High-quality NMR structure of human anti-apoptotic protein domain Mcl-1(171-327) for cancer drug design

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Liu, Gaohua ^a,c   Poppe, Leszek ^b   Aoki, Ken ^b   Yamane, Harvey ^b   Lewis, Jeffrey ^b   Szyperski, Thomas ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b AMGEN INC   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BH3 PROTEIN; MCL 1(171-327); POLYPEPTIDE; PROTEIN BCL 2; PROTEIN MCL 1; UNCLASSIFIED DRUG; MCL1 PROTEIN, HUMAN; PEPTIDE FRAGMENT; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG DESIGN; HUMAN VERSUS ANIMAL COMPARISON; IMAGE QUALITY; LIGAND BINDING; NUCLEAR MAGNETIC RESONANCE; PROTEIN MOTIF; RESIDUE ANALYSIS; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; SURFACE CHARGE; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; HUMAN; MOUSE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; PROTEIN TERTIARY STRUCTURE; STATIC ELECTRICITY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BINDING SITES; DRUG DESIGN; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MODELS, MOLECULAR; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STATIC ELECTRICITY;

EID: 84900410718     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096521     Document Type: Article

References (42)

1. Vogler M, Dinsdale D, Dyer MJ, Cohen GM (2009) Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ 16: 360-367.
2. Warr MR, Shore GC (2008) Unique biology of Mcl-1: therapeutic opportunities in cancer. Curr Mol Med 8: 138-147. (Pubitemid 351516833)
3. Gelinas C, White E (2005) BH3-only proteins in control: specificity regulates MCL-1 and BAK-mediated apoptosis. Genes Dev 19: 1263-1268. (Pubitemid 41003016)
4. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681. (Pubitemid 40825512)
5. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, et al. (2008) ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 68: 3421-3428.
6. Simmons MJ, Fan G, Zong WX, Degenhardt K, White E, et al. (2008) Bfl-1/A1 functions, similar to Mcl-1, as a selective tBid and Bak antagonist. Oncogene 27: 1421-1428. (Pubitemid 351317460)
7. Kang MH, Reynolds CP (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15: 1126-1132.
8. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242. (Pubitemid 30047768)
9. Czabotar PE, Lee EF, van Delft MF, Day CL, Smith BJ, et al. (2007) Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci U S A 104: 6217-6222. (Pubitemid 47186075)
10. Day CL, Chen L, Richardson SJ, Harrison PJ, Huang DC, et al. (2005) Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands. J Biol Chem 280: 4738-4744. (Pubitemid 40288644)
11. Fire E, Gulla SV, Grant RA, Keating AE (2010) Mcl-1-Bim complexes accommodate surprising point mutations via minor structural changes. Protein Sci 19: 507-519.
12. Day CL, Smits C, Fan FC, Lee EF, Fairlie WD, et al. (2008) Structure of the BH3 domains from the p53-inducible BH3-only proteins Noxa and Puma in complex with Mcl-1. J Mol Biol 380: 958-971.
13. Lee EF, Czabotar PE, van Delft MF, Michalak EM, Boyle MJ, et al. (2008) A novel BH3 ligand that selectively targets Mcl-1 reveals that apoptosis can proceed without Mcl-1 degradation. J Cell Biol 180: 341-355. (Pubitemid 351185920)
14. Friberg A, Vigil D, Zhao B, Daniels RN, Burke JP, et al. Discovery of potent myeloid cell leukemia 1 (Mcl-1) inhibitors using fragment-based methods and structure-based design. J Med Chem 56: 15-30.
15. Liu Q, Moldoveanu T, Sprules T, Matta-Camacho E, Mansur-Azzam N, et al. (2010) Apoptotic regulation by MCL-1 through heterodimerization. J Biol Chem 285: 19615-19624.
16. Lee EF, Czabotar PE, Yang H, Sleebs BE, Lessene G, et al. (2009) Conformational changes in Bcl-2 pro-survival proteins determine their capacity to bind ligands. J Biol Chem 284: 30508-30517.
17. Stewart ML, Fire E, Keating AE, Walensky LD (2010) The MCL-1 BH3 helix is an exclusive MCL-1 inhibitor and apoptosis sensitizer. Nat Chem Biol 6: 595-601.
18. Muppidi A, Doi K, Edwardraja S, Drake EJ, Gulick AM, et al. (2012) Rational design of proteolytically stable, cell-permeable peptide-based selective Mcl-1 inhibitors. J Am Chem Soc 134: 14734-14737.
