Proteomic analysis of kidney and protective effects of grape seed procyanidin B2 in db/db mice indicate MFG-E8 as a key molecule in the development of diabetic nephropathy

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 6, 2013, Pages 805-816

  Zhang, Zhen ^a   Li, Bao Ying ^a   Li, Xiao Li ^a   Cheng, Mei ^a   Yu, Fei ^a   Lu, Wei Da ^a   Cai, Qian ^a   Wang, Jun Fu ^b   Zhou, Rui Hai ^c   Gao, Hai Qing ^a   Shen, Lin ^a  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Db db mice; Diabetic nephropathy; Grape seed procyanidin B2; ITRAQ; MFG E8

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; GRAPE SEED PROCYANIDIN B2; LACTADHERIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROCYANIDIN DERIVATIVE; PROTEIN KINASE B; PROTEOME; RECOMBINANT LACTADHERIN; RECOMBINANT PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DRUG EFFICACY; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GRAPE; HISTOPATHOLOGY; ISOBARIC TAGS FOR RELATIVE AND ABSOLUTE QUANTIFICATION; KIDNEY; KIDNEY DYSFUNCTION; LIMIT OF QUANTITATION; MALE; MOLECULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEOMICS; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84875579060     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.02.022     Document Type: Article

References (58)

1. Atkins R.C. The epidemiology of chronic kidney disease. Kidney Int. Suppl. 2005, S14-S18.
2. Luis-Rodriguez D., Martinez-Castelao A., Gorriz J.L., De-Alvaro F., Navarro-Gonzalez J.F. Pathophysiological role and therapeutic implications of inflammation in diabetic nephropathy. World J. Diabetes 2012, 3:7-18.
3. Vivian E.M. Type 2 diabetes in children and adolescents-the next epidemic?. Curr. Med. Res. Opin. 2006, 22:297-306.
4. Navarro-Gonzalez J.F., Mora-Fernandez C. The role of inflammatory cytokines in diabetic nephropathy. J. Am. Soc. Nephrol. 2008, 19:433-442.
5. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N. Engl. J. Med. 1993, 329:977-986.
6. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998, 352:837-853.
7. Ohkubo Y., Kishikawa H., Araki E., Miyata T., Isami S., Motoyoshi S., Kojima Y., Furuyoshi N., Shichiri M. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res. Clin. Pract. 1995, 28:103-117.
8. Giunti S., Barit D., Cooper M.E. Diabetic nephropathy: from mechanisms to rational therapies. Minerva Med. 2006, 97:241-262.
9. 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.
10. Koya D., Hayashi K., Kitada M., Kashiwagi A., Kikkawa R., Haneda M. Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. J. Am. Soc. Nephrol. 2003, 14:S250-S253.
11. Takayanagi R., Inoguchi T., Ohnaka K. Clinical and experimental evidence for oxidative stress as an exacerbating factor of diabetes mellitus. J. Clin. Biochem. Nutr. 2011, 48:72-77.
12. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005, 54:1615-1625.
13. Vasavada N., Agarwal R. Role of oxidative stress in diabetic nephropathy. Adv. Chronic Kidney Dis. 2005, 12:146-154.
14. Kitada M., Kume S., Imaizumi N., Koya D. Resveratrol improves oxidative stress and protects against diabetic nephropathy through normalization of Mn-SOD dysfunction in AMPK/SIRT1-independent pathway. Diabetes 2011, 60:634-643.
15. Kuhad A., Chopra K. Attenuation of diabetic nephropathy by tocotrienol: involvement of NFκB signaling pathway. Life Sci. 2009, 84:296-301.
16. Palsamy P., Subramanian S. Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2-Keap1 signaling. Biochim. Biophys. Acta 2011, 1812:719-731.
17. Houde V., Grenier D., Chandad F. Protective effects of grape seed proanthocyanidins against oxidative stress induced by lipopolysaccharides of periodontopathogens. J. Periodontol. 2006, 77:1371-1379.
