Microfluidics: A New Tool for Modeling Cancer–Immune Interactions

Trends in Cancer

Volumn 2, Issue 1, 2016, Pages 6-19

  Boussommier Calleja, Alexandra ^a   Li, Ran ^a   Chen, Michelle B ^a   Wong, Siew Cheng ^b   Kamm, Roger D ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b AGENCY FOR SCIENCE   (Singapore)

Author keywords

drug screening; immunotherapy; metastatic cancer; microfluidics

Indexed keywords

CANCER CELL; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER RESEARCH; CELL INTERACTION; EXPERIMENTAL MODEL; HUMAN; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MICROFLUIDICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT;

EID: 84988736194     PISSN: 24058033     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.trecan.2015.12.003     Document Type: Review

References (115)

1. 1 Turcotte, S., Rosenberg, S.A., Immunotherapy for metastatic solid cancers. Adv. Surg. 45 (2011), 341–360.
2. 2 Pardoll, D.M., The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12 (2012), 252–264.
3. 3 Dranoff, G., Experimental mouse tumour models: what can be learnt about human cancer immunology?. Nat. Rev. Immunol. 12 (2011), 61–66.
4. 4 Whitesides, G.M., The origins and the future of microfluidics. Nature 442 (2006), 368–373.
5. 5 Kim, S., et al. Biological applications of microfluidic gradient devices. Integr. Biol., 2, 2010, 584.
6. 6 Patra, B., et al. A microfluidic device for uniform-sized cell spheroids formation, culture, harvesting and flow cytometry analysis. Biomicrofluidics, 7, 2013, 054114.
7. 7 Thaitrong, N., et al. Implementation of microfluidic sandwich ELISA for superior detection of plant pathogens. PLoS ONE, 8, 2013, e83231.
8. 8 Hughes, A.J., Herr, A.E., Microfluidic western blotting. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 21450–21455.
9. 9 Regehr, K.J., et al. Biological implications of polydimethylsiloxane-based microfluidic cell culture. Lab Chip 9 (2009), 2132–2139.
10. 10 Wyckoff, J., et al. High-resolution multiphoton imaging of tumors in vivo. Cold Spring Harb. Protoc. 2011 (2011), 1167–1184.
11. 11 Sahai, E., Illuminating the metastatic process. Nat. Rev. Cancer 7 (2007), 737–749.
12. 12 Chambers, A.F., et al. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2 (2002), 563–572.
13. 13 Kuo, C.T., et al. A spatiotemporally defined in vitro microenvironment for controllable signal delivery and drug screening. Analyst 139 (2014), 4846–4854.
14. 14 Kuo, C.T., et al. Modeling of cancer metastasis and drug resistance via biomimetic nano-cilia and microfluidics. Biomaterials 35 (2014), 1562–1571.
15. 15 Song, J.W., et al. Microfluidic endothelium for studying the intravascular adhesion of metastatic breast cancer cells. PLoS ONE, 4, 2009, e5756.
16. 16 Shin, M.K., et al. Integration of intra- and extravasation in one cell-based microfluidic chip for the study of cancer metastasis. Lab Chip 11 (2011), 3880–3887.
17. 17 Zhang, Q., et al. A microfluidic-based device for study of transendothelial invasion of tumor aggregates in realtime. Lab Chip, 12, 2012, 2837.
18. 18 Zervantonakis, I.K., et al. Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 13515–13520.
19. 19 Lee, H., et al. A microfluidic platform for quantitative analysis of cancer angiogenesis and intravasation. Biomicrofluidics, 8, 2014, 054102.
20. 20 Jeon, J.S., et al. In vitro model of tumor cell extravasation. PLoS ONE, 8, 2013, e56910.
21. 21 Chen, M.B., et al. Mechanisms of tumor cell extravasation in an in vitro microvascular network platform. Integr. Biol. (Camb.) 5 (2013), 1262–1271.
22. 22 Riahi, R., et al. A microfluidic model for organ-specific extravasation of circulating tumor cells. Biomicrofluidics, 8, 2014, 024103.
23. 23 Ehsan, S.M., et al. A three-dimensional in vitro model of tumor cell intravasation. Integr. Biol. (Camb.) 6 (2014), 603–610.
24. 24 Ghajar, C.M., et al. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 15 (2013), 807–817.
25. 25 Whisler, J.A., et al. Control of perfusable microvascular network morphology using a multiculture microfluidic system. Tissue Eng. Part C Methods 20 (2014), 543–552.
