1887

Chapter 26 : Switches and Signal Transduction Networks in the Cell Cycle

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Switches and Signal Transduction Networks in the Cell Cycle, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818319/9781555810894_Chap26-1.gif /docserver/preview/fulltext/10.1128/9781555818319/9781555810894_Chap26-2.gif

Abstract:

Cell differentiation in the gram-negative bacterium results from asymmetric cell division that produces two morphologically distinct progeny, a nonmotile stalked cell and a motile swarmer cell. Two examples are considered in this chapter. In the first, evidence is discussed that developmental events are coupled to the cell division cycle by a complex signal transduction pathway mediated by sensor histidine kinases and effector proteins. In the second, the role of the response regulator FlbD is examined in flagellum biosynthesis, where it functions as both a transcription activator and repressor to regulate the timing of flagellar () gene expression in the cell cycle. As discussed in the second part of this chapter, there is also experimental evidence that DNA synthesis is required for initiation of the gene transcription cascade. Pseudoreversion analysis of a temperature sensitive mutation identified cold-sensitive suppressors that map to three new cell division genes, , , and . DNA sequence analysis of and show that both genes encode proteins with carboxyterminal domains homologous to the histidine kinases of the bacterial sensor proteins. It is a known fact that that flagellum biosynthesis, activation of motility, and pili formation require the completion of successive cell division cycle checkpoints. The nature of the regulated target genes in flagellum biosynthesis is much better understood, but nothing is known of the class I genes that respond to the cell cycle signal and initiate the gene cascade.

Citation: Lane T, Benson A, Hecht G, Burton G, Newton A. 1995. Switches and Signal Transduction Networks in the Cell Cycle, p 403-417. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch26
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

. crescentus cell cycle. (A) The sequence of developmental events in the wild-type strain CB15 includes flagellum formation (fla), appearance of polar bacteriophage receptors (ϕ), activation of flagellum rotation (mot+), pili formation (pili), loss of motility (mot), loss of bacteriophage receptors (ϕ), and stalk formation. The periods corresponding to DNA synthesis (S), postsynthetic gap (G2), presynthetic gap (G1), as well as division initiation (DIVi), division progression (DIVp), and cell separation (CS) are indicated. (B) Nonmotile mutants assemble inactive flagella (designated as straight lines), are bacteriophage ϕCbK resistant, and fail to form stalks, but they divide normally ( ). (C) Cells blocked before the completion of DIVp form long unpinched filaments. Development is blocked, but flagellum biosynthesis continues; consequently, these cells do not form stalks but accumulate multiple inactive flagella at a single pole after several generations ( ).

Citation: Lane T, Benson A, Hecht G, Burton G, Newton A. 1995. Switches and Signal Transduction Networks in the Cell Cycle, p 403-417. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Predicted domain organization of histidine kinases PleC ( ) and DivJ ( ) and response regulators DivK ( ) and PleD (Hecht and Newton, unpublished data) deduced from translated DNA sequences. Closed boxes indicate transmembrane domains; H, N, G1, and G2 indicate conserved His, Asn, Asp-Xaa-Gly-Xaa-Gly, and Gly-Xaa-Gly-Xaa-Gly motifs, respectively; RR1 and RR2 are the two response regulator domains in PleD; D, K, and R indicate conserved Asp, Lys, and Arg residues, respectively.

Citation: Lane T, Benson A, Hecht G, Burton G, Newton A. 1995. Switches and Signal Transduction Networks in the Cell Cycle, p 403-417. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Roles of PleC, DivK, and DivJ in cell division and polar morphogenesis. This model proposes that the response regulator (RR) DivK acts at two different times in the cell cycle to control polar morphogenesis and cell division. Late in the cell cycle, DivK responds to the PleC histidine protein kinase (HPK) to initiate motility and stalk formation, and early in the subsequent cell cycle it responds to another sensor HPK, shown here as DivJ, to regulate cell division. For details, see text. Abbreviations: FLA, flagellum biosynthesis; MOT, motility; STK, stalk formation.