18. Shao Z.H., Becker L.B., Vanden Hoek T.L., Schumacker P.T., Li C.Q., Zhao D., Wojcik K., Anderson T., Qin Y., Dey L., Yuan C.S. Grape seed proanthocyanidin extract attenuates oxidant injury in cardiomyocytes. Pharmacol. Res. 2003, 47:463-469.
19. Vayalil P.K., Mittal A., Katiyar S.K. Proanthocyanidins from grape seeds inhibit expression of matrix metalloproteinases in human prostate carcinoma cells, which is associated with the inhibition of activation of MAPK and NF kappa B. Carcinogenesis 2004, 25:987-995.
20. Li B.Y., Cheng M., Gao H.Q., Ma Y.B., Xu L., Li X.H., Li X.L., You B.A. Back-regulation of six oxidative stress proteins with grape seed proanthocyanidin extracts in rat diabetic nephropathy. J. Cell. Biochem. 2008, 104:668-679.
21. Li X., Xiao Y., Gao H., Li B., Xu L., Cheng M., Jiang B., Ma Y. Grape seed proanthocyanidins ameliorate diabetic nephropathy via modulation of levels of AGE, RAGE and CTGF. Nephron Exp. Nephrol. 2009, 111:e31-e41.
22. Li X.L., Li B.Y., Gao H.Q., Cheng M., Xu L., Li X.H., Zhang W.D., Hu J.W. Proteomics approach to study the mechanism of action of grape seed proanthocyanidin extracts on arterial remodeling in diabetic rats. Int. J. Mol. Med. 2010, 25:237-248.
23. Chen D.M., Cai X., Kwik-Uribe C.L., Zeng R., Zhu X.Z. Inhibitory effects of procyanidin B(2) dimer on lipid-laden macrophage formation. J. Cardiovasc. Pharmacol. 2006, 48:54-70.
24. Li B.Y., Li X.L., Cai Q., Gao H.Q., Cheng M., Zhang J.H., Wang J.F., Yu F., Zhou R.H. Induction of lactadherin mediates the apoptosis of endothelial cells in response to advanced glycation end products and protective effects of grape seed procyanidin B2 and resveratrol. Apoptosis 2011, 16:732-745.
25. Mackenzie G.G., Adamo A.M., Decker N.P., Oteiza P.I. Dimeric procyanidin B2 inhibits constitutively active NF-kappaB in Hodgkin's lymphoma cells independently of the presence of IkappaB mutations. Biochem. Pharmacol. 2008, 75:1461-1471.
26. Dong Y.F., Liu L., Lai Z.F., Yamamoto E., Kataoka K., Nakamura T., Fukuda M., Tokutomi Y., Nako H., Ogawa H., Kim-Mitsuyama S. Aliskiren enhances protective effects of valsartan against type 2 diabetic nephropathy in mice. J. Hypertens. 2010, 28:1554-1565.
27. Adler S. Structure-function relationships associated with extracellular matrix alterations in diabetic glomerulopathy. J. Am. Soc. Nephrol. 1994, 5:1165-1172.
28. Koya D., Haneda M., Nakagawa H., Isshiki K., Sato H., Maeda S., Sugimoto T., Yasuda H., Kashiwagi A., Ways D.K., King G.L., Kikkawa R. 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. 2000, 14:439-447.
29. Steffes M.W., Osterby R., Chavers B., Mauer S.M. Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients. Diabetes 1989, 38:1077-1081.
30. Sharma K., McCue P., Dunn S.R. Diabetic kidney disease in the db/db mouse. Am. J. Physiol. Renal Physiol. 2003, 284:F1138-F1144.
31. Tesch G.H., Lim A.K. Recent insights into diabetic renal injury from the db/db mouse model of type 2 diabetic nephropathy. Am. J. Physiol. Renal Physiol. 2011, 300:F301-F310.
