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PMID: 2432074 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transport of a fluorescent macromolecule via endosomes to the vacuole in Saccharomyces cerevisiae.

The Journal of cell biology ·Vol. 104 ·No. 1 ·1987-01-00 ·Pages 67-75

Makarow M, Nevalainen LT

Abstract

Fluorescein isothiocyanate-conjugated dextran (FITC-dextran) is internalized by endocytosis into the lysosome-like vacuoles of Saccharomyces cerevisiae (Makarow, M., 1985, EMBO (Eur. Mol. Biol. Organ.) J. 4:1861-1866). Here we show that under energy depletion conditions FITC-dextran accumulated in a cytoplasmic compartment, from which it could be chased to the vacuole when the energy block was removed. The internal pH of the intermediate compartment under energy depletion was determined by fluorometry to be 5.8. The pH could be raised by the lysosomotropic agent ammonium chloride, the protonophore carbonyl cyanide p-trifluoromethoxyphenyl-hydrazone (CCCP) and the ATPase inhibitors dicyclohexylcarbodiimide (DCCD) and sodium vanadate. The pH of the vacuole was found to be 6.5. It was raised by ammonium chloride, CCCP, and DCCD, but not with sodium vanadate. Efrapeptin had no effect on the internal pH of either compartment. By dissecting the endocytic pathway, two portions of the route leading to the vacuole could be studied separately. The internalization of FITC-dextran from the extracellular fluid to the intermediate compartment followed linear kinetics, was independent of energy, and occurred at temperatures of between 15 degrees and 37 degrees C. Transfer of the marker from the intermediate compartment to the vacuole required energy, took place at temperatures between 19 degrees and 37 degrees C, and had a half-time of 7 min at 37 degrees C. Transport of the marker from the exterior of the cell to the vacuole did not require acidic pH values in the intermediate compartment or the vacuole. We suggest that the cytoplasmic compartment revealed by FITC-dextran, under energy depletion, represents the equivalent of the endosomes of mammalian cells.

