CIN85 modulates TGFβ signaling by promoting the presentation of TGFβ receptors on the cell surface

Journal of Cell Biology

Volumn 210, Issue 2, 2015, Pages 319-332

  Yakymovych, Ihor ^a   Yakymovych, Mariya ^a   Zang, Guangxiang ^b   Mu, Yabing ^b   Bergh, Anders ^b   Landström, Maréne ^a,b   Heldin, Carl Henrik ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; MUTANT PROTEIN; PROTEIN CIN85; PROTEIN SH3; RAB11 PROTEIN; SMAD2 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; PROTEIN BINDING; RAB PROTEIN; SH3KBP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; ANIMAL; CELL MEMBRANE; CHLOROCEBUS AETHIOPS; COS CELL LINE; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; MALE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROSTATE TUMOR; PROTEIN ANALYSIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; HEK293 CELLS; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84957659710     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201411025     Document Type: Article

References (49)

1. Aissouni, Y., G. Zapart, J.L. Iovanna, I. Dikic, and P. Soubeyran. 2005. CIN85 regulates the ability of MEKK4 to activate the p38 MAP kinase pathway. Biochem. Biophys. Res. Commun. 338:808-814. http://dx.doi.org/10.1016/j.bbrc.2005.10.032.
2. Arancibia-Carcamo, I.L., B.P. Fairfax, S.J. Moss, and J.T. Kittler. 2006. Studying the localization, surface stability and endocytosis of neurotransmitter receptors by antibody labeling and biotinylation approaches. In The Dynamic Synapse: Molecular Methods in Ionotropic Receptor Biology. J.T. Kittler and S.J. Moss, editors. CRC Press, Boca Raton, FL. 91-118.
3. Bezsonova, I., M.C. Bruce, S. Wiesner, H. Lin, D. Rotin, and J.D. Forman-Kay. 2008. Interactions between the three CIN85 SH3 domains and ubiquitin: implications for CIN85 ubiquitination. Biochemistry. 47:8937-8949. http://dx.doi.org/10.1021/bi800439t.
4. Chen, Y.G. 2009. Endocytic regulation of TGF-β signaling. Cell Res. 19:58-70. http://dx.doi.org/10.1038/cr.2008.315.
5. Chen, X., M.J. Rubock, and M. Whitman. 1996. A transcriptional partner for MAD proteins in TGF-β signalling. Nature. 383:691-696. http://dx.doi.org/10.1038/383691a0.
6. Dennler, S., S. Itoh, D. Vivien, P. ten Dijke, S. Huet, and J.-M. Gauthier. 1998. Direct binding of Smad3 and Smad4 to critical TGFβ-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17:3091-3100. http://dx.doi.org/10.1093/emboj/17.11.3091.
7. Di Guglielmo, G.M., C. Le Roy, A.F. Goodfellow, and J.L. Wrana. 2003. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat. Cell Biol. 5:410-421. http://dx.doi.org/10.1038/ncb975.
8. Dikic, I. 2002. CIN85/CMS family of adaptor molecules. FEBS Lett. 529:110-115. http://dx.doi.org/10.1016/S0014-5793(02)03188-5.
9. Franzén, P., H. Ichijo, and K. Miyazono. 1993. Different signals mediate transforming growth factor-β1-induced growth inhibition and extracellular matrix production in prostatic carcinoma cells. Exp. Cell Res. 207:1-7. http://dx.doi.org/10.1006/excr.1993.1156.
10. Gebäck, T., M.M. Schulz, P. Koumoutsakos, and M. Detmar. 2009. TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. Biotechniques. 46:265-274.
11. Gleason, R.J., A.M. Akintobi, B.D. Grant, and R.W. Padgett. 2014. BMP signaling requires retromer-dependent recycling of the type I receptor. Proc. Natl. Acad. Sci. USA. 111:2578-2583. http://dx.doi.org/10.1073/pnas.1319947111.
