Home LiteratureArticle Details
PMID: 7905002 Published · ppublish English Journal Article

Basolateral to apical transcytosis in polarized cells is indirect and involves BFA and trimeric G protein sensitive passage through the apical endosome.

The Journal of cell biology ·Vol. 124 ·No. 1-2 ·1994-01-00 ·Pages 83-100

Barroso M, Sztul ES

Abstract

We have used temperature and nocodazole blocks in an in vivo basolateral to apical transcytosis assay to dissociate the early transcytotic steps occurring during the formation of transcytotic vesicles and their microtubule-dependent translocation into the apical region, from the late steps when transcytotic cargo is delivered into the apical media. We found that polarized MDCK cells transfected with rabbit polymeric IgA receptor (pIgA-R) internalize basolaterally added pIgA-R ligand ([Fab]2 fragment of IgG against the receptor's ectodomain) at 17 degrees C but do not deliver it to the apical PM. Instead, the ligand accumulates in an apically localized transcytotic compartment, distal to the basolateral endosome and the microtubule-requiring translocation step. We have characterized this compartment and show that it is distinct from basolateral transferrin recycling endosomes, basolateral early endosomes or late endosomes or lysosomes. The apical transcytotic compartment colocalizes with the compartment containing apically recycling membrane markers (ricin and apically internalized pIgA-R ligand) but is distinct from the compartment receiving apically internalized fluid phase marker (BSA). This compartment is an intermediate station of the overall pathway since transcytotic ligand can exit the compartment and be released into the apical medium when cells preloaded at 17 degrees C are subsequently incubated at 37 degrees C. We have used this system to examine the effect of Brefeldin A (BFA) and the involvement of trimeric GTPases in the late (post apical transcytotic compartment) steps of the transcytotic pathway. We found that addition of BFA or cholera toxin, a known activator of Gs alpha, to cells preloaded with transcytotic ligand at 17 degrees C significantly inhibits the exit of ligand from the apical transcytotic compartment. General structure and function of the apical endosome are not affected since neither BFA nor cholera toxin inhibit the recycling of apically internalized membrane markers (ricin and pIgA-R ligand) from the same compartment. The data suggest that transcytosis connects the "membrane-sorting" sub-domain of the basolateral endosome with a homologous sub-domain of the apical endosome and that exit of transcytosing cargo from the apical endosome is controlled by a BFA and trimeric G protein sensitive mechanism, distinct from that used for recycling of apically internalized proteins (ricin or pIgA-R).

