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. 1996 Aug 1;15(15):3880–3889.

The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium.

S C Schuster 1, A A Noegel 1, F Oehme 1, G Gerisch 1, M I Simon 1
PMCID: PMC452086  PMID: 8670893

Abstract

We have used PCR to identify a Dictyostelium homolog of the bacterial two-component system. The gene dokA codes for a member of the hybrid histidine kinase family which is defined by the presence of conserved amino acid sequence motifs corresponding to an N-terminal receptor domain, a central kinase and a C-terminal response regulator moiety. Potential function of the regulator domain was demonstrated by phosphorylation in vitro. dokA mutants are deficient in the osmoregulatory pathway, resulting in premature cell death under high osmotic stress. Under less stringent osmotic conditions, cells grow at a normal rate, but development at the multicellular stage is altered. dokA is a member of a family of histidine kinase-like genes that play regulatory roles in eukaryotic cell function.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alex L. A., Simon M. I. Protein histidine kinases and signal transduction in prokaryotes and eukaryotes. Trends Genet. 1994 Apr;10(4):133–138. doi: 10.1016/0168-9525(94)90215-1. [DOI] [PubMed] [Google Scholar]
  2. Bourret R. B., Borkovich K. A., Simon M. I. Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu Rev Biochem. 1991;60:401–441. doi: 10.1146/annurev.bi.60.070191.002153. [DOI] [PubMed] [Google Scholar]
  3. Burbulys D., Trach K. A., Hoch J. A. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell. 1991 Feb 8;64(3):545–552. doi: 10.1016/0092-8674(91)90238-t. [DOI] [PubMed] [Google Scholar]
  4. Chang C., Kwok S. F., Bleecker A. B., Meyerowitz E. M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. doi: 10.1126/science.8211181. [DOI] [PubMed] [Google Scholar]
  5. Chang C., Meyerowitz E. M. Eukaryotes have "two-component" signal transducers. Res Microbiol. 1994 Jun-Aug;145(5-6):481–486. doi: 10.1016/0923-2508(94)90097-3. [DOI] [PubMed] [Google Scholar]
  6. Claros M. G., von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci. 1994 Dec;10(6):685–686. doi: 10.1093/bioinformatics/10.6.685. [DOI] [PubMed] [Google Scholar]
  7. Crovello C. S., Furie B. C., Furie B. Histidine phosphorylation of P-selectin upon stimulation of human platelets: a novel pathway for activation-dependent signal transduction. Cell. 1995 Jul 28;82(2):279–286. doi: 10.1016/0092-8674(95)90315-1. [DOI] [PubMed] [Google Scholar]
  8. Firtel R. A., Chapman A. L. A role for cAMP-dependent protein kinase A in early Dictyostelium development. Genes Dev. 1990 Jan;4(1):18–28. doi: 10.1101/gad.4.1.18. [DOI] [PubMed] [Google Scholar]
  9. Gottesman S., Stout V. Regulation of capsular polysaccharide synthesis in Escherichia coli K12. Mol Microbiol. 1991 Jul;5(7):1599–1606. doi: 10.1111/j.1365-2958.1991.tb01906.x. [DOI] [PubMed] [Google Scholar]
  10. Haugwitz M., Noegel A. A., Karakesisoglou J., Schleicher M. Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell. 1994 Oct 21;79(2):303–314. doi: 10.1016/0092-8674(94)90199-6. [DOI] [PubMed] [Google Scholar]
  11. Herskowitz I. MAP kinase pathways in yeast: for mating and more. Cell. 1995 Jan 27;80(2):187–197. doi: 10.1016/0092-8674(95)90402-6. [DOI] [PubMed] [Google Scholar]
