The alarmones (p)ppGpp are part of the heat shock response of Bacillus subtilis


Autoři: Heinrich Schäfer aff001;  Bertrand Beckert aff003;  Christian K. Frese aff002;  Wieland Steinchen aff004;  Aaron M. Nuss aff005;  Michael Beckstette aff005;  Ingo Hantke aff001;  Kristina Driller aff002;  Petra Sudzinová aff006;  Libor Krásný aff006;  Volkhard Kaever aff007;  Petra Dersch aff005;  Gert Bange aff004;  Daniel N. Wilson aff003;  Kürşad Turgay aff001
Působiště autorů: Institute of Microbiology, Leibniz Universität Hannover, Hannover, Germany aff001;  Max Planck Unit for the Science of Pathogens, Berlin, Germany aff002;  Institute for Biochemistry and Molecular Biology, University of Hamburg, Hamburg, Germany aff003;  Philipps-University Marburg, Center for Synthetic Microbiology (SYNMIKRO) and Department of Chemistry, Marburg, Germany aff004;  Department of Molecular Infection Biology, Helmholtz Centre for Infection Research, Braunschweig, Germany aff005;  Institute of Microbiology, Czech Academy of Sciences, Prague, Czech Republic aff006;  Hannover Medical School, Research Core Unit Metabolomics, Hannover, Germany aff007;  Institute of Infectiology, University of Münster, Münster, Germany aff008
Vyšlo v časopise: The alarmones (p)ppGpp are part of the heat shock response of Bacillus subtilis. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008275
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008275

Souhrn

Bacillus subtilis cells are well suited to study how bacteria sense and adapt to proteotoxic stress such as heat, since temperature fluctuations are a major challenge to soil-dwelling bacteria. Here, we show that the alarmones (p)ppGpp, well known second messengers of nutrient starvation, are also involved in the heat stress response as well as the development of thermo-resistance. Upon heat-shock, intracellular levels of (p)ppGpp rise in a rapid but transient manner. The heat-induced (p)ppGpp is primarily produced by the ribosome-associated alarmone synthetase Rel, while the small alarmone synthetases RelP and RelQ seem not to be involved. Furthermore, our study shows that the generated (p)ppGpp pulse primarily acts at the level of translation, and only specific genes are regulated at the transcriptional level. These include the down-regulation of some translation-related genes and the up-regulation of hpf, encoding the ribosome-protecting hibernation-promoting factor. In addition, the alarmones appear to interact with the activity of the stress transcription factor Spx during heat stress. Taken together, our study suggests that (p)ppGpp modulates the translational capacity at elevated temperatures and thereby allows B. subtilis cells to respond to proteotoxic stress, not only by raising the cellular repair capacity, but also by decreasing translation to concurrently reduce the protein load on the cellular protein quality control system.

Klíčová slova:

Bacillus subtilis – Cellular stress responses – DNA transcription – Heat shock response – Protein translation – Ribosomal RNA – Ribosomes – Thermal stresses


Zdroje

1. Storz G, Hengge R, American Society for Microbiology, editors. Bacterial stress responses. 2nd ed. Washington, DC: ASM Press; 2011.

2. Mogk A, Huber D, Bukau B. Integrating protein homeostasis strategies in prokaryotes. Cold Spring Harb Perspect Biol. 2011;3. doi: 10.1101/cshperspect.a004366 21441580

3. Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature. 2011;475: 324–332. doi: 10.1038/nature10317 21776078

4. Lindquist S. The Heat-Shock Response. Annual Review of Biochemistry. 1986;55: 1151–1191. doi: 10.1146/annurev.bi.55.070186.005443 2427013

5. Lim B, Gross CA. Cellular Response to Heat Shock and Cold Shock. In: Storz G, Hengge R, editors. Bacterial stress responses 2nd edition. Washington, DC: ASM press, American Society for Microbiology; 2010. pp. 93–114.

