Liver-Tumor Hybrid Organoids for Modeling Tumor Growth and Drug Response In Vitro

Annals of Biomedical Engineering

Volumn 43, Issue 10, 2015, Pages 2361-2373

  Skardal, Aleksander ^a   Devarasetty, Mahesh ^a   Rodman, Christopher ^a   Atala, Anthony ^a   Soker, Shay ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Drug screening; Metastasis; Organoids; Tissue engineering; Tumor models

Indexed keywords

CELL MEMBRANES; CELL PROLIFERATION; CELLS; CYTOLOGY; DISEASES; PATHOLOGY; TISSUE; TISSUE CULTURE; TISSUE ENGINEERING; TUMORS;

DRUG SCREENING; IMMUNOFLUORESCENT STAINING; METASTASIS; ORGANOIDS; PHENOTYPIC DIFFERENCES; ROTATING WALL VESSEL BIOREACTORS; THREEDIMENSIONAL (3-D); TUMOR MODELS;

DIAGNOSIS;

CELL SURFACE MARKER; FLUOROURACIL;

ARTICLE; BIOREACTOR; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DRUG RESPONSE; HUMAN; HUMAN CELL; HYBRID CELL; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; IN VIVO STUDY; LIVER METASTASIS; PHENOTYPE; PRIORITY JOURNAL; TISSUE CULTURE; TUMOR CELL INOCULATION; TUMOR GROWTH; TUMOR MODEL; WNT SIGNALING PATHWAY; COCULTURE; COLON TUMOR; DRUG EFFECTS; DRUG SCREENING; HEP-G2 CELL LINE; LIVER NEOPLASMS; METABOLISM; PATHOLOGY; PROCEDURES; TUMOR MICROENVIRONMENT;

COCULTURE TECHNIQUES; COLONIC NEOPLASMS; DRUG SCREENING ASSAYS, ANTITUMOR; FLUOROURACIL; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; ORGANOIDS; TUMOR MICROENVIRONMENT;

EID: 84941876769     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-015-1298-3     Document Type: Article

References (57)

