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PMID: 10373524 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

SDF-2 induction of terminal differentiation in Dictyostelium discoideum is mediated by the membrane-spanning sensor kinase DhkA.

Molecular and cellular biology ·Vol. 19 ·No. 7 ·1999-07-00 ·Pages 4750-6

Wang N, Söderbom F, Anjard C, Shaulsky G, Loomis WF

Abstract

SDF-2 is a peptide released by prestalk cells during culmination that stimulates prespore cells to encapsulate. Genetic evidence indicates that the response is dependent on the dhkA gene. This gene encodes a member of the histidine kinase family of genes that functions in two-component signal transduction pathways. The sequence of the N-terminal half of DhkA predicts two hydrophobic domains separated by a 310-amino-acid loop that could bind a ligand. By inserting MYC6 epitopes into DhkA, we were able to show that the loop is extracellular while the catalytic domain is cytoplasmic. Cells expressing the MYC epitope in the extracellular domain of DhkA were found to respond only if induced with 100-fold-higher levels of SDF-2 than required to induce dhkA+ cells; however, they could be induced to sporulate by addition of antibodies specific to the MYC epitope. To examine the enzymatic activity of DhkA, we purified the catalytic domain following expression in bacteria and observed incorporation of labelled phosphate from ATP consistent with histidine autophosphorylation. Site-directed mutagenesis of histidine1395 to glutamine in the catalytic domain blocked autophosphorylation. Furthermore, genetic analyses showed that histidine1395 and the relay aspartate2075 of DhkA are both critical to its function but that another histidine kinase, DhkB, can partially compensate for the lack of DhkA activity. Sporulation is drastically reduced in double mutants lacking both DhkA and DhkB. Suppressor studies indicate that the cyclic AMP (cAMP) phosphodiesterase RegA and the cAMP-dependent protein kinase PKA act downstream of DhkA.

