Origins of Metastatic Traits

Cancer Cell

Volumn 24, Issue 4, 2013, Pages 410-421

  Vanharanta, Sakari ^a   Massagué, Joan ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CYTOHESIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HISTONE H3; HYPOXIA INDUCIBLE FACTOR; K RAS PROTEIN; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53; SMAD4 PROTEIN; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; VASCULAR CELL ADHESION MOLECULE 1;

BREAST CANCER; CANCER SUSCEPTIBILITY; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CLONAL EVOLUTION; COLORECTAL CANCER; DISTANT METASTASIS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE FREQUENCY; GENE MAPPING; GENE MUTATION; GENETIC ANALYSIS; GLIOBLASTOMA; HUMAN; LIVER METASTASIS; LUNG CANCER; MEDULLOBLASTOMA; METASTASIS; MICROMETASTASIS; MUTATION RATE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; REVIEW; TRIPLE NEGATIVE BREAST CANCER; TROPISM; TUMOR GROWTH; VON HIPPEL LINDAU DISEASE; WNT SIGNALING PATHWAY;

EID: 84885352426     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.09.007     Document Type: Review

References (127)

1. Acharyya S., Oskarsson T., Vanharanta S., Malladi S., Kim J., Morris P.G., Manova-Todorova K., Leversha M., Hogg N., Seshan V.E., et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150:165-178.
2. Baccelli I., Schneeweiss A., Riethdorf S., Stenzinger A., Schillert A., Vogel V., Klein C., Saini M., Bäuerle T., Wallwiener M., et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat. Biotechnol. 2013, 31:539-544.
3. Beauchesne P. Letter to the editor: the natural history of extra-cranial metastasis from glioblastoma multiform [J Neurooncol DOI 10.1007/s11060-011-0575-8]. J.Neurooncol. 2012, 109:593-594.
4. Bernards R., Weinberg R.A. A progression puzzle. Nature 2002, 418:823.
5. Bos P.D., Zhang X.H., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., van de Vijver M.J., Gerald W.L., Foekens J.A., Massagué J. Genes that mediate breast cancer metastasis to the brain. Nature 2009, 459:1005-1009.
6. Bose R., Kavuri S.M., Searleman A.C., Shen W., Shen D., Koboldt D.C., Monsey J., Goel N., Aronson A.B., Li S., et al. Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov. 2013, 3:224-237.
7. Bozic I., Antal T., Ohtsuki H., Carter H., Kim D., Chen S., Karchin R., Kinzler K.W., Vogelstein B., Nowak M.A. Accumulation of driver and passenger mutations during tumor progression. Proc. Natl. Acad. Sci. USA 2010, 107:18545-18550.
8. Calon A., Espinet E., Palomo-Ponce S., Tauriello D.V., Iglesias M., Céspedes M.V., Sevillano M., Nadal C., Jung P., Zhang X.H., et al. Dependency of colorectal cancer on a TGF-β-driven program in stromal cells for metastasis initiation. Cancer Cell 2012, 22:571-584.
9. Campbell P.J., Yachida S., Mudie L.J., Stephens P.J., Pleasance E.D., Stebbings L.A., Morsberger L.A., Latimer C., McLaren S., Lin M.L., et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010, 467:1109-1113.
10. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. Cancer Genome Atlas Network.
11. Chambers A.F., Groom A.C., MacDonald I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2:563-572.
12. Chaturvedi P., Gilkes D.M., Wong C.C., Luo W., Zhang H., Wei H., Takano N., Schito L., Levchenko A., Semenza G.L. Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis. J.Clin. Invest. 2013, 123:189-205.
13. Chen Q., Zhang X.H., Massagué J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 2011, 20:538-549.
14. Cheung W.K., Zhao M., Liu Z., Stevens L.E., Cao P.D., Fang J.E., Westbrook T.F., Nguyen D.X. Control of alveolar differentiation by the lineage transcription factors GATA6 and HOPX inhibits lung adenocarcinoma metastasis. Cancer Cell 2013, 23:725-738.
