AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (2.6 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Review Article | Open Access

Culture models produced via biomanufacturing for neural tissue-like constructs based on primary neural and neural stem cells

Wei Chen1,2,3,§Ke Gai1,2,3,§Feng Lin1,2,3Wei Sun1,2,3,4Yu Song1,2,3( )
Biomanufacturing Center, Department of Mechanical Engineering, Tsinghua University, Beijing 100084, China
Biomanufacturing and Rapid Forming Technology Key Laboratory of Beijing, Beijing 100084, China
"Biomanufacturing and Engineering Living Systems" Innovation International Talents Base (111 Base), Beijing 100084, China
Department of Mechanical Engineering, Drexel University, Philadelphia, PA, USA

§ These authors contributed equally to this work.

Show Author Information

Abstract

Neural tissue-like constructs have important application potential in both neural tissue regeneration and individual medical treatment due to the ideal bioenvironment they provide for the growth of primary and stem cells. The biomaterials used in three-dimensional (3D) biomanufacturing techniques play a critical role in bioenvironment fabrication. They help optimize the manufacturing techniques and the long-term environment that supports cell structure and nutrient transmission. This paper reviews the current progress being made in the biomaterials utilized in neural cell cultures for in vitro bioenvironment construction. The following four requirements for biomaterials are evaluated: biocompatibility, porosity, supportability, and permeability. This study also summarizes the recent culture models based on primary neural cells. Furthermore, the biomaterials used for neural stem cell constructs are discussed. This study’s results indicate that compared with traditional two-dimensional (2D) cultures (with minimal biomaterial requirements), modulus 3D cultures greatly benefit from optimized biomaterials for long-term culturing.

