3gqi › Citations

The selectivity of receptor tyrosine kinase signaling is controlled by a secondary SH2 domain binding site.

Bae JH, Lew ED, Yuzawa S, Tomé F, Lax I, Schlessinger J
Cell 138 514-24 (2009)
Cited: 109 times
EuropePMC logo PMID: 19665973

Abstract

SH2 domain-mediated interactions represent a crucial step in transmembrane signaling by receptor tyrosine kinases. SH2 domains recognize phosphotyrosine (pY) in the context of particular sequence motifs in receptor phosphorylation sites. However, the modest binding affinity of SH2 domains to pY containing peptides may not account for and likely represents an oversimplified mechanism for regulation of selectivity of signaling pathways in living cells. Here we describe the crystal structure of the activated tyrosine kinase domain of FGFR1 in complex with a phospholipase Cgamma fragment. The structural and biochemical data and experiments with cultured cells show that the selectivity of phospholipase Cgamma binding and signaling via activated FGFR1 are determined by interactions between a secondary binding site on an SH2 domain and a region in FGFR1 kinase domain in a phosphorylation independent manner. These experiments reveal a mechanism for how SH2 domain selectivity is regulated in vivo to mediate a specific cellular process.

Reviews - 3gqi mentioned but not cited (4)

  1. Molecular mechanisms of fibroblast growth factor signaling in physiology and pathology. Belov AA, Mohammadi M. Cold Spring Harb Perspect Biol 5 a015958 (2013)
  2. The use of polyoxometalates in protein crystallography - An attempt to widen a well-known bottleneck. Bijelic A, Rompel A. Coord Chem Rev 299 22-38 (2015)
  3. 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)
  4. Fibroblast growth factor receptor fusions in cancer: opportunities and challenges. Chen L, Zhang Y, Yin L, Cai B, Huang P, Li X, Liang G. J Exp Clin Cancer Res 40 345 (2021)

Articles - 3gqi mentioned but not cited (33)

  1. Germline and somatic FGFR1 abnormalities in dysembryoplastic neuroepithelial tumors. Rivera B, Gayden T, Carrot-Zhang J, Nadaf J, Boshari T, Faury D, Zeinieh M, Blanc R, Burk DL, Fahiminiya S, Bareke E, Schüller U, Monoranu CM, Sträter R, Kerl K, Niederstadt T, Kurlemann G, Ellezam B, Michalak Z, Thom M, Lockhart PJ, Leventer RJ, Ohm M, MacGregor D, Jones D, Karamchandani J, Greenwood CM, Berghuis AM, Bens S, Siebert R, Zakrzewska M, Liberski PP, Zakrzewski K, Sisodiya SM, Paulus W, Albrecht S, Hasselblatt M, Jabado N, Foulkes WD, Majewski J. Acta Neuropathol 131 847-863 (2016)
  2. Mechanism of phosphorylation-induced activation of phospholipase C-gamma isozymes. Gresset A, Hicks SN, Harden TK, Sondek J. J Biol Chem 285 35836-35847 (2010)
  3. Structural and functional integration of the PLCγ interaction domains critical for regulatory mechanisms and signaling deregulation. Bunney TD, Esposito D, Mas-Droux C, Lamber E, Baxendale RW, Martins M, Cole A, Svergun D, Driscoll PC, Katan M. Structure 20 2062-2075 (2012)