  12. Hess J. F., Oosawa K., Matsumura P., Simon M. I. Protein phosphorylation is involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7609–7613. doi: 10.1073/pnas.84.21.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hopp T. P., Woods K. R. Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3824–3828. doi: 10.1073/pnas.78.6.3824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hopper N. A., Harwood A. J., Bouzid S., Véron M., Williams J. G. Activation of the prespore and spore cell pathway of Dictyostelium differentiation by cAMP-dependent protein kinase and evidence for its upstream regulation by ammonia. EMBO J. 1993 Jun;12(6):2459–2466. doi: 10.1002/j.1460-2075.1993.tb05900.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hrabak E. M., Willis D. K. The lemA gene required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators. J Bacteriol. 1992 May;174(9):3011–3020. doi: 10.1128/jb.174.9.3011-3020.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hua J., Chang C., Sun Q., Meyerowitz E. M. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science. 1995 Sep 22;269(5231):1712–1714. doi: 10.1126/science.7569898. [DOI] [PubMed] [Google Scholar]
  17. Huebner V. D., Matthews H. R. Phosphorylation of histidine in proteins by a nuclear extract of Physarum polycephalum plasmodia. J Biol Chem. 1985 Dec 25;260(30):16106–16113. [PubMed] [Google Scholar]
  18. Iuchi S., Matsuda Z., Fujiwara T., Lin E. C. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon. Mol Microbiol. 1990 May;4(5):715–727. doi: 10.1111/j.1365-2958.1990.tb00642.x. [DOI] [PubMed] [Google Scholar]
  19. Iuchi S. Phosphorylation/dephosphorylation of the receiver module at the conserved aspartate residue controls transphosphorylation activity of histidine kinase in sensor protein ArcB of Escherichia coli. J Biol Chem. 1993 Nov 15;268(32):23972–23980. [PubMed] [Google Scholar]
  20. Jermyn K. A., Berks M., Kay R. R., Williams J. G. Two distinct classes of prestalk-enriched mRNA sequences in Dictyostelium discoideum. Development. 1987 Aug;100(4):745–755. doi: 10.1242/dev.100.4.745. [DOI] [PubMed] [Google Scholar]
  21. Jermyn K. A., Williams J. G. An analysis of culmination in Dictyostelium using prestalk and stalk-specific cell autonomous markers. Development. 1991 Mar;111(3):779–787. doi: 10.1242/dev.111.3.779. [DOI] [PubMed] [Google Scholar]
  22. Kimmel A. R., Firtel R. A. Intervening sequences in a Dictyostelium gene that encodes a low abundance class mRNA. Nucleic Acids Res. 1980 Dec 11;8(23):5599–5610. doi: 10.1093/nar/8.23.5599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kuwayama H., Ecke M., Gerisch G., Van Haastert P. J. Protection against osmotic stress by cGMP-mediated myosin phosphorylation. Science. 1996 Jan 12;271(5246):207–209. doi: 10.1126/science.271.5246.207. [DOI] [PubMed] [Google Scholar]
  24. Kwon H. M., Handler J. S. Cell volume regulated transporters of compatible osmolytes. Curr Opin Cell Biol. 1995 Aug;7(4):465–471. doi: 10.1016/0955-0674(95)80002-6. [DOI] [PubMed] [Google Scholar]
  25. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  26. Leiting B., Noegel A. Construction of an extrachromosomally replicating transformation vector for Dictyostelium discoideum. Plasmid. 1988 Nov;20(3):241–248. doi: 10.1016/0147-619x(88)90030-3. [DOI] [PubMed] [Google Scholar]
  27. Lukat G. S., McCleary W. R., Stock A. M., Stock J. B. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):718–722. doi: 10.1073/pnas.89.2.718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Maeda T., Takekawa M., Saito H. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science. 1995 Jul 28;269(5223):554–558. doi: 10.1126/science.7624781. [DOI] [PubMed] [Google Scholar]
  29. Maeda T., Wurgler-Murphy S. M., Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature. 1994 May 19;369(6477):242–245. doi: 10.1038/369242a0. [DOI] [PubMed] [Google Scholar]
  30. Mager W. H., Varela J. C. Osmostress response of the yeast Saccharomyces. Mol Microbiol. 1993 Oct;10(2):253–258. [PubMed] [Google Scholar]
  31. Mizuno T., Wurtzel E. T., Inouye M. Cloning of the regulatory genes (ompR and envZ) for the matrix proteins of the Escherichia coli outer membrane. J Bacteriol. 1982 Jun;150(3):1462–1466. doi: 10.1128/jb.150.3.1462-1466.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mizuno T., Wurtzel E. T., Inouye M. Osmoregulation of gene expression. II. DNA sequence of the envZ gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem. 1982 Nov 25;257(22):13692–13698. [PubMed] [Google Scholar]
