Concepts of metastasis in flux: The stromal progression model

Seminars in Cancer Biology

Volumn 22, Issue 3, 2012, Pages 174-186

  Sleeman, Jonathan P ^a,b   Christofori, Gerhard ^c   Fodde, Riccardo ^d   Collard, John G ^e   Berx, Geert ^f,g   Decraene, Charles ^h,i   Rüegg, Curzio ^j  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^e NETHERLANDS CANCER INSTITUTE   (Netherlands)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g GHENT UNIVERSITY   (Belgium)

^h INSTITUT CURIE   (France)

ⁱ CNRS   (France)

^j University of Fribourg   (Switzerland)

more..

Author keywords

Cancer stem cell; Clonal selection; EMT; Metastasis; Metastatic niche; Microenvironment; Parallel progression; Seed and soil; Stromal progression

Indexed keywords

CALGRANULIN A; CALGRANULIN B; CD11B ANTIGEN; CHEMOKINE RECEPTOR CXCR4; ENDOGLIN; GELATINASE A; GELATINASE B; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1;

CANCER GROWTH; CANCER STEM CELL; CELL DIFFERENTIATION; DISEASE COURSE; EPITHELIAL MESENCHYMAL TRANSITION; METASTASIS; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR MICROENVIRONMENT;

COMPARATIVE GENOMIC HYBRIDIZATION; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMANS; MESENCHYMAL STROMAL CELLS; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC STEM CELLS; TUMOR MICROENVIRONMENT;

EID: 84861199307     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2012.02.007     Document Type: Review

References (183)

