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Biochemistry (Moscow)

, Volume 82, Issue 4, pp 413–425 | Cite as

Natural and chemotherapy-induced clonal evolution of tumors

  • M. K. Ibragimova
  • M. M. Tsyganov
  • N. V. LitviakovEmail author
Review

Abstract

Evolution and natural selection of tumoral clones in the process of transformation and the following carcinogenesis can be called natural clonal evolution. Its main driving factors are internal: genetic instability initiated by driver mutations and microenvironment, which enables selective pressure while forming the environment for cell transformation and their survival. We present our overview of contemporary research dealing with mechanisms of carcinogenesis in different localizations from precancerous pathologies to metastasis and relapse. It shows that natural clonal evolution establishes intratumoral heterogeneity and enables tumor progression. Tumors of monoclonal origin are of low-level intratumoral heterogeneity in the initial stages, and this increases with the size of the tumor. Tumors of polyclonal origin are of extremely high-level intratumoral heterogeneity in the initial stages and become more homogeneous when larger due to clonal expansion. In cases of chemotherapy-induced clonal evolution of a tumor, chemotherapy becomes the leading factor in treatment. The latest research shows that the impact of chemotherapy can radically increase the speed of clonal evolution and lead to new malignant and resistant clones that cause tumor metastasis. Another option of chemotherapy-induced clonal evolution is formation of a new dominant clone from a clone that was minor in the initial tumor and obtained free space due to elimination of sensitive clones by chemotherapy. As a result, in ~20% of cases, chemotherapy can stimulate metastasis and relapse of tumors due to clonal evolution. The conclusion of the overview formulates approaches to tumor treatment based on clonal evolution: in particular, precision therapy, prediction of metastasis stimulation in patients treated with chemotherapy, methods of genetic evaluation of chemotherapy efficiency and clonal-oriented treatment, and approaches to manipulating the clonal evolution of tumors are presented.

Keywords

clonal evolution tumor chemotherapy mutation metastasis 

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References

  1. 1.
    Nowell, P. C. (1976) The clonal evolution of tumor cell populations, Science, 194, 23–28.CrossRefPubMedGoogle Scholar
  2. 2.
    Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., Varela, I., Phillimore, B., Begum, S., McDonald, N. Q., Butler, A., Jones, D., Raine, K., Latimer, C., Santos, C. R., Nohadani, M., Eklund, A. C., Spencer-Dene, B., Clark, G., Pickering, L., Stamp, G., Gore, M., Szallasi, Z., Downward, J., Futreal, P. A., and Swanton, C. (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing, New Eng. J. Med., 366, 883–892.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Krakhmal, N. V., Zavyalova, M. V., Denisov, E. V., Vtorushin, S. V., and Perelmuter, V. M. (2015) Cancer invasion: patterns and mechanisms, Acta Naturae, 72, 17–28.Google Scholar
  4. 4.
    Gerashchenko, T. S., Denisov, E. V., Litviakov, N. V., Zavyalova, M. V., Vtorushin, S. V., Tsyganov, M. M., Perelmuter, V. M., and Cherdyntseva, N. V. (2013) Intratumor heterogeneity: nature and biological significance, Biochemistry (Moscow), 78, 1201–1215.CrossRefGoogle Scholar
  5. 5.
    Bhatia, S., Frangioni, J. V., Hoffman, R. M., Iafrate, A. J., and Polyak, K. (2012) The challenges posed by cancer heterogeneity, Nat. Biotechnol., 30, 604–610.CrossRefPubMedGoogle Scholar
  6. 6.
    Visvader, J. E. (2011) Cells of origin in cancer, Nature, 469, 314–322.CrossRefPubMedGoogle Scholar
  7. 7.
    Marusyk, A., and Polyak, K. (2010) Tumor heterogeneity: causes and consequences, Biochim. Biophys. Acta, 1805, 105–117.PubMedGoogle Scholar
  8. 8.
    Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation, Cell, 144, 646–674.CrossRefPubMedGoogle Scholar
  9. 9.
    Zavyalova, M. V., Perelmuter, V. M., Vtorushin, S. V., Denisov, E. V., Litvyakov, N. V., Slonimskaya, E. M., and Cherdyntseva, N. V. (2013) The presence of alveolar structures in invasive ductal NOS breast carcinoma is associated with lymph node metastasis, Diagn. Cytopathol., 41, 279282.CrossRefGoogle Scholar
  10. 10.
    Van Niekerk, G., Davids, L. M., Hattingh, S. M., and Engelbrecht, A. M. (2016) Cancer stem cells: a product of clonal evolution? Int. J. Cancer, 140, 993–999.CrossRefPubMedGoogle Scholar
  11. 11.
    Devarakonda, S., and Govindan, R. (2015) Clonal evolution: multiregion sequencing of esophageal adenocarcinoma before and after chemotherapy, Cancer Discov., 5, 796798.CrossRefGoogle Scholar
  12. 12.
    Fisher, R., Pusztai, L., and Swanton, C. (2013) Cancer heterogeneity: implications for targeted therapeutics, Br. J. Cancer, 108, 479–485.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Cross, W., Graham, T. A., and Wright, N. A. (2016) New paradigms in clonal evolution: punctuated equilibrium in cancer, J. Pathol., 240, 126–136.CrossRefPubMedGoogle Scholar
  14. 14.
    Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., Ramakrishna, M., Shlien, A., Cooke, S. L., Hinton, J., Menzies, A., Stebbings, L. A., Leroy, C., Jia, M., Rance, R., Mudie, L. J., Gamble, S. J., Stephens, P. J., McLaren, S., Tarpey, P. S., Papaemmanuil, E., Davies, H. R., Varela, I., McBride, D. J., Bignell, G. R., Leung, K., Butler, A. P., Teague, J. W., Martin, S., Jonsson, G., Mariani, O., Boyault, S., Miron, P., Fatima, A., Langerod, A., Aparicio, S. A., Tutt, A., Sieuwerts, A. M., Borg, A., Thomas, G., Salomon, A. V., Richardson, A. L., BorresenDale, A. L., Futreal, P. A., Stratton, M. R., and Campbell, P. J.; Breast Cancer Working Group of the International Cancer Genome Consortium (2012) The life history of 21 breast cancers, Cell, 149, 994–1007.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Navin, N., Krasnitz, A., Rodgers, L., Cook, K., Meth, J., Kendall, J., Riggs, M., Eberling, Y., Troge, J., Grubor, V., Levy, D., Lundin, P., Maner, S., Zetterberg, A., Hicks, J., and Wigler, M. (2010) Inferring tumor progression from genomic heterogeneity, Genome Res., 20, 68–80.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Ng, C. K., Pemberton, H. N., and Reis-Filho, J. S. (2014) Breast cancer intratumor genetic heterogeneity: causes and implications, Exp. Rev. Anticancer Ther., 12, 1021–1032.CrossRefGoogle Scholar
  17. 17.