6. Helmann JD, Wu MF, Kobel PA, Gamo FJ, Wilson M, Morshedi MM, et al. Global transcriptional response of Bacillus subtilis to heat shock. J Bacteriol. 2001;183: 7318–7328. doi: 10.1128/JB.183.24.7318-7328.2001 11717291

7. Winkler J, Seybert A, Konig L, Pruggnaller S, Haselmann U, Sourjik V, et al. Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J. 2010;29: 910–23. doi: 10.1038/emboj.2009.412 20094032

8. Völker U, Mach H, Schmid R, Hecker M. Stress proteins and cross-protection by heat shock and salt stress in Bacillus subtilis. J Gen Microbiol. 1992;138: 2125–2135. doi: 10.1099/00221287-138-10-2125 1362210

9. Runde S, Molière N, Heinz A, Maisonneuve E, Janczikowski A, Elsholz AKW, et al. The role of thiol oxidative stress response in heat-induced protein aggregate formation during thermotolerance in B acillus subtilis: Thiol oxidation in protein aggregate formation. Molecular Microbiology. 2014;91: 1036–1052.

10. Hecker M, Schumann W, Völker U. Heat-shock and general stress response in Bacillus subtilis. Molecular microbiology. 1996;19: 417–428. doi: 10.1046/j.1365-2958.1996.396932.x 8830234

11. Mogk A, Homuth G, Scholz C, Kim L, Schmid FX, Schumann W. The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J. 1997;16: 4579–4590. doi: 10.1093/emboj/16.15.4579 9303302

12. Krüger E, Hecker M. The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J Bacteriol. 1998;180: 6681–6688. 9852015

13. Elsholz AKW, Michalik S, Zühlke D, Hecker M, Gerth U. CtsR, the Gram-positive master regulator of protein quality control, feels the heat. The EMBO Journal. 2010;29: 3621–3629. doi: 10.1038/emboj.2010.228 20852588

14. Hecker M, Pané-Farré J, Völker U. SigB-Dependent General Stress Response in Bacillus subtilis and Related Gram-Positive Bacteria. Annual Review of Microbiology. 2007;61: 215–236. doi: 10.1146/annurev.micro.61.080706.093445 18035607

15. Nakano S, Küster-Schöck E, Grossman AD, Zuber P. Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc Natl Acad Sci USA. 2003;100: 13603–13608. doi: 10.1073/pnas.2235180100 14597697

16. Rochat T, Nicolas P, Delumeau O, Rabatinová A, Korelusová J, Leduc A, et al. Genome-wide identification of genes directly regulated by the pleiotropic transcription factor Spx in Bacillus subtilis. Nucleic Acids Res. 2012;40: 9571–9583. doi: 10.1093/nar/gks755 22904090

17. Schäfer H, Heinz A, Sudzinová P, Voß M, Hantke I, Krásný L, et al. Spx, the central regulator of the heat and oxidative stress response in B. subtilis, can repress transcription of translation-related genes. Mol Microbiol. 2019;111: 514–533. doi: 10.1111/mmi.14171 30480837

18. Leichert LIO, Scharf C, Hecker M. Global characterization of disulfide stress in Bacillus subtilis. J Bacteriol. 2003;185: 1967–1975. doi: 10.1128/JB.185.6.1967-1975.2003 12618461

19. Potrykus K, Cashel M. (p)ppGpp: still magical? Annu Rev Microbiol. 2008;62: 35–51. doi: 10.1146/annurev.micro.62.081307.162903 18454629

20. Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol. 2015;13: 298–309. doi: 10.1038/nrmicro3448 25853779

21. Haseltine WA, Block R. 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. 1973;70: 1564–1568. doi: 10.1073/pnas.70.5.1564 4576025

22. Wendrich TM, Blaha G, Wilson DN, Marahiel MA, Nierhaus KH. Dissection of the Mechanism for the Stringent Factor RelA. Molecular Cell. 2002;10: 779–788. doi: 10.1016/s1097-2765(02)00656-1 12419222