MeSH Terms
Animals Biological Transport/drug effects Brefeldin A Cell Line Cell Membrane/metabolism Cell Polarity Cholera Toxin/pharmacology Cyclopentanes/pharmacology Dogs Endocytosis/drug effects Endosomes/metabolism Epithelium/metabolism Exocytosis/drug effects GTP-Binding Proteins/physiology Ligands Microscopy, Fluorescence Microtubules/physiology Receptors, Fc/metabolism Ricin/metabolism
Chemicals
Cyclopentanes IgA receptor Ligands Receptors, Fc Brefeldin A Ricin Cholera Toxin GTP-Binding Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Barroso M
Department of Molecular Biology, Princeton University, New Jersey 08544.
Sztul E S
References (73)
73 references, click to expand
  1. ATP and cytosol requirements for transferrin recycling in intact and disrupted MDCK cells.
    EMBO J. 1990 Nov;9(11):3477-87 PMID: 2209555
  2. Binding of ARF and beta-COP to Golgi membranes: possible regulation by a trimeric G protein.
    Science. 1991 Nov 22;254(5035):1197-9 PMID: 1957170
  3. A novel approach to detect toxin-catalyzed ADP-ribosylation in intact cells: its use to study the action of Pasteurella multocida toxin.
    J Cell Biol. 1991 Nov;115(4):949-58 PMID: 1835459
  4. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF.
    Nature. 1992 Nov 26;360(6402):352-4 PMID: 1448152
  5. ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein.
    Cell. 1991 Oct 18;67(2):239-53 PMID: 1680566
  6. Binding of coatomer to Golgi membranes requires ADP-ribosylation factor.
    J Biol Chem. 1993 Jun 5;268(16):12083-9 PMID: 8505331
  7. SEC21 is a gene required for ER to Golgi protein transport that encodes a subunit of a yeast coatomer.
    Nature. 1992 Dec 10;360(6404):603-5 PMID: 1461285
  8. Brefeldin A: insights into the control of membrane traffic and organelle structure.
    J Cell Biol. 1992 Mar;116(5):1071-80 PMID: 1740466
  9. Endocytosis, intracellular transport and transcytosis of the toxic protein ricin by a polarized epithelium.
    Eur J Cell Biol. 1990 Feb;51(1):96-109 PMID: 2328741
  10. Transferrin receptor polarity and recycling accuracy in "tight" and "leaky" strains of Madin-Darby canine kidney cells.
    J Cell Biol. 1986 Nov;103(5):1767-79 PMID: 2877994
  11. Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis.
    Science. 1990 May 11;248(4956):742-5 PMID: 2110383
  12. 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
  13. Clathrin, adaptors, and sorting.
    Annu Rev Cell Biol. 1990;6:151-71 PMID: 2177341
  14. Structure and function of signal-transducing GTP-binding proteins.
    Annu Rev Biochem. 1991;60:349-400 PMID: 1909108
  15. Cholera toxin-catalyzed [32P]ADP-ribosylation of proteins.
    Methods Enzymol. 1991;195:267-80 PMID: 1903491
  16. Late endosomes derive from early endosomes by maturation.
    Cell. 1991 May 3;65(3):417-27 PMID: 1850321
  17. 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
  18. Molecular dissection of the secretory pathway.
    Nature. 1992 Jan 30;355(6359):409-15 PMID: 1734280
  19. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3303-14 PMID: 2600137
  20. Differential microtubule requirements for transcytosis in MDCK cells.
    EMBO J. 1990 Nov;9(11):3515-25 PMID: 2170116
  21. 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
  22. Radioactive labeling of proteins in vitro.
    J Biol Chem. 1971 Feb 10;246(3):831-2 PMID: 5100767
  23. 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
  24. Activation of ADP-ribosylation factor by Golgi membranes. Evidence for a brefeldin A- and protease-sensitive activating factor on Golgi membranes.
    J Biol Chem. 1993 May 5;268(13):9555-63 PMID: 8486645
  25. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process.
    J Cell Biol. 1993 Jun;121(6):1257-69 PMID: 8509447
  26. Intracellular targetting signals of polymeric immunoglobulin receptors are highly conserved between species.
    FEBS Lett. 1989 Aug 28;254(1-2):177-83 PMID: 2776882
  27. Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo.
    Cell. 1993 Jul 16;74(1):71-82 PMID: 8334707
  28. ADP ribosylation of membrane proteins from human fibroblasts. Effect of prior exposure of cells to choleragen.
    J Biol Chem. 1981 May 25;256(10):4895-9 PMID: 7228858
  29. The trans-Golgi network can be dissected structurally and functionally from the cisternae of the Golgi complex by brefeldin A.
    Eur J Cell Biol. 1992 Oct;59(1):92-105 PMID: 1468449
  30. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein beta-COP to Golgi membranes.
    Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6408-12 PMID: 1631136
  31. Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA.
    Cell. 1986 Aug 15;46(4):613-21 PMID: 3524859
  32. Forskolin: its biological and chemical properties.
    Adv Cyclic Nucleotide Protein Phosphorylation Res. 1986;20:1-150 PMID: 3028083
  33. Identification of a 200-kD, brefeldin-sensitive protein on Golgi membranes.
    J Cell Biol. 1992 Apr;117(1):27-38 PMID: 1556155
  34. 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
  35. Effects of brefeldin A on endocytosis, transcytosis and transport to the Golgi complex in polarized MDCK cells.
    J Cell Biol. 1992 Oct;119(2):259-72 PMID: 1400572
  36. Bile secretory apparatus: evidence for a vesicular transport mechanism for proteins in the rat, using horseradish peroxidase and [125I]insulin.
    Gastroenterology. 1980 Jun;78(6):1373-88 PMID: 6989703
  37. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2365-73 PMID: 2277063
