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Searching for Essential Genes in the Cancer Genome

  • M. A. PyatnitskiyEmail author
  • D. S. Karpov
  • S. A. Moshkovskii
Article
  • 45 Downloads

Abstract

The concept of essential genes, whose loss of functionality results in cell death, is one of the fundamental concepts of genetics and is important for basic and applied research. This field is particularly promising in oncology, because using the search for genetic vulnerabilities of cancer cells it is possible to identify new potential targets for antitumor therapy. The modern biotechnology capacities are used in large-scale projects for sequencing of somatic mutations in tumors, as well as for direct action on the genetic apparatus of cancer cells. They provided accumulation of a considerable body of knowledge about genetic variants and their phenotypic manifestations in tumors. In the near future this knowledge will find application in clinical practice. This review describes the main experimental and computational approaches to the search for essential genes with special emphasis on application of these methods in molecular oncology.

Keywords:

cancer genome essential genes CRISPR RNA interference synthetic lethals 

Notes

ACKNOWLEDGMENTS

This work is done in the frames of Fundamental Scientific Research Program of the Russian Academy of Sciences for 2013–2020.

COMPLIANCE WITH ETHICAL STANDARDS

Сonflict of interests. The authors declare that they have no conflict of interest.

Other statements. This article does not report any original experimental work involving animals or human participants.

REFERENCES

  1. 1.
    Brenner, S., Genetics, 1974, vol. 77, pp. 71–94.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Goebl, M.G. and Petes, T.D., Cell, 1986, vol. 46, pp. 983–992.CrossRefPubMedGoogle Scholar
  3. 3.
    Kamath, R.S., Fraser, A.G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M., Welchman, D.P., Zipperlen, P., and Ahringer, J., Nature, 2003, vol. 421, pp. 231–237.CrossRefPubMedGoogle Scholar
  4. 4.
    Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J.D., Bussey, H., Chu, A.M., Connelly, C., Davis, K., Dietrich, F., Dow, S.W., El Bakkoury, M., Foury, F., Friend, S.H., Gentalen, E., Giaever, G., Hegemann, J.H., Jones, T., Laub, M., Liao, H., Liebundguth, N., Lockhart, D.J., Lucau-Danila, A., Lussier, M., M’Rabet, N., Menard, P., Mittmann, M., Pai, C., Rebischung, C., Revuelta, J.L., Riles, L., Roberts, C.J., Ross-MacDonald, P., Scherens, B., Snyder, M., Sookhai-Mahadeo, S., Storms, R.K., Veronneau, S., Voet, M., Volckaert, G., Ward, T.R., Wysocki, R., Yen, G.S., Yu, K., Zimmermann, K., Philippsen, P., Johnston, M., and Davis, R.W., Science, 1999, vol. 285, pp. 901–906.CrossRefPubMedGoogle Scholar
  5. 5.
    Rabik, C.A. and Dolan, M.E., Cancer Treat. Rev., 2007, vol. 33, pp. 9–23.CrossRefPubMedGoogle Scholar
  6. 6.
    Pagliarini, R., Shao, W., and Sellers, W.R., EMBO Rep., 2015, vol. 16, pp. 280–296.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Shirasawa, S., Furuse, M., Yokoyama, N., and Sasazuki, T., Science, 1993, vol. 260, pp. 85–88.CrossRefPubMedGoogle Scholar
  8. 8.
    Harborth, J., Elbashir, S.M., Bechert, K., Tuschl, T., and Weber, K., J. Cell Sci., 2001, vol. 114, pp. 4557–4565.PubMedGoogle Scholar
  9. 9.
    Munoz, D.M., Cassiani, P.J., Li, L., Billy, E., Korn, J.M., Jones, M.D., Golji, J., Ruddy, D.A., Yu, K., McAllister, G., DeWeck, A., Abramowski, D., Wan, J., Shirley, M.D., Neshat, S.Y., Rakiec, D., de Beaumont, R., Weber, O., Kauffmann, A., McDonald, E.R., 3rd, Keen, N., Hofmann, F., Sellers, W.R., Schmelzle, T., Stegmeier, F., and Schlabach, M.R., Cancer Discov., 2016, vol. 6, pp. 900–913.CrossRefPubMedGoogle Scholar
  10. 10.
