Single-cell RNA Sequencing in Immunology

Page: [564 - 575] Pages: 12

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Abstract

The complex immune system is involved in multiple pathological processes. Single-cell RNA sequencing (scRNA-seq) is able to analyze complex cell mixtures correct to a single cell and single molecule, thus is qualified to analyze immune reactions in several diseases. In recent years, scRNA-seq has been applied in many researching fields and has presented many innovative results. In this review, we intend to provide an overview of single-cell RNA sequencing applications in immunology and a prospect of future directions.

Keywords: Single-cell RNA sequencing, immunology, cancer, autoimmune disease, transplantation, tumors.

Graphical Abstract

[1]
Furman, D.; Davis, M.M. New approaches to understanding the immune response to vaccination and infection. Vaccine, 2015, 33(40), 5271-5281.
[http://dx.doi.org/10.1016/j.vaccine.2015.06.117] [PMID: 26232539]
[2]
Massaia, A.; Chaves, P.; Samari, S.; Miragaia, R.J.; Meyer, K.; Teichmann, S.A.; Noseda, M. Single cell gene expression to understand the dynamic architecture of the heart. Front. Cardiovasc. Med., 2018, 5, 167.
[http://dx.doi.org/10.3389/fcvm.2018.00167] [PMID: 30525044]
[3]
Chen, H.; Ye, F.; Guo, G. Revolutionizing immunology with single-cell RNA sequencing. Cell. Mol. Immunol., 2019, 16(3), 242-249.
[http://dx.doi.org/10.1038/s41423-019-0214-4] [PMID: 30796351]
[4]
Papalexi, E.; Satija, R. Single-cell RNA sequencing to explore immune cell heterogeneity. Nat. Rev. Immunol., 2018, 18(1), 35-45.
[http://dx.doi.org/10.1038/nri.2017.76] [PMID: 28787399]
[5]
Luecken, M.D.; Theis, F.J. Current best practices in single-cell RNA-seq analysis: a tutorial. Mol. Syst. Biol., 2019, 15(6)e8746
[http://dx.doi.org/10.15252/msb.20188746] [PMID: 31217225]
[6]
Malone, A.F.; Wu, H.; Humphreys, B.D. Bringing renal biopsy interpretation into the molecular age with single-cell RNA sequencing. Semin. Nephrol., 2018, 38(1), 31-39.
[http://dx.doi.org/10.1016/j.semnephrol.2017.09.005] [PMID: 29291760]
[7]
Rosenberg, A.B.; Roco, C.M.; Muscat, R.A.; Kuchina, A.; Sample, P.; Yao, Z.; Graybuck, L.T.; Peeler, D.J.; Mukherjee, S.; Chen, W.; Pun, S.H.; Sellers, D.L.; Tasic, B.; Seelig, G. Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding. Science, 2018, 360(6385), 176-182.
[http://dx.doi.org/10.1126/science.aam8999] [PMID: 29545511]
[8]
Hashimshony, T.; Senderovich, N.; Avital, G.; Klochendler, A.; de Leeuw, Y.; Anavy, L.; Gennert, D.; Li, S.; Livak, K.J.; Rozenblatt-Rosen, O.; Dor, Y.; Regev, A.; Yanai, I. CEL-Seq2: sensitive highly-multiplexed single-cell RNA-Seq. Genome Biol., 2016, 17, 77.
[http://dx.doi.org/10.1186/s13059-016-0938-8] [PMID: 27121950]
[9]
Klein, A.M.; Mazutis, L.; Akartuna, I.; Tallapragada, N.; Veres, A.; Li, V.; Peshkin, L.; Weitz, D.A.; Kirschner, M.W. Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell, 2015, 161(5), 1187-1201.
[http://dx.doi.org/10.1016/j.cell.2015.04.044] [PMID: 26000487]
[10]
Parekh, S.; Ziegenhain, C.; Vieth, B.; Enard, W.; Hellmann, I. zUMIs - A fast and flexible pipeline to process RNA sequencing data with UMIs. Gigascience, 2018, 7(6)giy059
[http://dx.doi.org/10.1093/gigascience/giy059] [PMID: 29846586]
[11]
Griffiths, J.A.; Scialdone, A.; Marioni, J.C. Using single-cell genomics to understand developmental processes and cell fate decisions. Mol. Syst. Biol., 2018, 14(4)e8046
[http://dx.doi.org/10.15252/msb.20178046] [PMID: 29661792]
[12]
Cole, M.B.; Risso, D.; Wagner, A.; DeTomaso, D.; Ngai, J.; Purdom, E.; Dudoit, S.; Yosef, N. Performance assessment and selection of normalization procedures for single-cell RNA-seq. Cell Syst., 2019, 8(4), 315-328.e8.
