Rin-like, a novel regulator of endocytosis, acts as guanine nucleotide exchange factor for Rab5a and Rab22

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 6, 2011, Pages 1198-1210

  Woller, Barbara ^a   Luiskandl, Susan ^a   Popovic, Milica ^b   Prieler, Barbara E M ^a   Ikonge, Gloria ^a   Mutzl, Michaela ^a   Rehmann, Holger ^b   Herbst, Ruth ^a  

^a Medical University of Vienna   (Austria)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Endocytosis; GEF; MuSK; Rab5; Receptor tyrosine kinase

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; RAB22 PROTEIN; RAB5A PROTEIN; RIN LIKE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETON; ENDOCYTOSIS; EPIDERMAL GROWTH FACTOR; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOBLOTTING; MICE; MICROSCOPY, CONFOCAL; PROTEIN BINDING; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RATS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CHOLINERGIC; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 79955700248     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.03.005     Document Type: Article

References (49)

1. Carney D.S., Davies B.A., Horazdovsky B.F. Vps9 domain-containing proteins: activators of Rab5 GTPases from yeast to neurons. Trends Cell Biol. 2006, 16:27-35.
2. Han L., Colicelli J. A human protein selected for interference with Ras function interacts directly with Ras and competes with Raf1. Mol. Cell. Biol. 1995, 15:1318-1323.
3. 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 2001, 1:73-82.
4. 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. 1999, 274:15284-15291.
5. Vitale G., Alexandrov K., Ullrich O., Horiuchi H., Giner A., Dobson C., Baykova O., Gournier H., Stenmark H., Zerial M. The GDP/GTP cycle of Rab5 in the regulation of endocytotic membrane traffic. Cold Spring Harb. Symp. Quant. Biol. 1995, 60:211-220.
6. Delprato A., Merithew E., Lambright D.G. Structure, exchange determinants, and family-wide rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell 2004, 118:607-617.
7. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. reviews 2001, 2:107-117.
8. Kauppi M., Simonsen A., Bremnes B., Vieira A., Callaghan J., Stenmark H., Olkkonen V.M. The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J. Cell Sci. 2002, 115:899-911.
9. Simpson J.C., Griffiths G., Wessling-Resnick M., Fransen J.A., Bennett H., Jones A.T. A role for the small GTPase Rab21 in the early endocytic pathway. J. Cell Sci. 2004, 117:6297-6311.
10. Weigert R., Yeung A.C., Li J., Donaldson J.G. Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol. Biol. Cell 2004, 15:3758-3770.
11. Opdam F.J., Echard A., Croes H.J., van den Hurk J.A., van de Vorstenbosch R.A., Ginsel L.A., Goud B., Fransen J.A. The small GTPase Rab6B, a novel Rab6 subfamily member, is cell-type specifically expressed and localised to the Golgi apparatus. J. Cell Sci. 2000, 113(Pt 15):2725-2735.
12. Barbieri M.A., Kong C., Chen P.I., Horazdovsky B.F., Stahl P.D. The SRC homology 2 domain of Rin1 mediates its binding to the epidermal growth factor receptor and regulates receptor endocytosis. J. Biol. Chem. 2003, 278:32027-32036.
13. Deininger K., Eder M., Kramer E.R., Zieglgansberger W., Dodt H.U., Dornmair K., Colicelli J., Klein R. The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc. Natl Acad. Sci. U.S.A. 2008, 105:12539-12544.
14. Hunker C.M., Giambini H., Galvis A., Hall J., Kruk I., Veisaga M.L., Barbieri M.A. Rin1 regulates insulin receptor signal transduction pathways. Exp. Cell Res. 2006, 312:1106-1118.
15. Kajiho H., Saito K., Tsujita K., Kontani K., Araki Y., Kurosu H., Katada T. RIN3: a novel Rab5 GEF interacting with amphiphysin II involved in the early endocytic pathway. J. Cell Sci. 2003, 116:4159-4168.
16. Lai W.H., Cameron P.H., Wada I., Doherty J.J., Kay D.G., Posner B.I., Bergeron J.J. Ligand-mediated internalization, recycling, and downregulation of the epidermal growth factor receptor in vivo. J. Cell Biol. 1989, 109:2741-2749.
17. Sorkin A., von Zastrow M. Endocytosis and signalling: intertwining molecular networks. Nat. reviews 2009, 10:609-622.
18. Wu H., Xiong W., Lin M. To build a synapse: signaling pathways in neuromuscular junction assembly. Dev. Camb. Engl. 2010, 137:1017-1033.
19. Glass D.J., Bowen D.C., Stitt T.N., Radziejewski C., Bruno J., Ryan T.E., Gies D.R., Shah S., Mattsson K., Burden S.J., DiStefano P.S., Valenzuela D.M., DeChiara T.M., Yancopoulos G.D. Agrin acts via a MuSK receptor complex. Cell 1996, 85:513-523.
20. Kim N., Stiegler A.L., Cameron T.O., Hallock P.T., Gomez A.M., Huang J.H., Hubbard S.R., Dustin M.L., Burden S.J. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 2008, 135:334-342.
21. Zhang B., Luo S., Wang Q., Suzuki T., Xiong W.C., Mei L. LRP4 serves as a coreceptor of agrin. Neuron 2008, 60:285-297.
