Heparin responses in vascular smooth muscle cells involve cGMP-dependent protein kinase (PKG)

Journal of Cellular Physiology

Volumn 229, Issue 12, 2014, Pages 2142-2152

  Gilotti, Albert C ^a,c   Nimlamool, Wutigri ^a   Pugh, Raymond ^a,b   Slee, Joshua B ^a,d   Barthol, Trista C ^a   Miller, Elizabeth A ^a   Lowe Krentz, Linda J ^a  

^a LEHIGH UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC GMP; BROXURIDINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; FLUORESCEIN ISOTHIOCYANATE; HEPARIN; HEPARIN RECEPTOR ANTIBODY; ISOBUTYLMETHYLXANTHINE; KT 5823; MITOGEN ACTIVATED PROTEIN KINASE; PLATELET DERIVED GROWTH FACTOR; RECEPTOR ANTIBODY; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR ELK 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; RAT; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

ANIMALS; CELL PROLIFERATION; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION REGULATION; HEPARIN; MAP KINASE SIGNALING SYSTEM; MUSCLE, SMOOTH, VASCULAR; PHOSPHORYLATION; RATS; RECEPTORS, CELL SURFACE; THIONUCLEOTIDES;

EID: 84906706359     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24677     Document Type: Article

References (48)

