The Technology and Biology of Single-Cell RNA Sequencing

Molecular Cell

Volumn 58, Issue 4, 2015, Pages 610-620

  Kolodziejczyk, Aleksandra A ^a,b   Kim, Jong Kyoung ^a   Svensson, Valentine ^a   Marioni, John C ^a,b   Teichmann, Sarah A ^a,b  

^a EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

BIOINFORMATICS; GENE EXPRESSION; GENE REGULATORY NETWORK; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; REVERSE TRANSCRIPTION; REVIEW; RNA SEQUENCE; SINGLE CELL ANALYSIS; ALTERNATIVE RNA SPLICING; ANIMAL; BIOLOGICAL MODEL; CELL LINEAGE; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENETICS; PROCEDURES; SEQUENCE ANALYSIS;

ALTERNATIVE SPLICING; ANIMALS; CELL LINEAGE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENETIC VARIATION; HUMANS; MODELS, GENETIC; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS;

EID: 84929687805     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.04.005     Document Type: Review

References (85)

1. Amirel A.D., Davis K.L., Tadmor M.D., Simonds E.F., Levine J.H., Bendall S.C., Shenfeld D.K., Krishnaswamy S., Nolan G.P., Pe'er D. viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia. Nat. Biotechnol. 2013, 31:545-552.
2. Bar-Even A., Paulsson J., Maheshri N., Carmi M., O'Shea E., Pilpel Y., Barkai N. Noise in protein expression scales with natural protein abundance. Nat. Genet. 2006, 38:636-643.
3. Behjati S., Huch M., van Boxtel R., Karthaus W., Wedge D.C., Tamuri A.U., Martincorena I., Petljak M., Alexandrov L.B., Gundem G., et al. Genome sequencing of normal cells reveals developmental lineages and mutational processes. Nature 2014, 513:422-425.
4. Bendall S.C., Davis K.L., Amir A.D., Tadmor M.D., Simonds E.F., Chen T.J., Shenfeld D.K., Nolan G.P., Pe'er D. Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development. Cell 2014, 157:714-725.
5. Bengtsson M., Hemberg M., Rorsman P., Ståhlberg A. Quantification of mRNA in single cells and modelling of RT-qPCR induced noise. BMC Mol. Biol. 2008, 9:63.
6. Bhargava V., Ko P., Willems E., Mercola M., Subramaniam S. Quantitative transcriptomics using designed primer-based amplification. Sci. Rep. 2013, 3:1740.
7. Blake W.J., KAErn M., Cantor C.R., Collins J.J. Noise in eukaryotic gene expression. Nature 2003, 422:633-637.
8. Bowsher C.G., Swain P.S. Identifying sources of variation and theflow of information in biochemical networks. Proc. Natl. Acad. Sci. USA 2012, 109:E1320-E1328.
9. Brennecke P., Anders S., Kim J.K., Kołodziejczyk A.A., Zhang X., Proserpio V., Baying B., Benes V., Teichmann S.A., Marioni J.C., Heisler M.G. Accounting for technical noise in single-cell RNA-seq experiments. Nat. Methods 2013, 10:1093-1095.
10. Buettner F., Natarajan K.N., Casale F.P., Proserpio V., Scialdone A., Theis F.J., Teichmann S.A., Marioni J.C., Stegle O. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat. Biotechnol. 2015, 33:155-160.
11. Cloonan N., Forrest A.R., Kolle G., Gardiner B.B., Faulkner G.J., Brown M.K., Taylor D.F., Steptoe A.L., Wani S., Bethel G., et al. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat. Methods 2008, 5:613-619.
12. Crosetto N., Bienko M., van Oudenaarden A. Spatially resolved transcriptomics and beyond. Nat. Rev. Genet. 2015, 16:57-66.
13. Deng Q., Ramsköld D., Reinius B., Sandberg R. Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science 2014, 343:193-196.
14. Dey S.S., Kester L., Spanjaard B., Bienko M., van Oudenaarden A. Integrated genome and transcriptome sequencing of the same cell. Nat. Biotechnol. 2015, 33:285-289.
15. Eberwine J., Yeh H., Miyashiro K., Cao Y., Nair S., Finnell R., Zettel M., Coleman P. Analysis of gene expression in single live neurons. Proc. Natl. Acad. Sci. USA 1992, 89:3010-3014.
16. Elowitz M.B., Levine A.J., Siggia E.D., Swain P.S. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
17. Fan H.C., Fu G.K., Fodor S.P. Expression profiling. Combinatorial labeling of single cells for gene expression cytometry. Science 2015, 347:1258367.
18. Femino A.M., Fay F.S., Fogarty K., Singer R.H. Visualization of single RNA transcripts insitu. Science 1998, 280:585-590.
