Neuro-immune interactions at single-cell resolution in neurodevelopmental, infectious, and neurodegenerative diseases

References

• Absinta M, Maric D, Gharagozloo M, Garton T, Smith MD, Jin J, Fitzgerald KC, Song A, Liu P, Lin JP, et al. 2021. A lymphocyte-microglia-astrocyte axis in chronic active multiple sclerosis. Nature. 597(7878):709–714.
   PubMed Web of Science ®Google Scholar
• Attfield KE, Jensen LT, Kaufmann M, Friese MA, Fugger L. 2022. The immunology of multiple sclerosis. Nat Rev Immunol. doi:10.1038/s41577-022-00718-z.
   PubMed Web of Science ®Google Scholar
• Baek S, Lee I. 2020. Single-cell ATAC sequencing analysis: from data preprocessing to hypothesis generation. Comput Struct Biotechnol J. 18:1429–1439.
   PubMed Web of Science ®Google Scholar
• Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods. 10(12):1213–1218.
   PubMed Web of Science ®Google Scholar
• Buenrostro JD, Wu B, Chang HY, Greenleaf WJ. 2015. ATAC-seq: A method for assaying chromatin accessibility genome-wide. Curr Protoc Mol Biol. 109:21 29 21–21 29 29.
   PubMedGoogle Scholar
• Burgess DJ. 2019. Spatial transcriptomics coming of age. Nat Rev Genet. 20(6):317.
   PubMed Web of Science ®Google Scholar
• Ceban F, Ling S, Lui LMW, Lee Y, Gill H, Teopiz KM, Rodrigues NB, Subramaniapillai M, Di Vincenzo JD, Cao B, et al. 2022. Fatigue and cognitive impairment in post-COVID-19 syndrome: A systematic review and meta-analysis. Brain Behav Immun. 101:93–135.
   PubMed Web of Science ®Google Scholar
• Choi GB, Yim YS, Wong H, Kim S, Kim H, Kim SV, Hoeffer CA, Littman DR, Huh JR. 2016. The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science. 351(6276):933–939.
   PubMed Web of Science ®Google Scholar
• Choi SS, Lee HJ, Lim I, Satoh J, Kim SU. 2014. Human astrocytes: secretome profiles of cytokines and chemokines. PLoS One. 9(4):e92325.
   PubMed Web of Science ®Google Scholar
• Choi YH, Kim JK. 2019. Dissecting cellular heterogeneity using single-cell RNA sequencing. Mol Cells. 42(3):189–199.
   PubMed Web of Science ®Google Scholar
• Colonna M, Brioschi S. 2020. Neuroinflammation and neurodegeneration in human brain at single-cell resolution. Nat Rev Immunol. 20(2):81–82.
   PubMed Web of Science ®Google Scholar
• Daneman R, Prat A. 2015. The blood-brain barrier. Cold Spring Harb Perspect Biol. 7(1):a020412.
   PubMed Web of Science ®Google Scholar
• Darmanis S, Sloan SA, Zhang Y, Enge M, Caneda C, Shuer LM, Hayden Gephart MG, Barres BA, Quake SR. 2015. A survey of human brain transcriptome diversity at the single cell level. Proc Natl Acad Sci USA. 112(23):7285–7290.
   PubMed Web of Science ®Google Scholar
• de Lima K A, Rustenhoven J, Da Mesquita S, Wall M, Salvador AF, Smirnov I, Martelossi Cebinelli G, Mamuladze T, Baker W, Papadopoulos Z, et al. 2020. Meningeal γδ T cells regulate anxiety-like behavior via IL-17a signaling in neurons. Nat Immunol. 21(11):1421–1429.
   PubMed Web of Science ®Google Scholar
• Del-Aguila JL, Li Z, Dube U, Mihindukulasuriya KA, Budde JP, Fernandez MV, Ibanez L, Bradley J, Wang F, Bergmann K, Davenport R. 2019. A single-nuclei RNA sequencing study of Mendelian and sporadic AD in the human brain. Alzheimers Res Ther. 11(1):71.
   PubMed Web of Science ®Google Scholar
• Douaud G, Lee S, Alfaro-Almagro F, Arthofer C, Wang C, McCarthy P, Lange F, Andersson JL, Griffanti L, Duff E, Jbabdi S. 2022. SARS-CoV-2 is associated with changes in brain structure in UK biobank. Nature. 604(7907):697–707.
