In vivo biochemistry in bacterial cells using FRAP: Insight into the translation cycle

Biophysical Journal

Volumn 103, Issue 9, 2012, Pages 1848-1859

  Montero Llopis, Paula ^a,c   Sliusarenko, Oleksii ^a   Heinritz, Jennifer ^a   Jacobs Wagner, Christine ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ARTICLE; BIOSYNTHESIS; CAULOBACTER; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETICS; KINETICS; LARGE RIBOSOMAL SUBUNIT; METABOLISM; PROTEIN BINDING; PROTEIN SYNTHESIS; SMALL RIBOSOMAL SUBUNIT;

CAULOBACTER; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; KINETICS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); CAULOBACTER;

EID: 84868561007     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.09.035     Document Type: Article

References (77)

1. J. Spitzer From water and ions to crowded biomacromolecules: in vivo structuring of a prokaryotic cell Microbiol. Mol. Biol. Rev. 75 2011 491 506
2. S.B. Zimmerman, and S.O. Trach Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli J. Mol. Biol. 222 1991 599 620
3. H.X. Zhou, G. Rivas, and A.P. Minton Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys 37 2008 375 397
4. A.P. Minton How can biochemical reactions within cells differ from those in test tubes? J. Cell Sci. 119 2006 2863 2869
5. J.T. Mika, and B. Poolman Macromolecule diffusion and confinement in prokaryotic cells Curr. Opin. Biotechnol. 22 2011 117 126
6. B.L. Sprague, and J.G. McNally FRAP analysis of binding: proper and fitting Trends Cell Biol. 15 2005 84 91
7. J.G. McNally Quantitative FRAP in analysis of molecular binding dynamics in vivo Methods Cell Biol. 85 2008 329 351
8. M.A. Hallen, and A.T. Layton Expanding the scope of quantitative FRAP analysis J. Theor. Biol. 262 2010 295 305
9. M.B. Elowitz, and M.G. Surette S. Leibler Protein mobility in the cytoplasm of Escherichia coli J. Bacteriol. 181 1999 197 203
10. M.C. Konopka, and I.A. Shkel J.C. Weisshaar Crowding and confinement effects on protein diffusion in vivo J. Bacteriol. 188 2006 6115 6123
11. M. Kumar, M.S. Mommer, and V. Sourjik Mobility of cytoplasmic, membrane, and DNA-binding proteins in Escherichia coli Biophys. J. 98 2010 552 559
12. C.W. Mullineaux, and A. Nenninger C. Robinson Diffusion of green fluorescent protein in three cell environments in Escherichia coli J. Bacteriol. 188 2006 3442 3448
13. S. Bakshi, B.P. Bratton, and J.C. Weisshaar Subdiffraction-limit study of Kaede diffusion and spatial distribution in live Escherichia coli Biophys. J. 101 2011 2535 2544
14. J.T. Mika, and V. Krasnikov B. Poolman Evaluation of pulsed-FRAP and conventional-FRAP for determination of protein mobility in prokaryotic cells PLoS ONE 6 2011 e25664
15. G. van den Bogaart, and N. Hermans B. Poolman Protein mobility and diffusive barriers in Escherichia coli: consequences of osmotic stress Mol. Microbiol. 64 2007 858 871
16. S. Schulmeister, and M. Ruttorf V. Sourjik Protein exchange dynamics at chemoreceptor clusters in Escherichia coli Proc. Natl. Acad. Sci. USA 105 2008 6403 6408
17. B.S. Laursen, and H.P. Sorensen H.U. Sperling-Petersen Initiation of protein synthesis in bacteria Microbiol. Mol. Biol. Rev. 69 2005 101 123
18. A. Simonetti, and S. Marzi M. Yusupov A structural view of translation initiation in bacteria Cell. Mol. Life Sci. 66 2009 423 436
19. J.A. Dunkle, and J.H. Cate Ribosome structure and dynamics during translocation and termination Annu. Rev. Biophys 39 2010 227 244
20. G. Hirokawa, and R.M. Nijman A. Kaji The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits RNA 11 2005 1317 1328
21. F. Peske, M.V. Rodnina, and W. Wintermeyer Sequence of steps in ribosome recycling as defined by kinetic analysis Mol. Cell 18 2005 403 412
22. A.V. Zavialov, V.V. Hauryliuk, and M. Ehrenberg Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G Mol. Cell 18 2005 675 686
23. D.G. Dalbow, and R. Young Synthesis time of beta-galactosidase in Escherichia coli B/r as a function of growth rate Biochem. J. 150 1975 13 20