References

[1]
Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol 2014, 32(8): 773-785.
[2]
Gilmour AD, Woolley AJ, Poole-Warren LA, et al. A critical review of cell culture strategies for modelling intracortical brain implant material reactions. Biomaterials 2016, 91: 23-43.
[3]
Allmeling C, Jokuszies A, Reimers K, et al. Use of spider silk fibres as an innovative material in a biocompatible artificial nerve conduit. J Cell Mol Med 2006, 10(3): 770-777.
[4]
Prestwich GD. Hyaluronic acid-based clinical biomaterials derived for cell and molecule delivery in regenerative medicine. J Control Release 2011, 155(2): 193-199.
[5]
Onoe H, Okitsu T, Itou A, et al. Metre-long cell-laden microfibres exhibit tissue morphologies and functions. Nat Mater 2013, 12(6): 584-590.
[6]
Jakus AE, Secor EB, Rutz AL, et al. Three-dimensional printing of high-content graphene scaffolds for electronic and biomedical applications. ACS Nano 2015, 9(4): 4636-4648.
[7]
Schirmer KS, Gorkin R 3rd, Beirne S, et al. Cell compatible encapsulation of filaments into 3D hydrogels. Biofabrication 2016, 8(2): 025013.
[8]
Liu YX, Liu J, Chen SC, et al. Soft and elastic hydrogel-based microelectronics for localized low-voltage neuromodulation. Nat Biomed Eng 2019, 3(1): 58-68.
[9]
Mihai LA, Chin L, Janmey PA, et al. A comparison of hyperelastic constitutive models applicable to brain and fat tissues. J Royal Soc Interface 2015, 12(110): 0486.
[10]
Tang YJ, Lü GR, He SZ, et al. The application of shear wave elastography in the diagnosis of anaerobic encephalopathy in newborn rabbits (in Chinese). Chin J Ultrasound Med 2019, 35(8): 745-747.
[11]
Zarei M, Samimi A, Khorram M, et al. Fabrication and characterization of conductive polypyrrole/ chitosan/collagen electrospun nanofiber scaffold for tissue engineering application. Int J Biol Macromol 2021, 168: 175-186.
[12]
Magaz A, Li X, Gough JE, et al. Graphene oxide and electroactive reduced graphene oxide-based composite fibrous scaffolds for engineering excitable nerve tissue. Mater Sci Eng C Mater Biol Appl 2021, 119: 111632.
[13]
Zhang T, Yan KC, Ouyang LL, et al. Mechanical characterization of bioprinted in vitro soft tissue models. Biofabrication 2013, 5(4): 045010.
[14]
Ouyang LL, Yao R, Chen X, et al. 3D printing of HEK 293FT cell-laden hydrogel into macroporous constructs with high cell viability and normal biological functions. Biofabrication 2015, 7(1): 015010.
[15]
Ouyang LL, Yao R, Zhao Y, et al. Effect of bioink properties on printability and cell viability for 3D bioplotting of embryonic stem cells. Biofabrication 2016, 8(3): 035020.
[16]
Ouyang LL, Highley CB, Rodell CB, et al. 3D printing of shear-thinning hyaluronic acid hydrogels with secondary cross-linking. ACS Biomater Sci Eng 2016, 2(10): 1743-1751.
[17]
Ouyang LL, Highley CB, Sun W, et al. A generalizable strategy for the 3D bioprinting of hydrogels from nonviscous photo-crosslinkable inks. Adv Mater 2017, 29(8): 1604983.
[18]
Ouyang LL, Burdick JA, Sun W. Facile biofabrication of heterogeneous multilayer tubular hydrogels by fast diffusion-induced gelation. ACS Appl Mater Interfaces 2018, 10(15): 12424-12430.
[19]
Ouyang LL, Armstrong JPK, Chen Q, et al. Void-free 3D bioprinting for in situ endothelialization and microfluidic perfusion. Adv Funct Mater 2020, 30(1): 1908349.
[20]
Song Y, Su XL, Firouzian KF, et al. Engineering of brain-like tissue constructs via 3D cell-printing technology. Biofabrication 2020, 12(3): 035016.
[21]
Egger B, van Giesen L, Moraru M, et al. In vitro imaging of primary neural cell culture from Drosophila. Nat Protoc 2013, 8(5): 958-965.
[22]
Aubid NN, Liu Y, Vidal JMP, et al. Isolation and culture of porcine primary fetal progenitors and neurons from the developing dorsal telencephalon. J Vet Sci 2019, 20(2): e3.
[23]
Pan CP, Kumar C, Bohl S, et al. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol Cell Proteomics 2009, 8(3): 443-450.
[24]
Cadena M, Ning LQ, King A, et al. 3D bioprinting of neural tissues. Adv Healthc Mater 2021, 10(15): e2001600.
[25]
Dai XL, Ma C, Lan Q, et al. 3D bioprinted glioma stem cells for brain tumor model and applications of drug susceptibility. Biofabrication 2016, 8(4): 045005.
[26]
Firouzian KF, Song Y, Lin F, et al. Fabrication of a biomimetic spinal cord tissue construct with heterogenous mechanical properties using intrascaffold cell assembly. Biotechnol Bioeng 2020, 117(10): 3094-3107.
[27]
