Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

3D Culture Modelling: An Emerging Approach for Translational Cancer Research in Sarcomas

Author(s): Victoria Heredia-Soto, Andrés Redondo, José Juan Pozo Kreilinger, Virginia Martínez-Marín, Alberto Berjón and Marta Mendiola*

Volume 27, Issue 29, 2020

Page: [4778 - 4788] Pages: 11

DOI: 10.2174/0929867326666191212162102

Price: $65

Abstract

Sarcomas are tumours of mesenchymal origin, which can arise in bone or soft tissues. They are rare but frequently quite aggressive and with a poor outcome. New approaches are needed to characterise these tumours and their resistance mechanisms to current therapies, responsible for tumour recurrence and treatment failure. This review is focused on the potential of three-dimensional (3D) in vitro models, including multicellular tumour spheroids (MCTS) and organoids, and the latest data about their utility for the study on important properties for tumour development. The use of spheroids as a particularly valuable alternative for compound high throughput screening (HTS) in different areas of cancer biology is also discussed, which enables the identification of new therapeutic opportunities in commonly resistant tumours.

Keywords: 3D culture, in vitro models, sarcoma, multicellular tumour spheroids (MCTS), cancer, high throughput screening (HTS).

« Previous Next »
[1]
Taylor, B.S.; Barretina, J.; Maki, R.G.; Antonescu, C.R.; Singer, S.; Ladanyi, M. Advances in sarcoma genomics and new therapeutic targets. Nat. Rev. Cancer, 2011, 11(8), 541-557.
[http://dx.doi.org/10.1038/nrc3087] [PMID: 21753790]
[2]
Doyle, L.A. Sarcoma classification: an update based on the 2013 World Health Organization Classification of tumors of soft tissue and bone. Cancer, 2014, 120(12), 1763-1774.
[http://dx.doi.org/10.1002/cncr.28657] [PMID: 24648013]
[3]
(a)Nielsen, T.O.; West, R.B. Translating gene expression into clinical care: sarcomas as a paradigm. J. Clin. Oncol., 2010, 28(10), 1796-1805.
[http://dx.doi.org/10.1200/JCO.2009.26.1917] [PMID: 20194847]
(b)Bovée, J.V.; Hogendoorn, P.C. Molecular pathology of sarcomas: concepts and clinical implications. Virchows Arch., 2010, 456(2), 193-199.
[http://dx.doi.org/10.1007/s00428-009-0828-5] [PMID: 19787372]
[4]
Fletcher, C.D. The evolving classification of soft tissue tumours - an update based on the new 2013 WHO classification. Histopathology, 2014, 64(1), 2-11.
[http://dx.doi.org/10.1111/his.12267] [PMID: 24164390]
[5]
(a)Sugita, S.; Arai, Y.; Tonooka, A.; Hama, N.; Totoki, Y.; Fujii, T.; Aoyama, T.; Asanuma, H.; Tsukahara, T.; Kaya, M.; Shibata, T.; Hasegawa, T. A novel CIC-FOXO4 gene fusion in undifferentiated small round cell sarcoma: a genetically distinct variant of Ewing-like sarcoma. Am. J. Surg. Pathol., 2014, 38(11), 1571-1576.
[http://dx.doi.org/10.1097/PAS.0000000000000286] [PMID: 25007147]
(b)Graham, C.; Chilton-MacNeill, S.; Zielenska, M.; Somers, G.R. The CIC-DUX4 fusion transcript is present in a subgroup of pediatric primitive round cell sarcomas. Hum. Pathol, 2012, 43(2), 180-189.
[http://dx.doi.org/10.1016/j.humpath.2011.04.023] [PMID: 21813156]
[6]
Puls, F.; Niblett, A.; Marland, G.; Gaston, C.L.; Douis, H.; Mangham, D.C.; Sumathi, V.P.; Kindblom, L.G. BCOR-CCNB3 (Ewing-like) sarcoma: a clinicopathologic analysis of 10 cases, in comparison with conventional Ewing sarcoma. Am. J. Surg. Pathol., 2014, 38(10), 1307-1318.