26. 26 Kim, S., et al. Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip 13 (2013), 1489–1500.
27. 27 Jeon, J.S., et al. Generation of 3D functional microvascular networks with human mesenchymal stem cells in microfluidic systems. Integr. Biol. (Camb.) 6 (2014), 555–563.
28. 28 Bersini, S., et al. In vitro models of the metastatic cascade: from local invasion to extravasation. Drug Discov. Today 19 (2014), 735–742.
29. 29 Joyce, J.A., Pollard, J.W., Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9 (2009), 239–252.
30. 30 Fitzgerald, D.P., et al. Reactive glia are recruited by highly proliferative brain metastases of breast cancer and promote tumor cell colonization. Clin. Exp. Metastasis 25 (2008), 799–810.
31. 31 Fidler, I.J., The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat. Rev. Cancer 3 (2003), 453–458.
32. 32 Bersini, S., et al. A microfluidic 3D in vitro model for specificity of breast cancer metastasis to bone. Biomaterials 35 (2014), 2454–2461.
33. 33 Benam, K.H., et al. Engineered in vitro disease models. Annu. Rev. Pathol. Mech. Dis. 10 (2015), 195–262.
34. 34 Huh, D., et al. Reconstituting organ-level lung functions on a chip. Science 328 (2010), 1662–1668.
35. 35 Budhu, S., et al. The importance of animal models in tumor immunity and immunotherapy. Curr. Opin. Genet. Dev. 24 (2014), 46–51.
36. 36 DeWeerdt, S., Bacteriology: a caring culture. Nature 504 (2013), S4–S5.
37. 37 Kitamura, T., et al. Immune cell promotion of metastasis. Nat. Rev. Immunol. 15 (2015), 73–86.
38. 38 Schietinger, A., et al. Specificity in cancer immunotherapy. Semin. Immunol. 20 (2008), 276–285.
39. 39 Qian, B-Z., Pollard, J.W., Macrophage diversity enhances tumor progression and metastasis. Cell 141 (2010), 39–51.
40. 40 Vanneman, M., Dranoff, G., Combining immunotherapy and targeted therapies in cancer treatment. Nat. Rev. Cancer 12 (2012), 237–251.
41. 41 De Palma, M., Lewis, C.E., Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23 (2013), 277–286.
42. 42 Hughes, R., et al. Perivascular M2 macrophages stimulate tumor relapse after chemotherapy. Cancer Res. 75 (2015), 3479–3491.
43. 43 Moser, B., Willimann, K., Chemokines: role in inflammation and immune surveillance. Ann. Rheum. Dis. 63:Suppl. 2 (2004), ii84–ii89.
44. 44 Gopalakrishnan, N., et al. Infection and immunity on a chip: a compartmentalised microfluidic platform to monitor immune cell behaviour in real time. Lab Chip 15 (2015), 1481–1487.
45. 45 Junkin, M., Tay, S., Microfluidic single-cell analysis for systems immunology. Lab Chip 14 (2014), 1246–1260.
46. 46 Hirt, C., et al. “In vitro” 3D models of tumor–immune system interaction. Adv. Drug Deliv. Rev. 79–80 (2014), 145–154.
47. 47 Feder-Mengus, C., et al. New dimensions in tumor immunology: what does 3D culture reveal?. Trends Mol. Med. 14 (2008), 333–340.
48. 48 Agliari, E., et al. Cancer-driven dynamics of immune cells in a microfluidic environment. Sci. Rep., 4, 2014, 6639.
49. 49 Businaro, L., et al. Cross talk between cancer and immune cells: exploring complex dynamics in a microfluidic environment. Lab Chip 13 (2012), 229–239.
50. 50 Mattei, F., et al. A multidisciplinary study using in vivo tumor models and microfluidic cell-on-chip approach to explore the cross-talk between cancer and immune cells. J. Immunotoxicol. 11 (2014), 337–346.
51. 51 Hsu, T-H., et al. The migration speed of cancer cells influenced by macrophages and myofibroblasts co-cultured in a microfluidic chip. Integr. Biol., 4, 2012, 177.
52. 52 Huang, C.P., et al. Engineering microscale cellular niches for three-dimensional multicellular co-cultures. Lab Chip 9 (2009), 1740–1748.
53. 53 de Visser, K.E., et al. Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 6 (2006), 24–37.
54. 54 Bidwell, B.N., et al. Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape. Nat. Med. 18 (2012), 1224–1231.
55. 55 Eyles, J., et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J. Clin. Invest. 120 (2010), 2030–2039.
56. 56 Paolino, M., et al. The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells. Nature 507 (2014), 508–512.
57. 57 Granot, Z., et al. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20 (2011), 300–314.