  4. Asymmetric receptor contact is required for tyrosine autophosphorylation of fibroblast growth factor receptor in living cells. Bae JH, Boggon TJ, Tomé F, Mandiyan V, Lax I, Schlessinger J. Proc Natl Acad Sci U S A 107 2866-2871 (2010)
  5. FGFR1 mutations cause Hartsfield syndrome, the unique association of holoprosencephaly and ectrodactyly. Simonis N, Migeotte I, Lambert N, Perazzolo C, de Silva DC, Dimitrov B, Heinrichs C, Janssens S, Kerr B, Mortier G, Van Vliet G, Lepage P, Casimir G, Abramowicz M, Smits G, Vilain C. J Med Genet 50 585-592 (2013)
  6. Landscape of activating cancer mutations in FGFR kinases and their differential responses to inhibitors in clinical use. Patani H, Bunney TD, Thiyagarajan N, Norman RA, Ogg D, Breed J, Ashford P, Potterton A, Edwards M, Williams SV, Thomson GS, Pang CS, Knowles MA, Breeze AL, Orengo C, Phillips C, Katan M. Oncotarget 7 24252-24268 (2016)
  7. The Effect of Mutations on Drug Sensitivity and Kinase Activity of Fibroblast Growth Factor Receptors: A Combined Experimental and Theoretical Study. Bunney TD, Wan S, Thiyagarajan N, Sutto L, Williams SV, Ashford P, Koss H, Knowles MA, Gervasio FL, Coveney PV, Katan M. EBioMedicine 2 194-204 (2015)
  8. Structural basis for the activation of PLC-γ isozymes by phosphorylation and cancer-associated mutations. Hajicek N, Keith NC, Siraliev-Perez E, Temple BR, Huang W, Zhang Q, Harden TK, Sondek J. Elife 8 e51700 (2019)
  9. Two FGF Receptor Kinase Molecules Act in Concert to Recruit and Transphosphorylate Phospholipase Cγ. Huang Z, Marsiglia WM, Basu Roy U, Rahimi N, Ilghari D, Wang H, Chen H, Gai W, Blais S, Neubert TA, Mansukhani A, Traaseth NJ, Li X, Mohammadi M. Mol Cell 61 98-110 (2016)
  10. Itk tyrosine kinase substrate docking is mediated by a nonclassical SH2 domain surface of PLCgamma1. Min L, Joseph RE, Fulton DB, Andreotti AH. Proc Natl Acad Sci U S A 106 21143-21148 (2009)
  11. Identifying three-dimensional structures of autophosphorylation complexes in crystals of protein kinases. Xu Q, Malecka KL, Fink L, Jordan EJ, Duffy E, Kolander S, Peterson JR, Dunbrack RL. Sci Signal 8 rs13 (2015)
  12. Autoinhibition and phosphorylation-induced activation of phospholipase C-γ isozymes. Hajicek N, Charpentier TH, Rush JR, Harden TK, Sondek J. Biochemistry 52 4810-4819 (2013)
  13. Congenital hypogonadotropic hypogonadism with split hand/foot malformation: a clinical entity with a high frequency of FGFR1 mutations. Villanueva C, Jacobson-Dickman E, Xu C, Manouvrier S, Dwyer AA, Sykiotis GP, Beenken A, Liu Y, Tommiska J, Hu Y, Tiosano D, Gerard M, Leger J, Drouin-Garraud V, Lefebvre H, Polak M, Carel JC, Phan-Hug F, Hauschild M, Plummer L, Rey JP, Raivio T, Raivio T, Bouloux P, Sidis Y, Mohammadi M, Mohammadi M, de Roux N, Pitteloud N. Genet Med 17 651-659 (2015)
  14. Elucidation of a four-site allosteric network in fibroblast growth factor receptor tyrosine kinases. Chen H, Marsiglia WM, Cho MK, Huang Z, Deng J, Blais SP, Gai W, Bhattacharya S, Neubert TA, Traaseth NJ, Mohammadi M. Elife 6 e21137 (2017)
