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Three-dimensional neuronal cell culture: in pursuit of novel treatments for neurodegenerative disease

Published online by Cambridge University Press:  03 October 2017

Sarah-Sophia D. Carter ,
Xiao Liu ,
Zhilian Yue  and
Gordon G. Wallace
Sarah-Sophia D. Carter
Affiliation:
ARC Centre of Excellence for Electromaterials Science, Intelligent Polymer Research Institute, AIIM Facility, University of Wollongong, NSW 2522, Australia Utrecht University, Utrecht, The Netherlands
Xiao Liu
Affiliation:
ARC Centre of Excellence for Electromaterials Science, Intelligent Polymer Research Institute, AIIM Facility, University of Wollongong, NSW 2522, Australia
Zhilian Yue
Affiliation:
ARC Centre of Excellence for Electromaterials Science, Intelligent Polymer Research Institute, AIIM Facility, University of Wollongong, NSW 2522, Australia
Gordon G. Wallace*
Affiliation:
ARC Centre of Excellence for Electromaterials Science, Intelligent Polymer Research Institute, AIIM Facility, University of Wollongong, NSW 2522, Australia
*
Address all correspondence to Gordon G. Wallace at [email protected]
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Abstract

To gain a better understanding of the underlying mechanisms of neurological disease, relevant tissue models are imperative. Over the years, this realization has fuelled the development of novel tools and platforms, which aim at capturing in vivo complexity. One example is the field of biofabrication, which focuses on fabrication of three-dimensional (3D) biologically functional products in a controlled and automated manner. Herein, we provide a general overview of classical 3D cell culture platforms, particularly in the context of neurodegenerative disease. Subsequently, the focus is put on bioprinting-based biofabrication, its potential to advance 3D neuronal cell culture and, to conclude, the relevant translational bottlenecks, which will need to be considered as the field evolves.

Type
Biomaterials for 3D Cell Biology Prospective Articles
Information
MRS Communications , Volume 7 , Issue 3 , September 2017 , pp. 320 - 331
Copyright
Copyright © Materials Research Society 2017 

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References

1.Lee, J., Cuddihy, M.J., and Kotov, N.A.: Three-dimensional cell culture matrices: state of the art. Tissue Eng. B: Rev. 14, 61 (2008).Google Scholar
2.Edmondson, R., Broglie, J.J., Adcock, A.F., and Yang, L.: Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev. Technol. 12, 207 (2014).Google Scholar
3.Pampaloni, F., Reynaud, E.G., and Stelzer, E.H.: The third dimension bridges the gap between cell culture and live tissue. Nat. Rev. Mol. Cell Biol. 8, 839 (2007).Google Scholar
4.Santos, E., Hernández, R.M., Pedraz, J.L., and Orive, G.: Novel advances in the design of three-dimensional bio-scaffolds to control cell fate: translation from 2D to 3D. Trends Biotechnol. 30, 331 (2012).Google Scholar
5.Antoni, D., Burckel, H., Josset, E., and Noel, G.: Three-dimensional cell culture: a breakthrough in vivo. Int. J. Mol. Sci. 16, 5517 (2015).Google Scholar
6.McMurtrey, R.J.: Novel advancements in three-dimensional neural tissue engineering and regenerative medicine. Neural Regener. Res. 10, 352 (2015).Google Scholar
