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Endocytic Traffic in Polarized Epithelial Cells: Role of the Actin and Microtubule Cytoskeleton

Gerard Apodaca

Article first published online: 21 DEC 2001

DOI: 10.1034/j.1600-0854.2001.020301.x

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Volume 2, Issue 3, pages 149–159, March 2001

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Apodaca, G. (2001), Endocytic Traffic in Polarized Epithelial Cells: Role of the Actin and Microtubule Cytoskeleton. Traffic, 2: 149–159. doi: 10.1034/j.1600-0854.2001.020301.x

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Renal-Electrolyte Division of the Department of Medicine, Laboratory of Epithelial Biology, and Department of Cell Biology and Physiology, University of Pittsburgh, Pittsburgh, PA 15261, USA gla6@pitt.edu

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Issue published online: 21 DEC 2001
Article first published online: 21 DEC 2001
Received 16 November 2000, Accepted 27 November 2000

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1
Mays RW, Beck KA & Nelson WJ. Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Curr Opin Cell Biol 1994;6: 16–24.
2
Brown D & Stow JL. Protein trafficking and polarity in kidney epithelium: from cell biology to physiology. Physiol Rev 1996;76: 245–297.
3
Kelly RB. Microtubules, membrane traffic, and cell organization. Cell 1990;61: 5–7.
4
Mays RW, Beck KA & Nelson WJ. Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Current Opin Cell Biol 1994;6: 16–24.
5
Mukherjee S, Ghosh RN & Maxfield FR. Endocytosis. Physiol Rev 1997;77: 759–803.
6
Sever S, Damke H & Schmid SL. Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 2000;1: 385–392.DOI: 10.1034/j.1600-0854.2000.010503.x
Direct Link:
7
Parton RG, Joggerst B & Simons K. Regulated internalization of caveolae. J Cell Biol 1994;127: 1199–1215.
8
Lamaze C & Schmid SL. The emergence of clathrin-independent pinocytotic pathways. Curr Opin Cell Biol 1995;7: 573–580.
9
Christoforidis S, McBride HM, Burgoyne RD & Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 1999;397: 621–625.DOI: 10.1038/17618
10
Mallet WG & Maxfield FR. Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J Cell Biol 1999;146: 345–359.
11
Bomsel M, Prydz K, Parton RG, Gruenberg J & Simons K. Endocytosis in filter-grown Madin–Darby canine kidney cells. J Cell Biol 1989;109: 3243–3258.
12
Eker P, Holm PK, van Deurs B & Sandvig K. Selective regulation of apical endocytosis in polarized Madin–Darby canine kidney cells by mastoparan and cAMP. J Biol Chem 1994;269: 18607–18615.
13
Bucci C, Wandinger-Ness A, Lutcke A, Chiariello M, Bruni CB & Zerial M. Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells. Proc Natl Acad Sci USA 1994;91: 5061–5065.
14
Leung S-M, Ruiz WG & Apodaca G. Sorting of membrane and fluid at the apical pole of polarized MDCK cells. Mol Biol Cell 2000;11: 2131–2150.
15
Gokay KE & Wilson JM. Targeting of an apical endosomal protein to endosomes in MDCK cells. Traffic 2000;1: 354–365.DOI: 10.1034/j.1600-0854.2000.010408.x
Direct Link:
16
Fialka I, Steinlein P, Ahorn H, Böck G, Burbelo PD, Haberfellner M, Lottspeich F, Paiha K, Pasquali C & Huber LA. Identification of syntenin as a protein of the apical early endocytic compartment in Madin–Darby canine kidney cells. J Biol Chem 1999;274: 26233–26239.
17
Odorizzi G, Pearse A, Domingo D, Trowbridge IS & Hopkins CR. Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J Cell Biol 1996;135: 139–152.
18
