Modularity and predictability in cell signaling and decision making

Molecular Biology of the Cell

Volumn 25, Issue 22, 2014, Pages 3445-3450

  Atay, Oguzhan ^a   Skotheim, Jan M ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; REGULATOR PROTEIN;

CELL DIFFERENTIATION; CELL DIVISION; DECISION MAKING; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE INTERACTION; GENOMICS; INTRACELLULAR SIGNALING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; RNA SEQUENCE; SINGLE CELL ANALYSIS; STOCHASTIC MODEL; ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; CELL COMMUNICATION; CELL CYCLE; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC VARIABILITY; GENETICS; HUMAN; METABOLISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STATISTICS;

ANIMALS; APOPTOSIS; CELL COMMUNICATION; CELL CYCLE; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GENETIC VARIATION; HUMANS; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; STOCHASTIC PROCESSES;

EID: 84908582407     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-02-0718     Document Type: Review

References (56)

1. Acar M, Mettetal JT, Van Oudenaarden A (2008). Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40, 471-475.
2. Alon U (2007). Network motifs: theory and experimental approaches. Nat Rev Genet 8, 450-461.
3. Baltanás R, Bush A, Couto A, Durrieu L, Hohmann S, Colman-Lerner A (2013). Pheromone-induced morphogenesis improves osmoadaptation capacity by activating the HOG MAPK pathway. Sci Signal 6, ra26.
4. Bendall SC, Davis KL, Amir E-D, Tadmor MD, Simonds EF, Chen TJ, Shenfeld DK, Nolan GP, Pe'Er D (2014). Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development. Cell 157, 714-725.
5. Bendall SC, Simonds EF, Qiu P, Amir E-D, Krutzik PO, Finck R, Bruggner RV, Melamed R, Trejo A, Ornatsky OI, et al. (2011). Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332, 687-696.
6. Blake WJ, Kærn M, Cantor CR, Collins JJ (2003). Noise in eukaryotic gene expression. Nature 422, 633-637.
7. Boone C, Bussey H, Andrews BJ (2007). Exploring genetic interactions and networks with yeast. Nat Rev Genet 8, 437-449.
8. Brown CR, Mao C, Falkovskaia E, Jurica MS, Boeger H (2013). Linking stochastic fluctuations in chromatin structure and gene expression. PLoS Biol 11, e1001621.
9. Burrell RA, McGranahan N, Bartek J, Swanton C (2013). The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338-345.
10. Chang HH, Hemberg M, Barahona M, Ingber DE, Huang S (2008). Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544-547.
11. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J, Hillenmeyer ME, Davis RW, Nislow C, Giaever G (2005). Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169, 1915-1925.
12. Doncic A, Falleur-Fettig M, Skotheim J (2011). Distinct interactions select and maintain a specific cell fate. Mol Cell 43, 528-539.
13. Doncic A, Skotheim JM (2013). Feedforward regulation ensures stability and rapid reversibility of a cellular state. Mol Cell 50, 856-868.
14. Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002). Stochastic gene expression in a single cell. Science 297, 1183-1186.
15. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, Shabanowitz J, Hunt DF, White FM (2002). Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20, 301-305.
16. Garrenton LS, Braunwarth A, Irniger S, Hurt E, Kunzler M, Thorner J (2009). Nucleus-specific and cell cycle-regulated degradation of mitogen-activated protein kinase scaffold protein Ste5 contributes to the control of signaling competence. Mol Cell Biol 29, 582-601.
17. Gregor T, Tank DW, Wieschaus EF, Bialek W (2007). Probing the limits to positional information. Cell 130, 153-164.
18. Hartwell LH, Culotti J, Pringle JR, Reid BJ (1974). Genetic control of the cell division cycle in yeast. Science 183, 46-51.
19. Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999). From molecular to modular cell biology. Nature 402, C47-C52.
20. Holt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO (2009). Global analysis of Cdk1 substrate phosphorylation sites provides insiqhts into evolution. Science 325, 1682-1686.
21. Jaitin DA, Kenigsberg E, Keren-Shaul H, Elefant N, Paul F, Zaretsky I, Mildner A, Cohen N, Jung S, Tanay A, et al. (2014). Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 343, 776-779.
22. Johnson A (2014). Onset of CDK2 Activity Determines Passage Through the Restriction Point in Primary Cells. Thesis. Stanford University, Stanford, CA.
23. Kitano H (2004). Biological robustness. Nat Rev Genet 5, 826-837.
24. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, et al. (2006). Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440, 637-643.
