Tonicity-responsive enhancer binding protein regulates the expression of aldose reductase and protein kinase C δ in a mouse model of diabetic retinopathy

Experimental Eye Research

Volumn 122, Issue , 2014, Pages 13-19

  Park, Jeongsook ^a,b   Kim, Hwajin ^a   Park, So Yun ^a   Lim, Sun Woo ^c   Kim, Yoon Sook ^a   Lee, Dong Hoon ^a   Roh, Gu Seob ^a   Kim, Hyun Joon ^a   Kang, Sang Soo ^a   Cho, Gyeong Jae ^a   Jeong, Bo Young ^b   Kwon, H Moo ^d   Choi, Wan Sung ^a  

^a Gyeongsang National University School of Medicine   (South Korea)

^b Gyeongsang National University   (South Korea)

^c The Catholic University of Korea   (South Korea)

^d Ulsan National Institute of Science and Technology   (South Korea)

Author keywords

Aldose reductase; Diabetic retinopathy; Hyperglycemia; Protein kinase C; TonEBP

Indexed keywords

ALDEHYDE REDUCTASE; BINDING PROTEIN; GLUCOSE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE C DELTA; SMALL INTERFERING RNA; TONICITY RESPONSIVE ENHANCER BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; DIABETIC RETINOPATHY; GENE SILENCING; HETEROZYGOTE; HOMEOSTASIS; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IMMUNOFLUORESCENCE; IN VITRO STUDY; MALE; MOUSE; NERVE CELL; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; WILD TYPE;

ALDOSE REDUCTASE; DIABETIC RETINOPATHY; HYPERGLYCEMIA; PROTEIN KINASE C; TONEBP;

ALDEHYDE REDUCTASE; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; MALE; MICE; MICE, INBRED C57BL; NFATC TRANSCRIPTION FACTORS; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-BCL-2; RETINA; RETINAL GANGLION CELLS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS;

EID: 84896956241     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.03.001     Document Type: Article

References (51)

