Noncommutative Biology: Sequential Regulation of Complex Networks

PLoS Computational Biology

Volumn 12, Issue 8, 2016, Pages

  Letsou, William ^a   Cai, Long ^a  

^a California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTER CIRCUITS; CYTOLOGY; TRANSCRIPTION;

CELL TYPES; CELL VARIABILITY; GENES EXPRESSION; INFORMATION BOTTLENECK; NON-COMMUTATIVE; REGULATED GENES; SEQUENTIAL LOGIC; SEQUENTIAL REGULATION; SINGLE CELLS; TIME ORDERING;

COMPLEX NETWORKS;

PHOSPHATASE; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR;

ARTICLE; ARTIFICIAL NEURAL NETWORK; CELL FATE; COMPUTER SIMULATION; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC VARIABILITY; MATHEMATICAL COMPUTING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; BIOLOGY; GENE REGULATORY NETWORK; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES;

COMPUTATIONAL BIOLOGY; GENE REGULATORY NETWORKS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84988916641     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1005089     Document Type: Article

References (109)

1. Ma HW, Kumar B, Ditges U, Gunzer F, Buer J, Zeng AP, An extended transcriptional regulatory network of Escherichia coli and analysis of its hierarchical structure and network motifs. Nucleic Acids Res. 2004;32:6643–6649. doi: 10.1093/nar/gkh100915604458
2. Balaji S, Babu MM, Iyer LM, Luscombe NM, Aravind L, Comprehensive analysis of combinatorial regulation using the transcriptional regulatory network of yeast. J Mol Biol. 2006;360:213–227. doi: 10.1016/j.jmb.2006.04.02916762362
3. Guelzim N, Bottani S, Bourgine P, Képès F, Topological and causal structure of the yeast transcriptional regulatory network. Nat Genet. 2002;31:60–63. doi: 10.1038/ng87311967534
4. Pfeiffer A, Shi H, Tepperman JM, Zhang Y, Quail PH, Combinatorial complexity in a transcriptionally centered signaling hub in Arabidopsis. Mol Plant. 2014;7:1598–1618. doi: 10.1093/mp/ssu08725122696
5. Rhee DY, Cho DY, Zhai B, Slattery M, Ma L, Mintseris J, et al. Transcription factor networks in Drosophila melanogaster. Cell Rep. 2014;8:2031–2043. doi: 10.1016/j.celrep.2014.08.03825242320
6. Neph S, Stergachis AB, Reynolds A, Sandstrom R, Borenstein E, Stamatoyannopoulos J, Circuitry and dynamics of human transcription factor regulatory networks. Cell. 2012;150:1274–1286. doi: 10.1016/j.cell.2012.04.04022959076
7. Hua S, Kittler R, White KP, Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Cell. 2009;137:1259–1271. doi: 10.1016/j.cell.2009.04.04319563758
8. Lu H, Ward MG, Adeola O, Ajuwon KM, Regulation of adipocyte differentiation and gene expression-crosstalk between TGFβ and wnt signaling pathways. Mol Bio Rep. 2013;40:5237–5245. doi: 10.1007/s11033-013-2623-2
9. Iwanaszko M, Kimmel M, NF-κB and IRF pathways: cross-regulation on target genes promoter level. BMC Genomics. 2015;16:307. doi: 10.1186/s12864-015-1511-725888367
10. Varjosalo M, Keskitalo S, Drogen AV, Nurkkala H, Vichalkovski A, Aebersold R, et al. The protein interaction landscape of the human CMGC kinase group. Cell Rep. 2013;3:1306–1320. doi: 10.1016/j.celrep.2013.03.02723602568
11. Sacco F, Perfetto L, Castagnoli L, Cesareni G, The human phosphatase interactome: An intricate family portrait. FEBS Lett. 2012;586:2732–2739. doi: 10.1016/j.febslet.2012.05.00822626554
12. Sasaki T, Minamisawa G, Takahashi N, Matsuki N, Ikegaya Y, Reverse optical trawling for synaptic connections in situ. J Neurophysiol. 209;102:636–643. doi: 10.1152/jn.00012.2009
