To Lyse or not to Lyse: Transient-mediated stochastic fate determination in cells infected by bacteriophages

PLoS Computational Biology

Volumn 7, Issue 3, 2011, Pages

  Joh, Richard I ^a   Weitz, Joshua S ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DECISION MAKING; DYNAMICS; GENES; STOCHASTIC MODELS; STOCHASTIC SYSTEMS; TRANSIENT ANALYSIS;

CELL-FATE; CELLULARS; DATA COLLAPSE; DECISIONS MAKINGS; GENE DOSAGE; GENE REGULATORY NETWORKS; MULTIPLE STEADY STATE; STOCHASTIC DYNAMICS; STOCHASTICS; TRANSIENT DYNAMICS;

BACTERIOPHAGES;

MESSENGER RNA;

ARTICLE; BACTERIAL CELL; BACTERIAL INFECTION; BACTERIOPHAGE LAMBDA; CELL ASSAY; CELL FATE; CELL HETEROGENEITY; CONTROLLED STUDY; CYTOLYSIS; GENE DOSAGE; GENE REGULATORY NETWORK; GENOME ANALYSIS; LYSOGENIZATION; MOLECULAR DYNAMICS; NONHUMAN; QUANTITATIVE ANALYSIS; STEADY STATE; STOCHASTIC MODEL; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY;

ENTEROBACTERIA PHAGE LAMBDA;

BACTERIOPHAGE LAMBDA; COMPUTER SIMULATION; GENE EXPRESSION REGULATION, VIRAL; GENE REGULATORY NETWORKS; LYSOGENY;

EID: 79953657876     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002006     Document Type: Article

References (75)