1. Weiss L. Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metast Rev 2000, 19(I-XI):193-383.
2. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889, 133:571-573.
3. Ewing J. Neoplastic diseases: a treatise on tumors 1928, Saunders, Philadelphia. 3rd ed.
4. Goldman E.E. Relation of cancer cells to blood vessels and ducts. Lancet 1906, 1:23.
5. Sugarbaker E. Patterns of metastasis in human malignancies. Cancer Biol Rev 1981, 2:235-278.
6. Sleeman J.P. The lymph node as a bridgehead in the metastatic dissemination of tumors. Recent Results Cancer Res 2000, 157:55-81.
7. Sleeman J.P., Nazarenko I., Thiele W. Do all roads lead to Rome? Routes to metastasis development. J Int Cancer 2011, 128:2511-2526.
8. Klein C.A. Parallel progression of primary tumours and metastases. Nat Rev Cancer 2009, 9:302-312.
9. Fidler I.J., Kripke M.L. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977, 197:893-895.
10. Fidler I.J. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003, 3:453-458.
11. Talmadge J.E. Clonal selection of metastasis within the life history of a tumor. Cancer Res 2007, 67:11471-11475.
12. van't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536.
13. van de Vijver M.J., He Y.D., van't Veer L.J., Dai H., Hart A.A., Voskuil D.W., et al. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 2002, 347:1999-2009.
14. Buyse M., Loi S., van't Veer L., Viale G., Delorenzi M., Glas A.M., et al. Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. J Natl Cancer Inst 2006, 98:1183-1192.
15. Sotiriou C., Pusztai L. Gene-expression signatures in breast cancer. N Engl J Med 2009, 360:790-800.
16. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordon-Cardo C., et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549.
17. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., et al. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524.
18. Bos P.D., Zhang X.H., Nadal C., Shu W., Gomis R.R., Nguyen D.X., et al. Genes that mediate breast cancer metastasis to the brain. Nature 2009, 459:1005-1009.
19. 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, 5:744-749.
20. Bernards R., Weinberg R.A. A progression puzzle. Nature 2002, 418:823.
21. Weigelt B., Glas A.M., Wessels L.F., Witteveen A.T., Peterse J.L., van't Veer L.J. Gene expression profiles of primary breast tumors maintained in distant metastases. Proc Natl Acad Sci USA 2003, 100:15901-15905.
22. Stoecklein N.H., Klein C.A. Genetic disparity between primary tumours, disseminated tumour cells, and manifest metastasis. Int J Cancer 2010, 126:589-598.
23. Yachida S., Jones S., Bozic I., Antal T., Leary R., Fu B., et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
24. Norton L., Massague J. Is cancer a disease of self-seeding?. Nat Med 2006, 12:875-878.
25. Kim M.Y., Oskarsson T., Acharyya S., Nguyen D.X., Zhang X.H., Norton L., et al. Tumor self-seeding by circulating cancer cells. Cell 2009, 139:1315-1326.
26. Comen E., Norton L., Massague J. Clinical implications of cancer self-seeding. Nat Rev Clin Oncol 2011, 8:369-377.
27. Comen E.A., Norton L., Massague J. Breast cancer tumor size, nodal status, and prognosis: biology trumps anatomy. J Clin Oncol 2011, 29:2610-2612.
28. Kerbel R.S., Waghorne C., Korczak B., Lagarde A., Breitman M.L. Clonal dominance of primary tumours by metastatic cells: genetic analysis and biological implications. Cancer Surv 1988, 7:597-629.
29. Ling V., Chambers A.F., Harris J.F., Hill R.P. Quantitative genetic analysis of tumor progression. Cancer Metast Rev 1985, 4:173-192.
30. Pantel K., Brakenhoff R.H. Dissecting the metastatic cascade. Nat Rev Cancer 2004, 4:448-456.
31. Ramaswamy S., Ross K.N., Lander E.S., Golub T.R. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003, 33:49-54.
32. Husemann Y., Geigl J.B., Schubert F., Musiani P., Meyer M., Burghart E., et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008, 13:58-68.
33. Israeli R.S., Miller W.H., Su S.L., Powell C.T., Fair W.R., Samadi D.S., et al. Sensitive nested reverse transcription polymerase chain reaction detection of circulating prostatic tumor cells: comparison of prostate-specific membrane antigen and prostate-specific antigen-based assays. Cancer Res 1994, 54:6306-6310.
34. Mori M., Mimori K., Ueo H., Karimine N., Barnard G.F., Sugimachi K., et al. Molecular detection of circulating solid carcinoma cells in the peripheral blood: the concept of early systemic disease. Int J Cancer 1996, 68:739-743.
