Simulation of the M13 life cycle I: Assembly of a genetically-structured deterministic chemical kinetic simulation

Virology

Volumn 500, Issue , 2017, Pages 259-274

  Smeal, Steven W ^a   Schmitt, Margaret A ^a   Pereira, Ronnie Rodrigues ^a   Prasad, Ashok ^a   Fisk, John D ^a,b  

^a Engineering Research Center and Hydraulics Laboratory   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Computational biology; Genetically structured simulation; M13 bacteriophage; Systems biology; Virus life cycle

Indexed keywords

BACTERIOPHAGE DNA; MESSENGER RNA; RF1 DNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS DNA;

ARTICLE; BIOTECHNOLOGICAL PROCEDURES; CHEMICAL REACTION KINETICS; COMPUTER SIMULATION; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; ENTEROBACTERIA PHAGE M13; ENTEROBACTERIA PHAGE MS2; ENTEROBACTERIA PHAGE QBETA; ENTEROBACTERIA PHAGE T7; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE STUDY; REGULATORY MECHANISM; RNA DEGRADATION; RNA PROCESSING; RNA TRANSLATION; SYSTEMS BIOLOGY; VIROGENESIS; VIRUS ASSEMBLY; VIRUS PARTICLE; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS; VIRUS REPLICATION;

BACTERIOPHAGE M13; COMPUTER SIMULATION; DNA REPLICATION; KINETICS; PROTEIN BIOSYNTHESIS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84994500716     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2016.08.017     Document Type: Article

References (118)

1. Alberts, B., Frey, L., Delius, H., Isolation and characterization of gene 5 protein of filamentous bacterial viruses. J. Mol. Biol. 68:1 (1972), 139–152.
2. Allen, M., Bulte, J.W.M., Liepold, L., Basu, G., Zywicke, H.A., Frank, J.A., Young, M., Douglas, T., Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents. Magn. Reson. Med. 54:4 (2005), 807–812.
3. Arkin, A., Ross, J., McAdams, H.H., Stochastic kinetic analysis of developmental pathway bifurcation in phage lambda-infected Escherichia coli cells. Genetics 149:4 (1998), 1633–1648.
4. Arter, J.A., Taggart, D.K., McIntire, T.M., Penner, R.M., Weiss, G.A., Virus-pedot nanowires for biosensing. Nano Lett. 10:12 (2010), 4858–4862.
5. Asano, S., Higashitani, A., Horiuchi, K., Filamentous phage replication initiator protein gpII forms a covalent complex with the 5 ' end of the nick it introduced. Nucleic Acids Res. 27:8 (1999), 1882–1889.
6. Baker, D., Group, B.F., Church, G., Collins, J., Endy, D., Jacobson, J., Keasling, J., Modrich, P., Smolke, C., Weiss, R., Engineering life: building a fab for biology. Sci. Am. 294:6 (2006), 44–51.
7. Bennett, N.J., Gagic, D., Sutherland-Smith, A.J., Rakonjac, J., Characterization of a dual-function domain that mediates membrane insertion and excision of Ff filamentous bacteriophage. J. Mol. Biol. 411:5 (2011), 972–985.
8. Blumer, K.J., Ivey, M.R., Steege, D.A., Translational control of phage-f1 gene-expression by differential activities of the gene V, VII, IX and VIII initiation sites. J. Mol. Biol. 197:3 (1987), 439–451.
9. Blumer, K.J., Steege, D.A., 1982. Translational Capacities of the major in vivo bacteriophage f1 messenger RNAs. Federation Proceedings 41(4), pp. 1035–1035.
10. Blumer, K.J., Steege, D.A., Messenger-RNA processing in Escherichia -coli - an activity encoded by the host processes bacteriophage-F1 messenger-RNAs. Nucleic Acids Res. 12:4 (1984), 1847–1861.
11. Bremer, H., Dennis, P.P., Modulation of Chemical Composition and Other Parameters of the Cell by Growth Rate. Escherichia coli and Salmonella : Cellular and Molecular Biology. F.C. Neidhardt and R. 1996, ASM Press, Curtiss. Washington, D.C.
12. Buchholtz, F., Schneider, F.W., Computer-simulation of T3/T7-phage infection using lag times. Biophys. Chem. 26:2–3 (1987), 171–179.
13. Carrico, Z.M., Farkas, M.E., Zhou, Y., Hsiao, S.C., Marks, J.D., Chokhawala, H., Clark, D.S., Francis, M.B., N-terminal labeling of filamentous phage to create cancer marker imaging agents. ACS Nano 6:8 (2012), 6675–6680.
