a phosphatidylinositol-anchored heparan sulfate proteoglycan.
    J Cell Biol. 1991 Sep;114(6):1275-83 PMID: 1654337
  36. Production of the glycosylphosphatidylinositol-specific phospholipase D by the islets of Langerhans.
    J Biol Chem. 1991 Sep 25;266(27):17733-6 PMID: 1833386
  37. Multiple targets for brefeldin A.
    Cell. 1991 Nov 1;67(3):449-51 PMID: 1934055
  38. Factors affecting the ability of glycosylphosphatidylinositol-specific phospholipase D to degrade the membrane anchors of cell surface proteins.
    Biochem J. 1991 Oct 15;279 ( Pt 2):483-93 PMID: 1835378
  39. A soluble form of the F3 neuronal cell adhesion molecule promotes neurite outgrowth.
    J Cell Biol. 1992 May;117(4):877-87 PMID: 1315782
  40. Phosphatidic acid that accumulates in platelet-derived growth factor-stimulated Balb/c 3T3 cells is a potential mitogenic signal.
    J Biol Chem. 1992 Jun 5;267(16):10988-93 PMID: 1597441
  41. Phosphatidylinositol-glycan-specific phospholipase D is an amphiphilic glycoprotein that in serum is associated with high-density lipoproteins.
    Eur J Biochem. 1992 Jun 15;206(3):747-57 PMID: 1606959
  42. Spontaneous incorporation of the glycosyl-phosphatidylinositol-linked protein Thy-1 into cell membranes.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5231-5 PMID: 1351678
  43. Human recombinant soluble decay accelerating factor inhibits complement activation in vitro and in vivo.
    J Immunol. 1992 Sep 1;149(5):1736-43 PMID: 1380537
  44. New insights into the regulation of megakaryocytopoiesis by haematopoietic and fibroblastic growth factors and transforming growth factor beta 1.
    Br J Haematol. 1992 May;81(1):1-5 PMID: 1520606
  45. Colworth Medal Lecture. Glycosyl-phosphatidylinositol membrane anchors: the tale of a tail.
    Biochem Soc Trans. 1992 May;20(2):243-56 PMID: 1397606
  46. Formation of haematopoietic microenvironment and haematopoietic stem cells from single human bone marrow stem cells.
    Nature. 1992 Dec 24-31;360(6406):745-9 PMID: 1281519
  47. Basic fibroblast growth factor expression in human bone marrow and peripheral blood cells.
    Blood. 1993 Feb 1;81(3):631-8 PMID: 8427958
  48. Basic fibroblast growth factor promotes the proliferation of human megakaryocyte progenitor cells.
    Blood. 1993 Jul 15;82(2):430-5 PMID: 8329701
  49. Phase separation of integral membrane proteins in Triton X-114 solution.
    J Biol Chem. 1981 Feb 25;256(4):1604-7 PMID: 6257680
  50. Stromal cell associated haemopoiesis.
    J Cell Physiol Suppl. 1982;1:87-94 PMID: 7040421
  51. Monensin inhibits recycling of macrophage mannose-glycoprotein receptors and ligand delivery to lysosomes.
    Biochem J. 1984 Jun 15;220(3):665-75 PMID: 6087792
  52. Inhibition of complement activation on the surface of cells after incorporation of decay-accelerating factor (DAF) into their membranes.
    J Exp Med. 1984 Nov 1;160(5):1558-78 PMID: 6238120
  53. Distribution of decay-accelerating factor in the peripheral blood of normal individuals and patients with paroxysmal nocturnal hemoglobinuria.
    J Exp Med. 1985 Jul 1;162(1):75-92 PMID: 2409211
  54. Receptor-mediated endocytosis.
    Biochem J. 1985 Nov 15;232(1):1-14 PMID: 2867759
  55. Endogenous association of decay-accelerating factor (DAF) with C4b and C3b on cell membranes.
    J Immunol. 1986 May 1;136(9):3390-5 PMID: 2420889
  56. Identification of amine components in a glycolipid membrane-binding domain at the C-terminus of human erythrocyte acetylcholinesterase.
    Biochemistry. 1986 Jun 3;25(11):3098-105 PMID: 3524671
  57. The synthesis and turnover of 5'-nucleotidase in primary cultured hepatocytes.
    Biochim Biophys Acta. 1987 Jan 19;927(1):81-5 PMID: 3024739
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1994-04-01
Pages
1741-51
Language
English
Region
England
NLM ID
8208664
PMCID
PMC395007
Subset
IM
Grants
NCI NIH HHS · CA 34282 · United States
NCI NIH HHS · CA 49419 · United States
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