15. Chiang A.C., Massagué J. Molecular basis of metastasis. N.Engl. J. Med. 2008, 359:2814-2823.
16. Clark E.A., Golub T.R., Lander E.S., Hynes R.O. Genomic analysis of metastasis reveals an essential role for RhoC. Nature 2000, 406:532-535.
17. Comen E., Norton L., Massagué J. Clinical implications of cancer self-seeding. Nat. Rev. Clin. Oncol. 2011, 8:369-377.
18. DeNardo D.G., Barreto J.B., Andreu P., Vasquez L., Tawfik D., Kolhatkar N., Coussens L.M. CD4(+) Tcells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009, 16:91-102.
19. Diaz L.A., Williams R.T., Wu J., Kinde I., Hecht J.R., Berlin J., Allen B., Bozic I., Reiter J.G., Nowak M.A., et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012, 486:537-540.
20. Ding L., Ellis M.J., Li S., Larson D.E., Chen K., Wallis J.W., Harris C.C., McLellan M.D., Fulton R.S., Fulton L.L., et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010, 464:999-1005.
21. Ding Z., Wu C.J., Chu G.C., Xiao Y., Ho D., Zhang J., Perry S.R., Labrot E.S., Wu X., Lis R., et al. SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 2011, 470:269-273.
22. Ding L., Saunders T.L., Enikolopov G., Morrison S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481:457-462.
23. Ding Z., Wu C.J., Jaskelioff M., Ivanova E., Kost-Alimova M., Protopopov A., Chu G.C., Wang G., Lu X., Labrot E.S., et al. Telomerase reactivation following telomere dysfunction yields murine prostate tumors with bone metastases. Cell 2012, 148:896-907.
24. Eisinger-Mathason T.S., Zhang M., Qiu Q., Skuli N., Nakazawa M.S., Karakasheva T., Mucaj V., Shay J.E., Stangenberg L., Sadri N., et al. Hypoxia-dependent modification of collagen networks promotes sarcoma metastasis. Cancer Discov. 2013, Published online August 1, 2013. 10:1158/2159-8290.
25. Ell B., Kang Y. SnapShot: bone metastasis. Cell 2012, 151. 690-690.e1.
26. Erler J.T., Bennewith K.L., Nicolau M., Dornhöfer N., Kong C., Le Q.T., Chi J.T., Jeffrey S.S., Giaccia A.J. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006, 440:1222-1226.
27. Fearon E.R., Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990, 61:759-767.
28. Feld R., Rubinstein L.V., Weisenberger T.H. Sites of recurrence in resected stage I non-small-cell lung cancer: a guide for future studies. J.Clin. Oncol. 1984, 2:1352-1358.
29. Fidler I.J. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 2003, 3:453-458.
30. Fidler I.J., Kripke M.L. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977, 197:893-895.
31. Gao H., Chakraborty G., Lee-Lim A.P., Mo Q., Decker M., Vonica A., Shen R., Brogi E., Brivanlou A.H., Giancotti F.G. The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites. Cell 2012, 150:764-779.
32. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N.Engl. J. Med. 2012, 366:883-892.
33. Ghajar C.M., Peinado H., Mori H., Matei I.R., Evason K.J., Brazier H., Almeida D., Koller A., Hajjar K.A., Stainier D.Y., et al. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 2013, 15:807-817.
34. Gilkes D.M., Chaturvedi P., Bajpai S., Wong C.C., Wei H., Pitcairn S., Hubbi M.E., Wirtz D., Semenza G.L. Collagen prolyl hydroxylases are essential for breast cancer metastasis. Cancer Res. 2013, 73:3285-3296.
35. Gillies R.J., Verduzco D., Gatenby R.A. Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nat. Rev. Cancer 2012, 12:487-493.
36. Gocheva V., Wang H.W., Gadea B.B., Shree T., Hunter K.E., Garfall A.L., Berman T., Joyce J.A. IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev. 2010, 24:241-255.
37. Granot Z., Henke E., Comen E.A., King T.A., Norton L., Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 2011, 20:300-314.