12. Gout, I., G. Middleton, J. Adu, N.N. Ninkina, L.B. Drobot, V. Filonenko, G. Matsuka, A.M. Davies, M. Waterfield, and V.L. Buchman. 2000. Negative regulation of PI 3-kinase by Ruk, a novel adaptor protein. EMBO J. 19:4015-4025. http://dx.doi.org/10.1093/emboj/19.15.4015.
13. Havrylov, S., M.J. Redowicz, and V.L. Buchman. 2010. Emerging roles of Ruk/CIN85 in vesicle-mediated transport, adhesion, migration and malignancy. Traffic. 11:721-731. http://dx.doi.org/10.1111/j.1600-0854.2010.01061.x.
14. Heldin, C.-H., and A. Moustakas. 2012. Role of Smads in TGFβ signaling. Cell Tissue Res. 347:21-36. http://dx.doi.org/10.1007/s00441-011-1190-x.
15. Kardassis, D., C. Murphy, T. Fotsis, A. Moustakas, and C. Stournaras. 2009. Control of transforming growth factor βsignal transduction by small GTPases. FEBS J. 276:2947-2965. http://dx.doi.org/10.1111/j.1742-4658.2009.07031.x.
16. Karlsson, S., K. Kowanetz, A. Sandin, C. Persson, A. Ostman, C.H. Heldin, and C. Hellberg. 2006. Loss of T-cell protein tyrosine phosphatase induces recycling of the platelet-derived growth factor (PDGF) β-receptor but not the PDGF α-receptor. Mol. Biol. Cell. 17:4846-4855. http://dx.doi.org/10.1091/mbc. E06-04-0306.
17. Kim, J., D. Kang, B.K. Sun, J.-H. Kim, and J.J. Song. 2013. TRAIL/MEKK4/p38/HSP27/Akt survival network is biphasically modulated by the Src/CIN85/c-Cbl complex. Cell. Signal. 25:372-379. http://dx.doi.org/10.1016/j.cellsig.2012.10.010.
18. Kometani, K., T. Yamada, Y. Sasaki, T. Yokosuka, T. Saito, K. Rajewsky, M. Ishiai, M. Hikida, and T. Kurosaki. 2011. CIN85 drives B cell responses by linking BCR signals to the canonical NF-?B pathway. J. Exp. Med. 208:1447-1457. http://dx.doi.org/10.1084/jem.20102665.
19. Kowanetz, K., J. Terzic, and I. Dikic. 2003. Dab2 links CIN85 with clathrin-mediated receptor internalization. FEBS Lett. 554:81-87. http://dx.doi.org/10.1016/S0014-5793(03)01111-6.
20. Kowanetz, K., K. Husnjak, D. Höller, M. Kowanetz, P. Soubeyran, D. Hirsch, M.H.H. Schmidt, K. Pavelic, P. De Camilli, P.A. Randazzo, and I. Dikic. 2004. CIN85 associates with multiple effectors controlling intracellular trafficking of epidermal growth factor receptors. Mol. Biol. Cell. 15:3155-3166. http://dx.doi.org/10.1091/mbc. E03-09-0683.
21. Lin, H.-K., S. Bergmann, and P.P. Pandolfi. 2004. Cytoplasmic PML function in TGF-β signalling. Nature. 431:205-211. http://dx.doi.org/10.1038/nature02783.
22. Lynch, D.K., S.C. Winata, R.J. Lyons, W.E. Hughes, G.M. Lehrbach, V. Wasinger, G. Corthals, S. Cordwell, and R.J. Daly. 2003. A Cortactin-CD2-associated protein (CD2AP) complex provides a novel link between epidermal growth factor receptor endocytosis and the actin cytoskeleton. J. Biol. Chem. 278:21805-21813. http://dx.doi.org/10.1074/jbc. M211407200.
