Three-dimensional human neural culture on a chip recapitulating neuroinflammation and neurodegeneration

You Jung Kang, Yen N. Diep, Minh Tran, Van Thi Ai Tran, Ghuncha Ambrin, Huyen Ngo, Hansang Cho

Published: 2023-08-03 DOI: 10.1038/s41596-023-00861-4

microfluidics

neuroinflammation

brain-on-a-chip

neurodegeneration

neuron-glia interactions

AI 解读

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Stable isotope tracing to assess tumor metabolism in vivo

Measuring DNA modifications with the comet assay: a compendium of protocols

Detect-seq, a chemical labeling and biotin pull-down approach for the unbiased and genome-wide off-target evaluation of programmable cytosine base editors

A systems-level mass spectrometry-based technique for accurate and sensitive quantification of the RNA cap epitranscriptome

Spooling electrochemiluminescence spectroscopy: development, applications and beyond

Chronic, cortex-wide imaging of specific cell populations during behavior

Chromatin accessibility profiling by ATAC-seq

Global analysis of RNA-binding protein dynamics by comparative and enhanced RNA interactome capture

Pooled genetic perturbation screens with image-based phenotypes

查看全部

Sections

Figures

References

Linnerbauer, M., Wheeler, M. A. & Quintana, F. J. Astrocyte crosstalk in CNS inflammation. Neuron 108, 608–622 (2020).
Masuda, T., Sankowski, R., Staszewski, O. & Prinz, M. Microglia heterogeneity in the single-cell era. Cell Rep. 30, 1271–1281 (2020).
Tan, Y.-L., Yuan, Y. & Tian, L. Microglial regional heterogeneity and its role in the brain. Mol. Psychiatry 25, 351–367 (2020).
Cho, H. et al. Microfluidic chemotaxis platform for differentiating the roles of soluble and bound amyloid-β on microglial accumulation. Sci. Rep. 3, 1823 (2013).
Kim, Y. H. et al. A 3D human neural cell culture system for modeling Alzheimer’s disease. Nat. Protoc. 10, 985–1006 (2015).
Jairaman, A. et al. TREM2 regulates purinergic receptor-mediated calcium signaling and motility in human iPSC-derived microglia. eLife 11, e73021 (2022).
Zehntner, S. P. et al. Neutrophils that infiltrate the central nervous system regulate T cell responses. J. Immunol. 174, 5124–5131 (2005).
Sas, A. R. et al. A new neutrophil subset promotes CNS neuron survival and axon regeneration. Nat. Immunol. 21, 1496–1505 (2020).
Bodega, G. et al. Ammonia induces aquaporin-4 rearrangement in the plasma membrane of cultured astrocytes. Neurochem. Int. 61, 1314–1324 (2012).
Tran, V. T. A., Kang, Y. J., Kim, H.-K., Kim, H.-R. & Cho, H. Oral pathogenic bacteria-inducing neurodegenerative microgliosis in human neural cell platform. Int. J. Mol. Sci. 22, 6925 (2021).
Kang, Y. J., Tan, H.-Y., Lee, C. Y. & Cho, H. An air particulate pollutant induces neuroinflammation and neurodegeneration in human brain models. Adv. Sci. 8, 2101251 (2021).
Sofroniew, M. V. Astrocyte reactivity: subtypes, states, and functions in CNS innate immunity. Trends Immunol. 41, 758–770 (2020).
Waltl, I. & Kalinke, U. Beneficial and detrimental functions of microglia during viral encephalitis. Trends Neurosci. 45, 158–170 (2022).
Chun, H. et al. Severe reactive astrocytes precipitate pathological hallmarks of Alzheimer’s disease via H2O2− production. Nat. Neurosci. 23, 1555–1566 (2020).
Li, Q. & Barres, B. A. Microglia and macrophages in brain homeostasis and disease. Nat. Rev. Immunol. 18, 225–242 (2018).
