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Structural basis for a novel intrapeptidyl H-bond and reverse binding of c-Cbl-TKB domain substrates.

Ng C, Jackson RA, Buschdorf JP, Sun Q, Guy GR, Sivaraman J
EMBO J 27 804-16 (2008)
Related entries: 3bum, 3bun, 3buw, 3bux

Cited: 44 times
EuropePMC logo PMID: 18273061

Abstract

The c-Cbl tyrosine kinase binding domain (Cbl-TKB), essentially an 'embedded' SH2 domain, has a critical role in targeting proteins for ubiquitination. To address how this domain can bind to disparate recognition mofits and to determine whether this results in variations in substrate-binding affinity, we compared crystal structures of the Cbl-TKB domain complexed with phosphorylated peptides of Sprouty2, Sprouty4, epidermal growth factor receptor, Syk, and c-Met receptors and validated the binding with point-mutational analyses using full-length proteins. An obligatory, intrapeptidyl H-bond between the phosphotyrosine and the conserved asparagine or adjacent arginine is essential for binding and orients the peptide into a positively charged pocket on c-Cbl. Surprisingly, c-Met bound to Cbl in the reverse direction, which is unprecedented for SH2 domain binding. The necessity of this intrapeptidyl H-bond was confirmed with isothermal titration calorimetry experiments that also showed Sprouty2 to have the highest binding affinity to c-Cbl; this may enable the selective sequestration of c-Cbl from other target proteins.

Reviews - 3buo mentioned but not cited (1)

  1. Molecular mechanisms of SH2- and PTB-domain-containing proteins in receptor tyrosine kinase signaling. Wagner MJ, Stacey MM, Liu BA, Pawson T. Cold Spring Harb Perspect Biol 5 a008987 (2013)

Articles - 3buo mentioned but not cited (3)

  1. Structural basis for a novel intrapeptidyl H-bond and reverse binding of c-Cbl-TKB domain substrates. Ng C, Jackson RA, Buschdorf JP, Sun Q, Guy GR, Sivaraman J. EMBO J 27 804-816 (2008)
  2. De novo activating mutations drive clonal evolution and enhance clonal fitness in KMT2A-rearranged leukemia. Hyrenius-Wittsten A, Pilheden M, Sturesson H, Hansson J, Walsh MP, Song G, Kazi JU, Liu J, Ramakrishan R, Garcia-Ruiz C, Nance S, Gupta P, Zhang J, Rönnstrand L, Hultquist A, Downing JR, Lindkvist-Petersson K, Paulsson K, Järås M, Gruber TA, Ma J, Hagström-Andersson AK. Nat Commun 9 1770 (2018)
  3. Additional serine/threonine phosphorylation reduces binding affinity but preserves interface topography of substrate proteins to the c-Cbl TKB domain. Sun Q, Jackson RA, Ng C, Guy GR, Sivaraman J. PLoS One 5 e12819 (2010)


Reviews citing this publication (10)

  1. Protein tyrosine kinase regulation by ubiquitination: critical roles of Cbl-family ubiquitin ligases. Mohapatra B, Ahmad G, Nadeau S, Zutshi N, An W, Scheffe S, Dong L, Feng D, Goetz B, Arya P, Bailey TA, Palermo N, Borgstahl GE, Natarajan A, Raja SM, Naramura M, Band V, Band H. Biochim Biophys Acta 1833 122-139 (2013)
  2. Syk and pTyr'd: Signaling through the B cell antigen receptor. Geahlen RL. Biochim Biophys Acta 1793 1115-1127 (2009)
  3. The developing story of Sprouty and cancer. Masoumi-Moghaddam S, Amini A, Morris DL. Cancer Metastasis Rev 33 695-720 (2014)
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  5. The language of SH2 domain interactions defines phosphotyrosine-mediated signal transduction. Liu BA, Engelmann BW, Nash PD. FEBS Lett 586 2597-2605 (2012)
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  9. Survey of the year 2008: applications of isothermal titration calorimetry. Falconer RJ, Penkova A, Jelesarov I, Collins BM. J Mol Recognit 23 395-413 (2010)
  10. Cbl-family proteins as regulators of cytoskeleton-dependent phenomena. Lee H, Tsygankov AY. J Cell Physiol 228 2285-2293 (2013)

