Modulation of VEGF-induced endothelial cell cycle protein expression through cyclic AMP hydrolysis by PDE2 and PDE4

Thrombosis and Haemostasis

Volumn 92, Issue 3, 2004, Pages 634-645

  Favot, Laure ^a   Keravis, Thérèse ^a   Lugnier, Claire ^a  

^a CNRS   (France)

Author keywords

Angiogenesis and inhibitors; Endothelial cells; Gene expression; Protein function activity; Signal transduction

Indexed keywords

CELL CYCLE PROTEIN; CYCLIC AMP; CYCLIN A; CYCLIN D1; ISOENZYME; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHODIESTERASE; PHOSPHODIESTERASE INHIBITOR; PHOSPHODIESTERASE IV; PICLAMILAST; PROTEIN P21; PROTEIN P27; PROTEIN P42; PROTEIN P44; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; SIGNAL TRANSDUCTION; UPREGULATION;

3',5'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASE; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC AMP; CYCLIN A; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HUMANS; HYDROLYSIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; PHOSPHORIC DIESTER HYDROLASES; UMBILICAL VEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 4544298774     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH03-12-0768     Document Type: Article

References (56)

1. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-6.
2. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996; 86: 353-64.
3. Risau W. Mechanisms of angiogenesis. Nature 1997; 386: 671-4.
4. Leitman DC, Fiscus RR, Murad F. Forskolin, phosphodiesterase inhibitors, and cyclic AMP analogs inhibit proliferation of cultured bovine aortic endothelial cells. J Cell Physiol 1986; 127: 237-43.
5. D'Angelo G, Lee H, Weiner RI. cAMP-dependent protein kinase inhibits the mitogenic action of vascular endothelial growth factor and fibroblast growth factor in capillary endothelial cells by blocking Raf activation. J Cell Biochem 1997; 67: 353-66.
6. Favot L, Keravis T, Holl V, et al. VEGF-induced HUVEC migration and proliferation are decreased by PDE2 and PDE4 inhibitors. Thromb Haemost 2003; 90: 334-43.
7. Vadiveloo PK, Filonzi EL, Stanton HR, et al. G1 phase arrest of human smooth muscle cells by heparin, IL-4 and cAMP is linked to repression of cyclin D1 and cdk2. Atherosclerosis 1997; 133: 61-9.
8. Cook SJ, McCormick F. Inhibition by cAMP of Ras-dependent activation of Raf. Science 1993; 262: 1069-72.
9. Nigg EA. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 1995; 17: 471-80.
10. Vidal A, Koff A. Cell-cycle inhibitors: three families united by a common cause. Gene 2000; 247: 1-15.
11. Mehats C, Andersen CB, Filopanti M, et al. Cyclic nucleotide phosphodiesterases and their role in endocrine cell signaling. Trends Endocrinol Metab 2002; 13: 29-35.
12. Soderling SH, Beavo JA. Regulation of cAMP and cGMP signaling: new phosphodiesterases and new functions. Curr Opin Cell Biol 2000; 12: 174-9.
13. Francis SH, Turko IV, Corbin JD. Cyclic nucleotide phosphodiesterases: relating structure and function. Prog Nucleic Acid Res Mol Biol 2001; 65: 1-52.
14. Coudray C, Charon C, Komas N, et al. Evidence for the presence of several phosphodiesterase isoforms in brown adipose tissue of Zucker rats: modulation of PDE2 by the fa gene expression. FEBS Lett 1999; 456: 207-10.
15. Meacci E, Taira M, Moos Jr M, et al. Molecular cloning and expression of human myocardial cGMP-inhibited cAMP phosphodiesterase. Proc Natl Acad Sci USA 1992; 89: 3721-5.
16. Miki T, Taira M, Hockman S, et al. Characterization of the cDNA and gene encoding human PDE3B, the cGIP1 isoform of the human cyclic GMP-inhibited cyclic nucleotide phosphodiesterase family. Genomics 1996; 36: 476-85.
