A 3D Human Renal Cell Carcinoma-on-a-Chip for the Study of Tumor Angiogenesis

Neoplasia (United States)

Volumn 20, Issue 6, 2018, Pages 610-620

  Miller, Chris P ^a,b   Tsuchida, Connor ^c   Zheng, Ying ^a,b,c   Himmelfarb, Jonathan ^a   Akilesh, Shreeram ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b USA   (United States)

^c University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RELATED PROTEIN 4; PROSTAGLANDIN F; VASCULOTROPIN A; VASCULOTROPIN INHIBITOR; ANGIOGENIC FACTOR;

ANGIOGENESIS; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; HUVEC CELL LINE; KIDNEY CORTEX; MICROFLUIDICS; PRIMARY CULTURE; PRIORITY JOURNAL; RENAL CELL CARCINOMA; TISSUE ENGINEERING; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; UPREGULATION; CELL CULTURE TECHNIQUE; KIDNEY TUMOR; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PROCEDURES; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL;

ANGIOGENESIS INDUCING AGENTS; CARCINOMA, RENAL CELL; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; KIDNEY NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 85046654140     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2018.02.011     Document Type: Article

References (52)

1. National Cancer Institute, Surveillance, epidemiology, and end results program. Available from: https://seer.cancer.gov/statfacts/html/kidrp.html. (Accessed 21 September 2017)
2. Rini, BI, Campbell, SC, Escudier, B, Renal cell carcinoma. Lancet 373 (2009), 1119–1132.
3. Siegel, R, Naishadham, D, Jemal, A, Cancer statistics, 2013. CA Cancer J Clin 63 (2013), 11–30.
4. Gnarra, JR, Tory, K, Weng, Y, Schmidt, L, Wei, MH, Li, H, Latif, F, Liu, S, Chen, F, Duh, FM, et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet 7 (1994), 85–90.
5. Latif, F, Tory, K, Gnarra, J, Yao, M, Duh, FM, Orcutt, ML, Stackhouse, T, Kuzmin, I, Modi, W, Geil, L, et al. Identification of the von Hippel–Lindau disease tumor suppressor gene. Science 260 (1993), 1317–1320.
6. Forsythe, JA, Jiang, BH, Iyer, NV, Agani, F, Leung, SW, Koos, RD, Semenza, GL, Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16 (1996), 4604–4613.
7. Wettersten, HI, Aboud, OA, Lara, PN Jr., Weiss, RH, Metabolic reprogramming in clear cell renal cell carcinoma. Nat Rev Nephrol 13 (2017), 410–419.
8. Motzer, RJ, Hutson, TE, Tomczak, P, Michaelson, MD, Bukowski, RM, Rixe, O, Oudard, S, Negrier, S, Szczylik, C, Kim, ST, et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 356 (2007), 115–124.
9. Rini, BI, Atkins, MB, Resistance to targeted therapy in renal-cell carcinoma. Lancet Oncol 10 (2009), 992–1000.
10. Yang, JC, Haworth, L, Sherry, RM, Hwu, P, Schwartzentruber, DJ, Topalian, SL, Steinberg, SM, Chen, HX, Rosenberg, SA, A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349 (2003), 427–434.
11. Porter, SN, Baker, LC, Mittelman, D, Porteus, MH, Lentiviral and targeted cellular barcoding reveals ongoing clonal dynamics of cell lines in vitro and in vivo. Genome Biol, 15, 2014, R75.
12. Batchelder, CA, Martinez, ML, Duru, N, Meyers, FJ, Tarantal, AF, Three dimensional culture of human renal cell carcinoma organoids. PLoS One, 10, 2015, e0136758.
13. Kaelin, WG, Von Hippel-Lindau disease. Annu Rev Pathol 2 (2007), 145–173.
14. Haase, VH, Glickman, JN, Socolovsky, M, Jaenisch, R, Vascular tumors in livers with targeted inactivation of the von Hippel–Lindau tumor suppressor. Proc Natl Acad Sci U S A 98 (2001), 1583–1588.
15. Kleymenova, E, Everitt, JI, Pluta, L, Portis, M, Gnarra, JR, Walker, CL, Susceptibility to vascular neoplasms but no increased susceptibility to renal carcinogenesis in Vhl knockout mice. Carcinogenesis 25 (2004), 309–315.
16. Rankin, EB, Tomaszewski, JE, Haase, VH, Renal cyst development in mice with conditional inactivation of the von Hippel–Lindau tumor suppressor. Cancer Res 66 (2006), 2576–2583.