19. Frumkin D., Wasserstrom A., Itzkovitz S., Harmelin A., Rechavi G., Shapiro E. Amplification of multiple genomic loci from single cells isolated by laser micro-dissection of tissues. BMC Biotechnol. 2008, 8:17.
20. Fu G.K., Hu J., Wang P.H., Fodor S.P. Counting individual DNA molecules by the stochastic attachment of diverse labels. Proc. Natl. Acad. Sci. USA 2011, 108:9026-9031.
21. Grindberg R.V., Yee-Greenbaum J.L., McConnell M.J., Novotny M., O'Shaughnessy A.L.L., Lambert G.M., Araúzo-Bravo M.J., Lee J., Fishman M., Robbins G.E., et al. RNA-sequencing from single nuclei. Proc. Natl. Acad. Sci. USA 2013, 110:19802-19807.
22. Grün D., Kester L., van Oudenaarden A. Validation of noise models for single-cell transcriptomics. Nat. Methods 2014, 11:637-640.
23. Guo H., Zhu P., Wu X., Li X., Wen L., Tang F. Single-cell methylome landscapes of mouse embryonic stem cells and early embryos analyzed using reduced representation bisulfite sequencing. Genome Res. 2013, 23:2126-2135.
24. Hashimshony T., Wagner F., Sher N., Yanai I. CEL-Seq: single-cell RNA-Seq by multiplexed linear amplification. Cell Rep. 2012, 2:666-673.
25. Hayashi T., Shibata N., Okumura R., Kudome T., Nishimura O., Tarui H., Agata K. Single-cell gene profiling of planarian stem cells using fluorescent activated cell sorting and its "index sorting" function for stem cell research. Dev. Growth Differ. 2010, 52:131-144.
26. Huang H., Goto M., Tsunoda H., Sun L., Taniguchi K., Matsunaga H., Kambara H. Non-biased and efficient global amplification of a single-cell cDNA library. Nucleic Acids Res. 2014, 42:e12.
27. Hug H., Schuler R. Measurement of the number of molecules of a single mRNA species in a complex mRNA preparation. J.Theor. Biol. 2003, 221:615-624.
28. Islam S., Kjällquist U., Moliner A., Zajac P., Fan J.B., Lönnerberg P., Linnarsson S. Characterization of the single-cell transcriptional landscape by highly multiplex RNA-seq. Genome Res. 2011, 21:1160-1167.
29. Islam S., Kjällquist U., Moliner A., Zajac P., Fan J.B., Lönnerberg P., Linnarsson S. Highly multiplexed and strand-specific single-cell RNA 5' end sequencing. Nat. Protoc. 2012, 7:813-828.
30. Islam S., Zeisel A., Joost S., La Manno G., Zajac P., Kasper M., Lönnerberg P., Linnarsson S. Quantitative single-cell RNA-seq with unique molecular identifiers. Nat. Methods 2014, 11:163-166.
31. Jaitin D.A., Kenigsberg E., Keren-Shaul H., Elefant N., Paul F., Zaretsky I., Mildner A., Cohen N., Jung S., Tanay A., Amit I. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 2014, 343:776-779.
32. Jiang L., Schlesinger F., Davis C.A., Zhang Y., Li R., Salit M., Gingeras T.R., Oliver B. Synthetic spike-in standards for RNA-seq experiments. Genome Res. 2011, 21:1543-1551.
33. Junker J.P., Noël E.S., Guryev V., Peterson K.A., Shah G., Huisken J., McMahon A.P., Berezikov E., Bakkers J., van Oudenaarden A. Genome-wide RNA Tomography in the zebrafish embryo. Cell 2014, 159:662-675.
34. Kamme F., Salunga R., Yu J., Tran D.T., Zhu J., Luo L., Bittner A., Guo H.Q., Miller N., Wan J., Erlander M. Single-cell microarray analysis in hippocampus CA1: demonstration and validation of cellular heterogeneity. J.Neurosci. 2003, 23:3607-3615.
35. Ke R., Mignardi M., Pacureanu A., Svedlund J., Botling J., Wählby C., Nilsson M. In situ sequencing for RNA analysis in preserved tissue andcells. Nat. Methods 2013, 10:857-860.
36. Keays K.M., Owens G.P., Ritchie A.M., Gilden D.H., Burgoon M.P. Laser capture microdissection and single-cell RT-PCR without RNA purification. J.Immunol. Methods 2005, 302:90-98.
37. Kim J.K., Marioni J.C. Inferring the kinetics of stochastic gene expression from single-cell RNA-sequencing data. Genome Biol. 2013, 14:R7.
38. Kim D.H., Marinov G.K., Pepke S., Singer Z.S., He P., Williams B., Schroth G.P., Elowitz M.B., Wold B.J. Single-cell transcriptome analysis reveals dynamic changes in lncRNA expression during reprogramming. Cell Stem Cell 2015, 16:88-101.
39. Kivioja T., Vähärautio A., Karlsson K., Bonke M., Enge M., Linnarsson S., Taipale J. Counting absolute numbers of molecules using unique molecular identifiers. Nat. Methods 2012, 9:72-74.
