The Role of eNOS Phosphorylation in Causing Drug-induced Vascular Injury

Toxicologic Pathology

Volumn 42, Issue 4, 2014, Pages 709-724

  Tobin, Grainne A Mcmahon ^a   Zhang, Jun ^a   Goodwin, David ^a   Stewart, Sharron ^a   xu, Lin ^a   Knapton, Alan ^a   González, Carlos ^a   Bancos, Simona ^a   Zhang, Leshuai ^a,c   Lawton, Michael P ^b   Enerson, Bradley E ^b   Weaver, James L ^a   Morton, Daniel ^c   Tomlinson, Lindsay ^c  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b PFIZER INC   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

animal models; drug development; risk identification; vascular system

Indexed keywords

ADENOSINE; AZEPINE DERIVATIVE; CI 1044; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N-(2,3-DIHYDRO-1H-INDEN-1-YL)ADENOSINE; NICOTINAMIDE; NITRIC OXIDE; NITRITE; NOS3 PROTEIN, RAT; 6 [4 (1,4 DIHYDRO 4 OXO 1 PYRIDYL)PHENYL] 4,5 DIHYDRO 5 METHYL 3(2H) PYRIDAZINONE; FENOLDOPAM; LINSIDOMINE; MIDODRINE; N [9 AMINO 3,4,6,7 TETRAHYDRO 4 OXO 1 PHENYLPYRROLO[3,2,1 J,K][1,4]BENZODIAZEPINE 3 YL] 3 PYRIDINECARBOXAMIDE; N(G) NITROARGININE METHYL ESTER; NICORANDIL; PHOSPHODIESTERASE IV INHIBITOR; UNCLASSIFIED DRUG;

ADVERSE DRUG REACTION; ANALOGS AND DERIVATIVES; ANIMAL; AORTA; BLOOD; BLOOD VESSEL INJURY; CHEMICALLY INDUCED; DOSE RESPONSE; GENETICS; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RAT; SPRAGUE DAWLEY RAT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG INDUCED VASCULAR INJURY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; MESENTERY; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE; ANIMALS; AORTA; AZEPINES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-RELATED SIDE EFFECTS AND ADVERSE REACTIONS; MALE; NIACINAMIDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITRITES; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; VASCULAR SYSTEM INJURIES;

EID: 84902076012     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623314522885     Document Type: Article

References (39)