Zacchi P, Stenmark H, Parton RG, Orioli D, Lim F, Giner A, Mellman I, Zerial M & Murphy C. Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells. J Cell Biol 1998;140: 1039–1053.
19
Sheff DR, Daro EA, Hull M & Mellman I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 1999;145: 123–139.
20
Huber LA, Fialka I, Paiha K, Hunziker W, Sacks DB, Bähler M, Way M, Gagescu R & Gruenberg J. Both calmodulin and the unconventional myosin Myr4 regulate membrane trafficking along the recycling pathway of MDCK cells. Traffic 2000;1: 494–503.DOI: 10.1034/j.1600-0854.2000.010607.x
Direct Link:
21
Apodaca G, Katz LA & Mostov KE. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol 1994;125: 67–86.
22
Brown PS, Wang E, Aroeti B, Chapin SJ, Mostov KE & Dunn KW. Definition of distinct compartments in polarized Madin–Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling. Traffic 2000;1: 124–140.DOI: 10.1034/j.1600-0854.2000.010205.x
Direct Link:
23
Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, Altschuler YA, Ray GS & Godenring JR. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin–Darby canine kidney cells. Mol Biol Cell 1999;10: 47–61.
24
Hunziker W & Peters PJ. Rab17 localizes to recycling endosomes and regulates receptor-mediated transcytosis in epithelial cells. J Biol Chem 1998;273: 15734–15741.
25
Barroso M & Sztul E. Basolateral to apical transcytosis in polarized cells is indirect and involves BFA and trimeric G protein sensitive passage through the apical endosome. J Cell Biol 1994;124: 83–100.
26
Gibson A, Futter CE, Maxwell S, Allchin EH, Shipman M, Kraehenbuhl JP, Domingo D, Odorizzi G, Trowbridge IS & Hopkins CR. Sorting mechanisms regulating membrane protein traffic in the apical transcytotic pathway of polarized MDCK cells. J Cell Biol 1998;143: 81–94.
27
Breitfeld PP, Harris JM & Mostov KM. Postendocytotic sorting of the ligand for the polymeric immunoglobulin receptor in Madin–Darby canine kidney cells. J Cell Biol 1989;109: 475–486.
28
Wang E, Brown PS, Aroeti B, Chapin SJ, Mostov KE & Dunn KW. Apical and basolateral pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 2000;1: 480–493.DOI: 10.1034/j.1600-0854.2000.010606.x
Direct Link:
29
Van Ijzendoorn SCD, Maier O, Van Der Wouden JM & Hoekstra D. The subapical compartment and its role in intracellular trafficking and cell polarity. J Cell Physiol 2000;184: 151–160.DOI: 10.1002/1097-4652(200008)184:2<151::aid-jcp2>3.0.co;2-r
Direct Link:
30
Mostov KE, Verges M & Altschuler Y. Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol 2000;12: 483–490.DOI: 10.1016/s0955-0674(00)00120-4
31
Vale RD. Intracellular transport using microtubule-based motors. Ann Rev Cell Biol 1987;3: 347–378.
32
Woehlke G & Schliwa M. Walking on two heads: the many talents of kinesin. Nature Rev Mol Cell Biol 2000;1: 50–58.
33
Matter K, Bucher K & Hauri H-P. Microtubule perturbation retards both the direct and the indirect apical pathway but does not affect sorting of plasma membrane proteins in intestinal epithelial cells (Caco-2). EMBO J 1990;9: 3163–3170.
34
Piasek A & Thyberg J. Effects of colchicine on endocytosis of horseradish peroxidase by rat peritoneal macrophages. J Cell Sci 1980;45: 59–71.
35
Gekle M, Mildenberger S, Freudinger R, Schwerdt G & Silbernagl S. Albumin endocytosis in OK cells: dependence on actin and microtubules and regulation by protein kinases. Am J Physiol 1997;272: F668–F677.
36
Pratten MK & Lloyd JB. Effects of temperature, metabolic inhibitors and some other factors on fluid-phase and adsorptive pinocytosis by rat peritoneal macrophages. Biochem J 1979;180: 567–571.
37
