Polar localization of the CckA histidine kinase and cell cycle periodicity of the essential master regulator CtrA in Caulobacter crescentus

Journal of Bacteriology

Volumn 192, Issue 2, 2010, Pages 539-552

  Angelastro, Peter S ^a,c   Sliusarenko, Oleksii ^a   Jacobs Wagner, Christine ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HARTFORD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CIS ACTING ELEMENT; GREEN FLUORESCENT PROTEIN; MONOMER; PROTEIN HISTIDINE KINASE;

ARTICLE; BACTERIAL STRAIN; CATALYSIS; CAULOBACTER CRESCENTUS; CELL CYCLE; CELL CYCLE REGULATION; CHROMOSOME; ENZYME LOCALIZATION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL CYCLE; CELL POLARITY; CYTOKINESIS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GREEN FLUORESCENT PROTEINS; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PERIODICITY; PHOSPHORYLATION; PROTEIN KINASES; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION FACTORS;

CAULOBACTER VIBRIOIDES;

EID: 73649109892     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00985-09     Document Type: Article

References (57)

1. Biondi, E. G., S. J. Reisinger, J. M. Skerker, M. Arif, B. S. Perchuk, K. R. Ryan, and M. T. Laub. 2006. Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444:899-904.
2. Bowers, L. M., E. B. Shapland, and K. R. Ryan. 2008. Who's in charge here? Regulating cell cycle regulators. Curr. Opin. Microbiol. 11:547-552.
3. Bowman, G. R., L. R. Comolli, J. Zhu, M. Eckart, M. Koenig, K. H. Downing, W. E. Moerner, T. Earnest, and L. Shapiro. 2008. A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134:945-955.
4. Boyd, J. M. 2000. Localization of the histidine kinase PilS to the poles of Pseudomonas aeruginosa and identification of a localization domain. Mol. Microbiol. 36:153-162.
5. Brown, P. J., G. G. Hardy, M. J. Trimble, and Y. V. Brun. 2009. Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv. Microb. Physiol. 54:1-101.
6. Chen, Y. E., C. G. Tsokos, E. G. Biondi, B. S. Perchuk, and M. T. Laub. 2009. Dynamics of two phosphorelays controlling cell cycle progression in Caulobacter crescentus. J. Bacteriol. 191:7417-7429.
7. Collier, J., and L. Shapiro. 2007. Spatial complexity and control of a bacterial cell cycle. Curr. Opin. Biotechnol. 18:333-340.
8. Domian, I. J., K. C. Quon, and L. Shapiro. 1997. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90:415-424.
9. Domian, I. J., A. Reisenauer, and L. Shapiro. 1999. Feedback control of a master bacterial cell-cycle regulator. Proc. Natl. Acad. Sci. USA 96:6648-6653.
10. Duerig, A., S. Abel, M. Folcher, M. Nicollier, T. Schwede, N. Amiot, B. Giese, and U. Jenal. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23:93-104.
11. Dutta, R., and M. Inouye. 2000. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25:24-28.
12. Ebersbach, G., A. Briegel, G. J. Jensen, and C. Jacobs-Wagner. 2008. A self-associating protein critical for chromosome attachment, division, and polar organization in caulobacter. Cell 134:956-968.
13. Ely, B. 1991. Genetics of Caulobacter crescentus. Methods Enzymol. 204:372-384.
14. Evinger, M., and N. Agabian. 1977. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J. Bacteriol. 132:294-301.
15. Freeman, J. A., B. N. Lilley, and B. L. Bassler. 2000. A genetic analysis of the functions of LuxN: a two-component hybrid sensor kinase that regulates quorum sensing in Vibrio harveyi. Mol. Microbiol. 35:139-149.
16. Goley, E. D., A. A. Iniesta, and L. Shapiro. 2007. Cell cycle regulation in Caulobacter: location, location, location. J. Cell Sci. 120:3501-3507.
17. Hallez, R., J. Mignolet, V. Van Mullem, M. Wery, J. Vandenhaute, J. J. Letesson, C. Jacobs-Wagner, and X. De Bolle. 2007. The asymmetric distribution of the essential histidine kinase PdhS indicates a differentiation event in Brucella abortus. EMBO J. 26:1444-1455.
18. Hecht, G. B., T. Lane, N. Ohta, J. M. Sommer, and A. Newton. 1995. An essential single domain response regulator required for normal cell division and differentiation in Caulobacter crescentus. EMBO J. 14:3915-3924.
19. Holtzendorff, J., D. Hung, P. Brende, A. Reisenauer, P. H. Viollier, H. H. McAdams, and L. Shapiro. 2004. Oscillating global regulators control the genetic circuit driving a bacterial cell cycle. Science 304:983-987.
20. Holtzendorff, J., J. Reinhardt, and P. H. Viollier. 2006. Cell cycle control by oscillating regulatory proteins in Caulobacter crescentus. Bioessays 28:355-361.
21. Hsing, W., and T. J. Silhavy. 1997. Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J. Bacteriol. 179:3729-3735.
22. Hung, D. Y., and L. Shapiro. 2002. A signal transduction protein cues proteolytic events critical to Caulobacter cell cycle progression. Proc. Natl. Acad. Sci. USA 99:13160-13165.
23. Iniesta, A. A., P. T. McGrath, A. Reisenauer, H. H. McAdams, and L. Shapiro. 2006. A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc. Natl. Acad. Sci. USA 103:10935-10940.
24. Iniesta, A. A., and L. Shapiro. 2008. A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phosphosignaling cascade. Proc. Natl. Acad. Sci. USA 105:16602-16607.
