Signaling pathways in diabetic nephropathy

Histology and Histopathology

Volumn 31, Issue 10, 2016, Pages 1059-1067

  Kawanami, Daiji ^a   Matoba, Keiichiro ^a   Utsunomiya, Kazunori ^a  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Diabetic nephropathy; Hemodynamic mechanism; Metabolic pathways; Rho kinase

Indexed keywords

ANIMAL; DIABETIC NEPHROPATHY; HUMAN; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; DIABETIC NEPHROPATHIES; HUMANS; SIGNAL TRANSDUCTION;

EID: 84982920434     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: 10.14670/HH-11-777     Document Type: Review

References (78)

1. Adler A.I., Stevens R.J., Manley S.E., Bilous R.W., Cull C.A. and Holman R.R. (2003). Development and progression of nephropathy in type 2 diabetes: The united kingdom prospective diabetes study (ukpds 64). Kidney Int. 63, 225-232.
2. Arendshorst W.J., Brannstrom K. and Ruan X. (1999). Actions of angiotensin ii on the renal microvasculature. J. Am. Soc. Nephrol. 10 (Suppl 11), S149-161.
3. Asanuma K., Yanagida-Asanuma E., Faul C., Tomino Y., Kim K. and Mundel P. (2006). Synaptopodin orchestrates actin organization and cell motility via regulation of rhoa signalling. Nat. Cell Biol. 8, 485-491
4. Blanco D., Vicent S., Elizegi E., Pino I., Fraga M.F., Esteller M., Saffiotti U., Lecanda F. and Montuenga L.M. (2004). Altered expression of adhesion molecules and epithelial-mesenchymal transition in silicainduced rat lung carcinogenesis. Lab. Invest. 84, 999-1012.
5. Brenner B.M., Cooper M.E., de Zeeuw D., Keane W.F., Mitch W.E., Parving H.H., Remuzzi G., Snapinn S.M., Zhang Z., Shahinfar S. and Investigators R.S. (2001). Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N. Engl. J. Med. 345, 861-869.
6. Brownlee M. (2001). Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820.
7. Carmines P.K., Ohishi K. and Ikenaga H. (1996). Functional impairment of renal afferent arteriolar voltage-gated calcium channels in rats with diabetes mellitus. J. Clin. Invest. 98, 2564-2571.
8. Checherita I.A., Manda G., Hinescu M.E., Peride I., Niculae A., Bilha S., Gramaticu A., Voroneanu L. and Covic A. (2016). New molecular insights in diabetic nephropathy. Int. Urol. Nephrol. 48, 373-387.
9. Cherney D.Z., Perkins B.A., Soleymanlou N., Maione M., Lai V., Lee A., Fagan N.M., Woerle H.J., Johansen O.E., Broedl U.C. and von Eynatten M. (2014). Renal hemodynamic effect of sodium-glucose cotransporter 2 inhibition in patients with type 1 diabetes mellitus. Circulation 129, 587-597.
10. Craven P.A., Davidson C.M. and DeRubertis F.R. (1990). Increase in diacylglycerol mass in isolated glomeruli by glucose from de novo synthesis of glycerolipids. Diabetes 39, 667-674.
11. De Nicola L., Gabbai F.B., Liberti M.E., Sagliocca A., Conte G. and Minutolo R. (2014). Sodium/glucose cotransporter 2 inhibitors and prevention of diabetic nephropathy: Targeting the renal tubule in diabetes. Am. J. Kidney Dis. 64, 16-24.
12. Flyvbjerg A., Denner L., Schrijvers B.F., Tilton R.G., Mogensen T.H., Paludan S.R. and Rasch R. (2004). Long-term renal effects of a neutralizing rage antibody in obese type 2 diabetic mice. Diabetes 53, 166-172.
13. Forbes J.M., Fukami K. and Cooper M.E. (2007). Diabetic nephropathy: Where hemodynamics meets metabolism. Exp. Clin. Endocrinol. Diabetes 115, 69-84.
14. Forstermann U. and Sessa W.C. (2012). Nitric oxide synthases: Regulation and function. Eur. Heart J. 33, 829, 837a-837d.
15. Geraldes P. and King G.L. (2010). Activation of protein kinase c isoforms and its impact on diabetic complications. Circ. Res. 106, 1319-1331.
16. Gilbert R.E. (2014). Sodium-glucose linked transporter-2 inhibitors: Potential for renoprotection beyond blood glucose lowering? Kidney Int. 86, 693-700.