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  3. Tripartite degrons confer diversity and specificity on regulated protein degradation in the ubiquitin-proteasome system. Guharoy M, Bhowmick P, Sallam M, Tompa P. Nat Commun 7 10239 (2016)
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  6. SLiMPrints: conservation-based discovery of functional motif fingerprints in intrinsically disordered protein regions. Davey NE, Cowan JL, Shields DC, Gibson TJ, Coldwell MJ, Edwards RJ. Nucleic Acids Res 40 10628-10641 (2012)
  7. Structure of a novel phosphotyrosine-binding domain in Hakai that targets E-cadherin. Mukherjee M, Chow SY, Yusoff P, Seetharaman J, Ng C, Sinniah S, Koh XW, Asgar NF, Li D, Yim D, Jackson RA, Yew J, Qian J, Iyu A, Lim YP, Zhou X, Sze SK, Guy GR, Sivaraman J. EMBO J 31 1308-1319 (2012)
  8. Structural determinants of nuclear export signal orientation in binding to exportin CRM1. Fung HY, Fu SC, Brautigam CA, Chook YM. Elife 4 (2015)
  9. HECT domain-containing E3 ubiquitin ligase Nedd4 interacts with and ubiquitinates Sprouty2. Edwin F, Anderson K, Patel TB. J Biol Chem 285 255-264 (2010)
  10. Two structural motifs within canonical EF-hand calcium-binding domains identify five different classes of calcium buffers and sensors. Denessiouk K, Permyakov S, Denesyuk A, Permyakov E, Johnson MS. PLoS One 9 e109287 (2014)
  11. c-Cbl tyrosine kinase-binding domain mutant G306E abolishes the interaction of c-Cbl with CD38 and fails to promote retinoic acid-induced cell differentiation and G0 arrest. Shen M, Yen A. J Biol Chem 284 25664-25677 (2009)
  12. Phosphorylation of the MET receptor on juxtamembrane tyrosine residue 1001 inhibits its caspase-dependent cleavage. Deheuninck J, Goormachtigh G, Foveau B, Ji Z, Leroy C, Ancot F, Villeret V, Tulasne D, Fafeur V. Cell Signal 21 1455-1463 (2009)
  13. Casitas B-lineage lymphoma linker helix mutations found in myeloproliferative neoplasms affect conformation. Buetow L, Tria G, Ahmed SF, Hock A, Dou H, Sibbet GJ, Svergun DI, Huang DT. BMC Biol 14 76 (2016)
  14. High-throughput fluorescence polarization assay to identify inhibitors of Cbl(TKB)-protein tyrosine kinase interactions. Kumar EA, Charvet CD, Lokesh GL, Natarajan A. Anal Biochem 411 254-260 (2011)
  15. Peptide truncation leads to a twist and an unusual increase in affinity for casitas B-lineage lymphoma tyrosine kinase binding domain. Kumar EA, Yuan Z, Palermo NY, Dong L, Ahmad G, Lokesh GL, Kolar C, Kizhake S, Borgstahl GE, Band H, Natarajan A. J Med Chem 55 3583-3587 (2012)
  16. The paradox of conformational constraint in the design of Cbl(TKB)-binding peptides. Kumar EA, Chen Q, Kizhake S, Kolar C, Kang M, Chang CE, Borgstahl GE, Natarajan A. Sci Rep 3 1639 (2013)
  17. The Insect Peptide CopA3 Increases Colonic Epithelial Cell Proliferation and Mucosal Barrier Function to Prevent Inflammatory Responses in the Gut. Kim DH, Hwang JS, Lee IH, Nam ST, Hong J, Zhang P, Lu LF, Lee J, Seok H, Pothoulakis C, Lamont JT, Kim H. J Biol Chem 291 3209-3223 (2016)
  18. 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)
  19. Structural basis for the indispensable role of a unique zinc finger motif in LNX2 ubiquitination. Nayak D, Sivaraman J. Oncotarget 6 34342-34357 (2015)
