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Cbl promotes clustering of endocytic adaptor proteins.

Jozic D, Cárdenes N, Deribe YL, Moncalián G, Hoeller D, Groemping Y, Dikic I, Rittinger K, Bravo J
Nat Struct Mol Biol 12 972-9 (2005)
Cited: 42 times
EuropePMC logo PMID: 16228008

Abstract

The ubiquitin ligases c-Cbl and Cbl-b play a crucial role in receptor downregulation by mediating multiple monoubiquitination of receptors and promoting their sorting for lysosomal degradation. Their function is modulated through interactions with regulatory proteins including CIN85 and PIX, which recognize a proline-arginine motif in Cbl and thus promote or inhibit receptor endocytosis. We report the structures of SH3 domains of CIN85 and beta-PIX in complex with a proline-arginine peptide from Cbl-b. Both structures reveal a heterotrimeric complex containing two SH3 domains held together by a single peptide. Trimerization also occurs in solution and is facilitated by the pseudo-symmetrical peptide sequence. Moreover, ternary complexes of CIN85 and Cbl are formed in vivo and are important for the ability of Cbl to promote epidermal growth factor receptor (EGFR) downregulation. These results provide molecular explanations for a novel mechanism by which Cbl controls receptor downregulation.

Articles - 2ak5 mentioned but not cited (3)

  1. High-resolution global peptide-protein docking using fragments-based PIPER-FlexPepDock. Alam N, Goldstein O, Xia B, Porter KA, Kozakov D, Schueler-Furman O. PLoS Comput Biol 13 e1005905 (2017)
  2. Differential Recognition Preferences of the Three Src Homology 3 (SH3) Domains from the Adaptor CD2-associated Protein (CD2AP) and Direct Association with Ras and Rab Interactor 3 (RIN3). Rouka E, Simister PC, Janning M, Kumbrink J, Konstantinou T, Muniz JR, Joshi D, O'Reilly N, Volkmer R, Ritter B, Knapp S, von Delft F, Kirsch KH, Feller SM. J Biol Chem 290 25275-25292 (2015)
  3. dMM-PBSA: A New HADDOCK Scoring Function for Protein-Peptide Docking. Spiliotopoulos D, Kastritis PL, Melquiond AS, Bonvin AM, Musco G, Rocchia W, Spitaleri A. Front Mol Biosci 3 46 (2016)


Reviews citing this publication (7)

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  4. Proline-rich regions and motifs in trafficking: from ESCRT interaction to viral exploitation. Ren X, Hurley JH. Traffic 12 1282-1290 (2011)
  5. E3 ubiquitin ligase Cbl-b in innate and adaptive immunity. Liu Q, Zhou H, Langdon WY, Zhang J. Cell Cycle 13 1875-1884 (2014)
  6. Molecular structures of coat and coat-associated proteins: function follows form. Brett TJ, Traub LM. Curr Opin Cell Biol 18 395-406 (2006)
  7. Malfunctions within the Cbl interactome uncouple receptor tyrosine kinases from destructive transport. Dikic I, Schmidt MHH. Eur J Cell Biol 86 505-512 (2007)

Articles citing this publication (32)