  38. Multiple trimeric G-proteins on the trans-Golgi network exert stimulatory and inhibitory effects on secretory vesicle formation.
    EMBO J. 1992 Dec;11(13):4795-804 PMID: 1464309
  39. Receptor-mediated transport of IgG.
    J Cell Biol. 1984 Jul;99(1 Pt 2):159s-164s PMID: 6235233
  40. Selective inhibition of transcytosis by brefeldin A in MDCK cells.
    Cell. 1991 Nov 1;67(3):617-27 PMID: 1934063
  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. Control of protein traffic between distinct plasma membrane domains. Requirement for a novel 108,000 protein in the fusion of transcytotic vesicles with the apical plasma membrane.
    J Biol Chem. 1993 Jan 25;268(3):1876-85 PMID: 8420962
  43. Newly synthesized hepatocyte plasma membrane proteins are transported in transcytotic vesicles in the bile duct-ligated rat.
    Gastroenterology. 1993 Aug;105(2):554-71 PMID: 8335210
  44. 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
  45. 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
  46. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway.
    Cell. 1992 Sep 4;70(5):729-40 PMID: 1516131
  47. Cell surface polarity in epithelia.
    Annu Rev Cell Biol. 1985;1:243-88 PMID: 3939606
  48. Action of brefeldin A blocked by activation of a pertussis-toxin-sensitive G protein.
    Nature. 1992 Mar 26;356(6367):344-6 PMID: 1549178
  49. A heterotrimeric G protein, G alpha i-3, on Golgi membranes regulates the secretion of a heparan sulfate proteoglycan in LLC-PK1 epithelial cells.
    J Cell Biol. 1991 Sep;114(6):1113-24 PMID: 1910049
  50. Regulation of apical transport in epithelial cells by a Gs class of heterotrimeric G protein.
    Nature. 1993 Apr 1;362(6419):456-8 PMID: 8385268
  51. Transcytosis of the polymeric Ig receptor requires phosphorylation of serine 664 in the absence but not the presence of dimeric IgA.
    Cell. 1993 Jul 30;74(2):245-55 PMID: 8343953
  52. Marker enzymes in rat liver vesicles involved in transcellular transport.
    Eur J Biochem. 1989 Oct 1;184(3):567-74 PMID: 2553396
  53. Endocytosis in filter-grown Madin-Darby canine kidney cells.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3243-58 PMID: 2689455
  54. Endocytic vesicles in liver carry polymeric IgA from serum to bile.
    Biochim Biophys Acta. 1979 Oct 18;587(3):381-91 PMID: 549648
  55. Lumenal labeling of rat hepatocyte early endosomes. Presence of multiple membrane receptors and the Na+,K(+)-ATPase.
    J Biol Chem. 1992 Apr 25;267(12):8213-21 PMID: 1314820
  56. Tubular early endosomal networks in AtT20 and other cells.
    J Cell Biol. 1991 Nov;115(3):635-53 PMID: 1918157
  57. TGN38/41: a molecule on the move.
    Trends Cell Biol. 1993 Aug;3(8):252-5 PMID: 14731742
  58. Receptor-mediated endocytosis of polymeric IgA and galactosylated serum albumin in rat liver. Evidence for intracellular ligand sorting and identification of distinct endosomal compartments.
    Eur J Biochem. 1985 Feb 1;146(3):539-48 PMID: 2982599
  59. Mechanism of action of cholera toxin: effect of receptor density and multivalent binding on activation of adenylate cyclase.
    J Membr Biol. 1980;54(1):51-60 PMID: 6259358
  60. 'Coatomer': a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles.
    Nature. 1991 Jan 17;349(6306):248-51 PMID: 1898986
  61. Intracellular receptor sorting during endocytosis: comparative immunoelectron microscopy of multiple receptors in rat liver.
    Cell. 1984 May;37(1):195-204 PMID: 6327050
  62. 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
  63. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis.
    J Cell Biol. 1993 Jan;120(1):37-45 PMID: 8416994
  64. 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
  65. Evidence of a role for heterotrimeric GTP-binding proteins in endosome fusion.
    Science. 1992 Mar 27;255(5052):1695-7 PMID: 1348148
  66. A coat protein required for transcytotic traffic exists as a multimeric complex.
    Eur J Cell Biol. 1993 Jun;61(1):184-8 PMID: 8223703
  67. Intracellular and transcellular transport of secretory component and albumin in rat hepatocytes.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1582-91 PMID: 6630294
  68. Preservation of biological specimens for observation in a confocal fluorescence microscope and operational principles of confocal fluorescence microscopy.
    Methods Cell Biol. 1989;31:437-52 PMID: 2674628
  69. Role of heterotrimeric G proteins in membrane traffic.
    Mol Biol Cell. 1992 Dec;3(12):1317-28 PMID: 1493332
  70. Brefeldin A and the endocytic pathway. Possible implications for membrane traffic and sorting.
    FEBS Lett. 1992 Jul 27;307(1):93-6 PMID: 1639200
  71. Receptor-mediated endocytosis of asialoglycoproteins by rat hepatocytes: receptor-positive and receptor-negative endosomes.
    J Cell Biol. 1986 Mar;102(3):932-42 PMID: 3512582
  72. Protein traffic between distinct plasma membrane domains: isolation and characterization of vesicular carriers involved in transcytosis.
    Cell. 1991 Jan 11;64(1):81-9 PMID: 1986870
  73. Transcellular transport of polymeric IgA in the rat hepatocyte: biochemical and morphological characterization of the transport pathway.
    J Cell Biol. 1985 Dec;101(6):2113-23 PMID: 4066752
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-01-00
Pages
83-100
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119901
Subset
IM
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: [email protected]