   PubMed Web of Science ®Google Scholar
• Eze UC, Bhaduri A, Haeussler M, Nowakowski TJ, Kriegstein AR. 2021. Single-cell atlas of early human brain development highlights heterogeneity of human neuroepithelial cells and early radial glia. Nat Neurosci. 24(4):584–594.
   PubMed Web of Science ®Google Scholar
• Fernández-Castañeda, A., Lu, P., Geraghty, A.C., Song, E., Lee, M.H., Wood, J., O’Dea, M.R., Dutton, S., Shamardani, K., Nwangwu, K. and Mancusi, R. 2022. Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation. Cell. 185(14):2452–2468.e16.
   PubMed Web of Science ®Google Scholar
• Fullard JF, Lee HC, Voloudakis G, Suo S, Javidfar B, Shao Z, Peter C, Zhang W, Jiang S, Corvelo A, Wargnier H. 2021. Single-nucleus transcriptome analysis of human brain immune response in patients with severe COVID-19. Genome Med. 13(1):118.
   PubMed Web of Science ®Google Scholar
• Grindberg RV, Yee-Greenbaum JL, McConnell MJ, Novotny M, O’Shaughnessy AL, Lambert GM, Arauzo-Bravo MJ, Lee J, Fishman M, Robbins GE, et al. 2013. RNA-sequencing from single nuclei. Proc Natl Acad Sci USA. 110(49):19802–19807.
   PubMed Web of Science ®Google Scholar
• Grubman A, Chew G, Ouyang JF, Sun G, Choo XY, McLean C, Simmons RK, Buckberry S, Vargas-Landin DB, Poppe D, Pflueger J. 2019. A single-cell atlas of entorhinal cortex from individuals with Alzheimer’s disease reveals cell-type-specific gene expression regulation. Nat Neurosci. 22(12):2087–2097.
   PubMed Web of Science ®Google Scholar
• Guzman-Martinez L, Maccioni RB, Andrade V, Navarrete LP, Pastor MG, Ramos-Escobar N. 2019. Neuroinflammation as a common feature of neurodegenerative disorders. Front Pharmacol. 10:1008.
   PubMed Web of Science ®Google Scholar
• Haage V, De Jager PL. 2022. Neuroimmune contributions to Alzheimer’s disease: a focus on human data. Mol Psychiatry. doi:10.1038/s41380-022-01637-0.
   PubMedGoogle Scholar
• Hao Y, Hao S, Andersen-Nissen E, Mauck III WM, Zheng S, Butler A, Lee MJ, Wilk AJ, Darby C, Zager M, Hoffman P. 2021. Integrated analysis of multimodal single-cell data. Cell. 184(13):3573–3587.e29.
   PubMed Web of Science ®Google Scholar
• Herz J, Fu Z, Kim K, Dykstra T, Wall M, Li H, Salvador AF, Zou B, Yan N, Blackburn SM, Andrews PH. 2021. Gabaergic neuronal IL-4R mediates T cell effect on memory. Neuron. 109(22):3609–3618.e9.
   PubMed Web of Science ®Google Scholar
• Huang X, Hussain B, Chang J. 2021. Peripheral inflammation and blood-brain barrier disruption: effects and mechanisms. CNS Neurosci Ther. 27(1):36–47.
   PubMed Web of Science ®Google Scholar
• Hwang B, Lee JH, Bang D. 2018. Single-cell RNA sequencing technologies and bioinformaticspipelines. Exp Mol Med. 50(8):1–14.
   Google Scholar
• Jakel S, Agirre E, Mendanha Falcao A, van Bruggen D, Lee KW, Knuesel I, Malhotra D, Ffrench-Constant C, Williams A, Castelo-Branco G. 2019. Altered human oligodendrocyte heterogeneity in multiple sclerosis. Nature. 566(7745):543–547.
   PubMed Web of Science ®Google Scholar
• Jordao MJC, Sankowski R, Brendecke SM, Sagar LG, Tai YH, Tay TL, Schramm E, Armbruster S, Hagemeyer N, et al. 2019. Single-cell profiling identifies myeloid cell subsets with distinct fates during neuroinflammation. Science. 363:6425.
