Login Register Cart 0
Generic placeholder image

Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

The Impact of Royal Jelly against Hepatic Ischemia/Reperfusion-Induced Hepatocyte Damage in Rats: The Role of Cytoglobin, Nrf-2/HO-1/COX-4, and P38-MAPK/NF-κB-p65/TNF-α Signaling Pathways

Author(s): Fares E.M. Ali*, Heba M. Saad Eldien, Nashwa A.M. Mostafa, Abdulrahman H. Almaeen, Mohamed R.A. Marzouk, Khalid M. Eid, Ahmed H.E. Ghoziz, Abdelaziz F. Ebrahiem, Mohamed G. Hagag and Osama M. Ghogar

Volume 14, Issue 1, 2021

Published on: 14 May, 2020

Page: [88 - 100] Pages: 13

DOI: 10.2174/1874467213666200514223829

Price: $65

Abstract

Objective: The present study was conducted to elucidate the underlying molecular mechanism as well as the potential hepatoprotective effects of royal jelly (RJ) against hepatic ischemia/ reperfusion (IR) injury.

Methods: Rats were assigned into four groups; sham (received vehicle), IR (30 minutes ischemia and 45 minutes reperfusion), sham pretreated with RJ (200 mg/kg P.O.), and IR pretreated with RJ (200 mg/kg P.O.). The experiment lasted for 28 days.

Results: Hepatic IR significantly induced hepatic dysfunctions, as manifested by elevation of serum transaminases, ALP and LDH levels. Moreover, hepatic IR caused a significant up-regulation of P38-MAPK, NF-κB-p65, TNF-α and MDA levels along with marked down-regulation of Nrf-2, HO-1, COX-4, cytoglobin, IκBa, IL-10, GSH, GST and SOD levels. Additionally, marked histopathological changes were observed after hepatic IR injury. On the contrary, pretreatment with RJ significantly improved hepatic functions along with the alleviation of histopathological changes. Moreover, RJ restored oxidant/antioxidant balance as well as hepatic expressions of Nrf- 2, HO-1, COX-4, and cytoglobin. Simultaneously, RJ significantly mitigated the inflammatory response by down-regulation of P38-MAPK, NF-κB-p65, TNF-α expression.

Conclusion: The present results revealed that RJ has successfully protected the liver against hepatic IR injury through modulation of cytoglobin, Nrf-2/HO-1/COX-4, and P38-MAPK/NF-κB-p65/TNF- α signaling pathways.

Keywords: Royal jelly, hepatic IR, hepatoprotective, Nrf-2/HO-1/COX-4, cytoglobin, P38-MAPK/NF-κB-p65/TNF-α.

