Promising Strategies for the Development of Advanced In Vitro Models with High Predictive Power in Ischaemic Stroke Research
Abstract
:1. Introduction
2. Modelling Ischaemic Stroke In Vitro
2.1. Inducing Ischaemia-like Conditions In Vitro
2.2. Most Common Cellular Platforms in In Vitro Stroke Research
3. Factors Defining the Predictive Value of In Vitro Ischaemic Stroke Models
3.1. Origin of Cells or Tissue Used for In Vitro Models of Ischaemic Stroke
3.2. Multicellular Co-Culture Models for In Vitro Ischaemic Stroke Research
3.3. Dimensionality of Cell Culture Models for In Vitro Ischaemic Stroke Research
3.4. Implementation of Microfluidics Technology in In Vitro Models of Ischaemic Stroke
BBB/NVU Models
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Benjamin, E.J.; Blaha, M.J.; Chiuve, S.E.; Cushman, M.; Das, S.R.; Deo, R.; de Ferranti, S.D.; Floyd, J.; Fornage, M.; Gillespie, C.; et al. Heart Disease and Stroke Statistics-2017 Update: A Report from the American Heart Association. Circulation 2017, 135, e146–e603. [Google Scholar] [CrossRef] [PubMed]
- World Stroke Organization. Global Stroke Fact Sheet 2022; World Stroke Organization: Geneva, Switzerland, 2022. [Google Scholar]
- Kuriakose, D.; Xiao, Z. Pathophysiology and Treatment of Stroke: Present Status and Future Perspectives. Int. J. Mol. Sci. 2020, 21, 7609. [Google Scholar] [CrossRef] [PubMed]
- Brouns, R.; De Deyn, P.P. The complexity of neurobiological processes in acute ischemic stroke. Clin. Neurol. Neurosurg. 2009, 111, 483–495. [Google Scholar] [CrossRef] [PubMed]
- Moskowitz, M.A.; Lo, E.H.; Iadecola, C. The science of stroke: Mechanisms in search of treatments. Neuron 2010, 67, 181–198. [Google Scholar] [CrossRef] [Green Version]
- Jayaraj, R.L.; Azimullah, S.; Beiram, R.; Jalal, F.Y.; Rosenberg, G.A. Neuroinflammation: Friend and foe for ischemic stroke. J. Neuroinflamm. 2019, 16, 142. [Google Scholar] [CrossRef] [Green Version]
- Woodruff, T.M.; Thundyil, J.; Tang, S.C.; Sobey, C.G.; Taylor, S.M.; Arumugam, T.V. Pathophysiology, treatment, and animal and cellular models of human ischemic stroke. Mol. Neurodegener. 2011, 6, 11. [Google Scholar] [CrossRef] [Green Version]
- Mozaffarian, D.; Benjamin, E.J.; Go, A.S.; Arnett, D.K.; Blaha, M.J.; Cushman, M.; Das, S.R.; de Ferranti, S.; Despres, J.P.; Fullerton, H.J.; et al. Executive Summary: Heart Disease and Stroke Statistics—2016 Update: A Report from the American Heart Association. Circulation 2016, 133, 447–454. [Google Scholar] [CrossRef]
- Holloway, P.M.; Gavins, F.N. Modeling Ischemic Stroke In Vitro: Status Quo and Future Perspectives. Stroke 2016, 47, 561–569. [Google Scholar] [CrossRef] [Green Version]
- Antonic, A.; Sena, E.S.; Donnan, G.A.; Howells, D.W. Human in vitro models of ischaemic stroke: A test bed for translation. Transl. Stroke Res. 2012, 3, 306–309. [Google Scholar] [CrossRef] [Green Version]
- Fluri, F.; Schuhmann, M.K.; Kleinschnitz, C. Animal models of ischemic stroke and their application in clinical research. Drug Des. Dev. Ther. 2015, 9, 3445–3454. [Google Scholar] [CrossRef] [Green Version]
- Sommer, C.J. Ischemic stroke: Experimental models and reality. Acta Neuropathol. 2017, 133, 245–261. [Google Scholar] [CrossRef] [Green Version]
- Hu, X.; Li, P.; Guo, Y.; Wang, H.; Leak, R.K.; Chen, S.; Gao, Y.; Chen, J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 2012, 43, 3063–3070. [Google Scholar] [CrossRef] [Green Version]
- Datta, A.; Park, J.E.; Li, X.; Zhang, H.; Ho, Z.S.; Heese, K.; Lim, S.K.; Tam, J.P.; Sze, S.K. Phenotyping of an in vitro model of ischemic penumbra by iTRAQ-based shotgun quantitative proteomics. J. Proteome Res. 2010, 9, 472–484. [Google Scholar] [CrossRef]
- Tasca, C.I.; Dal-Cim, T.; Cimarosti, H. In vitro oxygen-glucose deprivation to study ischemic cell death. Methods Mol. Biol. 2015, 1254, 197–210. [Google Scholar] [CrossRef]
- Goldberg, M.P.; Choi, D.W. Combined oxygen and glucose deprivation in cortical cell culture: Calcium-dependent and calcium-independent mechanisms of neuronal injury. J. Neurosci. Off. J. Soc. Neurosci. 1993, 13, 3510–3524. [Google Scholar] [CrossRef]
- Ryou, M.G.; Mallet, R.T. An In Vitro Oxygen-Glucose Deprivation Model for Studying Ischemia-Reperfusion Injury of Neuronal Cells. Methods Mol. Biol. 2018, 1717, 229–235. [Google Scholar] [CrossRef]
- Kaneko, Y.; Pappas, C.; Tajiri, N.; Borlongan, C.V. Oxytocin modulates GABAAR subunits to confer neuroprotection in stroke in vitro. Sci. Rep. 2016, 6, 35659. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.H.; Wan, D.; Wan, G.R.; Wang, J.H.; Zhang, J.H.; Zhu, H.F. Catalpol induces cell activity to promote axonal regeneration via the PI3K/AKT/mTOR pathway in vivo and in vitro stroke model. Ann. Transl. Med. 2019, 7, 756. [Google Scholar] [CrossRef]
- Sun, M.S.; Jin, H.; Sun, X.; Huang, S.; Zhang, F.L.; Guo, Z.N.; Yang, Y. Free Radical Damage in Ischemia-Reperfusion Injury: An Obstacle in Acute Ischemic Stroke after Revascularization Therapy. Oxid. Med. Cell. Longev. 2018, 2018, 3804979. [Google Scholar] [CrossRef]
- Arumugam, T.V.; Chan, S.L.; Jo, D.G.; Yilmaz, G.; Tang, S.C.; Cheng, A.; Gleichmann, M.; Okun, E.; Dixit, V.D.; Chigurupati, S.; et al. Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke. Nat. Med. 2006, 12, 621–623. [Google Scholar] [CrossRef]
- Kim, M.J.; Hur, J.; Ham, I.H.; Yang, H.J.; Kim, Y.; Park, S.; Cho, Y.W. Expression and activity of the na-k ATPase in ischemic injury of primary cultured astrocytes. Korean J. Physiol. Pharmacol. 2013, 17, 275–281. [Google Scholar] [CrossRef] [Green Version]
- Wevers, N.R.; Nair, A.L.; Fowke, T.M.; Pontier, M.; Kasi, D.G.; Spijkers, X.M.; Hallard, C.; Rabussier, G.; van Vught, R.; Vulto, P.; et al. Modeling ischemic stroke in a triculture neurovascular unit on-a-chip. Fluids Barriers CNS 2021, 18, 59. [Google Scholar] [CrossRef]
- Park, H.S.; Han, K.H.; Shin, J.A.; Park, J.H.; Song, K.Y.; Kim, D.H. The neuroprotective effects of carnosine in early stage of focal ischemia rodent model. J. Korean Neurosurg. Soc. 2014, 55, 125–130. [Google Scholar] [CrossRef]
- Zitta, K.; Peeters-Scholte, C.; Sommer, L.; Parczany, K.; Steinfath, M.; Albrecht, M. Insights into the neuroprotective mechanisms of 2-iminobiotin employing an in-vitro model of hypoxic-ischemic cell injury. Eur. J. Pharmacol. 2016, 792, 63–69. [Google Scholar] [CrossRef]