32. Shimoike T., Inoguchi T., Umeda F., Nawata H., Kawano K., Ochi H. The meaning of serum levels of advanced glycosylation end products in diabetic nephropathy. Metabolism 2000, 49:1030-1035.
33. Busch M., Franke S., Ruster C., Wolf G. Advanced glycation end-products and the kidney. Eur. J. Clin. Invest. 2010, 40:742-755.
34. Tan A.L., Forbes J.M., Cooper M.E. AGE, RAGE, and ROS in diabetic nephropathy. Semin. Nephrol. 2007, 27:130-143.
35. Kolch W. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem. J. 2000, 351(Pt 2):289-305.
36. Cohen M.P., Shea E., Chen S., Shearman C.W. Glycated albumin increases oxidative stress, activates NF-kappa B and extracellular signal-regulated kinase (ERK), and stimulates ERK-dependent transforming growth factor-beta 1 production in macrophage RAW cells. J. Lab. Clin. Med. 2003, 141:242-249.
37. Liu W., Lan T., Xie X., Huang K., Peng J., Huang J., Shen X., Liu P., Huang H. S1P2 receptor mediates sphingosine-1-phosphate-induced fibronectin expression via MAPK signaling pathway in mesangial cells under high glucose condition. Exp. Cell Res. 2012, 318:936-943.
38. Nagai Y., Miyata K., Sun G.P., Rahman M., Kimura S., Miyatake A., Kiyomoto H., Kohno M., Abe Y., Yoshizumi M., Nishiyama A. Aldosterone stimulates collagen gene expression and synthesis via activation of ERK1/2 in rat renal fibroblasts. Hypertension 2005, 46:1039-1045.
39. Perlman A., Lawsin L.M., Kolachana P., Saji M., Moore J., Ringel M.D. Angiotensin II regulation of TGF-beta in murine mesangial cells involves both PI3 kinase and MAP kinase. Ann. Clin. Lab. Sci. 2004, 34:277-286.
40. Gu L., Hagiwara S., Fan Q., Tanimoto M., Kobata M., Yamashita M., Nishitani T., Gohda T., Ni Z., Qian J., Horikoshi S., Tomino Y. Role of receptor for advanced glycation end-products and signalling events in advanced glycation end-product-induced monocyte chemoattractant protein-1 expression in differentiated mouse podocytes. Nephrol. Dial. Transplant. 2006, 21:299-313.
41. Paez J., Sellers W.R. PI3K/PTEN/AKT pathway. A critical mediator of oncogenic signaling. Cancer Treat. Res. 2003, 115:145-167.
42. Kato M., Yuan H., Xu Z.G., Lanting L., Li S.L., Wang M., Hu M.C., Reddy M.A., Natarajan R. Role of the Akt/FoxO3a pathway in TGF-beta1-mediated mesangial cell dysfunction: a novel mechanism related to diabetic kidney disease. J. Am. Soc. Nephrol. 2006, 17:3325-3335.
43. Mahimainathan L., Das F., Venkatesan B., Choudhury G.G. Mesangial cell hypertrophy by high glucose is mediated by downregulation of the tumor suppressor PTEN. Diabetes 2006, 55:2115-2125.
44. Sun L., Kondeti V.K., Xie P., Raparia K., Kanwar Y.S. Epac1-mediated, high glucose-induced renal proximal tubular cells hypertrophy via the Akt/p21 pathway. Am. J. Pathol. 2011, 179:1706-1718.
45. Jope R.S., Johnson G.V. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 2004, 29:95-102.
46. Jiang Y., Cheng D.W., Levi E., Singh L.P. IGF-1 increases laminin, cyclin D1, and p21Cip1 expression in glomerular mesangial cells: an investigation of the intracellular signaling pathway and cell-cycle progression. J. Cell. Biochem. 2006, 98:208-220.
