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3D models of the bone marrow in health and disease: yesterday, today, and tomorrow

Published online by Cambridge University Press:  25 September 2018

Annamarija Raic ,
Toufik Naolou ,
Anna Mohra ,
Chandralekha Chatterjee  and
Cornelia Lee-Thedieck
Annamarija Raic
Affiliation:
Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces, 76344 Eggenstein-Leopoldshafen, Germany
Toufik Naolou
Affiliation:
Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces, 76344 Eggenstein-Leopoldshafen, Germany
Anna Mohra
Affiliation:
Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces, 76344 Eggenstein-Leopoldshafen, Germany
Chandralekha Chatterjee
Affiliation:
Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces, 76344 Eggenstein-Leopoldshafen, Germany
Cornelia Lee-Thedieck*
Affiliation:
Karlsruhe Institute of Technology (KIT), Institute of Functional Interfaces, 76344 Eggenstein-Leopoldshafen, Germany
*
Address all correspondence to Cornelia Lee-Thedieck at [email protected]
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Abstract

The complex interaction between hematopoietic stem cells (HSCs) and their microenvironment in the human bone marrow ensures a life-long blood production by balancing stem cell maintenance and differentiation. This so-called HSC niche can be disturbed by malignant diseases. Investigating their consequences on hematopoiesis requires a deep understanding of how the niches function in health and disease. To facilitate this, biomimetic models of the bone marrow are needed to analyze HSC maintenance and hematopoiesis under steady state and diseased conditions. Here, 3D bone marrow models, their fabrication methods (including 3D bioprinting), and implementations recapturing bone marrow functions in health and diseases are presented.

Type
Prospective Articles
Information
MRS Communications , Volume 9 , Issue 1 , March 2019 , pp. 37 - 52
Copyright
Copyright © Materials Research Society 2018 

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References

1.Crane, G.M., Jeffery, E., and Morrison, S.J.: Adult haematopoietic stem cell niches. Nat. Rev. Immunol. 17, 573 (2017).10.1038/nri.2017.53Google Scholar
2.Yoshihara, H., Arai, F., Hosokawa, K., Hagiwara, T., Takubo, K., Nakamura, Y., Gomei, Y., Iwasaki, H., Matsuoka, S., Miyamoto, K., Miyazaki, H., Takahashi, T., and Suda, T.: Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1, 685 (2007).10.1016/j.stem.2007.10.020Google Scholar
3.Calvi, L.M., Adams, G.B., Weibrecht, K.W., Weber, J.M., Olson, D.P., Knight, M.C., Martin, R.P., Schipani, E., Divieti, P., Bringhurst, F.R., Milner, L.A., Kronenberg, H.M., and Scadden, D.T.: Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841 (2003).10.1038/nature02040Google Scholar
4.Kunisaki, Y., Bruns, I., Scheiermann, C., Ahmed, J., Pinho, S., Zhang, D., Mizoguchi, T., Wei, Q., Lucas, D., Ito, K., Mar, J.C., Bergman, A., and Frenette, P.S.: Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502, 637 (2013).10.1038/nature12612Google Scholar
5.Acar, M., Kocherlakota, K.S., Murphy, M.M., Peyer, J.G., Oguro, H., Inra, C.N., Jaiyeola, C., Zhao, Z., Luby-Phelps, K., and Morrison, S.J.: Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature 526, 126 (2015).10.1038/nature15250Google Scholar
6.Winkler, I.G., Barbier, V., Nowlan, B., Jacobsen, R.N., Forristal, C.E., Patton, J.T., Magnani, J.L., and Levesque, J.P.: Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat. Med. 18, 1651 (2012).10.1038/nm.2969Google Scholar
7.Kiel, M.J., Yilmaz, O.H., Iwashita, T., Yilmaz, O.H., Terhorst, C., and Morrison, S.J.: SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109 (2005).10.1016/j.cell.2005.05.026Google Scholar
8.Fujisaki, J., Wu, J., Carlson, A.L., Silberstein, L., Putheti, P., Larocca, R., Gao, W., Saito, T.I., Lo Celso, C., Tsuyuzaki, H., Sato, T., Cote, D., Sykes, M., Strom, T.B., Scadden, D.T., and Lin, C.P.: In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474, 216 (2011).10.1038/nature10160Google Scholar
