Abstract

The number of circulating tumor cell (CTC) in the peripheral blood of cancer patients can be a valuable biomarker for cancer diagnosis and treatment monitoring. In this study, we implemented a custom-design video-rate confocal microscopy system in capable of direct visualization of fast flowing CTC at great saphenous vein (GSV) of a live animal model in vivo. Continuous acquisition of video-rate images at GSV revealed the highly dynamic time-dependent changes in the number of intravenously injected circulating tumor cells. By extracting a calibration factor through the hemocytometric analysis of intravenously injected long-circulating red blood cells, we established a novel quantitation method for CTC in whole body blood in vivo.

© 2015 Optical Society of America

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References

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2014 (2)

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Y. Hwang, J. Ahn, J. Mun, S. Bae, Y. U. Jeong, N. A. Vinokurov, and P. Kim, “In vivo analysis of THz wave irradiation induced acute inflammatory response in skin by laser-scanning confocal microscopy,” Opt. Express 22(10), 11465–11475 (2014).
[PubMed]

2013 (4)

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

Y. Ding, J. Wang, Z. Fan, D. Wei, R. Shi, Q. Luo, D. Zhu, and X. Wei, “Signal and depth enhancement for in vivo flow cytometer measurement of ear skin by optical clearing agents,” Biomed. Opt. Express 4(11), 2518–2526 (2013).
[Crossref] [PubMed]

Y. A. Menyaev, D. A. Nedosekin, M. Sarimollaoglu, M. A. Juratli, E. I. Galanzha, V. V. Tuchin, and V. P. Zharov, “Optical clearing in photoacoustic flow cytometry,” Biomed. Opt. Express 4(12), 3030–3041 (2013).
[Crossref] [PubMed]

2012 (4)

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

E. I. Galanzha and V. P. Zharov, “Photoacoustic flow cytometry,” Methods 57(3), 280–296 (2012).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

C. Alix-Panabières, H. Schwarzenbach, and K. Pantel, “Circulating tumor cells and circulating tumor DNA,” Annu. Rev. Med. 63(1), 199–215 (2012).
[Crossref] [PubMed]

2011 (5)

M. Yu, S. Stott, M. Toner, S. Maheswaran, and D. A. Haber, “Circulating tumor cells: approaches to isolation and characterization,” J. Cell Biol. 192(3), 373–382 (2011).
[Crossref] [PubMed]

S. Valastyan and R. A. Weinberg, “Tumor metastasis: molecular insights and evolving paradigms,” Cell 147(2), 275–292 (2011).
[Crossref] [PubMed]

H. Ledford, “Cancer theory faces doubts,” Nature 472(7343), 273 (2011).
[Crossref] [PubMed]

X. Zhe, M. L. Cher, and R. D. Bonfil, “Circulating tumor cells: finding the needle in the haystack,” Am. J. Cancer Res. 1(6), 740–751 (2011).
[PubMed]

M. Sarimollaoglu, D. A. Nedosekin, Y. Simanovsky, E. I. Galanzha, and V. P. Zharov, “In vivo photoacoustic time-of-flight velocity measurement of single cells and nanoparticles,” Opt. Lett. 36(20), 4086–4088 (2011).
[Crossref] [PubMed]

2010 (3)

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
[Crossref] [PubMed]

M. C. Miller, G. V. Doyle, and L. W. Terstappen, “Significance of circulating tumor cells detected by the CellSearch system in patients with metastatic breast colorectal and prostate cancer,” J. Oncol. 2010, 617421 (2010).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

2009 (3)

J. A. Joyce and J. W. Pollard, “Microenvironmental regulation of metastasis,” Nat. Rev. Cancer 9(4), 239–252 (2009).
[Crossref] [PubMed]

K. Polyak and R. A. Weinberg, “Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits,” Nat. Rev. Cancer 9(4), 265–273 (2009).
[Crossref] [PubMed]