    Aguirre, A.J., Meyers, R.M., Weir, B.A., Vazquez, F., Zhang, C.Z., Ben-David, U., Cook, A., Ha, G., Harrington, W.F., Doshi, M.B., Kost-Alimova, M., Gill, S., Xu, H., Ali, L.D., Jiang, G., Pantel, S., Lee, Y., Goodale, A., Cherniack, A. D., Oh, C., Kryukov, G., Cowley, G.S., Garraway, L.A., Stegmaier, K., Roberts, C.W., Golub, T.R., Meyerson, M., Root, D.E., Tsherniak, A., and Hahn, W.C., Cancer Discov., 2016, vol. 6, pp. 914–929.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Marcotte, R., Brown, K.R., Suarez, F., Sayad, A., Karamboulas, K., Krzyzanowski, P.M., Sircoulomb, F., Medrano, M., Fedyshyn, Y., Koh, J.L.Y., van Dyk, D., Fedyshyn, B., Luhova, M., Brito, G.C., Vizeacoumar, F.J., Vizeacoumar, F.S., Datti, A., Kasimer, D., Buzina, A., Mero, P., Misquitta, C., Normand, J., Haider, M., Ketela, T., Wrana, J.L., Rottapel, R., Neel, B.G., and Moffat, J., Cancer Discov., 2012, vol. 2, pp. 172–189.CrossRefPubMedGoogle Scholar
  12. 12.
    Cowley, G.S., Weir, B.A., Vazquez, F., Tamayo, P., Scott, J.A., Rusin, S., East-Seletsky, A., Ali, L.D., Gerath, W.F., Pantel, S.E., Lizotte, P.H., Jiang, G., Hsiao, J., Tsherniak, A., Dwinell, E., Aoyama, S., Okamoto, M., Harrington, W., Gelfand, E., Green, T.M., Tomko, M.J., Gopal, S., Wong, T.C., Li, H., Howell, S., Stransky, N., Liefeld, T., Jang, D., Bistline, J., Hill Meyers, B., Armstrong, S.A., Anderson, K.C., Stegmaier, K., Reich, M., Pellman, D., Boehm, J.S., Mesirov, J.P., Golub, T.R., Root, D.E., and Hahn, W.C., Sci. Data, 2014, vol. 1, 140035.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Druker, B.J., Blood, 2008, vol. 112, pp. 4808–4817.CrossRefPubMedGoogle Scholar
  14. 14.
    Hynes, N.E. and Lane, H.A., Nat. Rev. Cancer, 2005, vol. 5, pp. 341–354.CrossRefPubMedGoogle Scholar
  15. 15.
    Helming, K.C., Wang, X., Wilson, B.G., Vazquez, F., Haswell, J.R., Manchester, H.E., Kim, Y., Kryukov, G.V., Ghandi, M., Aguirre, A.J., Jagani, Z., Wang, Z., Garraway, L.A., Hahn, W.C., and Roberts, C.W., Nat. Med., 2014, vol. 20, pp. 251–254.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Hsu, T.Y., Simon, L.M., Neill, N.J., Marcotte, R., Sayad, A., Bland, C.S., Echeverria, G.V., Sun, T., Kurley, S.J., Tyagi, S., Karlin, K.L., Dominguez-Vidana, R., Hartman, J.D., Renwick, A., Scorsone, K., Bernardi, R.J., Skinner, S.O., Jain, A., Orellana, M., Lagisetti, C., Golding, I., Jung, S.Y., Neilson, J.R., Zhang, X.H., Cooper, T.A., Webb, T.R., Neel, B.G., Shaw, C.A., and Westbrook, T.F., Nature, 2015, vol. 525, pp. 384–388.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Housden, B.E., Muhar, M., Gemberling, M., Gersbach, C.A., Stainier, D.Y., Seydoux, G., Mohr, S.E., Zuber, J., and Perrimon, N., Nat. Rev. Genet., 2017, vol. 18, pp. 24–40.CrossRefPubMedGoogle Scholar
  18. 18.
