Tumor metastasis: Molecular insights and evolving paradigms

Cell

Volumn 147, Issue 2, 2011, Pages 275-292

  Valastyan, Scott ^a,b   Weinberg, Robert A ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

CANCER CELL; CANCER INVASION; CANCER SURVIVAL; CELL FUNCTION; CYTOLOGY; EPIGENETICS; EXTRAVASATION; GENETIC ANALYSIS; HUMAN; METASTASIS; MICROENVIRONMENT; MICROMETASTASIS; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; REVIEW; STROMA CELL;

EID: 80054686286     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.09.024     Document Type: Review

References (112)

1. J.A. Aguirre-Ghiso Models, mechanisms and clinical evidence for cancer dormancy Nat. Rev. Cancer 7 2007 834 846 (Pubitemid 350006258)
2. A.B. Al-Mehdi, K. Tozawa, A.B. Fisher, L. Shientag, A. Lee, and R.J. Muschel Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis Nat. Med. 6 2000 100 102 (Pubitemid 30048535)
3. P. Auguste, L. Fallavollita, N. Wang, J. Burnier, A. Bikfalvi, and P. Brodt The host inflammatory response promotes liver metastasis by increasing tumor cell arrest and extravasation Am. J. Pathol. 170 2007 1781 1792 (Pubitemid 47339320)
4. D. Barkan, H. Kleinman, J.L. Simmons, H. Asmussen, A.K. Kamaraju, M.J. Hoenorhoff, Z.Y. Liu, S.V. Costes, E.H. Cho, and S. Lockett Inhibition of metastatic outgrowth from single dormant tumor cells by targeting the cytoskeleton Cancer Res. 68 2008 6241 6250
5. D. Barkan, L.H. El Touny, A.M. Michalowski, J.A. Smith, I. Chu, A.S. Davis, J.D. Webster, S. Hoover, R.M. Simpson, J. Gauldie, and J.E. Green Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment Cancer Res. 70 2010 5706 5716
6. M.J. Bissell, and W.C. Hines Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression Nat. Med. 17 2011 320 329
7. P.D. Bos, X.H. Zhang, C. Nadal, W. Shu, R.R. Gomis, D.X. Nguyen, A.J. Minn, M.J. van de Vijver, W.L. Gerald, J.A. Foekens, and J. Massagué Genes that mediate breast cancer metastasis to the brain Nature 459 2009 1005 1009
8. S. Braun, F.D. Vogl, B. Naume, W. Janni, M.P. Osborne, R.C. Coombes, G. Schlimok, I.J. Diel, B. Gerber, and G. Gebauer A pooled analysis of bone marrow micrometastasis in breast cancer N. Engl. J. Med. 353 2005 793 802 (Pubitemid 41215488)
9. D.M. Brown, and E. Ruoslahti Metadherin, a cell surface protein in breast tumors that mediates lung metastasis Cancer Cell 5 2004 365 374 (Pubitemid 38482072)
10. J. Calbo, E. van Montfort, N. Proost, E. van Drunen, H.B. Beverloo, R. Meuwissen, and A. Berns A functional role for tumor cell heterogeneity in a mouse model of small cell lung cancer Cancer Cell 19 2011 244 256
11. P.J. Campbell, S. Yachida, L.J. Mudie, P.J. Stephens, E.D. Pleasance, L.A. Stebbings, L.A. Morsberger, C. Latimer, S. McLaren, and M.L. Lin The patterns and dynamics of genomic instability in metastatic pancreatic cancer Nature 467 2010 1109 1113
12. P. Carmeliet, and R.K. Jain Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases Nat. Rev. Drug Discov. 10 2011 417 427
13. A.F. Chambers, A.C. Groom, and I.C. MacDonald Dissemination and growth of cancer cells in metastatic sites Nat. Rev. Cancer 2 2002 563 572 (Pubitemid 37328923)