9.Chow, A., Lucas, D., Hidalgo, A., Mendez-Ferrer, S., Hashimoto, D., Scheiermann, C., Battista, M., Leboeuf, M., Prophete, C., van Rooijen, N., Tanaka, M., Merad, M., and Frenette, P.S.: Bone marrow CD169 + macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med. 208, 261 (2011).10.1084/jem.20101688Google Scholar
10.Arai, F., Hosokawa, K., Toyama, H., Matsumoto, Y., and Suda, T.: Role of N-cadherin in the regulation of hematopoietic stem cells in the bone marrow niche. Ann. N. Y. Acad. Sci. 1266, 72 (2012).10.1111/j.1749-6632.2012.06576.xGoogle Scholar
11.Schroeder, M.A. and DiPersio, J.F.: Mobilization of hematopoietic stem and leukemia cells. J. Leukocyte Biol. 91, 47 (2012).10.1189/jlb.0210085Google Scholar
12.Klein, G.: The extracellular matrix of the hematopoietic microenvironment. Experientia 51, 914 (1995).10.1007/BF01921741Google Scholar
13.Nilsson, S.K., Debatis, M.E., Dooner, M.S., Madri, J.A., Quesenberry, P.J., and Becker, P.S.: Immunofluorescence characterization of key extracellular matrix proteins in murine bone marrow in situ. J. Histochem. Cytochem. 46, 371 (1998).10.1177/002215549804600311Google Scholar
14.Rodgers, K.D., San Antonio, J.D., and Jacenko, O.: Heparan sulfate proteoglycans: a GAGgle of skeletal-hematopoietic regulators. Dev. Dyn. 237, 2622 (2008).10.1002/dvdy.21593Google Scholar
15.Goncharova, V., Serobyan, N., Iizuka, S., Schraufstatter, I., de Ridder, A., Povaliy, T., Wacker, V., Itano, N., Kimata, K., Orlovskaja, I.A., Yamaguchi, Y., and Khaldoyanidi, S.: Hyaluronan expressed by the hematopoietic microenvironment is required for bone marrow hematopoiesis. J. Biol. Chem. 287, 25419 (2012).10.1074/jbc.M112.376699Google Scholar
16.Coulombel, L., Auffray, I., Gaugler, M.H., and Rosemblatt, M.: Expression and function of integrins on hematopoietic progenitor cells. Acta Haematol. 97, 13 (1997).10.1159/000203655Google Scholar
17.Lee-Thedieck, C. and Spatz, J.P.: Biophysical regulation of hematopoietic stem cells. Biomater. Sci. 2, 1548 (2014).10.1039/C4BM00128AGoogle Scholar
18.Nelson, M.R. and Roy, K.: Bone-marrow mimicking biomaterial niches for studying hematopoietic stem and progenitor cells. J. Mater. Chem. B 4, 3490 (2016).10.1039/C5TB02644JGoogle Scholar
19.Walasek, M.A., van Os, R., and de Haan, G.: Hematopoietic stem cell expansion: challenges and opportunities. Ann. N. Y. Acad. Sci. 1266, 138 (2012).10.1111/j.1749-6632.2012.06549.xGoogle Scholar
20.Dombret, H. and Gardin, C.: An update of current treatments for adult acute myeloid leukemia. Blood 127, 53 (2016).10.1182/blood-2015-08-604520Google Scholar
21.Nombela-Arrieta, C. and Isringhausen, S.: The role of the bone marrow stromal compartment in the hematopoietic response to microbial infections. Front. Immunol. 7, 689 (2016).Google Scholar
22.Knight, A.: Animal experiments scrutinised: systematic reviews demonstrate poor human clinical and toxicological utility. Altex 24, 320 (2007).10.14573/altex.2007.4.320Google Scholar
23.Törnqvist, E., Annas, A., Granath, B., Jalkesten, E., Cotgreave, I., and Öberg, M.: Strategic focus on 3R principles reveals major reductions in the use of animals in pharmaceutical toxicity testing. PLoS ONE 9, e101638 (2014).10.1371/journal.pone.0101638Google Scholar
24.Choi, J.S., Mahadik, B.P., and Harley, B.A.C.: Engineering the hematopoietic stem cell niche: frontiers in biomaterial science. Biotechnol. J. 10, 1529 (2015).10.1002/biot.201400758Google Scholar
25.Mendez-Ferrer, S., Michurina, T.V., Ferraro, F., Mazloom, A.R., Macarthur, B.D., Lira, S.A., Scadden, D.T., Ma'ayan, A., Enikolopov, G.N., and Frenette, P.S.: Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466, 829 (2010).10.1038/nature09262Google Scholar
26.Kiernan, J., Damien, P., Monaghan, M., Shorr, R., McIntyre, L., Fergusson, D., Tinmouth, A., and Allan, D.: Clinical studies of ex vivo expansion to accelerate engraftment after umbilical cord blood transplantation: a systematic review. Transfus. Med. Rev. 31, 173 (2017).10.1016/j.tmrv.2016.12.004Google Scholar
