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Emerging Potential of Cancer Therapy—Binary Direct Interactions of Cancer and Stromal Cells

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Russian Journal of Genetics Aims and scope Submit manuscript

Out of clutter, find simplicity.

From discord, find harmony.

In the middle of difficulty lies opportunity.

Albert Einstein

Abstract

The review attempts to discuss the interaction of cancer cells and cells of the tumor microenvironment as well as the possibility of using them as a target for antitumor therapy.

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REFERENCES

  1. Sverdlov, E.D., Genetic surgery—a right strategy to attack cancer, Curr. Gene Ther., 2011, vol. 11, no. 6, pp. 501—531.

    Article  CAS  PubMed  Google Scholar 

  2. Sverdlov, E.D., Multidimensional complexity of cancer: simple solutions are needed, Biochemistry (Moscow), 2016, vol. 81, no. 7, pp. 731—738. https://doi.org/.10.1134/S0006297916070099.

    CAS  PubMed  Google Scholar 

  3. Alizadeh, A.A., Aranda, V., Bardelli, A., et al., Toward understanding and exploiting tumor heterogeneity, Nat. Med., 2015, vol. 21, no. 8, pp. 846—853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Schnekenburger, M., Florean, C., Dicato, M., and Diederich, M., Epigenetic alterations as a universal feature of cancer hallmarks and a promising target for personalized treatments, Curr. Top Med. Chem., 2016, vol. 16, no. 7, pp. 745—776. doi 10.2174/1568026615666150825141330

    Article  CAS  PubMed  Google Scholar 

  5. Hanahan, D. and Weinberg, R.A., The hallmarks of cancer, Cell, 2000, vol. 100, no. 1, pp. 57—70.

    Article  CAS  PubMed  Google Scholar 

  6. Ramamonjisoa, N. and Ackerstaff, E., Characterization of the tumor microenvironment and tumor—stroma interaction by non-invasive preclinical imaging, Front. Oncol., 2017, vol. 7, p. 3. doi 10.3389/fonc.2017.00003

    Article  PubMed  PubMed Central  Google Scholar 

  7. Weinberg, R.A., Coming full circle—from endless complexity to simplicity and back again, Cell, 2014, vol. 157, no. 1, pp. 267—271. doi 10.1016/j.cell.2014.03.004

    Article  CAS  PubMed  Google Scholar 

  8. Hanahan, D. and Coussens, L.M., Accessories to the crime: functions of cells recruited to the tumor microenvironment, Cancer Cell, 2012, vol. 21, no. 3, pp. 309—322. doi 10.1016/j.ccr.2012.02.022

    Article  CAS  PubMed  Google Scholar 

  9. Hanahan, D. and Weinberg, R.A., Hallmarks of cancer: the next generation, Cell, 2011, vol. 144, no. 5, pp. 646—674.

    Article  CAS  PubMed  Google Scholar 

  10. Horne, S.D., Pollick, S.A., and Heng, H.H., Evolutionary mechanism unifies the hallmarks of cancer, Int. J. Cancer, 2015, vol. 136, no. 9, pp. 2012—2021. doi 10.1002/ijc.29031

    Article  CAS  PubMed  Google Scholar 

  11. Fouad, Y.A. and Aanei, C., Revisiting the hallmarks of cancer, Am. J. Cancer Res., 2017, vol. 7, no. 5, pp. 1016—1036.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Orimo, A. and Weinberg, R.A., Stromal fibroblasts in cancer: a novel tumor-promoting cell type, Cell Cycle, 2006, vol. 5, no. 15, pp. 1597—1601. doi 10.4161/cc.5.15.3112

    Article  CAS  PubMed  Google Scholar 

  13. Gonda, T.A., Varro, A., Wang, T.C., and Tycko, B., Molecular biology of cancer-associated fibroblasts: can these cells be targeted in anti-cancer therapy?, Semin. Cell Dev. Biol., 2010, vol. 21, no. 1, pp. 2—10. doi 10.1016/j.semcdb.2009.10.001

