Proteome-Scale Investigation of Protein Allosteric Regulation Perturbed by Somatic Mutations in 7,000 Cancer Genomes

American Journal of Human Genetics

Volumn 100, Issue 1, 2017, Pages 5-20

  Shen, Qiancheng ^a   Cheng, Feixiong ^b,c   Song, Huili ^a   Lu, Weiqiang ^d   Zhao, Junfei ^c   An, Xiaoli ^a   Liu, Mingyao ^d   Chen, Guoqiang ^a   Zhao, Zhongming ^e   Zhang, Jian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SICHUAN UNIVERSITY   (China)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d EAST CHINA NORMAL UNIVERSITY   (China)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ANDROGEN RECEPTOR; ANTITHROMBIN III; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYTOCHROME P450 3A4; DIPYRIDAMOLE; ESTROGEN RECEPTOR BETA; FOCAL ADHESION KINASE 1; GLUCOKINASE; GRIA2 PROTEIN; HEXOKINASE 1; ITGAL PROTEIN; LEUKOTRIENE A4 HYDROLASE; MALT1 PROTEIN; MARDEPODECT; ME2 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 14; MUSCARINIC M2 RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHODIESTERASE; PHOSPHODIESTERASE 10A; PRKAA2 PROTEIN; PROLINE; PROTEIN; PROTEOME; SAMHD1 PROTEIN; SERPINE1 PROTEIN; SOMATOMEDIN C RECEPTOR; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

A-549 CELL LINE; ALLOSTERISM; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; BLADDER CARCINOMA; BREAST CARCINOMA; CANCER GENETICS; CANCER GENOME; CARCINOGENESIS; CONTROLLED STUDY; CUTANEOUS MELANOMA; CYSTADENOCARCINOMA; ENDOMETRIUM CARCINOMA; ESSENTIAL GENE; EVOLUTION; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENOME; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HEK293 CELL LINE; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; LUNG ADENOCARCINOMA; LUNG CANCER CELL LINE; MALIGNANT NEOPLASM; MICROARRAY ANALYSIS; MISSENSE MUTATION; MULTIPLE CANCER; OVARY ADENOCARCINOMA; PREDICTION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEOMICS; SOMATIC MUTATION; SQUAMOUS CELL LUNG CARCINOMA; STATISTICAL ANALYSIS; STOMACH ADENOCARCINOMA; TRANSITIONAL CELL CARCINOMA; TUMOR GENE; VALIDATION STUDY; ALLOSTERIC SITE; GENETICS; HUMAN GENOME; KAPLAN MEIER METHOD; LUNG TUMOR; MOLECULARLY TARGETED THERAPY; NEOPLASM; NON SMALL CELL LUNG CANCER; PROCEDURES; TRENDS; TUMOR CELL LINE;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; CARCINOGENESIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; GENOME, HUMAN; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; MUTATION, MISSENSE; NEOPLASMS; PROTEOME; PROTEOMICS;

EID: 85008178819     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.09.020     Document Type: Article

References (69)

1. 1 Siegel, R.L., Miller, K.D., Jemal, A., Cancer statistics, 2015. CA Cancer J. Clin. 65 (2015), 5–29.
2. 2 Weinstein, J.N., Collisson, E.A., Mills, G.B., Shaw, K.R., Ozenberger, B.A., Ellrott, K., Shmulevich, I., Sander, C., Stuart, J.M., Cancer Genome Atlas Research Network. The Cancer Genome Atlas Pan-Cancer analysis project. Nat. Genet. 45 (2013), 1113–1120.
3. 3 Hudson, T.J., Anderson, W., Artez, A., Barker, A.D., Bell, C., Bernabé, R.R., Bhan, M.K., Calvo, F., Eerola, I., Gerhard, D.S., et al., International Cancer Genome Consortium. International network of cancer genome projects. Nature 464 (2010), 993–998.
