Abstract

Three-dimensional (3D) models play an important role in understanding the behavior of a tumor in a well-defined microenvironment, because some aspects of tumor characteristics cannot be fully recapitulated in cell monolayers. In this study, a novel method is presented for the culture of tumor spheroids and for in vivo 3D cell growth simulation of a tumor on a 3D cell chip fabricated in the 3rd floor structure. Scanning electron microscopy and confocal imaging show that, soon after the adjacent tumor adheres to the micropatterned pillar sidewalls, they are subsequently pulled between the pillars in a suspended position. The half maximal inhibitory concentration (IC50) values of mitroxanthrone in the two-dimensional (2D) plate were at the concentration of 345.65 µg/ml. In contrast, the IC50 value of 3D mitroxanthrone in the 3D cell chip was not detected at the system. Our results indicated that 3D spheroids are generated in uniformly fabricated cancer cell chips, and large numbers of morphologically homogenous spheroids are easily produced. The result showed that the 3D cancer cell chip is more resistant to anticancer agents than 2D plate cell culture. Thus, the 3D cancer cell chip could be used for high-throughput investigations of the efficacy vs. toxicity of drugs or numerous other cancer spheroid cellular and biochemical assays.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]

2017 (1)

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

2016 (3)

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

2014 (1)

S. K. Martin, M. Kamelgarn, and N. Kyprianou, “Cytoskeleton targeting value in prostate cancer treatment,” Am. J. Clin. Exp. Urol. 2(1), 15–26 (2014).
[PubMed]

2013 (5)

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

S. Breslin and L. O’Driscoll, “Three-dimensional cell culture: the missing link in drug discovery,” Drug Discov. Today 18(5-6), 240–249 (2013).
[Crossref] [PubMed]

2012 (4)

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

2011 (1)

D. Huh, G. A. Hamilton, and D. E. Ingber, “From 3D cell culture to organs-on-chips,” Trends Cell Biol. 21(12), 745–754 (2011).
[Crossref] [PubMed]

2010 (1)

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

2009 (1)

D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

2008 (2)

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

2007 (3)

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

S. R. Khetani and S. N. Bhatia, “Microscale culture of human liver cells for drug development,” Nat. Biotechnol. 26(1), 120–126 (2007).
[Crossref] [PubMed]

2006 (3)

J. El-Ali, P. K. Sorger, and K. F. Jensen, “Cells on chips,” Nature 442(7101), 403–411 (2006).
[Crossref] [PubMed]

T. Ozben, “Mechanisms and strategies to overcome multiple drug resistance in cancer,” FEBS Lett. 580(12), 2903–2909 (2006).
[Crossref] [PubMed]

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

2005 (2)

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

J. Debnath and J. S. Brugge, “Modelling glandular epithelial cancers in three-dimensional cultures,” Nat. Rev. Cancer 5(9), 675–688 (2005).
[Crossref] [PubMed]

2002 (1)

M. M. Gottesman, “Mechanisms of cancer drug resistance,” Annu. Rev. Med. 53(1), 615–627 (2002).
[Crossref] [PubMed]

Alliston, T.

D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

An, J. H.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

Argnani, L.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Asselin, E.

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

Baccarani, M.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Bhatia, S. N.

S. R. Khetani and S. N. Bhatia, “Microscale culture of human liver cells for drug development,” Nat. Biotechnol. 26(1), 120–126 (2007).
[Crossref] [PubMed]

Breslin, S.

S. Breslin and L. O’Driscoll, “Three-dimensional cell culture: the missing link in drug discovery,” Drug Discov. Today 18(5-6), 240–249 (2013).
[Crossref] [PubMed]

Broccoli, A.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Brugge, J. S.

J. Debnath and J. S. Brugge, “Modelling glandular epithelial cancers in three-dimensional cultures,” Nat. Rev. Cancer 5(9), 675–688 (2005).
[Crossref] [PubMed]

Brzozka, Z.

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

Brzózka, Z.

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

Butcher, D. T.