14. H.Y. Chang, J.B. Sneddon, A.A. Alizadeh, R. Sood, R.B. West, K. Montgomery, J.T. Chi, M. van de Rijn, D. Botstein, and P.O. Brown Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds PLoS Biol. 2 2004 E7
15. L. Chen, S. Yang, J. Jakoncic, J.J. Zhang, and X.Y. Huang Migrastatin analogues target fascin to block tumour metastasis Nature 464 2010 1062 1066
16. H. Clevers The cancer stem cell: premises, promises and challenges Nat. Med. 17 2011 313 319
17. M. Cristofanilli, G.T. Budd, M.J. Ellis, A. Stopeck, J. Matera, M.C. Miller, J.M. Reuben, G.V. Doyle, W.J. Allard, L.W. Terstappen, and D.F. Hayes Circulating tumor cells, disease progression, and survival in metastatic breast cancer N. Engl. J. Med. 351 2004 781 791 (Pubitemid 39095313)
18. M.R. Dawson, D.G. Duda, D. Fukumura, and R.K. Jain VEGFR1-activity- independent metastasis formation Nature 461 2009 E4 E5, discussion E5
19. D.G. DeNardo, J.B. Barreto, P. Andreu, L. Vasquez, D. Tawfik, N. Kolhatkar, and L.M. Coussens CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages Cancer Cell 16 2009 91 102
20. C. Desmedt, B. Haibe-Kains, P. Wirapati, M. Buyse, D. Larsimont, G. Bontempi, M. Delorenzi, M. Piccart, and C. Sotiriou Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes Clin. Cancer Res. 14 2008 5158 5165
21. L. Ding, M.J. Ellis, S. Li, D.E. Larson, K. Chen, J.W. Wallis, C.C. Harris, M.D. McLellan, R.S. Fulton, and L.L. Fulton Genome remodelling in a basal-like breast cancer metastasis and xenograft Nature 464 2010 999 1005
22. B. Dirat, L. Bochet, M. Dabek, D. Daviaud, S. Dauvillier, B. Majed, Y.Y. Wang, A. Meulle, B. Salles, and S. Le Gonidec Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion Cancer Res. 71 2011 2455 2465
23. S. Douma, T. Van Laar, J. Zevenhoven, R. Meuwissen, E. Van Garderen, and D.S. Peeper Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB Nature 430 2004 1034 1039
24. J.M.L. Ebos, C.R. Lee, W. Cruz-Munoz, G.A. Bjarnason, J.G. Christensen, and R.S. Kerbel Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis Cancer Cell 15 2009 232 239
25. J.T. Erler, K.L. Bennewith, T.R. Cox, G. Lang, D. Bird, A. Koong, Q.T. Le, and A.J. Giaccia Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche Cancer Cell 15 2009 35 44
26. C. Fan, D.S. Oh, L. Wessels, B. Weigelt, D.S. Nuyten, A.B. Nobel, L.J. van't Veer, and C.M. Perou Concordance among gene-expression-based predictors for breast cancer N. Engl. J. Med. 355 2006 560 569 (Pubitemid 44200649)
27. I.J. Fidler The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited Nat. Rev. Cancer 3 2003 453 458 (Pubitemid 37328849)
28. G. Finak, N. Bertos, F. Pepin, S. Sadekova, M. Souleimanova, H. Zhao, H. Chen, G. Omeroglu, S. Meterissian, and A. Omeroglu Stromal gene expression predicts clinical outcome in breast cancer Nat. Med. 14 2008 518 527 (Pubitemid 351655218)
29. P. Friedl, and K. Wolf Tumour-cell invasion and migration: diversity and escape mechanisms Nat. Rev. Cancer 3 2003 362 374 (Pubitemid 37328856)
30. S. Giampieri, C. Manning, S. Hooper, L. Jones, C.S. Hill, and E. Sahai Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility Nat. Cell Biol. 11 2009 1287 1296
31. L.A. Gilbert, and M.T. Hemann DNA damage-mediated induction of a chemoresistant niche Cell 143 2010 355 366