[http://dx.doi.org/10.1097/PAS.0000000000000223] [PMID: 24805859]
[7]
Oliner, J.D.; Pietenpol, J.A.; Thiagalingam, S.; Gyuris, J.; Kinzler, K.W.; Vogelstein, B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature, 1993, 362(6423), 857-860.
[http://dx.doi.org/10.1038/362857a0] [PMID: 8479525]
[8]
Crozat, A.; Aman, P.; Mandahl, N.; Ron, D. Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature, 1993, 363(6430), 640-644.
[http://dx.doi.org/10.1038/363640a0] [PMID: 8510758]
[9]
Recine, F.; Bongiovanni, A.; Riva, N.; Fausti, V.; De Vita, A.; Mercatali, L.; Liverani, C.; Miserocchi, G.; Amadori, D.; Ibrahim, T. Update on the role of trabectedin in the treatment of intractable soft tissue sarcomas. OncoTargets Ther., 2017, 10, 1155-1164.
[http://dx.doi.org/10.2147/OTT.S127955] [PMID: 28260930]
[10]
Nussbaum, D.P.; Rushing, C.N.; Lane, W.O.; Cardona, D.M.; Kirsch, D.G.; Peterson, B.L.; Blazer, D.G., III Preoperative or postoperative radiotherapy versus surgery alone for retroperitoneal sarcoma: a case-control, propensity score-matched analysis of a nationwide clinical oncology database. Lancet Oncol., 2016, 17(7), 966-975.
[http://dx.doi.org/10.1016/S1470-2045(16)30050-X] [PMID: 27210906]
[11]
Group, E.S.E.S.N.W. ESMO/European Sarcoma Network Working Group. Soft tissue and visceral sarcomas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol., 2014, 25(Suppl. 3), iii102-iii112.
[http://dx.doi.org/10.1093/annonc/mdu254] [PMID: 25210080]
[12]
Judson, I.; Verweij, J.; Gelderblom, H.; Hartmann, J.T.; Schöffski, P.; Blay, J.Y.; Kerst, J.M.; Sufliarsky, J.; Whelan, J.; Hohenberger, P.; Krarup-Hansen, A.; Alcindor, T.; Marreaud, S.; Litière, S.; Hermans, C.; Fisher, C.; Hogendoorn, P.C. dei Tos, A.P.; van der Graaf, W.T. European Organisation and Treatment of Cancer Soft Tissue and Bone Sarcoma Group. Doxorubicin alone versus intensified doxorubicin plus ifosfamide for first-line treatment of advanced or metastatic soft-tissue sarcoma: a randomised controlled phase 3 trial. Lancet Oncol., 2014, 15(4), 415-423.
[http://dx.doi.org/10.1016/S1470-2045(14)70063-4] [PMID: 24618336]
[13]
(a)Khalifa, J.; Ouali, M.; Chaltiel, L.; Le Guellec, S.; Le Cesne, A.; Blay, J.Y.; Cousin, P.; Chaigneau, L.; Bompas, E.; Piperno-Neumann, S.; Bui-Nguyen, B.; Rios, M.; Delord, J.P.; Penel, N.; Chevreau, C. Efficacy of trabectedin in malignant solitary fibrous tumors: a retrospective analysis from the French Sarcoma Group. BMC Cancer, 2015, 15, 700.
[http://dx.doi.org/10.1186/s12885-015-1697-8] [PMID: 26472661]
(b)Sanfilippo, R.; Dileo, P.; Blay, J.Y.; Constantinidou, A.; Le Cesne, A.; Benson, C.; Vizzini, L.; Contu, M.; Baldi, G.G.; Dei Tos, A.P.; Casali, P.G. Trabectedin in advanced synovial sarcomas: a multicenter retrospective study from four European institutions and the Italian Rare Cancer Network. Anticancer Drugs, 2015, 26(6), 678-681.