  1. Structural basis for recognition of arginine methylated Piwi proteins by the extended Tudor domain. Liu K, Chen C, Guo Y, Lam R, Bian C, Xu C, Zhao DY, Jin J, MacKenzie F, Pawson T, Min J. Proc Natl Acad Sci U S A 107 18398-18403 (2010)
  2. Cool-1 functions as an essential regulatory node for EGF receptor- and Src-mediated cell growth. Feng Q, Baird D, Peng X, Wang J, Ly T, Guan JL, Cerione RA. Nat Cell Biol 8 945-956 (2006)
  3. Dysregulation of Rho GTPases in the αPix/Arhgef6 mouse model of X-linked intellectual disability is paralleled by impaired structural and synaptic plasticity and cognitive deficits. Ramakers GJ, Wolfer D, Rosenberger G, Kuchenbecker K, Kreienkamp HJ, Prange-Kiel J, Rune G, Richter K, Langnaese K, Masneuf S, Bösl MR, Fischer KD, Krugers HJ, Lipp HP, van Galen E, Kutsche K. Hum Mol Genet 21 268-286 (2012)
  4. Molecular mechanisms of ubiquitin-dependent membrane traffic. Hurley JH, Stenmark H. Annu Rev Biophys 40 119-142 (2011)
  5. Ubiquitinylation of Ig beta dictates the endocytic fate of the B cell antigen receptor. Zhang M, Veselits M, O'Neill S, Hou P, Reddi AL, Berlin I, Ikeda M, Nash PD, Longnecker R, Band H, Clark MR. J Immunol 179 4435-4443 (2007)
  6. Cell density-dependent inhibition of epidermal growth factor receptor signaling by p38alpha mitogen-activated protein kinase via Sprouty2 downregulation. Swat A, Dolado I, Rojas JM, Nebreda AR. Mol Cell Biol 29 3332-3343 (2009)
  7. Crystal structure of the SH3 domain of betaPIX in complex with a high affinity peptide from PAK2. Hoelz A, Janz JM, Lawrie SD, Corwin B, Lee A, Sakmar TP. J Mol Biol 358 509-522 (2006)
  8. CIN85 regulates dopamine receptor endocytosis and governs behaviour in mice. Shimokawa N, Haglund K, Hölter SM, Grabbe C, Kirkin V, Koibuchi N, Schultz C, Rozman J, Hoeller D, Qiu CH, Londoño MB, Ikezawa J, Jedlicka P, Stein B, Schwarzacher SW, Wolfer DP, Ehrhardt N, Heuchel R, Nezis I, Brech A, Schmidt MHH, Fuchs H, Gailus-Durner V, Klingenspor M, Bogler O, Wurst W, Deller T, de Angelis MH, Dikic I. EMBO J 29 2421-2432 (2010)
  9. Cbl escapes Cdc42-mediated inhibition by downregulation of the adaptor molecule betaPix. Schmidt MHH, Husnjak K, Szymkiewicz I, Haglund K, Dikic I. Oncogene 25 3071-3078 (2006)
  10. Structural basis for ubiquitin recognition by SH3 domains. He Y, Hicke L, Radhakrishnan I. J Mol Biol 373 190-196 (2007)
  11. CIN85 associates with endosomal membrane and binds phosphatidic acid. Zhang J, Zheng X, Yang X, Liao K. Cell Res 19 733-746 (2009)
  12. Abi-1 forms an epidermal growth factor-inducible complex with Cbl: role in receptor endocytosis. Tanos BE, Pendergast AM. Cell Signal 19 1602-1609 (2007)
  13. SH3KBP1-binding protein 1 prevents epidermal growth factor receptor degradation by the interruption of c-Cbl-CIN85 complex. Feng L, Wang JT, Jin H, Qian K, Geng JG. Cell Biochem Funct 29 589-596 (2011)
  14. Structural basis for ASPP2 recognition by the tumor suppressor p73. Canning P, von Delft F, Bullock AN. J Mol Biol 423 515-527 (2012)
  15. Cbl E3 Ligase Mediates the Removal of Nectin-1 from the Surface of Herpes Simplex Virus 1-Infected Cells. Deschamps T, Dogrammatzis C, Mullick R, Kalamvoki M. J Virol 91 e00393-17 (2017)
  16. The promiscuous binding of the Fyn SH3 domain to a peptide from the NS5A protein. Martin-Garcia JM, Luque I, Ruiz-Sanz J, Camara-Artigas A. Acta Crystallogr D Biol Crystallogr 68 1030-1040 (2012)
