Single-molecule investigations of the stringent response machinery in living bacterial cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 31, 2011, Pages

  English, Brian P ^a   Hauryliuk, Vasili ^a,b   Sanamrad, Arash ^a   Tankov, Stoyan ^a,b   Dekker, Nynke H ^a,c   Elf, Johan ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF TARTU   (Estonia)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Cytosolic diffusion; Photoactivated localization microscopy; Single particle tracking; Stroboscopic illumination

Indexed keywords

GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; GUANOSINE 3' DIPHOSPHATE 5' TRIPHOSPHATE; TRANSCRIPTION FACTOR RELA;

ARTICLE; BACTERIAL CELL; CATALYST; CELL CYCLE; CELL TRACKING; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVE SITE; FLUORESCENCE IMAGING; HEAT STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SYNTHESIS; RIBOSOME; STRINGENT RESPONSE MACHINERY;

AMINO ACIDS; BIOCATALYSIS; BLOTTING, WESTERN; CELL DIVISION; COMPUTER SIMULATION; CYTOSOL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLOW CYTOMETRY; GUANOSINE TETRAPHOSPHATE; KINETICS; LIGASES; LUMINESCENT PROTEINS; METHIONINE; MICROSCOPY, CONFOCAL; RIBOSOMES; TIME FACTORS; TRYPTOPHAN;

BACTERIA (MICROORGANISMS);

EID: 79961224232     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1102255108     Document Type: Article

References (60)