17. Takahashi SI, Nedachi T, Fukushima T, et al. Long-term hormonal regulation of the cAMP-specific phosphodiesterases in cultured FRTL-5 thyroid cells. Biochim Biophys Acta 2001; 1540: 68-81.
18. Klein-Soyer C, Beretz A, Millon-Collard R, et al. A simple in vitro model of mechanical injury of confluent cultured endothelial cells to study quantitatively the repair process. Thromb Haemost 1986; 56: 232-5.
19. Lowry OH, Rosebrough NJ, Farr AL, et al. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193: 265-75.
20. Keravis TM, Wells JN, Hardman JG. Cyclic nucleotide phosphodiesterase activities from pig coronary arteries. Lack of interconvertibility of major forms. Biochim Biophys Acta 1980; 613: 116-29.
21. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-9.
22. Lehrach H, Diamond D, Wozney JM, et al. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry 1977; 16: 4743-51.
23. Lugnier C, Keravis T, Le Bec A, et al. Characterization of cyclic nucleotide phosphodiesterase isoforms associated to isolated cardiac nuclei. Biochim Biophys Acta 1999; 1472: 431-46.
24. Podzuweit T, Nennstiel P, Muller A. Isozyme selective inhibition of cGMP-stimulated cyclic nucleotide phosphodiesterases by erythro-9-(2-hydroxy-3-nonyl) adenine. Cell Signal 1995; 7: 733-8.
25. Stoclet JC, Keravis T, Komas N, et al. Cyclic nucleotide phosphodiesterase as therapeutic targets in cardiovascular diseases. Exp Opin Invest Drugs 1995; 4: 1081-100.
26. van Oirschot BA, Stahl M, Lens SM, et al. Protein kinase A regulates expression of p27(kip1) and cyclin D3 to suppress proliferation of leukemic T cell lines. J Biol Chem 2001; 276: 33854-60.
27. Ogawa R, Streiff MB, Bugayenko A, et al. Inhibition of PDE4 phosphodiesterase activity induces growth suppression, apoptosis, glucocorticoid sensitivity, p53, and p21(WAF1/CIP1) proteins in human acute lymphoblastic leukemia cells. Blood 2002; 99: 3390-7.
28. Papapetropoulos A, Garcia-Cardena G, Madri JA, et al. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 1997; 100: 3131-9.
29. Liu H, Maurice DH. Phosphorylation-mediated activation and translocation of the cyclic AMP-specific phosphodiesterase PDE4D3 by cyclic AMP-dependent protein kinase and mitogen-activated protein kinases. A potential mechanism allowing for the coordinated regulation of PDE4D activity and targeting. J Biol Chem 1999; 274: 10557-65.
30. Baillie GS, MacKenzie SJ, McPhee I, et al. Sub-family selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 2000; 131: 811-9.
31. Baillie G, MacKenzie SJ, Houslay MD. Phorbol 12-myristate 13-acetate triggers the protein kinase A-mediated phosphorylation and activation of the PDE4D5 cAMP phosphodiesterase in human aortic smooth muscle cells through a route involving extracellular signal regulated kinase (ERK). Mol Pharmacol 2001; 60: 1100-11.
32. MacKenzie SJ, Baillie GS, McPhee I, et al. ERK2 mitogen-activated protein kinase binding, phosphorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases. The involvement of COOH-terminal docking sites and NH2-terminal UCR regions. J Biol Chem 2000; 275: 16609-17.
33. Vicini E, Conti M. Characterization of an intronic promoter of a cyclic adenosine 3′,5′-monophosphate (cAMP)-specific phosphodiesterase gene that confers hormone and cAMP inducibility. Mol Endocrinol 1997; 11: 839-50.
34. Mayo LD, Kessler KM, Pincheira R, et al. Vascular endothelial cell growth factor activates CRE-binding protein by signaling through the KDR receptor tyrosine kinase. J Biol Chem 2001; 276: 25184-9.
35. 2+-linked increase in coupled cAMP synthesis and hydrolysis is an early event in cholinergic and beta-adrenergic stimulation of parotid secretion. Proc Natl Acad Sci U S A 1988; 85: 7867-71.
