Cyclic GMP-Dependent Protein Kinases and the Cardiovascular System: Insights from Genetically Modified Mice

Circulation Research

Volumn 93, Issue 10, 2003, Pages 907-916

  Feil, Robert ^a   Lohmann, Suzanne M ^c   De Jonge, Hugo ^b   Walter, Ulrich ^c   Hofmann, Franz ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c NONE

Author keywords

Atherosclerosis; Cardiac hypertrophy; CGMP; Nitric oxide; Smooth muscle relaxation

Indexed keywords

ACETYLSALICYLIC ACID; ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM ACTIVATED POTASSIUM CHANNEL; CHLORIDE CHANNEL; CHLORIDE ION; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; DIPYRIDAMOLE; ENDOTHELIUM DERIVED HYPERPOLARIZING FACTOR; FIBRINOGEN RECEPTOR ANTAGONIST; GLYCERYL TRINITRATE; GUANYLATE CYCLASE; ISOENZYME; KT 5823; NATRIURETIC FACTOR; NITRIC OXIDE; PHOSPHODIESTERASE INHIBITOR; PROSTAGLANDIN SYNTHASE INHIBITOR; SODIUM ION;

ADRENAL CORTEX; ARTERIOLE; ARTERY DILATATION; ATHEROSCLEROSIS; BLOOD PRESSURE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; CELL CULTURE; CELL FUNCTION; CELL TYPE; DNA MODIFICATION; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SUBUNIT; ERECTILE DYSFUNCTION; GENE FUNCTION; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENE TARGETING; HOMEOSTASIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SPACE; KIDNEY FUNCTION; KNOCKOUT MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; PULMONARY HYPERTENSION; PURKINJE CELL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; THROMBOCYTE FUNCTION; THROMBOSIS; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM; VASODILATATION;

ANIMALS; BLOOD PLATELETS; BLOOD PRESSURE; CARDIOVASCULAR SYSTEM; CYCLIC GMP-DEPENDENT PROTEIN KINASES; HUMANS; KIDNEY; MICE; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; VASOMOTOR SYSTEM;

EID: 0242552817     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000100390.68771.CC     Document Type: Review

References (143)

1. Beavo JA, Brunton LL. Cyclic nucleotide research: still expanding after half a century. Nat Rev Mol Cell Biol. 2002;3:710-718.
2. Friebe A, Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ Res. 2003;93:96-105.
3. Kuhn M. Structure, regulation, and function ofof mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ Res. 2003;93:700-709.
4. Rybalkin SD, Yan C, Bornfeldt KE, Beavo JA. Cyclic GMP phosphodiesterases and regulation of smooth muscle function. Circ Res. 2003;93:280-291.
5. Hofmann F, Biel M, Feil R, Kleppisch T. Mouse models of NO/natriuretic peptide/cGMP kinase signaling. In: Of,fermanns S, Hein L, eds. Handbook of. Experimental Pharmacology. Vol 159. Heidelberg, Germany: Springer-Verlag; 2004:95-130.
6. Hanafy KA, Krumenacker JS, Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med Sci Monit. 2001;7:801-819.
7. Lohmann SM, Vaandrager AB, Smolenski A, Walter U, De Jonge HR. Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem Sci. 1997;22:307-312.
8. Pfeifer A, Ruth P, Dostmann W, Sausbier M, Klatt P, Hofmann F. Structure and function of cGMP-dependent protein kinases. Rev Physiol Biochem Pharmacol. 1999;135:105-149.
9. Wall ME, Francis SH, Corbin JD, Grimes K, Richie-Jannetta R, Kotera J, Macdonald BA, Gibson RR, Trewhella J. Mechanisms associated with cGMP binding and activation of' cGMP-dependent protein kinase. Proc Natl Acad Sci U S A. 2003;100:2380-2385.
10. Eigenthaler M, Lohmann SM, Walter U, Pilz RB. Signal transduction by cGMP-dependent protein kinases and their emerging roles in the regulation of cell adhesion and gene expression. Rev Physiol Biochem Pharmacol. 1999;135:173-209.
11. Hofmann F, Ammendola A, Schlossmann J. Rising behind NO: cGMP-dependent protein kinases. J Cell Sci. 2000;113:1671-1676.
12. Lincoln TM, Dey N, Sellak H. cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J Appl Physiol. 2001;91:1421-1430.
13. Carvajal JA, Germain AM, Huidobro-Toro JP, Weiner CP. Molecular mechanism ofn cGMP-mediated smooth muscle relaxation. J Cell Physiol. 2000;184:409-20.