32. V. Gocheva, H.W. Wang, B.B. Gadea, T. Shree, K.E. Hunter, A.L. Garfall, T. Berman, and J.A. Joyce IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion Genes Dev. 24 2010 241 255
33. J.G. Goetz, S. Minguet, I. Navarro-Lérida, J.J. Lazcano, R. Samaniego, E. Calvo, M. Tello, T. Osteso-Ibáñez, T. Pellinen, and A. Echarri Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis Cell 146 2011 148 163
34. S.I. Grivennikov, F.R. Greten, and M. Karin Immunity, inflammation, and cancer Cell 140 2010 883 899
35. W. Guo, and F.G. Giancotti Integrin signalling during tumour progression Nat. Rev. Mol. Cell Biol. 5 2004 816 826 (Pubitemid 39336275)
36. G.P. Gupta, and J. Massagué Cancer metastasis: building a framework Cell 127 2006 679 695 (Pubitemid 44781029)
37. G.P. Gupta, D.X. Nguyen, A.C. Chiang, P.D. Bos, J.Y. Kim, C. Nadal, R.R. Gomis, K. Manova-Todorova, and J. Massagué Mediators of vascular remodelling co-opted for sequential steps in lung metastasis Nature 446 2007 765 770 (Pubitemid 46582040)
38. G.P. Gupta, J. Perk, S. Acharyya, P. de Candia, V. Mittal, K. Todorova-Manova, W.L. Gerald, E. Brogi, R. Benezra, and J. Massagué ID genes mediate tumor reinitiation during breast cancer lung metastasis Proc. Natl. Acad. Sci. USA 104 2007 19506 19511
39. R.A. Gupta, N. Shah, K.C. Wang, J. Kim, H.M. Horlings, D.J. Wong, M.C. Tsai, T. Hung, P. Argani, and J.L. Rinn Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis Nature 464 2010 1071 1076
40. I.R. Hart, and I.J. Fidler Role of organ selectivity in the determination of metastatic patterns of B16 melanoma Cancer Res. 40 1980 2281 2287 (Pubitemid 10082239)
41. S. Hiratsuka, D.G. Duda, Y. Huang, S. Goel, T. Sugiyama, T. Nagasawa, D. Fukumura, and R.K. Jain C-X-C receptor type 4 promotes metastasis by activating p38 mitogen-activated protein kinase in myeloid differentiation antigen (Gr-1)-positive cells Proc. Natl. Acad. Sci. USA 108 2011 302 307
42. S. Hiratsuka, S. Goel, W.S. Kamoun, Y. Maru, D. Fukumura, D.G. Duda, and R.K. Jain Endothelial focal adhesion kinase mediates cancer cell homing to discrete regions of the lungs via E-selectin up-regulation Proc. Natl. Acad. Sci. USA 108 2011 3725 3730
43. S.J. Holland, A. Pan, C. Franci, Y. Hu, B. Chang, W. Li, M. Duan, A. Torneros, J. Yu, and T.J. Heckrodt R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer Cancer Res. 70 2010 1544 1554
44. M. Hu, J. Yao, D.K. Carroll, S. Weremowicz, H. Chen, D. Carrasco, A. Richardson, S. Violette, T. Nikolskaya, and Y. Nikolsky Regulation of in situ to invasive breast carcinoma transition Cancer Cell 13 2008 394 406 (Pubitemid 351609443)
45. Y. Huang, N. Song, Y. Ding, S. Yuan, X. Li, H. Cai, H. Shi, and Y. Luo Pulmonary vascular destabilization in the premetastatic phase facilitates lung metastasis Cancer Res. 69 2009 7529 7537
46. Y. Hüsemann, J.B. Geigl, F. Schubert, P. Musiani, M. Meyer, E. Burghart, G. Forni, R. Eils, T. Fehm, G. Riethmüller, and C.A. Klein Systemic spread is an early step in breast cancer Cancer Cell 13 2008 58 68 (Pubitemid 350309740)
47. M.P. Iwanicki, R.A. Davidowitz, M.R. Ng, A. Besser, T. Muranen, M. Merritt, G. Danuser, T. Ince, and J.S. Brugge Ovarian cancer spheroids use myosin-generated force to clear the mesothelium Cancer Discov 1 2011 144 157
