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18 - Study of tumor angiogenesis using microfluidic approaches

from Part II - Recent progress in cell mechanobiology

Published online by Cambridge University Press:  05 November 2015

By
Yoojin Shin ,
Sewoon Han ,
Hyo Eun Jeong ,
Jeong Ah Kim ,
Jessie S. Jeon  and
Seok Chung
Edited by
Yu Sun ,
Deok-Ho Kim  and
Craig A. Simmons
Yu Sun
Affiliation:
University of Toronto
Deok-Ho Kim
Affiliation:
University of Washington
Craig A. Simmons
Affiliation:
University of Toronto
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Summary

Tumor angiogenesis is a key regulator of tumor growth and metastasis. Assays allowing the analysis of tumor angiogenesis are an essential tool to elucidate the role played by the tumor microenvironment in regulating tumor angiogenesis. The assays should also be capable of systematically investigating the effects of physiologically relevant, mechanical and chemical stimuli and their synergistic interactions. The high optical resolution of microfluidic assays facilitates three-dimensional studies of cellular morphogenesis. Their versatility can be applied to study the multi-parameter control of angiogenic factors.

Type
Chapter
Information
Integrative Mechanobiology
Micro- and Nano- Techniques in Cell Mechanobiology
 , pp. 330 - 346
Publisher: Cambridge University Press
Print publication year: 2015

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References

Barkefors, I., Thorslund, S., Nikolajeff, F. and Kreuger, J. (2009). “A fluidic device to study directional angiogenesis in complex tissue and organ culture models.” Lab on a Chip 9: 529–535.CrossRefGoogle ScholarPubMed
Bayless, K. J., Salazar, R. and Davis, G. E. (2000). “RGD-dependent vacuolation and lumen formation observed during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the α v β3 and α 5 β 1 integrins.” The American Journal of Pathology 156: 1673–1683.CrossRefGoogle Scholar
Bersini, S., Jeon, J. S., Dubini, G., Arrigoni, C., Chung, S., Charest, J. L., Moretti, M. and Kamm, R. D. (2014). “A microfluidic 3-D in vitro model for specificity of breast cancer metastasis to bone.” Biomaterials 35: 2454–2461.CrossRefGoogle Scholar
Bettinger, C., Borenstein, J. T. and Tao, S. L. (2012). Microfluidic Cell Culture Systems. Oxford: William Andrew.Google Scholar
Bischel, L. L., Young, E. W., Mader, B. R. and Beebe, D. J. (2013). “Tubeless microfluidic angiogenesis assay with three-dimensional endothelial-lined microvessels. Biomaterials 34: 1471–1477.CrossRefGoogle ScholarPubMed
Carmeliet, P. (2000). “Mechanisms of angiogenesis and arteriogenesis.” Nature Medicine 6: 389–396.CrossRefGoogle ScholarPubMed
Carmeliet, P. and Jain, R. K. (2000). “Angiogenesis in cancer and other diseases.” Nature 407: 249–257.CrossRefGoogle ScholarPubMed
Carrion, B., Huang, C. P., Ghajar, C. M., Kachgal, S., Kniazeva, E., Jeon, N. L. and Putnam, A. J. (2010). “Recreating the perivascular niche ex vivo using a microfluidic approach.” Biotechnology and Bioengineering 107: 1020–1028.CrossRefGoogle ScholarPubMed
Chalupowicz, D. G., Chowdhury, Z. A., Bach, T. L., Barsigian, C. and Martinez, J. (1995). “Fibrin II induces endothelial cell capillary tube formation.” The Journal of cell Biology 130: 207–215.CrossRefGoogle ScholarPubMed
Chaw, K., Manimaran, M., Tay, E. and Swaminathan, S. (2007). “Multi-step microfluidic device for studying cancer metastasis.” Lab on a Chip 7: 1041–1047.CrossRefGoogle ScholarPubMed
Chen, M. B., Whisler, J. A., Jeon, J. S. and Kamm, R. D. (2013). “Mechanisms of tumor cell extravasation in an in vitro microvascular network platform.” Integrative Biology 5: 1262–1271.CrossRefGoogle Scholar
