Ras-Activated Endocytosis Is Mediated by the Rab5 Guanine Nucleotide Exchange Activity of RIN1

Developmental Cell

Volumn 1, Issue 1, 2001, Pages 73-82

  Tall, Gregory G ^a   Barbieri, M Alejandro ^b   Stahl, Philip D ^b   Horazdovsky, Bruce F ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; FUNGAL PROTEIN; RAB PROTEIN; RAS PROTEIN; RIN1 PROTEIN, MOUSE; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN; VPS9 PROTEIN, S CEREVISIAE;

ANIMAL; ARTICLE; CHEMISTRY; CHO CELL; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVE SITE; FIBROBLAST; GENE EXPRESSION; GENETICS; HAMSTER; IN VITRO STUDY; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; CARRIER PROTEINS; CATALYTIC DOMAIN; CHO CELLS; CRICETINAE; ENDOCYTOSIS; ENDOSOMES; FIBROBLASTS; FUNGAL PROTEINS; GENE EXPRESSION; MICE; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RAS PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 0035408008     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(01)00008-9     Document Type: Article

References (47)

1. Afar D.E.H., Han L., McLaughlin J., Wong S., Dhaka A., Parmar K., Rosenberg N., Witte O.N., Colicelli J. Regulation of the oncogenic activity of BCR-ABL by a tightly bound substrate protein RIN1. Immunity. 6:1997;773-782.
2. Agapov E.V., Frolov I., Lindenbach B.D., Prágai B.M., Schlesinger S., Rice C.M. Noncytopathic sindbis virus RNA vectors for heterologous gene expression. Proc. Natl. Acad. Sci. USA. 95:1998;12989-12994.
3. Baass P.C., Di Guglielmo G.M., Authier F., Posner B.I., Bergeron J.J.M. Compartmentalized signal transduction by receptor tyrosine kinases. Trends Cell Biol. 5:1995;465-470.
4. Bar-Sagi D., Feramisco J.R. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science. 233:1986;1061-1068.
5. Barbieri M.A., Hoffenberg S., Roberts R., Mukhopadhyay A., Pomrehn A., Dickey B.F., Stahl P.D. Evidence for a symmetrical requirement for Rab5-GTP in in vitro endosome-endosome fusion. J. Biol. Chem. 273:1998;25850-25855. a.
6. Barbieri M.A., Kohn A.D., Roth R.A., Stahl P.D. Protein Kinase B/akt and Rab5 mediate Ras activation of endocytosis. J. Biol. Chem. 273:1998;19367-19370. b.
7. Barbieri M.A., Roberts R., Gumusboga A., Highfield H., Alvarez-Dominguez C., Wells A., Stahl P.D. EGF and membrane trafficking. EGF receptor-activated endocytosis requires Rab5A J. Cell Biol. 151:2000;539-550.
8. Bucci C., Lütcke A., Steele-Mortimer O., Olkkonen V.M., Dupree P., Chiariello M., Bruni C.B., Simons K., Zerial M. Co-operative regulation of endocytosis by three rab5 isoforms. FEBS Lett. 366:1995;65-71.
9. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell. 70:1992;715-728.
10. Carpenter G., Cohen S. Epidermal growth factor. J. Biol. Chem. 265:1990;7709-7712.
11. Ceresa B.P., Schmid S.L. Regulation of signal transduction by endocytosis. Curr. Opin. Cell Biol. 12:2000;204-210.
12. Chen P., Gupta K., Wells A. Cell movement elicited by epidermal growth factor receptor requires kinase and autophosphorylation but is separable from mitogenesis. J. Cell Biol. 124:1994;547-555.
13. Chen W.S., Lazar C.S., Lund K.A., Welsh J.B., Chang C.P., Walton G.M., Der C.J., Wiley H.S., Gill G.N., Rosenfeld M.G. Functional independence of the epidermal growth factor receptor from a domain required for ligand-induced internalization and calcium regulation. Cell. 59:1989;33-43.
14. Cherniack A.D., Klarlund J.K., Czech M.P. Phosphorylation of the Ras nucleotide exchange factor son of sevenless by mitogen-activated protein kinase. J. Biol. Chem. 269:1994;4717-4720.
15. Colicelli J., Nicolette C., Birchmeier C., Rodgers L., Riggs M., Wigler M. Expression of three mammalian cDNAs that interfere with RAS function in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 88:1991;2913-2917.
16. de Vries-Smits A.M., Pronk G.J., Medema J.P., Burgering B.M., Bos J.L. Shc associates with an unphosphorylated form of the p21ras guanine nucleotide exchange factor mSOS. Oncogene. 10:1995;919-925.
17. Diaz R., Mayorga L.S., Stahl P.D. In vitro fusion of endosomes following receptor-mediated endocytosis. J. Biol. Chem. 263:1988;6093-6100.
18. Dong C., Waters S.B., Holt K.H., Pessin J.E. SOS phosphorylation and dissociation of the Grb2-SOS complex by ERK and JNK signaling pathways. J. Biol. Chem. 271:1996;6328-6332.
19. Ellis S., Mellor H. Regulation of endocytic traffic by Rho family GTPases. Trends Cell Biol. 10:2000;85-88.