    Article  CAS  PubMed  Google Scholar 

  14. De Palma, M. and Hanahan, D., The biology of personalized cancer medicine: facing individual complexities underlying hallmark capabilities, Mol. Oncol., 2012, vol. 6, no. 2, pp. 111—127. doi 10.1016/j.molonc.2012.01.011

    Article  PubMed  PubMed Central  Google Scholar 

  15. Gascard, P. and Tlsty, T.D., Carcinoma-associated fibroblasts: orchestrating the composition of malignancy, Genes Dev., 2016, vol. 30, no. 9, pp. 1002—1019. doi 10.1101/gad.279737.116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Chen, F., Zhuang, X., Lin, L., et al., New horizons in tumor microenvironment biology: challenges and opportunities, BMC Med., 2015, vol. 13, p. 45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gandellini, P., Andriani, F., Merlino, G., et al., Complexity in the tumour microenvironment: cancer associated fibroblast gene expression patterns identify both common and unique features of tumour—stroma crosstalk across cancer types, Semin. Cancer Biol., 2015, vol. 35, pp. 96—106. doi 10.1016/j.semcancer.2015.08.008

    Article  CAS  PubMed  Google Scholar 

  18. Stadler, M., Walter, S., Walzl, A., et al., Increased complexity in carcinomas: Analyzing and modeling the interaction of human cancer cells with their microenvironment, Semin. Cancer Biol., 2015, vol. 35, pp. 107—124. doi 10.1016/j.semcancer.2015.08.007

    Article  PubMed  Google Scholar 

  19. Zi, F., He, J., He, D., et al., Fibroblast activation protein alpha in tumor microenvironment: recent progression and implications (review), Mol. Med. Rep., 2015, vol. 11, no. 5, pp. 3203—3211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Raffaghello, L. and Dazzi, F., Classification and biology of tumour associated stromal cells, Immunol. Lett., 2015, vol. 168, no. 2, pp. 175—182. doi 10.1016/j.imlet.2015.06.016

    Article  CAS  PubMed  Google Scholar 

  21. Bizzarri, M. and Cucina, A., Tumor and the microenvironment: a chance to reframe the paradigm of carcinogenesis?, Biomed. Res. Int., 2014, vol. 2014, p. 934038. doi 10.1155/2014/934038

    Article  PubMed  PubMed Central  Google Scholar 

  22. Reina-Campos, M., Moscat, J., and Diaz-Meco, M., Metabolism shapes the tumor microenvironment, Curr. Opin. Cell Biol., 2017, vol. 48, pp. 47—53. doi 10.1016/j.ceb.2017.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sadelain, M., Riviere, I., and Brentjens, R., Targeting tumours with genetically enhanced t lymphocytes, Nat. Rev. Cancer, 2003, vol. 3, no. 1, pp. 35—45. doi 10.1038/nrc971

    Article  CAS  PubMed  Google Scholar 

  24. Schumacher, T.N. and Schreiber, R.D., Neoantigens in cancer immunotherapy, Science, 2015, vol. 348, no. 6230, pp. 69—74.

    Article  CAS  PubMed  Google Scholar 

  25. Martin, S.D., Coukos, G., Holt, R.A., and Nelson, B.H., Targeting the undruggable: immunotherapy meets personalized oncology in the genomic era, Ann. Oncol., 2015, vol. 26, no. 12, pp. 2367—2374.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Ziani, L., Chouaib, S., and Thiery, J., Alteration of the antitumor immune response by cancer-associated fibroblasts, Front. Immunol., 2018, vol. 9, p. 414. doi 10.3389/fimmu.2018.00414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. van der Burg, S.H., Arens, R., Ossendorp, F., et al., Vaccines for established cancer: overcoming the challenges posed by immune evasion, Nat. Rev. Cancer, 2016, vol. 16, no. 4, pp. 219—233.

    Article  CAS  PubMed  Google Scholar 

  28. Muenst, S., Laubli, H., Soysal, S.D., et al., The immune system and cancer evasion strategies: therapeutic concepts, J. Int. Med., 2016, vol. 279, no. 6, pp. 541—562.

