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PMID: 2170116 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Differential microtubule requirements for transcytosis in MDCK cells.

The EMBO journal ·Vol. 9 ·No. 11 ·1990-11-00 ·Pages 3515-25

Hunziker W, Mâle P, Mellman I

Abstract

Given the role of microtubules in directing the transport of many intracellular organelles, we investigated whether intact microtubules were also required for transcytosis across epithelia. Using polarized MDCK cells expressing receptors for the Fc domain of IgG (FcRII-B2) or polymeric immunoglobulin (pIg-R), we examined the involvement of microtubules in apical to basolateral and basolateral to apical transcytosis, respectively. While depolymerization of microtubules with nocodozole had no effect on apical to basolateral transcytosis via FcR, basolateral to apical transcytosis of dimeric IgA via pIg-R was almost completely blocked. Inhibition due to nocodozole was selective for basolateral to apical transcytosis, since neither endocytosis nor receptor recycling was significantly affected at either plasma membrane domain. As shown by confocal microscopy, the block in transcytosis was due to the inability of MDCK cells to translocate IgA-containing vesicles from the basolateral to the apical cytoplasm in the absence of an intact microtubule network. The nocodazole sensitive step could be partially by-passed, however, by allowing cells to internalize IgA at 17 degrees C prior to nocodazole treatment. Although incubation at 17 degrees C blocked release of IgA into the apical medium, it did not prevent translocation of IgA-containing vesicles to the apical cytoplasm. Thus, receptor-mediated transcytosis in opposite directions exhibits distinct requirements for microtubules, a feature which reflects the spatial organization of MDCK cells.

