Protein kinase C delta contributes to increase in EP3 agonist-induced contraction in mesenteric arteries from type 2 diabetic Goto-Kakizaki rats

Pflugers Archiv European Journal of Physiology

Volumn 463, Issue 4, 2012, Pages 593-602

  Ishida, Keiko ^a   Matsumoto, Takayuki ^a   Taguchi, Kumiko ^a   Kamata, Katsuo ^a   Kobayashi, Tsuneo ^a  

^a HOSHI UNIVERSITY   (Japan)

Author keywords

Caldesmon; PGE 2; PKC ; Type 2 diabetes; Vasocontraction

Indexed keywords

1 ACETYL 2 (8 CHLORO 10,11 DIHYDRODIBENZ[B,F][1,4]OXAZEPINE 10 CARBONYL)HYDRAZINE; 12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; CALDESMON; NITRIC OXIDE SYNTHASE INHIBITOR; PROSTAGLANDIN E RECEPTOR 3; PROSTAGLANDIN E2; PROTEIN KINASE C DELTA; ROTTLERIN; SULPROSTONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY CONSTRICTION; ARTERY TONE; ARTICLE; CONTROLLED STUDY; DIABETIC ANGIOPATHY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GOTO KAKIZAKI RAT; MALE; MUSCLE ISOMETRIC CONTRACTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SUPERIOR MESENTERIC ARTERY; UPREGULATION;

ANIMALS; CALMODULIN-BINDING PROTEINS; DIABETES MELLITUS, TYPE 2; DINOPROSTONE; MALE; MESENTERIC ARTERIES; MUSCLE, SMOOTH, VASCULAR; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; RATS; RATS, WISTAR; RECEPTORS, PROSTAGLANDIN E, EP3 SUBTYPE; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS;

EID: 84862782483     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-012-1088-9     Document Type: Article

References (69)