1. Solomon JM, Grossman AD, (1996) Who's competent and when: regulation of natural genetic competence in bacteria. Trends Genet 12: 150-155.
2. Stragier P, Losick R, (1996) Molecular genetics of sporulation in Bacillus subtilis. Annu Rev Gen 30: 297-341.
3. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S, (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
4. Ptashne M, (2004) A genetic switch. Phage lambda revisted. Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press, 3rd edition.
5. Morrison SJ, Shar NM, (1997) Regulatory mechanisms in stem cell biology. Cell 88: 287-298.
6. McAdams HH, Arkin A, (1999) It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet 15: 65-69.
7. Kaern M, Elston TC, Blake WJ, Collins JJ, (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-464.
8. Kaufmann BB, van Oudenaarden A, (2007) Stochastic gene expression: from single molecules to the proteome. Curr Opin Genet Dev 17: 107-112.
9. Spudich JL, Koshland DE Jr, (1976) Non-genetic individuality: chance in the single cell. Nature 262: 467-471.
10. Elowitz MB, Levine AJ, Siggia ED, Swain PS, (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186.
11. Maamar H, Raj A, Dubnau D, (2007) Noise in gene expression determines cell in Bacillus subtilis. Science 317: 526-529.
12. Maamar H, Dubnau D, (2005) Bistability in the Bacillus subtilis K-state (competence) system requires a positive feedback loop. Mol Microbiol 56: 615-624.
13. Losick R, Desplan C, (2008) Stochasticity and cell fate. Science 320: 65-68.
14. Xiong W, Ferrell JE Jr, (2003) A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426: 460-465.
15. Weinberger L, Dar RD, Simpson ML, (2008) Transient-mediated fate determination in a transcriptional circuit of HIV. Nat Gen 40: 466-470.
16. Alon U, (2007) An introduction to systems biology: Design principles of biological circuits. Boca Raton, FL Chapman & Hall.
17. Darling DA, Siegert AJF, (1953) The first passage problem for a continuous Markov process. Ann Math Statist 4: 624-639.
18. Redner S, (2001) A guide to first-passage processes. Cambridge, UK Cambridge University Press, 1st edition.
19. Hendrix RW, Roberts JW, Stahl FW, Weisberg RA, (1983) Lambda II. Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
20. Dodd IB, Shearwin KE, Egan JB, (2005) Revisited gene regulation in bacteriophage.λ. Curr Opin Genes Dev 15: 145-152.
21. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S, (2005) Switches in bacteriophage lambda development. Annu Rev Genet 39: 409-429.
22. Court DL, Oppenheim AB, Adhya SL, (2007) A new look at bacteriophage λ genetic networks. J Bacteriol 189: 298-304.
23. Kourilsky P, (1973) Lysogenization by bacteriophage lambda. I. Multiple infection and the lysogenic response. Mol Gen Genet 122: 183-195.
24. Kobiler O, Rokney A, Fredman N, Court DL, Stravans J, et al. (2005) Quantitative kinetic analysis of the bacteriophage λ genetic network. Proc Natl Acad Sci USA 102: 4470-4475.
25. Arkin A, Ross J, McAdams HH, (1998) Stochastic kinetic analysis of developmental pathway bifurcation in phage λ-infected Escherichia coli cells. Genetics 149: 1633-1648.
26. Singh A, Weinberger LS, (2009) Stochastic gene expression as a molecular switch for viral latency. Curr Opin Microbiol 12: 460-466.
27. St Pierre F, Endy D, (2008) Determination of cell fate selection during phage lambda infection. Proc Natl Acad Sci USA 105: 20705-20710.
28. Weitz JS, Mileyko Y, Joh RI, Voit EO, (2008) Collective decisions among bacterial viruses. Biophys J 95: 2673-2680.
29. Zeng L, Skinner SO, Zong C, Slippy J, Feiss M, et al. (2010) Decision making at a subcellular level determines the outcome of bacteriophage infection. Cell 141: 682-691.
30. Aurell E, Sneppen K, (2002) Epigenetics as a first exit problem. Phys Rev Lett 88: 048101.
31. Hochschild A, Ptashne M, (1984) Cooperative binding of lambda repressors to sites separated by integral turns of the DNA helix. Cell 44: 681-687.
32. Griffith J, Hochschild A, Ptashne M, (1986) DNA loops induced by cooperative binding of λ repressor. Nature 322: 750-752.
33. Babi c′ AC, Little JW, (2007) Cooperative DNA binding by CI repressor is dispensable in a phage λ variant. Proc Natl Acad Sci USA 104: 17741-17746.
34. Morelli MJ, ten Wolde PR, Allen RJ, (2009) DNA looping provides stability and robustness to the bacteriophage λ switch. Proc Natl Acad Sci USA 106: 8101-8106.
35. Ackers GK, Shea MA, (1982) Quantitative model for gene regulation by lambda phage repressor. Proc Natl Acad Sci USA 79: 1129-1133.
36. Shea MA, Ackers GK, (1985) The OR control system of bacteriophage lambda. A physical-chemical model for gene regulation. J Mol Biol 181: 211-230.
37. Terzi M, Levinthal C, (1967) Effects of λ-phage infection on bacterial synthesis. J Mol Biol 26: 525-530.
38. Howes WV, (1965) Protein synthesis in Escherichia coli: a phage mediated interruption of tranalasion. Biochim Biophys Acta 103: 711-713.
39. Birchler JA, Riddle NC, Auger DL, Veitia RA, (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21: 219-226.
40. Svenningsen SL, Tu KC, Bassler BL, (2009) Gene dosage compensation calibrates four regulatory RNAs to control Vibriio cholerae quorum sensing. EMBO J 28: 429-439.