Song Y, Lei Y, Yan XQ, et al. Biosensors of ZnO nanotetrapods and HEMT for detecting uric acid. In 2012 38th Annual Northeast Bioengineering Conference (NEBEC), Philadelphia, PA, USA, 2012, pp 345-346.
[28]
Liu BX, Jin ZZ, Chen HY, et al. Electrospun poly (L-lactic acid)/gelatine membranes loaded with doxorubicin for effective suppression of glioblastoma cell growth in vitro and in vivo. Regen Biomater 2021, 8(5): rbab043.
[29]
Alge CS, Hauck SM, Priglinger SG, et al. Differential protein profiling of primary versus immortalized human RPE cells identifies expression patterns associated with cytoskeletal remodeling and cell survival. J Proteome Res 2006, 5(4): 862-878.
[30]
Mota B, Herculano-Houzel S. Response to comments on “Cortical folding scales universally with surface area and thickness, not number of neurons”. Science 2016, 351(6275): 826.
[31]
Sauleau P, Lapouble E, Val-Laillet D, et al. The pig model in brain imaging and neurosurgery. Animal 2009, 3(8): 1138-1151.
[32]
Winterdahl M, Audrain H, Landau AM, et al. PET brain imaging of neuropeptide Y2 receptors using N-11C-methyl-JNJ-31020028 in pigs. J Nucl Med 2014, 55(4): 635-639.
[33]
Conrad MS, Dilger RN, Johnson RW. Brain growth of the domestic pig (Sus scrofa) from 2 to 24 weeks of age: a longitudinal MRI study. Dev Neurosci 2012, 34(4): 291-298.
[34]
Bjarkam CR, Glud AN, Orlowski D, et al. The telencephalon of the Göttingen minipig, cytoarchitecture and cortical surface anatomy. Brain Struct Funct 2017, 222(5): 2093-2114.
[35]
Li YCE, Jodat YA, Samanipour R, et al. Toward a neurospheroid niche model: optimizing embedded 3D bioprinting for fabrication of neurospheroid brain-like co-culture constructs. Biofabrication 2020, 13(1): .
[36]
Li F, Song Y, Dryer A, et al. Nondestructive evaluation of progressive neuronal changes in organotypic rat hippocampal slice cultures using ultrahigh-resolution optical coherence microscopy. Neurophotonics 2014, 1(2): 025002.
[37]
Landry MJ, Gu KE, Harris SN, et al. Tunable engineered extracellular matrix materials: polyelectrolyte multilayers promote improved neural cell growth and survival. Macromol Biosci 2019, 19(5): e1900036.
[38]
Martin AD, Chua SW, Au CG, et al. Peptide nanofiber substrates for long-term culturing of primary neurons. ACS Appl Mater Interfaces 2018, 10(30): 25127-25134.
[39]
Song Y, Pimentel C, Walters K, et al. Neuroprotective levels of IGF-1 exacerbate epileptogenesis after brain injury. Sci Rep 2016, 6: 32095.
[40]
Salaris F, Colosi C, Brighi C, et al. 3D bioprinted human cortical neural constructs derived from induced pluripotent stem cells. J Clin Med 2019, 8(10): E1595.
[41]
Yeon JY, Hwang JY, Lee HW, et al. Optimized clump culture methods for adult human multipotent neural cells. Int J Mol Sci 2018, 19(11): E3380.
[42]
Tang-Schomer MD, Wu WB, Kaplan DL, et al. In vitro 3D regeneration-like growth of human patient brain tissue. J Tissue Eng Regen Med 2018, 12(5): 1247-1260.
[43]
Khan J, Das G, Gupta V, et al. Neurosphere development from hippocampal and cortical embryonic mixed primary neuron culture: a potential platform for screening neurochemical modulator. ACS Chem Neurosci 2018, 9(11): 2870-2878.
[44]
Newland B, Ehret F, Hoppe F, et al. Macroporous heparin-based microcarriers allow long-term 3D culture and differentiation of neural precursor cells. Biomaterials 2020, 230: 119540.
[45]
Bunevicius A, Schregel K, Sinkus R, et al. Review: MR elastography of brain tumors. Neuroimage Clin 2020, 25: 102109.
[46]
Dai XL, Liu LB, Ouyang J, et al. Coaxial 3D bioprinting of self-assembled multicellular heterogeneous tumor fibers. Sci Rep 2017, 7(1): 1457.
[47]
Liu LB, Li XD, Zhang XZ, et al. Biomanufacturing of a novel in vitro biomimetic blood-brain barrier model. Biofabrication 2020, 12(3): 035008.
[48]
Wang XZ, Li XD, Dai XL, et al. Bioprinting of glioma stem cells improves their endotheliogenic potential. Colloids Surf B Biointerfaces 2018, 171: 629-637.
[49]
Wang XZ, Dai XL, Zhang XZ, et al. 3D bioprinted glioma cell-laden scaffolds enriching glioma stem cells via epithelial-mesenchymal transition. J Biomed Mater Res A 2019, 107(2): 383-391.
[50]
Gage FH, Kempermann G, Palmer TD, et al. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 1998, 36(2): 249-266.
[51]
Doetsch F, Caillé I, Lim DA, et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97(6): 703-716.
[52]
Matsushiro Y, Kato-Negishi M, Onoe H. Differentiation of 3D-shape-controlled mouse neural stem cell to neural tissues in closed agarose microchambers. Biotechnol Bioeng 2018, 115(6): 1614-1623.