23. Arenz S, Abdelshahid M, Sohmen D, Payoe R, Starosta AL, Berninghausen O, et al. The stringent factor RelA adopts an open conformation on the ribosome to stimulate ppGpp synthesis. Nucleic Acids Res. 2016;44: 6471–6481. doi: 10.1093/nar/gkw470 27226493

24. Brown A, Fernández IS, Gordiyenko Y, Ramakrishnan V. Ribosome-dependent activation of stringent control. Nature. 2016;534: 277–280. doi: 10.1038/nature17675 27279228

25. Loveland AB, Bah E, Madireddy R, Zhang Y, Brilot AF, Grigorieff N, et al. Ribosome•RelA structures reveal the mechanism of stringent response activation. Elife. 2016;5. doi: 10.7554/eLife.17029 27434674

26. Atkinson GC, Tenson T, Hauryliuk V. The RelA/SpoT Homolog (RSH) Superfamily: Distribution and Functional Evolution of ppGpp Synthetases and Hydrolases across the Tree of Life. Stiller JW, editor. PLoS ONE. 2011;6: e23479. doi: 10.1371/journal.pone.0023479 21858139

27. Wendrich TM, Marahiel MA. Cloning and characterization of a relA/spoT homologue from Bacillus subtilis. Mol Microbiol. 1997;26: 65–79. doi: 10.1046/j.1365-2958.1997.5511919.x 9383190

28. Nanamiya H, Kasai K, Nozawa A, Yun C-S, Narisawa T, Murakami K, et al. Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol. 2008;67: 291–304. doi: 10.1111/j.1365-2958.2007.06018.x 18067544

29. Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, et al. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet. 2008;4: e1000139. doi: 10.1371/journal.pgen.1000139 18670626

30. Boutte CC, Crosson S. Bacterial lifestyle shapes stringent response activation. Trends Microbiol. 2013;21: 174–180. doi: 10.1016/j.tim.2013.01.002 23419217

31. Irving SE, Corrigan RM. Triggering the stringent response: signals responsible for activating (p)ppGpp synthesis in bacteria. Microbiology. 2018;164: 268–276. doi: 10.1099/mic.0.000621 29493495

32. Lopez JM, Dromerick A, Freese E. Response of guanosine 5’-triphosphate concentration to nutritional changes and its significance for Bacillus subtilis sporulation. J Bacteriol. 1981;146: 605–613. 6111556

33. Kriel A, Bittner AN, Kim SH, Liu K, Tehranchi AK, Zou WY, et al. Direct regulation of GTP homeostasis by (p)ppGpp: a critical component of viability and stress resistance. Mol Cell. 2012;48: 231–241. doi: 10.1016/j.molcel.2012.08.009 22981860

34. Krásný L, Gourse RL. An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J. 2004;23: 4473–4483. doi: 10.1038/sj.emboj.7600423 15496987

35. Krásný L, Tišerová H, Jonák J, Rejman D, Šanderová H. The identity of the transcription +1 position is crucial for changes in gene expression in response to amino acid starvation in Bacillus subtilis. Molecular Microbiology. 2008;69: 42–54. doi: 10.1111/j.1365-2958.2008.06256.x 18433449

36. Geiger T, Wolz C. Intersection of the stringent response and the CodY regulon in low GC Gram-positive bacteria. Int J Med Microbiol. 2014;304: 150–155. doi: 10.1016/j.ijmm.2013.11.013 24462007

37. Ratnayake-Lecamwasam M, Serror P, Wong KW, Sonenshein AL. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 2001;15: 1093–1103. doi: 10.1101/gad.874201 11331605

38. Milon P, Tischenko E, Tomsic J, Caserta E, Folkers G, La Teana A, et al. The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci USA. 2006;103: 13962–13967. doi: 10.1073/pnas.0606384103 16968770

39. Corrigan RM, Bellows LE, Wood A, Gründling A. ppGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Gram-positive bacteria. Proc Natl Acad Sci USA. 2016;113: E1710–1719. doi: 10.1073/pnas.1522179113 26951678

40. Steinchen W, Bange G. The magic dance of the alarmones (p)ppGpp: The structural biology of the alarmones (p)ppGpp. Molecular Microbiology. 2016;101: 531–544.