38. Greaves M., Maley C.C. Clonal evolution in cancer. Nature 2012, 481:306-313.
39. Guise T.A. Breaking down bone: new insight into site-specific mechanisms of breast cancer osteolysis mediated by metalloproteinases. Genes Dev. 2009, 23:2117-2123.
40. Gupta G.P., Nguyen D.X., Chiang A.C., Bos P.D., Kim J.Y., Nadal C., Gomis R.R., Manova-Todorova K., Massagué J. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007, 446:765-770.
41. Gupta R.A., Shah N., Wang K.C., Kim J., Horlings H.M., Wong D.J., Tsai M.C., Hung T., Argani P., Rinn J.L., et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464:1071-1076.
42. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
43. Hemminki K., Sundquist J., Brandt A. Familial mortality and familial incidence in cancer. J.Clin. Oncol. 2011, 29:712-718.
44. Hess K.R., Varadhachary G.R., Taylor S.H., Wei W., Raber M.N., Lenzi R., Abbruzzese J.L. Metastatic patterns in adenocarcinoma. Cancer 2006, 106:1624-1633.
45. Hu G., Chong R.A., Yang Q., Wei Y., Blanco M.A., Li F., Reiss M., Au J.L., Haffty B.G., Kang Y. MTDH activation by 8q22 genomic gain promotes chemoresistance and metastasis of poor-prognosis breast cancer. Cancer Cell 2009, 15:9-20.
46. Hüsemann Y., Geigl J.B., Schubert F., Musiani P., Meyer M., Burghart E., Forni G., Eils R., Fehm T., Riethmüller G., Klein C.A. Systemic spread is an early step in breast cancer. Cancer Cell 2008, 13:58-68.
47. John S., Sabo P.J., Thurman R.E., Sung M.H., Biddie S.C., Johnson T.A., Hager G.L., Stamatoyannopoulos J.A. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 2011, 43:264-268.
48. Jones S., Chen W.D., Parmigiani G., Diehl F., Beerenwinkel N., Antal T., Traulsen A., Nowak M.A., Siegel C., Velculescu V.E., et al. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl. Acad. Sci. USA 2008, 105:4283-4288.
49. Kaelin W.G. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat. Rev. Cancer 2008, 8:865-873.
50. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
51. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., Richardson A.L., Polyak K., Tubo R., Weinberg R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007, 449:557-563.
52. Kessenbrock K., Plaks V., Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010, 141:52-67.
53. Kienast Y., von Baumgarten L., Fuhrmann M., Klinkert W.E., Goldbrunner R., Herms J., Winkler F. Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 2010, 16:116-122.
54. Kim M.Y., Oskarsson T., Acharyya S., Nguyen D.X., Zhang X.H., Norton L., Massagué J. Tumor self-seeding by circulating cancer cells. Cell 2009, 139:1315-1326.
55. Kim S.J., Kim J.S., Park E.S., Lee J.S., Lin Q., Langley R.R., Maya M., He J., Kim S.W., Weihua Z., et al. Astrocytes upregulate survival genes in tumor cells and induce protection from chemotherapy. Neoplasia 2011, 13:286-298.
56. Klein C.A. Parallel progression of primary tumours and metastases. Nat. Rev. Cancer 2009, 9:302-312.
57. Korpal M., Ell B.J., Buffa F.M., Ibrahim T., Blanco M.A., Celià-Terrassa T., Mercatali L., Khan Z., Goodarzi H., Hua Y., et al. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nat. Med. 2011, 17:1101-1108.
58. Kripke M.L., Gruys E., Fidler I.J. Metastatic heterogeneity of cells from an ultraviolet light-induced murine fibrosarcoma of recent origin. Cancer Res. 1978, 38:2962-2967.
59. Labelle M., Begum S., Hynes R.O. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 2011, 20:576-590.
60. Lim E., Metzger-Filho O., Winer E.P. The natural history ofhormone receptor-positive breast cancer. Oncology (Huntingt.) 2012, 26:688-694. 696.
61. Lin E.Y., Nguyen A.V., Russell R.G., Pollard J.W. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J.Exp. Med. 2001, 193:727-740.
