Application of single-cell RNA sequencing in probing oligodendroglia heterogeneity and neurological disorders
Received date: 2022-11-07
Revised date: 2023-01-13
Online published: 2023-01-18
Supported by
the National Natural Science Foundation of China-Regional Fund(82060234);the Basic Research Projects in Yunnan Province(202101BE070001-065);the Science and Technology Talents and Platform Program of Yunnan Science and Technology Department(202005AE160019)
In the central nervous system, oligodendrocytes are highly specialized myelinating glial cells that originate from oligodendrocyte precursor cells. In the past, research centered on the oligodendrocyte development, myelination, and the role of oligodendrocyte lineage in neurological disorders. The emerging single-cell RNA sequencing technology is a new tool to specifically identify cell-types at the transcriptome level, and recently have also been used to investigate oligodendrocyte lineage-related issues. In this review, we summarize the recent developments of single-cell RNA sequencing technologies and their application in the oligodendroglia heterogeneity and neurological disorders, thereby providing new ideas and references for the utilization of single-cell RNA sequencing technology in the research field of oligodendrocyte lineage and neurological disorders.
Xi Han, Fucheng Luo . Application of single-cell RNA sequencing in probing oligodendroglia heterogeneity and neurological disorders[J]. Hereditas(Beijing), 2023 , 45(3) : 198 -211 . DOI: 10.16288/j.yczz.22-306
| [1] | Pepper RE, Pitman KA, Cullen CL, Young KM. How do cells of the oligodendrocyte lineage affect neuronal circuits to influence motor function, memory and mood? Front Cell Neurosci, 2018, 12, 399. |
| [2] | Fünfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, M?bius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA. Glycolytic oligodendrocytes maintain myelin and long- term axonal integrity. Nature, 2012, 485(7399): 517-521. |
| [3] | Tang FC, Barbacioru C, Wang YZ, Nordman E, Lee C, Xu NL, Wang XH, Bodeau J, Tuch BB, Siddiqui A, Lao KQ, Surani MA. mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods, 2009, 6(5), 377-382. |
| [4] | Islam S, Kj?llquist U, Moliner A, Zajac P, Fan JB, L?nnerberg P, Linnarsson S. Characterization of the single-cell transcriptional landscape by highly multiplex RNA-seq. Genome Res, 2011, 21(7): 1160-1167. |
| [5] | Ramsk?ld D, Luo SJ, Wang Y-C, Li R, Deng QL, Faridani OR, Daniels GA, Khrebtukova I, Loring JF, Laurent LC, Schroth GP, Sandberg R. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat Biotechnol, 2012, 30(8): 777-782. |
| [6] | Picelli S, Bj?rklund ?K, Faridani OR, Sagasser S, Winberg G, Sandberg R. Smart-seq 2 for sensitive full- length transcriptome profiling in single cells. Nat Methods, 2013, 10(11): 1096-1098. |
| [7] | Hashimshony T, Wagner F, Sher N, Yanai I. CEL-Seq: Single-cell RNA-Seq by multiplexed linear amplification. Cell Rep, 2012, 2(3): 666-673. |