40. Kumar R.M., Cahan P., Shalek A.K., Satija R., DaleyKeyser A.J., Li H., Zhang J., Pardee K., Gennert D., Trombetta J.J., et al. Deconstructing transcriptional heterogeneity in pluripotent stem cells. Nature 2014, 516:56-61.
41. Kurimoto K., Yabuta Y., Ohinata Y., Ono Y., Uno K.D., Yamada R.G., Ueda H.R., Saitou M. An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res. 2006, 34:e42.
42. Kurimoto K., Yabuta Y., Ohinata Y., Saitou M. Global single-cell cDNA amplification to provide a template for representative high-density oligonucleotide microarray analysis. Nat. Protoc. 2007, 2:739-752.
43. Lam H.Y., Clark M.J., Chen R., Chen R., Natsoulis G., O'Huallachain M., Dewey F.E., Habegger L., Ashley E.A., Gerstein M.B., et al. Performance comparison of whole-genome sequencing platforms. Nat. Biotechnol. 2012, 30:78-82.
44. Lee J.H., Daugharthy E.R., Scheiman J., Kalhor R., Yang J.L., Ferrante T.C., Terry R., Jeanty S.S., Li C., Amamoto R., et al. Highly multiplexed subcellular RNA sequencing insitu. Science 2014, 343:1360-1363.
45. Lee M., Collins J.W., Aubrecht D.M., Sperling R.A., Solomon L., Ha J.W., Yi G.R., Weitz D.A., Manoharan V.N. Synchronized reinjection and coalescence of droplets in microfluidics. Lab Chip 2014, 14:509-513.
46. 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., et al. Transcriptome invivo analysis (TIVA) of spatially defined single cells in live tissue. Nat. Methods 2014, 11:190-196.
47. Macaulay I.C., Haerty W., Kumar P., Li Y.I., Hu T.X., Teng M.J., Goolam M., Saurat N., Coupland P., Shirley L.M., et al. G&T-seq: parallel sequencing of single-cell genomes and transcriptomes. Nat. Methods. 2015, Published online April 27, 2015. 10.1038/nmeth.3370.
48. Mahata B., Zhang X., Kolodziejczyk A.A., Proserpio V., Haim-Vilmovsky L., Taylor A.E., Hebenstreit D., Dingler F.A., Moignard V., Gottgens B., et al. Single-cell RNA sequencing reveals T helper cells synthesizing steroids de novo to contribute to immune homeostasis. Cell Rep. 2014, 7:1130-1142.
49. Marinov G.K., Williams B.A., McCue K., Schroth G.P., Gertz J., Myers R.M., Wold B.J. From single-cell to cell-pool transcriptomes: stochasticity in gene expression and RNA splicing. Genome Res. 2014, 24:496-510.
50. Marioni J.C., Mason C.E., Mane S.M., Stephens M., Gilad Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008, 18:1509-1517.
51. 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, 8:870-891.
52. Mitra R.D., Shendure J., Olejnik J., Edyta-Krzymanska-Olejnik, Church G.M. Fluorescent insitu sequencing on polymerase colonies. Anal. Biochem. 2003, 320:55-65.
53. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5:621-628.
54. Nagalakshmi U., Wang Z., Waern K., Shou C., Raha D., Gerstein M., Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320:1344-1349.
55. Nakamura T., Yabuta Y., Okamoto I., Aramaki S., Yokobayashi S., Kurimoto K., Sekiguchi K., Nakagawa M., Yamamoto T., Saitou M. SC3-seq: a method for highly parallel and quantitative measurement of single-cell gene expression. Nucleic Acids Res. 2015, Published online February 26, 2015. 10.1093/nar/gkv134.
56. Newman J.R., Ghaemmaghami S., Ihmels J., Breslow D.K., Noble M., DeRisi J.L., Weissman J.S. Single-cell proteomic analysis of S.cerevisiae reveals the architecture of biological noise. Nature 2006, 441:840-846.
57. Padovan-Merhar O., Raj A. Using variability in gene expression as a tool for studying gene regulation. Wiley Interdiscip. Rev. Syst. Biol. Med. 2013, 5:751-759.
58. Patel A.P., Tirosh I., Trombetta J.J., Shalek A.K., Gillespie S.M., Wakimoto H., Cahill D.P., Nahed B.V., Curry W.T., Martuza R.L., et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014, 344:1396-1401.
59. Peat J.R., Dean W., Clark S.J., Krueger F., Smallwood S.A., Ficz G., Kim J.K., Marioni J.C., Hore T.A., Reik W. Genome-wide bisulfite sequencing in zygotes identifies demethylation targets and maps the contribution of TET3 oxidation. Cell Rep. 2014, 9:1990-2000.
60. Picelli S., Björklund A.K., Faridani O.R., Sagasser S., Winberg G., Sandberg R. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 2013, 10:1096-1098.
