PUMA binding induces partial unfolding within BCL-xL to disrupt p53 binding and promote apoptosis

Nature Chemical Biology

Volumn 9, Issue 3, 2013, Pages 163-168

  Follis, Ariele Viacava ^a   Chipuk, Jerry E ^a,d   Fisher, John C ^a,b   Yun, Mi Kyung ^a   Grace, Christy R ^a   Nourse, Amanda ^a   Baran, Katherine ^a   Ou, Li ^a   Min, Lie ^a   White, Stephen W ^a,c   Green, Douglas R ^a   Kriwacki, Richard W ^a,c  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL XL; PROTEIN P53; PUMA PROTEIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; X RAY CRYSTALLOGRAPHY;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-X PROTEIN; HUMANS; MODELS, MOLECULAR; PROTEIN UNFOLDING; PROTO-ONCOGENE PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84874044758     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1166     Document Type: Article

References (57)

1. Green, D.R. & Kroemer, G. Cytoplasmic functions of the tumour suppressor p53. Nature 458, 1127-1130 (2009).
2. Chipuk, J.E., Bouchier-Hayes, L., Kuwana, T., Newmeyer, D.D. & Green, D.R. PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 309, 1732-1735 (2005). (Pubitemid 41285944)
3. Nakano, K. & Vousden, K.H. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7, 683-694 (2001). (Pubitemid 32706359)
4. Yu, J., Zhang, L., Hwang, P.M., Kinzler, K.W. & Vogelstein, B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell 7, 673-682 (2001). (Pubitemid 32706358)
5. Jeffers, J.R. et al. Puma is an essential mediator of p53-dependent and-independent apoptotic pathways. Cancer Cell 4, 321-328 (2003). (Pubitemid 37329796)
6. Chen, L. et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell 17, 393-403 (2005). (Pubitemid 40193310)
7. Kuwana, T. et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 17, 525-535 (2005). (Pubitemid 40269117)
8. Chipuk, J.E. et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303, 1010-1014 (2004). (Pubitemid 38209704)
9. Leu, J.I., Dumont, P., Hafey, M., Murphy, M.E. & George, D.L. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat. Cell Biol. 6, 443-450 (2004). (Pubitemid 38607505)
10. Chipuk, J.E. et al. Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc. Natl. Acad. Sci. USA 105, 20327-20332 (2008).
11. Hinds, M.G. et al. Bim, Bad and Bmf: intrinsically unstructured BH3-only proteins that undergo a localized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death Differ. 14, 128-136 (2007). (Pubitemid 44911900)
12. Sattler, M. et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275, 983-986 (1997). (Pubitemid 27087715)
13. Petros, A.M. et al. Rationale for Bcl-xL/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci. 9, 2528-2534 (2000). (Pubitemid 32105735)
14. Feng, W., Huang, S., Wu, H. & Zhang, M. Molecular basis of Bcl-xL′s target recognition versatility revealed by the structure of Bcl-xL in complex with the BH3 domain of Beclin-1. J. Mol. Biol. 372, 223-235 (2007). (Pubitemid 47223231)
15. Liu, X., Dai, S., Zhu, Y., Marrack, P. & Kappler, J.W. The structure of a Bcl-xL/Bim fragment complex: implications for Bim function. Immunity 19, 341-352 (2003). (Pubitemid 37153411)
16. Petros, A.M., Gunasekera, A., Xu, N., Olejniczak, E.T. & Fesik, S.W. Defining the p53 DNA-binding domain/Bcl-xL-binding interface using NMR. FEBS Lett. 559, 171-174 (2004). (Pubitemid 38186723)
17. Hagn, F. et al. BclxL changes conformation upon binding to wild-type but not mutant p53 DNA binding domain. J. Biol. Chem. 285, 3439-3450 (2010).
18. Muchmore, S.W. et al. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381, 335-341 (1996).
19. Berjanskii, M. & Wishart, D.S. NMR: prediction of protein flexibility. Nat. Protoc. 1, 683-688 (2006).
20. O′Neill, J.W., Manion, M.K., Maguire, B. & Hockenbery, D.M. BCL-XL dimerization by three-dimensional domain swapping. J. Mol. Biol. 356, 367-381 (2006). (Pubitemid 43099977)
21. Denisov, A.Y., Sprules, T., Fraser, J., Kozlov, G. & Gehring, K. Heat-induced dimerization of BCL-xL through α-helix swapping. Biochemistry 46, 734-740 (2007). (Pubitemid 46133589)
22. Day, C.L. et al. 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 (2008).
23. Smits, C., Czabotar, P.E., Hinds, M.G. & Day, C.L. Structural plasticity underpins promiscuous binding of the prosurvival protein A1. Structure 16, 818-829 (2008). (Pubitemid 351615010)
24. Nikolova, P.V., Henckel, J., Lane, D.P. & Fersht, A.R. Semirational design of active tumor suppressor p53 DNA binding domain with enhanced stability. Proc. Natl. Acad. Sci. USA 95, 14675-14680 (1998). (Pubitemid 29003689)
