The receptors recycling pathway contains two distinct populations of early endosomes with different sorting functions

Journal of Cell Biology

Volumn 145, Issue 1, 1999, Pages 123-139

  Sheff, David R ^a   Daro, Elizabeth A ^a,b   Hull, Michael ^a   Mellman, Ira ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AMGEN INC   (United States)

Author keywords

Endosomes; Receptor recycling; Sorting

Indexed keywords

ALUMINUM FLUORIDE; RAB PROTEIN; RECEPTOR PROTEIN; TRANSFERRIN RECEPTOR; ALUMINUM DERIVATIVE; CELL SURFACE RECEPTOR; FLUORIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN A POLYMER; RAB11 PROTEIN; SECRETORY COMPONENT; TETRAFLUOROALUMINATE;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; BINDING KINETICS; CONTROLLED STUDY; ENDOSOME; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RECEPTOR BINDING; REGULATORY MECHANISM; TRANSCYTOSIS; VALIDATION PROCESS; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CELL POLARITY; CLASSIFICATION; CYTOLOGY; DENSITY GRADIENT CENTRIFUGATION; DOG; ENDOCYTOSIS; EPITHELIUM CELL; KIDNEY; KINETICS; METABOLISM; PHYSIOLOGY;

ALUMINUM COMPOUNDS; ANIMALS; CELL LINE; CELL POLARITY; CENTRIFUGATION, DENSITY GRADIENT; DOGS; ENDOCYTOSIS; ENDOSOMES; EPITHELIAL CELLS; FLUORIDES; GTP-BINDING PROTEINS; IMMUNOGLOBULIN A; KIDNEY; KINETICS; MODELS, BIOLOGICAL; RAB GTP-BINDING PROTEINS; RAB4 GTP-BINDING PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, POLYMERIC IMMUNOGLOBULIN; RECEPTORS, TRANSFERRIN;

EID: 0033525930     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.1.123     Document Type: Article

References (50)