    Kittler, R., Putz, G., Pelletier, L., Poser, I., Heninger, A.K., Drechsel, D., Fischer, S., Konstantinova, I., Habermann, B., Grabner, H., Yaspo, M.L., Himmelbauer, H., Korn, B., Neugebauer, K., Pisabarro, M.T., and Buchholz, F., Nature, 2004, vol. 432, pp. 1036−1040.CrossRefPubMedGoogle Scholar
  19. 19.
    Shao, D.D., Tsherniak, A., Gopal, S., Weir, B.A., Tamayo, P., Stransky, N., Schumacher, S.E., Zack, T.I., Beroukhim, R., Garraway, L. A., Margolin, A.A., Root, D.E., Hahn, W.C., and Mesirov, J.P., Genome Res., 2013, vol. 23, pp. 665–678.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Tsherniak, A., Vazquez, F., Montgomery, P.G., Weir, B.A., Kryukov, G., Cowley, G.S., Gill, S., Harrington, W.F., Pantel, S., Krill-Burger, J.M., Meyers, R.M., Ali, L., Goodale, A., Lee, Y., Jiang, G., Hsiao, J., Gerath, W.F.J., Howell, S., Merkel, E., Ghandi, M., Garraway, L.A., Root, D.E., Golub, T.R., Boehm, J.S., and Hahn, W.C., Cell, 2017, vol. 170, pp. 564–576.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Bhinder, B. and Djaballah, H., Comb. Chem. High Throughput Screen, 2013, vol. 16, pp. 665–681.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. and Zhang, F., Science, 2013, vol. 339, pp. 819–823.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., and Charpentier, E., Science, 2012, vol. 337, pp. 816–821.CrossRefPubMedGoogle Scholar
  24. 24.
    Wang, T., Birsoy, K., Hughes, N.W., Krupczak, K.M., Post, Y., Wei, J.J., Lander, E.S., and Sabatini, D.M., Science, 2015, vol. 350, pp. 1096–1101.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Meyers, R.M., Bryan, J.G., McFarland, J.M., Weir, B.A., Sizemore, A.E., Xu, H., Dharia, N.V., Montgomery, P.G., Cowley, G.S., Pantel, S., Goodale, A., Lee, Y., Ali, L.D., Jiang, G., Lubonja, R., Harrington, W. F., Strickland, M., Wu, T., Hawes, D.C., Zhivich, V.A., Wyatt, M.R., Kalani, Z., Chang, J.J., Okamoto, M., Stegmaier, K., Golub, T.R., Boehm, J.S., Vazquez, F., Root, D.E., Hahn, W.C., and Tsherniak, A., Nat. Genet., 2017, vol. 49, pp. 1779–1784.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Shalem, O., Sanjana, N.E., Hartenian, E., Shi, X., Scott, D.A., Mikkelson, T., Heckl, D., Ebert, B.L., Root, D.E., Doench, J.G., and Zhang, F., Science, 2014, vol. 343, pp. 84–87.CrossRefPubMedGoogle Scholar
  27. 27.
    Hart, T., Chandrashekhar, M., Aregger, M., Steinhart, Z., Brown, K.R., MacLeod, G., Mis, M., Zimmermann, M., Fradet-Turcotte, A., Sun, S., Mero, P., Dirks, P., Sidhu, S., Roth, F.P., Rissland, O.S., Durocher, D., Angers, S., and Moffat, J., Cell, 2015, vol. 163, pp. 1515–1526.CrossRefPubMedGoogle Scholar
  28. 28.
    Hart, T., Brown, K.R., Sircoulomb, F., Rottapel, R., and Moffat, J., Mol. Syst. Biol., 2014, vol. 10, 733.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Bertomeu, T., Coulombe-Huntington, J., Chatr-Aryamontri, A., Bourdages, K.G., Coyaud, E., Raught, B., Xia, Y., and Tyers, M., Mol. Cell Biol., 2018, vol. 38, e00302-17.PubMedGoogle Scholar
  30. 30.
