Single-cell migration chip for chemotaxis-based microfluidic selection of heterogeneous cell populations

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Chen, Yu Chih ^a   Allen, Steven G ^b   Ingram, Patrick N ^a   Buckanovich, Ronald ^a   Merajver, Sofia D ^b,c   Yoon, Euisik ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MOTION; CHEMOTAXIS; DEVICES; HUMAN; MICROFLUIDIC ANALYSIS; PROCEDURES; SINGLE CELL ANALYSIS; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; HUMANS; MICROFLUIDIC ANALYTICAL TECHNIQUES; SINGLE-CELL ANALYSIS;

EID: 84929589961     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09980     Document Type: Article

References (55)

1. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell. 144, 646-674 (2011).
2. Steeg, P. S. Tumor metastasis: mechanistic insights and clinical challenges. Nat. Med. 12, 895-904 (2006).
3. Nathanson, S. D. Insights into the mechanisms of lymph node metastasis. Cancer 98, 413-423 (2003).
4. Sethi, N. & Kang, Y. Unravelling the complexity of metastasis - molecular understanding and targeted therapies. Nat. Rev. Cancer 11, 735-748 (2011).
5. Yoshida, B. A., Sokoloff, M. M., Welch, D. R. & Rinker-Schaeffer, C. W. Metastasis-suppressor genes: a review and perspective on an emerging field. J. Natl. Cancer Inst. 92, 1717-1730 (2000).
6. Gobeil, S., Zhu, X., Doillon, C. J. & Green, M. R. A genome-wide shRNA screen identifies GAS1 as a novel melanoma metastasis suppressor gene. Genes. Dev. 22, 2932-2940 (2008).
7. Shoushtari, A. N., Szmulewitz, R. Z. & Rinker-Schaeffer, C. W. Metastasis-suppressor genes in clinical practice: lost in translation? Nat. Rev. Clin Oncol 8, 333-342 (2011).
8. Steeg, P. S. Metastasis suppressors alter the signal transduction of cancer cells. Nat. Rev. Cancer 3, 55-63 (2003).
9. Rodriguez, L. G., Wu, X. & Guan, J. L. Wound-healing assay. Methods Mol. Biol. 294, 23-29 (2005).
10. Chen, H. C. Boyden chamber assay. Methods Mol. Biol. 294, 15-22 (2005).
11. Xie, Y. et al. A microchip-based model wound with multiple types of cells. Lab Chip. 11, 2819-2822 (2011).
12. Irimia, D., Charras, G., Agrawal, N., Mitchison, T. & Toner, M. Polar stimulation and constrained cell migration in microfluidic channels. Lab. Chip. 7, 1783-1790 (2007).
13. Shin, M. K., Kim, S. K. & Jung, H. Integration of intra- and extravasation in one cell-based microfluidic chip for the study of cancer metastasis. Lab. Chip. 11, 3880-3887 (2011).
14. Yan, J. & Irimia, D. Stochastic variations of migration speed between cells in clonal populations. Technology (Singap World Sci.) 2, 185-188 (2014).
15. Desai, S. P., Bhatia, S. N., Toner, M. & Irimia, D. Mitochondrial localization and the persistent migration of epithelial cancer cells. Biophys. J. 104, 2077-2088 (2013).
16. Bajpai, S., Mitchell, M. J., King, M. R. & Reinhart-King, C. A. A microfluidic device to select for cells based on chemotactic phenotype. Technology (Singap World Sci) 2, 101-105 (2014).
17. Irimia, D. & Toner, M. Spontaneous migration of cancer cells under conditions of mechanical confinement. Integr. Biol. (Camb) I, 506-512 (2009).
18. Mak, M., Reinhart-King, C. A. & Erickson, D. Microfabricated physical spatial gradients for investigating cell migration and invasion dynamics. PloS. One 6, e20825 (2011).
19. Gallego-Perez, D. et al. Microfabricated mimics of in vivo structural cues for the study of guided tumor cell migration. Lab. Chip. 12, 4424-4432 (2012).
20. Ko, Y. G., Co, C. C. & Ho, C. C. Gradient-free directional cell migration in continuous microchannels. Soft. Matter 9, 2467-2474 (2013).
21. Chung, S. et al. Cell migration into scaffolds under co-culture conditions in a microfluidic platform. Lab. Chip. 9, 269-275 (2009).
22. De Cock, L. J. et al. Engineered 3D microporous gelatin scaffolds to study cell migration. Chem. Commun. (Camb) 48, 3512-3514 (2012).
23. Chaw, K. C., Manimaran, M., Tay, E. H. & Swaminathan, S. Multi-step microfluidic device for studying cancer metastasis. Lab. Chip. 7, 1041-1047 (2007).
24. Kaji, H., Yokoi, T., Kawashima, T. & Nishizawa, M. Controlled cocultures of HeLa cells and human umbilical vein endothelial cells on detachable substrates. Lab. Chip. 9, 427-432 (2009).
25. Jeon, J. S., Zervantonakis, I. K., Chung, S., Kamm, R. D. & Charest, J. L. In vitro model of tumor cell extravasation. PloS. One 8, e56910 (2013).