E. I. Galanzha, E. V. Shashkov, P. M. Spring, J. Y. Suen, and V. P. Zharov, “In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser,” Cancer Res. 69(20), 7926–7934 (2009).
[Crossref] [PubMed]

2008 (2)

H. Lee, E. Sun, D. Ham, and R. Weissleder, “Chip-NMR biosensor for detection and molecular analysis of cells,” Nat. Med. 14(8), 869–874 (2008).
[Crossref] [PubMed]

S. J. Cohen, C. J. Punt, N. Iannotti, B. H. Saidman, K. D. Sabbath, N. Y. Gabrail, J. Picus, M. Morse, E. Mitchell, M. C. Miller, G. V. Doyle, H. Tissing, L. W. Terstappen, and N. J. Meropol, “Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer,” J. Clin. Oncol. 26(19), 3213–3221 (2008).
[PubMed]

2007 (2)

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
[Crossref] [PubMed]

W. He, H. Wang, L. C. Hartmann, J. X. Cheng, and P. S. Low, “In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11760–11765 (2007).
[Crossref] [PubMed]

2006 (2)

G. P. Gupta and J. Massagué, “Cancer metastasis: building a framework,” Cell 127(4), 679–695 (2006).
[Crossref] [PubMed]

P. S. Steeg, “Tumor metastasis: mechanistic insights and clinical challenges,” Nat. Med. 12(8), 895–904 (2006).
[Crossref] [PubMed]

2004 (3)

M. Cristofanilli, L. W. M. M. Terstappen, and D. F. Hayes, “Circulating epithelial cells in breast cancer - Reply,” N. Engl. J. Med. 351, 2453–2454 (2004).

I. Georgakoudi, N. Solban, J. Novak, W. L. Rice, X. Wei, T. Hasan, and C. P. Lin, “In vivo flow cytometry: A new method for enumerating circulating cancer cells,” Cancer Res. 64(15), 5044–5047 (2004).
[Crossref] [PubMed]

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(1), 77–79 (2004).
[Crossref] [PubMed]

2002 (1)

A. F. Chambers, A. C. Groom, and I. C. MacDonald, “Dissemination and growth of cancer cells in metastatic sites,” Nat. Rev. Cancer 2(8), 563–572 (2002).
[Crossref] [PubMed]

1999 (1)

R. A. Ghossein, S. Bhattacharya, and J. Rosai, “Molecular detection of micrometastases and circulating tumor cells in solid tumors,” Clin. Cancer Res. 5(8), 1950–1960 (1999).
[PubMed]

1970 (1)

I. J. Fidler, “Metastasis: quantitative analysis of distribution and fate of tumor embolilabeled with 125 I-5-Iodo-2′-Deoxyuridine,” J. Natl. Cancer Inst. 45(4), 773–782 (1970).
[PubMed]

Aceto, N.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Ahn, J.

Alagesan, B.

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

Alix-Panabières, C.

C. Alix-Panabières, H. Schwarzenbach, and K. Pantel, “Circulating tumor cells and circulating tumor DNA,” Annu. Rev. Med. 63(1), 199–215 (2012).
[Crossref] [PubMed]

Bae, S.

Balis, U. J.

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
[Crossref] [PubMed]

Bardeesy, N.

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

Bardia, A.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

Baselga, J.

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

Bell, D. W.

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
[Crossref] [PubMed]

Bhattacharya, S.

R. A. Ghossein, S. Bhattacharya, and J. Rosai, “Molecular detection of micrometastases and circulating tumor cells in solid tumors,” Clin. Cancer Res. 5(8), 1950–1960 (1999).
[PubMed]

Bonfil, R. D.