    Article  CAS  Google Scholar 

  29. Schreiber, R.D., Old, L.J., and Smyth, M.J., Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion, Science, 2011, vol. 331, no. 6024, pp. 1565—1570.

    Article  CAS  PubMed  Google Scholar 

  30. Escors, D., Tumour immunogenicity, antigen presentation and immunological barriers in cancer immunotherapy, New J. Sci., 2014, vol. 2014. doi 10.1155/2014/734515

  31. Stambrook, P.J., Maher, J., and Farzaneh, F., Cancer immunotherapy: whence and whither, Mol. Cancer Res., 2017, vol. 15, no. 6, pp. 635—650. doi 10.1158/1541-7786.MCR-16-0427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Baumeister, S.H., Freeman, G.J., Dranoff, G., and Sharpe, A.H., Coinhibitory pathways in immunotherapy for cancer, Annu. Rev. Immunol., 2016, vol. 34, pp. 539—573. doi 10.1146/annurev-immunol-032414-112049

    Article  CAS  PubMed  Google Scholar 

  33. Marin-Acevedo, J.A., Dholaria, B., Soyano, A.E., et al., Next generation of immune checkpoint therapy in cancer: New developments and challenges, J. Hematol. Oncol., 2018, vol. 11, no. 1, p. 39. doi 10.1186/s13045-018-0582-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Marcucci, F., Rumio, C., and Corti, A., Tumor cell-associated immune checkpoint molecules—drivers of malignancy and stemness, Biochim. Biophys. Acta, 2017, vol. 1868, no. 2, pp. 571—583. doi 10.1016/j.bbcan.2017.10.006

    CAS  Google Scholar 

  35. Sharma, P. and Allison, J.P., The future of immune checkpoint therapy, Science, 2015, vol. 348, no. 6230, pp. 56—61.

    Article  CAS  PubMed  Google Scholar 

  36. Sharpe, A.H., Introduction to checkpoint inhibitors and cancer immunotherapy, Immunol. Rev., 2017, vol. 276, no. 1, pp. 5—8. doi 10.1111/imr.12531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Allison, J.P., Immune checkpoint blockade in cancer therapy: the 2015 Lasker—Debakey clinical medical research award, JAMA, 2015, vol. 314, no. 11, pp. 1113—1114. doi 10.1001/jama.2015.11929

    Article  CAS  PubMed  Google Scholar 

  38. Villaruz, L.C., Kalyan, A., Zarour, H., and Socinski, M.A., Immunotherapy in lung cancer, Transl. Lung Cancer Res., 2014, vol. 3, no. 1, pp. 2—14. doi 10.3978/j.issn.2218-6751.2013.10.13

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Munhoz, R.R. and Postow, M.A., Clinical development of pd-1 in advanced melanoma, Cancer J., 2018, vol. 24, no. 1, pp. 7—14. doi 10.1097/PPO.0000000000000299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Postow, M. and Wolchok, J., Toxicities associated with checkpoint inhibitor immunotherapy, 2016. http://www.uptodate.com/contents/toxicities-associated-withcheckpoint-inhibitor-immunotherapy. Accessed February 22, 2018.

  41. Alexander, W., The checkpoint immunotherapy revolution: what started as a trickle has become a flood, despite some daunting adverse effects; new drugs, indications, and combinations continue to emerge, P. T., 2016, vol. 41, no. 3, pp. 185—191.

