XProteotoxic stress induces a cell-cycle arrest by stimulating lon to degrade the replication initiator DnaA

Cell

Volumn 154, Issue 3, 2013, Pages

  Jonas, Kristina ^a,c   Liu, Jing ^b   Chien, Peter ^b   Laub, Michael T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPEPTIDASE LA; PROTEIN; PROTEIN DNAJ; PROTEIN DNAK; PROTEIN GRPE; REPLICATION INITIATOR PROTEIN DNAA; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CAULOBACTER CRESCENTUS; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL DAMAGE; CONTROLLED STUDY; DNA DEGRADATION; DNA REPLICATION; ENZYME ACTIVATION; ENZYME STABILITY; GENE OVEREXPRESSION; GENETIC MANIPULATION; HEAT; HEAT SHOCK RESPONSE; LETHALITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN SYNTHESIS; PROTEOTOXIC STRESS; UNFOLDED PROTEIN RESPONSE;

CAULOBACTER VIBRIOIDES;

EID: 84881152360     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.06.034     Document Type: Article

References (52)

1. F. Arsène, T. Tomoyasu, and B. Bukau The heat shock response of Escherichia coli Int. J. Food Microbiol. 55 2000 3 9
2. M. Avedissian, D. Lessing, J.W. Gober, L. Shapiro, and S.L. Gomes Regulation of the Caulobacter crescentus dnaKJ operon J. Bacteriol. 177 1995 3479 3484
3. S.P. Bell The origin recognition complex: from simple origins to complex functions Genes Dev. 16 2002 659 672
4. N. Bruel, M.P. Castanié-Cornet, A.M. Cirinesi, G. Koningstein, C. Georgopoulos, J. Luirink, and P. Genevaux 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. 287 2012 44435 44446
5. M.F. Charette, G.W. Henderson, and A. Markovitz ATP hydrolysis-dependent protease activity of the lon (capR) protein of Escherichia coli K-12 Proc. Natl. Acad. Sci. USA 78 1981 4728 4732
6. J. Collier, and L. Shapiro Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter J. Bacteriol. 191 2009 5706 5716
7. E.A. Craig, and C.A. Gross Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16 1991 135 140
8. A.C. da Silva, R.C. Simão, M.F. Susin, R.L. Baldini, M. Avedissian, and S.L. Gomes Downregulation of the heat shock response is independent of DnaK and sigma32 levels in Caulobacter crescentus Mol. Microbiol. 49 2003 541 553
9. C. Fernandez-Fernandez, D. Gonzalez, and J. Collier Regulation of the activity of the dual-function DnaA protein in Caulobacter crescentus PLoS ONE 6 2011 e26028
10. P. Genevaux, C. Georgopoulos, and W.L. Kelley The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions Mol. Microbiol. 66 2007 840 857
11. S.A. Goff, and A.L. Goldberg Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes Cell 41 1985 587 595
12. K.G. Gora, A. Cantin, M. Wohlever, K.K. Joshi, B.S. Perchuk, P. Chien, and M.T. Laub Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus Mol. Microbiol. 87 2013 1277 1289
13. B. Gorbatyuk, and G.T. Marczynski Physiological consequences of blocked Caulobacter crescentus dnaA expression, an essential DNA replication gene Mol. Microbiol. 40 2001 485 497
14. B. Gorbatyuk, and G.T. Marczynski Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus Mol. Microbiol. 55 2005 1233 1245
15. E. Gur, and R.T. Sauer Recognition of misfolded proteins by Lon, a AAA(+) protease Genes Dev. 22 2008 2267 2277
16. E. Gur, and R.T. Sauer Degrons in protein substrates program the speed and operating efficiency of the AAA+ Lon proteolytic machine Proc. Natl. Acad. Sci. USA 106 2009 18503 18508
17. F.U. Hartl, and M. Hayer-Hartl Converging concepts of protein folding in vitro and in vivo Nat. Struct. Mol. Biol. 16 2009 574 581
18. T. Ishida, N. Akimitsu, T. Kashioka, M. Hatano, T. Kubota, Y. Ogata, K. Sekimizu, and T. Katayama DiaA, a novel DnaA-binding protein, ensures the timely initiation of Escherichia coli chromosome replication J. Biol. Chem. 279 2004 45546 45555
19. U. Jenal, and T. Fuchs An essential protease involved in bacterial cell-cycle control EMBO J. 17 1998 5658 5669
20. K. Jonas, Y.E. Chen, and M.T. Laub Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication Curr. Biol. 21 2011 1092 1101
21. Y. Jubete, M.R. Maurizi, and S. Gottesman Role of the heat shock protein DnaJ in the lon-dependent degradation of naturally unstable proteins J. Biol. Chem. 271 1996 30798 30803
22. J. Kato, and T. Katayama Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli EMBO J. 20 2001 4253 4262
23. H. Kawakami, and T. Katayama DnaA, ORC, and Cdc6: similarity beyond the domains of life and diversity Biochem. Cell Biol. 88 2010 49 62
24. Y. Kawasaki, C. Wada, and T. Yura Roles of Escherichia coli heat shock proteins DnaK, DnaJ and GrpE in mini-F plasmid replication Mol. Gen. Genet. 220 1990 277 282