4. 4 Kandoth, C., McLellan, M.D., Vandin, F., Ye, K., Niu, B., Lu, C., Xie, M., Zhang, Q., McMichael, J.F., Wyczalkowski, M.A., et al. Mutational landscape and significance across 12 major cancer types. Nature 502 (2013), 333–339.
5. 5 Vogelstein, B., Papadopoulos, N., Velculescu, V.E., Zhou, S., Diaz, L.A. Jr., Kinzler, K.W., Cancer genome landscapes. Science 339 (2013), 1546–1558.
6. 6 Cheng, F., Zhao, J., Zhao, Z., Advances in computational approaches for prioritizing driver mutations and significantly mutated genes in cancer genomes. Brief. Bioinform. 17 (2016), 642–656.
7. 7 Vuong, H., Cheng, F., Lin, C.C., Zhao, Z., Functional consequences of somatic mutations in cancer using protein pocket-based prioritization approach. Genome Med. 6 (2014), 81–95.
8. 8 De Smet, F., Christopoulos, A., Carmeliet, P., Allosteric targeting of receptor tyrosine kinases. Nat. Biotechnol. 32 (2014), 1113–1120.
9. 9 Eisenberg, D., Marcotte, E.M., Xenarios, I., Yeates, T.O., Protein function in the post-genomic era. Nature 405 (2000), 823–826.
10. 10 Nussinov, R., Tsai, C.J., Allostery in disease and in drug discovery. Cell 153 (2013), 293–305.
11. 11 Pe'er, D., Hacohen, N., Principles and strategies for developing network models in cancer. Cell 144 (2011), 864–873.
12. 12 Huang, S., Ernberg, I., Kauffman, S., Cancer attractors: a systems view of tumors from a gene network dynamics and developmental perspective. Semin. Cell Dev. Biol. 20 (2009), 869–876.
13. 13 Zhong, Q., Simonis, N., Li, Q.R., Charloteaux, B., Heuze, F., Klitgord, N., Tam, S., Yu, H., Venkatesan, K., Mou, D., et al. Edgetic perturbation models of human inherited disorders. Mol. Syst. Biol. 5 (2009), 321–330.
14. 14 Cheng, F., Liu, C., Lin, C.C., Zhao, J., Jia, P., Li, W.H., Zhao, Z., A Gene Gravity Model for the Evolution of Cancer Genomes: A Study of 3,000 Cancer Genomes across 9 Cancer Types. PLoS Comput. Biol., 11, 2015, e1004497.
15. 15 Huang, Z., Zhu, L., Cao, Y., Wu, G., Liu, X., Chen, Y., Wang, Q., Shi, T., Zhao, Y., Wang, Y., et al. ASD: a comprehensive database of allosteric proteins and modulators. Nucleic Acids Res. 39 (2011), D663–D669.
16. 16 Huang, Z., Mou, L., Shen, Q., Lu, S., Li, C., Liu, X., Wang, G., Li, S., Geng, L., Liu, Y., et al. ASD v2.0: updated content and novel features focusing on allosteric regulation. Nucleic Acids Res. 42 (2014), D510–D516.
17. 17 Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E., The Protein Data Bank. Nucleic Acids Res. 28 (2000), 235–242.
18. 18 UniProt Consortium. UniProt: a hub for protein information. Nucleic Acids Res. 43 (2015), D204–D212.
19. 19 Martin, A.C., Mapping PDB chains to UniProtKB entries. Bioinformatics 21 (2005), 4297–4301.
20. 20 Le Guilloux, V., Schmidtke, P., Tuffery, P., Fpocket: an open source platform for ligand pocket detection. BMC Bioinformatics 10 (2009), 168–179.
21. 21 Schmidtke, P., Bidon-Chanal, A., Luque, F.J., Barril, X., MDpocket: open-source cavity detection and characterization on molecular dynamics trajectories. Bioinformatics 27 (2011), 3276–3285.
