Diabetes-induced activation of protein kinase C inhibits store-operated Ca2+ uptake in rat retinal microvascular smooth muscle

Diabetologia

Volumn 46, Issue 9, 2003, Pages 1252-1259

  Curtis, T M ^a   Major, E H ^a   Trimble, E R ^a   Scholfield, C N ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Diabetes; L type Ca2+ channels; Microvessels; Protein kinase C; Retinal arterioles; Store operated Ca2+ channels

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM ION; CYCLOPIAZONIC ACID; FURA 2; INSULIN; LY 379196; MANNITOL; PHORBOL 13 ACETATE 12 MYRISTATE; POTASSIUM CHLORIDE; PROTEIN KINASE C; PROTEIN KINASE C ACTIVATOR; PROTEIN KINASE C BETA; PROTEIN KINASE C INHIBITOR; STAUROSPORINE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; CALCIUM DEPLETION; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; DIABETIC RETINOPATHY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; EXPOSURE; INJECTION; MALE; MICROFLUOROMETRY; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA ARTERY; RETINA BLOOD VESSEL; SMOOTH MUSCLE;

ANIMALS; ARTERIOLES; BIOLOGICAL TRANSPORT; BLOOD GLUCOSE; CALCIUM; DIABETES MELLITUS, EXPERIMENTAL; ENZYME ACTIVATION; ENZYME INHIBITORS; INDOLES; KINETICS; MALE; MANNITOL; MICROCIRCULATION; MUSCLE, SMOOTH, VASCULAR; MYCOTOXINS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; REFERENCE VALUES; RETINAL VESSELS; TETRADECANOYLPHORBOL ACETATE;

EID: 0141706414     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-003-1178-5     Document Type: Article

References (52)

1. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus (1993). The Diabetes Control and Complications Trial Research Group. N Engl J Med 329:977-986
2. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33) (1998). UK Prospective Diabetes Study (UKPDS) Group. Lancet 352:837-853
3. Grunwald JE, Brucker AJ, Schwartz SS et al. (1990) Diabetic glycemic control and retinal blood flow. Diabetes 39:602-607
4. Kohner EM, Patel V, Rassam SM (1995) Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 44:603-607
5. Schmetterer L, Wolzt M (1999) Ocular blood flow and associated functional deviations in diabetic retinopathy. Diabetologia 42:387-405
6. Kuwabara T, Cogan DG (1963) Retinal Vascular Patterns. VI. Mural Cells of the retinal capillaries. Arch Ophthalmol 69:492-502
7. Gardiner TA, Stitt AW, Anderson HR et al. (1994) Selective loss of vascular smooth muscle cells in the retinal microcirculation of diabetic dogs. Br J Ophthalmol 78:54-60
8. Bresnick GH, Davis MD, Myers FL et al. (1977) Clinicopathologic correlations in diabetic retinopathy. II. Clinical and histologic appearances of retinal capillary microaneurysms. Arch Ophthalmol 95:1215-1220
9. Engerman RL (1989) Pathogenesis of diabetic retinopathy. Diabetes 38:1203-1206
10. Kohner EM, Henkind P (1970) Correlation of fluorescein angiogram and retinal digest in diabetic retinopathy. Am J Ophthalmol 69:403-414
11. Koya D, King GL (1998) Protein kinase C activation and the development of diabetic complications. Diabetes 47: 859-866
12. Shiba T, Inoguchi T, Sportsman JR et al. (1993) Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am J Physiol 265:E783-E793
13. Xia P, Inoguchi T, Kern TS et al. (1994) Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes 43:1122-1129
14. Frank RN (2002) Potential new medical therapies for diabetic retinopathy: protein kinase C inhibitors. Am J Ophthalmol 133:693-698
15. Gopalakrishna R, Jaken S (2000) Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28:1349-1361
16. McPhail LC, Clayton CC, Snyderman R (1984) A potential second messenger role for unsaturated fatty acids: activation of Ca2+-dependent protein kinase. Science 224:622-625
17. Scholfield CN, Curtis TM (2000) Heterogeneity in cytosolic calcium regulation among different microvascular smooth muscle cells of the rat retina. Microvasc Res 59: 233-242
18. Carmo A, Cunha-vaz JG, Carvalho AP et al. (2000) Nitric oxide synthase activity in retinas from non-insulin-dependent diabetic Goto-Kakizaki rats: correlation with blood-retinal barrier permeability. Nitric Oxide 4:590-596
19. Takeda M, Mori F, Yoshida A et al. (2001) Constitutive nitric oxide synthase is associated with retinal vascular permeability in early diabetic rats. Diabetologia 44:1043-1050
20. Abu El-Asrar AM, Desmet S, Meersschaert A et al. (2001) Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus. Am J Ophthalmol 132:551-556
21. Johnson EI, Dunlop ME, Larkins RG (1999) Increased vasodilatory prostaglandin production in the diabetic rat retinal vasculature. Curr Eye Res 18:79-82
22. Curtis TM, Scholfield CN (1999) Attenuated endothelin responses in retinal microvessels from diabetic rats. J Physiol 515P:6P
23. Rivera AA, White CR, Guest LL et al. (1995) Hyperglycemia alters cytoplasmic Ca2+ responses to capacitative Ca2+ influx in rat aortic smooth muscle cells. Am J Physiol 269:C1482-C1488
24. Keef KD, Hume JR, Zhong J (2001) Regulation of cardiac and smooth muscle Ca(2+) channels (Ca(V)l.2a,b) by protein kinases. Am J Physiol Cell Physiol 281:C1743-C1756
25. Albert AP, Large WA (2002) Activation of store-operated channels by noradrenaline via protein kinase C in rabbit portal vein myocytes. J Physiol 544:113-125
26. Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450
27. Head RJ, Longhurst PA, Panek RL et al. (1987) A contrasting effect of the diabetic state upon the contractile responses of aortic preparations from the rat and rabbit. Br J Pharmacol 91:275-286
28. Fulton DJ, Hodgson WC, Sikorski BW et al. (1991) Attenuated responses to endothelin-1, KCl and CaCl2, but not noradrenaline, of aortae from rats with streptozotocin-induced diabetes mellitus. Br J Pharmacol 104:928-932
29. Carmines PK, Ohishi K, Ikenaga H (1996) Functional impairment of renal afferent arteriolar voltage-gated calcium channels in rats with diabetes mellitus. J Clin Invest 98:2564-2571
30. Hattori Y, Kawasaki H, Fukao M et al. (1996) Diminishment of contractions associated with depolarization-evoked activation of Ca2+ channels in diabetic rat aorta. J Vasc Res 33:454-462
31. Wang R, Liu Y, Sauve R et al. (1998) Hyperosmolality-induced abnormal patterns of calcium mobilization in smooth muscle cells from non-diabetic and diabetic rats. Mol Cell Biochem 183:79-85
32. Wang R, Wu Y, Tang G et al. (2000) Altered L-type Ca(2+) channel currents in vascular smooth muscle cells from experimental diabetic rats. Am J Physiol Heart Circ Physiol 278:H714-H722
33. McGinty A, Scholfield CN, Liu WH et al. (1999) Effect of glucose on endothelin-1-induced calcium transients in cultured bovine retinal pericytes. J Biol Chem 274:25250-25253
34. Curtis TM, Scholfield CN(2001) Nifedipine blocks Ca2+ store refilling through a pathway not involving L-type Ca2+ channels in rabbit arteriolar smooth muscle. J Physiol 532:609-623
35. Mene P, Pugliese G, Pricci F et al. (1997) High glucose level inhibits capacitative Ca2+ influx in cultured rat mesangial cells by a protein kinase C-dependent mechanism. Diabetologia 40:521-527
36. Wayman CP, McFadzean I, Gibson A et al. (1996) Two distinct membrane currents activated by cyclopiazonic acid-induced calcium store depletion in single smooth muscle cells of the mouse anococcygeus. Br J Pharmacol 117:566-572
37. Parekh AB, Foguet M, Lubbert H et al. (1993) Ca2+ oscillations and Ca2+ influx in Xenopus oocytes expressing a novel 5-hydroxytryptamine receptor. J Physiol 469:653-671
38. Chiono M, Mahey R, Tate G et al. (1995) Capacitative Ca2+ entry exclusively inhibits cAMP synthesis in C6-2B glioma cells. Evidence that physiologically evoked Ca2+ entry regulates Ca(2+)-inhibitable adenylyl cyclase in non-excitable cells. J Biol Chem 270:1149-1155
39. Cooper DM, Yoshimura M, Zhang Y et al. (1994) Capacitative Ca2+ entry regulates Ca(2+)-sensitive adenylyl cyclases. Biochem J 297 (Pt 3):437-440
40. McKenzie S, Marley PD (2002) Caffeine stimulates Ca(2+) entry through store-operated channels to activate tyrosine hydroxylase in bovine chromaffin cells. Eur J Neurosci 15:1485-1492
41. Crabtree GR, Clipstone NA (1994) Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu Rev Biochem 63:1045-1083
42. Parekh AB, Penner R (1997) Store depletion and calcium influx. Physiol Rev 77:901-930
43. Ma R, Pluznick J, Kudlacek P et al. (2001) Protein kinase C activates store-operated Ca(2+) channels in human glomerular mesangial cells. J Biol Chem 276:25759-25765
44. Way KJ, Katai N, King GL (2001) Protein kinase C and the development of diabetic vascular complications. Diabet Med 18:945-959
45. Ma R, Kudlacek PE, Sansom SC (2002) Protein kinase Calpha participates in activation of store-operated Ca2+ channels in human glomerular mesangial cells. Am J Physiol Cell Physiol 283:C1390-C1398
46. Liu WS, Heckman CA (1998) The sevenfold way of PKC regulation. Cell Signal 10:529-542
47. Horowitz A, Clement-Chomienne O, Walsh MP et al. (1996) Epsilon-isoenzyme of protein kinase C induces a Ca(2+)-independent contraction in vascular smooth muscle. Am J Physiol 271:C589-C594
48. Walker LA, Gailly P, Jensen PE et al. (1998) The unimportance of being (protein kinase C) epsilon. FASEB J 12: 813-821
49. Takagi C, King GL, Clermont AC et al. (1995) Reversal of abnormal retinal hemodynamics in diabetic rats by acarbose, an alpha-glucosidase inhibitor. Curr Eye Res 14:741-749
50. Ishii H, Jirousek MR, Koya D et al. (1996) Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science 272:728-731
51. Park JY, Takahara N, Gabriele A et al. (2000) Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes 49:1239-1248
52. Weber LP, Seto M, Sasaki Y et al. (2000) The involvement of protein kinase C in myosin phosphorylation and force development in rat tail arterial smooth muscle Biochem J 352 Pt 2:573-582