[PMID: 25763543]
[14]
Schöffski, P.; Chawla, S.; Maki, R.G.; Italiano, A.; Gelderblom, H.; Choy, E.; Grignani, G.; Camargo, V.; Bauer, S.; Rha, S.Y.; Blay, J.Y.; Hohenberger, P.; D’Adamo, D.; Guo, M.; Chmielowski, B.; Le Cesne, A.; Demetri, G.D.; Patel, S.R. Eribulin versus dacarbazine in previously treated patients with advanced liposarcoma or leiomyosarcoma: a randomised, open-label, multicentre, phase 3 trial. Lancet, 2016, 387(10028), 1629-1637.
[http://dx.doi.org/10.1016/S0140-6736(15)01283-0] [PMID: 26874885]
[15]
(a)Heinrich, M.C.; Corless, C.L.; Demetri, G.D.; Blanke, C.D.; von Mehren, M.; Joensuu, H.; McGreevey, L.S.; Chen, C.J.; Van den Abbeele, A.D.; Druker, B.J.; Kiese, B.; Eisenberg, B.; Roberts, P.J.; Singer, S.; Fletcher, C.D.; Silberman, S.; Dimitrijevic, S.; Fletcher, J.A. Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J. Clin. Oncol, 2003, 21(23), 4342-4349.
[http://dx.doi.org/10.1200/JCO.2003.04.190] [PMID: 14645423]
(b)Poveda, A.; del Muro, X.G.; López-Guerrero, J.A.; Martínez, V.; Romero, I.; Valverde, C.; Cubedo, R.; Martín-Broto, J. GEIS 2013 guidelines for gastrointestinal sarcomas (GIST). Cancer Chemother. Pharmacol, 2014, 74(5), 883-898.
[http://dx.doi.org/10.1007/s00280-014-2547-0] [PMID: 25193432]
[16]
(a)Malhotra, B.; Schuetze, S.M. Dermatofibrosarcoma protruberans treatment with platelet-derived growth factor receptor inhibitor: a review of clinical trial results. Curr. Opin. Oncol., 2012, 24(4), 419-424.
[http://dx.doi.org/10.1097/CCO.0b013e328353d78d] [PMID: 22510939]
(b)McArthur, G.A.; Demetri, G.D.; van Oosterom, A.; Heinrich, M.C.; Debiec-Rychter, M.; Corless, C.L.; Nikolova, Z.; Dimitrijevic, S.; Fletcher, J.A. Molecular and clinical analysis of locally advanced dermatofibrosarcoma protuberans treated with imatinib: Imatinib Target Exploration Consortium Study B2225. J. Clin. Oncol., 2005, 23(4), 866-873.
[http://dx.doi.org/10.1200/JCO.2005.07.088] [PMID: 15681532]
[17]
van der Graaf, W.T.; Blay, J.Y.; Chawla, S.P.; Kim, D.W.; Bui-Nguyen, B.; Casali, P.G.; Schöffski, P.; Aglietta, M.; Staddon, A.P.; Beppu, Y.; Le Cesne, A.; Gelderblom, H.; Judson, I.R.; Araki, N.; Ouali, M.; Marreaud, S.; Hodge, R.; Dewji, M.R.; Coens, C.; Demetri, G.D.; Fletcher, C.D.; Dei Tos, A.P.; Hohenberger, P.; Tissue, E.S.; Bone Sarcoma, G. EORTC Soft Tissue and Bone Sarcoma Group. PALETTE study group. Pazopanib for metastatic soft-tissue sarcoma (PALETTE): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet, 2012, 379(9829), 1879-1886.
[http://dx.doi.org/10.1016/S0140-6736(12)60651-5] [PMID: 22595799]
[18]
van der Graaf, W.T. Olaratumab in soft-tissue sarcomas. Lancet, 2016, 388(10043), 442-444.
[http://dx.doi.org/10.1016/S0140-6736(16)30788-7] [PMID: 27291995]
[19]
(a)Lim, J.; Poulin, N.M.; Nielsen, T.O. New strategies in sarcoma: linking genomic and immunotherapy approaches to molecular subtype. Clin. Cancer Res., 2015, 21(21), 4753-4759.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0831] [PMID: 26330427]
(b)Silveira, S.M.; Villacis, R.A.; Marchi, F.A. Barros Filho, Mde.C.; Drigo, S.A.; Neto, C.S.; Lopes, A.; da Cunha, I.W.; Rogatto, S.R. Genomic signatures predict poor outcome in undifferentiated pleomorphic sarcomas and leiomyosarcomas. PLoS One, 2013, 8(6), e67643.