| [8] | Kivioja T, V?h?rautio A, Karlsson K, Bonke M, Enge M, Linnarsson S, Taipale J. Counting absolute numbers of molecules using unique molecular identifiers. Nat Methods, 2012, 9(1): 72-74. |
| [9] | Hashimshony T, Senderovich N, Avital G, Klochendler A, de Leeuw Y, Anavy L, Gennert D, Li SQ, Livak KJ, Rozenblatt-Rosen O, Dor Y, Regev A, Yanai I. CEL-Seq2: sensitive highly-multiplexed single-cell RNA-Seq. Genome Biol, 2016, 17(1): 77. |
| [10] | Xin YR, Kim J, Ni M, Wei Y, Okamoto H, Lee J, Adler C, Cavino K, Murphy AJ, Yancopoulos GD, Lin HC, Gromada J. Use of the Fluidigm C1 platform for RNA sequencing of single mouse pancreatic islet cells. Proc Natl Acad Sci USA, 2016, 113(12): 3293-3298. |
| [11] | Pollen AA, Nowakowski TJ, Shuga J, Wang XH, Leyrat AA, Lui JH, Li NZ, Szpankowski L, Fowler B, Chen PL, Ramalingam N, Sun G, Thu M, Norris M, Lebofsky R, Toppani D, Kemp 2nd DW, Wong M, Clerkson B, Jones BN, Wu SQ, Knutsson L, Alvarado B, Wang J, Weaver LS, May AP, Jones RC, Unger MA, Kriegstein AR, West JAA. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat Biotechnol, 2014, 32(10): 1053-1058. |
| [12] | Macosko EZ, Basu A, Satija R, Nemesh J, Shekhar K, Goldman M, Tirosh I, Bialas AR, Kamitaki N, Martersteck EM, Trombetta JJ, Weitz DA, Sanes JR, Shalek AK, Regev A, McCarroll SA. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell, 2015, 161(5): 1202-1214. |
| [13] | Zheng GXY, Terry JM, Belgrader P, Ryvkin P, Bent ZW, Wilson R, Ziraldo SB, Wheeler TD, McDermott GP, Zhu JJ, Gregory MT, Shuga J, Montesclaros L, Underwood JG, Masquelier DA, Nishimura SY, Schnall-Levin M, Wyatt PW, Hindson CM, Bharadwaj R, Wong A, Ness KD, Beppu LW, Deeg HJ, McFarland C, Loeb KR, Valente WJ, Ericson NG, Stevens EA, Radich JP, Mikkelsen TS, Hindson BJ, Bielas JH. Massively parallel digital transcriptional profiling of single cells. Nat Commun, 2017, 8(1): 14049. |
| [14] | Fan HC, Fu GK, Fodor SPA. Expression profiling. Combinatorial labeling of single cells for gene expression cytometry. Science, 2015, 347(6222): 1258367. |
| [15] | Birey F, Andersen J, Makinson CD, Islam S, Wei W, Huber N, Fan HC, Metzler KRC, Panagiotakos G, Thom N, O’Rourke NA, Steinmetz LM, Bernstein JA, Hallmayer J, Huguenard JR, Pa?ca SP. Assembly of functionally integrated human forebrain spheroids. Nature, 2017, 545(7652): 54-59. |
| [16] | Svensson V, da Veiga Beltrame E, Pachter L. A curated database reveals trends in single-cell transcriptomics. Database(Oxford), 2020, 2020: baaa073. |
| [17] | Liu CY, Wu T, Fan F, Liu Y, Wu L, Junkin M, Wang ZF, Yu YY, Wang WM, Wei WB, Yuan Y, Wang MY, Cheng MN, Wei XY, Xu JS, Shi Q, Liu SP, Chen A, Wang O, Ni M, Zhang WW, Shang ZC, Lai YW, Guo PC, Ward C, Volpe G, Wang L, Zheng H, Liu Y, Peters BA, Beecher J, Zhang YW, Esteban MA, Hou Y, Xu X, Chen IJ, Liu LQ. A portable and cost-effective microfluidic system for massively parallel single-cell transcriptome profiling. BioRxiv, 2019. |