MeSH Terms
Adenosine Triphosphatases/antagonists & inhibitors Ammonium Chloride/pharmacology Biological Transport, Active/drug effects Carbonyl Cyanide m-Chlorophenyl Hydrazone/pharmacology Cell Compartmentation Dextrans/metabolism Endocytosis Endosomes/metabolism Fluorescein-5-isothiocyanate Fluoresceins Hydrogen-Ion Concentration Kinetics Organoids/metabolism Saccharomyces cerevisiae/metabolism,ultrastructure Spectrometry, Fluorescence Temperature Thiocyanates Vacuoles/metabolism
Chemicals
Dextrans Fluoresceins Thiocyanates Ammonium Chloride Carbonyl Cyanide m-Chlorophenyl Hydrazone Adenosine Triphosphatases Fluorescein-5-isothiocyanate
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Makarow M
Nevalainen L T
References (48)
48 references, click to expand
  1. Yeast and mammals utilize similar cytosolic components to drive protein transport through the Golgi complex.
    Proc Natl Acad Sci U S A. 1986 Mar;83(6):1622-6 PMID: 3513182
  2. A novel prefusion complex formed during protein transport between Golgi cisternae in a cell-free system.
    J Biol Chem. 1986 Feb 15;261(5):2202-7 PMID: 3003101
  3. Three-dimensional structure of endosomes in BHK-21 cells.
    Proc Natl Acad Sci U S A. 1986 May;83(9):2899-903 PMID: 3458249
  4. Commentary. Lysosomotropic agents.
    Biochem Pharmacol. 1974 Sep 15;23(18):2495-531 PMID: 4606365
  5. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents.
    Proc Natl Acad Sci U S A. 1978 Jul;75(7):3327-31 PMID: 28524
  6. Adsorptive endocytosis of Semliki Forest virus.
    J Mol Biol. 1980 Sep 25;142(3):439-54 PMID: 7463480
  7. Fusion of Semliki forest virus with the plasma membrane can be induced by low pH.
    J Cell Biol. 1980 Oct;87(1):264-72 PMID: 7419594
  8. Characterization of the plasma membrane Mg2+-ATPase from the yeast, Saccharomyces cerevisiae.
    J Biol Chem. 1979 May 10;254(9):3326-32 PMID: 155066
  9. Vesicular transport of cationized ferritin by the epithelium of the rat choroid plexus.
    J Cell Biol. 1981 Apr;89(1):131-9 PMID: 7228898
  10. Studies on a mammalian hepatic binding protein specific for asialoglycoproteins. Evidence for receptor recycling in isolated rat hepatocytes.
    J Biol Chem. 1980 Apr 10;255(7):3008-13 PMID: 6244303
  11. Low temperature selectively inhibits fusion between pinocytic vesicles and lysosomes during heterophagy of 125I-asialofetuin by the perfused rat liver.
    J Biol Chem. 1980 Jun 25;255(12):5971-8 PMID: 6155379
  12. On the entry of Semliki forest virus into BHK-21 cells.
    J Cell Biol. 1980 Feb;84(2):404-20 PMID: 6991511
  13. Chloroquine inhibits lysosomal enzyme pinocytosis and enhances lysosomal enzyme secretion by impairing receptor recycling.
    J Cell Biol. 1980 Jun;85(3):839-52 PMID: 7190150
  14. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway.
    Cell. 1980 Aug;21(1):205-15 PMID: 6996832
  15. The receptosome: an intermediate organelle of receptor mediated endocytosis in cultured fibroblasts.
    Cell. 1980 Aug;21(1):67-77 PMID: 6157480
  16. The galactose-specific recognition system of mammalian liver: the route of ligand internalization in rat hepatocytes.
    Cell. 1980 Aug;21(1):79-93 PMID: 7407914
  17. Membrane recycling by coated vesicles.
    Annu Rev Biochem. 1981;50:85-101 PMID: 7023370
  18. Properties of H+-translocating adenosine triphosphatase in vacuolar membranes of SAccharomyces cerevisiae.
    J Biol Chem. 1981 Nov 10;256(21):10859-63 PMID: 6116710
  19. Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances.
    J Cell Biol. 1981 Sep;90(3):656-64 PMID: 7287819
  20. Exocytosis of pinocytosed fluid in cultured cells: kinetic evidence for rapid turnover and compartmentation.
    J Cell Biol. 1981 Dec;91(3 Pt 1):716-27 PMID: 7328118
  21. Rapid acidification of endocytic vesicles containing alpha 2-macroglobulin.
    Cell. 1982 Mar;28(3):643-51 PMID: 6176331
  22. Identification and characterization of a proton pump on lysosomes by fluorescein-isothiocyanate-dextran fluorescence.
    Proc Natl Acad Sci U S A. 1982 May;79(9):2758-62 PMID: 6178109
  23. Weak bases and ionophores rapidly and reversibly raise the pH of endocytic vesicles in cultured mouse fibroblasts.