1. Adamis AP (2002) Is diabetic retinopathy an inflammatory disease? Br J Ophthalmol 86:363-365
2. Allahdadi KJ, Duling LC, Walker BR, Kanagy NL (2008) Eucapnic intermittent hypoxia augments endothelin-1 vasoconstriction in rats: role of PKCdelta. Am J Physiol Heart Circ Physiol 294:H920-H927 (Pubitemid 351253304)
3. Ayalasomayajula SP, Amrite AC, Kompella UB (2004) Inhibition of cyclooxygenase-2, but not cyclooxygenase-1, reduces prostaglandin E2 secretion from diabetic rat retinas. Eur J Pharmacol 498:275-278 (Pubitemid 39208089)
4. Bagi Z, Erdei N, Toth A, Li W, Hintze TH, Koller A, Kaley G (2005) Type 2 diabetic mice have increased arteriolar tone and blood pressure: enhanced release of COX-2-derived constrictor prostaglandins. Arterioscler Thromb Vasc Biol 25:1610-1616 (Pubitemid 41098929)
5. Barton M (2010) Obesity and aging: determinants of endothelial cell dysfunction and atherosclerosis. Pflugers Arch 460:825-837
6. Boer U, Neuschafer-Rube F, Moller U, Puschel GP (2000) Requirement of N-glycosylation of the prostaglandin E2 receptor EP3beta for correct sorting to the plasma membrane but not for correct folding. Biochem J 350:839-847
7. Casado V, Cortes A, Mallol J, Perez-Capote K, Ferre S, Lluis C, Franco R, Canela EI (2009) GPCR homomers and heteromers: a better choice as targets for drug development than GPCRmonomers? Pharmacol Ther 124:248-257
8. Cheng T, Cao W, Wen R, Steinberg RH, LaVail MM (1998) Prostaglandin E2 induces vascular endothelial growth factor and basic fibroblast growth factor mRNA expression in cultured rat Muller cells. Invest Ophthalmol Vis Sci 39:581-591 (Pubitemid 28110692)
9. Coleman RA, Smith WL, Narumiya S (1994) International Union of Pharmacology classification of prostanoid receptors: properties, distribution, and structure of the receptors and their subtypes. Pharmacol Rev 46:205-229 (Pubitemid 24185151)
10. Das Evcimen N, King GL (2007) The role of protein kinase C activation and the vascular complications of diabetes. Pharmacol Res 55:498-510 (Pubitemid 46962309)
11. Ding H, Triggle CR (2010) Endothelial dysfunction in diabetes: multiple targets for treatment. Pflugers Arch 459:977-994
12. Dowal L, Flaumenhaft R (2010) Targeting platelet G-protein coupled receptors (GPCRs): looking beyond conventional GPCR antagonism. Curr Vasc Pharmacol 8:140-154
13. Ergul A (2011) Endothelin-1 and diabetic complications: focus on the vasculature. Pharmacol Res 63:477-482
14. Feletou M, Huang Y, Vanhoutte PM (2010) Vasoconstrictor prostanoids. Pflugers Arch 459:941-950
15. Fleming I (2010) Molecular mechanisms underlying the activation of eNOS. Pflugers Arch 459:793-806
16. Gao Y (2010) The multiple actions of NO. Pflugers Arch 459:829-839
17. Goto Y, Kakizaki M, Masaki N (1976) Production of spontaneous diabetic rats by repetition of selective breeding. Tohoku J Exp Med 119:85-90
18. Hadi HA, Suwaidi JA (2007) Endothelial dysfunction in diabetes mellitus. Vasc Health Risk Manag 3:853-876
19. Hilgers RH, Webb RC (2005) Molecular aspects of arterial smooth muscle contraction: focus on Rho. Exp Biol Med 230:829-835 (Pubitemid 41785882)
20. Horowitz A, Menice CB, Laporte R, Morgan KG (1996) Mechanisms of smooth muscle contraction. Physiol Rev 76:967-1003 (Pubitemid 26346813)
21. Huang C, Tai HH (1998) Prostaglandin E2 receptor EP3alpha subtype: the role of N-glycosylation in ligand binding as revealed by site-directed mutagenesis. Prostaglandins Leukot Essent Fatty Acids 59:265-271 (Pubitemid 28523776)
22. Idris I, Gray S, Donnelly R (2001) Protein kinase C activation: isozyme-specific effects on metabolism and cardiovascular complications in diabetes. Diabetologia 44:659-673 (Pubitemid 32846021)
23. Ikebe M, Hornick T (1991) Determination of the phosphorylation sites of smooth muscle caldesmon by protein kinase C. Arch Biochem Biophys 288:538-542
24. Ishida K, Matsumoto T, Taguchi K, Kamata K, Kobayashi T (2011) Mechanisms underlying altered extracellular nucleotide-induced contractions in mesenteric arteries from rats in later-stage type 2 diabetes: effect of ANG II type 1 receptor antagonism. Am J Physiol Heart Circ Physiol 301:H1850-H1861
25. Jadhav V, Jabre A, Lin SZ, Lee TJ (2004) EP1- and EP3-receptors mediate prostaglandin E2-induced constriction of porcine large cerebral arteries. J Cereb Blood Flow Metab 24:1305-1316 (Pubitemid 40019155)
26. Jones RL, Qian YM, Chan KM, Yim AP (1998) Characterization of a prostanoid EP3-receptor in guinea-pig aorta: partial agonist action of the non-prostanoid ONO-AP-324. Brit J Pharmacol 125:1288-1296 (Pubitemid 28542539)