1. Bauer P. M. Fulton D. Boo Y. C. Sorescu G. P. Kemp B. E. Jo H. Sessa W. C. (2003). Compensatory phosphorylation and protein-protein interactions revealed by loss of function and gain of function mutants of multiple serine phosphorylation sites in endothelial nitric-oxide synthase. J Biol Chem 278, 14841–9.
2. Bjørgo E. Solheim S. A. Abrahamsen H. Baillie G. S. Brown K. M. Berge T. Okkenhaug K. Houslay M. D. Taskén K. (2010). Cross talk between phosphatidylinositol 3-kinase and cyclic AMP (cAMP)-protein kinase a signaling pathways at the level of a protein kinase B/beta-arrestin/cAMP phosphodiesterase 4 complex. Mol Cell Biol 30, 1660–72.
3. Boo Y. C. Hwang J. Sykes M. Michell B. J. Kemp B. E. Lum H. Jo H. (2002). Shear stress stimulates phosphorylation of eNOS at Ser635 by a protein kinase A-dependent mechanism. Am J Physiol Heart Circ Physiol 283, H1819–28.
4. Bredt D. S. Snyder S. H. (1990). Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. PNAS 87, 682–85.
5. Brott D. A. Richardson R. J. Louden C. A. (2012). Evidence for the nitric oxide pathway as a potential mode of action in fenoldopam-induced vascular injury. Toxicol Pathol 40, 874–86.
6. Burnouf C. Auclair E. Avenel N. Bertin B. Bigot C. Calvet A. Chan K. Durand C. Fasquelle V. Féru F. Gilbertsen R. Jacobelli H. Kebsi A. Lallier E. Maignel J. Martin B. Milano S. Ouagued M. Pascal Y. Pruniaux M. P. Puaud J. Rocher M. N. Terrasse C. Wrigglesworth R. Doherty A. M. (2000). Synthesis, structure-activity relationships and pharmacological profile of 9-amino-4-oxo-1-phenyl-3,4,6, 7-trtrahydro[1,4]diazepino[6,7,1-hi]indoles: Discovery of potent selective phosphodiesterase type 4 inhibitors. J Med Chem 43, 4850–67.
7. Cale J. M. Bird I. M. (2006). Dissociation of endothelial nitric oxide synthase phosphorylation and activity in uterine artery endothelial cells. Am J Physiol Heart Circ Physiol 290, H1433–55.
8. Chen Z. P. Mitchelhill K. I. Mitchell B. J. Stapleton D. Rodriguez-Crespo I. Witters L. A. Power D. A. Ortiz de Montellano P. R. Kemp B. E. (1999). AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett 443, 285–9.
9. B.B.J., Dekkers, K., Raké, M., Schmidt, Distinct PKA and Epac compartmentalization in airway function and plasticity, Pharmacol & Therap, (2013), 137, 248-265
10. Desjardins F. Delisle C. Gratton J.-P. (2012). Modulation of the cochaperone AHA1 regulates heat-shock protein 90 and endothelial NO synthase activation by vascular endothelial growth factor. Arterioscler Thromb Vasc Biol 32, 2484–92.
11. Fleming I. (2010). Molecular mechanisms underlying the activation of eNOS. Pflugers Arch 459, 793–806.
12. Förstermann U. Sessa W. C. (2012). Nitric oxide synthases: Regulation and function. Eur Heart J 33, 829–37.
13. Fulton D. Church J. E. Ruan L. Li C. Sood S. G. Kemp B. E. Jennings I. G. Venema R. C. (2005). Src Kinase activates endothelial nitric-oxide synthase by phosphorylating Tyr-83. J Biol Chem 280, 35943–52.
14. Fulton D. Gratton J. P. McCabe T. J. Fontana J. Fujio Y. Walsh K. Franke T. F. Papapetropoulos A. Sessa W. C. (1999). Regulation of endothelium-derived nitric oxide by the protein Akt. Nature 399, 597–601.
15. Fulton D. Ruan L. Sood S. G. Li C. Zhang Q. Venema R. C. (2008). Agonist-stimulated endothelial nitric oxide synthase activation and vascular relaxation. Role of eNOS phosphorylation at Tyr83. Circ Res 102, 497–504.
16. Hanton G. Sobry C. Daguès N. Provost J. -P. Le Net J. -L. Comby P. Chevalier S. (2008). Characterisation of the vascular and inflammatory lesions induced by the PDE4 inhibitor CI-1044 in the dog. Toxicol Lett 179, 15–22.
17. Heaslip R. J. Lombardo L. J. Golankiewicz J. M. Ilsemann B. A. Evans D. Y. Sickels B. D. Mudrick J. K. Bagli J. Weichman B. M. (1994). Phosphodiesterase-IV inhibition, respiratory muscle relaxation and bronchodilation by WAY-PDA-641. J Pharmacol Exp Ther 268, 888–96.
18. Hornbeck P. V. Kornhauser J. M. Tkachev S. Zhang B. Skrypek E. Murray B. Latham V. Sullivan M. (2012). PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40, D261–D270.
19. Kerns W. D. Arena E. Macia R. A. Bugelski P. J. Matthews W. D. Morgan D. G. (1989). Pathogenesis of arterial lesions induced by dopaminergic compounds in the rat. Toxicol Pathol 17, 203–13.