   Web of Science ®Google Scholar
• Kalish BT, Kim E, Finander B, Duffy EE, Kim H, Gilman CK, Yim YS, Tong L, Kaufman RJ, Griffith EC, et al. 2021. Maternal immune activation in mice disrupts proteostasis in the fetal brain. Nat Neurosci. 24(2):204–213.
   PubMed Web of Science ®Google Scholar
• Kamath T, Abdulraouf A, Burris SJ, Langlieb J, Gazestani V, Nadaf NM, Balderrama K, Vanderburg C, Macosko EZ. 2022. Single-cell genomic profiling of human dopamine neurons identifies a population that selectively degenerates in Parkinson’s disease. Nat Neurosci. 25(5):588–595.
   PubMed Web of Science ®Google Scholar
• Karpus WJ. 2020. Cytokines and chemokines in the pathogenesis of experimental autoimmune encephalomyelitis. J Immunol. 204(2):316–326.
   PubMed Web of Science ®Google Scholar
• Kaufmann M, Evans H, Schaupp AL, Engler JB, Kaur G, Willing A, Kursawe N, Schubert C, Attfield KE, Fugger L, Friese MA. 2021. Identifying CNS-colonizing T cells as potential therapeutic targets to prevent progression of multiple sclerosis. Med (N Y). 2(3):296–312 e298.
   PubMedGoogle Scholar
• Kepinska AP, Iyegbe CO, Vernon AC, Yolken R, Murray RM, Pollak TA. 2020. Schizophrenia and influenza at the centenary of the 1918-1919 spanish influenza pandemic: mechanisms of psychosis risk. Front Psychiatry. 11:72.
   PubMed Web of Science ®Google Scholar
• Kwon HK, Choi GB, Huh JR. 2022. Maternal inflammation and its ramifications on fetal neurodevelopment. Trends Immunol. 43(3):230–244.
   PubMed Web of Science ®Google Scholar
• La Manno G, Siletti K, Furlan A, Gyllborg D, Vinsland E, Mossi Albiach A, Mattsson Langseth C, Khven I, Lederer AR, Dratva LM, Johnsson A. 2021. Molecular architecture of the developing mouse brain. Nature. 596(7870):92–96.
   PubMed Web of Science ®Google Scholar
• Lau SF, Cao H, Fu AKY, Ip NY. 2020. Single-nucleus transcriptome analysis reveals dysregulation of angiogenic endothelial cells and neuroprotective glia in Alzheimer’s disease. Proc Natl Acad Sci USA. 117(41):25800–25809.
   PubMed Web of Science ®Google Scholar
• Lee BK, Magnusson C, Gardner RM, Blomstrom A, Newschaffer CJ, Burstyn I, Karlsson H, Dalman C. 2015. Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders. Brain Behav Immun. 44:100–105.
   PubMed Web of Science ®Google Scholar
• Lempriere S. 2021. Single-cell transcriptomics reveals neuroinflammation in severe COVID-19. Nat Rev Neurol. 17(8):461.
   PubMed Web of Science ®Google Scholar
• Leng K, Li E, Eser R, Piergies A, Sit R, Tan M, Neff N, Li SH, Rodriguez RD, Suemoto CK, Leite REP. 2021. Molecular characterization of selectively vulnerable neurons in Alzheimer’s disease. Nat Neurosci. 24(2):276–287.
   PubMed Web of Science ®Google Scholar
• Li Q, Barres BA. 2018. Microglia and macrophages in brain homeostasis and disease. Nat Rev Immunol. 18(4):225–242.
   PubMed Web of Science ®Google Scholar
• Li Z, Tyler WA, Zeldich E, Santpere Baro G, Okamoto M, Gao T, Li M, Sestan N, Haydar TF. 2020. Transcriptional priming as a conserved mechanism of lineage diversification in the developing mouse and human neocortex. Sci Adv. 6. doi:10.1126/sciadv.abd206.
   Web of Science ®Google Scholar
• Liu L, Besson-Girard S, Ji H, Gehring K, Bulut B, Kaya T, Usifo F, Simons M, Gokce O. 2021. Dissociation of microdissected mouse brain tissue for artifact free single-cell RNA sequencing. STAR Protoc. 2(2):100590.
   PubMedGoogle Scholar
• Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH. 2012. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun. 26(4):607–616.
   PubMed Web of Science ®Google Scholar
• Manabe T, Heneka MT. 2022. Cerebral dysfunctions caused by sepsis during ageing. Nat Rev Immunol. 22:444–458.