14. Cashman, J.S., Webster, R.E., Steege, D.A., Transcription of Bacteriophage-Fl - the Major in vivo RNAs. J. Biol. Chem. 255:6 (1980), 2554–2562.
15. Chan, L.Y., Kosuri, S., Endy, D., Refactoring bacteriophage T7. Mol. Syst. Biol., 1, 2005, 0018, 2005.0018.
16. De Paepe, M., De Monte, S., Robert, L., Lindner, A.B., Taddei, F., Emergence of variability in isogenic escherichia coli populations infected by a filamentous virus. PLoS One, 5(7), 2010, e11823, 10.1371/journal.pone.0011823.
17. Dotto, G.P., Enea, V., Zinder, N.D., Functional-analysis of bacteriophage-F1 intergenic region. Virology 114:2 (1981), 463–473.
18. Douglas, T., Young, M., Host-guest encapsulation of materials by assembled virus protein cages. Nature 393:6681 (1998), 152–155.
19. Douglas, T., Young, M., Virus particles as templates for materials synthesis. Adv. Mat. 11:8 (1999), 679–681.
20. Duca, K.A., Lam, V., Keren, I., Endler, E.E., Letchworth, G.J., Novella, I.S., Yin, J., Quantifying viral propagation in vitro: toward a method for characterization of complex phenotypes. Biotechnol. Prog. 17:6 (2001), 1156–1165.
21. Edens, L., Konings, R.N.H., Schoenmakers, J.G.G., Cascade Mechanism of transcription in bacteriophage M13-DNA. Virology 86:2 (1978), 354–367.
22. Edens, L., Vanwezenbeek, P., Konings, R.N.H., Schoenmakers, J.G.G., Mapping of promoter sites on genome of bacteriophage-M13. Eur. J. Biochem. 70:2 (1976), 577–587.
23. Eigen, M., Biebricher, C.K., Gebinoga, M., Gardiner, W.C., The hypercycle - coupling of RNA and protein-biosynthesis in the infection cycle of an RNA Bacteriophage. Biochemistry 30:46 (1991), 11005–11018.
24. Eigen, M., Schuster, P., The Hypercycle - A principle of natural self-organization Parta. emergence of the hypercycle. Naturwissenschaften 64:11 (1977), 541–565.
25. Ekiert, D.C., Friesen, R.H.E., Bhabha, G., Kwaks, T., Jongeneelen, M., Yu, W.L., Ophorst, C., Cox, F., Korse, H., Brandenburg, B., Vogels, R., Brakenhoff, J.P.J., Kompier, R., Koldijk, M.H., Cornelissen, L., Poon, L.L.M., Peiris, M., Koudstaal, W., Wilson, I.A., Goudsmit, J., A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:6044 (2011), 843–850.
26. Ekiert, D.C., Kashyap, A.K., Steel, J., Rubrum, A., Bhabha, G., Khayat, R., Lee, J.H., Dillon, M.A., O'Neil, R.E., Faynboym, A.M., Horowitz, M., Horowitz, L., Ward, A.B., Palese, P., Webby, R., Lerner, R.A., Bhatt, R.R., Wilson, I.A., Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489:7417 (2012), 526–532.
27. Endy, D., Foundations for engineering biology. Nature 438:7067 (2005), 449–453.
28. Endy, D., Kong, D., Yin, J., Intracellular kinetics of a growing virus: a genetically structured simulation for bacteriophage T7. Biotechnol. Bioeng. 55:2 (1997), 375–389.
29. Endy, D., Yin, J., Toward antiviral strategies that resist viral escape. Antimicrob. Agents Chemother. 44:4 (2000), 1097–1099.
30. Endy, D., You, L.C., Yin, J., Molineux, I.J., Computation, prediction, and experimental tests of fitness for bacteriophage T7 mutants with permuted genomes. Proc. Natl. Acad. Sci. USA 97:10 (2000), 5375–5380.
31. Feng, J.N., Model, P., Russel, M., A trans-envelope protein complex needed for filamentous phage assembly and export. Mol. Microbiol. 34:4 (1999), 745–755.
32. Flenniken, M.L., Liepold, L.O., Crowley, B.E., Willits, D.A., Young, M.J., Douglas, T., Selective attachment and release of a chemotherapeutic agent from the interior of a protein cage architecture. Chem. Commun. 4 (2005), 447–449.