26. Culligan, K. et al. A detailed appraisal of mesocolic lymphangiology - an immunohistochemical and stereological analysis. J. Anat. 225, 463-472 (2014).
27. Zhong, S. Q., Xu, Y. D., Zhang, Y. F., Hai, L. S. & Tang, F. C. Three-dimensional structure of lymphatics in rabbit stomach. World J. Gastroenterol 4, 550-552 (1998).
28. Nakayama, A., Ogawa, A., Fukuta, Y. & Kudo, K. Relation between lymphatic vessel diameter and clinicopathologic parameters in squamous cell carcinomas of the oral region. Cancer 86, 200-206 (1999).
29. Altschuler, S. J. & Wu, L. F. Cellular heterogeneity: do differences make a difference? Cell. 141, 559-563 (2010).
30. Magee, J. A., Piskounova, E. & Morrison, S. J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell. 21, 283-296 (2012).
31. Negrini, S., Gorgoulis, V. G. & Halazonetis, T. D. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell. Biol. II, 220-228 (2010).
32. Hong, S., Pan, Q. & Lee, L. P. Single-cell level co-culture platform for intercellular communication. Integr. Biol. (Camb) 4, 374-380 (2012).
33. Zheng, C. et al. Live cell imaging analysis of the epigenetic regulation of the human endothelial cell migration at single-cell resolution. Lab. Chip. 12, 3063-3072 (2012).
34. Kraning-Rush, C. M., Carey, S. P., Lampi, M. C. & Reinhart-King, C. A. Microfabricated collagen tracks facilitate single cell metastatic invasion in 3D. Integr. Biol. (Camb) 5, 606-616 (2013).
35. Mak, M. & Erickson, D. Mechanical decision trees for investigating and modulating single-cell cancer invasion dynamics. Lab. Chip. 14, 964-971 (2014).
36. Pushkarsky, I. et al. Automated single-cell motility analysis on a chip using lensfree microscopy. Sci. Rep. 4, 4717 (2014).
37. Stroka, K. M. et al. Water permeation drives tumor cell migration in confined microenvironments. Cell. 157, 611-623 (2014).
38. Rosenthal, D. T. et al. p38gamma promotes breast cancer cell motility and metastasis through regulation of RhoC GTPase, cytoskeletal architecture, and a novel leading edge behavior. Cancer Res. 71, 6338-6349 (2011).
39. Frimat, J. P. et al. A microfluidic array with cellular valving for single cell co-culture. Lab. Chip. 11, 231-237 (2011).
40. Tan, W. H. & Takeuchi, S. A trap-and-release integrated microfluidic system for dynamic microarray applications. Proc Natl Acad Sci U S A 104, 1146-1151 (2007).
41. Chen, Y. C. et al. Paired single cell co-culture microenvironments isolated by two-phase flow with continuous nutrient renewal. Lab Chip. 14, 2941-2947 (2014).
42. Joyce, J. A. & Pollard, J. W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252 (2009).
43. Kakinuma, T. & Hwang, S. T. Chemokines, chemokine receptors, and cancer metastasis. J Leukoc Biol. 79, 639-651 (2006).
44. Koizumi, K., Hojo, S., Akashi, T., Yasumoto, K. & Saiki, I. Chemokine receptors in cancer metastasis and cancer cell-derived chemokines in host immune response. Cancer Sci. 98, 1652-1658 (2007).
45. Walker, G. M. et al. Effects of flow and diffusion on chemotaxis studies in a microfabricated gradient generator. Lab. Chip. 5, 611-618 (2005).
46. Scarpino, S. et al. Hepatocyte growth factor (HGF) stimulates tumour invasiveness in papillary carcinoma of the thyroid. J. Pathol 189, 570-575 (1999).
47. Wei, W., Kong, B., Yang, Q. & Qu, X. Hepatocyte growth factor enhances ovarian cancer cell invasion through downregulation of thrombospondin-1. Cancer Biol. Ther. 9, 79-87 (2010).
48. Yang, J. & Weinberg, R. A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell. 14, 818-829 (2008).
49. Kalluri, R. & Weinberg, R. A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428 (2009).
50. Nieto, M. A. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell. Dev. Biol. 27, 347-376 (2011).
51. Rosenthal, D. T. et al. RhoC impacts the metastatic potential and abundance of breast cancer stem cells. PloS. One 7, e40979 (2012).
52. Kleer, C. G. et al. RhoC-GTPase is a novel tissue biomarker associated with biologically aggressive carcinomas of the breast. Breast. Cancer Res. Treat. 93, 101-110 (2005).
53. Qi, X. et al. p38gamma mitogen-activated protein kinase integrates signaling crosstalk between Ras and estrogen receptor to increase breast cancer invasion. Cancer Res. 66, 7540-7547 (2006).
54. Lehman, H. L. et al. Regulation of inflammatory breast cancer cell invasion through Akt1/PKBalpha phosphorylation of RhoC GTPase. Mol. Cancer Res. 10, 1306-1318 (2012).
55. Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic. Acids. Res. 30, e36 (2002).