Intratumoural heterogeneity as a major challenge for cancer modelling and successful treatment


by Johanna Pruller, PhD

Randall Division of Cell and Molecular Biophysics, King's College London UK, johanna.prueller@kcl.ac.uk

https://orcid.org/0000-0002-1946-9920


https://doi.org/10.57098/SciRevs.Biology.2.1.2


References

  1. Del Monte, U. (2009). Does the cell number 109 still really fit one gram of tumor tissue? Cell Cycle, 8(3), 505–

    506. https://doi.org/10.4161/cc.8.3.7608

  2. Devita, V. T., Young, R. C., & Canellos, G. P. (1975). Combination versus single agent chemotherapy: A review of the basis for selection of drug treatment of cancer. Cancer, 35(1), 98–110. https://doi.org/10.1002/1097-0142(197501)35:1<98::AID-CNCR2820350115>3.0.CO;2-B

  3. Balkwill, F., & Mantovani, A. (2001). Inflammation and cancer: Back to Virchow? The Lancet, 357(9255), 539–

    545. https://doi.org/10.1016/S0140-6736(00)04046-0

  4. Zhu, L., Jiang, M., Wang, H., Sun, H., Zhu, J., Zhao, W., Fang, Q., Yu, J., Chen, P., Wu, S., Zheng, Z., & He, Y. (2021). A narrative review of tumor heterogeneity and challenges to tumor drug therapy. Annals of Translational Medicine, 9(16), 1351–1351. https://doi.org/10.21037/atm-21-1948

  5. Nowell, P. (1976). The Clonal Evolution of Tumor Cell Populations. 194(4260), 23–28.

  6. Dagogo-Jack, I., & Shaw, A. T. (2018). Tumour heterogeneity and resistance to cancer therapies. Nature Reviews Clinical Oncology, 15(2), 81–94. https://doi.org/10.1038/nrclinonc.2017.166

  7. Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., & Kinzler, K. W. (2013). Cancer Genome Landscapes. Science, 339(6127), 1546–1558. https://doi.org/10.1126/science.1235122

  8. Caiado, F., Silva-Santos, B., & Norell, H. (2016). Intra-tumour heterogeneity—Going beyond genetics.

    The FEBS Journal, 283(12), 2245–2258. https://doi.org/10.1111/febs.13705

  9. Bhang, H. C., Ruddy, D. A., Krishnamurthy Radhakrishna, V., Caushi, J. X., Zhao, R., Hims, M. M., Singh,

    A. P., Kao, I., Rakiec, D., Shaw, P., Balak, M., Raza, A., Ackley, E., Keen, N., Schlabach, M. R., Palmer, M., Leary, R. J., Chiang, D. Y., Sellers, W. R., … Stegmeier, F. (2015). Studying clonal dynamics in response to cancer therapy using high-complexity barcoding. Nature Medicine, 21(5), 440–448. https://doi.org/10.1038/ nm.3841

  10. Kwak, E. L., Ahronian, L. G., Siravegna, G., Mussolin, B., Borger, D. R., Godfrey, J. T., Jessop, N. A., Clark, J. W., Blaszkowsky, L. S., Ryan, D. P., Lennerz, J. K., Iafrate, A. J., Bardelli, A., Hong, T. S., & Cor coran, R. B. (2015). Molecular Heterogeneity and Receptor Coamplification Drive Resistance to Targeted Therapy in MET-Amplified Esophagogastric Cancer. Cancer Discovery, 5(12), 1271–1281. https://doi.org/ 10.1158/2159-8290.CD-15-0748

  11. Cleaver, J. E., & Crowley, E. (2002). UV damage, DNA repair and skin carcinogenesis. Frontiers in Bio science: A Journal and Virtual Library, 7, d1024-1043.

