High glucose decreases expression and activity of p-glycoprotein in cultured human retinal pigment epithelium possibly through iNOS induction

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Zhang, Yuehong ^a   Li, Chunmei ^b   Sun, Xuerong ^b   Kuang, Xielan ^b   Ruan, Xiangcai ^a  

^a GUANGZHOU FIRST PEOPLE'S HOSPITAL   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLUCOSE; GLYCOPROTEIN P; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; NITRITE; PREGNANE X RECEPTOR; RHODAMINE 123; ABCB1 PROTEIN, HUMAN; ENZYME INHIBITOR; NOS2 PROTEIN, HUMAN; STEROID RECEPTOR;

ARTICLE; BLOOD RETINA BARRIER; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INDUCTION; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INDUCIBLE NITRIC OXIDE SYNTHASE GENE; INTRACELLULAR SIGNALING; LONG TERM EXPOSURE; P GLYCOPROTEIN GENE; PIGMENT CELL; PREGNANE X RECEPTOR GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; TISSUE CULTURE; BIOSYNTHESIS; CELL LINE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; PIGMENT EPITHELIUM;

CELL LINE; CELLS, CULTURED; ENZYME INDUCTION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; P-GLYCOPROTEIN; RECEPTORS, STEROID; RETINAL PIGMENT EPITHELIUM; RNA, MESSENGER;

EID: 84857184854     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031631     Document Type: Article

References (53)