27.Pineault, N. and Abu-Khader, A.: Advances in umbilical cord blood stem cell expansion and clinical translation. Exp. Hematol. 43, 498 (2015).Google Scholar
28.Brandrup, J., Immergut, E.H., and Grulke, E.A.: Polymer Handbook, 4th ed. John Wiley and Sons: New York, 1999).Google Scholar
29.Muth, C.A., Steinl, C., Klein, G., and Lee-Thedieck, C.: Regulation of hematopoietic stem cell behavior by the nanostructured presentation of extracellular matrix components. PLoS ONE 8, e54778 (2013).10.1371/journal.pone.0054778Google Scholar
30.Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E.: Matrix elasticity directs stem cell lineage specification. Cell 126, 677 (2006).10.1016/j.cell.2006.06.044Google Scholar
31.Lee-Thedieck, C. and Spatz, J.P.: Artificial niches: biomimetic materials for hematopoietic stem cell culture. Macromol. Rapid Commun. 33, 1432 (2012).Google Scholar
32.Kumar, S.S., Hsiao, J.H., Ling, Q.D., Dulinska-Molak, I., Chen, G., Chang, Y., Chang, Y., Chen, Y.H., Chen, D.C., Hsu, S.T., and Higuchi, A.: The combined influence of substrate elasticity and surface-grafted molecules on the ex vivo expansion of hematopoietic stem and progenitor cells. Biomaterials 34, 7632 (2013).Google Scholar
33.Zhang, C.C. and Lodish, H.F.: Murine hematopoietic stem cells change their surface phenotype during ex vivo expansion. Blood 105, 4314 (2005).Google Scholar
34.Zhou, Y., Chen, H., Li, H., and Wu, Y.: 3D culture increases pluripotent gene expression in mesenchymal stem cells through relaxation of cytoskeleton tension. J. Cell. Mol. Med. 21, 1073 (2017).10.1111/jcmm.12946Google Scholar
35.Rodling, L., Schwedhelm, I., Kraus, S., Bieback, K., Hansmann, J., and Lee-Thedieck, C.: 3D models of the hematopoietic stem cell niche under steady-state and active conditions. Sci. Rep. 7, 4625 (2017).Google Scholar
36.Cook, M.M., Futrega, K., Osiecki, M., Kabiri, M., Rice, A., Atkinson, K., Brooke, G., and Doran, M.: Micromarrows—three-dimensional coculture of hematopoietic stem cells and mesenchymal stromal cells. Tissue Eng. Part C 18, 319 (2012).10.1089/ten.tec.2011.0159Google Scholar
37.Costa, E.C., de Melo-Diogo, D., Moreira, A.F., Carvalho, M.P., and Correia, I.J.: Spheroids formation on non-adhesive surfaces by liquid overlay technique: considerations and practical approaches. Biotechnol. J. 13, 1–12 (2018).10.1002/biot.201700417Google Scholar
38.Salamanna, F., Contartese, D., Maglio, M., and Fini, M.: A systematic review on in vitro 3D bone metastases models: a new horizon to recapitulate the native clinical scenario? Oncotarget 7, 44803–44820 (2016).10.18632/oncotarget.8394Google Scholar
39.Sitarski, A.M., Fairfield, H., Falank, C., and Reagan, M.R.: 3d tissue engineered in vitro models of cancer in bone. ACS. Biomater. Sci. Eng. 4, 324 (2018).10.1021/acsbiomaterials.7b00097Google Scholar
40.Necas, J., Bartosikova, L., Brauner, P., and Kolar, J.: Hyaluronic acid (hyaluronan): a review. Vet. Med. 53, 397 (2008).10.17221/1930-VETMEDGoogle Scholar
41.Fairbanks, B.D., Singh, S.P., Bowman, C.N., and Anseth, K.S.: Photodegradable, photoadaptable hydrogels via radical-mediated disulfide fragmentation reaction. Macromolecules 44, 2444 (2011).10.1021/ma200202wGoogle Scholar
42.Zhang, J., Skardal, A., and Prestwich, G.D.: Engineered extracellular matrices with cleavable crosslinkers for cell expansion and easy cell recovery. Biomaterials 29, 4521 (2008).10.1016/j.biomaterials.2008.08.008Google Scholar
43.Kharkar, P.M., Kiick, K.L., and Kloxin, A.M.: Designing degradable hydrogels for orthogonal control of cell microenvironments. Chem. Soc. Rev. 42, 7335 (2013).10.1039/C3CS60040HGoogle Scholar
44.Cheng, F.R., Su, T., Cao, J., Luo, X.L., Li, L., Pu, Y., and He, B.: Environment-stimulated nanocarriers enabling multi-active sites for high drug encapsulation as an “on demand” drug release system. J. Mater. Chem. B 6, 2258 (2018).10.1039/C8TB00132DGoogle Scholar