19. Acton TB, Gunsalus KC, Xiao R, Ma LC, Aramini J, et al. (2005) Robotic cloning and Protein Production Platform of the Northeast Structural Genomics Consortium. Methods Enzymol 394: 210-243. (Pubitemid 40460917)
20. Jansson M, Li YC, Jendeberg L, Anderson S, Montelione GT, et al. (1996) High-level production of uniformly N-15- and C-13-enriched fusion proteins in Escherichia coli. J Biomol NMR 7: 131-141. (Pubitemid 126709551)
21. Neri D, Szyperski T, Otting G, Senn H, Wuthrich K (1989) Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling. Biochemistry 28: 7510-7516. (Pubitemid 19238098)
22. Kim S, Szyperski T (2003) GFT NMR, a new approach to rapidly obtain precise high-dimensional NMR spectral information. J Am Chem Soc 125: 1385-1393. (Pubitemid 36159850)
23. Atreya HS, Szyperski T (2004) G-matrix Fourier transform NMR spectroscopy for complete protein resonance assignment. Proc Natl Acad Sci U S A 101: 9642-9647. (Pubitemid 38869289)
24. Liu GH, Shen Y, Atreya HS, Parish D, Shao Y, et al. (2005) NMR data collection and analysis protocol for high-throughput protein structure determination. Proc Natl Acad Sci U S A 102: 10487-10492. (Pubitemid 41061581)
25. Shen Y, Atreya HS, Liu GH, Szyperski T (2005) G-matrix Fourier transform NOESY-based protocol for high-quality protein structure determination. J Am Chem Soc 127: 9085-9099. (Pubitemid 40897602)
26. Penhoat CH, Li Z, Atreya HS, Kim S, Yee A, et al. (2005) NMR solution structure of Thermotoga maritima protein TM1509 reveals a Zn-metallopro-tease- like tertiary structure. J Struct Funct Genomics 6: 51-62. (Pubitemid 40898075)
27. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, et al. (1995) Nmrpipe - a Multidimensional Spectral Processing System Based on Unix Pipes. J Biomol NMR 6: 277-293.
28. Bartels C, Xia TH, Billeter M, Guntert P, Wuthrich K (1995) The Program Xeasy for Computer-Supported Nmr Spectral-Analysis of Biological Macromolecules. J Biomol NMR 6: 1-10.
29. Moseley HNB, Monleon D, Montelione GT (2001) Automatic determination of protein backbone resonance assignments from triple resonance nuclear magnetic resonance data. Meth Enzymology 339: 91-108. (Pubitemid 32666558)
30. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, et al. (2008) BioMagResBank. Nucleic Acids Res 36: D402-408. (Pubitemid 351149757)
31. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302. (Pubitemid 29143535)
32. Guntert P, Mumenthaler C, Wuthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Bio 273: 283-298. (Pubitemid 27460230)
33. Herrmann T, Guntert P, Wuthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Bio 319: 209-227. (Pubitemid 34729497)
34. Huang YPJ, Moseley HNB, Baran MC, Arrowsmith C, Powers R, et al. (2005) An integrated platform for automated analysis of protein NMR structures. Meth Enzymology 394: 210-243.
35. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallographica Section D-Biological Crystallography 54: 905-921.
36. Koradi R, Billeter M, Wuthrich K (1996) MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55. (Pubitemid 26152976)
37. Delano WL (2002) PyMOL molecular graphics system. Available: http://www.pymol.org
38. Laskowski RA, Macarthur MW, Moss DS, Thornton JM (1993) Procheck - a Program to Check the Stereochemical Quality of Protein Structures. J Appl Crystallogr 26: 283-291.
39. Word JM, Bateman RC, Presley BK, Lovell SC, Richardson DC (2000) Exploring steric constraints on protein mutations using MAGE/PROBE. Pro Sci 9: 2251-2259. (Pubitemid 32104162)
40. Huang YJ, Powers R, Montelione GT (2005) Protein NMR recall, precision, and F-measure scores (RPF scores): Structure quality assessment measures based on information retrieval statistics. J Am Chem Soc 127: 1665-1674. (Pubitemid 40229151)
41. Dutta S, Gulla S, Chen TS, Fire E, Grant RA, et al. (2010) Determinants of BH3 binding specificity for Mcl-1 versus Bcl-xL. J Mol Biol 398: 747-762.
42. Bhattacharya A, Tejero R, Montelione GT (2007) Evaluating protein structures determined by structural genomics consortia. Proteins 66, 778-795.