Can Royal Jelly Protect against Renal Ischemia/Reperfusion Injury in Rats?

10.4103/CJP.CJP_36_19

Mohammad Reza Salahshoor；Cyrus Jalili；Shiva Roshankhah

Ischemia/reperfusion ； renal injury ； royal jelly

The Chinese Journal of Physiology

62卷3期（2019 / 06 / 30）

131 - 137

英文

Royal jelly (RJ) is a honeybee secretion, has numerous medicinal properties in particular antioxidant activities. Ischemia/reperfusion (I/R) is one of the main challenges in acute kidney damage. This study was designed to assess the anti-inflammatory and protective effects of RJ against I/R-induced renal disorders. Forty male rats were randomly divided into four groups (n = 10) as sham (0.9% saline) group, I/R group, RJ group (treated for 15 consecutive days by gavage with 300 mg/kg/day RJ), and I/R + RJ group that were pretreated for 15 consecutive days by gavage with 300 mg/kg/day of RJ. The I/R-induced renal inflammation was evaluated by determining leukocyte infiltration and mRNA expression level of intercellular adhesion molecule-1 and tumor necrotic factor-alpha (TNF-α). Antioxidant capacity of kidneys and thiobarbituric acid reactive species was measured in kidneys for the evaluation of oxidative stress. In addition, the diameter of renal glomeruli, kidney function indicators, and serum nitrite oxide (NO) levels was determined. The I/R increased the completely measured parameters, except the tissue ferric reducing/antioxidant power (FRAP) level, which was decreased compared to the sham group (P ＜ 0.05). However, pretreatment with RJ reduced significantly blood urea nitrogen, kidney malondialdehyde, creatinine, glomerular diameter, leukocyte infiltration, levels of TNF-α, adhesion molecule-1 expression, and NO and increased tissue FRAP compared to the I/R group (P ＜ 0.05). It seems that RJ administration improved I/R-induced acute kidney injury.