1. Achilli, T. M., J. Meyer, and J. R. Morgan. Advances in the formation, use and understanding of multi-cellular spheroids. Expert Opin. Biol. Ther. 12:1347–1360, 2012.
2. Attoub, S., C. Rivat, S. Rodrigues, S. Van Bocxlaer, M. Bedin, E. Bruyneel, C. Louvet, M. Kornprobst, T. Andre, M. Mareel, J. Mester, and C. Gespach. The c-kit tyrosine kinase inhibitor STI571 for colorectal cancer therapy. Cancer Res. 62:4879–4883, 2002.
3. Barrila, J., A. Radtke, A. Crabbé, S. Sarker, M. M. Herbst-Kralovetz, C. M. Ott, and C. A. Nickerson. Organotypic 3D cell culture models: using the rotating wall vessel to study host-pathogen interactions. Nat. Rev. Microbiol. 8:791–801, 2010.
4. Behrens, J. Control of beta-catenin signaling in tumor development. Ann. NY Acad. Sci. 910:21–33, 2000; (discussion 33–25).
5. Botchkina, I. L., R. A. Rowehl, D. E. Rivadeneira, M. S. Karpeh, Jr., H. Crawford, A. Dufour, J. Ju, Y. Wang, Y. Leyfman, and G. I. Botchkina. Phenotypic subpopulations of metastatic colon cancer stem cells: genomic analysis. Cancer Genom. Proteom. 6:19–29, 2009.
6. Brantjes, H., N. Barker, J. van Es, and H. Clevers. TCF: Lady Justice casting the final verdict on the outcome of Wnt signalling. Biol. Chem. 383:255–261, 2002.
7. Brattain, M. G., W. D. Fine, F. M. Khaled, J. Thompson, and D. E. Brattain. Heterogeneity of malignant cells from a human colonic carcinoma. Cancer Res. 41:1751–1756, 1981.
8. Burdick, J. A., and G. D. Prestwich. Hyaluronic acid hydrogels for biomedical applications. Adv. Mater. 23:H41–H56, 2011.
9. Bursac, N., Y. Loo, K. Leong, and L. Tung. Novel anisotropic engineered cardiac tissues: studies of electrical propagation. Biochem. Biophys. Res. Commun. 361:847–853, 2007.
10. Carterson, A. J., K. Honer zu Bentrup, C. M. Ott, M. S. Clarke, D. L. Pierson, C. R. Vanderburg, K. L. Buchanan, C. A. Nickerson, and M. J. Schurr. A549 lung epithelial cells grown as three-dimensional aggregates: alternative tissue culture model for Pseudomonas aeruginosa pathogenesis. Infect. Immun. 73:1129–1140, 2005.
11. Drewitz, M., M. Helbling, N. Fried, M. Bieri, W. Moritz, J. Lichtenberg, and J. M. Kelm. Towards automated production and drug sensitivity testing using scaffold-free spherical tumor microtissues. Biotechnol. J. 6:1488–1496, 2011.
12. Erickson, I. E., A. H. Huang, C. Chung, R. T. Li, J. A. Burdick, and R. L. Mauck. Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels. Tissue Eng. Part A 15:1041–1052, 2009.
13. Frye, C. A., and C. W. Patrick. Three-dimensional adipose tissue model using low shear bioreactors. Vitro Cell Dev. Biol. Anim. 42:109–114, 2006.
14. Gavert, N. and A. Ben-Ze’ev. Coordinating changes in cell adhesion and phenotype during EMT-like processes in cancer. F1000 Biol Rep. 2:86, 2010.
15. Gerecht, S., J. A. Burdick, L. S. Ferreira, S. A. Townsend, R. Langer, and G. Vunjak-Novakovic. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc. Natl. Acad. Sci. USA. 104:11298–11303, 2007.
16. Hjelm, B. E., A. N. Berta, C. A. Nickerson, C. J. Arntzen, and M. M. Herbst-Kralovetz. Development and characterization of a three-dimensional organotypic human vaginal epithelial cell model. Biol. Reprod. 82:617–627, 2010.
17. Ho, W. J., E. A. Pham, J. W. Kim, C. W. Ng, J. H. Kim, D. T. Kamei, and B. M. Wu. Incorporation of multicellular spheroids into 3D polymeric scaffolds provides an improved tumor model for screening anticancer drugs. Cancer Sci. 101:2637–2643, 2010.
18. Honer zu Bentrup, K., R. Ramamurthy, C. M. Ott, K. Emami, M. Nelman-Gonzalez, J. W. Wilson, E. G. Richter, T. J. Goodwin, J. S. Alexander, D. L. Pierson, N. Pellis, K. L. Buchanan, and C. A. Nickerson. Three-dimensional organotypic models of human colonic epithelium to study the early stages of enteric salmonellosis. Microbes. Infect. 8:1813–1825, 2006.