1. Congdon NG, Friedman DS, Lietman T, (2003) Important causes of visual impairment in the world today. JAMA 290: 2057-2060.
2. Wood JP, Chidlow G, Graham M, Osborne NN, (2004) Energy substrate requirements of rat retinal pigmented epithelial cells in culture: relative importance of glucose, amino acids, and monocarboxylates. Invest Ophthalmol Vis Sci 45: 1272-1280.
3. Simo R, Villarroel M, Corraliza L, Hernandez C, Garcia-Ramirez M, (2010) The retinal pigment epithelium: something more than a constituent of the blood-retinal barrier-implications for the pathogenesis of diabetic retinopathy. J Biomed Biotechnol 2010: 190724.
4. Frank RN, (2004) Diabetic retinopathy. N Engl J Med 350: 48-58.
5. Naggar H, Ola MS, Moore P, Huang W, Bridges CC, et al. (2002) Downregulation of reduced-folate transporter by glucose in cultured RPE cells and in RPE of diabetic mice. Invest Ophthalmol Vis Sci 43: 556-563.
6. Harhaj NS, Antonetti DA, (2004) Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 36: 1206-1237.
7. Barber AJ, Gardner TW, Abcouwer SF, (2010) The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci 52: 1156-1163.
8. Villarroel M, Garcia-Ramirez M, Corraliza L, Hernandez C, Simo R, (2009) Effects of high glucose concentration on the barrier function and the expression of tight junction proteins in human retinal pigment epithelial cells. Exp Eye Res 89: 913-920.
9. Liu Y, Liu H, Yang J, Liu X, Lu S, et al. (2008) Increased amyloid beta-peptide (1-40) level in brain of streptozotocin-induced diabetic rats. Neuroscience 153: 796-802.
10. Bellamy WT, (1996) P-glycoproteins and multidrug resistance. Annu Rev Pharmacol Toxicol 36: 161-183.
11. Nawa A, Fujita Hamabe W, Tokuyama S, (2010) Inducible nitric oxide synthase-mediated decrease of intestinal P-glycoprotein expression under streptozotocin-induced diabetic conditions. Life Sci 86: 402-409.
12. Moriyama M, Sugawara I, Hamada H, Tsuruo T, Kato T, et al. (1991) Elevated expression of P-glycoprotein in kidney and urinary bladder cancers. Tohoku J Exp Med 164: 191-201.
13. Bauer B, Hartz AM, Fricker G, Miller DS, (2005) Modulation of p-glycoprotein transport function at the blood-brain barrier. Exp Biol Med (Maywood) 230: 118-127.
14. Mannermaa E, Vellonen KS, Ryhanen T, Kokkonen K, Ranta VP, et al. (2009) Efflux protein expression in human retinal pigment epithelium cell lines. Pharm Res 26: 1785-1791.
15. Constable PA, Lawrenson JG, Dolman DE, Arden GB, Abbott NJ, (2006) P-Glycoprotein expression in human retinal pigment epithelium cell lines. Exp Eye Res 83: 24-30.
16. Wu KC, Pan HJ, Yin HS, Chen MR, Lu SC, et al. (2009) Change in P-glycoprotein and caveolin protein expression in brain striatum capillaries in New Zealand obese mice with type 2 diabetes. Life Sci 85: 775-781.
17. Maeng HJ, Kim MH, Jin HE, Shin SM, Tsuruo T, et al. (2007) Functional induction of P-glycoprotein in the blood-brain barrier of streptozotocin-induced diabetic rats: evidence for the involvement of nuclear factor-kappaB, a nitrosative stress-sensitive transcription factor, in the regulation. Drug Metab Dispos 35: 1996-2005.
18. van Waarde WM, Verkade HJ, Wolters H, Havinga R, Baller J, et al. (2002) Differential effects of streptozotocin-induced diabetes on expression of hepatic ABC-transporters in rats. Gastroenterology 122: 1842-1852.
19. Nowicki MT, Aleksunes LM, Sawant SP, Dnyanmote AV, Mehendale HM, et al. (2008) Renal and hepatic transporter expression in type 2 diabetic rats. Drug Metab Lett 2: 11-17.
20. Tramonti G, Xie P, Wallner EI, Danesh FR, Kanwar YS, (2006) Expression and functional characteristics of tubular transporters: P-glycoprotein, PEPT1, and PEPT2 in renal mass reduction and diabetes. Am J Physiol Renal Physiol 291: F972-980.
21. Bauer B, Hartz AM, Fricker G, Miller DS, (2004) Pregnane X receptor up-regulation of P-glycoprotein expression and transport function at the blood-brain barrier. Mol Pharmacol 66: 413-419.
22. Davis AA, Bernstein PS, Bok D, Turner J, Nachtigal M, et al. (1995) A human retinal pigment epithelial cell line that retains epithelial characteristics after prolonged culture. Invest Ophthalmol Vis Sci 36: 955-964.
23. Kennedy BG, Mangini NJ, (2002) P-glycoprotein expression in human retinal pigment epithelium. Mol Vis 8: 422-430.
24. Luker GD, Nilsson KR, Covey DF, Piwnica-Worms D, (1999) Multidrug resistance (MDR1) P-glycoprotein enhances esterification of plasma membrane cholesterol. J Biol Chem 274: 6979-6991.
25. Ford JM, Bruggemann EP, Pastan I, Gottesman MM, Hait WN, (1990) Cellular and biochemical characterization of thioxanthenes for reversal of multidrug resistance in human and murine cell lines. Cancer Res 50: 1748-1756.
26. Lee JS, Paull K, Alvarez M, Hose C, Monks A, et al. (1994) Rhodamine efflux patterns predict P-glycoprotein substrates in the National Cancer Institute drug screen. Mol Pharmacol 46: 627-638.
27. Kowluru RA, Engerman RL, Kern TS, (2000) Abnormalities of retinal metabolism in diabetes or experimental galactosemia VIII. Prevention by aminoguanidine. Curr Eye Res 21: 814-819.