22. 22 Alexandrov, L.B., Nik-Zainal, S., Wedge, D.C., Aparicio, S.A., Behjati, S., Biankin, A.V., Bignell, G.R., Bolli, N., Borg, A., Børresen-Dale, A.L., et al. Australian Pancreatic Cancer Genome Initiative ICGC Breast Cancer Consortium ICGC MMML-Seq Consortium, ICGC PedBrain. Signatures of mutational processes in human cancer. Nature 500 (2013), 415–421.
23. 23 Davoli, T., Xu, A.W., Mengwasser, K.E., Sack, L.M., Yoon, J.C., Park, P.J., Elledge, S.J., Cumulative haploinsufficiency and triplosensitivity drive aneuploidy patterns and shape the cancer genome. Cell 155 (2013), 948–962.
24. 24 Forbes, S.A., Bindal, N., Bamford, S., Cole, C., Kok, C.Y., Beare, D., Jia, 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. 39 (2011), D945–D950.
25. 25 Wang, K., Li, M., Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38 (2010), e164–e171.
26. 26 Ng, P.C., Henikoff, S., SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res. 31 (2003), 3812–3814.
27. 27 Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S., Sunyaev, S.R., A method and server for predicting damaging missense mutations. Nat. Methods 7 (2010), 248–249.
28. 28 Stenson, P.D., Ball, E.V., Mort, M., Phillips, A.D., Shiel, J.A., Thomas, N.S., Abeysinghe, S., Krawczak, M., Cooper, D.N., Human Gene Mutation Database (HGMD): 2003 update. Hum. Mutat. 21 (2003), 577–581.
29. 29 Cowley, M.J., Pinese, M., Kassahn, K.S., Waddell, N., Pearson, J.V., Grimmond, S.M., Biankin, A.V., Hautaniemi, S., Wu, J., PINA v2.0: mining interactome modules. Nucleic Acids Res. 40 (2012), D862–D865.
30. 30 Breuer, K., Foroushani, A.K., Laird, M.R., Chen, C., Sribnaia, A., Lo, R., Winsor, G.L., Hancock, R.E., Brinkman, F.S., Lynn, D.J., InnateDB: systems biology of innate immunity and beyond—recent updates and continuing curation. Nucleic Acids Res. 41 (2013), D1228–D1233.
31. 31 Dinkel, H., Chica, C., Via, A., Gould, C.M., Jensen, L.J., Gibson, T.J., Diella, F., Phospho.ELM: a database of phosphorylation sites—update 2011. Nucleic Acids Res. 39 (2011), D261–D267.
32. 32 Keshava Prasad, T.S., Goel, R., Kandasamy, K., Keerthikumar, S., Kumar, S., Mathivanan, S., Telikicherla, D., Raju, R., Shafreen, B., Venugopal, A., et al. Human Protein Reference Database—2009 update. Nucleic Acids Res. 37 (2009), D767–D772.
33. 33 Newman, R.H., Hu, J., Rho, H.S., Xie, Z., Woodard, C., Neiswinger, J., Cooper, C., Shirley, M., Clark, H.M., Hu, S., et al. Construction of human activity-based phosphorylation networks. Mol. Syst. Biol. 9 (2013), 655–666.
34. 34 Hu, J., Rho, H.S., Newman, R.H., Zhang, J., Zhu, H., Qian, J., PhosphoNetworks: a database for human phosphorylation networks. Bioinformatics 30 (2014), 141–142.
35. 35 Hornbeck, P.V., Kornhauser, J.M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B., Latham, V., Sullivan, M., PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40 (2012), D261–D270.
36. 36 Cheng, F., Jia, P., Wang, Q., Lin, C.C., Li, W.H., Zhao, Z., Studying tumorigenesis through network evolution and somatic mutational perturbations in the cancer interactome. Mol. Biol. Evol. 31 (2014), 2156–2169.
37. 37 Cheng, F., Jia, P., Wang, Q., Zhao, Z., Quantitative network mapping of the human kinome interactome reveals new clues for rational kinase inhibitor discovery and individualized cancer therapy. Oncotarget 5 (2014), 3697–3710.