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M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
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A. F. Chambers, A. C. Groom, and I. C. MacDonald, “Dissemination and growth of cancer cells in metastatic sites,” Nat. Rev. Cancer 2(8), 563–572 (2002).
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W. He, H. Wang, L. C. Hartmann, J. X. Cheng, and P. S. Low, “In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11760–11765 (2007).
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X. Zhe, M. L. Cher, and R. D. Bonfil, “Circulating tumor cells: finding the needle in the haystack,” Am. J. Cancer Res. 1(6), 740–751 (2011).
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M. Cristofanilli, L. W. M. M. Terstappen, and D. F. Hayes, “Circulating epithelial cells in breast cancer - Reply,” N. Engl. J. Med. 351, 2453–2454 (2004).

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S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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Donaldson, M. C.

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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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
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S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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W. He, H. Wang, L. C. Hartmann, J. X. Cheng, and P. S. Low, “In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11760–11765 (2007).
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Hartwell, K.

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
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Hasan, T.

I. Georgakoudi, N. Solban, J. Novak, W. L. Rice, X. Wei, T. Hasan, and C. P. Lin, “In vivo flow cytometry: A new method for enumerating circulating cancer cells,” Cancer Res. 64(15), 5044–5047 (2004).
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Hayes, D. F.

M. Cristofanilli, L. W. M. M. Terstappen, and D. F. Hayes, “Circulating epithelial cells in breast cancer - Reply,” N. Engl. J. Med. 351, 2453–2454 (2004).

He, W.

W. He, H. Wang, L. C. Hartmann, J. X. Cheng, and P. S. Low, “In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11760–11765 (2007).
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Herschkowitz, J. I.

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
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Hollier, B. G.

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
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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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
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K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

Iannotti, N.

S. J. Cohen, C. J. Punt, N. Iannotti, B. H. Saidman, K. D. Sabbath, N. Y. Gabrail, J. Picus, M. Morse, E. Mitchell, M. C. Miller, G. V. Doyle, H. Tissing, L. W. Terstappen, and N. J. Meropol, “Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer,” J. Clin. Oncol. 26(19), 3213–3221 (2008).
[PubMed]

Irimia, D.

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
[Crossref] [PubMed]

Isakoff, S. J.

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
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[Crossref] [PubMed]

Ryan, D. P.

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
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Ryan, P.

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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S. J. Cohen, C. J. Punt, N. Iannotti, B. H. Saidman, K. D. Sabbath, N. Y. Gabrail, J. Picus, M. Morse, E. Mitchell, M. C. Miller, G. V. Doyle, H. Tissing, L. W. Terstappen, and N. J. Meropol, “Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer,” J. Clin. Oncol. 26(19), 3213–3221 (2008).
[PubMed]

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S. J. Cohen, C. J. Punt, N. Iannotti, B. H. Saidman, K. D. Sabbath, N. Y. Gabrail, J. Picus, M. Morse, E. Mitchell, M. C. Miller, G. V. Doyle, H. Tissing, L. W. Terstappen, and N. J. Meropol, “Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer,” J. Clin. Oncol. 26(19), 3213–3221 (2008).
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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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
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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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
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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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
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E. I. Galanzha, E. V. Shashkov, P. M. Spring, J. Y. Suen, and V. P. Zharov, “In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser,” Cancer Res. 69(20), 7926–7934 (2009).
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Shioda, T.

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M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
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S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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E. I. Galanzha, E. V. Shashkov, P. M. Spring, J. Y. Suen, and V. P. Zharov, “In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser,” Cancer Res. 69(20), 7926–7934 (2009).
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M. Yu, S. Stott, M. Toner, S. Maheswaran, and D. A. Haber, “Circulating tumor cells: approaches to isolation and characterization,” J. Cell Biol. 192(3), 373–382 (2011).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
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M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
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E. I. Galanzha, E. V. Shashkov, P. M. Spring, J. Y. Suen, and V. P. Zharov, “In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser,” Cancer Res. 69(20), 7926–7934 (2009).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

Tissing, H.