  15. A novel mode of protein kinase inhibition exploiting hydrophobic motifs of autoinhibited kinases: discovery of ATP-independent inhibitors of fibroblast growth factor receptor. Eathiraj S, Palma R, Hirschi M, Volckova E, Nakuci E, Castro J, Chen CR, Chan TC, France DS, Ashwell MA. J Biol Chem 286 20677-20687 (2011)
  16. Structural insights and activating mutations in diverse pathologies define mechanisms of deregulation for phospholipase C gamma enzymes. Liu Y, Bunney TD, Khosa S, Macé K, Beckenbauer K, Askwith T, Maslen S, Stubbs C, de Oliveira TM, Sader K, Skehel M, Gavin AC, Phillips C, Katan M. EBioMedicine 51 102607 (2020)
  17. Serine phosphorylation of the insulin-like growth factor I (IGF-1) receptor C-terminal tail restrains kinase activity and cell growth. Kelly GM, Buckley DA, Kiely PA, Adams DR, O'Connor R. J Biol Chem 287 28180-28194 (2012)
  18. Polyoxometalates: more than a phasing tool in protein crystallography. Bijelic A, Rompel A. ChemTexts 4 10 (2018)
  19. Comprehensive functional evaluation of variants of fibroblast growth factor receptor genes in cancer. Nakamura IT, Kohsaka S, Ikegami M, Ikeuchi H, Ueno T, Li K, Beyett TS, Koyama T, Shimizu T, Yamamoto N, Takahashi F, Takahashi K, Eck MJ, Mano H. NPJ Precis Oncol 5 66 (2021)
  20. Phosphorylation of serine 779 in fibroblast growth factor receptor 1 and 2 by protein kinase C(epsilon) regulates Ras/mitogen-activated protein kinase signaling and neuronal differentiation. Lonic A, Powell JA, Kong Y, Thomas D, Holien JK, Truong N, Parker MW, Guthridge MA. J Biol Chem 288 14874-14885 (2013)
  21. Bacterial Phytochrome as a Scaffold for Engineering of Receptor Tyrosine Kinases Controlled with Near-Infrared Light. Leopold AV, Pletnev S, Verkhusha VV. J Mol Biol 432 3749-3760 (2020)
  22. Computational tools for the interactive exploration of proteomic and structural data. Morris JH, Meng EC, Ferrin TE. Mol Cell Proteomics 9 1703-1715 (2010)
  23. Functional characterization of phospholipase C-γ2 mutant protein causing both somatic ibrutinib resistance and a germline monogenic autoinflammatory disorder. Walliser C, Wist M, Hermkes E, Zhou Y, Schade A, Haas J, Deinzer J, Désiré L, Li SSC, Stilgenbauer S, Milner JD, Gierschik P. Oncotarget 9 34357-34378 (2018)
  24. Identification of a novel oncogenic mutation of FGFR4 in gastric cancer. Futami T, Kawase T, Mori K, Asaumi M, Kihara R, Shindoh N, Kuromitsu S. Sci Rep 9 14627 (2019)
  25. Dynamic Allostery in PLCγ1 and Its Modulation by a Cancer Mutation Revealed by MD Simulation and NMR. Koss H, Bunney TD, Esposito D, Martins M, Katan M, Driscoll PC. Biophys J 115 31-45 (2018)
  26. Genetic testing facilitates prepubertal diagnosis of congenital hypogonadotropic hypogonadism. Xu C, Lang-Muritano M, Phan-Hug F, Dwyer AA, Sykiotis GP, Cassatella D, Acierno J, Mohammadi M, Pitteloud N. Clin Genet 92 213-216 (2017)
  27. Time-resolved FRET reports FGFR1 dimerization and formation of a complex with its effector PLCγ1. Perdios L, Bunney TD, Warren SC, Dunsby C, French PMW, Tate EW, Katan M. Adv Biol Regul 60 6-13 (2016)