[http://dx.doi.org/10.1016/j.cels.2019.03.010] [PMID: 31022373]
[13]
Chen, G.; Ning, B.; Shi, T. Single-cell RNA-seq technologies and related computational data analysis. Front. Genet., 2019, 10, 317.
[http://dx.doi.org/10.3389/fgene.2019.00317] [PMID: 31024627]
[14]
Ramsköld, D.; Luo, S.; Wang, Y-C.; Li, R.; Deng, Q.; Faridani, O.R.; Daniels, G.A.; Khrebtukova, I.; Loring, J.F.; Laurent, L.C.; Schroth, G.P.; Sandberg, R. Full-length mRNA-seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol., 2012, 30(8), 777-782.
[http://dx.doi.org/10.1038/nbt.2282] [PMID: 22820318]
[15]
Picelli, S.; Björklund, Å.K.; Faridani, O.R.; Sagasser, S.; Winberg, G.; Sandberg, R. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods, 2013, 10(11), 1096-1098.
[http://dx.doi.org/10.1038/nmeth.2639] [PMID: 24056875]
[16]
Mazutis, L.; Gilbert, J.; Ung, W.L.; Weitz, D.A.; Griffiths, A.D.; Heyman, J.A. Single-cell analysis and sorting using droplet-based microfluidics. Nat. Protoc., 2013, 8(5), 870-891.
[http://dx.doi.org/10.1038/nprot.2013.046] [PMID: 23558786]
[17]
Stewart, B.J.; Ferdinand, J.R.; Clatworthy, M.R. Using single-cell technologies to map the human immune system - implications for nephrology. Nat. Rev. Nephrol., 2019, 16(2), 112-128.
[PMID: 31831877]
[18]
De Simone, M.; Rossetti, G.; Pagani, M. Single cell T cell receptor sequencing: Techniques and future challenges. Front. Immunol., 2018, 9, 1638.
[http://dx.doi.org/10.3389/fimmu.2018.01638] [PMID: 30072991]
[19]
Kim, D.; Park, D. Deep sequencing of B cell receptor repertoire. BMB Rep., 2019, 52(9), 540-547.
[http://dx.doi.org/10.5483/BMBRep.2019.52.9.192] [PMID: 31383253]
[20]
Lovatt, D.; Ruble, B.K.; Lee, J.; Dueck, H.; Kim, T.K.; Fisher, S.; Francis, C.; Spaethling, J.M.; Wolf, J.A.; Grady, M.S.; Ulyanova, A.V.; Yeldell, S.B.; Griepenburg, J.C.; Buckley, P.T.; Kim, J.; Sul, J-Y.; Dmochowski, I.J.; Eberwine, J. Transcriptome in vivo analysis (TIVA) of spatially defined single cells in live tissue. Nat. Methods, 2014, 11(2), 190-196.
[http://dx.doi.org/10.1038/nmeth.2804] [PMID: 24412976]
[21]
Buenrostro, J.D.; Giresi, P.G.; Zaba, L.C.; Chang, H.Y.; Greenleaf, W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods, 2013, 10(12), 1213-1218.
[http://dx.doi.org/10.1038/nmeth.2688] [PMID: 24097267]
[22]
Buenrostro, J.D.; Wu, B.; Litzenburger, U.M.; Ruff, D.; Gonzales, M.L.; Snyder, M.P.; Chang, H.Y.; Greenleaf, W.J. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature, 2015, 523(7561), 486-490.
[http://dx.doi.org/10.1038/nature14590] [PMID: 26083756]
[23]
Park, J.; Shrestha, R.; Qiu, C.; Kondo, A.; Huang, S.; Werth, M.; Li, M.; Barasch, J.; Suszták, K. Single-cell transcriptomics of the mouse kidney reveals potential cellular targets of kidney disease. Science, 2018, 360(6390), 758-763.
[http://dx.doi.org/10.1126/science.aar2131] [PMID: 29622724]
[24]
Kriz, W.; Bankir, L. The Renal Commission of the International Union of Physiological Sciences (IUPS). A standard nomenclature for structures of the kidney. Kidney Int., 1988, 33(1), 1-7.
[http://dx.doi.org/10.1038/ki.1988.1] [PMID: 3352156]
[25]
See, P.; Dutertre, C-A.; Chen, J.; Günther, P.; McGovern, N.; Irac, S.E.; Gunawan, M.; Beyer, M.; Händler, K.; Duan, K.; Sumatoh, H.R.B.; Ruffin, N.; Jouve, M.; Gea-Mallorquí, E.; Hennekam, R.C.M.; Lim, T.; Yip, C.C.; Wen, M.; Malleret, B.; Low, I.; Shadan, N.B.; Fen, C.F.S.; Tay, A.; Lum, J.; Zolezzi, F.; Larbi, A.; Poidinger, M.; Chan, J.K.Y.; Chen, Q.; Rénia, L.; Haniffa, M.; Benaroch, P.; Schlitzer, A.; Schultze, J.L.; Newell, E.W.; Ginhoux, F. Mapping the human DC lineage through the integration of high-dimensional techniques. Science, 2017, 356(6342)eaag3009
[http://dx.doi.org/10.1126/science.aag3009] [PMID: 28473638]
[26]
Cella, M.; Jarrossay, D.; Facchetti, F.; Alebardi, O.; Nakajima, H.; Lanzavecchia, A.; Colonna, M. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med., 1999, 5(8), 919-923.
