The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms

PLoS Biology

Volumn 2, Issue 9, 2004, Pages

  Schnatwinkel, Carsten ^a   Christoforidis, Savvas ^b   Lindsay, Margaret R ^c   Uttenweiler Joseph, Sandrine ^d   Wilm, Matthias ^d   Parton, Robert G ^c   Zerial, Marino ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY OF IOANNINA   (Greece)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; RAB PROTEIN; RABANKYRIN 5; UNCLASSIFIED DRUG; ANDROSTANE DERIVATIVE; ENZYME INHIBITOR; GUANOSINE TRIPHOSPHATASE; INOSITOL PHOSPHATE; LIPOSOME; RECOMBINANT PROTEIN; SIGNAL PEPTIDE; WORTMANNIN;

ANIMAL CELL; ARTICLE; CELL FUSION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PINOCYTOSIS; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; ADENOVIRUS; ANIMAL; CELL LINE; CELL MEMBRANE; CELL STRAIN 3T3; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; DOG; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROSCOPY; MOLECULAR CLONING; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; PLASMID; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; TIME; TUMOR CELL LINE;

ANIMALIA;

ADENOVIRIDAE; ANDROSTADIENES; ANIMALS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CLONING, MOLECULAR; DOGS; DOWN-REGULATION; ENDOCYTOSIS; ENDOSOMES; ENZYME INHIBITORS; EPITHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION; GTP PHOSPHOHYDROLASES; HUMANS; INOSITOL PHOSPHATES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOSOMES; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; MOVEMENT; NIH 3T3 CELLS; PINOCYTOSIS; PLASMIDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RAB5 GTP-BINDING PROTEINS; RECOMBINANT PROTEINS; RNA INTERFERENCE; TIME FACTORS;

EID: 19344365468     PISSN: 15449173     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pbio.0020261     Document Type: Article

References (95)