- Zitta, K.; Meybohm, P.; Bein, B.; Rodde, C.; Steinfath, M.; Scholz, J.; Albrecht, M. Hypoxia-induced cell damage is reduced by mild hypothermia and postconditioning with catalase in-vitro: Application of an enzyme based oxygen deficiency system. Eur. J. Pharmacol. 2010, 628, 11–18. [Google Scholar] [CrossRef]
- Mueller, S.; Millonig, G.; Waite, G.N. The GOX/CAT system: A novel enzymatic method to independently control hydrogen peroxide and hypoxia in cell culture. Adv. Med. Sci. 2009, 54, 121–135. [Google Scholar] [CrossRef] [Green Version]
- Andjelkovic, A.V.; Stamatovic, S.M.; Phillips, C.M.; Martinez-Revollar, G.; Keep, R.F. Modeling blood-brain barrier pathology in cerebrovascular disease in vitro: Current and future paradigms. Fluids Barriers CNS 2020, 17, 44. [Google Scholar] [CrossRef]
- Lyu, Z.; Park, J.; Kim, K.M.; Jin, H.J.; Wu, H.; Rajadas, J.; Kim, D.H.; Steinberg, G.K.; Lee, W. A neurovascular-unit-on-a-chip for the evaluation of the restorative potential of stem cell therapies for ischaemic stroke. Nat. Biomed. Eng. 2021, 5, 847–863. [Google Scholar] [CrossRef]
- Von Engelhardt, J.; Coserea, I.; Pawlak, V.; Fuchs, E.C.; Kohr, G.; Seeburg, P.H.; Monyer, H. Excitotoxicity in vitro by NR2A- and NR2B-containing NMDA receptors. Neuropharmacology 2007, 53, 10–17. [Google Scholar] [CrossRef]
- Vagaska, B.; Gillham, O.; Ferretti, P. Modelling human CNS injury with human neural stem cells in 2- and 3-Dimensional cultures. Sci. Rep. 2020, 10, 6785. [Google Scholar] [CrossRef] [Green Version]
- Akaneya, Y.; Enokido, Y.; Takahashi, M.; Hatanaka, H. In vitro model of hypoxia: Basic fibroblast growth factor can rescue cultured CNS neurons from oxygen-deprived cell death. J. Cereb. Blood Flow Metab. 1993, 13, 1029–1032. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, S.Y.; Hu, Y.F.; Li, W.P.; Wu, Y.M.; Ji, Z.; Wang, S.N.; Li, K.; Pan, S.Y. Intermittent hypothermia is neuroprotective in an in vitro model of ischemic stroke. Int. J. Biol. Sci. 2014, 10, 873–881. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, H.C.; Yi, T.Z.; Huang, F.G.; Wei, Y.; Luo, X.P.; Luo, Q.S. Role of long noncoding RNA MEG3/miR-378/GRB2 axis in neuronal autophagy and neurological functional impairment in ischemic stroke. J. Biol. Chem. 2020, 295, 14125–14139. [Google Scholar] [CrossRef] [PubMed]
- Le Feber, J.; Tzafi Pavlidou, S.; Erkamp, N.; van Putten, M.J.; Hofmeijer, J. Progression of Neuronal Damage in an In Vitro Model of the Ischemic Penumbra. PLoS ONE 2016, 11, e0147231. [Google Scholar] [CrossRef]
- Humpel, C. Organotypic brain slice cultures: A review. Neuroscience 2015, 305, 86–98. [Google Scholar] [CrossRef] [Green Version]
- Jorfi, M.; D’Avanzo, C.; Kim, D.Y.; Irimia, D. Three-Dimensional Models of the Human Brain Development and Diseases. Adv. Healthc. Mater. 2018, 7, 1700723. [Google Scholar] [CrossRef] [Green Version]
- Li, Q.; Han, X.; Wang, J. Organotypic Hippocampal Slices as Models for Stroke and Traumatic Brain Injury. Mol. Neurobiol. 2016, 53, 4226–4237. [Google Scholar] [CrossRef] [Green Version]
- Bonde, C.; Noraberg, J.; Noer, H.; Zimmer, J. Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation of hippocampal slice cultures. Neuroscience 2005, 136, 779–794. [Google Scholar] [CrossRef]
- Laake, J.H.; Haug, F.M.; Wieloch, T.; Ottersen, O.P. A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res. Protoc. 1999, 4, 173–184. [Google Scholar] [CrossRef]
- Noraberg, J.; Poulsen, F.R.; Blaabjerg, M.; Kristensen, B.W.; Bonde, C.; Montero, M.; Meyer, M.; Gramsbergen, J.B.; Zimmer, J. Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr. Drug Targets CNS Neurol. Disord. 2005, 4, 435–452. [Google Scholar] [CrossRef]
- Richard, M.J.; Saleh, T.M.; El Bahh, B.; Zidichouski, J.A. A novel method for inducing focal ischemia in vitro. J. Neurosci. Methods 2010, 190, 20–27. [Google Scholar] [CrossRef] [Green Version]
- Gertz, C.C.; Lui, J.H.; LaMonica, B.E.; Wang, X.; Kriegstein, A.R. Diverse behaviors of outer radial glia in developing ferret and human cortex. J. Neurosci. Off. J. Soc. Neurosci. 2014, 34, 2559–2570. [Google Scholar] [CrossRef]
- Kawaguchi, A. Neuronal Delamination and Outer Radial Glia Generation in Neocortical Development. Front. Cell Dev. Biol. 2020, 8, 623573. [Google Scholar] [CrossRef]
- Syvanen, S.; Lindhe, O.; Palner, M.; Kornum, B.R.; Rahman, O.; Langstrom, B.; Knudsen, G.M.; Hammarlund-Udenaes, M. Species differences in blood-brain barrier transport of three positron emission tomography radioligands with emphasis on P-glycoprotein transport. Drug Metab. Dispos. 2009, 37, 635–643. [Google Scholar] [CrossRef] [Green Version]
- Warren, M.S.; Zerangue, N.; Woodford, K.; Roberts, L.M.; Tate, E.H.; Feng, B.; Li, C.; Feuerstein, T.J.; Gibbs, J.; Smith, B.; et al. Comparative gene expression profiles of ABC transporters in brain microvessel endothelial cells and brain in five species including human. Pharmacol. Res. 2009, 59, 404–413. [Google Scholar] [CrossRef]
- Williams, S.M.; Sullivan, R.K.; Scott, H.L.; Finkelstein, D.I.; Colditz, P.B.; Lingwood, B.E.; Dodd, P.R.; Pow, D.V. Glial glutamate transporter expression patterns in brains from multiple mammalian species. Glia 2005, 49, 520–541. [Google Scholar] [CrossRef]
- Davalos, A.; Castillo, J.; Serena, J.; Noya, M. Duration of glutamate release after acute ischemic stroke. Stroke 1997, 28, 708–710. [Google Scholar] [CrossRef]
- Seok, J.; Warren, H.S.; Cuenca, A.G.; Mindrinos, M.N.; Baker, H.V.; Xu, W.; Richards, D.R.; McDonald-Smith, G.P.; Gao, H.; Hennessy, L.; et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 2013, 110, 3507–3512. [Google Scholar] [CrossRef] [Green Version]
- Smith, A.M.; Dragunow, M. The human side of microglia. Trends Neurosci. 2014, 37, 125–135. [Google Scholar] [CrossRef]
- Sharp, F.R.; Jickling, G.C. Modeling immunity and inflammation in stroke: Differences between rodents and humans? Stroke 2014, 45, e179–e180. [Google Scholar] [CrossRef] [Green Version]
- Du, Y.; Deng, W.; Wang, Z.; Ning, M.; Zhang, W.; Zhou, Y.; Lo, E.H.; Xing, C. Differential subnetwork of chemokines/cytokines in human, mouse, and rat brain cells after oxygen-glucose deprivation. J. Cereb. Blood Flow Metab. 2017, 37, 1425–1434. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chang, R.; Algird, A.; Bau, C.; Rathbone, M.P.; Jiang, S. Neuroprotective effects of guanosine on stroke models In Vitro and In Vivo. Neurosci. Lett. 2008, 431, 101–105. [Google Scholar] [CrossRef] [PubMed]
