APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment

Cell

Volumn 116, Issue 3, 2004, Pages 445-456

  Miaczynska, Marta ^a   Christoforidis, Savvas ^a,e   Giner, Angelika ^a   Shevchenko, Anna ^a   Uttenweiler Joseph, Sandrine ^b,f   Habermann, Bianca ^a,d   Wilm, Matthias ^b   Parton, Robert G ^c   Zerial, Marino ^a  

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

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d Scionics Computer Innovation GmbH   (Germany)

^e UNIVERSITY OF IOANNINA   (Greece)

^f INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HISTONE DEACETYLASE; PROTEIN APPL1; PROTEIN APPL2; RAB PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENDOSOME; GENE EXPRESSION REGULATION; GENE STRUCTURE; HUMAN; HUMAN CELL; MITOGENESIS; MOLECULAR MODEL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

EID: 1642417606     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(04)00117-5     Document Type: Article

References (60)

1. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 16:2000;351-356.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST. a new generation of protein database search programs Nucleic Acids Res. 25:1997;3389-3402.
3. Barbieri M.A., Roberts R.L., Gumusboga A., Highfield H., Alvarez-Dominguez C., Wells A., Stahl P.D. Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a. J. Cell Biol. 151:2000;539-550.
4. 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.
5. Cavalli V., Vilbois F., Corti M., Marcote M.J., Tamura K., Karin M., Arkinstall S., Gruenberg J. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol. Cell. 7:2001;421-432.
6. Christoforidis S., McBride H.M., Burgoyne R.D., Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature. 397:1999;621-625. a.
7. Christoforidis S., Miaczynska M., Ashman K., Wilm M., Zhao L., Yip S.-C., Waterfield M.D., Backer J.M., Zerial M. Phosphoinositide-3-kinases are Rab5 effectors. Nat. Cell Biol. 1:1999;249-252. b.
8. Defize L.H., Boonstra J., Meisenhelder J., Kruijer W., Tertoolen L.G., Tilly B.C., Hunter T., van Bergen en Henegouwen P.M., Moolenaar W.H., de Laat S.W. Signal transduction by epidermal growth factor occurs through the subclass of high affinity receptors. J. Cell Biol. 109:1989;2495-2507.
9. Di Fiore P.P., De Camilli P. Endocytosis and signaling. an inseparable partnership Cell. 106:2001;1-4.
10. Dowler S., Currie R.A., Campbell D.G., Deak M., Kular G., Downes C.P., Alessi D.R. Identification of pleckstrin-homology-domain-containing proteins with novel phosphoinositide-binding specificities. Biochem. J. 351:2000;19-31.
11. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 411:2001;494-498.
12. Elliott K., Ge K., Du W., Prendergast G.C. The c-Myc-interacting adaptor protein Bin1 activates a caspase-independent cell death program. Oncogene. 19:2000;4669-4684.
13. Feng Q., Zhang Y. The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev. 15:2001;827-832.
14. Fischer, D., Barret, C., Bryson, K., Elofsson, A., Godzik, A., Jones, D., Karplus, K.J., Kelley, L.A., MacCallum, R.M., Pawowski, K., et al. (1999). CAFASP-1: critical assessment of fully automated structure prediction methods. Proteins (Suppl.), 209-217.
15. Forcet C., Ye X., Granger L., Corset V., Shin H., Bredesen D.E., Mehlen P. The dependence receptor DCC (deleted in colorectal cancer) defines an alternative mechanism for caspase activation. Proc. Natl. Acad. Sci. USA. 98:2001;3416-3421.
16. Grimes M.L., Zhou J., Beattie E.C., Yuen E.C., Hall D.E., Valletta J.S., Topp K.S., LaVail J.H., Bunnett N.W., Mobley W.C. Endocytosis of activated TrkA. evidence that nerve growth factor induces formation of signaling endosomes J. Neurosci. 16:1996;7950-7964.