Gruenberg J, Griffiths G & Howell K. 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;108: 1301–1316.
38
Bomsel M, Parton R, Kuznetsov SA, Schroer TA & Gruenberg J. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 1990;62: 719–731.
39
McGraw TE, Dunn KW & Maxfield FR. Isolation of a temperature-sensitive variant Chinese hamster ovary cell line with a morpholotgically altered endocytic recycling compartment. J Cell Physiol 1993;155: 579–594.
Direct Link:
40
Breitfeld PP, McKinnon WC & Mostov KE. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells. J Cell Biol 1990;111: 2365–2373.
41
Hunziker W, Mâle P & Mellman I. Differential microtubule requirements for transcytosis in MDCK cells. EMBO J 1990;9: 3515–3525.
42
Bomsel M. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med 1997;3: 42–47.
43
Mermall V, Post PL & Mooseker MS. Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 1998;279: 527–533.DOI: 10.1126/science.279.5350.527
44
Tuxworth RI & Titus MA. Unconventional myosins: anchors in the membrane traffic relay. Traffic 2000;1: 11–18.DOI: 10.1034/j.1600-0854.2000.010103.x
Direct Link:
45
Alexander JS, Jackson SA, Chaney E, Kevil CG & Haselton FR. The role of cadherin endocytosis in endothelial barrier regulation: involvement of protein kinase C and actin-cadherin interactions. Inflammation 1998;22: 419–433.
46
Smedsrod B, Johansson S & Pertoft H. Studies in vivo and in vitro on the uptake and degradation of soluble collagen α1(I) chains in rat liver endothelial and Kupffer cells. Biochem 1985;228: 415–424.
- CAS,
- Web of Science® Times Cited: 62
47
Durrbach A, Louvard D & Coudrier E. Actin filaments facilitate two steps of endocytosis. J Cell Sci 1996;109: 457–465.
48
Kyle ME, Nakae D, Sakaida I, Miccadei S & Farber JL. Endocytosis of superoxide dismutase is required in order for the enzyme to protect hepatocytes from cytotoxicity of hydrogen peroxide. J Biol Chem 1988;263: 3784–3789.
49
Kaufman SS, Blain PL, Park JHY & Tuma DJ. Role of microfilaments in asialoglycoprotein processing in adult and developing liver. Am J Physiol 1990;259: G639–G645.
50
Gottlieb TA, Ivanov IE, Adesnik M & Sabatini DD. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 1993;120: 695–710.
51
Shurety W, Stewart NL & Stow JL. Fluid-phase markers in the basolateral endocytic pathway accumulate in response to the actin assembly-promoting drug jasplakinolide. Mol Biol Cell 1998;9: 957–975.
52
Blok J, Scheven BAA, Mulder-Stapel AA, Ginsel LA & Daems WT. Endocytosis in absorptive cells of cultured human small-intestinal tissue: effect of cytochalasin B and D. Cell Tissue Res 1982;222: 113–126.
53
Shurety W, Bright NA & Luzio JP. The effects of cytochalasin D and phorbol myristate acetate on the apical endocytosis of ricin in polarised Caco-2 cells. J Cell Sci 1996;109: 2927–2935.
54
Jackman MR, Shurety W, Ellis JA & Luzio JP. Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J Cell Sci 1994;107: 2547–2556.
55
Song JC, Hrnjez BJ, Farokhzad OC & Matthews JB. PKC-ɛ regulates basolateral endocytosis in human T84 intestinal epithelia: role of F-actin and MARCKS. Am J Physiol 1999;277: C1239–C1249.
56
Dibas A, Mia A & Yorio T. Microfilament network is needed for the endocytosis of water channels and not for apical membrane insertion upon vasopressin action. Proc Soc Exp Biol Med 1999;223: 203–209.
- PubMed,
- Web of Science® Times Cited: 4
57
Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol 1987;105: 1473–1478.
58
Yao X, Chaponnier C, Gabbiani G & Forte JG. Polarized distribution of actin isoforms in gastric parietal cells. Mol Biol Cell 1995;6: 541–557.
59