48. S. Jones, W.D. Chen, G. Parmigiani, F. Diehl, N. Beerenwinkel, T. Antal, A. Traulsen, M.A. Nowak, C. Siegel, and V.E. Velculescu Comparative lesion sequencing provides insights into tumor evolution Proc. Natl. Acad. Sci. USA 105 2008 4283 4288 (Pubitemid 351754372)
49. J.A. Joyce, and J.W. Pollard Microenvironmental regulation of metastasis Nat. Rev. Cancer 9 2009 239 252
50. Y. Kang, P.M. Siegel, W. Shu, M. Drobnjak, S.M. Kakonen, C. Cordón-Cardo, T.A. Guise, and J. Massagué A multigenic program mediating breast cancer metastasis to bone Cancer Cell 3 2003 537 549 (Pubitemid 36808649)
51. S.Y. Kang, O.J. Halvorsen, K. Gravdal, N. Bhattacharya, J.M. Lee, N.W. Liu, B.T. Johnston, A.B. Johnston, S.A. Haukaas, and K. Aamodt Prosaposin inhibits tumor metastasis via paracrine and endocrine stimulation of stromal p53 and Tsp-1 Proc. Natl. Acad. Sci. USA 106 2009 12115 12120
52. K. Kessenbrock, V. Plaks, and Z. Werb Matrix metalloproteinases: regulators of the tumor microenvironment Cell 141 2010 52 67
53. M.Y. Kim, T. Oskarsson, S. Acharyya, D.X. Nguyen, X.H. Zhang, L. Norton, and J. Massagué Tumor self-seeding by circulating cancer cells Cell 139 2009 1315 1326
54. C.A. Klein Parallel progression of primary tumours and metastases Nat. Rev. Cancer 9 2009 302 312
55. H. Kouros-Mehr, S.K. Bechis, E.M. Slorach, L.E. Littlepage, M. Egeblad, A.J. Ewald, S.Y. Pai, I.C. Ho, and Z. Werb GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model Cancer Cell 13 2008 141 152 (Pubitemid 351163164)
56. K.R. Levental, H. Yu, L. Kass, J.N. Lakins, M. Egeblad, J.T. Erler, S.F. Fong, K. Csiszar, A. Giaccia, and W. Weninger Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 2009 891 906
57. W. Liu, S. Laitinen, S. Khan, M. Vihinen, J. Kowalski, G. Yu, L. Chen, C.M. Ewing, M.A. Eisenberger, and M.A. Carducci Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer Nat. Med. 15 2009 559 565
58. J. Lu, G. Getz, E.A. Miska, E. Alvarez-Saavedra, J. Lamb, D. Peck, A. Sweet-Cordero, B.L. Ebert, R.H. Mak, and A.A. Ferrando MicroRNA expression profiles classify human cancers Nature 435 2005 834 838 (Pubitemid 40839735)
59. K.J. Luzzi, I.C. MacDonald, E.E. Schmidt, N. Kerkvliet, V.L. Morris, A.F. Chambers, and A.C. Groom Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases Am. J. Pathol. 153 1998 865 873 (Pubitemid 28419039)
60. L. Ma, F. Reinhardt, E. Pan, J. Soutschek, B. Bhat, E.G. Marcusson, J. Teruya-Feldstein, G.W. Bell, and R.A. Weinberg Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model Nat. Biotechnol. 28 2010 341 347
61. R. Mazzieri, F. Pucci, D. Moi, E. Zonari, A. Ranghetti, A. Berti, L.S. Politi, B. Gentner, J.L. Brown, L. Naldini, and M. De Palma Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells Cancer Cell 19 2011 512 526
62. S.S. McAllister, A.M. Gifford, A.L. Greiner, S.P. Kelleher, M.P. Saelzler, T.A. Ince, F. Reinhardt, L.N. Harris, B.L. Hylander, E.A. Repasky, and R.A. Weinberg Systemic endocrine instigation of indolent tumor growth requires osteopontin Cell 133 2008 994 1005 (Pubitemid 351787747)
63. S. Meng, D. Tripathy, E.P. Frenkel, S. Shete, E.Z. Naftalis, J.F. Huth, P.D. Beitsch, M. Leitch, S. Hoover, and D. Euhus Circulating tumor cells in patients with breast cancer dormancy Clin. Cancer Res. 10 2004 8152 8162 (Pubitemid 40053373)
