Activation of RhoA/ROCK regulates NF-κB signaling pathway in experimental diabetic nephropathy

Molecular and Cellular Endocrinology

Volumn 369, Issue 1-2, 2013, Pages 86-97

  Xie, Xi ^a,b   Peng, Jing ^c   Chang, Xiuting ^a   Huang, Kaipeng ^a   Huang, Juan ^a   Wang, Shaogui ^a   Shen, Xiaoyan ^a   Liu, Peiqing ^a   Huang, Heqing ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b HAINAN UNIVERSITY   (China)

^c YUEBEI PEOPLE S HOSPITAL   (China)

Author keywords

Diabetic nephropathy; Fasudil; Fibronectin; NF B; RhoA ROCK

Indexed keywords

FASUDIL; FIBRONECTIN; INTERCELLULAR ADHESION MOLECULE 1; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DNA BINDING; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE TRANSLOCATION; GLUCOSE BLOOD LEVEL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; MALE; MESANGIUM CELL; NF KAPPA B SIGNALING PATHWAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEPHROPATHIES; GLUCOSE; MALE; MESANGIAL CELLS; NF-KAPPA B; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA;

EID: 84875053382     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.01.007     Document Type: Article

References (48)

1. Anwar K.N., Fazal F., Malik A.B., Rahman A. RhoA/Rho-associated kinase pathway selectively regulates thrombin-induced intercellular adhesion molecule-1 expression in endothelial cells via activation of I kappa B kinase beta and phosphorylation of RelA/p65. Journal of Immunology 2004, 173:6965-6972.
2. Axelsson J., Rippe A., Rippe B. Acute hyperglycemia induces rapid, reversible increases in glomerular permeability in nondiabetic rats. American Journal of Physiology - Renal Physiology 2010, 298:F1306-F1312.
3. Bondar I.A., Klimontov V.V., Nadeev A.P. Urinary excretion of proinflammatory cytokines and transforming growth factor beta at early stages of diabetic nephropathy. Terapevticheskii Arkhiv 2008, 80:52-56.
4. Bunting K., Rao S., Hardy K., Woltring D., Denyer G.S., Wang J., Gerondakis S., Shannon M.F. Genome-wide analysis of gene expression in T cells to identify targets of the NF-kappa B transcription factor c-Rel. Journal of Immunology 2007, 178:7097-7109.
5. Chow F.Y., Nikolic-Paterson D.J., Ozols E., Atkins R.C., Tesch G.H. Intercellular adhesion molecule-1 deficiency is protective against nephropathy in type 2 diabetic db/db mice. Journal of the American Society of Nephrology 2005, 16:1711-1722.
6. Cooper M.E. Interaction of metabolic and haemodynamic factors in mediating experimental diabetic nephropathy. Diabetologia 2001, 44:1957-1972.
7. Danesh F.R., Sadeghi M.M., Amro N., Philips C., Zeng L., Lin S., Sahai A., Kanwar Y.S. 3-Hydroxy-3-methylglutaryl CoA reductase inhibitors prevent high glucose-induced proliferation of mesangial cells via modulation of Rho GTPase/p21 signaling pathway: implications for diabetic nephropathy. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:8301-8305.
8. Fazal F., Bijli K.M., Minhajuddin M., Rein T., Finkelstein J.N., Rahman A. Essential role of cofilin-1 in regulating thrombin-induced RelA/p65 nuclear translocation and intercellular adhesion molecule 1 (ICAM-1) expression in endothelial cells. Journal of Biological Chemistry 2009, 284:21047-21056.
9. Gambaro G., Weigert C., Ceol M., Schleicher E.D. Inhibition of transforming growth factor-beta 1 gene overexpression as a strategy to prevent fibrosis. Advanced Glycation End Products in Nephrology 2001, 131:107-113.
10. Geoffroy K., Wiernsperger N., Lagarde M., El Bawab S. Bimodal effect of advanced glycation end products on mesangial cell proliferation is mediated by neutral ceramidase regulation and endogenous sphingolipids. Journal of Biological Chemistry 2004, 279:34343-34352.
11. Ghosh S., Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002, 109(Suppl.):S81.
12. Gojo A., Utsunomiya K., Taniguchi K., Yokota T., Ishizawa S., Kanazawa Y., Kurata H., Tajima N. The Rho-kinase inhibitor, fasudil, attenuates diabetic nephropathy in streptozotocin-induced diabetic rats. European Journal of Pharmacology 2007, 568:242-247.
