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PMID: 8280098 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Phospholipase C in Dictyostelium discoideum. Identification of stimulatory and inhibitory surface receptors and G-proteins.

The Biochemical journal ·Vol. 297 ( Pt 1) ·1994-01-01 ·Pages 189-93

Bominaar AA, Van Haastert PJ

Abstract

A combined biochemical and genetic approach was used to show that phospholipase C in the cellular slime mould Dictyostelium is under dual regulation by the chemoattractant cyclic AMP (cAMP). This dual regulation involves stimulatory and inhibitory surface receptors and G-proteins. In wild-type cells both cAMP and guanosine 5'-[gamma-thio]triphosphate (GTP[S]) stimulated phospholipase C. In contrast, mutant fgd A, lacking the G-protein alpha-subunit G alpha 2, showed no stimulation by either cAMP or GTP[S], indicating that G alpha 2 is the stimulatory G-protein. In mutant fgd C cAMP did not stimulate phospholipase C, but stimulation by GTP[S] was normal, suggesting that the defect in this mutant is upstream of the stimulatory G alpha 2. Inhibition of phospholipase C was achieved in wild-type cells by the partial antagonist 3'-deoxy-3'-aminoadenosine 3',5'-phosphate (3'NH-cAMP). This inhibition was no longer observed in transformed cell lines lacking either the surface cAMP receptor cAR1 or the G-protein alpha-subunit G alpha 1; in these cells the agonist cAMP still activated phospholipase C. These results indicate that Dictyostelium phospholipase C is regulated via a stimulatory and an inhibitory pathway. The inhibitory pathway is composed of the surface receptor cAR1 and the G-protein G1. The stimulatory pathway consists of an unknown cAMP receptor (possibly the fgd C gene product) and the G-protein G2.

