Akt and RhoA activation in response to high glucose require caveolin-1 phosphorylation in mesangial cells

American Journal of Physiology - Renal Physiology

Volumn 306, Issue 11, 2014, Pages

  Wu, Su Zhen ^a   Peng, Fang Fang ^a   Li, Jia Lin ^b   Ye, Feng ^a   Lei, Shao Qing ^a   Zhang, Bai Fang ^a,c  

^a WUHAN UNIVERSITY   (China)

^b GANNAN MEDICAL UNIVERSITY   (China)

^c HUBEI PROVINCIAL KEY LABORATORY OF DEVELOPMENTALLY ORIGINATED DISEASE   (China)

Author keywords

Caveolin 1 phosphorylation; Extracellular matrix; Glomerular sclerosis

Indexed keywords

2,3 DIHYDRO 2 OXO 3 (4,5,6,7 TETRAHYDRO 1H INDOL 2 YLMETHYLENE) 1H INDOLE 5 SULFONIC ACID DIMETHYLAMIDE; CAVEOLIN 1; FIBRONECTIN; GLUCOSE; PROTEIN KINASE B; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RUBOXISTAURIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CORTEX; MALE; MESANGIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE; UPREGULATION; WESTERN BLOTTING;

CAVEOLIN-1 PHOSPHORYLATION; EXTRACELLULAR MATRIX; GLOMERULAR SCLEROSIS;

ANIMALS; CAVEOLIN 1; DIABETES MELLITUS, EXPERIMENTAL; GLUCOSE; MALE; MESANGIAL CELLS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84901714326     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00447.2013     Document Type: Article

References (65)