- Lorenz, L.; Dang, J.; Misiak, M.; Tameh Abolfazl, A.; Beyer, C.; Kipp, M. Combined 17beta-oestradiol and progesterone treatment prevents neuronal cell injury in cortical but not midbrain neurones or neuroblastoma cells. J. Neuroendocrinol. 2009, 21, 841–849. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Eaton, E.D.; Wills, T.E.; McCann, S.K.; Antonic, A.; Howells, D.W. Human Ischaemic Cascade Studies Using SH-SY5Y Cells: A Systematic Review and Meta-Analysis. Transl. Stroke Res. 2018, 9, 564–574. [Google Scholar] [CrossRef] [Green Version]
- Marcoli, M.; Bonfanti, A.; Roccatagliata, P.; Chiaramonte, G.; Ongini, E.; Raiteri, M.; Maura, G. Glutamate efflux from human cerebrocortical slices during ischemia: Vesicular-like mode of glutamate release and sensitivity to A(2A) adenosine receptor blockade. Neuropharmacology 2004, 47, 884–891. [Google Scholar] [CrossRef]
- Marcoli, M.; Cervetto, C.; Castagnetta, M.; Sbaffi, P.; Maura, G. 5-HT control of ischemia-evoked glutamate efflux from human cerebrocortical slices. Neurochem. Int. 2004, 45, 687–691. [Google Scholar] [CrossRef]
- Werth, J.L.; Park, T.S.; Silbergeld, D.L.; Rothman, S.M. Excitotoxic swelling occurs in oxygen and glucose deprived human cortical slices. Brain Res. 1998, 782, 248–254. [Google Scholar] [CrossRef]
- Mitsios, N.; Gaffney, J.; Krupinski, J.; Mathias, R.; Wang, Q.; Hayward, S.; Rubio, F.; Kumar, P.; Kumar, S.; Slevin, M. Expression of signaling molecules associated with apoptosis in human ischemic stroke tissue. Cell Biochem. Biophys. 2007, 47, 73–86. [Google Scholar] [CrossRef]
- Mitsios, N.; Saka, M.; Krupinski, J.; Pennucci, R.; Sanfeliu, C.; Wang, Q.; Rubio, F.; Gaffney, J.; Kumar, P.; Kumar, S.; et al. A microarray study of gene and protein regulation in human and rat brain following middle cerebral artery occlusion. BMC Neurosci. 2007, 8, 93. [Google Scholar] [CrossRef] [Green Version]
- Mitsios, N.; Pennucci, R.; Krupinski, J.; Sanfeliu, C.; Gaffney, J.; Kumar, P.; Kumar, S.; Juan-Babot, O.; Slevin, M. Expression of cyclin-dependent kinase 5 mRNA and protein in the human brain following acute ischemic stroke. Brain Pathol. 2007, 17, 11–23. [Google Scholar] [CrossRef]
- Liu, Y. Human In Vitro Models of Ischaemic Stroke: New Strategies for Neuroprotection. Ph.D. Thesis, University of Melbourn, Melbourn, Australia, 2018. [Google Scholar]
- Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131, 861–872. [Google Scholar] [CrossRef] [Green Version]
- Staerk, J.; Dawlaty, M.M.; Gao, Q.; Maetzel, D.; Hanna, J.; Sommer, C.A.; Mostoslavsky, G.; Jaenisch, R. Reprogramming of human peripheral blood cells to induced pluripotent stem cells. Cell Stem Cell 2010, 7, 20–24. [Google Scholar] [CrossRef] [Green Version]
- Lippmann, E.S.; Azarin, S.M.; Kay, J.E.; Nessler, R.A.; Wilson, H.K.; Al-Ahmad, A.; Palecek, S.P.; Shusta, E.V. Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat. Biotechnol. 2012, 30, 783–791. [Google Scholar] [CrossRef]
- Tcw, J.; Wang, M.; Pimenova, A.A.; Bowles, K.R.; Hartley, B.J.; Lacin, E.; Machlovi, S.I.; Abdelaal, R.; Karch, C.M.; Phatnani, H.; et al. An Efficient Platform for Astrocyte Differentiation from Human Induced Pluripotent Stem Cells. Stem Cell Rep. 2017, 9, 600–614. [Google Scholar] [CrossRef] [Green Version]
- Gunhanlar, N.; Shpak, G.; van der Kroeg, M.; Gouty-Colomer, L.A.; Munshi, S.T.; Lendemeijer, B.; Ghazvini, M.; Dupont, C.; Hoogendijk, W.J.G.; Gribnau, J.; et al. A simplified protocol for differentiation of electrophysiologically mature neuronal networks from human induced pluripotent stem cells. Mol. Psychiatry 2018, 23, 1336–1344. [Google Scholar] [CrossRef] [Green Version]
- Gonzalez, R.; Garitaonandia, I.; Abramihina, T.; Wambua, G.K.; Ostrowska, A.; Brock, M.; Noskov, A.; Boscolo, F.S.; Craw, J.S.; Laurent, L.C.; et al. Deriving dopaminergic neurons for clinical use. A practical approach. Sci. Rep. 2013, 3, 1463. [Google Scholar] [CrossRef] [Green Version]
- Abud, E.M.; Ramirez, R.N.; Martinez, E.S.; Healy, L.M.; Nguyen, C.H.H.; Newman, S.A.; Yeromin, A.V.; Scarfone, V.M.; Marsh, S.E.; Fimbres, C.; et al. iPSC-Derived Human Microglia-like Cells to Study Neurological Diseases. Neuron 2017, 94, 278–293.e9. [Google Scholar] [CrossRef] [Green Version]
- Haenseler, W.; Sansom, S.N.; Buchrieser, J.; Newey, S.E.; Moore, C.S.; Nicholls, F.J.; Chintawar, S.; Schnell, C.; Antel, J.P.; Allen, N.D.; et al. A Highly Efficient Human Pluripotent Stem Cell Microglia Model Displays a Neuronal-Co-culture-Specific Expression Profile and Inflammatory Response. Stem Cell Rep. 2017, 8, 1727–1742. [Google Scholar] [CrossRef] [Green Version]
- McQuade, A.; Coburn, M.; Tu, C.H.; Hasselmann, J.; Davtyan, H.; Blurton-Jones, M. Development and validation of a simplified method to generate human microglia from pluripotent stem cells. Mol. Neurodegener. 2018, 13, 67. [Google Scholar] [CrossRef]
- Konttinen, H.; Cabral-da-Silva, M.E.C.; Ohtonen, S.; Wojciechowski, S.; Shakirzyanova, A.; Caligola, S.; Giugno, R.; Ishchenko, Y.; Hernandez, D.; Fazaludeen, M.F.; et al. PSEN1DeltaE9, APPswe, and APOE4 Confer Disparate Phenotypes in Human iPSC-Derived Microglia. Stem Cell Rep. 2019, 13, 669–683. [Google Scholar] [CrossRef] [Green Version]
- Muffat, J.; Li, Y.; Yuan, B.; Mitalipova, M.; Omer, A.; Corcoran, S.; Bakiasi, G.; Tsai, L.H.; Aubourg, P.; Ransohoff, R.M.; et al. Efficient derivation of microglia-like cells from human pluripotent stem cells. Nat. Med. 2016, 22, 1358–1367. [Google Scholar] [CrossRef] [Green Version]
- Krencik, R.; Zhang, S.C. Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat. Protoc. 2011, 6, 1710–1717. [Google Scholar] [CrossRef] [Green Version]
- Shaltouki, A.; Peng, J.; Liu, Q.; Rao, M.S.; Zeng, X. Efficient generation of astrocytes from human pluripotent stem cells in defined conditions. Stem Cells 2013, 31, 941–952. [Google Scholar] [CrossRef]
- Shi, Y.; Kirwan, P.; Livesey, F.J. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat. Protoc. 2012, 7, 1836–1846. [Google Scholar] [CrossRef]
- Yan, Y.; Shin, S.; Jha, B.S.; Liu, Q.; Sheng, J.; Li, F.; Zhan, M.; Davis, J.; Bharti, K.; Zeng, X.; et al. Efficient and rapid derivation of primitive neural stem cells and generation of brain subtype neurons from human pluripotent stem cells. Stem Cells Transl. Med. 2013, 2, 862–870. [Google Scholar] [CrossRef]
