Grape seed proanthocyanidin extract ameliorates diabetic bladder dysfunction via the activation of the Nrf2 pathway

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Chen, Shouzhen ^a   Zhu, Yaofeng ^a   Liu, Zhifeng ^a,b   Gao, Zhaoyun ^c   Li, Baoying ^a   Zhang, Dongqing ^a   Zhang, Zhaocun ^a   Jiang, Xuewen ^a   Liu, Zhengfang ^a   Meng, Lingquan ^a   Yang, Yue ^a   Shi, Benkang ^a  

^a SHANDONG UNIVERSITY   (China)

^b The Central Hospital of Tai'an   (China)

^c People's Hospital of Yinan County   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GLUTATHIONE PEROXIDASE; GRAPE SEED EXTRACT; HEME OXYGENASE 1; MALONALDEHYDE; NERVE GROWTH FACTOR; PROANTHOCYANIDIN; PROTEIN BAX; PROTEIN BCL 2; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; GRAPE SEED PROANTHOCYANIDINS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BLADDER DYSFUNCTION; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFICACY; ENZYME ACTIVITY; FEMALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; BLADDER; COMPLICATION; DIABETES COMPLICATIONS; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; WISTAR RAT;

RATTUS; VITACEAE;

ANIMALS; APOPTOSIS; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; GRAPE SEED EXTRACT; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROANTHOCYANIDINS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; URINARY BLADDER;

EID: 84929379749     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126457     Document Type: Article

References (53)