25. Kussell E, Leibler S (2005). Ecology: phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075-2078.
26. Lewis ACF, Jones NS, Porter MA, Deane CM (2012). What evidence is there for the homology of protein-protein interactions? PLoS Comput Biol 8, e1002645.
27. Lindsley DL, Sandler L, Baker BS, Carpenter AT, Denell RE, Hall JC, Jacobs PA, Miklos GL, Davis BK, Gethmann RC, et al. (1972). Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71, 157-184.
28. Losick R, Desplan C (2008). Stochasticity and cell fate. Science 320, 65-68.
29. Lynch M (2007). The evolution of genetic networks by non-adaptive processes. Nat Rev Genet 8, 803-813.
30. Maamar H, Raj A, Dubnau D (2007). Noise in gene expression determines cell fate in Bacillus subtilis. Science 317, 526-529.
31. Maisonneuve E, Castro-Camargo M, Gerdes K (2013). (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154, 1140-1150.
32. Masel J, Siegal ML (2009). Robustness: mechanisms and consequences. Trends Genet 25, 395-403.
33. Navin N, Kendall J, Troge J, Andrews P, Rodgers L, McIndoo J, Cook K, Stepansky A, Levy D, Esposito D, et al. (2011). Tumour evolution inferred by single-cell sequencing. Nature 472, 90-95.
34. Newman JRS, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS (2006). Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840-846.
35. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, Cahill DP, Nahed BV, Curry WT, Martuza RL, et al. (2014). Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344, 1396-1401.
36. Patterson JC, Klimenko ES, Thorner J (2010). Single-cell analysis reveals that insulation maintains signaling specificity between two yeast MAPK pathways with common components. Sci Signal 3, ra75.
37. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S (2006). Stochastic mRNA synthesis in mammalian cells. PLoS Biol 4, e309.
38. Raj A, Rifkin SA, Andersen E, Van Oudenaarden A (2010). Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918.
39. Raj A, van Oudenaarden A (2008). Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226.
40. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, et al. (2005). Towards a proteome-scale map of the human protein-protein interaction network. Nature 437, 1173-1178.
41. Salathé M, Van Cleve J, Feldman MW (2009). Evolution of stochastic switching rates in asymmetric fitness landscapes. Genetics 182, 1159-1164.
42. Skotheim JM, Di Talia S, Siggia ED, Cross FR (2008). Positive feedback of G1 cyclins ensures coherent cell cycle entry. Nature 454, 291-296.
43. Smith A (2013). Nanog heterogeneity: tilting at windmills? Cell Stem Cell 13, 6-7.
44. Sorre B, Warmflash A, Brivanlou AH, Siggia E (2014). Encoding of temporal signals by the TGF-β pathway and implications for embryonic patterning. Dev Cell 30, 334-342.
45. Spencer SL, Cappell SD, Tsai FC, Overton KW, Wang CL, Meyer T (2013). The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell 155, 369-383.
46. Springer M, Weissman JS, Kirschner MW (2010). A general lack of compensation for gene dosage in yeast. Mol Syst Biol 6, 368.
47. Strickfaden SC, Winters MJ, Ben-Ari G, Lamson RE, Tyers M, Pryciak P (2007). A mechanism for cell-cycle regulation of MAP kinase signaling in a yeast differentiation pathway. Cell 128, 519-531.
48. Süel GM, Kulkarni RP, Dworkin J, Garcia-Ojalvo J, Elowitz MB (2007). Tunability and noise dependence in differentiation dynamics. Science 315, 1716-1719.
49. Tkacik G, Callan CG, Bialek W (2008). Information flow and optimization in transcriptional regulation. Proc Natl Acad Sci USA 105, 12265-12270.
50. Treutlein B, Brownfield DG, Wu AR, Neff NF, Mantalas GL, Espinoza FH, Desai TJ, Krasnow MA, Quake SR (2014). Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509, 371-375.
51. Tuch BB, Li H, Johnson AD (2008). Evolution of eukaryotic transcription circuits. Science 319, 1797-1799.
52. Warmflash A, Zhang Q, Sorre B, Vonic A, Siggia ED, Brivanlou AH (2012). Dynamics of TGF-β signaling reveal adaptive and pulsatile behaviors reflected in the nuclear localization of transcription factor Smad4. Proc Natl Acad Sci USA 109, E1947-E1956.
53. Weinberger LS, Dar RD, Simpson ML (2008). Transient-mediated fate determination in a transcriptional circuit of HIV. Nat Genet 40, 466-470.
54. Wernet MF, Mazzoni EO, Çelik A, Duncan DM, Duncan I, Desplan C (2006). Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 440, 174-180.
55. Xiong W, Ferrell JE (2003). A positive-feedback-based bistable "memory module" that governs a cell fate decision. Nature 426, 460-465.
56. Yao G, Lee TJ, Mori S, Nevins JR, You L (2008). A bistable Rb-E2F switch underlies the restriction point. Nat Cell Biol 10, 476-482.