45.Madl, C.M., LeSavage, B.L., Dewi, R.E., Dinh, C.B., Stowers, R.S., Khariton, M., Lampe, K.J., Nguyen, D., Chaudhuri, O., Enejder, A., and Heilshorn, S.C.: Maintenance of neural progenitor cell stemness in 3D hydrogels requires matrix remodelling. Nat. Mater. 16, 1233 (2017).10.1038/nmat5020Google Scholar
46.Henderson, T.M.A., Ladewig, K., Haylock, D.N., McLean, K.M., and O'Connor, A.J.: Cryogels for biomedical applications. J. Mater. Chem. B 1, 2682 (2013).10.1039/c3tb20280aGoogle Scholar
47.Raic, A., Rodling, L., Kalbacher, H., and Lee-Thedieck, C.: Biomimetic macroporous PEG hydrogels as 3D scaffolds for the multiplication of human hematopoietic stem and progenitor cells. Biomaterials 35, 929 (2014).10.1016/j.biomaterials.2013.10.038Google Scholar
48.Ferreira, M.S., Jahnen-Dechent, W., Labude, N., Bovi, M., Hieronymus, T., Zenke, M., Schneider, R.K., and Neuss, S.: Cord blood-hematopoietic stem cell expansion in 3D fibrin scaffolds with stromal support. Biomaterials 33, 6987 (2012).10.1016/j.biomaterials.2012.06.029Google Scholar
49.Kotha, S.S., Hayes, B.J., Phong, K.T., Redd, M.A., Bomsztyk, K., Ramakrishnan, A., Torok-Storb, B., and Zheng, Y.: Engineering a multicellular vascular niche to model hematopoietic cell trafficking. Stem Cell. Res. Ther. 9, 77 (2018).Google Scholar
50.Sieh, S., Lubik, A.A., Clements, J.A., Nelson, C.C., and Hutmacher, D.W.: Interactions between human osteoblasts and prostate cancer cells in a novel 3D in vitro model. Organogenesis 6, 181 (2010).10.4161/org.6.3.12041Google Scholar
51.Bello, A.B., Park, H., and Lee, S.H.: Current approaches in biomaterial-based hematopoietic stem cell niches. Acta Biomater. 72, 1 (2018).10.1016/j.actbio.2018.03.028Google Scholar
52.Torisawa, Y.S., Spina, C.S., Mammoto, T., Mammoto, A., Weaver, J.C., Tat, T., Collins, J.J., and Ingber, D.E.: Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat. Methods 11, 663 (2014).10.1038/nmeth.2938Google Scholar
53.Reinisch, A., Hernandez, D.C., Schallmoser, K., and Majeti, R.: Generation and use of a humanized bone-marrow-ossicle niche for hematopoietic xenotransplantation into mice. Nat. Protoc. 12, 2169 (2017).10.1038/nprot.2017.088Google Scholar
54.Riether, C., Schurch, C.M., and Ochsenbein, A.F.: Regulation of hematopoietic and leukemic stem cells by the immune system. Cell Death Differ. 22, 187 (2015).10.1038/cdd.2014.89Google Scholar
55.Stieglitz, E. and Loh, M.L.: Genetic predispositions to childhood leukemia. Ther. Adv. Hematol. 4, 270 (2013).10.1177/2040620713498161Google Scholar
56.Lapidot, T., Sirard, C., Vormoor, J., Murdoch, B., Hoang, T., Caceres-Cortes, J., Minden, M., Paterson, B., Caligiuri, M.A., and Dick, J.E.: A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645 (1994).10.1038/367645a0Google Scholar
57.Brenner, A.K., Nepstad, I., and Bruserud, Ø.: Mesenchymal stem cells support survival and proliferation of primary human acute myeloid leukemia cells through heterogeneous molecular mechanisms. Front. Immunol. 8, 106 (2017).10.3389/fimmu.2017.00106Google Scholar
58.Schepers, K., Pietras, E.M., Reynaud, D., Flach, J., Binnewies, M., Garg, T., Wagers, A.J., Hsiao, E.C., and Passegue, E.: Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 13, 285 (2013).10.1016/j.stem.2013.06.009Google Scholar
59.Jacamo, R., Chen, Y., Wang, Z., Ma, W., Zhang, M., Spaeth, E.L., Wang, Y., Battula, V.L., Mak, P.Y., Schallmoser, K., Ruvolo, P., Schober, W.D., Shpall, E.J., Nguyen, M.H., Strunk, D., Bueso-Ramos, C.E., Konoplev, S., Davis, R.E., Konopleva, M., and Andreeff, M.: Reciprocal leukemia-stroma VCAM-1/VLA-4-dependent activation of NF-kappaB mediates chemoresistance. Blood 123, 2691 (2014).10.1182/blood-2013-06-511527Google Scholar
60.Saito, Y., Uchida, N., Tanaka, S., Suzuki, N., Tomizawa-Murasawa, M., Sone, A., Najima, Y., Takagi, S., Aoki, Y., Wake, A., Taniguchi, S., Shultz, L.D., and Ishikawa, F.: Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat. Biotechnol. 28, 275 (2010).10.1038/nbt.1607Google Scholar