D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

Caldwell, S. A.

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

Casadei, B.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Celli, M.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Chae, H. N.

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

Chiang, C. L.

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

Chitcholtan, K.

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

Choi, J.-W.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

Chudy, M.

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

Clark, D. S.

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

Clements, J. A.

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

Cui, J.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Cui Tomshine, J.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Debnath, J.

J. Debnath and J. S. Brugge, “Modelling glandular epithelial cancers in three-dimensional cultures,” Nat. Rev. Cancer 5(9), 675–688 (2005).
[Crossref] [PubMed]

Derenzini, E.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Ding, H.

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Dong, W.-F.

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Dordick, J. S.

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

Dybko, A.

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

El-Ali, J.

J. El-Ali, P. K. Sorger, and K. F. Jensen, “Cells on chips,” Nature 442(7101), 403–411 (2006).
[Crossref] [PubMed]

Evans, J. J.

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

Fanti, S.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Feng, Q.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Gan, Y.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Gandolfi, L.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Gottesman, M. M.

M. M. Gottesman, “Mechanisms of cancer drug resistance,” Annu. Rev. Med. 53(1), 615–627 (2002).
[Crossref] [PubMed]

Guo, Y. H.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Ha, C. W.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

Hamilton, G. A.

D. Huh, G. A. Hamilton, and D. E. Ingber, “From 3D cell culture to organs-on-chips,” Trends Cell Biol. 21(12), 745–754 (2011).
[Crossref] [PubMed]

Han, S.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Hou, L.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Huang, R. Y.

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

Huh, D.

D. Huh, G. A. Hamilton, and D. E. Ingber, “From 3D cell culture to organs-on-chips,” Trends Cell Biol. 21(12), 745–754 (2011).
[Crossref] [PubMed]

Hutmacher, D. W.

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

Ingber, D. E.

D. Huh, G. A. Hamilton, and D. E. Ingber, “From 3D cell culture to organs-on-chips,” Trends Cell Biol. 21(12), 745–754 (2011).
[Crossref] [PubMed]

Jensen, K. F.

J. El-Ali, P. K. Sorger, and K. F. Jensen, “Cells on chips,” Nature 442(7101), 403–411 (2006).
[Crossref] [PubMed]

Jiang, Q.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Jordan, E. T.

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

Jung, J.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

Kamelgarn, M.

S. K. Martin, M. Kamelgarn, and N. Kyprianou, “Cytoskeleton targeting value in prostate cancer treatment,” Am. J. Clin. Exp. Urol. 2(1), 15–26 (2014).
[PubMed]

Khetani, S. R.

S. R. Khetani and S. N. Bhatia, “Microscale culture of human liver cells for drug development,” Nat. Biotechnol. 26(1), 120–126 (2007).
[Crossref] [PubMed]

Kim, D. P.

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

Kim, D.-H.

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

Kong, H.-J.

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

Kuo, C. T.

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

Kwapiszewski, R.

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

Kyprianou, N.

S. K. Martin, M. Kamelgarn, and N. Kyprianou, “Cytoskeleton targeting value in prostate cancer treatment,” Am. J. Clin. Exp. Urol. 2(1), 15–26 (2014).
[PubMed]

Lee, H.

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

Lee, K.-J.

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

Lee, K.-S.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

Lee, S. H.

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

Li, C. L.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Liang, X. J.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Lim, T. W.

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

Linhardt, R. J.

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

Loessner, D.

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

Lutolf, M. P.

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

Ma, H. L.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Martin, S. K.

S. K. Martin, M. Kamelgarn, and N. Kyprianou, “Cytoskeleton targeting value in prostate cancer treatment,” Am. J. Clin. Exp. Urol. 2(1), 15–26 (2014).
[PubMed]

McBride, K. W.

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

Meli, L.

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

Nan, K. J.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Noh, H. M.

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

O’Driscoll, L.

S. Breslin and L. O’Driscoll, “Three-dimensional cell culture: the missing link in drug discovery,” Drug Discov. Today 18(5-6), 240–249 (2013).
[Crossref] [PubMed]

Ozben, T.

