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Cancer initiation and progression within the cancer microenvironment

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Abstract

Within the cancer microenvironment, the growth and proliferation of cancer cells in the primary site as well as in the metastatic site represent a global biological phenomenon. To understand the growth, proliferation and progression of cancer either by local expansion and/or metastasis, it is important to understand the cancer microenvironment and host response to cancer growth. Melanoma is an excellent model to study the interaction of cancer initiation and growth in relationship to its microenvironment. Social evolution with cooperative cellular groups within an organism is what gives rise to multicellularity in the first place. Cancer cells evolve to exploit their cellular environment. The foundations of multicellular cooperation break down in cancer because those cells that misbehave have an evolutionary advantage over their normally behaving neighbors. It is important to classify evolutionary and ecological aspects of cancer growth, thus, data for cancer growth and outcomes need to be collected to define these parameters so that accurate predictions of how cancer cells may proliferate and metastasize can be developed.

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References

  1. Darwin C (1859) The origin of species. John Murray, London

    Google Scholar 

  2. Watson JD, Crick FH (1953) Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171:737–738

    Article  CAS  PubMed  Google Scholar 

  3. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    CAS  PubMed  Google Scholar 

  4. Hanahan D, Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21:309–322

    Article  CAS  PubMed  Google Scholar 

  5. Maman S, Witz IP (2018) A history of exploring cancer in context. Nat Rev Cancer 18:359–376

    Article  CAS  PubMed  Google Scholar 

  6. Hellman S (1997) Darwin’s clinical relevance. Cancer 79:2275–2281

    Article  CAS  PubMed  Google Scholar 

  7. Watson JD (1996) Introduction to the Jean Mitchell Watson Lecture. University of Chicago, Chicago, 23 April 1996

  8. Greaves M (2000) Cancer: the evolutionary legacy. Oxford University Press, New York

    Google Scholar 

  9. Anderson KG, Stromnes IM, Greenberg PD (2017) Obstacles posed by the tumor microenvironment to T cell activity: a case for synergistic therapies. Cancer Cell 31:311–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Erez N, Truitt M, Olson P et al (2010) Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 17:135–147

    Article  CAS  PubMed  Google Scholar 

  11. Tao L, Huang G, Song H et al (2017) Cancer associated fibroblasts: an essential role in the tumor microenvironment. Oncol Lett 14:2611–2620

    Article  PubMed  PubMed Central  Google Scholar 

  12. Whatcott CJ, Diep CH, Jiang P et al (2015) Desmoplasia in primary tumors and metastatic lesions of pancreatic cancer. Clin Cancer Res 21:3561–3568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Nikitovic D, Tzardi M, Berdiaki A et al (2015) Cancer microenvironment and inflammation: role of hyaluronan. Front Immunol 6:169

    Article  PubMed  PubMed Central  Google Scholar 

  14. Toole BP (2004) Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 4:528–539

    Article  CAS  PubMed  Google Scholar 

  15. DuFort CC, DelGiorno KE, Hingorani SR (2016) Mounting pressure in the microenvironment: fluids, solids, and cells in pancreatic ductal adenocarcinoma. Gastroenterology 150:1545–1557

    Article  PubMed  Google Scholar 

  16. Singha NC, Nekoroski T, Zhao C et al (2015) Tumor-associated hyaluronan limits efficacy of monoclonal antibody therapy. Mol Cancer Ther 14:523–532

    Article  CAS  PubMed  Google Scholar 

  17. Ahrens T, Assmann V, Fieber C et al (2001) CD44 is the principal mediator of hyaluronic-acid-induced melanoma cell proliferation. J Invest Dermatol 116:93–101

    Article  CAS  PubMed  Google Scholar 

  18. Hearing VJ, Leong SP (2006) From melanocytes to melanoma; the progression to malignancy. Humana Press, Totowa

    Book  Google Scholar 

  19. Miller AJ, Mihm MC Jr (2006) Melanoma. N Engl J Med 355:51–65

    Article  CAS  PubMed  Google Scholar 

  20. Uong A, Zon LI (2010) Melanocytes in development and cancer. J Cell Physiol 222:38–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Testa U, Castelli G, Pelosi E (2017) Melanoma: genetic abnormalities, tumor progression, clonal evolution and tumor initiating cells. Med Sci (Basel) 5:28

    Google Scholar 

  22. Rigel DS, Carucci JA (2000) Malignant melanoma: prevention, early detection, and treatment in the 21st century. CA Cancer J Clin 50:215–236 (quiz 237–240)

    Article  CAS  PubMed  Google Scholar 

  23. Elias EG, Hasskamp JH, Sharma BK (2010) Cytokines and growth factors expressed by human cutaneous melanoma. Cancers (Basel) 2:794–808

    Article  CAS  Google Scholar 

  24. Hirakawa S, Brown LF, Kodama S et al (2007) VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109:1010–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Karaman S, Detmar M (2014) Mechanisms of lymphatic metastasis. J Clin Invest 124:922–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pereira ER, Kedrin D, Seano G et al (2018) Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science 359:1403–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Brown M, Assen FP, Leithner A et al (2018) Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science 359:1408–1411

