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Journal of Pharmacology and Experimental Therapeutics

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Research ArticleCARDIOVASCULAR

Modulation of Cyclic AMP Production by Signal Transduction Pathways in Preglomerular Microvessels and Microvascular Smooth Muscle Cells

Travis C. Jackson, Zaichuan Mi and Edwin K. Jackson
Journal of Pharmacology and Experimental Therapeutics July 2004, 310 (1) 349-358; DOI: https://doi.org/10.1124/jpet.103.063081
Travis C. Jackson
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Zaichuan Mi
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Edwin K. Jackson
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Abstract

Cyclic AMP affects microvascular smooth muscle contraction and growth. Therefore, it is important to elucidate mechanisms regulating cyclic AMP production in microvascular smooth muscle. In this study, we determined whether several signal transduction pathways regulate receptor-induced cyclic AMP in isolated preglomerular microvessels and microvascular smooth muscle cells. Preglomerular microvessels were incubated with isoproterenol (β-adrenoceptor agonist) and with and without U73122 (phospholipase C inhibitor), GF109203X (protein kinase C inhibitor), 1-butanol (phospholipase D inhibitor), CGP77675 (c-src inhibitor), HA1077 (Rho kinase inhibitor), Y27632 (Rho kinase inhibitor), LY294002 (phosphatidylinositol-3-kinase inhibitor), dipenyleneiodonium (NADPH oxidase inhibitor), or Tempol (superoxide dismutase mimetic). Cultured preglomerular microvascular smooth muscle cells were incubated with isoproterenol or forskolin (direct activator of adenylyl cyclase) and with or without U73122, C2-ceramide (phospholipase D inhibitor), or PP1 [src family inhibitor, 1-(1,1-dimethylethyl)-1-(4-methylphenyl)-1H-pyrazolo[3,4-d]pyrimidin-4-amine]. All studies were conducted with 3-isobutyl-1-methylxanthine (broad-spectrum phosphodiesterase inhibitor) to eliminate changes in cyclic AMP degradation. In microvessels isoproterenol-induced cyclic AMP was not affected by Y27632, HA1007, LY294002, dipenylene-iodonium, or Tempol; was increased by U73122 and GF109203X; and was decreased by 1-butanol and CGP77675. In cells, U73122 increased and C2-ceramide and PP1 decreased isoproterenol-induced cyclic AMP. Forskolin-induced cyclic AMP was not altered. These results indicate that receptor-mediated activation of adenylyl cyclase is 1) not modulated by Rho kinase, phosphatidylinositol-3-kinase, NADPH oxidase, or superoxide; 2) is attenuated by phospholipase C and protein kinase C; and 3) is augmented by phospholipase D and src. Phospholipase C, phospholipase D, and src modulate receptor-induced cyclic AMP by affecting β-adrenoreceptor/G protein/adenylyl cyclase coupling rather than by directly affecting adenylyl cyclase activity.

Footnotes

  • This work was supported by National Institutes of Health Grant HL069846.

  • DOI: 10.1124/jpet.103.063081.

  • ABBREVIATIONS: PGSMC, preglomerular microvascular smooth muscle cell; RT, room temperature; MOPS, 3-(N-morpholino)propanesulfonic acid; PBS, phosphate-buffered saline; PPI, 1-(1,1-dimethylethyl)-1-(4-methylphenyl)-1H-pyrazolo[3,4-d]pyrimidin-4-amine; ANOVA, analysis of variance; LSD, least significant difference; U73122, 1-(6-((17β)-3-methoxyestra-1,3,5[10]-trien-17-yl)amino]hexyl)-1H-pyrrole-2,5-dione; GF109203X, 2-[1-(3-dimethylaminopropyl)-1H-indol-3-yl]-3-(1H-indol-3-yl)maleimide; CGP77675, 1-(2-{4-[4-amino-5-(3-methoxyphenyl)pyrrolo[2,3-d]pyrimidin-7-yl]phenyl}ethyl)piperidin-4-ol; HA1077, 1-(5-isoquinolinesulfonyl)homopiperazine; Y27632, trans-4-[(1R)-1-aminoethyl]-N-4-pyridinylcyclohexanecarboxamide; LY294002, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one.

    • Received November 17, 2003.
    • Accepted April 12, 2004.
  • The American Society for Pharmacology and Experimental Therapeutics
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Journal of Pharmacology and Experimental Therapeutics: 310 (1)
Journal of Pharmacology and Experimental Therapeutics
Vol. 310, Issue 1
1 Jul 2004
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Research ArticleCARDIOVASCULAR

Modulation of Cyclic AMP Production by Signal Transduction Pathways in Preglomerular Microvessels and Microvascular Smooth Muscle Cells

Travis C. Jackson, Zaichuan Mi and Edwin K. Jackson
Journal of Pharmacology and Experimental Therapeutics July 1, 2004, 310 (1) 349-358; DOI: https://doi.org/10.1124/jpet.103.063081

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Research ArticleCARDIOVASCULAR

Modulation of Cyclic AMP Production by Signal Transduction Pathways in Preglomerular Microvessels and Microvascular Smooth Muscle Cells

Travis C. Jackson, Zaichuan Mi and Edwin K. Jackson
Journal of Pharmacology and Experimental Therapeutics July 1, 2004, 310 (1) 349-358; DOI: https://doi.org/10.1124/jpet.103.063081
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