Size sensors in bacteria, cell cycle control, and size control

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  Robert, Lydia ^a,b,c  

^a UMR1319 MICALIS   (France)

^b AGROPARISTECH   (France)

^c CNRS   (France)

Author keywords

Bacterial cell cycle; DnaA; FtsZ; Incremental model; MinCD; Replication initiation; Size control

Indexed keywords

CARDIOLIPIN; CYCLIN DEPENDENT KINASE; FTSZ PROTEIN; REPLICATION INITIATOR PROTEIN DNAA;

BIOSENSOR; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIVISION; CELL ELONGATION; CELL SIZE; CHROMOSOME SEGREGATION; CYTOKINESIS; DNA DAMAGE; DNA REPLICATION; DOWNSTREAM PROCESSING; NONHUMAN; PHOSPHOLIPID MEMBRANE; REVIEW; SIGNAL PROCESSING;

BACTERIA (MICROORGANISMS);

EID: 84931269353     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00515     Document Type: Review

References (86)

1. Addinall, S. G., and Holland, B. (2002). The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J. Mol. Biol. 318, 219-236. doi: 10.1016/S0022-2836(02)00024-4.
2. Adler, H., Fisher, W. D., Cohen, A., and Hardigree, A. A. (1967). Miniature Escherichia coli cells deficient in DNA. Proc. Natl. Acad. Sci. U.S.A. 57, 321-326.
3. Amir, A. (2014). Cell size regulation in bacteria. Phys. Rev. Lett. 112:208102. doi: 10.1103/PhysRevLett.112.208102.
4. Arias, E. E., and Walter, J. C. (2006). PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8, 84-90. doi: 10.1038/ncb1346.
5. Atlung, T., Løbner-Olesen, A., and Hansen, F. G. (1987). Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli. Mol. Gen. Genet. 206, 51-59.
6. Bates, D., and Kleckner, N. (2005). Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121, 899-911. doi: 10.1016/j.cell.2005.04.013.
7. Ben-Yehuda, S., and Losick, R. (2002). Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109, 257-266. doi: 10.1016/S0092-8674(02)00698-0.
8. Bernhardt, T. G., and De Boer, P. A. J. (2005). Slma, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18, 555-564. doi: 10.1016/j.molcel.2005.04.012.
9. Bi, E. F., and Lutkenhaus, J. (1991). Ftsz ring structure associated with division in Escherichia coli. Nature 354, 161-164.
10. Bisicchia, P., Arumugam, S., Schwille, P., and Sherratt, D. (2013). MinC, MinD, and MinE drive counter-oscillation of early-cell-division proteins prior to Escherichia coli septum formation. mBio 4:e00856-13. doi: 10.1128/mBio.00856-13.
11. Boeneman, K., Fossum, S., Yang, Y., Fingland, N., Skarstad, K., and Crooke, E. (2009). Escherichia coli DnaA forms helical structures along the longitudinal cell axis distinct from MreB filaments. Mol. Microbiol. 72, 645-657. doi: 10.1111/j.1365-2958.2009.06674.x.
12. Boye, E., Stokke, T., Kleckner, N., and Skarstad, K. (1996). Coordinating dna replication initiation with cell growth: differential roles for DnaA and SeqA proteins. Proc. Natl. Acad. Sci. U.S.A. 93, 12206-12211.
13. Campbell, J. L., and Kleckner, N. (1990). E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62, 967-979.
14. Campos, M., Surovtsev, I. V., Kato, S., Paintdakhi, A., Beltran, B., Ebmeier, S. E., et al. (2014). A constant size extension drives bacterial cell size homeostasis. Cell 159, 1433-1446. doi: 10.1016/j.cell.2014.11.022.
15. Chien, A.-C., Hill, N. S., and Levin, P. A. (2012). Cell size control in bacteria. Curr. Biol. 22, R340-R349. doi: 10.1016/j.cub.2012.02.032.
16. Collier, J., and Shapiro, L. (2009). Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J. Bacteriol. 191, 5706-5716. doi: 10.1128/JB.00525-09.
17. Cooper, S. (1969). Cell division and dna replication following a shift to a richer medium. J. Mol. Biol. 43, 1-11.
18. Cooper, S., and Helmstetter, C. E. (1968). Chromosome replication and the division cycle of Escherichia coli. J. Mol. Biol. 31, 519-540.
19. De Boer, P. A., Crossley, R. E., and Rothfield, L. I. (1989). A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56, 641-649.