1. Baldini P, De Vito P, Fraziano M, Mattioli P, Luly P, Di Nardo P. 2002. Atrial natriuretic factor inhibits mitogen-induced growth in aortic smooth muscle cells. J Cell Physiol 193:103-109.
2. Begum N, Song Y, Rienzie J, Ragolia L. 1998. Vascular smooth muscle cell growth and insulin regulation of mitogen-activated protein kinase in hypertension. Am J Physiol 275:C42-C49.
3. Blaukovitch CI, Pugh R, Gilotti AC, Kanyi D, Lowe-Krentz LJ. 2010. Heparin treatment of vascular smooth muscle cells results in the synthesis of the dual-specificity phosphatase MKP-1. J Cell Biochem 110:382-391.
4. Brunet S, Roux D, Lenomand P, Dowd S, Keyse S, Pouysségur J. 1999. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J 18:664-674.
5. Castellot JJ, Jr., Addonizio ML, Rosenberg R, Karnovsky MJ. 1981. Cultured endothelial cells produce a heparinlike inhibitor of smooth muscle cell growth. J Cell Biol 90:372-379.
6. Castellot JJJ, Wong K, Herman B, Hoover RL, Albertini DF, Wright TC, Caleb BL, Karnovsky MJ. 1985. Binding and internalization of heparin by vascular smooth muscle cells. J Cell Physiol 124:13-20.
7. Castellot JJJ, Pukac LA, Caleb BL, Wright TC, Karnovsky MJ. 1989. Heparin selectively inhibits a protein kinase C-dependent mechanism of cell cycle progression in calf aortic smooth muscle cells. J Cell Biol 109:3147-3155.
8. Cheah LS, Gwee M, Das R, Ballard H, Yang YF, Daniel EE, Kwan CY. 2002. Evidence for the existence of a constitutive nitric oxide synthase in vascular smooth muscle. Clin Exp Pharmacol Physiol 29:725-727.
9. Chen J, Crossland RF, Noorani MM, Marrelli SP. 2009. Inhibition of TRPC1/TRPC3 by PKG contributes to NO-mediated vasorelaxation. Am J Physiol Heart Circ Physiol 297:H417-H424.
10. Choi C, Sellak H, Brown FM, Lincoln TM. 2010. CGMP-dependent protein kinase and the regulation of vascular smooth muscle cell gene expression: possible involvement of Elk-1 sumoylation. Am J Physiol Heart Circ Physiol 299:H1660-H1670.
11. Clowes AW, Karnovsky MJ. 1977. Suppression by heparin of smooth muscle cell proliferation in injured arteries. Nature 265:625-626.
12. 2+ levels by atriopeptin and 8-bromo-cyclic GMP is mediated by cGMP-dependent protein kinase. J Biol Chem 264:1146-1155.
13. Dey N, Busch J, Frnacis S, Corbin J, Lincoln T. 2009. Cyclic GMP specifically suppresses type-1α cGMP-dependent protein kinase expression by ubiquitination. Cell Signal 21:859-866.
14. kip1. J Biol Chem 280:15682-15689.
15. Feil R, Lohmann S, de Jonge H, Walter U, Hofmann F. 2003. Cyclic GMP-dependent protein kinases and the cardiovascular system. Insights from genetically modified mice. Circ Res 93:907-916.
16. 2+ signaling in afferent arteriolar vascular smooth muscle. Am J Physiol Heart Circ Physiol 298:H144-H151.
17. Furst R, Brueckl C, Kuebler W, Zahler S, Krotz F, Gorlach A, Vollmar A, Kiemer A. 2005. Atrial natriuretic peptide induces mitogen-activated protein kinase phosphatase-1 in human endothelial cells via Rac1 and NAD(P)H oxidase/Nox2-activation. Circ Res 96:43-53.
18. Hofmann F, Feil R, Kleppisch T, Schlossmann J. 2006. Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol Rev 86:1-23.
19. Horstman D, Fischer L, Kouretas P, Hannan R, Rich G. 2002. Role of nitric oxide in heparin-induced atenuation of hypoxic pulmonary vascular remodeling. J Appl Physiol 92:2012-2018.
20. Jacob A, Molkentin JD, Smolenski A, Lohmann SM, Begum N. 2002. Insulin inhibits PDGF-directed VSMC migration via NO/cGMP increase of MKP-1 and its inactivation of MAPKs. Am J Physiol Cell Physiol 283:C704-C713.
21. Lin G, Chow S, Lin J, Wang G, Lue T, Lin C-S. 2004. Effect of cell passage and density on protein kinase G expression and activation in vascular smooth muscle cells. J Cell Biochem 92:104-112.
22. Lincoln T, Wu X, Sellak H, Dey N, Choi CS. 2006. Regulation of vascular smooth muscle cell phenotype by cyclic GMP and cyclic GMP-dependent protein kinase. Front Biosci 11:356-367.
23. Liu YT, Song L, Templeton DM. 2007. Heparin suppresses lipid raft-mediated signaling and ligand-independent EGF receptor activation. J Cell Physiol 211:205-212.
24. Melichar VO, Behr-Roussel D, Zabel U, Uttenthal LO, Rodrigo J, Rupin A, Verbeuren TJ, Kumar HSA, Schmidt HH. 2004. Reduced cGMP signaling associated with neointimal proliferation and vascular dysfunction in late-stage atherosclerosis. Proc Natl Acad Sci USA 101:16671-16676.
25. Nausch LW, Ledoux J, Bonev AD, Nelson MT, Dostmann WR. 2008. Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc Natl Acad Sci USA 105:365-370.
