Protein expression analyses at the single cell level

Molecules

Volumn 19, Issue 9, 2014, Pages 13932-13947

  Ohno, Masae ^a   Karagiannis, Peter ^a   Taniguchi, Yuichi ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Burst; Protein expression; Proteome analysis; Single cell analysis; Single molecule fluorescence microscopy; Stochastic gene expression

Indexed keywords

PROTEOME;

ALGORITHM; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; PROTEIN SYNTHESIS; SINGLE CELL ANALYSIS; STATISTICS;

ALGORITHMS; ANIMALS; GENE EXPRESSION PROFILING; HUMANS; PROTEIN BIOSYNTHESIS; PROTEOME; SINGLE-CELL ANALYSIS; STOCHASTIC PROCESSES;

EID: 84907100148     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules190913932     Document Type: Review

References (64)

1. Elowitz, M.B.; Levine, A.J.; Siggia, E.D.; Swain, P.S. Stochastic gene expression in a single cell. Science 2002, 297, 1183-1186.
2. Eldar, A.; Elowitz, M.B. Functional roles for noise in genetic circuits. Nature 2010, 467, 167-173.
3. Raj, A.; van Oudenaaden, A. Nature, nurture, or chance: Stochastic gene expression and its consequences. Cell 2008, 135, 216-226.
4. 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.
5. Tietjen, I.; Rihel, J.M.; Cao, Y.; Koentges, G.; Zakhary, L.; Dulac, C. Single-Cell transcriptional analysis of neuronal progenitors. Neuron 2003, 38, 161-175.
6. Wu, M.; Singh, A.K. Single-Cell protein analysis. Curr. Opin. Biotechnol. 2012, 23, 83-88.
7. Mellors, J.S.; Jorabchi, K.; Smith, L.M.; Ramsey, J.M. Integrated microfluidic device for automated single cell analysis using electrophoretic separation and electrospray ionization mass spectrometry. Anal. Chem. 2010, 82, 967-973.
8. Rosenfeld, N.; Young, J.W.; Alon, U.; Swain, P.S.; Elowitz, M.B. Gene regulation at the single-cell level. Science 2005, 307, 1962-1965.
9. Cai, L.; Friedman, N.; Xie, X.S. Stochastic protein expression in individual cells at the single molecule level. Nature 2006, 440, 358-362.
10. Yu, J.; Xiao, J.; Ren, X.; Lao, K.; Xie, X.S. Probing gene expression in live cells, one protein molecule at a time. Science 2006, 311, 1600-1603.
11. 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.
12. 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.
13. De Sousa Abreu, R.; Penalva, L.O.; Marcotte, E.M.; Vogel, C. Global signatures of protein and mRNA expression levels. Mol. Biosyst. 2009, 5, 1512-1526.
14. Schwanhäusser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control. Nature 2011, 473, 337-342.
15. Lu, P.; Vogel, C.; Wang, R.; Yao, X.; Marcotte, E.M. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 2007, 25, 117-124.
16. Schrimpf, S.P.; Weiss, M.; Reiter, L.; Ahrens, C.H.; Jovanovic, M.; Malmström, J.; Brunner, E.; Mohanty, S.; Lercher, M.J.; Hunziker, P.E.; et al. Comparative functional analysis of the Caenorhabditis elegans and Drosophila melanogaster proteomes. PLoS Biol. 2009, 7, e48.
17. Laurent, J.M.; Vogel, C.; Kwon, T.; Craig, S.A.; Boutz, D.R.; Huse, H.K.; Nozue, K.; Walia, H.; Whiteley, M.; Ronald, P.C.; et al. Protein abundances are more conserved than mRNA abundances across diverse taxa. Proteomics 2010, 10, 4209-4212.
18. Khan, Z.; Ford, M.J.; Cusanovich, D.A.; Mitrano, A.; Pritchard, J.K.; Gilad, Y. Primate transcript and protein expression levels evolve under compensatory selection pressures. Science 2013, 342, 1100-1104.
19. Golding, I.; Paulsson, J.; Zawilski, S.M.; Cox, E.C. Real-Time kinetics of gene activity in individual bacteria. Cell 2005, 123, 1025-1036.
20. Le, T.T.; Harlepp, S.; Guet, C.C.; Dittmar, K.; Emonet, T.; Pan, T.; Cluzel, P. Real-Time RNA profiling within a single bacterium. Proc. Natl. Acad. Sci. USA 2005, 102, 9160-9164.