38. 38 Benita, Y., Cao, Z., Giallourakis, C., Li, C., Gardet, A., Xavier, R.J., Gene enrichment profiles reveal T-cell development, differentiation, and lineage-specific transcription factors including ZBTB25 as a novel NF-AT repressor. Blood 115 (2010), 5376–5384.
39. 39 Cheng, F., Zhao, J., Fooksa, M., Zhao, Z., A network-based drug repositioning infrastructure for precision cancer medicine through targeting significantly mutated genes in the human cancer genomes. J. Am. Med. Inform. Assoc. 23 (2016), 681–691.
40. 40 Hamosh, A., Scott, A.F., Amberger, J.S., Bocchini, C.A., McKusick, V.A., Online Mendelian Inheritance in Man (OMIM), a knowledgebase of human genes and genetic disorders. Nucleic Acids Res. 33 (2005), D514–D517.
41. 41 Zhang, M., Zhu, C., Jacomy, A., Lu, L.J., Jegga, A.G., The orphan disease networks. Am. J. Hum. Genet. 88 (2011), 755–766.
42. 42 Cheng, F., Liu, C., Jiang, J., Lu, W., Li, W., Liu, G., Zhou, W., Huang, J., Tang, Y., Prediction of drug-target interactions and drug repositioning via network-based inference. PLoS Comput. Biol., 8, 2012, e1002503.
43. 43 Hirsh, A.E., Fraser, H.B., Wall, D.P., Adjusting for selection on synonymous sites in estimates of evolutionary distance. Mol. Biol. Evol. 22 (2005), 174–177.
44. 44 Bezginov, A., Clark, G.W., Charlebois, R.L., Dar, V.U., Tillier, E.R., Coevolution reveals a network of human proteins originating with multicellularity. Mol. Biol. Evol. 30 (2013), 332–346.
45. 45 Capra, J.A., Williams, A.G., Pollard, K.S., ProteinHistorian: tools for the comparative analysis of eukaryote protein origin. PLoS Comput. Biol., 8, 2012, e1002567.
46. 46 Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature 511 (2014), 543–550.
47. 47 Li, B., Dewey, C.N., RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12 (2011), 323–339.
48. 48 Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Methodol. 57 (1995), 289–300.
49. 49 Hochberg, Y., Benjamini, Y., More powerful procedures for multiple significance testing. Stat. Med. 9 (1990), 811–818.
50. 50 Zhao, G.C., Sun, M., Wilde, S.A., Li, S.Z., A Paleo-Mesoproterozoic supercontinent: assembly, growth and breakup. Earth Sci. Rev. 67 (2004), 91–123.
51. 51 Wenthur, C.J., Gentry, P.R., Mathews, T.P., Lindsley, C.W., Drugs for allosteric sites on receptors. Annu. Rev. Pharmacol. Toxicol. 54 (2014), 165–184.
52. 52 Tzoneva, G., Perez-Garcia, A., Carpenter, Z., Khiabanian, H., Tosello, V., Allegretta, M., Paietta, E., Racevskis, J., Rowe, J.M., Tallman, M.S., et al. Activating mutations in the NT5C2 nucleotidase gene drive chemotherapy resistance in relapsed ALL. Nat. Med. 19 (2013), 368–371.
53. 53 Zhang, L., Hu, A., Yuan, H., Cui, L., Miao, G., Yang, X., Wang, L., Liu, J., Liu, X., Wang, S., et al. A missense mutation in the CHRM2 gene is associated with familial dilated cardiomyopathy. Circ. Res. 102 (2008), 1426–1432.
54. 54 Cheng, F., Li, W., Zhou, Y., Li, J., Shen, J., Lee, P.W., Tang, Y., Prediction of human genes and diseases targeted by xenobiotics using predictive toxicogenomic-derived models (PTDMs). Mol. Biosyst. 9 (2013), 1316–1325.