  20. Structural insights into a HECT-type E3 ligase AREL1 and its ubiquitination activities in vitro. Singh S, Ng J, Nayak D, Sivaraman J. J Biol Chem 294 19934-19949 (2019)
  21. An adjacent arginine, and the phosphorylated tyrosine in the c-Met receptor target sequence, dictates the orientation of c-Cbl binding. Sun Q, Ng C, Guy GR, Sivaraman J. FEBS Lett 585 281-285 (2011)
  22. DEGRONOPEDIA: a web server for proteome-wide inspection of degrons. Szulc NA, Stefaniak F, Piechota M, Soszyńska A, Piórkowska G, Cappannini A, Bujnicki JM, Maniaci C, Pokrzywa W. Nucleic Acids Res 52 W221-W232 (2024)
  23. Phosphorylation control of the ubiquitin ligase Cbl is conserved in choanoflagellates. Amacher JF, Hobbs HT, Cantor AC, Shah L, Rivero MJ, Mulchand SA, Kuriyan J. Protein Sci 27 923-932 (2018)
  24. Structural flexibility regulates phosphopeptide-binding activity of the tyrosine kinase binding domain of Cbl-c. Takeshita K, Tezuka T, Isozaki Y, Yamashita E, Suzuki M, Kim M, Yamanashi Y, Yamamoto T, Nakagawa A. J Biochem 152 487-495 (2012)
  25. Engineering SH2 Domains with Tailored Specificities and Affinities. Martyn GD, Veggiani G, Sidhu SS. Methods Mol Biol 2705 307-348 (2023)
  26. An innate pathogen sensing strategy involving ubiquitination of bacterial surface proteins. Apte S, Bhutda S, Ghosh S, Sharma K, Barton TE, Dibyachintan S, Sahay O, Roy S, Sinha AR, Adicherla H, Rakshit J, Tang S, Datey A, Santra S, Joseph J, Sasidharan S, Hammerschmidt S, Chakravortty D, Oggioni MR, Santra MK, Neill DR, Banerjee A. Sci Adv 9 eade1851 (2023)
  27. Oral intake of rice overexpressing ubiquitin ligase inhibitory pentapeptide prevents atrophy in denervated skeletal muscle. Nakao R, Shen W, Shimajiri Y, Kainou K, Sato Y, Ulla A, Ohnishi K, Ninomiya M, Ohno A, Uchida T, Tanaka M, Akama K, Matsui T, Nikawa T. NPJ Sci Food 5 25 (2021)
  28. The Abl/Abi signaling links WAVE regulatory complex to Cbl E3 ubiquitin ligase and is essential for breast cancer cell metastasis. Jiang P, Tang S, Hudgins H, Smalligan T, Zhou X, Kamat A, Dharmarpandi J, Naguib T, Liu X, Dai Z. Neoplasia 32 100819 (2022)
  29. Autoinflammation in patients with leukocytic CBL loss of heterozygosity is caused by constitutive ERK-mediated monocyte activation. Bohlen J, Bagarić I, Vatovec T, Ogishi M, Ahmed SF, Cederholm A, Buetow L, Sobrino S, Le Floc'h C, Arango-Franco CA, Seabra L, Michelet M, Barzaghi F, Leardini D, Saettini F, Vendemini F, Baccelli F, Catala A, Gambineri E, Veltroni M, Aguilar de la Red Y, Rice GI, Consonni F, Berteloot L, Largeaud L, Conti F, Roullion C, Masson C, Bessot B, Seeleuthner Y, Le Voyer T, Rinchai D, Rosain J, Neehus AL, Erazo-Borrás L, Li H, Janda Z, Cho EJ, Muratore E, Soudée C, Lainé C, Delabesse E, Goulvestre C, Ma CS, Puel A, Tangye SG, André I, Bole-Feysot C, Abel L, Erlacher M, Zhang SY, Béziat V, Lagresle-Peyrou C, Six E, Pasquet M, Alsina L, Aiuti A, Zhang P, Crow YJ, Landegren N, Masetti R, Huang DT, Casanova JL, Bustamante J. J Clin Invest 134 e181604 (2024)
  30. Sleuthing biochemical evidence to elucidate unassigned electron density in a CBL-SLAP2 crystal complex. Wybenga-Groot LE, McGlade CJ. Acta Crystallogr F Struct Biol Commun 77 37-46 (2021)


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