    PubMed  PubMed Central  Google Scholar 

  42. Calabrese, L. and Velcheti, V., Checkpoint immunotherapy: good for cancer therapy, bad for rheumatic diseases, Ann. Rheum. Dis., 2017, vol. 76, no. 1, pp. 1—3. doi 10.1136/annrheumdis-2016-209782

    Article  CAS  PubMed  Google Scholar 

  43. Madden, D.L., From a patient advocate’s perspective: does cancer immunotherapy represent a paradigm shift?, Curr. Oncol. Rep., 2018, vol. 20, no. 1, p. 8. doi 10.1007/s11912-018-0662-5

    Article  PubMed  Google Scholar 

  44. Abdin, S.M., Zaher, D.M., Arafa, E.A., and Omar, H.A., Tackling cancer resistance by immunotherapy: updated clinical impact and safety of pd-1/pd-l1 inhibitors, Cancers (Basel), 2018, vol. 10, no. 2. doi 10.3390/cancers10020032

  45. Postow, M.A. and Hellmann, M.D., Adverse events associated with immune checkpoint blockade, N. Engl. J. Med., 2018, vol. 378, no. 12, p. 1165.

    Article  PubMed  Google Scholar 

  46. Brown, J.S., Sundar, R., and Lopez, J., Combining DNA damaging therapeutics with immunotherapy: more haste, less speed, Br. J. Cancer., 2018, vol. 118, no. 3, pp. 312—324. doi 10.1038/bjc.2017.376

    Article  CAS  PubMed  Google Scholar 

  47. Hosoi, A., Takeda, K., Nagaoka, K., et al., Increased diversity with reduced “Diversity evenness” of tumor infiltrating t-cells for the successful cancer immunotherapy, Sci. Rep., 2018, vol. 8, no. 1, p. 1058. doi 10.1038/s41598-018-19548-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Perrimon, N., Pitsouli, C., and Shilo, B.Z., Signaling mechanisms controlling cell fate and embryonic patterning, Cold Spring Harbor Perspect. Biol., 2012, vol. 4, no. 8. a005975. doi 10.1101/cshperspect.a005975

    Article  CAS  Google Scholar 

  49. Sundar, R., Chenard-Poirier, M., Collins, D.C., and Yap, T.A., Imprecision in the era of precision medicine in non-small cell lung cancer, Front. Med. (Lausanne), 2017, vol. 4, p. 39. doi 10.3389/fmed.2017.00039

    Article  Google Scholar 

  50. Minocha, S. and Das, S., Gleevec (imatinib): a breakthrough in cancer treatment, J. Drug Discovery Ther., 2017, vol. 5, no. 8, pp. 13—17.

    CAS  Google Scholar 

  51. Mallick, P., Complexity and information: cancer as a multi-scale complex adaptive system, in Physical Science and Engineering Advances in Life Science and Oncology, 2015, pp. 5—29.

  52. Prasad, V., Perspective: the precision-oncology illusion, Nature, 2016, vol. 537, no. 7619, p. S63. doi 10.1038/537S63a

    Article  CAS  PubMed  Google Scholar 

  53. Tannock, I.F. and Hickman, J.A., Limits to personalized cancer medicine, N. Engl. J. Med., 2016, vol. 375, no. 13, pp. 1289—1294. doi 10.1056/NEJMsb1607705

    Article  PubMed  Google Scholar 

  54. Haynes, B., Sarma, A., Nangia-Makker, P., and Shekhar, M.P., Breast cancer complexity: implications of intratumoral heterogeneity in clinical management, Cancer Metastasis Rev., 2017, vol. 36, no. 3, pp. 547—555. doi 10.1007/s10555-017-9684-y

    Article  PubMed  PubMed Central  Google Scholar 

  55. Taube, J.M., Anders, R.A., Young, G.D., et al., Colocalization of inflammatory response with b7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape, Sci. Transl. Med., 2012, vol. 4, no. 127, pp. 127—137. doi 10.1126/scitranslmed.3003689

    Article  CAS  Google Scholar 

  56. Cogdill, A.P., Andrews, M.C., and Wargo, J.A., Hallmarks of response to immune checkpoint blockade, Br. J. Cancer, 2017, vol. 117, no. 1, pp. 1—7. doi 10.1038/bjc.2017.136