  17. Inhibition of CIN85-mediated invasion by a novel SH3 domain binding motif in the lysyl oxidase propeptide. Sato S, Zhao Y, Imai M, Simister PC, Feller SM, Trackman PC, Kirsch KH, Sonenshein GE. PLoS One 8 e77288 (2013)
  18. Isoform-selective interaction of the adaptor protein Tks5/FISH with Sos1 and dynamins. Rufer AC, Rumpf J, von Holleben M, Beer S, Rittinger K, Groemping Y. J Mol Biol 390 939-950 (2009)
  19. The adaptor protein CIN85 assembles intracellular signaling clusters for B cell activation. Kühn J, Wong LE, Pirkuliyeva S, Schulz K, Schwiegk C, Fünfgeld KG, Keppler S, Batista FD, Urlaub H, Habeck M, Becker S, Griesinger C, Wienands J. Sci Signal 9 ra66 (2016)
  20. The high resolution NMR structure of the third SH3 domain of CD2AP. Ortega Roldan JL, Romero Romero ML, Ora A, Ab E, Lopez Mayorga O, Azuaga AI, van Nuland NA. J Biomol NMR 39 331-336 (2007)
  21. c-Cbl regulates αPix-mediated cell migration and invasion. Seong MW, Park JH, Yoo HM, Yang SW, Oh KH, Ka SH, Park DE, Lee ST, Chung CH. Biochem Biophys Res Commun 455 153-158 (2014)
  22. High-resolution crystal structure of spectrin SH3 domain fused with a proline-rich peptide. Gushchina LV, Gabdulkhakov AG, Nikonov SV, Filimonov VV. J Biomol Struct Dyn 29 485-495 (2011)
  23. Molecular basis of interactions between SH3 domain-containing proteins and the proline-rich region of the ubiquitin ligase Itch. Desrochers G, Cappadocia L, Lussier-Price M, Ton AT, Ayoubi R, Serohijos A, Omichinski JG, Angers A. J Biol Chem 292 6325-6338 (2017)
  24. Novel insights into the mechanisms of CIN85 SH3 domains binding to Cbl proteins: solution-based investigations and in vivo implications. Ababou A, Pfuhl M, Ladbury JE. J Mol Biol 387 1120-1136 (2009)
  25. Multimeric and differential binding of CIN85/CD2AP with two atypical proline-rich sequences from CD2 and Cbl-b*. Ceregido MA, Garcia-Pino A, Ortega-Roldan JL, Casares S, López Mayorga O, Bravo J, van Nuland NA, Azuaga AI. FEBS J 280 3399-3415 (2013)
  26. E3 ligase-inactivation rewires CBL interactome to elicit oncogenesis by hijacking RTK-CBL-CIN85 axis. Ahmed SF, Buetow L, Gabrielsen M, Lilla S, Sibbet GJ, Sumpton D, Zanivan S, Hedley A, Clark W, Huang DT. Oncogene 40 2149-2164 (2021)
  27. In Silico Identification of Potential Druggable Binding Sites on CIN85 SH3 Domain. Vittorio S, Seidel T, Garon A, Gitto R, Langer T, De Luca L. Int J Mol Sci 22 E534 (2021)
  28. Reply to "The binding stoichiometry of CIN85 SH3 domain A and Cbl-b". Jozic D, Cárdenes N, Deribe YL, Moncalián G, Hoeller D, Groemping Y, Dikic I, Rittinger K, Bravo J. Nat Struct Mol Biol 15 891-892 (2008)
  29. Letter The binding stoichiometry of CIN85 SH3 domain A and cbl-b. Ababou A, Pfuhl M, Ladbury JE. Nat Struct Mol Biol 15 890-1; author reply 891-2 (2008)
  30. Exploring Molecular Contacts of MUC1 at CIN85 Binding Interface to Address Future Drug Design Efforts. Gulotta MR, Vittorio S, Gitto R, Perricone U, De Luca L. Int J Mol Sci 22 2208 (2021)
  31. Effects on exocytosis by two HSV-1 mutants unable to block autophagy. Waisner H, Lasnier S, Suma SM, Kalamvoki M. J Virol e0075723 (2023)
  32. Studying the Association of TKS4 and CD2AP Scaffold Proteins and Their Implications in the Partial Epithelial-Mesenchymal Transition (EMT) Process. Kurilla A, László L, Takács T, Tilajka Á, Lukács L, Novák J, Pancsa R, Buday L, Vas V. Int J Mol Sci 24 15136 (2023)


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