    Stephens, P. J., Tarpey, P. S., Davies, H., Van, Loo P., Greenman, C., Wedge, D. C., Nik-Zainal, S., Martin, S., Varela, I., Bignell, G. R., Yates, L. R., Papaemmanuil, E., Beare, D., Butler, A., Cheverton, A., Gamble, J., Hinton, J., Jia, M., Jayakumar, A., Jones, D., Latimer, C., Lau, K. W., McLaren, S., McBride, D. J., Menzies, A., Mudie, L., Raine, K., Rad, R., Chapman, M. S., Teague, J., Easton, D., Langerod, A., Lee, M. T., Shen, C. Y., Tee, B. T., Huimin, B. W., Broeks, A., Vargas, A. C., Turashvili, G., Martens, J., Fatima, A., Miron, P., Chin, S. F., Thomas, G., Boyault, S., Mariani, O., Lakhani, S. R., Van de Vijver, M., Van’t Veer, L., Foekens, J., Desmedt, C., Sotiriou, C., Tutt, A., Caldas, C., Reis-Filho, J. S., Aparicio, S. A., Salomon, A. V., Borresen-Dale, A. L., Richardson, A. L., Campbell, P. J., Futreal, P. A., Stratton, M. R., and Oslo Breast Cancer Consortium (OSBREAC) (2012) The landscape of cancer genes and mutational processes in breast cancer, Nature, 486, 400–404.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Alexandrov, L. B., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., 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., Imielinsk, M., Jager, N., Jones, D. T. W., 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., Schumacher, T. N., Span, P. N., Teague, J. W., Totoki, Y., Tutt, A. N. J., Valdes-Mas, R., van Buuren, M. M., Van’t Veer, L., Vincent-Salomon, A., Waddell, N., Yates, L. R., Australian Pancreatic Cancer Genome Initiative, ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, ICGC PedBrain, 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. (2013) Signatures of mutational processes in human cancer, Nature, 500, 415–421.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Bhatia, S., Frangioni, J. V., Hoffman, R. M., Iafrate, A. J., and Polyak, K. (2012) The challenges posed by cancer heterogeneity, Nat. Biotechnol., 30, 604–610.CrossRefPubMedGoogle Scholar
  20. 20.
    Greaves, M., and Maley, C. C. (2012) Clonal evolution in cancer, Nature, 481, 306–313.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    McGranahan, N., and Swanton, C. (2015) Biological and therapeutic impact of intratumor heterogeneity in cancer evolution, Cancer Cell, 27, 15–26.CrossRefPubMedGoogle Scholar
  22. 22.
    Michor, F., and Polyak, K. (2010) The origins and implications of intratumor heterogeneity, Cancer Prevent. Res., 3, 1361–1364.CrossRefGoogle Scholar
  23. 23.
    Greaves, M., and Ford, A. M. (2015) Chromosome translocations, cancer initiation and clonal evolution, in Chromosomal Translocations and Genome Rearrangements in Cancer (Rowley, J. D., Le Beau, M. M., and Rabbitts, T. H., eds.), Springer, pp. 53–72.CrossRefGoogle Scholar
  24. 24.
    Giancotti, F. G. (2013) Mechanisms governing metastatic dormancy and reactivation, Cell, 155, 750–764.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Apostoli, A. J., and Ailles, L. (2016) Clonal evolution and tumor-initiating cells: new dimensions in cancer patient treatment, Crit. Rev. Clin. Lab. Sci., 53, 40–51.CrossRefPubMedGoogle Scholar
  26. 26.
    Almendro, V., Marusyk, A., and Polyak, K. (2013) Cellular heterogeneity and molecular evolution in cancer, Annu. Rev. Pathol. Mech. Dis., 8, 277–302.CrossRefGoogle Scholar
  27. 27.
    Almendro, V., Kim, H. J., Cheng, Y.-K., Gonen, M., Itzkovitz, S., Argani, P., Van Oudenaarden, A., Sukumar, S., Michor, F., and Polyak, K. (2014) Genetic and phenotypic diversity in breast tumor metastases, Cancer Res., 74, 1338–1348.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Polyak, K. (2014) Tumor heterogeneity confounds and illuminates: a case for Darwinian tumor evolution, Nat. Med., 20, 344–346.CrossRefPubMedGoogle Scholar
  29. 29.
    Cho, S. Y., Xu, M., Roboz, J., Lu, M., Mascarenhas, J., and Hoffman, R. (2010) The effect of CXCL12 processing on CD34+ cell migration in myeloproliferative neoplasms, Cancer Res., 70, 3402–3410.CrossRefPubMedGoogle Scholar
  30. 30.