35. Ennis R.D., Katz A.E., de Vries G.M., Heitjan D.F., O'Toole K.M., Rubin M., et al. Detection of circulating prostate carcinoma cells via an enhanced reverse transcriptase-polymerase chain reaction assay in patients with early stage prostate carcinoma independence from other pretreatment characteristics. Cancer 1997, 79:2402-2408.
36. Melchior S.W., Corey E., Ellis W.J., Ross A.A., Layton T.J., Oswin M.M., et al. Early tumor cell dissemination in patients with clinically localized carcinoma of the prostate. Clin Cancer Res 1997, 3:249-256.
37. Weitz J., Kienle P., Lacroix J., Willeke F., Benner A., Lehnert T., et al. Dissemination of tumor cells in patients undergoing surgery for colorectal cancer. Clin Cancer Res 1998, 4:343-348.
38. Kuukasjarvi T., Karhu R., Tanner M., Kahkonen M., Schaffer A., Nupponen N., et al. Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer. Cancer Res 1997, 57:1597-1604.
39. Torres L., Ribeiro F.R., Pandis N., Andersen J.A., Heim S., Teixeira M.R. Intratumor genomic heterogeneity in breast cancer with clonal divergence between primary carcinomas and lymph node metastases. Breast Cancer Res Treat 2007, 102:143-155.
40. Santos S.C., Cavalli I.J., Ribeiro E.M., Urban C.A., Lima R.S., Bleggi-Torres L.F., et al. Patterns of DNA copy number changes in sentinel lymph node breast cancer metastases. Cytogenet Genome Res 2008, 122:16-21.
41. Lu X., Mu E., Wei Y., Riethdorf S., Yang Q., Yuan M., et al. VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging alpha4beta1-positive osteoclast progenitors. Cancer Cell 2011, 20:701-714.
42. Podsypanina K., Du Y.C., Jechlinger M., Beverly L.J., Hambardzumyan D., Varmus H. Seeding and propagation of untransformed mouse mammary cells in the lung. Science 2008, 321:1841-1844.
43. Ansieau S., Bastid J., Doreau A., Morel A.P., Bouchet B.P., Thomas C., et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008, 14:79-89.
44. Jones S., Chen W.D., Parmigiani G., Diehl F., Beerenwinkel N., Antal T., et al. Comparative lesion sequencing provides insights into tumor evolution. Proc Natl Acad Sci USA 2008, 105:4283-4288.
45. Gonzaga-Jauregui C., Lupski J.R., Gibbs R.A. Human genome sequencing in health and disease. Annu Rev Med 2012, 63:35-61.
46. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8:755-768.
47. Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
48. Dalerba P., Dylla S.J., Park I.K., Liu R., Wang X., Cho R.W., et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007, 104:10158-10163.
49. Huang C.Y., Lee C.Y., Chen M.Y., Yang W.H., Chen Y.H., Chang C.H., et al. Stromal cell-derived factor-1/CXCR4 enhanced motility of human osteosarcoma cells involves MEK1/2 ERK and NF-kappaB-dependent pathways. J Cell Physiol 2009, 221:204-212.
50. 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, 445:106-110.
51. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
52. Vermeulen L., De Sousa E.M.F., van der Heijden M., Cameron K., de Jong J.H., Borovski T., et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010, 12:468-476.
53. Dieter S.M., Ball C.R., Hoffmann C.M., Nowrouzi A., Herbst F., Zavidij O., et al. Distinct types of tumor-initiating cells form human colon cancer tumors and metastases. Cell Stem Cell 2011, 9:357-365.
54. + cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010, 6:603-615.
55. Tang D.G. Understanding cancer stem cell heterogeneity and plasticity. Cell Res 2012, 10.1038/cr.2012.13.
56. Chaffer C.L., Brueckmann I., Scheel C., Kaestli A.J., Wiggins P.A., Rodrigues L.O., et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci USA 2011, 108:7950-7955.
57. Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644.
58. Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11:69-82.
59. Beck B., Driessens G., Goossens S., Youssef K.K., Kuchnio A., Caauwe A., et al. A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 2011, 478:399-403.
60. Borovski T., De Sousa E.M.F., Vermeulen L., Medema J.P. Cancer stem cell niche: the place to be. Cancer Res 2011, 71:634-639.
61. Charles N., Ozawa T., Squatrito M., Bleau A.M., Brennan C.W., Hambardzumyan D., et al. Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010, 6:141-152.
62. Aguirre-Ghiso J.A. Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 2007, 7:834-846.
63. Morgan T.M., Lange P.H., Porter M.P., Lin D.W., Ellis W.J., Gallaher I.S., et al. Disseminated tumor cells in prostate cancer patients after radical prostatectomy and without evidence of disease predicts biochemical recurrence. Clin Cancer Res 2009, 15:677-683.
64. Horak C.E., Lee J.H., Marshall J.C., Shreeve S.M., Steeg P.S. The role of metastasis suppressor genes in metastatic dormancy. APMIS 2008, 116:586-601.
