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The structural and dynamic response of MAGI-1 PDZ1 with noncanonical domain boundaries to the binding of human papillomavirus E6.

Charbonnier S, Nominé Y, Ramírez J, Luck K, Chapelle A, Stote RH, Travé G, Kieffer B, Atkinson RA
J Mol Biol 406 745-63 (2011)
Cited: 37 times
EuropePMC logo PMID: 21238461

Abstract

PDZ domains are protein interaction domains that are found in cytoplasmic proteins involved in signaling pathways and subcellular transport. Their roles in the control of cell growth, cell polarity, and cell adhesion in response to cell contact render this family of proteins targets during the development of cancer. Targeting of these network hubs by the oncoprotein E6 of "high-risk" human papillomaviruses (HPVs) serves to effect the efficient disruption of cellular processes. Using NMR, we have solved the three-dimensional solution structure of an extended construct of the second PDZ domain of MAGI-1 (MAGI-1 PDZ1) alone and bound to a peptide derived from the C-terminus of HPV16 E6, and we have characterized the changes in backbone dynamics and hydrogen bonding that occur upon binding. The binding event induces quenching of high-frequency motions in the C-terminal tail of the PDZ domain, which contacts the peptide upstream of the canonical X-[T/S]-X-[L/V] binding motif. Mutations designed in the C-terminal flanking region of the PDZ domain resulted in a significant decrease in binding affinity for E6 peptides. This detailed analysis supports the notion of a global response of the PDZ domain to the binding event, with effects propagated to distal sites, and reveals unexpected roles for the sequences flanking the canonical PDZ domain boundaries.

Reviews - 2kpk mentioned but not cited (1)

  1. Specificity in PDZ-peptide interaction networks: Computational analysis and review. Amacher JF, Brooks L, Hampton TH, Madden DR. J Struct Biol X 4 100022 (2020)

Articles - 2kpk mentioned but not cited (5)

  1. Evidence of conformational selection driving the formation of ligand binding sites in protein-protein interfaces. Bohnuud T, Kozakov D, Vajda S. PLoS Comput Biol 10 e1003872 (2014)
  2. Peptide-Protein Binding Investigated by Far-IR Spectroscopy and Molecular Dynamics Simulations. Cote Y, Nominé Y, Ramirez J, Hellwig P, Stote RH. Biophys J 112 2575-2588 (2017)
  3. Molecular insights into the interaction of HPV-16 E6 variants against MAGI-1 PDZ1 domain. Araujo-Arcos LE, Montaño S, Bello-Rios C, Garibay-Cerdenares OL, Leyva-Vázquez MA, Illades-Aguiar B. Sci Rep 12 1898 (2022)
  4. Ensemble-Based Analysis of the Dynamic Allostery in the PSD-95 PDZ3 Domain in Relation to the General Variability of PDZ Structures. Dudola D, Hinsenkamp A, Gáspári Z. Int J Mol Sci 21 E8348 (2020)
  5. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


Reviews citing this publication (12)

  1. Papillomavirus E6 oncoproteins. Vande Pol SB, Klingelhutz AJ. Virology 445 115-137 (2013)
  2. NMR approaches for structural analysis of multidomain proteins and complexes in solution. Göbl C, Madl T, Simon B, Sattler M. Prog Nucl Magn Reson Spectrosc 80 26-63 (2014)
  3. The Human Papillomavirus E6 PDZ Binding Motif: From Life Cycle to Malignancy. Ganti K, Broniarczyk J, Manoubi W, Massimi P, Mittal S, Pim D, Szalmas A, Thatte J, Thomas M, Tomaić V, Banks L. Viruses 7 3530-3551 (2015)
  4. The emerging contribution of sequence context to the specificity of protein interactions mediated by PDZ domains. Luck K, Charbonnier S, Travé G. FEBS Lett 586 2648-2661 (2012)
  5. Structural Features of Tight-Junction Proteins. Heinemann U, Schuetz A. Int J Mol Sci 20 E6020 (2019)
  6. Ligand binding by PDZ domains. Chi CN, Bach A, Strømgaard K, Gianni S, Jemth P. Biofactors 38 338-348 (2012)
  7. Emerging Themes in PDZ Domain Signaling: Structure, Function, and Inhibition. Liu X, Fuentes EJ. Int Rev Cell Mol Biol 343 129-218 (2019)
  8. Structural Insights in Multifunctional Papillomavirus Oncoproteins. Suarez I, Trave G. Viruses 10 E37 (2018)
  9. HPV E6 oncoprotein as a potential therapeutic target in HPV related cancers. Manzo-Merino J, Thomas M, Fuentes-Gonzalez AM, Lizano M, Banks L. Expert Opin Ther Targets 17 1357-1368 (2013)
  10. In Silico Approaches: A Way to Unveil Novel Therapeutic Drugs for Cervical Cancer Management. Gomes D, Silvestre S, Duarte AP, Venuti A, Soares CP, Passarinha L, Sousa Â. Pharmaceuticals (Basel) 14 741 (2021)
  11. Dynamic, but Not Necessarily Disordered, Human-Virus Interactions Mediated through SLiMs in Viral Proteins. Elkhaligy H, Balbin CA, Gonzalez JL, Liberatore T, Siltberg-Liberles J. Viruses 13 2369 (2021)
  12. Human papillomavirus and host genetic polymorphisms in carcinogenesis: a systematic review and meta-analysis. Habbous S, Pang V, Xu W, Amir E, Liu G. J Clin Virol 61 220-229 (2014)

Articles citing this publication (19)

