Mitotic phosphorylation of rab4 prevents binding to a specific receptor on endosome membranes

EMBO Journal

Volumn 16, Issue 15, 1997, Pages 4497-4507

  Ayad, Nagi ^a   Hull, Michael ^a   Mellman, Ira ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endosomal membrane; GTPase; Mitosis; Phosphorylation; rab4

Indexed keywords

CELL MEMBRANE PROTEIN; CHAPERONE; ELASTASE; GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE; RAB PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSOL; ENDOSOME; MEMBRANE BINDING; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING;

ANIMALS; CDC2 PROTEIN KINASE; CHO CELLS; CRICETINAE; CYTOSOL; ENDOSOMES; GTP-BINDING PROTEINS; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; INTRACELLULAR MEMBRANES; KINETICS; MEMBRANE PROTEINS; MITOSIS; PANCREATIC ELASTASE; PHOSPHORYLATION; PROTEIN BINDING; RAB4 GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SOLUBILITY;

ANIMALIA;

EID: 0030835887     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.15.4497     Document Type: Article

References (41)

1. Amigorena, S., Drake, J., Webster, P. and Mellman, I. (1994) Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature, 369, 113-120.
2. Bailly, E., Touchot, N., Zahraoui, A., Goud, B. and Bornens, M. (1991) p34cdc2 protein kinase phosphorylates two small GTP-binding proteins of the rab family. Nature, 350, 715-718.
3. Bordier, C. (1981) Phase separation of integral membrane proteins in TX-114 solution. J. Biol. Chem., 256, 1604-1607.
4. Brennwald, P. and Novick, P. (1993) Interaction of three domains that distinguishing the Ras related GTP binding proteins Ypt1 from SEC4. Nature, 362, 557-560.
5. Bucci, C., Parton, R., Mather, I., Stunnenberg, H., Simons, K. and Zerial, M. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell, 70, 715-728.
6. Burton, J., Roberts, D., Montaldi, M., Novick, P. and DeCamilli, P. (1993) A mammalian guanine-nucleotide releasing protein enhances function of yeast secretory protein sec4. Nature, 361, 464-466.
7. Burton, J., Burns, M.E., Gatt, E., Augustine, G.J. and DeCamilli, P. (1994) Specific interactions of mss4 with members of the rab GTPase subfamily. EMBO J., 13, 5539-5546.
8. Chavrier, P. Vingron, M., Sander, C., Simons, K. and Zerial, M. (1990) Molecular cloning of YPT1/SEC4-related cDNAs from an epithelial cell line. Mol. Cell. Biol., 10, 6578-6585.
9. Chavrier, P., Gorvel, J.P., Stelzer, E., Simons, K., Gruenberg, J. and Zerial, M. (1991) Hypervariable C-terminal domain of rab proteins acts as a targeting signal. Nature, 353, 769-772.
10. Cormont, M., Tanti, J.F., Zahraoui, A., Van, O.E., Tavitian, A., Le, M. and Brustel, Y. (1993) Insulin and okadaic acid induce rab4 redistribution in adipocytes. J. Biol. Chem., 268, 19491-19497.
11. Daro, E., van der Sluijs, P., Galli, T. and Mellman, I. (1996) rab4 and cellubrevin define early endosome populations on the pathway of transferrin receptor recycling. Proc. Natl Acad. Sci. USA, 93, 9559-9564.
12. Dirac-Svejstrup, A., Soldati, T., Shapiro, A. and Pfeffer, S. (1995) rab-GDI presents functional rab9 to the intracellular transport machinery and contributes selectivity to rab9 membrane recruitment. J. Biol. Chem., 269, 15427-15430.
13. Featherstone, C., Griffiths, G. and Warren, G. (1985) Newly synthesized G protein of vesicular stomatitis virus is not transported to the Golgi complex in mitotic cells. J. Cell Biol., 101, 2036-2046.
14. Fuchs, R., Ellinger, A., Pavelka, M., Mellman, I. and Klapper, H. (1994) Rat liver endocytic coated vesicles do not exhibit ATP dependent acidification in vitro. Proc. Natl Acad. Sci. USA, 91, 4811-4815
15. Garrett, M.D., Zahner, J.E., Cheney, C.M. and Novick, P.J. (1994) GDI1 encodes a GDP dissociation inhibitor that plays an essential role in the yeast secretory pathway. EMBO J., 13, 1718-1728.
16. Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K. and Elledge, S.J. (1993) The p21 CDK-interacting protein Cip1 is a potent inhibitor of GF1 cyclin dependent kinases. Cell, 45, 805-815.
17. Horiuchi, H., Giner, A., Hoflack, B. and Zerial, M. (1995) A GDP/GTP exchange-stimulatory activity for the rab5-rabGDI complex on clathrin-coated vesicles from bovine brain. J. Biol. Chem., 270, 11257-11262.