S. J. Cohen, C. J. Punt, N. Iannotti, B. H. Saidman, K. D. Sabbath, N. Y. Gabrail, J. Picus, M. Morse, E. Mitchell, M. C. Miller, G. V. Doyle, H. Tissing, L. W. Terstappen, and N. J. Meropol, “Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer,” J. Clin. Oncol. 26(19), 3213–3221 (2008).
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S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

M. Yu, S. Stott, M. Toner, S. Maheswaran, and D. A. Haber, “Circulating tumor cells: approaches to isolation and characterization,” J. Cell Biol. 192(3), 373–382 (2011).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
[Crossref] [PubMed]

Tsukrov, D. I.

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
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Ulkus, L.

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Ulman, M. J.

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
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Vinokurov, N. A.

Waltman, B. A.

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

Wang, H.

W. He, H. Wang, L. C. Hartmann, J. X. Cheng, and P. S. Low, “In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11760–11765 (2007).
[Crossref] [PubMed]

Wang, J.

Wei, D.

Wei, X.

Wei, X. B.

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

Weinberg, R. A.

S. Valastyan and R. A. Weinberg, “Tumor metastasis: molecular insights and evolving paradigms,” Cell 147(2), 275–292 (2011).
[Crossref] [PubMed]

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
[Crossref] [PubMed]

K. Polyak and R. A. Weinberg, “Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits,” Nat. Rev. Cancer 9(4), 265–273 (2009).
[Crossref] [PubMed]

Weissleder, R.

H. Lee, E. Sun, D. Ham, and R. Weissleder, “Chip-NMR biosensor for detection and molecular analysis of cells,” Nat. Med. 14(8), 869–874 (2008).
[Crossref] [PubMed]

Wells, M. N.

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

Weng, X. F.

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

Winokur, D.

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

Wittner, B. S.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

Wu, W. Z.

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

Xega, K.

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

Yan, J.

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

Yang, J.

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
[Crossref] [PubMed]

Yu, M.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

M. Yu, S. Stott, M. Toner, S. Maheswaran, and D. A. Haber, “Circulating tumor cells: approaches to isolation and characterization,” J. Cell Biol. 192(3), 373–382 (2011).
[Crossref] [PubMed]

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

Zharov, V. P.

Y. A. Menyaev, D. A. Nedosekin, M. Sarimollaoglu, M. A. Juratli, E. I. Galanzha, V. V. Tuchin, and V. P. Zharov, “Optical clearing in photoacoustic flow cytometry,” Biomed. Opt. Express 4(12), 3030–3041 (2013).
[Crossref] [PubMed]

E. I. Galanzha and V. P. Zharov, “Photoacoustic flow cytometry,” Methods 57(3), 280–296 (2012).
[Crossref] [PubMed]

M. Sarimollaoglu, D. A. Nedosekin, Y. Simanovsky, E. I. Galanzha, and V. P. Zharov, “In vivo photoacoustic time-of-flight velocity measurement of single cells and nanoparticles,” Opt. Lett. 36(20), 4086–4088 (2011).
[Crossref] [PubMed]

E. I. Galanzha, E. V. Shashkov, P. M. Spring, J. Y. Suen, and V. P. Zharov, “In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser,” Cancer Res. 69(20), 7926–7934 (2009).
[Crossref] [PubMed]

Zhe, X.

X. Zhe, M. L. Cher, and R. D. Bonfil, “Circulating tumor cells: finding the needle in the haystack,” Am. J. Cancer Res. 1(6), 740–751 (2011).
[PubMed]

Zhou, A. Y.

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
[Crossref] [PubMed]

Zhou, J.

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

Zhu, D.