62. Liu W., Laitinen S., Khan S., Vihinen M., Kowalski J., Yu G., Chen L., Ewing C.M., Eisenberger M.A., Carducci M.A., et al. Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat. Med. 2009, 15:559-565.
63. Lu X., Mu E., Wei Y., Riethdorf S., Yang Q., Yuan M., Yan J., Hua Y., Tiede B.J., Lu X., et al. VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging α4β1-positive osteoclast progenitors. Cancer Cell 2011, 20:701-714.
64. Lun M., Lok E., Gautam S., Wu E., Wong E.T. The natural history of extracranial metastasis from glioblastoma multiforme. J.Neurooncol. 2011, 105:261-273.
65. Luzzi K.J., MacDonald I.C., Schmidt E.E., Kerkvliet N., Morris V.L., Chambers A.F., Groom A.C. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153:865-873.
66. Magnon C., Hall S.J., Lin J., Xue X., Gerber L., Freedland S.J., Frenette P.S. Autonomic nerve development contributes to prostate cancer progression. Science 2013, 341:1236361.
67. Malanchi I., Santamaria-Martínez A., Susanto E., Peng H., Lehr H.A., Delaloye J.F., Huelsken J. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2012, 481:85-89.
68. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
69. McAllister S.S., Gifford A.M., Greiner A.L., Kelleher S.P., Saelzler M.P., Ince T.A., Reinhardt F., Harris L.N., Hylander B.L., Repasky E.A., Weinberg R.A. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 2008, 133:994-1005.
70. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., Viale A., Olshen A.B., Gerald W.L., Massagué J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524.
71. Minn A.J., Gupta G.P., Padua D., Bos P., Nguyen D.X., Nuyten D., Kreike B., Zhang Y., Wang Y., Ishwaran H., et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc. Natl. Acad. Sci. USA 2007, 104:6740-6745.
72. Nagrath S., Sequist L.V., Maheswaran S., Bell D.W., Irimia D., Ulkus L., Smith M.R., Kwak E.L., Digumarthy S., Muzikansky A., et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 2007, 450:1235-1239.
73. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., Cook K., Stepansky A., Levy D., Esposito D., et al. Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
74. Nguyen D.X., Bos P.D., Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 2009, 9:274-284.
75. Nguyen D.X., Chiang A.C., Zhang X.H., Kim J.Y., Kris M.G., Ladanyi M., Gerald W.L., Massagué J. WNT/TCF signaling through LEF1 and HOXB9 mediates lung adenocarcinoma metastasis. Cell 2009, 138:51-62.
76. Nieman K.M., Kenny H.A., Penicka C.V., Ladanyi A., Buell-Gutbrod R., Zillhardt M.R., Romero I.L., Carey M.S., Mills G.B., Hotamisligil G.S., et al. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 2011, 17:1498-1503.
77. Nowell P.C. The clonal evolution of tumor cell populations. Science 1976, 194:23-28.
78. Ocaña O.H., Córcoles R., Fabra A., Moreno-Bueno G., Acloque H., Vega S., Barrallo-Gimeno A., Cano A., Nieto M.A. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 2012, 22:709-724.
79. Oskarsson T., Acharyya S., Zhang X.H., Vanharanta S., Tavazoie S.F., Morris P.G., Downey R.J., Manova-Todorova K., Brogi E., Massagué J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 2011, 17:867-874.
80. Padua D., Zhang X.H., Wang Q., Nadal C., Gerald W.L., Gomis R.R., Massagué J. TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 2008, 133:66-77.
81. Park Y.G., Zhao X., Lesueur F., Lowy D.R., Lancaster M., Pharoah P., Qian X., Hunter K.W. Sipa1 is a candidate for underlying the metastasis efficiency modifier locus Mtes1. Nat. Genet. 2005, 37:1055-1062.
82. Pavlidis N., Pentheroudakis G. Cancer of unknown primary site. Lancet 2012, 379:1428-1435.
83. Pencheva N., Tran H., Buss C., Huh D., Drobnjak M., Busam K., Tavazoie S.F. Convergent multi-miRNA targeting of ApoE drives LRP1/LRP8-dependent melanoma metastasis and angiogenesis. Cell 2012, 151:1068-1082.