    Blomen, V.A., Majek, P., Jae, L.T., Bigenzahn, J.W., Nieuwenhuis, J., Staring, J., Sacco, R., van Diemen, F.R., Olk, N., Stukalov, A., Marceau, C., Janssen, H., Carette, J.E., Bennett, K.L., Colinge, J., Superti-Furga, G., and Brummelkamp, T.R., Science, 2015, vol. 350, pp. 1092–1096.CrossRefPubMedGoogle Scholar
  31. 31.
    Peng, R., Lin, G. and Li, J., FEBS J., 2016, vol. 283, pp. 1218–1231.CrossRefPubMedGoogle Scholar
  32. 32.
    Luo, B., Cheung, H.W., Subramanian, A., Sharifnia, T., Okamoto, M., Yang, X., Hinkle, G., Boehm, J.S., Beroukhim, R., Weir, B.A., Mermel, C., Barbie, D.A., Awad, T., Zhou, X., Nguyen, T., Piqani, B., Li, C., Golub, T.R., Meyerson, M., Hacohen, N., Hahn, W.C., Lander, E.S., Sabatini, D.M., and Root, D.E., Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 20380–20385.CrossRefPubMedGoogle Scholar
  33. 33.
    Evers, B., Jastrzebski, K., Heijmans, J.P., Grernrum, W., Beijersbergen, R.L., and Bernards, R., Nat. Biotechnol., 2016, vol. 34, pp. 631–633.CrossRefPubMedGoogle Scholar
  34. 34.
    Morgens, D.W., Deans, R.M., Li, A., and Bassik, M.C., Nat. Biotechnol., 2016, vol. 34, pp. 634–636.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Bissell, M.J. and Hines, W.C., Nat. Med., 2011, vol. 17, pp. 320–329.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Wilson, A.C., Carlson, S.S., and White, T.J., Ann. Rev. Biochem., 1977, vol. 46, pp. 573–639.CrossRefPubMedGoogle Scholar
  37. 37.
    Nei, M. and Gojobori, T., Mol. Biol. Evol., 1986, vol. 3, pp. 418–426.PubMedGoogle Scholar
  38. 38.
    Ostrow, S.L., Barshir, R., DeGregori, J., Yeger-Lotem, E., and Hershberg, R., PLoS Genet., 2014, vol. 10, e1004239.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Ovens, K. and Naugler, C., Theor. Biol. Med. Model., 2012, vol. 9, 44.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Pyatnitskiy, M., Karpov, D., Poverennaya, E., Lisitsa, A., and Moshkovskii, S., PLoS One, 2015, vol. 10, e0142819.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Martincorena, I., Raine, K. M., Gerstung, M., Dawson, K.J., Haase, K., Van Loo, P., Davies, H., Stratton, M.R., and Campbell, P.J., Cell, 2017, vol. 171, pp. 1029–1041.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Van den Eynden, J. and Larsson E., Front Genet., 2017, vol. 8, 74.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Alexandrov, L.B., Nik-Zainal, S., Wedge, D.C., Aparicio, S.A., Behjati, S., Biankin, A.V., Bignell, G.R., Bolli, N., Borg, A., Borresen-Dale, A.L., Boyault, S., Burkhardt, B., Butler, A.P., Caldas, C., Davies, H.R., Desmedt, C., Eils, R., Eyfjord, J.E., Foekens, J.A., Greaves, M., Hosoda, F., Hutter, B., Ilicic, T., Imbeaud, S., Imielinski, M., Jager, N., Jones, D.T., Jones, D., Knappskog, S., Kool, M., Lakhani, S.R., Lopez-Otin, C., Martin, S., Munshi, N.C., Nakamura, H., Northcott, P.A., Pajic, M., Papaemmanuil, E., Paradiso, A., Pearson, J. V., Puente, X.S., Raine, K., Ramakrishna, M., Richardson, A.L., Richter, J., Rosenstiel, P., Schlesner, M., Schuma-cher, T.N., Span, P.N., Teague, J.W., Totoki, Y., Tutt, A.N., Valdes-Mas, R., van Buuren, M.M., van’t Veer, L., Vincent-Salomon, A., Waddell, N., Yates, L.R., Zucman-Rossi, J., Futreal, P.A., McDermott, U., Lichter, P., Meyerson, M., Grimmond, S.M., Siebert, R., Campo, E., Shibata, T., Pfister, S.M., Campbell, P.J., and Stratton, M.R., Nature, 2013, vol. 500, pp. 415–421.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Alexandrov, L.B. and Stratton, M.R., Curr. Opin. Genet. Dev., 2014, vol. 24, pp. 52–60.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Weghorn, D. and Sunyaev, S., Nat. Genet., 2017, vol. 49, pp. 1785–1788.CrossRefPubMedGoogle Scholar
  46. 46.