1. Ferreira D, Li XC. Oligomeric proanthocyanidins: naturally occurring O-heterocycles. Nat Prod Rep. 2000; 17:193-212. PMID: 10821113
2. Asha Devi S, Sagar Chandrasekar BK, Manjula KR, Ishii N. Grape seed proanthocyanidin lowers brain oxidative stress in adult and middle-aged rats. Exp Gerontol. 2011; 46:958-964. doi: 10.1016/j.exger. 2011.08.006 PMID: 21871550
3. Li J, Liu H, Ramachandran S, Waypa GB, Yin JJ, Li CQ, et al. Grape seed proanthocyanidins ameliorate Doxorubicin-induced cardiotoxicity. Am J Chin Med. 2010; 38:569-584. PMID: 20503473
4. Bagchi D, Garg A, Krohn RL, Bagchi M, Tran MX, Stohs SJ. Oxygen free radical scavenging abilities of vitamins C and E, and a grape seed proanthocyanidin extract in vitro. Res Commun Mol Pathol Pharmacol. 1997; 95:179-189. PMID: 9090754
5. Yu F, Li BY, Li XL, Cai Q, Zhang Z, Cheng M, et al. Proteomic analysis of aorta and protective effects of grape seed procyanidin B2 in db/db mice reveal a critical role of milk fat globule epidermal growth factor-8 in diabetic arterial damage. PLoS One. 2012; 7:e52541. doi: 10.1371/journal.pone.0052541 PMID: 23285083
6. Ulusoy S, Ozkan G, Mungan S, Orem A, Yulug E, Alkanat M, et al. GSPE is superior to NAC in the prevention of contrast-induced nephropathy: might this superiority be related to caspase 1 and calpain 1? Life Sci. 2014; 103:101-110. doi: 10.1016/j.lfs.2014.03.030 PMID: 24727104
7. Ulusoy S, Ozkan G, Alkanat M, Mungan S, Yulug E, Orem A. Perspective on rhabdomyolysis-induced acute kidney injury and new treatment options. Am J Nephrol. 2013; 38:368-378. doi: 10.1159/000355537 PMID: 24158126
8. Vinson JA, Mandarano MA, Shuta DL, Bagchi M, Bagchi D. Beneficial effects of a novel IH636 grape seed proanthocyanidin extract and a niacin-bound chromium in a hamster atherosclerosis model. Mol Cell Biochem. 2002; 240:99-103. PMID: 12487376
9. Cui XP, Li BY, Gao HQ, Wei N, Wang WL, Lu M. Effects of grape seed proanthocyanidin extracts on peripheral nerves in streptozocin-induced diabetic rats. J Nutr Sci Vitaminol (Tokyo). 2008; 54:321-328. PMID: 18797155
10. Kirschner-Hermanns R, Daneshgari F, Vahabi B, Birder L, Oelke M, Chacko S. Does diabetes mellitus-induced bladder remodeling affect lower urinary tract function? ICI-RS 2011. Neurourol Urodyn. 2012; 31:359-364. doi: 10.1002/nau.22228 PMID: 22415965
11. Daneshgari F, Liu G, Birder L, Hanna-Mitchell AT, Chacko S. Diabetic bladder dysfunction: current translational knowledge. J Urol. 2009; 182:S18-26. doi: 10.1016/j.juro.2009.08.070 PMID: 19846137
12. Liu G, Daneshgari F. Diabetic bladder dysfunction. Chin Med J (Engl). 2014; 127:1357-1364. PMID: 24709194
13. Roberts CK, Sindhu KK. Oxidative stress and metabolic syndrome. Life Sci. 2009; 84:705-712. doi: 10. 1016/j.lfs.2009.02.026 PMID: 19281826
14. Kanika ND, Chang J, Tong Y, Tiplitsky S, Lin J, Yohannes E, et al. Oxidative stress status accompanying diabetic bladder cystopathy results in the activation of protein degradation pathways. BJU Int. 2011; 107:1676-1684. doi: 10.1111/j.1464-410X.2010.09655.x PMID: 21518418
15. Ha US, Bae WJ, Kim SJ, Yoon BI, Jang H, Hong SH, et al. Protective effect of cyanidin-3-O-beta-Dglucopyranoside fraction from mulberry fruit pigment against oxidative damage in streptozotocin-induced diabetic rat bladder. Neurourol Urodyn. 2013; 32:493-499. doi: 10.1002/nau.22334 PMID: 23129268
16. Li Y, Shi B, Wang D, Wang P, Laudon V, Zhang J, et al. Nerve growth factor and substance P: expression in a rat model of diabetic bladder. Int Urol Nephrol. 2011; 43:109-116. doi: 10.1007/s11255-010-9747-2 PMID: 20490673
17. Wang D, Li Y, Hou G, Wang P, Zhang J, Laudon V, et al. Pygeum africanum: effect on oxidative stress in early diabetes-induced bladder. Int Urol Nephrol. 2010; 42:401-408. doi: 10.1007/s11255-009-9610-5 PMID: 19609708
18. Ishii T, Itoh K, Yamamoto M. Roles of Nrf2 in activation of antioxidant enzyme genes via antioxidant responsive elements. Methods Enzymol. 2002; 348:182-190. PMID: 11885271
19. Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal. 2005; 7:385-394. PMID: 15706085