7.Caliari, S.R. and Burdick, J.A.: A practical guide to hydrogels for cell culture. Nat. Methods 13, 405 (2016).Google Scholar
8.Banerjee, S. and Bhat, M.A.: Neuron-glial interactions in blood-brain barrier formation. Annu. Rev. Neurosci. 30, 235 (2007).Google Scholar
9.Struzyna, L.A., Katiyar, K., and Cullen, D.K.: Living scaffolds for neuroregeneration. Curr. Opin. Solid State Mater. Sci. 18, 308 (2014).Google Scholar
10.Miller, J.P. and Jacobs, G.A.: Relationships between neuronal structure and function. J. Exp. Biol. 112, 129 (1984).Google Scholar
11.Araque, A. and Navarrete, M.: Glial cells in neuronal network function. Phil. Trans. R. Soc. B 365, 2375 (2010).Google Scholar
12.Barros, C.S., Franco, S.J., and Müller, U.: Extracellular matrix: functions in the nervous system. Cold Spring Harbor Perspect. Biol. 3, a005108 (2011).Google Scholar
13.Bradke, F. and Dotti, C.G.: Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr. Opin. Neurobiol. 10, 574 (2000).Google Scholar
14.Kleinman, H.K., Philp, D., and Hoffman, M.P.: Role of the extracellular matrix in morphogenesis. Curr. Opin. Biotechnol. 14, 526 (2003).Google Scholar
15.Cullen, D.K., Wolf, J.A., Vernekar, V.N., Vukasinovic, J., and LaPlaca, M.C.: Neural tissue engineering and biohybridized microsystems for neurobiological investigation in vitro (Part 1). Crit. Rev. Biomed. Eng. 39, 201 (2011).Google Scholar
16.Liedmann, A., Frech, S., Morgan, P.J., Rolfs, A., and Frech, M.J.: Differentiation of human neural progenitor cells in functionalized hydrogel matrices. BioRes. Open Access 1, 16 (2012).Google Scholar
17.Tang-Schomer, M.D., White, J.D., Tien, L.W., Schmitt, L.I., Valentin, T.M., Graziano, D.J., Hopkins, A.M., Omenetto, F.G., Haydon, P.G., and Kaplan, D.L.: Bioengineered functional brain-like cortical tissue. Proc. Natl Acad. Sci. USA 111, 13811 (2014).Google Scholar
18.Haycock, J.W.: 3D cell culture: a review of current approaches and techniques. 3D Cell Cult.: Methods Protoc. 695, 1 (2011).Google Scholar
19.Knight, E. and Przyborski, S.: Advances in 3D cell culture technologies enabling tissue-like structures to be created in vitro. J. Anat. 227, 746 (2015).Google Scholar
20.Pereira, J.F., Awatade, N.T., Loureiro, C.A., Matos, P., Amaral, M.D., and Jordan, P.: The third dimension: new developments in cell culture models for colorectal research. Cell. Mol. Life Sci. 73, 3971 (2016).Google Scholar
21.Liu, Y., Gill, E., and Huang, Y.Y.S.: Microfluidic on-chip biomimicry for 3D cell culture: a fit-for-purpose investigation from the end user standpoint. Future Sci. OA 3, FSO173 (2017).Google Scholar
22.Melchels, F.P., Domingos, M.A., Klein, T.J., Malda, J., Bartolo, P.F., and Hutmacher, D.W.: Additive manufacturing of tissues and organs. Prog. Polym. Sci. 37, 1079 (2012).Google Scholar
23.Malda, J., Visser, J., Melchels, F.P., Jüngst, T., Hennink, W.E., Dhert, W.J., Groll, J., and Hutmacher, D.W.: 25th anniversary article: engineering hydrogels for biofabrication. Adv. Mater. 25, 5011 (2013).Google Scholar
24.Groll, J., Boland, T., Blunk, T., Burdick, J.A., Cho, D.-W., Dalton, P.D., Derby, B., Forgacs, G., Li, Q., Mironov, V.A., Moroni, L., Nakamura, M., Shu, W., Takeuchi, S., Vozzi, G., Woodfield, T.B.F., Xu, T., Yoo, J.J., and Malda, J.: Biofabrication: reappraising the definition of an evolving field. Biofabrication 8, 013001 (2016).Google Scholar