23. Massagué, J. 2008. TGFβ in cancer. Cell. 134:215-230. http://dx.doi.org/10.1016/j.cell.2008.07.001.
24. Mishra, L., and B. Marshall. 2006. Adaptor proteins and ubiquinators in TGF-β signaling. Cytokine Growth Factor Rev. 17:75-87. http://dx.doi.org/10.1016/j.cytogfr.2005.09.001.
25. Mitchell, H., A. Choudhury, R.E. Pagano, and E.B. Leof. 2004. Liganddependent and-independent transforming growth factor-βreceptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol. Biol. Cell. 15:4166-4178. http://dx.doi.org/10.1091/mbc. E04-03-0245.
26. Mu, Y., R. Sundar, N. Thakur, M. Ekman, S.K. Gudey, M. Yakymovych, A. Hermansson, H. Dimitriou, M.T. Bengoechea-Alonso, J. Ericsson, et al. 2011. TRAF6 ubiquitinates TGFβ type I receptor to promote its cleavage and nuclear translocation in cancer. Nat. Commun. 2:330. http://dx.doi.org/10.1038/ncomms1332.
27. Mu, Y., S.K. Gudey, and M. Landström. 2012. Non-Smad signaling pathways. Cell Tissue Res. 347:11-20. http://dx.doi.org/10.1007/s00441-011-1201-y.
28. Narita, T., T. Nishimura, K. Yoshizaki, and T. Taniyama. 2005. CIN85 associates with TNF receptor 1 via Src and modulates TNF-α-induced apoptosis. Exp. Cell Res. 304:256-264. http://dx.doi.org/10.1016/j.yexcr.2004.11.005.
29. Ostrom, R.S., and P.A. Insel. 2006. Methods for the study of signaling molecules in membrane lipid rafts and caveolae. Methods Mol. Biol. 332:181-191.
30. Penheiter, S.G., R.D. Singh, C.E. Repellin, M.C. Wilkes, M. Edens, P.H. Howe, R.E. Pagano, and E.B. Leof. 2010. Type II transforming growth factor-β receptor recycling is dependent upon the clathrin adaptor protein Dab2. Mol. Biol. Cell. 21:4009-4019. http://dx.doi.org/10.1091/mbc. E09-12-1019.
31. Persson, U., H. Izumi, S. Souchelnytskyi, S. Itoh, S. Grimsby, U. Engström, C.H. Heldin, K. Funa, and P. ten Dijke. 1998. The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434:83-87. http://dx.doi.org/10.1016/S0014-5793(98)00954-5.
32. Peruzzi, G., R. Molfetta, F. Gasparrini, L. Vian, S. Morrone, M. Piccoli, L. Frati, A. Santoni, and R. Paolini. 2007. The adaptor molecule CIN85 regulates Syk tyrosine kinase level by activating the ubiquitin-proteasome degradation pathway. J. Immunol. 179:2089-2096. http://dx.doi.org/10.4049/jimmunol.179.4.2089.
33. Petrelli, A., G.F. Gilestro, S. Lanzardo, P.M. Comoglio, N. Migone, and S. Giordano. 2002. The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature. 416:187-190. http://dx.doi.org/10.1038/416187a.
34. Rønning, S.B., N.M. Pedersen, I.H. Madshus, and E. Stang. 2011. CIN85 regulates ubiquitination and degradative endosomal sorting of the EGF receptor. Exp. Cell Res. 317:1804-1816. http://dx.doi.org/10.1016/j.yexcr.2011.05.016.
35. Schroeder, B., S.G. Weller, J. Chen, D. Billadeau, and M.A. McNiven. 2010. A Dyn2-CIN85 complex mediates degradative traffic of the EGFR by regulation of late endosomal budding. EMBO J. 29:3039-3053. http://dx.doi.org/10.1038/emboj.2010.190.
36. Schroeder, B., S. Srivatsan, A. Shaw, D. Billadeau, and M.A. McNiven. 2012. CIN85 phosphorylation is essential for EGFR ubiquitination and sorting into multivesicular bodies. Mol. Biol. Cell. 23:3602-3611. http://dx.doi.org/10.1091/mbc. E11-08-0666.
