Mutation-induced protein interaction kinetics changes affect apoptotic network dynamic properties and facilitate oncogenesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 30, 2015, Pages E4046-E4054

  Zhao, Linjie ^a   Sun, Tanlin ^a   Pei, Jianfeng ^a   Ouyang, Qi ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

Dynamic bifurcation; Mutation enrichment; Mutation induced oncogenesis; Parameter sensitivity analysis; Protein interaction kinetics

Indexed keywords

BIM PROTEIN; CASPASE 8; PROTEASOME; PROTEIN; PROTEIN A; PROTEIN B; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN;

APOPTOSIS; ARTICLE; BINDING KINETICS; CARCINOGENESIS; CELL DEATH; CELL MEMBRANE PERMEABILITY; CHROMOSOME TRANSLOCATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVATION; EQUILIBRIUM CONSTANT; GENE LOCATION; GENE REGULATORY NETWORK; GENE TRANSLOCATION; HYDROGEN BOND; INDUCED MUTATION; MATHEMATICAL MODEL; MISSENSE MUTATION; MOLECULAR DYNAMICS; NONLINEAR SYSTEM; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; STEADY STATE; CELL TRANSFORMATION; CHEMISTRY; CLUSTER ANALYSIS; GENETICS; HUMAN; KINETICS; METABOLISM; MITOCHONDRION; MUTATION; NEOPLASM; PROTEIN ANALYSIS; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; THEORETICAL MODEL; THERMODYNAMICS;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARCINOGENESIS; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; HUMANS; KINETICS; MITOCHONDRIA; MODELS, THEORETICAL; MOLECULAR DYNAMICS SIMULATION; MUTATION; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 84938149088     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1502126112     Document Type: Article

References (55)