64. D. Miles, N. Harbeck, B. Escudier, H. Hurwitz, L. Saltz, E. Van Cutsem, J. Cassidy, B. Mueller, and F. Sirzén Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials J. Clin. Oncol. 29 2011 83 88
65. A.J. Minn, G.P. Gupta, P.M. Siegel, P.D. Bos, W. Shu, D.D. Giri, A. Viale, A.B. Olshen, W.L. Gerald, and J. Massagué Genes that mediate breast cancer metastasis to lung Nature 436 2005 518 524 (Pubitemid 41112921)
66. S. Nagrath, L.V. Sequist, S. Maheswaran, D.W. Bell, D. Irimia, L. Ulkus, M.R. Smith, E.L. Kwak, S. Digumarthy, and A. Muzikansky Isolation of rare circulating tumour cells in cancer patients by microchip technology Nature 450 2007 1235 1239
67. N. Navin, J. Kendall, J. Troge, P. Andrews, L. Rodgers, J. McIndoo, K. Cook, A. Stepansky, D. Levy, and D. Esposito Tumour evolution inferred by single-cell sequencing Nature 472 2011 90 94
68. D.X. Nguyen, P.D. Bos, and J. Massagué Metastasis: from dissemination to organ-specific colonization Nat. Rev. Cancer 9 2009 274 284
69. K.P. Olive, M.A. Jacobetz, C.J. Davidson, A. Gopinathan, D. McIntyre, D. Honess, B. Madhu, M.A. Goldgraben, M.E. Caldwell, and D. Allard Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457 1461
70. T. Oskarsson, P. Nagorny, I.J. Krauss, L. Perez, M. Mandal, G. Yang, O. Ouerfelli, D. Xiao, M.A. Moore, J. Massagué, and S.J. Danishefsky Diverted total synthesis leads to the generation of promising cell-migration inhibitors for treatment of tumor metastasis: in vivo and mechanistic studies on the migrastatin core ether analog J. Am. Chem. Soc. 132 2010 3224 3228
71. T. Oskarsson, S. Acharyya, X.H.F. Zhang, S. Vanharanta, S.F. Tavazoie, P.G. Morris, R.J. Downey, K. Manova-Todorova, E. Brogi, and J. Massagué Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs Nat. Med. 17 2011 867 874
72. T.P. Padera, A.H. Kuo, T. Hoshida, S. Liao, J. Lobo, K.R. Kozak, D. Fukumura, and R.K. Jain Differential response of primary tumor versus lymphatic metastasis to VEGFR-2 and VEGFR-3 kinase inhibitors cediranib and vandetanib Mol. Cancer Ther. 7 2008 2272 2279
73. D. Padua, X.H. Zhang, Q. Wang, C. Nadal, W.L. Gerald, R.R. Gomis, and J. Massagué TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4 Cell 133 2008 66 77 (Pubitemid 351442989)
74. M. Pez-Ribes, E. Allen, J. Hudock, T. Takeda, H. Okuyama, F. Viñals, M. Inoue, G. Bergers, D. Hanahan, and O. Casanovas Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis Cancer Cell 15 2009 220 231
75. S. Paik, S. Shak, G. Tang, C. Kim, J. Baker, M. Cronin, F.L. Baehner, M.G. Walker, D. Watson, and T. Park A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer N. Engl. J. Med. 351 2004 2817 2826 (Pubitemid 40051905)
76. D. Palmieri, D.O. Halverson, T. Ouatas, C.E. Horak, M. Salerno, J. Johnson, W.D. Figg, M. Hollingshead, S. Hursting, and D. Berrigan Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptor-negative breast cancer J. Natl. Cancer Inst. 97 2005 632 642 (Pubitemid 40812627)
77. K. Pantel, R.H. Brakenhoff, and B. Brandt Detection, clinical relevance and specific biological properties of disseminating tumour cells Nat. Rev. Cancer 8 2008 329 340 (Pubitemid 351596394)