41. Vinogradova DS, Zegarra V, Maksimova E, Nakamoto JA, Kasatsky P, Paleskava A, et al. How the initiating ribosome copes with ppGpp to translate mRNAs. PLoS Biol. 2020;18: e3000593. doi: 10.1371/journal.pbio.3000593 31995552

42. Kanjee U, Ogata K, Houry WA. Direct binding targets of the stringent response alarmone (p)ppGpp: Protein targets of ppGpp. Molecular Microbiology. 2012;85: 1029–1043. doi: 10.1111/j.1365-2958.2012.08177.x 22812515

43. Zhang Y, Zborníková E, Rejman D, Gerdes K. Novel (p)ppGpp Binding and Metabolizing Proteins of Escherichia coli. MBio. 2018;9. doi: 10.1128/mBio.02188-17 29511080

44. Wang B, Dai P, Ding D, Del Rosario A, Grant RA, Pentelute BL, et al. Affinity-based capture and identification of protein effectors of the growth regulator ppGpp. Nat Chem Biol. 2019;15: 141–150. doi: 10.1038/s41589-018-0183-4 30559427

45. Bokinsky G, Baidoo EEK, Akella S, Burd H, Weaver D, Alonso-Gutierrez J, et al. HipA-triggered growth arrest and β-lactam tolerance in Escherichia coli are mediated by RelA-dependent ppGpp synthesis. J Bacteriol. 2013;195: 3173–3182. doi: 10.1128/JB.02210-12 23667235

46. Dalebroux ZD, Swanson MS. ppGpp: magic beyond RNA polymerase. Nat Rev Microbiol. 2012;10: 203–212. doi: 10.1038/nrmicro2720 22337166

47. Mostertz J, Scharf C, Hecker M, Homuth G. Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology (Reading, Engl). 2004;150: 497–512.

48. Hantke I, Schäfer H, Janczikowski A, Turgay K. YocM a small heat shock protein can protect Bacillus subtilis cells during salt stress. Mol Microbiol. 2019;111: 423–440. doi: 10.1111/mmi.14164 30431188

49. Gaca AO, Kudrin P, Colomer-Winter C, Beljantseva J, Liu K, Anderson B, et al. From (p)ppGpp to (pp)pGpp: Characterization of Regulatory Effects of pGpp Synthesized by the Small Alarmone Synthetase of Enterococcus faecalis. J Bacteriol. 2015;197: 2908–2919. doi: 10.1128/JB.00324-15 26124242

50. Hecker M, Völker U, Heim C. RelA-independent (p)ppGpp accumulation and heat shock protein induction after salt stress in Bacillus subtilis. FEMS Microbiology Letters. 1989;58: 125–128. doi: 10.1111/j.1574-6968.1989.tb03031.x

51. Pöther D-C, Liebeke M, Hochgräfe F, Antelmann H, Becher D, Lalk M, et al. Diamide triggers mainly S Thiolations in the cytoplasmic proteomes of Bacillus subtilis and Staphylococcus aureus. J Bacteriol. 2009;191: 7520–7530. doi: 10.1128/JB.00937-09 19837798

52. Drzewiecki K, Eymann C, Mittenhuber G, Hecker M. The yvyD gene of Bacillus subtilis is under dual control of sigmaB and sigmaH. J Bacteriol. 1998;180: 6674–6680. 9852014

53. Tagami K, Nanamiya H, Kazo Y, Maehashi M, Suzuki S, Namba E, et al. Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. Microbiologyopen. 2012;1: 115–134. doi: 10.1002/mbo3.16 22950019