[http://dx.doi.org/10.1038/11360] [PMID: 10426316]
[27]
Schlitzer, A.; Loschko, J.; Mair, K.; Vogelmann, R.; Henkel, L.; Einwächter, H.; Schiemann, M.; Niess, J-H.; Reindl, W.; Krug, A. Identification of CCR9- murine plasmacytoid DC precursors with plasticity to differentiate into conventional DCs. Blood, 2011, 117(24), 6562-6570.
[http://dx.doi.org/10.1182/blood-2010-12-326678] [PMID: 21508410]
[28]
Ito, T.; Yang, M.; Wang, Y-H.; Lande, R.; Gregorio, J.; Perng, O.A.; Qin, X-F.; Liu, Y-J.; Gilliet, M. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J. Exp. Med., 2007, 204(1), 105-115.
[http://dx.doi.org/10.1084/jem.20061660] [PMID: 17200410]
[29]
Breton, G.; Lee, J.; Zhou, Y.J.; Schreiber, J.J.; Keler, T.; Puhr, S.; Anandasabapathy, N.; Schlesinger, S.; Caskey, M.; Liu, K.; Nussenzweig, M.C. Circulating precursors of human CD1c+ and CD141+ dendritic cells. J. Exp. Med., 2015, 212(3), 401-413.
[http://dx.doi.org/10.1084/jem.20141441] [PMID: 25687281]
[30]
Crinier, A.; Milpied, P.; Escalière, B.; Piperoglou, C.; Galluso, J.; Balsamo, A.; Spinelli, L.; Cervera-Marzal, I.; Ebbo, M.; Girard-Madoux, M.; Jaeger, S.; Bollon, E.; Hamed, S.; Hardwigsen, J.; Ugolini, S.; Vély, F.; Narni-Mancinelli, E.; Vivier, E. High-dimensional single-cell analysis identifies organ-specific signatures and conserved NK cell subsets in humans and mice. Immunity, 2018, 49(5), 971-986.e5.
[http://dx.doi.org/10.1016/j.immuni.2018.09.009] [PMID: 30413361]
[31]
Masopust, D.; Soerens, A.G. Tissue-resident T cells and other resident leukocytes. Annu. Rev. Immunol., 2019, 37, 521-546.
[http://dx.doi.org/10.1146/annurev-immunol-042617-053214] [PMID: 30726153]
[32]
Guha, A.; Vasconcelos, M.; Cai, Y.; Yoneda, M.; Hinds, A.; Qian, J.; Li, G.; Dickel, L.; Johnson, J.E.; Kimura, S.; Guo, J.; McMahon, J.; McMahon, A.P.; Cardoso, W.V. Neuroepithelial body microenvironment is a niche for a distinct subset of Clara-like precursors in the developing airways. Proc. Natl. Acad. Sci. USA, 2012, 109(31), 12592-12597.
[http://dx.doi.org/10.1073/pnas.1204710109] [PMID: 22797898]
[33]
Xu, Y.; Wang, Y.; Besnard, V.; Ikegami, M.; Wert, S.E.; Heffner, C.; Murray, S.A.; Donahue, L.R.; Whitsett, J.A. Transcriptional programs controlling perinatal lung maturation. PLoS One, 2012, 7(8)e37046
[http://dx.doi.org/10.1371/journal.pone.0037046] [PMID: 22916088]
[34]
Treutlein, B.; Brownfield, D.G.; Wu, A.R.; Neff, N.F.; Mantalas, G.L.; Espinoza, F.H.; Desai, T.J.; Krasnow, M.A.; Quake, S.R. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature, 2014, 509(7500), 371-375.
[http://dx.doi.org/10.1038/nature13173] [PMID: 24739965]
[35]
Bunders, M.J.; van der Loos, C.M.; Klarenbeek, P.L.; van Hamme, J.L.; Boer, K.; Wilde, J.C.H.; de Vries, N.; van Lier, R.A.W.; Kootstra, N.; Pals, S.T.; Kuijpers, T.W. Memory CD4(+)CCR5(+) T cells are abundantly present in the gut of newborn infants to facilitate mother-to-child transmission of HIV-1. Blood, 2012, 120(22), 4383-4390.
