Minimal residual disease in solid neoplasia: New frontier or red-herring?

Cancer Treatment Reviews

Volumn 38, Issue 2, 2012, Pages 101-110

  Mordant, Pierre ^a,b   Loriot, Yohann ^a,c   Lahon, Benoît ^a,b   Castier, Yves ^b   Lesèche, Guy ^b   Soria, Jean Charles ^c   Massard, Christophe ^c   Deutsch, Eric ^a,c  

^a Institut Gustave Roussy   (France)

^b BICHAT HOSPITAL   (France)

^c INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Cancer stem cells; Circulating tumor cells; Disseminated tumor cells micrometastasis; Minimal residual disease

Indexed keywords

ALDEHYDE DEHYDROGENASE; BETA CATENIN; BIOLOGICAL MARKER; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HERMES ANTIGEN; K RAS PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; STEM CELL FACTOR RECEPTOR; THROMBOSPONDIN; UROKINASE RECEPTOR; VASCULOTROPIN;

ADVANCED CANCER; BLOOD FLOW; BREAST CANCER; CANCER STEM CELL; CELL SURVIVAL; CIRCULATING TUMOR CELL; COLORECTAL CANCER; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE MUTATION; HUMAN; LUNG CANCER; MICROMETASTASIS; MINIMAL RESIDUAL DISEASE; NONHUMAN; PRIMARY TUMOR; REVIEW; SOLID TUMOR; TUMOR MICROENVIRONMENT;

FEMALE; HUMANS; MALE; NEOPLASM, RESIDUAL; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; NEOPLASTIC STEM CELLS;

EID: 84856327694     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2011.04.014     Document Type: Review

References (107)