1. Allen LA, Aderem A (1996) Mechanisms of phagocytosis. Curr Opin Immunol 8: 36-40.
2. Altschuler Y, Liu S-H, Katz L, Tang K, Hardy S, et al. (1999) ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin-Darby canine kidney cells. J Cell Biol 147: 7-12.
3. Amyere M, Payrastre B, Krause U, Van Der Smissen P, Veithen A, et al. (2000) Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Mol Biol Cell 11: 3453-3467.
4. Amyere M, Mettlen M, Van D, Platek A, Payrastre B, et al. (2002) Origin, originality, functions, subversions and molecular signalling of macropinocytosis. Int J Med Microbiol 291: 487-494.
5. Araki N, Johnson MT, Swanson JA (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 135: 1249-1260.
6. Bardwell VJ, Treisman R (1994) The POZ domain: A conserved protein-protein interaction motif. Genes Dev 8: 1664-1677.
7. Bar-Sagi D, Feramisco JR (1986) Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science 233: 1061-1068.
8. Bennett V, Chen L (2001) Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Curr Opin Cell Biol 13: 61-67.
9. Bomsel M, Prydz K, Parton RG, Gruenberg J, Simons K (1989) Endocytosis in filter-grown Madin-Darby canine kidney cells. J Cell Biol 109: 3243-3258.
10. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, et al. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715-728.
11. Bucci C, Wandinger-Ness A, Lutcke A, Chiariello M, Bruni CB, et al. (1994) Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells. Proc Natl Acad Sci U S A 91: 5061-5065.
12. Bucci C, Lutcke A, Steele-Mortimer O, Olkkonen VM, Dupree P, et al. (1995) Co-operative regulation of endocytosis by three Rab5 isoforms. FEBS Lett 366: 65-71.
13. Carpentier JL, Lew DP, Paccaud JP, Gil R, Iacopetta B, et al. (1991) Internalization pathway of C3b receptors in human neutrophils and its transmodulation by chemoattractant receptors stimulation. Cell Regul 2: 41-55.
14. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62: 317-329.
15. Christensen EI, Birn H, Verroust P, Moestrup SK (1998) Membrane receptors for endocytosis in the renal proximal tubule. Int Rev Cytol 180:237-284.
16. Christoforidis S, Zerial M (2000) Purification and identification of novel Rab effectors using affinity chromatography. Methods 20: 403-410.
17. Christoforidis S, McBride HM, Burgoyne RD, Zerial M (1999a) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397: 621-625.
18. Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, et al. (1999b) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1: 249-252.
19. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422: 37-44.
20. Corey DP, Sotomayor M (2004) Hearing: Tightrope act. Nature 428: 901-903.
21. de Baey A, Lanzavecchia A (2000) The role of aquaporins in dendritic cell macropinocytosis. J Exp Med 191: 743-748.
22. de Hoop MJ, Huber LA, Stenmark H, Williamson E, Zerial M, et al. (1994) The involvement of the small GTP-binding protein Rab5a in neuronal endocytosis. Neuron 13: 11-22.
23. Denker SP, Barber DL (2002a) Ion transport proteins anchor and regulate the cytoskeleton. Curr Opin Cell Biol 14: 214-220.
24. Denker SP, Barber DL (2002b) Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 159: 1087-1096.
25. Dharmawardhane S, Schurmann A, Sells MA, Chernoff J, Schmid SL, et al. (2000) Regulation of macropinocytosis by p21-activated kinase-1. Mol Biol Cell 11: 3341-3352.
26. Francis CL, Ryan TA, Jones BD, Smith SJ, Falkow S (1993) Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364: 639-642.
27. Furukawa M, He YJ, Borchers C, Xiong Y (2003) Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat Cell Biol 5:1001-1007.
28. Galan JE, Zhou D (2000) Striking a balance: Modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci U S A 97: 8754-8761.
29. Gesualdo L, Di Paolo S, Calabro A, Milani S, Maiorano E, et al. (1996) Expression of epidermal growth factor and its receptor in normal and diseased human kidney: An immunohistochemical and in situ hybridization study. Kidney Int 49: 656-665.
30. Goligorsky MS, Hruska KA (1986) Transcytosis in cultured proximal tubular cells. J Membr Biol 93: 237-247.
31. Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) rab5 controls early endosome fusion in vitro. Cell 64: 915-925.
32. Gottlieb TA, Ivanov IE, Adesnik M, Sabatini DD (1993) Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 120: 695-710.
33. Haigler HT, McKanna JA, Cohen S (1979) Rapid stimulation of pinocytosis in human carcinoma cells A-431 by epidermal growth factor. J Cell Biol 83: 82-90.