13. Ha H.J., Yu M.R., Choi Y.J., Kitamura M., Lee H.B. Role of high glucose-induced nuclear factor-kappa B activation in monocyte chemoattractant protein-1 expression by mesangial cells. Journal of the American Society of Nephrology 2002, 13.
14. Hamid S.A., Bower H.S., Baxter G.F. Rho kinase activation plays a major role as a mediator of irreversible injury in reperfused myocardium. American Journal of Physiology - Heart and Circulatory Physiology 2007, 292:H2598-H2606.
15. Honjo M., Tanihara H., Inatani M., Kido N., Sawamura T., Yue B.Y., Narumiya S., Honda Y. Effects of rho-associated protein kinase inhibitor Y-27632 on intraocular pressure and outflow facility. Investigative Ophthalmology & Visual Science 2001, 42:137-144.
16. Iwamoto M., Mizuiri S., Arita M., Hemmi H. Nuclear factor-kappa B activation in diabetic rat kidney: evidence for involvement of P-selectin in diabetic nephropathy. Tohoku Journal of Experimental Medicine 2005, 206:163-171.
17. Jiang Q., Liu P.Q., Wu X.Q., Liu W.H., Shen X.Y., Lan T.A., Xu S.W., Peng J., Xie X., Huang H.Q. Berberine attenuates lipopolysaccharide-induced extracelluar matrix accumulation and inflammation in rat mesangial cells: involvement of NF-kappa B signaling pathway. Molecular and Cellular Endocrinology 2011, 331:34-40.
18. Jin L., Ying Z., Hilgers R.H., Yin J., Zhao X., Imig J.D., Webb R.C. Increased RhoA/Rho-kinase signaling mediates spontaneous tone in aorta from angiotensin II-induced hypertensive rats. Journal of Pharmacology and Experimental Therapeutics 2006, 318:288-295.
19. Kikuchi Y., Yamada M., Imakfire T., Kushiyama T., Higashi K., Hyodo N., Yamamoto K., Oda T., Suzuki S., Miura S. A Rho-kinase inhibitor, fasudil, prevents development of diabetes and nephropathy in insulin-resistant diabetic rats. Journal of Endocrinology 2007, 192:595-603.
20. Kolavennu V., Zeng L., Peng H., Wang Y., Danesh F.R. Targeting of RhoA/ROCK signaling ameliorates progression of diabetic nephropathy independent of glucose control. Diabetes 2008, 57:714-723.
21. Komers R., Oyama T.T., Beard D.R., Anderson S. Effects of systemic inhibition of Rho kinase on blood pressure and renal haemodynamics in diabetic rats. British Journal of Pharmacology 2011, 162:163-174.
22. Komers R., Oyama T.T., Beard D.R., Tikellis C., Xu B., Lotspeich D.F., Anderson S. Rho kinase inhibition protects kidneys from diabetic nephropathy without reducing blood pressure. Kidney International 2011, 79:432-442.
23. Krepinsky J.C., Ingram A.J., Tang D., Wu D., Liu L., Scholey J.W. Nitric oxide inhibits stretch-induced MAPK activation in mesangial cells through RhoA inactivation. Journal of the American Society of Nephrology 2003, 14:2790-2800.
24. Kumar A., Takada Y., Boriek A.M., Aggarwal B.B. Nuclear factor-kappa B: its role in health and disease. Journal of Molecular Medicine - JMM 2004, 82:434-448.
25. Lan T., Shen X., Liu P., Liu W., Xu S., Xie X., Jiang Q., Li W., Huang H. Berberine ameliorates renal injury in diabetic C57BL/6 mice: involvement of suppression of SphK-S1P signaling pathway. Archives of Biochemistry and Biophysics 2010, 502:112-120.
26. Liu W.H., Zhang X.Y., Liu P.Q., Shen X.Y., Lan T.A., Li W.Y., Jiang Q., Xie X., Huang H.Q. Effects of berberine on matrix accumulation and NF-kappa B signal pathway in alloxan-induced diabetic mice with renal injury. European Journal of Pharmacology 2010, 638:150-155.
27. Loirand G., Guerin P., Pacaud P. Rho kinases in cardiovascular physiology and pathophysiology. Circulation Research 2006, 98:322-334.
28. Mariappan M.M. Signaling mechanisms in the regulation of renal matrix metabolism in diabetes. Experimental Diabetes Research 2012, 2012:749812.
29. Mason R.M., Wahab N.A. Extracellular matrix metabolism in diabetic nephropathy. Journal of the American Society of Nephrology 2003, 14:1358-1373.
30. Massey A.R., Miao L., Smith B.N., Liu J., Kusaka I., Zhang J.H., Tang J. Increased RhoA translocation in renal cortex of diabetic rats. Life Sciences 2003, 72:2943-2952.