Citation: Lane T, Benson A, Hecht G, Burton G, Newton A. 1995. Switches and Signal Transduction Networks in the Cell Cycle, p 403-417. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

(A) Sequence of gene expression during the cell cycle. The graph illustrates the sequence and timing of class II, III, and IV gene transcription during the cell cycle. The periods of the presynthetic gap (Gl), synthesis (S), and postsynthetic gap (G2) are indicated above the graph. (B) The flagellar hierarchy. Genes encoding proteins that are necessary for gene synthesis are arranged in hierarchical order based on epistasis experiments. The promoter structures of genes at each level are listed at the left, along with the class to which they belong. σ and σ are hypothetical σ-factors that direct transcription from the unique promoters of the class IIA and class IIB genes

Citation: Lane T, Benson A, Hecht G, Burton G, Newton A. 1995. Switches and Signal Transduction Networks in the Cell Cycle, p 403-417. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch26
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818319.chap26
1. Abeles, F. B. 1992. Ethylene in Plant Biology, 2nd ed. Academic Press, New York.
2. Anderson, D. K.,, N. Ohta,, J. Wu,, and A. Newton. 1995. Regulation of the Caulobacter crescentus rpoN gene and function of the purified σ 54 in flagellar gene transcription. Mol. Gen. Genet. 246: 697 706.
3. Barrett, J. T.,, C. S. Rhodes,, D. M. Ferber,, B. Jenkins,, S. A. Kuhl,, and B. Ely. 1982. Construction of a genetic map for Caulobacter crescentus. J. Bacteriol. 149: 889 896.
4. Benson, A.,, and A. Newton. Unpublished data.
5. Benson, A. K.,, G. Ramakrishnan,, N. Ohta,, J. Feng,, A. Ninfa,, and A. Newton. 1994a. The Caulobacter crescentus HbD protein acts at ftr sequence elements both to activate and repress transcription of cell cycle regulated flagellar genes. Proc. Natl. Acad. Sci. USA 91: 4989 4993.
6. Benson, A. K.,, J. Wu,, and A. Newton. 1994b. The role of F1bD in regulation of flagellar gene transcription in Caulobacter crescentus. Res. Microbiol. 12: 420 430.
7. Bourret, R. B.,, J. F. Hess,, and M. I. Simon. 1990. Conserved aspartate residues and phosphorylation in signal transduction by the chemotaxis protein CheY. Proc. Natl. Acad. Sci. USA 87: 41 45.
8. Brewin, N. J. 1993. The Rhizobium-legume symbiosis: plant morphogenesis in a nodule. Semin. Cell Biol. 4: 149 156.
9. Brun, Y. V.,, G. Marczynski,, and L. Shapiro. 1994. The expression of asymmetry during Caulobacter cell differentiation. Annu. Rev. Biochem. 63: 419 450.
10. Brun, Y. V.,, and L. Shapiro. 1992. A temporally controlled σ-factor is required for polar morphogenesis and normal cell division in Caulobacter. Genes Dev. 6: 2395 2408.
11. Burton, G.,, and A. Newton. Unpublished data.
12. Chang, C.,, S. F. Kwok,, A. B. Bleecker,, and E. M. Meyerowitz. 1993. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262: 539 544.
13. Chen, L.-S.,, D. Mullin,, and A. Newton. 1986. Identification, nucleotide sequence, and control of developmentally regulated promoters in the hook operon region of Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 83: 2860 2864.
14. Degnen, S. X.,, and A. Newton. 1972. Chromosome replication during development in Caulobacter crescentus. J. Mol. Biol. 64: 671 680.
15. Dingwall, A.,, J. D. Garman,, and L. Shapiro. 1992a. Organization and ordered expression of Caulobacter genes encoding flagellar basal body rod and ring proteins J. Mol. Biol. 228: 1147 1162.