25.Derby, B.: Bioprinting: inkjet printing proteins and hybrid cell-containing materials and structures. J. Mater. Chem. 18, 5717 (2008).Google Scholar
26.Przedborski, S., Vila, M., and Jackson-Lewis, V.: Series introduction: neurodegeneration: what is it and where are we? J. Clin. Invest. 111, 3 (2003).Google Scholar
27.Yiannopoulou, K.G. and Papageorgiou, S.G.: Current and future treatments for Alzheimer's disease. Therap. Adv. Neurol. Disord. 6, 19 (2013).Google Scholar
28.Korolev, I.O.: Alzheimer's disease: a clinical and basic science review. Med. Stud. Res. J. 4, 24 (2014).Google Scholar
29.Dharmarajan, T.S. and Gunturu, S.G.: Alzheimer's disease: a healthcare burden of epidemic proportion. Am. Health Drug Benefits 2, 3 (2009).Google Scholar
30.Cuny, G.D.: Neurodegenerative diseases: challenges and opportunities. Future Med. Chem. 4, 1647 (2012).Google Scholar
31.Wimo, A., Jönsson, L., Bond, J., Prince, M., and Winblad, B.: The worldwide economic impact of dementia 2010. Alzheimers Dement. 9, 1 (2013).Google Scholar
32.Donev, R., Kolev, M., Millet, B., and Thome, J.: Neuronal death in Alzheimer's disease and therapeutic opportunities. J. Cell. Mol. Med. 13, 4329 (2009).Google Scholar
33.Deleglise, B., Magnifico, S., Duplus, E., Vaur, P., Soubeyre, V., Belle, M., Vignes, M., Viovy, J.L., Jacotot, E., Peyrin, J.M., and Brugg, B.: β-amyloid induces a dying-back process and remote trans-synaptic alterations in a microfluidic-based reconstructed neuronal network. Acta Neuropathol. Commun. 2, 145 (2014).Google Scholar
34.Heneka, M.T., Carson, M.J., El Khoury, J., Landreth, G.E., Brosseron, F., Feinstein, D.L., Jacobs, A.H., Wyss-Coray, T., Vitorica, J., Ransohoff, R.M., Herrup, K., Frautschy, S.A., Finsen, B., Brown, G.C., Verkhratsky, A., Yamanaka, K., Koistinaho, J., Latz, E., Halle, A., Petzold, G.C., Town, T., Morgan, D., Shinohara, M.L., Perry, V.H., Holmes, C., Bazan, N.G., Brooks, D.J., Hunot, S., Joseph, B., Deigendesch, N., Garaschuk, O., Boddeke, E., Dinarello, C.A., Breitner, J.C., Cole, G.M., Golenbock, D.T., and Kummer, M.P.: Neuroinflammation in Alzheimer's disease. Lancet Neurol. 14, 388 (2015).Google Scholar
35.Lunn, J.S., Sakowski, S.A., Hur, J., and Feldman, E.L.: Stem cell technology for neurodegenerative diseases. Ann. Neurol. 70, 353 (2011).Google Scholar
36.Achilli, T.M., Meyer, J., and Morgan, J.R.: Advances in the formation, use and understanding of multi-cellular spheroids. Expert Opin Biol. Ther. 12, 1347 (2012).Google Scholar
37.Simian, M. and Bissell, M.J.: Organoids: a historical perspective of thinking in three dimensions. J. Cell Biol. 216, 31 (2017).Google Scholar
38.Fang, Y. and Eglen, R.M.: Three-dimensional cell cultures in drug discovery and development. SLAS DISCOV.: Adv. Life Sci. R&D. doi: 10.1177/2472555217696795, Published online 17 March 2017.Google Scholar
39.Mehta, G., Hsiao, A.Y., Ingram, M., Luker, G.D., and Takayama, S.: Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J. Control. Release 164, 192 (2012).Google Scholar
40.Fennema, E., Rivron, N., Rouwkema, J., van Blitterswijk, C., and de Boer, J.: Spheroid culture as a tool for creating 3D complex tissues. Trends Biotechnol. 31, 108 (2013).Google Scholar