14. Smolenski A, Burkhardt AM, Eigenthaler M, Butt E, Gambaryan S, Lohmann SM, Walter U. Functional analysis of cGMP-dependent protein kinases I and II as mediators of NO/cGMP effects. Naunyn Schmiedebergs Arch Pharmacol. 1998;358:134-139.
15. Schwede F, Maronde E, Genieser H, Jastorff B. Cyclic nucleotide analogs as biochemical tools and prospective drugs. Pharmacol Ther. 2000;87:199-226.
16. Burkhardt M, Glazova M, Gambaryan S, Vollkommer T, Butt E, Bader B, Heermeier K, Lincoln TM, Walter U, Palmetshofer A. KT5823 inhibits cGMP-dependent protein kinase activity in vitro but not in intact human platelets and rat mesangial cells. J Biol Chem. 2000;275:33536-33541.
17. Cornwell TL, Soff GA, Traynor AE, Lincoln TM. Regulation of the expression of cyclic GMP-dependent protein kinase by cell density in vascular smooth muscle cells. J Vasc Res. 1994;31:330-337.
18. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, Wang GX, Korth M, Aszodi A, Andersson KE, Krombach F, Mayerhofer A, Ruth P, Fassler R, Hofmann F. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J. 1998;17:3045-3051.
19. Persson K, Pandita RK, Aszodi A, Ahmad M, Pfeifer A, Fassler R, Andersson KE. Functional characteristics of urinary tract smooth muscles in mice lacking cGMP protein kinase type I. Am J Physiol Regul Integr Comp Physiol. 2000;279:R1112-R1120.
20. Ny L, Pfeifer A, Aszodi A, Ahmad M, Alm P, Hedlund P, Fassler R, Andersson KE. Impaired relaxation of stomach smooth muscle in mice lacking cyclic GMP-dependent protein kinase I. Br J Pharmacol. 2000;129:395-401.
21. Hedlund P, Aszodi A, Pfeifer A, Alm P, Hofmann F, Ahmad M, Fassler R, Andersson KE. Erectile dysfunction in cyclic GMP-dependent kinase I-deficient mice. Proc Natl Acad Sci USA. 2000;97:2349-2354.
22. Massberg S, Sausbier M, Klatt P, Bauer M, Pfeifer A, Siess W, Fassler R, Ruth P, Krombach F, Hofmann F. Increased adhesion and aggregation of platelets lacking cyclic guanosine 3′,5′-monophosphate kinase 1. J Exp Med. 1999;189:1255-1264.
23. Li Z, Xi X, Gu M, Feil R, Ye RD, Eigenthaler M, Hofmann F, Du X. A stimulatory role for cGMP-dependent protein kinase in platelet activation. Cell. 2003;112:77-86.
24. Schmidt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, Rathjen FG. cGMP-mediated signaling via cGKIα is required for the guidance and connectivity of sensory axons. J Cell Biol. 2002;159:489-498.
25. Wegener JW, Nawrath H, Wolfsgruber W, Kuhbandner S, Werner C, Hofmann F, Feil R. cGMP-dependent protein kinase I mediates the negative inotropic effect of cGMP in the murine myocardium. Circ Res. 2002;90:18-20.
26. Metzger D, Feil R. Engineering the mouse genome by site-specific recombination. Curr Opin Biotechnol. 1999;10:470-476.
27. Tronche F, Casanova E, Turiault M, Sahly I, Kellendonk C. When reverse genetics meets physiology: the use of site-specific recombinases in mice. FEBS Lett. 2002;529:116-121.
28. Wolfsgruber W, Feil S, Brummer S, Kuppinger O, Hofmann F, Feil R. A pro-atherogenic role for cGMP-dependent protein kinase in vascular smooth muscle cells. Proc Natl Acad Sci U S A. In press.
29. Kleppisch T, Wolfsgruber W, Feil S, Allmann R, Wotjak CT, Goebbels S, Nave K-A, Hofmann F, Feil R. Hippocampal cyclic GMP-dependent protein kinase I supports an age- and protein synthesis-dependent component of long-term potentiation but is not essential for spatial reference and contextual memory. J Neurosci. 2003;23:6005-6012.
30. Feil R, Hartmann J, Luo C, Wolfsgruber W, Schilling K, Feil S, Barski JJ, Meyer M, Konnerth A, De Zeeuw CI, Hofmann F. Impairment of LTD and cerebellar leaming by Purkinje cell-specific ablation of cGMP-dependent protein kinase I. J Cell Biol. In press.