20. Den Blaauwen, T., Buddelmeijer, N., Aarsman, M. E., Hameete, C. M., and Nanninga, N. (1999). Timing of FtsZ assembly in Escherichia coli. J. Bacteriol. 181, 5167-5175.
21. Di Talia, S., Skotheim, J. M., Bean, J. M., Siggia, E. D., and Cross, F. R. (2007). The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448, 947-951. doi: 10.1038/nature06072.
22. Di Ventura, B., Knecht, B., Andreas, H., Godinez, W. J., Fritsche, M., Rohr, K., et al. (2013). Chromosome segregation by the Escherichia coli min system. Mol. Syst. Biol. 9:686. doi: 10.1038/msb.2013.44.
23. Domínguez-Escobar, J., Chastanet, A., Crevenna, A. H., Fromion, V., Wedlich-Söldner, R., and Carballido-López, R. (2011). Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333, 225-228. doi: 10.1126/science.1203466.
24. Donachie, W. D. (1968). Relationship between cell size and time of initiation of dna replication. Nature 219, 1077-1079.
25. Donachie, W. D., and Blakely, G. W. (2003). Coupling the initiation of chromosome replication to cell size in Escherichia coli. Curr. Opin. Microbiol. 6, 146-150. doi: 10.1016/S1369-5274(03)00026-2.
26. Fantes, P., and Nurse, P. (1977). Control of cell size at division in fission yeast by a growth-modulated size control over nuclear division. Exp. Cell Res. 107, 377-386.
27. Fantes, P. A. (1977). Control of cell size and cycle time in Schizosaccharomyces pombe. J. Cell Sci. 24, 51-67.
28. Fantes, P. A., and Nurse, P. (1978). Control of the timing of cell division in fission yeast: cell size mutants reveal a second control pathway. Exp. Cell Res. 115, 317-329.
29. Fujimitsu, K., Senriuchi, T., and Katayama, T. (2009). Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA. Genes Dev. 23, 1221-1233. doi: 10.1101/gad.1775809.
30. Goley, E. D., Iniesta, A. A., and Shapiro, L. (2007). Cell cycle regulation in Caulobacter: location, location, location. J. Cell Sci. 120, 3501-3507. doi: 10.1242/jcs.005967.
31. Haeusser, D. P., and Levin, P. A. (2008). The great divide: coordinating cell cycle events during bacterial growth and division. Curr. Opin. Microbiol. 11, 94-99. doi: 10.1016/j.mib.2008.02.008.
32. Hale, C. A., Meinhardt, H., and de Boer, P. A. (2001). Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J. 20, 1563-1572. doi: 10.1093/emboj/20.7.1563.
33. Harry, E., Monahan, L., and Thompson, L. (2006). Bacterial cell division: the mechanism and its precison. Int. Rev. Cytol. 253, 27-94. doi: 10.1016/S0074-7696(06)53002-5.
34. Hartwell, L. H., and Weinert, T. A. (1989). Checkpoints: controls that ensure the order of cell cycle events. Science 246, 629-634.
35. Hill, N. S., Kadoya, R., Chattoraj, D. K., and Levin, P. A. (2012). Cell size and the initiation of DNA replication in bacteria. PLoS Genet. 8:e1002549. doi: 10.1371/journal.pgen.1002549.
36. Hu, Z., and Lutkenhaus, J. (1999). Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol. Microbiol. 34, 82-90.
37. Huang, Y., Chew, T. G., Ge, W., and Balasubramanian, M. K. (2007). Polarity determinants Tea1p, Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev. Cell 12, 987-996. doi: 10.1016/j.devcel.2007.03.015.
38. Iyer-Biswas, S., Wright, C. S., Henry, J. T., Lo, K., Burov, S., Lin, Y., et al. (2014). Scaling laws governing stochastic growth and division of single bacterial cells. Proc. Natl. Acad. Sci. U.S.A. 111, 15912-15917. doi: 10.1073/pnas.1403232111.
39. Johnston, G. C., Pringle, J. R., and Hartwell, L. H. (1977). Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp. Cell Res. 105, 79-98.
40. Jun, S., and Taheri-Araghi, S. (2015). Cell-size maintenance: universal strategy revealed. Trends Microbiol. 23, 4-6. doi: 10.1016/j.tim.2014.12.001.
41. Jun, S., and Wright, A. (2010). Entropy as the driver of chromosome segregation. Nat. Rev. Microbiol. 8, 600-607. doi: 10.1038/nrmicro2391.