33. Fulford, W., Model, P., Gene-X of bacteriophage-F1 is required for phage dna-synthesis - mutagenesis of in-frame overlapping genes. J. Mol. Biol. 178:2 (1984), 137–153.
34. Ghosh, D., Kohli, A.G., Moser, F., Endy, D., Belcher, A.M., Refactored M13 bacteriophage as a platform for tumor cell imaging and drug delivery. ACS Synth. Biol. 1:12 (2012), 576–582.
35. Goodrich, A.F., Steege, D.A., Roles of polyadenylation and nucleolytic cleavage in the filamentous phage mRNA processing and decay pathways in Escherichia coli. RNA-a Publ. RNA Soc. 5:7 (1999), 972–985.
36. Gu, Z., Liu, J., Cao, K., Zhang, J., Wang, J., Centrality-based pathway enrichment: a systematic approach for finding significant pathways dominated by key genes. BMC Syst. Biol., 6(56), 2012, 10.1186/1752–0509-6-56.
37. Haigh, N.G., Webster, R.E., The pI and pXI assembly proteins serve separate and essential roles in filamentous phage assembly. J. Mol. Biol. 293:5 (1999), 1017–1027.
38. Hammond, B.J., Quantitative study of the control of Hiv-1 gene-expression. J. Theor. Biol. 163:2 (1993), 199–221.
39. Horabin, J.I., Webster, R.E., Morphogenesis of F1 filamentous bacteriophage - increased expression of gene-I inhibits bacterial-growth. J. Mol. Biol. 188:3 (1986), 403–413.
40. Iveyhoyle, M., Steege, D.A., Translation of phage-F1 gene-VII occurs from an inherently defective initiation site made functional by coupling. J. Mol. Biol. 208:2 (1989), 233–244.
41. Karauzum, H., Chen, G., Abaandou, L., Mahmoudieh, M., Boroun, A.R., Shulenin, S., Devi, V.S., Stavale, E., Warfield, K.L., Zeitlin, L., Roy, C.J., Sidhu, S.S., Aman, M.J., Synthetic human monoclonal antibodies toward staphylococcal enterotoxin B (Seb) protective against toxic shock syndrome. J. Biol. Chem. 287:30 (2012), 25203–25215.
42. Kay, B.K., Winter, J., McCafferty, J.D., Phage Display of Peptides and Proteins a Laboratory Manual. 1996, Academic Press, San Diego.
43. Kelman, Z., O'Donnell, M., DNA-polymerase-III holoenzyme - structure and function of a chromosomal replicating machine. Annu. Rev. Biochem. 64 (1995), 171–200.
44. Kim, H., Yin, J., Energy-efficient growth of phage Q beta in Escherichia coli. Biotechnol. Bioeng. 88:2 (2004), 148–156.
45. Kindt, J., Tzlil, S., Ben-Shaul, A., Gelbart, W.M., DNA packaging and ejection forces in bacteriophage. Proc. Natl. Acad. Sci. USA 98:24 (2001), 13671–13674.
46. Koide, S., Sidhu, S.S., The importance of being tyrosine: lessons in molecular recognition from minimalist synthetic binding protiens. ACS Chem. Biol. 4:5 (2009), 325–334.
47. Kokoska, R.J., Steege, D.A., Appropriate expression of filamentous phage F1 DNA replication genes II and X requires RNAse E-dependent processing and separate mRNAs. J. Bacteriol. 180:12 (1998), 3245–3249.
48. Kozak, M., A profusion of controls. J. Cell Biol. 107:1 (1988), 1–7.
49. Lafarina, M., Model, P., Transcription in bacteriophage F1-infected Escherichia-coli messenger populations in the infected cell. J. Mol. Biol. 164:3 (1983), 377–393.
50. Lerner, T.J., Model, P., The steady-state of coliphage-F1 - DNA-synthesis late in infection. Virology 115:2 (1981), 282–294.
51. Lin, A., Jimenez, J., Derr, J., Vera, P., Manapat, M.L., Esvelt, K.M., Villanueva, L., Liu, D.R., Chen, I.A., Inhibition of bacterial conjugation by phage M13 and its protein g3p: quantitative analysis and model. PLoS One, 6(5), 2011, e19991, 10.1371/journal.pone.0019991.
52. Linderoth, N.A., Simon, M.N., Russel, M., The filamentous phage pIV multimer visualized by scanning transmission electron microscopy. Science 278:5343 (1997), 1635–1638.