[http://dx.doi.org/10.1182/blood-2012-06-437566] [PMID: 23033270]
[36]
Li, N.; van Unen, V.; Abdelaal, T.; Guo, N.; Kasatskaya, S.A.; Ladell, K.; McLaren, J.E.; Egorov, E.S.; Izraelson, M.; Chuva de Sousa Lopes, S.M.; Höllt, T.; Britanova, O.V.; Eggermont, J.; de Miranda, N.F.C.C.; Chudakov, D.M.; Price, D.A.; Lelieveldt, B.P.F.; Koning, F. Memory CD4+ T cells are generated in the human fetal intestine. Nat. Immunol., 2019, 20(3), 301-312.
[http://dx.doi.org/10.1038/s41590-018-0294-9] [PMID: 30664737]
[37]
Saelens, W.; Cannoodt, R.; Todorov, H.; Saeys, Y. A comparison of single-cell trajectory inference methods. Nat. Biotechnol., 2019, 37(5), 547-554.
[http://dx.doi.org/10.1038/s41587-019-0071-9] [PMID: 30936559]
[38]
Wagner, A.; Regev, A.; Yosef, N. Revealing the vectors of cellular identity with single-cell genomics. Nat. Biotechnol., 2016, 34(11), 1145-1160.
[http://dx.doi.org/10.1038/nbt.3711] [PMID: 27824854]
[39]
Farhadian, S.F.; Mehta, S.S.; Zografou, C.; Robertson, K.; Price, R.W.; Pappalardo, J.; Chiarella, J.; Hafler, D.A.; Spudich, S.S. Single-cell RNA sequencing reveals microglia-like cells in cerebrospinal fluid during virologically suppressed HIV. JCI Insight, 2018, 3(18)121718
[http://dx.doi.org/10.1172/jci.insight.121718] [PMID: 30232286]
[40]
Keren-Shaul, H.; Spinrad, A.; Weiner, A.; Matcovitch-Natan, O.; Dvir-Szternfeld, R.; Ulland, T.K.; David, E.; Baruch, K.; Lara-Astaiso, D.; Toth, B.; Itzkovitz, S.; Colonna, M.; Schwartz, M.; Amit, I. A unique microglia type associated with restricting development of Alzheimer’s disease. Cell, 2017, 169(7), 1276-1290.e17.
[http://dx.doi.org/10.1016/j.cell.2017.05.018] [PMID: 28602351]
[41]
Krasemann, S.; Madore, C.; Cialic, R.; Baufeld, C.; Calcagno, N.; El Fatimy, R.; Beckers, L.; O’Loughlin, E.; Xu, Y.; Fanek, Z.; Greco, D.J.; Smith, S.T.; Tweet, G.; Humulock, Z.; Zrzavy, T.; Conde-Sanroman, P.; Gacias, M.; Weng, Z.; Chen, H.; Tjon, E.; Mazaheri, F.; Hartmann, K.; Madi, A.; Ulrich, J.D.; Glatzel, M.; Worthmann, A.; Heeren, J.; Budnik, B.; Lemere, C.; Ikezu, T.; Heppner, F.L.; Litvak, V.; Holtzman, D.M.; Lassmann, H.; Weiner, H.L.; Ochando, J.; Haass, C.; Butovsky, O. The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity, 2017, 47(3), 566-581.e9.
[http://dx.doi.org/10.1016/j.immuni.2017.08.008] [PMID: 28930663]
[42]
Adam, M.; Potter, A.S.; Potter, S.S. Psychrophilic proteases dramatically reduce single-cell RNA-seq artifacts: a molecular atlas of kidney development. Development, 2017, 144(19), 3625-3632.
[http://dx.doi.org/10.1242/dev.151142] [PMID: 28851704]
[43]
Lu, Y.; Ye, Y.; Yang, Q.; Shi, S. Single-cell RNA-sequence analysis of mouse glomerular mesangial cells uncovers mesangial cell essential genes. Kidney Int., 2017, 92(2), 504-513.
[http://dx.doi.org/10.1016/j.kint.2017.01.016] [PMID: 28320530]
[44]
Halpern, K.B.; Shenhav, R.; Matcovitch-Natan, O.; Toth, B.; Lemze, D.; Golan, M.; Massasa, E.E.; Baydatch, S.; Landen, S.; Moor, A.E.; Brandis, A.; Giladi, A.; Avihail, A.S.; David, E.; Amit, I.; Itzkovitz, S. Single-cell spatial reconstruction reveals global division of labour in the mammalian liver. Nature, 2017, 542(7641), 352-356.