25. A.C. Leonard, and J.E. Grimwade Regulation of DnaA assembly and activity: taking directions from the genome Annu. Rev. Microbiol. 65 2011 19 35
26. J.A. Lesley, and L. Shapiro SpoT regulates DnaA stability and initiation of DNA replication in carbon-starved Caulobacter crescentus J. Bacteriol. 190 2008 6867 6880
27. G.T. Marczynski Chromosome methylation and measurement of faithful, once and only once per cell cycle chromosome replication in Caulobacter crescentus J. Bacteriol. 181 1999 1984 1993
28. H. Merrikh, and A.D. Grossman Control of the replication initiator DnaA by an anti-cooperativity factor Mol. Microbiol. 82 2011 434 446
29. H. Murray, and J. Errington Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA Cell 135 2008 74 84
30. M.F. Noirot-Gros, E. Dervyn, L.J. Wu, P. Mervelet, J. Errington, S.D. Ehrlich, and P. Noirot An expanded view of bacterial DNA replication Proc. Natl. Acad. Sci. USA 99 2002 8342 8347
31. G. Nonaka, M. Blankschien, C. Herman, C.A. Gross, and V.A. Rhodius Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress Genes Dev. 20 2006 1776 1789
32. T. Nyström Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol. Microbiol. 54 2004 855 862
33. T.A. Phillips, R.A. VanBogelen, and F.C. Neidhardt lon gene product of Escherichia coli is a heat-shock protein J. Bacteriol. 159 1984 283 287
34. F. Rodriguez, F. Arsène-Ploetze, W. Rist, S. Rüdiger, J. Schneider-Mergener, M.P. Mayer, and B. Bukau Molecular basis for regulation of the heat shock transcription factor sigma32 by the DnaK and DnaJ chaperones Mol. Cell 32 2008 347 358
35. A. Rowley, G.C. Johnston, B. Butler, M. Werner-Washburne, and R.A. Singer Heat shock-mediated cell cycle blockage and G1 cyclin expression in the yeast Saccharomyces cerevisiae Mol. Cell. Biol. 13 1993 1034 1041
36. M.F. Susin, R.L. Baldini, F. Gueiros-Filho, and S.L. Gomes GroES/GroEL and DnaK/DnaJ have distinct roles in stress responses and during cell cycle progression in Caulobacter crescentus J. Bacteriol. 188 2006 8044 8053
37. J.A. Taylor, M.C. Ouimet, R. Wargachuk, and G.T. Marczynski The Caulobacter crescentus chromosome replication origin evolved two classes of weak DnaA binding sites Mol. Microbiol. 82 2011 312 326
38. T. Tomoyasu, T. Ogura, T. Tatsuta, and B. Bukau Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli Mol. Microbiol. 30 1998 567 581
39. T. Tomoyasu, A. Mogk, H. Langen, P. Goloubinoff, and B. Bukau Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol Mol. Microbiol. 40 2001 397 413
40. E.W. Trotter, L. Berenfeld, S.A. Krause, G.A. Petsko, and J.V. Gray Protein misfolding and temperature up-shift cause G1 arrest via a common mechanism dependent on heat shock factor in Saccharomycescerevisiae Proc. Natl. Acad. Sci. USA 98 2001 7313 7318
41. V. Tsilibaris, G. Maenhaut-Michel, and L. Van Melderen Biological roles of the Lon ATP-dependent protease Res. Microbiol. 157 2006 701 713
42. C.G. Tsokos, and M.T. Laub Polarity and cell fate asymmetry in Caulobacter crescentus Curr. Opin. Microbiol. 15 2012 744 750
43. L. Waxman, and A.L. Goldberg Selectivity of intracellular proteolysis: protein substrates activate the ATP-dependent protease (La) Science 232 1986 500 503
44. R. Wright, C. Stephens, G. Zweiger, L. Shapiro, and M.R. Alley Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation Genes Dev. 10 1996 1532 1542
45. J. Yochem, H. Uchida, M. Sunshine, H. Saito, C.P. Georgopoulos, and M. Feiss Genetic analysis of two genes, dnaJ and dnaK, necessary for Escherichia coli and bacteriophage lambda DNA replication Mol. Gen. Genet. 164 1978 9 14
46. A. Zawilak-Pawlik, A. Kois, K. Stingl, I.G. Boneca, P. Skrobuk, J. Piotr, R. Lurz, J. Zakrzewska-Czerwińska, and A. Labigne HobA - a novel protein involved in initiation of chromosomal replication in Helicobacter pylori Mol. Microbiol. 65 2007 979 994
47. M. Zylicz The Escherichia coli chaperones involved in DNA replication Philos. Trans. R. Soc. Lond. B Biol. Sci. 339 1993 271 277 discussion 277-278
48. B. Ely Genetics of Caulobacter crescentus Methods Enzymol. 204 1991 372 384
49. K.G. Gora, C.G. Tsokos, Y.E. Chen, B.S. Srinivasan, B.S. Perchuk, and M.T. Laub A cell-type-specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus Mol. Cell 39 2010 455 467
50. H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin 1000 Genome Project Data Processing Subgroup The Sequence Alignment/Map format and SAMtools Bioinformatics 25 2009 2078 2079
51. J.M. Skerker, M.S. Prasol, B.S. Perchuk, E.G. Biondi, and M.T. Laub Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis PLoS Biol. 3 2005 e334
52. K.H. Wang, R.T. Sauer, and T.A. Baker ClpS modulates but is not essential for bacterial N-end rule degradation Genes Dev. 21 2007 403 408