Home LiteratureArticle Details
PMID: 1400573 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The morphology but not the function of endosomes and lysosomes is altered by brefeldin A.

The Journal of cell biology ·Vol. 119 ·No. 2 ·1992-10-00 ·Pages 273-85

Wood SA, Brown WJ

Abstract

Brefeldin A (BFA) induces the formation of an extensively fused network of membranes derived from the trans-Golgi network (TGN) and early endosomes (EE). We describe in detail here the unaffected passage of endocytosed material through the fused TGN/EE compartments to lysosomes in BFA-treated cells. We also confirmed that BFA caused the formation of tubular lysosomes, although the kinetics and extent of tubulation varied greatly between different cell types. The BFA-induced tubular lysosomes were often seen to form simple networks. Formation of tubular lysosomes was microtubule-mediated and energy-dependent; interestingly, however, maintenance of the tubulated lysosomes only required microtubules and was insensitive to energy poisons. Upon removal of BFA, the tubular lysosomes rapidly recovered in an energy-dependent process. In most cell types examined, the extensive TGN/EE network is ephemeral, eventually collapsing into a compact cluster of tubulo-vesicular membranes in a process that precedes the formation of tubular lysosomes. However, in primary bovine testicular cells, the BFA-induced TGN/EE network was remarkably stable (for > 12 h). During this time, the TGN/EE network coexisted with tubular lysosomes, however, the two compartments remained completely separate. These results show that BFA has multiple, profound effects on the morphology of various compartments of the endosome-lysosome system. In spite of these changes, endocytic traffic can continue through the altered compartments suggesting that transport occurs through noncoated vesicles or through vesicles that are insensitive to BFA.