    J Cell Biol. 1982 Nov;95(2 Pt 1):676-81 PMID: 6183281
  24. Receptor-mediated endocytosis of transferrin and the uptake of fe in K562 cells: identification of a nonlysosomal acidic compartment.
    Proc Natl Acad Sci U S A. 1982 Oct;79(20):6186-90 PMID: 6292894
  25. Endocytosis and the recycling of plasma membrane.
    J Cell Biol. 1983 Jan;96(1):1-27 PMID: 6298247
  26. Serial-section analysis of coated pits and vesicles involved in adsorptive pinocytosis in cultured fibroblasts.
    J Cell Biol. 1983 Jan;96(1):277-81 PMID: 6131075
  27. Recycling receptors: the round-trip itinerary of migrant membrane proteins.
    Cell. 1983 Mar;32(3):663-7 PMID: 6299572
  28. Penetration of Semliki Forest virus from acidic prelysosomal vacuoles.
    Cell. 1983 Mar;32(3):931-40 PMID: 6831562
  29. pH and the recycling of transferrin during receptor-mediated endocytosis.
    Proc Natl Acad Sci U S A. 1983 Apr;80(8):2258-62 PMID: 6300903
  30. Binding of apotransferrin to K562 cells: explanation of the transferrin cycle.
    Proc Natl Acad Sci U S A. 1983 Apr;80(8):2263-6 PMID: 6300904
  31. Acidification of macrophage and fibroblast endocytic vesicles in vitro.
    Proc Natl Acad Sci U S A. 1983 Jun;80(11):3334-8 PMID: 6190176
  32. Transepithelial transport of a viral membrane glycoprotein implanted into the apical plasma membrane of Madin-Darby canine kidney cells. I. Morphological evidence.
    J Cell Biol. 1983 Sep;97(3):627-37 PMID: 6885914
  33. Rapid acidification of endocytic vesicles containing asialoglycoprotein in cells of a human hepatoma line.
    J Cell Biol. 1983 Dec;97(6):1762-76 PMID: 6315742
  34. Identification of coated vesicles in Saccharomyces cerevisiae.
    J Cell Biol. 1984 Jan;98(1):341-6 PMID: 6368570
  35. Temperature-dependent internalization of virus glycoproteins in cells infected with a mutant of Semliki Forest virus.
    EMBO J. 1982;1(2):191-6 PMID: 6765172
  36. Endosome pH measured in single cells by dual fluorescence flow cytometry: rapid acidification of insulin to pH 6.
    J Cell Biol. 1984 May;98(5):1757-62 PMID: 6144684
  37. Uncoating of influenza virus in endosomes.
    J Virol. 1984 Aug;51(2):497-504 PMID: 6431119
  38. Transcytosis of the G protein of vesicular stomatitis virus after implantation into the apical plasma membrane of Madin-Darby canine kidney cells. I. Involvement of endosomes and lysosomes.
    J Cell Biol. 1984 Sep;99(3):796-82 PMID: 6088557
  39. Recycling of the asialoglycoprotein receptor in isolated rat hepatocytes. ATP depletion blocks receptor recycling but not a single round of endocytosis.
    J Biol Chem. 1985 Jan 10;260(1):128-33 PMID: 3965443
  40. Semliki Forest virus penetration from endosomes: a morphological study.
    Biol Cell. 1984;51(2):181-5 PMID: 6240300
  41. Purification and properties of H+-translocating, Mg2+-adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae.
    J Biol Chem. 1985 Jan 25;260(2):1090-5 PMID: 2857169
  42. Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change.
    J Biol Chem. 1985 Mar 10;260(5):2973-81 PMID: 3972812
  43. Endocytosis in yeast: several of the yeast secretory mutants are defective in endocytosis.
    Cell. 1985 Apr;40(4):1001-9 PMID: 3886157
  44. Endocytosis in Saccharomyces cerevisiae: internalization of enveloped viruses into spheroplasts.
    EMBO J. 1985 Jul;4(7):1855-60 PMID: 2992948
  45. Endocytosis in Saccharomyces cerevisiae: internalization of alpha-amylase and fluorescent dextran into cells.
    EMBO J. 1985 Jul;4(7):1861-6 PMID: 2411550
  46. A test of clathrin function in protein secretion and cell growth.
    Science. 1985 Nov 29;230(4729):1009-14 PMID: 2865811
  47. Reconstitution of an endocytic fusion event in a cell-free system.
    Cell. 1985 Dec;43(3 Pt 2):643-52 PMID: 4075403
  48. Interorganelle transfer and glycosylation of yeast invertase in vitro.
    Proc Natl Acad Sci U S A. 1986 Apr;83(7):2017-21 PMID: 2421286
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1987-01-00
Pages
67-75
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2117040
Subset
IM
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