34. Hewlett LJ, Prescott AR, Watts C (1994) The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 124: 689-703.
35. Holm PK, Eker P, Sandvig K, van Deurs B (1995) Phorbol myristate acetate selectively stimulates apical endocytosis via protein kinase C in polarized MDCK cells. Exp Cell Res 217: 157-168.
36. Holt M, Cooke A, Wu MM, Lagnado L (2003) Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J Neurosci 23: 1329-1339.
37. Hooshmand-Rad R, Claesson-Welsh L, Wennstrom S, Yokote K, Siegbahn A, et al. (1997) Involvement of phosphatidylinositide 3′-kinase and Rac in platelet-derived growth factor-induced actin reorganization and chemotaxis. Exp Cell Res 234: 434-441.
38. Horiuchi H, Lippe R, McBride HM, Rubino M, Woodman P, et al. (1997) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90: 1149-1159.
39. Howard J, Bechstedt S (2004) Hypothesis: a helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol 14: R224-R226.
40. Ikonomov OC, Sbrissa D, Foti M, Carpentier JL, Shisheva A (2003) PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol Biol Cell 14: 4581-4591 Epub 2003 August 4587.
41. Jackman MR, Shurety W, Ellis JA, Luzio JP (1994) Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J Cell Sci 107: 2547-2556.
42. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106: 145-155.
43. Kobayashi A, Yamagiwa H, Hoshino H, Muto A, Sato K, et al. (2000) A combinatorial code for gene expression generated by transcription factor Bach2 and MAZR (MAZ-related factor) through the BTB/POZ domain. Mol Cell Biol 20: 1733-1746.
44. Kryl D, Yacoubian T, Haapasalo A, Castren E, Lo D, et al. (1999) Subcellular localization of full-length and truncated Trk receptor isoforms in polarized neurons and epithelial cells. J Neurosci 19: 5823-5833.
45. Kuriyama H, Asakawa S, Minoshima S, Maruyama H, Ishii N, et al. (2000) Characterization and chromosomal mapping of a novel human gene, ANKHZN. Gene 253: 151-160.
46. Kutateladze TG, Ogburn KD, Watson WT, de Beer T, Emr SD, et al. (1999) Phosphatidylinositol 3-phosphate recognition by the FYVE domain. Mol Cell 3: 805-811.
47. Lanzetti L, Rybin V, Malabarba MG, Christoforidis S, Scita G, et al. (2000) The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature 408: 374-377.
48. Lewis WH (1931) Pinocytosis. Johns Hopkins Hosp Bull 49: 17-27.
49. Li G, D'Souza-Schorey C, Barbieri MA, Cooper JA, Stahl PD (1997) Uncoupling of membrane ruffling and pinocytosis during Ras signal transduction. J Biol Chem 272: 10337-10340.
50. Liou W, Geuze HJ, Slot JW (1996) Improving structural integrity of cryosections for immunogold labeling. Histochem Cell Biol 106: 41-58.
51. Lubman OY, Korolev SV, Kopan R (2004) Anchoring notch genetics and biochemistry; structural analysis of the ankyrin domain sheds light on existing data. Mol Cell 13: 619-626.
52. Marston DJ, Dickinson S, Nobes CD (2003) Rac-dependent transendocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat Cell Biol 5: 879-888.
53. Matter K, Hunziker W, Mellman I (1992) Basolateral sorting of LDL receptor in MDCK cells: The cytoplasmic domain contains two tyrosinedependent targeting determinants. Cell 71: 741-753.
54. McBride HM, Rybin V, Murphy C, Giner A, Teasdale R, et al. (1999) Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98: 377-386.
55. McLauchlan H, Newell J, Morrice N, Osborne A, West M, et al. (1998) A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr Biol 8: 34-45.
56. Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. J Membr Biol 179: 79-102.
57. Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M (1999) Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 8: 34-45.
58. Nielsen E, Christoforidis S, Uttenweiler-Joseph S, Miaczynska M, Dewitte F, et al. (2000) Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol 151: 601-612.
59. Otter-Nilsson M, Hendriks R, Pecheur-Huet E-I, Hoekstra D, Nilsson T (1999) Cytosolic ATPases, p97 and NSF, are sufficient to mediate rapid membrane fusion. EMBO J 18: 2074-2083.
60. Pelkmans L, Kartenbeck J, Helenius A (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3: 473-483.
61. Pillion DJ, Haskell JF, Atchison JA, Ganapathy V, Leibach FH (1989) Receptors for IGF-I, but not for IGF-II, on proximal colon epithelial cell apical membranes. Am J Physiol 257: E27-E34.
62. Pryciak PM, Hartwell LH (1996) AKR1 encodes a candidate effector of the G beta gamma complex in the Saccharomyces cerevisiae pheromone response pathway and contributes to control of both cell shape and signal transduction. Mol Cell Biol 16: 2614-2626.