  12. Roberts, S. A., & Gordenin, D. A. (2014). Hypermutation in human cancer genomes: Footprints and mechanisms. Nature Reviews. Cancer, 14(12), 786–800. https://doi.org/10.1038/nrc3816

  13. Wei Dai, Y. Y. (2014). Genomic Instability and Cancer. Journal of Carcinogenesis & Mutagenesis, 05(02). https://doi.org/10.4172/2157-2518.1000165

  14. Carter, S. L., Eklund, A. C., Kohane, I. S., Harris, L. N., & Szallasi, Z. (2006). A signature of chromosomal in stability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nature Genetics, 38(9), 1043–1048. https://doi.org/10.1038/ng1861

  15. Andersson, N., Bakker, B., Karlsson, J., Valind, A., Holmquist Mengelbier, L., Spierings, D. C. J., Foijer, F., & Gisselsson, D. (2020). Extensive Clonal Branching Shapes the Evolutionary History of High-Risk Pe diatric Cancers. Cancer Research, 80(7), 1512–1523. https://doi.org/10.1158/0008-5472.CAN-19-3468

  16. Gainor, J. F., Dardaei, L., Yoda, S., Friboulet, L., Leshchiner, I., Katayama, R., Dagogo-Jack, I., Gadgeel, S., Schultz, K., Singh, M., Chin, E., Parks, M., Lee, D., DiCecca, R. H., Lockerman, E., Huynh, T., Lo gan, J., Ritter house, L. L., Le, L. P., … Shaw, A. T. (2016). Molecular Mechanisms of Resistance to First- and Second-Generation ALK Inhibitors in ALK-Rearranged Lung Cancer. Cancer Discovery, 6(10), 1118–1133. https://doi.org/10.1158/2159-8290.CD-16-0596

  17. Yu, H. A., Arcila, M. E., Rekhtman, N., Sima, C. S., Zakowski, M. F., Pao, W., Kris, M. G., Miller, V. A., Ladanyi, M., & Riely, G. J. (2013). Analysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-mutant lung cancers. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 19(8), 2240–2247. https://doi.org/10.1158/1078-0432.CCR-12-2246

  18. Shaw, A. T., Friboulet, L., Leshchiner, I., Gainor, J. F., Bergqvist, S., Brooun, A., Burke, B. J., Deng, Y.-L.,

    Liu, W., Dardaei, L., Frias, R. L., Schultz, K. R., Logan, J., James, L. P., Smeal, T., Timofeevski, S., Katayama, R., Iafrate, A. J., Le, L., … Engelman, J. A. (2016). Resensitization to Crizotinib by the Lorlatinib ALK Resistance Mutation L1198F. The New England Journal of Medicine, 374(1), 54–61. https://doi.org/10.1056/NEJMoa1508887

  19. Yu, H. A., Arcila, M. E., Hellmann, M. D., Kris, M. G., Ladanyi, M., & Riely, G. J. (2014). Poor response to er lotinib in patients with tumors containing baseline EGFR T790M mutations found by routine clinical molecu lar testing. Annals of Oncology: Official Journal of the European Society for Medical Oncology, 25(2), 423–428. https://doi.org/10.1093/annonc/mdt573

  20. Di Girolamo, C., Walters, S., Benitez Majano, S., Rachet, B., Coleman, M. P., Njagi, E. N., & Morris, M. (2018). Characteristics of patients with missing information on stage: A population-based study of patients di agnosed with colon, lung or breast cancer in England in 2013. BMC Cancer, 18(1), 492. https://doi.org/10.1186/ s12885-018-4417-3

  21. Dexter, D. L., Spremulli, E. N., Fligiel, Z., Barbosa, J. A., Vogel, R., VanVoorhees, A., & Calabresi, P. (1981). Heterogeneity of cancer cells from a single human colon carcinoma. The American Journal of Medicine, 71(6), 949–956. https://doi.org/10.1016/0002-9343(81)90312-0

