Single-cell states versus single-cell atlases - two classes of heterogeneity that differ in meaning and method

Current Opinion in Biotechnology

Volumn 39, Issue , 2016, Pages 120-125

  Janes, Kevin A ^a  

^a University of Virginia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DEPTH PROFILING;

APPROPRIATE TECHNIQUES; CELLULAR DIVERSITY; COMPLEX TISSUES; IN-SITU METHODS; MICROENVIRONMENTS; MICROFLUIDIC-BASED; MOLECULAR SIGNATURES; QUANTITATIVE ACCURACY;

CELLS;

COMPLEMENTARY DNA; MESSENGER RNA;

ACCURACY; CELL HETEROGENEITY; CELL ISOLATION; CYTOMETRY; EXTRACELLULAR MATRIX; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; MICROENCAPSULATION; MICROFLUIDICS; PRIORITY JOURNAL; REVIEW; SINGLE CELL ANALYSIS; TRANSCRIPTOMICS; ANIMAL; CELL FUNCTION; GENE REGULATORY NETWORK; PROCEDURES;

ANIMALS; CELL PHYSIOLOGICAL PHENOMENA; GENE REGULATORY NETWORKS; HUMANS; SINGLE-CELL ANALYSIS;

EID: 84961918745     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2016.03.015     Document Type: Review

References (49)

