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J Appl Physiol 91: 1421-1430, 2001;
8750-7587/01 $5.00
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Vol. 91, Issue 3, 1421-1430, September 2001

HIGHLIGHTED TOPICS
Signal Transduction in Smooth Muscle
Invited Review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression

Thomas M. Lincoln, Nupur Dey, and Hassan Sellak

Department of Pathology, Division of Molecular and Cellular Pathology, University of Alabama at Birmingham, Birmingham, Alabama 35294-0019

cGMP is a second messenger that produces its effects by interacting with intracellular receptor proteins. In smooth muscle cells, one of the major receptors for cGMP is the serine/threonine protein kinase, cGMP-dependent protein kinase (PKG). PKG has been shown to catalyze the phosphorylation of a number of physiologically relevant proteins whose function it is to regulate the contractile activity of the smooth muscle cell. These include proteins that regulate free intracellular calcium levels, the cytoskeleton, and the phosphorylation state of the regulatory light chain of smooth muscle myosin. Other studies have shown that vascular smooth muscle cells (VSMCs) that are cultured in vitro may cease to express PKG and will, coincidentally, acquire a noncontractile, synthetic phenotype. The restoration of PKG expression to the synthetic phenotype VSMC results in the cells acquiring a more contractile phenotype. These more recent studies suggest that PKG controls VSMC gene expression that, in turn, regulates phenotypic modulation of the cells. Therefore, the regulation of PKG gene expression appears to be linked to phenotypic modulation of VSMC. Because several vascular disorders are related to the accumulation of synthetic, fibroproliferative VSMC in the vessel wall, it is likely that changes in the activity of the nitric oxide/cGMP/PKG pathway is involved the development of these diseases.

vascular smooth muscle cells; nitric oxide


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L. V. Gonzalez Bosc, M. K. Wilkerson, K. N. Bradley, D. M. Eckman, D. C. Hill-Eubanks, and M. T. Nelson
Intraluminal Pressure Is a Stimulus for NFATc3 Nuclear Accumulation: ROLE OF CALCIUM, ENDOTHELIUM-DERIVED NITRIC OXIDE, AND cGMP-DEPENDENT PROTEIN KINASE
J. Biol. Chem., March 12, 2004; 279(11): 10702 - 10709.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Bonnevier, R. Fassler, A. P. Somlyo, A. V. Somlyo, and A. Arner
Modulation of Ca2+ Sensitivity by Cyclic Nucleotides in Smooth Muscle from Protein Kinase G-deficient Mice
J. Biol. Chem., February 13, 2004; 279(7): 5146 - 5151.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Q. Q. Huang, S. A. Fisher, and F. V. Brozovich
Unzipping the Role of Myosin Light Chain Phosphatase in Smooth Muscle Cell Relaxation
J. Biol. Chem., January 2, 2004; 279(1): 597 - 603.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
T. Chitapanarux, S. L. Chen, H. Lee, A. C. Melton, and H. F. Yee Jr.
C-type natriuretic peptide induces human colonic myofibroblast relaxation
Am J Physiol Gastrointest Liver Physiol, January 1, 2004; 286(1): G31 - G36.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. B. Pilz and D. E. Casteel
Regulation of Gene Expression by Cyclic GMP
Circ. Res., November 28, 2003; 93(11): 1034 - 1046.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
U. Hink, M. Oelze, P. Kolb, M. Bachschmid, M.-H. Zou, A. Daiber, H. Mollnau, M. August, S. Baldus, N. Tsilimingas, et al.
Role for peroxynitrite in the inhibition of prostacyclin synthase in nitrate tolerance
J. Am. Coll. Cardiol., November 19, 2003; 42(10): 1826 - 1834.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. Feil, S. M. Lohmann, H. de Jonge, U. Walter, and F. Hofmann
Cyclic GMP-Dependent Protein Kinases and the Cardiovascular System: Insights From Genetically Modified Mice
Circ. Res., November 14, 2003; 93(10): 907 - 916.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
W. Wolfsgruber, S. Feil, S. Brummer, O. Kuppinger, F. Hofmann, and R. Feil
A proatherogenic role for cGMP-dependent protein kinase in vascular smooth muscle cells
PNAS, November 11, 2003; 100(23): 13519 - 13524.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
T. Munzel, R. Feil, A. Mulsch, S. M. Lohmann, F. Hofmann, and U. Walter
Physiology and Pathophysiology of Vascular Signaling Controlled by Cyclic Guanosine 3',5'-Cyclic Monophosphate-Dependent Protein Kinase
Circulation, November 4, 2003; 108(18): 2172 - 2183.
[Full Text] [PDF]