[http://dx.doi.org/10.1038/nature21065] [PMID: 28166538]
[45]
MacParland, S.A.; Liu, J.C.; Ma, X-Z.; Innes, B.T.; Bartczak, A.M.; Gage, B.K.; Manuel, J.; Khuu, N.; Echeverri, J.; Linares, I.; Gupta, R.; Cheng, M.L.; Liu, L.Y.; Camat, D.; Chung, S.W.; Seliga, R.K.; Shao, Z.; Lee, E.; Ogawa, S.; Ogawa, M.; Wilson, M.D.; Fish, J.E.; Selzner, M.; Ghanekar, A.; Grant, D.; Greig, P.; Sapisochin, G.; Selzner, N.; Winegarden, N.; Adeyi, O.; Keller, G.; Bader, G.D.; McGilvray, I.D. Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations. Nat. Commun., 2018, 9(1), 4383.
[http://dx.doi.org/10.1038/s41467-018-06318-7] [PMID: 30348985]
[46]
Peng, J.; Sun, B.F.; Chen, C.Y.; Zhou, J.Y.; Chen, Y.S.; Chen, H.; Liu, L.; Huang, D.; Jiang, J.; Cui, G.S.; Yang, Y.; Wang, W.; Guo, D.; Dai, M.; Guo, J.; Zhang, T.; Liao, Q.; Liu, Y.; Zhao, Y.L.; Han, D.L.; Zhao, Y.; Yang, Y.G.; Wu, W. Single-cell RNA-seq highlights intra-tumoral heterogeneity and malignant progression in pancreatic ductal adenocarcinoma. Cell Res., 2019, 29(9), 725-738.
[http://dx.doi.org/10.1038/s41422-019-0195-y] [PMID: 31273297]
[47]
Scheper, W.; Kelderman, S.; Fanchi, L.F.; Linnemann, C.; Bendle, G.; de Rooij, M.A.J.; Hirt, C.; Mezzadra, R.; Slagter, M.; Dijkstra, K.; Kluin, R.J.C.; Snaebjornsson, P.; Milne, K.; Nelson, B.H.; Zijlmans, H.; Kenter, G.; Voest, E.E.; Haanen, J.B.A.G.; Schumacher, T.N. Low and variable tumor reactivity of the intratumoral TCR repertoire in human cancers. Nat. Med., 2019, 25(1), 89-94.
[http://dx.doi.org/10.1038/s41591-018-0266-5] [PMID: 30510250]
[48]
Zheng, C.; Zheng, L.; Yoo, J-K.; Guo, H.; Zhang, Y.; Guo, X.; Kang, B.; Hu, R.; Huang, J.Y.; Zhang, Q.; Liu, Z.; Dong, M.; Hu, X.; Ouyang, W.; Peng, J.; Zhang, Z. Landscape of infiltrating T cells in liver cancer revealed by single-cell sequencing. Cell, 2017, 169(7), 1342-1356.e16.
[http://dx.doi.org/10.1016/j.cell.2017.05.035] [PMID: 28622514]
[49]
Hindley, J.P.; Ferreira, C.; Jones, E.; Lauder, S.N.; Ladell, K.; Wynn, K.K.; Betts, G.J.; Singh, Y.; Price, D.A.; Godkin, A.J.; Dyson, J.; Gallimore, A. Analysis of the T-cell receptor repertoires of tumor-infiltrating conventional and regulatory T cells reveals no evidence for conversion in carcinogen-induced tumors. Cancer Res., 2011, 71(3), 736-746.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-1797] [PMID: 21156649]
[50]
Plitas, G.; Konopacki, C.; Wu, K.; Bos, P.D.; Morrow, M.; Putintseva, E.V.; Chudakov, D.M.; Rudensky, A.Y.; Regulatory, T. Regulatory T cells exhibit distinct features in human breast cancer. Immunity, 2016, 45(5), 1122-1134.
[http://dx.doi.org/10.1016/j.immuni.2016.10.032] [PMID: 27851913]
[51]
Zilionis, R.; Engblom, C.; Pfirschke, C.; Savova, V.; Zemmour, D.; Saatcioglu, H.D.; Krishnan, I.; Maroni, G.; Meyerovitz, C.V.; Kerwin, C.M.; Choi, S.; Richards, W.G.; De Rienzo, A.; Tenen, D.G.; Bueno, R.; Levantini, E.; Pittet, M.J.; Klein, A.M. Single-cell transcriptomics of human and mouse lung cancers reveals conserved myeloid populations across individuals and species. Immunity, 2019, 50(5), 1317-1334.e10.
[http://dx.doi.org/10.1016/j.immuni.2019.03.009] [PMID: 30979687]
[52]
Zhang, L.; Yu, X.; Zheng, L.; Zhang, Y.; Li, Y.; Fang, Q.; Gao, R.; Kang, B.; Zhang, Q.; Huang, J.Y.; Konno, H.; Guo, X.; Ye, Y.; Gao, S.; Wang, S.; Hu, X.; Ren, X.; Shen, Z.; Ouyang, W.; Zhang, Z. Lineage tracking reveals dynamic relationships of T cells in colorectal cancer. Nature, 2018, 564(7735), 268-272.