54. Cashel M. The Control of Ribonucleic Acid Synthesis in Escherichia coli : IV. RELEVANCE OF UNUSUAL PHOSPHORYLATED COMPOUNDS FROM AMINO ACID-STARVED STRINGENT STRAINS. Journal of Biological Chemistry. 1969;244: 3133–3141. 4893338

55. Schreiber G, Metzger S, Aizenman E, Roza S, Cashel M, Glaser G. Overexpression of the relA gene in Escherichia coli. J Biol Chem. 1991;266: 3760–3767. 1899866

56. Nouri H, Monnier A-F, Fossum-Raunehaug S, Maciag-Dorszynska M, Cabin-Flaman A, Képès F, et al. Multiple links connect central carbon metabolism to DNA replication initiation and elongation in Bacillus subtilis. DNA Res. 2018. doi: 10.1093/dnares/dsy031 30256918

57. Lopez JM, Marks CL, Freese E. The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. Biochim Biophys Acta. 1979;587: 238–252. doi: 10.1016/0304-4165(79)90357-x 114234

58. Tojo S, Satomura T, Kumamoto K, Hirooka K, Fujita Y. Molecular Mechanisms Underlying the Positive Stringent Response of the Bacillus subtilis ilv-leu Operon, Involved in the Biosynthesis of Branched-Chain Amino Acids. J Bacteriol. 2008;190: 6134–6147. doi: 10.1128/JB.00606-08 18641142

59. Tojo S, Kumamoto K, Hirooka K, Fujita Y. Heavy involvement of stringent transcription control depending on the adenine or guanine species of the transcription initiation site in glucose and pyruvate metabolism in Bacillus subtilis. J Bacteriol. 2010;192: 1573–1585. doi: 10.1128/JB.01394-09 20081037

60. Kriel A, Brinsmade SR, Tse JL, Tehranchi AK, Bittner AN, Sonenshein AL, et al. GTP Dysregulation in Bacillus subtilis Cells Lacking (p)ppGpp Results in Phenotypic Amino Acid Auxotrophy and Failure To Adapt to Nutrient Downshift and Regulate Biosynthesis Genes. Journal of Bacteriology. 2014;196: 189–201. doi: 10.1128/JB.00918-13 24163341

61. Eymann C, Homuth G, Scharf C, Hecker M. Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol. 2002;184: 2500–2520. doi: 10.1128/JB.184.9.2500-2520.2002 11948165

62. Zhang S, Haldenwang WG. RelA is a component of the nutritional stress activation pathway of the Bacillus subtilis transcription factor sigma B. J Bacteriol. 2003;185: 5714–5721. doi: 10.1128/JB.185.19.5714-5721.2003 13129942

63. Zhang S, Haldenwang WG. Contributions of ATP, GTP, and redox state to nutritional stress activation of the Bacillus subtilis sigmaB transcription factor. J Bacteriol. 2005;187: 7554–7560. doi: 10.1128/JB.187.22.7554-7560.2005 16267279

64. Molière N, Hoßmann J, Schäfer H, Turgay K. Role of Hsp100/Clp Protease Complexes in Controlling the Regulation of Motility in Bacillus subtilis. Front Microbiol. 2016;7: 315. doi: 10.3389/fmicb.2016.00315 27014237

65. Paget MSB, Molle V, Cohen G, Aharonowitz Y, Buttner MJ. Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon. Molecular Microbiology. 2001;42: 1007–1020. doi: 10.1046/j.1365-2958.2001.02675.x 11737643

66. Gaca AO, Abranches J, Kajfasz JK, Lemos JA. Global transcriptional analysis of the stringent response in Enterococcus faecalis. Microbiology (Reading, Engl). 2012;158: 1994–2004.