21. Chubb, J.R.; Trcek, T.; Shenoy, S.M.; Singer, R.H. Transcriptional pulsing of a developmental gene. Curr. Biol. 2006, 16, 1018-1025.
22. Yunger, S.; Rosenfeld, L.; Garini, Y.; Shav-Tal, Y. Single-Allele analysis of transcription kinetics in living mammalian cells. Nat. Methods 2010, 7, 631-633.
23. 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.
24. So, L.H.; Ghosh, A.; Zong, C.; Sepúlveda, L.A.; Segev, R.; Golding, I. General properties of transcriptional time series in Escherichia coli. Nat. Genet. 2011, 43, 554-560.
25. 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.
26. Raj, A.; Peskin, C.S.; Tranchina, D.; Vargas, D.Y.; Tyagi, S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 2006, 4, e309.
27. Paré, A.; Lemons, D.; Kosman, D.; Beaver, W.; Freund, Y.; McGinnis, W. Visualization of individual Scr mRNAs during Drosophila embryogenesis yields evidence for transcriptional bursting. Curr. Biol. 2009, 19, 2037-2042.
28. Sanchez, A.; Golding, I. Genetic determinants and cellular constraints in noisy gene expression. Science 2013, 342, 1188-1193.
29. Chong, S.; Chen, C.; Ge, H.; Xie, X.S. Mechanism of transcriptional bursting in bacteria. Cell 2014, 158, 314-326.
30. Peccoud, J.; Ycart, B. Markovian modeling of gene-product synthesis. Theor. Popul. Biol. 1995, 48, 222-234.
31. Shahrezaei, V.; Swain, P.S. Analytical distributions for stochastic gene expression. Proc. Natl. Acad. Sci. USA 2008, 105, 17256-17261.
32. Paulsson, J.; Ehrenberg, M. Random signal fluctuations can reduce random fluctuations in regulated components of chemical regulatory networks. Phys. Rev. Lett. 2000, 84, 5447-5450.
33. Friedman, N.; Cai, L.; Xie, X.S. Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys. Rev. Lett. 2006, 97, 168302.
34. Paulsson, J. Summing up the noise in gene networks. Nature 2004, 427, 415-418.
35. Choi, P.J.; Cai, L.; Frieda, K.; Xie, X.S. A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 2008, 322, 442-446.
36. Nagai, T.; Ibata, K.; Park, E.S.; Kubota, M.; Mikoshiba, K.; Miyawaki, A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 2002, 20, 87-90.
37. Elf, J.; Li, G.W.; Xie, X.S. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 2007, 316, 1191-1194.
38. Betzig, E.; Patterson, G.H.; Sougrat, R.; Lindwasser, O.W.; Olenych, S.; Bonifacino, J.S.; Davidson, M.W.; Lippincott-Schwartz, J.; Hess, H.F. Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313, 1642-1645.
39. Rust, M.J.; Bates, M.; Zhuang, X. Sub-Diffraction-Limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 2006, 3, 793-795.
40. Durisic, N.; Laparra-Cuervo, L.; Sandoval-Alvarez, A.; Borbely, J.S.; Lakadamyali, M. Single-Molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate. Nat. Methods 2014, 11, 156-162.
41. Lee, S.H.; Shin, J.Y.; Lee, A.; Bustamante, C. Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM). Proc. Natl. Acad. Sci. USA 2012, 109, 17436-17441.
42. Wang, S.; Moffitt, J.R.; Dempsey, G.T.; Xie, X.S.; Zhuang, X. Characterization and development of photoactivatable fluorescent proteins for single-molecule-based superresolution imaging. Proc. Natl. Acad. Sci. USA 2014, 111, 8452-8457.
43. Huang, B.; Wu, H.; Bhaya, D.; Grossman, A.; Granier, S.; Kobilka, B.K.; Zare, R.N. Counting low-copy number proteins in a single cell. Science 2007, 315, 81-84.
44. Levsky, J.M.; Shenoy, S.M.; Pezo, R.C.; Singer, R.H. Single-cell gene expression profiling. Science 2002, 297, 836-840.
45. Lubeck, E.; Cai, L. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat. Methods 2012, 9, 743-748.
46. Lubeck, E.; Coskun, A.F.; Zhiyentayev, T.; Ahmad, M.; Cai, L. Single-cell in situ RNA profiling by sequential hybridization. Nat. Methods 2014, 11, 360-361.