42. Katayama, T., Ozaki, S., Keyamura, K., and Fujimitsu, K. (2010). Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat. Rev. Microbiol. 8, 163-170. doi: 10.1038/nrmicro2314.
43. Kato, J.-I., and Katayama, T. (2001). Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 20, 4253-4262. doi: 10.1093/emboj/20.15.4253.
44. Kelly, A. J., Sackett, M. J., Din, N., Quardokus, E., and Brun, Y. V. (1998). Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev. 12, 880-893.
45. Kitagawa, R., Mitsuki, H., Okazaki, T., and Ogawa, T. (1996). A novel DnaA protein-binding site at 94.7 min on the Escherichia coli chromosome. Mol. Microbiol. 19, 1137-1147.
46. Kjeldgaard, N., Maaløe, O., and Schaechter, M. (1958). The transition between different physiological states during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19, 607-616.
47. Kurokawa, K., Nishida, S., Emoto, A., Sekimizu, K., and Katayama, T. (1999). Replication cycle-coordinated change of the adenine nucleotide-bound forms of dnaa protein in Escherichia coli. EMBO J. 18, 6642-6652.
48. Løbner-Olesen, A., Skarstad, K., Hansen, F. G., von Meyenburg, K., and Boye, E. (1989). The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57, 881-889.
49. Longo, D., and Hasty, J. (2006). Dynamics of single-cell gene expression. Mol. Syst. Biol. 2:64. doi: 10.1038/msb4100110.
50. Lutkenhaus, J. (2007). Assembly dynamics of the bacterial minCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539-562. doi: 10.1146/annurev.biochem.75.103004.142652.
51. Martin, S. G., and Berthelot-Grosjean, M. (2009). Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 459, 852-856. doi: 10.1038/nature08054.
52. Margolin, W. (2005). Ftsz and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6, 862-871. doi: 10.1038/nrm1745.
53. Messer, W. (2002). The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate dna replication. FEMS Microbiol. Rev. 26, 355-374. doi: 10.1016/S0168-6445(02)00127-4.
54. Moseley, J. B., Mayeux, A., Paoletti, A., and Nurse, P. (2009). A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 459, 857-860. doi: 10.1038/nature08074.
55. Mulder, E., and Woldringh, C. L. (1989). Actively replicating nucleoids influence positioning of division sites in Escherichia coli filaments forming cells lacking DNA. J. Bacteriol. 171, 4303-4314.
56. Murray, A. W., and Hunt, T. (1993). The Cell Cycle: an Introduction. New York, NY: Oxford University Press.
57. Nishitani, H., Sugimoto, N., Roukos, V., Nakanishi, Y., Saijo, M., Obuse, C., et al. (2006). Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 25, 1126-1136. doi: 10.1038/sj.emboj.7601002.
58. Nobs, J.-B., and Maerkl, S. J. (2014). Long-term single cell analysis of S. pombe on a microfluidic microchemostat array. PLoS ONE 9:e93466. doi: 10.1371/journal.pone.0093466.
59. Novák, B. (2013). Pom1 is not the size ruler. Cell Cycle 12, 3463-3464. doi: 10.4161/cc.26818.
60. Nozaki, S., Niki, H., and Ogawa, T. (2009). Replication initiator DnaA of Escherichia coli changes its assembly form on the replication origin during the cell cycle. J. Bacteriol. 191, 4807-4814. doi: 10.1128/JB.00435-09.
61. Osella, M., Nugent, E., and Lagomarsino, M. C. (2014). Concerted control of Escherichia coli cell division. Proc. Natl. Acad. Sci. U.S.A. 111, 3431-3435. doi: 10.1073/pnas.1313715111.
62. Padte, N. N., Martin, S. G., Howard, M., and Chang, F. (2006). The cell-end factor Pom1p inhibits Mid1p in specification of the cell division plane in fission yeast. Curr. Biol. 16, 2480-2487. doi: 10.1016/j.cub.2006.11.024.
63. Pan, K. Z., Saunders, T. E., Flor-Parra, I., Howard, M., and Chang, F. (2014). Cortical regulation of cell size by a sizer cdr2p. Elife 3:e02040. doi: 10.7554/eLife.02040.
64. Quardokus, E., Din, N., and Brun, Y. V. (1996). Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter. Proc. Natl. Acad. Sci. U.S.A. 93, 6314-6319.
