'Latent drivers' expand the cancer mutational landscape

Current Opinion in Structural Biology

Volumn 32, Issue , 2015, Pages 25-32

  Nussinov, Ruth ^a,b   Tsai, Chung Jung ^a  

^a FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERISM; CANCER GENETICS; CANCER GROWTH; DRIVER MUTATION; GENOME ANALYSIS; HUMAN; LATENT DRIVER MUTATION; MULTIGENE FAMILY; MUTATION; MUTATION RATE; PASSENGER MUTATION; PROTEIN DATABASE; REVIEW; SIGNAL TRANSDUCTION; TUMOR PROMOTION; ANIMAL; CHEMICAL STRUCTURE; GENETICS; NEOPLASM;

PROTEIN;

ANIMALS; HUMANS; MODELS, MOLECULAR; MUTATION; NEOPLASMS; PROTEINS;

EID: 84922683604     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.01.004     Document Type: Review

References (64)

1. Vogelstein B., Papadopoulos N., Velculescu V.E., Zhou S.B., Diaz L.A., Kinzler K.W. Cancer genome landscapes. Science 2013, 339:1546-1558.
2. Welch J.S., Ley T.J., Link D.C., Miller C.A., Larson D.E., Koboldt D.C., Wartman L.D., Lamprecht T.L., Liu F.L., Xia J., et al. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012, 150:264-278.
3. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
4. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
5. Thiagalingam S., Lengauer C., Leach F.S., Schutte M., Hahn S.A., Overhauser J., Willson J.K.V., Markowitz S., Hamilton S.R., Kern S.E., et al. Evaluation of candidate tumour suppressor genes on chromosome 18 in colorectal cancers. Nat Genet 1996, 13:343-346.
6. Nussinov R., Tsai C.-J. Allostery in disease and in drug discovery. Cell 2013, 153:293-305.
7. Egeblad M., Nakasone E.S., Werb Z. Tumors as organs: complex tissues that interface with the entire organism. Dev Cell 2010, 18:884-901.
8. Merlo L.M.F., Pepper J.W., Reid B.J., Maley C.C. Cancer as an evolutionary and ecological process. Nat Rev Cancer 2006, 6:924-935.
9. Greaves M., Maley C.C. Clonal evolution in cancer. Nature 2012, 481:306-313.
10. Youn A., Simon R. Identifying cancer driver genes in tumor genome sequencing studies. Bioinformatics 2011, 27:175-181.
11. Bignell G.R., Greenman C.D., Davies H., Butler A.P., Edkins S., Andrews J.M., Buck G., Chen L.N., Beare D., Latimer C., et al. Signatures of mutation and selection in the cancer genome. Nature 2010, 463:893-898.
12. Stratton M.R., Campbell P.J., Futreal P.A. The cancer genome. Nature 2009, 458:719-724.
13. Roskoski R. The ErbB/HER family of protein-tyrosine kinases and cancer. Pharmacol Res 2014, 79:34-74.
14. Poulikakos P.I., Zhang C., Bollag G., Shokat K.M., Rosen N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010, 464:427-430.
15. Nakamura A., Arita T., Tsuchiya S., Donelan J., Chouitar J., Carideo E., Galvin K., Okaniwa M., Ishikawa T., Yoshida S. Antitumor activity of the selective Pan-RAF inhibitor TAK-632 in BRAF inhibitor-resistant melanoma. Cancer Res 2013, 73:7043-7055.
16. Knievel J., Schulz W.A., Greife A., Hader C., Lubke T., Schmitz I., Albers P., Niegisch G. Multiple mechanisms mediate resistance to sorafenib in urothelial cancer. Int J Mol Sci 2014, 15:20500-20517.
17. Nussinov R., Jang H., Tsai C.-J. The structural basis for cancer treatment decisions. Oncotarget 2014, 5:7285-7302.
18. Pelizzola M., Ecker J.R. The DNA methylome. FEBS Lett 2011, 585:1994-2000.
19. Miller D.G. On the nature of susceptibility to cancer - the presidential-address. Cancer 1980, 46:1307-1318.
20. Beerenwinkel N., Antal T., Dingli D., Traulsen A., Kinzler K.W., Velculescu V.E., Vogelstein B., Nowak M.A. Genetic progression and the waiting time to cancer. PLoS Comp Biol 2007, 3:2239-2246.
21. Ozbabacan S.E.A., Gursoy A., Nussinov R., Keskin O. The structural pathway of interleukin 1 (IL-1) initiated signaling reveals mechanisms of oncogenic mutations and SNPs in inflammation and cancer. PLoS Comp Biol 2014, 10:e1003470.
22. Tuncbag N., Kar G., Gursoy A., Keskin O., Nussinov R. Towards inferring time dimensionality in protein-protein interaction networks by integrating structures: the p53 example. Mol Biosyst 2009, 5:1770-1778.
