Microfluidics Enabled Bottom-Up Engineering of 3D Vascularized Tumor for Drug Discovery
Open accessAbstract
Development of high-fidelity three-dimensional (3D) models to recapitulate the tumor microenvironment is essential for studying tumor biology and discovering anticancer drugs. Here we report a method to engineer the 3D microenvironment of human tumors, by encapsulating cancer cells in the core of microcapsules with a hydrogel shell for miniaturized 3D culture to obtain avascular microtumors first. The microtumors are then used as the building blocks for assembling with endothelial cells and other stromal cells to create macroscale 3D vascularized tumor. Cells in the engineered 3D microenvironment can yield significantly larger tumors in vivo than 2D-cultured cancer cells. Furthermore, the 3D vascularized tumors are 4.7 and 139.5 times more resistant to doxorubicin hydrochloride (a commonly used chemotherapy drug) than avascular microtumors and 2D-cultured cancer cells, respectively. Moreover, this high drug resistance of the 3D vascularized tumors can be overcome by using nanoparticle-mediated drug delivery. The high-fidelity 3D tumor model may be valuable for studying the effect of microenvironment on tumor progression, invasion, and metastasis and for developing effective therapeutic strategy to fight against cancer.
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The cancer cells within vascularized 3D-tumors were more resistant to DOX when compared to avascular microtumors and to 2D-cultured cancer cell monolayers (4.7- to 140-fold, respectively).
“The cancer cells within vascularized 3D-tumors were also more resistant to DOX when compared to avascular microtumors and to 2D-cultured cancer cell monolayers (4.7- to 140-fold, respectively).”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [57]
The Results and Discussion section reports that vascularized 3D tumors had a DOX IC50 4.7 times that of avascular microtumors and 139.5 times that of 2D-cultured MCF-7 cells. However, the vascularized-tumor IC50 was measured across all three cell types in the model, not cancer cells alone, so the fold changes are not established specifically for the cancer cells. (LLM, conf=0.82)
Experimental — accuracy not yet measuredAgarwal et al. found that cells could produce significantly larger cell aggregates in these 3D microenvironments than in 2D-culture systems.
“Agarwal et al. found that cells could produce significantly larger cell aggregates in these 3D microenvironments than in 2D-culture systems.”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [57]
In Results and Discussion, “Fabrication and characterization of avascular μtumors” (page unavailable), the paper reports that MCF-7 cells formed aggregates during 3D culture. It does not report that those aggregates were significantly larger than aggregates in 2D culture; its 3D-versus-2D comparisons concern other outcomes, including in vivo tumorigenicity and blood-vessel size. (LLM, conf=0.84)
Experimental — accuracy not yet measured3D culture systems more closely recapitulate the architecture and physiology of human solid tumors than traditional 2D systems.
“An extensive body of experimental evidence has established that 3D culture systems more closely recapitulate the architecture and the physiology of human solid tumors when compared with traditional 2D systems.”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [57]
Relevant features of cancer progression and the effectiveness of anticancer pharmaceutical compounds cannot be properly recapitulated in 2D cell culture systems.
“While 2D systems were the first workhorses in cancer research, a vast body of experimental evidence confirms that the relevant features of the cancer progression, and the effectiveness of anticancer pharmaceutical compounds, cannot be properly recapitulated in 2D cell culture systems [8,57,93].”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [57]
The presence of vascularization is one of the landmarks of tumor environments.
“The presence of vascularization is one of the landmarks of tumor environments [57,180].”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [57]
High-fidelity 3D models, such as the one presented by Agarwal et al., may be powerful tools that will provide insight into key processes of cancer progression that involve the role of vasculature within the tumor microenvironment.
“High-fidelity 3D models, such as the one presented by Agarwal et al. [57], may be powerful tools that will provide insight into key processes of cancer progression that involve the role of vasculature within the tumor microenvironment.”
From The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors (2019) · cites this paper as [57]
Gelatin-based hydrogels could support colorectal cancer organoid growth and metabolism comparably to those cultured in Geltrex.
“these gelatin‐based hydrogels could support colorectal cancer organoid growth and metabolism comparably to those cultured in Geltrex.”
From 3D Biomimetic Models to Reconstitute Tumor Microenvironment In Vitro: Spheroids, Organoids, and Tumor‐on‐a‐Chip (2023) · cites this paper as [94]
The Results section on avascular μtumors reports growth of MCF-7 breast cancer cells in collagen and collagen–alginate matrices. Searches for Geltrex and colorectal cancer organoids found no passage comparing their growth or metabolism in gelatin-based hydrogels with Geltrex cultures. No page numbers were provided for the indexed passages. (LLM, conf=0.77)
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Self-citation
- Authors
- Agarwal, P., Wang, H., Sun, M., Xu, J., Zhao, S., Liu, Z., Gooch, K. J., Zhao, Y., Lu, X., & He, X.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- He, Xiaoming
- ORCID
- Venue
- ACS Nano
- Publisher
- American Chemical Society (ACS)
- Published
- 2017-06-19
- Volume
- 11
- Issue
- 7
- Pages
- 6691-6702
- ISSN
- 1936-0851 (ISSN-L)
- 1936-086X
- PMC
- PMC5663446
- OpenAlex
- W2626777224
- Cited by
- 168
- References
- 62
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 25 · 2023: 22 · 2022: 23 · 2021: 32 · 2020: 13 · 2019: 13 · 2018: 14 · 2017: 2
- FWCI
- 5.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- ACS Nano (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01 CA206366)
- American Cancer Society (120936-RSG-11-109-01-CDD)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- 3D tumor models, tumor microenvironment, microfluidics, microcapsules, vascularized tumors, endothelial cells, doxorubicin resistance, anticancer drug discovery, nanoparticle drug delivery, chemoresistance
- MeSH terms
- Animals, Antineoplastic Agents, Drug Screening Assays, Antitumor, Female, Humans, Mice, Nude, Neoplasms, Neovascularization, Pathologic, Cell Culture Techniques, Drug Discovery, Lab-On-A-Chip Devices, Tumor Microenvironment, Human Umbilical Vein Endothelial Cells, MCF-7 Cells
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