    Van den Eynden, J., Basu, S., and Larsson, E., PLoS Genet., 2016, vol. 12, e1006506.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Jeong, H., Mason, S.P., Barabasi, A.L., and Oltvai, Z.N., Nature, 2001, vol. 411, pp. 41–42.CrossRefPubMedGoogle Scholar
  48. 48.
    Yu, H.Y., Greenbaum, D., Lu, H.X., Zhu, X.W., and Gerstein, M., Trends Genet., 2004, vol. 20, pp. 227–231.CrossRefPubMedGoogle Scholar
  49. 49.
    del Rio, G., Koschutzki, D., and Coello, G., BMC Syst. Biol., 2009, vol. 3, 102.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Luo, J. and Qi, Y., PLoS One, 2015, vol. 10, e0131418.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Qin, C., Sun, Y., and Dong, Y., PLoS One, 2016, vol. 11, e0161042.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    da Silva, J.P.M., Acencio, M.L., Mornbach, J.C.M., Vieira, R., da Silva, J.C., Lemke, N., and Sinigagliac, M., Physica A, 2008, vol. 387, pp. 1049–1055.CrossRefGoogle Scholar
  53. 53.
    Liu, Y.Y., Slotine, J.J., and Barabasi, A.L., Nature, 2011, vol. 473, pp. 167–173.CrossRefPubMedGoogle Scholar
  54. 54.
    Wu, L., Li, M., Wang, J., and Wu, F.X., Bioinformatics, 2018, vol. 34, pp. 1428–1430.CrossRefPubMedGoogle Scholar
  55. 55.
    Wuchty, S., Proc. Natl. Acad. Sci. USA, 2014, vol. 111, pp. 7156–7160.CrossRefPubMedGoogle Scholar
  56. 56.
    Khuri, S. and Wuchty, S., BMC Bioinformatics, 2015, vol. 16, 109.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kanhaiya, K., Czeizler, E., Gratie, C., and Petre, I., Sci. Rep., 2017, vol. 7, 10327.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Edwards, J.S. and Palsson, B.O., Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 5528–5533.CrossRefPubMedGoogle Scholar
  59. 59.
    Heavner, B.D., Smallbone, K., Price, N.D., and Walker, L.P., Database (Oxford), 2013, vol. 2013, bat059.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Karr, J.R., Sanghvi, J.C., Macklin, D.N., Gutschow, M.V., Jacobs, J.M., Bolival, B., Jr., Assad-Garcia, N., Glass, J.I., and Covert, M.W., Cell, 2012, vol. 150, pp. 389–401.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Maximchik, P.V., Kulikov, A.V., Zhivotovsky, B.D., and Gogvadze, V.G., Biochemistry (Moscow), 2016, vol. 81, pp. 65–79.PubMedGoogle Scholar
  62. 62.
    Hanahan, D. and Weinberg, R.A., Cell, 2011, vol. 144, pp. 646–674.CrossRefPubMedGoogle Scholar
  63. 63.