T. Ozben, “Mechanisms and strategies to overcome multiple drug resistance in cancer,” FEBS Lett. 580(12), 2903–2909 (2006).
[Crossref] [PubMed]

Parent, S.

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

Park, S. H.

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

Pellegrini, C.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Pham, T. A.

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

Pileri, S.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Poletti, V.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Quirini, F.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Reginato, M. J.

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

Ren, J.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Rizzi, S. C.

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

Shan, X.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Shi, Y.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Sodunke, T. R.

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

Son, Y.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

Sorger, P. K.

J. El-Ali, P. K. Sorger, and K. F. Jensen, “Cells on chips,” Nature 442(7101), 403–411 (2006).
[Crossref] [PubMed]

Stefoni, V.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Stelmachowska, A.

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

Stok, K. S.

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

Sun, H.-B.

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Sykes, P. H.

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

Tian, T.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Turner, K. K.

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

Wang, D.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Wang, H.

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

Wang, J.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Wang, W.

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

Wang, Y.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Weaver, V. M.

D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

Wo, A. M.

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

Wu, Y.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Xia, H.

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Xu, B.-B.

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Yang, D.-Y.

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

Yang, H. K.

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

Yang, X.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Yi, S. W.

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

Yuan, Y.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Zhang, W. G.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Zhang, Y.-L.

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Zhang, Z.

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Zhao, N.

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Zinzani, P. L.

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

Ziólkowska, K.

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

Zou, G.

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Adv. Funct. Mater. (1)

T. A. Pham, D. P. Kim, T. W. Lim, S. H. Park, D.-Y. Yang, and K.-S. Lee, “Three-dimensional SiCN ceramic microstructures via nano-stereolithography of inorganic polymer photoresists,” Adv. Funct. Mater. 16(9), 1235–1241 (2006).
[Crossref]

Am. J. Clin. Exp. Urol. (1)

S. K. Martin, M. Kamelgarn, and N. Kyprianou, “Cytoskeleton targeting value in prostate cancer treatment,” Am. J. Clin. Exp. Urol. 2(1), 15–26 (2014).
[PubMed]

Annu. Rev. Med. (1)

M. M. Gottesman, “Mechanisms of cancer drug resistance,” Annu. Rev. Med. 53(1), 615–627 (2002).
[Crossref] [PubMed]

Appl. Phys. Lett. (2)

D.-Y. Yang, S. H. Park, T. W. Lim, H.-J. Kong, S. W. Yi, H. K. Yang, and K.-S. Lee, “Ultraprecise microreproduction of a three-dimensional artistic sculpture by multipath scanning method in two-photon photopolymerization,” Appl. Phys. Lett. 90(1), 013113 (2007).
[Crossref]

S. H. Park, S. H. Lee, D.-Y. Yang, H.-J. Kong, and K.-S. Lee, “Subregional slicing method to increase three-dimensional nanofabrication efficiency in two-photon polymerization,” Appl. Phys. Lett. 87(15), 154108 (2005).
[Crossref]

Appl. Phys., A Mater. Sci. Process. (1)

T. W. Lim, Y. Son, D.-Y. Yang, H.-J. Kong, K.-S. Lee, and S. H. Park, “Highly effective three-dimensional large-scale microfabrication using a continuous scanning method,” Appl. Phys., A Mater. Sci. Process. 92(3), 541–545 (2008).
[Crossref]

Biomaterials (3)

T. R. Sodunke, K. K. Turner, S. A. Caldwell, K. W. McBride, M. J. Reginato, and H. M. Noh, “Micropatterns of Matrigel for three-dimensional epithelial cultures,” Biomaterials 28(27), 4006–4016 (2007).
[Crossref] [PubMed]

D. Loessner, K. S. Stok, M. P. Lutolf, D. W. Hutmacher, J. A. Clements, and S. C. Rizzi, “Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells,” Biomaterials 31(32), 8494–8506 (2010).
[Crossref] [PubMed]