13. Vickaryous MK, Hall BK, Human cell type diversity, evolution, development, and classification with special reference to cells derived from the neural crest. Biol Rev Camb Philos Soc. 2006;81:425–455. doi: 10.1017/S146479310600706816790079
14. Ohnishi Y, Huber W, Tsumura A, Kang M, Xenopoulos P, Kurimoto K, et al. Cell-to-cell expression variability followed by signal reinforcement progressively segregates early mouse lineages. Nat Cell Biol. 2014;16:27–37. doi: 10.1038/ncb288124292013
15. Yan L, Yang M, Guo H, Yang L, Wu J, Li R, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mo Biol. 2013;20:1131–1139. doi: 10.1038/nsmb.2660
16. Zeisel A, Muñoz-Manchado AB, Codeluppi S, Lönnerberg P, La Manno G, Juréus A, et al. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science. 2015;347:1138–1142. doi: 10.1126/science.aaa193425700174
17. Jaitin DA, Kenigsberg E, Keren-Shaul H, Elefant N, Paul F, Zaretsky I, et al. Massively parallel Single-Cell RNA-seq for marker-free decomposition of tissues into cell types. Science. 2014;343:776–779. doi: 10.1126/science.124765124531970
18. Moignard V, Woodhouse S, Haghverdi L, Lilly AJ, Tanaka Y, Wilkinson AC, et al. Decoding the regulatory network of early blood development from single-cell gene expression measurements. Nat Biotechnol. 2015;33:269–276. doi: 10.1038/nbt.315425664528
19. Treutlein B, Brownfield DG, Wu AR, Neff NF, Mantalas GL, Espinoza FH, et al. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature. 2014;509:371–375. doi: 10.1038/nature1317324739965
20. Brunskill EW, Park JS, Chung E, Chen F, Magella B, Potter SS, Single cell dissection of early kidney development: multilineage priming. Development. 2014;141:3093–3101. doi: 10.1242/dev.11060125053437
21. Vogelstein B, Kinzler KW, Cancer genes and the pathways they control. Nat Med. 2004;10:789–799. doi: 10.1038/nm108715286780
22. Gerhart J, Kerschner M, Cells, Embryos, and Evolution. Blackwell Science; 1997.
23. Wilson NK, Foster SD, Wang X, Knezevic K, Schütte J, Kaimakis P, et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell. 2010;7:532–542. doi: 10.1016/j.stem.2010.07.01620887958
24. Kaplan T, Li XY, Sabo PJ, Thomas S, Stamatoyannopoulos JA, Biggin MD, et al. Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet. 2011;7:e1001290. doi: 10.1371/journal.pgen.100129021304941
25. He X, Samee MA, Blatti C, Sinha S, Thermodynamics-based models of transcriptional regulation by enhancers: the roles of synergistic activation, cooperative binding and short-range repression. PLoS Comput Biol. 2010;6:e1000935. doi: 10.1371/journal.pcbi.100093520862354
26. Thomas R, Boolean formalization of genetic control circuits. J Theor Biol. 1973;42:563–585. doi: 10.1016/0022-5193(73)90247-64588055
27. Kauffman SA, Metabolic stability and epigenesis in randomly constructed genetic nets. J Theor Biol. 1969;22:437–467. doi: 10.1016/0022-5193(69)90015-05803332
28. Davidich MI, Bornholdt S, Boolean network model predicts cell cycle sequence of fission yeast. PLoS ONE. 2008;3:e1672. doi: 10.1371/journal.pone.000167218301750
29. Fauré A, Naldi A, Chaouiya C, Thieffry D, Dynamical analysis of a generic Boolean model for the control of the mammalian cell cycle. Bioinformatics. 2006;22:e124–e131. doi: 10.1093/bioinformatics/btl21016873462
30. Buchler NE, Gerland U, Hwa T, On schemes of combinatorial transcription logic. Proc Natl Acad Sci U S A. 2003;100:5136–5141. doi: 10.1073/pnas.093031410012702751