  22. Manzella, G., Schreck, L. D., Breunis, W. B., Molenaar, J., Merks, H., Barr, F. G., Sun, W., Römmele, M.,

    Zhang, L., Tchinda, J., Ngo, Q. A., Bode, P., Delattre, O., Surdez, D., Rekhi, B., Niggli, F. K., Schäfer, B. W., & Wachtel, M. (2020). Phenotypic profiling with a living biobank of primary rhabdomyosarcoma unravels dis ease heterogeneity and AKT sensitivity. Nature Communications, 11(1), 4629. https://doi.org/10.1038/s41467-020-18388-7

  23. Ben-David, U., Siranosian, B., Ha, G., Tang, H., Oren, Y., Hinohara, K., Strathdee, C. A., Dempster, J., Lyons,

    N. J., Burns, R., Nag, A., Kugener, G., Cimini, B., Tsvetkov, P., Maruvka, Y. E., O’Rourke, R., Garrity, A., Tubelli,

    A. A., Bandopadhayay, P., … Golub, T. R. (2018). Genetic and transcriptional evolution alters cancer cell line

    drug response. Nature, 560(7718), 325–330. https://doi.org/10.1038/s41586-018-0409-3

  24. Liu, Y., Mi, Y., Mueller, T., Kreibich, S., Williams, E. G., Van Drogen, A., Borel, C., Frank, M., Germain, P.-

    L., Bludau, I., Mehnert, M., Seifert, M., Emmenlauer, M., Sorg, I., Bezrukov, F., Bena, F. S., Zhou, H., Dehio, C., Testa, G., … Aebersold, R. (2019). Multi-omic measurements of heterogene ity in HeLa cells across laborato ries. Nature Biotechnology, 37(3), 314–322. https://doi.org/10.1038/s41587-019-0037-y

  25. Hynds, R. E., Vladimirou, E., & Janes, S. M. (2018). The secret lives of cancer cell lines. Disease Models & Mechanisms, 11(11). https://doi.org/10.1242/dmm.037366

  26. Domura, R., Sasaki, R., Ishikawa, Y., & Okamoto, M. (2017). Cellular Morphology-Mediated Prolifera tion and Drug Sensitivity of Breast Cancer Cells. Journal of Functional Biomaterials, 8(2), 18. htts://doi.org/ 10.3390/jfb8020018

  27. Yin, Z., Sadok, A., Sailem, H., McCarthy, A., Xia, X., Li, F., Garcia, M. A., Evans, L., Barr, A. R., Perri mon, N., Marshall, C. J., Wong, S. T. C., & Bakal, C. (2013). A screen for morphological complexity identi fies regulators of switch-like transitions between discrete cell shapes. Nature Cell Biology, 15(7), 860–871. https://doi.org/10.1038/ncb2764

  28. Ayyoub, M., Scarlata, C.-M., Hamaï, A., Pignon, P., & Valmori, D. (2014). Expression of MAGE-A3/6 in Primary Breast Cancer is Associated With Hormone Receptor Negative Status, High Histologic Grade, and Poor Survival: Journal of Immunotherapy, 37(2), 73–76. https://doi.org/10.1097/CJI.0000000000000013

  29. Wu, P.-H., Phillip, J. M., Khatau, S. B., Chen, W.-C., Stirman, J., Rosseel, S., Tschudi, K., Van Patten, J., Wong, M., Gupta, S., Baras, A. S., Leek, J. T., Maitra, A., & Wirtz, D. (2015). Evolution of cellular morpho-phenotypes in cancer metastasis. Scientific Reports, 5, 18437. https://doi.org/10.1038/srep18437

  30. Minn, A. J., Kang, Y., Serganova, I., Gupta, G. P., Giri, D. D., Doubrovin, M., Ponomarev, V., Gerald, W. L., Blasberg, R., & Massagué, J. (2005). Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. The Journal of Clinical Investigation, 115(1), 44–55. https://doi.org/10.1172/JCI22320