    Verstovsek, S., Kantarjian, H., Mesa, R. A., Pardanani, A. D., Cortes-Franco, J., Thomas, D. A., Estrov, Z., Fridman, J. S., Bradley, E. C., Erickson-Viitanen, S., Vaddi, K., Levy, R., and Tefferi, A. (2010) Safety and efficacy of INCB018424, a JAK1 and JAK2 inhibitor, in myelofibrosis, New Eng. J. Med., 363, 1117–1127.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Tefferi, A., Thiele, J., Vannucchi, A., and Barbui, T. (2014) An overview on CALR and CSF3R mutations and a proposal for revision of WHO diagnostic criteria for myeloproliferative neoplasms, Leukemia, 28, 1407–1413.CrossRefPubMedGoogle Scholar
  32. 32.
    Tefferi, A., Vaidya, R., Caramazza, D., Finke, C., Lasho, T., and Pardanani, A. (2011) Circulating interleukin (IL)-8, IL-2R, IL-12, and IL-15 levels are independently prognostic in primary myelofibrosis: a comprehensive cytokine profiling study, J. Clin. Oncol., 29, 1356–1363.CrossRefPubMedGoogle Scholar
  33. 33.
    Thomas, L. K., Bermejo, J. L., Vinokurova, S., Jensen, K., Bierkens, M., Steenbergen, R., Bergmann, M., von Knebel Doeberitz, M., and Reuschenbach, M. (2014) Chromosomal gains and losses in human papillomavirusassociated neoplasia of the lower genital tract–a systematic review and meta-analysis, Eur. J. Cancer, 50, 85–98.CrossRefPubMedGoogle Scholar
  34. 34.
    Luhn, P., Houldsworth, J., Cahill, L., Schiffman, M., Castle, P. E., Zuna, R. E., Dunn, S. T., Gold, M. A., Walker, J., and Wentzensen, N. (2013) Chromosomal gains measured in cytology samples from women with abnormal cervical cancer screening results, Gynecol. Oncol., 130, 595600.CrossRefGoogle Scholar
  35. 35.
    Murphy, B. J., Dorudi, S., and Bustin, S. A. (2007) Molecular staging of colorectal cancer: new paradigm or waste of time? Exp. Opin. Med. Diagn., 1, 31–45.CrossRefGoogle Scholar
  36. 36.
    Sowalsky, A. G., Ye, H., Bubley, G. J., and Balk, S. P. (2013) Clonal progression of prostate cancers from Gleason grade 3 to grade 4, Cancer Res., 73, 1050–1055.CrossRefPubMedGoogle Scholar
  37. 37.
    Campbell, P. J., Yachida, S., Mudie, L. J., Stephens, P. J., Pleasance, E. D., Stebbings, L. A., Morsberger, L. A., Latimer, C., McLaren, S., and Lin, M.-L. (2010) The patterns and dynamics of genomic instability in metastatic pancreatic cancer, Nature, 467, 1109–1113.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Makohon-Moore, A. P., Zhang, M., Reiter, J. G., Bozic, I., Wong, F., Jiao, Y., Chatterjee, K., Nowak, M., Papadopoulos, N., and Vogelstein, B. (2015) Clonal evolution defines the natural history of metastatic pancreatic cancer, Cancer Res., 75, 4137–4137.CrossRefGoogle Scholar
  39. 39.
    Li, X., Galipeau, P. C., Paulson, T. G., Sanchez, C. A., Arnaudo, J., Liu, K., Sather, C. L., Kostadinov, R. L., Odze, R. D., and Kuhner, M. K. (2014) Temporal and spatial evolution of somatic chromosomal alterations: a casecohort study of Barrett’s esophagus, Cancer Prevent. Res., 7, 114–127.CrossRefGoogle Scholar
  40. 40.
    Aparicio, S., and Caldas, C. (2013) The implications of clonal genome evolution for cancer medicine, New Eng. J. Med., 368, 842–851.CrossRefPubMedGoogle Scholar
  41. 41.
