Literature DB >> 7937993

Expression of cAMP-dependent protein kinase in prespore cells is sufficient to induce spore cell differentiation in Dictyostelium.

S K Mann1, D L Richardson, S Lee, A R Kimmel, R A Firtel.   

Abstract

The activity of cAMP-dependent protein kinase (PKA) is required for proper development at several stages during the Dictyostelium life cycle. We present evidence that activation of PKA is rate-limiting for the differentiation of prespore cells to spores and that PKA activation may be the developmental trigger for sporulation. Strains that overexpress the gene encoding the catalytic subunit of PKA (PKAcat) or lack a functional regulatory subunit (rdeC strains) undergo rapid, heterochronic development. We show that overexpression of PKAcat in prespore cell is sufficient to directly induce expression of the spore maturation marker spiA and differentiation to spores, in a cell-autonomous manner. Moreover, overexpression of PKAcat in prespore cells can bypass a mutation that blocks an earlier developmental step to induce spiA expression. Our results suggest that the regulatory pathway in prespore cells between the activation of PKA and spiA induction/spore maturation is quite short and that PKAcat expression in prespore cells may mediate spore differentiation at the level of transcription. This induction of sporulation requires the prior activation of the prespore cell pathway. In addition, we show that beta-galactosidase activity expressed from a PKAcat promoter/lacZ reporter construct is highly enriched in the anterior prestalk A region during the tipped aggregate, slug, and early culminant stages and that this pattern switches abruptly to a prespore pattern at the time of spore maturation, supporting the proposed role of PKA in this process.

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Year:  1994        PMID: 7937993      PMCID: PMC45061          DOI: 10.1073/pnas.91.22.10561

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

1.  Analysis of a spatially regulated phosphotyrosine phosphatase identifies tyrosine phosphorylation as a key regulatory pathway in Dictyostelium.

Authors:  P K Howard; B M Sefton; R A Firtel
Journal:  Cell       Date:  1992-11-13       Impact factor: 41.582

2.  Multiple roles for cAMP-dependent protein kinase during Dictyostelium development.

Authors:  A J Harwood; N A Hopper; M N Simon; S Bouzid; M Veron; J G Williams
Journal:  Dev Biol       Date:  1992-01       Impact factor: 3.582

3.  A developmentally regulated, putative serine/threonine protein kinase is essential for development in Dictyostelium.

Authors:  S K Mann; R A Firtel
Journal:  Mech Dev       Date:  1991-09       Impact factor: 1.882

Review 4.  Transmembrane signal transduction pathways in Dictyostelium.

Authors:  P J Van Haastert
Journal:  Adv Second Messenger Phosphoprotein Res       Date:  1991

5.  Cyclic AMP regulation of early gene expression in Dictyostelium discoideum: mediation via the cell surface cyclic AMP receptor.

Authors:  S K Mann; R A Firtel
Journal:  Mol Cell Biol       Date:  1987-01       Impact factor: 4.272

6.  Conditions that elevate intracellular cyclic AMP levels promote spore formation in Dictyostelium.

Authors:  B B Riley; B R Jensen; S L Barclay
Journal:  Differentiation       Date:  1989-07       Impact factor: 3.880

7.  A cytosolic cyclic AMP-dependent protein kinase in Dictyostelium discoideum. I. Properties.

Authors:  I H Majerfeld; B H Leichtling; J A Meligeni; E Spitz; H V Rickenberg
Journal:  J Biol Chem       Date:  1984-01-10       Impact factor: 5.157

8.  A cAMP-dependent protein kinase is present in differentiating Dictyostelium discoideum cells.

Authors:  J Gunzburg; M Veron
Journal:  EMBO J       Date:  1982       Impact factor: 11.598

9.  Overexpression of Dd PK2 protein kinase causes rapid development and affects the intracellular cAMP pathway of Dictyostelium discoideum.

Authors:  C Anjard; S Pinaud; R R Kay; C D Reymond
Journal:  Development       Date:  1992-07       Impact factor: 6.868

10.  Induction of terminal differentiation of Dictyostelium by cAMP-dependent protein kinase and opposing effects of intracellulr and extracellular cAMP on stalk cell differentiation.

Authors:  N A Hopper; C Anjard; C D Reymond; J G Williams
Journal:  Development       Date:  1993-09       Impact factor: 6.868

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  19 in total

Review 1.  cAMP signaling in Dictyostelium. Complexity of cAMP synthesis, degradation and detection.

Authors:  Shweta Saran; Marcel E Meima; Elisa Alvarez-Curto; Karin E Weening; Daniel E Rozen; Pauline Schaap
Journal:  J Muscle Res Cell Motil       Date:  2002       Impact factor: 2.698

2.  An intersection of the cAMP/PKA and two-component signal transduction systems in Dictyostelium.

Authors:  P A Thomason; D Traynor; G Cavet; W T Chang; A J Harwood; R R Kay
Journal:  EMBO J       Date:  1998-05-15       Impact factor: 11.598

Review 3.  Genetic networks that regulate development in Dictyostelium cells.

Authors:  W F Loomis
Journal:  Microbiol Rev       Date:  1996-03

4.  A two-component histidine kinase gene that functions in Dictyostelium development.

Authors:  N Wang; G Shaulsky; R Escalante; W F Loomis
Journal:  EMBO J       Date:  1996-08-01       Impact factor: 11.598

5.  Evidence that a combined activator-repressor protein regulates Dictyostelium stalk cell differentiation.

Authors:  T Kawata; A Early; J Williams
Journal:  EMBO J       Date:  1996-06-17       Impact factor: 11.598

6.  Constitutively active protein kinase A disrupts motility and chemotaxis in Dictyostelium discoideum.

Authors:  Hui Zhang; Paul J Heid; Deborah Wessels; Karla J Daniels; Tien Pham; William F Loomis; David R Soll
Journal:  Eukaryot Cell       Date:  2003-02

7.  Identification and characterization of DdPDE3, a cGMP-selective phosphodiesterase from Dictyostelium.

Authors:  H Kuwayama; H Snippe; M Derks; J Roelofs; P J Van Haastert
Journal:  Biochem J       Date:  2001-02-01       Impact factor: 3.857

Review 8.  Role of PKA in the timing of developmental events in Dictyostelium cells.

Authors:  W F Loomis
Journal:  Microbiol Mol Biol Rev       Date:  1998-09       Impact factor: 11.056

9.  G{alpha}5 subunit-mediated signalling requires a D-motif and the MAPK ERK1 in Dictyostelium.

Authors:  Brent Raisley; Hoai-Nghia Nguyen; Jeffrey A Hadwiger
Journal:  Microbiology (Reading)       Date:  2009-12-17       Impact factor: 2.777

10.  Loss of cAMP-specific phosphodiesterase rescues spore development in G protein mutant in dictyostelium.

Authors:  David J Schwebs; Hoai-Nghia Nguyen; Jamison A Miller; Jeffrey A Hadwiger
Journal:  Cell Signal       Date:  2014-02       Impact factor: 4.315

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