| [18] | Rodriguez-Meira A, Buck G, Clark SA, Povinelli BJ, Alcolea V, Louka E, McGowan S, Hamblin A, Sousos N, Barkas N, Giustacchini A, Psaila B, Jacobsen SEW, Thongjuea S, Mead AJ. Unravelling intratumoral heterogeneity through high-sensitivity single-cell mutational analysis and parallel RNA sequencing. Mol Cell, 2019, 73(6): 1292-1305.e8. |
| [19] | Zachariadis V, Cheng HT, Andrews N, Enge M. A highly scalable method for joint whole-genome sequencing and gene-expression profiling of single cells. Mol Cell, 2020, 80(3): 541-553.e5. |
| [20] | Mimitou EP, Lareau CA, Chen KY, Zorzetto-Fernandes AL, Hao YH, Takeshima Y, Luo W, Huang TS, Yeung BZ, Papalexi E, Thakore PI, Kibayashi T, Wing JB, Hata M, Satija R, Nazor KL, Sakaguchi S, Ludwig LS, Sankaran VG, Regev A, Smibert P. Scalable, multimodal profiling of chromatin accessibility, gene expression and protein levels in single cells. Nat Biotechnol, 2021, 39(10): 1246-1258. |
| [21] | Swanson E, Lord C, Reading J, Heubeck AT, Genge PC, Thomson Z, Weiss MD, Li XJ, Savage AK, Green RR, Torgerson TR, Bumol TF, Graybuck LT, Skene PJ. Simultaneous trimodal single-cell measurement of transcripts, epitopes, and chromatin accessibility using TEA-seq. ELife, 2021, 10: e63632. |
| [22] | Klein AM, Mazutis L, Akartuna I, Tallapragada N, Veres A, Li V, Peshkin L, Weitz DA, Kirschner MW. Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell, 2015, 161(5): 1187-1201. |
| [23] | Madissoon E, Wilbrey-Clark A, Miragaia RJ, Saeb-Parsy K, Mahbubani KT, Georgakopoulos N, Harding P, Polanski K, Huang N, Nowicki-Osuch K, Fitzgerald RC, Loudon KW, Ferdinand JR, Clatworthy MR, Tsingene A, van Dongen S, Dabrowska M, Patel M, Stubbington MJT, Teichmann SA, Stegle O, Meyer KB. scRNA-seq assessment of the human lung, spleen, and esophagus tissue stability after cold preservation. Genome Biol, 2020, 21(1): 1. |
| [24] | Harris RM, Kao H, Alarcon JM, Hofmann HA, Fenton AA. Hippocampal transcriptomic responses to enzyme- mediated cellular dissociation. Hippocampus, 2019, 29(9): 876-882. |
| [25] | Grindberg RV, Yee-Greenbaum JL, McConnell MJ, Novotny M, O’Shaughnessy AL, Lambert GM, Araúzo- Bravo MJ, Lee J, Fishman M, Robbins GE, Lin XY, Venepally P, Badger JH, Galbraith DW, Gage FH, Lasken RS. RNA-sequencing from single nuclei. Proc Natl Acad Sci USA, 2013, 110(49): 19802-19807. |
| [26] | Thrupp N, Sala Frigerio C, Wolfs L, Skene NG, Fattorelli N, Poovathingal S, Fourne Y, Matthews PM, Theys T, Mancuso R, de Strooper B, Fiers M. Single-nucleus RNA-Seq is not suitable for detection of microglial activation genes in humans. Cell Rep, 2020, 32(13): 108189. |
| [27] | Lassmann H. The birth of oligodendrocytes in the anatomical and neuropathological literature: the seminal contribution of Pío del Río-Hortega. Clin Neuropathol, 2012, 31(11): 435-436. |
| [28] | Marques S, Zeisel A, Codeluppi S, van Bruggen D, Mendanha Falc?o A, Xiao L, Li HL, H?ring M, Hochgerner H, Romanov RA, Gyllborg D, Mu?oz-Manchado A, La Manno G, L?nnerberg P, Floriddia EM, Rezayee F, Ernfors P, Arenas E, Hjerling-Leffler J, Harkany T, Richardson WD, Linnarsson S, Castelo-Branco G. Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science, 2016, 352(6291): 1326-1329. |