31. Pfeifer A, Aszodi A, Seidler U, Ruth P, Hofmann F, Fassler R. Intestinal secretory defects and dwarfism in mice lacking cGMP-dependent protein kinase II. Science. 1996;274:2082-2086.
32. Miyazawa T, Ogawa Y, Chusho H, Yasoda A, Tamura N, Komatsu Y, Pfeifer A, Hofmann F, Nakao K. Cyclic GMP-dependent protein kinase II plays a critical role in C-type natriuretic peptide-mediated endochondral ossification. Endocrinology. 2002;143:3604-3610.
33. Vaandrager AB, Bot AG, Ruth P, Pfeifer A, Hofmann F, De Jonge HR. Differenfial role of cyclic GMP-dependent protein kinase II in ion transport in murine small intestine and colon. Gastroenterology. 2000;118:108-114.
34. Wagner C, Pfeifer A, Ruth P, Hofmann F, Kurtz A. Role of cGMP-kinase II in the control of renin secretion and renin expression. J Clin Invest. 1998;102:1576-1582.
35. Oster H, Werner C, Magnone MC, Mayser H, Feil R, Seeliger MW, Hofmann F, Albrecht U. cGMP-dependent protein kinase II modulates mPer1 and mPer2 gene induction and influences phase shifts of the circadian clock. Curr Biol. 2003;13:725-733.
36. Garbers DL, Dubois SK. The molecular basis of hypertension. Annu Rev Biochem. 1999;68:127-155.
37. Sausbier M, Schubert R, Voigt V, Himeiss C, Pfeifer A, Korth M, Kleppisch T, Ruth P, Hofmann F. Mechanisms of NO/cGMP-dependent vasorelaxation. Circ Res. 2000;87:825-830.
38. Koeppen K, Feil R, Feil S, Hofmann F, Pohl U, de Wit C. NO-, but not ACh-induced arteriolar dilations are impaired in cGMP-dependent protein kinase k. o. mice. Pflugers Arch. 2003;445:19. Abstract.
39. Brandes RP, Schmitz-Winnenthal FH, Feletou M, Godecke A, Huang PL, Vanhoutte PM, Fleming I, Busse R. An endothelium-derived hyperpolarizing factor distinct from NO and prostacyclin is a major endothelium-dependent vasodilator in resistance vessels of wild-type and endothelial NO synthase knockout mice. Proc Natl Acad Sci U S A. 2000;97:9747-9752.
40. Schlossmann J, Ammendola A, Ashman K, Zong X, Huber A, Neubauer G, Wang GX, Allescher HD, Korth M, Wilm M, Hofmann F, Ruth P. Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Iβ. Nature. 2000;404:197-201.
41. Raeymaekers L, Hofmann F, Casteels R. Cyclic GMP-dependent protein kinase phosphorylates phospholamban in isolated sarcoplasmic reticulum from cardiac and smooth muscle. Biochem J. 1988;252:269-273.
42. Koller A, Schlossmann J, Ashman K, Uttenweiler-Joseph S, Ruth P, Hofmann F. Association of phospholamban with a cGMP kinase signaling complex. Biochem Biophys Res Commun. 2003;300:155-160.
43. i homeostasis and cyclic nucleotide relaxation in aorta of phospholamban-deficient mice. Am J Physiol. 1999;277:H963-H970.
44. 2+)ATPase in vascular smooth muscle. J Biochem (Tokyo). 1987;101:287-290.
45. Feil R, Gappa N, Rutz M, Schlossmann J, Rose CR, Konnerth A, Brummer S, Kuhbandner S, Hofmann F. Functional reconstitution of vascular smooth muscle cells with cGMP-dependent protein kinase I isoforms. Circ Res. 2002;90:1080-1086.
46. Somlyo AP, Somlyo AV. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol. 2000;522:177-185.
47. Surks HK, Mochizuki N, Kasai Y, Georgescu SP, Tang KM, Ito M, Lincoln TM, Mendelsohn ME. Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase Iα. Science. 1999;286:1583-1587.
48. 2+ sensitization of contraction in vascular smooth muscle. J Biol Chem. 2000;275:21722-21729.
49. 2+-desensitizing effect in smooth muscle. J Biol Chem. 2001;276:24519-24524.