78. K. Podsypanina, Y.C. Du, M. Jechlinger, L.J. Beverly, D. Hambardzumyan, and H. Varmus Seeding and propagation of untransformed mouse mammary cells in the lung Science 321 2008 1841 1844
79. B. Psaila, and D. Lyden The metastatic niche: adapting the foreign soil Nat. Rev. Cancer 9 2009 285 293
80. B.Z. Qian, J. Li, H. Zhang, T. Kitamura, J. Zhang, L.R. Campion, E.A. Kaiser, L.A. Snyder, and J.W. Pollard CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis Nature 475 2011 222 225
81. B.Z. Qian, and J.W. Pollard Macrophage diversity enhances tumor progression and metastasis Cell 141 2010 39 51
82. S. Ramaswamy, K.N. Ross, E.S. Lander, and T.R. Golub A molecular signature of metastasis in primary solid tumors Nat. Genet. 33 2003 49 54 (Pubitemid 36068681)
83. L. Ricci-Vitiani, R. Pallini, M. Biffoni, M. Todaro, G. Invernici, T. Cenci, G. Maira, E.A. Parati, G. Stassi, L.M. Larocca, and R. De Maria Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells Nature 468 2010 824 828
84. E. Sahai Illuminating the metastatic process Nat. Rev. Cancer 7 2007 737 749 (Pubitemid 47463672)
85. Z.T. Schafer, A.R. Grassian, L. Song, Z. Jiang, Z. Gerhart-Hines, H.Y. Irie, S. Gao, P. Puigserver, and J.S. Brugge Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment Nature 461 2009 109 113
86. O. Schmidt-Kittler, T. Ragg, A. Daskalakis, M. Granzow, A. Ahr, T.J. Blankenstein, M. Kaufmann, J. Diebold, H. Arnholdt, and P. Muller From latent disseminated cells to overt metastasis: genetic analysis of systemic breast cancer progression Proc. Natl. Acad. Sci. USA 100 2003 7737 7742 (Pubitemid 36760039)
87. H. Schwarzenbach, D.S. Hoon, and K. Pantel Cell-free nucleic acids as biomarkers in cancer patients Nat. Rev. Cancer 11 2011 426 437
88. N. Sethi, X. Dai, C.G. Winter, and Y. Kang Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells Cancer Cell 19 2011 192 205
89. M. Shackleton, E. Quintana, E.R. Fearon, and S.J. Morrison Heterogeneity in cancer: cancer stem cells versus clonal evolution Cell 138 2009 822 829
90. T. Shibue, and R.A. Weinberg Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs Proc. Natl. Acad. Sci. USA 106 2009 10290 10295
91. Y. Shimono, M. Zabala, R.W. Cho, N. Lobo, P. Dalerba, D. Qian, M. Diehn, H. Liu, S.P. Panula, and E. Chiao Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells Cell 138 2009 592 603
92. M. Sonoshita, M. Aoki, H. Fuwa, K. Aoki, H. Hosogi, Y. Sakai, H. Hashida, A. Takabayashi, M. Sasaki, and S. Robine Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling Cancer Cell 19 2011 125 137
93. P.S. Steeg Tumor metastasis: mechanistic insights and clinical challenges Nat. Med. 12 2006 895 904 (Pubitemid 44175140)
94. S.L. Stott, C.H. Hsu, D.I. Tsukrov, M. Yu, D.T. Miyamoto, B.A. Waltman, S.M. Rothenberg, A.M. Shah, M.E. Smas, and G.K. Korir Isolation of circulating tumor cells using a microvortex-generating herringbone-chip Proc. Natl. Acad. Sci. USA 107 2010 18392 18397
95. M.R. Stratton Exploring the genomes of cancer cells: progress and promise Science 331 2011 1553 1558
96. S. Tabaris, Z. Dong, M.G. Annis, A. Omeroglu, F. Pepin, V. Ouellet, C. Russo, M. Hassanain, P. Metrakos, and Z. Diaz Claudin-2 is selectively enriched in and promotes the formation of breast cancer liver metastases through engagement of integrin complexes Oncogene 30 2011 1318 1328