| [29] | Blum JA, Klemm S, Shadrach JL, Guttenplan KA, Nakayama L, Kathiria A, Hoang PT, Gautier O, Kaltschmidt JA, Greenleaf WJ, Gitler AD. Single-cell transcriptomic analysis of the adult mouse spinal cord reveals molecular diversity of autonomic and skeletal motor neurons. Nat Neurosci, 2021, 24(4): 572-583. |
| [30] | Floriddia EM, Louren?o T, Zhang SP, van Bruggen D, Hilscher MM, Kukanja P, Gon?alves Dos Santos JP, Alt?nk?k M, Yokota C, Llorens-Bobadilla E, Mulinyawe SB, Gr?os M, Sun LO, Frisén J, Nilsson M, Castelo- Branco G. Distinct oligodendrocyte populations have spatial preference and different responses to spinal cord injury. Nat Commun, 2020, 11(1): 5860. |
| [31] | Zeisel A, Hochgerner H, L?nnerberg P, Johnsson A, Memic F, van der Zwan J, H?ring M, Braun E, Borm LE, La Manno G, Codeluppi S, Furlan A, Lee K, Skene N, Harris KD, Hjerling-Leffler J, Arenas E, Ernfors P, Marklund U, Linnarsson S. Molecular architecture of the mouse nervous system. Cell, 2018, 174(4): 999-1014.e22. |
| [32] | Zeisel A, Mu?oz-Manchado AB, Codeluppi S, L?nnerberg P, La Manno G, Juréus A, Marques S, Munguba H, He LQ, Betsholtz C, Rolny C, Castelo-Branco G, Hjerling-Leffler J, Linnarsson S. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science, 2015, 347(6226): 1138-1142. |
| [33] | Huang W, Bhaduri A, Velmeshev D, Wang SH, Wang L, Rottkamp CA, Alvarez-Buylla A, Rowitch DH, Kriegstein AR. Origins and proliferative states of human oligodendrocyte precursor cells. Cell, 2020, 182(3): 594-608.e11. |
| [34] | Yin CH, Zhou X, Yao YG, Wang W, Wu Q, Wang XQ. Abundant self-amplifying intermediate progenitors in the subventricular zone of the Chinese tree shrew neocortex. Cereb Cortex, 2020, 30(5): 3370-3380. |
| [35] | Chamling X, Kallman A, Fang WX, Berlinicke CA, Mertz JL, Devkota P, Pantoja IEM, Smith MD, Ji ZC, Chang C, Kaushik A, Chen LB, Whartenby KA, Calabresi PA, Mao HQ, Ji HK, Wang TH, Zack DJ. Single-cell transcriptomic reveals molecular diversity and developmental heterogeneity of human stem cell-derived oligodendrocyte lineage cells. Nat Commun, 2021, 12(1): 652. |
| [36] | Buchanan J, Elabbady L, Collman F, Jorstad NL, Bakken TE, Ott C, Glatzer J, Bleckert AA, Bodor AL, Brittan D, Bumbarger DJ, Mahalingam G, Seshamani S, Schneider- Mizell C, Takeno MM, Torres R, Yin WJ, Hodge RD, Castro M, Dorkenwald S, Ih D, Jordan CS, Kemnitz N, Lee K, Lu R, Macrina T, Mu S, Popovych S, Silversmith WM, Tartavull I, Turner NL, Wilson AM, Wong W, Wu JP, Zlateski A, Zung J, Lippincott-Schwartz J, Lein ES, Seung HS, Bergles DE, Reid RC, da Costa NM. Oligodendrocyte precursor cells prune axons in the mouse neocortex. BioRxiv, 2021. |
| [37] | Habib N, Avraham-Davidi I, Basu A, Burks T, Shekhar K, Hofree M, Choudhury SR, Aguet F, Gelfand E, Ardlie K, Weitz DA, Rozenblatt-Rosen O, Zhang F, Regev A. Massively parallel single-nucleus RNA-seq with DroNc- seq. Nat Methods, 2017, 14(10): 955-958. |