53. Mao, C.B., Solis, D.J., Reiss, B.D., Kottmann, S.T., Sweeney, R.Y., Hayhurst, A., Georgiou, G., Iverson, B., Belcher, A.M., Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303:5655 (2004), 213–217.
54. Mao, J.Y., Belcher, A.M., Van Vliet, K.J., Genetically engineered phage fibers and coatings for antibacterial applications. Adv. Funct. Mater. 20:2 (2011), 209–214.
55. Marciano, D.K., Russel, M., Simon, S.M., An aqueous channel for filamentous phage export. Science 284:5419 (1999), 1516–1519.
56. Marvin, D.A., Hohn, B., Filamentous bacterial viruses. Bacteriol. Rev. 33:2 (1969), 172–209.
57. Maslak, M., Jaworski, M.D., Martin, C.T., Tests of a model for promoter recognition by T7-RNA polymerase - thymine methyl-group contacts. Biochemistry 32:16 (1993), 4270–4274.
58. Matochko, W.L., Li, S.C., Tang, S.K.Y., Derda, R., Prospective identification of parasitic sequences in phage display screens. Nucleic Acids Res. 42:3 (2014), 1784–1798.
59. McAdams, H.H., Shapiro, L., Circuit simulation of genetic networks. Science 269:5224 (1995), 650–656.
60. Meyer, T.F., Geider, K., Enzymatic-synthesis of bacteriophage-fd viral-DNA. Nature 296:5860 (1982), 828–832.
61. Milo, R., Jorgensen, P., Moran, U., Weber, G., Springer, M., Bionumbers-the database of key numbers in molecular and cell biology. Nucleic Acids Res. 38 (2010), D750–D753.
62. Model, P., McGill, C., Mazur, B., Fulford, W.D., The replication of bacteriophage-f1 - gene-v protein regulates the synthesis of gene-II protein. Cell 29:2 (1982), 329–335.
63. Model, P., Russel, M., Filamenteous Bacteriophages. 2, 1988, The Bacteriophages. R. Calendar, New York, Plenem, 375–456.
64. Moses, P.B., Boeke, J.D., Horiuchi, K., Zinder, N.D., Restructuring the bacteriophage F1 genome - expression of gene 8 in the intergenic space. Virology 104:2 (1980), 267–278.
65. Opalka, N., Beckmann, R., Boisset, N., Simon, M.N., Russel, M., Darst, S.A., Structure of the filamentous phage Piv multimer by cryo-electron microscopy. J. Mol. Biol. 325:3 (2003), 461–470.
66. Palsson, B.O., Keasling, J.D., Emerson, S.G., The regulatory mechanisms of human immunodeficiency virus-replication predict multiple expression rates. Proc. Natl. Acad. Sci. USA 87:2 (1990), 772–776.
67. Papavoine, C.H.M., Christiaans, B.E.C., Folmer, R.H.A., Konings, R.N.H., Hilbers, C.W., Solution structure of the M13 major coat protein in detergent micelles: a basis for a model of phage assembly involving specific residues. J. Mol. Biol. 282:2 (1998), 401–419.
68. Petrenko, V.A., Smith, G.P., Phages from landscape libraries as substitute antibodies. Protein Eng. 13:8 (2000), 589–592.
69. Ploss, M., Kuhn, A., Kinetics of filamentous phage assembly. Phys. Biol., 7, 2010, 4.
70. Pratt, D., Erdahl, W.S., Genetic control of bacteriophage M13 DNA synthesis. J. Mol. Biol. 37:1 (1968), 181–200.
71. Rakonjac, J., Bennett, N.J., Spagnuolo, J., Gagic, D., Russel, M., Filamentous bacteriophage: biology, phage display and nanotechnology applications. Curr. Issues Mol. Biol. 13:2 (2011), 51–75.
72. Rakonjac, J., Feng, J.N., Model, P., Filamentous phage are released from the bacterial membrane by a two-step mechanism involving a short c-terminal fragment of pIII. J. Mol. Biol. 289:5 (1999), 1253–1265.
73. Rakonjac, J., Model, P., Roles of pIII in filamentous phage assembly. J. Mol. Biol. 282:1 (1998), 25–41.
74. Rapoza, M.P., Webster, R.E., The products of gene-I and the overlapping in-frame gene-XI are required for filamentous phage assembly. J. Mol. Biol. 248:3 (1995), 627–638.
75. Ray, D.S., Replication of bacteriophage M13 0.2. Role of replicative forms in single-strand synthesis. J. Mol. Biol. 43:3 (1969), 631–&.