1. Advani, R.J., H.R. Bae, J.B. Bock, D.S. Chao, Y.C. Doung, R. Prekeris, J.S. Yoo, and R.H. Schcller. 1998. Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J. Biol. Chem. 273:10317-10324.
2. Apodaca, G., L.A. Katz, and K.E. Mostov. 1994. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125: 67-86.
3. Barroso, M., and E.S. Sztul. 1994. 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. 124:83-100.
4. Besterman, J.M., J.A. Airhart, R.C. Woodworth, and R.B. Low. 1981. Exocytosis and pinocytosed fluid in cultured cells: kinetic evidence for rapid turnover and compartmentation. J. Cell Biol. 91:716-727.
5. Breitfeld, P.P., J.M. Harris, and K.E. Mostov. 1989. Postendocytotic sorting of the ligand for the polymeric immunoglobulin receptor in Madin-Darby canine kidney cells. J. Cell Biol. 109:475-486.
6. Breitfeld, P.P., J.E. Casanova, W.C. McKinnon, and K.E. Mostov. 1990. Deletions in the cytoplasmic domain of the polymeric immunoglobulin receptor differentially affect endocytotic rate and postendocytotic traffic. J. Biol. Chem. 265:13750-13757.
7. Casanova, J.E., P.P. Breitfeld, S.A. Ross, and K.E. Mostov. 1990. Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis. Science. 248:742-745.
8. Ciechanover, A., A.L. Schwartz, A. Cautry-Varsat, and H.F. Lodish. 1983. Kinetics of internalization of transferrin and the transferrin receptor in a human hepatoma cell line. J. Biol. Chem. 258:9681-9689.
9. Daniel, W.W. 1987. Biostatistics: A Foundation for Analysis in the Health Sciences. John Wiley & Sons, New York. 127-187.
10. Daro, E., P. Van der Sluijs, T. Galli, and I. Mellman. 1996. Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc. Natl. Acad. Sci. USA. 93:9559-9564.
11. French, A.R., and D.A. Lauffenburger. 1997. Controlling receptor/ligand trafficking: effects of cellular and molecular properties on endosomal sorting. Ann. Biomed. Eng. 25:690-707.
12. Futter, C.E., A. Gibson, E.H. Allchin, S. Maxwell, L.J. Ruddock, G. Odorizzi, D. Domingo, I.S. Trowbridge, and C.R. Hopkins. 1998. In polarized MDCK cells basolateral vesicles arise from clathrin-γ-adaptin-coated domains on endosomal tubules. J. Cell Biol. 141:611-623.
13. Ghosh, R.N., and F.R. Maxfield. 1995. Evidence for nonvectorial, retrograde transferrin traffic in the early endosomes of Hep2 cells. J. Cell Biol. 128:549-561.
14. Ghosh, R.N., D.L. Gelman, and F.R. Maxfield. 1994. Quantification of low density lipoprotein and transferrin endocytic sorting in Hep2 cells using confocal microscopy. J. Cell Sci. 107:2177-2189.
15. Gibson, A., C.E. Futter, S. Maxwell, E.H. Allchin, M. Shipman, J. Kraehenbuhl, D. Domingo, G. Odorizzi, I.S. Trowbridge, and C.R. Hopkins. 1998. Sorting mechanisms regulating membrane protein traffic in the apical transcytotic pathway of polarized MDCK cells. J. Cell Biol. 143:81-94.
16. Green, S.A., K.P. Zimmer, G. Griffiths, and I. Mellman. 1987. Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins. J. Cell Biol. 105:1227-1240.
17. Gruenberg, J., and F.R. Maxfield. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
18. Hopkins, C.R. 1994. Internalization of polypeptide growth factor receptors and the regulation of transcription. Biochem. Pharmacol. 47:151-154.
19. Hopkins, C.R., and I.S, Trowbridge. 1983. Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells. J. Cell Biol. 97:508-521.
20. Hunziker, W., and P.J. Peters. 1998. Rab17 localizes to recycling endosomes and regulates receptor-mediated transcytosis in epithelial cells. J. Biol. Chem. 273:15734-15741.
21. Hunziker, W., J.A. Whitney, and I. Mellman. 1991. Selective inhibition of transcytosis by Brefeldin A in MDCK cells. Cell. 67:617-627.
22. Lai, A., A. Gibson, C.R. Hopkins, and I.S. Trowbridge. 1998. Signal-dependent trafficking of beta-amyloid precursor protein-transferrin receptor chimeras in Madin-Darby canine kidney cells. J. Biol. Chem. 273:3732-3739.
23. Lauffenburger, D.A., and A.R. French. 1996. Intracellular receptor/ligand sorting based on endosomal retenton components. Biotechnol. Bioeng. 51:281-297.
24. Lutcke, A., S. Jansson, R.G. Parton, P. Chavrier, A. Valencia, L.A. Huber, E. Lehtonen, and M. Zerial. 1993. Rab17, a novel small GTPase, is specific for epithelial cells and is induced during cell polarization. J. Cell Biol. 121:553-564.
25. Marsh, E.W., P.L. Loepold, N.L. Jones, and F.R. Maxfield. 1995. Oligomerized transferrin receptors are selectively retained by a lumenal sorting signal in a long-lived endocytic recycling compartment. J. Cell Biol. 129:1509-1522.
26. Matlin, K.S. 1992. W(h)ither default? Sorting and polarization in epithelial cells. Curr. Opin. Cell Biol. 4:623-628.
27. Matter, K., and I. Mellman. 1994. Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr. Opin. Cell Biol. 6:545-554.
28. Matter, K., W. Hunziker, and I. Mellman. 1992. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine dependent targeting determinants. Cell. 71:1-20.
29. Matter, K., J.A. Whitney, E. Miller, and I. Mellman. 1993. Common signals control LDL receptor sorting in endosomes and the Golgi of MDCK cells. Cell. 74:1053-1064.
30. Mayor, S., J.F. Presley, and F.R. Maxfield. 1993. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol. 121:1257-1269.
31. Mellman, I. 1996. Endocytosis and molecular sorting. Ann. Rev. Cell Dev. Biol. 12:575-625.
32. Mellman, I., and K. Simons. 1992. The Golgi complex: in vitro veritas? Cell. 68: 829-840.
33. Mostov, K.E. 1995. Regulation of protein traffic in polarized epithelial cells. Histol. Histopathol. 10:423-431.
34. Mostov, K.E., M. Friedlander, and G. Blobel. 1984. The receptor for transepithelial transport of IgA and IgM contains multiple immunoglobulin-like domains. Nature. 308:37-43.
35. Motulsky, H.J., and L.A. Ransnas. 1987. Fitting curves to data using nonlinear regression: a practical and nonmathematical review. FASEB (Fed. Am. Soc. Exp. Biol.) J. 1:365-374.
36. Odorizzi, G., A. Pearse, D. Domingo, I.S. Trowbridge, and C.R. Hopkins. 1996. Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J. Cell Biol. 135:139-152.
37. - cells. Som. Cell Mol. Genet. 14:473-487.
38. Owensby, D.A., P.A. Morton, and A.L. Schwartz. 1989. Quantitative evaluation of receptor-mediated endocytosis. Methods Cell Biol. 32:305-327.
39. Podbilewicz, B., and I. Mellman. 1990. ATP and cytosol requirements for transferrin recycling in intact and disrupted MDCK cells. EMBO (Eur. Mol. Biol. Organ.) J. 9:3477-3487.
40. Presley, J.F., S. Mayor, K.W. Dunn, L.S. Johnson, T.E. McGraw, and F.R. Maxfield. 1993. The End2 mutation in CHO cells slows the exit of transferrin receplors from the recycling compartment but bulk membrane recycling if unaffected. J. Cell Biol. 122:1231-1241.
41. Schaerer, E., F. Verrey, L. Racine, C. Tallichet, M. Reinhardt, and J.P. Kraehenbuhl. 1990. Polarized transport of the polymeric immunoglobulin receptor in transfected rabbit mammary epithelial cells. J. Cell Biol. 110:987-998.
42. Schmid, S.L., R. Fuchs, P. Male, and I. Mellman. 1988. Two distinct subpopulations of endosomes involved in membrane recycling and transport to lysosomes. Cell. 52:73-83.
43. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
44. Song, W., G. Apodaca, and K. Mostov. 1994. Transcylosis of the polymeric immunoglobulin receptor is regulated in multiple intracellular compartments. J. Biol. Chem. 269:29474-29480.
45. Sternweis, P.C., and A.G. Gilman. 1982. Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride. Proc. Natl. Acad. Sci. USA. 79:4888-4891.
46. Trowbridge, I.S., R.A. Newman, D.L. Domingo, and C. Sauvage. 1984. Transferrin receptors: structure and function. Biochem. Pharmacol. 33:925-932.
47. Ullrich, O., S. Reinsch, S. Urbe, M. Zerial, and R.G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913-924.
48. Wiley, H.S., and D.D. Cunningham. 1982. The endocytic rate constant. J. Biol. Chem. 257:4222-4229.
49. Yamashiro, D.J., B. Tycko, S.R. Fluss, and F.R. Maxfield. 1984. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell. 37:789-800.
50. Zacchi, P., H. Stenmark, R.G. Parton, D. Orioli, F. Lim, A. Giner, I. Mellman, M. Zerial, and C. Murphy. 1998. Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells. J. Cell Biol. 140:1039-1053.