L. Meli, E. T. Jordan, D. S. Clark, R. J. Linhardt, and J. S. Dordick, “Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems,” Biomaterials 33(35), 9087–9096 (2012).
[Crossref] [PubMed]

Biosens. Bioelectron. (1)

K. Ziółkowska, A. Stelmachowska, R. Kwapiszewski, M. Chudy, A. Dybko, and Z. Brzózka, “Long-term three-dimensional cell culture and anticancer drug activity evaluation in a microfluidic chip,” Biosens. Bioelectron. 40(1), 68–74 (2013).
[Crossref] [PubMed]

Drug Discov. Today (1)

S. Breslin and L. O’Driscoll, “Three-dimensional cell culture: the missing link in drug discovery,” Drug Discov. Today 18(5-6), 240–249 (2013).
[Crossref] [PubMed]

Exp. Cell Res. (1)

K. Chitcholtan, E. Asselin, S. Parent, P. H. Sykes, and J. J. Evans, “Differences in growth properties of endometrial cancer in three dimensional (3D) culture and 2D cell monolayer,” Exp. Cell Res. 319(1), 75–87 (2013).
[Crossref] [PubMed]

FEBS Lett. (1)

T. Ozben, “Mechanisms and strategies to overcome multiple drug resistance in cancer,” FEBS Lett. 580(12), 2903–2909 (2006).
[Crossref] [PubMed]

Hematol. Oncol. (1)

P. L. Zinzani, C. Pellegrini, L. Gandolfi, B. Casadei, E. Derenzini, A. Broccoli, F. Quirini, L. Argnani, S. Pileri, M. Celli, S. Fanti, V. Poletti, V. Stefoni, and M. Baccarani, “Extranodal marginal zone B-cell lymphoma of the lung: experience with fludarabine and mitoxantrone-containing regimens,” Hematol. Oncol. 31(4), 183–188 (2013).
[Crossref] [PubMed]

J. Biomed. Nanotechnol. (1)

K.-J. Lee, J. H. An, C. W. Ha, Y. Son, D.-Y. Yang, J. Jung, K.-S. Lee, and J.-W. Choi, “3D Hierarchical, pyramid-based cancer cell chip for the detection of anticancer drug effects,” J. Biomed. Nanotechnol. 12(12), 2125–2138 (2016).
[Crossref]

Lab Chip (1)

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13(9), 1677–1690 (2013).
[Crossref] [PubMed]

Laser Photonics Rev. (1)

H. Wang, Y.-L. Zhang, W. Wang, H. Ding, and H.-B. Sun, “On-chip laser processing for the development of multifunctional microfluidic chips,” Laser Photonics Rev. 11(2), 1600116 (2017).
[Crossref]

Mol. Imaging (1)

H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, “Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration,” Mol. Imaging 11(6), 487–498 (2012).
[PubMed]

Nanotechnology (1)

L. Hou, Q. Feng, Y. Wang, X. Yang, J. Ren, Y. Shi, X. Shan, Y. Yuan, Y. Wang, and Z. Zhang, “Multifunctional hyaluronic acid modified graphene oxide loaded with mitoxantrone for overcoming drug resistance in cancer,” Nanotechnology 27(1), 015701 (2016).
[Crossref] [PubMed]

Nat. Biotechnol. (1)

S. R. Khetani and S. N. Bhatia, “Microscale culture of human liver cells for drug development,” Nat. Biotechnol. 26(1), 120–126 (2007).
[Crossref] [PubMed]

Nat. Rev. Cancer (2)

D. T. Butcher, T. Alliston, and V. M. Weaver, “A tense situation: forcing tumour progression,” Nat. Rev. Cancer 9(2), 108–122 (2009).
[Crossref] [PubMed]

J. Debnath and J. S. Brugge, “Modelling glandular epithelial cancers in three-dimensional cultures,” Nat. Rev. Cancer 5(9), 675–688 (2005).
[Crossref] [PubMed]

Nature (1)