[http://dx.doi.org/10.1371/journal.pone.0067643] [PMID: 23825657]
[20]
Riegman, P.H.; Dinjens, W.N.; Oosterhuis, J.W. Biobanking for interdisciplinary clinical research. Pathobiology, 2007, 74(4), 239-244.
[http://dx.doi.org/10.1159/000104451] [PMID: 17709966]
[21]
Riegman, P.H.; Morente, M.M.; Betsou, F.; de Blasio, P.; Geary, P. Marble Arch International Working Group on Biobanking for Biomedical Research. Biobanking for better healthcare. Mol. Oncol., 2008, 2(3), 213-222.
[http://dx.doi.org/10.1016/j.molonc.2008.07.004] [PMID: 19383342]
[22]
TCGA’s Study of Adult Soft Tissue Sarcoma. National Cancer Institute (NIH), https://www.cancer.gov/about-nci/organization/ccg/research/structural-genomics/tcga/studied-cancers/sarcoma [30 October 2019];
[23]
Barretina, J.; Caponigro, G.; Stransky, N.; Venkatesan, K.; Margolin, A.A.; Kim, S.; Wilson, C.J.; Lehár, J.; Kryukov, G.V.; Sonkin, D.; Reddy, A.; Liu, M.; Murray, L.; Berger, M.F.; Monahan, J.E.; Morais, P.; Meltzer, J.; Korejwa, A.; Jané-Valbuena, J.; Mapa, F.A.; Thibault, J.; Bric-Furlong, E.; Raman, P.; Shipway, A.; Engels, I.H.; Cheng, J.; Yu, G.K.; Yu, J.; Aspesi, P., Jr; de Silva, M.; Jagtap, K.; Jones, M.D.; Wang, L.; Hatton, C.; Palescandolo, E.; Gupta, S.; Mahan, S.; Sougnez, C.; Onofrio, R.C.; Liefeld, T.; MacConaill, L.; Winckler, W.; Reich, M.; Li, N.; Mesirov, J.P.; Gabriel, S.B.; Getz, G.; Ardlie, K.; Chan, V.; Myer, V.E.; Weber, B.L.; Porter, J.; Warmuth, M.; Finan, P.; Harris, J.L.; Meyerson, M.; Golub, T.R.; Morrissey, M.P.; Sellers, W.R.; Schlegel, R.; Garraway, L.A. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature, 2012, 483(7391), 603-607.
[http://dx.doi.org/10.1038/nature11003] [PMID: 22460905]
[24]
Bignell, G.R.; Greenman, C.D.; Davies, H.; Butler, A.P.; Edkins, S.; Andrews, J.M.; Buck, G.; Chen, L.; Beare, D.; Latimer, C.; Widaa, S.; Hinton, J.; Fahey, C.; Fu, B.; Swamy, S.; Dalgliesh, G.L.; Teh, B.T.; Deloukas, P.; Yang, F.; Campbell, P.J.; Futreal, P.A.; Stratton, M.R. Signatures of mutation and selection in the cancer genome. Nature, 2010, 463(7283), 893-898.
[http://dx.doi.org/10.1038/nature08768] [PMID: 20164919]
[25]
Yamada, K.M.; Cukierman, E. Modeling tissue morphogenesis and cancer in 3D. Cell, 2007, 130(4), 601-610.
[http://dx.doi.org/10.1016/j.cell.2007.08.006] [PMID: 17719539]
[26]
(a)Baker, B.M.; Chen, C.S. Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J. Cell Sci, 2012, 125(Pt 13), 3015-3024.
[http://dx.doi.org/10.1242/jcs.079509] [PMID: 22797912]
(b)Minchinton, A.I.; Tannock, I.F. Drug penetration in solid tumours. Nat. Rev. Cancer, 2006, 6(8), 583-592.