1. Anderson PW, McGill JB, Tuttle KR. Protein kinase C beta inhibition: the promise for treatment of diabetic nephropathy. Curr Opin Nephrol Hypertens 16: 397-402, 2007.
2. Bach LA. Rho kinase inhibition: a new approach for treating diabetic nephropathy? Diabetes 57: 532-533, 2008.
3. Bianchi F, Mattii L, D'Alessandro D, Moscato S, Segnani C, Dolfi A, Bernardini N. Cellular and subcellular localization of the small G protein RhoA in the human and rat embryonic and adult kidney. Acta Histochem 105: 89-97, 2003.
4. Boivin D, Béliveau R. Subcellular distribution and membrane association of Rho-related small GTP-binding proteins in kidney cortex. Am J Physiol Renal Fluid Electrolyte Physiol 269: F180-F189, 1995.
5. Bucci M, Roviezzo F, Brancaleone V, Lin MI, Di Lorenzo A, Cicala C, Pinto A, Sessa WC, Farneti S, Fiorucci S, Cirino G. Diabetic mouse angiopathy is linked to progressive sympathetic receptor deletion coupled to an enhanced caveolin-1 expression. Arterioscler Thromb Vasc Biol 24: 721-726, 2004.
6. Cao H, Courchesne WE, Mastick CC. A phosphotyrosine-dependent protein interaction screen reveals a role for phosphorylation of caveolin-1 on tyrosine 14: recruitment of C-terminal Src kinase. J Biol Chem 277: 8771-8774, 2002.
7. Cantley LC. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657, 2002.
8. Cohen AW, Combs TP, Scherer PE, Lisanti MP. Role of caveolin and caveolae in insulin signaling and diabetes. Am J Physiol Endocrinol Metab 285: E1151-E1160, 2003.
9. Demová H, Komers R. Determination of caveolin-1 in renal caveolar and non-caveolar fractions in experimental type 1 diabetes. Physiol Res 58: 563-568, 2009.
10. Goetz JG, Lajoie P, Wiseman SM, Nabi IR. Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev 27: 715-735, 2008.
11. 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. Eur J Pharmacol 568: 242-247, 2007.
12. Hanada M, Feng J, Hemmings BA. Structure, regulation and function of PKB/AKT: a major therapeutic target. Biochim Biophys Acta 1697: 3-16, 2004.
13. Haneda M, Koya D, Isono M, Kikkawa R. Overview of glucose signaling in mesangial cells in diabetic nephropathy. J Am Soc Nephrol 14: 1374-1382, 2003.
14. Heusinger-Ribeiro JEM, Wahab NA, Goppelt-Struebe M. Expression of connective tissue growth factor in human renal fibroblasts: regulatory roles of RhoA and cAMP. J Am Soc Nephrol 12: 1853-1861, 2001.
15. Ishii H, Jirousek MR, Koya D, Takagi C, Xia P, Clermont A, Bursell SE, Kern TS, Ballas LM, Heath WF, Stramm LE, Feener EP, King GL. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science 272: 728-731, 1996.
16. Kanwar YS, Wada J, Sun L, Xie P, Wallner EI, Chen S, Chugh S, Danesh FR. Diabetic nephropathy: mechanisms of renal disease progression. Exp Biol Med (Maywood) 233: 4-11, 2008.
17. Kapor-Drezgic J, Zhou X, Babazono T, Dlugosz JA, Hohman T, Whiteside C. Effect of high glucose on mesangial cell protein kinase C-delta and-epsilon is polyol pathway-dependent. J Am Soc Nephrol 10: 1193-1203, 1999.
18. Kelly DJ, Buck D, Cox AJ, Zhang Y, Gilbert RE. Effects on protein kinase C-β inhibition on glomerular vascular endothelial growth factor expression and endothelial cells in advanced experimental diabetic nephropathy. Am J Physiol Renal Physiol 293: F565-F574, 2007.
19. Kelly DJ, Zhang Y, Hepper C, Gow RM, Jaworski K, Kemp BE, Wilkinson-Berka JL, Gilbert RE. Protein kinase C beta inhibition attenuates the progression of experimental diabetic nephropathy in the presence of continued hypertension. Diabetes 52: 512-518, 2003.
20. Kikuchi Y, Yamada M, Imakiire 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 insulinresistant diabetic rats. J Endocrinol 192: 595-596, 2007.
21. Kim YN, Wiepz GJ, Guadarrama AG, Bertics PJ. Epidermal growth factor-stimulated tyrosine phosphorylation of caveolin-1. Enhanced caveolin-1 tyrosine phosphorylation following aberrant epidermal growth factor receptor status. J Biol Chem 275: 7481-7491, 2000.
22. Kolavennu V, Zeng L, Peng H, Wang Y, Danesh FR. Targeting of RhoA/ROCK signaling ameliorates progression of diabetic nephropathy independent of glucose control. Diabetes 57: 714-723, 2008.