17. Gojo A., Utsunomiya K., Taniguchi K., Yokota T., Ishizawa S., Kanazawa Y., Kurata H. and Tajima N. (2007). The rho-kinase inhibitor, fasudil, attenuates diabetic nephropathy in streptozotocininduced diabetic rats. Eur. J. Pharmacol. 568, 242-247.
18. Hayashi K., Epstein M., Loutzenhiser R. and Forster H. (1992). Impaired myogenic responsiveness of the afferent arteriole in streptozotocininduced diabetic rats: Role of eicosanoid derangements. J. Am. Soc. Nephrol. 2, 1578-1586.
19. Helal I., Fick-Brosnahan G.M., Reed-Gitomer B. and Schrier R.W. (2012). Glomerular hyperfiltration: Definitions, mechanisms and clinical implications. Nat. Rev. Nephrol. 8, 293-300.
20. Hofmann M.A., Drury S., Fu C., Qu W., Taguchi A., Lu Y., Avila C., Kambham N., Bierhaus A., Nawroth P., Neurath M.F., Slattery T., Beach D., McClary J., Nagashima M., Morser J., Stern D. and Schmidt A.M. (1999). Rage mediates a novel proinflammatory axis: A central cell surface receptor for s100/calgranulin polypeptides. Cell 97, 889-901.
21. Inoguchi T., Li P., Umeda F., Yu H.Y., Kakimoto M., Imamura M., Aoki T., Etoh T., Hashimoto T., Naruse M., Sano H., Utsumi H. and Nawata H. (2000). High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase c--dependent activation of nad(p)h oxidase in cultured vascular cells. Diabetes 49, 1939-1945.
22. Ishii H., Jirousek M.R., Koya D., Takagi C., Xia P., Clermont A., Bursell S.E., Kern T.S., Ballas L.M., Heath W.F., Stramm L.E., Feener E.P. and King G.L. (1996). Amelioration of vascular dysfunctions in diabetic rats by an oral pkc beta inhibitor. Science 272, 728-731.
23. Ishii H., Tada H. and Isogai S. (1998). An aldose reductase inhibitor prevents glucose-induced increase in transforming growth factorbeta and protein kinase c activity in cultured mesangial cells. Diabetologia 41, 362-364.
24. Ishizaki T., Maekawa M., Fujisawa K., Okawa K., Iwamatsu A., Fujita A., Watanabe N., Saito Y., Kakizuka A., Morii N. and Narumiya S. (1996). The small gtp-binding protein rho binds to and activates a 160 kda ser/thr protein kinase homologous to myotonic dystrophy kinase. EMBO J. 15, 1885-1893.
25. Ishizawa S., Takahashi-Fujigasaki J., Kanazawa Y., Matoba K., Kawanami D., Yokota T., Iwamoto T., Tajima N., Manome Y. and Utsunomiya K. (2014). Sphingosine-1-phosphate induces differentiation of cultured renal tubular epithelial cells under rho kinase activation via the s1p2 receptor. Clin. Exp. Nephrol. 18, 844-852.
26. Isoe T., Makino Y., Mizumoto K., Sakagami H., Fujita Y., Honjo J., Takiyama Y., Itoh H. and Haneda M. (2010). High glucose activates HIF-1-mediated signal transduction in glomerular mesangial cells through a carbohydrate response element binding protein. Kidney Int. 78, 48-59.
27. Jensen L.J., Denner L., Schrijvers B.F., Tilton R.G., Rasch R. and Flyvbjerg A. (2006). Renal effects of a neutralising rage-antibody in long-term streptozotocin-diabetic mice. J. Endocrinol. 188, 493-501.
28. Kagami S., Border W.A., Miller D.E. and Noble N.A. (1994). Angiotensin ii stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J. Clin. Invest. 93, 2431-2437.
29. Kashihara N., Haruna Y., Kondeti V.K. and Kanwar Y.S. (2010). Oxidative stress in diabetic nephropathy. Curr. Med. Chem. 17, 4256-4269.
30. Koya D., Haneda M., Nakagawa H., Isshiki K., Sato H., Maeda S., Sugimoto T., Yasuda H., Kashiwagi A., Ways D.K., King G.L. and Kikkawa R. (2000). Amelioration of accelerated diabetic mesangial expansion by treatment with a pkc beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J. 14, 439-447.
31. Li H., Horke S. and Forstermann U. (2014). Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis 237, 208-219.
32. Liu E., Morimoto M., Kitajima S., Koike T., Yu Y., Shiiki H., Nagata M., Watanabe T. and Fan J. (2007). Increased expression of vascular endothelial growth factor in kidney leads to progressive impairment of glomerular functions. J. Am. Soc. Nephrol. 18, 2094-2104.