1. zur Hausen H. Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 2000, 92(9):690-698.
2. Morrison R., Schleicher S.M., Sun Y., et al. Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J Oncol 2011, 1:941876.
3. Kort E.J., Paneth N., Vande Woude G.F. The decline in US cancer mortality in people born since 1925. Cancer Res 2009, 69(16):6500-6505.
4. Altekruse SF, Kosary CL, Krapcho M, Neyman N, Aminou R, Waldron W, et al., editors. SEER Cancer Statistics Review, 1975-2007. Bethesda, MD: National Cancer Institute; 2010. based on November 2009 SEER data submission, posted to the SEER web site. http://seer.cancer.gov/csr/1975_2007/.
5. Coghlin C., Murray G.I. Current and emerging concepts in tumour metastasis. J Pathol 2010, 222(1):1-15.
6. Massard C., Deutsch E., Soria J.C. Tumour stem cell-targeted treatment: elimination or differentiation. Ann Oncol 2006, 17(11):1620-1624.
7. Lapidot T., Sirard C., Vormoor J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367(6464):645-648.
8. Singh S.K., Clarke I.D., Terasaki M., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003, 63(18):5821-5828.
9. Suva M.L., Riggi N., Janiszewska M., et al. EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res 2009, 69(24):9211-9218.
10. Todaro M., Alea M.P., Di Stefano A.B., et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007, 1(4):389-402.
11. Storms R.W., Trujillo A.P., Springer J.B., et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci USA 1999, 96(16):9118-9123.
12. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8(10):755-768.
13. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100(7):3983-3988.
14. Singh S.K., Hawkins C., Clarke I.D., et al. Identification of human brain tumour initiating cells. Nature 2004, 432(7015):396-401.
15. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445(7123):106-110.
16. Lang S.H., Frame F.M., Collins A.T. Prostate cancer stem cells. J Pathol 2009, 217(2):299-306.
17. Prince M.E., Sivanandan R., Kaczorowski A., et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007, 104(3):973-978.
18. Hermann P.C., Huber S.L., Herrler T., et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1(3):313-323.
19. Eramo A., Lotti F., Sette G., et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008, 15(3):504-514.
20. Yang Z.F., Ho D.W., Ng M.N., et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008, 13(2):153-166.
21. Schatton T., Murphy G.F., Frank N.Y., et al. Identification of cells initiating human melanomas. Nature 2008, 451(7176):345-349.
22. Komuro H., Saihara R., Shinya M., et al. Identification of side population cells (stem-like cell population) in pediatric solid tumor cell lines. J Pediatr Surg 2007, 42(12):2040-2045.
23. Levina V., Marrangoni A.M., DeMarco R., Gorelik E., Lokshin A.E. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS One 2008, 3(8):e3077.
24. Yu F., Yao H., Zhu P., et al. Let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007, 131(6):1109-1123.
25. Li H.Z., Yi T.B., Wu Z.Y. Suspension culture combined with chemotherapeutic agents for sorting of breast cancer stem cells. BMC Cancer 2008, 8:135.
26. Calcagno A.M., Salcido C.D., Gillet J.P., et al. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. J Natl Cancer Inst 2010, 102(21):1637-1652.
27. Ho M.M., Ng A.V., Lam S., Hung J.Y. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007, 67(10):4827-4833.
28. Di Fiore R., Santulli A., Ferrante R.D., et al. Identification and expansion of human osteosarcoma-cancer-stem cells by long-term 3-aminobenzamide treatment. J Cell Physiol 2009, 219(2):301-313.
29. Ma L., Lai D., Liu T., Cheng W., Guo L. Cancer stem-like cells can be isolated with drug selection in human ovarian cancer cell line SKOV3. Acta Biochim Biophys Sin (Shanghai) 2010, 42(9):593-602.
30. Dessein A.F., Stechly L., Jonckheere N., et al. Autocrine induction of invasive and metastatic phenotypes by the MIF-CXCR4 axis in drug-resistant human colon cancer cells. Cancer Res 2010, 70(11):4644-4654.
31. Chauchereau A., Al Nakouzi N., Gaudin C., et al. Stemness markers characterize IGR-CaP1, a new cell line derived from primary epithelial prostate cancer. Exp Cell Res 2011, 317(3):262-275.
32. Dylla S.J., Beviglia L., Park I.K., et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 2008, 3(6):e2428.
33. Bradshaw D.M., Arceci R.J. Clinical relevance of transmembrane drug efflux as a mechanism of multidrug resistance. J Clin Oncol 1998, 16(11):3674-3690.