27. 2. Brit J Pharmacol 162:521-531
28. Kashihara T, Nakayama K, Ishikawa T (2008) Distinct roles of protein kinase C isoforms in myogenic constriction of rat posterior cerebral arteries. J Pharmacol Sci 108:446-454
29. Kazuyama E, Saito M, Kinoshita Y, Satoh I, Dimitriadis F, Satoh K (2009) Endothelial dysfunction in the early- and late-stage type 2 diabetic Goto-Kakizaki rat aorta. Mol Cell Biochem 332:95-102
30. Kelly-Cobbs A, Elgebaly MM, Li W, Ergul A (2011) Pressureindependent cerebraovascular remodeling and changes in myogenic reactivity in diabetic Goto-Kakizaki rat in response to glycaemic control. Acta Physiol 203:245-251
31. Kim HR, Appel S, Vetterkind S, Gangopadhyay SS, Morgan KG (2008) Smooth muscle signalling pathways in health and disease. J Cell Mol Med 12:2165-2180
32. Kobayashi K, Murata T, Hori M, Ozaki H (2011) Prostaglandin E2-prostanoid EP3 signal induces vascular contraction via nPKC and ROCK activation in rat mesenteric artery. Eur J Pharmacol 660:375-380
33. Kobayashi T, Matsumoto T, Ooishi K, Kamata K (2004) Differential expression of alpha2D-adrenoceptor and eNOS in aortas from early and later stages of diabetes in Goto-Kakaizaki rats. Am J Physiol Heart Circ Physiol 287:H135-H143 (Pubitemid 38802345)
34. Koller A, Kaley G (1990) Prostaglandins mediate arteriolar dilation to increased blood flow velocity in skeletal muscle microcirculation. Circ Res 67:529-534 (Pubitemid 20242595)
35. Li X, Ma C, Zhu D, Meng L, Guo L, Wang Y, Zhang L, Li Z, Li E (2010) Increased expression and altered subcellular distribution of PKC-δ and PKC-ε in pulmonary arteries exposed to hypoxia and 15-HETE. Prostaglandins Other Lipid Mediat 93:84-92
36. Matsumoto T, Ishida K, Nakayama N, Kobayashi T, Kamata K (2009) Involvement of NO and MEK/ERK pathway in enhancement of endothelin-1-induced mesenteric artery contraction in later-stage type 2 diabetic Goto-Kakizaki rat. Am J Physiol Heart Circ Physiol 296:H1388-H1397
37. Matsumoto T, Ishida K, Nakayama N, Taguchi K, Kobayashi T, Kamata K (2010) Mechanisms underlying the losartan treatmentinduced improvement in the endothelial dysfunction seen in mesenteric arteries from type 2 diabetic rats. Pharmacol Res 62:271-281
38. Matsumoto T, Ishida K, Taguchi K, Kobayashi T, Kamata K (2010) Losartan normalizes endothelium-derived hyperpolarizing factor-mediated relaxation by activating Ca2+-activated K+channels in mesenteric artery from type 2 diabetic GK rat. J Pharmacol Sci 112:299-309
39. Matsumoto T, Ishida K, Taguchi K, Kobayashi T, Kamata K (2010) Short-term angiotensin-1 receptor antagonism in type 2 diabetic Goto-Kakizaki rats normalizes endothelin-1-induced mesenteric artery contraction. Peptides 31:609-617
40. McCormick C, Jones RL, Kennedy S, Wadsworth RM (2010) Activation of prostanoid EP receptors by prostacyclin analogues in rabbit iliac artery: implications for anti-restenotic potential. Eur J Pharmacol 641:160-167
41. Michel T, Vanhoutte PM (2010) Cellular signaling and NO production. Pflugers Arch 459:807-816
42. Myers TO, Messina EJ, Rodrigues AM, Gerritsen ME (1985) Altered aortic and cremaster muscle prostaglandin synthesis in diabetic rats. Am J Physiol 249:E374-E379 (Pubitemid 16201161)
43. Narumiya S, Sugimoto Y, Ushikubi F (1999) Prostanoid receptors: structures, properties, and functions. Physiol Rev 79:1193-1226 (Pubitemid 29473315)
44. Natarajan R, Nadler JL (2004) Lipid inflammatory mediators in diabetic vascular disease. Arterioscler Thromb Vasc Biol 24:1542-1548 (Pubitemid 39180875)
45. Nemoto S, Kobayashi T, Taguchi K, Matsumoto T, Kamata K (2011) Losartan improves aortic endothelium-dependent relaxation via proline-rich tyrosine kinase 2/Src/Akt pathway in type 2 diabetic Goto-Kakizaki rats. Am J Physiol Heart Circ Physiol 301:H2383-H2394
46. Obara K, Nishizawa S, Koide M, Nozawa K, Mitate A, Ishikawa T, Nakayama K (2005) Interactive role of protein kinase C-delta with rho-kinase in the development of cerebral vasospasm in a canine two-hemorrhage model. J Vasc Res 42:67-76 (Pubitemid 40187044)
47. Okon EB, Szado T, Laher I, McManus B, van Breemen C (2003) Augmented contractile response of vascular smooth muscle in a diabetic mouse model. J Vasc Res 40:520-530 (Pubitemid 38186462)
48. Parekh DB, ZieglerW, Parker PJ (2000) Multiple pathways control protein kinase C phosphorylation. EMBO J 19:496-503 (Pubitemid 30093722)