1. Anil Kumar P., Bhanuprakash Reddy G. Focus on molecules: aldose reductase. Exp. Eye Res. 2007, 85:739-740.
2. Aramburu J., Drews-Elger K., Estrada-Gelonch A., Minguillon J., Morancho B., Santiago V., Lopez-Rodriguez C. Regulation of the hypertonic stress response and other cellular functions by the Rel-like transcription factor NFAT5. Biochem. Pharmacol. 2006, 72:1597-1604.
3. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
4. Chang K.C., Laffin B., Ponder J., Enzsoly A., Nemeth J., LaBarbera D.V., Petrash J.M. Beta-glucogallin reduces the expression of lipopolysaccharide-induced inflammatory markers by inhibition of aldose reductase in murine macrophages and ocular tissues. Chem. Biol. Interact. 2013, 202:283-287.
5. Cheung A.K., Fung M.K., Lo A.C., Lam T.T., So K.F., Chung S.S., Chung S.K. Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes 2005, 54:3119-3125.
6. Chung S.S., Ho E.C., Lam K.S., Chung S.K. Contribution of polyol pathway to diabetes-induced oxidative stress. J.Am. Soc. Nephrol. 2003, 14:S233-S236.
7. Cogan D.G., Kinoshita J.H., Kador P.F., Robison G., Datilis M.B., Cobo L.M., Kupfer C. NIH conference. Aldose reductase and complications of diabetes. Ann. Intern. Med. 1984, 101:82-91.
8. Craven P.A., Studer R.K., DeRubertis F.R. Impaired nitric oxide-dependent cyclic guanosine monophosphate generation in glomeruli from diabetic rats. Evidence for protein kinase C-mediated suppression of the cholinergic response. J.Clin. Investig. 1994, 93:311-320.
9. Du Y., Tang J., Li G., Berti-Mattera L., Lee C.A., Bartkowski D., Gale D., Monahan J., Niesman M.R., Alton G., Kern T.S. Effects of p38 MAPK inhibition on early stages of diabetic retinopathy and sensory nerve function. Investig. Ophthalmol. Vis. Sci. 2010, 51:2158-2164.
10. Fong D.S., Aiello L.P., Ferris F.L., Klein R. Diabetic retinopathy. Diabetes Care 2004, 27:2540-2553.
11. Forbes J.M., Coughlan M.T., Cooper M.E. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 2008, 57:1446-1454.
12. Ganz M.B., Seftel A. Glucose-induced changes in protein kinase C and nitric oxide are prevented by vitamin E. Am. J. Physiol. Endocrinol. Metab. 2000, 278:E146-E152.
13. Geraldes P., Hiraoka-Yamamoto J., Matsumoto M., Clermont A., Leitges M., Marette A., Aiello L.P., Kern T.S., King G.L. Activation of PKC-delta and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat. Med. 2009, 15:1298-1306.
14. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circ. Res. 2010, 107:1058-1070.
15. Glogowski E.A., Tsiani E., Zhou X., Fantus I.G., Whiteside C. High glucose alters the response of mesangial cell protein kinase C isoforms to endothelin-1. Kidney Int. 1999, 55:486-499.
16. Halterman J.A., Kwon H.M., Leitinger N., Wamhoff B.R. NFAT5 expression in bone marrow-derived cells enhances atherosclerosis and drives macrophage migration. Front. Physiol. 2012, 3:313.
17. Halterman J.A., Kwon H.M., Wamhoff B.R. Tonicity-independent regulation of the osmosensitive transcription factor TonEBP (NFAT5). Am. J. Physiol. Cell Physiol. 2012, 302:C1-C8.
18. Hammes H.P., Du X., Edelstein D., Taguchi T., Matsumura T., Ju Q., Lin J., Bierhaus A., Nawroth P., Hannak D., Neumaier M., Bergfeld R., Giardino I., Brownlee M. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat. Med. 2003, 9:294-299.
19. Handler J.S., Kwon H.M. Transcriptional regulation by changes in tonicity. Kidney Int. 2001, 60:408-411.
20. Hempel A., Maasch C., Heintze U., Lindschau C., Dietz R., Luft F.C., Haller H. High glucose concentrations increase endothelial cell permeability via activation of protein kinase C alpha. Circ. Res. 1997, 81:363-371.
21. Ho H.T., Chung S.K., Law J.W., Ko B.C., Tam S.C., Brooks H.L., Knepper M.A., Chung S.S. Aldose reductase-deficient mice develop nephrogenic diabetes insipidus. Mol. Cell. Biol. 2000, 20:5840-5846.
22. Ishii H., Koya D., King G.L. Protein kinase C activation and its role in the development of vascular complications in diabetes mellitus. J.Mol. Med. (Berl.) 1998, 76:21-31.
23. Kador P.F., Kinoshita J.H. Role of aldose reductase in the development of diabetes-associated complications. Am. J. Med. 1985, 79:8-12.
24. Kador P.F., Zhang P., Makita J., Zhang Z., Guo C., Randazzo J., Kawada H., Haider N., Blessing K. Novel diabetic mouse models as tools for investigating diabetic retinopathy. PLoS One 2012, 7:e49422.
25. Kao Y.L., Donaghue K., Chan A., Knight J., Silink M. A novel polymorphism in the aldose reductase gene promoter region is strongly associated with diabetic retinopathy in adolescents with type 1 diabetes. Diabetes 1999, 48:1338-1340.
26. Kato N., Yashima S., Suzuki T., Nakayama Y., Jomori T. Long-term treatment with fidarestat suppresses the development of diabetic retinopathy in STZ-induced diabetic rats. J.Diabetes Complicat. 2003, 17:374-379.