34. Covello K.L., Kehler J., Yu H., et al. HIF-2alpha regulates oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 2006, 20(5):557-570.
35. Gordan J.D., Bertout J.A., Hu C.J., Diehl J.A., Simon M.C. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007, 11(4):335-347.
36. Baumann M., Krause M., Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 2008, 8(7):545-554.
37. Bao S., Wu Q., McLendon R.E., et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444(7120):756-760.
38. Krause M., Zips D., Thames H.D., Kummermehr J., Baumann M. Preclinical evaluation of molecular-targeted anticancer agents for radiotherapy. Radiother Oncol 2006, 80(2):112-122.
39. Almog N. Molecular mechanisms underlying tumor dormancy. Cancer Lett 2010, 294(2):139-146.
40. Black W.C., Welch H.G. Advances in diagnostic imaging and overestimations of disease prevalence and the benefits of therapy. N Engl J Med 1993, 328(17):1237-1243.
41. Harach H.R., Franssila K.O., Wasenius V.M. Occult papillary carcinoma of the thyroid. A " normal" finding in finland. A systematic autopsy study. Cancer 1985, 56(3):531-538.
42. Nielsen M., Thomsen J.L., Primdahl S., Dyreborg U., Andersen J.A. Breast cancer and atypia among young and middle-aged women: a study of 110 medicolegal autopsies. Br J Cancer 1987, 56(6):814-819.
43. Haas G.P., Delongchamps N., Brawley O.W., Wang C.Y., de la Roza G. The worldwide epidemiology of prostate cancer: perspectives from autopsy studies. Can J Urol 2008, 15(1):3866-3871.
44. Almog N., Henke V., Flores L., et al. Prolonged dormancy of human liposarcoma is associated with impaired tumor angiogenesis. FASEB J 2006, 20(7):947-949.
45. Ranganathan A.C., Adam A.P., Aguirre-Ghiso J.A. Opposing roles of mitogenic and stress signaling pathways in the induction of cancer dormancy. Cell Cycle 2006, 5(16):1799-1807.
46. Quesnel B. Tumor dormancy and immunoescape. APMIS 2008, 116(7-8):685-694.
47. Almog N., Ma L., Raychowdhury R., et al. Transcriptional switch of dormant tumors to fast-growing angiogenic phenotype. Cancer Res 2009, 69(3):836-844.
48. Troyanovsky B., Levchenko T., Mansson G., Matvijenko O., Holmgren L. Angiomotin: an angiostatin binding protein that regulates endothelial cell migration and tube formation. J Cell Biol 2001, 152(6):1247-1254.
49. Goss P., Allan A.L., Rodenhiser D.I., Foster P.J., Chambers A.F. New clinical and experimental approaches for studying tumor dormancy: does tumor dormancy offer a therapeutic target?. APMIS 2008, 116(7-8):552-568.
50. Kusumbe A.P., Bapat S.A. Cancer stem cells and aneuploid populations within developing tumors are the major determinants of tumor dormancy. Cancer Res 2009, 69(24):9245-9253.
51. Eccles S.A., Welch D.R. Metastasis: recent discoveries and novel treatment strategies. Lancet 2007, 369(9574):1742-1757.
52. Pantel K., Cote R.J., Fodstad O. Detection and clinical importance of micrometastatic disease. J Natl Cancer Inst 1999, 91(13):1113-1124.
53. Allard W.J., Matera J., Miller M.C., et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res 2004, 10(20):6897-6904.
54. Rolle A., Gunzel R., Pachmann U., Willen B., Hoffken K., Pachmann K. Increase in number of circulating disseminated epithelial cells after surgery for non-small cell lung cancer monitored by MAINTRAC(R) is a predictor for relapse: a preliminary report. World J Surg Oncol 2005, 3(1):18.
55. Nagrath S., Sequist L.V., Maheswaran S., et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 2007, 450(7173):1235-1239.
56. Pinzani P., Salvadori B., Simi L., et al. Isolation by size of epithelial tumor cells in peripheral blood of patients with breast cancer: correlation with real-time reverse transcriptase-polymerase chain reaction results and feasibility of molecular analysis by laser microdissection. Hum Pathol 2006, 37(6):711-718.
57. Ge M., Shi D., Wu Q., Wang M., Li L. Fluctuation of circulating tumor cells in patients with lung cancer by real-time fluorescent quantitative-PCR approach before and after radiotherapy. J Cancer Res Ther 2005, 1(4):221-226.
58. Bremnes R.M., Sirera R., Camps C. Circulating tumour-derived DNA and RNA markers in blood: a tool for early detection, diagnostics, and follow-up?. Lung Cancer 2005, 49(1):1-12.
59. Van der Auwera I., Peeters D., Benoy I.H., et al. Circulating tumour cell detection: a direct comparison between the CellSearch system, the AdnaTest and CK-19/mammaglobin RT-PCR in patients with metastatic breast cancer. Br J Cancer 2010, 102(2):276-284.