Fujimoto LM, Roth R, Heuser JE & Schmid SL. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 2000;1: 161–171.DOI: 10.1034/j.1600-0854.2000.010208.x
Direct Link:
60
Sandvig K & vanDeurs B. Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis. J Biol Chem 1990;265: 6382–6388.
61
Lamaze C, Fujimoto LM, Yin HL & Schmid SL. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J Biol Chem 1997;272: 20332–20335.
62
Haigler HT, McKanna JA & Cohen S. Rapid stimulation of pinocytosis in human carcinoma cells A-431 by epidermal growth factor. J Cell Biol 1979;83: 82–90.
63
Salisbury JL, Condeelis JS & Satir P. Role of coated vesicles, microfilaments, and calmodulin in receptor-mediated endoctyosis by cultured B lymphoblastoid cells. J Cell Biol 1980;87: 132–141.
64
Novak KD, Peterson MD, Reedy MC & Titus MA. Dictyostelium myosin I double mutants exhibit conditional defects in pinocytosis. J Cell Biol 1995;131: 1205–1221.
65
Kübler E & Riezman H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J 1993;12: 2855–2862.
66
Geli MI & Riezman H. Role of type I myosins in receptor-mediated endocytosis in yeast. Science 1996;272: 533–535.
67
Klaus GG. Dissociation of pinocytosis and phagocytosis by peritoneal macrophages. Exp Cell Res 1973;79: 73–78.
68
Sako Y & Kusumi A. Compartmentalized structure of the plasma membrane for receptor movements as revealed by nanometer-level motion analysis. J Cell Biol 1994;125: 1251–1264.
69
Orci L, Gabbay KH & Malaisse WJ. Pancreatic beta-cell web: its possible role in insulin secretion. Science 1972;175: 1128–1130.
70
Valentijn K, Valentijn JA & Jamieson JD. Role of actin in regulated exocytosis and compensatory membrane retrieval: insights from an old acquaintance. Biochem Biophys Res Commun 1999;266: 652–661.DOI: 10.1006/bbrc.1999.1883
71
Verrey F, Groscurth P & Bolliger U. Cytoskeletal discruption in A6 kidney cells: impact on endo/exocytosis and NaCl transport regulation by antidiuretic hormone. J Membr Biol 1995;145: 193–204.
72
Radhakrishna H, Al-Awar O, Khachikian Z & Donaldson JG. ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J Cell Sci 1999;112: 855–866.
73
Altschuler Y, Liu S-H, Katz L, Tang K, Hardy S, Brodsky F, Apodaca G & Mostov K. ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin–Darby canine kidney cells. J Cell Biol 1999;147: 7–12.
74
Gaidarov I, Santini F, Warren RA & Keen JH. Spatial control of coated-pit dynamics in living cells. Naure Cell Biol 1999;1: 1–8.
75
Engqvist-Goldstein AEY, Kessels MM, Chopra VS, Hayden MR & Drubin DG. An actin-binding protein of the Sla2/huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles. J Cell Biol 1999;147: 1503–1518.
76
Qualmann B, Kessels MM & Kelly RB. Molecular links between endocytosis and the actin cytoskeleton. J Cell Bio 2000;150: F111–F116.
77
Witke W, Podtelejnikov AV, DiNardo A, Sutherland JD, Gurniak CB, Dotti C & Mann M. In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J 1998;17: 967–976.DOI: 10.1093/emboj/17.4.967
78
Qualmann B, Roos J, DiGregario PJ & Kelly RB. Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott–Aldrich syndrome protein. Mol Biol Cell 1999;10: 501–513.
79
Buss F, Kendrick-Jones J, Lionne C, Knight AE, Coté GP & Luzio JP. The localization of myosin VI at the Golgi complex and leading edge of fibroblasts and its phosphorylation and recruitment into membrane ruffles of A431 cells after growth factor stimulation. J Cell Biol 1998;143: 1535–1545.
80
Wells AL, Lin AW, Chen LQ, Safer D, Cain SM, Hasson T, Carragher BO, Milligan RA & Sweeney HL. Myosin VI is an actin-based motor that moves backwards. Nature 1999;401: 505–508.DOI: 10.1038/46835