1. Potrykus K, Cashel M (2008) (p)ppGpp: Still magical? Annu Rev Microbiol 62:35-51.
2. Haseltine WA, Block R (1973) Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci USA 70:1564-1568.
3. Vrentas CE, et al. (2008) Still looking for the magic spot: The crystallographically defined binding site for ppGpp on RNA polymerase is unlikely to be responsible for rRNA transcription regulation. J Mol Biol 377:551-564.
4. Wang JD, Sanders GM, Grossman AD (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128:865-875. (Pubitemid 46341409)
5. Milon P, et al. (2006) The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci U S A 103:13962-13967. (Pubitemid 44452965)
6. Mitkevich VA, et al. (2010) Thermodynamic characterization of ppGpp binding to EF-G or IF2 and of initiator tRNA binding to free IF2 in the presence of GDP, GTP, or ppGpp. J Mol Biol 402:838-846.
7. Jenvert RMK, Schiavone LH (2005) Characterization of the tRNA and ribosomedependent pppGpp-synthesis by recombinant stringent factor from Escherichia coli. FEBS J 272:685-695.
8. Jain V, Saleem-Batcha R, China A, Chatterji D (2006) Molecular dissection of the mycobacterial stringent response protein Rel. Protein Sci 15:1449-1464. (Pubitemid 43800016)
9. Avarbock D, Salem J, Li LS, Wang ZM, Rubin H (1999) Cloning and characterization of a bifunctional RelA SpoT homologue from Mycobacterium tuberculosis. Gene 233:261-269. (Pubitemid 29353246)
10. Wendrich TM, Blaha G, Wilson DN, Marahiel MA, Nierhaus KH (2002) Dissection of the mechanism for the stringent factor RelA. Mol Cell 10:779-788. (Pubitemid 35335633)
11. Hauryliuk VV (2006) GTPases of prokaryotic translational apparatus. Mol Biol (Mosk) 40:769-783.
12. Stirpe F, Battelli MG (2006) Ribosome-inactivating proteins: Progress and problems. Cell Mol Life Sci 63:1850-1866.
13. Ishitani R, Yokoyama S, Nureki O (2008) Structure, dynamics, and function of RNA modification enzymes. Curr Opin Struct Biol 18:330-339.
14. Bremer H, Dennis P, eds. (1996) Modulation of Chemical Composition and other Parameters of the Cell by Growth Rate (ASM, Washington, DC).
15. Betzig E, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-1645. (Pubitemid 44414039)
16. Hess ST, Girirajan TP, Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91:4258-4272. (Pubitemid 44887284)
17. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793-795. (Pubitemid 44445825)
18. Manley S, et al. (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5:155-157. (Pubitemid 351181741)
19. Gibbs KA, et al. (2004) Complex spatial distribution and dynamics of an abundant Escherichia coli outer membrane protein, LamB. Mol Microbiol 53:1771-1783. (Pubitemid 39265321)
20. Elf J, Li GW, Xie XS (2007) Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316:1191-1194. (Pubitemid 46877481)
21. Niu L, Yu J (2008) Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys J 95:2009-2016.
22. Sahl SJ, Leutenegger M, Hilbert M, Hell SW, Eggeling C (2010) Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids. Proc Natl Acad Sci USA 107:6829-6834.
23. Xie XS, Yu J, Yang WY (2006) Living cells as test tubes. Science 312:228-230.
24. McKinney SA, Murphy CS, Hazelwood KL, Davidson MW, Looger LL (2009) A bright and photostable photoconvertible fluorescent protein. Nat Methods 6:131-133.
25. Gurskaya NG, et al. (2006) Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat Biotechnol 24:461-465.
26. Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-1877. (Pubitemid 35024347)
27. Ando R, Mizuno H, Miyawaki A (2004) Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306:1370-1373. (Pubitemid 39532513)
28. Mascarenhas J, Weber MH, Graumann PL (2001) Specific polar localization of ribosomes in Bacillus subtilis depends on active transcription. EMBO Rep 2:685-689. (Pubitemid 32798710)
29. Lewis PJ, Thaker SD, Errington J (2000) Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19:710-718. (Pubitemid 30093744)
30. Montero Llopis P, et al. (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466:77-81.
31. Golding I, Cox EC (2004) RNA dynamics in live Escherichia coli cells. Proc Natl Acad Sci USA 101:11310-11315. (Pubitemid 39038343)
32. Golding I, Cox EC (2006) Physical nature of bacterial cytoplasm. Phys Rev Lett 96:098102.
33. Lindner AB, Madden R, Demarez A, Stewart EJ, Taddei F (2008) Asymmetric segregation of protein aggregates is associatedwith cellular aging and rejuvenation. Proc Natl Acad Sci USA 105:3076-3081. (Pubitemid 351723670)
34. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645. (Pubitemid 30412767)
35. Pedersen FS, Kjeldgaard NO (1977) Analysis of the relA gene product of Escherichia coli. Eur J Biochem 76:91-97. (Pubitemid 8117400)
36. Uzan M, Danchin A (1976) A rapid test for the rel A mutation in E. coli. Biochem Biophys Res Commun 69:751-758.
37. Vrljic M, Nishimura SY, Brasselet S, Moerner WE, McConnell HM (2002) Translational diffusion of individual class II MHC membrane proteins in cells. Biophys J 83:2681-2692. (Pubitemid 35265760)
38. Tosa T, Pizer LI (1971) Biochemical bases for the antimetabolite action of L-serine hydroxamate. J Bacteriol 106:972-982.
39. Riesenberg D, Bergter F, Kari C (1984) Effect of serine hydroxamate and methyl alpha-D-glucopyranoside treatment on nucleoside polyphosphate pools, RNA and protein accumulation in Streptomyces hygroscopicus. J Gen Microbiol 130:2549-2558. (Pubitemid 14016444)
40. Lemaux PG, Herendeen SL, Bloch PL, Neidhardt FC (1978) Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell 13:427-434.
41. Ryals J, Little R, Bremer H (1982) Control of RNA synthesis in Escherichia coli after a shift to higher temperature. J Bacteriol 151:1425-1432. (Pubitemid 13230847)
42. Gallant J, Palmer L, Pao CC (1977) Anomalous synthesis of ppGpp in growing cells. Cell 11:181-185. (Pubitemid 8126066)
43. Elowitz MB, Surette MG, Wolf PE, Stock JB, Leibler S (1999) Protein mobility in the cytoplasm of Escherichia coli. J Bacteriol 181:197-203. (Pubitemid 29013671)
44. Cluzel P, Surette M, Leibler S (2000) An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287:1652-1655. (Pubitemid 30127766)
45. Haustein E, Schwille P (2007) Fluorescence correlation spectroscopy: Novel variations of an established technique. Annu Rev Biophys Biomol Struct 36:151-169. (Pubitemid 46998114)
46. Elf J, Ehrenberg M (2005) Near-critical behavior of aminoacyl-tRNA pools in E. coli at rate-limiting supply of amino acids. Biophys J 88:132-146. (Pubitemid 40070664)
47. Lund E, Kjeldgaard NO (1972) Metabolism of guanosine tetraphosphate in Escherichia coli. Eur J Biochem 28:316-326.
48. Endo Y, Tsurugi K (1988) The RNA N-glycosidase activity of ricin A-chain. The characteristics of the enzymatic activity of ricin A-chain with ribosomes and with rRNA. J Biol Chem 263:8735-8739.
49. Fersht A (1998) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (W. H. Freeman, New York).
50. Buckstein MH, He J, Rubin H (2008) Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J Bacteriol 190:718-726. (Pubitemid 351360088)
51. Mechold U, Murphy H, Brown L, Cashel M (2002) Intramolecular regulation of the opposing (p)ppGpp catalytic activities of Rel(Seq), the Rel/Spo enzyme from Streptococcus equisimilis. J Bacteriol 184:2878-2888. (Pubitemid 34517809)
52. Kao HP, Verkman AS (1994) Tracking of single fluorescent particles in three dimensions: Use of cylindrical optics to encode particle position. Biophys J 67:1291-1300. (Pubitemid 24272983)
53. Connolly K, Culver G (2009) Deconstructing ribosome construction. Trends Biochem Sci 34:256-263.
54. Pulk A, et al. (2010) Ribosome reactivation by replacement of damaged proteins. Mol Microbiol 75:801-814.
55. Sojka L, Fucik V, Krasny L, Barvik I, Jonak J (2007) YbxF, a protein associated with exponential-phase ribosomes in Bacillus subtilis. J Bacteriol 189:4809-4814. (Pubitemid 47025593)
56. Izutsu K, et al. (2001) Escherichia coli ribosome-associated protein SRA, whose copy number increases during stationary phase. J Bacteriol 183:2765-2773. (Pubitemid 32319278)
57. Wada A, Yamazaki Y, Fujita N, Ishihama A (1990) Structure and probable genetic location of a "ribosome modulation factor" associated with 100S ribosomes in stationaryphase Escherichia coli cells. Proc Natl Acad Sci USA 87:2657-2661.
58. Ortiz JO, et al. (2010) Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J Cell Biol 190:613-621.
59. Agafonov DE, Kolb VA, Spirin AS (2001) Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep 2:399-402. (Pubitemid 32509955)
60. Mortensen KI, Churchman LS, Spudich JA, Flyvbjerg H (2010) Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat Methods 7:377-381.