- Ehrlich, M.; Mozafari, S.; Glatza, M.; Starost, L.; Velychko, S.; Hallmann, A.L.; Cui, Q.L.; Schambach, A.; Kim, K.P.; Bachelin, C.; et al. Rapid and efficient generation of oligodendrocytes from human induced pluripotent stem cells using transcription factors. Proc. Natl. Acad. Sci. USA 2017, 114, E2243–E2252. [Google Scholar] [CrossRef] [Green Version]
- Juntunen, M.; Hagman, S.; Moisan, A.; Narkilahti, S.; Miettinen, S. In Vitro Oxygen-Glucose Deprivation-Induced Stroke Models with Human Neuroblastoma Cell- and Induced Pluripotent Stem Cell-Derived Neurons. Stem Cells Int. 2020, 2020, 8841026. [Google Scholar] [CrossRef]
- Patel, R.; Page, S.; Al-Ahmad, A.J. Isogenic blood-brain barrier models based on patient-derived stem cells display inter-individual differences in cell maturation and functionality. J. Neurochem. 2017, 142, 74–88. [Google Scholar] [CrossRef]
- DeStefano, J.G.; Xu, Z.S.; Williams, A.J.; Yimam, N.; Searson, P.C. Effect of shear stress on iPSC-derived human brain microvascular endothelial cells (dhBMECs). Fluids Barriers CNS 2017, 14, 20. [Google Scholar] [CrossRef] [Green Version]
- Linville, R.M.; DeStefano, J.G.; Sklar, M.B.; Xu, Z.; Farrell, A.M.; Bogorad, M.I.; Chu, C.; Walczak, P.; Cheng, L.; Mahairaki, V.; et al. Human iPSC-derived blood-brain barrier microvessels: Validation of barrier function and endothelial cell behavior. Biomaterials 2019, 190–191, 24–37. [Google Scholar] [CrossRef]
- Nikolakopoulou, P.; Rauti, R.; Voulgaris, D.; Shlomy, I.; Maoz, B.M.; Herland, A. Recent progress in translational engineered in vitro models of the central nervous system. Brain 2020, 143, 3181–3213. [Google Scholar] [CrossRef] [PubMed]
- Mukda, S.; Tsai, C.Y.; Leu, S.; Yang, J.L.; Chan, S.H.H. Pinin protects astrocytes from cell death after acute ischemic stroke via maintenance of mitochondrial anti-apoptotic and bioenergetics functions. J. Biomed. Sci. 2019, 26, 43. [Google Scholar] [CrossRef] [PubMed]
- Sun, X.; Jung, J.H.; Arvola, O.; Santoso, M.R.; Giffard, R.G.; Yang, P.C.; Stary, C.M. Stem Cell-Derived Exosomes Protect Astrocyte Cultures from In Vitro Ischemia and Decrease Injury as Post-stroke Intravenous Therapy. Front. Cell. Neurosci. 2019, 13, 394. [Google Scholar] [CrossRef] [PubMed]
- Alluri, H.; Anasooya Shaji, C.; Davis, M.L.; Tharakan, B. Oxygen-glucose deprivation and reoxygenation as an in vitro ischemia-reperfusion injury model for studying blood-brain barrier dysfunction. J. Vis. Exp. JoVE 2015, 99, e52699. [Google Scholar] [CrossRef] [Green Version]
- Xu, J.; He, L.; Ahmed, S.H.; Chen, S.W.; Goldberg, M.P.; Beckman, J.S.; Hsu, C.Y. Oxygen-glucose deprivation induces inducible nitric oxide synthase and nitrotyrosine expression in cerebral endothelial cells. Stroke 2000, 31, 1744–1751. [Google Scholar] [CrossRef] [Green Version]
- Salvador, E.; Burek, M.; Forster, C.Y. Stretch and/or oxygen glucose deprivation (OGD) in an in vitro traumatic brain injury (TBI) model induces calcium alteration and inflammatory cascade. Front. Cell. Neurosci. 2015, 9, 323. [Google Scholar] [CrossRef]
- Itoh, Y.; Takaoka, R.; Ohira, M.; Abe, T.; Tanahashi, N.; Suzuki, N. Reactive oxygen species generated by mitochondrial injury in human brain microvessel endothelial cells. Clin. Hemorheol. Microcirc. 2006, 34, 163–168. [Google Scholar]
- Kokubu, Y.; Yamaguchi, T.; Kawabata, K. In Vitro model of cerebral ischemia by using brain microvascular endothelial cells derived from human induced pluripotent stem cells. Biochem. Biophys. Res. Commun. 2017, 486, 577–583. [Google Scholar] [CrossRef]
- Chen, J.; Sun, L.; Ding, G.B.; Chen, L.; Jiang, L.; Wang, J.; Wu, J. Oxygen-Glucose Deprivation/Reoxygenation Induces Human Brain Microvascular Endothelial Cell Hyperpermeability Via VE-Cadherin Internalization: Roles of RhoA/ROCK2. J. Mol. Neurosci. 2019, 69, 49–59. [Google Scholar] [CrossRef]
- Neuhaus, W.; Burek, M.; Djuzenova, C.S.; Thal, S.C.; Koepsell, H.; Roewer, N.; Forster, C.Y. Addition of NMDA-receptor antagonist MK801 during oxygen/glucose deprivation moderately attenuates the upregulation of glucose uptake after subsequent reoxygenation in brain endothelial cells. Neurosci. Lett. 2012, 506, 44–49. [Google Scholar] [CrossRef] [Green Version]
- Pannasch, U.; Vargova, L.; Reingruber, J.; Ezan, P.; Holcman, D.; Giaume, C.; Sykova, E.; Rouach, N. Astroglial networks scale synaptic activity and plasticity. Proc. Natl. Acad. Sci. USA 2011, 108, 8467–8472. [Google Scholar] [CrossRef] [Green Version]
- Rouach, N.; Koulakoff, A.; Abudara, V.; Willecke, K.; Giaume, C. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 2008, 322, 1551–1555. [Google Scholar] [CrossRef]
- Chandrasekaran, A.; Avci, H.X.; Leist, M.; Kobolak, J.; Dinnyes, A. Astrocyte Differentiation of Human Pluripotent Stem Cells: New Tools for Neurological Disorder Research. Front. Cell. Neurosci. 2016, 10, 215. [Google Scholar] [CrossRef] [Green Version]
- Kuijlaars, J.; Oyelami, T.; Diels, A.; Rohrbacher, J.; Versweyveld, S.; Meneghello, G.; Tuefferd, M.; Verstraelen, P.; Detrez, J.R.; Verschuuren, M.; et al. Sustained synchronized neuronal network activity in a human astrocyte co-culture system. Sci. Rep. 2016, 6, 36529. [Google Scholar] [CrossRef] [Green Version]
- Tang, X.; Zhou, L.; Wagner, A.M.; Marchetto, M.C.; Muotri, A.R.; Gage, F.H.; Chen, G. Astroglial cells regulate the developmental timeline of human neurons differentiated from induced pluripotent stem cells. Stem Cell Res. 2013, 11, 743–757. [Google Scholar] [CrossRef] [Green Version]
- Odawara, A.; Saitoh, Y.; Alhebshi, A.H.; Gotoh, M.; Suzuki, I. Long-term electrophysiological activity and pharmacological response of a human induced pluripotent stem cell-derived neuron and astrocyte co-culture. Biochem. Biophys. Res. Commun. 2014, 443, 1176–1181. [Google Scholar] [CrossRef] [Green Version]
- Johnson, M.A.; Weick, J.P.; Pearce, R.A.; Zhang, S.C. Functional neural development from human embryonic stem cells: Accelerated synaptic activity via astrocyte coculture. J. Neurosci. Off. J. Soc. Neurosci. 2007, 27, 3069–3077. [Google Scholar] [CrossRef] [Green Version]
- Kierdorf, K.; Prinz, M. Microglia in steady state. J. Clin. Investig. 2017, 127, 3201–3209. [Google Scholar] [CrossRef] [Green Version]
- Haenseler, W.; Rajendran, L. Concise Review: Modeling Neurodegenerative Diseases with Human Pluripotent Stem Cell-Derived Microglia. Stem Cells 2019, 37, 724–730. [Google Scholar] [CrossRef] [Green Version]