33. Lu M., Kuroki M., Amano S., Tolentino M., Keough K., Kim I., Bucala R. and Adamis A.P. (1998). Advanced glycation end products increase retinal vascular endothelial growth factor expression. J. Clin. Invest. 101, 1219-1224.
34. Makino H., Haneda M., Babazono T., Moriya T., Ito S., Iwamoto Y., Kawamori R., Takeuchi M., Katayama S. (2007). Prevention of transition from incipient to overt nephropathy with telmisartan in patients with type 2 diabetes. Diabetes Care 30, 1577-1578.
35. Matoba K., Kawanami D., Ishizawa S., Kanazawa Y., Yokota T. and Utsunomiya K. (2010). Rho-kinase mediates tnf-alpha-induced mcp-1 expression via p38 mapk signaling pathway in mesangial cells. Biochem. Biophys. Res. Commun. 402, 725-730.
36. Matoba K., Kawanami D., Okada R., Tsukamoto M., Kinoshita J., Ito T., Ishizawa S., Kanazawa Y., Yokota T., Murai N., Matsufuji S., Takahashi-Fujigasaki J. and Utsunomiya K. (2013). Rho-kinase inhibition prevents the progression of diabetic nephropathy by downregulating hypoxia-inducible factor 1alpha. Kidney Int. 84, 545-554.
37. Matoba K., Kawanami D., Tsukamoto M., Kinoshita J., Ito T., Ishizawa S., Kanazawa Y., Yokota T., Murai N., Matsufuji S. and Utsunomiya K. (2014). Rho-kinase regulation of tnf-alpha-induced nuclear translocation of nf-kappab rela/p65 and m-csf expression via p38 mapk in mesangial cells. Am. J. Physiol. Renal. Physiol. 307, F571-580.
38. Mehta D., Rahman A. and Malik A.B. (2001). Protein kinase c-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J. Biol. Chem. 276, 22614-22620.
39. Menne J., Shushakova N., Bartels J., Kiyan Y., Laudeley R., Haller H., Park J.K. and Meier M. (2013). Dual inhibition of classical protein kinase c-alpha and protein kinase c-beta isoforms protects against experimental murine diabetic nephropathy. Diabetes 62, 1167-1174.
40. Menne J., Park J.K., Boehne M., Elger M., Lindschau C., Kirsch T., Meier M., Gueler F., Fiebeler A., Bahlmann F.H., Leitges M. and Haller H. (2004). Diminished loss of proteoglycans and lack of albuminuria in protein kinase c-alpha-deficient diabetic mice. Diabetes 53, 2101-2109.
41. Mima A., Kitada M., Geraldes P., Li Q., Matsumoto M., Mizutani K., Qi W., Li C., Leitges M., Rask-Madsen C. and King G.L. (2012). Glomerular vegf resistance induced by pkcdelta/shp-1 activation and contribution to diabetic nephropathy. FASEB J. 26, 2963-2974.
42. Nagahama T., Hayashi K., Ozawa Y., Takenaka T. and Saruta T. (2000). Role of protein kinase c in angiotensin ii-induced constriction of renal microvessels. Kidney Int. 57, 215-223.
43. Nayak B.K., Shanmugasundaram K., Friedrichs W.E., Cavaglierii R.C., Patel M., Barnes J. and Block K. (2016). Hif-1 mediates renal fibrosis in ove26 type 1 diabetic mice. Diabetes (in press)
44. Newton A.C. (2001). Protein kinase C: Structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev. 101, 2353-2364.
45. Nielsen R., Christensen E.I. and Birn H. (2016). Megalin and cubilin in proximal tubule protein reabsorption: From experimental models to human disease. Kidney Int. 89, 58-67.
46. Ohshiro Y., Ma R.C., Yasuda Y., Hiraoka-Yamamoto J., Clermont A.C., Isshiki K., Yagi K., Arikawa E., Kern T.S. and King G.L. (2006). Reduction of diabetes-induced oxidative stress, fibrotic cytokine expression, and renal dysfunction in protein kinase cbeta-null mice. Diabetes 55, 3112-3120.
47. Ozdamar B., Bose R., Barrios-Rodiles M., Wang H.R., Zhang Y. and Wrana J.L. (2005). Regulation of the polarity protein par6 by tgfbeta receptors controls epithelial cell plasticity. Science 307, 1603-1609.