60. Gervasoni A., Monasterio Munoz R.M., Wengler G.S., Rizzi A., Zaniboni A., Parolini O. Molecular signature detection of circulating tumor cells using a panel of selected genes. Cancer Lett 2008, 263(2):267-279.
61. Sieuwerts A.M., Kraan J., Bolt-de Vries J., et al. Molecular characterization of circulating tumor cells in large quantities of contaminating leukocytes by a multiplex real-time PCR. Breast Cancer Res Treat 2009, 118(3):455-468.
62. Bidard F.C., Vincent-Salomon A., Sigal-Zafrani B., et al. Prognosis of women with stage IV breast cancer depends on detection of circulating tumor cells rather than disseminated tumor cells. Ann Oncol 2008, 19(3):496-500.
63. Cohen S.J., Punt C.J., Iannotti N., et al. Prognostic significance of circulating tumor cells in patients with metastatic colorectal cancer. Ann Oncol 2009, 20(7):1223-1229.
64. Coumans F.A., Doggen C.J., Attard G., de Bono J.S., Terstappen L.W. All circulating EpCAM+CK+CD45- objects predict overall survival in castration-resistant prostate cancer. Ann Oncol 2010, 21(9):1851-1857.
65. Fehm T., Sagalowsky A., Clifford E., et al. Cytogenetic evidence that circulating epithelial cells in patients with carcinoma are malignant. Clin Cancer Res 2002, 8(7):2073-2084.
66. Maheswaran S., Sequist L.V., Nagrath S., et al. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 2008, 359(4):366-377.
67. Ameri K., Luong R., Zhang H., et al. Circulating tumour cells demonstrate an altered response to hypoxia and an aggressive phenotype. Br J Cancer 2010, 102(3):561-569.
68. Ignatiadis M., Kallergi G., Ntoulia M., et al. Prognostic value of the molecular detection of circulating tumor cells using a multimarker reverse transcription-PCR assay for cytokeratin 19, mammaglobin A, and HER2 in early breast cancer. Clin Cancer Res 2008, 14(9):2593-2600.
69. Lang J.E., Mosalpuria K., Cristofanilli M., et al. HER2 status predicts the presence of circulating tumor cells in patients with operable breast cancer. Breast Cancer Res Treat 2009, 113(3):501-507.
70. Munzone E., Nole F., Goldhirsch A., et al. Changes of HER2 status in circulating tumor cells compared with the primary tumor during treatment for advanced breast cancer. Clin Breast Cancer 2010, 10(5):392-397.
71. Chen Y.F., Wang J.Y., Wu C.H., Chen F.M., Cheng T.L., Lin S.R. Detection of circulating cancer cells with K-ras oncogene using membrane array. Cancer Lett 2005, 229(1):115-122.
72. Helzer K.T., Barnes H.E., Day L., Harvey J., Billings P.R., Forsyth A. Circulating tumor cells are transcriptionally similar to the primary tumor in a murine prostate model. Cancer Res 2009, 69(19):7860-7866.
73. Paci M., Maramotti S., Bellesia E., et al. Circulating plasma DNA as diagnostic biomarker in non-small cell lung cancer. Lung cancer 2009, 64(1):92-97.
74. Okumura Y., Tanaka F., Yoneda K., et al. Circulating tumor cells in pulmonary venous blood of primary lung cancer patients. Ann Thorac Surg 2009, 87(6):1669-1675.
75. Chen T.F., Jiang G.L., Fu X.L., et al. CK19 mRNA expression measured by reverse-transcription polymerase chain reaction (RT-PCR) in the peripheral blood of patients with non-small cell lung cancer treated by chemo-radiation: An independent prognostic factor. Lung cancer 2007, 56(1):105-114.
76. Ross J.S., Slodkowska E.A. Circulating and disseminated tumor cells in the management of breast cancer. Am J Clin Pathol 2009, 132(2):237-245.
77. Uen Y.H., Lu C.Y., Tsai H.L., et al. Persistent presence of postoperative circulating tumor cells is a poor prognostic factor for patients with stage I-III colorectal cancer after curative resection. Ann Surg Oncol 2008, 15(8):2120-2128.
78. Papavasiliou P., Fisher T., Kuhn J., Nemunaitis J., Lamont J. Circulating tumor cells in patients undergoing surgery for hepatic metastases from colorectal cancer. Proc (Bayl Univ Med Cent) 2010, 23(1):11-14.
79. Peach G., Kim C., Zacharakis E., Purkayastha S., Ziprin P. Prognostic significance of circulating tumour cells following surgical resection of colorectal cancers: a systematic review. Br J Cancer 2010, 102(9):1327-1334.
80. Tol J., Koopman M., Miller M.C., et al. Circulating tumour cells early predict progression-free and overall survival in advanced colorectal cancer patients treated with chemotherapy and targeted agents. Ann Oncol 2010, 21(5):1006-1012.