22. DeChiara T.M., Bowen D.C., Valenzuela D.M., Simmons M.V., Poueymirou W.T., Thomas S., Kinetz E., Compton D.L., Rojas E., Park J.S., Smith C., DiStefano P.S., Glass D.J., Burden S.J., Yancopoulos G.D. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 1996, 85:501-512.
23. Gautam M., Noakes P.G., Moscoso L., Rupp F., Scheller R.H., Merlie J.P., Sanes J.R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 1996, 85:525-535.
24. Weatherbee S.D., Anderson K.V., Niswander L.A. LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Dev. Camb. Engl. 2006, 133:4993-5000.
25. Watty A., Neubauer G., Dreger M., Zimmer M., Wilm M., Burden S.J. The in vitro and in vivo phosphotyrosine map of activated MuSK. Proc. Natl Acad. Sci. U.S.A. 2000, 97:4585-4590.
26. Mossier B., Togel M., Fuchs K., Sieghart W. Immunoaffinity purification of gamma-aminobutyric acidA (GABAA) receptors containing gamma 1-subunits. Evidence for the presence of a single type of gamma-subunit in GABAA receptors. J. Biol. Chem. 1994, 269:25777-25782.
27. Herbst R., Burden S.J. The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J. 2000, 19:67-77.
28. Glass D.J., Apel E.D., Shah S., Bowen D.C., DeChiara T.M., Stitt T.N., Sanes J.R., Yancopoulos G.D. Kinase domain of the muscle-specific receptor tyrosine kinase (MuSK) is sufficient for phosphorylation but not clustering of acetylcholine receptors: required role for the MuSK ectodomain?. Proc. Natl Acad. Sci. U.S.A. 1997, 94:8848-8853.
29. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 1987, 7:2745-2752.
30. Schaeper U., Gehring N.H., Fuchs K.P., Sachs M., Kempkes B., Birchmeier W. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J. Cell Biol. 2000, 149:1419-1432.
31. Lumeng C., Phelps S., Crawford G.E., Walden P.D., Barald K., Chamberlain J.S. Interactions between beta 2-syntrophin and a family of microtubule-associated serine/threonine kinases. Nat. Neurosci. 1999, 2:611-617.
32. Vojtek A.B., Hollenberg S.M. Ras-Raf interaction: two-hybrid analysis. Meth. Enzymol. 1995, 255:331-342.
33. Nizhynska V., Neumueller R., Herbst R. Phosphoinositide 3-kinase acts through RAC and Cdc42 during agrin-induced acetylcholine receptor clustering. Dev. Neurobiol. 2007, 67:1047-1058.
34. Schnatwinkel C., Christoforidis S., Lindsay M.R., Uttenweiler-Joseph S., Wilm M., Parton R.G., Zerial M. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2004, 2:E261.
35. Rehmann H. Characterization of the activation of the Rap-specific exchange factor Epac by cyclic nucleotides. Meth. Enzymol. 2006, 407:159-173.
36. Zhou H., Glass D.J., Yancopoulos G.D., Sanes J.R. Distinct domains of MuSK mediate its abilities to induce and to associate with postsynaptic specializations. J. Cell Biol. 1999, 146:1133-1146.
37. Saito K., Murai J., Kajiho H., Kontani K., Kurosu H., Katada T. A novel binding protein composed of homophilic tetramer exhibits unique properties for the small GTPase Rab5. J. Biol. Chem. 2002, 277:3412-3418.
38. Pereira-Leal J.B., Seabra M.C. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 2001, 313:889-901.
39. Kong C., Su X., Chen P.I., Stahl P.D. Rin1 interacts with signal-transducing adaptor molecule (STAM) and mediates epidermal growth factor receptor trafficking and degradation. J. Biol. Chem. 2007, 282:15294-15301.
40. Bromann P.A., Weiner J.A., Apel E.D., Lewis R.M., Sanes J.R. A putative ariadne-like E3 ubiquitin ligase (PAUL) that interacts with the muscle-specific kinase (MuSK). Gene Expr. Patterns 2004, 4:77-84.
41. Lu Z., Je H.S., Young P., Gross J., Lu B., Feng G. Regulation of synaptic growth and maturation by a synapse-associated E3 ubiquitin ligase at the neuromuscular junction. J. Cell Biol. 2007, 177:1077-1089.
42. Zhu D., Yang Z., Luo Z., Luo S., Xiong W.C., Mei L. Muscle-specific receptor tyrosine kinase endocytosis in acetylcholine receptor clustering in response to agrin. J. Neurosci. 2008, 28:1688-1696.
43. Garcia-Osta A., Tsokas P., Pollonini G., Landau E.M., Blitzer R., Alberini C.M. MuSK expressed in the brain mediates cholinergic responses, synaptic plasticity, and memory formation. J. Neurosci. 2006, 26:7919-7932.
44. Barbieri M.A., Fernandez-Pol S., Hunker C., Horazdovsky B.H., Stahl P.D. Role of rab5 in EGF receptor-mediated signal transduction. Eur. J. Cell Biol. 2004, 83:305-314.
45. Wang Y., Waldron R.T., Dhaka A., Patel A., Riley M.M., Rozengurt E., Colicelli J. The RAS effector RIN1 directly competes with RAF and is regulated by 14-3-3 proteins. Mol. Cell. Biol. 2002, 22:916-926.
46. Delprato A., Lambright D.G. Structural basis for Rab GTPase activation by VPS9 domain exchange factors. Nat. Struct. Mol. Biol. 2007, 14:406-412.
47. Bos J.L., Rehmann H., Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007, 129:865-877.
48. Doherty G.J., McMahon H.T. Mechanisms of endocytosis. Annu. Rev. Biochem. 2009, 78:857-902.
49. Orth J.D., McNiven M.A. Get off my back! Rapid receptor internalization through circular dorsal ruffles. Cancer Res. 2006, 66:11094-11096.