[53]
Liu DH, Pavathuparambil Abdul Manaph N, Al-Hawwas M, et al. Coating materials for neural stem/ progenitor cell culture and differentiation. Stem Cells Dev 2020, 29(8): 463-474.
[54]
Rao SS, Winter JO. Adhesion molecule-modified biomaterials for neural tissue engineering. Front Neuroeng 2009, 2: 6.
[55]
Ma W, Tavakoli T, Derby E, et al. Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev Biol 2008, 8: 90.
[56]
Darrabie MD, Kendall WF Jr, Opara EC. Characteristics of poly-l-ornithine-coated alginate microcapsules. Biomaterials 2005, 26(34): 6846-6852.
[57]
Buzanska L, Ruiz A, Zychowicz M, et al. Patterned growth and differentiation of human cord blood-derived neural stem cells on bio-functionalized surfaces. Acta Neurobiol Exp (Wars) 2009, 69(1): 24-36.
[58]
Ge HF, Tan L, Wu PF, et al. Poly-L-ornithine promotes preferred differentiation of neural stem/progenitor cells via ERK signalling pathway. Sci Rep 2015, 5: 15535.
[59]
Pacherník J, Esner M, Bryja V, et al. Neural differentiation of mouse embryonic stem cells grown in monolayer. Reprod Nutr Dev 2002, 42(4): 317-326.
[60]
Hall PE, Lathia JD, Caldwell MA, et al. Laminin enhances the growth of human neural stem cells in defined culture media. BMC Neurosci 2008, 9: 71.
[61]
Moore L, Skop NB, Rothbard DE, et al. Tethered growth factors on biocompatible scaffolds improve stemness of cultured rat and human neural stem cells and growth of oligodendrocyte progenitors. Methods 2018, 133: 54-64.
[62]
Flanagan LA, Rebaza LM, Derzic S, et al. Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 2006, 83(5): 845-856.
[63]
Hughes CS, Postovit LM, Lajoie GA. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 2010, 10(9): 1886-1890.
[64]
Koutsopoulos S, Zhang SG. Long-term three-dimensional neural tissue cultures in functionalized self-assembling peptide hydrogels, matrigel and collagen I. Acta Biomater 2013, 9(2): 5162-5169.
[65]
Ouyang LL, Yao R, Mao SS, et al. Three-dimensional bioprinting of embryonic stem cells directs highly uniform embryoid body formation. Biofabrication 2015, 7(4): 044101.
[66]
Li Y, Li L, Chen ZN, et al. Engineering-derived approaches for iPSC preparation, expansion, differentiation and applications. Biofabrication 2017, 9(3): 032001.
[67]
Li Y, Jiang XL, Li L, et al. 3D printing human induced pluripotent stem cells with novel hydroxypropyl chitin bioink: scalable expansion and uniform aggregation. Biofabrication 2018, 10(4): 044101.
[68]
Han J, Xiao ZF, Chen L, et al. Maintenance of the self-renewal properties of neural progenitor cells cultured in three-dimensional collagen scaffolds by the REDD1-mTOR signal pathway. Biomaterials 2013, 34(8): 1921-1928.
[69]
Huang F, Shen Q, Zhao JT. Growth and differentiation of neural stem cells in a three-dimensional collagen gel scaffold. Neural Regen Res 2013, 8(4): 313-319.
[70]
Martin CA, Radhakrishnan S, Nagarajan S, et al. An innovative bioresorbable gelatin based 3D scaffold that maintains the stemness of adipose tissue derived stem cells and the plasticity of differentiated neurons. RSC Adv 2019, 9(25): 14452-14464.
[71]
Bozza A, Coates EE, Incitti T, et al. Neural differentiation of pluripotent cells in 3D alginate-based cultures. Biomaterials 2014, 35(16): 4636-4645.
[72]
Lin HS, Du Q, Li Q, et al. Hydrogel-based bioprocess for scalable manufacturing of human pluripotent stem cell-derived neural stem cells. ACS Appl Mater Interfaces 2018, 10(35): 29238-29250.
[73]
Zheng XS, Yang XF, Liu WG, et al. A novel method for culturing neural stem cells. In Vitro Cell Dev Biol Anim 2007, 43(5/6): 155-158.
[74]
Hsu CC, George JH, Waller S, et al. Increased connectivity of hiPSC-derived neural networks in multiphase granular hydrogel scaffolds. Bioact Mater 2022, 9: 358-372.
[75]
Liu S, Xie YY, Wang LD, et al. A multi-channel collagen scaffold loaded with neural stem cells for the repair of spinal cord injury. Neural Regen Res 2021, 16(11): 2284-2292.
[76]
Lampe KJ, Heilshorn SC. Building stem cell niches from the molecule up through engineered peptide materials. Neurosci Lett 2012, 519(2): 138-146.
[77]
Temple S. The development of neural stem cells. Nature 2001, 414(6859): 112-117.
[78]
Gage FH. Mammalian neural stem cells. Science 2000, 287(5457): 1433-1438.
[79]
Eftekhari BS, Eskandari M, Janmey PA, et al. Surface topography and electrical signaling: single and synergistic effects on neural differentiation of stem cells. Adv Funct Mater 2020, 30(25): 1907792.
[80]