76. Rhee, J.K., Baksh, M., Nycholat, C., Paulson, J.C., Kitagishi, H., Finn, M.G., Glycan-targeted virus-like nanoparticles for photodynamic therapy. Biomacromolecules 13:8 (2012), 2333–2338.
77. Russel, M., Protein-protein interactions during filamentous phage assembly. J. Mol. Biol. 231:3 (1993), 689–697.
78. Russel, M., Moving through the membrane with filamentous phages. Trends Microbiol. 3:6 (1995), 223–228.
79. Russel, M., Linderoth, N.A., Sali, A., Filamentous phage assembly: variation on a protein export theme. Gene 192:1 (1997), 23–32.
80. Russel, M., Model, P., Filamentous Phage The Bacteriophages R. Calendar, 2006, Oxford University Press, Oxford.
81. Salis, H.M., The Ribosome Binding Site Calculator. Synthetic Biology, Pt B: Computer Aided Design and DNA Assembly. C. Voigt. San Diego, Elsevier. 498, 2011, Academic Press Inc, 19–42.
82. Salis, H.M., Mirsky, E.A., Voigt, C.A., Automated design of synthetic ribosome binding sites to control protein expression. Nat. Biotechnol. 27:10 (2009), 946–950.
83. Sanghvi, A.B., Miller, K.P.H., Belcher, A.M., Schmidt, C.E., Biomaterials functionalization using a novel peptide that selectively binds to a conducting polymer. Nat. Mater. 4:6 (2005), 496–502.
84. Scott, M., Gunderson, C.W., Mateescu, E.M., Zhang, Z., Hwa, T., Interdependence of cell growth and gene expression: origins and consequences. Science 330:6007 (2010), 1099–1102.
85. Seeburg, P.H., Nusslein, C., Schaller, H., Interaction of RNA-polymerase with promoters from bacteriophage-Fd. Eur. J. Biochem. 74:1 (1977), 107–113.
86. Smeal, S.W., Schmitt, M.A., Pereira, R.R., Prasad, A., Fisk, J.D., 2016. Simulation of the M13 life cycle II: investigation of the control mechanisms of M13 infection and establishment of the carrier state. (Companion Paper).
87. Smith, G.P., Filamentous fusion phage - novel expression vectors that display cloned antigens on the virion surface. Science 228:4705 (1985), 1315–1317.
88. Smits, M.A., Jansen, J., Konings, R.N.H., Schoenmakers, J.G.G., Initiation and termination signals for transcription in bacteriophage-M13. Nucleic Acids Res. 12:10 (1984), 4071–4081.
89. Spagnuolo, J., Opalka, N., Wen, W.X., Gagic, D., Chabaud, E., Bellini, P., Bennett, M.D., Norris, G.E., Darst, S.A., Russel, M., Rakonjac, J., Identification of the gate regions in the primary structure of the secretin Piv. Mol. Microbiol. 76:1 (2010), 133–150.
90. Srivastava, R., You, L., Summers, J., Yin, J., Stochastic vs. deterministic modeling of intracellular viral kinetics. J. Theor. Biol. 218:3 (2002), 309–321.
91. Steege, D.A., Emerging features of mRNA decay in bacteria. RNA-a Publ. RNA Soc. 6:8 (2000), 1079–1090.
92. Steinmetz, N.F., Ablack, A.L., Hickey, J.L., Ablack, J., Manocha, B., Mymryk, J.S., Luyt, L.G., Lewis, J.D., Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin-releasing peptide receptors. Small 7:12 (2011), 1664–1672.
93. Stump, M.D., Steege, D.A., Functional analysis of filamentous phage F1 mRNA processing sites. RNA-a Publ. RNA Soc. 2:12 (1996), 1286–1294.
94. Suthiwangcharoen, N., Li, T., Li, K., Thompson, P., You, S.J., Wang, Q., M13 bacteriophage-polymer nanoassemblies as drug delivery vehicles. Nano Res. 4:5 (2011), 483–493.
95. Travers, A., Muskhelishvili, G., DNA supercoiling - a global transcriptional regulator for enterobacterial growth?. Nat. Rev. Microbiol. 3:2 (2005), 157–169.
96. Tsukada, K., Okazaki, M., Kita, H., Inokuchi, Y., Urabe, I., Yomo, T., Quantitative analysis of the bacteriophage Q beta infection cycle. Biochim. Biophys. Acta Gen. Subj. 1790:1 (2009), 65–70.