97. D. Tarin, J.E. Price, M.G. Kettlewell, R.G. Souter, A.C. Vass, and B. Crossley Mechanisms of human tumor metastasis studied in patients with peritoneovenous shunts Cancer Res. 44 1984 3584 3592 (Pubitemid 14098615)
98. J.P. Thiery, H. Acloque, R.Y.J. Huang, and M.A. Nieto Epithelial-mesenchymal transitions in development and disease Cell 139 2009 871 890
99. S. Valastyan, and R.A. Weinberg MicroRNAs: Crucial multi-tasking components in the complex circuitry of tumor metastasis Cell Cycle 8 2009 3506 3512
100. S. Valastyan, F. Reinhardt, N. Benaich, D. Calogrias, A.M. Szász, Z.C. Wang, J.E. Brock, A.L. Richardson, and R.A. Weinberg A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis Cell 137 2009 1032 1046
101. S. Valastyan, A. Chang, N. Benaich, F. Reinhardt, and R.A. Weinberg Activation of miR-31 function in already-established metastases elicits metastatic regression Genes Dev. 25 2011 646 659
102. L.J. van 't Veer, H. Dai, M.J. van de Vijver, Y.D. He, A.A. Hart, M. Mao, H.L. Peterse, K. van der Kooy, M.J. Marton, and A.T. Witteveen Gene expression profiling predicts clinical outcome of breast cancer Nature 415 2002 530 536 (Pubitemid 34130608)
103. W. Wang, S. Goswami, K. Lapidus, A.L. Wells, J.B. Wyckoff, E. Sahai, R.H. Singer, J.E. Segall, and J.S. Condeelis Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors Cancer Res. 64 2004 8585 8594 (Pubitemid 39552071)
104. R. Wang, K. Chadalavada, J. Wilshire, U. Kowalik, K.E. Hovinga, A. Geber, B. Fligelman, M. Leversha, C. Brennan, and V. Tabar Glioblastoma stem-like cells give rise to tumour endothelium Nature 468 2010 829 833
105. B. Weigelt, A.M. Glas, L.F. Wessels, A.T. Witteveen, J.L. Peterse, and L.J. van't Veer Gene expression profiles of primary breast tumors maintained in distant metastases Proc. Natl. Acad. Sci. USA 100 2003 15901 15905 (Pubitemid 38021087)
106. K.N. Weilbaecher, T.A. Guise, and L.K. McCauley Cancer to bone: a fatal attraction Nat. Rev. Cancer 11 2011 411 425
107. S. Weis, J. Cui, L. Barnes, and D. Cheresh Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis J. Cell Biol. 167 2004 223 229 (Pubitemid 39435066)
108. M.M. Winslow, T.L. Dayton, R.G.W. Verhaak, C. Kim-Kiselak, E.L. Snyder, D.M. Feldser, D.D. Hubbard, M.J. DuPage, C.A. Whittaker, and S. Hoersch Suppression of lung adenocarcinoma progression by Nkx2-1 Nature 473 2011 101 104
109. J.B. Wyckoff, Y. Wang, E.Y. Lin, J.F. Li, S. Goswami, E.R. Stanley, J.E. Segall, J.W. Pollard, and J. Condeelis Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors Cancer Res. 67 2007 2649 2656 (Pubitemid 46548952)
110. S. Yachida, S. Jones, I. Bozic, T. Antal, R. Leary, B. Fu, M. Kamiyama, R.H. Hruban, J.R. Eshleman, and M.A. Nowak Distant metastasis occurs late during the genetic evolution of pancreatic cancer Nature 467 2010 1114 1117
111. S.L. Yu, H.Y. Chen, G.C. Chang, C.Y. Chen, H.W. Chen, S. Singh, C.L. Cheng, C.J. Yu, Y.C. Lee, and H.S. Chen MicroRNA signature predicts survival and relapse in lung cancer Cancer Cell 13 2008 48 57 (Pubitemid 350309743)
112. X.H. Zhang, Q. Wang, W. Gerald, C.A. Hudis, L. Norton, M. Smid, J.A. Foekens, and J. Massagué Latent bone metastasis in breast cancer tied to Src-dependent survival signals Cancer Cell 16 2009 67 78