31. Peter IS, Faure E, Davidson EH, Predictive computation of genomic logic processing functions in embryonic development. Proc Natl Acad Sci U S A. 2012;109:16434–16442. doi: 10.1073/pnas.120785210922927416
32. Isshiki T, Pearson B, Holbrook S, Doe CQ, Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell. 2001;106:511–521. doi: 10.1016/S0092-8674(01)00465-211525736
33. Chan EAW, Teng G, Corbett E, Choudhury KR, Bassing CH, Krangel DGSMS, Peripheral subnuclear positioning suppresses Tcrb recombination and segregates Tcrb alleles from RAG2. Proc Natl Acad Sci U S A. 2013;110:E4628–E4637. doi: 10.1073/pnas.131084611024218622
34. Sayegh CE, Jhunjhunwala S, Riblet R, Murre C, Visualization of looping involving the immunoglobulin heavy-chain locus in developing B cells. Genes Dev. 2005;19:322–327. doi: 10.1101/gad.125430515687256
35. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 1998;12:3156–3161. doi: 10.1101/gad.12.20.31569784490
36. Shifley ET, Kenny AP, Rankin SA, Zorn AM, Prolonged FGF signaling is necessary for lung and liver induction in Xenopus. BMC Dev Biol. 2012;6:27. doi: 10.1186/1471-213X-12-27
37. Iyengar L, Wang Q, Rasko JE, McAvoy JW, Lovicu FJ, Duration of ERK1/2 phosphorylation induced by FGF or ocular media determines lens cell fate. Differentiation. 2007;75:662–668. doi: 10.1111/j.1432-0436.2007.00167.x17381542
38. Wada N, Nohno T, Differential Response of Shh Expression Between Chick Forelimb and Hindlimb Buds by FGF-4. Dev Dyn. 2001;221:402–411. doi: 10.1002/dvdy.115011500977
39. Iwasaki H, Mizuno S, Arinobu Y, Ozawa H, Mori Y, Shigematsu H, et al. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 2006;20:3010–3021. doi: 10.1101/gad.149350617079688
40. Ginther MR, Ramus DFWSJ, Hippocampal neurons encode different episodes in an overlapping sequence of odors task. J Neurosci. 2011;31:2706–2711. doi: 10.1523/JNEUROSCI.3413-10.201121325539
41. Agster KL, Fortin NJ, Eichenbaum H, The hippocampus and disambiguation of overlapping sequences. J Neurosci. 2002;22:5760–5768. 12097529
42. Moro SI, Tolboom M, Khayat PS, Roelfsema PR, Neuronal activity in the visual cortex reveals the temporal order of cognitive operations. J Neurosci. 2010;30:16293–16303. doi: 10.1523/JNEUROSCI.1256-10.201021123575
43. Ham TS, Lee SK, Keasling JD, Arkin AP, Design and construction of a double inversion recombination switch for heritable sequential genetic memory. PLoS One. 2008;3:e2815. doi: 10.1371/journal.pone.000281518665232
44. Payne JL, Wagner A, Constraint and contingency in multifunctional gene regulatory circuits. PLoS Comput Biol. 2013;9:e1003071. doi: 10.1371/journal.pcbi.100307123762020
45. Eldar A, Social conflict drives the evolutionary divergence of quorum sensing. Proc Natl Acad Sci U S A. 2011;108:13635–13640. doi: 10.1073/pnas.110292310821807995
46. Wang X, Minasov G, Shoichet BK, Evolution of an Antibiotic Resistance Enzyme Constrained by Stability and Activity Trade-offs. J Mol Bio. 2002;320:85–95. doi: 10.1016/S0022-2836(02)00400-X
47. Blount ZD, Borland CZ, Lenski RE, Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci U S A. 2008;105:7899–7906. doi: 10.1073/pnas.080315110518524956
48. Albeck JG, Mills GB, Brugge JS, Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals. Mol Cell. 2013;49:249–261. doi: 10.1016/j.molcel.2012.11.00223219535