61.Cook, G.J., and Pardee, T.S.: Animal models of leukemia: any closer to the real thing? Cancer Metastasis Rev. 32, 63 (2013).10.1007/s10555-012-9405-5Google Scholar
62.de Jong, M., and Maina, T.: Of mice and humans: are they the same?–Implications in cancer translational research. J. Nucl. Med. 51, 501 (2010).10.2967/jnumed.109.065706Google Scholar
63.Demetrius, L.: Of mice and men. EMBO Rep. 6, S39 (2005).Google Scholar
64.Ishikawa, F., Yoshida, S., Saito, Y., Hijikata, A., Kitamura, H., Tanaka, S., Nakamura, R., Tanaka, T., Tomiyama, H., Saito, N., Fukata, M., Miyamoto, T., Lyons, B., Ohshima, K., Uchida, N., Taniguchi, S., Ohara, O., Akashi, K., Harada, M., and Shultz, L.D.: Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat. Biotechnol. 25, 1315 (2007).10.1038/nbt1350Google Scholar
65.Cogle, C.R., Goldman, D.C., Madlambayan, G.J., Leon, R.P., Masri, A.A., Clark, H.A., Asbaghi, S.A., Tyner, J.W., Dunlap, J., Fan, G., Kovacsovics, T., Liu, Q., Meacham, A., Hamlin, K.L., Hromas, R.A., Scott, E.W., and Fleming, W.H.: Functional Integration of Acute Myeloid Leukemia into the Vascular Niche. Leukemia 28, 1978 (2014).10.1038/leu.2014.109Google Scholar
66.Bray, L.J., Binner, M., Korner, Y., von Bonin, M., Bornhauser, M., and Werner, C.: A three-dimensional ex vivo tri-culture model mimics cell-cell interactions between acute myeloid leukemia and the vascular niche. Haematologica 102, 1215 (2017).Google Scholar
67.Bruce, A., Evans, R., Mezan, R., Shi, L., Moses, B.S., Martin, K.H., Gibson, L.F., and Yang, Y.: Three-dimensional microfluidic tri-culture model of the bone marrow microenvironment for study of acute lymphoblastic leukemia. PLoS ONE 10, e0140506 (2015).10.1371/journal.pone.0140506Google Scholar
68.Trimarco, V., Ave, E., Facco, M., Chiodin, G., Frezzato, F., Martini, V., Gattazzo, C., Lessi, F., Giorgi, C.A., Visentin, A., Castelli, M., Severin, F., Zambello, R., Piazza, F., Semenzato, G., and Trentin, L.: Cross-talk between chronic lymphocytic leukemia (CLL) tumor B cells and mesenchymal stromal cells (MSCs): implications for neoplastic cell survival. Oncotarget 6, 42130 (2015).10.18632/oncotarget.6239Google Scholar
69.Tavor, S., Petit, I., Porozov, S., Avigdor, A., Dar, A., Leider-Trejo, L., Shemtov, N., Deutsch, V., Naparstek, E., Nagler, A., and Lapidot, T.: CXCR4 regulates migration and development of human acute myelogenous leukemia stem cells in transplanted NOD/SCID mice. Cancer Res. 64, 2817 (2004).10.1158/0008-5472.CAN-03-3693Google Scholar
70.Mills, S.C., Goh, P.H., Kudatsih, J., Ncube, S., Gurung, R., Maxwell, W., and Mueller, A.: Cell migration towards CXCL12 in leukemic cells compared to breast cancer cells. Cell. Signal. 28, 316 (2016).10.1016/j.cellsig.2016.01.006Google Scholar
71.Cho, B.-S., Kim, H.-J., and Konopleva, M.: Targeting the CXCL12/CXCR4 axis in acute myeloid leukemia: from bench to bedside. Korean J. Intern. Med. 32, 248 (2017).10.3904/kjim.2016.244Google Scholar
72.Liou, A., Delgado-Martin, C., Teachey, D.T., and Hermiston, M.L.: The CXCR4/CXCL12 axis mediates chemotaxis, survival, and chemoresistance in t-cell acute lymphoblastic leukemia. Blood 124, 3629 (2014).10.1182/blood.V124.21.3629.3629Google Scholar
73.Weisberg, E., Azab, A.K., Manley, P.W., Kung, A.L., Christie, A.L., Bronson, R., Ghobrial, I.M., and Griffin, J.D.: Inhibition of CXCR4 in CML cells disrupts their interaction with the bone marrow microenvironment and sensitizes them to nilotinib: potentiation of nilotinib by CXCR4 antagonist. Leukemia 26, 985 (2012).Google Scholar
74.Weisberg, E.L., Sattler, M., Azab, A.K., Eulberg, D., Kruschinski, A., Manley, P.W., Stone, R., and Griffin, J.D.: Inhibition of SDF-1-induced migration of oncogene-driven myeloid leukemia by the L-RNA aptamer (Spiegelmer), NOX-A12, and potentiation of tyrosine kinase inhibition. Oncotarget 8, 109973 (2017).Google Scholar