49. Potenza MA, Nacci C, Gagliardi S, Montagnani M (2011) Cardiovascular complications in diabetes: lessons from animal models. Curr Med Chem 18:1806-1819
50. Qian YM, Jones RL, Chan KM, Stock AI, Ho JK (1994) Potent contractile actions of prostanoid EP3-receptor agonists on human isolated pulmonary artery. Brit J Pharmacol 113:369-374 (Pubitemid 24310729)
51. Reaven GM (2011) Insulin resistance: the link between obesity and cardiovascular disease. Med Clin North Am 95:875-892
52. Sachidanandam K, Elgebaly MM, Harris AK, Hutchinson JR, Mezzetti EM, Portik-Dobos V, Ergul A (2008) Effect of chronic and selective endothelin receptor antagonism on microvascular function in type 2 diabetes. Am J Physiol Heart Circ Physiol 294:H2743-H2749
53. Salamanca DA, Khalil RA (2005) Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension. Biochem Pharmacol 70:1537-1547 (Pubitemid 41540347)
54. Schubert R, Lidington D, Bolz SS (2008) The emerging role of Ca2+ sensitivity regulation in promoting myogenic vasoconstriction. Cardiovasc Res 77:8-18 (Pubitemid 351195169)
55. Shum WW, Le GY, Jones RL, Gurney AM, Sasaki Y (2003) Involvement of Rho-kinase in contraction of guinea-pig aorta induced by prostanoid EP3 receptor agonists. Brit J Pharmacol 139:1449-1461 (Pubitemid 37174659)
56. Sobue K, Sellers JR (1991) Caldesmon, a novel regulatory protein in smooth muscle and nonmuscle actomyosin systems. J Biol Chem 266:12115-12118 (Pubitemid 21907062)
57. Soltoff SP (2007) Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta. Trends Pharmacol Sci 28:453-458
58. Sterin-Borda L, Franchi AM, Borda ES, Del Castillo E, Gimeno MF, Gimeno AL (1984) Augmented thromboxane generation by mesenteric arteries from pancreatectomized diabetic dogs is coincident with the vascular tone enhancement evoked by Na arachidonate and prostacyclin. Eur J Pharmacol 103:211-221 (Pubitemid 14028976)
59. Sun H, Kanamaru K, Ito M, Suzuki H, Kojima T, Waga S, Kureishi Y, Nakano T (1998) Myosin light chain phosphorylation and contractile proteins in a canine two-hemorrhage model of subarachnoid hemorrhage. Stroke 29:2149-2154 (Pubitemid 28443533)
60. Tanaka T, Ohta H, Kanda K, Tanaka T, Hidaka H, Sobue K (1990) Phosphorylation of high-Mr caldesmon by protein kinase C modulates the regulatory function of this protein on the interaction between actin and myosin. Eur J Biochem 188:495-500 (Pubitemid 20109501)
61. Tang EH, Jensen BL, Skott O, Leung GP, Feletou M, Man RY, Vanhoutte PM (2008) The role of prostaglandin E and thromboxaneprostanoid receptors in the response to prostaglandin E2 in the aorta ofWistar Kyoto rats and spontaneously hypertensive rats. Cardiovasc Res 78:130-138 (Pubitemid 351430954)
62. Ueki N, Sobue K, Kanda K, Hada T, Higashino K (1987) Expression of high and low molecular weight caldesmons during phenotypic modulation of smooth muscle cells. Proc Natl Acad Sci USA 84:9049-9053
63. Van Crombruggen K, Van Nassauw L, Derycke L, Timmermans JP, Holtappels G, Hall D, Bachert C (2011) Capsaicin-induced vasodilatation in human nasal vasculature is mediated by modulation of cyclooxygenase-2 activity and abrogated by sulprostone. Naunyn Schmiedebergs Arch Pharmacol 383:613-626
64. Virdis A, Ghiadoni L, Taddei S (2010) Human endothelial dysfunction: EDCFs. Pflugers Arch 459:1015-1023
65. Walsh MP, Horowitz A, Clement-Chomienne O, Andrea JE, Allen BG, Morgan KG (1996) Protein kinase C mediation of Ca(2+)- independent contractions of vascular smooth muscle. Biochem Cell Biol 74:485-502 (Pubitemid 126734111)
66. Woodward DF, Jones RL, Narumiya S (2011) International Union of Basic and Clinical Pharmacology. LXXXIII: classification of prostanoid receptors, updating 15 years of progress. Pharmacol Rev 63:471-538
67. Wright DH, Abran D, Bhattacharya M, Hou X, Bernier SG, Bouayad A, Fouron JC, Vazquez-Tello A, Beauchamp MH, Clyman RI, Peri K, Varma DR, Chemtob S (2001) Prostanoid receptors: ontogeny and implications in vascular physiology. Am J Physiol Regul Integr Comp Physiol 281:R1343-R1360
68. Yamagishi S, Nakamura K, Matsui T (2009) Regulation of advanced glycation end product (AGE)-receptor (RAGE) system by PPAR gamma agonists and its implication in cardiovascular disease. Pharmacol Res 60:174-178
69. Yuhki K, Kojima F, Kashiwagi H, Kawabe J, Fujino T, Narumiya S, Ushikubi F (2011) Roles of prostanoids in the pathogenesis of cardiovascular diseases: novel insights fromknockoutmouse studies. Pharmacol Ther 129:195-205