Structure of a stapled peptide antagonist bound to nutlin-resistant Mdm2

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Chee, Sharon Min Qi ^a   Wongsantichon, Jantana ^b   Soo Tng, Quah ^a   Robinson, Robert ^b   Joseph, Thomas L ^c   Verma, Chandra ^c,d,e   Lane, David P ^a   Brown, Christopher J ^a   Ghadessy, Farid J ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c BIOINFORMATICS INSTITUTE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

IMIDAZOLE DERIVATIVE; MDM2 PROTEIN, HUMAN; NUTLIN 3; PEPTIDE; PIPERAZINE DERIVATIVE; PROTEIN BINDING; PROTEIN MDM2; PROTEIN P53; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; BINDING COMPETITION; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE POLARIZATION; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN CONFORMATION; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING, COMPETITIVE; CELL LINE; CRYSTALLOGRAPHY, X-RAY; FLUORESCENCE POLARIZATION; HUMANS; IMIDAZOLES; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PIPERAZINES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS C-MDM2; RECOMBINANT PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84905841311     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104914     Document Type: Article

References (39)

1. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51: 6304-6311.
2. Kuerbitz SJ, Plunkett BS, Walsh WV, Kastan MB (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Natl Acad Sci U S A 89: 7491-7495.
3. Beroud C, Soussi T (1997) p53 and APC gene mutations: software and databases. Nucleic Acids Res 25: 138. (Pubitemid 27303169)
4. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, et al. (2010) Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466: 869-873.
5. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B (1992) Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 358: 80-83.
6. Bond GL, Hu W, Bond EE, Robins H, Lutzker SG, et al. (2004) A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans. Cell 119: 591-602. (Pubitemid 39535748)
7. Momand J, Zambetti GP, Olson DC, George D, Levine AJ (1992) The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69: 1237-1245.
8. Haupt Y, Maya R, Kazaz A, Oren M (1997) Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299. (Pubitemid 27220766)
9. Kubbutat MH, Jones SN, Vousden KH (1997) Regulation of p53 stability by Mdm2. Nature 387: 299-303. (Pubitemid 27220767)
10. Honda R, Tanaka H, Yasuda H (1997) Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 420: 25-27. (Pubitemid 28037193)
11. Bernal F, Tyler AF, Korsmeyer SJ, Walensky LD, Verdine GL (2007) Reactivation of the p53 tumor suppressor pathway by a stapled p53 peptide. J Am Chem Soc 129: 2456-2457. (Pubitemid 46364050)
12. Liu M, Li C, Pazgier M, Mao Y, Lv Y, et al. (2010) D-peptide inhibitors of the p53-MDM2 interaction for targeted molecular therapy of malignant neoplasms. Proc Natl Acad Sci U S A 107: 14321-14326.
13. See HY, Lane DP (2010) A novel unstructured scaffold based on 4EBP1 enables the functional display of a wide range of bioactive peptides. J Mol Biol 404: 819-831.
14. Shangary S, Wang S (2009) Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy. Annu Rev Pharmacol Toxicol 49: 223-241.
15. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, et al. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303: 844-848. (Pubitemid 38174664)
16. Wei SJ, Joseph T, Sim AY, Yurlova L, Zolghadr K, et al. (2013) In vitro selection of mutant HDM2 resistant to Nutlin inhibition. PLoS One 8: e62564.
17. Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, et al. (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274: 948-953. (Pubitemid 26398409)
18. Brown CJ, Quah ST, Jong J, Goh AM, Chiam PC, et al. (2012) Stapled Peptides with Improved Potency and Specificity That Activate p53. ACS Chem Biol.
19. Wei SJ, Joseph T, Chee S, Li L, Yurlova L, et al. (2013) Inhibition of nutlinresistant HDM2 mutants by stapled peptides. PLoS One 8: e81068.
20. Walensky LD, Kung AL, Escher I, Malia TJ, Barbuto S, et al. (2004) Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305: 1466-1470. (Pubitemid 39167667)
21. Kim YW, Grossmann TN, Verdine GL (2011) Synthesis of all-hydrocarbon stapled alpha-helical peptides by ring-closing olefin metathesis. Nat Protoc 6: 761-771.
22. Verdine GL, Walensky LD (2007) The challenge of drugging undruggable targets in cancer: lessons learned from targeting BCL-2 family members. Clin Cancer Res 13: 7264-7270.
23. Phillips C, Roberts LR, Schade M, Bazin R, Bent A, et al. (2011) Design and structure of stapled peptides binding to estrogen receptors. J Am Chem Soc 133: 9696-9699.
24. Pazgier M, Liu M, Zou G, Yuan W, Li C, et al. (2009) Structural basis for high-affinity peptide inhibition of p53 interactions with MDM2 and MDMX. Proc Natl Acad Sci U S A 106: 4665-4670.
25. Baek S, Kutchukian PS, Verdine GL, Huber R, Holak TA, et al. (2012) Structure of the stapled p53 peptide bound to Mdm2. J Am Chem Soc 134: 103-106.
26. Anil B, Riedinger C, Endicott JA, Noble ME (2013) The structure of an MDM2-Nutlin-3a complex solved by the use of a validated MDM2 surface-entropy reduction mutant. Acta Crystallogr D Biol Crystallogr 69: 1358-1366.
27. Popowicz GM, Czarna A, Rothweiler U, Szwagierczak A, Krajewski M, et al. (2007) Molecular basis for the inhibition of p53 by Mdmx. Cell Cycle 6: 2386-2392. (Pubitemid 350064092)
28. Dastidar SG, Lane DP, Verma CS (2008) Multiple peptide conformations give rise to similar binding affinities: molecular simulations of p53-MDM2. J Am Chem Soc 130: 13514-13515.
29. Dastidar SG, Lane DP, Verma CS (2009) Modulation of p53 binding to MDM2: computational studies reveal important roles of Tyr100. BMC Bioinformatics 10 Suppl 15: S6.
30. Schon O, Friedler A, Bycroft M, Freund SM, Fersht AR (2002) Molecular mechanism of the interaction between MDM2 and p53. J Mol Biol 323: 491-501. (Pubitemid 35283675)
31. Kallen J, Goepfert A, Blechschmidt A, Izaac A, Geiser M, et al. (2009) Crystal Structures of Human MdmX (HdmX) in Complex with p53 Peptide Analogues Reveal Surprising Conformational Changes. J Biol Chem 284: 8812-8821.
32. Brown CJ, Dastidar SG, Quah ST, Lim A, Chia B, et al. (2011) C-terminal substitution of MDM2 interacting peptides modulates binding affinity by distinctive mechanisms. PLoS One 6: e24122.
33. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674. (Pubitemid 47080256)
34. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255. (Pubitemid 27235885)
35. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
36. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
37. Lebedev AA, Young P, Isupov MN, Moroz OV, Vagin AA, et al. (2012) JLigand: a graphical tool for the CCP4 template-restraint library. Acta Crystallogr D Biol Crystallogr 68: 431-440.
38. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
39. Lu X, Burbidge SA, Griffin S, Smith HM (1996) Discordance between accumulated p53 protein level and its transcriptional activity in response to u.v. radiation. Oncogene 13: 413-418. (Pubitemid 26334874)