20. Gorvel J.P., Chavier P., Zerial M., Gruenberg J. RAB5 controls early endosome fusion in vitro. Cell. 64:1991;915-925.
21. Haigler H.T., McKanna J.A., Cohen S. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J. Cell Biol. 81:1979;382-395.
22. Hama H., Tall G.G., Horazdovsky B.F. Vps9p is a guanine nucleotide exchange factor involved in vesicle-mediated vacuolar protein transport. J. Biol. Chem. 274:1999;15284-15291.
23. Han L., Colicelli J. A human protein selected for interference with Ras function interacts directly with Ras and competes with Raf1. Mol. Cell. Biol. 15:1995;1318-1323.
24. Han L., Wong D., Dhaka A., Afar D., White M., Xie W., Herschman H., Witte O., Colicelli J. Protein binding and signaling properties of RIN1 suggest a unique effector function. Proc. Nat. Acad. Sci. USA. 94:1997;4954-4959.
25. Hannon G.J., Demetrick D., Beach D. Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev. 7:1993;2378-2391.
26. ras in fibroblasts. J. Biol. Chem. 274:1999;34350-34360.
27. Horiuchi H., Lippe R., McBride H.M., Rubino M., Woodman P., Stenmark H., Rybin V., Wilm M., Ashman K., Mann M., Zerial M. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell. 90:1997;1149-1159.
28. Lamaze C., Chuang T.H., Terlecky L.J., Bokoch G.M., Schmid S.L. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature. 382:1996;177-179.
29. Langlois W.J., Sasaoka T., Saltiel A.R., Olefsky J.M. Negative feedback regulation and desensitization of insulin- and epidermal growth factor-stimulated p21ras activation. J. Biol. Chem. 270:1995;25320-25323.
30. Lemmon M.A., Schlessinger J. Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci. 19:1994;459-463.
31. Li G., D'Souza-Schorey C., Barbieri M.A., Roberts R.L., Klippel A., Williams L.T., Stahl P.D. Evidence for phosphatidyl 3-kinase as a regulator of endocytosis via activation of Rab5. Proc. Natl. Acad. Sci. USA. 92:1995;10207-10211.
32. Li G., D'Souza-Schorey D., Barbieri M.A., Cooper J.A., Stahl P.D. Uncoupling of membrane ruffling and pinocytosis during Ras signal transduction. J. Biol. Chem. 272:1997;10337-10340.
33. Mayorga L.S., Diaz R., Colombo M.I., Stahl P.D. GTPγS stimulation of endosome fusion suggests a role for a GTP-binding protein in the priming of vesicles before fusion. Cell Regul. 1:1989;113-124.
34. Mellman I. Endocytosis and Molecular Sorting. Annu. Rev. Cell Dev. Biol. 12:1996;575-625.
35. Ponting C.P., Benjamin D.R. A novel family of Ras-binding domains. Trends Biochem. Sci. 21:1996;422-425.
36. Porfiri E., McCormick F. Regulation of epidermal growth factor receptor signaling by phosphorylation of the ras exchange factor hSOS1. J. Biol. Chem. 271:1996;5871-5877.
37. Riese D.J. II, Stern D.F. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays. 20:1998;41-48.
38. Roberts R.L., Barbieri M.A., Pryse K.M., Chua M., Morisaki J.H., Stahl P.D. Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112:1999;3667-3675.
39. Rozakis A.M., van der Geer P., Mbamalu G., Pawson T. MAP kinase phosphorylation of mSos1 promotes dissociation of mSos1-Shc and mSos1-EGF receptor complexes. Oncogene. 11:1995;1417-1426.
40. Sorkin A., Waters C., Overholser K.O., Carpenter G. Multiple autophosphorylation site mutations of the epidermal growth factor receptor. J. Biol. Chem. 266:1991;8355-8362.
41. Stenmark H., Parton R.G., Steele-Mortimer O., Lutcke A., Gruenberg J., Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13:1994;1287-1296.
42. Tall G.G., Hama H., DeWald D.B., Horazdovsky B.F. The phosphatidylinositol 3-phosphate binding protein Vac1p interacts with a Rab GTPase and a Sec1p homologue to facilitate vesicle-mediated vacuolar protein sorting. Mol. Biol. Cell. 10:1999;1873-1889.
43. Vieira A.V., Lamaze C., Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 274:1996;2086-2089.
44. Vojtek A.B., Hollenberg S.M., Cooper J.A. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell. 74:1993;205-214.
45. Wells A. EGF receptor. Int. J. Biochem. Cell Biol. 31:1999;637-643.
46. Wells A., Welsh J.B., Lazar C.S., Wiley H.S., Gill G.N., Rosenfeld M.G. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science. 247:1990;962-964.
47. White M.A., Nicolette C., Minden A., Polverino A., Wan Aelst L., Karin M., Wigler M.H. Multiple Ras functions can contribute to mammalian cell transformation. Cell. 80:1995;533-541.