Zhu, H.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Am. J. Cancer Res. (1)

X. Zhe, M. L. Cher, and R. D. Bonfil, “Circulating tumor cells: finding the needle in the haystack,” Am. J. Cancer Res. 1(6), 740–751 (2011).
[PubMed]

Annu. Rev. Med. (1)

C. Alix-Panabières, H. Schwarzenbach, and K. Pantel, “Circulating tumor cells and circulating tumor DNA,” Annu. Rev. Med. 63(1), 199–215 (2012).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Cancer Res. (3)

E. I. Galanzha, E. V. Shashkov, P. M. Spring, J. Y. Suen, and V. P. Zharov, “In vivo, noninvasive, label-free detection and eradication of circulating metastatic melanoma cells using two-color photoacoustic flow cytometry with a diode laser,” Cancer Res. 69(20), 7926–7934 (2009).
[Crossref] [PubMed]

Z. C. Fan, J. Yan, G. D. Liu, X. Y. Tan, X. F. Weng, W. Z. Wu, J. Zhou, and X. B. Wei, “Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis,” Cancer Res. 72(10), 2683–2691 (2012).
[Crossref] [PubMed]

I. Georgakoudi, N. Solban, J. Novak, W. L. Rice, X. Wei, T. Hasan, and C. P. Lin, “In vivo flow cytometry: A new method for enumerating circulating cancer cells,” Cancer Res. 64(15), 5044–5047 (2004).
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Cell (3)

S. Valastyan and R. A. Weinberg, “Tumor metastasis: molecular insights and evolving paradigms,” Cell 147(2), 275–292 (2011).
[Crossref] [PubMed]

G. P. Gupta and J. Massagué, “Cancer metastasis: building a framework,” Cell 127(4), 679–695 (2006).
[Crossref] [PubMed]

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Clin. Cancer Res. (1)

R. A. Ghossein, S. Bhattacharya, and J. Rosai, “Molecular detection of micrometastases and circulating tumor cells in solid tumors,” Clin. Cancer Res. 5(8), 1950–1960 (1999).
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J. Biomed. Opt. (1)

K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

J. Cell Biol. (1)

M. Yu, S. Stott, M. Toner, S. Maheswaran, and D. A. Haber, “Circulating tumor cells: approaches to isolation and characterization,” J. Cell Biol. 192(3), 373–382 (2011).
[Crossref] [PubMed]

J. Clin. Oncol. (1)

S. J. Cohen, C. J. Punt, N. Iannotti, B. H. Saidman, K. D. Sabbath, N. Y. Gabrail, J. Picus, M. Morse, E. Mitchell, M. C. Miller, G. V. Doyle, H. Tissing, L. W. Terstappen, and N. J. Meropol, “Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer,” J. Clin. Oncol. 26(19), 3213–3221 (2008).
[PubMed]

J. Natl. Cancer Inst. (1)

I. J. Fidler, “Metastasis: quantitative analysis of distribution and fate of tumor embolilabeled with 125 I-5-Iodo-2′-Deoxyuridine,” J. Natl. Cancer Inst. 45(4), 773–782 (1970).
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J. Oncol. (1)

M. C. Miller, G. V. Doyle, and L. W. Terstappen, “Significance of circulating tumor cells detected by the CellSearch system in patients with metastatic breast colorectal and prostate cancer,” J. Oncol. 2010, 617421 (2010).
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Methods (1)

E. I. Galanzha and V. P. Zharov, “Photoacoustic flow cytometry,” Methods 57(3), 280–296 (2012).
[Crossref] [PubMed]

N. Engl. J. Med. (1)

M. Cristofanilli, L. W. M. M. Terstappen, and D. F. Hayes, “Circulating epithelial cells in breast cancer - Reply,” N. Engl. J. Med. 351, 2453–2454 (2004).

Nat. Med. (2)

P. S. Steeg, “Tumor metastasis: mechanistic insights and clinical challenges,” Nat. Med. 12(8), 895–904 (2006).
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H. Lee, E. Sun, D. Ham, and R. Weissleder, “Chip-NMR biosensor for detection and molecular analysis of cells,” Nat. Med. 14(8), 869–874 (2008).
[Crossref] [PubMed]

Nat. Rev. Cancer (3)

K. Polyak and R. A. Weinberg, “Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits,” Nat. Rev. Cancer 9(4), 265–273 (2009).
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A. F. Chambers, A. C. Groom, and I. C. MacDonald, “Dissemination and growth of cancer cells in metastatic sites,” Nat. Rev. Cancer 2(8), 563–572 (2002).
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J. A. Joyce and J. W. Pollard, “Microenvironmental regulation of metastasis,” Nat. Rev. Cancer 9(4), 239–252 (2009).
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Nature (3)