    Article  PubMed  PubMed Central  Google Scholar 

  57. Teng, M.W., Ngiow, S.F., Ribas, A., and Smyth, M.J., Classifying cancers based on t-cell infiltration and pd-l1, Cancer Res., 2015, vol. 75, no. 11, pp. 2139—2145. doi 10.1158/0008-5472.CAN-15-0255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zhang, Y. and Chen, L., Classification of advanced human cancers based on tumor immunity in the microenvironment (time) for cancer immunotherapy, JAMA Oncol., 2016, vol. 2, no. 11, pp. 1403—1404. doi 10.1001/jamaoncol.2016.2450

    Article  PubMed  PubMed Central  Google Scholar 

  59. Koh, J., Ock, C.Y., Kim, J.W., et al., Clinicopathologic implications of immune classification by pd-l1 expression and cd8-positive tumor-infiltrating lymphocytes in stage ii and iii gastric cancer patients, Oncotarget, 2017, vol. 8, no. 16, pp. 26356—26367. doi 10.18632/oncotarget.15465

    PubMed  PubMed Central  Google Scholar 

  60. Ock, C.Y., Keam, B., Kim, S., et al., Pan-cancer immunogenomic perspective on the tumor microenvironment based on pd-l1 and cd8 t-cell infiltration, Clin. Cancer Res., 2016, vol. 22, no. 9, pp. 2261—2270. doi 10.1158/1078-0432.CCR-15-2834

    Article  CAS  PubMed  Google Scholar 

  61. Loo, K. and Daud, A., Emerging biomarkers as predictors to anti-pd1/pd-l1 therapies in advanced melanoma, Immunotherapy, 2016, vol. 8, no. 7, pp. 775—784. doi 10.2217/imt-2016-0039

    Article  CAS  PubMed  Google Scholar 

  62. Dempke, W.C.M., Fenchel, K., Uciechowski, P., and Dale, S.P., Second- and third-generation drugs for immuno-oncology treatment—the more the better?, Eur. J. Cancer, 2017, vol. 74, pp. 55—72. doi 10.1016/j.ejca.2017.01.001

    Article  CAS  PubMed  Google Scholar 

  63. Fearon, D.T., The carcinoma-associated fibroblast expressing fibroblast activation protein and escape from immune surveillance, Cancer Immunol. Res., 2014, vol. 2, no. 3, pp. 187—193. doi 10.1158/2326-6066.CIR-14-0002

    Article  CAS  PubMed  Google Scholar 

  64. Day, D., Monjazeb, A.M., Sharon, E., et al., From famine to feast: developing early-phase combination immunotherapy trials wisely, Clin. Cancer Res., 2017, vol. 23, no. 17, pp. 4980—4991. doi 10.1158/1078-0432.CCR-16-3064

    Article  PubMed  PubMed Central  Google Scholar 

  65. Lamprecht, S., Sigal-Batikoff, I., Shany, S., et al., Teaming up for trouble: cancer cells, transforming growth factor-beta1 signaling and the epigenetic corruption of stromal naive fibroblasts, Cancers (Basel), 2018, vol. 10, no. 3. doi 10.3390/cancers10030061

  66. Kalluri, R., The biology and function of fibroblasts in cancer, Nat. Rev. Cancer, 2016, vol. 16, no. 9, pp. 582—598. doi 10.1038/nrc.2016.73

    Article  CAS  PubMed  Google Scholar 

  67. Shiga, K., Hara, M., Nagasaki, T., et al., Cancer-associated fibroblasts: their characteristics and their roles in tumor growth, Cancers (Basel), 2015, vol. 7, no. 4, pp. 2443—2458. doi 10.3390/cancers7040902

    Article  PubMed  PubMed Central  Google Scholar 

  68. Pidsley, R., Zotenko, E., Peters, T.J., et al., Critical evaluation of the illumina methylationepic beadchip microarray for whole-genome DNA methylation profiling, Genome Biol., 2016, vol. 17, no. 1, p. 208. doi 10.1186/s13059-016-1066-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Liao, Z., Tan, Z.W., Zhu, P., and Tan, N.S., Cancer-associated fibroblasts in tumor microenvironment— accomplices in tumor malignancy, Cell. Immunol., 2018. doi 10.1016/j.cellimm.2017.12.003