MeSH Terms
Animals Cyclic AMP/analogs & derivatives,pharmacology Dictyostelium/enzymology,genetics Enzyme Activation/drug effects GTP-Binding Proteins/physiology Guanosine 5'-O-(3-Thiotriphosphate)/pharmacology Inositol 1,4,5-Trisphosphate/metabolism Inositol Polyphosphate 5-Phosphatases Mutation Phosphoric Monoester Hydrolases/metabolism Receptors, Cyclic AMP/genetics,physiology Type C Phospholipases/antagonists & inhibitors,metabolism
Chemicals
Receptors, Cyclic AMP Guanosine 5'-O-(3-Thiotriphosphate) 3'-deoxy-3'aminocyclic-3',5'-AMP Inositol 1,4,5-Trisphosphate Cyclic AMP Phosphoric Monoester Hydrolases Inositol Polyphosphate 5-Phosphatases Type C Phospholipases GTP-Binding Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bominaar A A
Department of Biochemistry, University of Groningen, The Netherlands.
Van Haastert P J
References (39)
39 references, click to expand
  1. Adenylate cyclase activity in Dictyostelium discoideum amoebae and its changes during differentiation.
    FEBS Lett. 1976 Sep 15;68(1):125-8 PMID: 183985
  2. A soluble factor and GTP gamma S are required for Dictyostelium discoideum guanylate cyclase activity.
    Biochim Biophys Acta. 1992 Apr 30;1135(1):73-8 PMID: 1350467
  3. Regulation and function of G alpha protein subunits in Dictyostelium.
    Cell. 1989 Apr 21;57(2):265-75 PMID: 2539262
  4. A chemoattractant receptor controls development in Dictyostelium discoideum.
    Science. 1988 Sep 16;241(4872):1467-72 PMID: 3047871
  5. Guanine nucleotide-dependent inhibition of phospholipase C in human endothelial cells.
    J Biol Chem. 1990 May 15;265(14):7920-6 PMID: 1692318
  6. Studies of inositol phospholipid-specific phospholipase C.
    Science. 1989 May 5;244(4904):546-50 PMID: 2541501
  7. The cyclic nucleotide specificity of three cAMP receptors in Dictyostelium.
    J Biol Chem. 1992 Mar 5;267(7):4600-7 PMID: 1537842
  8. Molecular cloning and expression of a phosphoinositide-specific phospholipase C of Dictyostelium discoideum.
    J Biol Chem. 1992 Sep 15;267(26):18387-92 PMID: 1326523
  9. Gene targeting of the aggregation stage cAMP receptor cAR1 in Dictyostelium.
    Genes Dev. 1991 Apr;5(4):572-82 PMID: 1849108
  10. Dynamics and function of the inositolcycle in Dictyostelium discoideum.
    Dev Genet. 1991;12(1-2):19-24 PMID: 1646692
  11. Determination of inositol 1,4,5-trisphosphate levels in Dictyostelium by isotope dilution assay.
    Anal Biochem. 1989 Feb 15;177(1):115-9 PMID: 2545115
  12. RNA in cytoplasmic and nuclear fractions of cellular slime mold amebas.
    J Cell Biol. 1970 May;45(2):399-407 PMID: 5535143
  13. Protein kinase C phosphorylates human platelet inositol trisphosphate 5'-phosphomonoesterase, increasing the phosphatase activity.
    Cell. 1986 Sep 12;46(6):951-8 PMID: 3019558
  14. Structure and expression of the cAMP cell-surface receptor.
    Dev Genet. 1988;9(4-5):227-35 PMID: 3243022
  15. Selective induction of gene expression and second-messenger accumulation in Dictyostelium discoideum by the partial chemotactic antagonist 8-p-chlorophenylthioadenosine 3',5'-cyclic monophosphate.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9219-23 PMID: 11607223
  16. Chemoattractant and guanosine 5'-[gamma-thio]triphosphate induce the accumulation of inositol 1,4,5-trisphosphate in Dictyostelium cells that are labelled with [3H]inositol by electroporation.
    Biochem J. 1989 Mar 1;258(2):577-86 PMID: 2539811
  17. Dictyostelium transiently expresses eight distinct G-protein alpha-subunits during its developmental program.
    Biochem Biophys Res Commun. 1991 Sep 30;179(3):1141-7 PMID: 1930158
  18. Adenylate cyclase activity oscillations as signals for cell aggregation in Dictyostelium discoideum.
    Nature. 1977 Mar 17;266(5599):259-61 PMID: 191758
  19. Inhibition of inositol phospholipids metabolism and calcium mobilization by cyclic AMP-increasing agents and phorbol ester in neutrophils.
    Biochem Biophys Res Commun. 1986 Sep 30;139(3):1272-8 PMID: 3021152
  20. The regulation of adenylate cyclase by guanine nucleotides in Dictyostelium discoideum membranes.
    Eur J Biochem. 1987 Jan 15;162(2):251-8 PMID: 3100295
  21. Inositol tris- and polyphosphate formation during chemotaxis of Dictyostelium.
    J Cell Sci. 1989 Aug;93 ( Pt 4):585-92 PMID: 2558121
  22. Binding of cAMP and adenosine derivatives to Dictyostelium discoideum cells. Relationships of binding, chemotactic, and antagonistic activities.
    J Biol Chem. 1983 Aug 25;258(16):9643-8 PMID: 6309779
  23. Evidence that a guanine nucleotide-binding protein linked to a muscarinic receptor inhibits directly phospholipase C.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4889-93 PMID: 2162060
  24. Feedback regulation of phospholipase C-beta by protein kinase C.
    J Biol Chem. 1990 Oct 15;265(29):17941-5 PMID: 2211670
  25. Signal transduction in Dictyostelium fgd A mutants with a defective interaction between surface cAMP receptors and a GTP-binding regulatory protein.
    J Cell Biol. 1988 Aug;107(2):521-8 PMID: 2843545
  26. Identification of Dictyostelium G alpha genes expressed during multicellular development.
    Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8213-7 PMID: 1910174
  27. GTP analogues stimulate inositol trisphosphate formation transiently in Dictyostelium.
    J Cell Sci. 1987 May;87 ( Pt 4):513-8 PMID: 2821029
  28. Multiple alpha subunits of guanine nucleotide-binding proteins in Dictyostelium.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):4892-6 PMID: 2500658
  29. 3':5'-cyclic AMP-dependent 3':5'-cyclic GMP accumulation in Dictyostelium discoideum.
    Proc Natl Acad Sci U S A. 1977 Jun;74(6):2348-51 PMID: 196287
  30. Abberant chemotaxis and differentiation in Dictyostelium mutant fgdC with a defective regulation of receptor-stimulated phosphoinositidase C.
    J Cell Sci. 1991 Dec;100 ( Pt 4):825-31 PMID: 1667662
  31. Regulation of D-myo-inositol 1,4,5-trisphosphate 3-kinase by cAMP-dependent protein kinase and protein kinase C.
    J Biol Chem. 1990 Jun 25;265(18):10367-72 PMID: 2162347
  32. An islet activating protein-sensitive G protein is involved in dopamine inhibition of angiotensin and thyrotropin-releasing hormone-stimulated inositol phosphate production in anterior pituitary cells.
    J Biol Chem. 1987 Nov 5;262(31):15106-10 PMID: 3117793
  33. Inositol phosphates and cell signalling.
    Nature. 1989 Sep 21;341(6239):197-205 PMID: 2550825
  34. Regulatory properties of magnesium-dependent guanylate cyclase in Dictyostelium discoideum membranes.
    J Biol Chem. 1989 Mar 15;264(8):4329-35 PMID: 2564393
  35. Surface receptor-mediated activation of adenylate cyclase in Dictyostelium. Regulation by guanine nucleotides in wild-type cells and aggregation deficient mutants.
    J Biol Chem. 1986 Nov 15;261(32):15121-5 PMID: 3771567
  36. Phospholipase C in Dictyostelium discoideum. Cyclic AMP surface receptor and G-protein-regulated activity in vitro.
    Biochem J. 1994 Jan 1;297 ( Pt 1):181-7 PMID: 8280097
  37. A novel, specific binding protein assay for quantitation of intracellular inositol 1,3,4,5-tetrakisphosphate (InsP4) using a high-affinity InsP4 receptor from cerebellum.
    FEBS Lett. 1989 Aug 28;254(1-2):155-8 PMID: 2550275
  38. Cyclic 3',5' AMP relay in Dictyostelium discoideum. II. Requirements for the initiation and termination of the response.
    J Cell Biol. 1979 Feb;80(2):300-9 PMID: 222770
  39. Molecular insights into eukaryotic chemotaxis.
    FASEB J. 1991 Dec;5(15):3078-85 PMID: 1743439
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1994-01-01
Pages
189-93
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1137809
Subset
IM
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