17. Hayes S., Chawla A., Corvera S. TGF beta receptor internalization into EEA1-enriched early endosomes. role in signaling to Smad2 J. Cell Biol. 158:2002;1239-1249.
18. Horiuchi H., Lippé 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.
19. Humphrey G.W., Wang Y., Russanova V.R., Hirai T., Qin J., Nakatani Y., Howard B.H. Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1. J. Biol. Chem. 276:2001;6817-6824.
20. Johannessen L.E., Ringerike T., Molnes J., Madshus I.H. Epidermal growth factor receptor efficiently activates mitogen-activated protein kinase in HeLa cells and Hep2 cells conditionally defective in clathrin-dependent endocytosis. Exp. Cell Res. 260:2000;136-145.
21. Kao A.W., Ceresa B.P., Santeler S.R., Pessin J.E. Expression of a dominant interfering dynamin mutant in 3T3L1 adipocytes inhibits GLUT4 endocytosis without affecting insulin signaling. J. Biol. Chem. 273:1998;25450-25457.
22. Keino-Masu K., Masu M., Hinck L., Leonardo E.D., Chan S.S., Culotti J.G., Tessier-Lavigne M. Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell. 87:1996;175-185.
23. Lanzetti L., Rybin V., Malabarba M.G., Christoforidis S., Scita G., Zerial M., Di Fiore P.P. The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature. 408:2000;374-377.
24. Lippe R., Miaczynska M., Rybin V., Runge A., Zerial M. Functional synergy between Rab5 effector rabaptin-5 and exchange factor rabex-5 when physically associated in a complex. Mol. Biol. Cell. 12:2001;2219-2228.
25. Liu X., Erikson R.L. Polo-like kinase (Plk)1 depletion induces apoptosis in cancer cells. Proc. Natl. Acad. Sci. USA. 100:2003;5789-5794.
26. Liu J., Yao F., Wu R., Morgan M., Thorburn A., Finley R.L. Jr., Chen Y.Q. Mediation of the DCC apoptotic signal by DIP13 alpha. J. Biol. Chem. 277:2002;26281-26285.
27. Lu X., Horvitz H.R. lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell. 95:1998;981-991.
28. Lu Z., Murray J.T., Luo W., Li H., Wu X., Xu H., Backer J.M., Chen Y.G. Transforming growth factor beta activates Smad2 in the absence of receptor endocytosis. J. Biol. Chem. 277:2002;29363-29368.
29. Luetterforst R., Stang E., Zorzi N., Carozzi A., Way M., Parton R.G. Molecular characterization of caveolin association with the Golgi complex. identification of a cis-Golgi targeting domain in the caveolin molecule J. Cell Biol. 145:1999;1443-1459.
30. Luo J., Su F., Chen D., Shiloh A., Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature. 408:2000;377-381.
31. Martinu L., Santiago-Walker A., Qi H., Chou M.M. Endocytosis of epidermal growth factor receptor regulated by Grb2-mediated recruitment of the Rab5 GAP RN-tre. J. Biol. Chem. 277:2002;50996-51002.
32. McPherson P.S., Kay B.K., Hussain N.K. Signaling on the endocytic pathway. Traffic. 2:2001;375-384.
33. Miaczynska M., Zerial M. Mosaic organization of the endocytic pathway. Exp. Cell Res. 272:2002;8-14.
34. Mitsuuchi Y., Johnson S.W., Sonoda G., Tanno S., Golemis E.A., Testa J.R. Identification of a chromosome 3p14.3-21.1 gene, APPL, encoding an adaptor molecule that interacts with the oncoprotein-serine/threonine kinase AKT2. Oncogene. 18:1999;4891-4898.
35. Nakai K., Horton P. Psort. a program for detecting sorting signals in proteins and predicting their subcellular localization Trends Biochem. Sci. 24:1999;34-36.
36. Nielsen E., Christoforidis S., Uttenweiler-Joseph S., Miaczynska M., Dewitte F., Wilm M., Hoflack B., Zerial M. Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J. Cell Biol. 151:2000;601-612.