| [38] | Haldipur P, Aldinger KA, Bernardo S, Deng M, Timms AE, Overman LM, Winter C, Lisgo SN, Razavi, Silvestri E, Manganaro L, Adle-Biassette H, Guimiot F, Russo R, Kidron D, Hof PR, Gerrelli D, Lindsay SJ, Dobyns WB, Glass IA, Alexandre P, Millen KJ. Spatiotemporal expansion of primary progenitor zones in the developing human cerebellum. Science, 2019, 366(6464): 454-460. |
| [39] | J?kel S, Agirre E, Mendanha Falc?o A, van Bruggen D, Lee KW, Knuesel I, Malhotra D, Ffrench-Constant C, Williams A, Castelo-Branco G. Altered human oligodendrocyte heterogeneity in multiple sclerosis. Nature, 2019, 566(7745): 543-547. |
| [40] | Falc?o AM, van Bruggen D, Marques S, Meijer M, J?kel S, Agirre E, Samudyata, Floriddia EM, Vanichkina DP, Ffrench-Constant C, Williams A, Guerreiro-Cacais AO, Castelo-Branco G. Disease-specific oligodendrocyte lineage cells arise in multiple sclerosis. Nat Med, 2018, 24(12): 1837-1844. |
| [41] | Lake BB, Chen S, Sos BC, Fan J, Kaeser GE, Yung YC, Duong TE, Gao D, Chun J, Kharchenko PV, Zhang K. Integrative single-cell analysis of transcriptional and epigenetic states in the human adult brain. Nat Biotechnol, 2018, 36(1): 70-80. |
| [42] | Kihara Y, Zhu YJ, Jonnalagadda D, Romanow W, Palmer C, Siddoway B, Rivera R, Dutta R, Trapp BD, Chun J. Single-nucleus RNA-seq of normal-appearing brain regions in relapsing-remitting vs. secondary progressive multiple sclerosis: implications for the efficacy of fingolimod. Front Cell Neurosci, 2022, 16: 918041. |
| [43] | Schirmer L, Velmeshev D, Holmqvist S, Kaufmann M, Werneburg S, Jung D, Vistnes S, Stockley JH, Young A, Steindel M, Tung B, Goyal N, Bhaduri A, Mayer S, Engler JB, Bayraktar OA, Franklin RJM, Haeussler M, Reynolds R, Schafer DP, Friese MA, Shiow LR, Kriegstein AR, Rowitch DH. Neuronal vulnerability and multilineage diversity in multiple sclerosis. Nature, 2019, 573(7772): 75-82. |
| [44] | Huang Y, Mucke L. Alzheimer mechanisms and therapeutic strategies. Cell, 2012, 148(6): 1204-1222. |
| [45] | Zalocusky KA, Najm R, Taubes AL, Hao YX, Yoon SY, Koutsodendris N, Nelson MR, Rao A, Bennett DA, Bant J, Amornkul DJ, Xu Q, An A, Cisne-Thomson O, Huang YD. Neuronal ApoE upregulates MHC-I expression to drive selective neurodegeneration in Alzheimer’s disease. Nat Neurosci, 2021, 24(6): 786-798. |
| [46] | Mathys H, Davila-Velderrain J, Peng ZY, Gao F, Mohammadi S, Young JZ, Menon M, He L, Abdurrob F, Jiang XQ, Martorell AJ, Ransohoff RM, Hafler BP, Bennett DA, Kellis M, Tsai LH. Single-cell transcriptomic analysis of Alzheimer’s disease. Nature, 2019, 570(7761): 332-337. |
| [47] | Grubman A, Chew G, Ouyang JF, Sun GZ, Choo XY, McLean C, Simmons RK, Buckberry S, Vargas-Landin DB, Poppe D, Pflueger J, Lister R, Rackham OJL, Petretto E, Polo JM. A single-cell atlas of entorhinal cortex from individuals with Alzheimer’s disease reveals cell-type- specific gene expression regulation. Nat Neurosci, 2019, 22(12): 2087-2097. |