19. Karakiulakis, G., C. Papanikolaou, S. M. Jankovic, A. Aletras, E. Papakonstantinou, E. Vretou, and V. Mirtsou-Fidani. Increased type IV collagen-degrading activity in metastases originating from primary tumors of the human colon. Invasion Metastasis 17:158–168, 1997.
20. LaMarca, H. L., C. M. Ott, K. Honer Zu Bentrup, C. L. Leblanc, D. L. Pierson, A. B. Nelson, A. B. Scandurro, G. S. Whitley, C. A. Nickerson, and C. A. Morris. Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta. 26:709–720, 2005.
21. Leach, J. B., K. A. Bivens, C. N. Collins, and C. E. Schmidt. Development of photocrosslinkable hyaluronic acid-polyethylene glycol-peptide composite hydrogels for soft tissue engineering. J. Biomed. Mater. Res. A. 70:74–82, 2004.
22. Liu, Y., X. Z. Shu, and G. D. Prestwich. Tumor engineering: orthotopic cancer models in mice using cell-loaded, injectable, cross-linked hyaluronan-derived hydrogels. Tissue Eng. 13:1091–1101, 2007.
23. Macedo, F. I., and T. Makarawo. Colorectal hepatic metastasis: Evolving therapies. World. J. Hepatol. 6:453–463, 2014.
24. May, J. E., J. Xu, H. R. Morse, N. D. Avent, and C. Donaldson. Toxicity testing: the search for an in vitro alternative to animal testing. Br. J. Biomed. Sci. 66:160–165, 2009.
25. McGrail, D. J., R. Mezencev, Q. M. Kieu, J. F. McDonald, and M. R. Dawson. SNAIL-induced epithelial-to-mesenchymal transition produces concerted biophysical changes from altered cytoskeletal gene expression. FASEB J. 29:1–10, 2014.
26. Miki, D., K. Dastgheib, T. Kim, A. Pfister-Serres, K. A. Smeds, M. Inoue, D. L. Hatchell, and M. W. Grinstaff. A photopolymerized sealant for corneal lacerations. Cornea 21:393–399, 2002.
27. Myers, T. A., C. A. Nickerson, D. Kaushal, C. M. Ott, K. Honer zu Bentrup, M. Nelman-Gonzalez, R. Ramamurthy, D. L. Pierson, and M. T. Philipp. Closing the phenotypic gap between transformed neuronal cell lines in culture and untransformed neurons. J. Neurosci. Methods 174:31–41, 2008.
28. Navran, S. The application of low shear modeled microgravity to 3D cell biology and tissue engineering. Biotechnol. Annu. Rev. 14:275–296, 2008.
29. Nickerson, C. A., and C. M. Ott. A new dimension in modeling infectious disease. ASM News. 70:169–175, 2004.
30. Nickerson, C. A., T. J. Goodwin, J. Terlonge, C. M. Ott, K. L. Buchanan, W. C. Uicker, K. Emami, C. L. LeBlanc, R. Ramamurthy, M. S. Clarke, C. R. Vanderburg, T. Hammond, and D. L. Pierson. Three-dimensional tissue assemblies: novel models for the study of Salmonella enterica serovar Typhimurium pathogenesis. Infect. Immun. 69:7106–7120, 2001.
31. Nickerson, C. A., E. G. Richter, and C. M. Ott. Studying host-pathogen interactions in 3D: organotypic models for infectious disease and drug development. J Neuroimmune Pharmacol. 2:26–31, 2007.
32. Nishioka, M., K. Ueno, S. Hazama, T. Okada, K. Sakai, Y. Suehiro, N. Okayama, H. Hirata, M. Oka, K. Imai, R. Dahiya, and Y. Hinoda. Possible involvement of Wnt11 in colorectal cancer progression. Mol. Carcinog. 52:207–217, 2013.
33. Ogunwobi, O. O., and C. Liu. Therapeutic and prognostic importance of epithelial-mesenchymal transition in liver cancers: insights from experimental models. Crit. Rev. Oncol. Hematol. 83:319–328, 2012.
34. Orsulic, S., O. Huber, H. Aberle, S. Arnold, and R. Kemler. E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. J. Cell Sci. 112(Pt 8):1237–1245, 1999.
35. Prestwich, G. D. Evaluating drug efficacy and toxicology in three dimensions: using synthetic extracellular matrices in drug discovery. Acc. Chem. Res. 41:139–148, 2008.
36. Sainz, Jr., B., V. TenCate, and S. L. Uprichard. Three-dimensional Huh7 cell culture system for the study of Hepatitis C virus infection. Virol J. 6:103, 2009.
37. Schwarz, R. P., T. J. Goodwin, and D. A. Wolf. Cell culture for three-dimensional modeling in rotating-wall vessels: an application of simulated microgravity. J Tissue Cult. Methods. 14:51–57, 1992.