65. Barkan D., El Touny L.H., Michalowski A.M., Smith J.A., Chu I., Davis A.S., et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res 2010, 70:5706-5716.
66. Eyles J., Puaux A.L., Wang X., Toh B., Prakash C., Hong M., et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 2010, 120:2030-2039.
67. McAllister S.S., Gifford A.M., Greiner A.L., Kelleher S.P., Saelzler M.P., Ince T.A., et al. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 2008, 133:994-1005.
68. Naumov G.N., Townson J.L., MacDonald I.C., Wilson S.M., Bramwell V.H., Groom A.C., et al. Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases. Breast Cancer Res Treat 2003, 82:199-206.
69. Knutsen T., Mickley L.A., Ried T., Green E.D., du Manoir S., Schrock E., et al. Cytogenetic and molecular characterization of random chromosomal rearrangements activating the drug resistance gene MDR1/P-glycoprotein, in drug-selected cell lines and patients with drug refractory ALL. Genes Chromosomes Cancer 1998, 23:44-54.
70. Mickley L.A., Spengler B.A., Knutsen T.A., Biedler J.L., Fojo T. Gene rearrangement: a novel mechanism for MDR-1 gene activation. J Clin Invest 1997, 99:1947-1957.
71. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
72. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783.
73. Kienast Y., von Baumgarten L., Fuhrmann M., Klinkert W.E., Goldbrunner R., Herms J., et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med 2010, 16:116-122.
74. Nguyen D.X., Massague J. Genetic determinants of cancer metastasis. Nat Rev Genet 2007, 8:341-352.
75. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
76. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
77. Sarrio D., Rodriguez-Pinilla S.M., Hardisson D., Cano A., Moreno-Bueno G., Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008, 68:989-997.
78. Tarin D., Thompson E.W., Newgreen D.F. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 2005, 65:5996-6000. [discussion 6000-5991].
79. Cavallaro U., Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 2004, 4:118-132.
80. Onder T.T., Gupta P.B., Mani S.A., Yang J., Lander E.S., Weinberg R.A. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008, 68:3645-3654.
81. Perl A.K., Wilgenbus P., Dahl U., Semb H., Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998, 392:190-193.
82. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7:131-142.
83. Christofori G. New signals from the invasive front. Nature 2006, 441:444-450.
84. Berx G., Raspe E., Christofori G., Thiery J.P., Sleeman J.P. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer. Clin Exp Metast 2007, 24:587-597.
85. Yilmaz M., Maass D., Tiwari N., Waldmeier L., Schmidt P., Lehembre F., et al. Transcription factor Dlx2 protects from TGFbeta-induced cell-cycle arrest and apoptosis. EMBO J 2011, 30:4489-4499.
86. Brabletz S., Brabletz T. The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer?. EMBO Rep 2010, 11:670-677.
87. Ma L., Young J., Prabhala H., Pan E., Mestdagh P., Muth D., et al. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010, 12:247-256.
88. Nicoloso M.S., Spizzo R., Shimizu M., Rossi S., Calin G.A. MicroRNAs-the micro steering wheel of tumour metastases. Nat Rev Cancer 2009, 9:293-302.
89. McDonald O.G., Wu H., Timp W., Doi A., Feinberg A.P. Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition. Nat Struct Mol Biol 2011, 18:867-874.
90. Davalos V., Moutinho C., Villanueva A., Boque R., Silva P., Carneiro F., et al. Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 2011.
91. Ellenbroek S.I., Iden S., Collard J.G. Cell polarity proteins and cancer. Semin Cancer Biol 2012, 22:208-215.
92. Wang X., Nie J., Zhou Q., Liu W., Zhu F., Chen W., et al. Downregulation of Par-3 expression and disruption of Par complex integrity by TGF-beta during the process of epithelial to mesenchymal transition in rat proximal epithelial cells. Biochim Biophys Acta 2008, 1782:51-59.
93. Viloria-Petit A.M., David L., Jia J.Y., Erdemir T., Bane A.L., Pinnaduwage D., et al. A role for the TGFbeta-Par6 polarity pathway in breast cancer progression. Proc Natl Acad Sci USA 2009, 106:14028-14033.
94. Peinado H., Olmeda D., Cano A. Snail Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat Rev Cancer 2007, 7:415-428.
95. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1420-1428.
96. Savagner P. The epithelial-mesenchymal transition (EMT) phenomenon. Ann Oncol 2010, 21(Suppl. 7):vii89-vii92.
97. Lee J.M., Dedhar S., Kalluri R., Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006, 172:973-981.