24. M.A. Sorensen, C.G. Kurland, and S. Pedersen Codon usage determines translation rate in Escherichia coli J. Mol. Biol. 207 1989 365 377
25. M.A. Sorensen, and U. Vogel S. Pedersen The rates of macromolecular chain elongation modulate the initiation frequencies for transcription and translation in Escherichia coli Antonie van Leeuwenhoek 63 1993 323 331
26. R. Young, and H. Bremer Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate Biochem. J. 160 1976 185 194
27. Y. Wang, B.D. Jones, and Y.V. Brun A set of ftsZ mutants blocked at different stages of cell division in Caulobacter Mol. Microbiol. 40 2001 347 360
28. P. Montero Llopis, and A.F. Jackson C. Jacobs-Wagner Spatial organization of the flow of genetic information in bacteria Nature 466 2010 77 81
29. M. Thanbichler, A.A. Iniesta, and L. Shapiro A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus Nucleic Acids Res. 35 2007 e137
30. M. Evinger, and N. Agabian Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells J. Bacteriol. 132 1977 294 301
31. O. Sliusarenko, and J. Heinritz C. Jacobs-Wagner High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics Mol. Microbiol. 80 2011 612 627
32. M.C. Konopka, and K.A. Sochacki J.C. Weisshaar Cytoplasmic protein mobility in osmotically stressed Escherichia coli J. Bacteriol. 191 2009 231 237
33. J.T. Mika, and G. van den Bogaart B. Poolman Molecular sieving properties of the cytoplasm of Escherichia coli and consequences of osmotic stress Mol. Microbiol. 77 2010 200 207
34. A.J. Kelly, and M.J. Sackett Y.V. Brun Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter Genes Dev. 12 1998 880 893
35. A. Thom, and C.J. Apelt Field Computations in Engineering and Physics 1961 D. Van Nostrand London
36. B.P. English, and V. Hauryliuk J. Elf Single-molecule investigations of the stringent response machinery in living bacterial cells Proc. Natl. Acad. Sci. USA 108 2011 E365 E373
37. S.F. Lee, and M.A. Thompson W.E. Moerner Super-resolution imaging of the nucleoid-associated protein HU in Caulobacter crescentus Biophys. J. 100 2011 L31 L33
38. C. Robinow, and E. Kellenberger The bacterial nucleoid revisited Microbiol. Rev. 58 1994 211 232
39. A. Briegel, and D.P. Dias G.J. Jensen Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography Mol. Microbiol. 62 2006 5 14
40. J. Marvaldi, and J. Pichon G. Marchis-Mouren Individual ribosomal protein pool size and turnover rate in Escherichia coli J. Mol. Biol. 84 1974 83 96
41. P. Gamba, and J.W. Veening R.A. Daniel Two-step assembly dynamics of the Bacillus subtilis divisome J. Bacteriol. 191 2009 4186 4194
42. A.D. Russell, and R.H. Fountain Aspects of the mechanism of action of some cephalosporins J. Bacteriol. 106 1971 65 69
43. S. Bakshi, and A. Siryaporn J.C. Weisshaar Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells Mol. Microbiol. 85 2012 21 38
44. H.A. De Boer, and A.J. Bakker M. Gruber The role of energy-generating processes in the degradation of guanosine tetrophosphate, ppGpp, in Escherichia coli Biochim. Biophys. Acta 432 1976 361 368
45. M. Aviram, and A. Hershko Proceedings: energy requirement of the breakdown of RNA in cultured hepatoma cells Isr. J. Med. Sci. 11 1975 1200
46. E.A. Park, and H.E. Morgan Energy dependence of RNA degradation in rabbit reticulocytes Am. J. Physiol. 247 1984 C390 C395
47. L. Jarett, and R.W. Hendler 2,4-Dinitrophenol and azide as inhibitors of protein and ribonucleic acid synthesis in anaerobic yeast Biochemistry 6 1967 1693 1703
48. J. Forchhammer, and L. Lindahl Growth rate of polypeptide chains as a function of the cell growth rate in a mutant of Escherichia coli 15 J. Mol. Biol. 55 1971 563 568
49. G. Mangiarotti, and D. Schlessinger Polyribosome metabolism in Escherichia coli. I. Extraction of polyribosomes and ribosomal subunits from fragile, growing Escherichia coli J. Mol. Biol. 20 1966 123 143
50. L.A. Phillips, B. Hotham-Iglewski, and R.M. Franklin Polyribosomes of Escherichia coli. II. Experiments to determine the in vivo distribution of polysomes, ribosomes and ribosomal subunits J. Mol. Biol. 45 1969 23 38
