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Clinical & Experimental Metastasis

, Volume 35, Issue 5–6, pp 361–367 | Cite as

Cancer initiation and progression within the cancer microenvironment

  • Stanley P. Leong
  • Athena Aktipis
  • Carlo Maley
Review

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.

Keywords

Cancer microenvironment Cancer evolution Natural selection Cancer ecology 

References

  1. 1.
    Darwin C (1859) The origin of species. John Murray, LondonGoogle Scholar
  2. 2.
    Watson JD, Crick FH (1953) Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171:737–738CrossRefGoogle Scholar
  3. 3.
    Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674PubMedPubMedCentralGoogle Scholar
  4. 4.
    Hanahan D, Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21:309–322CrossRefGoogle Scholar
  5. 5.
    Maman S, Witz IP (2018) A history of exploring cancer in context. Nat Rev Cancer 18:359–376CrossRefGoogle Scholar
  6. 6.
    Hellman S (1997) Darwin’s clinical relevance. Cancer 79:2275–2281CrossRefGoogle Scholar
  7. 7.
    Watson JD (1996) Introduction to the Jean Mitchell Watson Lecture. University of Chicago, Chicago, 23 April 1996Google Scholar
  8. 8.
    Greaves M (2000) Cancer: the evolutionary legacy. Oxford University Press, New YorkGoogle Scholar
  9. 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 31:311–325CrossRefGoogle Scholar
  10. 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 17:135–147CrossRefGoogle Scholar
  11. 11.
    Tao L, Huang G, Song H et al (2017) Cancer associated fibroblasts: an essential role in the tumor microenvironment. Oncol Lett 14:2611–2620CrossRefGoogle Scholar
  12. 12.
    Whatcott CJ, Diep CH, Jiang P et al (2015) Desmoplasia in primary tumors and metastatic lesions of pancreatic cancer. Clin Cancer Res 21:3561–3568CrossRefGoogle Scholar
  13. 13.
    Nikitovic D, Tzardi M, Berdiaki A et al (2015) Cancer microenvironment and inflammation: role of hyaluronan. Front Immunol 6:169CrossRefGoogle Scholar
  14. 14.
    Toole BP (2004) Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer 4:528–539CrossRefGoogle Scholar
  15. 15.
    DuFort CC, DelGiorno KE, Hingorani SR (2016) Mounting pressure in the microenvironment: fluids, solids, and cells in pancreatic ductal adenocarcinoma. Gastroenterology 150:1545–1557CrossRefGoogle Scholar
  16. 16.
    Singha NC, Nekoroski T, Zhao C et al (2015) Tumor-associated hyaluronan limits efficacy of monoclonal antibody therapy. Mol Cancer Ther 14:523–532CrossRefGoogle Scholar
  17. 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 116:93–101CrossRefGoogle Scholar
  18. 18.
    Hearing VJ, Leong SP (2006) From melanocytes to melanoma; the progression to malignancy. Humana Press, TotowaCrossRefGoogle Scholar
  19. 19.
    Miller AJ, Mihm MC Jr (2006) Melanoma. N Engl J Med 355:51–65CrossRefGoogle Scholar
  20. 20.
    Uong A, Zon LI (2010) Melanocytes in development and cancer. J Cell Physiol 222:38–41CrossRefGoogle Scholar
  21. 21.
    Testa U, Castelli G, Pelosi E (2017) Melanoma: genetic abnormalities, tumor progression, clonal evolution and tumor initiating cells. Med Sci (Basel) 5:28Google Scholar
  22. 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)CrossRefGoogle Scholar
  23. 23.
    Elias EG, Hasskamp JH, Sharma BK (2010) Cytokines and growth factors expressed by human cutaneous melanoma. Cancers (Basel) 2:794–808CrossRefGoogle Scholar
  24. 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 109:1010–1017CrossRefGoogle Scholar
  25. 25.
    Karaman S, Detmar M (2014) Mechanisms of lymphatic metastasis. J Clin Invest 124:922–928CrossRefGoogle Scholar
  26. 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 359:1403–1407CrossRefGoogle Scholar
  27. 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 359:1408–1411CrossRefGoogle Scholar
  28. 28.
    Cady B (1984) Lymph node metastases. Indicators, but not governors of survival. Arch Surg 119:1067–1072CrossRefGoogle Scholar
  29. 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 29:699–706CrossRefGoogle Scholar
  30. 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)CrossRefGoogle Scholar
  31. 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)PubMedPubMedCentralGoogle Scholar
  32. 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 34:345–350CrossRefGoogle Scholar
  33. 33.
    Pardoll DM (2012) The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12:252–264CrossRefGoogle Scholar
  34. 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 printGoogle Scholar
  35. 35.
    Smith JM, Szathmáry, E (1997) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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) 5:266–275CrossRefGoogle Scholar
  38. 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 135–176Google Scholar
  39. 39.
    Aceto N, Bardia A, Miyamoto DT et al (2014) Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158:1110–1122CrossRefGoogle Scholar
  40. 40.
    Maley CC, Aktipis A, Graham TA et al (2017) Classifying the evolutionary and ecological features of neoplasms. Nat Rev Cancer 17:605–619CrossRefGoogle Scholar
  41. 41.
    Lloyd MC, Rejniak KA, Brown JS et al (2015) Pathology to enhance precision medicine in oncology: lessons from landscape ecology. Adv Anat Pathol 22:267–272CrossRefGoogle Scholar
  42. 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 17:131CrossRefGoogle Scholar
  43. 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 28:373–382CrossRefGoogle Scholar
  44. 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 8:327ra326CrossRefGoogle Scholar
  45. 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 313:1960–1964CrossRefGoogle Scholar
  46. 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 102:18538–18543CrossRefGoogle Scholar
  47. 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 31:860–867CrossRefGoogle Scholar
  48. 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 32:2959–2966CrossRefGoogle Scholar
  49. 49.
    Motz GT, Coukos G (2013) Deciphering and reversing tumor immune suppression. Immunity 39:61–73CrossRefGoogle Scholar
  50. 50.
    Galon J, Angell HK, Bedognetti D, Marincola FM (2013) The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 39:11–26CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Stanley P. Leong
    • 1
  • Athena Aktipis
    • 2
  • Carlo Maley
    • 2
  1. 1.Department of Surgery and Melanoma CenterCalifornia Pacific Medical Center and Research InstituteSan FranciscoUSA
  2. 2.Arizona Cancer and Evolution Center, Biodesign InstituteArizona State UniversityTempeUSA

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