Chrobak, K. M., Potter, D. R. and Tien, J. (2006). “Formation of perfused, functional microvascular tubes in vitro.” Microvascular Research 71: 185–196.CrossRefGoogle ScholarPubMed
Chung, S., Sudo, R., Mack, P. J., Wan, C.-R., Vickerman, V. and Kamm, R. D. (2009a). “Cell migration into scaffolds under co-culture conditions in a microfluidic platform.” Lab on a Chip 9: 269–275.CrossRefGoogle Scholar
Chung, S., Sudo, R., Vickerman, V., Zervantonakis, I. K. and Kamm, R. D. (2010). “Microfluidic platforms for studies of angiogenesis, cell migration, and cell-cell interactions.” Annals of Biomedical Engineering 38: 1164–1177.CrossRefGoogle ScholarPubMed
Chung, S., Sudo, R., Zervantonakis, I. K., Rimchala, T. and Kamm, R. D. (2009b). “Surface‐treatment‐induced three‐dimensional capillary morphogenesis in a microfluidic platform.” Advanced Materials 21: 4863–4867.CrossRefGoogle Scholar
Dai, X., Cai, S., Ye, Q., Jiang, J., Yan, X., Xiong, X., Jiang, Q., et al. (2011). “A novel in vitro angiogenesis model based on a microfluidic device.” Chinese Science Bulletin 56: 3301–3309.CrossRefGoogle Scholar
Eilken, H. M. and Adams, R. H. (2010). “Dynamics of endothelial cell behavior in sprouting angiogenesis.” Current Opinion in Cell Biology 22: 617–625.CrossRefGoogle ScholarPubMed
Farahat, W. A., Wood, L. B., Zervantonakis, I. K., Schor, A., Ong, S., Neal, D., Kamm, R. D. et al. (2012). “Ensemble analysis of angiogenic growth in three-dimensional microfluidic cell cultures.” PloS One 7: e37333.CrossRefGoogle ScholarPubMed
Ferrari, G., Pintucci, G., Seghezzi, G., Hyman, K., Galloway, A. C. and Mignatti, P. (2006). “VEGF, a prosurvival factor, acts in concert with TGF-β1 to induce endothelial cell apoptosis.” Proceedings of the National Academy of Sciences 103: 17260–17265.CrossRefGoogle ScholarPubMed
Figg, W. and Folkman, J. (2008). Angiogenesis: An Integrative Approach from Science to Medicine. New York: Springer.CrossRefGoogle Scholar
Folkman, J. (1995). “Angiogenesis in cancer, vascular, rheumatoid and other disease.” Nature Medicine 1: 27–30.CrossRefGoogle ScholarPubMed
George, E. L., Baldwin, H. S. and Hynes, R. O. (1997). “Fibronectins are essential for heart and blood vessel morphogenesis but are dispensable for initial specification of precursor cells.” Blood 90: 3073–3081.CrossRefGoogle ScholarPubMed
Ghajar, C. M., Blevins, K. S., Hughes, C. C., George, S. C. and Putnam, A. J. (2006). “Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation.” Tissue Engineering 12: 2875–2888.CrossRefGoogle ScholarPubMed
Grant, D. S., Yenisey, C., Rose, R. W., Tootell, M., Santra, M. and Iozzo, R. V. (2002). “Decorin suppresses tumor cell-mediated angiogenesis.” Oncogene 21: 4765–4777.CrossRefGoogle ScholarPubMed
Helm, C.-L. E., Fleury, M. E., Zisch, A. H., Boschetti, F. and Swartz, M. A. (2005). “Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism.” Proceedings of the National Academy of Sciences of the United States of America 102: 15779–15784.CrossRefGoogle ScholarPubMed
Huang, C. P., Lu, J., Seon, H., Lee, A. P., Flanagan, L. A., Kim, H.-Y., Putnam, A. J. et al. (2009). “Engineering microscale cellular niches for three-dimensional multicellular co-cultures.” Lab on a Chip 9: 1740–1748.CrossRefGoogle ScholarPubMed
Jain, R. K., di Tomaso, E., Duda, D. G., Loeffler, J. S., Sorensen, A. G. and Batchelor, T. T. (2007). “Angiogenesis in brain tumours.” Nature Reviews Neuroscience 8: 610–622.CrossRefGoogle ScholarPubMed
Järveläinen, H., Sainio, A., Koulu, M., Wight, T. N. and Penttinen, R. (2009). “Extracellular matrix molecules: potential targets in pharmacotherapy.” Pharmacological Reviews 61: 198–223.CrossRefGoogle ScholarPubMed
