Effect of Croatian propolis on diabetic nephropathy and liver toxicity in mice

BMC Complementary and Alternative Medicine

Volumn 12, Issue , 2012, Pages

  Oršolić, Nada ^a   Sirovina, Damir ^a   Končić, Marijana Zovko ^b   Lacković, Gordana ^a   Gregorović, Gordana ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

Alloxan; Diabetes; Kidney; Liver; Mice; Propolis

Indexed keywords

ANTIOXIDANT; MALONALDEHYDE; PROPOLIS;

ALLOXAN DIABETES MELLITUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; CELL VACUOLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DRUG EFFECT; EOSINOPHILIA; FATTY ACID METABOLISM; HISTOPATHOLOGY; IN VIVO STUDY; LIPID PEROXIDATION; LIVER TOXICITY; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; SURVIVAL;

ALLOXAN; ANIMALS; ANTIOXIDANTS; CROATIA; DIABETIC NEPHROPATHIES; FEMALE; HUMANS; KIDNEY; LIPID PEROXIDATION; LIVER; MALE; MALONDIALDEHYDE; MICE; OXIDATIVE STRESS; PLANT EXTRACTS; PROPOLIS;

EID: 84864523207     PISSN: None     EISSN: 14726882     Source Type: Journal    
DOI: 10.1186/1472-6882-12-117     Document Type: Article

References (67)