84. Pharoah P.D., Dunning A.M., Ponder B.A., Easton D.F. Association studies for finding cancer-susceptibility genetic variants. Nat. Rev. Cancer 2004, 4:850-860.
85. Png K.J., Halberg N., Yoshida M., Tavazoie S.F. A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature 2012, 481:190-194.
86. 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.
87. Popiolek M., Rider J.R., Andrén O., Andersson S.O., Holmberg L., Adami H.O., Johansson J.E. Natural history of early, localized prostate cancer: a final report from three decades of follow-up. Eur. Urol. 2013, 63:428-435.
88. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
89. Qin J., Wu S.P., Creighton C.J., Dai F., Xie X., Cheng C.M., Frolov A., Ayala G., Lin X., Feng X.H., et al. COUP-TFII inhibits TGF-β-induced growth barrier to promote prostate tumorigenesis. Nature 2013, 493:236-240.
90. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456:593-598.
91. Rhim A.D., Mirek E.T., Aiello N.M., Maitra A., Bailey J.M., McAllister F., Reichert M., Beatty G.L., Rustgi A.K., Vonderheide R.H., et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012, 148:349-361.
92. Ross-Innes C.S., Stark R., Teschendorff A.E., Holmes K.A., Ali H.R., Dunning M.J., Brown G.D., Gojis O., Ellis I.O., Green A.R., et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 2012, 481:389-393.
93. Roussos E.T., Condeelis J.S., Patsialou A. Chemotaxis in cancer. Nat. Rev. Cancer 2011, 11:573-587.
94. Schwitalla S., Ziegler P.K., Horst D., Becker V., Kerle I., Begus-Nahrmann Y., Lechel A., Rudolph K.L., Langer R., Slotta-Huspenina J., et al. Loss of p53 in enterocytes generates an inflammatory microenvironment enabling invasion and lymph node metastasis of carcinogen-induced colorectal tumors. Cancer Cell 2013, 23:93-106.
95. Scott K.L., Nogueira C., Heffernan T.P., van Doorn R., Dhakal S., Hanna J.A., Min C., Jaskelioff M., Xiao Y., Wu C.J., et al. Proinvasion metastasis drivers in early-stage melanoma are oncogenes. Cancer Cell 2011, 20:92-103.
96. Sethi N., Dai X., Winter C.G., Kang Y. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 2011, 19:192-205.
97. Shah S.P., Morin R.D., Khattra J., Prentice L., Pugh T., Burleigh A., Delaney A., Gelmon K., Guliany R., Senz J., et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009, 461:809-813.
98. Shiozawa Y., Pedersen E.A., Havens A.M., Jung Y., Mishra A., Joseph J., Kim J.K., Patel L.R., Ying C., Ziegler A.M., 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.
99. Sledge G.W. Heading in a new direction: drug permeability in breast cancer brain metastasis. Clin. Cancer Res. 2010, 16:5605-5607.
100. Sonoshita M., Aoki M., Fuwa H., Aoki K., Hosogi H., Sakai Y., Hashida H., Takabayashi A., Sasaki M., Robine S., et al. Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling. Cancer Cell 2011, 19:125-137.
101. Spinola M., Leoni V., Pignatiello C., Conti B., Ravagnani F., Pastorino U., Dragani T.A. Functional FGFR4 Gly388Arg polymorphism predicts prognosis in lung adenocarcinoma patients. J.Clin. Oncol. 2005, 23:7307-7311.
102. Staller P., Sulitkova J., Lisztwan J., Moch H., Oakeley E.J., Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 2003, 425:307-311.
103. Stott S.L., Lee R.J., Nagrath S., Yu M., Miyamoto D.T., Ulkus L., Inserra E.J., Ulman M., Springer S., Nakamura Z., et al. Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci. Transl. Med. 2010, 2:25ra23.
104. Stratton M.R., Campbell P.J., Futreal P.A. The cancer genome. Nature 2009, 458:719-724.
105. Talmadge J.E., Fidler I.J. Cancer metastasis is selective or random depending on the parent tumour population. Nature 1982, 297:593-594.