[http://dx.doi.org/10.1038/nrc1893] [PMID: 16862189]
[27]
Durand, R.E.; Raleigh, J.A. Identification of nonproliferating but viable hypoxic tumor cells in vivo. Cancer Res., 1998, 58(16), 3547-3550.
[PMID: 9721858]
[28]
Hirschhaeuser, F.; Menne, H.; Dittfeld, C.; West, J.; Mueller-Klieser, W.; Kunz-Schughart, L.A. Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol., 2010, 148(1), 3-15.
[http://dx.doi.org/10.1016/j.jbiotec.2010.01.012] [PMID: 20097238]
[29]
(a)Sutherland, R.M.; Durand, R.E. Radiation response of multicell spheroids-an in vitro tumour model. Curr. Top. Radiat. Res. Q., 1976, 11(1), 87-139.
[PMID: 128440]
(b)Sutherland, R.M.; Sordat, B.; Bamat, J.; Gabbert, H.; Bourrat, B.; Mueller-Klieser, W. Oxygenation and differentiation in multicellular spheroids of human colon carcinoma. Cancer Res., 1986, 46(10), 5320-5329.
[PMID: 3756881]
[30]
Teicher, B.A.; Polley, E.; Kunkel, M.; Evans, D.; Silvers, T.; Delosh, R.; Laudeman, J.; Ogle, C.; Reinhart, R.; Selby, M.; Connelly, J.; Harris, E.; Monks, A.; Morris, J. Sarcoma cell line screen of oncology drugs and investigational agents identifies patterns associated with gene and microRNA Expression. Mol. Cancer Ther., 2015, 14(11), 2452-2462.
[http://dx.doi.org/10.1158/1535-7163.MCT-15-0074] [PMID: 26351324]
[31]
Foty, R. A simple hanging drop cell culture protocol for generation of 3D spheroids. J. Vis. Exp., 2011, (51), e2720.
[http://dx.doi.org/10.3791/2720] [PMID: 21587162]
[32]
Vinci, M.; Gowan, S.; Boxall, F.; Patterson, L.; Zimmermann, M.; Court, W.; Lomas, C.; Mendiola, M.; Hardisson, D.; Eccles, S.A. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol., 2012, 10, 29.
[http://dx.doi.org/10.1186/1741-7007-10-29] [PMID: 22439642]
[33]
Kessel, S.; Cribbes, S.; Déry, O.; Kuksin, D.; Sincoff, E.; Qiu, J.; Chan, L.L. High-throughput 3D tumor spheroid screening method for cancer drug discovery using celigo image cytometry. SLAS Technol., 2017, 22(4), 454-465.
[http://dx.doi.org/10.1177/2211068216652846] [PMID: 27272155]
[34]
Shelper, T.B.; Lovitt, C.J.; Avery, V.M. Assessing drug efficacy in a miniaturized pancreatic cancer in vitro 3D cell culture model. Assay Drug Dev. Technol., 2016, 14(7), 367-380.
[http://dx.doi.org/10.1089/adt.2016.737] [PMID: 27552143]
[35]
Laporte, A.N.; Barrott, J.J.; Yao, R.J.; Poulin, N.M.; Brodin, B.A.; Jones, K.B.; Underhill, T.M.; Nielsen, T.O. HDAC and proteasome inhibitors synergize to activate pro-apoptotic factors in synovial sarcoma. PLoS One, 2017, 12(1), e0169407.
[http://dx.doi.org/10.1371/journal.pone.0169407] [PMID: 28056055]
[36]
Singh, S.K.; Clarke, I.D.; Terasaki, M.; Bonn, V.E.; Hawkins, C.; Squire, J.; Dirks, P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res., 2003, 63(18), 5821-5828.
[PMID: 14522905]
[37]
(a)Fujii, H.; Honoki, K.; Tsujiuchi, T.; Kido, A.; Yoshitani, K.; Takakura, Y. Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int. J. Oncol., 2009, 34(5), 1381-1386.
[PMID: 19360350]
(b)Gibbs, C.P.; Kukekov, V.G.; Reith, J.D.; Tchigrinova, O.; Suslov, O.N.; Scott, E.W.; Ghivizzani, S.C.; Ignatova, T.N.; Steindler, D.A. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia, 2005, 7(11), 967-976.