16. Dingwall, A.,, J. W. Gober,, and L. Shapiro. 1990. Identification of a Caulobacter basal body structural gene and a cis-acting site required for activation of transcription J. Bacteriol. 172: 6066 6076.
17. Dingwall, A.,, W. Y. Zhuang,, K. Quon,, and L. Shapiro. 1992b. Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA rephcation. J. Bacteriol. 174: 1760 1768.
18. Gilles-Gonzalez, M. A.,, G. S. Ditta,, and D. R. Helinski. 1991. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature (London) 350: 170 172.
19. Gober, J. W.,, R. Champer,, S. Reuter,, and L. Shapiro. 1991. Expression of positional information during cell differentiation in Caulobacter. Cell 64: 381 391.
20. Gober, J. W.,, and L. Shapiro. 1992. A developmentally regulated Caulobacter flagellar promoter is activated by 3' enhancer and IHF binding elements. Mol. Biol. Cell 3: 913 926.
21. Gottfert, M. 1993. Regulation and function of rhizobial nodulation genes. FEMS Microbiol. Rev. 10: 39 63.
22. Haselkorn, R. 1992. Developmentally regulated gene rearrangements in prokaryotes. Annu. Rev. Genet. 26: 113 130.
23. Hecht, G. B.,, T. Lane,, J. Sommer,, and A. Newton. Submitted for publication.
24. Hecht, G. B.,, and A. Newton. Unpublished data.
25. Helmann, J. D.,, and M. J. Chamberlin. 1987. DNA sequence analysis suggests that expression of flagellar and chemotaxis genes in Escherichia coli and Salmonella typhimurium is controlled by an alternative a factor. Proc. Natl. Acad. Sci. USA 84: 6422 6424.
26. Horvitz, H. R.,, and I. Herskowitz. 1992. Mechanisms of asymmetric cell division: two B's or not two B's, that is the question. Cell 68: 237 255.
27. Huguenel, E. D.,, and A. Newton. 1982. Localization of surface structures during procaryotic differentiation: role of cell division in Caulobacter crescentus. Differentiation 21: 71 78.
28. Khambaty, F. M.,, and B. Ely. 1992. Molecular genetics of the flgI region and its role in flagellum biosynthesis in Caulobacter crescentus. J. Bacteriol. 174: 4101 4109.
29. Kim, S. K.,, D. Kaiser,, and A. Kuspa. 1992. Control of cell density and pattern by intercellular signaling in Myxococcus development. Annu. Rev. Microbiol. 46: 117 139.
30. Kustu, S.,, E. Santero,, J. Keener,, D. Popham,, and D. Weiss. 1989. Expression of σ 54 ( ntrA)-dependent genes is probably united by a common mechanism. Microbiol. Rev. 53: 367 376.
31. Lane, T.,, N. Ohta,, and A. Newton. Unpublished data.
32. Macnab, R. M. 1992. Genetics and biogenesis of bacterial flagella. Annu. Rev. Genet. 26: 131 158.
33. Maeda, T.,, S. M. Wurler-Murphy,, and H. Saito. 1994. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature (London) 369: 242 245.
34. Minnich, S. A.,, and A. Newton. 1987. Promoter mapping and cell cycle regulation of flagellin gene transcription in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 84: 1142 1146.
35. Minnich, S. A.,, N. Ohta,, N. Taylor,, and A. Newton. 1988. Role of the 25-, 27-, and 29-kilodalton flagellins in Caulobacter crescentus cell motihty: method for construction of deletion and Tn5 insertion mutants by gene replacement. J. Bacteriol. 170: 3953 3960.
36. Mullin, D.,, S. Minnich,, L. S. Chen,, and A. Newton. 1987. A set of positively regulated flagellar gene promoters in Caulobacter crescentus with sequence homology to the nif gene promoters of Klebsiella pneumoniae. J. Mol. Biol. 195: 939 943.
37. Mullin, D. A.,, and A. Newton. 1989. Ntr-like promoters and upstream regulatory sequence ftr are required for transcription of a developmentally regulated Caulobacter crescentus flagellar gene. J. Bacteriol. 171: 3218 3227.
