Single Mammalian Cells Compensate for Differences in Cellular Volume and DNA Copy Number through Independent Global Transcriptional Mechanisms

Molecular Cell

Volumn 58, Issue 2, 2015, Pages 339-352

  Padovan Merhar, Olivia ^a   Nair, Gautham P ^b   Biaesch, Andrew G ^b   Mayer, Andreas ^c   Scarfone, Steven ^a   Foley, Shawn W ^d   Wu, Angela R ^e   Churchman, L Stirling ^c   Singh, Abhyudai ^f   Raj, Arjun ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e Stanford University   (United States)

^f UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MESSENGER RNA;

ARTICLE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL FUSION; CELL LEVEL; CELL SIZE; CELL VOLUME; CONTROLLED STUDY; CORRELATIONAL STUDY; DNA CONTENT; DNA DEGRADATION; DNA REPLICATION; DNA TRANSCRIPTION; GENE DOSAGE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; SINGLE CELL ANALYSIS; TRANSCRIPTION REGULATION; ANIMAL; CAENORHABDITIS ELEGANS; CELL CULTURE; CYTOLOGY; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETICS; MALE; MOLECULAR GENETICS; PREPUCE; PROCEDURES; SEQUENCE ANALYSIS;

MAMMALIA;

ANIMALS; CAENORHABDITIS ELEGANS; CELLS, CULTURED; FIBROBLASTS; FORESKIN; GENE DOSAGE; GENE EXPRESSION; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MOLECULAR SEQUENCE DATA; S PHASE; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS; TRANSCRIPTION, GENETIC;

EID: 84928214314     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.03.005     Document Type: Article

References (61)