- De Vocht, N.; Praet, J.; Reekmans, K.; Le Blon, D.; Hoornaert, C.; Daans, J.; Berneman, Z.; Van der Linden, A.; Ponsaerts, P. Tackling the physiological barriers for successful mesenchymal stem cell transplantation into the central nervous system. Stem Cell Res. Ther. 2013, 4, 101. [Google Scholar] [CrossRef] [Green Version]
- Blanchette, M.; Daneman, R. Formation and maintenance of the BBB. Mech. Dev. 2015, 138 Pt 1, 8–16. [Google Scholar] [CrossRef]
- Janzer, R.C.; Raff, M.C. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 1987, 325, 253–257. [Google Scholar] [CrossRef]
- Sivandzade, F.; Cucullo, L. In-Vitro blood-brain barrier modeling: A review of modern and fast-advancing technologies. J. Cereb. Blood Flow Metab. 2018, 38, 1667–1681. [Google Scholar] [CrossRef]
- Nzou, G.; Wicks, R.T.; Wicks, E.E.; Seale, S.A.; Sane, C.H.; Chen, A.; Murphy, S.V.; Jackson, J.D.; Atala, A.J. Human Cortex Spheroid with a Functional Blood Brain Barrier for High-Throughput Neurotoxicity Screening and Disease Modeling. Sci. Rep. 2018, 8, 7413. [Google Scholar] [CrossRef] [Green Version]
- Desestret, V.; Riou, A.; Chauveau, F.; Cho, T.H.; Devillard, E.; Marinescu, M.; Ferrera, R.; Rey, C.; Chanal, M.; Angoulvant, D.; et al. In vitro and in vivo models of cerebral ischemia show discrepancy in therapeutic effects of M2 macrophages. PLoS ONE 2013, 8, e67063. [Google Scholar] [CrossRef]
- Kaushal, V.; Schlichter, L.C. Mechanisms of microglia-mediated neurotoxicity in a new model of the stroke penumbra. J. Neurosci. Off. J. Soc. Neurosci. 2008, 28, 2221–2230. [Google Scholar] [CrossRef]
- Lai, A.Y.; Todd, K.G. Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 2008, 56, 259–270. [Google Scholar] [CrossRef]
- Mai, N.; Prifti, V.; Kim, M.; Halterman, M.W. Characterization of neutrophil-neuronal co-cultures to investigate mechanisms of post-ischemic immune-mediated neurotoxicity. J. Neurosci. Methods 2020, 341, 108782. [Google Scholar] [CrossRef]
- Chaitanya, G.V.; Minagar, A.; Alexander, J.S. Neuronal and astrocytic interactions modulate brain endothelial properties during metabolic stresses of in vitro cerebral ischemia. Cell Commun. Signal. 2014, 12, 7. [Google Scholar] [CrossRef] [Green Version]
- Shindo, A.; Maki, T.; Mandeville, E.T.; Liang, A.C.; Egawa, N.; Itoh, K.; Itoh, N.; Borlongan, M.; Holder, J.C.; Chuang, T.T.; et al. Astrocyte-Derived Pentraxin 3 Supports Blood-Brain Barrier Integrity under Acute Phase of Stroke. Stroke 2016, 47, 1094–1100. [Google Scholar] [CrossRef]
- Von Bartheld, C.S.; Bahney, J.; Herculano-Houzel, S. The search for true numbers of neurons and glial cells in the human brain: A review of 150 years of cell counting. J. Comp. Neurol. 2016, 524, 3865–3895. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ryu, S.; Kwon, J.; Park, H.; Choi, I.Y.; Hwang, S.; Gajulapati, V.; Lee, J.Y.; Choi, Y.; Varani, K.; Borea, P.A.; et al. Amelioration of Cerebral Ischemic Injury by a Synthetic Seco-nucleoside LMT497. Exp. Neurobiol. 2015, 24, 31–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Centeno, E.G.Z.; Cimarosti, H.; Bithell, A. 2D versus 3D human induced pluripotent stem cell-derived cultures for neurodegenerative disease modelling. Mol. Neurodegener. 2018, 13, 27. [Google Scholar] [CrossRef] [PubMed]
- Rothenbucher, T.S.P.; Martinez-Serrano, A. Human cerebral organoids and neural 3D tissues in basic research, and their application to study neurological diseases. Future Neurol. 2019, 14, FNL3. [Google Scholar] [CrossRef] [Green Version]
- Kelava, I.; Lancaster, M.A. Dishing out mini-brains: Current progress and future prospects in brain organoid research. Dev. Biol. 2016, 420, 199–209. [Google Scholar] [CrossRef] [Green Version]
- Gong, J.; Meng, T.; Yang, J.; Hu, N.; Zhao, H.; Tian, T. Three-dimensional in vitro tissue culture models of brain organoids. Exp. Neurol. 2021, 339, 113619. [Google Scholar] [CrossRef]
- Brawner, A.T.; Xu, R.; Liu, D.; Jiang, P. Generating CNS organoids from human induced pluripotent stem cells for modeling neurological disorders. Int. J. Physiol. Pathophysiol. Pharmacol. 2017, 9, 101–111. [Google Scholar]
- Pasca, A.M.; Sloan, S.A.; Clarke, L.E.; Tian, Y.; Makinson, C.D.; Huber, N.; Kim, C.H.; Park, J.Y.; O’Rourke, N.A.; Nguyen, K.D.; et al. Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat. Methods 2015, 12, 671–678. [Google Scholar] [CrossRef] [Green Version]
- Lancaster, M.A.; Knoblich, J.A. Generation of cerebral organoids from human pluripotent stem cells. Nat. Protoc. 2014, 9, 2329–2340. [Google Scholar] [CrossRef] [Green Version]
- Lancaster, M.A.; Renner, M.; Martin, C.A.; Wenzel, D.; Bicknell, L.S.; Hurles, M.E.; Homfray, T.; Penninger, J.M.; Jackson, A.P.; Knoblich, J.A. Cerebral organoids model human brain development and microcephaly. Nature 2013, 501, 373–379. [Google Scholar] [CrossRef]
- Pamies, D.; Barreras, P.; Block, K.; Makri, G.; Kumar, A.; Wiersma, D.; Smirnova, L.; Zang, C.; Bressler, J.; Christian, K.M.; et al. A human brain microphysiological system derived from induced pluripotent stem cells to study neurological diseases and toxicity. Altex 2017, 34, 362–376. [Google Scholar] [CrossRef] [Green Version]
- Jo, J.; Xiao, Y.; Sun, A.X.; Cukuroglu, E.; Tran, H.D.; Goke, J.; Tan, Z.Y.; Saw, T.Y.; Tan, C.P.; Lokman, H.; et al. Midbrain-like Organoids from Human Pluripotent Stem Cells Contain Functional Dopaminergic and Neuromelanin-Producing Neurons. Cell Stem Cell 2016, 19, 248–257. [Google Scholar] [CrossRef] [Green Version]
- Muguruma, K.; Nishiyama, A.; Kawakami, H.; Hashimoto, K.; Sasai, Y. Self-organization of polarized cerebellar tissue in 3D culture of human pluripotent stem cells. Cell Rep. 2015, 10, 537–550. [Google Scholar] [CrossRef] [Green Version]
- Sakaguchi, H.; Kadoshima, T.; Soen, M.; Narii, N.; Ishida, Y.; Ohgushi, M.; Takahashi, J.; Eiraku, M.; Sasai, Y. Generation of functional hippocampal neurons from self-organizing human embryonic stem cell-derived dorsomedial telencephalic tissue. Nat. Commun. 2015, 6, 8896. [Google Scholar] [CrossRef] [Green Version]
- Qian, X.; Nguyen, H.N.; Song, M.M.; Hadiono, C.; Ogden, S.C.; Hammack, C.; Yao, B.; Hamersky, G.R.; Jacob, F.; Zhong, C.; et al. Brain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure. Cell 2016, 165, 1238–1254. [Google Scholar] [CrossRef] [Green Version]