    Nilsson, A. and Nielsen, J., Metab. Eng., 2017, vol. 43, pp. 103–112.CrossRefPubMedGoogle Scholar
  64. 64.
    Duarte, N.C., Becker, S.A., Jamshidi, N., Thiele, I., Mo, M.L., Vo, T.D., Srivas, R., and Palsson, B.O., Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 1777–1782.CrossRefPubMedGoogle Scholar
  65. 65.
    Swainston, N., Smallbone, K., Hefzi, H., Dobson, P.D., Brewer, J., Hanscho, M., Zielinski, D.C., Ang, K.S., Gardiner, N.J., Gutierrez, J.M., Kyriakopoulos, S., Lakshmanan, M., Li, S., Liu, J.K., Martinez, V.S., Orellana, C.A., Quek, L.E., Thomas, A., Zanghellini, J., Borth, N., Lee, D.Y., Nielsen, L.K., Kell, D.B., Lewis, N.E., and Mendes, P., Metabolomics, 2016, vol. 12, 109.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Jerby, L., Shlomi, T., and Ruppin, E., Mol. Syst. Biol., 2010, vol. 6, 401.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Wang, Y., Eddy, J.A., and Price, N.D., BMC Syst. Biol., 2012, vol. 6, 153.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Agren, R., Bordel, S., Mardinoglu, A., Pornputtapong, N., Nookaew, I., and Nielsen, J., PLoS Comput. Biol., 2012, vol. 8, e1002518.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Agren, R., Mardinoglu, A., Asplund, A., Kampf, C., Uhlen, M., and Nielsen, J., Mol. Syst. Biol., 2014, vol. 10, 721.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Orth, J.D., Thiele, I., and Palsson B.O., Nat. Biotechnol., 2010, vol. 28, pp. 245–248.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Gatto, F., Miess, H., Schulze, A., and Nielsen, J., Sci. Rep., 2015, vol. 5, 10738.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Cairns, R.A., Harris, I.S., and Mak, T.W., Nat. Rev. Cancer, 2011, vol. 11, pp. 85–95.CrossRefPubMedGoogle Scholar
  73. 73.
    Becker, S.A. and Palsson, B.O., BMC Syst. Biol., 2008, vol. 2, 14.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Opdam, S., Richelle, A., Kellman, B., Li, S., Zielinski, D.C., and Lewis, N.E., Cell Syst., 2017, vol. 4, pp. 318–329.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Ghaffari, P., Mardinoglu, A., Asplund, A., Shoaie, S., Kampf, C., Uhlen, M., and Nielsen, J., Sci. Rep., 2015, vol. 5, 8183.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Gonen, M., Weir, B.A., Cowley, G.S., Vazquez, F., Guan, Y., Jaiswal, A., Karasuyama, M., Uzunangelov, V., Wang, T., Tsherniak, A., Howell, S., Marbach, D., Hoff, B., Norman, T.C., Airola, A., Bivol, A., Bunte, K., Carlin, D., Chopra, S., Deran, A., Ellrott, K., Gopalacharyulu, P., Graim, K., Kaski, S., Khan, S.A., Newton, Y., Ng, S., Pahikkala, T., Paull, E., Sokolov, A., Tang, H., Tang, J., Wennerberg, K., Xie, Y., Zhan, X., Zhu, F., Aittokallio, T., Mamitsuka, H., Stuart, J. M., Boehm, J.S., Root, D.E., Xiao, G., Stolovitzky, G., Hahn, W.C., and Margolin, A.A., Cell Syst., 2017, vol. 5, pp. 485–497.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Dobzhansky, T., Genetics, 1946, vol. 31, pp. 269–290.