50. Sausbier MSR, Zhao H, Feil S, Feil R, Zhou XB, Kort M, Hofmann F, Amtz C, Ruth P. Genetic ablation of the BK K channel in mice attenuates relaxation of small arteries and causes hypertension. Naunnyn Schmiedebergs Arch Pharmacol. 2003;367:R10. Abstract.
51. Werner C, Pryzwansky KB, Hofmann F. Cyclic GMP kinase I affects murine neutrophil migration and superoxide production. Naunyn Schmiedebergs Arch Pharmacol. 2001;363:R81. Abstract.
52. Wyatt TA, Naftilan AJ, Francis SH, Corbin JD. ANF elicits phosphorylation of the cGMP phosphodiesterase in vascular smooth muscle cells. Am J Physiol. 1998;274:H448-H455.
53. Rybalkin SD, Rybalkina IG, Feil R, Hofmann F, Beavo JA. Regulation of cGMP-specific phosphodiesterase (PDE5) phosphorylation in smooth muscle cells. J Biol Chem. 2002;277:3310-3317.
54. Mullershausen F, Friebe A, Feil R, Thompson WJ, Hofmann F, Koesling D. Direct activation of PDE5 by cGMP: long-term effects within NO/cGMP signaling. J Cell Biol. 2003;160:719-727.
55. Cornwell TL, Arnold E, Boerth NJ, Lincoln TM. Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP. Am J Physiol. 1994;267:C1405-C1413.
56. Soff GA, Cornwell TL, Cundiff DL, Gately S, Lincoln TM. Smooth muscle cell expression of type I cyclic GMP-dependent protein kinase is suppressed by continuous exposure to nitrovasodilators, theophylline, cyclic GMP, and cyclic AMP. J Clin Invest. 1997;100:2580-2587.
57. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, Zetsche B, Hammer RE, Herz J, Kuhn M. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci U S A. 2002;99:7142-7147.
58. Shi W, Wang X, Shih DM, Laubach VE, Navab M, Lusis AJ. Paradoxical reduction of fatty streak formation in mice lacking endothelial nitric oxide synthase. Circulation. 2002;105:2078-2082.
59. Ozaki M, Kawashima S, Yamashita T, Hirase T, Namiki M, Inoue N, Hirata K, Yasui H, Sakurai H, Yoshida Y, Masada M, Yokoyama M. Overexpression of endothelial nitric oxide synthase accelerates atherosclerotic lesion formation in apoE-deficient mice. J Clin Invest. 2002;110:331-340.
60. Kuhlencordt PJ, Chen J, Han F, Astern J, Huang PL. Genetic deficiency of inducible nitric oxide synthase reduces atherosclerosis and lowers plasma lipid peroxides in apolipoprotein E-knockout mice. Circulation. 2001;103:3099-3104.
61. Chyu KY, Dimayuga P, Zhu J, Nilsson J, Kaul S, Shah PK, Cercek B. Decreased neointimal thickening after arterial wall injury in inducible nitric oxide synthase knockout mice. Circ Res. 1999;85:1192-1198.
62. Tolbert T, Thompson JA, Bouchard P, Oparil S. Estrogen-induced vasoprotection is independent of inducible nitric oxide synthase expression: Evidence from the mouse carotid artery ligation model. Circulation. 2001;104:2740-2745.
63. Detmers PA, Hernandez M, Mudgett J, Hassing H, Burton C, Mundt S, Chun S, Fletcher D, Card DJ, Lisnock J, Weikel R, Bergstrom JD, Shevell DE, Hermanowski-Vosatka A, Sparrow CP, Chao YS, Rader DJ, Wright SD, Pure E. Deficiency in inducible nitric oxide synthase results in reduced atherosclerosis in apolipoprotein E-deficient mice. J Immunol. 2000;165:3430-3435.
64. Sennlaub F, Courtois Y, Goureau O. Inducible nitric oxide synthase mediates the change from retinal to vitreal neovascularization in ischemic retinopathy. J Clin Invest. 2001;107:717-725.
65. -/- mice are ameliorated by enalapril treatment. J Clin Invest. 2000;105:451-458.
66. Kuhlencordt PJ, Gyurko R, Han F, Scherrer-Crosbie M, Aretz TH, Hajjar R, Picard MH, Huang PL. Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation. 2001;104:448-454.
67. Moroi M, Zhang L, Yasuda T, Virmani R, Gold HK, Fishman MC, Huang PL. Interaction of genetic deficiency of endothelial nitric oxide, gender, and pregnancy in vascular response to injury in mice. J Clin Invest. 1998;101:1225-1232.
68. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest. 1998;101:731-736.