23. Komers R. Rho kinase inhibition in diabetic nephropathy. Curr Opin Nephrol Hypertens 20: 77-83, 2011.
24. Komers R, Oyama TT, Beard DR, Tikellis C, Xu B, Lotspeich DF, Anderson S. Rho kinase inhibition protects kidneys from diabetic nephropathy without reducing blood pressure. Kidney Int 79: 432-442, 2011.
25. Komers R, Schutzer WE, Reed JF, Lindsley JN, Oyama TT, Buck DC, Mader SL, Anderson S. Altered endothelial nitric oxide synthase targeting and conformation and caveolin-1 expression in the diabetic kidney. Diabetes 55: 1651-1659, 2006.
26. Koya D, Jirousek MR, Lin YW, Ishii H, Kuboki K, King GL. Characterization of protein kinase C-b isoform activation on the gene expression of transforming factor-b, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Invest 100: 115-126, 1997.
27. Koya D, Haneda M, Nakagawa H, Isshiki K, Sato H, Maeda S, Sugimoto T, Yasuda H, Kashiwagi A, Ways DK, King GL, Kikkawa R. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J 14: 439-447, 2000.
28. Krepinsky JC, Ingram AJ, Tang D, Wu D, Liu L, Scholey JW. Nitric oxide inhibits stretch-induced MAPK activation in mesangial cells through RhoA inactivation. J Am Soc Nephrol 14: 2790-2800, 2003.
29. Li S, Seitz R, Lisanti MP. Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J Biol Chem 271: 3863-3868, 1996.
30. Lu T, Zhang DM, Wang XL, He T, Wang RX, Chai Q, Katusic ZS, Lee HC. Regulation of coronary arterial BK channels by caveolaemediated angiotensin II signaling in diabetes mellitus. Circ Res 106: 1164-1173, 2010.
31. Marks JB, Raskin P. Nephropathy and hypertension in diabetes. Med Clin North Am 82: 877-907, 1998.
32. Mason RM, Wahab NA. Extracellular matrix metabolism in diabetic nephropathy. J Am Soc Nephrol 14: 1358-1373, 2003.
33. Massey AR, Miao L, Smith BN, Liu J, Kusaka I, Zhang JH, Tang J. Increased RhoA translocation in renal cortex of diabetic rats. Life Sci 72: 2943-2952, 2003.
34. Meier M, Park JK, Overheu D, Kirsch T, Lindschau C, Gueler F, Leitges M, Menne J, Haller H. Deletion of protein kinase C-beta isoform in vivo reduces renal hypertrophy but not albuminuria in the streptozotocin-induced diabetic mouse model. Diabetes 56: 346-354, 2007.
35. Moriyama T, Tsuruta Y, Shimizu A, Itabashi M, Takei T, Horita S, Uchida K, Nitta K. The significance of caveolae in the glomeruli in glomerular disease. J Clin Pathol 64: 504-509, 2011.
36. Nethe M, Hordijk PL. A model for phospho-caveolin-1-driven turnover of focal adhesions. Cell Adh Migr 5: 59-64, 2011.
37. Ohshiro Y, Ma RC, Yasuda Y, Hiraoka-Yamamoto J, Clermont AC, Isshiki K, Yagi K, Arikawa E, Kern TS, King GL. Reduction of diabetes-induced oxidative stress, fibrotic cytokine expression, and renal dysfunction in protein kinase Cbeta-null mice. Diabetes 55: 3112-3120, 2006.
38. Peng F, Wu D, Gao B, Ingram AJ, Zhang B, Chorneyko K, McKenzie R, Krepinsky JC. RhoA/Rho-kinase contribute to the pathogenesis of diabetic renal disease. Diabetes 57: 1683-1692, 2008.
39. Peng F, Wu D, Ingram AJ, Zhang BF, Gao B, Krepinsky JC. RhoA activation in mesangial cells by mechanical strain depends on caveolae and caveolin-1 interaction. J Am Soc Nephrol 18: 189-198, 2007.
40. Peng F, Zhang B, Wu D, Ingram AJ, Gao B, Krepinsky JC. TGFβ-induced RhoA activation and fibronectin production in mesangial cells requires caveolae. Am J Physiol Renal Physiol 295: F153-F164, 2008.
41. Pfaff IL, Wagner HJ, Vallon V. Immunolocalization of protein kinase C isoenzymes alpha, beta1 and betaII in rat kidney. J Am Soc Nephrol 10: 1861-1873, 1999.
42. Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev 54: 431-467, 2002.
43. Razani B, Lisanti MP. Caveolins and caveolae: molecular and functional relationships. Exp Cell Res 271: 36-44, 2001.
44. Redling S, Pfaff IL, Leitges M, Vallon V. Immunolocalization of protein kinase C isoenzymes α, βI, βII, δ, and in mouse kidney. Am J Physiol Renal Physiol 287: F289-F298, 2004.