49. Nelson DE, Ihekwaba AE, Elliott M, Johnson JR, Gibney CA, Foreman BE, et al. Oscillations in NF-κB signaling control the dynamics of gene expression. Science. 2004;306:704–708. doi: 10.1126/science.109996215499023
50. Kellogg RA, Tian C, Lipniacki T, Quake SR, Tay S, Digital signaling decouples activation probability and population heterogeneity. elife. 2015;4:e08931. doi: 10.7554/eLife.0893126488364
51. Lahav G, Rosenfeld N, Sigal A, Geva-Zatorsky N, Levine AJ, Elowitz MB, et al. Dynamics of the p53-Mdm2 feedback loop in individual cells. Nat Genet. 2004;36:147–150. doi: 10.1038/ng129314730303
52. Lin Y, Sohn CH, Dalal CK, Cai L, Elowitz MB, Combinatorial gene regulation by modulation of relative pulse timing. Nature. 2015;527:54–58. doi: 10.1038/nature1571026466562
53. Cai L, Dalal CK, Elowitz MB, Frequency-modulated nuclear localization bursts coordinate gene regulation. Nature. 2008;455:485–490. doi: 10.1038/nature0729218818649
54. Dalal CK, Cai L, Lin Y, Rahbar K, Elowitz MB, Pulsatile dynamics in the yeast proteome. Curr Biol. 2014;24:2189–2194. doi: 10.1016/j.cub.2014.07.07625220054
55. Roach PJ, Multisite and hierarchal protein phosphorylation. J Biol Chem. 1991;266:14139–14141. 1650349
56. Thomson M, Gunawardena J, Unlimited multistability in multisite phosphorylation systems. Nature. 2009;460:274–277. doi: 10.1038/nature0810219536158
57. Brewbaker C, A combinatorial interpretation of the poly-Bernoulli numbers and two Fermat analogues. Integers. 2008;8:A02. Available from: http://www.eudml.org/doc/130297.
58. Kaneko M, Poly-Bernoulli numbers. Journal de théorie des nombres de Bordeaux. 1997;9:221–228.
59. Martin GE, Counting: The Art of Enumerative Combinatorics. Springer; 2001.
60. Tanay A, Regev A, Shamir R, Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci U S A. 2005;102:7203–7206. doi: 10.1073/pnas.050252110215883364
61. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I, Brugman W, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell. 2010;38:603–613. doi: 10.1016/j.molcel.2010.03.01620513434
62. Zullo JM, Demarco IA, Piqué-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, et al. DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell. 2012;149:1474–1487. doi: 10.1016/j.cell.2012.04.03522726435
63. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell. 2010;143:212–224. doi: 10.1016/j.cell.2010.09.00920888037
64. Edwards R, Glass L, Combinatorial explosion in model gene networks. Chaos. 2000;10:691–704. doi: 10.1063/1.128699712779419
65. Green JA, Rees D, On semi-groups in which xr = x. Mathematical Proceedings of the Cambridge Philosophical Society. 1952;48:35–40. doi: 10.1017/S0305004100027341
66. Takahashi K, Yamanaka S, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–676. doi: 10.1016/j.cell.2006.07.02416904174
67. Murray RM, Sastry SS, Nonholonomic motion planning: steering using sinusoids. IEEE Transactions on Automatic Control. 1993;38:700–716. doi: 10.1109/9.277235
68. Sternberg S, Lie Algebras. Book online; 2004. p. 7–32. Available from: http://www.math.harvard.edu/~shlomo.
69. Carravetta M, Levitt MH, Long-lived nuclear spin states in high-field solution NMR. J Am Chem Soc. 2004;126:6228–6229. doi: 10.1021/ja049093115149209
70. Attanasio C, Nord AS, Zhu Y, Blow MJ, Biddie SC, Mendenhall EM, et al. Tissue-specific SMARCA4 binding at active and repressed regulatory elements during embryogenesis. Genome Res. 2014;24:920–929. doi: 10.1101/gr.168930.11324752179