65. Raskin, D. M., and de Boer, P. A. (1999). Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 4971-4976.
66. Robert, L., Hoffmann, M., Krell, N., Aymerich, S., Robert, J., and Doumic, M. (2014). Division in Escherichia coli is triggered by a size-sensing rather than a timing mechanism. BMC Biol. 12:17. doi: 10.1186/1741-7007-12-17.
67. Rosenfeld, N., Young, J. W., Alon, U., Swain, P. S., and Elowitz, M. B. (2005). Gene regulation at the single-cell level. Science 307, 1962-1965. doi: 10.1126/science.1106914.
68. Schaechter, M., MaalOe, O., and Kjeldgaard, N. O. (1958). Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. Microbiology 19, 592-606.
69. Sekimizu, K., and Kornberg, A. (1988). Cardiolipin activation of DnaA protein, the initiation protein of replication in Escherichia coli. J. Biol. Chem. 263, 7131-7135.
70. Simmons, L. A., Foti, J. J., Cohen, S. E., and Walker, G. C. (2008). The SOS regulatory network. Ecosal Plus 2008, 1-48. doi: 10.1128/ecosalplus.5.4.3.
71. Soifer, I., Robert, L., Barkai, N., and Amir, A. (2014). Single-cell analysis of growth in budding yeast and bacteria reveals a Common size regulation strategy. Available online at: http://arxiv.org/abs/1410.4771.
72. Sompayrac, L., and Maaløe, O. (1973). Autorepressor model for control of dna replication. Nature 241, 133-135.
73. Soufo, C. D., Soufo, H. J. D., Noirot-Gros, M.-F., Steindorf, A., Noirot, P., and Graumann, P. L. (2008). Cell-cycle-dependent spatial sequestration of the DnaA replication initiator protein in Bacillus subtilis. Dev. Cell 15, 935-941. doi: 10.1016/j.devcel.2008.09.010.
74. Sveiczer, A., Novak, B., and Mitchison, J. M. (1996). The size control of fission yeast revisited. J. Cell Sci. 109(Pt 12), 2947-2957.
75. Swulius, M. T., and Jensen, G. J. (2012). The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-terminal yellow fluorescent protein tag. J. Bacteriol. 194, 6382-6386. doi: 10.1128/JB.00505-12.
76. Taheri-Araghi, S., Bradde, S., Sauls, J. T., Hill, N. S., Levin, P. A., Paulsson, J., et al. (2015). Cell-size control and homeostasis in bacteria. Curr. Biol. 25, 385-391. doi: 10.1016/j.cub.2014.12.009.
77. Thanedar, S., and Margolin, W. (2004). Ftsz exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167-1173. doi: 10.1016/j.cub.2004.06.048.
78. Tsukanov, R., Reshes, G., Carmon, G., Fischer-Friedrich, E., Gov, N., Fishov, I., et al. (2011). Timing of Z-ring localization in Escherichia coli. Phys. Biol. 8:066003. doi: 10.1088/1478-3975/8/6/066003.
79. Turner, J. J., Ewald, J. C., and Skotheim, J. M. (2012). Cell size control in yeast. Curr. Biol. 22, R350-R359. doi: 10.1016/j.cub.2012.02.041.
80. Van Teeffelen, S., Wang, S., Furchtgott, L., Huang, K. C., Wingreen, N. S., Shaevitz, J. W., et al. (2011). The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc. Natl. Acad. Sci. U.S.A. 108, 15822-15827. doi: 10.1073/pnas.1108999108.
81. Voorn, W., Koppes, L., and Grover, N. (1993). Mathematics of cell division in Escherichia coli: comparison between sloppy-size and incremental-size kinetics. Curr. Top. Mol. Gen. 1, 187-194.
82. Wang, X., Llopis, P. M., and Rudner, D. Z. (2013). Organization and segregation of bacterial chromosomes. Nat. Rev. Genet. 14, 191-203. doi: 10.1038/nrg3375.
83. Wold, S., Skarstad, K., Steen, H. B., Stokke, T., and Boye, E. (1994). The initiation mass for dna replication in Escherichia coli K-12 is dependent on growth rate. Eur. Mol. Biol. Organ. J. 13, 2097-2102.
84. Wood, E., and Nurse, P. (2013). Pom1 and cell size homeostasis in fission yeast. Cell Cycle 12, 3417-3425. doi: 10.4161/cc.26462.
85. Wu, L. J., and Errington, J. (2004). Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117, 915-925. doi: 10.1016/j.cell.2004.06.002.
86. Wu, L. J., and Errington, J. (2011). Nucleoid occlusion and bacterial cell division. Nat. Rev. Microbiol. 10, 8-12. doi: 10.1038/nrmicro2671.