98. Jo M., Lester R.D., Montel V., Eastman B., Takimoto S., Gonias S.L. Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling. J Biol Chem 2009, 284:22825-22833.
99. Pinner S., Jordan P., Sharrock K., Bazley L., Collinson L., Marais R., et al. Intravital imaging reveals transient changes in pigment production and Brn2 expression during metastatic melanoma dissemination. Cancer Res 2009, 69:7969-7977.
100. Niinaka Y., Harada K., Fujimuro M., Oda M., Haga A., Hosoki M., et al. Silencing of autocrine motility factor induces mesenchymal-to-epithelial transition and suppression of osteosarcoma pulmonary metastasis. Cancer Res 2010, 70:9483-9493.
101. Yan W., Cao Q.J., Arenas R.B., Bentley B., Shao R. GATA3 inhibits breast cancer metastasis through the reversal of epithelial-mesenchymal transition. J Biol Chem 2010, 285:14042-14051.
102. Blanco M.J., Barrallo-Gimeno A., Acloque H., Reyes A.E., Tada M., Allende M.L., et al. Snail1a and Snail1b cooperate in the anterior migration of the axial mesendoderm in the zebrafish embryo. Development 2007, 134:4073-4081.
103. Friedl P., Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003, 3:362-374.
104. Giampieri S., Manning C., Hooper S., Jones L., Hill C.S., Sahai E. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009, 11:1287-1296.
105. Madsen C.D., Sahai E. Cancer dissemination-lessons from leukocytes. Dev Cell 2010, 19:13-26.
106. Sleeman J.P., Thiery J.P. SnapShot: the epithelial-mesenchymal transition. Cell 2011, 145(162):e161.
107. Tran D.D., Corsa C.A., Biswas H., Aft R.L., Longmore G.D. Temporal and spatial cooperation of Snail1 and Twist1 during epithelial-mesenchymal transition predicts for human breast cancer recurrence. Mol Cancer Res 2011, 9:1644-1657.
108. Browne G., Sayan A.E., Tulchinsky E. ZEB proteins link cell motility with cell cycle control and cell survival in cancer. Cell Cycle 2010, 9:886-891.
109. Singh A., Settleman J. Oncogenic K-ras " addiction" and synthetic lethality. Cell Cycle 2009, 8:2676-2677.
110. Floor S., van Staveren W.C., Larsimont D., Dumont J.E., Maenhaut C. Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: distinct, overlapping or same populations. Oncogene 2011, 30:4609-4621.
111. Fischer A.N., Fuchs E., Mikula M., Huber H., Beug H., Mikulits W. PDGF essentially links TGF-beta signaling to nuclear beta-catenin accumulation in hepatocellular carcinoma progression. Oncogene 2007, 26:3395-3405.
112. Vega S., Morales A.V., Ocana O.H., Valdes F., Fabregat I., Nieto M.A. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev 2004, 18:1131-1143.
113. Mejlvang J., Kriajevska M., Vandewalle C., Chernova T., Sayan A.E., Berx G., et al. Direct repression of cyclin D1 by SIP1 attenuates cell cycle progression in cells undergoing an epithelial mesenchymal transition. Mol Biol Cell 2007, 18:4615-4624.
114. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
115. Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009, 11:1487-1495.
116. Singh A., Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010, 29:4741-4751.
117. Le N.H., Franken P., Fodde R. Tumour-stroma interactions in colorectal cancer: converging on beta-catenin activation and cancer stemness. Br J Cancer 2008, 98:1886-1893.
118. Brabletz T., Jung A., Reu S., Porzner M., Hlubek F., Kunz-Schughart L.A., et al. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA 2001, 98:10356-10361.
119. Fodde R., Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 2007, 19:150-158.
120. Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
121. Psaila B., Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009, 9:285-293.
122. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
123. Hiratsuka S., Watanabe A., Aburatani H., Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 2006, 8:1369-1375.
124. Hiratsuka S., Watanabe A., Sakurai Y., Akashi-Takamura S., Ishibashi S., Miyake K., et al. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 2008, 10:1349-1355.
125. Kaplan R.N., Rafii S., Lyden D. Preparing the " soil" : the premetastatic niche. Cancer Res 2006, 66:11089-11093.
126. Erler J.T., Bennewith K.L., Cox T.R., Lang G., Bird D., Koong A., et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009, 15:35-44.
127. Wong C.C., Gilkes D.M., Zhang H., Chen J., Wei H., Chaturvedi P., et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci USA 2011, 108:16369-16374.
128. Wong C.C., Zhang H., Gilkes D.M., Chen J., Wei H., Chaturvedi P., et al. Inhibitors of hypoxia-inducible factor 1 block breast cancer metastatic niche formation and lung metastasis. J Mol Med (Berl) 2012.