38. Mullin, D. A.,, and A. Newton. 1993. A σ 54promoter and downstream sequence elements ftr2 and ftr3 are required for regulated expression of divergent transcription units flaN and flbG in Caulobacter crescentus. J. Bacteriol. 175: 2067 2076.
39. Newton, A.,, G. Hecht,, T. Lane,, and N. Ohta,. 1994. Role of histidine protein kinases and response regulators in cell division and polar morphogenesis in Caulobacter crescentus, p. 296 301. In A. M. Torriani-Gorini,, E. Yagil,, and S. Silver (ed.), Cellular and Molecular Biology of Phosphate and Phosphorylated Compounds in Microorganisms. American Society for Microbiology, Washington, D.C..
40. Newton, A.,, and N. Ohta. 1990. Regulation of the cell division cycle and differentiation in bacteria. Annu. Rev. Microbiol. 44: 689 719.
41. Newton, A.,, N. Ohta,, G. Ramakrishnan,, D. Mullin,, and G. Raymond. 1989. Genetic switching in the flagellar gene hierarchy of Caulobacter requires negative as well as positive regulation of transcription. Proc. Natl. Acad. Sci. USA 86: 6651 6655.
42. Ninfa, A. J.,, D. A. Mullin,, G. Ramakrishnan,, and A. Newton. 1989. Escherichia coli σ-54 RNA polymerase recognizes Caulobacter crescentus flaK and flaN flagellar gene promoters in vitro. J. Bacteriol. 171: 383 391.
43. Ohta, N.,, L.-S. Chen,, D. Mullin,, and A. Newton. 1991. Timing of flagellar gene expression in the Caulobacter cell cycle is determined by a transcriptional cascade of positive regulatory genes. J. Bacteriol. 173: 1514 1522.
44. Ohta, N.,, L.-S. Chen,, E. Swanson,, and A. Newton. 1985. Transcriptional regulation of a periodically controlled flagellar gene operon in Caulobacter crescentus. J. Mol. Biol. 186: 107 115.
45. Ohta, N.,, T. Lane,, E. G. Ninfa,, J. M. Sommer,, and A. Newton. 1992. A histidine protein kinase homologue required for regulation of bacterial cell division and differentiation. Proc. Natl. Acad. Sci. USA 89: 10297 10301.
46. Osley, M. A.,, M. Sheffery,, and A. Newton. 1977. Regulation of flagellin synthesis in the cell cycle of Caulobacter: dependence on DNA replication. Cell 12: 393 400.
47. Ota, I. M.,, and A. Varshavsky. 1993. A yeast protein similar to bacterial two-component regulators. Science 262: 566 569.
48. Parkinson, J. S.,, and E. C. Kofoid. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26: 71 112.
49. Porter, S. C.,, A. K. North,, A. B. Wedel,, and S. Kustu. 1993. Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation. Genes Dev. 7: 2258 2273.
50. Ramakrishnan, G.,, and A. Newton. 1990. FlbD of Caulobacter crescentus is a homologue of NtrC (NR I) and activates sigma-54 dependent flagellar gene promoters. Proc. Natl. Acad. Sci. USA 87: 2369 2373.
51. Ramakrishnan, G.,, and A. Newton. Unpublished data.
52. Ramakrishnan, G.,, J.-L. Zhao ,, and A. Newton. 1991. The cell-cycle regulated flagellar gene flbF of Caulobacter crescentus is homologous to the virulence locus (lcrD) of Yersinia pestis. J. Bacteriol. 173: 7283 7292.
53. Ramakrishnan, G.,, J. - L. Zhao, and A. Newton. 1994. Multiple structural proteins are required for both transcriptional activation and negative autoregulation of Caulobacter flagellar genes. J. Bacteriol. 176: 7587 7600.
54. Sanders, D. A.,, B. L. Gillece-Castro,, A. M. Stock,, A. L. Burlingame,, and D. E. Koshland. 1989. Identification of the site of phosphorylation of the chemotaxis response regulator protein CheY. J. Biol. Chem. 264: 21770 21778.
55. Schroder, I.,, C. D. Wolin,, R. Cavicchioli,, and R. P. Gunsalus. 1994. Phosphorylation and dephosphorylation of the NarQ, NarX, and NarL proteins of the nitrate-dependent two-component regulatory system of Escherichia coli. J. Bacteriol. 176: 4985 4992.