25. Jacobs, C., N. Ausmees, S. J. Cordwell, L. Shapiro, and M. T. Laub. 2003. Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol. Microbiol. 47:1279-1290.
26. Jacobs, C., I. J. Domian, J. R. Maddock, and L. Shapiro. 1999. Cell cycledependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 97:111-120.
27. Jacobs, C., D. Hung, and L. Shapiro. 2001. Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc. Natl. Acad. Sci. USA 98:4095-4100.
28. Jenal, U., and T. Fuchs. 1998. An essential protease involved in bacterial cell-cycle control. EMBO J. 17:5658-5669.
29. Jenal, U., J. White, and L. Shapiro. 1994. Caulobacter flagellar function, but not assembly, requires FliL, a non-polarly localized membrane protein present in all cell types. J. Mol. Biol. 243:227-244.
30. Judd, E. M., K. R. Ryan, W. E. Moerner, L. Shapiro, and H. H. McAdams. 2003. Fluorescence bleaching reveals asymmetric compartment formation prior to cell division in Caulobacter. Proc. Natl. Acad. Sci. USA 100:8235-8240.
31. Kass, M., A. Witkin, and D. Terzopoulos. 1988. Snakes: active contour models. Int. J. Comput. Vis. 1:321-331.
32. Lam, H., J. Y. Matroule, and C. Jacobs-Wagner. 2003. The asymmetric spatial distribution of bacterial signal transduction proteins coordinates cell cycle events. Dev. Cell 5:149-159.
33. Lam, H., W. B. Schofield, and C. Jacobs-Wagner. 2006. A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124:1011-1023.
34. Laub, M. T., S. L. Chen, L. Shapiro, and H. H. McAdams. 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc. Natl. Acad. Sci. USA 99:4632-4637.
35. Laub, M. T., L. Shapiro, and H. H. McAdams. 2007. Systems biology of Caulobacter. Annu. Rev. Genet. 41:429-441.
36. Letunic, I., T. Doerks, and P. Bork. 2009. SMART 6: recent updates and new developments. Nucleic Acids Res. 37:D229-D232.
37. Matroule, J. Y., H. Lam, D. T. Burnette, and C. Jacobs-Wagner. 2004. Cytokinesis monitoring during development; rapid pole-to-pole shuttling of a signaling protein by localized kinase and phosphatase in Caulobacter. Cell 118:579-590.
38. McGrath, P. T., A. A. Iniesta, K. R. Ryan, L. Shapiro, and H. H. McAdams. 2006. A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124:535-547.
39. McGrath, P. T., H. Lee, L. Zhang, A. A. Iniesta, A. K. Hottes, M. H. Tan, N. J. Hillson, P. Hu, L. Shapiro, and H. H. McAdams. 2007. High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat. Biotechnol. 25:584-592.
40. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Paul, R., T. Jaeger, S. Abel, I. Wiederkehr, M. Folcher, E. G. Biondi, M. T. Laub, and U. Jenal. 2008. Allosteric regulation of histidine kinases by their cognate response regulator determines cell fate. Cell 133:452-461.
42. Purcell, E. B., C. C. Boutte, and S. Crosson. 2008. Two-component signaling systems and cell cycle control in Caulobacter crescentus. Adv. Exp. Med. Biol. 631:122-130.
43. Quon, K. C., G. T. Marczynski, and L. Shapiro. 1996. Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84:83-93.
44. Quon, K. C., B. Yang, I. J. Domian, L. Shapiro, and G. T. Marczynski. 1998. Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc. Natl. Acad. Sci. USA 95:120-125.
45. Ryan, K. R., S. Huntwork, and L. Shapiro. 2004. Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis. Proc. Natl. Acad. Sci. USA 101:7415-7420.
46. Ryan, K. R., E. M. Judd, and L. Shapiro. 2002. The CtrA response regulator essential for Caulobacter crescentus cell-cycle progression requires a bipartite degradation signal for temporally controlled proteolysis. J. Mol. Biol. 324:443-455.
47. Schultz, J., F. Milpetz, P. Bork, and C. P. Ponting. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 95:5857-5864.
48. Skerker, J. M., M. S. Prasol, B. S. Perchuk, E. G. Biondi, and M. T. Laub. 2005. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol. 3:e334.
49. Spencer, W., R. Siam, M. C. Ouimet, D. P. Bastedo, and G. T. Marczynski. 2009. CtrA, a global response regulator, uses a distinct second category of weak DNA binding sites for cell cycle transcription control in Caulobacter crescentus. J. Bacteriol. 191:5458-5470.
50. Stock, A. M., V. L. Robinson, and P. N. Goudreau. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215.
51. Tanaka, T., S. K. Saha, C. Tomomori, R. Ishima, D. Liu, K. I. Tong, H. Park, R. Dutta, L. Qin, M. B. Swindells, T. Yamazaki, A. M. Ono, M. Kainosho, M. Inouye, and M. Ikura. 1998. NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ. Nature 396:88-92.
52. Taylor, B. L., and I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
53. Tsien, R. Y. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-544.
54. Viollier, P. H., N. Sternheim, and L. Shapiro. 2002. A dynamically localized histidine kinase controls the asymmetric distribution of polar pili proteins. EMBO J. 21:4420-4428.
55. Wheeler, R. T., and L. Shapiro. 1999. Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol. Cell 4:683-694.
56. Wu, J., N. Ohta, and A. Newton. 1998. An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter. Proc. Natl. Acad. Sci. USA 95:1443-1448.
57. Zacharias, D. A., J. D. Violin, A. C. Newton, and R. Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913-916.