1. Ajamieh, HH,Menéndez, S,Martínez-Sánchez, G,Candelario-Jalil, E,Re, L,Giuliani, A(2004).Effects of ozone oxidative preconditioning on nitric oxide generation and cellular redox balance in a rat model of hepatic ischaemia‑reperfusion.Liver Int,24,55-62.
2. Alhasson, F,Seth, RK,Sarkar, S,Kimono, DA,Albadrani, MS,Dattaroy, D(2018).High circulatory leptin mediated NOX‑2‑peroxynitrite‑miR21 axis activate mesangial cells and promotes renal inflammatory pathology in nonalcoholic fatty liver disease.Redox Biol,17,1-5.
3. Ali, RM,Al‑Shorbagy, MY,Helmy, MW,El‑Abhar, HS(2018).Role of Wnt4/β‑catenin, ang II/TGFβ, ACE2, NF‑κB, and IL‑18 in attenuating renal ischemia/reperfusion‑induced injury in rats treated with Vit D and pioglitazone.Eur J Pharmacol,831,68-76.
4. Almeer, RS,AlBasher, GI,Alarifi, S,Alkahtani, S,Ali, D,Abdel Moneim, AE(2019).Royal jelly attenuates cadmium‑induced nephrotoxicity in male mice.Sci Rep,9,5825.
5. Almeer, RS,Kassab, RB,AlBasher, GI,Alarifi, S,Alkahtani, S,Ali, D(2019).Royal jelly mitigates cadmium‑induced neuronal damage in mouse cortex.Mol Biol Rep,46,119-131.
6. Aslan, Z,Aksoy, L(2015).Anti‑inflammatory effects of royal jelly on ethylene glycol induced renal inflammation in rats.Int Braz J Urol,41,1008-1013.
7. Azab, KS,Bashandy, M,Salem, M,Ahmed, O,Tawfik, Z,Helal, H(2011).Royal jelly modulates oxidative stress and tissue injury in gamma irradiated male wister albino rats.N Am J Med Sci,3,268-276.
8. Byrami, G,Boskabady, MH,Jalali, S,Farkhondeh, T(2013).The effect of the extract of crocus sativus on tracheal responsiveness and plasma levels of IL‑4, IFN‑γ, total NO and nitrite in ovalbumin sensitized guinea‑pigs.J Ethnopharmacol,147,530-535.
9. Cosimi, AB,Conti, D,Delmonico, FL,Preffer, FI,Wee, SL,Rothlein, R(1990).In vivo effects of monoclonal antibody to ICAM‑1 (CD54) in nonhuman primates with renal allografts.J Immunol,144,4604-4612.
10. Dalfardi, M,Taghavi, MM,Shariati Kohbanani, M,Taghipour, Z,Nosratabadi, R,Jalili, C(2019).Protective and modulatory effects of royal jelly used against the induced changes in silver nanoparticles on the hippocampus of male rats.Nanomed J,6,136-141.
11. Esfandiari, E,Roshankhah, S,Mardani, M,Hashemibeni, B,Naghsh, E,Kazemi, M(2014).The effect of high frequency electric field on enhancement of chondrogenesis in human adipose‑derived stem cells.Iran J Basic Med Sci,17,571-576.
12. Ferdinandy, P,Schulz, R(2003).Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia‑reperfusion injury and preconditioning.Br J Pharmacol,138,532-543.
13. Flor, RJ,Williams, KN,O’Keeffe, T(2018).Acute kidney injury.Surg Crit Care Emerg Surg,17,159-167.
14. Grigoryev, DN,Liu, M,Hassoun, HT,Cheadle, C,Barnes, KC,Rabb, H(2008).The local and systemic inflammatory transcriptome after acute kidney injury.J Am Soc Nephrol,19,547-558.
15. Hossen, MS,Nahar, T,Gan, SH,Khalil, M(2019).Bioinformatics and therapeutic insights on proteins in royal jelly.Curr Proteomics,16,84-101.
16. Jalili, C,Makalani, F,Roshankhah, S,Sohrabi, K,Salahshoor, MR(2017).Protective effect of resveratrol against morphine damage to kidneys of mice.Int J Morphol,35,1409-1415.
17. Jalili, C,Moradi, D,Roshankhah, S,Salahshoor, MR(2019).Effect of pentoxifylline on kidney damage induced by nitrosamine in male rats.Res Pharm Sci,14,64-73.
18. Kanbur, M,Eraslan, G,Beyaz, L,Silici, S,Liman, BC,Altinordulu, S(2009).The effects of royal jelly on liver damage induced by paracetamol in mice.Exp Toxicol Pathol,61,123-132.
19. Karadeniz, A,Simsek, N,Karakus, E,Yildirim, S,Kara, A,Can, I(2011).Royal jelly modulates oxidative stress and apoptosis in liver and kidneys of rats treated with cisplatin.Oxid Med Cell Longev,2011,981793.
20. Kelly, KJ,Williams, WW, Jr.,Colvin, RB,Meehan, SM,Springer, TA,Gutierrez‑Ramos, JC(1996).Intercellular adhesion molecule‑1‑deficient mice are protected against ischemic renal injury.J Clin Invest,97,1056-1063.
21. Li, QP,Wei, RB,Yang, X,Zheng, XY,Su, TY,Huang, MJ(2019).Protective effects and mechanisms of shenhua tablet () on toll‑like receptors in rat model of renal ischemia‑reperfusion injury.Chin J Integr Med,25,44-37.
22. Mahmoudzadeh, L,Najafi, H,Ashtiyani, SC,Yarijani, ZM.(2017).Anti‑inflammatory and protective effects of saffron extract in ischaemia/reperfusion‑induced acute kidney injury.Nephrology,22,748-754.
23. Maqsoudlou, A,Mahoonak, AS,Mora, L,Mohebodini, H,Toldrá, F,Ghorbani, M(2019).Peptide identification in alcalase hydrolysated pollen and comparison of its bioactivity with royal jelly.Food Res Int,116,905-915.
24. Momeni, A,Salahshoor, MR,Jalili, F,Jalili, C(2017).Investigation of the effect of royal jelly on amount of nitric oxide in ovariectomized rats.Pharmacophore,8
25. Najafi, H,Owji, SM,Kamali‑Sarvestani, E,Moosavi, SM(2016).A1 ‑adenosine receptor activation has biphasic roles in development of acute kidney injury at 4 and 24 h of reperfusion following ischaemia in rats.Exp Physiol,101,913-931.
26. Perrone, S,Weiss, MD,Proietti, F,Rossignol, C,Cornacchione, S,Bazzini, F(2018).Identification of a panel of cytokines in neonates with hypoxic ischemic encephalopathy treated with hypothermia.Cytokine,111,119-124.
27. Rabb, H,Daniels, F,O’Donnell, M,Haq, M,Saba, SR,Keane, W(2000).Pathophysiological role of T lymphocytes in renal ischemia‑reperfusion injury in mice.Am J Physiol Renal Physiol,279,F525-F531.
28. Roshankhah, SH,Salahshoor, MR,Jalili, F,Karimi, F,Sohrabi, M,Jalili, C(2017).Crocin effects on the nicotine‑induce ovary injuries in female rat.Int J Life Sci Pharm,7,1-8.
29. Salahshoor, MR,Roshankhah, S,Hosseni, P,Jalili, C(2018).Genistein improves liver damage in male mice exposed to morphine.Chin Med J,131,1598-1604.
30. Silici, S,Ekmekcioglu, O,Eraslan, G,Demirtas, A(2009).Antioxidative effect of royal jelly in cisplatin‑induced testes damage.Urology,74,545-551.
31. Star, RA(1998).Treatment of acute renal failure.Kidney Int,54,1817-1831.
32. Viuda‑Martos, M,Ruiz‑Navajas, Y,Fernández‑López, J,Pérez‑Alvarez, JA(2008).Functional properties of honey, propolis, and royal jelly.J Food Sci,73,R117-R124.
33. Yonei, Y,Shibagaki, K,Tsukada, N,Nagasu, N,Inagaki, Y,Miyamoto, K(1997).Case report: Haemorrhagic colitis associated with royal jelly intake.J Gastroenterol Hepatol,12,495-499.

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