51. L.A. Phillips, B. Hotham-Iglewski, and R.M. Franklin Polyribosomes of Escherichia coli. I. Effects of monovalent cations on the distribution of polysomes, ribosomes and ribosomal subunits J. Mol. Biol. 40 1969 279 288
52. F. Varricchio, and R. Monier Ribosome patterns in Escherichia coli growing at various rates J. Bacteriol. 108 1971 105 110
53. S.C. Weber, A.J. Spakowitz, and J.A. Theriot Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci Proc. Natl. Acad. Sci. USA 109 2012 7338 7343
54. E. Oh, and A.H. Becker B. Bukau Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo Cell 147 2011 1295 1308
55. H. Bremer, and P.P. Dennis Modulation of chemical composition and other parameters of the cell by growth rate F.C. Neidhardt, Escherichia coli and Salmonella 1996 ASM Press Washington 1553 1569
56. M.A. Sorensen, and S. Pedersen Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate J. Mol. Biol. 222 1991 265 280
57. S.T. Liang, and Y.C. Xu H. Bremer mRNA composition and control of bacterial gene expression J. Bacteriol. 182 2000 3037 3044
58. S. Proshkin, and A.R. Rahmouni E. Nudler Cooperation between translating ribosomes and RNA polymerase in transcription elongation Science 328 2010 504 508
59. D.I. Svergun, and J.S. Pedersen M.H. Koch Solution scattering from 50S ribosomal subunit resolves inconsistency between electron microscopic models Proc. Natl. Acad. Sci. USA 91 1994 11826 11830
60. J.L. Hansen, P.B. Moore, and T.A. Steitz Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit J. Mol. Biol. 330 2003 1061 1075
61. M. Ormö, and A.B. Cubitt S.J. Remington Crystal structure of the Aequorea victoria green fluorescent protein Science 273 1996 1392 1395
62. A. Nenninger, G. Mastroianni, and C.W. Mullineaux Size dependence of protein diffusion in the cytoplasm of Escherichia coli J. Bacteriol. 192 2010 4535 4540
63. A. Bancaud, and S. Huet J. Ellenberg Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin EMBO J. 28 2009 3785 3798
64. D. Schlessinger, and C. Gurgo D. Apirion Polyribosome metabolism in growing and nongrowing Escherichia coli Cold Spring Harb. Symp. Quant. Biol. 34 1969 231 242
65. J.E. Cabrera, and D.J. Jin The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues Mol. Microbiol. 50 2003 1493 1505
66. R.B. Jensen, and L. Shapiro The Caulobacter crescentus smc gene is required for cell cycle progression and chromosome segregation Proc. Natl. Acad. Sci. USA 96 1999 10661 10666
67. A. Okuyama, and N. Machiyama N. Tanaka Inhibition by kasugamycin of initiation complex formation on 30S ribosomes Biochem. Biophys. Res. Commun. 43 1971 196 199
68. E. Schneider, M. Blundell, and D. Kennell Translation and mRNA decay Mol. Gen. Genet. 160 1978 121 129
69. A.C. Kaberdina, and W. Szaflarski I. Moll An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis? Mol. Cell 33 2009 227 236
70. M. Takanami, and T. Okamoto Interaction of ribosomes and synthetic polyribonucleotides J. Mol. Biol. 7 1963 323 333
71. T. Okamoto, and M. Takanami Interaction of ribosomes and natural polyribonucleotides Biochim. Biophys. Acta 76 1963 266 274
72. B. Lin, D.A. Thayer, and J.R. Maddock The Caulobacter crescentus CgtAC protein cosediments with the free 50S ribosomal subunit J. Bacteriol. 186 2004 481 489
73. J.A. Bernstein, and A.B. Khodursky S.N. Cohen Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays Proc. Natl. Acad. Sci. USA 99 2002 9697 9702
74. M. Pertea, and K. Ayanbule S.L. Salzberg OperonDB: a comprehensive database of predicted operons in microbial genomes Nucleic Acids Res. 37 Database issue 2009 D479 D482
75. P. Bogacki, and L.F. Shampine A 3(2) pair of Runge-Kutta formulas Appl. Math. Lett. 2 1989 321 325
76. J.A. Nelder, and R. Mead A simplex method for function minimization Comput. J. 7 1965 308 313
77. M.E. Marks, and C.M. Castro-Rojas S. Crosson The genetic basis of laboratory adaptation in Caulobacter crescentus J. Bacteriol. 192 2010 3678 3688