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PMID: 8139539 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Acetylcholine muscarinic m1 receptor regulation of cyclic AMP synthesis controls growth factor stimulation of Raf activity.

Molecular and cellular biology ·Vol. 14 ·No. 4 ·1994-04-00 ·Pages 2343-51

Russell M, Winitz S, Johnson GL

Abstract

Acetylcholine muscarinic m2 receptors (m2R) couple to heterotrimeric Gi proteins and activate the Ras/Raf/mitogen-activated protein kinase pathway and phosphatidylinositol 3-kinase in Rat 1a cells. In contrast to the m2R, stimulation of the acetylcholine muscarinic m1 receptor (m1R) does not activate the Ras/Raf/mitogen-activated protein kinase regulatory pathway in Rat 1a cells but rather causes a pronounced inhibition of epidermal growth factor and platelet-derived growth factor receptor activation of Raf. In Rat 1a cells, m1R stimulation of phospholipase C beta and the marked rise in intracellular calcium stimulated cyclic AMP (cAMP) synthesis, resulting in the activation of protein kinase A. Stimulation of protein kinase A inhibited Raf activation in response to growth factors. Platelet-derived growth factor receptor stimulation of phosphatidylinositol 3-kinase activity was not affected by either m1R stimulation or protein kinase A activation in response to forskolin-stimulated cAMP synthesis. GTP loading of Ras in response to growth factors was unaffected by protein kinase A activation but was partially inhibited by carbachol stimulation of the m1R. Therefore, protein kinase A action at the Ras/Raf activation interface selectively inhibited only one branch of the signal transduction network initiated by tyrosine kinases. Specific adenylyl cyclases responding to different signals, including calcium, with enhanced cAMP synthesis will regulate Raf activation in response to Ras.GTP. Taken together, the data indicate that G protein-coupled receptors can positively and negatively regulate the responsiveness of tyrosine kinase-stimulated mitogenic response pathways.