81
Coudrier E, Durrbach A & Louvard D. Do unconventional myosins exert functions in dynamics of membrane compartments. FEBS Lett 1992;307: 87–92.
82
Merrifield CJ, Moss SE, Ballestrem C, Imhof BA, Giese G, Wunderlich I & Almers W. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nature Cell Biol 1999;1: 72–74.
83
Taunton J, Rowning BA, Coughlin ML, Wu M, Moon RT, Mitchison TJ & Larabell CA. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol 2000;1489: 519–530.
- CrossRef,
- Web of Science® Times Cited: 273
84
van Deurs B, Holm PK, Kayser L & Sandvig K. Delivery to lysosomes in the human carcinoma cell line Hep-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. Eur J Cell Biol 1995;66: 309–323.
85
Maples CJ, Ruiz WG & Apodaca G. Both microtubules and actin filaments are required for efficient postendocytic traffic of the polymeric immunoglobulin receptor in polarized Madin–Darby canine kidney cells. J Biol Chem 1997;272: 6741–6751.
86
Durrbach A, Raposo G, Tenza D, Louvard D & Coudrier E. Truncated brush border myosin I affects membrane traffic in polarized epithelial cells. Traffic 2000;1: 411–424.DOI: 10.1034/j.1600-0854.2000.010506.x
Direct Link:
87
Leung S-M, Rojas R, Maples C, Flynn C, Ruiz WG, Jou T-S & Apodaca G. Modulation of endocytic traffic in polarized MDCK cells by the small GTPase RhoA. Mol Biol Cell 1999;10: 4369–4384.
88
Pol A, Ortega D & Enrich C. Identification of cytoskeleton-associated proteins in isolated rat liver endosomes. Biochem J 1997;327: 741–746.
89
Fath KR & Burgess DR. Membrane mobility mediated by unconventional myosin. Curr Opin Cell Biol 1994;6: 131–135.
90
Raposo G, Cordonnier M-N, Tenza D, Menichi B, Dürrbach A, Louvard D & Coudrier E. Association of myosin I alpha with endosomes and lysosomes in mammalian cells. Mol Biol Cell 1999;10: 1477–1494.
91
Durrbach A, Collins K, Matsudaira P, Louvard D & Coudrier E. Brush border myosin-I truncated in the motor domain impairs the distribution and the function of endocytic compartments in an hepatoma cell line. Proc Natl Acad Sci USA 1996;93: 7053–7058.DOI: 10.1073/pnas.93.14.7053
92
Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EHK & Simons K. The subcellular organization of Madin–Darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol 1989;109: 2817–2832.
93
Wu X, Bowers B, Rao K, Wei Q & Hammer JA. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo. J Cell Biol 1998;143: 1899–1918.
94
Fath KR, Trimbur GM & Burgess DR. Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J Cell Biol 1994;126: 661–675.
95
Hall A. Rho GTPases and the actin cyotskeleton. Science 1998;279: 509–514.DOI: 10.1126/science.279.5350.509
96
Van Aelst L & D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Devel 1997;11: 2295–2322.
97
Ellis S & Mellor H. Regulation of endocytic traffic by Rho family GTPases. T Cell Biol 2000;10: 85–88.
98
Lamaze C, Chuang T-H, Terlecky LJ, Bokoch GM & Schmid SL. Regulation of receptor-mediated endocytosis by Rho and Rac1. Nature 1996;382: 177–179.
99
Jou T-S, Leung S-M, Fung LM, Ruiz WG, Nelson WJ & Apodaca G. Selective alterations in biosynthetic and endocytic protein traffic in Madin–Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell 2000;11: 287–304.
100
Kroschewski R, Hall A & Mellman I. Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells. Nature Cell Biol 1999;1: 8–13.

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Endocytic Traffic in Polarized Epithelial Cells: Role of the Actin and Microtubule Cytoskeleton

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