71. Kudron M, Niu W, Lu Z, Wang G, Gerstein M, Snyder M, et al. Tissue-specific direct targets of Caenorhabditis elegans Rb/E2F dictate distinct somatic and germline programs. Genome Biol. 2013;14:R5. doi: 10.1186/gb-2013-14-1-r523347407
72. Noordermeer D, de Wit E, Klous P, van de Werken H, Simonis M, Lopez-Jones M, et al. Variegated gene expression caused by cell-specific long-range DNA interactions. Nat Cell Biol. 2011;13:944–951. doi: 10.1038/ncb227821706023
73. Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E, Dean W, et al. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature. 2013;502:59–64. doi: 10.1038/nature1259324067610
74. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet. 2010;42:53–61. doi: 10.1038/ng.49620010836
75. Marsman J, Horsfield JA, Long distance relationships: Enhancer-promoter communication and dynamic gene transcription. Biochim Biophys Acta. 2012;18–19:1217–1227. doi: 10.1016/j.bbagrm.2012.10.008
76. Handoko L, Xu H, Li G, Ngan CY, Chew E, Schnapp M, et al. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet. 2011;43:630–638. doi: 10.1038/ng.85721685913
77. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, et al. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev. 2006;20:2349–2354. doi: 10.1101/gad.39950616951251
78. Bell AC, West AG, Felsenfeld G, The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell. 1999;98:387–396. doi: 10.1016/S0092-8674(00)81967-410458613
79. Hou C, Zhao H, Tanimoto K, Dean A, CTCF-dependent enhancer-blocking by alternative chromatin loop formation. Proc Natl Acad Sci U S A. 2008;105:20398–20403. doi: 10.1073/pnas.080850610619074263
80. Guertin MJ, Lis JT, Mechanisms by which transcription factors gain access to target sequence elements in chromatin. Curr Opin Genet Dev. 2013;23:116–123. doi: 10.1016/j.gde.2012.11.00823266217
81. Zentner GE, Tesar PJ, Scacheri PC, Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res. 2011;21:1273–1283. doi: 10.1101/gr.122382.11121632746
82. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 2007;448:553–560. doi: 10.1038/nature0600817603471
83. Mossman D, Kim KT, Scott RJ, Demethylation by 5-aza-2’-deoxycytidine in colorectal cancer cells targets genomic DNA whilst promoter CpG island methylation persists. BMC Cancer. 2010;10:366. doi: 10.1186/1471-2407-10-36620618997
84. Yoshida M, Kijima M, Akita M, Beppu T, Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J Biol Chem. 1990;265:17174–17179. 2211619
85. Dannengerg LO, Edenberg HJ, Epigenetics of gene expression in human hepatoma cells: expression profiling the response to inhibition of DNA methylation and histone deacetylation. BMC Genomics. 2006;7:181. doi: 10.1186/1471-2164-7-181
86. Qi Y, Fan P, Hao Y, Han B, Fang Y, Feng M, et al. Phosphoproteomic analysis of protein phosphorylation networks in the hypopharyngeal gland of honeybee workers (Apis mellifera ligustica). J Proteome Res. 2015;14:4647–4661. doi: 10.1021/acs.jproteome.5b0053026384081
87. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell. 2010;143:1174–1189. doi: 10.1016/j.cell.2010.12.00121183079
88. Schmidt B, Marrone DF, Markus EJ, Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Behav Brain Res. 2012;226:56–65.
89. Brown TI, Ross RS, Keller JB, Hasselmo ME, Stern CE, Which way was I going? Contextual retrieval supports the disambiguation of well learned overlapping navigational routes. J Neurosci. 2010;30:7414–7422. doi: 10.1523/JNEUROSCI.6021-09.201020505108