  28. Characterization of the membrane interactions of phospholipase Cγ reveals key features of the active enzyme. Le Huray KIP, Bunney TD, Pinotsis N, Kalli AC, Katan M. Sci Adv 8 eabp9688 (2022)
  29. Conformational transition of FGFR kinase activation revealed by site-specific unnatural amino acid reporter and single molecule FRET. Perdios L, Lowe AR, Saladino G, Bunney TD, Thiyagarajan N, Alexandrov Y, Dunsby C, French PM, Chin JW, Gervasio FL, Tate EW, Katan M. Sci Rep 7 39841 (2017)
  30. Dynamics of allosteric regulation of the phospholipase C-γ isozymes upon recruitment to membranes. Siraliev-Perez E, Stariha JTB, Hoffmann RM, Temple BRS, Zhang Q, Hajicek N, Jenkins ML, Burke JE, Sondek J. Elife 11 e77809 (2022)
  31. Gatekeeper mutations activate FGF receptor tyrosine kinases by destabilizing the autoinhibited state. Besch A, Marsiglia WM, Mohammadi M, Zhang Y, Traaseth NJ. Proc Natl Acad Sci U S A 120 e2213090120 (2023)
  32. Peptide-based NTA(Ni)-nanodiscs for studying membrane enhanced FGFR1 kinase activities. Liu J, Zhu L, Zhang X, Wu B, Zhu P, Zhao H, Wang J. PeerJ 7 e7234 (2019)
  33. A CURE Biochemistry Laboratory Module to Study Protein-Protein Interactions by NMR Spectroscopy. Marsiglia WM, Qamra R, Jackson KM, Traaseth NJ. J Chem Educ 97 437-442 (2020)


Reviews citing this publication (21)

  1. Cell signaling by receptor tyrosine kinases. Lemmon MA, Schlessinger J. Cell 141 1117-1134 (2010)
  2. Post-translational modifications in signal integration. Deribe YL, Pawson T, Dikic I. Nat Struct Mol Biol 17 666-672 (2010)
  3. Receptor tyrosine kinases: legacy of the first two decades. Schlessinger J. Cold Spring Harb Perspect Biol 6 a008912 (2014)
  4. PLC regulation: emerging pictures for molecular mechanisms. Bunney TD, Katan M. Trends Biochem Sci 36 88-96 (2011)
  5. The phospholipase C isozymes and their regulation. Gresset A, Sondek J, Harden TK. Subcell Biochem 58 61-94 (2012)
  6. Asymmetric tyrosine kinase arrangements in activation or autophosphorylation of receptor tyrosine kinases. Bae JH, Schlessinger J. Mol Cells 29 443-448 (2010)
  7. The language of SH2 domain interactions defines phosphotyrosine-mediated signal transduction. Liu BA, Engelmann BW, Nash PD. FEBS Lett 586 2597-2605 (2012)
  8. Dysfunction of phospholipase Cγ in immune disorders and cancer. Koss H, Bunney TD, Behjati S, Katan M. Trends Biochem Sci 39 603-611 (2014)
  9. Evolution of SH2 domains and phosphotyrosine signalling networks. Liu BA, Nash PD. Philos Trans R Soc Lond B Biol Sci 367 2556-2573 (2012)
  10. High-throughput analysis of peptide-binding modules. Liu BA, Engelmann BW, Nash PD. Proteomics 12 1527-1546 (2012)
  11. Perspective: Dynamics of receptor tyrosine kinase signaling complexes. Mayer BJ. FEBS Lett 586 2575-2579 (2012)
  12. TREM2/PLCγ2 signalling in immune cells: function, structural insight, and potential therapeutic modulation. Magno L, Bunney TD, Mead E, Svensson F, Bictash MN. Mol Neurodegener 16 22 (2021)
  13. SOCS and Herpesviruses, With Emphasis on Cytomegalovirus Retinitis. Alston CI, Dix RD. Front Immunol 10 732 (2019)
  14. SH2 Domain Binding: Diverse FLVRs of Partnership. Jaber Chehayeb R, Boggon TJ. Front Endocrinol (Lausanne) 11 575220 (2020)
