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Do locally advanced and metastatic human epithelial cancers evolve in ‘placental/decidual-like microenvironments’?

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Abstract

Successful tumor microenvironments eventually kill the host. They are not only meant to nourish and protect tumor development, but to give them the right “soil” for perpetual malignant properties such as tissue invasion and metastasis. This can only be achieved if cancers avoid immune vigilance. A similar situation occurs in mammalian placental pregnancy but feto-maternal tolerance is required for a correct physiological process only until birth. Once a cancer microenvironment has acquired the genetic and epigenetic “placental immune editing switches” (PIES) phenotype, it seems likely that it will keep them “available”, whenever needed, for the rest of its development, because it gives cellular clones a competitive advantage to pass unnoticed by the host’s immune system. This allows primary cancers and their metastasis to continue growing in spite of new and changing antigenic landscapes.

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References

  1. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell. 2004;6:17–32.

    Article  CAS  PubMed  Google Scholar 

  2. Bar J, Feniger-Barish R, Lukashchuk N, Shaham H, Moskovits N, Goldfinger N, et al. Cancer cells suppress p53 in adjacent fibroblasts. Oncogene. 2009;28:933–6.

    Article  CAS  PubMed  Google Scholar 

  3. Barnes TA, Amir E. HYPE or HOPE: the prognostic value of infiltrating immune cells in cancer. Br J Cancer. 2017;117:451–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Carmona-Fontaine C, Deforet M, Akkari L, Thompson CB, Joyce JA, Xavier JB. Metabolic origins of spatial organization in the tumor microenvironment. Proc Natl Acad Sci USA. 2017;114:2934–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3:401–10.

    Article  CAS  PubMed  Google Scholar 

  6. Bidwell BN, Slaney CY, Withana NP, Forster S, Cao Y, Loi S, et al. Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape. Nat Med. 2012;18:1224–31.

    Article  CAS  PubMed  Google Scholar 

  7. Bigley AB, Simpson RJ. NK cells and exercise: implications for cancer immunotherapy and survivorship. Discov Med. 2015;19:433–45.

    PubMed  Google Scholar 

  8. Brentnall TA, Crispin DA, Rabinovitch PS, Haggitt RC, Rubin CE, Stevens AC, et al. Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology. 1994;107:369–78.

    Article  CAS  PubMed  Google Scholar 

  9. Bronte V, Brandau S, Chen S-H, Colombo MP, Frey AB, Greten TF, et al. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun. 2016;7:12150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Casazza A, Laoui D, Wenes M, Rizzolio S, Bassani N, Mambretti M, et al. Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity. Cancer Cell. 2013;24:695–709.

    Article  CAS  PubMed  Google Scholar 

  11. Catanzaro JM, Sheshadri N, Pan J-A, Sun Y, Shi C, Li J, et al. Oncogenic Ras induces inflammatory cytokine production by upregulating the squamous cell carcinoma antigens SerpinB3/B4. Nat Commun. 2014;5:3729.

    Article  CAS  PubMed  Google Scholar 

  12. Chaput N, Lepage P, Coutzac C, Soularue E, Le Roux K, Monot C, et al. Baseline gut microbiota predicts clinical response and colitis in metastatic melanoma patients treated with ipilimumab. Ann Oncol. 2017;28:1368–79.

    Article  CAS  PubMed  Google Scholar 

  13. Cheon H, Borden EC, Stark GR. Interferons and their stimulated genes in the tumor microenvironment. Semin Oncol. 2014;41:156–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chiba T, Marusawa H, Seno H, Watanabe N. Mechanism for gastric cancer development by Helicobacter pylori infection. J Gastroenterol Hepatol. 2008;23:1175–81.

    Article  CAS  PubMed  Google Scholar 

  15. Cleary MP, Grossmann ME. Minireview: obesity and breast cancer: the estrogen connection. Endocrinology. 2009;150:2537–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cooks T, Harris CC, Oren M. Caught in the cross fire: p53 in inflammation. Carcinogenesis. 2014;35:1680–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Cooks T, Pateras IS, Tarcic O, Solomon H, Schetter AJ, Wilder S, et al. Mutant p53 prolongs NF-κB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell. 2013;23:634–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Coppé J-P, Patil CK, Rodier F, Sun Y, Muñoz DP, Goldstein J, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 2008;6:2853–68.

    Article  CAS  PubMed  Google Scholar 

  19. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. De Boeck A, Hendrix A, Maynard D, Van Bockstal M, Daniëls A, Pauwels P, et al. Differential secretome analysis of cancer-associated fibroblasts and bone marrow-derived precursors to identify microenvironmental regulators of colon cancer progression. Proteomics. 2013;13:379–88.

    Article  CAS  PubMed  Google Scholar 

  21. Di Minin G, Bellazzo A, Dal Ferro M, Chiaruttini G, Nuzzo S, Bicciato S, et al. Mutant p53 reprograms TNF signaling in cancer cells through interaction with the tumor suppressor DAB2IP. Mol Cell. 2014;56:617–29.

