Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis

Cell

Volumn 158, Issue 5, 2014, Pages 1110-1122

  Aceto, Nicola ^a   Bardia, Aditya ^a   Miyamoto, David T ^a   Donaldson, Maria C ^a   Wittner, Ben S ^a   Spencer, Joel A ^b,c   Yu, Min ^a   Pely, Adam ^b,c   Engstrom, Amanda ^a   Zhu, Huili ^a   Brannigan, Brian W ^a   Kapur, Ravi ^a   Stott, Shannon L ^a   Shioda, Toshi ^a   Ramaswamy, Sridhar ^a   Ting, David T ^a   Lin, Charles P ^b,c   Toner, Mehmet ^a   Haber, Daniel A ^a,d   Maheswaran, Shyamala ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLAKOGLOBIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; BREAST METASTASIS; CANCER PATIENT; CELL ADHESION; CELL AGGREGATION; CELL JUNCTION; CIRCULATING TUMOR CELL; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; METASTASIS POTENTIAL; MODEL; MOUSE; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; RNA SEQUENCE; ANIMAL; BREAST TUMOR; DISEASE MODEL; MALE; METABOLISM; METASTASIS; NONOBESE DIABETIC MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PROSTATE TUMOR; SCID MOUSE; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; TUMOR CELL LINE; TUMOR EMBOLISM;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; GAMMA CATENIN; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; PROSTATIC NEOPLASMS; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS;

EID: 84907342688     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.07.013     Document Type: Article

References (52)