37. Panopoulou E., Gillooly D.J., Wrana J.L., Zerial M., Stenmark H., Murphy C., Fotsis T. Early endosomal regulation of Smad-dependent signaling in endothelial cells. J. Biol. Chem. 277:2002;18046-18052.
38. Pelkmans L., Kartenbeck J., Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:2001;473-483.
39. Rubino M., Miaczynska M., Lippe R., Zerial M. Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J. Biol. Chem. 275:2000;3745-3748.
40. Rybin V., Ullrich O., Rubino M., Alexandrov K., Simon I., Seabra M.C., Goody R., Zerial M. GTPase activity of rab5 acts as a timer for endocytic membrane fusion. Nature. 383:1996;266-269.
41. Ryseck R.P., MacDonald-Bravo H., Zerial M., Bravo R. Coordinate induction of fibronectin, fibronectin receptor, tropomyosin, and actin genes in serum-stimulated fibroblasts. Exp. Cell Res. 180:1989;537-545.
42. Sakamuro D., Elliott K.J., Wechsler-Reya R., Prendergast G.C. BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat. Genet. 14:1996;69-77.
43. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool. identification of signaling domains Proc. Natl. Acad. Sci. USA. 95:1998;5857-5864.
44. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 68:1996;850-858.
45. Shevchenko A., Chernushevich I., Ens W., Standing K.G., Thomson B., Wilm M., Mann M. Rapid 'de novo' peptide sequencing by a combination of nanoelectrospray, isotopic labeling and a quadrupole/time-of flight mass spectrometer. Rapid Commun. Mass Spectrom. 11:1997;1015-1024.
46. Simonsen A., Lippé R., Christoforidis S., Gaullier J.-M., Brech A., Callaghan J., Toh B.-H., Murphy C., Zerial M., Stenmark H. EEA1 links phosphatidylinositol 3-kinase function to Rab5 regulation of endosome fusion. Nature. 394:1998;494-498.
47. Sorkin A., Von Zastrow M. Signal transduction and endocytosis. close encounters of many kinds Nat. Rev. Mol. Cell Biol. 3:2002;600-614.
48. Stenmark H., Parton R.G., Steele-Mortimer O., Lütcke A., Gruenberg J., Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13:1994;1287-1296.
49. Tall G.G., Barbieri M.A., Stahl P.D., Horazdovsky B.F. Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell. 1:2001;73-82.
50. Tarricone C., Xiao B., Justin N., Walker P.A., Rittinger K., Gamblin S.J., Smerdon S.J. The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature. 411:2001;215-219.
51. Tsukazaki T., Chiang T.A., Davison A.F., Attisano L., Wrana J.L. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell. 95:1998;779-791.
52. Unhavaithaya Y., Shin T.H., Miliaras N., Lee J., Oyama T., Mello C.C. MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans. Cell. 111:2002;991-1002.
53. Van Aelst L., Joneson T., Bar-Sagi D. Identification of a novel Rac1-interacting protein involved in membrane ruffling. EMBO J. 15:1996;3778-3786.
54. Vieira A.V., Lamaze C., Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 274:1996;2086-2089.
55. Vousden K.H. p53. death star Cell. 103:2000;691-694.
56. Worthylake D.K., Rossman K.L., Sondek J. Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1. Nature. 408:2000;682-688.
57. Wunderlich W., Fialka I., Teis D., Alpi A., Pfeifer A., Parton R.G., Lottspeich F., Huber L.A. A novel 14-kilodalton protein interacts with the mitogen-activated protein kinase scaffold mp1 on a late endosomal/lysosomal compartment. J. Cell Biol. 152:2001;765-776.
58. Yarden Y. The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur. J. Cancer. 37(Suppl. 4):2001;S3-S8.
59. Yoshida M., Horinouchi S., Beppu T. Trichostatin A and trapoxin. novel chemical probes for the role of histone acetylation in chromatin structure and function Bioessays. 17:1995;423-430.
60. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2:2001;107-117.