45. Runyan CE, Schnaper HW, Poncelet AC. The phosphatidylinositol 3-kinase/Akt pathway enhances Smad3-stimulated mesangial cell collagen I expression in response to transforming growth factor-beta1. J Biol Chem 279: 2632-2639, 2004.
46. Samarakoon R, Chitnis SS, Higgins SP, Higgins CE, Krepinsky JC, Higgins PJ. Redox-induced Src kinase and caveolin-1 signaling in TGF-β1-initiated SMAD2/3 activation and PAI-1 expression. PLOS ONE 6: e22896, 2011.
47. Sanguinetti AR, Cao H, Corley Mastick C. Fyn is required for oxidative-and hyperosmotic-stress-induced tyrosine phosphorylation of caveolin-1. Biochem J 376: 159-168, 2003.
48. Sanguinetti AR, Mastick CC. c-Abl is required for oxidative stressinduced phosphorylation of caveolin-1 on tyrosine 14. Cell Signal 15: 289-298, 2003.
49. Schena FP, Gesualdo L. Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol 16: S30-S33, 2005.
50. Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolaemediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 127: 1217-1232, 1994.
51. Sedding DG, Hermsen J, Seay U, Eickelberg O, Kummer W, Schwencke C, Strasser RH, Tillmanns H, Braun-Dullaeus RC. Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ Res 96: 635-642, 2005.
52. Sharpe CC, Hendry BM. Signaling: focus on Rho in renal disease. J Am Soc Nephrol 14: 261-264, 2003.
53. Sun GP, Kohno M, Guo P, Nagai Y, Miyata K, Fan YY, Kimura S, Kiyomoto H, Ohmori K, Li DT, Abe Y, Nishiyama A. Involvements of Rho-Kinase and TGF-beta pathways in aldosterone-induced renal injury. J Am Soc Nephrol 17: 2193-2201, 2006.
54. Tamai O, Oka N, Kikuchi T, Koda Y, Soejima M, Wada Y, Fujisawa M, Tamaki K, Kawachi H, Shimizu F, Kimura H, Imaizumi T, Okuda S. Caveolae in mesangial cells and caveolin expression in mesangial proliferative glomerulonephritis. Kidney Int 59: 471-480, 2001.
55. Tian C, Zhang R, Ye X, Zhang C, Jin X, Yamori Y, Hao L, Sun X, Ying C. Resveratrol ameliorates high-glucose-induced hyperpermeability mediated by caveolae via VEGF/KDR pathway. Genes Nutr 8: 231-239, 2013.
56. Ushio-Fukai M, Hilenski L, Santanam N, Becker PL, Ma Y, Griendling KK, Alexander RW. Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J Biol Chem 276: 48269-48275, 2001.
57. Ushio-Fukai M, Zuo L, Ikeda S, Tojo T, Patrushev NA, Alexander RW. cAbl tyrosine kinase mediates reactive oxygen species-and caveolindependent AT1 receptor signaling in vascular smooth muscle: role in vascular hypertrophy. Circ Res 97: 829-836, 2005.
58. Wu D, Peng F, Zhang BF, Ingram AL, Gao B, Krepinsky JC. Collagen I induction by high glucose levels is mediated by epidermal growth factor receptor and phosphoinositide 3-kinase/Akt signalling in mesangial cells. Diabetologia 50: 2008-2018, 2007.
59. Wu D, Peng F, Zhang BF, Ingram AJ, Kelly DJ, Gilbert RE, Gao B, Krepinsky JC. PKC-beta1 mediates glucose-induced Akt activation and TGF-beta1 upregulation in mesangial cells. J Am Soc Nephrol 20: 554-566, 2009.
60. Wu D, Peng F, Zhang B, Ingram AJ, Kelly DJ, Gilbert RE, Gao B, Kumar S, Krepinsky JC. EGFR-PLCγ1 signaling mediates high glucose-induced PKCβ1-Akt activation and collagen I upregulation in mesangial cells. Am J Physiol Renal Physiol 297: F822-F834, 2009.
61. Wu T, Zhang B, Ye F, Xiao Z. A potential role for caveolin-1 in VEGF-induced fibronectin upregulation in mesangial cells: involvement of VEGFR2 and Src. Am J Physiol Renal Physiol 304: F820-F830, 2013.
62. Xin X, Khan ZA, Chen S, Chakrabarti S. Glucose-induced Akt1 activation mediates fibronectin synthesis in endothelial cells. Diabetologia 48: 2428-2436, 2005.
63. Yin X, Li B, Chen H, Catt KJ. Differential signaling pathways in angiotensin II-and epidermal growth factor-stimulated hepatic C9 cells. Mol Pharmacol 74: 1223-1233, 2008.
64. Zhang B, Peng F, Wu D, Ingram AJ, Gao B, Krepinsky JC. Caveolin-1 phosphorylation is required for stretch-induced EGFR and Akt activation in mesangial cells. Cell Signal 19: 1690-1700, 2007.
65. Zhang Y, Peng F, Gao B, Ingram AJ, Krepinsky JC. High glucoseinduced RhoA activation requires caveolae and PKCβ1-mediated ROS generation. Am J Physiol Renal Physiol 302: F159-F172, 2012.