[http://dx.doi.org/10.1038/s41586-018-0694-x] [PMID: 30479382]
[53]
Wei, S.C.; Levine, J.H.; Cogdill, A.P.; Zhao, Y.; Anang, N.A.S.; Andrews, M.C.; Sharma, P.; Wang, J.; Wargo, J.A.; Pe’er, D.; Allison, J.P. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell, 2017, 170(6), 1120-1133.e17.
[http://dx.doi.org/10.1016/j.cell.2017.07.024] [PMID: 28803728]
[54]
Guo, X.; Zhang, Y.; Zheng, L.; Zheng, C.; Song, J.; Zhang, Q.; Kang, B.; Liu, Z.; Jin, L.; Xing, R.; Gao, R.; Zhang, L.; Dong, M.; Hu, X.; Ren, X.; Kirchhoff, D.; Roider, H.G.; Yan, T.; Zhang, Z. Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing. Nat. Med., 2018, 24(7), 978-985.
[http://dx.doi.org/10.1038/s41591-018-0045-3] [PMID: 29942094]
[55]
Giustacchini, A.; Thongjuea, S.; Barkas, N.; Woll, P.S.; Povinelli, B.J.; Booth, C.A.G.; Sopp, P.; Norfo, R.; Rodriguez-Meira, A.; Ashley, N.; Jamieson, L.; Vyas, P.; Anderson, K.; Segerstolpe, Å.; Qian, H.; Olsson-Strömberg, U.; Mustjoki, S.; Sandberg, R.; Jacobsen, S.E.W.; Mead, A.J. Single-cell transcriptomics uncovers distinct molecular signatures of stem cells in chronic myeloid leukemia. Nat. Med., 2017, 23(6), 692-702.
[http://dx.doi.org/10.1038/nm.4336] [PMID: 28504724]
[56]
Landau, D.A.; Tausch, E.; Taylor-Weiner, A.N.; Stewart, C.; Reiter, J.G.; Bahlo, J.; Kluth, S.; Bozic, I.; Lawrence, M.; Böttcher, S.; Carter, S.L.; Cibulskis, K.; Mertens, D.; Sougnez, C.L.; Rosenberg, M.; Hess, J.M.; Edelmann, J.; Kless, S.; Kneba, M.; Ritgen, M.; Fink, A.; Fischer, K.; Gabriel, S.; Lander, E.S.; Nowak, M.A.; Döhner, H.; Hallek, M.; Neuberg, D.; Getz, G.; Stilgenbauer, S.; Wu, C.J. Mutations driving CLL and their evolution in progression and relapse. Nature, 2015, 526(7574), 525-530.
[http://dx.doi.org/10.1038/nature15395] [PMID: 26466571]
[57]
Wang, L.; Fan, J.; Francis, J.M.; Georghiou, G.; Hergert, S.; Li, S.; Gambe, R.; Zhou, C.W.; Yang, C.; Xiao, S.; Cin, P.D.; Bowden, M.; Kotliar, D.; Shukla, S.A.; Brown, J.R.; Neuberg, D.; Alessi, D.R.; Zhang, C-Z.; Kharchenko, P.V.; Livak, K.J.; Wu, C.J. Integrated single-cell genetic and transcriptional analysis suggests novel drivers of chronic lymphocytic leukemia. Genome Res., 2017, 27(8), 1300-1311.
[http://dx.doi.org/10.1101/gr.217331.116] [PMID: 28679620]
[58]
Zheng, G.X.Y.; Terry, J.M.; Belgrader, P.; Ryvkin, P.; Bent, Z.W.; Wilson, R.; Ziraldo, S.B.; Wheeler, T.D.; McDermott, G.P.; Zhu, J.; Gregory, M.T.; Shuga, J.; Montesclaros, L.; Underwood, J.G.; Masquelier, D.A.; Nishimura, S.Y.; Schnall-Levin, M.; Wyatt, P.W.; Hindson, C.M.; Bharadwaj, R.; Wong, A.; Ness, K.D.; Beppu, L.W.; Deeg, H.J.; McFarland, C.; Loeb, K.R.; Valente, W.J.; Ericson, N.G.; Stevens, E.A.; Radich, J.P.; Mikkelsen, T.S.; Hindson, B.J.; Bielas, J.H. Massively parallel digital transcriptional profiling of single cells. Nat. Commun., 2017, 8, 14049.