20. Scapagnini G, Vasto S, Abraham NG, Caruso C, Zella D, Fabio G. Modulation of Nrf2/ARE pathway by food polyphenols: a nutritional neuroprotective strategy for cognitive and neurodegenerative disorders. Mol Neurobiol. 2011; 44:192-201. doi: 10.1007/s12035-011-8181-5 PMID: 21499987
21. Niture SK, Khatri R, Jaiswal AK. Regulation of Nrf2-an update. Free Radic Biol Med. 2014; 66:36-44. doi: 10.1016/j.freeradbiomed.2013.02.008 PMID: 23434765
22. Zhang M, An C, Gao Y, Leak RK, Chen J, Zhang F. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog Neurobiol. 2013; 100:30-47. doi: 10.1016/j.pneurobio.2012.09.003 PMID: 23025925
23. Whitman SA, Long M, Wondrak GT, Zheng H, Zhang DD. Nrf2 modulates contractile and metabolic properties of skeletal muscle in streptozotocin-induced diabetic atrophy. Exp Cell Res. 2013; 319:2673-2683. doi: 10.1016/j.yexcr.2013.07.015 PMID: 23896025
24. Jiang X, Bai Y, Zhang Z, Xin Y, Cai L. Protection by sulforaphane from type 1 diabetes-induced testicular apoptosis is associated with the up-regulation of Nrf2 expression and function. Toxicol Appl Pharmacol. 2014; 279:198-210. doi: 10.1016/j.taap.2014.06.009 PMID: 24967692
25. Chen S, Zhu Y, Feng X, Zhang Z, Li S, Shi B. Changes in alpha1-adrenoceptor and NGF/proNGF pathway: a possible mechanism in diabetic urethral dysfunction. Urol Int. 2014; 93:344-351. doi: 10.1159/000355711 PMID: 24577043
26. Torimoto K, Hirao Y, Matsuyoshi H, de Groat WC, Chancellor MB, Yoshimura N. alpha1-Adrenergic mechanism in diabetic urethral dysfunction in rats. J Urol. 2005; 173:1027-1032. PMID: 15711370
27. Liu CM, Zheng GH, Ming QL, Chao C, Sun JM. Sesamin protects mouse liver against nickel-induced oxidative DNA damage and apoptosis by the PI3K-Akt pathway. J Agric Food Chem. 2013; 61:1146-1154. doi: 10.1021/jf304562b PMID: 23317420
28. Li WJ, Oh SJ. Diabetic cystopathy is associated with PARP/JNK/mitochondrial apoptotic pathway-mediated bladder apoptosis. Neurourol Urodyn. 2010; 29:1332-1337. doi: 10.1002/nau.20869 PMID: 20879002
29. Sasaki K, Chancellor MB, Phelan MW, Yokoyama T, Fraser MO, Seki S, et al. Diabetic cystopathy correlates with a long-term decrease in nerve growth factor levels in the bladder and lumbosacral dorsal root Ganglia. J Urol. 2002; 168:1259-1264. PMID: 12187278
30. Ali TK, Al-Gayyar MM, Matragoon S, Pillai BA, Abdelsaid MA, Nussbaum JJ, et al. Diabetes-induced peroxynitrite impairs the balance of pro-nerve growth factor and nerve growth factor, and causes neurovascular injury. Diabetologia. 2011; 54:657-668. doi: 10.1007/s00125-010-1935-1 PMID: 20957344
31. Kaplan SA, Blaivas JG. Diabetic cystopathy. J Diabet Complications. 1988; 2:133-139. PMID: 2975663
32. Arrellano-Valdez F, Urrutia-Osorio M, Arroyo C, Soto-Vega E. A comprehensive review of urologic complications in patients with diabetes. Springerplus. 2014; 3:549. doi: 10.1186/2193-1801-3-549 PMID: 25332855
33. Frimodt-Moller C. Diabetic cystopathy. A review of the urodynamic and clinical features of neurogenic bladder dysfunction in diabetes mellitus. Dan Med Bull. 1978; 25:49-60. PMID: 344005
34. Moller CF, Olesen KP. Diabetic cystopathy. IV: Micturition cystourethrography compared with urodynamic investigation. Dan Med Bull. 1976; 23:291-294. PMID: 1009798
35. Langdale CL, Thor KB, Marson L, Burgard EC. Maintenance of bladder innervation in diabetes: a stereological study of streptozotocin-treated female rats. Auton Neurosci. 2014; 185:59-66. doi: 10.1016/j. autneu.2014.06.007 PMID: 25066250
36. Ren LM, Zhuo YJ, Hao ZS, He HM, Lu HG, Zhao D. Berberine improves neurogenic contractile response of bladder detrusor muscle in streptozotocin-induced diabetic rats. J Ethnopharmacol. 2013; 150:1128-1136. doi: 10.1016/j.jep.2013.10.039 PMID: 24184080
37. Changolkar AK, Hypolite JA, Disanto M, Oates PJ, Wein AJ, Chacko S. Diabetes induced decrease in detrusor smooth muscle force is associated with oxidative stress and overactivity of aldose reductase. J Urol. 2005; 173:309-313. PMID: 15592102