41.Dingle, Y-T. L., Boutin, M.E., Chirila, A.M., Livi, L.L., Labriola, N.R., Jakubek, L.M., Morgan, J.R., Darling, E.M., Kauer, J.A., and Hoffman-Kim Diane, D.: Three-dimensional neural spheroid culture: an in vitro model for cortical studies. Tissue Eng. C: Methods 21, 1274 (2015).Google Scholar
42.Boutin, M.E., Kramer, L.L., Livi, L.L., Brown, T., Moore, C., and Hoffman-Kim, D.: A three-dimensional neural spheroid model for capillary-like network formation. J. Neurosci. Methods. doi 10.1016/j.jneumeth.2017.01.014, Published online 29 January 2017.Google Scholar
43.Ranga, A., Gjorevski, N., and Lutolf, M.P.: Drug discovery through stem cell-based organoid models. Adv. Drug Delivery. Rev. 69, 19 (2014).Google Scholar
44.Fatehullah, A., Tan, S.H., and Barker, N.: Organoids as an in vitro model of human development and disease. Nat. Cell Biol. 18, 246 (2016).Google Scholar
45.Schneeberger, K., Spee, B., Costa, P., Sachs, N., Clevers, H., and Malda, J.: Converging biofabrication and organoid technologies: the next frontier in hepatic and intestinal tissue engineering? Biofabrication 9, 013001 (2017).Google Scholar
46.Raja, W.K., Mungenast, A.E., Lin, Y.T., Ko, T., Abdurrob, F., Seo, J., and Tsai, L.H.: Self-Organizing 3D human neural tissue derived from induced pluripotent stem cells recapitulate Alzheimer's disease phenotypes. PLoS ONE 11, e0161969 (2016).Google Scholar
47.O'brien, F.J.: Biomaterials & scaffolds for tissue engineering. Mater. Today 14, 88 (2011).Google Scholar
48.Breslin, S. and O'Driscoll, L.: Three-dimensional cell culture: the missing link in drug discovery. Drug Discov. Today 18, 240 (2013).Google Scholar
49.Chan, B.P. and Leong, K.W.: Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur. Spine J. 17, 467 (2008).Google Scholar
50.Murphy, A.R., Laslett, A., O'Brien, C.M., and Cameron, N.R.: Scaffolds for 3D in vitro culture of neural lineage cells. Acta Biomater. 54, 1 (2017).Google Scholar
51.Frampton, J.P., Hynd, M.R., Shuler, M.L., and Shain, W.: Fabrication and optimization of alginate hydrogel constructs for use in 3D neural cell culture. Biomed. Mater. 6, 015002 (2011).Google Scholar
52.Lai, Y., Cheng, K., and Kisaalita, W.: Three dimensional neuronal cell cultures more accurately model voltage gated calcium channel functionality in freshly dissected nerve tissue. PLoS ONE 7, e45074 (2012).Google Scholar
53.Choi, S.H., Kim, Y.H., Hebisch, M., Sliwinski, C., Lee, S., D'Avanzo, C., Chen, H., Hooli, B., Asselin, C., Muffat, J., and Klee, J.B.: A three-dimensional human neural cell culture model of Alzheimer's disease. Nature 515, 274 (2014).Google Scholar
54.Kraus, D., Boyle, V., Leibig, N., Stark, G.B., and Penna, V.: The neuro-spheroid—a novel 3D in vitro model for peripheral nerve regeneration. J. Neurosci. Methods 246, 97 (2015).Google Scholar
55.van der Meer, A.D. and van den Berg, A.: Organs-on-chips: breaking the in vitro impasse. Integr. Biol. 4, 461 (2012).Google Scholar
56.Bhatia, S.N. and Ingber, D.E.: Microfluidic organs-on-chips. Nat. Biotechnol. 32, 760 (2014).Google Scholar
57.Yi, Y., Park, J., Lim, J., Lee, C.J., and Lee, S.H.: Central nervous system and its disease models on a chip. Trends Biotechnol. 33, 762 (2015).Google Scholar