31. Mezzano S., Aros C., Droguett A., Burgos M.E., Ardiles L., Flores C., Schneider H., Ruiz-Ortega M., Egido J. NF-kappa B activation and overexpression of regulated genes in human diabetic nephropathy. Nephrology Dialysis Transplantation 2004, 19:2505-2512.
32. Mueller B.K., Mack H., Teusch N. Rho kinase, a promising drug target for neurological disorders. Nature Reviews Drug Discovery 2005, 4:387-398.
33. Murphy M., Docherty N.G., Griffin B., Howlin J., McArdle E., McMahon R., Schmid H., Kretzler M., Droguett A., Mezzano S., Brady H.R., Furlong F., Godson C., Martin F. IHG-1 amplifies TGF-beta1 signaling and is increased in renal fibrosis. Journal of the American Society of Nephrology 2008, 19:1672-1680.
34. Navarro-Gonzalez J.F., Mora-Fernandez C., de Fuentes M.M., Garcia-Perez J. Inflammatory molecules and pathways in the pathogenesis of diabetic nephropathy. Nature Reviews Nephrology 2011, 7:327-340.
35. Okada S., Shikata K., Matsuda M., Ogawa D., Usui H., Kido Y., Nagase R., Wada J., Shikata Y., Makino H. Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes 2003, 52:2586-2593.
36. Peng F., Wu D., Gao B., Ingram A.J., Zhang B., Chorneyko K., McKenzie R., Krepinsky J.C. RhoA/Rho-kinase contribute to the pathogenesis of diabetic renal disease. Diabetes 2008, 57:1683-1692.
37. Ramana K.V., Friedrich B., Srivastava S., Bhatnagar A., Srivastava S.K. Activation of nuclear factor-kappa B by hyperglycemia in vascular smooth muscle cells is regulated by aldose reductase. Diabetes 2004, 53:2910-2920.
38. Ridley A.J. Rho family proteins: coordinating cell responses. Trends in Cell Biology. 2001, 11:471-477.
39. Rikitake Y., Kim H.H., Huang Z.H., Seto M., Yano K., Asano T., Moskowitz M.A., Liao J.K. Inhibition of rho kinase (ROCK) leads to increased cerebral blood flow and stroke protection. Stroke 2005, 36:2251-2257.
40. Ritz E., Rychlik I., Locatelli F., Halimi S. End-stage renal failure in type 2 diabetes: a medical catastrophe of worldwide dimensions. American Journal of Kidney Diseases 1999, 34:795-808.
41. Schmid H., Boucherot A., Yasuda Y., Henger A., Brunner B., Eichinger F., Nitsche A., Kiss E., Bleich M., Grone H.J., Nelson P.J., Schlondorff D., Cohen C.D., Kretzler M. Modular activation of nuclear factor-kappa B transcriptional programs in human diabetic nephropathy. Diabetes 2006, 55:2993-3003.
42. Sharma K., Jin Y., Guo J., Ziyadeh F.N. Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes 1996, 45:522-530.
43. Sheu M.L., Ho F.M., Chao K.F., Kuo M.L., Liu S.H. Activation of phosphoinositide 3-kinase in response to high glucose leads to regulation of reactive oxygen species-related nuclear factor-kappa B activation and cyclooxygenase-2 expression in mesangial cells. Molecular Pharmacology 2004, 66:187-196.
44. Somlyo A.P., Somlyo A.V. Signal transduction through the RhoA/Rho-kinase pathway in smooth muscle. Journal of Muscle Research and Cell Motility 2004, 25:613-615.
45. Tuttle K.R. Linking metabolism and immunology: diabetic nephropathy is an inflammatory disease. Journal of the American Society of Nephrology 2005, 16:1537-1538.
46. Wang A., Ziyadeh F.N., Lee E.Y., Pyagay P.E., Sung S.H., Sheardown S.A., Laping N.J., Chen S. Interference with TGF-beta signaling by Smad3-knockout in mice limits diabetic glomerulosclerosis without affecting albuminuria. American Journal of Physiology - Renal Physiology 2007, 293:F1657.
47. Yang W.S., Seo J.W., Han N.J., Choi J., Lee K.U., Ahn H., Lee S.K., Park S.K. High glucose-induced NF-kappa B activation occurs via tyrosine phosphorylation of I kappa B alpha in human glomerular endothelial cells: involvement of Syk tyrosine kinase. American Journal of Physiology - Renal Physiology 2008, 294:F1065-F1075.
48. Zhou L., Liu F., Huang X.R., Chen H., Chung A.C., Shi J., Wei L., Lan H.Y., Fu P. Amelioration of albuminuria in ROCK1 knockout mice with streptozotocin-induced diabetic kidney disease. American Journal of Nephrology 2011, 34:468-475.