90. Leutgeb JK, Leutgeb S, Moser MB, Moser MI, Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science. 2007;315:961–966. doi: 10.1126/science.113580117303747
91. Chadwick MJ, Maguire DHMA, Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI. Learn Mem. 2011;18:742–746. doi: 10.1101/lm.023671.11122086391
92. Waddington CH, The cybernetics of development. In: The Strategy of the Genes. George Allen & Unwin Ltd.; 1957. p. 11–58.
93. Huang S, Systems biology of stem cells: three useful perspectives to help overcome the paradigm of linear pathways. Philos Trans R Soc Lond B Biol Sci. 2011;366:2247–2259. doi: 10.1098/rstb.2011.000821727130
94. St Johnston D, Nüsslein-Volhard C, The origin of pattern and polarity in the Drosophila embryo. Cell. 1992;68:201–219. doi: 10.1016/0092-8674(92)90466-P1733499
95. Akashi K, He X, Chen J, Iwasaki H, Niu C, Steenhard B, et al. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood. 2003;101:383–389. doi: 10.1182/blood-2002-06-178012393558
96. Biddie SC, John S, Sabo PJ, Thurman RE, Johnson TA, Schiltz RL, et al. Transcription Factor AP1 Potentiates Chromatin Accessibility and Glucocorticoid Receptor Binding. Mol Cell. 2011;43:145–155. doi: 10.1016/j.molcel.2011.06.01621726817
97. Voss TC, Schiltz RL, Sung MH, Yen PM, Stamatoyannopoulos JA, Biddie SC, et al. Dynamic Exchange at Regulatory Elements during Chromatin Remodeling Underlies Assisted Loading Mechanism. Cell. 2011;146:544–554. doi: 10.1016/j.cell.2011.07.00621835447
98. Huang S, Guo YP, May G, Enver T, Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev Biol. 2007;305:695–713. doi: 10.1016/j.ydbio.2007.02.03617412320
99. Ferrell J, Bistability, bifurcations, and Waddington’s epigenetic landscape. Curr Biol. 2012;22:R458–456. doi: 10.1016/j.cub.2012.03.04522677291
100. Romero PA, Arnold FH, Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol. 2008;10:866–876. doi: 10.1038/nrm2805
101. Fritz G, Buchler NE, Hwa T, Gerland U, Designing sequential transcription logic: a simple genetic circuit for conditional memory. Syst Synth Biol. 2007;1:89–98. doi: 10.1007/s11693-007-9006-819003438
102. Margulies D, Felder CE, Melman G, Shanzer A, A molecular keypad lock: a photochemical device capable of authorizing password entries. J Am Chem Soc. 2007;129:347–354. doi: 10.1021/ja065317z17212414
103. Lou C, Liu X, Ni M, Huang Y, Huang Q, Huang L, et al. Synthesizing a novel genetic sequential logic circuit: a push-on push-off switch. Mol Syst Biol. 2010;6:350. doi: 10.1038/msb.2010.220212522
104. Voight CA, Genetic parts to program bacteria. Curr Opin Biotechnol. 2006;23:548–557. doi: 10.1016/j.copbio.2006.09.001
105. Rao CV, Expanding the synthetic biology toolbox: engineering orthogonal regulators of gene expression. Curr Opin Biotechnol. 2012;23:689–694. doi: 10.1016/j.copbio.2011.12.01522237017
106. Lubeck E, Coskun AF, Zhiyentayev T, Ahmad M, Cai L, Single-cell in situ RNA profiling by sequential hybridization. Nat Methods. 2014;11:360–361. doi: 10.1038/nmeth.289224681720
107. Groh C, Moldovanu B, Sela A, Sunde U, Optimal seedings in elimination tournaments. Economic Theory. 2008;49:59–80. doi: 10.1007/s00199-008-0356-6
108. Fudenberg D, Maskin E, Evolution and cooperation in noisy repeated games. In: The American Economic Review. vol. 80. American Economic Association; 1990. p. 274–279. Available from: http://www.jstor.org/stable/2006583.
109. Kim HK, Krotov DS, Lee JY, Poly-Bernoulli numbers and lonesum matrices. arXiv. 2011;1103.4884.