    Article  CAS  PubMed  Google Scholar 

  28. Cady B (1984) Lymph node metastases. Indicators, but not governors of survival. Arch Surg 119:1067–1072

    Article  CAS  PubMed  Google Scholar 

  29. Morton DL (2012) Overview and update of the phase III Multicenter Selective Lymphadenectomy Trials (MSLT-I and MSLT-II) in melanoma. Clin Exp Metastasis 29:699–706

    Article  PubMed  PubMed Central  Google Scholar 

  30. Giuliano AE, Dale PS, Turner RR et al (1995) Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg 222:394–399 (discussion 399–401)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Morton DL, Hoon DS, Cochran AJ et al (2003) Lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: therapeutic utility and implications of nodal microanatomy and molecular staging for improving the accuracy of detection of nodal micrometastases. Ann Surg 238:538–549 (discussion 549–550)

    PubMed  PubMed Central  Google Scholar 

  32. Rios-Cantu A, Lu Y, Melendez-Elizondo V et al (2017) Is the non-sentinel lymph node compartment the next site for melanoma progression from the sentinel lymph node compartment in the regional nodal basin? Clin Exp Metastasis 34:345–350

    Article  PubMed  PubMed Central  Google Scholar 

  33. Pardoll DM (2012) The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12:252–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Swe T, Kim K (2018) Update on systemic therapy for advanced cutaneous melanoma and recent development of novel drugs. Clin Exp Metastasis, Epub ahead of print

  35. Smith JM, Szathmáry, E (1997) The major transitions in evolution. Oxford University Press, Oxford

    Google Scholar 

  36. Aktipis CA, Boddy AM, Jansen G et al (2015) Cancer across the tree of life: cooperation and cheating in multicellularity. Philos Trans R Soc Lond B. https://doi.org/10.1098/rstb.2014.0219.

    Article  Google Scholar 

  37. Aktipis CA, Maley CC, Pepper JW (2012) Dispersal evolution in neoplasms: the role of disregulated metabolism in the evolution of cell motility. Cancer Prev Res (Philadelphia) 5:266–275

    Article  Google Scholar 

  38. Schiffman JD, White RM, Graham TA, Huang Q, Aktipis CA (2016) The Darwinian dynamics of motility and metastasis. Frontiers in cancer research. Springer, New York, pp 135–176

    Google Scholar 

  39. Aceto N, Bardia A, Miyamoto DT et al (2014) Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158:1110–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Maley CC, Aktipis A, Graham TA et al (2017) Classifying the evolutionary and ecological features of neoplasms. Nat Rev Cancer 17:605–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lloyd MC, Rejniak KA, Brown JS et al (2015) Pathology to enhance precision medicine in oncology: lessons from landscape ecology. Adv Anat Pathol 22:267–272

    Article  PubMed  PubMed Central  Google Scholar 

  42. Maley CC, Koelble K, Natrajan R et al (2015) An ecological measure of immune-cancer colocalization as a prognostic factor for breast cancer. Breast Cancer Res 17:131

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kirilovsky A, Marliot F, El Sissy C et al (2016) Rational bases for the use of the Immunoscore in routine clinical settings as a prognostic and predictive biomarker in cancer patients. Int Immunol 28:373–382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mlecnik B, Bindea G, Kirilovsky A et al (2016) The tumor microenvironment and Immunoscore are critical determinants of dissemination to distant metastasis. Sci Transl Med 8:327ra326

    Article  Google Scholar 

  45. Galon J, Costes A, Sanchez-Cabo F et al (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:1960–1964

    Article  CAS  PubMed  Google Scholar 

  46. Sato E, Olson SH, Ahn J et al (2005) Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 102:18538–18543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Loi S, Sirtaine N, Piette F et al (2013) Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02–98. J Clin Oncol 31:860–867

    Article  CAS  PubMed  Google Scholar 

  48. Adams S, Gray RJ, Demaria S et al (2014) Prognostic value of tumor-infiltrating lymphocytes in triple-negative breast cancers from two phase III randomized adjuvant breast cancer trials: ECOG 2197 and ECOG 1199. J Clin Oncol 32:2959–2966

    Article  PubMed  PubMed Central  Google Scholar 

  49. Motz GT, Coukos G (2013) Deciphering and reversing tumor immune suppression. Immunity 39:61–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Galon J, Angell HK, Bedognetti D, Marincola FM (2013) The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 39:11–26

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Surgery and Melanoma Center, California Pacific Medical Center and Research Institute, San Francisco, USA

    Stanley P. Leong

  2. Arizona Cancer and Evolution Center, Biodesign Institute, Arizona State University, Tempe, USA

    Athena Aktipis & Carlo Maley

Authors
  1. Stanley P. Leong
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  2. Athena Aktipis
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  3. Carlo Maley
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Correspondence to Stanley P. Leong.

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Leong, S.P., Aktipis, A. & Maley, C. Cancer initiation and progression within the cancer microenvironment. Clin Exp Metastasis 35, 361–367 (2018). https://doi.org/10.1007/s10585-018-9921-y

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  • DOI: https://doi.org/10.1007/s10585-018-9921-y

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