48. Peng F., Wu D., Gao B., Ingram A.J., Zhang B., Chorneyko K., McKenzie R. and Krepinsky J.C. (2008). Rhoa/rho-kinase contribute to the pathogenesis of diabetic renal disease. Diabetes 57, 1683-1692.
49. Peng H., Luo P., Li Y., Wang C., Liu X., Ye Z., Li C. and Lou T. (2013). Simvastatin alleviates hyperpermeability of glomerular endothelial cells in early-stage diabetic nephropathy by inhibition of rhoa/rock1. PLoS One 8, e80009.
50. Peng H., Li Y., Wang C., Zhang J., Chen Y., Chen W., Cao J., Wang Y., Hu Z. and Lou T. (2016). Rock1 induces endothelial-tomesenchymal transition in glomeruli to aggravate albuminuria in diabetic nephropathy. Sci. Rep. 6, 20304.
51. Premaratne E., Verma S., Ekinci E.I., Theverkalam G., Jerums G. and MacIsaac R.J. (2015). The impact of hyperfiltration on the diabetic kidney. Diabetes Metab. 41, 5-17.
52. Ramasamy R., Yan S.F. and Schmidt A.M. (2011). Receptor for age (rage): Signaling mechanisms in the pathogenesis of diabetes and its complications. Ann. NY Acad. Sci. 1243, 88-102.
53. Rask-Madsen C. and King G.L. (2013). Vascular complications of diabetes: Mechanisms of injury and protective factors. Cell. Metab. 17, 20-33.
54. Reiniger N., Lau K., McCalla D., Eby B., Cheng B., Lu Y., Qu W., Quadri N., Ananthakrishnan R., Furmansky M., Rosario R., Song F., Rai V., Weinberg A., Friedman R., Ramasamy R., D’Agati V. and Schmidt A.M. (2010). Deletion of the receptor for advanced glycation end products reduces glomerulosclerosis and preserves renal function in the diabetic ove26 mouse. Diabetes 59, 2043-2054.
55. Rikitake Y. and Liao J.K. (2005). Rho-kinase mediates hyperglycemiainduced plasminogen activator inhibitor-1 expression in vascular endothelial cells. Circulation 111, 3261-3268.
56. Ruiz-Ortega M., Lorenzo O., Ruperez M., Konig S., Wittig B. and Egido J. (2000). Angiotensin ii activates nuclear transcription factor kappab through at(1) and at(2) in vascular smooth muscle cells: Molecular mechanisms. Circ Res 86, 1266-1272.
57. Sanchez A.P. and Sharma K. (2009). Transcription factors in the pathogenesis of diabetic nephropathy. Expert. Rev. Mol. Med. 11, e13.
58. Schleicher E.D. and Weigert C. (2000). Role of the hexosamine biosynthetic pathway in diabetic nephropathy. Kidney Int. (Suppl 77), S13-18.
59. Scivittaro V., Ganz M.B. and Weiss M.F. (2000). Ages induce oxidative stress and activate protein kinase c-beta(ii) in neonatal mesangial cells. Am. J. Physiol. Renal. Physiol. 278, F676-683.
60. Taguchi A., Blood D.C., del Toro G., Canet A., Lee D.C., Qu W., Tanji N., Lu Y., Lalla E., Fu C., Hofmann M.A., Kislinger T., Ingram M., Lu A., Tanaka H., Hori O., Ogawa S., Stern D.M. and Schmidt A.M. (2000). Blockade of rage-amphoterin signalling suppresses tumour growth and metastases. Nature 405, 354-360.
61. Tikellis C., Brown R., Head G.A., Cooper M.E. and Thomas M.C. (2014). Angiotensin-converting enzyme 2 mediates hyperfiltration associated with diabetes. Am. J. Physiol. Renal. Physiol. 306, F773-780.
62. Vlassara H., Striker L.J., Teichberg S., Fuh H., Li Y.M. and Steffes M. (1994). Advanced glycation end products induce glomerular sclerosis and albuminuria in normal rats. Proc. Natl. Acad. Sci. USA 91, 11704-11708.
63. Wang D., Luo P., Wang Y., Li W., Wang C., Sun D., Zhang R., Su T., Ma X., Zeng C., Wang H., Ren J. and Cao F. (2013). Glucagon-like peptide-1 protects against cardiac microvascular injury in diabetes via a camp/pka/rho-dependent mechanism. Diabetes 62, 1697-1708.
64. Wang W., Wang Y., Long J., Wang J., Haudek S.B., Overbeek P., Chang B.H., Schumacker P.T. and Danesh F.R. (2012). Mitochondrial fission triggered by hyperglycemia is mediated by rock1 activation in podocytes and endothelial cells. Cell Metab. 15, 186-200.