1. Kandoth C, et al. (2013) Mutational landscape and significance across 12 major cancer types. Nature 502(7471):333-339.
2. Dahl F, et al. (2007) Multigene amplification and massively parallel sequencing for cancer mutation discovery. Proc Natl Acad Sci USA 104(22):9387-9392.
3. Alexandrov LB, et al.; Australian Pancreatic Cancer Genome Initiative; ICGC Breast Cancer Consortium; ICGC MMML-Seq Consortium; ICGC PedBrain (2013) Signatures of mutational processes in human cancer. Nature 500(7463):415-421.
4. Stratton MR, Campbell PJ, Futreal PA (2009) The cancer genome. Nature 458(7239):719-724.
5. Jones S, et al. (2008) Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321(5897):1801-1806.
6. Ding L, et al. (2008) Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455(7216):1069-1075.
7. Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455(7216):1061-1068.
8. Bild AH, Potti A, Nevins JR (2006) Linking oncogenic pathways with therapeutic opportunities. Nat Rev Cancer 6(9):735-741.
9. Pe'er D, Hacohen N (2011) Principles and strategies for developing network models in cancer. Cell 144(6):864-873.
10. Kreeger PK, Lauffenburger DA (2010) Cancer systems biology: A network modeling perspective. Carcinogenesis 31(1):2-8.
11. Ferrell JE, Jr, Tsai TY, Yang Q (2011) Modeling the cell cycle: Why do certain circuits oscillate? Cell 144(6):874-885.
12. Zhang XP, Liu F, Cheng Z, Wang W (2009) Cell fate decision mediated by p53 pulses. Proc Natl Acad Sci USA 106(30):12245-12250.
13. Ma W, Trusina A, El-Samad H, Lim WA, Tang C (2009) Defining network topologies that can achieve biochemical adaptation. Cell 138(4):760-773.
14. Stites EC, Trampont PC, Ma Z, Ravichandran KS (2007) Network analysis of oncogenic Ras activation in cancer. Science 318(5849):463-467.
15. Chen J, Yue H, Ouyang Q (2014) Correlation between oncogenic mutations and parameter sensitivity of the apoptosis pathway model. PLOS Comput Biol 10(1):e1003451.
16. Tait SW, Green DR (2010) Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 11(9):621-632.
17. Spencer SL, Sorger PK (2011) Measuring and modeling apoptosis in single cells. Cell 144(6):926-939.
18. Chipuk JE, Bouchier-Hayes L, Green DR (2006) Mitochondrial outer membrane permeabilization during apoptosis: The innocent bystander scenario. Cell Death Differ 13(8):1396-1402.
19. Llambi F, Green DR (2011) Apoptosis and oncogenesis: Give and take in the BCL-2 family. Curr Opin Genet Dev 21(1):12-20.
20. Youle RJ, Strasser A (2008) The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9(1):47-59.
21. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94(4):491-501.
22. Lovell JF, et al. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135(6):1074-1084.
23. Kim H, et al. (2009) Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 36(3):487-499.
24. Hsu Y-T, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X (L) during apoptosis. Proc Natl Acad Sci USA 94(8):3668-3672.
25. Tan C, et al. (2006) Auto-activation of the apoptosis protein Bax increases mitochondrial membrane permeability and is inhibited by Bcl-2. J Biol Chem 281(21):14764-14775.
26. Happo L, Strasser A, Cory S (2012) BH3-only proteins in apoptosis at a glance. J Cell Sci 125(Pt 5):1081-1087.
27. Chen C, et al. (2007) Modeling of the role of a Bax-activation switch in the mitochondrial apoptosis decision. Biophys J 92(12):4304-4315.
28. Leber B, Lin J, Andrews DW (2007) Embedded together: The life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 12(5):897-911.
29. Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK (2006) Physicochemical modelling of cell signalling pathways. Nat Cell Biol 8(11):1195-1203.
30. Lu M, Jolly MK, Levine H, Onuchic JN, Ben-Jacob E (2013) MicroRNA-based regulation of epithelial-hybrid-mesenchymal fate determination. Proc Natl Acad Sci USA 110(45):18144-18149.
31. Ferrell JE, Jr, et al. (2009) Simple, realistic models of complex biological processes: Positive feedback and bistability in a cell fate switch and a cell cycle oscillator. FEBS Lett 583(24):3999-4005.
32. Lee YS, Liu OZ, Hwang HS, Knollmann BC, Sobie EA (2013) Parameter sensitivity analysis of stochastic models provides insights into cardiac calcium sparks. Biophys J 104(5):1142-1150.
33. Yue H, et al. (2006) Insights into the behaviour of systems biology models from dynamic sensitivity and identifiability analysis: A case study of an NF-kappaB signalling pathway. Mol Biosyst 2(12):640-649.
34. Forbes SA, et al. (2015) COSMIC: Exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res 43(Database Issue):D805-D811.
35. Yamamoto H, Sawai H, Perucho M (1997) Frameshift somatic mutations in gastrointestinal cancer of the microsatellite mutator phenotype. Cancer Res 57(19):4420-4426.
36. Sherry ST, et al. (2001) dbSNP: The NCBI database of genetic variation. Nucleic Acids Res 29(1):308-311.
37. Billen LP, Shamas-Din A, Andrews DW (2008) Bid: A Bax-like BH3 protein. Oncogene 27(Suppl 1):S93-S104.
38. Schinzel A, et al. (2004) Conformational control of Bax localization and apoptotic activity by Pro168. J Cell Biol 164(7):1021-1032.
39. Gil J, Yamamoto H, Zapata JM, Reed JC, Perucho M (1999) Impairment of the proapoptotic activity of Bax by missense mutations found in gastrointestinal cancers. Cancer Res 59(9):2034-2037.
40. Vogelstein B, et al. (2013) Cancer genome landscapes. Science 339(6127):1546-1558.
41. Ku B, Liang C, Jung JU, Oh BH (2011) Evidence that inhibition of BAX activation by BCL-2 involves its tight and preferential interaction with the BH3 domain of BAX. Cell Res 21(4):627-641.
42. Zha H, et al. (1996) Structure-function comparisons of the proapoptotic protein Bax in yeast and mammalian cells. Mol Cell Biol 16(11):6494-6508.
43. Czabotar PE, et al. (2013) Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 152(3):519-531.
44. Dhillon AS, Hagan S, Rath O, Kolch W (2007) MAP kinase signalling pathways in cancer. Oncogene 26(22):3279-3290.
45. Schreiber G (2002) Kinetic studies of protein-protein interactions. Curr Opin Struct Biol 12(1):41-47.
46. Tiwary P, Limongelli V, Salvalaglio M, Parrinello M (2015) Kinetics of protein-ligand unbinding: Predicting pathways, rates, and rate-limiting steps. Proc Natl Acad Sci USA 112(5):E386-E391.
47. Fredriksson NJ, Ny L, Nilsson JA, Larsson E (2014) Systematic analysis of noncoding somatic mutations and gene expression alterations across 14 tumor types. Nat Genet 46(12):1258-1263.
48. O'Farrell TJ, Ghosh P, Dobashi N, Sasaki CY, Longo DL (2004) Comparison of the effect of mutant and wild-type p53 on global gene expression. Cancer Res 64(22):8199-8207.
49. Tank EM, True HL (2009) Disease-associated mutant ubiquitin causes proteasomal impairment and enhances the toxicity of protein aggregates. PLoS Genet 5(2):e1000382.
50. Albeck JG, Burke JM, Spencer SL, Lauffenburger DA, Sorger PK (2008) Modeling a snap-action, variable-delay switch controlling extrinsic cell death. PLoS Biol 6(12):2831-2852.
51. The 1000 Genomes Project Consortium (2010) A map of human genome variation from population-scale sequencing. Nature 467(7319):1061-1073.
52. Ikegaki N, Katsumata M, Minna J, Tsujimoto Y (1994) Expression of bcl-2 in small cell lung carcinoma cells. Cancer Res 54(1):6-8.
53. Monni O, et al. (1997) BCL2 overexpression associated with chromosomal amplification in diffuse large B-cell lymphoma. Blood 90(3):1168-1174.
54. Rampino N, et al. (1997) Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 275(5302):967-969.
55. Gohlke H, Kiel C, Case DA (2003) Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes. J Mol Biol 330(4):891-913.