    Shah, S. P., Roth, A., Goya, R., Oloumi, A., Ha, G., Zhao, Y., Turashvili, G., Ding, J., Tse, K., and Haffari, G. (2012) The clonal and mutational evolution spectrum of primary triple-negative breast cancers, Nature, 486, 395–399.PubMedGoogle Scholar
  42. 42.
    Wang, Y., Waters, J., Leung, M. L., Unruh, A., Roh, W., Shi, X., Chen, K., Scheet, P., Vattathil, S., and Liang, H. (2014) Clonal evolution in breast cancer revealed by single nucleus genome sequencing, Nature, 512, 155–160.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Zavyalova, M. V., Denisov, E. V., Tashireva, L. A., Gerashchenko, T. S., Litviakov, N. V., Skryabin, N. A., Vtorushin, S. V., Telegina, N. S., Slonimskaya, E. M., and Cherdyntseva, N. V. (2013) Phenotypic drift as a cause for intratumoral morphological heterogeneity of invasive ductal breast carcinoma not otherwise specified, Bio Res. Open Access, 2, 148–154.CrossRefGoogle Scholar
  44. 44.
    Denisov, E. V., Litviakov, N. V., Zavyalova, M. V., Perelmuter, V. M., Vtorushin, S. V., Tsyganov, M. M., Gerashchenko, T. S., Garbukov, E. Y., Slonimskaya, E. M., and Cherdyntseva, N. V. (2014) Intratumoral morphological heterogeneity of breast cancer: neoadjuvant chemotherapy efficiency and multidrug resistance gene expression, Sci. Rep., 4, 1–7.CrossRefGoogle Scholar
  45. 45.
    Eirew, P., Steif, A., Khattra, J., Ha, G., Yap, D., Farahani, H., Gelmon, K., Chia, S., Mar, C., and Wan, A. (2015) Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution, Nature, 518, 422426.Google Scholar
  46. 46.
    Janiszewska, M., and Polyak, K. (2015) Clonal evolution in cancer: a tale of twisted twines, Cell Stem Cell, 16, 11–12.CrossRefPubMedGoogle Scholar
  47. 47.
    Marusyk, A., Almendro, V., and Polyak, K. (2012) Intratumour heterogeneity: a looking glass for cancer? Nat. Rev. Cancer, 12, 323–334.CrossRefPubMedGoogle Scholar
  48. 48.
    Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., and Ramakrishna, M. (2012) The life history of 21 breast cancers, Cell, 149, 994–1007.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Kreso, A., and Dick, J. E. (2014) Evolution of the cancer stem cell model, Cell Stem Cell, 14, 275–291.CrossRefPubMedGoogle Scholar
  50. 50.
    Ding, L., Ley, T. J., Larson, D. E., Miller, C. A., Koboldt, D. C., Welch, J. S., Ritchey, J. K., Young, M. A., Lamprecht, T., and McLellan, M. D. (2012) Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing, Nature, 481, 506–510.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Keats, J. J., Chesi, M., Egan, J. B., Garbitt, V. M., Palmer, S. E., Braggio, E., Van Wier, S., Blackburn, P. R., Baker, A. S., and Dispenzieri, A. (2012) Clonal competition with alternating dominance in multiple myeloma, Blood, 120, 1067–1076.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Jiang, Y., Redmond, D., Nie, K., Eng, K. W., Clozel, T., Martin, P., Tan, L. H., Melnick, A. M., Tam, W., and Elemento, O. (2014) Deep sequencing reveals clonal evolution patterns and mutation events associated with relapse in B-cell lymphomas, Gen. Biol., 15, 412–420.CrossRefGoogle Scholar
  53. 53.