63. Racoosin EL, Swanson JA (1992) M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci 102: 867-880.
64. Racoosin EL, Swanson JA (1993) Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 121: 1011-1020.
65. Radhakrishna H, Klausner RD, Donaldson JG (1996) Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J Cell Biol 134: 935-947.
66. Ridley AJ (1994) Membrane ruffling and signal transduction. Bioessays 16: 321-327.
67. Rubino M, Miaczynska M, Lippe R, Zerial M (2000) Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem 275: 3745-3748.
68. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2: 411-423.
69. Sandvig K, van Deurs B (1990) Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis. J Biol Chem 265: 6382-6388.
70. Sandvig K, Llorente A, Rodal SK, Eker P, Garred O, et al. (2000) Apical macropinocytosis in polarized MDCK cells: Regulation by Nethylmaleimide-sensitive proteins. Eur J Cell Biol 79: 447-457.
71. Sansonetti PJ (1997) Molecular and cellular bases of intestinal epithelial cell invasion by Shigella flexneri. C R Biol 320: 729-734.
72. Shao Y, Akmentin W, Toledo-Aral JJ, Rosenbaum J, Valdez G, et al. (2002) Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J Cell Biol 157: 679-691.
73. Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, et al. (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion [comments]. Nature 394: 494-498.
74. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149: 901-914.
75. Steinman RM, Swanson J (1995) The endocytic activity of dendritic cells. J Exp Med 182: 283-288.
76. Steinman RM, Brodie SE, Cohn ZA (1976) Membrane flow during pinocytosis. A stereologic analysis. J Cell Biol 68: 665-687.
77. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A, Gruenberg J, et al. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13: 1287-1296.
78. Stenmark H, Aasland R, Toh BH, D'Arrigo A (1996) Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J Biol Chem 271: 24048-24054.
79. Sun P, Yamamoto H, Suetsugu S, Miki H, Takenawa T, et al. (2003) Small GTPase Rah/Rab34 is associated with membrane ruffles and macropinosomes and promotes macropinosome formation. J Biol Chem 278: 4063-4071.
80. Swanson JA (1989) Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J Cell Sci 94: 135-142.
81. Tall GG, Barbieri MA, Stahl PD, Horazdoversusky BF (2001) Rasactivated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev Cell 1: 73-82.
82. Tokuyasu KT, Maher PA, Singer SJ (1984) Distributions of vimentin and desmin in developing chick myotubes in vivo. I. Immunofluorescence study. J Cell Biol 98: 1961-1972.
83. Tuma PL, Finnegan CM, Yi J-H, Hubbard AL (1999) Evidence for apical endocytosis in polarized hepatic cells: Phosphoinositide 3-kinase inhibitors lead to the lysosomal accumulation of resident apical plasma membrane proteins. J Cell Biol 145: 1089-1102.
84. Unkeless JC (1979) Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J Exp Med 150: 580-596.
85. Veithen A, Cupers P, Baudhuin P, Courtoy PJ (1996) v-Src induces constitutive macropinocytosis in rat fibroblasts. J Cell Sci 109: 2005-2012.
86. Weigmann A, Corbeil D, Hellwig A, Huttner WB (1997) Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of nonepithelial cells. Proc Natl Acad Sci U S A 94: 12425-12430.
87. West MA, Bretscher MS, Watts C (1989) Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 109: 2731-2739.
88. West MA, Prescott AR, Eskelinen EL, Ridley AJ, Watts C (2000) Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 10: 839-848.
89. Wilm M, Shevchenko A, Houthaeve T, Breit S, Schweigerer L, et al. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379: 466-469.
90. Yang D, Buchholz F, Huang Z, Goga A, Chen C-Y, et al. (2002) Short RNA duplexes produced by hydrolysis with Escherichia coli RNase III mediate effective RNA interference in mammalian cells. Proc Natl Acad Sci U S A 99: 9942-9947.
91. Zacchi P, Stenmark H, Parton RG, Orioli D, Lim F, et al. (1998) Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells. J Cell Biol 140: 1039-1053.
92. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117.
93. Zerial M, Christoforidis S, DeRenzis S, Nielsen E, Murphy C (2001) Assay to detect substances useful for therapy. International patent application CA2384306.
94. 32P]phosphatidylinositol trisphosphate levels, alters Factin distribution and impairs pinocytosis. J Cell Sci 111: 283-294.
95. Zimmer M, Palmer A, Kohler J, Klein R (2003) EphB-ephrinB bidirectional endocytosis terminates adhesion allowing contact mediated repulsion. Nat Cell Biol 5: 869-878.