[http://dx.doi.org/10.1593/neo.05394] [PMID: 16331882]
[38]
Wahl, J.; Bogatyreva, L.; Boukamp, P.; Rojewski, M.; van Valen, F.; Fiedler, J.; Hipp, N.; Debatin, K.M.; Beltinger, C. Ewing’s sarcoma cells with CD57-associated increase of tumorigenicity and with neural crest-like differentiation capacity. Int. J. Cancer, 2010, 127(6), 1295-1307.
[http://dx.doi.org/10.1002/ijc.25163] [PMID: 20104521]
[39]
Liu, A.; Feng, B.; Gu, W.; Cheng, X.; Tong, T.; Zhang, H.; Hu, Y. The CD133+ subpopulation of the SW982 human synovial sarcoma cell line exhibits cancer stem-like characteristics. Int. J. Oncol., 2013, 42(4), 1399-1407.
[http://dx.doi.org/10.3892/ijo.2013.1826] [PMID: 23416969]
[40]
Salerno, M.; Avnet, S.; Bonuccelli, G.; Eramo, A.; De Maria, R.; Gambarotti, M.; Gamberi, G.; Baldini, N. Sphere-forming cell subsets with cancer stem cell properties in human musculoskeletal sarcomas. Int. J. Oncol., 2013, 43(1), 95-102.
[http://dx.doi.org/10.3892/ijo.2013.1927] [PMID: 23636271]
[41]
Aydemir, E.; Bayrak, O.F.; Sahin, F.; Atalay, B.; Kose, G.T.; Ozen, M.; Sevli, S.; Dalan, A.B.; Yalvac, M.E.; Dogruluk, T.; Türe, U. Characterization of cancer stem-like cells in chordoma. J. Neurosurg., 2012, 116(4), 810-820.
[http://dx.doi.org/10.3171/2011.12.JNS11430] [PMID: 22283189]
[42]
Bai, C.; Yang, M.; Fan, Z.; Li, S.; Gao, T.; Fang, Z. Associations of chemo- and radio-resistant phenotypes with the gap junction, adhesion and extracellular matrix in a three-dimensional culture model of soft sarcoma. J. Exp. Clin. Cancer Res., 2015, 34, 58.
[http://dx.doi.org/10.1186/s13046-015-0175-0] [PMID: 26055407]
[43]
Edmondson, R.; Broglie, J.J.; Adcock, A.F.; Yang, L. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev. Technol., 2014, 12(4), 207-218.
[http://dx.doi.org/10.1089/adt.2014.573] [PMID: 24831787]
[44]
Fong, E.L.; Lamhamedi-Cherradi, S.E.; Burdett, E.; Ramamoorthy, V.; Lazar, A.J.; Kasper, F.K.; Farach-Carson, M.C.; Vishwamitra, D.; Demicco, E.G.; Menegaz, B.A.; Amin, H.M.; Mikos, A.G.; Ludwig, J.A. Modeling Ewing sarcoma tumors in vitro with 3D scaffolds. Proc. Natl. Acad. Sci. USA, 2013, 110(16), 6500-6505.
[http://dx.doi.org/10.1073/pnas.1221403110] [PMID: 23576741]
[45]
Monderer, D.; Luseau, A.; Bellec, A.; David, E.; Ponsolle, S.; Saiagh, S.; Bercegeay, S.; Piloquet, P.; Denis, M.G.; Lodé, L.; Rédini, F.; Biger, M.; Heymann, D.; Heymann, M.F.; Le Bot, R.; Gouin, F.; Blanchard, F. New chondrosarcoma cell lines and mouse models to study the link between chondrogenesis and chemoresistance. Lab. Invest., 2013, 93(10), 1100-1114.
[http://dx.doi.org/10.1038/labinvest.2013.101] [PMID: 23958880]
[46]
Gemoll, T.; Epping, F.; Heinrich, L.; Fritzsche, B.; Roblick, U.J.; Szymczak, S.; Hartwig, S.; Depping, R.; Bruch, H.P.; Thorns, C.; Lehr, S.; Paech, A.; Habermann, J.K. Increased cathepsin D protein expression is a biomarker for osteosarcomas, pulmonary metastases and other bone malignancies. Oncotarget, 2015, 6(18), 16517-16526.