67. Schmidt EK, Clavarino G, Ceppi M, Pierre P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods. 2009;6: 275–277. doi: 10.1038/nmeth.1314 19305406

68. Svitil AL, Cashel M, Zyskind JW. Guanosine tetraphosphate inhibits protein synthesis in vivo. A possible protective mechanism for starvation stress in Escherichia coli. J Biol Chem. 1993;268: 2307–2311. 8428905

69. Diez S, Ryu J, Caban K, Gonzalez RL, Dworkin J. (p)ppGpp directly regulates translation initiation during entry into quiescence. bioRxiv. 2019; 807917. doi: 10.1101/807917

70. Zhang S, Scott JM, Haldenwang WG. Loss of ribosomal protein L11 blocks stress activation of the Bacillus subtilis transcription factor sigma(B). J Bacteriol. 2001;183: 2316–2321. doi: 10.1128/JB.183.7.2316-2321.2001 11244072

71. Beckert B, Abdelshahid M, Schäfer H, Steinchen W, Arenz S, Berninghausen O, et al. Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. EMBO J. 2017;36: 2061–2072. doi: 10.15252/embj.201696189 28468753

72. Trinquier A, Ulmer JE, Gilet L, Figaro S, Hammann P, Kuhn L, et al. tRNA Maturation Defects Lead to Inhibition of rRNA Processing via Synthesis of pppGpp. Molecular Cell. 2019;0. doi: 10.1016/j.molcel.2019.03.030 31003868

73. Engman J, von Wachenfeldt C. Regulated protein aggregation: a mechanism to control the activity of the ClpXP adaptor protein YjbH. Mol Microbiol. 2015;95: 51–63. doi: 10.1111/mmi.12842 25353645

74. Fitzsimmons LF, Liu L, Kim J-S, Jones-Carson J, Vázquez-Torres A. Salmonella Reprograms Nucleotide Metabolism in Its Adaptation to Nitrosative Stress. Aballay A, editor. mBio. 2018;9: e00211–18. doi: 10.1128/mBio.00211-18 29487237

75. Hyduke DR, Jarboe LR, Tran LM, Chou KJY, Liao JC. Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli. Proceedings of the National Academy of Sciences. 2007;104: 8484–8489. doi: 10.1073/pnas.0610888104 17494765

76. Richardson AR, Payne EC, Younger N, Karlinsey JE, Thomas VC, Becker LA, et al. Multiple Targets of Nitric Oxide in the Tricarboxylic Acid Cycle of Salmonella enterica Serovar Typhimurium. Cell Host & Microbe. 2011;10: 33–43. doi: 10.1016/j.chom.2011.06.004 21767810

77. Gallant J, Palmer L, Pao CC. Anomalous synthesis of ppGpp in growing cells. Cell. 1977;11: 181–185. doi: 10.1016/0092-8674(77)90329-4 326415

78. Katz A, Orellana O. Protein Synthesis and the Stress Response. In: Biyani M, editor. Cell-Free Protein Synthesis. InTech; 2012.

79. Kramer GF, Baker JC, Ames BN. Near-UV stress in Salmonella typhimurium: 4-thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response. J Bacteriol. 1988;170: 2344–2351. doi: 10.1128/jb.170.5.2344-2351.1988 3283108

80. Hahn J, Tanner AW, Carabetta VJ, Cristea IM, Dubnau D. ComGA-RelA interaction and persistence in the Bacillus subtilis K-state. Mol Microbiol. 2015;97: 454–471. doi: 10.1111/mmi.13040 25899641

81. Scott JM, Haldenwang WG. Obg, an essential GTP binding protein of Bacillus subtilis, is necessary for stress activation of transcription factor sigma(B). J Bacteriol. 1999;181: 4653–4660. 10419966

82. Bruel N, Castanié-Cornet M-P, Cirinesi A-M, Koningstein G, Georgopoulos C, Luirink J, et al. Hsp33 controls elongation factor-Tu stability and allows Escherichia coli growth in the absence of the major DnaK and trigger factor chaperones. J Biol Chem. 2012;287: 44435–44446. doi: 10.1074/jbc.M112.418525 23148222