20. Li Y. Zheng J. Bird I. M. Magness R. R. (2005). Effects of pulsatile shear stress on signaling mechanisms controlling nitric oxide production, endothelial nitric oxide synthase phosphorylation, and expression in ovine fetoplacental artery endothelial cells. Endothelium 12, 21–39.
21. Losco P. E. Evans E. W. Barat S. A. Blackshear P. E. Reyderman L. Fine J. S. Bober L. A. Anthes J. C. Mirro E. J. Cuss F. M. (2004). The toxicity of SCH 351591, a novel phosphodiesterase-4 inhibitor, in Cynomolgus monkeys. Toxicol Pathol 32, 295–308.
22. Maurice D. H. (2011). Subcellular signaling in the endothelium: Cyclic nucleotides take their place. Curr Opinion Pharmacol 11, 656–64.
23. Mount P. F. Kemp B. E. Power D. A. (2007). Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 42, 271–9.
24. Pacher P. Beckman J. S. Liaudet L. (2007). Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87, 315–424.
25. Pellegrin M. Miguet-Alfonsi C. Berthelot A. Mazzolai L. Laurant P. (2011). Long-term swimming exercise does not modulate the Akt-dependent endothelial nitric oxide synthase phosphorylation in healthy mice. Can J Physiol Pharmacol 89, 72–76.
26. Sessa W. C. (2004). eNOS at a glance. J Cell Sci 117, 2427–9.
27. Shen B. Kwan H. Y. Ma X. Wong C. O. Du J. Huang Y. Yao X. (2011). cAMP activates TRPC6 channels via the phosphatidylinositol 3-kinase (PI3K)-protein kinase B (PKB)-mitogen-activated protein kinase kinase (MEK)-ERK1/2 signaling pathway. J Biol Chem 286, 19439–45.
28. Sheth C. M. Enerson B. E. Peters D. Lawton M. D. Weaver J. L. (2011). Effects of modulating in vivo nitric oxide production on the incidence and severity of PDE4 inhibitor-induced vascular injury in Sprague-Dawley rats. Toxicol Sci 122, 7–15.
29. Slim R. M. Song Y. Albassam M. Dethloff L. A. (2003). Apoptosis and nitrative stress associated with phosphodiesterase inhibitor-induced mesenteric vasculitis in rats. Toxicol Pathol 31, 638–45.
30. Sobota J. T. (1989). Review of cardiovascular findings in humans treated with minoxidil. Toxicol Pathol 17, 193–202.
31. Tawa H. Rikitake Y. Takahashi M. Amano H. Miyata M. Satomi-Kobayashi S. Kinugasa M. Nagamatsu Y. Majima T. Ogita H. Miyoshi J. Hirata K. Takai Y. (2010). Role of afadin in vascular endothelial growth factor- and sphingosine 1-phosphate-induced angiogenesis. Circ Res 106, 1731–42.
32. van Hooren K. W. van Agtmaal E. L. Fernandez-Borja M. van Mourik J. A. Voorberg J. Bierings R. (2012). The Epac-Rap1 signaling pathway controls cAMP-mediated exocytosis of Weibel-Palade bodies in endothelial cells. J Biol Chem 287, 24713–20.
33. Weaver J. L. Snyder R. Knapton A. Herman E. H. Honchel R. Miller T. Espandiari P. Smith R. Gu Y. -Z. Goodsaid F. M. Rosenblum I. Y. Sistare F. D. Zhang J. Hanig J. (2008). Biomarkers in peripheral blood associated with vascular injury in Sprague-Dawley rats treated with the phosphodiesterase IV inhibitors SCH 351591 and SCH 534385. Toxicol Pathol 36, 840–9.
34. Weaver J. L. Zhang J. Knapton A. Miller T. Espandiari P. Smith R. Gu Y. -Z. Snyder R. D. (2010). Early events in vascular injury in the rat induced by the phosphodiesterase IV inhibitor SCH 351591. Toxicol Pathol 38, 738–44.
35. Yamanaka D. Akama T. Fukushima T. Nedachi T. Kawasaki C. Chida K. Minami S. Suzuki K. Hakuno F. Takahashi S. (2012). Phosphatidylinositol 3-kinase-binding protein, PI3KAP/XB130, is required for cAMP-induced amplification of IGF mitogenic activity in FRTL-5 thyroid cells. Mol Endocrinol 26, 1043–55.
36. Zhang J. Herman E. H. Knapton A. Chadwick D. P. Whitehurst V. E. Koerner J. E. Papoian T. Ferrans V. J. Sistare F. D. (2002). SK&F 95654-induced acute cardiovascular toxicity in Sprague-Dawley rats-histopathologic, electron microscopic and immunohistochemical studies. Toxicol Pathol 30, 152–63.
37. Zhang J. Snyder R. D. Herman E. H. Knapton A. Honchel R. Miller T. Espandiari P. Goodsaid F. M. Rosenblum I. Y. Hanig J. P. Sistare F. D. Weaver J. L. (2008). Histopathology of vascular injury in Sprague-Dawley rats treated with phosphodiesterase IV inhibitor SCH 351591 or SCH 534385. Toxicol Pathol 36, 827–39.
38. Zhang Q. J. McMillin S. L. Tanner J. M. Palionyte M. Abel E. D. Symons J. D. (2009). Endothelial nitric oxide synthase phosphorylation in treadmill-running mice: Role of vascular signaling kinases. J Physiol 587, 3922–20.
39. Zhang X.-P. Hintze T. H. (2006). cAMP signal transduction induces eNOS activation by promoting PKB phosphorylation. Am J Physiol Heart Circ Physiol 290, H2376–2384.