61. Pollen A.A., Nowakowski T.J., Shuga J., Wang X., Leyrat A.A., Lui J.H., Li N., Szpankowski L., Fowler B., Chen P., et al. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat. Biotechnol. 2014, 32:1053-1058.
62. Quail M.A., Smith M., Coupland P., Otto T.D., Harris S.R., Connor T.R., Bertoni A., Swerdlow H.P., Gu Y. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 2012, 13:341.
63. Raj A., Peskin C.S., Tranchina D., Vargas D.Y., Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 2006, 4:e309.
64. Raj A., van den Bogaard P., Rifkin S.A., van Oudenaarden A., Tyagi S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 2008, 5:877-879.
65. 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., et al. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 2012, 30:777-782.
66. Sasagawa Y., Nikaido I., Hayashi T., Danno H., Uno K.D., Imai T., Ueda H.R. Quartz-Seq: a highly reproducible and sensitive single-cell RNA sequencing method, reveals non-genetic gene-expression heterogeneity. Genome Biol. 2013, 14:R31.
67. Shalek A.K., Satija R., Adiconis X., Gertner R.S., Gaublomme J.T., Raychowdhury R., Schwartz S., Yosef N., Malboeuf C., Lu D., et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 2013, 498:236-240.
68. Shalek A.K., Satija R., Shuga J., Trombetta J.J., Gennert D., Lu D., Chen P., Gertner R.S., Gaublomme J.T., Yosef N., et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 2014, 510:363-369.
69. Smallwood S.A., Lee H.J., Angermueller C., Krueger F., Saadeh H., Peat J., Andrews S.R., Stegle O., Reik W., Kelsey G. Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat. Methods 2014, 11:817-820.
70. Stegle O., Teichmann S.A., Marioni J.C. Computational and analytical challenges in single-cell transcriptomics. Nat. Rev. Genet. 2015, 16:133-145.
71. Subkhankulova T., Gilchrist M.J., Livesey F.J. Modelling and measuring single cell RNA expression levels find considerable transcriptional differences among phenotypically identical cells. BMC Genomics 2008, 9:268.
72. Tang F., Barbacioru C., Wang Y., Nordman E., Lee C., Xu N., Wang X., Bodeau J., Tuch B.B., Siddiqui A., et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods 2009, 6:377-382.
73. Tang F., Barbacioru C., Bao S., Lee C., Nordman E., Wang X., Lao K., Surani M.A. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 2010, 6:468-478.
74. Taniguchi K., Kajiyama T., Kambara H. Quantitative analysis of gene expression in a single cell by qPCR. Nat. Methods 2009, 6:503-506.
75. Trapnell C., Cacchiarelli D., Grimsby J., Pokharel P., Li S., Morse M., Lennon N.J., Livak K.J., Mikkelsen T.S., Rinn J.L. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 2014, 32:381-386.
76. 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, 509:371-375.
77. Tyagi S., Kramer F.R. Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 1996, 14:303-308.
78. Wang J., Fan H.C., Behr B., Quake S.R. Genome-wide single-cell analysis of recombination activity and de novo mutation rates in human sperm. Cell 2012, 150:402-412.
79. Wang L., Wang S., Li W. RSeQC: quality control of RNA-seq experiments. Bioinformatics 2012, 28:2184-2185.
80. Warren L., Bryder D., Weissman I.L., Quake S.R. Transcription factor profiling in individual hematopoietic progenitors by digital RT-PCR. Proc. Natl. Acad. Sci. USA 2006, 103:17807-17812.
81. Wilhelm B.T., Marguerat S., Watt S., Schubert F., Wood V., Goodhead I., Penkett C.J., Rogers J., Bähler J. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 2008, 453:1239-1243.
82. Xue Z., Huang K., Cai C., Cai L., Jiang C.Y., Feng Y., Liu Z., Zeng Q., Cheng L., Sun Y.E., et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 2013, 500:593-597.
83. Yan L., Yang M., Guo H., Yang L., Wu J., Li R., Liu P., Lian Y., Zheng X., Yan J., et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 2013, 20:1131-1139.
84. Zeisel A., Muñoz-Manchado A.B., Codeluppi S., Lönnerberg P., La Manno G., Juréus A., Marques S., Munguba H., He L., Betsholtz C., et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 2015, 347:1138-1142.
85. Zong C., Lu S., Chapman A.R., Xie X.S. Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science 2012, 338:1622-1626.