1. Oršolić N, Bašić I. Honey Bee Products and their Polyphenolic Compounds in Tretment of Diabetes. Phytopharmacology and Therapetutic Values IV 2008, 455-471. LLC, U.S.A: Studium Press, Govil JN, Singh VK, [Recent Progress in Medical Plants, vol 22.].
2. Yue KK, Chung WS, Leung AW, Cheng CH. Redox changes precede the occurrence of oxidative stress in eyes and aorta, but not in kidneys of diabetic rats. Life Sci 2003, 73:2557-2570. 10.1016/S0024-3205(03)00662-3, 12967680.
3. Obrosova IG, Minchenko AG, Vasupuram R, White L, Abatan OI, Kumagai AK, Frank RN, Stevens MJ. Aldose reductase inhibitor fidarestat prevents retinal oxidative stress and vascular endothelial growth factor overexpression in streptozotocin-diabetic rats. Diabetes 2003, 52:864-871. 10.2337/diabetes.52.3.864, 12606532.
4. Ha H, Kim KH. Role of oxidative stress in the development of diabetic nephropathy. Kidney Int 1995, 48:18-21.
5. Ruiz-Muñoz LM, Vidal-Vanaclocha F, Lampreabe I. Enalaprilat inhibits hydrogen peroxide production by murine mesangial cells exposed to high glucose concentrations. Nephrol Dial Transplant 1997, 12:456-464. 10.1093/ndt/12.3.456, 9075124.
6. Hunt JV, Bottoms MA, Mitchinson MJ. Oxidative alterations in the experimental glycation model of diabetes mellitus are due to protein-glucose adduct oxidation. Some fundamental differences in proposed mechanisms of glucose oxidation and oxidant production. Biochem J 1993, 291:529-535. 1132557, 8484733.
7. Anjaneyulu M, Chopra K. Effect of irbesartan on the antioxidant defence system and nitric oxide release in diabetic rat kidney. Am J Nephrol 2004, 24:488-496. 10.1159/000080722, 15353911.
8. Yue KK, Leung SN, Man PM, Yeung WF, Chung WS, Lee KW, Leung AW, Cheng CH. Alterations in antioxidant enzyme activities in the eyes, aorta and kidneys of diabetic rats relevant to the onset of oxidative stress. Life Sci 2005, 77:721-734. 10.1016/j.lfs.2004.10.081, 15936347.
9. Oršolić N, Gajski G, Garaj-Vrhovac V, D{stroke}ikić D, Prskalo Z, Sirovina D. DNA-protective effects of quercetin or naringenin in alloxan-induced diabetic mice. Eur J Pharmacol 2011, 656:110-118. 10.1016/j.ejphar.2011.01.021, 21277296.
10. Will JC, Vinicor F, Calle EE. Is diabetes mellitus associated with prostate cancer incidence and survival?. Epidemiology 1999, 10:313-318. 10.1097/00001648-199905000-00021, 10230844.
11. Maisonneuve P, Agodoa L, Gellert R, Stewart JH, Buccianti G, Lowenfels AB, Wolfe RA, Jones E, Disney AP, Briggs D, McCredie M, Boyle P. Cancer in patients on dialysis for end-stage renal disease: an international collaborative study. Lancet 1999, 354:93-99. 10.1016/S0140-6736(99)06154-1, 10408483.
12. Bankova V, De Castro SL, Marcucci MC. Propolis: recent advances in chemistry and plant origin. Apidologie 2000, 31:3-15.
13. Sobočanec S, Šverko V, Balog T, Šarić A, Rusak G, Likic S, Kusić B, Katalinić V, Radić S, Marotti T. Oxidant/antioxidant properties of croatian native propolis. J Agric Food Chem 2006, 54:8018-8026. 10.1021/jf0612023, 17032004.
14. Kosalec I, Sanković K, Zovko M, Oršolić N, Bakmaz M, Kalod{stroke}era Z, Pepeljnjak S. Antimicrobial and Antioxidant Activity of Propolis from Croatia and Brazil: a Comparative Study. Scientific evidence of the use of propolis in ehtnomedicine 2008, 175-194. Kerala: Transworld Research Network, Oršolić N, Bašić I.
15. Natarajan K, Singh S, Burker TR, Grunberger D, Aggarwal BB. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci USA 1996, 93:9090-9095. 10.1073/pnas.93.17.9090, 38600, 8799159.
16. Khalil ML. Biological activity of bee propolis in health and disease. Asian Pac J Cancer Prev 2006, 7:22-31.
17. Oršolić N, Bašić I. Immunomodulation by water-soluble derivate of propolis (WSDP) a factor of antitumor reactivity. J Ethnopharmacol 2003, 84:265-273. 10.1016/S0378-8741(02)00329-X, 12648825.
18. Oršolić N, Bašić I. Cancer prevention by Propolis and its Polyphenolic Compounds in Experimental Animals. Phytochemistry and Pharmacology III 2007, 55-113. LLC, U.S.A: Studium Press, Singh VK, Govil JN, Arunachalam C, [Recent Progress in Medicinal Plants, vol 17.].
19. Sforcin JM. Propolis and the immune system: a review. J Ethnopharmacol 2007, 113:1-14. 10.1016/j.jep.2007.05.012, 17580109.
20. Fischer G, Vidor T. Propolis as an immune system modulator substance. Scientific evidence of the use of propolis in ethnomedicine 2008, 133-147. Kerala: Transworld Research Network, Oršolić N, Bašić I.