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Costanzo, M., VanderSluis, B., Koch, E.N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S.D., Pelechano, V., Styles, E.B., Billmann, M., van Leeuwen, J., van Dyk, N., Lin, Z.Y., Kuzmin, E., Nelson, J., Piotrowski, J. S., Srikumar, T., Bahr, S., Chen, Y., Deshpande, R., Kurat, C.F., Li, S.C., Li, Z., Usaj, M.M., Okada, H., Pascoe, N., San Luis, B.J., Sharifpoor, S., Shuteriqi, E., Simpkins, S.W., Snider, J., Suresh, H.G., Tan, Y., Zhu, H., Malod-Dognin, N., Janjic, V., Przulj, N., Troyanskaya, O.G., Stagljar, I., Xia, T., Ohya, Y., Gingras, A.C., Raught, B., Boutros, M., Steinmetz, L.M., Moore, C.L., Rosebrock, A.P., Caudy, A.A., Myers, C.L., Andrews, B., and Boone, C., Science, 2016, vol. 353, no. 6306, aaf1420.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Haber, J.E., Braberg, H., Wu, Q., Alexander, R., Haase, J., Ryan, C., Lipkin-Moore, Z., Franks-Skiba, K.E., Johnson, T., Shales, M., Lenstra, T.L., Holstege, F.C., Johnson, J.R., Bloom, K., and Krogan, N.J., Cell Rep., 2013, vol. 3, pp. 2168–2178.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Hartwell, L.H., Szankasi, P., Roberts, C.J., Murray, A.W., and Friend, S.H., Science, 1997, vol. 278, pp. 1064−1068.CrossRefPubMedGoogle Scholar
  81. 81.
    Dhanjal, J.K., Radhakrishnan, N., and Sundar, D., Methods, 2017, vol. 131, pp. 66–73.CrossRefPubMedGoogle Scholar
  82. 82.
    Thompson, J.M., Nguyen, Q.H., Singh, M., and Razorenova, O.V., Yale J. Biol. Med., 2015, vol. 88, pp. 145–155.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Jerby-Arnon, L., Pfetzer, N., Waldman, Y.Y., McGarry, L., James, D., Shanks, E., Seashore-Ludlow, B., Weinstock, A., Geiger, T., Clemons, P.A., Gottlieb, E., and Ruppin, E., Cell, 2014, vol. 158, pp. 1199–1209.CrossRefPubMedGoogle Scholar
  84. 84.
    Sinha, S., Thomas, D., Chan, S., Gao, Y., Brunen, D., Torabi, D., Reinisch, A., Hernandez, D., Chan, A., Rankin, E.B., Bernards, R., Majeti, R., and Dill, D.L., Nat. Commun., 2017, vol. 8, 15580.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Jacunski, A., Dixon, S.J., and Tatonetti N.P., PLoS Comput. Biol., 2015, vol. 11, e1004506.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Duffy, S., Fam, H.K., Wang, Y.K., Styles, E.B., Kim, J.H., Ang, J.S., Singh, T., Larionov, V., Shah, S.P., Andrews, B., Boerkoel, C.F., and Hieter P., Proc. Natl. Acad. Sci. USA, 2016, vol. 113, pp. 9967–9976.CrossRefPubMedGoogle Scholar
  87. 87.
    Reid, R.J., Du, X., Sunjevaric, I., Rayannavar, V., Dittmar, J., Bryant, E., Maurer, M., and Rothstein, R., Genetics, 2016, vol. 204, pp. 807–819.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Megchelenbrink, W., Katzir, R., Lu, X., Ruppin, E., and Notebaart, R.A., Proc. Natl. Acad. Sci. USA, 2015, vol. 112, pp. 12217–12222.CrossRefPubMedGoogle Scholar
  89. 89.
    Aksoy, B.A., Demir, E., Babur, O., Wang, W., Jing, X., Schultz, N., and Sander, C., Bioinformatics, 2014, vol. 30, pp. 2051−2059.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    O’Neil, N.J., Bailey, M. L., and Hieter, P., Nat. Rev. Genet., 2017, vol. 18, pp. 613–623.CrossRefPubMedGoogle Scholar
  91. 91.
    Bouwman, P. and Jonkers, J., Clin. Cancer Res., 2014, vol. 20, pp. 540–547.CrossRefPubMedGoogle Scholar
  92. 92.