129. Zumsteg A., Christofori G. Corrupt policemen: inflammatory cells promote tumor angiogenesis. Curr Opin Oncol 2009, 21:60-70.
130. Cichon M.A., Degnim A.C., Visscher D.W., Radisky D.C. Microenvironmental influences that drive progression from benign breast disease to invasive breast cancer. J Mammary Gland Biol Neoplasia 2010, 15:389-397.
131. Shiozawa Y., Pedersen E.A., Havens A.M., Jung Y., Mishra A., Joseph J., et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 2011, 121:1298-1312.
132. Psaila B., Lyden D., Roberts I. Megakaryocytes malignancy and bone marrow vascular niches. J Thromb Haemost 2011.
133. Cameron M.D., Schmidt E.E., Kerkvliet N., Nadkarni K.V., Morris V.L., Groom A.C., et al. Temporal progression of metastasis in lung: cell survival, dormancy, and location dependence of metastatic inefficiency. Cancer Res 2000, 60:2541-2546.
134. Lukanidin E., Sleeman J.P. Building the niche: The role of the S100 proteins in metastatic growth. Semin Cancer Biol 2012, 22:216-225.
135. Finger E.C., Giaccia A.J. Hypoxia, inflammation, and the tumor microenvironment in metastatic disease. Cancer Metast Rev 2010, 29:285-293.
136. Eltzschig H.K., Carmeliet P. Hypoxia and inflammation. N Engl J Med 2011, 364:656-665.
137. Chen Q., Zhang X.H., Massague J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 2011, 20:538-549.
138. Hiratsuka S., Nakamura K., Iwai S., Murakami M., Itoh T., Kijima H., et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002, 2:289-300.
139. Malanchi I., Santamaria-Martinez A., Susanto E., Peng H., Lehr H.A., Delaloye J.F., et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2011, 481:85-89.
140. Oskarsson T., Acharyya S., Zhang X.H., Vanharanta S., Tavazoie S.F., Morris P.G., et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 2011, 17:867-874.
141. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 2006, 18:516-523.
142. Schober M., Fuchs E. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-beta and integrin/focal adhesion kinase (FAK) signaling. Proc Natl Acad Sci USA 2011, 108:10544-10549.
143. Barkan D., Green J.E., Chambers A.F. Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur J Cancer 2010, 46:1181-1188.
144. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
145. Goetz J.G., Minguet S., Navarro-Lerida I., Lazcano J.J., Samaniego R., Calvo E., et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
146. Dupont S., Morsut L., Aragona M., Enzo E., Giulitti S., Cordenonsi M., et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474:179-183.
147. Cordenonsi M., Zanconato F., Azzolin L., Forcato M., Rosato A., Frasson C., et al. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 2011, 147:759-772.
148. Schrader J., Gordon-Walker T.T., Aucott R.L., van Deemter M., Quaas A., Walsh S., et al. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 2011, 53:1192-1205.
149. Leight J.L., Wozniak M.A., Chen S., Lynch M.L., Chen C.S. Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial-mesenchymal transition. Mol Biol Cell 2012.
150. Peinado H., Lavotshkin S., Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 2011, 21:139-146.
151. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009, 9:581-593.
152. Jung T., Castellana D., Klingbeil P., Cuesta Hernandez I., Vitacolonna M., Orlicky D.J., et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 2009, 11:1093-1105.
153. Grange C., Tapparo M., Collino F., Vitillo L., Damasco C., Deregibus M.C., et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 2011, 71:5346-5356.
154. Castellana D., Zobairi F., Martinez M.C., Panaro M.A., Mitolo V., Freyssinet J.M., et al. Membrane microvesicles as actors in the establishment of a favorable prostatic tumoral niche: a role for activated fibroblasts and CX3CL1-CX3CR1 axis. Cancer Res 2009, 69:785-793.
155. Rhodes L.V., Bratton M.R., Zhu Y., Tilghman S.L., Muir S.E., Salvo V.A., et al. Effects of SDF-1-CXCR4 signaling on microRNA expression and tumorigenesis in estrogen receptor-alpha (ER-alpha)-positive breast cancer cells. Exp Cell Res 2011, 317:2573-2581.
156. Onoue T., Uchida D., Begum N.M., Tomizuka Y., Yoshida H., Sato M. Epithelial-mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells. Int J Oncol 2006, 29:1133-1138.
157. Wang Z., Ma Q., Liu Q., Yu H., Zhao L., Shen S., et al. Blockade of SDF-1/CXCR4 signalling inhibits pancreatic cancer progression in vitro via inactivation of canonical Wnt pathway. Br J Cancer 2008, 99:1695-1703.
158. Taki M., Higashikawa K., Yoneda S., Ono S., Shigeishi H., Nagayama M., et al. Up-regulation of stromal cell-derived factor-1alpha and its receptor CXCR4 expression accompanied with epithelial-mesenchymal transition in human oral squamous cell carcinoma. Oncol Rep 2008, 19:993-998.