Jeon, J. S., Bersini, S., Gilardi, M., Dubini, G., Charest, J. L., Moretti, M. and Kamm, R. D. (2014a). “Human 3-D vascularized organotypic microfluidic assays to study breast cancer cell extravasation.” Proceedings of the National Academy of Sciences: 201417115.CrossRefGoogle Scholar
Jeon, J. S., Bersini, S., Whisler, J. A., Chen, M. B., Dubini, G., Charest, J. L., Moretti, M. et al. (2014b). “Generation of 3-D functional microvascular networks with human mesenchymal stem cells in microfluidic systems.” Integrative Biology 6: 555–563.CrossRefGoogle Scholar
Jeon, J. S., Zervantonakis, I. K., Chung, S., Kamm, R. D. and Charest, J. L. (2013). “In vitro model of tumor cell extravasation.” PloS One 8: e56910.CrossRefGoogle ScholarPubMed
Jeong, G. S., Han, S., Shin, Y., Kwon, G. H., Kamm, R. D., Lee, S.-H. and Chung, S. (2011a). “Sprouting angiogenesis under a chemical gradient regulated by interactions with an endothelial monolayer in a microfluidic platform.” Analytical Chemistry 83: 8454–8459.CrossRefGoogle Scholar
Jeong, G. S., Kwon, G. H., Kang, A. R., Jung, B. Y., Park, Y., Chung, S. and Lee, S.-H. (2011b). “Microfluidic assay of endothelial cell migration in 3D interpenetrating polymer semi-network HA-Collagen hydrogel.” Biomedical Microdevices 13: 717–723.CrossRefGoogle ScholarPubMed
Kim, C., Chung, S., Yuchun, L., Kim, M.-C., Chan, J. K., Asada, H. H. and Kamm, R. D. (2012). “In vitro angiogenesis assay for the study of cell-encapsulation therapy.” Lab on a Chip 12: 2942–2950.CrossRefGoogle Scholar
Kim, C., Kasuya, J., Jeon, J., Chung, S. and Kamm, R. D. (2015). “A quantitative microfluidic angiogenesis screen for studying anti-angiogenic therapeutic drugs.” Lab on a Chip 15: 301–310.CrossRefGoogle ScholarPubMed
Kim, S., Lee, H., Chung, M. and Jeon, N. L. (2013). “Engineering of functional. perfusable 3-D microvascular networks on a chip.” Lab on a Chip 13: 1489–1500.CrossRefGoogle Scholar
Mack, P. J., Zhang, Y., Chung, S., Vickerman, V., Kamm, R. D. and García-Cardeña, G. (2009). “Biomechanical regulation of endothelium-dependent events critical for adaptive remodeling.” Journal of Biological Chemistry 284: 8412–8420.CrossRefGoogle ScholarPubMed
Maeshima, Y., Colorado, P. C. and Kalluri, R. (2000). “Two RGD-independent αvβ3 integrin binding sites on tumstatin regulate distinct anti-tumor properties.” Journal of Biological Chemistry 275: 23745–23750.CrossRefGoogle ScholarPubMed
Metheny-Barlow, L. J. and Li, L. Y. (2003). “The enigmatic role of angiopoietin-1 in tumor angiogenesis.” Cell Research 13: 309–317.CrossRefGoogle ScholarPubMed
Miller, J. S., Stevens, K. R., Yang, M. T., Baker, B. M., Nguyen, D.-H. T., Cohen, D. M., Toro, E., et al. (2012). “Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues.” Nature Materials 11: 768–774.CrossRefGoogle ScholarPubMed
Moya, M. L., Hsu, Y.-H., Lee, A. P., Hughes, C. C. and George, S. C. (2013). “In vitro perfused human capillary networks.” Tissue Engineering Part C: Methods 19: 730–737.CrossRefGoogle ScholarPubMed
mustonen, T. and Alitalo, K. (1995). “Endothelial receptor tyrosine kinases involved in angiogenesis.” The Journal of Cell Biology 129: 895–898.CrossRefGoogle ScholarPubMed
Nakayasu, K., Hayashi, N., Okisaka, S. and Sato, N. (1992). “Formation of capillary-like tubes by vascular endothelial cells cocultivated with keratocytes.” Investigative Ophthalmology & Visual Science 33: 3050–3057.Google ScholarPubMed
Ng, C. P., Helm, C.-L. E. and Swartz, M. A. (2004). “Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro.” Microvascular Research 68: 258–264.CrossRefGoogle ScholarPubMed