106. Talmadge J.E., Fidler I.J. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res. 2010, 70:5649-5669.
107. Tavazoie S.F., Alarcón C., Oskarsson T., Padua D., Wang Q., Bos P.D., Gerald W.L., Massagué J. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152.
108. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
109. Tsai J.H., Donaher J.L., Murphy D.A., Chau S., Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 2012, 22:725-736.
110. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
111. Valastyan S., Reinhardt F., Benaich N., Calogrias D., Szász A.M., Wang Z.C., Brock J.E., Richardson A.L., Weinberg R.A. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009, 137:1032-1046.
112. van 't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., Peterse H.L., van der Kooy K., Marton M.J., Witteveen A.T., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536.
113. van de Vijver M.J., He Y.D., van't Veer L.J., Dai H., Hart A.A., Voskuil D.W., Schreiber G.J., Peterse J.L., Roberts C., Marton M.J., et al. A gene-expression signature as a predictor of survival in breast cancer. N.Engl. J. Med. 2002, 347:1999-2009.
114. Vanharanta S., Shu W., Brenet F., Hakimi A.A., Heguy A., Viale A., Reuter V.E., Hsieh J.J., Scandura J.M., Massagué J. Epigenetic expansion of VHL-HIF signal output drives multiorgan metastasis in renal cancer. Nat. Med. 2013, 19:50-56.
115. Vesely M.D., Kershaw M.H., Schreiber R.D., Smyth M.J. Natural innate and adaptive immunity to cancer. Annu. Rev. Immunol. 2011, 29:235-271.
116. Weis S., Cui J., Barnes L., Cheresh D. Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J.Cell Biol. 2004, 167:223-229.
117. Werner J., Combs S.E., Springfeld C., Hartwig W., Hackert T., Büchler M.W. Advanced-stage pancreatic cancer: therapy options. Nat. Rev. Clin. Oncol. 2013, 10:323-333.
118. Winslow M.M., Dayton T.L., Verhaak R.G., Kim-Kiselak C., Snyder E.L., Feldser D.M., Hubbard D.D., DuPage M.J., Whittaker C.A., Hoersch S., et al. Suppression of lung adenocarcinoma progression by Nkx2-1. Nature 2011, 473:101-104.
119. Wolf M.J., Hoos A., Bauer J., Boettcher S., Knust M., Weber A., Simonavicius N., Schneider C., Lang M., Stürzl M., et al. Endothelial CCR2 signaling induced by colon carcinoma cells enables extravasation via the JAK2-Stat5 and p38MAPK pathway. Cancer Cell 2012, 22:91-105.
120. Wu X., Northcott P.A., Dubuc A., Dupuy A.J., Shih D.J., Witt H., Croul S., Bouffet E., Fults D.W., Eberhart C.G., et al. Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature 2012, 482:529-533.
121. Xing F., Kobayashi A., Okuda H., Watabe M., Pai S.K., Pandey P.R., Hirota S., Wilber A., Mo Y.Y., Moore B.E., et al. Reactive astrocytes promote the metastatic growth of breast cancer stem-like cells by activating Notch signalling in brain. EMBO Mol. Med. 2013, 5:384-396.
122. Yachida S., Jones S., Bozic I., Antal T., Leary R., Fu B., Kamiyama M., Hruban R.H., Eshleman J.R., Nowak M.A., et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
123. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
124. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
125. Yu M., Ting D.T., Stott S.L., Wittner B.S., Ozsolak F., Paul S., Ciciliano J.C., Smas M.E., Winokur D., Gilman A.J., et al. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 2012, 487:510-513.
126. Zhang X.H., Wang Q., Gerald W., Hudis C.A., Norton L., Smid M., Foekens J.A., Massagué J. Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009, 16:67-78.
127. Zhang X.H., Jin X., Malladi S., Zou Y., Wen Y.H., Brogi E., Smid M., Foekens J.A., Massagué J. Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma. Cell 2013, 154:1060-1073.