J. El-Ali, P. K. Sorger, and K. F. Jensen, “Cells on chips,” Nature 442(7101), 403–411 (2006).
[Crossref] [PubMed]

NPG Asia Mater. (1)

C. T. Kuo, C. L. Chiang, R. Y. Huang, H. Lee, and A. M. Wo, “Configurable 2D and 3D spheroid tissue cultures on bioengineered surfaces with acquisition of epithelial–mesenchymal transition characteristics,” NPG Asia Mater. 4(9), e27 (2012).
[Crossref]

Oncol. Rep. (1)

C. L. Li, T. Tian, K. J. Nan, N. Zhao, Y. H. Guo, J. Cui, J. Wang, and W. G. Zhang, “Survival advantages of multicellular spheroids vs. monolayers of HepG2 cells in vitro,” Oncol. Rep. 20(6), 1465–1471 (2008).
[PubMed]

Sci. Adv. Mater. (1)

J. H. An, K.-J. Lee, D.-H. Kim, H. N. Chae, and K.-S. Lee, “Skin fibroblast cells on 3D skin cell chip using Nanngold platform structures and three-floor structures,” Sci. Adv. Mater. 8(11), 2147–2152 (2016).
[Crossref]

Sensor Actuator B. (1)

K. Ziółkowska, R. Kwapiszewski, A. Stelmachowska, M. Chudy, A. Dybko, and Z. Brzozka, “Development of a three-dimensional microfluidic system for long-term tumor spheroid culture,” Sensor Actuator B. 173, 908–913 (2012).
[Crossref]

Trends Cell Biol. (1)

D. Huh, G. A. Hamilton, and D. E. Ingber, “From 3D cell culture to organs-on-chips,” Trends Cell Biol. 21(12), 745–754 (2011).
[Crossref] [PubMed]

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Figures (5)

Fig. 1
Fig. 1 Schematic diagram of the process for 3D cell chip. Manual stages control the X, Y, and Z positions of the piezoelectric stages of the specimen. The piezoelectric stages control the X, Y, and Z positions of the specimen over the range of 800 μm × 800 μm × 400 μm with the resolution of 0.1 nm. A femtosecond laser (mode-locked Ti-sapphire laser) was used as a laser beam source; the laser has the wavelength of 780 nm, ultrashort pulse duration below 100 fs, and the repetition rate of 80 MHz. A λ/2 plate and polarizing beam splitter were used to control the laser power.
Fig. 2
Fig. 2 The SEM image of the 3D cancer cell chip fabricated on the ITO glass. The structure consists of three floors. The dimensions of each unit compartment are 12 μm × 12 μm × 12 μm. The first floor consists of 64 compartments, the second floor consists of 36 compartments, and the third floor consists of 16 compartments.
Fig. 3
Fig. 3 The SEM images of prostate cancer cells on the fabricated 3D cell chip and 2D plate
Fig. 4
Fig. 4 Confocal microscopic image of F-actin in the prostate cancer cells (Du 145 cells) in the 2D plate and the 3D cell chip. Immunofluorescence images of F-actin in Du145 cells cultured for 5 days in the 2D plate (a-c) and the 3D cell chip (d-f). Confocal microscopy images of cells with F-actin staining (green) using a FITC-conjugated antibody. Nuclei (blue) stained with 4,6-diamidino-2-phenylindole (DAPI). Merged image (f) of F-actin and the DAPI staining. The images were acquired using a Zeiss Axioimager M1 microscope or Leica-SP2 UV confocal microscope using the LSM imaging software program (Carl Zeiss, Jena, Germany) (scale bars: 10 μm).
Fig. 5
Fig. 5 Anticancer drug-induced apoptotic cell death in the Du145 cells in the 2D plate and the 3D cell chip. Cytotoxicity of mitroxanthrone in the Du145 cancer cells as determined using the MTT assay. The effect of mitroxanthrone (100, 200, 300, 400, and 500 μg/ml) on cell viability compared to the control group. *p<0.05 vs. 2D plate control.

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