Nguyen, D.-H. T., Stapleton, S. C., Yang, M. T., Cha, S. S., Choi, C. K., Galie, P. A. and Chen, C. S. (2013). “Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro.” Proceedings of the National Academy of Sciences 110: 6712–6717.CrossRefGoogle ScholarPubMed
Nissen, L. J., Cao, R., Hedlund, E.-M., Wang, Z., Zhao, X., Wetterskog, D., Funa, K., et al. (2007). “Angiogenic factors FGF2 and PDGF-BB synergistically promote murine tumor neovascularization and metastasis.” The Journal of Clinical Investigation 117: 2766–2777.CrossRefGoogle ScholarPubMed
Rodríguez-Manzaneque, J. C., Lane, T. F., Ortega, M. A., Hynes, R. O., Lawler, J. and Iruela-Arispe, M. L. (2001). “Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor.” Proceedings of the National Academy of Sciences 98: 12485–12490.CrossRefGoogle ScholarPubMed
Rørth, P. (2009). “Collective cell migration.” Annual Review of Cell and Developmental 25: 407–429.CrossRefGoogle ScholarPubMed
Semenza, G. L. (1998). “Hypoxia-inducible factor 1: master regulator of O2 homeostasis.” Current Opinion in Genetics & Development 8: 588–594.CrossRefGoogle ScholarPubMed
Shamloo, A., Xu, H. and Heilshorn, S. (2011). “Mechanisms of vascular endothelial growth factor-induced pathfinding by endothelial sprouts in biomaterials.” Tissue Engineering Part A 18: 320–330.CrossRefGoogle ScholarPubMed
Shin, Y., Han, S., Jeon, J. S., Yamamoto, K., Zervantonakis, I. K., Sudo, R., Kamm, R. D. et al. (2012). “Microfluidic assay for simultaneous culture of multiple cell types on surfaces or within hydrogels.” Nature Protocols 7: 1247–1259.CrossRefGoogle ScholarPubMed
Shin, Y., Jeon, J. S., Han, S., Jung, G.-S., Shin, S., Lee, S.-H., Sudo, R., et al. (2011). “In vitro 3D collective sprouting angiogenesis under orchestrated ANG-1 and VEGF gradients.” Lab on a Chip 11: 2175–2181.CrossRefGoogle ScholarPubMed
Shin, Y., Kim, H., Han, S., Won, J., Jeong, H. E., Lee, E. S., Kamm, R. D., et al. (2013). “Extracellular matrix heterogeneity regulates three‐dimensional morphologies of breast adenocarcinoma cell invasion.” Advanced Healthcare Materials 2: 790–794.CrossRefGoogle ScholarPubMed
Shin, Y., Yang, K., Han, S., Park, H. J., Seok Heo, Y., Cho, S. W. and Chung, S. (2014). “Reconstituting vascular microenvironment of neural stem cell niche in three‐dimensional extracellular matrix.” Advanced Healthcare Materials 3: 1457–1464.CrossRefGoogle ScholarPubMed
Shiu, Y.-T., Weiss, J. A., Hoying, J. B., Iwamoto, M. N., Joung, I. S. and Quam, C. T. (2004). “The role of mechanical stresses in angiogenesis.” Critical Reviews in Biomedical Engineering 33: 431–510.Google Scholar
Song, J. W. and Munn, L. L. (2011). “Fluid forces control endothelial sprouting.” Proceedings of the National Academy of Sciences 108: 15342–15347.CrossRefGoogle ScholarPubMed
Steeg, P. S. (2006). “Tumor metastasis: mechanistic insights and clinical challenges.” Nature Medicine 12: 895–904.CrossRefGoogle ScholarPubMed
Stroock, A. D. and Fischbach, C. (2010). “Microfluidic culture models of tumor angiogenesis.” Tissue Engineering Part A 16: 2143–2146.CrossRefGoogle ScholarPubMed
Sudo, R., Chung, S., Zervantonakis, I. K., Vickerman, V., Toshimitsu, Y., Griffith, L. G. and Kamm, R. D. (2009). “Transport-mediated angiogenesis in 3-D epithelial coculture.” The FASEB Journal 23: 2155–2164.CrossRefGoogle Scholar
Swartz, M. A. and Lund, A. W. (2012). “Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity.” Nature Reviews Cancer 12: 210–219.CrossRefGoogle ScholarPubMed