1. Z. Aktary, and M. Pasdar Plakoglobin: role in tumorigenesis and metastasis Int. J. Cell Biol. 2012 2012 189521
2. D. Alford, and J. Taylor-Papadimitriou Cell adhesion molecules in the normal and cancerous mammary gland J. Mammary Gland Biol. Neoplasia 1 1996 207 218
3. C. Alix-Panabières, and K. Pantel Circulating tumor cells: liquid biopsy of cancer Clin. Chem. 59 2013 110 118
4. I. Baccelli, A. Schneeweiss, S. Riethdorf, A. Stenzinger, A. Schillert, V. Vogel, C. Klein, M. Saini, T. Bäuerle, and M. Wallwiener et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay Nat. Biotechnol. 31 2013 539 544
5. 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
6. U. Cavallaro, and G. Christofori Cell adhesion and signalling by cadherins and Ig-CAMs in cancer Nat. Rev. Cancer 4 2004 118 132
7. E.H. Cho, M. Wendel, M. Luttgen, C. Yoshioka, D. Marrinucci, D. Lazar, E. Schram, J. Nieva, L. Bazhenova, and A. Morgan et al. Characterization of circulating tumor cell aggregates identified in patients with epithelial tumors Phys. Biol. 9 2012 016001
8. D.G. Duda, A.M. Duyverman, M. Kohno, M. Snuderl, E.J. Steller, D. Fukumura, and R.K. Jain Malignant cells facilitate lung metastasis by bringing their own soil Proc. Natl. Acad. Sci. USA 107 2010 21677 21682
9. J. El Khoury, S.E. Hickman, C.A. Thomas, L. Cao, S.C. Silverstein, and J.D. Loike Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils Nature 382 1996 716 719
10. I.J. Fidler The relationship of embolic homogeneity, number, size and viability to the incidence of experimental metastasis Eur. J. Cancer 9 1973 223 227
11. I.J. Fidler The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited Nat. Rev. Cancer 3 2003 453 458
12. P. Friedl, and D. Gilmour Collective cell migration in morphogenesis, regeneration and cancer Nat. Rev. Mol. Cell Biol. 10 2009 445 457
13. D. Garrod, and M. Chidgey Desmosome structure, composition and function Biochim. Biophys. Acta 1778 2008 572 587
14. S. Hakimelahi, H.R. Parker, A.J. Gilchrist, M. Barry, Z. Li, R.C. Bleackley, and M. Pasdar Plakoglobin regulates the expression of the anti-apoptotic protein BCL-2 J. Biol. Chem. 275 2000 10905 10911
15. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
16. T.J. Harris, and U. Tepass Adherens junctions: from molecules to morphogenesis Nat. Rev. Mol. Cell Biol. 11 2010 502 514
17. 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
18. F.T. Kolligs, B. Kolligs, K.M. Hajra, G. Hu, M. Tani, K.R. Cho, and E.R. Fearon gamma-catenin is regulated by the APC tumor suppressor and its oncogenic activity is distinct from that of beta-catenin Genes Dev. 14 2000 1319 1331
19. M. Labelle, S. Begum, and R.O. Hynes Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis Cancer Cell 20 2011 576 590
20. H. Ledford Cancer theory faces doubts Nature 472 2011 273
21. L.A. Liotta, M.G. Saidel, and J. Kleinerman The significance of hematogenous tumor cell clumps in the metastatic process Cancer Res. 36 1976 889 894
22. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, and M. Shipitsin et al. The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
23. 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
24. D.T. Miyamoto, R.J. Lee, S.L. Stott, D.T. Ting, B.S. Wittner, M. Ulman, M.E. Smas, J.B. Lord, B.W. Brannigan, and J. Trautwein et al. Androgen receptor signaling in circulating tumor cells as a marker of hormonally responsive prostate cancer Cancer Discov 2 2012 995 1003
25. B. Molnar, A. Ladanyi, L. Tanko, L. Sréter, and Z. Tulassay Circulating tumor cell clusters in the peripheral blood of colorectal cancer patients Clin. Cancer Res. 7 2001 4080 4085
26. 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 et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology Nature 450 2007 1235 1239
27. D.X. Nguyen, P.D. Bos, and J. Massagué Metastasis: from dissemination to organ-specific colonization Nat. Rev. Cancer 9 2009 274 284
28. E. Ozkumur, A.M. Shah, J.C. Ciciliano, B.L. Emmink, D.T. Miyamoto, E. Brachtel, M. Yu, P.I. Chen, B. Morgan, and J. Trautwein et al. Inertial focusing for tumor antigen-dependent and -independent sorting of rare circulating tumor cells Sci. Transl. Med. 5 2013 79ra47
29. E.J. Robson, W.T. Khaled, K. Abell, and C.J. Watson Epithelial-to- mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines Differentiation 74 2006 254 264
30. H. Shiina, J.E. Breault, W.W. Basset, H. Enokida, S. Urakami, L.C. Li, S.T. Okino, M. Deguchi, M. Kaneuchi, and M. Terashima et al. Functional Loss of the gamma-catenin gene through epigenetic and genetic pathways in human prostate cancer Cancer Res. 65 2005 2130 2138