17. Fu, L, Wang, G, Shevchuk, MM, Nanus, DM, Gudas, LJ, Generation of a mouse model of Von Hippel–Lindau kidney disease leading to renal cancers by expression of a constitutively active mutant of HIF1alpha. Cancer Res 71 (2011), 6848–6856.
18. Harlander, S, Schonenberger, D, Toussaint, NC, Prummer, M, Catalano, A, Brandt, L, Moch, H, Wild, PJ, Frew, IJ, Combined mutation in Vhl, Trp53 and Rb1 causes clear cell renal cell carcinoma in mice. Nat Med 23 (2017), 869–877.
19. Chen, W, Hill, H, Christie, A, Kim, MS, Holloman, E, Pavia-Jimenez, A, Homayoun, F, Ma, Y, Patel, N, Yell, P, et al. Targeting renal cell carcinoma with a HIF-2 antagonist. Nature 539 (2016), 112–117.
20. Pavia-Jimenez, A, Tcheuyap, VT, Brugarolas, J, Establishing a human renal cell carcinoma tumorgraft platform for preclinical drug testing. Nat Protoc 9 (2014), 1848–1859.
21. Sivanand, S, Pena-Llopis, S, Zhao, H, Kucejova, B, Spence, P, Pavia-Jimenez, A, Yamasaki, T, McBride, DJ, Gillen, J, Wolff, NC, et al. A validated tumorgraft model reveals activity of dovitinib against renal cell carcinoma. Sci Transl Med, 4, 2012, 137ra175.
22. Tran, TA, Leong, HS, Pavia-Jimenez, A, Fedyshyn, S, Yang, J, Kucejova, B, Sivanand, S, Spence, P, Xie, XJ, Pena-Llopis, S, et al. Fibroblast growth factor receptor-dependent and -independent paracrine signaling by sunitinib-resistant renal cell carcinoma. Mol Cell Biol 36 (2016), 1836–1855.
23. Weber, EJ, Chapron, A, Chapron, BD, Voellinger, JL, Lidberg, KA, Yeung, CK, Wang, Z, Yamaura, Y, Hailey, DW, Neumann, T, et al. Development of a microphysiological model of human kidney proximal tubule function. Kidney Int 90 (2016), 627–637.
24. Network TCGAR, Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499 (2013), 43–49.
25. Bjerregaard, H, Pedersen, S, Kristensen, SR, Marcussen, N, Reference genes for gene expression analysis by real-time reverse transcription polymerase chain reaction of renal cell carcinoma. Diagn Mol Pathol 20 (2011), 212–217.
26. Cross, VL, Zheng, Y, Won Choi, N, Verbridge, SS, Sutermaster, BA, Bonassar, LJ, Fischbach, C, Stroock, AD, Dense type I collagen matrices that support cellular remodeling and microfabrication for studies of tumor angiogenesis and vasculogenesis in vitro. Biomaterials 31 (2010), 8596–8607.
27. Nagao, RJ, Xu, J, Luo, P, Xue, J, Wang, Y, Kotha, S, Zeng, W, Fu, X, Himmelfarb, J, Zheng, Y, Decellularized human kidney cortex hydrogels enhance kidney microvascular endothelial cell maturation and quiescence. Tissue Eng Part A 22 (2016), 1140–1150.
28. Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T, Preibisch, S, Rueden, C, Saalfeld, S, Schmid, B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 9 (2012), 676–682.
29. COMSOL, Multiphysics Modeling Software. Available from: https://www.comsol.com/.
30. Cho, CH, Park, J, Nagrath, D, Tilles, AW, Berthiaume, F, Toner, M, Yarmush, ML, Oxygen uptake rates and liver-specific functions of hepatocyte and 3T3 fibroblast co-cultures. Biotechnol Bioeng 97 (2007), 188–199.
31. Rudge, JS, Holash, J, Hylton, D, Russell, M, Jiang, S, Leidich, R, Papadopoulos, N, Pyles, EA, Torri, A, Wiegand, SJ, et al. VEGF Trap complex formation measures production rates of VEGF, providing a biomarker for predicting efficacious angiogenic blockade. Proc Natl Acad Sci U S A 104 (2007), 18363–18370.
32. Ahn, J, Sei, YJ, Jeon, NL, Kim, Y, Tumor microenvironment on a chip: the progress and future perspective. Bioengineering (Basel), 4, 2017, E64.
33. Weeber, F, Ooft, SN, Dijkstra, KK, Voest, EE, Tumor organoids as a pre-clinical cancer model for drug discovery. Cell Chem Biol 24 (2017), 1092–1100.
34. Weiswald, LB, Bellet, D, Dangles-Marie, V, Spherical cancer models in tumor biology. Neoplasia 17 (2015), 1–15.