47. Lin Y.P., Hsu M.E., Chiou Y.Y., Hsu H.Y., Tsai H.C., Peng Y.J., Lu C.Y., Pan C.Y., Yu W.C., Chen C.H., Chi C.W., Lin C.H. Comparative proteomic analysis of rat aorta in a subtotal nephrectomy model. Proteomics 2010, 10:2429-2443.
48. Aziz M.M., Ishihara S., Mishima Y., Oshima N., Moriyama I., Yuki T., Kadowaki Y., Rumi M.A., Amano Y., Kinoshita Y. MFG-E8 attenuates intestinal inflammation in murine experimental colitis by modulating osteopontin-dependent alphavbeta3 integrin signaling. J. Immunol. 2009, 182:7222-7232.
49. Hanayama R., Tanaka M., Miwa K., Shinohara A., Iwamatsu A., Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002, 417:182-187.
50. Motegi S., Leitner W.W., Lu M., Tada Y., Sardy M., Wu C., Chavakis T., Udey M.C. Pericyte-derived MFG-E8 regulates pathologic angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2024-2034.
51. Silvestre J.S., Thery C., Hamard G., Boddaert J., Aguilar B., Delcayre A., Houbron C., Tamarat R., Blanc-Brude O., Heeneman S., Clergue M., Duriez M., Merval R., Levy B., Tedgui A., Amigorena S., Mallat Z. Lactadherin promotes VEGF-dependent neovascularization. Nat. Med. 2005, 11:499-506.
52. Wang M., Fu Z., Wu J., Zhang J., Jiang L., Khazan B., Telljohann R., Zhao M., Krug A.W., Pikilidou M., Monticone R.E., Wersto R., Van Eyk J., Lakatta E.G. MFG-E8 activates proliferation of vascular smooth muscle cells via integrin signaling. Aging Cell 2012, 11:500-508.
53. Fu Z., Wang M., Gucek M., Zhang J., Wu J., Jiang L., Monticone R.E., Khazan B., Telljohann R., Mattison J., Sheng S., Cole R.N., Spinetti G., Pintus G., Liu L., Kolodgie F.D., Virmani R., Spurgeon H., Ingram D.K., Everett A.D., Lakatta E.G., Van Eyk J.E. Milk fat globule protein epidermal growth factor-8: a pivotal relay element within the angiotensin II and monocyte chemoattractant protein-1 signaling cascade mediating vascular smooth muscle cells invasion. Circ. Res. 2009, 104:1337-1346.
54. Hagiwara S., Makita Y., Gu L., Tanimoto M., Zhang M., Nakamura S., Kaneko S., Itoh T., Gohda T., Horikoshi S., Tomino Y. Eicosapentaenoic acid ameliorates diabetic nephropathy of type 2 diabetic KKAy/Ta mice: involvement of MCP-1 suppression and decreased ERK1/2 and p38 phosphorylation. Nephrol. Dial. Transplant. 2006, 21:605-615.
55. Wu D., Peng F., Zhang B., Ingram A.J., Gao B., Krepinsky J.C. Collagen I induction by high glucose levels is mediated by epidermal growth factor receptor and phosphoinositide 3-kinase/Akt signalling in mesangial cells. Diabetologia 2007, 50:2008-2018.
56. Juhaszova M., Zorov D.B., Kim S.H., Pepe S., Fu Q., Fishbein K.W., Ziman B.D., Wang S., Ytrehus K., Antos C.L., Olson E.N., Sollott S.J. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 2004, 113:1535-1549.
57. Nishihara M., Miura T., Miki T., Tanno M., Yano T., Naitoh K., Ohori K., Hotta H., Terashima Y., Shimamoto K. Modulation of the mitochondrial permeability transition pore complex in GSK-3beta-mediated myocardial protection. J. Mol. Cell. Cardiol. 2007, 43:564-570.
58. Landau D., Eshet R., Troib A., Gurman Y., Chen Y., Rabkin R., Segev Y. Increased renal Akt/mTOR and MAPK signaling in type I diabetes in the absence of IGF type 1 receptor activation. Endocrine 2009, 36:126-134.