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 Circ. Res.Home page
V. Gerzanich, A. Ivanov, S. Ivanova, J. B. Yang, H. Zhou, Y. Dong, and J. M. Simard
Alternative Splicing of cGMP-Dependent Protein Kinase I in Angiotensin-Hypertension: Novel Mechanism for Nitrate Tolerance in Vascular Smooth Muscle
Circ. Res., October 31, 2003; 93(9): 805 - 812.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
A. L. Kleschyov, M. Oelze, A. Daiber, Y. Huang, H. Mollnau, E. Schulz, K. Sydow, B. Fichtlscherer, A. Mulsch, and T. Munzel
Does Nitric Oxide Mediate the Vasodilator Activity of Nitroglycerin?
Circ. Res., October 31, 2003; 93 (9): e104 - e112.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
N. Airhart, Y.-F. Yang, C. T. Roberts Jr., and M. Silberbach
Atrial Natriuretic Peptide Induces Natriuretic Peptide Receptor-cGMP-dependent Protein Kinase Interaction
J. Biol. Chem., October 3, 2003; 278(40): 38693 - 38698.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
G. G. Geary and J. N. Buchholz
Selected Contribution: Effects of aging on cerebrovascular tone and [Ca2+]i
J Appl Physiol, October 1, 2003; 95(4): 1746 - 1754.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
F. J. Rivero-Vilches, S De Frutos, M Saura, D Rodriguez-Puyol, and M Rodriguez-Puyol
Differential relaxing responses to particulate or soluble guanylyl cyclase activation on endothelial cells: a mechanism dependent on PKG-I{alpha} activation by NO/cGMP
Am J Physiol Cell Physiol, October 1, 2003; 285(4): C891 - C898.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
Y. Gao, S. Dhanakoti, E. M. Trevino, F. C. Sander, A. M. Portugal, and J. U. Raj
Effect of oxygen on cyclic GMP-dependent protein kinase-mediated relaxation in ovine fetal pulmonary arteries and veins
Am J Physiol Lung Cell Mol Physiol, September 1, 2003; 285(3): L611 - L618.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
X. Wang, G. Trottier, and R. Loutzenhiser
Determinants of renal afferent arteriolar actions of bradykinin: evidence that multiple pathways mediate responses attributed to EDHF
Am J Physiol Renal Physiol, September 1, 2003; 285(3): F540 - F549.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. W. Park and L.-N. Wei
Regulation of c-myc Gene by Nitric Oxide via Inactivating NF-{kappa}B Complex in P19 Mouse Embryonal Carcinoma Cells
J. Biol. Chem., August 8, 2003; 278(32): 29776 - 29782.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
T. C. Resta
Hypoxic regulation of nitric oxide signaling in vascular smooth muscle
Am J Physiol Lung Cell Mol Physiol, August 1, 2003; 285(2): L293 - L295.
[Full Text] [PDF]

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 DiabetesHome page
S. Wang, X. Wu, T. M. Lincoln, and J. E. Murphy-Ullrich
Expression of Constitutively Active cGMP-Dependent Protein Kinase Prevents Glucose Stimulation of Thrombospondin 1 Expression and TGF-{beta} Activity
Diabetes, August 1, 2003; 52(8): 2144 - 2150.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
C. J. Mingone, S. A. Gupte, T. Iesaki, and M. S. Wolin
Hypoxia enhances a cGMP-independent nitric oxide relaxing mechanism in pulmonary arteries
Am J Physiol Lung Cell Mol Physiol, August 1, 2003; 285(2): L296 - L304.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
T. Matsumoto, L. V. d'uscio, D. Eguchi, M. Akiyama, L. A. Smith, and Z. S. Katusic
Protective Effect of Chronic Vitamin C Treatment on Endothelial Function of Apolipoprotein E-Deficient Mouse Carotid Artery
J. Pharmacol. Exp. Ther., July 1, 2003; 306(1): 103 - 108.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
K. S. Murthy, H. Zhou, J. R. Grider, and G. M. Makhlouf
Inhibition of sustained smooth muscle contraction by PKA and PKG preferentially mediated by phosphorylation of RhoA
Am J Physiol Gastrointest Liver Physiol, June 1, 2003; 284(6): G1006 - G1016.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Hou, J. Lascola, N. O. Dulin, R. D. Ye, and D. D. Browning
Activation of cGMP-dependent Protein Kinase by Protein Kinase C
J. Biol. Chem., May 2, 2003; 278(19): 16706 - 16712.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
V. Gerzanich, S. Ivanova, H. Zhou, and J. M. Simard
Mislocalization of eNOS and Upregulation of Cerebral Vascular Ca2+ Channel Activity in Angiotensin-Hypertension
Hypertension, May 1, 2003; 41(5): 1124 - 1130.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
V. Sauzeau, M. Rolli-Derkinderen, C. Marionneau, G. Loirand, and P. Pacaud
RhoA Expression Is Controlled by Nitric Oxide through cGMP-dependent Protein Kinase Activation
J. Biol. Chem., March 7, 2003; 278(11): 9472 - 9480.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
K. S. Murthy and H. Zhou
Selective phosphorylation of the IP3R-I in vivo by cGMP-dependent protein kinase in smooth muscle
Am J Physiol Gastrointest Liver Physiol, February 1, 2003; 284(2): G221 - G230.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
B. Adegunloye, E. Lamarre, and R. S. Moreland
Quinine Inhibits Vascular Contraction Independent of Effects on Calcium or Myosin Phosphorylation
J. Pharmacol. Exp. Ther., January 1, 2003; 304(1): 294 - 300.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
I. Fleming and R. Busse
Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2003; 284(1): R1 - R12.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
M. P. Bracamonte, M. Jayachandran, K. S. Rud, and V. M. Miller
Acute effects of 17beta -estradiol on femoral veins from adult gonadally intact and ovariectomized female pigs
Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2389 - H2396.
[Abstract] [Full Text] [PDF]