  15. Emerging roles of PLCγ1 in endothelial biology. Chen D, Simons M. Sci Signal 14 eabc6612 (2021)
  16. Imaging strategies for receptor tyrosine kinase dimers in living cells. Zhang X, Yin J, Pan W, Li Y, Li N, Tang B. Anal Bioanal Chem 415 67-82 (2023)
  17. Metabolic Messengers: fibroblast growth factor 1. Gasser E, Sancar G, Downes M, Evans RM. Nat Metab 4 663-671 (2022)
  18. Novel Roles of SH2 and SH3 Domains in Lipid Binding. Sipeki S, Koprivanacz K, Takács T, Kurilla A, László L, Vas V, Buday L. Cells 10 1191 (2021)
  19. PLCγ2 impacts microglia-related effectors revealing variants and pathways important in Alzheimer's disease. Li K, Ran B, Wang Y, Liu L, Li W. Front Cell Dev Biol 10 999061 (2022)
  20. Therapeutic Effects of Coumarins with Different Substitution Patterns. Flores-Morales V, Villasana-Ruíz AP, Garza-Veloz I, González-Delgado S, Martinez-Fierro ML. Molecules 28 2413 (2023)
  21. Activation Mechanisms and Diverse Functions of Mammalian Phospholipase C. Kanemaru K, Nakamura Y. Biomolecules 13 915 (2023)

Articles citing this publication (51)

  1. Structure of lipid kinase p110β/p85β elucidates an unusual SH2-domain-mediated inhibitory mechanism. Zhang X, Vadas O, Perisic O, Anderson KE, Clark J, Hawkins PT, Stephens LR, Williams RL. Mol Cell 41 567-578 (2011)
  2. A potent and highly specific FN3 monobody inhibitor of the Abl SH2 domain. Wojcik J, Hantschel O, Grebien F, Kaupe I, Bennett KL, Barkinge J, Jones RB, Koide A, Superti-Furga G, Koide S. Nat Struct Mol Biol 17 519-527 (2010)
  3. Insights into the aberrant activity of mutant EGFR kinase domain and drug recognition. Gajiwala KS, Feng J, Ferre R, Ryan K, Brodsky O, Weinrich S, Kath JC, Stewart A. Structure 21 209-219 (2013)
  4. SH2 domains recognize contextual peptide sequence information to determine selectivity. Liu BA, Jablonowski K, Shah EE, Engelmann BW, Jones RB, Nash PD. Mol Cell Proteomics 9 2391-2404 (2010)
  5. Fibronectin induces endothelial cell migration through β1 integrin and Src-dependent phosphorylation of fibroblast growth factor receptor-1 at tyrosines 653/654 and 766. Zou L, Cao S, Kang N, Huebert RC, Shah VH. J Biol Chem 287 7190-7202 (2012)
  6. SH2 Domains Serve as Lipid-Binding Modules for pTyr-Signaling Proteins. Park MJ, Sheng R, Silkov A, Jung DJ, Wang ZG, Xin Y, Kim H, Thiagarajan-Rosenkranz P, Song S, Yoon Y, Nam W, Kim I, Kim E, Lee DG, Chen Y, Singaram I, Wang L, Jang MH, Hwang CS, Honig B, Ryu S, Lorieau J, Kim YM, Cho W. Mol Cell 62 7-20 (2016)
  7. Noncanonical tandem SH2 enables interaction of elongation factor Spt6 with RNA polymerase II. Diebold ML, Loeliger E, Koch M, Winston F, Cavarelli J, Romier C. J Biol Chem 285 38389-38398 (2010)
  8. Phosphotyrosine recognition domains: the typical, the atypical and the versatile. Kaneko T, Joshi R, Feller SM, Li SS. Cell Commun Signal 10 32 (2012)
  9. Illuminating the molecular mechanisms of tyrosine kinase inhibitor resistance for the FGFR1 gatekeeper mutation: the Achilles' heel of targeted therapy. Sohl CD, Ryan MR, Luo B, Frey KM, Anderson KS. ACS Chem Biol 10 1319-1329 (2015)