21. Chen C, Weng M, Wu C, Lin J. Comparison of radical scavenging activity, cytotoxic effects and apoptosis induction in human melanoma cells by Taiwanese propolis from different sources. CAM 2004, 1:175-185.
22. Abd El-Hady FK, Hegazi AG, Wollenweber E. Effect of Egyptian propolis on the susceptibility of LDL to oxidative modification and its antiviral activity with special emphasis on chemical composition. Z Naturforsch 2007, 62:645-655.
23. Orsi RO, Sforcin JM, Funari SR, Bankova V. Effects of Brazilian and Bulgarian propolis on bactericidal activity of macrophages against Salmonella Typhimurium. Int Immunopharmacol 2005, 5:359-368. 10.1016/j.intimp.2004.10.003, 15652765.
24. Silici S, Kutluca S. Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. J Ethnopharmacol 2005, 99:69-73. 10.1016/j.jep.2005.01.046, 15848022.
25. Oršolić N, Saranović AB, Bašić I. Direct and indirect mechanism(s) of antitumour activity of propolis and its polyphenolic compounds. Planta Med 2006, 72:20-27. 10.1055/s-2005-873167, 16450291.
26. Russo A, Cardile V, Sanchez F, Troncoso N, Vanella A, Garbarino JA. Chilean propolis: antioxidant activity and antiproliferative action in human tumor cell lines. Life Sci 2004, 76:545-558. 10.1016/j.lfs.2004.07.019, 15556167.
27. Benković V, Kopjar N, Horvat Kneževic A, D{stroke}ikić D, Bašić I, Ramić S, Viculin T, Knežević F, Oršolić N. Evaluation of radioprotective effects of propolis and quercetin on human white blood cells in vitro. Biol Pharm Bull 2008, 31:1778-1785. 10.1248/bpb.31.1778, 18758076.
28. Oršolić N, Horvat Knežević A, Benković V, Bašić I. Benefits of use of propolis and related flavonoids against the toxicity of chemotherapeutic agents. Scientific evidence of the use of propolis in ehtnomedicine 2008, 195-222. Kerala: Transworld Research Network, Oršolić N, Bašić I.
29. Oršolić N, Benković V, Lisičić D, D{stroke}ikić D, Erhardt J, Horvat Knežević A. Protective effects of propolis and related polyphenolic/flavonoid compounds against toxicity induced by irinotecan. Med Oncol 2010, 27:1346-1358. 10.1007/s12032-009-9387-5, 20013318.
30. Beyer G, Melzig MF. Effects of propolis on hypoxanthine-xanthine oxidase-induced toxicity in cultivated human cells and on neutrophil elastase activity. Biol Pharm Bull 2005, 28:1183-1186. 10.1248/bpb.28.1183, 15997094.
31. Zhu W, Li YH, Chen ML, Hu FL. Protective effects of Chinese and Brazilian propolis treatment against hepatorenal lesion in diabetic rats. Hum Exp Toxicol 2011, 30:1246-1255. 10.1177/0960327110387456, 20956460.
32. Han X, Shen T, Lou H. Dietary Polyphenols and Their Biological Significance. Int J Mol Sci 2007, 8:950-988.
33. El-Sayed SM, Abo-Salem OM, Aly HA, Mansour AM. Potential antidiabetic and hypolipidemic effects of propolis extract in streptozotocin-induced diabetic rats. Pak J Pharm Sci 2009, 22:168-174.
34. Popova M, Bankova V, Butovska D, Petkov V, Nikolova-Damyanova B, Sabatini AG, Marcazzan GL, Bogdanov S. Validated methods for the quantification of biologically active constituents of poplar-type propolis. Phytochem Analysis 2004, 15:235-240.
35. Chang CC, Yang MH, Wen HM, Chern JC. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 2002, 10:178-182.
36. Kosalec I, Bakmaz M, Pepelnjak S, Knežević S. Quantitative analysis of the flavonoids in raw propolis from northern Croatia. Acta Pharm Nord 2004, 54:65-72.
37. Amarowicz R, Pegg RB, Rahimi-Moghaddam P, Barl B, Weil JA. Free-radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chem 2004, 84:551-562.
38. Al-Saikhan MS, Howard LR, Miller JC. Antioxidant activity and total phenolics in different genotypes of potato (Solanum tuberosum L.). J Food Sci 1995, 60:341-347.
39. Končić ZM, Kremer D, Gruz J, Strnad M, Biševac G, Kosalec I, Piljac-Žegarac J, Karlović K, Šamec D. Antioxidant and antimicrobial properties of Moltkia petraea (Tratt.) Griseb. flower, leaf and stem infusions. Food Chem Toxicol 2010, 48:1537-1542. 10.1016/j.fct.2010.03.021, 20304028.
40. Yen GC, Chen H-Y. Antioxidant activity of various tea extracts in relation to their antimutagenicity. J Agric Food Chem 1995, 43:27-37.
41. Decker EA, Welch B. Role of ferritin as a lipid oxidation catalyst in muscle food. J Agric Food Chem 1990, 38:674-677.
42. Bradfor MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