36. Georget M, Mateo P, Vandecasteele G, et al. Cyclic AMP compartmentation due to increased cAMP-phosphodiesterase activity in transgenic mice with a cardiac-directed expression of the human adenylyl cyclase type 8 (AC8). FASEB J 2003; 17: 1380-91.
37. Houslay MD, Milligan G. Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem Sci 1997; 22: 217-24.
38. Yu Y, Sato D. MAP Kinases, Phosphatidylinositol 3-kinase, and p70 S6 kinase mediate the mitogenic response of human endothelial cells to vascular endothelial growth factor. J Cell Physiol 1999; 178: 235-46.
39. Pursiheimo JP, Kieksi A, Jalkanen M, et al. Protein kinase A balances the growth factor-induced Ras/ERK signaling. FEBS Lett 2002; 521: 157-64.
40. Koyama H, Bornfeldt KE, Fukumoto S, et al. Molecular pathways of cyclic nucleotide-induced inhibition of arterial smooth muscle cell proliferation. J Cell Physiol 2001; 186: 1-10.
41. Schaeffer HJ, Schwender CF. Enzyme inhibitors: Bridging hydrophobic and hydrophilic regions on adenosine deaminase with some 9-(2-hydroxy-3-alkyl)adenines. J Med Chem 1974; 17: 6-8.
42. Smolenski RT, Kochan Z, McDouall R, et al. Endothelial nucleotide catabolism and adenosine production. Cardiovasc Res 1994; 8: 100-4.
43. Sexl V, Mancusi G, Baumgartner-Parzer S, et al. Stimulation of human umbilical vein endothelial cell proliferation by A2-adenosine and beta 2-adrenoceptors. Br J Pharmacol 1995; 114: 1577-86.
44. Elsayed YA, Sausville EA. Selected novel anticancer treatments targeting cell signaling proteins. Oncologist 2001; 6: 517-57.
45. Sherr CJ, Roberts JM. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 1995; 9: 1149-63.
46. Goukassian D, Diez-Juan A, Asahara T, et al. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J 2001; 15: 1877-85.
47. Bastians H, Townsley FM, Ruderman JV. The cyclin-dependent kinase inhibitor p27(Kip1) induces N-temninal proteolytic cleavage of cyclin A. Proc Natl Acad Sci USA 1998; 95: 15374-81.
48. Hsieh TC, Juan G, Darzynkiewicz Z, et al. Resveratrol increases nitric oxide synthase, induces accumulation of p53 and p21(WAF1/CIP1), and suppresses cultured bovine pulmonary artery endothelial cell proliferation by perturbing progression through S and G2. Cancer Res 1999; 59: 2596-601.
49. Kato JY, Matsuoka M, Polyak K, et al. Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell 1994; 79: 487-96.
50. Lee TH, Chuang LY, Hung WC. Induction of p21WAF1 expression via Sp1-binding sites by tamoxifen in estrogen receptor-negative lung cancer cells. Oncogene 2000; 19: 3766-73
51. Lee HT, Kay EP. Regulatory role of cAMP on expression of Cdk4 and p27(Kip1) by inhibiting phosphatidylinositol 3-kinase in corneal endothelial cells. Invest Ophthalmol Vis Sci 2003; 44: 3816-25.
52. Houslay MD, Adams DR. PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 2003; 370: 1-18.
53. Dell'Acqua ML, Scott JD. Protein kinase A anchoring. J Biol Chem 1997; 272: 12881-4.
54. Dodge KL, Khouangsathiene S, Kapiloff MS, et al. mAKAP assembles a protein kinase A/PDE4 phosphodiesterase cAMP signaling module. EMBO J 2001; 20: 1921-30.
55. Terry R, Cheung YF, Praestegaard M, et al. Occupancy of the catalytic site of the PDE4A4 cyclic AMP phosphodiesterase by rolipram triggers the dynamic redistribution of this specific isoform in living cells through a cyclic AMP independent process. Cell Signal 2003; 15: 955-71.
56. Fukumoto S, Koyama H, Hosoi M, et al. Distinct role of cAMP and cGMP in the cell cycle control of vascular smooth muscle cells: cGMP delays cell cycle transition through suppression of cyclin D1 and cyclin-dependent kinase 4 activation. Circ Res 1999; 85: 985-91.