23. Engin H.B., Keskin O., Nussinov R., Gursoy A. A strategy based on protein-protein interface motifs may help in identifying drug off-targets. J Chem Inf Model 2012, 52:2273-2286.
24. Engin H.B., Gursoy A., Nussinov R., Keskin O. Network-based strategies can help mono-and poly-pharmacology drug discovery: a systems biology view. Curr Pharm Des 2014, 20:1201-1207.
25. Shan Y., Eastwood M.P., Zhang X., Kim E.T., Arkhipov A., Dror R.O., Jumper J., Kuriyan J., Shaw D.E. Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 2012, 149:860-870.
26. Sutto L., Gervasio F.L. Effects of oncogenic mutations on the conformational free-energy landscape of EGFR kinase. Proc Natl Acad Sci U S A 2013, 110:10616-10621.
27. Tsai C.J., Nussinov R. The free energy landscape in translational science: how can somatic mutations result in constitutive oncogenic activation?. Phys Chem Chem Phys 2014, 16:6332-6341.
28. Tsai C.-J., Nussinov R. The molecular basis of targeting protein kinases in cancer therapeutics. Semin Cancer Biol 2013, 23:235-242.
29. Tsai C.-J., Nussinov R. A unified view of "How Allostery Works". PLoS Comput Biol 2014, 10:e1003394.
30. Gajiwala K.S., Feng J., Ferre R., Ryan K., Brodsky O., Weinrich S., Kath J.C., Stewart A. Insights into the aberrant activity of mutant EGFR kinase domain and drug recognition. Structure 2013, 21:209-219.
31. Yoshikawa S., Kukimoto-Niino M., Parker L., Handa N., Terada T., Fujimoto T., Terazawa Y., Wakiyama M., Sato M., Sano S., et al. Structural basis for the altered drug sensitivities of non-small cell lung cancer-associated mutants of human epidermal growth factor receptor. Oncogene 2013, 32:27-38.
32. Zhang X., Gureasko J., Shen K., Cole P.A., Kuriyan J. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 2006, 125:1137-1149.
33. Yun C.-H., Boggon T.J., Li Y., Woo M.S., Greulich H., Meyerson M., Eck M.J. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 2007, 11:217-227.
34. Nussinov R., Tsai C.J., Ma B. The underappreciated role of allostery in the cellular network. Annu Rev Biophys 2013, 42:169-189.
35. Nussinov R., Ma B., Tsai C.-J., Csermely P. Allosteric conformational barcodes direct signaling in the cell. Structure 2013, 21:1509-1521.
36. Nussinov R., Tsai C.J., Xin F., Radivojac P. Allosteric post-translational modification codes. Trends Biochem Sci 2012, 37:447-554.
37. Ciriello G., Miller M.L., Aksoy B.A., Senbabaoglu Y., Schultz N., Sander C. Emerging landscape of oncogenic signatures across human cancers. Nat Genet 2013, 45:1127-1133.
38. Wang G.M., Wong H.Y., Konishi H., Blair B.G., Abukhdeir A.M., Gustin J.P., Rosen D.M., Denmeade S.R., Rasheed Z., Matsui W., et al. Single copies of mutant KRAS and mutant PIK3CA cooperate in immortalized human epithelial cells to induce tumor formation. Cancer Res 2013, 73:3248-3261.
39. Wichmann C., Quagliano-Lo Coco I., Yildiz O., Chen-Wichmann L., Weber H., Syzonenko T., Doring C., Brendel C., Ponnusamy K., Kinner A., et al. Activating c-KIT mutations confer oncogenic cooperativity and rescue RUNX1/ETO-induced DNA damage and apoptosis in human primary CD34+ hematopoietic progenitors. Leukemia 2014, 10.1038/leu.2014.179.
40. Hashimoto K., Rogozin I.B., Panchenko A.R. Oncogenic potential is related to activating effect of cancer single and double somatic mutations in receptor tyrosine kinases. Hum Mutat 2012, 33:1566-1575.
41. Bradshaw J.M. The Src, Syk, and Tec family kinases: distinct types of molecular switches. Cell Signal 2010, 22:1175-1184.
42. Nussinov R., Tsai C.-J. Free energy diagrams for protein function. Chem Biol 2014, 21:311-318.
43. Roche-Lestienne C., Soenen-Cornu V., Grardel-Duflos N., Lai J.L., Philippe N., Facon T., Fenaux P., Preudhomme C. Several types of mutations of the Abl gene can be found in chronic myeloid leukemia patients resistant to ST157, and they can pre-exist to the onset of treatment. Blood 2002, 100:1014-1018.
44. Mullighan C.G., Phillips L.A., Su X.P., Ma J., Miller C.B., Shurtleff S.A., Downing J.R. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 2008, 322:1377-1380.