| [48] | Morabito S, Miyoshi E, Michael N, Shahin S, Martini AC, Head E, Silva J, Leavy K, Perez-Rosendahl M, Swarup V. Single-nucleus chromatin accessibility and transcriptomic characterization of Alzheimer’s disease. Nat Genet, 2021, 53(8): 1143-1155. |
| [49] | Del-Aguila JL, Li Z, Dube U, Mihindukulasuriya KA, Budde JP, Fernandez MV, Ibanez L, Bradley J, Wang FX, Bergmann K, Davenport R, Morris JC, Holtzman DM, Perrin RJ, Benitez BA, Dougherty J, Cruchaga C, Harari O. A single-nuclei RNA sequencing study of Mendelian and sporadic AD in the human brain. Alzheimers Res Ther, 2019, 11(1): 71. |
| [50] | Reynolds RH, Botía J, Nalls MA, International Parkinson’s Disease Genomics Consortium (IPDGC), System Genomics of Parkinson’s Disease (SGPD), Hardy J, Gagliano Taliun SA, Ryten M. Moving beyond neurons: the role of cell type-specific gene regulation in Parkinson’s disease heritability. NPJ Park Dis, 2019, 5: 6. |
| [51] | Wang QQ, Wang CM, Ji BY, Zhou JW, Yang CQ, Chen J. Hapln2 in neurological diseases and its potential as therapeutic target. Front Aging Neurosci, 2019, 11: 60. |
| [52] | Teeple E, Joshi P, Pande R, Huang YY, Karambe A, Latta-Mahieu M, Sardi SP, Cedazo-Minguez A, Klinger KW, Flores-Morales A, Madden SL, Rajpal D, Kumar D. Single nuclei sequencing of human putamen oligodendrocytes reveals altered heterogeneity and disease-associated changes in Parkinson’s disease and multiple system atrophy. BioRxiv, 2021. |
| [53] | Smaji? S, Prada-Medina CA, Landoulsi Z, Ghelfi J, Delcambre S, Dietrich C, Jarazo J, Henck J, Balachandran S, Pachchek S, Morris CM, Antony P, Timmermann B, Sauer S, Pereira SL, Schwamborn JC, May P, Grünewald A, Spielmann M. Single-cell sequencing of human midbrain reveals glial activation and a Parkinson-specific neuronal state. Brain, 2022, 145(3): 964-978. |
| [54] | Adams L, Song MK, Tanaka Y, Kim YS. Single-nuclei paired multiomic analysis of young, aged, and Parkinson’s disease human midbrain reveals age- and disease- associated glial changes and their contribution to Parkinson’s disease. MedRxiv, 2022. |
| [55] | Al-Dalahmah O, Sosunov AA, Shaik A, Ofori K, Liu Y, Vonsattel JP, Adorjan I, Menon V, Goldman JE. Single- nucleus RNA-seq identifies Huntington disease astrocyte states. Acta Neuropathol Commun, 2020, 8(1): 19. |
| [56] | Malaiya S, Cortes-Gutierrez M, Herb BR, Coffey SR, Legg SRW, Cantle JP, Colantuoni C, Carroll JB, Ament SA. Single-nucleus RNA-Seq reveals dysregulation of striatal cell identity due to Huntington’s disease mutations. J Neurosci, 2021, 41(25): 5534-5552. |
| [57] | Ferrari Bardile C, Garcia-Miralles M, Caron NS, Rayan NA, Langley SR, Harmston N, Rondelli AM, Teo RTY, Waltl S, Anderson LM, Bae H-G, Jung S, Williams A, Prabhakar S, Petretto E, Hayden MR, Pouladi MA. Intrinsic mutant HTT-mediated defects in oligodendroglia cause myelination deficits and behavioral abnormalities in Huntington disease. Proc Natl Acad Sci USA, 2019, 116(19): 9622-9627. |