MeSH Terms
Animals Biological Transport/drug effects Cell Line Cell Membrane/metabolism Dogs Endocytosis/drug effects Epithelium/metabolism,ultrastructure Immunoglobulin A/metabolism In Vitro Techniques Intracellular Membranes/metabolism Kidney Microtubules/metabolism Nocodazole/pharmacology Organelles/physiology Receptors, Cell Surface/metabolism Receptors, Fc/metabolism
Chemicals
Immunoglobulin A Receptors, Cell Surface Receptors, Fc polymeric IgA Nocodazole
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hunziker W
Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06510.
Mâle P
Mellman I
References (43)
43 references, click to expand
  1. Internalization and rapid recycling of macrophage Fc receptors tagged with monovalent antireceptor antibody: possible role of a prelysosomal compartment.
    J Cell Biol. 1984 Apr;98(4):1163-9 PMID: 6715403
  2. Microtubules, membrane traffic, and cell organization.
    Cell. 1990 Apr 6;61(1):5-7 PMID: 2180584
  3. 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
  4. 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
  5. 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
  6. Microtubule distribution in cultured cells and intact tissues: improved immunolabeling resolution through the use of reversible embedment cytochemistry.
    Proc Natl Acad Sci U S A. 1985 Oct;82(20):6889-93 PMID: 3901009
  7. Autoregulation of tubulin synthesis in hepatocytes and fibroblasts.
    J Cell Biol. 1985 Nov;101(5 Pt 1):1763-72 PMID: 3902854
  8. Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitrocellulose filters.
    EMBO J. 1985 Nov;4(11):2781-92 PMID: 4065093
  9. Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity.
    J Cell Biol. 1986 May;102(5):1853-67 PMID: 2871031
  10. Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA.
    Cell. 1986 Aug 15;46(4):613-21 PMID: 3524859
  11. The trans Golgi network: sorting at the exit site of the Golgi complex.
    Science. 1986 Oct 24;234(4775):438-43 PMID: 2945253
  12. Microtubule-acting drugs lead to the nonpolarized delivery of the influenza hemagglutinin to the cell surface of polarized Madin-Darby canine kidney cells.
    J Cell Biol. 1987 Feb;104(2):231-41 PMID: 2879845
  13. Control of microtubule nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable detyrosinated microtubules.
    J Cell Biol. 1987 Sep;105(3):1283-96 PMID: 2888771
  14. Vesicle fusion and formation at the surface of pinocytic vacuoles in macrophages.
    J Cell Biol. 1968 Sep;38(3):629-32 PMID: 5664229
  15. The association of a class of saltatory movements with microtubules in cultured cells.
    J Cell Biol. 1970 May;45(2):334-54 PMID: 5513607
  16. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors.
    J Exp Med. 1979 Sep 19;150(3):580-96 PMID: 90108
  17. Synthesis of membrane glycoproteins in rat small-intestinal villus cells. Effect of colchicine on the redistribution of L-[1,5,6-3H]fucose-labelled membrane glycoproteins among Golgi, lateral basal and microvillus membranes.
    Biochem J. 1979 Jul 15;182(1):213-21 PMID: 496909
  18. Internalization and degradation of macrophage Fc receptors during receptor-mediated phagocytosis.
    J Cell Biol. 1983 Mar;96(3):887-95 PMID: 6833386
  19. Biosynthesis of intestinal microvillar proteins. Role of the Golgi complex and microtubules.
    Biochem J. 1983 Oct 15;216(1):37-42 PMID: 6651778
  20. Microtubule-depolymerizing agents inhibit asialo-orosomucoid delivery to lysosomes but not its endocytosis or degradation in isolated rat hepatocytes.
    Biochim Biophys Acta. 1983 Dec 19;763(4):368-76 PMID: 6652115
  21. A time-lapse video image intensification analysis of cytoplasmic organelle movements during endosome translocation.
    J Cell Biol. 1984 Feb;98(2):565-76 PMID: 6693496
  22. Intracellular receptor sorting during endocytosis: comparative immunoelectron microscopy of multiple receptors in rat liver.
    Cell. 1984 May;37(1):195-204 PMID: 6327050
  23. Cell surface polarity in epithelia.
    Annu Rev Cell Biol. 1985;1:243-88 PMID: 3939606
  24. The molecular biology of Gaucher disease and the potential for gene therapy.
    Cold Spring Harb Symp Quant Biol. 1986;51 Pt 2:1047-52 PMID: 3472751
  25. Translocation and clustering of endosomes and lysosomes depends on microtubules.
    J Cell Biol. 1987 Sep;105(3):1253-65 PMID: 3308906
  26. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties.
    J Cell Biol. 1987 Sep;105(3):1273-82 PMID: 2958482
  27. Receptor-mediated vectorial transcytosis of epidermal growth factor by Madin-Darby canine kidney cells.
    J Cell Biol. 1987 Oct;105(4):1595-601 PMID: 3312235
  28. Tight junction structure and ZO-1 content are identical in two strains of Madin-Darby canine kidney cells which differ in transepithelial resistance.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2401-8 PMID: 3058723
  29. Nocodazole, a microtubule-active drug, interferes with apical protein delivery in cultured intestinal epithelial cells (Caco-2).
    J Cell Biol. 1989 Jan;108(1):13-22 PMID: 2642910
  30. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro.
    J Cell Biol. 1989 Apr;108(4):1301-16 PMID: 2538480
  31. Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium.
    J Cell Biol. 1989 Jul;109(1):179-89 PMID: 2568363
  32. Postendocytotic sorting of the ligand for the polymeric immunoglobulin receptor in Madin-Darby canine kidney cells.
    J Cell Biol. 1989 Aug;109(2):475-86 PMID: 2760105
  33. Morphogenesis of the polarized epithelial cell phenotype.
    Science. 1989 Aug 18;245(4919):718-25 PMID: 2672330
  34. Microtubules are involved in the secretion of proteins at the apical cell surface of the polarized epithelial cell, Madin-Darby canine kidney.
    J Biol Chem. 1989 Oct 5;264(28):16837-46 PMID: 2777809
  35. Human IgG Fc receptor (hFcRII; CD32) exists as multiple isoforms in macrophages, lymphocytes and IgG-transporting placental epithelium.
    EMBO J. 1989 Dec 1;8(12):3657-66 PMID: 2531080
  36. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2817-32 PMID: 2592406
  37. The biogenesis of lysosomes.
    Annu Rev Cell Biol. 1989;5:483-525 PMID: 2557062
  38. Endocytosis in filter-grown Madin-Darby canine kidney cells.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3243-58 PMID: 2689455
  39. 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
  40. 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
  41. Endocytic pathways in polarized Caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces.
    J Cell Biol. 1990 Feb;110(2):337-48 PMID: 2298809
  42. 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
  43. The receptor for transepithelial transport of IgA and IgM contains multiple immunoglobulin-like domains.
    Nature. 1984 Mar 1-7;308(5954):37-43 PMID: 6322002
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1990-11-00
Pages
3515-25
Language
English
Region
England
NLM ID
8208664
PMCID
PMC552100
Subset
IM
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