MeSH Terms
Adenosine Triphosphate/metabolism Animals Anti-Bacterial Agents/pharmacology Biological Transport/drug effects,physiology Biomarkers Brefeldin A Cathepsin D/isolation & purification Cell Compartmentation Cells, Cultured Cyclopentanes/pharmacology Endocytosis/drug effects,physiology Energy Metabolism Humans Immunohistochemistry Kinetics Lysosomes/drug effects,physiology,ultrastructure Microtubules/physiology Organelles/drug effects,physiology,ultrastructure Subcellular Fractions
Chemicals
Anti-Bacterial Agents Biomarkers Cyclopentanes Brefeldin A Adenosine Triphosphate Cathepsin D
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Wood S A
Section of Biochemistry Molecular and Cell Biology, Cornell University, Ithaca, New York 14850.
Brown W J
References (35)
35 references, click to expand
  1. Late endosomes derive from early endosomes by maturation.
    Cell. 1991 May 3;65(3):417-27 PMID: 1850321
  2. Brefeldin A: insights into the control of membrane traffic and organelle structure.
    J Cell Biol. 1992 Mar;116(5):1071-80 PMID: 1740466
  3. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae.
    Cell. 1991 Mar 22;64(6):1183-95 PMID: 2004424
  4. Clathrin, adaptors, and sorting.
    Annu Rev Cell Biol. 1990;6:151-71 PMID: 2177341
  5. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway.
    Cell. 1990 Mar 9;60(5):821-36 PMID: 2178778
  6. Tubular lysosomes and their drug reactivity in cultured resident macrophages and in cell-free medium.
    Exp Cell Res. 1990 Oct;190(2):283-9 PMID: 2209729
  7. Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes.
    J Biol Chem. 1986 Aug 25;261(24):11398-403 PMID: 2426273
  8. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER.
    Cell. 1989 Mar 10;56(5):801-13 PMID: 2647301
  9. Immunoperoxidase methods for the localization of antigens in cultured cells and tissue sections by electron microscopy.
    Methods Cell Biol. 1989;31:553-69 PMID: 2674632
  10. The distribution of 215-kilodalton mannose 6-phosphate receptors within cis (heavy) and trans (light) Golgi subfractions varies in different cell types.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):9001-5 PMID: 2962195
  11. Tubular lysosome morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1921-5 PMID: 3550801
  12. Phorbol esters and horseradish peroxidase stimulate pinocytosis and redirect the flow of pinocytosed fluid in macrophages.
    J Cell Biol. 1985 Mar;100(3):851-9 PMID: 3972898
  13. Three-dimensional visualization of coated vesicle formation in fibroblasts.
    J Cell Biol. 1980 Mar;84(3):560-83 PMID: 6987244
  14. The arguments for pre-existing early and late endosomes.
    Trends Cell Biol. 1991 Jul;1(1):5-9 PMID: 14731803
  15. A mutation that impairs the ability of lipoprotein receptors to localise in coated pits on the cell surface of human fibroblasts.
    Nature. 1977 Dec 22-29;270(5639):695-9 PMID: 201867
  16. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes.
    Cell. 1991 Nov 1;67(3):591-600 PMID: 1657400
  17. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic.
    Cell. 1991 Nov 1;67(3):601-16 PMID: 1682055
  18. Molecular dissection of the secretory pathway.
    Nature. 1992 Jan 30;355(6359):409-15 PMID: 1734280
  19. Biosynthesis of lysosomal enzymes in cells of the End3 complementation group conditionally defective in endosomal acidification.
    Somat Cell Mol Genet. 1991 Mar;17(2):137-50 PMID: 1849319
  20. Endosomes can undergo an ATP-dependent density increase in the absence of dense lysosomes.
    Eur J Cell Biol. 1990 Apr;51(2):229-34 PMID: 1972063
  21. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells.
    Cell. 1990 Aug 24;62(4):719-31 PMID: 2143699
  22. Microtubule depolymerization inhibits transport of cathepsin D from the Golgi apparatus to lysosomes.
    J Cell Sci. 1990 Aug;96 ( Pt 4):711-20 PMID: 2178166
  23. Dissociation of a 110-kD peripheral membrane protein from the Golgi apparatus is an early event in brefeldin A action.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2295-306 PMID: 2277061
  24. The biogenesis of lysosomes.
    Annu Rev Cell Biol. 1989;5:483-525 PMID: 2557062
  25. Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein.
    J Cell Biol. 1986 May;102(5):1593-605 PMID: 2871029
  26. Translocation and clustering of endosomes and lysosomes depends on microtubules.
    J Cell Biol. 1987 Sep;105(3):1253-65 PMID: 3308906
  27. Unusual lysosomes in aortic smooth muscle cells: presence in living and rapidly frozen cells.
    J Cell Biol. 1986 May;102(5):1615-22 PMID: 3700469
  28. Maturation models for endosome and lysosome biogenesis.
    Trends Cell Biol. 1991 Oct;1(4):77-82 PMID: 14731781
  29. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators.
    Cell. 1992 Apr 3;69(1):129-38 PMID: 1555237
  30. Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes.
    J Cell Biol. 1992 Apr;117(2):301-10 PMID: 1560027
  31. 100-kD proteins of Golgi- and trans-Golgi network-associated coated vesicles have related but distinct membrane binding properties.
    J Cell Biol. 1992 Jun;117(6):1171-9 PMID: 1607381
  32. Effects of brefeldin A on the endocytic route. Redistribution of mannose 6-phosphate/insulin-like growth factor II receptors to the cell surface.
    J Biol Chem. 1991 Dec 25;266(36):24829-33 PMID: 1662218
  33. Radial extension of macrophage tubular lysosomes supported by kinesin.
    Nature. 1990 Aug 30;346(6287):864-6 PMID: 1697403
  34. PtK1 cells contain a nondiffusible, dominant factor that makes the Golgi apparatus resistant to brefeldin A.
    J Cell Biol. 1991 Jun;113(5):1009-23 PMID: 1710224
  35. Selective inhibition of transcytosis by brefeldin A in MDCK cells.
    Cell. 1991 Nov 1;67(3):617-27 PMID: 1934063
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1992-10-00
Pages
273-85
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289644
Subset
IM
Grants
NIDDK NIH HHS · DK37249 · United States
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