1. 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.
2. Bensaude O. Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity?. Transcription 2011, 2:103-108.
3. Bhatt D.M., Pandya-Jones A., Tong A.-J., Barozzi I., Lissner M.M., Natoli G., Black D.L., Smale S.T. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 2012, 150:279-290.
4. Bowsher C.G., Swain P.S. Identifying sources of variation and the flow of information in biochemical networks. Proc. Natl. Acad. Sci. USA 2012, 109:E1320-E1328.
5. 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.
6. Bryan A.K., Hecht V.C., Shen W., Payer K., Grover W.H., Manalis S.R. Measuring single cell mass, volume, and density with dual suspended microchannel resonators. Lab Chip 2014, 14:569-576.
7. Chubb J.R., Trcek T., Shenoy S.M., Singer R.H. Transcriptional pulsing of a developmental gene. Curr. Biol. 2006, 16:1018-1025.
8. Crissman H.A., Steinkamp J.A. Rapid, simultaneous measurement of DNA, protein, and cell volume in single cells from large mammalian cell populations. J.Cell Biol. 1973, 59:766-771.
9. Dar R.D., Razooky B.S., Singh A., Trimeloni T.V., McCollum J.M., Cox C.D., Simpson M.L., Weinberger L.S. Transcriptional burst frequency and burst size are equally modulated across the human genome. Proc. Natl. Acad. Sci. USA 2012, 109:17454-17459.
10. das Neves R.P., Jones N.S., Andreu L., Gupta R., Enver T., Iborra F.J. Connecting variability in global transcription rate to mitochondrial variability. PLoS Biol. 2010, 8:e1000560.
11. Devonshire A.S., Elaswarapu R., Foy C.A. Evaluation of external RNA controls for the standardisation of gene expression biomarker measurements. BMC Genomics 2010, 11:662.
12. Elowitz M.B., Levine A.J., Siggia E.D., Swain P.S. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
13. Eward K.L., Van Ert M.N., Thornton M., Helmstetter C.E. Cyclin mRNA stability does not vary during the cell cycle. Cell Cycle 2004, 3:1057-1061.
14. Femino A.M., Fay F.S., Fogarty K., Singer R.H. Visualization of single RNA transcripts insitu. Science 1998, 280:585-590.
15. Fraser R.S., Nurse P. Altered patterns of ribonucleic acid synthesis during the cell cycle: a mechanism compensating for variation in gene concentration. J.Cell Sci. 1979, 35:25-40.
16. Golding I., Paulsson J., Zawilski S.M., Cox E.C. Real-time kinetics of gene activity in individual bacteria. Cell 2005, 123:1025-1036.
17. Grün D., Kester L., van Oudenaarden A. Validation of noise models for single-cell transcriptomics. Nat. Methods 2014, 11:637-640.
18. Hansen R.S., Thomas S., Sandstrom R., Canfield T.K., Thurman R.E., Weaver M., Dorschner M.O., Gartler S.M., Stamatoyannopoulos J.A. Sequencing newly replicated DNA reveals widespread plasticity in human replication timing. Proc. Natl. Acad. Sci. USA 2010, 107:139-144.
19. Jao C.Y., Salic A. Exploring RNA transcription and turnover invivo by using click chemistry. Proc. Natl. Acad. Sci. USA 2008, 105:15779-15784.
20. Johnston I.G., Gaal B., Neves R.P., Enver T., Iborra F.J., Jones N.S. Mitochondrial variability as a source of extrinsic cellular noise. PLoS Comput. Biol. 2012, 8:e1002416.
21. Kimura H., Tao Y., Roeder R.G., Cook P.R. Quantitation of RNA polymerase II and its transcription factors in an HeLa cell: little soluble holoenzyme but significant amounts of polymerases attached to the nuclear substructure. Mol. Cell. Biol. 1999, 19:5383-5392.
22. Kimura H., Sugaya K., Cook P.R. The transcription cycle of RNA polymerase II in living cells. J.Cell Biol. 2002, 159:777-782.
23. Levesque M.J., Raj A. Single-chromosome transcriptional profiling reveals chromosomal gene expression regulation. Nat. Methods 2013, 10:246-248.
24. Levsky J.M., Shenoy S.M., Pezo R.C., Singer R.H. Single-cell gene expression profiling. Science 2002, 297:836-840.
25. Li G.-W., Xie X.S. Central dogma at the single-molecule level in living cells. Nature 2011, 475:308-315.
26. Lin C.Y., Lovén J., Rahl P.B., Paranal R.M., Burge C.B., Bradner J.E., Lee T.I., Young R.A. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012, 151:56-67.
27. Maamar H., Cabili M.N., Rinn J., Raj A. linc-HOXA1 is a noncoding RNA that represses Hoxa1 transcription in cis. Genes Dev. 2013, 27:1260-1271.
28. Marguerat S., Bähler J. Coordinating genome expression with cell size. Trends Genet. 2012, 28:560-565.
29. Marguerat S., Schmidt A., Codlin S., Chen W., Aebersold R., Bähler J. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 2012, 151:671-683.
30. 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.
31. Miettinen T.P., Pessa H.K.J., Caldez M.J., Fuhrer T., Diril M.K., Sauer U., Kaldis P., Björklund M. Identification of transcriptional and metabolic programs related to mammalian cell size. Curr. Biol. 2014, 24:598-608.