83. Maaβ S, Wachlin G, Bernhardt J, Eymann C, Fromion V, Riedel K, et al. Highly precise quantification of protein molecules per cell during stress and starvation responses in Bacillus subtilis. Mol Cell Proteomics. 2014;13: 2260–2276. doi: 10.1074/mcp.M113.035741 24878497

84. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334: 1081–1086. doi: 10.1126/science.1209038 22116877

85. Rallu F, Gruss A, Ehrlich SD, Maguin E. Acid- and multistress-resistant mutants of Lactococcus lactis: identification of intracellular stress signals. Molecular Microbiology. 2000;35: 517–528. doi: 10.1046/j.1365-2958.2000.01711.x 10672175

86. VanBogelen RA, Kelley PM, Neidhardt FC. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol. 1987;169: 26–32. doi: 10.1128/jb.169.1.26-32.1987 3539918

87. Abranches J, Martinez AR, Kajfasz JK, Chávez V, Garsin DA, Lemos JA. The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J Bacteriol. 2009;191: 2248–2256. doi: 10.1128/JB.01726-08 19168608

88. Okada Y, Makino S, Tobe T, Okada N, Yamazaki S. Cloning of rel from Listeria monocytogenes as an osmotolerance involvement gene. Appl Environ Microbiol. 2002;68: 1541–1547. doi: 10.1128/AEM.68.4.1541-1547.2002 11916666

89. Yang X, Ishiguro EE. Temperature-Sensitive Growth and Decreased Thermotolerance Associated with relA Mutations in Escherichia coli. J Bacteriol. 2003;185: 5765–5771. doi: 10.1128/JB.185.19.5765-5771.2003 13129947

90. Khakimova M, Ahlgren HG, Harrison JJ, English AM, Nguyen D. The stringent response controls catalases in Pseudomonas aeruginosa and is required for hydrogen peroxide and antibiotic tolerance. J Bacteriol. 2013;195: 2011–2020. doi: 10.1128/JB.02061-12 23457248

91. Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Press; 2001.

92. Spizizen J. TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. Proc Natl Acad Sci USA. 1958;44: 1072–1078. doi: 10.1073/pnas.44.10.1072 16590310

93. Nakano MM, Zhu Y, Liu J, Reyes DY, Yoshikawa H, Zuber P. Mutations conferring amino acid residue substitutions in the carboxy-terminal domain of RNA polymerase alpha can suppress clpX and clpP with respect to developmentally regulated transcription in Bacillus subtilis. Mol Microbiol. 2000;37: 869–884. doi: 10.1046/j.1365-2958.2000.02052.x 10972808

94. Arnaud M, Chastanet A, Débarbouillé M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol. 2004;70: 6887–6891. doi: 10.1128/AEM.70.11.6887-6891.2004 15528558

95. Stülke J, Hanschke R, Hecker M. Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J Gen Microbiol. 1993;139: 2041–2045. doi: 10.1099/00221287-139-9-2041 8245830

96. Lamy M-C, Zouine M, Fert J, Vergassola M, Couve E, Pellegrini E, et al. CovS/CovR of group B streptococcus: a two-component global regulatory system involved in virulence: The CovS/CovR regulatory system of Streptococcus agalactiae. Molecular Microbiology. 2004;54: 1250–1268. doi: 10.1111/j.1365-2958.2004.04365.x 15554966

97. Nuss AM, Heroven AK, Waldmann B, Reinkensmeier J, Jarek M, Beckstette M, et al. Transcriptomic Profiling of Yersinia pseudotuberculosis Reveals Reprogramming of the Crp Regulon by Temperature and Uncovers Crp as a Master Regulator of Small RNAs. Sharma CM, editor. Genet PLoS. 2015;11: e1005087. doi: 10.1371/journal.pgen.1005087 25816203

98. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 22388286

99. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

100. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11: R106. doi: 10.1186/gb-2010-11-10-r106 20979621

101. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30: 207–210. doi: 10.1093/nar/30.1.207 11752295