Volterra, A. & Meldolesi, J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626–640 (2005).
Kang, Y. J., Diep, Y. N., Tran, M. & Cho, H. Therapeutic targeting strategies for early- to late-staged Alzheimer’s disease. Int. J. Mol. Sci. 21, 9591 (2020).
Heneka, M. T. et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 14, 388–405 (2015).
Park, J. et al. A 3D human triculture system modeling neurodegeneration and neuroinflammation in Alzheimer’s disease. Nat. Neurosci. 21, 941–951 (2018).
Kinney, J. W. et al. Inflammation as a central mechanism in Alzheimer’s disease. Alzheimers Dement. 4, 575–590 (2018).
Tan, H.-Y., Cho, H. & Lee, L. P. Human mini-brain models. Nat. Biomed. Eng. 5, 11–25 (2021).
Kang, Y. J. & Cho, H. Human brain organoids in Alzheimer’s disease. Organoid 1, e5 (2021).
Keren-Shaul, H. et al. A unique microglia type associated with restricting development of Alzheimer’s disease. Cell 169, 1276–1290.e17 (2017).
McQuade, A. et al. Gene expression and functional deficits underlie TREM2-knockout microglia responses in human models of Alzheimer’s disease. Nat. Comm. 11, 5370 (2020).
Lee, C. Y. D. & Landreth, G. E. The role of microglia in amyloid clearance from the AD brain. J. Neural Transm. 117, 949–960 (2010).
Gui, X. et al. Botulinum toxin type A promotes microglial M2 polarization and suppresses chronic constriction injury-induced neuropathic pain through the P2X7 receptor. Cell Biosci. 10, 45 (2020).
Pitanga, B. P., Nascimento, R. P., Silva, V. D. & Costa, S. L. The role of astrocytes in metabolism and neurotoxicity of the pyrrolizidine alkaloid monocrotaline, the main toxin of Crotalaria retusa. Front. Pharmacol. 3, 144 (2012).
Spiteri, A. G., Wishart, C. L., Pamphlett, R., Locatelli, G. & King, N. J. C. Microglia and monocytes in inflammatory CNS disease: integrating phenotype and function. Acta Neuropathol. 143, 179–224 (2022).
Jankowsky, J. L. & Zheng, H. Practical considerations for choosing a mouse model of Alzheimer’s disease. Mol. Neurodegener. 12, 89 (2017).
Drummond, E. & Wisniewski, T. Alzheimer’s disease: experimental models and reality. Acta Neuropathol. 133, 155–175 (2017).
Vignal, C. et al. Effects of urban coarse particles inhalation on oxidative and inflammatory parameters in the mouse lung and colon. Part. Fibre Toxicol. 14, 46 (2017).
Papadimitriou, C. et al. 3D culture method for Alzheimer’s disease modeling reveals interleukin-4 rescues Aβ42-induced loss of human neural stem cell plasticity. Dev. Cell 46, 85–101.e8 (2018).
Fang, Y. et al. The adhesion and migration of microglia to β-amyloid (Aβ) is decreased with aging and inhibited by Nogo/NgR pathway. J. Neuroinflammation 15, 210 (2018).
Omar Zaki, S. S., Kanesan, L., Leong, M. Y. D. & Vidyadaran, S. The influence of serum-supplemented culture media in a transwell migration assay. Cell Biol. Int. 43, 1201–1204 (2019).
Wang, S. et al. α-Synuclein, a chemoattractant, directs microglial migration via H2O2-dependent Lyn phosphorylation. Proc. Natl Acad. Sci. USA 112, E1926–E1935 (2015).
Wu, H.-j. et al. Analysis of microglial migration by a micropipette assay. Nat. Protoc. 9, 491–500 (2014).
Akther, F., Yakob, S. B., Nguyen, N. T. & Ta, H. T. Surface modification techniques for endothelial cell seeding in PDMS microfluidic devices. Biosensors 10, 182 (2020).