   PubMed Web of Science ®Google Scholar
• Masuda T, Sankowski R, Staszewski O, Bottcher C, Amann L, Sagar SC, Nessler S, Kunz P, van Loo G, et al. 2019. Spatial and temporal heterogeneity of mouse and human microglia at single-cell resolution. Nature. 566(7744):388–392.
   PubMed Web of Science ®Google Scholar
• Mathys H, Adaikkan C, Gao F, Young JZ, Manet E, Hemberg M, De Jager PL, Ransohoff RM, Regev A, Tsai LH. 2017. Temporal tracking of microglia activation in neurodegeneration at single-cell resolution. Cell Rep. 21(2):366–380.
   PubMed Web of Science ®Google Scholar
• Mathys H, Davila-Velderrain J, Peng Z, Gao F, Mohammadi S, Young JZ, Menon M, He L, Abdurrob F, Jiang X, Martorell AJ. 2019. Single-cell transcriptomic analysis of Alzheimer’s disease. Nature. 570(7761):332–337.
   PubMed Web of Science ®Google Scholar
• Miedema A, Gerrits E, Brouwer N, Jiang Q, Kracht L, Meijer M, Nutma E, Peferoen-Baert R, Pijnacker AT, Wesseling EM, Wijering MH. 2022. Brain macrophages acquire distinct transcriptomes in multiple sclerosis lesions and normal appearing white matter. Acta Neuropathol Commun. 10(1):8.
   PubMed Web of Science ®Google Scholar
• Morabito S, Miyoshi E, Michael N, Shahin S, Martini AC, Head E, Silva J, Leavy K, Perez-Rosendahl M, Swarup V. 2021. Single-nucleus chromatin accessibility and transcriptomic characterization of Alzheimer’s disease. Nat Genet. 53(8):1143–1155.
   PubMed Web of Science ®Google Scholar
• Nott A, Holtman IR, Coufal NG, Schlachetzki JCM, Yu M, Hu R, Han CZ, Pena M, Xiao J, Wu Y, et al. 2019. Brain cell type-specific enhancer-promoter interactome maps and disease - risk association. Science. 366(6469):1134–1139.
   Google Scholar
• Omari KM, John GR, Sealfon SC, Raine CS. 2005. Cxc chemokine receptors on human oligodendrocytes: implications for multiple sclerosis. Brain. 128(Pt 5):1003–1015.
   PubMedGoogle Scholar
• Patterson PH. 2009. Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav Brain Res. 204(2):313–321.
   PubMed Web of Science ®Google Scholar
• Polioudakis D, de la Torre-Ubieta L, Langerman J, Elkins AG, Shi X, Stein JL, Vuong CK, Nichterwitz S, Gevorgian M, Opland CK, Lu D. 2019. A single-cell transcriptomic atlas of human neocortical development during Mid-gestation. Neuron. 103(5):785–801.e8. e788.
   PubMed Web of Science ®Google Scholar
• Prieto GA, Cotman CW. 2017. Cytokines and cytokine networks target neurons to modulate long-term potentiation. Cytokine Growth Factor Rev. 34:27–33.
   PubMed Web of Science ®Google Scholar
• Salvador AF, de Lima KA, Kipnis J. 2021. Neuromodulation by the immune system: a focus on cytokines. Nat Rev Immunol. 21(8):526–541.
   PubMed Web of Science ®Google Scholar
• Schafflick D, Xu CA, Hartlehnert M, Cole M, Schulte-Mecklenbeck A, Lautwein T, Wolbert J, Heming M, Meuth SG, Kuhlmann T, Gross CC. 2020. Integrated single cell analysis of blood and cerebrospinal fluid leukocytes in multiple sclerosis. Nat Commun. 11(1):247.
   PubMed Web of Science ®Google Scholar
• Schirmer L, Velmeshev D, Holmqvist S, Kaufmann M, Werneburg S, Jung D, Vistnes S, Stockley JH, Young A, Steindel M, Tung B. 2019. Neuronal vulnerability and multilineage diversity in multiple sclerosis. Nature. 573(7772):75–82.
   PubMed Web of Science ®Google Scholar
• Shin Yim Y, Park A, Berrios J, Lafourcade M, Pascual LM, Soares N, Yeon Kim J, Kim S, Kim H, Waisman A, Littman DR. 2017. Reversing behavioural abnormalities in mice exposed to maternal inflammation. Nature. 549(7673):482–487.