58. 58 Fidler, I.J., Macrophages and metastasis – a biological approach to cancer therapy. Cancer Res. 45 (1985), 4714–4726.
59. 59 Edris, B., et al. Antibody therapy targeting the CD47 protein is effective in a model of aggressive metastatic leiomyosarcoma. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 6656–6661.
60. 60 Labelle, M., et al. Platelets guide the formation of early metastatic niches. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), E3053–E3061.
61. 61 Labelle, M., et al. Direct signaling between platelets and cancer cells induces an epithelial–mesenchymal-like transition and promotes metastasis. Cancer Cell 20 (2011), 576–590.
62. 62 Vacchelli, E., et al. Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science 350 (2015), 972–978.
63. 63 Wyckoff, J.B., et al. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 60 (2000), 2504–2511.
64. 64 Liu, P.F., et al. A bladder cancer microenvironment simulation system based on a microfluidic co-culture model. Oncotarget 6 (2015), 37695–37705.
65. 65 Chen, W., et al. Emerging microfluidic tools for functional cellular immunophenotyping: a new potential paradigm for immune status characterization. Front. Oncol., 3, 2013, 98.
66. 66 Ramadan, Q., Gijs, M.A.M., In vitro micro-physiological models for translational immunology. Lab Chip 15 (2015), 614–636.
67. 67 Lin, F., Butcher, E.C., T cell chemotaxis in a simple microfluidic device. Lab Chip 6 (2006), 1462–1469.
68. 68 Halilovic, I., et al. Neutrophil migration under spatially-varying chemoattractant gradient profiles. Biomed. Microdevices 17 (2015), 1–7.
69. 69 Sundd, P., et al. ‘Slings’ enable neutrophil rolling at high shear. Nature 488 (2012), 399–403.
70. 70 Han, S., et al. A versatile assay for monitoring in vivo-like transendothelial migration of neutrophils. Lab Chip, 12, 2012, 3861.
71. 71 Kim, S.K., et al. Inflammatory mimetic microfluidic chip by immobilization of cell adhesion molecules for T cell adhesion. Analyst, 137, 2012, 4062.
72. 72 Zhang, B., et al. A standalone perfusion platform for drug testing and target validation in micro-vessel networks. Biomicrofluidics 7 (2013), 1–13.
73. 73 Srigunapalan, S., et al. A microfluidic membrane device to mimic critical components of the vascular microenvironment. Biomicrofluidics 5 (2011), 1–9.
74. 74 Nesmith, A.P., et al. Human airway musculature on a chip: an in vitro model of allergic asthmatic bronchoconstriction and bronchodilation. Lab Chip 14 (2014), 3925–3936.
75. 75 Kim, H.J., et al. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip, 12, 2012, 2165.
76. 76 Ma, C., et al. A clinical microchip for evaluation of single immune cells reveals high functional heterogeneity in phenotypically similar T cells. Nat. Med. 17 (2011), 738–743.
77. 77 Kotz, K.T., et al. Clinical microfluidics for neutrophil genomics and proteomics. Nat. Med. 16 (2010), 1042–1047.
78. 78 Zhu, H., et al. A microdevice for multiplexed detection of T-cell-secreted cytokines. Lab Chip 8 (2008), 2197–2205.
79. 79 Chen, W., et al. Surface-micromachined microfiltration membranes for efficient isolation and functional immunophenotyping of subpopulations of immune cells. Adv. Healthc. Mater. 2 (2013), 965–975.
80. 80 Lee Szeto, G., et al. Microfluidic squeezing for intracellular antigen loading in polyclonal B-cells as cellular vaccines. Sci. Rep., 5, 2015, 10276.
81. 81 Hou, H.W., et al. Isolation and retrieval of circulating tumor cells using centrifugal forces. Sci. Rep., 3, 2013, 1259.
82. 82 Cox, M.C., et al. Toward the broad adoption of 3D tumor models in the cancer drug pipeline. ACS Biomater. Sci. Eng. 1 (2015), 877–894.
83. 83 van Duinen, V., et al. Microfluidic 3D cell culture: from tools to tissue models. Curr. Opin. Biotechnol. 35 (2015), 118–126.
84. 84 Sackmann, E.K., et al. The present and future role of microfluidics in biomedical research. Nature 507 (2014), 181–189.
85. 85 Labelle, M., Hynes, R.O., The initial hours of metastasis: the importance of cooperative host–tumor cell interactions during hematogenous dissemination. Cancer Discov. 2 (2012), 1091–1099.
86. 86 Streets, A.M., Huang, Y., Chip in a lab: microfluidics for next generation life science research. Biomicrofluidics, 7, 2013, 11302.