  1. Structural basis for hijacking of cellular LxxLL motifs by papillomavirus E6 oncoproteins. Zanier K, Charbonnier S, Sidi AO, McEwen AG, Ferrario MG, Poussin-Courmontagne P, Cura V, Brimer N, Babah KO, Ansari T, Muller I, Stote RH, Cavarelli J, Vande Pol S, Travé G. Science 339 694-698 (2013)
  2. Quantifying domain-ligand affinities and specificities by high-throughput holdup assay. Vincentelli R, Luck K, Poirson J, Polanowska J, Abdat J, Blémont M, Turchetto J, Iv F, Ricquier K, Straub ML, Forster A, Cassonnet P, Borg JP, Jacob Y, Masson M, Nominé Y, Reboul J, Wolff N, Charbonnier S, Travé G. Nat Methods 12 787-793 (2015)
  3. Stabilization of HPV16 E6 protein by PDZ proteins, and potential implications for genome maintenance. Nicolaides L, Davy C, Raj K, Kranjec C, Banks L, Doorbar J. Virology 414 137-145 (2011)
  4. Putting into practice domain-linear motif interaction predictions for exploration of protein networks. Luck K, Fournane S, Kieffer B, Masson M, Nominé Y, Travé G. PLoS One 6 e25376 (2011)
  5. Stereochemical preferences modulate affinity and selectivity among five PDZ domains that bind CFTR: comparative structural and sequence analyses. Amacher JF, Cushing PR, Brooks L, Boisguerin P, Madden DR. Structure 22 82-93 (2014)
  6. Targeting the Two Oncogenic Functional Sites of the HPV E6 Oncoprotein with a High-Affinity Bivalent Ligand. Ramirez J, Poirson J, Foltz C, Chebaro Y, Schrapp M, Meyer A, Bonetta A, Forster A, Jacob Y, Masson M, Deryckère F, Travé G. Angew Chem Int Ed Engl 54 7958-7962 (2015)
  7. Downregulation of MAGI1 associates with poor prognosis of hepatocellular carcinoma. Zhang G, Liu T, Wang Z. J Invest Surg 25 93-99 (2012)
  8. Extensions of PSD-95/discs large/ZO-1 (PDZ) domains influence lipid binding and membrane targeting of syntenin-1. Wawrzyniak AM, Vermeiren E, Zimmermann P, Ivarsson Y. FEBS Lett 586 1445-1451 (2012)
  9. Dynamic control of RSK complexes by phosphoswitch-based regulation. Gógl G, Biri-Kovács B, Póti ÁL, Vadászi H, Szeder B, Bodor A, Schlosser G, Ács A, Turiák L, Buday L, Alexa A, Nyitray L, Reményi A. FEBS J 285 46-71 (2018)
  10. Structural insights into a wildtype domain of the oncoprotein E6 and its interaction with a PDZ domain. Mischo A, Ohlenschläger O, Hortschansky P, Ramachandran R, Görlach M. PLoS One 8 e62584 (2013)
  11. An RNA Aptamer Targets the PDZ-Binding Motif of the HPV16 E6 Oncoprotein. Belyaeva TA, Nicol C, Cesur O, Travé G, Blair GE, Stonehouse NJ. Cancers (Basel) 6 1553-1569 (2014)
  12. Structural and functional characterization of the PDZ domain of the human phosphatase PTPN3 and its interaction with the human papillomavirus E6 oncoprotein. Genera M, Samson D, Raynal B, Haouz A, Baron B, Simenel C, Guerois R, Wolff N, Caillet-Saguy C. Sci Rep 9 7438 (2019)
  13. MAGI1 Inhibits the Proliferation, Migration and Invasion of Glioma Cells. Li ZY, Li XH, Tian GW, Zhang DY, Gao H, Wang ZY. Onco Targets Ther 12 11281-11290 (2019)
  14. MAGI-1 PDZ2 Domain Blockade Averts Adenovirus Infection via Enhanced Proteolysis of the Apical Coxsackievirus and Adenovirus Receptor. Alghamri MS, Sharma P, Williamson TL, Readler JM, Yan R, Rider SD, Hostetler HA, Cool DR, Kolawole AO, Excoffon KJDA. J Virol 95 e0004621 (2021)
  15. Production and characterization of a retinoic acid receptor RARγ construction encompassing the DNA binding domain and the disordered N-terminal proline rich domain. Martinez-Zapien D, Delsuc MA, Travé G, Lutzing R, Rochette-Egly C, Kieffer B. Protein Expr Purif 95 113-120 (2014)
  16. A new NMR technique to probe protein-ligand interaction. Viéville JM, Charbonnier S, Eberling P, Starck JP, Delsuc MA. J Pharm Biomed Anal 89 18-23 (2014)
  17. NMR assignment of a PDZ domain in complex with a HPV51 E6 derived N-terminally pyroglutamic acid modified peptide. Mischo A, Ohlenschläger O, Ramachandran R, Görlach M. Biomol NMR Assign 7 47-49 (2013)
  18. Structural and biochemical analysis of the PTPN4 PDZ domain bound to the C-terminal tail of the human papillomavirus E6 oncoprotein. Lee HS, Yun HY, Lee EW, Shin HC, Kim SJ, Ku B. J Microbiol 60 395-401 (2022)
  19. Crystal Structures of Plk1 Polo-Box Domain Bound to the Human Papillomavirus Minor Capsid Protein L2-Derived Peptide. Jung S, Lee HS, Shin HC, Choi JS, Kim SJ, Ku B. J Microbiol 61 755-764 (2023)


Related citations provided by authors (1)

  1. 13C, 15N and 1H resonance assignment of the PDZ1 domain of MAGI-1 using QUASI.. Charbonnier S, Coutouly MA, Kieffer B, Travé G, Atkinson RA J Biomol NMR 36 Suppl 1 33 (2006)

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