58.Choi, Y.J., Chae, S., Kim, J.H., Barald, K.F., Park, J.Y., and Lee, S.H.: Neurotoxic amyloid beta oligomeric assemblies recreated in microfluidic platform with interstitial level of slow flow. Sci. Rep. 3, 1921 (2013).Google Scholar
59.Cho, H., Hashimoto, T., Wong, E., Hori, Y., Wood, L.B., Zhao, L., Haigis, K.M., Hyman, B.T., and Irimia, D.: Microfluidic chemotaxis platform for differentiating the roles of soluble and bound amyloid-β on microglial accumulation. Sci. Rep. 3, 1823 (2013).Google Scholar
60.Kunze, A., Meissner, R., Brando, S., and Renaud, P.: Co-pathological connected primary neurons in a microfluidic device for Alzheimer studies. Biotechnol. Bioeng. 108, 2241 (2011).Google Scholar
61.Song, H.L., Shim, S., Kim, D.H., Won, S.H., Joo, S., Kim, S., Jeon, N.L., and Yoon, S.Y.: β-Amyloid is transmitted via neuronal connections along axonal membranes. Ann. Neurol. 75, 88 (2014).Google Scholar
62.Dujardin, S., Lécolle, K., Caillierez, R., Bégard, S., Zommer, N., Lachaud, C., Carrier, S., Dufour, N., Aurégan, G., Winderickx, J., Hantraye, P., Déglon, N., Colin, M., and Buée, L.: Neuron-to-neuron wild-type Tau protein transfer through a trans-synaptic mechanism: relevance to sporadic tauopathies. Acta Neuropathol. Commun. 2, 14 (2014).Google Scholar
63.Calafate, S., Buist, A., Miskiewicz, K., Vijayan, V., Daneels, G., De Strooper, B., De Wit, J., Verstrekenand, P., and Moechars, D.: Synaptic contacts enhance cell-to-cell tau pathology propagation. Cell Rep. 11, 1176 (2015).Google Scholar
64.Murphy, S.V. and Atala, A.: 3D bioprinting of tissues and organs. Nat. Biotechnol. 32, 773 (2014).Google Scholar
65.Hölzl, K., Lin, S., Tytgat, L., Van Vlierberghe, S., Gu, L., and Ovsianikov, A.: Bioink properties before, during and after 3D bioprinting. Biofabrication 8, 032002 (2016).Google Scholar
66.Xu, T., Jin, J., Gregory, C., Hickman, J.J., and Boland, T.: Inkjet printing of viable mammalian cells. Biomaterials 26, 93 (2005).Google Scholar
67.Xu, T., Gregory, C.A., Molnar, P., Cui, X., Jalota, S., Bhaduri, S.B., and Boland, T.: Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials 27, 3580 (2006).Google Scholar
68.Lorber, B., Hsiao, W.K., Hutchings, I.M., and Martin, K.R.: Adult rat retinal ganglion cells and glia can be printed by piezoelectric inkjet printing. Biofabrication 6, 015001 (2013).Google Scholar
69.Tse, C., Whiteley, R., Yu, T., Stringer, J., MacNeil, S., Haycock, J.W., and Smith, P.J.: Inkjet printing Schwann cells and neuronal analogue NG108-15 cells. Biofabrication 8, 015017 (2016).Google Scholar
70.Lee, Y.B., Polio, S., Lee, W., Dai, G., Menon, L., Carroll, R.S., and Yoo, S.S.: Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture. Exp. Neurol. 223, 645 (2010).Google Scholar
71.Hsieh, F.Y., Lin, H.H., and Hsu, S.H.: 3D bioprinting of neural stem cell-laden thermoresponsive biodegradable polyurethane hydrogel and potential in central nervous system repair. Biomaterials 71, 48 (2015).Google Scholar
72.Lozano, R., Stevens, L., Thompson, B.C., Gilmore, K.J., Gorkin, R., Stewart, E.M., in het Panhuis, M., Romero-Ortega, M., and Wallace, G.G.: 3D printing of layered brain-like structures using peptide modified gellan gum substrates. Biomaterials 67, 264 (2015).Google Scholar