41. Springer M, Weissman JS, Kirschner MW, (2010) A general lack of compensation for gene dosage in yeast. Mol Syst Biol 6: 368.
42. Gardner TS, Cantor CR, Collins JJ, (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-342.
43. Cherry JL, Adler FR, (2000) How to make a biological switch. J Theor Biol 203: 117-133.
44. Lipshtat A, Loinger A, Balaban NQ, Biham O, (2006) Genetic toggle switch without cooperative binding. Phys Rev Lett 96: 188101.
45. Süel MB, Garcia-Ojalvo J, Liberman LM, Elowitz MB, (2006) An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440: 545-550.
46. Ziv E, Nemenman I, Wiggins CH, (2007) Optimal signal processing in small stochastic biochemical networks. PLoS ONE 2: e1077.
47. Stewart FM, Levin BR, (1984) The population biology of bacterial viruses: Why be temperate? Theor Pop Biol 26: 93-117.
48. Avlund M, Dodd IB, Semsey S, Sneppen K, Krishna S, (2009) Why do phage play dice? J Virol 83: 11416-11420.
49. Veening J, Smits WK, Kulpers OP, (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62: 193-210.
50. Gudelj I, Weitz JS, Ferenci T, Horner-Devine MC, Marx CJ, et al. (2010) An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure. Ecol Lett 13: 1073-1084.
51. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, et al. (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39: 1256-1260.
52. DeLuna A, Vetsigian K, Shoresh N, Hegreness M, Colon-Gonzalez M, et al. (2008) Exposing the fitness contribution of duplicated genes. Nat Genet 40: 676-681.
53. Mileyko Y, Joh RI, Weitz JS, (2008) Small-scale copy number variation and large-scale changes in gene expression. Proc Natl Acad Sci USA 105: 16659-16664.
54. Schuster-Böckler B, Conrad D, Bateman A, (2010) Dosage sensitivity shapes the evolution of copy-number varied regions. PLoS ONE 5: e9474.
55. Ben-Israel H, Kleinberger T, (2002) Adenovirus and cell cycle control. Front Biocsi 7: d1369-d1395.
56. Sherratt DJ, (2003) Bacterial chromosome dynamics. Science 301: 780-785.
57. Russell JH, Keiler KC, (2009) Subcellular localization of a bacterial regulatory RNA. Proc Natl Acad Sci USA 106: 16405-16409.
58. Thanbichler M, Shapiro L, (2008) Getting organized-how bacterial cells move proteins and DNA. Nat Rev Microbiol 6: 28-40.
59. Edgar R, Rokney A, Feeney M, Semsey S, Kessel M, et al. (2008) Bacteriophage infection is targeted to cellular poles. Mol Microbiol 68: 1107-1116.
60. Marshall CJ, (1995) Specificity of receptop tyrosine kinase signaling: transient versus susained extracellular signal-regulated kinase activation. Cell 80: 179-185.
61. Ebisuya M, Kondoh K, Nishida E, (2005) The duration, magnitude and compartmentalization of EKR MAP kinase activity: mechanisms for providing signaling specificity. J Cell Sci 118: 2997-3002.
62. Mangan S, Itzkovitz S, Zaslaver A, Alon U, (2006) The incoherent feed-forward loop accelerates the response-time of the gal system of Escherichia coli. J Mol Biol 356: 1073-1081.
63. Parua PK, Datta AB, Parrack P, (2010) Specific hydrophobic residues in the α 4 helix of λ CII are crucial for maintaining its tetrameric structure and directing the lysogenic choice. J Gen Virol 91: 306-312.
64. Révet B, von Wilcken-Bergmann B, Bessert H, Barker A, Muller-Hill B, (1999) Four dimers of λ repressor bound to two suitably spaced pairs of lambda operators form octamers and DNA loops over large distances. Curr Biol 9: 151-154.
65. Gillespie DT, (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 82: 2340-2361.
66. Hawley DK, Johnson AD, McClure WR, (1985) Functional and physical characterization of transcription initiation complexes in the bacteriophage λ OR region. J Biol Chem 260: 8618-8626.
67. Pakula AA, Young VB, Sauer RT, (1986) Bacteriophage lambda cro mutations: effects on activity and intracellular degradation. Proc Natl Acad Sci USA 83: 8829-8833.
68. Kobiler O, Koby S, Teff D, Court D, Oppenheim AB, (2002) The phage λ CII transcriptional activator carries a C-terminal domain signaling for rapid proteolysis. Proc Natl Acad Sci USA 99: 14964-14969.
69. Court D, Crombrugghe B, Adhya S, Gottesman M, (1980) Bacteriophage lambda Hin function II. Enhanced stability of lambda messenger RNA. J Mol Biol 138: 731-743.
70. Hwang JJ, Brosn S, Gussin GN, (1988) Characterization of a doubly mutant derivative of the lambda PRM promoter. Effects of mutations on activation of PRM. J Mol Biol 200: 695-708.
71. Sauer RT, Pabo CO, Meyer BJ, Ptashne M, Backman KC, (1979) Regulatory functions of the lambda. Repressor reside in the amino-terminal domain. Nature 279: 396-400.
72. Burz D, Becket D, Benson N, Ackers GK, (1994) Self-assembly of bacteriophage λ CI repressor: effects of single-site mutations on the monomer-dimer equilibrium. Biochemistry 33: 8399-8405.
73. Jana R, Hazbun TR, Mollah AK, Mossing MC, (1997) A folded monomeric intermediate in the formation of lambda Cro dimer-dna complexes. J Mol Biol 273: 402-416.
74. Darling PJ, Holt JM, Ackers GK, (2000) Couple energetics of λ cro repressor self-assembly and site-specific DNA operator binding. I: Analysis of cro dimerization from nanomolar to micromolar concentrations. Biochemistry 39: 11500-11507.
75. Levine E, Hwa T, (2008) Small RNAs establish gene expression thresholds. Curr Opin Microbiol 11: 574-579.