75.Shen, Z.H., Zeng, D.F., Wang, X.Y., Ma, Y.Y., Zhang, X., and Kong, P.Y.: Targeting of the leukemia microenvironment by c(RGDfV) overcomes the resistance to chemotherapy in acute myeloid leukemia in biomimetic polystyrene scaffolds. Oncol. Lett. 12, 3278 (2016).10.3892/ol.2016.5042Google Scholar
76.Blanco, T.M., Mantalaris, A., Bismarck, A., and Panoskaltsis, N.: The development of a three-dimensional scaffold for ex vivo biomimicry of human acute myeloid leukaemia. Biomaterials 31, 2243 (2010).10.1016/j.biomaterials.2009.11.094Google Scholar
77.Favreau, A.J., Vary, C.P.H., Brooks, P.C., and Sathyanarayana, P.: Cryptic collagen IV promotes cell migration and adhesion in myeloid leukemia. Cancer Med. 3, 265 (2014).10.1002/cam4.203Google Scholar
78.Shin, J.W. and Mooney, D.J.: Extracellular matrix stiffness causes systematic variations in proliferation and chemosensitivity in myeloid leukemias. Proc. Natl. Acad. Sci. USA 113, 12126 (2016).Google Scholar
79.Vu, T.T., Lim, C., and Lim, M.: Characterization of leukemic cell behaviors in a soft marrow mimetic alginate hydrogel. J. Biomed. Mater. Res. B Appl. Biomater. 100, 1980 (2012).Google Scholar
80.Gupta, G.P. and Massagué, J.: Cancer metastasis: building a framework. Cell 127, 679 (2006).Google Scholar
81.Fidler, I.J.: The pathogenesis of cancer metastasis: the “seed and soil” hypothesis revisited. Nat. Rev. Cancer 3, 453 (2003).10.1038/nrc1098Google Scholar
82.Macedo, F., Ladeira, K., Pinho, F., Saraiva, N., Bonito, N., Pinto, L., and Goncalves, F.: Bone metastases: an overview. Oncol. Rev. 11, 321 (2017).Google Scholar
83.Massagué, J. and Obenauf, A.C.: Metastatic colonization by circulating tumour cells. Nature 529, 298 (2016).10.1038/nature17038Google Scholar
84.Peitzsch, C., Tyutyunnykova, A., Pantel, K., and Dubrovska, A.: Cancer stem cells: the root of tumor recurrence and metastases, Semin. Cancer Biol. 44, 10 (2017).10.1016/j.semcancer.2017.02.011Google Scholar
85.Obenauf, A.C. and Massagué, J.: Surviving at a distance: organ-specific metastasis. Trends. Cancer. 1, 76 (2015).10.1016/j.trecan.2015.07.009Google Scholar
86.Chambers, A., Groom, A., and MacDonald, I.: Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563ā (2002).Google Scholar
87.Roodman, G.D. and Silbermann, R.: Mechanisms of osteolytic and osteoblastic skeletal lesions. Bonekey. Rep. 4, 1 (2015).Google Scholar
88.Sitarski, A.M., Fairfield, H., Falank, C., and Reagan, M.R.: 3D tissue engineered in vitro models of cancer in bone. ACS BACS Biomater Sci. Eng. 4, 324 (2017).10.1021/acsbiomaterials.7b00097Google Scholar
89.Butcher, D.T., Alliston, T., and Weaver, V.M.: A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108 (2009).Google Scholar
90.Kang, Y., Siegel, P.M., Shu, W., Drobnjak, M., Kakonen, S.M., Cordón-Cardo, C., Guise, T.A., and Massagué, J.: A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537 (2003).Google Scholar
91.Shiozawa, Y., Pedersen, E.A., Havens, A.M., Jung, Y., Mishra, A., Joseph, J., Kim, J.K., Patel, L.R., Ying, C., Ziegler, A.M., Pienta, M.J., Song, J., Wang, J., Loberg, R.D., Krebsbach, P.H., Pienta, K.J., and Taichman, R.S.: Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J. Clin. Invest. 121, 1298 (2011).Google Scholar
92.Insua-Rodríguez, J., and Oskarsson, T.: The extracellular matrix in breast cancer. Adv. Drug Del. Rev. 97, 41 (2016).10.1016/j.addr.2015.12.017Google Scholar
93.Nath, S. and Devi, G.R.: Three-dimensional culture systems in cancer research: focus on tumor spheroid model. Pharmacol. Ther. 163, 94 (2016).10.1016/j.pharmthera.2016.03.013Google Scholar
94.Xu, X., Farach-Carson, M.C., and Jia, X.: Three-dimensional in vitro tumor models for cancer research and drug evaluation. Biotechnol. Adv. 32, 1256 (2014).10.1016/j.biotechadv.2014.07.009Google Scholar
95.Pan, T., Fong, E.L., Martinez, M., Harrington, D.A., Lin, S.-H., Farach-Carson, M.C., and Satcher, R.L.: Three-dimensional (3D) culture of bone-derived human 786-O renal cell carcinoma retains relevant clinical characteristics of bone metastases. Cancer Lett. 365, 89 (2015).10.1016/j.canlet.2015.05.019Google Scholar