  70. Tran, E., Chinnasamy, D., Yu, Z., et al., Immune targeting of fibroblast activation protein triggers recognition of multipotent bone marrow stromal cells and cachexia, J. Exp. Med., 2013, vol. 210, no. 6, pp. 1125—1135. doi 10.1084/jem.20130110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Bhome, R., Al Saihati, H.A., Goh, R.W., et al., Translational aspects in targeting the stromal tumour microenvironment: from bench to bedside, New Horiz. Transl. Med., 2016, vol. 3, no. 1, pp. 9—21. doi 10.1016/j.nhtm.2016.03.001

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Kumar, V., Patel, S., Tcyganov, E., and Gabrilovich, D.I., The nature of myeloid-derived suppressor cells in the tumor microenvironment, Trends Immunol., 2016, vol. 37, no. 3, pp. 208—220. doi 10.1016/j.it.2016.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Jacobs, J., Smits, E., Lardon, F., et al., Immune checkpoint modulation in colorectal cancer: what’s new and what to expect, J. Immunol. Res., 2015, vol. 2015, p. 158038. doi 10.1155/2015/158038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Lakins, M.A., Ghorani, E., Munir, H., et al., Cancer-associated fibroblasts induce antigen-specific deletion of cd8 (+) t cells to protect tumour cells, Nat. Commun., 2018, vol. 9, no. 1, p. 948. doi 10.1038/s41467-018-03347-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Rozali, E.N., Hato, S.V., Robinson, B.W., et al., Programmed death ligand 2 in cancer-induced immune suppression, Clin. Dev. Immunol., 2012, vol. 2012, p. 656340. doi 10.1155/2012/656340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Nazareth, M.R., Broderick, L., Simpson-Abelson, M.R., et al., Characterization of human lung tumor-associated fibroblasts and their ability to modulate the activation of tumor-associated t cells, J. Immunol., 2007, vol. 178, no. 9, pp. 5552—5562.

    Article  CAS  PubMed  Google Scholar 

  77. Khalili, J.S., Liu, S., Rodriguez-Cruz, T.G., et al., Oncogenic braf(v600e) promotes stromal cell-mediated immunosuppression via induction of interleukin-1 in melanoma, Clin. Cancer Res., 2012, vol. 18, no. 19, pp. 5329—5340. doi 10.1158/1078-0432.CCR-12-1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Costa, A., Kieffer, Y., Scholer-Dahirel, A., et al., Fibroblast heterogeneity and immunosuppressive environment in human breast cancer, Cancer Cell, 2018, vol. 33, no. 3, pp. 463—479. e410. doi 10.1016/j.ccell.2018. 01.011

  79. Choe, C., Shin, Y.S., Kim, S.H., et al., Tumor-stromal interactions with direct cell contacts enhance motility of non-small cell lung cancer cells through the hedgehog signaling pathway, Anticancer Res., 2013, vol. 33, no. 9, pp. 3715—3723.

    CAS  PubMed  Google Scholar 

  80. Yamaguchi, H. and Sakai, R., Direct interaction between carcinoma cells and cancer associated fibroblasts for the regulation of cancer invasion, Cancers (Basel), 2015, vol. 7, no. 4, pp. 2054—2062. doi 10.3390/cancers7040876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Semba, S., Kodama, Y., Ohnuma, K., et al., Direct cancer-stromal interaction increases fibroblast proliferation and enhances invasive properties of scirrhous-type gastric carcinoma cells, Br. J. Cancer, 2009, vol. 101, no. 8, pp. 1365—1373. doi 10.1038/sj.bjc. 6605309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    I. V. Alekseenko, G. S. Monastyrskaya & E. D. Sverdlov

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  1. I. V. Alekseenko
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Alekseenko, I.V., Monastyrskaya, G.S. & Sverdlov, E.D. Emerging Potential of Cancer Therapy—Binary Direct Interactions of Cancer and Stromal Cells. Russ J Genet 54, 1416–1428 (2018). https://doi.org/10.1134/S1022795418120025

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