[http://dx.doi.org/10.1038/ncomms14049] [PMID: 28091601]
[59]
Stephenson, W.; Donlin, L.T.; Butler, A.; Rozo, C.; Bracken, B.; Rashidfarrokhi, A.; Goodman, S.M.; Ivashkiv, L.B.; Bykerk, V.P.; Orange, D.E.; Darnell, R.B.; Swerdlow, H.P.; Satija, R. Single-cell RNA-seq of rheumatoid arthritis synovial tissue using low-cost microfluidic instrumentation. Nat. Commun., 2018, 9(1), 791.
[http://dx.doi.org/10.1038/s41467-017-02659-x] [PMID: 29476078]
[60]
Kernfeld, E.M.; Genga, R.M.J.; Neherin, K.; Magaletta, M.E.; Xu, P.; Maehr, R. A single-cell transcriptomic atlas of thymus organogenesis resolves cell types and developmental maturation. Immunity, 2018, 48(6), 1258-1270.e6.
[http://dx.doi.org/10.1016/j.immuni.2018.04.015] [PMID: 29884461]
[61]
Martin, J.C.; Chang, C.; Boschetti, G.; Ungaro, R.; Giri, M.; Grout, J.A.; Gettler, K.; Chuang, L-S.; Nayar, S.; Greenstein, A.J.; Dubinsky, M.; Walker, L.; Leader, A.; Fine, J.S.; Whitehurst, C.E.; Mbow, M.L.; Kugathasan, S.; Denson, L.A.; Hyams, J.S.; Friedman, J.R.; Desai, P.T.; Ko, H.M.; Laface, I.; Akturk, G.; Schadt, E.E.; Salmon, H.; Gnjatic, S.; Rahman, A.H.; Merad, M.; Cho, J.H.; Kenigsberg, E. Single-cell analysis of crohn’s disease lesions identifies a pathogenic cellular module associated with resistance to anti-TNF therapy. Cell, 2019, 178(6), 1493-1508.e20.
[http://dx.doi.org/10.1016/j.cell.2019.08.008] [PMID: 31474370]
[62]
Der, E.; Ranabothu, S.; Suryawanshi, H.; Akat, K.M.; Clancy, R.; Morozov, P.; Kustagi, M.; Czuppa, M.; Izmirly, P.; Belmont, H.M.; Wang, T.; Jordan, N.; Bornkamp, N.; Nwaukoni, J.; Martinez, J.; Goilav, B.; Buyon, J.P.; Tuschl, T.; Putterman, C. Single cell RNA sequencing to dissect the molecular heterogeneity in lupus nephritis. JCI Insight, 2017, 2(9), 93009.
[http://dx.doi.org/10.1172/jci.insight.93009] [PMID: 28469080]
[63]
Dangi, A.; Yu, S.; Luo, X. Emerging approaches and technologies in transplantation: the potential game changers. Cell. Mol. Immunol., 2019, 16(4), 334-342.
[http://dx.doi.org/10.1038/s41423-019-0207-3] [PMID: 30760918]
[64]
Wu, H.; Malone, A.F.; Donnelly, E.L.; Kirita, Y.; Uchimura, K.; Ramakrishnan, S.M.; Gaut, J.P.; Humphreys, B.D. Single-cell transcriptomics of a human kidney allograft biopsy specimen defines a diverse inflammatory response. J. Am. Soc. Nephrol., 2018, 29(8), 2069-2080.
[http://dx.doi.org/10.1681/ASN.2018020125] [PMID: 29980650]
[65]
Reyfman, P.A.; Walter, J.M.; Joshi, N.; Anekalla, K.R.; McQuattie-Pimentel, A.C.; Chiu, S.; Fernandez, R.; Akbarpour, M.; Chen, C-I.; Ren, Z.; Verma, R.; Abdala-Valencia, H.; Nam, K.; Chi, M.; Han, S.; Gonzalez-Gonzalez, F.J.; Soberanes, S.; Watanabe, S.; Williams, K.J.N.; Flozak, A.S.; Nicholson, T.T.; Morgan, V.K.; Hrusch, C.L.; Guzy, R.D.; Bonham, C.A.; Sperling, A.I.; Bag, R.; Hamanaka, R.B.; Mutlu, G.M.; Yeldandi, A.V.; Marshall, S.A.; Shilatifard, A.; Amaral, L.A.N.; Perlman, H.; Sznajder, J.I.; Winter, D.R.; Hinchcliff, M.; Argento, A.C.; Gillespie, C.T.; D’Amico Dematte, J.; Jain, M.; Singer, B.D.; Ridge, K.M.; Gottardi, C.J.; Lam, A.P.; Bharat, A.; Bhorade, S.M.; Budinger, G.R.S.; Misharin, A.V. Single-cell transcriptomic analysis of human lung reveals complex multicellular changes during pulmonary fibrosis. Am. J. Respir. Crit. Care Med., 2019, 199(12), 1517-1536.