- Huang, W.K.; Wong, S.Z.H.; Pather, S.R.; Nguyen, P.T.T.; Zhang, F.; Zhang, D.Y.; Zhang, Z.; Lu, L.; Fang, W.; Chen, L.; et al. Generation of hypothalamic arcuate organoids from human induced pluripotent stem cells. Cell Stem Cell 2021, 28, 1657–1670.e10. [Google Scholar] [CrossRef]
- Mariani, J.; Coppola, G.; Zhang, P.; Abyzov, A.; Provini, L.; Tomasini, L.; Amenduni, M.; Szekely, A.; Palejev, D.; Wilson, M.; et al. FOXG1-Dependent Dysregulation of GABA/Glutamate Neuron Differentiation in Autism Spectrum Disorders. Cell 2015, 162, 375–390. [Google Scholar] [CrossRef] [Green Version]
- Dang, J.; Tiwari, S.K.; Lichinchi, G.; Qin, Y.; Patil, V.S.; Eroshkin, A.M.; Rana, T.M. Zika Virus Depletes Neural Progenitors in Human Cerebral Organoids through Activation of the Innate Immune Receptor TLR3. Cell Stem Cell 2016, 19, 258–265. [Google Scholar] [CrossRef] [Green Version]
- Garcez, P.P.; Loiola, E.C.; Madeiro da Costa, R.; Higa, L.M.; Trindade, P.; Delvecchio, R.; Nascimento, J.M.; Brindeiro, R.; Tanuri, A.; Rehen, S.K. Zika virus impairs growth in human neurospheres and brain organoids. Science 2016, 352, 816–818. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.K.; Velazquez Sanchez, C.; Chen, M.; Morin, P.J.; Wells, J.M.; Hanlon, E.B.; Xia, W. Three Dimensional Human Neuro-Spheroid Model of Alzheimer’s Disease Based on Differentiated Induced Pluripotent Stem Cells. PLoS ONE 2016, 11, e0163072. [Google Scholar] [CrossRef] [Green Version]
- Raja, W.K.; Mungenast, A.E.; Lin, Y.T.; Ko, T.; Abdurrob, F.; Seo, J.; Tsai, L.H. Self-Organizing 3D Human Neural Tissue Derived from Induced Pluripotent Stem Cells Recapitulate Alzheimer’s Disease Phenotypes. PLoS ONE 2016, 11, e0161969. [Google Scholar] [CrossRef] [Green Version]
- Leite, P.E.C.; Pereira, M.R.; Harris, G.; Pamies, D.; Dos Santos, L.M.G.; Granjeiro, J.M.; Hogberg, H.T.; Hartung, T.; Smirnova, L. Suitability of 3D human brain spheroid models to distinguish toxic effects of gold and poly-lactic acid nanoparticles to assess biocompatibility for brain drug delivery. Part. Fibre Toxicol. 2019, 16, 22. [Google Scholar] [CrossRef]
- Zeng, Y.; Win-Shwe, T.T.; Ito, T.; Sone, H. A three-dimensional neurosphere system using human stem cells for nanotoxicology studies. In Organoids and Mini-Organs; Academic Press: Cambridge, MA, USA, 2018. [Google Scholar]
- Lee, C.T.; Bendriem, R.M.; Wu, W.W.; Shen, R.F. 3D brain Organoids derived from pluripotent stem cells: Promising experimental models for brain development and neurodegenerative disorders. J. Biomed. Sci. 2017, 24, 59. [Google Scholar] [CrossRef] [Green Version]
- Hartley, B.J.; Brennand, K.J. Neural organoids for disease phenotyping, drug screening and developmental biology studies. Neurochem. Int. 2017, 106, 85–93. [Google Scholar] [CrossRef]
- Cakir, B.; Xiang, Y.; Tanaka, Y.; Kural, M.H.; Parent, M.; Kang, Y.J.; Chapeton, K.; Patterson, B.; Yuan, Y.; He, C.S.; et al. Engineering of human brain organoids with a functional vascular-like system. Nat. Methods 2019, 16, 1169–1175. [Google Scholar] [CrossRef]
- Shi, Y.; Sun, L.; Wang, M.; Liu, J.; Zhong, S.; Li, R.; Li, P.; Guo, L.; Fang, A.; Chen, R.; et al. Vascularized human cortical organoids (vOrganoids) model cortical development in vivo. PLoS Biol. 2020, 18, e3000705. [Google Scholar] [CrossRef]
- Kook, M.G.; Lee, S.E.; Shin, N.; Kong, D.; Kim, D.H.; Kim, M.S.; Kang, H.K.; Choi, S.W.; Kang, K.S. Generation of Cortical Brain Organoid with Vascularization by Assembling with Vascular Spheroid. Int. J. Stem Cells 2022, 15, 85–94. [Google Scholar] [CrossRef]
- Ginhoux, F.; Prinz, M. Origin of microglia: Current concepts and past controversies. Cold Spring Harb. Perspect. Biol. 2015, 7, a020537. [Google Scholar] [CrossRef] [Green Version]
- Fagerlund, I.; Dougalis, A.; Shakirzyanova, A.; Gomez-Budia, M.; Pelkonen, A.; Konttinen, H.; Ohtonen, S.; Fazaludeen, M.F.; Koskuvi, M.; Kuusisto, J.; et al. Microglia-like Cells Promote Neuronal Functions in Cerebral Organoids. Cells 2021, 11, 124. [Google Scholar] [CrossRef]
- Xu, R.; Boreland, A.J.; Li, X.; Erickson, C.; Jin, M.; Atkins, C.; Pang, Z.P.; Daniels, B.P.; Jiang, P. Developing human pluripotent stem cell-based cerebral organoids with a controllable microglia ratio for modeling brain development and pathology. Stem Cell Rep. 2021, 16, 1923–1937. [Google Scholar] [CrossRef]
- Abreu, C.M.; Gama, L.; Krasemann, S.; Chesnut, M.; Odwin-Dacosta, S.; Hogberg, H.T.; Hartung, T.; Pamies, D. Microglia Increase Inflammatory Responses in iPSC-Derived Human BrainSpheres. Front. Microbiol. 2018, 9, 2766. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Wang, S.N.; Xu, T.Y.; Miao, Z.W.; Su, D.F.; Miao, C.Y. Organoid technology for brain and therapeutics research. CNS Neurosci. Ther. 2017, 23, 771–778. [Google Scholar] [CrossRef] [PubMed]
- Koo, B.; Choi, B.; Park, H.; Yoon, K.J. Past, Present, and Future of Brain Organoid Technology. Mol. Cells 2019, 42, 617–627. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.S.; Kim, D.H.; Kang, H.K.; Kook, M.G.; Choi, S.W.; Kang, K.S. Modeling of Hypoxic Brain Injury through 3D Human Neural Organoids. Cells 2021, 10, 234. [Google Scholar] [CrossRef] [PubMed]
- Daviaud, N.; Chevalier, C.; Friedel, R.H.; Zou, H. Distinct Vulnerability and Resilience of Human Neuroprogenitor Subtypes in Cerebral Organoid Model of Prenatal Hypoxic Injury. Front. Cell. Neurosci. 2019, 13, 336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Breedam, E.; Nijak, A.; Buyle-Huybrecht, T.; Di Stefano, J.; Boeren, M.; Govaerts, J.; Quarta, A.; Swartenbroekx, T.; Jacobs, E.Z.; Menten, B.; et al. Luminescent Human iPSC-Derived Neurospheroids Enable Modeling of Neurotoxicity after Oxygen-glucose Deprivation. Neurotherapeutics 2022, 2, 550–569. [Google Scholar] [CrossRef] [PubMed]
- Iwasa, N.; Matsui, T.K.; Iguchi, N.; Kinugawa, K.; Morikawa, N.; Sakaguchi, Y.M.; Shiota, T.; Kobashigawa, S.; Nakanishi, M.; Matsubayashi, M.; et al. Gene Expression Profiles of Human Cerebral Organoids Identify PPAR Pathway and PKM2 as Key Markers for Oxygen-Glucose Deprivation and Reoxygenation. Front. Cell. Neurosci. 2021, 15, 605030. [Google Scholar] [CrossRef]
- Ko, E.; Poon, M.L.S.; Park, E.; Cho, Y.; Shin, J.H. Engineering 3D Cortical Spheroids for an In Vitro Ischemic Stroke Model. ACS Biomater. Sci. Eng. 2021, 7, 3845–3860. [Google Scholar] [CrossRef]
- Lin, C.H.; Nicol, C.J.B.; Cheng, Y.C.; Yen, C.; Wang, Y.S.; Chiang, M.C. Neuroprotective effects of resveratrol against oxygen glucose deprivation induced mitochondrial dysfunction by activation of AMPK in SH-SY5Y cells with 3D gelatin scaffold. Brain Res. 2020, 1726, 146492. [Google Scholar] [CrossRef]