| [58] | Osipovitch M, Asenjo Martinez A, Mariani JN, Cornwell A, Dhaliwal S, Zou LS, Chandler-Militello D, Wang S, Li XJ, Benraiss SJ, Agate R, Lampp A, Benraiss A, Windrem MS, Goldman SA. Human ESC-derived chimeric mouse models of Huntington’s disease reveal cell-intrinsic defects in glial progenitor cell differentiation. Cell Stem Cell, 2019, 24(1): 107-122.e7. |
| [59] | Lim RG, Al-Dalahmah O, Wu J, Gold MP, Reidling JC, Tang GM, Adam M, Dansu D, Park H-J, Casaccia P, Miramontes R, Reyes-Ortiz AM, Lau A, Khan F, Paryani F, Tang A, Ofori K, Miyoshi E, Michael N, Geller N, Flowers XE, Vonsattel JP, Davidson S, Menon V, Swarup V, Fraenkel E, Goldman JE, Thompson LM. Single nuclei RNAseq analysis of HD mouse models and human brain reveals impaired oligodendrocyte maturation and potential role for thiamine metabolism. BioRxiv, 2022. |
| [60] | Nagy C, Maitra M, Tanti A, Suderman M, Théroux J-F, Davoli MA, Perlman K, Yerko V, Wang YC, Tripathy SJ, Pavlidis P, Mechawar N, Ragoussis J, Turecki G. Single-nucleus transcriptomics of the prefrontal cortex in major depressive disorder implicates oligodendrocyte precursor cells and excitatory neurons. Nat Neurosci, 2020, 23(6): 771-781. |
| [61] | Birey F, Kloc M, Chavali M, Hussein I, Wilson M, Christoffel DJ, Chen T, Frohman MA, Robinson JK, Russo SJ, Maffei A, Aguirre A.Genetic and stress-induced loss of NG 2 glia triggers emergence of depressive-like behaviors through reduced secretion of FGF2. Neuron, 2015, 88(5): 941-956. |
| [62] | Agarwal D, Sandor C, Volpato V, Caffrey TM, Monzón- Sandoval J, Bowden R, Alegre-Abarrategui J, Wade- Martins R, Webber C. A single-cell atlas of the human substantia nigra reveals cell-specific pathways associated with neurological disorders. Nat Commun, 2020, 11(1): 4183. |
| [63] | Yang AC, Kern F, Losada PM, Agam MR, Maat CA, Schmartz GP, Fehlmann T, Stein JA, Schaum N, Lee DP, Calcuttawala K, Vest RT, Berdnik D, Lu NN, Hahn O, Gate D, McNerney MW, Channappa D, Cobos I, Ludwig N, Schulz-Schaeffer WJ, Keller A, Wyss-Coray T.Dysregulation of brain and choroid plexus cell types in severe COVID-19. Nature, 2021, 595(7868), 565-571. |
| [64] | Benito-Kwiecinski S, Giandomenico SL, Sutcliffe M, Riis ES, Freire-Pritchett P, Kelava I, Wunderlich S, Martin U, Wray GA, McDole K, Lancaster MA. An early cell shape transition drives evolutionary expansion of the human forebrain. Cell, 2021, 184(8), 2084-2102.e19. |
| [65] | Chen A, Liao S, Cheng MN, Ma KL, Wu L, Lai YW, Qiu XJ, Yang J, Xu JS, Hao SJ, Wang X, Lu HF, Chen X, Liu X, Huang X, Li Z, Hong Y, Jiang YJ, Peng J, Liu S, Shen MZ, Liu CY, Li QS, Yuan Y, Wei XY, Zheng HW, Feng WM, Wang ZF, Liu Y, Wang ZH, Yang YZ, Xiang HT, Han L, Qin BM, Guo PC, Lai GY, Mu?oz-Cánoves P, Maxwell PH, Thiery JP, Wu Q-F, Zhao FX, Chen BC, Li M, Dai X, Wang S, Kuang HY, Hui JH, Wang LQ, Fei JF, Wang O, Wei XF, Lu HR, Wang B, Liu SP, Gu Y, Ni M, Zhang WW, Mu F, Yin Y, Yang HM, Lisby M, Cornall RJ, Mulder J, Uhlén M, Esteban MA, Li YX, Liu LQ, Xu X, Wang J. Spatiotemporal transcriptomic atlas of mouse organogenesis using DNA nanoball-patterned arrays. Cell, 2022, 185(10): 1777-1792.e21. |
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