    Oshima, K., Khiabanian, H., Da Silva-Almeida, A. C., Tzoneva, G., Abate, F., Ambesi-Impiombato, A., SanchezMartin, M., Carpenter, Z., Penson, A., and Perez-Garcia, A. (2016) Mutational landscape, clonal evolution patterns, and role of RAS mutations in relapsed acute lymphoblastic leukemia, PNAS, 201608420.Google Scholar
  54. 54.
    Malcikova, J., Stano-Kozubik, K., Tichy, B., Kantorova, B., Pavlova, S., Tom, N., Radova, L., Smardova, J., Pardy, F., and Doubek, M. (2015) Detailed analysis of therapydriven clonal evolution of TP53 mutations in chronic lymphocytic leukemia, Leukemia, 29, 877–885.CrossRefPubMedGoogle Scholar
  55. 55.
    Johnson, B. E., Mazor, T., Hong, C., Barnes, M., Aihara, K., McLean, C. Y., Fouse, S. D., Yamamoto, S., and Ueda, H. (2014) Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma, Science, 343, 189193.Google Scholar
  56. 56.
    Wu, X., Northcott, P. A., Dubuc, A., Dupuy, A. J., Shih, D. J. H., Witt, H., Croul, S., Bouffet, E., Fults, D. W., and Eberhart, C. G. (2012) Clonal selection drives genetic divergence of metastatic medulloblastoma, Nature, 482, 529–533.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Gonzalez, D., Martinez, P., Wade, R., Hockley, S., Oscier, D., Matutes, E., Dearden, C. E., Richards, S. M., Catovsky, D., and Morgan, G. J. (2011) Mutational status of the TP53 gene as a predictor of response and survival in patients with chronic lymphocytic leukemia: results from the LRF CLL4 trial, J. Clin. Oncol., 29, 2223–2229.CrossRefPubMedGoogle Scholar
  58. 58.
    Landau, D. A., Tausch, E., Bttcher, S., Stewart, C., Bozic, I., Leischner, I., Rosebrock, D., Taylor-Weiner, A., Mertens, D., and Sougnez, C. (2015) Quantitative clonal dynamics define mechanisms of CLL evolution in response to combination chemotherapy, Blood, 126, 362–362.Google Scholar
  59. 59.
    Wang, J., Cazzato, E., Ladewig, E., Frattini, V., Rosenbloom, D. I., Zairis, S., Abate, F., Liu, Z., Elliott, O., and Shin, Y.-J. (2016) Clonal evolution of glioblastoma under therapy, Nat. Genet., 48, 768–796.CrossRefPubMedGoogle Scholar
  60. 60.
    Chen, Z.-Y., Zhong, W.-Z., Zhang, X.-C., Su, J., Yang, X.N., Chen, Z.-H., Yang, J.-J., Zhou, Q., Yan, H.-H., and An, S.-J. (2012) EGFR mutation heterogeneity and the mixed response to EGFR tyrosine kinase inhibitors of lung adenocarcinomas, Oncologist, 17, 978–985.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Cheng, X., and Chen, H. (2014) Tumor heterogeneity and resistance to EGFR-targeted therapy in advanced nonsmall cell lung cancer: challenges and perspectives, Onco Targets Ther., 7, 1689–1704.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Murugaesu, N., Wilson, G. A., Birkbak, N. J., Watkins, T. B., McGranahan, N., Kumar, S., Abbassi-Ghadi, N., Salm, M., Mitter, R., and Horswell, S. (2015) Tracking the genomic evolution of esophageal adenocarcinoma through neoadjuvant chemotherapy, Cancer Discov., 8, 821–831.CrossRefGoogle Scholar
  63. 63.
    Findlay, J. M., Castro-Giner, F., Makino, S., Rayner, E., Kartsonaki, C., Cross, W., Kovac, M., Ulahannan, D., Palles, C., and Gillies, R. S. (2016) Differential clonal evolution in oesophageal cancers in response to neo-adjuvant chemotherapy, Nat. Commun., 7, 1–13.CrossRefGoogle Scholar
  64. 64.