26. Ottlinger ME, Pukac LA, Karnovsky MJ. 1993. Heparin inhibits mitogen-activated protein kinase activation in intact rat vascular smooth muscle cells. J Biol Chem 268:19173-19176.
27. Patton WAI, Granzow CA, Getts LA, Thomas SC, Zotter LM, Gunzel KA, Lowe-Krentz LJ. 1995. Identification of a heparin-binding protein using monoclonal antibodies that block heparin binding to porcine aortic endothelial cells. Biochem J 311:461-469.
28. 2+ oscillations. J Gen Physiol 135:247-259.
29. Peterson T, Kleppe L, Caplice N, Pan S, Mueske C, Simari R. 1999. The regulation of caveolin expression and localization by serum and heparin in vascular smooth muscle cells. Biochem Biophys Res Commun 265:722-727.
30. Pilz R, Broderick K. 2005. Role of cyclic GMP in gene regulation. Front Biosci 10:1239-1268.
31. Pukac LA, Carter JE, Ottlinger ME, Karnovsky MJ. 1997. Mechanisms of inhibition by heparin of PDGF stimulated MAP kinase activation in vascular smooth muscle cells. J Cell Physiol 172:69-78.
32. 1 phase of the cell cycle. J Biol Chem 264:6990-6995.
33. Rodríguez A, Gómez-Ambrosi J, Catalán V, Fortuno A, Frühbeck G. 2010. Leptin inhibits the proliferation of vascular smooth muscle cells induced by angiotensin II through nitric oxide-dependent mechanisms. Mediators Inflamm. DOI: 10.1155/2010/105489.
34. Rohan PJ, Davis P, Moskaluk CA, Kearns M, Krutzsch H, Siebenlist U, Kelly K. 1993. PAC-1: A mitogen-induced nuclear protein-tyrosine phosphatase. Science 259:1763-1769.
35. Sato J, Nair K, Hiddinga J, Eberhardt N, Fitzpatrick L, Katusic Z, O'Brien T. 2000. ENOS gene transfer to vascular smooth muscle cells inhibits cell proliferation via upregulation of p27 and p21 and not apoptosis. Cardiovasc Res 47:697-706.
36. Savage JM, Gilotti AC, Granzow CA, Molina F, Lowe-Krentz LJ. 2001. Antibodies against a heparin receptor slow cell proliferation and decrease MAPK activation in vascular smooth muscle cells. J Cell Physiol 187:283-293.
37. Schlossmann J, Desch M. 2011. IRAG and novel PKG targeting in the cardiovascular system. Am J Physiol Heart Circ Physiol 301:H672-H682.
38. Schwappacher R, Kilic A, Kojonazarov B, Lang M, Diep T, Zhuang S, Gawlowski T, Schermuly RT, Pfeifer A, Boss GR, Pilz RB. 2013. A molecular mechanism for therapeutic effects of cGMP-elevating agents in pulmonary arterial hypertension. J Biol Chem 288:16557-16566.
39. Shin HS, Lee HJ, Nishida M, Lee MS, Tamura R, Yamashita S, Matsuzawa Y, Lee IK, Koh GY. 2003. Betacellulin and amphiregulin induce upregulation of cyclin D1 and DNA synthesis activity through differential signaling pathways in vascular smooth muscle cells. Circ Res 93:302-310.
40. Su J, Scholz P, Weiss H. 2005. Differential effects of cGMP produced by soluble and particulate guanylyl cyclase on mouse ventricular myocytes. Exp Biol Med 230:242-250.
41. Sugimoto T, Haneda M, Togawa M, Isono M, Shikano T, Araki S, Nakagawa T, Kashiwagi A, Guan KL, Kikkawa R. 1996. Atrial natriuretic peptide induces the expression of MKP-1, a mitogen-activated protein kinase phosphatase, in glomerular mesangial cells. J Biol Chem 271:544-547.
42. Takahashi S, Lin H, Geshi N, Mori Y, Kawarabayashi Y, Takami N, Mori M, Honda A, Inoue R. 2008. Nitric oxide-cGMP-protein kinase G pathway negatively regulates vascular transient receptor potential channel TRPC6. J Physiol 586:4209-4223.
43. Tantini B, Manes A, Fiumana E, Pignatti C, Guarnieri C, Zannoli R, Branzi A, Galie N. 2005. Antiproliferative effect of sildenafil on human pulmonary artery smooth muscle cells. Basic Res Cardiol 100:131-138.
44. Tete H, Schroeder R, Stahl R, Wolf G. 2001. Atrial natriuretic peptide attenuates ANG II-induced hypertrophy of renal tubular cells. Am J Physiol Renal Physiol 281:F81-F90.
45. Wang S, Li Y. 2009. Expression of constitutively active cGMP-dependent protein kinase inhibits glucose-induced vascular smooth muscle cell proliferation. Am J Physiol Heart Circ Physiol 297:H2075-H2083.
46. Wu JJ, Dent P, Jelinek T, Wolfman A, Weber M, Sturgill T. 1993. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3′, 5′-monophosphate. Science 262:1065-1069.
47. Yordy JS, Muise-Helmericks RC. 2000. Signal transduction and the Ets family of transcription factors. Oncogene 19:6503-6513.
48. Zhuang D, Balani P, Pu Q, Thakran S, Hassid A. 2011. Suppression of PKG by PDGF or nitric oxide in differentiated aortic smooth muscle cells: Obligatory role of protein tyrosine phosphatase 1B. Am J Physiol Heart Circ Physiol 300:H57-H63.