87. 87 Chen, Q., et al. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 20 (2011), 538–549.
88. 88 Cheon, D-J., Orsulic, S., Mouse models of cancer. Annu. Rev. Pathol. 6 (2011), 95–119.
89. 89 Choi, S.Y.C., et al. Lessons from patient-derived xenografts for better in vitro modeling of human cancer. Adv. Drug Deliv. Rev. 79–80 (2014), 222–237.
90. 90 Liu, S., Leach, S.D., Zebrafish models for cancer. Annu. Rev. Pathol. 6 (2011), 71–93.
91. 91 Konantz, M., et al. Zebrafish xenografts as a tool for in vivo studies on human cancer. Ann. N. Y. Acad. Sci. 1266 (2012), 124–137.
92. 92 Deryugina, E.I., Quigley, J.P., Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis. Cell 130 (2009), 1119–1130.
93. 93 Leong, H.S., et al. Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep. 8 (2014), 1558–1570.
94. 94 Unger, C., et al. Modeling human carcinomas: physiologically relevant 3D models to improve anti-cancer drug development. Adv. Drug Deliv. Rev. 79–80 (2014), 50–67.
95. 95 Qian, B., et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS ONE, 4, 2009, e6562.
96. 96 Kimlin, L.C., et al. In vitro three-dimensional (3D) models in cancer research: an update. Mol. Carcinog. 52 (2013), 167–182.
97. 97 Polacheck, W.J., et al. Microfluidic platforms for mechanobiology. Lab Chip 13 (2013), 2252–2267.
98. 98 Lee, P.J., et al. An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture. Biotechnol. Bioeng. 97 (2007), 1340–1346.
99. 99 Shi, M., et al. Glia co-culture with neurons in microfluidic platforms promotes the formation and stabilization of synaptic contacts. Lab Chip 13 (2013), 3008–3021.
100. 100 Trkov, S., et al. Micropatterned 3-dimensional hydrogel system to study human endothelial–mesenchymal stem cell interactions. J. Tissue Eng. Regen. Med. 4 (2011), 205–215.
101. 101 Jang, K-J., et al. Fluid-shear-stress-induced translocation of aquaporin-2 and reorganization of actin cytoskeleton in renal tubular epithelial cells. Integr. Biol. 3 (2011), 134–141.
102. 102 Huh, D., et al. From 3D cell culture to organs-on-chips. Trends Cell Biol. 21 (2011), 745–754.
103. 103 Polacheck, W.J., et al. Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 11115–11120.
104. 104 Shin, Y., et al. Extracellular matrix heterogeneity regulates three-dimensional morphologies of breast adenocarcinoma cell invasion. Adv. Healthc. Mater. 2 (2013), 790–794.
105. 105 Sundararaghavan, H.G., et al. Neurite growth in 3D collagen gels with gradients of mechanical properties. Biotechnol. Bioeng. 102 (2009), 632–643.
106. 106 Sung, K.E., et al. Control of 3-dimensional collagen matrix polymerization for reproducible human mammary fibroblast cell culture in microfluidic devices. Biomaterials 30 (2009), 4833–4841.
107. 107 Sung, K.E., et al. Transition to invasion in breast cancer: a microfluidic in vitro model enables examination of spatial and temporal effects. Integr. Biol. (Camb.) 3 (2011), 439–450.
108. 108 Bischel, L.L., et al. Microfluidic model of ductal carcinoma in situ with 3D, organotypic structure. BMC Cancer 15 (2015), 1–10.
109. 109 Acosta, M.A., et al. A microfluidic device to study cancer metastasis under chronic and intermittent hypoxia. Biomicrofluidics, 8, 2014, 054117.
110. 110 Wyckoff, J.B., et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 67 (2007), 2649–2656.
111. 111 Pisano, M., et al. An in vitro model of the tumor–lymphatic microenvironment with simultaneous transendothelial and luminal flows reveals mechanisms of flow enhanced invasion. Integr. Biol. 7 (2015), 525–533.
112. 112 Kim, J., et al. Cooperative actions of p21WAF1 and p53 induce Slug protein degradation and suppress cell invasion. EMBO Rep. 15 (2014), 1062–1068.
113. 113 Chaw, K.C., et al. Multi-step microfluidic device for studying cancer metastasis. Lab Chip 7 (2007), 1041–1047.
114. 114 Kim, J., et al. Rapid apoptosis in the pulmonary vasculature distinguishes non-metastatic from metastatic melanoma cells. Cancer Lett. 213 (2004), 203–212.
115. 115 Wong, C.W., et al. Apoptosis: an early event in metastatic inefficiency apoptosis. Cancer Res. 61 (2001), 333–338.