47. Huh, W.K.; Falvo, J.V.; Gerke, L.C.; Carroll, A.S.; Howson, R.W.; Weissman, J.S.; O'Shea, E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425, 686-691.
48. Sarov, M.; Murray, J.I.; Schanze, K.; Pozniakovski, A.; Niu, W.; Angermann, K.; Hasse, S.; Rupprecht, M.; Vinis, E.; Tinney, M.; et al. A genome-scale resource for in vivo tag-based protein function exploration in C. elegans. Cell 2012, 150, 855-866.
49. Sigal, A.; Danon, T.; Cohen, A.; Milo, R.; Geva-Zatorsky, N.; Lustig, G.; Liron, Y.; Alon, U.; Perzov, N. Generation of a fluorescently labeled endogenous protein library in living human cells. Nat. Protoc. 2007, 2, 1515-1527.
50. Ghaemmaghami, S.; Huh, W.K.; Bower, K.; Howson, R.W.; Belle, A.; Dephoure, N.; O'Shea, E.K.; Weissman, J.S. Global analysis of protein expression in yeast. Nature 2003, 425, 737-741.
51. Cohen, A.A.; Geva-Zatorsky, N.; Eden, E.; Frenkel-Morgenstern, M.; Issaeva, I.; Sigal, A.; Milo, R.; Cohen-Saidon, C.; Liron, Y.; Kam, Z.; et al. Dynamic proteomics of individual cancer cells in response to a drug. Science 2008, 322, 1511-1516.
52. 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.
53. Shi, Q.; Qin, L.; Wei, W.; Geng, F.; Fan, R.; Shin, Y.S.; Guo, D.; Hood, L.; Mischel, P.S.; Heath, J.R. Single-cell proteomic chip for profiling intracellular signaling pathways in single tumor cells. Proc. Natl. Acad. Sci. USA 2012, 109, 419-424.
54. Wakamoto, Y.; Dhar, N.; Chait, R.; Schneider, K.; Signorino-Gelo, F.; Leibler, S.; McKinney, J.D. Dynamic persistence of antibiotic-stressed mycobacteria. Science 2013, 339, 91-95.
55. Cai, L.; Dalal, C.K.; Elowitz, M.B. Frequency-Modulated nuclear localization bursts coordinate gene regulation. Nature 2008, 455, 485-490.
56. Stewart-Ornstein, J.; Weissman, J.S.; El-Samad, H. Cellular noise regulons underlie fluctuations in Saccharomyces cerevisiae. Mol. Cell 2012, 45, 483-493.
57. Sigal, A.; Milo, R.; Cohen, A.; Geva-Zatorsky, N.; Klein, Y.; Alaluf, I.; Swerdlin, N.; Perzov, N.; Danon, T.; Liron, Y.; et al. Dynamic proteomics in individual human cells uncovers widespread cell-cycle dependence of nuclear proteins. Nat. Methods 2006, 3, 525-531.
58. Kim, H.; Kim, J.S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 2014, 15, 321-334.
59. Huisken, J.; Swoger, J.; Bene, F.D.; Wittbrodt, J.; Stelzer, E.H. Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 2004, 305, 1007-1009.
60. Ritter, J.G.; Veith, R.; Veenendaal, A.; Siebrasse, J.P.; Kubitscheck, U. Light sheet microscopy for single molecule tracking in living tissue. PLoS One 2010, 5, e11639.
61. Gebhardt, J.C.; Suter, D.M.; Roy, R.; Zhao, Z.W.; Chapman, A.R.; Basu, S.; Maniatis, T.; Xie, X.S. Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat. Methods 2013, 10, 421-426.
62. Leuchowius, K.J.; Clausson, C.M.; Grannas, K.; Erbilgin, Y.; Botling, J.; Zieba, A.; Landegren, U.; Söderberg, O. Parallel visualization of multiple protein complexes in individual cells in tumor tissue. Parallel visualization of multiple protein complexes in individual cells in tumor tissue. Mol. Cell. Proteomics 2013, 12, 1563-1571.
63. Bandura, D.R.; Baranov, V.I.; Ornatsky, O.I.; Antonov, A.; Kinach, R.; Lou, X.; Pavlov, S.; Vorobiev, S.; Dick, J.E.; Tanner, S.D. Mass cytometry: Technique for real time single cell multitarget immunoassay based on inductively coupled plasma time-of-flight mass spectrometry. Anal. Chem. 2009, 81, 6813-6822.
64. Bendall, S.C.; Simonds, E.F.; Qiu, P.; Amir, E.A.D.; Krutzik, P.O.; Finck, R.; Bruggner, R.V.; Melamed, R.; Trejo, A.; Ornatsky, O.I.; et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 2011, 332, 687-696.