  33. Nagasawa S., Tokishita S., Aiba H., Mizuno T. A novel sensor-regulator protein that belongs to the homologous family of signal-transduction proteins involved in adaptive responses in Escherichia coli. Mol Microbiol. 1992 Mar;6(6):799–807. doi: 10.1111/j.1365-2958.1992.tb01530.x. [DOI] [PubMed] [Google Scholar]
  34. Newell P. C., Telser A., Sussman M. Alternative developmental pathways determined by environmental conditions in the cellular slime mold Dictyostelium discoideum. J Bacteriol. 1969 Nov;100(2):763–768. doi: 10.1128/jb.100.2.763-768.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Noegel A., Gerisch G., Stadler J., Westphal M. Complete sequence and transcript regulation of a cell adhesion protein from aggregating Dictyostelium cells. EMBO J. 1986 Jul;5(7):1473–1476. doi: 10.1002/j.1460-2075.1986.tb04384.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Noegel A., Harloff C., Hirth P., Merkl R., Modersitzki M., Stadler J., Weinhart U., Westphal M., Gerisch G. Probing an adhesion mutant of Dictyostelium discoideum with cDNA clones and monoclonal antibodies indicates a specific defect in the contact site A glycoprotein. EMBO J. 1985 Dec 30;4(13B):3805–3810. doi: 10.1002/j.1460-2075.1985.tb04151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Noegel A., Welker D. L., Metz B. A., Williams K. L. Presence of nuclear associated plasmids in the lower eukaryote Dictyostelium discoideum. J Mol Biol. 1985 Sep 20;185(2):447–450. doi: 10.1016/0022-2836(85)90416-4. [DOI] [PubMed] [Google Scholar]
  38. Ota I. M., Varshavsky A. A yeast protein similar to bacterial two-component regulators. Science. 1993 Oct 22;262(5133):566–569. doi: 10.1126/science.8211183. [DOI] [PubMed] [Google Scholar]
  39. Parkinson J. S., Kofoid E. C. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. doi: 10.1146/annurev.ge.26.120192.000443. [DOI] [PubMed] [Google Scholar]
  40. Rudolph J., Tolliday N., Schmitt C., Schuster S. C., Oesterhelt D. Phosphorylation in halobacterial signal transduction. EMBO J. 1995 Sep 1;14(17):4249–4257. doi: 10.1002/j.1460-2075.1995.tb00099.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schulkes C., Schaap P. cAMP-dependent protein kinase activity is essential for preaggregative gene expression in Dictyostelium. FEBS Lett. 1995 Jul 17;368(2):381–384. doi: 10.1016/0014-5793(95)00676-z. [DOI] [PubMed] [Google Scholar]
  42. Segall J. E., Kuspa A., Shaulsky G., Ecke M., Maeda M., Gaskins C., Firtel R. A., Loomis W. F. A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol. 1995 Feb;128(3):405–413. doi: 10.1083/jcb.128.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sharp P. M., Devine K. M. Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do 'prefer' optimal codons. Nucleic Acids Res. 1989 Jul 11;17(13):5029–5039. doi: 10.1093/nar/17.13.5029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Swanson R. V., Schuster S. C., Simon M. I. Expression of CheA fragments which define domains encoding kinase, phosphotransfer, and CheY binding activities. Biochemistry. 1993 Aug 3;32(30):7623–7629. doi: 10.1021/bi00081a004. [DOI] [PubMed] [Google Scholar]
  45. Wang N., Shaulsky G., Escalante R., Loomis W. F. A two-component histidine kinase gene that functions in Dictyostelium development. EMBO J. 1996 Aug 1;15(15):3890–3898. [PMC free article] [PubMed] [Google Scholar]
  46. Witke W., Schleicher M., Noegel A. A. Redundancy in the microfilament system: abnormal development of Dictyostelium cells lacking two F-actin cross-linking proteins. Cell. 1992 Jan 10;68(1):53–62. doi: 10.1016/0092-8674(92)90205-q. [DOI] [PubMed] [Google Scholar]

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