96.Kwon, H., Kim, H.J., Rice, W.L., Subramanian, B., Park, S.H., Georgakoudi, I., and Kaplan, D.L.: Development of an in vitro model to study the impact of BMP-2 on metastasis to bone. J. Tissue Eng. Regen. Med. 4, 590 (2010).Google Scholar
97.Cox, R.F., Jenkinson, A., Pohl, K., O'Brien, F.J., and Morgan, M.P.: Osteomimicry of mammary adenocarcinoma cells in vitro; increased expression of bone matrix proteins and proliferation within a 3D collagen environment. PLoS ONE 7, e41679 (2012).10.1371/journal.pone.0041679Google Scholar
98.Fitzgerald, K.A., Guo, J., Raftery, R.M., Castaño, I.M., Curtin, C.M., Gooding, M., Darcy, R., O'Brien, F.J., and O'Driscoll, C.M.: Nanoparticle-mediated siRNA delivery assessed in a 3D co-culture model simulating prostate cancer bone metastasis. Int. J. Pharm. 511, 1058 (2016).10.1016/j.ijpharm.2016.07.079Google Scholar
99.Marlow, R. and Dontu, G.: Modeling the breast cancer bone metastatic niche in complex three-dimensional cocultures. In Mammary Stem Cells, del Mar Vivanco, Maria, ed., Humana Press: New York, 2015; p. 213.10.1007/978-1-4939-2519-3_12Google Scholar
100.Dhurjati, R., Krishnan, V., Shuman, L.A., Mastro, A.M., and Vogler, E.A.: Metastatic breast cancer cells colonize and degrade three-dimensional osteoblastic tissue in vitro. Clin. Exp. Metastasis 25, 741 (2008).Google Scholar
101.Krishnan, V., Vogler, E.A., Sosnoski, D.M., and Mastro, A.M.: In vitro mimics of bone remodeling and the vicious cycle of cancer in bone. J. Cell. Physiol. 229, 453 (2014).10.1002/jcp.24464Google Scholar
102.Bersini, S., Jeon, J.S., Dubini, G., Arrigoni, C., Chung, S., Charest, J.L., Moretti, M., and Kamm, R.D.: A microfluidic 3D in vitro model for specificity of breast cancer metastasis to bone. Biomaterials 35, 2454 (2014).Google Scholar
103.Campbell, T., Williams, C., Ivanova, O., and Garrett, B.: Could 3D printing change the world. Technologies, Potential, and Implications of Additive Manufacturing, Atlantic Council, Washington, DC (2011).Google Scholar
104.Patra, S. and Young, V.: A review of 3D printing techniques and the future in biofabrication of bioprinted tissue. Cell Biochem. Biophys. 74, 93 (2016).10.1007/s12013-016-0730-0Google Scholar
105.Arrigoni, C., Gilardi, M., Bersini, S., Candrian, C., and Moretti, M.: Bioprinting and organ-on-chip applications towards personalized medicine for bone diseases. Stem Cell Rev. 13, 407 (2017).Google Scholar
106.Temple, J.P., Hutton, D.L., Hung, B.P., Huri, P.Y., Cook, C.A., Kondragunta, R., Jia, X., and Grayson, W.L.: Engineering anatomically shaped vascularized bone grafts with hASCs and 3D-printed PCL scaffolds. J. Biomed. Mater. Res. A 102, 4317 (2014).Google Scholar
107.Chia, H.N. and Wu, B.M.: Recent advances in 3D printing of biomaterials. J. Biol. Eng. 9, 4 (2015).10.1186/s13036-015-0001-4Google Scholar
108.Groll, J., Boland, T., Blunk, T., Burdick, J.A., Cho, D.-W., Dalton, P.D., Derby, B., Forgacs, G., Li, Q., and Mironov, V.A.: Biofabrication: reappraising the definition of an evolving field. Biofabrication. 8, 013001 (2016).10.1088/1758-5090/8/1/013001Google Scholar
109.Gao, G., Schilling, A.F., Yonezawa, T., Wang, J., Dai, G., and Cui, X.: Bioactive nanoparticles stimulate bone tissue formation in bioprinted three-dimensional scaffold and human mesenchymal stem cells. Biotechnol. J. 9, 1304 (2014).10.1002/biot.201400305Google Scholar
110.Catros, S., Fricain, J.-C., Guillotin, B., Pippenger, B., Bareille, R., Remy, M., Lebraud, E., Desbat, B., Amédée, J., and Guillemot, F.: Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication. 3, 025001 (2011).Google Scholar
111.Chang, C.-H., Lin, C.-Y., Liu, F.-H., Chen, M.H.-C., Lin, C.-P., Ho, H.-N., and Liao, Y.-S.: 3D printing bioceramic porous scaffolds with good mechanical property and cell affinity. PLoS ONE 10, e0143713 (2015).Google Scholar
112.Wüst, S., Godla, M.E., Müller, R., and Hofmann, S.: Tunable hydrogel composite with two-step processing in combination with innovative hardware upgrade for cell-based three-dimensional bioprinting. Acta Biomater. 10, 630 (2014).Google Scholar