Thyboll, J., Kortesmaa, J., Cao, R., Soininen, R., Wang, L., Iivanainen, A., Sorokin, L., et al. (2002). “Deletion of the laminin α4 chain leads to impaired microvessel maturation.” Molecular and Cellular Biology 22: 1194–1202.CrossRefGoogle ScholarPubMed
Verbridge, S. S., Chakrabarti, A., Delnero, P., Kwee, B., Varner, J. D., Stroock, A. D. and Fischbach, C. (2013). “Physicochemical regulation of endothelial sprouting in a 3-D microfluidic angiogenesis model.” Journal of Biomedical Materials Research Part A 101: 2948–2956.CrossRefGoogle Scholar
Vickerman, V., Blundo, J., Chung, S. and Kamm, R. (2008). “Design, fabrication and implementation of a novel multi-parameter control microfluidic platform for three-dimensional cell culture and real-time imaging.” Lab on a Chip 8: 1468–1477.CrossRefGoogle ScholarPubMed
Vickerman, V. and Kamm, R. D. (2012). “Mechanism of a flow-gated angiogenesis switch: early signaling events at cell-matrix and cell-cell junctions.” Integrative Biology 4: 863–874.CrossRefGoogle ScholarPubMed
Weis, S. M. and Cheresh, D. A. (2011). “Tumor angiogenesis: molecular pathways and therapeutic targets.” Nature Medicine 17: 1359–1370.CrossRefGoogle ScholarPubMed
Whisler, J. A., Chen, M. B. and Kamm, R. D. (2012). “Control of perfusable microvascular network morphology using a multiculture microfluidic system.” Tissue Engineering Part C: Methods 7: 543–552.Google Scholar
Wong, A. P., Perez-Castillejos, R., Christopher Love, J. and Whitesides, G. M. (2008). “Partitioning microfluidic channels with hydrogel to construct tunable 3-D cellular microenvironments.” Biomaterials 29: 1853–1861.CrossRefGoogle ScholarPubMed
Woyach, J. A. and Shah, M. H. (2009). “New therapeutic advances in the management of progressive thyroid cancer.” Endocrine-Related Cancer 16: 715–731.CrossRefGoogle ScholarPubMed
Xu, X., Yang, G., Zhang, H. and Prestwich, G. D. (2009). “Evaluating dual activity LPA receptor pan-antagonist/autotaxin inhibitors as anti-cancer agents in vivo using engineered human tumors.” Prostaglandins & Other Lipid Mediators 89: 140–146.CrossRefGoogle ScholarPubMed
Yang, K., Han, S., Shin, Y., Ko, E., Kim, J., Park, K. I., Chung, S. et al. (2013). “A microfluidic array for quantitative analysis of human neural stem cell self-renewal and differentiation in three-dimensional hypoxic microenvironment.” Biomaterials 34: 6607–6614.CrossRefGoogle ScholarPubMed
Yeon, J. H., Ryu, H. R., Chung, M., Hu, Q. P. and Jeon, N. L. (2012). “In vitro formation and characterization of a perfusable three-dimensional tubular capillary network in microfluidic devices.” Lab on a Chip 12: 2815–2822.CrossRefGoogle ScholarPubMed
Yoshida, A., Anand-Apte, B. and Zetter, B. R. (1996). “Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor.” Growth Factors 13: 57–64.CrossRefGoogle ScholarPubMed
Young, E. W., Wheeler, A. R. and Simmons, C. A. (2007). “Matrix-dependent adhesion of vascular and valvular endothelial cells in microfluidic channels.” Lab on a Chip 7: 1759–1766.CrossRefGoogle ScholarPubMed
Zervantonakis, I. K., Hughes-Alford, S. K., Charest, J. L., Condeelis, J. S., Gertler, F. B. and Kamm, R. D. (2012). “Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function.” Proceedings of the National Academy of Sciences 109: 13515–13520.CrossRefGoogle ScholarPubMed
Zetter, P., and Bruce, R. (1998). “Angiogenesis and tumor metastasis.” Annual Review of Medicine 49: 407–424.CrossRefGoogle ScholarPubMed
Zheng, Y., Chen, J., Craven, M., Choi, N. W., Totorica, S., Diaz-Santana, A., Kermani, P., et al. (2012). “In vitro microvessels for the study of angiogenesis and thrombosis.” Proceedings of the National Academy of Sciences 109: 9342–9347.CrossRefGoogle Scholar

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