[66]
Weigt, S.S.; Wang, X.; Palchevskiy, V.; Gregson, A.L.; Patel, N.; DerHovanessian, A.; Shino, M.Y.; Sayah, D.M.; Birjandi, S.; Lynch, J.P., III; Saggar, R.; Ardehali, A.; Ross, D.J.; Palmer, S.M.; Elashoff, D.; Belperio, J.A. Gene expression profiling of bronchoalveolar lavage cells preceding a clinical diagnosis of chronic lung allograft dysfunction. PLoS One, 2017, 12(1)e0169894
[http://dx.doi.org/10.1371/journal.pone.0169894] [PMID: 28103284]
[67]
Mimitou, E.P.; Cheng, A.; Montalbano, A.; Hao, S.; Stoeckius, M.; Legut, M.; Roush, T.; Herrera, A.; Papalexi, E.; Ouyang, Z.; Satija, R.; Sanjana, N.E.; Koralov, S.B.; Smibert, P. Multiplexed detection of proteins, transcriptomes, clonotypes and CRISPR perturbations in single cells. Nat. Methods, 2019, 16(5), 409-412.
[http://dx.doi.org/10.1038/s41592-019-0392-0] [PMID: 31011186]
[68]
Wu, H.; Kirita, Y.; Donnelly, E.L.; Humphreys, B.D. Advantages of single-nucleus over single-cell RNA sequencing of adult kidney: rare cell types and novel cell states revealed in fibrosis. J. Am. Soc. Nephrol., 2019, 30(1), 23-32.
[http://dx.doi.org/10.1681/ASN.2018090912] [PMID: 30510133]
[69]
Masuda, T.; Sankowski, R.; Staszewski, O.; Böttcher, C.; Amann, L. Sagar; Scheiwe, C.; Nessler, S.; Kunz, P.; van Loo, G.; Coenen, V.A.; Reinacher, P.C.; Michel, A.; Sure, U.; Gold, R.; Grün, D.; Priller, J.; Stadelmann, C.; Prinz, M. Spatial and temporal heterogeneity of mouse and human microglia at single-cell resolution. Nature, 2019, 566(7744), 388-392.
[http://dx.doi.org/10.1038/s41586-019-0924-x] [PMID: 30760929]
[70]
See, P.; Lum, J.; Chen, J.; Ginhoux, F. A single-cell sequencing guide for immunologists. Front. Immunol., 2018, 9, 2425.
[http://dx.doi.org/10.3389/fimmu.2018.02425] [PMID: 30405621]
[71]
Shum, E.Y.; Walczak, E.M.; Chang, C.; Christina Fan, H. Quantitation of mRNA transcripts and proteins using the BD Rhapsody™ single-cell analysis system. Adv. Exp. Med. Biol., 2019, 1129, 63-79.
[http://dx.doi.org/10.1007/978-981-13-6037-4_5] [PMID: 30968361]
[72]
Zhang, X.; Li, T.; Liu, F.; Chen, Y.; Yao, J.; Li, Z.; Huang, Y.; Wang, J. Comparative analysis of droplet-based ultra-high-throughput single-cell RNA-seq systems. Mol. Cell, 2019, 73(1), 130-142.e5.
[http://dx.doi.org/10.1016/j.molcel.2018.10.020] [PMID: 30472192]
[73]
Goldstein, L.D.; Chen, Y-J.J.; Dunne, J.; Mir, A.; Hubschle, H.; Guillory, J.; Yuan, W.; Zhang, J.; Stinson, J.; Jaiswal, B.; Pahuja, K.B.; Mann, I.; Schaal, T.; Chan, L.; Anandakrishnan, S.; Lin, C-W.; Espinoza, P.; Husain, S.; Shapiro, H.; Swaminathan, K.; Wei, S.; Srinivasan, M.; Seshagiri, S.; Modrusan, Z. Massively parallel nanowell-based single-cell gene expression profiling. BMC Genomics, 2017, 18(1), 519.
[http://dx.doi.org/10.1186/s12864-017-3893-1] [PMID: 28687070]
[74]
Ashton, J.M.; Rehrauer, H.; Myers, J.; Myers, J.; Zanche, M.; Balys, M.; Foox, J.; Mason, C.E.; Steen, R.; Kuentzel, M.; Aquino, C.; Garcia-Reyero, N.; Chittur, S.V. Comparative analysis of single-cell RNA sequencing platforms and methods. bioRxiv, 2020.
[http://dx.doi.org/10.1101/2020.07.20.212100]
[75]
Huang, X.T.; Li, X.; Qin, P.Z.; Zhu, Y.; Xu, S.N.; Chen, J.P. Technical advances in single-cell rna sequencing and applications in normal and malignant hematopoiesis. Front. Oncol., 2018, 8, 582.
[http://dx.doi.org/10.3389/fonc.2018.00582] [PMID: 30581771]