    Article  CAS  PubMed  Google Scholar 

  22. Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev Cancer. 2013;13:759–71.

    Article  CAS  PubMed  Google Scholar 

  23. Ferrara N, Adamis AP. Ten years of anti-vascular endothelial growth factor therapy. Nat Rev Drug Discov. 2016;15:385–403.

    Article  CAS  PubMed  Google Scholar 

  24. De Palma M, Biziato D, Petrova TV. Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer. 2017;17:457–74.

    Article  CAS  PubMed  Google Scholar 

  25. Holtan SG, Creedon DJ, Haluska P, Markovic SN. Cancer and pregnancy: parallels in growth, invasion, and immune modulation and implications for cancer therapeutic agents. Mayo Clin Proc. 2009;84:985–1000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, et al. The cellular and molecular origin of tumor-associated macrophages. Science. 2014;344:921–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359:97–103.

    Article  CAS  PubMed  Google Scholar 

  28. Iyengar NM, Gucalp A, Dannenberg AJ, Hudis CA. Obesity and cancer mechanisms: tumor microenvironment and inflammation. J Clin Oncol. 2016;34:4270–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bronchud MH, Tresserra F, Xu W, Warren S, Cusido M, Zantop B, et al. Placental immune editing switch (PIES): learning about immunomodulatory pathways from a unique case report. Oncotarget. 2016;7:83817–27.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Bronchud MH, Tresserra F, Zantop BS. Epigenetic changes found in uterine decidual and placental tissues can also be found in the breast cancer microenvironment of the same unique patient: description and potential interpretations. Oncotarget. 2018;9:6028–41.

    Article  PubMed  Google Scholar 

  31. Bronchud MH. Are aggressive epithelial cancers “a disease” of Eutherian mammals? Ecancermedicalscience. 2018;12:840.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nagy A, Gócza E, Diaz EM, Prideaux VR, Iványi E, Markkula M, et al. Embryonic stem cells alone are able to support fetal development in the mouse. Development. 1990;110:815–21.

    CAS  PubMed  Google Scholar 

  33. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science. 1998;282:2072–5.

    Article  CAS  PubMed  Google Scholar 

  34. Kunath T, Arnaud D, Uy GD, Okamoto I, Chureau C, Yamanaka Y, et al. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development. 2005;132:1649–61.

    Article  CAS  PubMed  Google Scholar 

  35. Lu C-W, Yabuuchi A, Chen L, Viswanathan S, Kim K, Daley GQ. Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet. 2008;40:921–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Erb TM, Schneider C, Mucko SE, Sanfilippo JS, Lowry NC, Desai MN, et al. Paracrine and epigenetic control of trophectoderm differentiation from human embryonic stem cells: the role of bone morphogenic protein 4 and histone deacetylases. Stem Cells Dev. 2011;20:1601–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Frank HG. Chapter 10: placental development. In: Polin RA, Abman SH, Rowitch DH, Benitz WE, Fox WW, editors. Fetal and neonatal physiology. 5th ed. Philadelphia: Elsevier; 2017.

    Google Scholar 

  38. Ferris E, Abegglen LM, Schiffman JD, Gregg C. Accelerated evolution in distinctive species reveals candidate elements for clinically relevant traits, including mutation and cancer resistance. Cell Rep. 2018;22:2742–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Rothschild BM, Tanke DH, Helbling M, Martin LD. Epidemiologic study of tumors in dinosaurs. Naturwissenschaften. 2003;90:495–500.

    Article  CAS  PubMed  Google Scholar 

  40. Tollis M, Boddy AM, Maley CC. Peto’s Paradox: how has evolution solved the problem of cancer prevention? BMC Biol. 2017;15:60.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Briggs JA, Weinreb C, Wagner DE, Megason S, Peshkin L, Kirschner MW, et al. The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution. Science. 2018;360:eaar5780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. McDole K, Guignard L, Amat F, Berger A, Malandain G, Royer LA. In toto imaging and reconstruction of post-implantation mouse development at the single-cell level. Cell. 2018. https://doi.org/10.1016/j.cell.2018.09.031.

    Article  PubMed  Google Scholar 

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Acknowledgements

I would like to thank Ana María Moreno (Madrid) and Mary Darlow (Barcelona) for their competent help with text and references editing.

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Correspondence to M. Hernández-Bronchud.

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This work was carried out with no outside or institutional grants. The author is not, at present, under any relevant contractual obligations with any pharmaceutical companies.

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Hernández-Bronchud, M. Do locally advanced and metastatic human epithelial cancers evolve in ‘placental/decidual-like microenvironments’?. Clin Transl Oncol 21, 160–166 (2019). https://doi.org/10.1007/s12094-018-1982-5

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  • DOI: https://doi.org/10.1007/s12094-018-1982-5

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