113.Hwang, K.-S., Choi, J.-W., Kim, J.-H., Chung, H.Y., Jin, S., Shim, J.-H., Yun, W.-S., Jeong, C.-M., and Huh, J.-B.: Comparative efficacies of collagen-based 3D printed PCL/PLGA/β-TCP composite block bone grafts and biphasic calcium phosphate bone substitute for bone regeneration. Materials (Basel) 10, 421 (2017).10.3390/ma10040421Google Scholar
114.Alluri, R., Jakus, A., Bougioukli, S., Pannell, W., Sugiyama, O., Tang, A., Shah, R., and Lieberman, J.R.: 3D printed hyperelastic “bone” scaffolds and regional gene therapy: a novel approach to bone healing. J. Biomed. Mater. Res. A 106, 1104 (2018).10.1002/jbm.a.36310Google Scholar
115.Zhang, W., Lian, Q., Li, D., Wang, K., Hao, D., Bian, W., He, J., and Jin, Z.: Cartilage repair and subchondral bone migration using 3D printing osteochondral composites: a one-year-period study in rabbit trochlea. BioMed Res. Int. 2014, 1 (2014).Google Scholar
116.Zhu, W., Xu, C., Ma, B.-P., Zheng, Z.-B., Li, Y.-L., Ma, Q., Wu, G.-L., and Weng, X.-S.: Three-dimensional printed scaffolds with gelatin and platelets enhance in vitro preosteoblast growth behavior and the sustained-release effect of growth factors. Chin. Med. J. 129, 2576 (2016).10.4103/0366-6999.192770Google Scholar
117.Murphy, S.V. and Atala, A.: 3D bioprinting of tissues and organs. Nat. Biotechnol. 32, 773 (2014).10.1038/nbt.2958Google Scholar
118.Adepu, S., Dhiman, N., Laha, A., Sharma, C.S., Ramakrishna, S., and Khandelwal, M.: Three-dimensional bioprinting for bone tissue regeneration. Curr. Opin. Biomed. Eng. 2, 22 (2017).Google Scholar
119.Peng, W., Unutmaz, D., and Ozbolat, I.T.: Bioprinting towards physiologically relevant tissue models for pharmaceutics. Trends Biotechnol. 34, 722 (2016).10.1016/j.tibtech.2016.05.013Google Scholar
120.Gungor-Ozkerim, P.S., Inci, I., Zhang, Y.S., Khademhosseini, A., and Dokmeci, M.R.: Bioinks for 3D bioprinting: an overview. Biomater. Sci 6, 915 (2018).10.1039/C7BM00765EGoogle Scholar
121.Cui, H., Zhu, W., Nowicki, M., Zhou, X., Khademhosseini, A., and Zhang, L.G.: Hierarchical fabrication of engineered vascularized bone biphasic constructs via dual 3D bioprinting: integrating regional bioactive factors into architectural design. Adv. Healthc. Mater. 5, 2174 (2016).Google Scholar
122.Hospodiuk, M., Dey, M., Sosnoski, D., and Ozbolat, I.T.: The bioink: a comprehensive review on bioprintable materials. Biotechnol. Adv. 35, 217 (2017).10.1016/j.biotechadv.2016.12.006Google Scholar
123.Jungst, T., Smolan, W., Schacht, K., Scheibel, T., and Groll, J.: Strategies and molecular design criteria for 3D printable hydrogels. Chem. Rev. 116, 1496 (2016).10.1021/acs.chemrev.5b00303Google Scholar
124.Kang, H.W., Lee, S.J., Ko, I.K., Kengla, C., Yoo, J.J., and Atala, A.: A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat. Biotechnol. 34, 312 (2016).10.1038/nbt.3413Google Scholar
125.Liu, W., Zhang, Y.S., Heinrich, M.A., De Ferrari, F., Jang, H.L., Bakht, S.M., Alvarez, M.M., Yang, J., Li, Y.-C., Trujillo-de Santiago, G., Miri, A.K., Zhu, K., Khoshakhlagh, P., Prakash, G., Cheng, H., Guan, X., Zhong, Z., Ju, J., Zhu, G.H., Jin, X., Shin, S.R., Dokmeci, M.R., and Khademhosseini, A.: Rapid continuous multimaterial extrusion bioprinting. Adv. Mater. 29, 1604630 (2017).10.1002/adma.201604630Google Scholar
126.Zhou, X., Castro, N.J., Zhu, W., Cui, H., Aliabouzar, M., Sarkar, K., and Zhang, L.G.: Improved human bone marrow mesenchymal stem cell osteogenesis in 3D bioprinted tissue scaffolds with low intensity pulsed ultrasound stimulation. Sci. Rep. 6, 1 (2016).Google Scholar
127.Braham, M.V., Ahlfeld, T., Akkineni, A.R., Minnema, M.C., Dhert, W.J., Öner, F.C., Robin, C., Lode, A., Gelinsky, M., and Alblas, J.: Endosteal and perivascular subniches in a 3D bone marrow model for multiple myeloma. Tissue Eng. Part C. Methods 24, 300 (2018).10.1089/ten.tec.2017.0467Google Scholar