  10. Hen egg-white lysozyme crystallisation: protein stacking and structure stability enhanced by a Tellurium(VI)-centred polyoxotungstate. Bijelic A, Molitor C, Mauracher SG, Al-Oweini R, Kortz U, Rompel A. Chembiochem 16 233-241 (2015)
  11. Evolving specificity from variability for protein interaction domains. Kaneko T, Sidhu SS, Li SS. Trends Biochem Sci 36 183-190 (2011)
  12. Distinct sets of FGF receptors sculpt excitatory and inhibitory synaptogenesis. Dabrowski A, Terauchi A, Strong C, Umemori H. Development 142 1818-1830 (2015)
  13. Competition between Grb2 and Plcγ1 for FGFR2 regulates basal phospholipase activity and invasion. Timsah Z, Ahmed Z, Lin CC, Melo FA, Stagg LJ, Leonard PG, Jeyabal P, Berrout J, O'Neil RG, Bogdanov M, Ladbury JE. Nat Struct Mol Biol 21 180-188 (2014)
  14. Structural mimicry of a-loop tyrosine phosphorylation by a pathogenic FGF receptor 3 mutation. Huang Z, Chen H, Blais S, Neubert TA, Li X, Mohammadi M. Structure 21 1889-1896 (2013)
  15. Two closely spaced tyrosines regulate NFAT signaling in B cells via Syk association with Vav. Chen CH, Martin VA, Gorenstein NM, Geahlen RL, Post CB. Mol Cell Biol 31 2984-2996 (2011)
  16. Quantification of shape and cell polarity reveals a novel mechanism underlying malformations resulting from related FGF mutations during facial morphogenesis. Li X, Young NM, Tropp S, Hu D, Xu Y, Hallgrímsson B, Marcucio RS. Hum Mol Genet 22 5160-5172 (2013)
  17. CDC42 binds PAK4 via an extended GTPase-effector interface. Ha BH, Boggon TJ. Proc Natl Acad Sci U S A 115 531-536 (2018)
  18. Src binds cortactin through an SH2 domain cystine-mediated linkage. Evans JV, Ammer AG, Jett JE, Bolcato CA, Breaux JC, Martin KH, Culp MV, Gannett PM, Weed SA. J Cell Sci 125 6185-6197 (2012)
  19. Structural basis for the interaction between the growth factor-binding protein GRB10 and the E3 ubiquitin ligase NEDD4. Huang Q, Szebenyi DM. J Biol Chem 285 42130-42139 (2010)
  20. Tyrosine kinase BMX phosphorylates phosphotyrosine-primed motif mediating the activation of multiple receptor tyrosine kinases. Chen S, Jiang X, Gewinner CA, Asara JM, Simon NI, Cai C, Cantley LC, Balk SP. Sci Signal 6 ra40 (2013)
  21. Unusual binding interactions in PDZ domain crystal structures help explain binding mechanisms. Elkins JM, Gileadi C, Shrestha L, Phillips C, Wang J, Muniz JR, Doyle DA. Protein Sci 19 731-741 (2010)
  22. Double-edged sword effect of biochanin to inhibit nuclear factor kappaB: suppression of serine/threonine and tyrosine kinases. Manna SK. Biochem Pharmacol 83 1383-1392 (2012)
  23. Grb14 inhibits FGF receptor signaling through the regulation of PLCγ recruitment and activation. Browaeys-Poly E, Blanquart C, Perdereau D, Antoine AF, Goenaga D, Luzy JP, Chen H, Garbay C, Issad T, Cailliau K, Cailliau K, Burnol AF. FEBS Lett 584 4383-4388 (2010)
  24. FGFs in endochondral skeletal development. Degnin CR, Laederich MB, Horton WA. J Cell Biochem 110 1046-1057 (2010)