37. Shimokawa, N., K. Haglund, S.M. Hölter, C. Grabbe, V. Kirkin, N. Koibuchi, C. Schultz, J. Rozman, D. Hoeller, C.-H. Qiu, et al. 2010. CIN85 regulates dopamine receptor endocytosis and governs behaviour in mice. EMBO J. 29:2421-2432. http://dx.doi.org/10.1038/emboj.2010.120.
38. Sorrentino, A., N. Thakur, S. Grimsby, A. Marcusson, V. von Bulow, N. Schuster, S. Zhang, C.-H. Heldin, and M. Landström. 2008. The type I TGF-β receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat. Cell Biol. 10:1199-1207. http://dx.doi.org/10.1038/ncb1780.
39. Soubeyran, P., K. Kowanetz, I. Szymkiewicz, W.Y. Langdon, and I. Dikic. 2002. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature. 416:183-187. http://dx.doi.org/10.1038/416183a.
40. Sundar, R., S.K. Gudey, C.H. Heldin, and M. Landström. 2015. TRAF6 promotes TGFβ-induced invasion and cell-cycle regulation via Lys63-linked polyubiquitination of Lys178 in TGFβ type I receptor. Cell Cycle. 14:554-565. http://dx.doi.org/10.4161/15384101.2014.990302.
41. Szymkiewicz, I., K. Kowanetz, P. Soubeyran, A. Dinarina, S. Lipkowitz, and I. Dikic. 2002. CIN85 participates in Cbl-b-mediated down-regulation of receptor tyrosine kinases. J. Biol. Chem. 277:39666-39672. http://dx.doi.org/10.1074/jbc. M205535200.
42. Szymkiewicz, I., O. Shupliakov, and I. Dikic. 2004. Cargo-and compartment-selective endocytic scaffold proteins. Biochem. J. 383:1-11. http://dx.doi.org/10.1042/BJ20040913.
43. Thompson, T.C., L.D. Truong, T.L. Timme, D. Kadmon, B.K. McCune, K.C. Flanders, P.T. Scardino, and S.H. Park. 1992. Transforming growth factor β1 as a biomarker for prostate cancer. J. Cell. Biochem. Suppl. 16H:54-61. http://dx.doi.org/10.1002/jcb.240501212.
44. Watanabe, S., H. Take, K. Takeda, Z.X. Yu, N. Iwata, and S. Kajigaya. 2000. Characterization of the CIN85 adaptor protein and identification of components involved in CIN85 complexes. Biochem. Biophys. Res. Commun. 278:167-174. http://dx.doi.org/10.1006/bbrc.2000.3760.
45. Xu, P., J. Liu, and R. Derynck. 2012. Post-translational regulation of TGF-β receptor and Smad signaling. FEBS Lett. 586:1871-1884. http://dx.doi.org/10.1016/j.febslet.2012.05.010.
46. Yakymovych, I., P. Ten Dijke, C.-H. Heldin, and S. Souchelnytskyi. 2001. Regulation of Smad signaling by protein kinase C. FASEB J. 15:553-555.
47. Yamashita, M., K. Fatyol, C. Jin, X. Wang, Z. Liu, and Y.E. Zhang. 2008. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-β. Mol. Cell. 31:918-924. http://dx.doi.org/10.1016/j.molcel.2008.09.002.
48. Zhang, J., X. Zheng, X. Yang, and K. Liao. 2009. CIN85 associates with endosomal membrane and binds phosphatidic acid. Cell Res. 19:733-746. http://dx.doi.org/10.1038/cr.2009.51.
49. Zhu, L., L. Wang, X. Luo, Y. Zhang, Q. Ding, X. Jiang, X. Wang, Y. Pan, and Y. Chen. 2012. Tollip, an intracellular trafficking protein, is a novel modulator of the transforming growth factor-β signaling pathway. J. Biol. Chem. 287:39653-39663. http://dx.doi.org/10.1074/jbc. M112.388009.