97. Tzlil, S., Kindt, J.T., Gelbart, W.M., Ben-Shaul, A., Forces and pressures in DNA packaging and release from viral capsids. Biophys. J. 84:3 (2003), 1616–1627.
98. Udit, A.K., Brown, S., Baksh, M.M., Finn, M.G., Immobilization of bacteriophage Q beta on metal-derivatized surfaces via polyvalent display of hexahistidine tag. J. Inorg. Biochem. 102:12 (2008), 2142–2146.
99. Vanwezenbeek, P., Hulsebos, T.J.M., Schoenmakers, J.G.G., Nucleotide-sequence of the filamentous bacteriophage M13-DNA genome - comparison with phage-Fd. Gene 11:1–2 (1980), 129–148.
100. Voigt, C.A., Synthetic biology. ACS Synth. Biol. 1:1 (2012), 1–2.
101. Wan, Z., Varshavsky, J., Teegala, S., McLawrence, J., Goddard, N.L., Measuring the rate of conjugal plasmid transfer in a bacterial population using quantitative PCR. Biophys. J. 101:1 (2011), 237–244.
102. Wan, Z.M., Goddard, N.L., Competition between conjugation and M13 phage infection in Escherichia coli in the absence of selection pressure: a kinetic study. G3-Genes Genomes Genet. 2:10 (2012), 1137–1144.
103. Weiss, G.A., Penner, R.M., The promise of phage display: customized affinity and specificity. Anal. Chem. 80:9 (2008), 3082–3089.
104. Wu, L.Y., Lee, L.A., Niu, Z.W., Ghoshroy, S., Wang, Q., Visualizing cell extracellular matrix (ECM) deposited by cells cultured on aligned bacteriophage M13 thin films. Langmuir 27:15 (2011), 9490–9496.
105. Yen, T.S.B., Webster, R.E., Translational control of bacteriophage-F1 gene-II and gene-X proteins by gene-V protein. Cell 29:2 (1982), 337–345.
106. Yoo, P.J., Nam, K.T., Qi, J.F., Lee, S.K., Park, J., Belcher, A.M., Hammond, P.T., Spontaneous assembly of viruses on multilayered polymer surfaces. Nat. Mater. 5:3 (2006), 234–240.
107. Yoo, S.Y., Merzlyak, A., Lee, S.W., Facile growth factor immobilization platform based on engineered phage matrices. Soft Matter. 7:5 (2011), 1660–1666.
108. You, L., Yin, J., Evolutionary design on a budget: robustness and optimality of bacteriophage T7. IEE Proc.: Syst. Biol. 153:2 (2006), 46–52.
109. You, L.C., Suthers, P.F., Yin, J., Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico. J. Bacteriol. 184:7 (2002), 1888–1894.
110. You, L.C., Yin, J., Amplification and spread of viruses in a growing plaque. J. Theor. Biol. 200:4 (1999), 365–373.
111. You, L.C., Yin, J., Patterns of regulation from mRNA and protein time series. Metab. Eng. 2:3 (2000), 210–217.
112. You, L.C., Yin, J., Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics 160:4 (2002), 1273–1281.
113. Young, R., Wang, I.N., Roof, W.D., Phages will out: strategies of host cell lysis. Trends Microbiol 8:3 (2000), 120–128.
114. Yu, J.S., Kokoska, R.J., Khemici, V., Steege, D.A., In-frame overlapping genes: the challenges for regulating gene expression. Mol. Microbiol 63:4 (2007), 1158–1172.
115. Zaman, G., Smetsers, A., Kaan, A., Schoenmakers, J., Konings, R., Regulation of expression of the genome of bacteriophage-M13 - gene-V protein regulated translation of the messenger-RNAs encoded by gene-I, gene-III, gene-V and gene-X.". Biochim. Biophys. Acta 1089:2 (1991), 183–192.
116. Zaman, G.J.R., Kaan, A.M., Schoenmakers, J.G.G., Konings, R.N.H., Gene-V protein-mediated translational regulation of the synthesis of gene-II protein of the filamentous bacteriophage-M13 - a dispensable function of the filamentous-phage genome. J. Bacteriol. 174:2 (1992), 595–600.
117. Zaman, G.J.R., Schoenmakers, J.G.G., Konings, R.N.H., Translational regulation of M13 Gene-II protein by its cognate single-stranded-DNA binding-protein. Eur. J. Biochem. 189:1 (1990), 119–124.
118. Zlotnick, A., To build a virus capsid - an equilibrium-model of the self-assembly of polyhedral protein complexes. J. Mol. Biol. 241:1 (1994), 59–67.