H. Ledford, “Cancer theory faces doubts,” Nature 472(7343), 273 (2011).
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S. Nagrath, L. V. Sequist, S. Maheswaran, D. W. Bell, D. Irimia, L. Ulkus, M. R. Smith, E. L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U. J. Balis, R. G. Tompkins, D. A. Haber, and M. Toner, “Isolation of rare circulating tumour cells in cancer patients by microchip technology,” Nature 450(7173), 1235–1239 (2007).
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M. Yu, D. T. Ting, S. L. Stott, B. S. Wittner, F. Ozsolak, S. Paul, J. C. Ciciliano, M. E. Smas, D. Winokur, A. J. Gilman, M. J. Ulman, K. Xega, G. Contino, B. Alagesan, B. W. Brannigan, P. M. Milos, D. P. Ryan, L. V. Sequist, N. Bardeesy, S. Ramaswamy, M. Toner, S. Maheswaran, and D. A. Haber, “RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis,” Nature 487(7408), 510–513 (2012).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (2)

Proc. Natl. Acad. Sci. U.S.A. (2)

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, G. K. Korir, F. P. Floyd, A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, and M. Toner, “Isolation of circulating tumor cells using a microvortex-generating herringbone-chip,” Proc. Natl. Acad. Sci. U.S.A. 107(43), 18392–18397 (2010).
[Crossref] [PubMed]

W. He, H. Wang, L. C. Hartmann, J. X. Cheng, and P. S. Low, “In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11760–11765 (2007).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. USA (1)

J. H. Taube, J. I. Herschkowitz, K. Komurov, A. Y. Zhou, S. Gupta, J. Yang, K. Hartwell, T. T. Onder, P. B. Gupta, K. W. Evans, B. G. Hollier, P. T. Ram, E. S. Lander, J. M. Rosen, R. A. Weinberg, and S. A. Mani, “Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes,” Proc. Natl. Acad. Sci. USA 107(35), 15449–15454 (2010).
[Crossref] [PubMed]

Science (1)

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, A. M. Shah, K. F. Concannon, M. C. Donaldson, L. V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition,” Science 339(6119), 580–584 (2013).
[Crossref] [PubMed]

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Figures (4)

Fig. 1
Fig. 1

Schematic of intravital custom-built video-rate laser scanning confocal microscope system and illustration of great saphenous vein (GSV) in the mouse leg: ND, neutral density filer; DBS, dichroic beam splitter; BPF, band pass filter; M, mirror; PMT, photomultiplier tube; OBJ, objective lens.

Fig. 2
Fig. 2

In vivo imaging of intravenous injected circulating CT26 colorectal cancer cells at great saphenous vein (GSV), (a) Raw image and processed results with increasing object size threshold, (b) Time-domain kinetics of the number of detected object with different object size threshold. Inset shows the magnified curve during 15-20 minutes after the IV injection. Scale bar, 20µm.

Fig. 3
Fig. 3

Size-dependent analysis of circulating tumor cells and cellular fragment detected at GSV, (a) Histogram representing the size distribution of detected circulating objects at different time points, (b) Time-dependent changes of detected objects size distribution.

Fig. 4
Fig. 4

In vivo quantitation of CTCs through hemocytometric analysis of intravenously injected RBCs in whole body, (a) Representative images of fast flowing CT26 cell and RBC captured in GSV at video-rate (30 frames/second). (b) Number of circulating CT26 cells and RBCs detected at GSV after IV injection. After 3 minutes, average account of CT26 cells and RBCs were maintained at ~9.7 ± 2.2 and ~122.8 ± 13.6 per 30 seconds, respectively. (c) Distribution of circulating CT26 cells and RBCs after 3 minutes to 1 hour. Scale bar is 20µm.

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