    Kreso, A., O’brien, C. A., van Galen, P., Gan, O. I., Notta, F., Brown, A. M., Ng, K., Ma, J., Wienholds, E., and Dunant, C. (2013) Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer, Science, 339, 543–548.CrossRefPubMedGoogle Scholar
  65. 65.
    Diaz, L. A., Jr., Williams, R. T., Wu, J., Kinde, I., Hecht, J. R., Berlin, J., Allen, B., Bozic, I., Reiter, J. G., and Nowak, M. A. (2012) The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers, Nature, 486, 537–540.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Misale, S., Yaeger, R., Hobor, S., Scala, E., Janakiraman, M., Liska, D., Valtorta, E., Schiavo, R., Buscarino, M., and Siravegna, G. (2012) Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer, Nature, 486, 532–536.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Prandi, D., Baca, S. C., Romanel, A., Barbieri, C. E., Mosquera, J.-M., Fontugne, J., Beltran, H., Sboner, A., Garraway, L. A., Rubin, M. A., and Demichelis, F. (2014) Unraveling the clonal hierarchy of somatic genomic aberrations, Gen. Biol., 15, 439–450.CrossRefGoogle Scholar
  68. 68.
    Litviakov, N., Cherdyntseva, N., Ibragimova, M., Tsyganov, M., Kazantseva, P., Kzhyshkowska, J., and Slonimskaya, E. (2015) 299P: The clonal evolution of a breast tumor during neoadjuvant chemotherapy and metastasis, Ann. Oncol., 27, Suppl. 6, vi94.Google Scholar
  69. 69.
    Jiang, Y.-Z., Yu, K.-D., Bao, J., Peng, W.-T., and Shao, Z.M. (2014) Favorable prognostic impact in loss of TP53 and PIK3CA mutations after neoadjuvant chemotherapy in breast cancer, Cancer Res., 74, 3399–3407.CrossRefPubMedGoogle Scholar
  70. 70.
    Hughes, A. E., Magrini, V., Demeter, R., Miller, C. A., Fulton, R., Fulton, L. L., Eades, W. C., Elliott, K., Heath, S., Westervelt, P., Ding, L., Conrad, D. F., White, B. S., Shao, J., Link, D. C., DiPersio, J. F., Mardis, E. R., Wilson, R. K., Ley, T. J., Walter, M. J., and Graubert, T. A. (2014) Clonal architecture of secondary acute myeloid leukemia defined by single-cell sequencing, PLoS Genet., 10, e1004462.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Gundem, G., Van Loo, P., Kremeyer, B., Alexandrov, L. B., Tubio, J. M., Papaemmanuil, E., Brewer, D. S., Kallio, H. M., Hognas, G., Annala, M., Kivinummi, K., Goody, V., Latimer, C., O’ Meara, S., Dawson, K. J., Isaacs, W., Emmert-Buck, M. R., Nykter, M., Foster, C., Kote-Jarai, Z., Easton, D., Whitaker, H. C., Neal, D. E., Cooper, C. S., Eeles, R. A., Visakorpi, T., Campbell, P. J., McDermott, U., Wedge, D. C., Bova, G. S., and ICGC Prostate UK Group (2015) The evolutionary history of lethal metastatic prostate cancer, Nature, 520, 353–357.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Naxerova, K., and Jain, R. K. (2015) Using tumour phylogenetics to identify the roots of metastasis in humans, Nat. Rev. Clin. Oncol., 12, 258–272.CrossRefPubMedGoogle Scholar

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© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • M. K. Ibragimova
    • 1
    • 2
  • M. M. Tsyganov
    • 1
    • 2
  • N. V. Litviakov
    • 1
    • 2
    Email author
  1. 1.Cancer Research InstituteTomsk National Research Medical Center of the Russian Academy of SciencesTomskRussia
  2. 2.National Research Tomsk State UniversityTomskRussia

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