69. Chen J, Kuhlencordt PJ, Astern J, Gyurko R, Huang PL. Hypertension does not account for the accelerated atherosclerosis and development of aneurysms in male apolipoprotein e/endothelial nitric oxide synthase double knockout mice. Circulation. 2001;104:2391-2394.
70. Koglin J, Glysing-Jensen T, Mudgett JS, Russell ME. Exacerbated transplant arteriosclerosis in inducible nitric oxide-deficient mice. Circulation. 1998;97:2059-2065.
71. Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med. 2002;8:1249-1256.
72. Hassid A, Arabshahi H, Bourcier T, Dhaunsi GS, Matthews C. Nitric oxide selectively amplifies FGF-2-induced mitogenesis in primary rat aortic smooth muscle cells. Am J Physiol. 1994;267:HI040-HI048.
73. Thomae KR, Nakayama DK, Billiar TR, Simmons RL, Pitt BR, Davies P. The effect of nitric oxide on fetal pulmonary artery smooth muscle growth. J Surg Res. 1995;59:337-343.
74. Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromocyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest. 1989;83:1774-1777.
75. Kariya K, Kawahara Y, Araki S, Fukuzaki H, Takai Y. Antiproliferative action of cyclic GMP-elevating vasodilators in cultured rabbit aortic smooth muscle cells. Atherosclerosis. 1989;80:143-147.
76. Sarkar R, Webb RC. Does nitric oxide regulate smooth muscle cell proliferation? A critical appraisal. J Vasc Res. 1998;35:135-142.
77. Anderson PG, Boerth NJ, Liu M, McNamara DB, Cornwell TL, Lincoln TM. Cyclic GMP-dependent protein kinase expression in coronary arterial smooth muscle in response to balloon catheter injury. Arterioscler Thromb Vasc Biol. 2000;20:2192-2197.
78. Sinnaeve P, Chiche JD, Gillijns H, Van Pelt N, Wirthlin D, Van De Werf F, Collen D, Bloch KD, Janssens S. Overexpression of a constitutively active protein kinase G mutant reduces neointima formation and in-stent restenosis. Circulation. 2002;105:2911-2916.
79. Monks D, Lange V, Silber RE, Markert T, Walter U, Nehls V. Expression of cGMP-dependent protein kinase I and its substrate VASP in neointimal cells of the injured rat carotid artery. Eur J Clin Invest. 1998;28:416-423.
80. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 1992;258:468-471.
81. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
82. Zhang R, Wang L, Zhang L, Chen J, Zhu Z, Zhang Z, Chopp M. Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ Res. 2003;92:308-313.
83. Yamahara K, Itoh H, Chun TH, Ogawa Y, Yamashita J, Sawada N, Fukunaga Y, Sone M, Yurugi-Kobayashi T, Miyashita K, Tsujimoto H, Kook H, Feil R, Garbers DL, Hofmann F, Nakao K. Significance and therapeutic potential of the natriuretic pepfides/cGMP/cGMP-dependent protein kinase pathway in vascular regeneration. Proc Natl Acad Sci U S A. 2003;100:3404-3409.
84. Gudi T, Huvar I, Meinecke M, Lohmann SM, Boss GR, Pilz RB. Regulation of gene expression by cGMP-dependent protein kinase: transactivation of the c-fos promoter. J Biol Chem. 1996;271:4597-4600.
85. Gudi T, Lohmann SM, Pilz RB. Regulation of gene expression by cyclic GMP-dependent protein kinase requires nuclear translocation of the kinase: identification of a nuclear localization signal. Mol Cell Biol. 1997;17:5244-5254.
86. Collins SP, Uhler MD. Cyclic AMP- and cyclic GMP-dependent protein kinases differ in their regulation of cyclic AMP response element-dependent gene transcription. J Biol Chem. 1999;274:8391-8404.
87. Browning DD, Mc Shane M, Marty C, Ye RD. Functional analysis of type 1α cGMP-dependent protein kinase using green fluorescent fusion proteins. J Biol Chem. 2001;276:13039-13048.
88. Casteel DE, Zhuang S, Gudi T, Tang J, Vuica M, Desiderio S, Pilz RB. cGMP-dependent protein kinase 1β physically and functionally interacts with the transcriptional regulator TFII-I. J Biol Chem. 2002;277:32003-32014.
89. Pilz RB, Casteel DE. Regulation of gene expression by cyclic GMP. Circ Res. In press.
90. Komalavilas P, Shah PK, Jo H, Lincoln TM. Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem. 1999;274:34301-34309.