28. do Carmo A, Lopes C, Santos M, Proenca R, Cunha-Vaz J, et al. (1998) Nitric oxide synthase activity and L-arginine metabolism in the retinas from streptozotocin-induced diabetic rats. Gen Pharmacol 30: 319-324.
29. Abu El-Asrar AM, Desmet S, Meersschaert A, Dralands L, Missotten L, 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.
30. Woo HB, Shin WS, Lee S, Ahn CM, (2005) Synthesis of novel curcumin mimics with asymmetrical units and their anti-angiogenic activity. Bioorg Med Chem Lett 15: 3782-3786.
31. Kim YK, Song YJ, Seo DW, Kang DW, Lee HY, et al. (2007) Reversal of multidrug resistance by 4-chloro-N-(3-((E)-3-(4-hydroxy-3-methoxyphenyl)acryloyl)phenyl)benzamide through the reversible inhibition of P-glycoprotein. Biochem Biophys Res Commun 355: 136-142.
32. Dussault I, Forman BM, (2002) The nuclear receptor PXR: a master regulator of "homeland" defense. Crit Rev Eukaryot Gene Expr 12: 53-64.
33. Uchiyama T, Matsuda Y, Wada M, Takahashi S, Fujita T, (2005) Functional regulation of Na+-dependent neutral amino acid transporter ASCT2 by S-nitrosothiols and nitric oxide in Caco-2 cells. FEBS Lett 579: 2499-2506.
34. Heemskerk S, van Koppen A, van den Broek L, Poelen GJ, Wouterse AC, et al. (2007) Nitric oxide differentially regulates renal ATP-binding cassette transporters during endotoxemia. Pflugers Arch 454: 321-334.
35. Zhou SF, (2008) Structure, function and regulation of P-glycoprotein and its clinical relevance in drug disposition. Xenobiotica 38: 802-832.
36. Juan CC, Lien CC, Chang CL, Huang YH, Ho LT, (2008) Involvement of iNOS and NO in TNF-alpha-downregulated resistin gene expression in 3T3-L1 adipocytes. Obesity (Silver Spring) 16: 1219-1225.
37. Wang JH, Scollard DA, Teng S, Reilly RM, Piquette-Miller M, (2005) Detection of P-glycoprotein activity in endotoxemic rats by 99mTc-sestamibi imaging. J Nucl Med 46: 1537-1545.
38. Kalitsky-Szirtes J, Shayeganpour A, Brocks DR, Piquette-Miller M, (2004) Suppression of drug-metabolizing enzymes and efflux transporters in the intestine of endotoxin-treated rats. Drug Metab Dispos 32: 20-27.
39. Hartmann G, Vassileva V, Piquette-Miller M, (2005) Impact of endotoxin-induced changes in P-glycoprotein expression on disposition of doxorubicin in mice. Drug Metab Dispos 33: 820-828.
40. Sparrow JR, Nathan C, Vodovotz Y, (1994) Cytokine regulation of nitric oxide synthase in mouse retinal pigment epithelial cells in culture. Exp Eye Res 59: 129-139.
41. Goureau O, Hicks D, Courtois Y, De Kozak Y, (1994) Induction and regulation of nitric oxide synthase in retinal Muller glial cells. J Neurochem 63: 310-317.
42. Holtkamp GM, Kijlstra A, Peek R, de Vos AF, (2001) Retinal pigment epithelium-immune system interactions: cytokine production and cytokine-induced changes. Prog Retin Eye Res 20: 29-48.
43. Goureau O, Hicks D, Courtois Y, (1994) Human retinal pigmented epithelial cells produce nitric oxide in response to cytokines. Biochem Biophys Res Commun 198: 120-126.
44. Zech JC, Pouvreau I, Cotinet A, Goureau O, Le Varlet B, et al. (1998) Effect of cytokines and nitric oxide on tight junctions in cultured rat retinal pigment epithelium. Invest Ophthalmol Vis Sci 39: 1600-1608.
45. Zheng L, Du Y, Miller C, Gubitosi-Klug RA, Ball S, et al. (2007) Critical role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes. Diabetologia 50: 1987-1996.
46. Kern TS, (2007) Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007: 95103.
47. Du Y, Smith MA, Miller CM, Kern TS, (2002) Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine. J Neurochem 80: 771-779.
48. Kern TS, Tang J, Mizutani M, Kowluru RA, Nagaraj RH, et al. (2000) Response of capillary cell death to aminoguanidine predicts the development of retinopathy: comparison of diabetes and galactosemia. Invest Ophthalmol Vis Sci 41: 3972-3978.
49. Kuwano M, Uchiumi T, Hayakawa H, Ono M, Wada M, et al. (2003) The basic and clinical implications of ABC transporters, Y-box-binding protein-1 (YB-1) and angiogenesis-related factors in human malignancies. Cancer Sci 94: 9-14.
50. Toell A, Kroncke KD, Kleinert H, Carlberg C, (2002) Orphan nuclear receptor binding site in the human inducible nitric oxide synthase promoter mediates responsiveness to steroid and xenobiotic ligands. J Cell Biochem 85: 72-82.
51. Mitchell BF, Mitchell JM, Chowdhury J, Tougas M, Engelen SM, et al. (2005) Metabolites of progesterone and the pregnane X receptor: a novel pathway regulating uterine contractility in pregnancy? Am J Obstet Gynecol 192: 1304-1313; discussion 1313-1305.
52. Hartley DP, Dai X, He YD, Carlini EJ, Wang B, et al. (2004) Activators of the rat pregnane X receptor differentially modulate hepatic and intestinal gene expression. Mol Pharmacol 65: 1159-1171.
53. Rosenfeld JM, Vargas R Jr, Xie W, Evans RM, (2003) Genetic profiling defines the xenobiotic gene network controlled by the nuclear receptor pregnane X receptor. Mol Endocrinol 17: 1268-1282.