1. Altschuler S.J., Wu L.F. Cellular heterogeneity: do differences make a difference?. Cell 2010, 141:559-563.
2. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2013, 154:274-284.
3. Junker J.P., van Oudenaarden A. Every cell is special: genome-wide studies add a new dimension to single-cell biology. Cell 2014, 157:8-11.
4. 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.
5. Lujan E., Zunder E.R., Ng Y.H., Goronzy I.N., Nolan G.P., Wernig M. Early reprogramming regulators identified by prospective isolation and mass cytometry. Nature 2015, 521:352-356.
6. 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.
7. Lee M.C., Lopez-Diaz F.J., Khan S.Y., Tariq M.A., Dayn Y., Vaske C.J., Radenbaugh A.J., Kim H.J., Emerson B.M., Pourmand N. Single-cell analyses of transcriptional heterogeneity during drug tolerance transition in cancer cells by RNA sequencing. Proc Natl Acad Sci U S A 2014, 111:E4726-E4735.
8. Pelkmans L. Cell Biology. Using cell-to-cell variability - a new era in molecular biology. Science 2012, 336:425-426.
9. Wichterle H., Gifford D., Mazzoni E. Neuroscience. Mapping neuronal diversity one cell at a time. Science 2013, 341:726-727.
10. Singh A., Bokes P. Consequences of mRNA transport on stochastic variability in protein levels. Biophys J 2012, 103:1087-1096.
11. Raser J.M., O'Shea E.K. Noise in gene expression: origins, consequences, and control. Science 2005, 309:2010-2013.
12. Padovan-Merhar O., Nair G.P., Biaesch A.G., Mayer A., Scarfone S., Foley S.W., Wu A.R., Churchman L.S., Singh A., Raj A. Single mammalian cells compensate for differences in cellular volume and DNA copy number through independent global transcriptional mechanisms. Mol Cell 2015, 58:339-352.
13. Kempe H., Schwabe A., Cremazy F., Verschure P.J., Bruggeman F.J. The volumes and transcript counts of single cells reveal concentration homeostasis and capture biological noise. Mol Biol Cell 2015, 26:797-804.
14. Levine J.H., Simonds E.F., Bendall S.C., Davis K.L., Amir el A.D., Tadmor M.D., Litvin O., Fienberg H.G., Jager A., Zunder E.R., et al. Data-driven phenotypic dissection of AML reveals progenitor-like cells that correlate with prognosis. Cell 2015, 162:184-197.
15. 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.
16. Grün D., Lyubimova A., Kester L., Wiebrands K., Basak O., Sasaki N., Clevers H., van Oudenaarden A. Single-cell messenger RNA sequencing reveals rare intestinal cell types. Nature 2015.
17. Darmanis S., Sloan S.A., Zhang Y., Enge M., Caneda C., Shuer L.M., Hayden Gephart M.G., Barres B.A., Quake S.R. A survey of human brain transcriptome diversity at the single cell level. Proc Natl Acad Sci U S A 2015, 112:7285-7290.
18. Brennecke P., Anders S., Kim J.K., Kolodziejczyk A.A., Zhang X., Proserpio V., Baying B., Benes V., Teichmann S.A., Marioni J.C., et al. Accounting for technical noise in single-cell RNA-seq experiments. Nat Methods 2013, 10:1093-1095.
19. Kharchenko P.V., Silberstein L., Scadden D.T. Bayesian approach to single-cell differential expression analysis. Nat Methods 2014, 11:740-742.
20. Kang B.H., Jensen K.J., Hatch J.A., Janes K.A. Simultaneous profiling of 194 distinct receptor transcripts in human cells. Sci Signal 2013, 6:rs13.
21. Jaitin D.A., Kenigsberg E., Keren-Shaul H., Elefant N., Paul F., Zaretsky I., Mildner A., Cohen N., Jung S., Tanay A., et al. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 2014, 343:776-779.
22. 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.
23. Steininger R.J., Rajaram S., Girard L., Minna J.D., Wu L.F., Altschuler S.J. On comparing heterogeneity across biomarkers. Cytometry A 2015, 87:558-567.
24. 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.
25. Hines W.C., Su Y., Kuhn I., Polyak K., Bissell M.J. Sorting out the FACS: a devil in the details. Cell Rep 2014, 6:779-781.
26. Emmert-Buck M.R., Bonner R.F., Smith P.D., Chuaqui R.F., Zhuang Z., Goldstein S.R., Weiss R.A., Liotta L.A. Laser capture microdissection. Science 1996, 274:998-1001.
27. Fan H.C., Fu G.K., Fodor S.P. Expression profiling. Combinatorial labeling of single cells for gene expression cytometry. Science 2015, 347:1258367.
28. 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, 161:1187-1201.
29. Macosko E.Z., Basu A., Satija R., Nemesh J., Shekhar K., Goldman M., Tirosh I., Bialas A.R., Kamitaki N., Martersteck E.M., et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 2015, 161:1202-1214.
30. Kivioja T., Vaharautio 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.
31. Eberwine J., Sul J.Y., Bartfai T., Kim J. The promise of single-cell sequencing. Nat Methods 2014, 11:25-27.
32. Picelli S., Bjorklund 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.
33. Picelli S., Faridani O.R., Bjorklund A.K., Winberg G., Sagasser S., Sandberg R. Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc 2014, 9:171-181.
34. Wang C.C., Jamal L., Janes K.A. Normal morphogenesis of epithelial tissues and progression of epithelial tumors. Wiley Interdiscip Rev Syst Biol Med 2012, 4:51-78.
35. Zhao B., Li L., Wang L., Wang C.Y., Yu J., Guan K.L. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev 2012, 26:54-68.
36. Geller S.F., Lewis G.P., Fisher S.K. FGFR1, signaling, and AP-1 expression after retinal detachment: reactive Muller and RPE cells. Invest Ophthalmol Vis Sci 2001, 42:1363-1369.
37. Shibata Y., Nakamura H., Kato S., Tomoike H. Cellular detachment and deformation induce IL-8 gene expression in human bronchial epithelial cells. J Immunol 1996, 156:772-777.
38. Wang C.C., Bajikar S.S., Jamal L., Atkins K.A., Janes K.A. A time- and matrix-dependent TGFBR3-JUND-KRT5 regulatory circuit in single breast epithelial cells and basal-like premalignancies. Nat Cell Biol 2014, 16:345-356.
39. Giesen C., Wang H.A., Schapiro D., Zivanovic N., Jacobs A., Hattendorf B., Schuffler P.J., Grolimund D., Buhmann J.M., Brandt S., et al. Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat Methods 2014, 11:417-422.
40. Angelo M., Bendall S.C., Finck R., Hale M.B., Hitzman C., Borowsky A.D., Levenson R.M., Lowe J.B., Liu S.D., Zhao S., et al. Multiplexed ion beam imaging of human breast tumors. Nat Med 2014, 20:436-442.
41. Battich N., Stoeger T., Pelkmans L. Image-based transcriptomics in thousands of single human cells at single-molecule resolution. Nat Methods 2013, 10:1127-1133.
42. Battich N., Stoeger T., Pelkmans L. Control of transcript variability in single mammalian cells. Cell 2015, 163:1596-1610.
43. Chen K.H., Boettiger A.N., Moffitt J.R., Wang S., Zhuang X. RNA imaging, spatially resolved, highly multiplexed RNA profiling in single cells. Science 2015, 348:aaa6090.
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 in situ. Science 2014, 343:1360-1363.
45. Janes K.A., Wang C.C., Holmberg K.J., Cabral K., Brugge J.S. Identifying single-cell molecular programs by stochastic profiling. Nat Methods 2010, 7:311-317.
46. Wang L., Janes K.A. Stochastic profiling of transcriptional regulatory heterogeneities in tissues, tumors and cultured cells. Nat Protoc 2013, 8:282-301.
47. 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.
48. Bajikar S.S., Fuchs C., Roller A., Theis F.J., Janes K.A. Parameterizing cell-to-cell regulatory heterogeneities via stochastic transcriptional profiles. Proc Natl Acad Sci U S A 2014, 111:E626-E635.
49. Betzig E. Single molecules, cells, and super-resolution optics (nobel lecture). Angew Chem Int Ed Engl 2015, 54:8034-8053.