45. Forbes S.A., Bindal N., Bamford S., Cole C., Kok C.Y., Beare D., Jia M.M., Shepherd R., Leung K., Menzies A., et al. COSMIC: mining complete cancer genomes in the catalogue of somatic mutations in cancer. Nucleic Acids Res 2011, 39:D945-D950.
46. Heim D., Budczies J., Stenzinger A., Treue D., Hufnagl P., Denkert C., Dietel M., Klauschen F. Cancer beyond organ and tissue specificity: next-generation-sequencing gene mutation data reveal complex genetic similarities across major cancers. Int J Cancer 2014, 135:2362-2369.
47. Onken M.D., Winkler A.E., Kanchi K.L., Chalivendra V., Law J.H., Rickert C.G., Kallogjeri D., Judd N.P., Dunn G.P., Piccirillo J.F., et al. A surprising cross-species conservation in the genomic landscape of mouse and human oral cancer identifies a transcriptional signature predicting metastatic disease. Clin Cancer Res 2014, 20:2873-2884.
48. Sparano J.A., Golden A.A.J., Montagna C. Translating the TCGA breast cancer results into clinical practice: searching for therapeutic clues. Oncology 2013, 27:1284-1286.
49. Ma C.X., Ellis M.J. The cancer genome atlas: clinical applications for breast cancer. Oncology 2013, 27:1263-1269.
50. Michaelson J.J., Shi Y.J., Gujral M., Zheng H.C., Malhotra D., Jin X., Jian M.H., Liu G.M., Greer D., Bhandari A., et al. Whole-genome sequencing in autism identifies hot spots for de novo germline mutation. Cell 2012, 151:1431-1442.
51. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 2002, 298:1911-1912.
52. Chin L., Meyerson M., Aldape K., Bigner D., Mikkelsen T., VandenBerg S., Kahn A., Penny R., Ferguson M.L., Gerhard D.S., et al. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068.
53. Carter H., Karchin R. Predicting the functional consequences of somatic missense mutations found in tumors. Methods Mol Biol 2014, 1101:135-159.
54. Shan Y.B., Seeliger M.A., Eastwood M.P., Frank F., Xu H.F., Jensen M.O., Dror R.O., Kuriyan J., Shaw D.E. A conserved protonation-dependent switch controls drug binding in the Abl kinase. Proc Natl Acad Sci U S A 2009, 106:139-144.
55. Yi K.H., Axtmayer J., Gustin J.P., Rajpurohit A., Lauring J. Functional analysis of non-hotspot AKT1 mutants found in human breast cancers identifies novel driver mutations: implications for personalized medicine. Oncotarget 2013, 4:29-34.
56. Parikh C., Janakiraman V., Wu W.I., Foo C.K., Kljavin N.M., Chaudhuri S., Stawiski E., Lee B., Lin J., Li H., et al. Disruption of PH-kinase domain interactions leads to oncogenic activation of AKT in human cancers. Proc Natl Acad Sci U S A 2012, 109:19368-19373.
57. Smith G., Bounds R., Wolf H., Steele R.J.C., Carey F.A., Wolf C.R. Activating K-Ras mutations outwith 'hotspot' codons in sporadic colorectal tumours - implications for personalised cancer medicine. Br J Cancer 2010, 102:693-703.
58. Lesterhuis W.J., Bosco A., Lake R.A. Comment on "Drug Discovery: turning the titanic. Sci Trans Med 2014, 6:229le.
59. van Hagen P., Hulshof M., van Lanschot J.J.B., Steyerberg E.W., Henegouwen M.I.V., Wijnhoven B.P.L., Richel D.J., Nieuwenhuijzen G.A.P., Hospers G.A.P., Bonenkamp J.J., et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 2012, 366:2074-2084.
60. Nussinov R., Tsai C.-J., Mattos C. 'Pathway drug cocktail': targeting Ras signaling based on structural pathways. Trends Mol Med 2013, 19:695-704.
61. Li M., Petukh M., Alexov E., Panchenko A.R. Predicting the impact of missense mutations on protein-protein binding affinity. J Chem Theory Comput 2014, 10(4):1770-1780.
62. Stefl S., Nishi H., Petukh M., Panchenko A.R., Alexov E. Molecular mechanisms of disease-causing missense mutations. J Mol Biol 2013, 425:3919-3936.
63. Blacklock K., Verkhivker G.M. Computational modeling of allosteric regulation in the hsp90 chaperones: a statistical ensemble analysis of protein structure networks and allosteric communications. PLoS Comput Biol 2014, 10(6):e1003679.
64. Dixit A., Verkhivker G.M. Computational modeling of allosteric communication reveals organizing principles of mutation-induced signaling in ABL and EGFR kinases. PLoS Comput Biol 2011, 7(10):e1002179.