102. Dugar G, Herbig A, Förstner KU, Heidrich N, Reinhardt R, Nieselt K, et al. High-Resolution Transcriptome Maps Reveal Strain-Specific Regulatory Features of Multiple Campylobacter jejuni Isolates. Hughes D, editor. PLoS Genetics. 2013;9: e1003495. doi: 10.1371/journal.pgen.1003495 23696746

103. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA. 1979;76: 4350–4354. doi: 10.1073/pnas.76.9.4350 388439

104. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227: 680–685. doi: 10.1038/227680a0 5432063

105. Neuhoff V, Arold N, Taube D, Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis. 1988;9: 255–262. doi: 10.1002/elps.1150090603 2466658

106. Yarmolinsky MB, Haba GL. INHIBITION BY PUROMYCIN OF AMINO ACID INCORPORATION INTO PROTEIN. Proc Natl Acad Sci USA. 1959;45: 1721–1729. doi: 10.1073/pnas.45.12.1721 16590564

107. Nathans D. PUROMYCIN INHIBITION OF PROTEIN SYNTHESIS: INCORPORATION OF PUROMYCIN INTO PEPTIDE CHAINS. Proc Natl Acad Sci USA. 1964;51: 585–592. doi: 10.1073/pnas.51.4.585 14166766

108. Krüger E, Witt E, Ohlmeier S, Hanschke R, Hecker M. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J Bacteriol. 2000;182: 3259–3265. doi: 10.1128/jb.182.11.3259-3265.2000 10809708

109. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9: 676–682. doi: 10.1038/nmeth.2019 22743772

110. Ihara Y, Ohta H, Masuda S. A highly sensitive quantification method for the accumulation of alarmone ppGpp in Arabidopsis thaliana using UPLC-ESI-qMS/MS. J Plant Res. 2015;128: 511–518. doi: 10.1007/s10265-015-0711-1 25752614

111. Steinchen W, Schuhmacher JS, Altegoer F, Fage CD, Srinivasan V, Linne U, et al. Catalytic mechanism and allosteric regulation of an oligomeric (p)ppGpp synthetase by an alarmone. Proc Natl Acad Sci USA. 2015;112: 13348–13353. doi: 10.1073/pnas.1505271112 26460002

112. Hughes CS, Moggridge S, Müller T, Sorensen PH, Morin GB, Krijgsveld J. Single-pot, solid-phase-enhanced sample preparation for proteomics experiments. Nat Protoc. 2019;14: 68–85. doi: 10.1038/s41596-018-0082-x 30464214

113. Plubell DL, Wilmarth PA, Zhao Y, Fenton AM, Minnier J, Reddy AP, et al. Extended Multiplexing of Tandem Mass Tags (TMT) Labeling Reveals Age and High Fat Diet Specific Proteome Changes in Mouse Epididymal Adipose Tissue. Mol Cell Proteomics. 2017;16: 873–890. doi: 10.1074/mcp.M116.065524 28325852

114. Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47: D442–D450. doi: 10.1093/nar/gky1106 30395289

115. Zhu B, Stülke J. SubtiWiki in 2018: from genes and proteins to functional network annotation of the model organism Bacillus subtilis. Nucleic Acids Research. 2018;46: D743–D748. doi: 10.1093/nar/gkx908 29788229

116. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2018. https://www.R-project.org/

117. Yu G, Wang L-G, Han Y, He Q-Y. clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters. OMICS: A Journal of Integrative Biology. 2012;16: 284–287. doi: 10.1089/omi.2011.0118 22455463

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 3

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Kurz originály vs. generika
nový kurz
Autoři:

Klinická farmakokinetika betablokátorů
Autoři:

Současné možnosti terapie osteoartrózy
Autoři: MUDr. Jakub Holešovský

Preferovaná úlevová léčba Asthma Bronchiale
Autoři: PharmDr. Petr Sedlák

Inhibitory karboanhydrázy v léčbě glaukomu
Autoři: MUDr. Petr Výborný, CSc., FEBO

Všechny kurzy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se