38. Ochodnicky P, Cruz CD, Yoshimura N, Michel MC. Nerve growth factor in bladder dysfunction: contributing factor, biomarker, and therapeutic target. Neurourol Urodyn. 2011; 30:1227-1241. doi: 10.1002/nau.21022 PMID: 21520250
39. Ustuner MC, Kabay S, Ozden H, Guven G, Yucel M, Olgun EG, et al. The protective effects of vitamin E on urinary bladder apoptosis and oxidative stress in streptozotocin-induced diabetic rats. Urology. 2010; 75:902-906. doi: 10.1016/j.urology.2009.06.003 PMID: 19683803
40. Sato M, Bagchi D, Tosaki A, Das DK. Grape seed proanthocyanidin reduces cardiomyocyte apoptosis by inhibiting ischemia/reperfusion-induced activation of JNK-1 and C-JUN. Free Radic Biol Med. 2001; 31:729-737. PMID: 11557310
41. Su L, Deng Y, Zhang Y, Li C, Zhang R, Sun Y, et al. Protective effects of grape seed procyanidin extract against nickel sulfate-induced apoptosis and oxidative stress in rat testes. Toxicol Mech Methods. 2011; 21:487-494. doi: 10.3109/15376516.2011.556156 PMID: 21417627
42. Song Q, Shi Z, Bi W, Liu R, Zhang C, Wang K, et al. Beneficial effect of grape seed proanthocyanidin extract in rabbits with steroid-induced osteonecrosis via protecting against oxidative stress and apoptosis. J Orthop Sci. 2014.
43. Gao Z, Liu G, Hu Z, Li X, Yang X, Jiang B, et al. Grape seed proanthocyanidin extract protects from cisplatin-induced nephrotoxicity by inhibiting endoplasmic reticulum stress-induced apoptosis. Mol Med Rep. 2014; 9:801-807. doi: 10.3892/mmr.2014.1883 PMID: 24399449
44. Tiveron C, Fasulo L, Capsoni S, Malerba F, Marinelli S, Paoletti F, et al. ProNGF\NGF imbalance triggers learning and memory deficits, neurodegeneration and spontaneous epileptic-like discharges in transgenic mice. Cell Death Differ. 2013; 20:1017-1030. doi: 10.1038/cdd.2013.22 PMID: 23538417
45. Klein R, Jing SQ, Nanduri V, O'Rourke E, Barbacid M. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell. 1991; 65:189-197. PMID: 1849459
46. Masoudi R, Ioannou MS, Coughlin MD, Pagadala P, Neet KE, Clewes O, et al. Biological activity of nerve growth factor precursor is dependent upon relative levels of its receptors. J Biol Chem. 2009; 284:18424-18433. doi: 10.1074/jbc.M109.007104 PMID: 19389705
47. Liu P, Kemper LJ, Wang J, Zahs KR, Ashe KH, Pasinetti GM. Grape seed polyphenolic extract specifically decreases abeta∗56 in the brains of Tg2576 mice. J Alzheimers Dis. 2011; 26:657-666. doi: 10. 3233/JAD-2011-110383 PMID: 21743132
48. Roy Chowdhury S, Sengupta S, Biswas S, Sinha TK, Sen R, Basak RK, et al. Bacterial Fucose-Rich Polysaccharide Stabilizes MAPK-Mediated Nrf2/Keap1 Signaling by Directly Scavenging Reactive Oxygen Species during Hydrogen Peroxide-Induced Apoptosis of Human Lung Fibroblast Cells. PLoS One. 2014; 9:e113663. doi: 10.1371/journal.pone.0113663 PMID: 25412177
49. Mimura J, Kosaka K, Maruyama A, Satoh T, Harada N, Yoshida H, et al. Nrf2 regulates NGF mRNA induction by carnosic acid in T98G glioblastoma cells and normal human astrocytes. J Biochem. 2011; 150:209-217. doi: 10.1093/jb/mvr065 PMID: 21596795
50. Hsu YY, Tseng YT, Lo YC. Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol Appl Pharmacol. 2013; 272:787-796. doi: 10. 1016/j.taap.2013.08.008 PMID: 23954465
51. Kumar SV, Nagesh A, Leena M, Shravani G, Chandrasekar V. Incidence of metabolic syndrome and its characteristics of patients attending a diabetic outpatient clinic in a tertiary care hospital. J Nat Sci Biol Med. 2013; 4:57-62. doi: 10.4103/0976-9668.107261 PMID: 23633836
52. Geetha T, Rege SD, Mathews SE, Meakin SO, White MF, Babu JR. Nerve growth factor receptor TrkA, a new receptor in insulin signaling pathway in PC12 cells. J Biol Chem. 2013; 288:23807-23813. doi: 10.1074/jbc.M112.436279 PMID: 23749991
53. Lu M, Xu L, Li B, Zhang W, Zhang C, Feng H, et al. Protective effects of grape seed proanthocyanidin extracts on cerebral cortex of streptozotocin-induced diabetic rats through modulating AGEs/RAGE/NF-kappaB pathway. J Nutr Sci Vitaminol (Tokyo). 2010; 56:87-97. PMID: 20495289