- Bokhari, M.; Carnachan, R.J.; Cameron, N.R.; Przyborski, S.A. Culture of HepG2 liver cells on three dimensional polystyrene scaffolds enhances cell structure and function during toxicological challenge. J. Anat. 2007, 211, 567–576. [Google Scholar] [CrossRef]
- Van Duinen, V.; Trietsch, S.J.; Joore, J.; Vulto, P.; Hankemeier, T. Microfluidic 3D cell culture: From tools to tissue models. Curr. Opin. Biotechnol. 2015, 35, 118–126. [Google Scholar] [CrossRef] [Green Version]
- Shin, H.S.; Kim, H.J.; Min, S.K.; Kim, S.H.; Lee, B.M.; Jeon, N.L. Compartmental culture of embryonic stem cell-derived neurons in microfluidic devices for use in axonal biology. Biotechnol. Lett. 2010, 32, 1063–1070. [Google Scholar] [CrossRef]
- Taylor, A.M.; Dieterich, D.C.; Ito, H.T.; Kim, S.A.; Schuman, E.M. Microfluidic local perfusion chambers for the visualization and manipulation of synapses. Neuron 2010, 66, 57–68. [Google Scholar] [CrossRef] [Green Version]
- Coquinco, A.; Kojic, L.; Wen, W.; Wang, Y.T.; Jeon, N.L.; Milnerwood, A.J.; Cynader, M. A microfluidic based in vitro model of synaptic competition. Mol. Cell. Neurosci. 2014, 60, 43–52. [Google Scholar] [CrossRef]
- Taylor, A.M.; Blurton-Jones, M.; Rhee, S.W.; Cribbs, D.H.; Cotman, C.W.; Jeon, N.L. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2005, 2, 599–605. [Google Scholar] [CrossRef]
- Park, J.; Koito, H.; Li, J.; Han, A. Microfluidic compartmentalized co-culture platform for CNS axon myelination research. Biomed. Microdevices 2009, 11, 1145–1153. [Google Scholar] [CrossRef] [Green Version]
- Samson, A.J.; Robertson, G.; Zagnoni, M.; Connolly, C.N. Neuronal networks provide rapid neuroprotection against spreading toxicity. Sci. Rep. 2016, 6, 33746. [Google Scholar] [CrossRef] [Green Version]
- Demers, C.J.; Soundararajan, P.; Chennampally, P.; Cox, G.A.; Briscoe, J.; Collins, S.D.; Smith, R.L. Development-on-chip: In vitro neural tube patterning with a microfluidic device. Development 2016, 143, 1884–1892. [Google Scholar] [CrossRef] [Green Version]
- Park, J.Y.; Kim, S.K.; Woo, D.H.; Lee, E.J.; Kim, J.H.; Lee, S.H. Differentiation of neural progenitor cells in a microfluidic chip-generated cytokine gradient. Stem Cells 2009, 27, 2646–2654. [Google Scholar] [CrossRef] [Green Version]
- Uzel, S.G.; Amadi, O.C.; Pearl, T.M.; Lee, R.T.; So, P.T.; Kamm, R.D. Simultaneous or Sequential Orthogonal Gradient Formation in a 3D Cell Culture Microfluidic Platform. Small 2016, 12, 612–622. [Google Scholar] [CrossRef] [Green Version]
- Mauleon, G.; Fall, C.P.; Eddington, D.T. Precise spatial and temporal control of oxygen within in vitro brain slices via microfluidic gas channels. PLoS ONE 2012, 7, e43309. [Google Scholar] [CrossRef] [Green Version]
- Oppegard, S.C.; Nam, K.H.; Carr, J.R.; Skaalure, S.C.; Eddington, D.T. Modulating temporal and spatial oxygenation over adherent cellular cultures. PLoS ONE 2009, 4, e6891. [Google Scholar] [CrossRef]
- Adler, M.; Polinkovsky, M.; Gutierrez, E.; Groisman, A. Generation of oxygen gradients with arbitrary shapes in a microfluidic device. Lab Chip 2010, 10, 388–391. [Google Scholar] [CrossRef] [Green Version]
- Lo, J.F.; Sinkala, E.; Eddington, D.T. Oxygen gradients for open well cellular cultures via microfluidic substrates. Lab Chip 2010, 10, 2394–2401. [Google Scholar] [CrossRef] [Green Version]
- Liu, P.; Fu, L.; Song, Z.; Man, M.; Yuan, H.; Zheng, X.; Kang, Q.; Shen, D.; Song, J.; Li, B.; et al. Three dimensionally printed nitrocellulose-based microfluidic platform for investigating the effect of oxygen gradient on cells. Analyst 2021, 146, 5255–5263. [Google Scholar] [CrossRef]
- Koens, R.; Tabata, Y.; Serrano, J.C.; Aratake, S.; Yoshino, D.; Kamm, R.D.; Funamoto, K. Microfluidic platform for three-dimensional cell culture under spatiotemporal heterogeneity of oxygen tension. APL Bioeng. 2020, 4, 016106. [Google Scholar] [CrossRef]
- Fridman, I.B.; Ugolini, G.S.; VanDelinder, V.; Cohen, S.; Konry, T. High throughput microfluidic system with multiple oxygen levels for the study of hypoxia in tumor spheroids. Biofabrication 2021, 13, 035037. [Google Scholar] [CrossRef]
- Brennan, M.D.; Rexius-Hall, M.L.; Elgass, L.J.; Eddington, D.T. Oxygen control with microfluidics. Lab Chip 2014, 14, 4305–4318. [Google Scholar] [CrossRef] [PubMed]
- Park, J.; Lee, B.K.; Jeong, G.S.; Hyun, J.K.; Lee, C.J.; Lee, S.H. Three-dimensional brain-on-a-chip with an interstitial level of flow and its application as an in vitro model of Alzheimer’s disease. Lab Chip 2015, 15, 141–150. [Google Scholar] [CrossRef] [PubMed]
- Yin, F.; Zhu, Y.; Wang, Y.; Qin, J. Engineering Brain Organoids to Probe Impaired Neurogenesis Induced by Cadmium. ACS Biomater. Sci. Eng. 2018, 4, 1908–1915. [Google Scholar] [CrossRef] [PubMed]
- Akay, M.; Hite, J.; Avci, N.G.; Fan, Y.; Akay, Y.; Lu, G.; Zhu, J.J. Drug Screening of Human GBM Spheroids in Brain Cancer Chip. Sci. Rep. 2018, 8, 15423. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Wang, L.; Zhu, Y.; Qin, J. Human brain organoid-on-a-chip to model prenatal nicotine exposure. Lab Chip 2018, 18, 851–860. [Google Scholar] [CrossRef]
- Kosodo, Y.; Suetsugu, T.; Kobayashi, T.J.; Matsuzaki, F. Systematic time-dependent visualization and quantitation of the neurogenic rate in brain organoids. Biochem. Biophys. Res. Commun. 2017, 483, 94–100. [Google Scholar] [CrossRef]
- Andjelkovic, A.V.; Stamatovic, S.M.; Keep, R.F. The protective effects of preconditioning on cerebral endothelial cells in vitro. J. Cereb. Blood Flow Metab. 2003, 23, 1348–1355. [Google Scholar] [CrossRef] [Green Version]
- Foroutan, S.; Brillault, J.; Forbush, B.; O’Donnell, M.E. Moderate-to-severe ischemic conditions increase activity and phosphorylation of the cerebral microvascular endothelial cell Na+-K+-Cl− cotransporter. Am. J. Physiol. Cell Physiol. 2005, 289, C1492–C1501. [Google Scholar] [CrossRef]
- Gesuete, R.; Orsini, F.; Zanier, E.R.; Albani, D.; Deli, M.A.; Bazzoni, G.; De Simoni, M.G. Glial cells drive preconditioning-induced blood-brain barrier protection. Stroke 2011, 42, 1445–1453. [Google Scholar] [CrossRef] [Green Version]
- Tornabene, E.; Helms, H.C.C.; Pedersen, S.F.; Brodin, B. Effects of oxygen-glucose deprivation (OGD) on barrier properties and mRNA transcript levels of selected marker proteins in brain endothelial cells/astrocyte co-cultures. PLoS ONE 2019, 14, e0221103. [Google Scholar] [CrossRef]