18. Meyer, D. and Dobberstein, B. (1980) A membrane component essential for vectorial transport across the ER: requirement for extraction and reassociation with the membrane. J. Cell Biol., 87, 498-502.
19. Nigg, E.A. (1993) Cellular substrates of p34cdc2 kinase and its companion cyclin dependent kinases. Trends Cell Biol., 3, 296-301.
20. Novick, P. and Garrett, M.D. (1994) Vesicular transport: no exchange without receipt. Nature, 369, 18-19.
21. Peter, F., Nuoffer, C., Pind, S.N. and Balch, W.E. (1994) GDI is essential for rab1 function in budding from the ER and transport through the Golgi stack. J. Cell Biol., 126, 1393-1406.
22. Pfeffer, S.R. (1994) rab GTPases: master regulators of membrane trafficking. Curr. Opin. Cell Biol., 6, 522-526.
23. Pfeffer, S.R., Dirac-Svejstrup, A. and Soldati, T. (1995) rab GDP dissociation inhibitor: putting rab GTPases in the right place. J. Biol. Chem., 270, 17057-17059.
24. Rabouille, C., Levine, T., Peters, J. and Warren, G. (1995) An NSF-like ATPase, p97, and NSF mediate sisternal regrowth from mitotic Golgi fragments. Cell, 82, 905-914.
25. Sager, P., Brown, P.A. and Berlin, R.D. (1984) Analysis of transferrin recycling in mitotic and interphase HeLa cells by quantitative fluorescence microscopy. Cell, 39, 275-282.
26. Sasaki, T., Kikuchi, A., Araki, S., Hata, Y., Isomura, M., Kuroda, S. and Takai, Y. (1990) Purification and characterization from bovine brain cytosol of a protein that inhibits the dissociation of GDP from and the subsequent binding of GTP to smg p25A, a ras p21 like GTP-binding protein. J. Biol. Chem., 265, 2333-2337.
27. Schmid, S.L., Fuchs, R., Male, P. and Mellman, I. (1988) Two distinct subpopulations of endosomes involved in membrane recycling and transport to lysosomes. Cell, 52, 73-83.
28. Schmid, S., Fuchs, R., Kielian, M., Helenius, A. and Mellman, I. (1989) Acidification of endosome subpopulations in wild type chinese hamster ovary cells and temperature sensitive acidification mutants. J. Cell Biol., 10, 1291-1300.
29. Soldati, T., Riederer, M. and Pfeffer, S.R. (1993) rab GDI: a solubilizing and recycling factor for rab9 protein. Mol. Biol. Cell. 4, 425-434.
30. Soldati, T., Shapiro, A.D., Dirac-Svejstrup, A. and Pfeffer, S. (1994) Membrane targeting of the small GTPase rab9 is accompanied by nucleotide exchange. Nature, 369, 76-78.
31. Soldati, T., Rancano, C., Geissler, H. and Pfeffer, S. (1995a) rab7 and rab9 are recruited onto late endosomes by biochemically distinguishable processes. J. Biol. Chem., 270, 25541-25548.
32. Soldati, T., Shapiro, A. and Pfeffer, S. (1995b) Reconstitutution of rab9 endosomal targeting and nucleotide exchange using purified rab9-GDP dissociation inhibitor complexes and endosome-enriched membanes. Methods Enzymol., 257, 253-259.
33. Souter, E., Pypaert, M. and Warren, G. (1993) The Golgi stack reassembles during telophase before arrival of proteins transported from the ER. J. Cell Biol., 122, 533-540.
34. Ullrich, O., Stenmark, H., Alexandrov, K., Huber, L., Kaibuchi, K., Sasaki, T., Takai, Y. and Zerial, M. (1993) rab GDI as a general regulator for the membrane association of rab proteins. J. Biol. Chem., 268, 18143-18150.
35. Ullrich, O., Horiuchi, H., Bucci, C. and Zerial, M. (1994) Membrane association of rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange. Nature, 368, 157-160.
36. van der Sluijs, P., Hull, M., Zahraoui, A., Tavitian, A., Goud, B. and Mellman, I. (1991) The small GTP-binding protein rab4 is associated with early endosomes. Proc. Natl Acad. Sci. USA, 88, 6313-6317.
37. van der Sluijs, P., Hull, M., Huber, L., Male, P., Goud, B. and Mellman, I. (1992a) Reversible phosphorylation-dephosphorylation determines the localization of rab4 during the cell cycle. EMBO J., 11, 4379-4389.
38. van der Sluijs, P., Hull, M., Webster, P., Goud, B. and Mellman, I. (1992b) The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell, 70, 729-740.
39. Walter, P., Jackson, R., Marcus, M., Lingappa, V. and Blobel, G. (1979) Tryptic dissection and reconstitution of translocation activity for nascent presecretory proteins across microsomal membranes. Proc. Natl Acad. Sci. USA, 76, 1795-1799.
40. Warren, G. (1993) Membrane partitioning during cell division. Annu. Rev. Biochem., 62, 323-348.
41. Whitney, J.A., Gomez, M., Sheff, D., Kreis, T.E. and Mellman, I. (1995) Cytoplasmic coat proteins involved in endosome function. Cell, 83, 703-713.