  25. Secondary PDZ domain-binding site on class B plexins enhances the affinity for PDZ-RhoGEF. Pascoe HG, Gutowski S, Chen H, Brautigam CA, Chen Z, Sternweis PC, Zhang X. Proc Natl Acad Sci U S A 112 14852-14857 (2015)
  26. Antagonizing STAT5B dimerization with an osmium complex. Liu LJ, Wang W, Kang TS, Liang JX, Liu C, Kwong DWJ, Wong VKW, Ma DL, Leung CH. Sci Rep 6 36044 (2016)
  27. Novel FGFR1 mutations in Kallmann syndrome and normosmic idiopathic hypogonadotropic hypogonadism: evidence for the involvement of an alternatively spliced isoform. Gonçalves C, Gonçalves C, Bastos M, Pignatelli D, Borges T, Aragüés JM, Fonseca F, Pereira BD, Socorro S, Lemos MC. Fertil Steril 104 1261-7.e1 (2015)
  28. Extended Synaptotagmin Interaction with the Fibroblast Growth Factor Receptor Depends on Receptor Conformation, Not Catalytic Activity. Tremblay MG, Herdman C, Guillou F, Mishra PK, Baril J, Bellenfant S, Moss T. J Biol Chem 290 16142-16156 (2015)
  29. Translocation of exogenous FGF1 into cytosol and nucleus is a periodic event independent of receptor kinase activity. Zakrzewska M, Sørensen V, Jin Y, Wiedlocha A, Olsnes S. Exp Cell Res 317 1005-1015 (2011)
  30. Dynamic, structural and thermodynamic basis of insulin-like growth factor 1 kinase allostery mediated by activation loop phosphorylation. Li Y, Nam K. Chem Sci 8 3453-3464 (2017)
  31. Synthesis and Biological Screening of New 4-Hydroxycoumarin Derivatives and Their Palladium(II) Complexes. Avdović EH, Petrović IP, Stevanović MJ, Saso L, Dimitrić Marković JM, Filipović ND, Živić MŽ, Cvetić Antić TN, Žižić MV, Todorović NV, Vukić M, Trifunović SR, Marković ZS. Oxid Med Cell Longev 2021 8849568 (2021)
  32. Targeting fibroblast growth factor receptors to combat aggressive ependymoma. Lötsch D, Kirchhofer D, Englinger B, Jiang L, Okonechnikov K, Senfter D, Laemmerer A, Gabler L, Pirker C, Donson AM, Bannauer P, Korbel P, Jaunecker CN, Hübner JM, Mayr L, Madlener S, Schmook MT, Ricken G, Maaß K, Grusch M, Holzmann K, Grasl-Kraupp B, Spiegl-Kreinecker S, Hsu J, Dorfer C, Rössler K, Azizi AA, Foreman NK, Peyrl A, Haberler C, Czech T, Slavc I, Filbin MG, Pajtler KW, Kool M, Berger W, Gojo J. Acta Neuropathol 142 339-360 (2021)
  33. Cellular phosphatase activity of C1-Ten/Tensin2 is controlled by Phosphatidylinositol-3,4,5-triphosphate binding through the C1-Ten/Tensin2 SH2 domain. Kim E, Kim DH, Singaram I, Jeong H, Koh A, Lee J, Cho W, Ryu SH. Cell Signal 51 130-138 (2018)
  34. Deciphering Phosphotyrosine-Dependent Signaling Networks in Cancer by SH2 Profiling. Machida K, Khenkhar M, Nollau P. Genes Cancer 3 353-361 (2012)
  35. Identification of a new interaction mode between the Src homology 2 domain of C-terminal Src kinase (Csk) and Csk-binding protein/phosphoprotein associated with glycosphingolipid microdomains. Tanaka H, Akagi K, Oneyama C, Tanaka M, Sasaki Y, Kanou T, Lee YH, Yokogawa D, Dobenecker MW, Nakagawa A, Okada M, Ikegami T. J Biol Chem 288 15240-15254 (2013)
  36. FGFR1 Kinase Inhibitors: Close Regioisomers Adopt Divergent Binding Modes and Display Distinct Biophysical Signatures. Klein T, Tucker J, Holdgate GA, Norman RA, Breeze AL. ACS Med Chem Lett 5 166-171 (2014)