- Vemula, S.; Roder, K.E.; Yang, T.; Bhat, G.J.; Thekkumkara, T.J.; Abbruscato, T.J. A functional role for sodium-dependent glucose transport across the blood-brain barrier during oxygen glucose deprivation. J. Pharmacol. Exp. Ther. 2009, 328, 487–495. [Google Scholar] [CrossRef]
- Wu, L.; Ye, Z.M.; Pan, Y.; Li, X.L.; Fu, X.; Zhang, B.; Li, Y.F.; Lin, W.R.; Li, X.L.; Gao, Q.C. Vascular endothelial growth factor aggravates cerebral ischemia and reperfusion-induced blood-brain-barrier disruption through regulating LOC102640519/HOXC13/ZO-1 signaling. Exp. Cell Res. 2018, 369, 275–283. [Google Scholar] [CrossRef]
- Cucullo, L.; Couraud, P.O.; Weksler, B.; Romero, I.A.; Hossain, M.; Rapp, E.; Janigro, D. Immortalized human brain endothelial cells and flow-based vascular modeling: A marriage of convenience for rational neurovascular studies. J. Cereb. Blood Flow Metab. 2008, 28, 312–328. [Google Scholar] [CrossRef] [Green Version]
- Krizanac-Bengez, L.; Mayberg, M.R.; Cunningham, E.; Hossain, M.; Ponnampalam, S.; Parkinson, F.E.; Janigro, D. Loss of shear stress induces leukocyte-mediated cytokine release and blood-brain barrier failure in dynamic in vitro blood-brain barrier model. J. Cell. Physiol. 2006, 206, 68–77. [Google Scholar] [CrossRef]
- Krizanac-Bengez, L.; Hossain, M.; Fazio, V.; Mayberg, M.; Janigro, D. Loss of flow induces leukocyte-mediated MMP/TIMP imbalance in dynamic in vitro blood-brain barrier model: Role of pro-inflammatory cytokines. Am. J. Physiol. Cell Physiol. 2006, 291, C740–C749. [Google Scholar] [CrossRef] [Green Version]
- Cameron, T.; Bennet, T.; Rowe, E.M.; Anwer, M.; Wellington, C.L.; Cheung, K.C. Review of Design Considerations for Brain-on-a-Chip Models. Micromachines 2021, 12, 441. [Google Scholar] [CrossRef]
- Booth, R.; Kim, H. Characterization of a microfluidic in vitro model of the blood-brain barrier (muBBB). Lab Chip 2012, 12, 1784–1792. [Google Scholar] [CrossRef]
- Griep, L.M.; Wolbers, F.; de Wagenaar, B.; ter Braak, P.M.; Weksler, B.B.; Romero, I.A.; Couraud, P.O.; Vermes, I.; van der Meer, A.D.; van den Berg, A. BBB on chip: Microfluidic platform to mechanically and biochemically modulate blood-brain barrier function. Biomed. Microdevices 2013, 15, 145–150. [Google Scholar] [CrossRef]
- Achyuta, A.K.; Conway, A.J.; Crouse, R.B.; Bannister, E.C.; Lee, R.N.; Katnik, C.P.; Behensky, A.A.; Cuevas, J.; Sundaram, S.S. A modular approach to create a neurovascular unit-on-a-chip. Lab Chip 2013, 13, 542–553. [Google Scholar] [CrossRef]
- Walter, F.R.; Valkai, S.; Kincses, A.; Veszelka, S.; Ormos, P.; Deli, M.A.; Der, A. Lab-on-a-Chip Tool for Modeling Biological Barriers. J. Neuroimmune Pharmacol. 2016, 11, S49–S50. [Google Scholar] [CrossRef] [Green Version]
- Brown, J.A.; Pensabene, V.; Markov, D.A.; Allwardt, V.; Neely, M.D.; Shi, M.J.; Britt, C.M.; Hoilett, O.S.; Yang, Q.; Brewer, B.M.; et al. Recreating blood-brain barrier physiology and structure on chip: A novel neurovascular microfluidic bioreactor. Biomicrofluidics 2015, 9, 054124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katt, M.E.; Shusta, E.V. In vitro models of the blood-brain barrier: Building in physiological complexity. Curr. Opin. Chem. Eng. 2020, 30, 42–52. [Google Scholar] [CrossRef] [PubMed]
- Cho, H.S.; Seo, J.H.; Wong, K.H.K.; Terasaki, Y.; Park, J.; Bong, K.; Arai, K.; Lo, E.H.; Irimia, D. Three-Dimensional Blood-Brain Barrier Model for in vitro Studies of Neurovascular Pathology. Sci. Rep. 2015, 5, 15222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adriani, G.; Ma, D.L.; Pavesi, A.; Kamm, R.D.; Goh, E.L.K. A 3D neurovascular microfluidic model consisting of neurons, astrocytes and cerebral endothelial cells as a blood-brain barrier. Lab Chip 2017, 17, 448–459. [Google Scholar] [CrossRef]
- Herland, A.; van der Meer, A.D.; FitzGerald, E.A.; Park, T.E.; Sleeboom, J.J.; Ingber, D.E. Distinct Contributions of Astrocytes and Pericytes to Neuroinflammation Identified in a 3D Human Blood-Brain Barrier on a Chip. PLoS ONE 2016, 11, e0150360. [Google Scholar] [CrossRef] [Green Version]
- Partyka, P.P.; Godsey, G.A.; Galie, J.R.; Kosciuk, M.C.; Acharya, N.K.; Nagele, R.G.; Galie, P.A. Mechanical stress regulates transport in a compliant 3D model of the blood-brain barrier. Biomaterials 2017, 115, 30–39. [Google Scholar] [CrossRef]
- Faley, S.L.; Neal, E.H.; Wang, J.X.; Bosworth, A.M.; Weber, C.M.; Balotin, K.M.; Lippmann, E.S.; Bellan, L.M. iPSC-Derived Brain Endothelium Exhibits Stable, Long-Term Barrier Function in Perfused Hydrogel Scaffolds. Stem Cell Rep. 2019, 12, 474–487. [Google Scholar] [CrossRef] [Green Version]
- Van Dijk, C.G.M.; Brandt, M.M.; Poulis, N.; Anten, J.; van der Moolen, M.; Kramer, L.; Homburg, E.; Louzao-Martinez, L.; Pei, J.; Krebber, M.M.; et al. A new microfluidic model that allows monitoring of complex vascular structures and cell interactions in a 3D biological matrix. Lab Chip 2020, 20, 1827–1844. [Google Scholar] [CrossRef]
- Bouhrira, N.; DeOre, B.J.; Sazer, D.W.; Chiaradia, Z.; Miller, J.S.; Galie, P.A. Disturbed flow disrupts the blood-brain barrier in a 3D bifurcation model. Biofabrication 2020, 12, 025020. [Google Scholar] [CrossRef]
- Yu, F.; Kumar, N.D.O.S.; Foo, L.C.; Ng, S.H.; Hunziker, W.; Choudhury, D. A pump-free tricellular blood-brain barrier on-a-chip model to understand barrier property and evaluate drug response. Biotechnol. Bioeng. 2020, 117, 1127–1136. [Google Scholar] [CrossRef]
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Van Breedam, E.; Ponsaerts, P. Promising Strategies for the Development of Advanced In Vitro Models with High Predictive Power in Ischaemic Stroke Research. Int. J. Mol. Sci. 2022, 23, 7140. https://doi.org/10.3390/ijms23137140
Van Breedam E, Ponsaerts P. Promising Strategies for the Development of Advanced In Vitro Models with High Predictive Power in Ischaemic Stroke Research. International Journal of Molecular Sciences. 2022; 23(13):7140. https://doi.org/10.3390/ijms23137140
Chicago/Turabian StyleVan Breedam, Elise, and Peter Ponsaerts. 2022. "Promising Strategies for the Development of Advanced In Vitro Models with High Predictive Power in Ischaemic Stroke Research" International Journal of Molecular Sciences 23, no. 13: 7140. https://doi.org/10.3390/ijms23137140