81. Scher H.I., Jia X., de Bono J.S., et al. Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: a reanalysis of IMMC38 trial data. Lancet Oncol 2009, 10(3):233-239.
82. Shaffer D.R., Leversha M.A., Danila D.C., et al. Circulating tumor cell analysis in patients with progressive castration-resistant prostate cancer. Clin Cancer Res 2007, 13(7):2023-2029.
83. Attard G., Swennenhuis J.F., Olmos D., et al. Characterization of ERG, AR and PTEN gene status in circulating tumor cells from patients with castration-resistant prostate cancer. Cancer Res 2009, 69(7):2912-2918.
84. Smirnov D.A., Zweitzig D.R., Foulk B.W., et al. Global gene expression profiling of circulating tumor cells. Cancer Res 2005, 65(12):4993-4997.
85. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002, 2(6):442-454.
86. Brabletz T., Jung A., Spaderna S., Hlubek F., Kirchner T. Opinion: Migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 2005, 5(9):744-749.
87. Pierga J.Y., Bonneton C., Vincent-Salomon A., et al. Clinical significance of immunocytochemical detection of tumor cells using digital microscopy in peripheral blood and bone marrow of breast cancer patients. Clin Cancer Res 2004, 10(4):1392-1400.
88. Pantel K., Brakenhoff R.H., Brandt B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 2008, 8(5):329-340.
89. Aguirre-Ghiso J.A. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 2007, 7(11):834-846.
90. Monteiro J., Fodde R. Cancer stemness and metastasis: therapeutic consequences and perspectives. Eur J Cancer 2010, 46(7):1198-1203.
91. Mego M., Mani S.A., Cristofanilli M. Molecular mechanisms of metastasis in breast cancer-clinical applications. Nat Rev Clin Oncol 2010, 7(12):693-701.
92. Aktas B., Tewes M., Fehm T., Hauch S., Kimmig R., Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 2009, 11(4):R46.
93. Reuben J.M., Lee B.N., Li C., et al. Circulating tumor cells and biomarkers: implications for personalized targeted treatments for metastatic breast cancer. Breast J 2010, 16(3):327-330.
94. Armstrong AJ, Oltean S, Marengo M, Chen L, Kemeny G, Herold CI, et al. Plasticity, stemness, and aggressive behavior in preclinical models and circulating prostate cancer cells: importance of the transitional phenotypic state to lethal cancer biology. American Society of Clinical oncology (ASCO) 2010 Genitourinary Cancers Symposium. Abstract 172.
95. Cohen S.J., Punt C.J., Iannotti N., et al. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol 2008, 26(19):3213-3221.
96. Cristofanilli M., Budd G.T., Ellis M.J., et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 2004, 351(8):781-791.
97. de Bono J.S., Scher H.I., Montgomery R.B., et al. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin Cancer Res 2008, 14(19):6302-6309.
98. Hayes D.F., Cristofanilli M., Budd G.T., et al. Circulating tumor cells at each follow-up time point during therapy of metastatic breast cancer patients predict progression-free and overall survival. Clin Cancer Res 2006, 12(14 Pt 1):4218-4224.
99. Danila D.C., Heller G., Gignac G.A., et al. Circulating tumor cell number and prognosis in progressive castration-resistant prostate cancer. Clin Cancer Res 2007, 13(23):7053-7058.
100. Hiraiwa K., Takeuchi H., Hasegawa H., et al. Clinical significance of circulating tumor cells in blood from patients with gastrointestinal cancers. Ann Surg Oncol 2008, 15(11):3092-3100.
101. Sastre J., Maestro M.L., Puente J., et al. Circulating tumor cells in colorectal cancer: correlation with clinical and pathological variables. Ann Oncol 2008, 19(5):935-938.
102. Tomlins S.A., Rhodes D.R., Perner S., et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310(5748):644-648.
103. Kumar-Sinha C., Tomlins S.A., Chinnaiyan A.M. Recurrent gene fusions in prostate cancer. Nat Rev Cancer 2008, 8(7):497-511.
104. Lynch T.J., Bell D.W., Sordella R., et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004, 350(21):2129-2139.
105. Flaherty K.T., Puzanov I., Kim K.B., et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010, 363(9):809-819.
106. Leversha M.A., Han J., Asgari Z., et al. Fluorescence in situ hybridization analysis of circulating tumor cells in metastatic prostate cancer. Clin Cancer Res 2009, 15(6):2091-2097.
107. Attard G., Swennenhuis J.F., Olmos D., et al. Characterization of ERG, AR and PTEN gene status in circulating tumor cells from patients with castration-resistant prostate cancer. Cancer Res 2009, 69(7):2912-2918.