25. Joerger, A.C., Allen, M.D. & Fersht, A.R. Crystal structure of a superstable mutant of human p53 core domain. Insights into the mechanism of rescuing oncogenic mutations. J. Biol. Chem. 279, 1291-1296 (2004). (Pubitemid 38082653)
26. Xu, H. et al. The MDM2-binding region in the transactivation domain of p53 also acts as a Bcl-X-L-binding motif. Biochemistry 48, 12159-12168 (2009).
27. Letai, A. et al. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2, 183-192 (2002). (Pubitemid 41043974)
28. Kim, H. et al. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell 36, 487-499 (2009).
29. Ren, D. et al. BID, BIM, and PUMA are essential for activation of the BAX-and BAK-dependent cell death program. Science 330, 1390-1393 (2010).
30. Miyashita, O., Onuchic, J.N. & Wolynes, P.G. Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc. Natl. Acad. Sci. USA 100, 12570-12575 (2003). (Pubitemid 37339939)
31. Swain, J.F. & Gierasch, L.M. The changing landscape of protein allostery. Curr. Opin. Struct. Biol. 16, 102-108 (2006). (Pubitemid 43221878)
32. Frederick, K.K., Marlow, M.S., Valentine, K.G. & Wand, A.J. Conformational entropy in molecular recognition by proteins. Nature 448, 325-329 (2007). (Pubitemid 47080342)
33. Henzler-Wildman, K. & Kern, D. Dynamic personalities of proteins. Nature 450, 964-972 (2007). (Pubitemid 350273626)
34. Tzeng, S.R. & Kalodimos, C.G. Dynamic activation of an allosteric regulatory protein. Nature 462, 368-372 (2009).
35. Boehr, D.D., McElheny, D., Dyson, H.J. & Wright, P.E. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638-1642 (2006). (Pubitemid 44414038)
36. Masterson, L.R. et al. Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy. Proc. Natl. Acad. Sci. USA 108, 6969-6974 (2011).
37. Smock, R.G. & Gierasch, L.M. Sending signals dynamically. Science 324, 198-203 (2009).
38. Wang, Y., Filippov, I., Richter, C., Luo, R. & Kriwacki, R.W. Solution NMR studies of an intrinsically unstructured protein within a dilute, 75 kDa eukaryotic protein assembly; probing the practical limits for efficiently assigning polypeptide backbone resonances. ChemBioChem 6, 2242-2246 (2005).
39. Laue, T.M., Shah, B.D., Ridgeway, T.M. & Pelletier, S.L. Computer-aided interpretation of analytical sedimentation data for proteins in Analytical Ultracentrifugation in Biochemistry and Polymer Science (eds. S.E. Harding, A.J. Rowe & J.C. Horton) 90-125 (The Royal Society of Chemistry, 1992).
40. Schuck, P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619 (2000). (Pubitemid 30141584)
41. Schuck, P., Perugini, M.A., Gonzales, N.R., Howlett, G.J. & Schubert, D. Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82, 1096-1111 (2002). (Pubitemid 34111246)
42. Balbo, A., Brown, P.H., Braswell, E.H. & Schuck, P. Measuring protein-protein interactions by equilibrium sedimentation. Curr. Prot. Immunol. 18, 188 (2007).
43. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
44. Keller, R.J.J. Optimizing the Process of Nuclear Magnetic Resonance Spectrum Analysis and Computer Aided Resonance Assignment. PhD thesis, Eidgenossische Technishe Hochschule (2005).
45. Religa, T.L., Ruschak, A.M., Rosenzweig, R. & Kay, L.E. Site-directed methyl group labeling as an NMR probe of structure and dynamics in supramolecular protein systems: applications to the proteasome and to the ClpP protease. J. Am. Chem. Soc. 133, 9063-9068 (2011).
46. Tugarinov, V. & Kay, L.E. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J. Am. Chem. Soc. 125, 13868-13878 (2003). (Pubitemid 37386061)
47. Tugarinov, V. & Kay, L.E. An isotope labeling strategy for methyl TROSY spectroscopy. J. Biomol. NMR 28, 165-172 (2004). (Pubitemid 38232795)
48. Tugarinov, V., Choy, W.Y., Orekhov, V.Y. & Kay, L.E. Solution NMR-derived global fold of a monomeric 82-kDa enzyme. Proc. Natl. Acad. Sci. USA 102, 622-627 (2005). (Pubitemid 40282715)
49. Güntert, P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378 (2004).
50. Cornilescu, G., Delaglio, F. & Bax, A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (1999). (Pubitemid 29143535)
51. Pettersen, E.F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
52. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. & Thornton, J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (1996). (Pubitemid 126706801)
53. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L. & Schwede, T. The SWISS-MODEL Repository and associated resources. Nucleic Acids Res. 37, D387-D392 (2009).
54. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
55. Zwart, P.H. et al. Automated structure solution with the PHENIX suite. Methods Mol. Biol. 426, 419-435 (2008).
56. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
57. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).