38. Serban, M. A., A. Scott, and G. D. Prestwich. Use of hyaluronan-derived hydrogels for three-dimensional cell culture and tumor xenografts. Curr. Protoc. Cell Biol. Chapter 10:Unit 10.14, 2008. doi:10.1002/0471143030.cb1014s40
39. Shu, X. Z., Y. Liu, F. S. Palumbo, Y. Luo, and G. D. Prestwich. In situ crosslinkable hyaluronan hydrogels for tissue engineering. Biomaterials 25:1339–1348, 2004.
40. Shu, X. Z., S. Ahmad, Y. Liu, and G. D. Prestwich. Synthesis and evaluation of injectable, in situ crosslinkable synthetic extracellular matrices for tissue engineering. J. Biomed. Mater. Res. A. 79:902–912, 2006.
41. Skardal, A. Hyaluronan and gelatin biomaterials for bioprinting engineered tissues. Department of Bioengineering, University of Utah. Ph.D. Dissertation:208, 2010.
42. Skardal, A., S. F. Sarker, A. Crabbe, C. A. Nickerson, and G. D. Prestwich. The generation of 3D tissue models based on hyaluronan hydrogel-coated microcarriers within a rotating wall vessel bioreactor. Biomaterials 31:8426–8435, 2010.
43. Skardal, A., J. Zhang, L. McCoard, S. Oottamasathien, and G. D. Prestwich. Dynamically crosslinked gold nanoparticle—hyaluronan hydrogels. Adv. Mater. 22:4736–4740, 2010.
44. Skardal, A., J. Zhang, and G. D. Prestwich. Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 31:6173–6181, 2010.
45. Skardal, A., L. Smith, S. Bharadwaj, A. Atala, S. Soker, and Y. Zhang. Tissue specific synthetic ECM hydrogels for 3D in vitro maintenance of hepatocyte function. Biomaterials 33:4565–4575, 2012.
46. Smith, Y. C., K. K. Grande, S. B. Rasmussen, and A. D. O’Brien. Novel three-dimensional organoid model for evaluation of the interaction of uropathogenic Escherichia coli with terminally differentiated human urothelial cells. Infect. Immun. 74:750–757, 2006.
47. Steinert, G., S. Scholch, M. Koch, and J. Weitz. Biology and significance of circulating and disseminated tumour cells in colorectal cancer. Langenbecks Arch Surg. 397:535–542, 2012.
48. Strillacci, A., M. C. Valerii, P. Sansone, C. Caggiano, A. Sgromo, L. Vittori, M. Fiorentino, G. Poggioli, F. Rizzello, M. Campieri, and E. Spisni. Loss of miR-101 expression promotes Wnt/beta-catenin signalling pathway activation and malignancy in colon cancer cells. J. Pathol. 229:379–389, 2013.
49. Tania, M., M. A. Khan, and J. Fu. Epithelial to mesenchymal transition inducing transcription factors and metastatic cancer. Tumour Biol. 35:7335–7342, 2014.
50. Unsworth, B. R., and P. I. Lelkes. Growing tissues in microgravity. Nat. Med. 4:901–907, 1998.
51. Vandamme, T. F. Use of rodents as models of human diseases. J. Pharm. Bioallied. Sci. 6:2–9, 2014.
52. Wheeler, S. E., A. M. Clark, D. P. Taylor, C. L. Young, V. C. Pillai, D. B. Stolz, R. Venkataramanan, D. Lauffenburger, L. Griffith, and A. Wells. Spontaneous dormancy of metastatic breast cancer cells in an all human liver microphysiologic system. Br. J. Cancer. 111(12):2342–2350, 2014.
53. Wilson, P. M., P. V. Danenberg, P. G. Johnston, H. J. Lenz, and R. D. Ladner. Standing the test of time: targeting thymidylate biosynthesis in cancer therapy. Nat. Rev. Clin. Oncol. 11:282–298, 2014.
54. Yoffe, B., G. J. Darlington, H. E. Soriano, B. Krishnan, D. Risin, N. R. Pellis, and V. I. Khaoustov. Cultures of human liver cells in simulated microgravity environment. Adv. Space Res. 24:829–836, 1999.
55. Yoshioka, T., H. Mishima, Y. Ohyabu, S. Sakai, H. Akaogi, T. Ishii, H. Kojima, J. Tanaka, N. Ochiai, and T. Uemura. Repair of large osteochondral defects with allogeneic cartilaginous aggregates formed from bone marrow-derived cells using RWV bioreactor. J. Orthop. Res. 25:1291–1298, 2007.
56. Young, M., L. Ordonez, and A. R. Clarke. What are the best routes to effectively model human colorectal cancer? Mol. Oncol. 7:178–189, 2013.
57. Zaman, M. H., L. M. Trapani, A. L. Sieminski, D. Mackellar, H. Gong, R. D. Kamm, A. Wells, D. A. Lauffenburger, and P. Matsudaira. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA. 103:10889–10894, 2006.