Fan, D.-H., Yuan, S.-W. & Shen, Y.-M. Surface modification with BSA blocking based on in situ synthesized gold nanoparticles in poly(dimethylsiloxane) microchip. Colloids Surf. B 75, 608–611 (2010).
Trantidou, T., Elani, Y., Parsons, E. & Ces, O. Hydrophilic surface modification of PDMS for droplet microfluidics using a simple, quick, and robust method via PVA deposition. Microsyst. Nanoeng. 3, 16091 (2017).
Wu, D., Zhao, B., Dai, Z., Qin, J. & Lin, B. Grafting epoxy-modified hydrophilic polymers onto poly(dimethylsiloxane) microfluidic chip to resist nonspecific protein adsorption. Lab Chip 6, 942–947 (2006).
Ren, K., Zhou, J. & Wu, H. Materials for microfluidic chip fabrication. Acc. Chem. Res. 46, 2396–2406 (2013).
Zhang, B., Korolj, A., Lai, B. F. L. & Radisic, M. Advances in organ-on-a-chip engineering. Nat. Rev. Mater. 3, 257–278 (2018).
Bhatia, S. N. & Ingber, D. E. Microfluidic organs-on-chips. Nat. Biotechnol. 32, 760–772 (2014).
Ralay Ranaivo, H. & Wainwright, M. S. Albumin activates astrocytes and microglia through mitogen-activated protein kinase pathways. Brain Res. 1313, 222–231 (2010).
Schafer, D. P. et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691–705 (2012).
Li, Y., Du, X.-F., Liu, C.-S., Wen, Z.-L. & Du, J.-L. Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23, 1189–1202 (2012).
Alghamri, M. S. et al. G-CSF secreted by mutant IDH1 glioma stem cells abolishes myeloid cell immunosuppression and enhances the efficacy of immunotherapy. Sci. Adv. 7, eabh3243 (2021).
Sielska, M. et al. Tumour-derived CSF2/granulocyte macrophage colony stimulating factor controls myeloid cell accumulation and progression of gliomas. Br. J. Cancer 123, 438–448 (2020).
Ghoochani, A. et al. MIF-CD74 signaling impedes microglial M1 polarization and facilitates brain tumorigenesis. Oncogene 35, 6246–6261 (2016).
Yonai, R., Sato, R. & Nasu, M. Cerebral edema induced by hyperammonemia: a case report. Am. J. Emerg. Med. 34, 2461.e3–2461.e5 (2016).
Rama Rao, K. V., Jayakumar, A. R., Tong, X., Curtis, K. M. & Norenberg, M. D. Brain aquaporin-4 in experimental acute liver failure. J. Neuropathol. Exp. Neurol. 69, 869–879 (2010).
Rungta, R. L. et al. The cellular mechanisms of neuronal swelling underlying cytotoxic edema. Cell 161, 610–621 (2015).
Back, A. et al. Ammonia-induced brain swelling and neurotoxicity in an organotypic slice model. Neurol. Res. 33, 1100–1108 (2011).
Tanaka, S. et al. CD206 expression in induced microglia-like cells from peripheral blood as a surrogate biomarker for the specific immune microenvironment of neurosurgical diseases including glioma. Front. Immunol. 12, 670131 (2021).
Scott, T. R., Kronsten, V. T., Hughes, R. D. & Shawcross, D. L. Pathophysiology of cerebral oedema in acute liver failure. World J. Gastroenterol. 19, 9240–9255 (2013).
Angelova, P. R. et al. Hyperammonaemia induces mitochondrial dysfunction and neuronal cell death. JHEP Rep. 4, 100510 (2022).
Niknahad, H., Jamshidzadeh, A., Heidari, R., Zarei, M. & Ommati, M. M. Ammonia-induced mitochondrial dysfunction and energy metabolism disturbances in isolated brain and liver mitochondria, and the effect of taurine administration: relevance to hepatic encephalopathy treatment. Clin. Exp. Hepatol. 3, 141–151 (2017).

Three-dimensional human neural culture on a chip recapitulating neuroinflammation and neurodegeneration

Supplementary information

推荐阅读