31. 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 et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip Proc. Natl. Acad. Sci. USA 107 2010 18392 18397
32. F. Tang, C. Barbacioru, E. Nordman, B. Li, N. Xu, V.I. Bashkirov, K. Lao, and M.A. Surani RNA-Seq analysis to capture the transcriptome landscape of a single cell Nat. Protoc. 5 2010 516 535
33. D. Tarin, E.W. Thompson, and D.F. Newgreen The fallacy of epithelial mesenchymal transition in neoplasia Cancer Res. 65 2005 5996 6000 discussion 6000-6001
34. M. Yu, S. Stott, M. Toner, S. Maheswaran, and D.A. Haber Circulating tumor cells: approaches to isolation and characterization J. Cell Biol. 192 2011 373 382
35. M. Yu, D.T. Ting, S.L. Stott, B.S. Wittner, F. Ozsolak, S. Paul, J.C. Ciciliano, M.E. Smas, D. Winokur, and A.J. Gilman et al. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis Nature 487 2012 510 513
36. M. Yu, A. Bardia, B.S. Wittner, S.L. Stott, M.E. Smas, D.T. Ting, S.J. Isakoff, J.C. Ciciliano, M.N. Wells, and A.M. Shah et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition Science 339 2013 580 584
37. 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
38. X.H. Zhang, X. Jin, S. Malladi, Y. Zou, Y.H. Wen, E. Brogi, M. Smid, J.A. Foekens, and J. Massagué Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma Cell 154 2013 1060 1073
39. M. Chanrion, V. Negre, H. Fontaine, N. Salvetat, F. Bibeau, G. Mac Grogan, L. Mauriac, D. Katsaros, F. Molina, C. Theillet, and J.M. Darbon A gene expression signature that can predict the recurrence of tamoxifen-treated primary breast cancer Clin. Cancer Res. 14 2008 1744 1752
40. K. Chin, S. DeVries, J. Fridlyand, P.T. Spellman, R. Roydasgupta, W.L. Kuo, A. Lapuk, R.M. Neve, Z. Qian, and T. Ryder et al. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies Cancer Cell 10 2006 529 541
41. C. Desmedt, F. Piette, S. Loi, Y. Wang, F. Lallemand, B. Haibe-Kains, G. Viale, M. Delorenzi, Y. Zhang, M.S. d'Assignies TRANSBIG Consortium Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series Clin. Cancer Res. 13 2007 3207 3214
42. Y. Li, L. Zou, Q. Li, B. Haibe-Kains, R. Tian, Y. Li, C. Desmedt, C. Sotiriou, Z. Szallasi, and J.D. Iglehart et al. Amplification of LAPTM4B and YWHAZ contributes to chemotherapy resistance and recurrence of breast cancer Nat. Med. 16 2010 214 218
43. S. Loi, B. Haibe-Kains, C. Desmedt, P. Wirapati, F. Lallemand, A.M. Tutt, C. Gillet, P. Ellis, K. Ryder, and J.F. Reid et al. Predicting prognosis using molecular profiling in estrogen receptor-positive breast cancer treated with tamoxifen BMC Genomics 9 2008 239
44. X.J. Ma, Z. Wang, P.D. Ryan, S.J. Isakoff, A. Barmettler, A. Fuller, B. Muir, G. Mohapatra, R. Salunga, and J.T. Tuggle et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen Cancer Cell 5 2004 607 616
45. A.J. Minn, G.P. Gupta, D. Padua, P. Bos, D.X. Nguyen, D. Nuyten, B. Kreike, Y. Zhang, Y. Wang, and H. Ishwaran et al. Lung metastasis genes couple breast tumor size and metastatic spread Proc. Natl. Acad. Sci. USA 104 2007 6740 6745
46. J. Novak, I. Georgakoudi, X. Wei, A. Prossin, and C.P. Lin In vivo flow cytometer for real-time detection and quantification of circulating cells Opt. Lett. 29 2004 77 79
47. M. Schmidt, D. Böhm, C. von Törne, E. Steiner, A. Puhl, H. Pilch, H.A. Lehr, J.G. Hengstler, H. Kölbl, and M. Gehrmann The humoral immune system has a key prognostic impact in node-negative breast cancer Cancer Res. 68 2008 5405 5413
48. C. Sotiriou, P. Wirapati, S. Loi, A. Harris, S. Fox, J. Smeds, H. Nordgren, P. Farmer, V. Praz, and B. Haibe-Kains et al. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis J. Natl. Cancer Inst. 98 2006 262 272
49. M.J. van de Vijver, Y.D. He, L.J. van't Veer, H. Dai, A.A. Hart, D.W. Voskuil, G.J. Schreiber, J.L. Peterse, C. Roberts, and M.J. Marton et al. A gene-expression signature as a predictor of survival in breast cancer N. Engl. J. Med. 347 2002 1999 2009
50. 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 et al. Gene expression profiling predicts clinical outcome of breast cancer Nature 415 2002 530 536
51. Y. Wang, J.G. Klijn, Y. Zhang, A.M. Sieuwerts, M.P. Look, F. Yang, D. Talantov, M. Timmermans, M.E. Meijer-van Gelder, and J. Yu et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer Lancet 365 2005 671 679
52. L. Wang, Z. Feng, X. Wang, X. Wang, and X. Zhang DEGseq: an R package for identifying differentially expressed genes from RNA-seq data Bioinformatics 26 2010 136 138