73.Gu, Q., Tomaskovic-Crook, E., Lozano, R., Chen, Y., Kapsa, R.M., Zhou, Q., Wallace, G.G., and Crook, J.M.: Functional 3D neural mini-tissues from printed gel-based bioink and human neural stem cells. Adv. Healthc. Mater. 5, 1429 (2016).Google Scholar
74.Gu, Q., Tomaskovic-Crook, E., Wallace, G.G., and Crook, J.M.: 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv. Healthc. Mater. 6, 1700175 (2017).Google Scholar
75.Mironov, V., Visconti, R.P., Kasyanov, V., Forgacs, G., Drake, C.J., and Markwald, R.R.: Organ printing: tissue spheroids as building blocks. Biomaterials 30, 2164 (2009).Google Scholar
76.Mironov, V., Khesuani, Y.D., Bulanova, E.A., Koudan, E.V., Parfenov, V.A., Knyazeva, A.D., Mitryashkin, A.N., Replyanski, N., Kasyanov, V.A., and DAS, F.P.: Patterning of tissue spheroids biofabricated from human fibroblasts on the surface of electrospun polyurethane matrix using 3D bioprinter. Int. J. Bioprint. 2, 45 (2016).Google Scholar
77.Yi, H.G., Lee, H., and Cho, D.W.: 3D printing of organs-on-chips. Bioengineering 4, 10 (2017).Google Scholar
78.Johnson, B.N., Lancaster, K.Z., Hogue, I.B., Meng, F., Kong, Y.L., Enquist, L.W., and McAlpine, M.C.: 3D printed nervous system on a chip. Lab. Chip 16, 1393 (2016).Google Scholar
79.Rezende, R.A., Selishchev, S.V., Kasyanov, V.A., da Silva, J.V.L., and Mironov, V.A.: An organ biofabrication line: enabling technology for organ printing. Part I: from BIOCAD to biofabricators of spheroids. Biomed. Eng. 47, 116 (2013).Google Scholar
80.Atala, A. and Yoo, J.J.: Essentials of 3D Biofabrication and Translation (Academic Press, Cambridge, Massachusetts, 2015), pp. 19–41.Google Scholar
81.Chimene, D., Lennox, K.K., Kaunas, R.R., and Gaharwar, A.K.: Advanced bioinks for 3D printing: a materials science perspective. Ann. Biomed. Eng. 44, 2090 (2016).Google Scholar
82.Gao, B., Yang, Q., Zhao, X., Jin, G., Ma, Y., and Xu, F.: 4D bioprinting for biomedical applications. Trends Biotechnol. 34, 746 (2016).Google Scholar
83.Li, Y.C., Zhang, Y.S., Akpek, A., Shin, S.R., and Khademhosseini, A.: 4D bioprinting: the next-generation technology for biofabrication enabled by stimuli-responsive materials. Biofabrication 9, 012001 (2016).Google Scholar
84.Hourd, P., Medcalf, N., Segal, J., and Williams, D.J.: A 3D bioprinting exemplar of the consequences of the regulatory requirements on customized processes. Regen. Med. 10, 863 (2015).Google Scholar
85.Chhaya, M.P., Poh, P.S., Balmayor, E.R., van Griensven, M., Schantz, J.T., and Hutmacher, D.W.: Additive manufacturing in biomedical sciences and the need for definitions and norms. Expert Rev. Med. Devices 12, 537 (2015).Google Scholar
86.Baker, H.B., McQuilling, J.P., and King, N.M.: Ethical considerations in tissue engineering research: case studies in translation. Methods 99, 135 (2016).Google Scholar
87.Otto, I.A., Breugem, C.C., Malda, J., and Bredenoord, A.L.: Ethical considerations in the translation of regenerative biofabrication technologies into clinic and society. Biofabrication 8, 042001 (2016).Google Scholar
88.Gilbert, F., O'Connell, C.D., Mladenovska, T., and Dodds, S.: Print me an organ? Ethical and regulatory issues emerging from 3D bioprinting in medicine. Sci. Eng. Ethics. doi: 10.1007/s11948-017-9874-6, Published online 09 February 2017.Google Scholar