55. 55 Davies, H., Bignell, G.R., Cox, C., Stephens, P., Edkins, S., Clegg, S., Teague, J., Woffendin, H., Garnett, M.J., Bottomley, W., et al. Mutations of the BRAF gene in human cancer. Nature 417 (2002), 949–954.
56. 56 Hobbs, G.A., Der, C.J., Rossman, K.L., RAS isoforms and mutations in cancer at a glance. J. Cell Sci. 129 (2016), 1287–1292.
57. 57 Carpten, J.D., Faber, A.L., Horn, C., Donoho, G.P., Briggs, S.L., Robbins, C.M., Hostetter, G., Boguslawski, S., Moses, T.Y., Savage, S., et al. A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature 448 (2007), 439–444.
58. 58 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 4 (2013), 29–34.
59. 59 Zhao, Q., Gu, X., Zhang, C., Lu, Q., Chen, H., Xu, L., Blocking M2 muscarinic receptor signaling inhibits tumor growth and reverses epithelial-mesenchymal transition (EMT) in non-small cell lung cancer (NSCLC). Cancer Biol. Ther. 16 (2015), 634–643.
60. 60 Slattery, M.L., Lundgreen, A., Wolff, R.K., MAP kinase genes and colon and rectal cancer. Carcinogenesis 33 (2012), 2398–2408.
61. 61 Chen, X., Wang, S., Wu, N., Yang, C.S., Leukotriene A4 hydrolase as a target for cancer prevention and therapy. Curr. Cancer Drug Targets 4 (2004), 267–283.
62. 62 Visakorpi, T., Hyytinen, E., Koivisto, P., Tanner, M., Keinänen, R., Palmberg, C., Palotie, A., Tammela, T., Isola, J., Kallioniemi, O.P., In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat. Genet. 9 (1995), 401–406.
63. 63 Fujishige, K., Kotera, J., Michibata, H., Yuasa, K., Takebayashi, S., Okumura, K., Omori, K., Cloning and characterization of a novel human phosphodiesterase that hydrolyzes both cAMP and cGMP (PDE10A). J. Biol. Chem. 274 (1999), 18438–18445.
64. 64 Handa, N., Mizohata, E., Kishishita, S., Toyama, M., Morita, S., Uchikubo-Kamo, T., Akasaka, R., Omori, K., Kotera, J., Terada, T., et al. Crystal structure of the GAF-B domain from human phosphodiesterase 10A complexed with its ligand, cAMP. J. Biol. Chem. 283 (2008), 19657–19664.
65. 65 Zhao, J., Cheng, F., Wang, Y., Arteaga, C.L., Zhao, Z., Systematic prioritization of druggable mutations in ∼5000 genomes across 16 cancer types using a structural genomics-based approach. Mol. Cell. Proteomics 15 (2016), 642–656.
66. 66 Kamburov, A., Lawrence, M.S., Polak, P., Leshchiner, I., Lage, K., Golub, T.R., Lander, E.S., Getz, G., Comprehensive assessment of cancer missense mutation clustering in protein structures. Proc. Natl. Acad. Sci. USA 112 (2015), E5486–E5495.
67. 67 Mitternacht, S., Berezovsky, I.N., Binding leverage as a molecular basis for allosteric regulation. PLoS Comput. Biol., 7, 2011, e1002148.
68. 68 Goncearenco, A., Mitternacht, S., Yong, T., Eisenhaber, B., Eisenhaber, F., Berezovsky, I.N., SPACER: Server for predicting allosteric communication and effects of regulation. Nucleic Acids Res., 41, 2013 W266–72.
69. 69 Skora, L., Mestan, J., Fabbro, D., Jahnke, W., Grzesiek, S., NMR reveals the allosteric opening and closing of Abelson tyrosine kinase by ATP-site and myristoyl pocket inhibitors. Proc. Natl. Acad. Sci. USA 110 (2013), E4437–E4445.