    Scholl, C., Frohling, S., Dunn, I.F., Schinzel, A.C., Barbie, D.A., Kim, S.Y., Silver, S.J., Tamayo, P., Wadlow, R.C., Ramaswamy, S., Dohner, K., Bullinger, L., Sandy, P., Boehm, J.S., Root, D.E., Jacks, T., Hahn, W.C., and Gilliland, D.G., Cell, 2009, vol. 137, pp. 821–834.CrossRefPubMedGoogle Scholar
  93. 93.
    Babij, C., Zhang, Y., Kurzeja, R.J., Munzli, A., Shehabeldin, A., Fernando, M., Quon, K., Kassner, P.D., Ruefli-Brasse, A.A., Watson, V.J., Fajardo, F., Jackson, A., Zondlo, J., Sun, Y., Ellison, A.R., Plewa, C.A., San, M.T., Robinson, J., McCarter, J., Schwandner, R., Judd, T., Carnahan, J., and Dussault, I., Cancer Res., 2011, vol. 71, pp. 5818–5826.CrossRefPubMedGoogle Scholar
  94. 94.
    Jaiswal, A., Peddinti, G., Akimov, Y., Wennerberg, K., Kuznetsov, S., Tang, J., and Aittokallio, T., Genome Med., 2017, vol. 9, 51.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Zhang, F. and Lupski, J.R., Hum. Mol. Genet., 2015, vol. 24, pp. R102–R110.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Kircher, M., Witten, D.M., Jain, P., O’Roak, B.J., Cooper, G.M., and Shendure, J., Nat. Genet., 2014, vol. 46, pp. 310–315.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Zhou, J. and Troyanskaya, O.G., Nat. Methods, 2015, vol. 12, pp. 931–934.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Ionita-Laza, I., McCallum, K., Xu, B., and Buxbaum, J.D., Nat. Genet., 2016, vol. 48, pp. 214–220.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    ENCODE Project Consortium, Nature, 2012, vol. 489, pp. 57−74.Google Scholar
  100. 100.
    Hu, X., Sood, A.K., Dang, C.V., and Zhang, L., Curr. Opin. Genet. Dev., 2018, vol. 48, pp. 8–15.CrossRefPubMedGoogle Scholar
  101. 101.
    Notzold, L., Frank, L., Gandhi, M., Polycarpou-Schwarz, M., Gross, M., Gunkel, M., Beil, N., Erfle, H., Harder, N., Rohr, K., Trendel, J., Krijgsveld, J., Longerich, T., Schirmacher, P., Boutros, M., Erhardt, S., and Diederichs, S., Sci. Rep., 2017, vol. 7, 2265.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Zhao, J., Liu, Y., Zhang, W., Zhou, Z., Wu, J., Cui, P., Zhang, Y., and Huang, G., Cell Cycle, 2015, vol. 14, pp. 3112–3123.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Wu, Y., Tan, C., Weng, W.W., Deng, Y., Zhang, Q.Y., Yang, X.Q., Gan, H.L., Wang, T., Zhang, P.P., Xu, M.D., Wang, Y.Q., and Wang, C.F., Am. J. Cancer Res., 2016, vol. 6, pp. 285–299.PubMedPubMedCentralGoogle Scholar
  104. 104.
    Zhu, S., Li, W., Liu, J., Chen, C.H., Liao, Q., Xu, P., Xu, H., Xiao, T., Cao, Z., Peng, J., Yuan, P., Brown, M., Liu, X.S., and Wei, W., Nat. Biotechnol., 2016, vol. 34, pp. 1279–1286.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • M. A. Pyatnitskiy
    • 1
    • 2
    Email author
  • D. S. Karpov
    • 1
    • 3
  • S. A. Moshkovskii
    • 1
    • 4
  1. 1.Institute of Biomedical ChemistryMoscowRussia
  2. 2.Higher School of EconomicsMoscowRussia
  3. 3.Engelhardt Institute of Molecular Biology, Russian Academy of SciencesMoscowRussia
  4. 4.Pirogov Russian National Research Medical UniversityMoscowRussia

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