MeSH Terms
Animals Catalytic Domain Cell Differentiation Cell Membrane/enzymology,metabolism Dictyostelium/drug effects,metabolism,physiology Intercellular Signaling Peptides and Proteins Membrane Proteins/genetics,metabolism Mutagenesis, Site-Directed Peptides Phosphorylation Protein Kinases/genetics,metabolism Proteins/metabolism,pharmacology Protozoan Proteins Recombinant Fusion Proteins/genetics,metabolism
Chemicals
Intercellular Signaling Peptides and Proteins Membrane Proteins Peptides Proteins Protozoan Proteins Recombinant Fusion Proteins SDF-2 protein, Dictyostelium discoideum Protein Kinases DhkA protein, Dictyostelium discoideum DhkB protein, Dictyostelium discoideum
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wang N
Center for Molecular Genetics, Department of Biology, University of California-San Diego, La Jolla, California 92093, USA.
Söderbom F
Anjard C
Shaulsky G
Loomis W F
References (40)
40 references, click to expand
  1. Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase.
    Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3416-21 PMID: 8622950
  2. Initial cell type divergence in Dictyostelium is independent of DIF-1.
    Dev Biol. 1996 Mar 15;174(2):214-20 PMID: 8631494
  3. A two-component histidine kinase gene that functions in Dictyostelium development.
    EMBO J. 1996 Aug 1;15(15):3890-8 PMID: 8670894
  4. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor.
    Cell. 1996 Sep 20;86(6):865-75 PMID: 8808622
  5. Genetic networks that regulate development in Dictyostelium cells.
    Microbiol Rev. 1996 Mar;60(1):135-50 PMID: 8852898
  6. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction.
    Science. 1996 Nov 8;274(5289):982-5 PMID: 8875940
  7. Developmental signal transduction pathways uncovered by genetic suppressors.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15260-5 PMID: 8986798
  8. Sorting of the initial cell types in Dictyostelium is dependent on the tipA gene.
    Dev Biol. 1997 May 1;185(1):34-41 PMID: 9169048
  9. Histidine kinases in signal transduction pathways of eukaryotes.
    J Cell Sci. 1997 May;110 ( Pt 10):1141-5 PMID: 9191038
  10. Signal transduction pathways leading to spore differentiation in Dictyostelium discoideum.
    Dev Biol. 1998 Jan 15;193(2):146-55 PMID: 9473320
  11. A cAMP-phosphodiesterase controls PKA-dependent differentiation.
    Development. 1998 Feb;125(4):691-9 PMID: 9435289
  12. CD40 ligation and IL-4 use different mechanisms of transcriptional activation of the human lymphotoxin alpha promoter in B cells.
    Eur J Immunol. 1998 Mar;28(3):901-6 PMID: 9541585
  13. Intracellular signal transduction mediated by ligation of MHC class I molecules.
    Tissue Antigens. 1998 Mar;51(3):215-23 PMID: 9550321
  14. The hybrid histidine kinase dhkB regulates spore germination in Dictyostelium discoideum.
    Dev Biol. 1998 Apr 15;196(2):171-83 PMID: 9576830
  15. An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium.
    EMBO J. 1998 May 15;17(10):2838-45 PMID: 9582277
  16. Production and activity of spore differentiation factors (SDFs) in Dictyostelium.
    Development. 1998 Oct;125(20):4067-75 PMID: 9735367
  17. A new class of rapidly developing mutants in Dictyostelium discoideum: implications for cyclic AMP metabolism and cell differentiation.
    Dev Biol. 1983 Jan;95(1):200-10 PMID: 6298035
  18. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli.
    Proc Natl Acad Sci U S A. 1986 Aug;83(16):5909-13 PMID: 2874557
  19. Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors.
    Mol Cell Biol. 1986 Nov;6(11):3973-83 PMID: 3025622
  20. Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions.
    Methods Cell Biol. 1987;28:9-29 PMID: 3298997
  21. Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC.
    Proc Natl Acad Sci U S A. 1988 Jul;85(14):4976-80 PMID: 2839825
  22. Growth factor receptor tyrosine kinases.
    Annu Rev Biochem. 1988;57:443-78 PMID: 3052279
  23. Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis.
    Nature. 1988 Nov 10;336(6195):139-43 PMID: 3185734
  24. RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli.
    J Bacteriol. 1990 Feb;172(2):659-69 PMID: 2404948
  25. cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes.
    Annu Rev Biochem. 1990;59:971-1005 PMID: 2165385
  26. A prespore gene, Dd31, expressed during culmination of Dictyostelium discoideum.
    Dev Biol. 1991 Apr;144(2):269-80 PMID: 2010032
  27. Signal transduction pathways involving protein phosphorylation in prokaryotes.
    Annu Rev Biochem. 1991;60:401-41 PMID: 1883200
  28. Mutation of protein kinase A causes heterochronic development of Dictyostelium.
    Nature. 1992 Mar 12;356(6365):171-2 PMID: 1312226
  29. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8803-7 PMID: 1326764
  30. Overexpression of Dd PK2 protein kinase causes rapid development and affects the intracellular cAMP pathway of Dictyostelium discoideum.
    Development. 1992 Jul;115(3):785-90 PMID: 1330484
  31. The phosphorelay signal transduction pathway in the initiation of Bacillus subtilis sporulation.
    J Cell Biochem. 1993 Jan;51(1):55-61 PMID: 8432743
  32. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.
    Science. 1993 Oct 22;262(5133):539-44 PMID: 8211181
  33. Cell type regulation in response to expression of ricin A in Dictyostelium.
    Dev Biol. 1993 Nov;160(1):85-98 PMID: 8224551
  34. A two-component system that regulates an osmosensing MAP kinase cascade in yeast.
    Nature. 1994 May 19;369(6477):242-5 PMID: 8183345
  35. Protein histidine kinases and signal transduction in prokaryotes and eukaryotes.
    Trends Genet. 1994 Apr;10(4):133-8 PMID: 8029829
  36. Cross-linking CD40 on B cells rapidly activates nuclear factor-kappa B.
    J Immunol. 1994 Nov 15;153(10):4357-66 PMID: 7525701
  37. A multidrug resistance transporter/serine protease gene is required for prestalk specialization in Dictyostelium.
    Genes Dev. 1995 May 1;9(9):1111-22 PMID: 7744252
  38. Progression of an inductive signal activates sporulation in Dictyostelium discoideum.
    Development. 1994 Oct;120(10):2891-900 PMID: 7607079
  39. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor.
    Science. 1995 Jul 28;269(5223):554-8 PMID: 7624781
  40. The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium.
    EMBO J. 1996 Aug 1;15(15):3880-9 PMID: 8670893
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1999-07-00
Pages
4750-6
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC84273
Subset
IM
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