91. Begum N, Sandu OA, Ito M, Lohmann SM, Smolenski A. Active Rho kinase (ROK-a) associates with insulin receptor substrate-1 and inhibits insulin signaling in vascular smooth muscle cells. J Biol Chem. 2002;277:6214-6222.
92. Hood J, Granger HJ. Protein kinase G mediates vascular endothelial growth factor-induced Raf-1 activation and proliferation in human endothelial cells. J Biol Chem. 1998;273:23504-23508.
93. Kook H, Itoh H, Choi BS, Sawada N, Doi K, Hwang TJ, Kim KK, Arai H, Baik YH, Nakao K. Physiological concentration of atrial natriuretic peptide induces endothelial regeneration in vitro. Am J Physiol Heart Circ Physiol. 2003;284:H1388-H1397.
94. Bouchie JL, Hansen H, Feener EP. Natriuretic factors and nitric oxide suppress plasminogen activator inhibitor-1 expression in vascular smooth muscle cells: role of cGMP in the regulation of the plasminogen system. Arterioscler Thromb Vasc Biol. 1998;18:1771-1779.
95. Luttun A, Lupu F, Storkebaum E, Hoylaerts MF, Moons L, Crawley J, Bono F, Poole AR, Tipping P, Herbert JM, Collen D, Carmeliet P. Lack of plasminogen activator inhibitor-1 promotes growth and abnormal matrix remodeling of advanced atherosclerotic plaques in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2002;22:499-505.
96. van Nieuw Amerongen GP, van Hinsbergh VW. Cytoskeletal effects of rho-like small guanine nucleotide-binding proteins in the vascular system. Arterioscler Thromb Vasc Biol. 2001;21:300-311.
97. Sauzeau V, Rolli-Derkinderen M, Marionneau C, Loirand G, Pacaud P. RhoA Expression is controlled by nitric oxide through cGMP-dependent protein kinase activafion. J Biol Chem. 2003;278:9472-9480.
98. Gudi T, Chen JC, Casteel DE, Seasholtz TM, Boss GR, Pilz RB. cGMP-dependent protein kinase inhibits serum-response element-dependent transcription by inhibiting rho activation and functions. J Biol Chem. 2002;277:37382-37393.
99. Reinhard M, Jarchau T, Walter U. Actin-based motility: stop and go with Ena/VASP proteins. Trends Biochem Sci. 2001;26:243-249.
100. Gertler FB, Niebuhr K, Reinhard M, Wehland J, Soriano P. Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Cell. 1996;87:227-239.
101. Bear JE, Loureiro JJ, Libova I, Fassler R, Wehland J, Gertler FB. Negative regulation of fibroblast motility by Ena/VASP proteins. Cell. 2000;101:717-728.
102. Walter U. Physiological role of cGMP and cGMP-dependent protein kinase in the cardiovascular system. Rev Physiol Biochem Pharmacol. 1989;113:41-88.
103. Rybalkin SD, Rybalkina IG, Shimizu-Albergine M, Tang XB, Beavo JA. PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO J. 2003;22:469-478.
104. Schwarz UR, Walter U, Eigenthaler M. Taming platelets with cyclic nucleotides. Biochem Pharmacol. 2001;62:1153-1161.
105. Bhatt DL, Topol EJ. Scientific and therapeutic advances in antiplatelet therapy. Nat Rev Drug Discov. 2003;2:15-28.
106. Stasch JP, Schmidt P, Alonso-Alija C, Apeler H, Dembowsky K, Haerter M, Heil M, Minuth T, Perzbom E, Pleiss U, Schramm M, Schroeder W, Schroder H, Stahl E, Steinke W, Wunder F. NO- and haem-independent activation of soluble guanylyl cyclase: molecular basis and cardiovascular implications of a new pharmacological principle. Br J Pharmacol. 2002;136:773-783.
107. Aktas B, Utz A, Hoenig-Liedl P, Walter U, Geiger J. Dipyridamole enhances NO/cGMP-mediated vasodilator-stimulated phosphoprotein phosphorylation and signaling in human platelets: in vitro and in vivo/ex vivo studies. Stroke. 2003;34:764-769.
108. Eigenthaler M, Ullrich H, Geiger J, Horstrup K, Honig-Liedl P, Wiebecke D, Walter U. Defective nitrovasodilator-stimulated protein phosphorylation and calcium regulation in cGMP-dependent protein kinase-deficient human platelets of chronic myelocytic leukemia. J Biol Chem. 1993;268:13526-13531.