159. Bertran E., Caja L., Navarro E., Sancho P., Mainez J., Murillo M.M., et al. Role of CXCR4/SDF-1 alpha in the migratory phenotype of hepatoma cells that have undergone epithelial-mesenchymal transition in response to the transforming growth factor-beta. Cell Signal 2009, 21:1595-1606.
160. Duda D.G., Kozin S.V., Kirkpatrick N.D., Xu L., Fukumura D., Jain R.K. CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies?. Clin Cancer Res 2011, 17:2074-2080.
161. Lopez-Novoa J.M., Nieto M.A. Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 2009, 1:303-314.
162. Dohadwala M., Wang G., Heinrich E., Luo J., Lau O., Shih H., et al. The role of ZEB1 in the inflammation-induced promotion of EMT in HNSCC. Otolaryngol Head Neck Surg 2010, 142:753-759.
163. Peinado H., Del Carmen Iglesias-de la Cruz M., Olmeda D., Csiszar K., Fong K.S., Vega S., et al. A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J 2005, 24:3446-3458.
164. Orlichenko L.S., Radisky D.C. Matrix metalloproteinases stimulate epithelial-mesenchymal transition during tumor development. Clin Exp Metast 2008, 25:593-600.
165. Morra L., Moch H. Periostin expression and epithelial-mesenchymal transition in cancer: a review and an update. Virchows Arch 2011, 459:465-475.
166. Lin Q., Yun Z. Impact of the hypoxic tumor microenvironment on the regulation of cancer stem cell characteristics. Cancer Biol Ther 2010, 9:949-956.
167. Hofstetter C.P., Burkhardt J.K., Shin B.J., Gursel D.B., Mubita L., Gorrepati R., et al. Protein phosphatase 2A mediates dormancy of glioblastoma multiforme-derived tumor stem-like cells during hypoxia. PLoS One 2012, 7:e30059.
168. Charafe-Jauffret E., Ginestier C., Iovino F., Wicinski J., Cervera N., Finetti P., et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009, 69:1302-1313.
169. Ginestier C., Liu S., Diebel M.E., Korkaya H., Luo M., Brown M., et al. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest 2010, 120:485-497.
170. Cristofanilli M., Braun S. Circulating tumor cells revisited. JAMA 2010, 303:1092-1093.
171. Molloy T.J., Bosma A.J., Baumbusch L.O., Synnestvedt M., Borgen E., Russnes H.G., et al. The prognostic significance of tumour cell detection in the peripheral blood versus the bone marrow in 733 early-stage breast cancer patients. Breast Cancer Res 2011, 13:R61.
172. Pantel K., Alix-Panabieres C. The clinical significance of circulating tumor cells. Nat Clin Pract Oncol 2007, 4:62-63.
173. Bednarz-Knoll N., Alix-Panabieres C., Pantel K. Clinical relevance and biology of circulating tumor cells. Breast Cancer Res 2011, 13:228.
174. Cristofanilli M., Budd G.T., Ellis M.J., Stopeck A., Matera J., Miller M.C., et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 2004, 351:781-791.
175. de Bono J.S., Scher H.I., Montgomery R.B., Parker C., Miller M.C., Tissing H., et al. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin Cancer Res 2008, 14:6302-6309.
176. Cristofanilli M., Hayes D.F., Budd G.T., Ellis M.J., Stopeck A., Reuben J.M., et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J Clin Oncol 2005, 23:1420-1430.
177. Bidard F.C., Mathiot C., Delaloge S., Brain E., Giachetti S., de Cremoux P., et al. Single circulating tumor cell detection and overall survival in nonmetastatic breast cancer. Ann Oncol 2010, 21:729-733.
178. Liu M.C., Shields P.G., Warren R.D., Cohen P., Wilkinson M., Ottaviano Y.L., et al. Circulating tumor cells: a useful predictor of treatment efficacy in metastatic breast cancer. J Clin Oncol 2009, 27:5153-5159.
179. Yu M., Stott S., Toner M., Maheswaran S., Haber D.A. Circulating tumor cells: approaches to isolation and characterization. J Cell Biol 2011, 192:373-382.
180. Fehm T., Muller V., Aktas B., Janni W., Schneeweiss A., Stickeler E., et al. HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res Treat 2010, 124:403-412.
181. Riethdorf S., Muller V., Zhang L., Rau T., Loibl S., Komor M., et al. Detection and HER2 expression of circulating tumor cells: prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res 2010, 16:2634-2645.
182. Munzone E., Nole F., Goldhirsch A., Botteri E., Esposito A., Zorzino L., 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, 10:392-397.
183. Kallergi G., Agelaki S., Kalykaki A., Stournaras C., Mavroudis D., Georgoulias V. Phosphorylated EGFR and PI3K/Akt signaling kinases are expressed in circulating tumor cells of breast cancer patients. Breast Cancer Res 2008, 10:R80.