32. Nair G., Walton T., Murray J.I., Raj A. Gene transcription is coordinated with, but not dependent on, cell divisions during C. elegans embryonic fate specification. Development 2013, 140:3385-3394.
33. Newman J.R.S., 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.
34. Nie Z., Hu G., Wei G., Cui K., Yamane A., Resch W., Wang R., Green D.R., Tessarollo L., Casellas R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012, 151:68-79.
35. Pomerantz J.H., Mukherjee S., Palermo A.T., Blau H.M. Reprogramming to a muscle fate by fusion recapitulates differentiation. J.Cell Sci. 2009, 122:1045-1053.
36. Raj A., van Oudenaarden A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 2008, 135:216-226.
37. Raj A., van Oudenaarden A. Single-molecule approaches to stochastic gene expression. Annu. Rev. Biophys. 2009, 38:255-270.
38. Raj A., Tyagi S. Detection of individual endogenous RNA transcripts insitu using multiple singly labeled probes. Methods Enzymol. 2010, 472:365-386.
39. Raj A., Peskin C.S., Tranchina D., Vargas D.Y., Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 2006, 4:e309.
40. 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.
41. Robertson K.D., Keyomarsi K., Gonzales F.A., Velicescu M., Jones P.A. Differential mRNA expression of the human DNA methyltransferases (DNMTs) 1, 3a and 3b during the G(0)/G(1) to S phase transition in normal and tumor cells. Nucleic Acids Res. 2000, 28:2108-2113.
42. Sanchez A., Golding I. Genetic determinants and cellular constraints in noisy gene expression. Science 2013, 342:1188-1193.
43. Schmidt E.E., Schibler U. Cell size regulation, a mechanism that controls cellular RNA accumulation: consequences on regulation of the ubiquitous transcription factors Oct1 and NF-Y and the liver-enriched transcription factor DBP. J.Cell Biol. 1995, 128:467-483.
44. Senecal A., Munsky B., Proux F., Ly N., Braye F.E., Zimmer C., Mueller F., Darzacq X. Transcription factors modulate c-Fos transcriptional bursts. Cell Rep. 2014, 8:75-83.
45. 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.
46. Springer M., Weissman J.S., Kirschner M.W. A general lack of compensation for gene dosage in yeast. Mol. Syst. Biol. 2010, 6:368.
47. Suter D.M., Molina N., Gatfield D., Schneider K., Schibler U., Naef F. Mammalian genes are transcribed with widely different bursting kinetics. Science 2011, 332:472-474.
48. Swain P.S., Elowitz M.B., Siggia E.D. Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc. Natl. Acad. Sci. USA 2002, 99:12795-12800.
49. Swift J., Ivanovska I.L., Buxboim A., Harada T., Dingal P.C.D.P., Pinter J., Pajerowski J.D., Spinler K.R., Shin J.-W., Tewari M., et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013, 341:1240104.
50. Tani H., Mizutani R., Salam K.A., Tano K., Ijiri K., Wakamatsu A., Isogai T., Suzuki Y., Akimitsu N. Genome-wide determination of RNA stability reveals hundreds of short-lived noncoding transcripts in mammals. Genome Res. 2012, 22:947-956.
51. Taniguchi Y., Choi P.J., Li G.-W., Chen H., Babu M., Hearn J., Emili A., Xie X.S. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2010, 329:533-538.
52. Tzur A., Kafri R., LeBleu V.S., Lahav G., Kirschner M.W. Cell growth and size homeostasis in proliferating animal cells. Science 2009, 325:167-171.
53. Vargas D.Y., Raj A., Marras S.A.E., Kramer F.R., Tyagi S. Mechanism of mRNA transport in the nucleus. Proc. Natl. Acad. Sci. USA 2005, 102:17008-17013.
54. Volfson D., Marciniak J., Blake W.J., Ostroff N., Tsimring L.S., Hasty J. Origins of extrinsic variability in eukaryotic gene expression. Nature 2006, 439:861-864.
55. Watanabe N., Ishihara T., Ohshima Y. Mutants carrying two sma mutations are super small in the nematode C. elegans. Genes Cells 2007, 12:603-609.
56. Whitfield M.L., Sherlock G., Saldanha A.J., Murray J.I., Ball C.A., Alexander K.E., Matese J.C., Perou C.M., Hurt M.M., Brown P.O., Botstein D. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell 2002, 13:1977-2000.
57. Wu C.-Y., Rolfe P.A., Gifford D.K., Fink G.R. Control of transcription by cell size. PLoS Biol. 2010, 8:e1000523.
58. Wu A.R., Neff N.F., Kalisky T., Dalerba P., Treutlein B., Rothenberg M.E., Mburu F.M., Mantalas G.L., Sim S., Clarke M.F., Quake S.R. Quantitative assessment of single-cell RNA-sequencing methods. Nat. Methods 2014, 11:41-46.
59. Wuarin J., Schibler U. Physical isolation of nascent RNA chains transcribed by RNA polymerase II: evidence for cotranscriptional splicing. Mol. Cell. Biol. 1994, 14:7219-7225.
60. Zenklusen D., Larson D.R., Singer R.H. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol. 2008, 15:1263-1271.
61. Zhurinsky J., Leonhard K., Watt S., Marguerat S., Bähler J., Nurse P. A coordinated global control over cellular transcription. Curr. Biol. 2010, 20:2010-2015.