109. Massberg S, Gruener S, Konrad I, Garcia Arguinzonis MI, Eigenthaler M, Hemler K, Kersting J, Schulz C, Mueller I, Besta F, Nieswandt B, Heinzmann U, Walter U, Gawaz M. Enhanced in vivo platelet adhesion in vasodilator-stimulated phosphoprotein (VASP)-deficient mice. Blood. August 21, 2003; DOI 10.1182/blood-2002-11-3417. Available at: www.bloodjoumal.org. Accessed October 14, 2003.
110. El-Daher SS, Patel Y, Siddiqua A, Hassock S, Edmunds S, Maddison B, Patel G, Goulding D, Lupu F, Wojcikiewicz RJ, Authi KS. Distinct localization and function of (1,4,5)IP3 receptor subtypes and the (1,3,4,5)IP4 receptor GAP1(IP4BP) in highly purified human platelet membranes. Blood. 2000;95:3412-3422.
111. Butt E, Immler D, Meyer HE, Kotlyarov A, Laass K, Gaestel M. Heat shock protein 27 is a substrate of cGMP-dependent protein kinase in intact human platelets: phosphorylation-induced actin polymerization caused by HSP27 mutants. J Biol Chem. 2001;276:7108-7113.
112. Butt E, Gambaryan S, Gottfert N, Galler A, Marcus K, Meyer HE. Actin binding of human LIM and SH3 protein is regulated by cGMP- and cAMP-dependent protein kinase phosphorylation on serine 146. J Biol Chem. 2003;278:15601-15607.
113. Miura Y, Kaibuchi K, Itoh T, Corbin JD, Francis SH, Takai Y. Phosphorylation of smg p21B/rap1B p21 by cyclic GMP-dependent protein kinase. FEBS Lett. 1992;297:171-174.
114. Aktas B, Honig-Liedl P, Walter U, Geiger J. Inhibition of platelet P2Y12 and α2A receptor signaling by cGMP-dependent protein kinase. Biochem Pharmacol. 2002;64:433-439.
115. Gorelick PB. Stroke prevention therapy beyond antithrombotics: unifying mechanisms in ischemic stroke pathogenesis and implications for therapy. Stroke. 2002;33:862-875.
116. Kelly RA, Balligand JL, Smith TW. Nitric oxide and cardiac function. Circ Res. 1996;79:363-380.
117. Vandecasteele G, Eschenhagen T, Scholz H, Stein B, Verde I, Fischmeister R. Muscarinic and β-adrenergic regulation of heart rate, force of contraction and calcium current is preserved in mice lacking endothelial nitric oxide synthase. Nat Med. 1999;5:331-334.
118. Godecke A, Heinicke T, Kamkin A, Kiseleva I, Strasser RH, Decking UK, Stumpe T, Isenberg G, Schrader J. Inotropic response to β-adrenergic receptor stimulation and anti-adrenergic effect of ACh in endothelial NO synthase-deficient mouse hearts. J Physiol. 2001;532:195-204.
119. Stein BC, Levin RI. Natriuretic peptides: physiology, therapeutic potential, and risk stratification in ischemic heart disease. Am Heart J. 1998;135:914-923.
120. John SW, Krege JH, Oliver PM, Hagaman JR, Hodgin JB, Pang SC, Flynn TG, Smithies O. Genetic decreases in atrial natriuretic peptide and salt-sensitive hypertension. Science. 1995;267:679-681.
121. Oliver PM, Fox JE, Kim R, Rockman HA, Kim HS, Reddick RL, Pandey KN, Milgram SL, Smithies O, Maeda N. Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proc Natl Acad Sci U S A. 1997;94:14730-14735.
122. Kishimoto I, Rossi K, Garbers DL. A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy. Proc Natl Acad Sci USA. 2001;98:2703-2706.
123. Knowles JW, Esposito G, Mao L, Hagaman JR, Fox JE, Smithies O, Rockman HA, Maeda N. Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice. J Clin Invest. 2001;107:975-984.
124. Holtwick R, Van Eickels M, Skryabin BV, Baba HA, Bubikat A, Begrow F, Schneider MD, Garbers DL, Kuhn M. Pressure-independent cardiac hypertrophy in mice with cardiomyocyte-restricted inactivation of the atrial natriuretic peptide receptor guanylyl cyclase-A. J Clin Invest. 2003;111:1399-1407.