65. Wautier M.P., Chappey O., Corda S., Stern D.M., Schmidt A.M. and Wautier J.L. (2001). Activation of nadph oxidase by age links oxidant stress to altered gene expression via rage. Am. J. Physiol. Endocrinol. Metab. 280, E685-694.
66. Weigert C., Brodbeck K., Lehmann R., Haring H.U. and Schleicher E.D. (2001). Overexpression of glutamine:Fructose-6-phosphateamidotransferase induces transforming growth factor-beta1 synthesis in nih-3t3 fibroblasts. FEBS Lett. 488, 95-99.
67. Weigert C., Friess U., Brodbeck K., Haring H.U. and Schleicher E.D. (2003). Glutamine:Fructose-6-phosphate aminotransferase enzyme activity is necessary for the induction of tgf-beta1 and fibronectin expression in mesangial cells. Diabetologia 46, 852-855.
68. Welsh G.I., Hale L.J., Eremina V., Jeansson M., Maezawa Y., Lennon R., Pons D.A., Owen R.J., Satchell S.C., Miles M.J., Caunt C.J., McArdle C.A., Pavenstadt H., Tavare J.M., Herzenberg A.M., Kahn C.R., Mathieson P.W., Quaggin S.E., Saleem M.A. and Coward R.J. (2010). Insulin signaling to the glomerular podocyte is critical for normal kidney function. Cell Metab. 12, 329-340.
69. Wendt T.M., Tanji N., Guo J., Kislinger T.R., Qu W., Lu Y., Bucciarelli L.G., Rong L.L., Moser B., Markowitz G.S., Stein G., Bierhaus A., Liliensiek B., Arnold B., Nawroth P.P., Stern D.M., D'Agati V.D. and Schmidt A.M. (2003). Rage drives the development of glomerulosclerosis and implicates podocyte activation in the pathogenesis of diabetic nephropathy. Am. J. Pathol. 162, 1123-1137.
70. Wu G., Xu M., Xu K. and Hu Y. (2013). Benidipine protects kidney through inhibiting rock1 activity and reducing the epitheliummesenchymal transdifferentiation in type 1 diabetic rats. J. Diabetes Res. 2013, 174526.
71. Xia P., Inoguchi T., Kern T.S., Engerman R.L., Oates P.J. and King G.L. (1994). Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase c pathway in diabetes and hypergalactosemia. Diabetes 43, 1122-1129.
72. Yagihashi S. (1997). Pathogenetic mechanisms of diabetic neuropathy: Lessons from animal models. J. Peripher. Nerv. Syst. 2, 113-132.
73. Yale J.F., Bakris G., Cariou B., Nieto J., David-Neto E., Yue D., Wajs E., Figueroa K., Jiang J., Law G., Usiskin K., Meininger G. (2014). Efficacy and safety of canagliflozin over 52 weeks in patients with type 2 diabetes mellitus and chronic kidney disease. Diabetes Obes. Metab. 16, 1016-1027.
74. Yang X., Ongusaha P.P., Miles P.D., Havstad J.C., Zhang F., So W.V., Kudlow J.E., Michell R.H., Olefsky J.M., Field S.J. and Evans R.M. (2008). Phosphoinositide signalling links o-glcnac transferase to insulin resistance. Nature 451, 964-969.
75. Zeng L., Xu H., Chew T.L., Eng E., Sadeghi M.M., Adler S., Kanwar Y.S. and Danesh F.R. (2005). HMG CoA reductase inhibition modulates VEGf-induced endothelial cell hyperpermeability by preventing rhoa activation and myosin regulatory light chain phosphorylation. FASEB J. 19, 1845-1847.
76. Zhang K., Zhang H., Xiang H., Liu J., Liu Y., Zhang X., Wang J. and Tang Y. (2013). Tgf-beta1 induces the dissolution of tight junctions in human renal proximal tubular cells: Role of the rhoa/rock signaling pathway. Int. J. Mol. Med. 32, 464-468.
77. Zhou L., Liu F., Huang X.R., Chen H., Chung A.C., Shi J., Wei L., Lan H.Y. and Fu P. (2011a). Amelioration of albuminuria in rock1 knockout mice with streptozotocin-induced diabetic kidney disease. Am. J. Nephrol. 34, 468-475.
78. Zhou Q., Gensch C. and Liao J.K. (2011b). Rho-associated coiled-coilforming kinases (rocks): Potential targets for the treatment of atherosclerosis and vascular disease. Trends. Pharmacol. Sci. 32, 167-173.