MeSH Terms
Adenylyl Cyclases/metabolism Animals Atropine/pharmacology Calcium-Calmodulin-Dependent Protein Kinases/metabolism Carbachol/pharmacology Cell Line Colforsin/pharmacology Cyclic AMP/metabolism Cyclic AMP-Dependent Protein Kinases/metabolism Enzyme Activation Epidermal Growth Factor/pharmacology ErbB Receptors/drug effects,physiology GTP-Binding Proteins/metabolism Gene Expression Guanosine Triphosphate/pharmacology Kinetics Models, Biological Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor)/metabolism Platelet-Derived Growth Factor/pharmacology Protein Serine-Threonine Kinases/metabolism Proto-Oncogene Proteins/drug effects,metabolism Proto-Oncogene Proteins c-raf Rats Receptor Protein-Tyrosine Kinases/metabolism Receptors, Muscarinic/biosynthesis,physiology Receptors, Platelet-Derived Growth Factor/drug effects,physiology Transfection
Chemicals
Platelet-Derived Growth Factor Proto-Oncogene Proteins Receptors, Muscarinic Colforsin Epidermal Growth Factor Atropine Guanosine Triphosphate Carbachol Cyclic AMP Phosphotransferases (Alcohol Group Acceptor) ErbB Receptors Receptor Protein-Tyrosine Kinases Receptors, Platelet-Derived Growth Factor Protein Serine-Threonine Kinases Proto-Oncogene Proteins c-raf Cyclic AMP-Dependent Protein Kinases Calcium-Calmodulin-Dependent Protein Kinases GTP-Binding Proteins Adenylyl Cyclases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Russell M
Division of Basic Sciences, National Jewish Center for Immunology and Respiratory Medicine, Denver, Colorado 80206.
Winitz S
Johnson G L
References (40)
40 references, click to expand
  1. Calcium and muscarinic agonist stimulation of type I adenylylcyclase in whole cells.
    J Biol Chem. 1992 Jun 25;267(18):12440-2 PMID: 1319996
  2. Inhibition by cAMP of Ras-dependent activation of Raf.
    Science. 1993 Nov 12;262(5136):1069-72 PMID: 7694367
  3. 95-kilodalton B-Raf serine/threonine kinase: identification of the protein and its major autophosphorylation site.
    Mol Cell Biol. 1992 Sep;12(9):3733-42 PMID: 1508179
  4. Adenylyl cyclases.
    Cell. 1992 Sep 18;70(6):869-72 PMID: 1525824
  5. The primary structure of MEK, a protein kinase that phosphorylates the ERK gene product.
    Science. 1992 Oct 16;258(5081):478-80 PMID: 1411546
  6. Phosphatidylinositol 3-kinase: a novel effector.
    Cell Growth Differ. 1992 Oct;3(10):747-52 PMID: 1332743
  7. Stimulation of specific types of Gs-stimulated adenylyl cyclases by phorbol ester treatment.
    J Biol Chem. 1993 Feb 25;268(6):3829-32 PMID: 8440678
  8. A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf.
    Science. 1993 Apr 16;260(5106):315-9 PMID: 8385802
  9. Phospholipase C-gamma 1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal.
    Cell. 1993 Apr 23;73(2):321-34 PMID: 7682895
  10. Epitope-tagged Gq alpha subunits: expression of GTPase-deficient alpha subunits persistently stimulates phosphatidylinositol-specific phospholipase C but not mitogen-activated protein kinase activity regulated by the M1 muscarinic acetylcholine receptor.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4077-81 PMID: 7683419
  11. Selective coupling of the human anaphylatoxin C5a receptor and alpha 16 in human kidney 293 cells.
    FEBS Lett. 1993 May 24;323(1-2):132-4 PMID: 8388335
  12. Receptor stimulated accumulation of phosphatidylinositol (3,4,5)-trisphosphate by G-protein mediated pathways in human myeloid derived cells.
    EMBO J. 1993 Jun;12(6):2265-73 PMID: 8389691
  13. Inhibition of cloned adenylyl cyclases by mutant-activated Gi-alpha and specific suppression of type 2 adenylyl cyclase inhibition by phorbol ester treatment.
    J Biol Chem. 1993 Jun 15;268(17):12253-6 PMID: 8389756
  14. Complex formation between RAS and RAF and other protein kinases.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6213-7 PMID: 8327501
  15. Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1.
    Nature. 1993 Jul 22;364(6435):308-13 PMID: 8332187
  16. Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro.
    Nature. 1993 Jul 22;364(6435):352-5 PMID: 8332195
  17. Mammalian Ras interacts directly with the serine/threonine kinase Raf.
    Cell. 1993 Jul 16;74(1):205-14 PMID: 8334704
  18. Synthesis of phosphatidylinositol 3,4,5-trisphosphate in permeabilized neutrophils regulated by receptors and G-proteins.
    J Biol Chem. 1993 Aug 15;268(23):17162-72 PMID: 8394332
  19. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase by G protein and tyrosine kinase oncoproteins.
    J Biol Chem. 1993 Aug 25;268(24):17896-901 PMID: 8394352
  20. Involvement of Ras and Raf in the Gi-coupled acetylcholine muscarinic m2 receptor activation of mitogen-activated protein (MAP) kinase kinase and MAP kinase.
    J Biol Chem. 1993 Sep 15;268(26):19196-9 PMID: 8396128
  21. cAMP antagonizes p21ras-directed activation of extracellular signal-regulated kinase 2 and phosphorylation of mSos nucleotide exchange factor.
    EMBO J. 1993 Nov;12(11):4211-20 PMID: 8223435
  22. Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinase.
    J Biol Chem. 1977 Jul 25;252(14):4888-94 PMID: 194899
  23. Inositol trisphosphate, a novel second messenger in cellular signal transduction.
    Nature. 1984 Nov 22-28;312(5992):315-21 PMID: 6095092
  24. A potent synthetic peptide inhibitor of the cAMP-dependent protein kinase.
    J Biol Chem. 1986 Jan 25;261(3):989-92 PMID: 3511044
  25. Inositol 1,4,5-trisphosphate and inositol 1,2-cyclic 4,5-trisphosphate are minor components of total mass of inositol trisphosphate in thrombin-stimulated platelets. Rapid formation of inositol 1,3,4-trisphosphate.
    J Biol Chem. 1987 Dec 25;262(36):17268-71 PMID: 2826415
  26. Detection of nerve growth factor and epidermal growth factor-regulated protein kinases in PC12 cells with synthetic peptide substrates.
    Mol Pharmacol. 1989 Mar;35(3):331-8 PMID: 2784535
  27. Mutation of glycine 49 to valine in the alpha subunit of GS results in the constitutive elevation of cyclic AMP synthesis.
    Biochemistry. 1989 May 30;28(11):4547-51 PMID: 2548581
  28. A transfected m1 muscarinic acetylcholine receptor stimulates adenylate cyclase via phosphatidylinositol hydrolysis.
    J Biol Chem. 1989 Dec 5;264(34):20356-62 PMID: 2555356
  29. Thrombin-dependent association of phosphatidylinositol-3 kinase with p60c-src and p59fyn in human platelets.
    Mol Cell Biol. 1990 Jul;10(7):3806-9 PMID: 2162481
  30. Platelet-derived growth factor stimulates formation of active p21ras.GTP complex in Swiss mouse 3T3 cells.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5993-7 PMID: 2198577
  31. Reconstitutively active G protein-coupled receptors purified from baculovirus-infected insect cells.
    J Biol Chem. 1991 Jan 5;266(1):519-27 PMID: 1845979
  32. Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase.
    J Biol Chem. 1991 Aug 15;266(23):15277-85 PMID: 1651323
  33. Biophysical properties and microfilament assembly in neutrophils: modulation by cyclic AMP.
    J Cell Biol. 1991 Sep;114(6):1179-90 PMID: 1716633
  34. MAP kinase is constitutively activated in gip2 and src transformed rat 1a fibroblasts.
    J Biol Chem. 1992 Apr 25;267(12):7987-90 PMID: 1314814
  35. Reconstitution of agonist-stimulated phosphatidylinositol 4,5-bisphosphate hydrolysis using purified m1 muscarinic receptor, Gq/11, and phospholipase C-beta 1.
    J Biol Chem. 1992 Apr 25;267(12):8081-8 PMID: 1341877
  36. GTPase-activating protein and phosphatidylinositol 3-kinase bind to distinct regions of the platelet-derived growth factor receptor beta subunit.
    Mol Cell Biol. 1992 Jun;12(6):2534-44 PMID: 1375321
  37. Protein kinase A antagonizes platelet-derived growth factor-induced signaling by mitogen-activated protein kinase in human arterial smooth muscle cells.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10300-4 PMID: 7694289
  38. Increasing cAMP attenuates activation of mitogen-activated protein kinase.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10305-9 PMID: 7694290
  39. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3',5'-monophosphate.
    Science. 1993 Nov 12;262(5136):1065-9 PMID: 7694366
  40. Raf-1 activates MAP kinase-kinase.
    Nature. 1992 Jul 30;358(6385):417-21 PMID: 1322500
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1994-04-00
Pages
2343-51
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC358601
Subset
IM
Grants
NCI NIH HHS · CA09313 · United States
NIDDK NIH HHS · DK37871 · United States
NIGMS NIH HHS · GM30324 · United States
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