Malatesta P, Appolloni I, Calzolari F. Radial glia and neural stem cells. Cell Tissue Res 2008, 331(1): 165-178.
[81]
Teo BK, Wong ST, Lim CK, et al. Nanotopography modulates mechanotransduction of stem cells and induces differentiation through focal adhesion kinase. ACS Nano 2013, 7(6): 4785-4798.
[82]
Jain D, Mattiassi S, Goh EL, et al. Extracellular matrix and biomimetic engineering microenvironment for neuronal differentiation. Neural Regen Res 2020, 15(4): 573-585.
[83]
Sthanam L, Saxena N, Mistari VK, et al. Initial priming on soft substrates enhances subsequent topography-induced neuronal differentiation in ESCs but not in MSCs. ACS Biomater Sci Eng 2018, 5(1): 180-192.
[84]
Saha K, Keung AJ, Irwin EF, et al. Substrate modulus directs neural stem cell behavior. Biophys J 2008, 95(9): 4426-4438.
[85]
Shi WT, He R, Liu YL. 3D printing scaffolds with hydrogel materials for biomedical applications. Eur J Bio Med Res 2015, 1(3): 3.
[86]
Puckert C, Tomaskovic-Crook E, Gambhir S, et al. Molecular interactions and forces of adhesion between single human neural stem cells and gelatin methacrylate hydrogels of varying stiffness. Acta Biomater 2020, 106: 156-169.
[87]
Arulmoli J, Wright HJ, Phan DTT, et al. Combination scaffolds of salmon fibrin, hyaluronic acid, and laminin for human neural stem cell and vascular tissue engineering. Acta Biomater 2016, 43: 122-138.
[88]
Bento AR, Quelhas P, Oliveira MJ, et al. Three-dimensional culture of single embryonic stem-derived neural/stem progenitor cells in fibrin hydrogels: neuronal network formation and matrix remodelling. J Tissue Eng Regen Med 2017, 11(12): 3494-3507.
[89]
Ouyang LL, Armstrong JPK, Lin YY, et al. Expanding and optimizing 3D bioprinting capabilities using complementary network bioinks. Sci Adv 2020, 6(38): eabc5529.
[90]
Chew L, Añonuevo A, Knock E. Generating cerebral organoids from human pluripotent stem cells. Neural Progenit Cells 2022: 177-199.
[91]
Pham MT, Pollock KM, Rose MD, et al. Generation of human vascularized brain organoids. Neuroreport 2018, 29(7): 588-593.
[92]
Simsa R, Rothenbücher T, Gürbüz H, et al. Brain organoid formation on decellularized porcine brain ECM hydrogels. PLoS One 2021, 16(1): e0245685.
[93]
Han HW, Hou YT, Hsu SH. Angiogenic potential of co-spheroids of neural stem cells and endothelial cells in injectable gelatin-based hydrogel. Mater Sci Eng C Mater Biol Appl 2019, 99: 140-149.
[94]
Zhu YJ, Wang L, Yin FC, et al. Probing impaired neurogenesis in human brain organoids exposed to alcohol. Integr Biol (Camb) 2017, 9(12): 968-978.
[95]
Kunze A, Giugliano M, Valero A, et al. Micropatterning neural cell cultures in 3D with a multi-layered scaffold. Biomaterials 2011, 32(8): 2088-2098.
[96]
Johnson BN, Lancaster KZ, Zhen GH, et al. 3D printed anatomical nerve regeneration pathways. Adv Funct Mater 2015, 25(39): 6205-6217.
[97]
Kapr J, Petersilie L, Distler T, et al. Human induced pluripotent stem cell-derived neural progenitor cells produce distinct neural 3D in vitro models depending on alginate/gellan gum/laminin hydrogel blend properties. Adv Healthc Mater 2021, 10(16): e2100131.
[98]
Harris AR, Wallace GG. Organic electrodes and communications with excitable cells. Adv Funct Mater 2018, 28(12): 1700587.
[99]
Wang SP, Guan S, Li WF, et al. 3D culture of neural stem cells within conductive PEDOT layer-assembled chitosan/gelatin scaffolds for neural tissue engineering. Mater Sci Eng C Mater Biol Appl 2018, 93: 890-901.
[100]
Solanki A, Chueng ST, Yin PT, et al. Axonal alignment and enhanced neuronal differentiation of neural stem cells on graphene-nanoparticle hybrid structures. Adv Mater 2013, 25(38): 5477-5482.
[101]
Jiang ZY, Song Q, Tang ML, et al. Enhanced migration of neural stem cells by microglia grown on a three-dimensional graphene scaffold. ACS Appl Mater Interfaces 2016, 8(38): 25069-25077.
Brain Science Advances
Pages 220-238
Cite this article:
Chen W, Gai K, Lin F, et al. Culture models produced via biomanufacturing for neural tissue-like constructs based on primary neural and neural stem cells. Brain Science Advances, 2021, 7(4): 220-238. https://doi.org/10.26599/BSA.2021.9050021

690

Views

65

Downloads

1

Crossref

Altmetrics

Received: 29 November 2021
Revised: 20 December 2021
Accepted: 03 January 2022
Published: 10 January 2022
© The authors 2021.

This article is published with open access at journals.sagepub.com/home/BSA

Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/ en-us/nam/open-access-at-sage).

Return