56. Sheffery, M.,, and A. Newton. 1981. Regulation of periodic protein synthesis in the cell cycle: control of initiation and termination of flagellar gene expression. Cell 24: 49 57.
57. Shimkets, L. J. 1990. Social and developmental biology of the myxobacteria. Microbiol. Rev. 54: 473 501.
58. Sommer, J. M.,, and A. Newton. 1988. Sequential regulation of developmental events during polar morphogenesis in Caulobacter crescentus: assembly of pili on swarmer cells requires cell separation. J. Bacteriol. 170: 409 415.
59. Sommer, J. M.,, and A. Newton. 1989. Turning off flagellum rotation requires the pleiotropic gene pleD:pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus. J. Bacteriol. 171: 392 401.
60. Sommer J. M.,, and A. Newton. 1991. Pseudoreversion analysis indicates a direct role of cell division genes in polar morphogenesis and differentiation in Caulobacter crescentus. Genetics 129: 623 630.
61. Stephens, C. M.,, and L. Shapiro. 1993. An unusual promoter controls cell-cycle regulation and dependence on DNA replication of the Caulobacter fliLM early flagellar operon. Mol. Microbiol. 9: 1169 1179.
62. Stock, A. M.,, J. M. Mottonen,, J. B. Stock,, and C. E. Schutt. 1989. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature (London) 337: 745 749.
63. Stock, J. B.,, A. J. Ninfa,, and A. M. Stock. 1989. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53: 450 490.
64. Terrana, B.,, and A. Newton. 1976. Requirement of cell division step for stalk formation in Caulobacter crescentus. J. Bacteriol. 128: 456 462.
65. VanWay, S. M.,, A. Newton,, A. H. Mullin,, and D. A. Mullin. 1993. Identification of the promoter and a negative regulatory element, ftr4 that is needed for cell cycle timing of fliF operon expression in Caulobacter crescentus. J. Bacteriol. 175: 367 376.
66. Volz, K. 1993. Structural conservation in the CheY superfamily. Biochemistry 32: 11741 11753.
67. Wang, S. P.,, P. L. Sharma,, P. V. Schoenlein,, and B. Ely. 1993. A histidine protein kinase is involved in polar organelle development in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 90: 630 634.
68. Wanner, B. L. 1992. Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria? J. Bacteriol. 174: 2053 2058.
69. Weiss, V.,, F. Claverie-Martin,, and B. Magasanik. 1992. Phosphorylation of nitrogen regulator I of Escherichia coli induces strong cooperative binding to DNA essential for activation of transcription. Proc. Natl. Acad. Sci. USA 89: 5088 5092.
70. Wingrove, J. A.,, E. K. Mangan,, and J. W. Gober. 1993. Spatial and temporal phosphorylation of a transcriptional activator regulates pole-specific gene expression in Caulobacter. Genes Dev. 7: 1979 1992.
71. Wingrove, J. A.,, and J. W. Gober. 1994. A σ54 transcriptional activator also functions as a polespecific repressor in Caulobacter. Genes Dev. 8: 1839 1852.
72. Wolk, C. P. 1991. Genetic analysis of cyanobacterial development. Curr. Opin. Genet. Dev. 1: 336 341.
73. Wu, J.,, A. Benson,, and A. Newton. Submitted for publication.
74. Xu., H.,, A. Dingwall,, and L. Shapiro. 1989. Negative transcriptional regulation in the Caulobacter flagellar hierarchy. Proc. Natl. Acad. Sci. USA 86: 6656 6660.
75. Yu, J.,, and L. Shapiro. 1992. Early Caulobacter crescentus genes fliL and fliM are required for flagellar gene expression and normal cell divison. J. Bacteriol. 174: 3327 3338.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error