27. Kim Y.H., Kim Y.S., Park C.H., Chung I.Y., Yoo J.M., Kim J.G., Lee B.J., Kang S.S., Cho G.J., Choi W.S. Protein kinase C-delta mediates neuronal apoptosis in the retinas of diabetic rats via the Akt signaling pathway. Diabetes 2008, 57:2181-2190.
28. 2+/calmodulin-dependent protein kinase II activity in diabetic mouse retina. Diabetes 2010, 59:1825-1835.
29. Kim Y.H., Park S.Y., Park J., Kim Y.S., Hwang E.M., Park J.Y., Roh G.S., Kim H.J., Kang S.S., Cho G.J., Choi W.S. Reduction of experimental diabetic vascular leakage and pericyte apoptosis in mice by delivery of alphaA-crystallin with a recombinant adenovirus. Diabetologia 2012, 55:2835-2844.
30. Kleinman M.E., Baffi J.Z., Ambati J. The multifactorial nature of retinal vascular disease. Ophthalmologica 2010, 224(Suppl.1):16-24.
31. Ko B.C., Ruepp B., Bohren K.M., Gabbay K.H., Chung S.S. Identification and characterization of multiple osmotic response sequences in the human aldose reductase gene. J.Biol. Chem. 1997, 272:16431-16437.
32. Lee S.D., Choi S.Y., Lim S.W., Lamitina S.T., Ho S.N., Go W.Y., Kwon H.M. TonEBP stimulates multiple cellular pathways for adaptation to hypertonic stress: organic osmolyte-dependent and -independent pathways. Am. J. Physiol. Ren. Physiol. 2011, 300:F707-F715.
33. Miyakawa H., Woo S.K., Dahl S.C., Handler J.S., Kwon H.M. Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2538-2542.
34. Oates P.J., Mylari B.L. Aldose reductase inhibitors: therapeutic implications for diabetic complications. Expert Opin. Investig. Drugs 1999, 8:2095-2119.
35. Obrosova I.G., Minchenko A.G., Vasupuram R., White L., Abatan O.I., Kumagai A.K., Frank R.N., Stevens M.J. Aldose reductase inhibitor fidarestat prevents retinal oxidative stress and vascular endothelial growth factor overexpression in streptozotocin-diabetic rats. Diabetes 2003, 52:864-871.
36. Olmos P., Bastias M.J., Vollrath V., Toro L., Trincado A., Salinas P., Claro J.C., Lopez J.M., Acosta A.M., Miquel J.F., Castro J. C(-106)T polymorphism of the aldose reductase gene and the progression rate of diabetic retinopathy. Diabetes Res. Clin. Pract. 2006, 74:175-182.
37. Padival A.K., Hawkins K.S., Huang C. High glucose-induced membrane translocation of PKC betaI is associated with Arf6 in glomerular mesangial cells. Mol. Cell. Biochem 2004, 258:129-135.
38. Ramana K.V., Friedrich B., Tammali R., West M.B., Bhatnagar A., Srivastava S.K. Requirement of aldose reductase for the hyperglycemic activation of protein kinase C and formation of diacylglycerol in vascular smooth muscle cells. Diabetes 2005, 54:818-829.
39. Ramasamy R., Goldberg I.J. Aldose reductase and cardiovascular diseases, creating human-like diabetic complications in an experimental model. Circ. Res. 2010, 106:1449-1458.
40. Robison W.G., McCaleb M.L., Feld L.G., Michaelis O.E.t., Laver N., Mercandetti M. Degenerated intramural pericytes ('ghost cells') in the retinal capillaries of diabetic rats. Curr. Eye Res. 1991, 10:339-350.
41. Sheetz M.J., King G.L. Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 2002, 288:2579-2588.
42. Simo R., Hernandez C. Neurodegeneration in the diabetic eye: new insights and therapeutic perspectives. Trends Endocrinol. Metab. 2013, 25:23-33.
43. Soriano F.G., Pacher P., Mabley J., Liaudet L., Szabo C. Rapid reversal of the diabetic endothelial dysfunction by pharmacological inhibition of poly(ADP-ribose) polymerase. Circ. Res. 2001, 89:684-691.
44. Stitt A., Gardiner T.A., Alderson N.L., Canning P., Frizzell N., Duffy N., Boyle C., Januszewski A.S., Chachich M., Baynes J.W., Thorpe S.R. The AGE inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes. Diabetes 2002, 51:2826-2832.
45. Sun W., Oates P.J., Coutcher J.B., Gerhardinger C., Lorenzi M. Aselective aldose reductase inhibitor of a new structural class prevents or reverses early retinal abnormalities in experimental diabetic retinopathy. Diabetes 2006, 55:2757-2762.
46. Yabe-Nishimura C. Aldose reductase in glucose toxicity: a potential target for the prevention of diabetic complications. Pharmacol. Rev. 1998, 50:21-33.
47. Yagihashi S., Yamagishi S.I., Wada Ri R., Baba M., Hohman T.C., Yabe-Nishimura C., Kokai Y. Neuropathy in diabetic mice overexpressing human aldose reductase and effects of aldose reductase inhibitor. Brain 2001, 124:2448-2458.
48. Yang B., Hodgkinson A.D., Oates P.J., Kwon H.M., Millward B.A., Demaine A.G. Elevated activity of transcription factor nuclear factor of activated T-cells 5 (NFAT5) and diabetic nephropathy. Diabetes 2006, 55:1450-1455.
49. Yerneni K.K., Bai W., Khan B.V., Medford R.M., Natarajan R. Hyperglycemia-induced activation of nuclear transcription factor kappaB in vascular smooth muscle cells. Diabetes 1999, 48:855-864.
50. Yoon H.J., You S., Yoo S.A., Kim N.H., Kwon H.M., Yoon C.H., Cho C.S., Hwang D., Kim W.U. NF-AT5 is a critical regulator of inflammatory arthritis. Arthritis Rheum. 2011, 63:1843-1852.
51. Zheng L., Szabo C., Kern T.S. Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-kappaB. Diabetes 2004, 53:2960-2967.