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 Cardiovasc ResHome page
A. J Wilson and L. H Clapp
The molecular site of action of KATP channel inhibitors determines their ability to inhibit iNOS-mediated relaxation in rat aorta
Cardiovasc Res, October 1, 2002; 56(1): 154 - 163.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Gudi, J. C. Chen, D. E. Casteel, T. M. Seasholtz, G. R. Boss, and R. B. Pilz
cGMP-dependent Protein Kinase Inhibits Serum-response Element-dependent Transcription by Inhibiting Rho Activation and Functions
J. Biol. Chem., September 27, 2002; 277(40): 37382 - 37393.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L.-M. Postovit, M. A. Adams, G. E. Lash, J. P. Heaton, and C. H. Graham
Oxygen-mediated Regulation of Tumor Cell Invasiveness. INVOLVEMENT OF A NITRIC OXIDE SIGNALING PATHWAY
J. Biol. Chem., September 13, 2002; 277(38): 35730 - 35737.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. E. Casteel, S. Zhuang, T. Gudi, J. Tang, M. Vuica, S. Desiderio, and R. B. Pilz
cGMP-dependent Protein Kinase Ibeta Physically and Functionally Interacts with the Transcriptional Regulator TFII-I
J. Biol. Chem., August 23, 2002; 277(35): 32003 - 32014.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Wang, M. Eto, W. D. Steers, A. P. Somlyo, and A. V. Somlyo
RhoA-mediated Ca2+ Sensitization in Erectile Function
J. Biol. Chem., August 16, 2002; 277(34): 30614 - 30621.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
R. Feil, N. Gappa, M. Rutz, J. Schlossmann, C. R. Rose, A. Konnerth, S. Brummer, S. Kuhbandner, and F. Hofmann
Functional Reconstitution of Vascular Smooth Muscle Cells With cGMP-Dependent Protein Kinase I Isoforms
Circ. Res., May 31, 2002; 90(10): 1080 - 1086.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
H. Sellak, X. Yang, X. Cao, T. Cornwell, G. A. Soff, and T. Lincoln
Sp1 Transcription Factor as a Molecular Target for Nitric Oxide- and Cyclic Nucleotide-Mediated Suppression of cGMP-Dependent Protein Kinase-I{alpha} Expression in Vascular Smooth Muscle Cells
Circ. Res., March 8, 2002; 90(4): 405 - 412.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
M. Yu, C.-W. Sun, K. G. Maier, D. R. Harder, and R. J. Roman
Mechanism of cGMP contribution to the vasodilator response to NO in rat middle cerebral arteries
Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1724 - H1731.
[Abstract] [Full Text] [PDF]

Home page
 Circ. Res.Home page
H. Sellak, X. Yang, X. Cao, T. Cornwell, G. A. Soff, and T. Lincoln
Sp1 Transcription Factor as a Molecular Target for Nitric Oxide- and Cyclic Nucleotide-Mediated Suppression of cGMP-Dependent Protein Kinase-I{alpha} Expression in Vascular Smooth Muscle Cells
Circ. Res., March 8, 2002; 90(4): 405 - 412.
[Abstract] [Full Text] [PDF]


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