Graphical Abstract

[1]
Meirelles, R.F., Junior; Salvalaggio, P.; Rezende, M.B.; Evangelista, A.S.; Guardia, B.D.; Matielo, C.E.; Neves, D.B.; Pandullo, F.L.; Felga, G.E.; Alves, J.A.; Curvelo, L.A.; Diaz, L.G.; Rusi, M.B.; Viveiros Mde, M.; Almeida, M.D.; Pedroso, P.T.; Rocco, R.A.; Meira Filho, S.P. Liver transplantation: history, outcomes and perspectives., 2015, 13, 149-152..
[http://dx.doi.org/10.1590/S1679-45082015RW3164]
[2]
Nastos, C.; Kalimeris, K.; Papoutsidakis, N.; Tasoulis, M.K.; Lykoudis, P.M.; Theodoraki, K.; Nastou, D.; Smyrniotis, V.; Arkadopoulos, N. Global consequences of liver ischemia/reperfusion injury. Oxid. Med. Cell. Longev., 2014, 2014906965
[http://dx.doi.org/10.1155/2014/906965] [PMID: 24799983]
[3]
Yang, W.; Chen, J.; Meng, Y.; Chen, Z.; Yang, J. Novel Targets for Treating Ischemia-Reperfusion Injury in the Liver. Int. J. Mol. Sci., 2018, 19(5)E1302
[http://dx.doi.org/10.3390/ijms19051302] [PMID: 29701719]
[4]
Jaeschke, H.; Woolbright, B.L. Current strategies to minimize hepatic ischemia-reperfusion injury by targeting reactive oxygen species. Transplant. Rev. (Orlando), 2012, 26(2), 103-114.
[http://dx.doi.org/10.1016/j.trre.2011.10.006] [PMID: 22459037]
[5]
Kamel, EO; Hassanein, EH; Ahmed, MA; Ali, FE Perindopril ameliorates hepatic IR injury via regulation of NF‐κB‐p65/TLR‐4, JAK1/STAT‐3, Nrf‐2 and PI3K/Akt/mTOR signaling pathways. The Anatomical Record., 2019. ahead of print
[6]
Peralta, C.; Jiménez-Castro, M.B.; Gracia-Sancho, J. Hepatic ischemia and reperfusion injury: effects on the liver sinusoidal milieu. J. Hepatol., 2013, 59(5), 1094-1106.
[http://dx.doi.org/10.1016/j.jhep.2013.06.017] [PMID: 23811302]
[7]
Mahmoud, A.R.; Ali, F.E.M.; Abd-Elhamid, T.H.; Hassanein, E.H.M. Coenzyme Q10 protects hepatocytes from ischemia reperfusion-induced apoptosis and oxidative stress via regulation of Bax/Bcl-2/PUMA and Nrf-2/FOXO-3/Sirt-1 signaling pathways. Tissue Cell, 2019, 60, 1-13.
[http://dx.doi.org/10.1016/j.tice.2019.07.007] [PMID: 31582012]
[8]
Vilatoba, M.; Eckstein, C.; Bilbao, G.; Frennete, L.; Eckhoff, D.E.; Contreras, J.L. 17beta-estradiol differentially activates mitogen-activated protein-kinases and improves survival following reperfusion injury of reduced-size liver in mice. Transplant. Proc., 2005, 37(1), 399-403.
[http://dx.doi.org/10.1016/j.transproceed.2004.12.053] [PMID: 15808658]
[9]
Lawrence, T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb. Perspect. Biol., 2009, 1(6)a001651
[http://dx.doi.org/10.1101/cshperspect.a001651] [PMID: 20457564]
[10]
Grenz, A.; Schenk, M.; Zipfel, A.; Viebahn, R. TNF-alpha and its receptors mediate graft rejection and loss after liver transplantation. Clin. Chem. Lab. Med., 2000, 38(11), 1183-1185.
[http://dx.doi.org/10.1515/CCLM.2000.184] [PMID: 11156356]
[11]
Muriel, P. NF-kappaB in liver diseases: a target for drug therapy. J. Appl. Toxicol., 2009, 29(2), 91-100.
[http://dx.doi.org/10.1002/jat.1393] [PMID: 18937212]
[12]
Thuy Le, T.T.; Hai, N.T.; Hai, H.; Kawada, N. Pathophysiological role of cytoglobin, the fourth globin in mammals, in liver diseases. Histol. Histopathol., 2016, 31(3), 257-267.
[http://dx.doi.org/10.14670/hh-11-694] [PMID: 26554615]
[13]
Ali, F.E.M.; Bakr, A.G.; Abo-Youssef, A.M.; Azouz, A.A.; Hemeida, R.A.M. Targeting Keap-1/Nrf-2 pathway and cytoglobin as a potential protective mechanism of diosmin and pentoxifylline against cholestatic liver cirrhosis. Life Sci., 2018, 207, 50-60.
[http://dx.doi.org/10.1016/j.lfs.2018.05.048] [PMID: 29852187]
[14]