43. Ohkawa H, Ohishi N, Yagi K. Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-358. 10.1016/0003-2697(79)90738-3, 36810.
44. Blois MS. Antioxidant determinations by the use of a stable free radical. Nature 1958, 181:1199-1201.
45. Hakim ZS, Patel BK, Goyal RK. Effects of chronic ramipril treatment in streptozotocin-induced diabetic rats. Indian J Physiol Pharmacol 1997, 41:353-360.
46. Rajkumar L, Srinivasan N, Balasubramanian K, Govindarajulu P. Increased degradation of dermal collagen in diabetic rats. Indian J Exp Biol 1991, 29:1081-1083.
47. Fuliang HU, Hepburn HR, Xuan H, Chen M, Daya S, Radloff SE. Effects of propolis on blood glucose, blood lipid and free radicals in rats with diabetes mellitus. Pharmacol Res 2005, 51:147-152. 10.1016/j.phrs.2004.06.011, 15629260.
48. Abo-Salem OM, El Edel RH, Harisa GEI, El Halawany N, Ghonaim MM. Experimental Diabetic Nephropathy Can be Prevented by Propolis: Effect on Metabolic Disturbances and Renal Oxidative Parameters. Pak J Pharm Sci 2009, 22:205-210.
49. Bhadauria M, Nirala SK, Shukla S. Propolis protects CYP2E1enzymatic activity and oxidative stress induced by carbon tetrachloride. Mol Cell Biochem 2007, 302:215-224. 10.1007/s11010-007-9443-4, 17410408.
50. Nordmann R, Ribière C, Rouach H. Ethanol-induced lipid peroxidation and oxidative stress in extrahepatic tissues. Alcohol Alcohol 1990, 25:231-237.
51. Ragavan B, Krishnakumari S. Effect of T. Arjuna Stem Bark Extract on Histopathology of Liver, Kidney and Pancreas of Alloxan-Induced Diabetic Rats. Afr J Biochem Res 2006, 9:189-197.
52. Khalil M, Mohamed G, Dallak M, Al-Hashem F, Sakr H, Eid RA, Adly MA, Al-Khateeb M, Banihani S, Hassan Z, Bashir N. The Effect of Citrullus colocynthis Pulp Extract on the Liver of Diabetic Rats a Light and Scanning Electron Microscopic Study. Am J Biochem Biotechnol 2010, 6:155-163.
53. Vinagre AS. Rönnau AD́SRO, Pereira SF, Silveira LU, Wiilland EF, Suyenaga ES: Anti-diabetic effects of Campomanesia xanthocarpa (Berg) leaf decoction. Braz. J Pharm Sci 2010, 46:169-177.
54. AL-Rawi MM. Effect of Trifolium sp. Flowers extracts on the Status of Liver Histology of Streptozotocin-induced Diabetic Rats. S J B S 2007, 14:21-28.
55. Hamada Y, Fukagawa M. A possible role of thioredoxin interacting protein in the pathogenesis of streptozotocin-induced diabetic nephropathy. Kobe Med Sci 2007, 53:53-61.
56. Teoh SL, Latiff AA, Das S. Histological changes in the kidneys of experimental diabetic rats fed with Momordica charantia (bitter gourd) extract. Rom J Morphol Embryol 2010, 51:91-95.
57. Prabhakar S, Starnes J, Shi S, Lonis B, Tran R. Diabetic nephropathy is associated with oxidative stress and decreased renal nitric oxide production. J Am Soc Nephrol 2007, 8:2945-2952.
58. Fioretto P, Mauer M. Histopathology of diabetic nephropathy. Semin Nephrol 2007, 27:195-207. 10.1016/j.semnephrol.2007.01.012, 2746982, 17418688.
59. Wolf G, Chen SD, Ziyadeh FN. From the periphery of the glomerular capillary wall toward the center of disease - Podocyte injury comes of age in diabetic nephropathy. Diabetes 2005, 54:1626-1634. 10.2337/diabetes.54.6.1626, 15919782.
60. Baehr G. Über sie sekretion von glykogen in diabetikernieren. Beitr Z Path Anat u z allg Path 1913, 56:1-12.
61. Saundby R. The bradshawe lecture on the morbid anatomy of diabetes mellitus. Br Med J 1890, 2:435-440. 10.1136/bmj.2.1547.435, 2208095, 20753115.
62. Bunarević A. Patologija 1985, Zagreb: JUMENA.
63. Kolankaya D, Selmanoglu G, Sorkun K, Salih B. Protective effects of Turkish propolis on alcohol-induced serum lipid changes and liver injury in male rats. Food Chem 2002, 78:213-217.
64. Issa AY, Volate SR, Wargovich MJ. The role of phytochemicals in inhibition of cancer and inflammation: New directions and perspectives. J Food Compos Anal 2006, 19:405-419.
65. Galey JB. Potential use of iron chelators against oxidative damage. Adv Pharmacol 1997, 38:167-203.
66. Wang B, Lien Y, Yu Z. Supercritical fluid extractive fractionation - study of the antioxidant activities of propolis. Food Chem 2004, 86:237-243.
67. Orhan I, Şenol FS, Gülpinar AR, Kartal M, Şekeroglu N, Deveci M, Kan Y, Şener B. Acetylcholinesterase inhibitory and antioxidant properties of Cyclotrichium niveum, Thymus praecox subsp. caucasicus var. caucasicus, Echinacea purpurea and E. pallid. Food Chem Toxicol 2009, 47:1304-1310. 10.1016/j.fct.2009.03.004, 19285534.