   PubMed Web of Science ®Google Scholar
• Smajić S, Prada-Medina CA, Landoulsi Z, Ghelfi J, Delcambre S, Dietrich C, Jarazo J, Henck J, Balachandran S, Pachchek S, Morris CM. 2022. Single-cell sequencing of human midbrain reveals glial activation and a Parkinson-specific neuronal state. Brain. 145(3):964–978.
   PubMed Web of Science ®Google Scholar
• Smith SE, Li J, Garbett K, Mirnics K, Patterson PH. 2007. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci. 27(40):10695–10702.
   PubMed Web of Science ®Google Scholar
• Solomon T. 2021. Neurological infection with SARS-CoV-2 — the story so far. Nat Rev Neurol. 17(2):65–66.
   PubMed Web of Science ®Google Scholar
• Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S, Wynshaw-Boris A, Colamarino SA, Lein ES, Courchesne E. 2014. Patches of disorganization in the neocortex of children with autism. N Engl J Med. 370(13):1209–1219.
   PubMed Web of Science ®Google Scholar
• Tansey MG, Wallings RL, Houser MC, Herrick MK, Keating CE, Joers V. 2022. Inflammation and immune dysfunction in Parkinson disease. Nat Rev Immunol. doi:10.1038/s41577-022-00684-6.
   PubMed Web of Science ®Google Scholar
• Tran PB, Miller RJ. 2003. Chemokine receptors: signposts to brain development and disease. Nat Rev Neurosci. 4(6):444–455.
   PubMed Web of Science ®Google Scholar
• Vainchtein ID, Chin G, Cho FS, Kelley KW, Miller JG, Chien EC, Liddelow SA, Nguyen PT, Nakao-Inoue H, Dorman LC, Akil O. 2018. Astrocyte-derived interleukin-33 promotes microglial synapse engulfment and neural circuit development. Science. 359(6381):1269–1273.
   PubMed Web of Science ®Google Scholar
• Velmeshev D, Schirmer L, Jung D, Haeussler M, Perez Y, Mayer S, Bhaduri A, Goyal N, Rowitch DH, Kriegstein AR. 2019. Single-cell genomics identifies cell type-specific molecular changes in autism. Science. 364(6441):685–689.
   PubMed Web of Science ®Google Scholar
• Vuong HE, Pronovost GN, Williams DW, Coley EJL, Siegler EL, Qiu A, Kazantsev M, Wilson CJ, Rendon T, Hsiao EY. 2020. The maternal microbiome modulates fetal neurodevelopment in mice. Nature. 586(7828):281–286.
   PubMed Web of Science ®Google Scholar
• Wang M, Song WM, Ming C, Wang Q, Zhou X, Xu P, Krek A, Yoon Y, Ho L, Orr ME, Yuan GC. 2022. Guidelines for bioinformatics of single-cell sequencing data analysis in Alzheimer’s disease: review, recommendation, implementation and application. Mol Neurodegener. 17(1):17.
   PubMed Web of Science ®Google Scholar
• Wolf FA, Angerer P, Theis FJ. 2018. Scanpy: large-scale single-cell gene expression data analysis. Genome Biol. 19(1):15.
   PubMed Web of Science ®Google Scholar
• Yang AC, Kern F, Losada PM, Agam MR, Maat CA, Schmartz GP, Fehlmann T, Stein JA, Schaum N, Lee DP, Calcuttawala K. 2021. Dysregulation of brain and choroid plexus cell types in severe COVID-19. Nature. 595(7868):565–571.
   PubMed Web of Science ®Google Scholar
• Yang AC, Vest RT, Kern F, Lee DP, Agam M, Maat CA, Losada PM, Chen MB, Schaum N, Khoury N, Toland A. 2022. A human brain vascular atlas reveals diverse mediators of Alzheimer’s risk. Nature. 603(7903):885–892.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Song WM, Andhey PS, Swain A, Levy T, Miller KR, Poliani PL, Cominelli M, Grover S, Gilfillan S, Cella M. 2020. Human and mouse single-nucleus transcriptomics reveal TREM2-dependent and TREM2-independent cellular responses in Alzheimer’s disease. Nat Med. 26(1):131–142.
   PubMed Web of Science ®Google Scholar