  37. Synthesis of purin-2-yl and purin-6-yl-aminoglucitols as C-nucleosidic ATP mimics and biological evaluation as FGFR3 inhibitors. Tak-Tak L, Barbault F, Maurel F, Busca P, Le Merrer Y. Eur J Med Chem 46 1254-1262 (2011)
  38. The development and application of a quantitative peptide microarray based approach to protein interaction domain specificity space. Engelmann BW, Kim Y, Wang M, Peters B, Rock RS, Nash PD. Mol Cell Proteomics 13 3647-3662 (2014)
  39. A novel conserved phosphotyrosine motif in the Drosophila fibroblast growth factor signaling adaptor Dof with a redundant role in signal transmission. Csiszar A, Vogelsang E, Beug H, Leptin M. Mol Cell Biol 30 2017-2027 (2010)
  40. Disease-causing mutation in extracellular and intracellular domain of FGFR1 protein: computational approach. Rajith B, George Priya Doss C. Appl Biochem Biotechnol 169 1659-1671 (2013)
  41. Effects of FGFR2 kinase activation loop dynamics on catalytic activity. Karp JM, Sparks S, Cowburn D. PLoS Comput Biol 13 e1005360 (2017)
  42. Nuclear magnetic resonance analysis of the conformational state of cancer mutant of fibroblast growth factor receptor 1 tyrosine kinase domain. Kobashigawa Y, Amano S, Yoza K, Himeno R, Amemiya S, Morioka H, Yokogawa M, Kumeta H, Schlessinger J, Inagaki F. Genes Cells 21 350-357 (2016)
  43. News Out of the box binding determines specificity of SH2 domain interaction. Müller S, Knapp S. Structure 17 1040-1041 (2009)
  44. Effects of multiple enzyme-substrate interactions in basic units of cellular signal processing. Seaton DD, Krishnan J. Phys Biol 9 045009 (2012)
  45. Exposed: The Many and Varied Roles of Phospholipase C γ SH2 Domains. Driscoll PC. J Mol Biol 427 2731-2733 (2015)
  46. Recruitment of phospholipase Cγ1 to the non-structural membrane protein pK15 of Kaposi Sarcoma-associated herpesvirus promotes its Src-dependent phosphorylation. Samarina N, Ssebyatika G, Tikla T, Waldmann JY, Abere B, Nanna V, Marasco M, Carlomagno T, Krey T, Schulz TF. PLoS Pathog 17 e1009635 (2021)
  47. Structural characterization of recombinant human fibroblast growth factor receptor 2b kinase domain upon interaction with omega fatty acids. Moghadasi M, Ilghari D, Sirati-Sabet M, Amini A, Asghari H, Gheibi N. Chem Phys Lipids 202 21-27 (2017)
  48. Synthesis and Cytotoxicity Evaluation of Novel Coumarin-Palladium(II) Complexes against Human Cancer Cell Lines. Avdović EH, Antonijević M, Simijonović D, Roca S, Topić DV, Grozdanić N, Stanojković T, Radojević I, Vojinović R, Marković Z. Pharmaceuticals (Basel) 16 49 (2022)
  49. Diverse p120RasGAP interactions with doubly phosphorylated partners EphB4, p190RhoGAP, and Dok1. Vish KJ, Stiegler AL, Boggon TJ. J Biol Chem 299 105098 (2023)
  50. Lipid Binding of SH2 Domains. Cho W, Berkley K, Sharma A. Methods Mol Biol 2705 239-253 (2023)
  51. Molecular insight into the autoinhibition of a master regulator of lipid signalling in human disease. Burke JE. EBioMedicine 52 102634 (2020)


Quick links