[http://dx.doi.org/10.18632/oncotarget.4140] [PMID: 26203049]
[47]
Roy, M.; Finley, S.D. Metabolic reprogramming dynamics in tumor spheroids: Insights from a multicellular, multiscale model. PLOS Comput. Biol., 2019, 15(6), e1007053.
[http://dx.doi.org/10.1371/journal.pcbi.1007053] [PMID: 31185009]
[48]
Jimenez Valencia, A.M.; Wu, P.H.; Yogurtcu, O.N.; Rao, P.; DiGiacomo, J.; Godet, I.; He, L.; Lee, M.H.; Gilkes, D.; Sun, S.X.; Wirtz, D. Collective cancer cell invasion induced by coordinated contractile stresses. Oncotarget, 2015, 6(41), 43438-43451.
[http://dx.doi.org/10.18632/oncotarget.5874] [PMID: 26528856]
[49]
Xu, X.; Farach-Carson, M.C.; Jia, X. Three-dimensional in vitro tumor models for cancer research and drug evaluation. Biotechnol. Adv., 2014, 32(7), 1256-1268.
[http://dx.doi.org/10.1016/j.biotechadv.2014.07.009] [PMID: 25116894]
[50]
Lamhamedi-Cherradi, S.E.; Santoro, M.; Ramammoorthy, V.; Menegaz, B.A.; Bartholomeusz, G.; Iles, L.R.; Amin, H.M.; Livingston, J.A.; Mikos, A.G.; Ludwig, J.A. 3D tissue-engineered model of Ewing’s sarcoma. Adv. Drug Deliv. Rev., 2014, 79-80, 155-171.
[http://dx.doi.org/10.1016/j.addr.2014.07.012] [PMID: 25109853]
[51]
Gershovich, J.G.; Dahlin, R.L.; Kasper, F.K.; Mikos, A.G. Enhanced osteogenesis in cocultures with human mesenchymal stem cells and endothelial cells on polymeric microfiber scaffolds. Tissue Eng. Part A, 2013, 19(23-24), 2565-2576.
[http://dx.doi.org/10.1089/ten.tea.2013.0256] [PMID: 23799306]
[52]
Hirt, C.; Papadimitropoulos, A.; Mele, V.; Muraro, M.G.; Mengus, C.; Iezzi, G.; Terracciano, L.; Martin, I.; Spagnoli, G.C. “In vitro” 3D models of tumor-immune system interaction. Adv. Drug Deliv. Rev., 2014, 79-80, 145-154.
[http://dx.doi.org/10.1016/j.addr.2014.05.003] [PMID: 24819215]
[53]
Sutherland, R.M.; McCredie, J.A.; Inch, W.R. Growth of multicell spheroids in tissue culture as a model of nodular carcinomas. J. Natl. Cancer Inst., 1971, 46(1), 113-120.
[PMID: 5101993]
[54]
Lancaster, M.A.; Knoblich, J.A. Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 2014, 345(6194), 1247125.
[http://dx.doi.org/10.1126/science.1247125] [PMID: 25035496]
[55]
Brodin, B.A.; Wennerberg, K.; Lidbrink, E.; Brosjö, O.; Potdar, S.; Wilson, J.N.; Ma, L.; Moens, L.N.; Hesla, A.; Porovic, E.; Bernhardsson, E.; Papakonstantinou, A.; Bauer, H.; Tsagkozis, P.; von Sivers, K.; Wejde, J.; Östling, P.; Kallioniemi, O.; Stragliotto, C.L. Drug sensitivity testing on patient-derived sarcoma cells predicts patient response to treatment and identifies c-Sarc inhibitors as active drugs for translocation sarcomas. Br. J. Cancer, 2019, 120(4), 435-443.
[http://dx.doi.org/10.1038/s41416-018-0359-4] [PMID: 30745580]

Rights & Permissions Print Cite
Article Metrics
65
7
World Chagas Disease
© 2024 Bentham Science Publishers | Privacy Policy