125. Calderone A, Thaik CM, Takahashi N, Chang DL, Colucci WS. Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J Clin Invest. 1998;101:812-818.
126. Wollert KC, Fiedler B, Gambaryan S, Smolenski A, Heineke J, Butt E, Trautwein C, Lohmann SM, Drexler H. Gene transfer of cGMP-dependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes. Hypertension. 2002;39:87-92.
127. Fiedler B, Lohmann SM, Smolenski A, Linnemuller S, Pieske B, Schroder F, Molkentin JD, Drexler H, Wollert KC. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc Natl Acad Sci U S A. 2002;99:11363-11368.
128. Forte LR, London RM, Freeman RH, Krause WJ. Guanylin peptides: renal actions mediated by cyclic GMP. Am J Physiol Renal Physiol. 2000;278:F180-F191.
129. Roczniak A, Burns KD. Nitric oxide stimulates guanylate cyclase and regulates sodium transport in rabbit proximal tubule. Am J Physiol. 1996;270:F106-F115.
130. Dubois SK, Kishimoto I, Lillis TO, Garbers DL. A genetic model defines the importance of the atrial natriuretic peptide receptor (guanylyl cyclase-A) in the regulation of kidney function. Proc Natl Acad Sci U S A. 2000;97:4369-4373.
131. Ballermann BJ, Zeidel ML. Atrial natriuretic hormone. In: Seldin DW, Giebisch G, eds. The Kidney: Physiology and Pathophysiology. 2nd ed. New York, NY: Raven Press; 1992:1843-1884.
132. Kurtz A, Wagner C. Role of nitric oxide in the control of renin secretion. Am J Physiol. 1998;275:F849-F862.
133. Gambaryan S, Hausler C, Markert T, Pohler D, Jarchau T, Walter U, Haase W, Kurtz A, Lohmann SM. Expression of type II cGMP-dependent protein kinase in rat kidney is regulated by dehydration and correlated with renin gene expression. J Clin Invest. 1996;98:662-670.
134. Gambaryan S, Wagner C, Smolenski A, Walter U, Poller W, Haase W, Kurtz A, Lohmann SM. Endogenous or overexpressed cGMP-dependent protein kinases inhibit cAMP-dependent renin release from rat isolated perfused kidney, microdissected glomeruli, and isolated juxtaglomerular cells. Proc Natl Acad Sci USA. 1998;95:9003-9008.
135. Joyce NC, DeCamilli P, Lohmann SM, Walter U. cGMP-dependent protein kinase is present in high concentrations in contractile cells of the kidney vasculature. J Cyclic Nucleotide Protein Phosphor Res. 1986;11:191-198.
136. + exchanger. Nat Genet. 1998;19:282-285.
137. + exchangers NHE2 and NHE3 in intestinal epithelial cell line C2/bbe. Am J Physiol. 1998;275: C693-C701.
138. Sindice A, Basoglu C, Cerci A, Hirsch JR, Potthast R, Kuhn M, Ghanekar Y, Visweswariah SS, Schlatter E. Guanylin, uroguanylin, and heat-stable enterotoxin activate guanylate cyclase C and/or a pertussis toxin-sensitive G protein in human proximal tubule cells. J Biol Chem. 2002;277:17758-17764.
139. Eklof AC, Holtback U, Svennilson J, Fienberg A, Greengard P, Aperia A. Increased blood pressure and loss of ANP-induced natriuresis in mice lacking DARPP-32 gene. Clin Exp Hypertens. 2001;23:449-460.
140. Kibble JD, Balloch KJ, Neal AM, Hill C, White S, Robson L, Green R, Taylor CJ. Renal proximal tubule function is preserved in Cftr(tm2cam) deltaF508 cystic fibrosis mice. J Physiol. 2001;532:449-457.
141. 2+ reabsorption in rabbit kidney requires membrane-targeted, cGMP-dependent protein kinase type II. Proc Natl Acad Sci USA. 1999;96:6084-6089.
142. Woo AL, Noonan WT, Schultheis PJ, Neumann JC, Manning PA, Lorenz JN, Shull GE. Renal function in NHE3-deficient mice with transgenic rescue of small intestinal absorptive defect. Am J Physiol Renal Physiol. 2003;284:F1190-F1198.
143. Nakamura Y, Moss AJ, Brown MW, Kinoshita M, Kawai C. Long-term nitrate use may be deleterious in ischemic heart disease: a study using the databases from two large-scale postinfarction studies. Multicenter Myocardial Ischemia Research Group. Am Heart J. 1999;138:577-585.