35. Tourovskaia, A, Fauver, M, Kramer, G, Simonson, S, Neumann, T, Tissue-engineered microenvironment systems for modeling human vasculature. Exp Biol Med (Maywood) 239 (2014), 1264–1271.
36. Li, R, Hebert, JD, Lee, TA, Xing, H, Boussommier-Calleja, A, Hynes, RO, Lauffenburger, DA, Kamm, RD, Macrophage-secreted TNFalpha and TGFbeta1 influence migration speed and persistence of cancer cells in 3D tissue culture via independent pathways. Cancer Res 77 (2017), 279–290.
37. Pavesi, A, Tan, AT, Koh, S, Chia, A, Colombo, M, Antonecchia, E, Miccolis, C, Ceccarello, E, Adriani, G, Raimondi, MT, et al. A 3D microfluidic model for preclinical evaluation of TCR-engineered T cells against solid tumors. JCI Insight, 2, 2017, e89762.
38. Chen, MB, Whisler, JA, Frose, J, Yu, C, Shin, Y, Kamm, RD, On-chip human microvasculature assay for visualization and quantification of tumor cell extravasation dynamics. Nat Protoc 12 (2017), 865–880.
39. Jeon, JS, Bersini, S, Gilardi, M, Dubini, G, Charest, JL, Moretti, M, Kamm, RD, Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation. Proc Natl Acad Sci U S A 112 (2015), 214–219.
40. Moya, M, Tran, D, George, SC, An integrated in vitro model of perfused tumor and cardiac tissue. Stem Cell Res Ther, 4(Suppl 1), 2013, S15.
41. Sobrino, A, Phan, DT, Datta, R, Wang, X, Hachey, SJ, Romero-Lopez, M, Gratton, E, Lee, AP, George, SC, Hughes, CC, 3D microtumors in vitro supported by perfused vascular networks. Sci Rep, 6, 2016, 31589.
42. Bray, LJ, Werner, C, Evaluation of three-dimensional in vitro models to study tumor angiogenesis. ACS Biomater Sci Eng, 2017, 10.1021/acsbiomaterials.7b00139.
43. Correa de Sampaio, P, Auslaender, D, Krubasik, D, Failla, AV, Skepper, JN, Murphy, G, English, WR, A heterogeneous in vitro three dimensional model of tumour-stroma interactions regulating sprouting angiogenesis. PLoS One, 7, 2012, e30753.
44. Janvier, R, Sourla, A, Koutsilieris, M, Doillon, CJ, Stromal fibroblasts are required for PC-3 human prostate cancer cells to produce capillary-like formation of endothelial cells in a three-dimensional co-culture system. Anticancer Res 17 (1997), 1551–1557.
45. Kim, S, Lee, H, Chung, M, Jeon, NL, Engineering of functional, perfusable 3D microvascular networks on a chip. Lab Chip 13 (2013), 1489–1500.
46. Szot, CS, Buchanan, CF, Freeman, JW, Rylander, MN, In vitro angiogenesis induced by tumor-endothelial cell co-culture in bilayered, collagen I hydrogel bioengineered tumors. Tissue Eng Part C Methods 19 (2013), 864–874.
47. Zheng, Y, Sun, Y, Yu, X, Shao, Y, Zhang, P, Dai, G, Fu, J, Angiogenesis in liquid tumors: an in vitro assay for leukemic-cell-induced bone marrow angiogenesis. Adv Healthc Mater 5 (2016), 1014–1024.
48. Gerlinger, M, Rowan, AJ, Horswell, S, Math, M, Larkin, J, Endesfelder, D, Gronroos, E, Martinez, P, Matthews, N, Stewart, A, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366 (2012), 883–892.
49. Augustin, HG, Koh, GY, Organotypic vasculature: from descriptive heterogeneity to functional pathophysiology. Science, 357, 2017.
50. Nolan, DJ, Ginsberg, M, Israely, E, Palikuqi, B, Poulos, MG, James, D, Ding, BS, Schachterle, W, Liu, Y, Rosenwaks, Z, et al. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell 26 (2013), 204–219.
51. Ligresti, G, Nagao, RJ, Xue, J, Choi, YJ, Xu, J, Ren, S, Aburatani, T, Anderson, SK, MacDonald, JW, Bammler, TK, et al. A novel three-dimensional human peritubular microvascular system. J Am Soc Nephrol 27 (2016), 2370–2381.
52. Tykodi, SS, Satoh, S, Deming, JD, Chou, J, Harrop, R, Warren, EH, CD8+ T-cell clones specific for the 5T4 antigen target renal cell carcinoma tumor-initiating cells in a murine xenograft model. J Immunother 35 (2012), 523–533.