Thi Thanh Hai, N.; Thuy, L.T.T.; Shiota, A.; Kadono, C.; Daikoku, A.; Hoang, D.V.; Dat, N.Q.; Sato-Matsubara, M.; Yoshizato, K.; Kawada, N. Selective overexpression of cytoglobin in stellate cells attenuates thioacetamide-induced liver fibrosis in mice. Sci. Rep., 2018, 8(1), 17860.
[http://dx.doi.org/10.1038/s41598-018-36215-4] [PMID: 30552362]
[15]
Hua, S.; Ma, M.; Fei, X.; Zhang, Y.; Gong, F.; Fang, M. Glycyrrhizin attenuates hepatic ischemia-reperfusion injury by suppressing HMGB1-dependent GSDMD-mediated kupffer cells pyroptosis. Int. Immunopharmacol., 2019, 68, 145-155.
[http://dx.doi.org/10.1016/j.intimp.2019.01.002] [PMID: 30634142]
[16]
Mahmoud, A.M.; Hozayen, W.G.; Hasan, I.H.; Shaban, E.; Bin-Jumah, M. Umbelliferone Ameliorates CCl4-Induced Liver Fibrosis in Rats by Upregulating PPARγ and Attenuating Oxidative Stress, Inflammation, and TGF-β1/Smad3 Signaling. Inflammation, 2019, 42(3), 1103-1116.
[http://dx.doi.org/10.1007/s10753-019-00973-8] [PMID: 30741365]
[17]
Liu, Q.; Zhu, L.; Cheng, C.; Hu, Y.Y.; Feng, Q. Natural Active Compounds from Plant Food and Chinese Herbal Medicine for Nonalcoholic Fatty Liver Disease. Curr. Pharm. Des., 2017, 23(34), 5136-5162.
[http://dx.doi.org/10.2174/1381612823666170918120643] [PMID: 28925892]
[18]
Tamura, S.; Kono, T.; Harada, C.; Yamaguchi, K.; Moriyama, T. Estimation and characterisation of major royal jelly proteins obtained from the honeybee Apis merifera. Food Chem., 2009, 114(4), 1491-1497.
[http://dx.doi.org/10.1016/j.foodchem.2008.11.058]
[19]
Pourmoradian, S.; Mahdavi, R.; Mobasseri, M.; Faramarzi, E.; Mobasseri, M. Effects of royal jelly supplementation on glycemic control and oxidative stress factors in type 2 diabetic female: a randomized clinical trial. Chin. J. Integr. Med., 2014, 20(5), 347-352.
[http://dx.doi.org/10.1007/s11655-014-1804-8] [PMID: 24610413]
[20]
Aslan, Z.; Aksoy, L. Anti-inflammatory effects of royal jelly on ethylene glycol induced renal inflammation in rats. Int. Braz J Urol, 2015, 41(5), 1008-1013.
[http://dx.doi.org/10.1590/S1677-5538.IBJU.2014.0470] [PMID: 26689528]
[21]
Almeer, R.S.; Alarifi, S.; Alkahtani, S.; Ibrahim, S.R.; Ali, D.; Moneim, A. The potential hepatoprotective effect of royal jelly against cadmium chloride-induced hepatotoxicity in mice is mediated by suppression of oxidative stress and upregulation of Nrf2 expression. Biomed Pharmacother., 2018, 106, 1490-1498..
[http://dx.doi.org/10.1016/j.biopha.2018.07.089]
[22]
You, M.M.; Chen, Y.F.; Pan, Y.M.; Liu, Y.C.; Tu, J.; Wang, K.; Hu, F.L. Royal jelly attenuates LPS-induced inflammation in BV-2 microglial cells through modulating NF-κB and p38/JNK signaling pathways. Mediators of inflammation, 2018, 2018
[23]
Salahshoor, M.R.; Jalili, C.; Roshankhah, S. Can royal jelly protect against renal ischemia/reperfusion injury in rats? Chin. J. Physiol., 2019, 62(3), 131-137.
[http://dx.doi.org/10.4103/CJP.CJP_36_19] [PMID: 31249267]
[24]
Mishima, S.; Suzuki, K.M.; Isohama, Y.; Kuratsu, N.; Araki, Y.; Inoue, M.; Miyata, T. Royal jelly has estrogenic effects in vitro and in vivo. J. Ethnopharmacol., 2005, 101(1-3), 215-220.
[http://dx.doi.org/10.1016/j.jep.2005.04.012] [PMID: 15946813]
[25]
Suzuki, K.M.; Isohama, Y.; Maruyama, H.; Yamada, Y.; Narita, Y.; Ohta, S.; Araki, Y.; Miyata, T.; Mishima, S. Estrogenic activities of Fatty acids and a sterol isolated from royal jelly. Evid. Based Complement. Alternat. Med., 2008, 5(3), 295-302.
[http://dx.doi.org/10.1093/ecam/nem036] [PMID: 18830443]
[26]
Narita, Y.; Ohta, S.; Suzuki, K.M.; Nemoto, T.; Abe, K.; Mishima, S. Effects of long-term administration of royal jelly on pituitary weight and gene expression in middle-aged female rats. Biosci. Biotechnol. Biochem., 2009, 73(2), 431-433.
[http://dx.doi.org/10.1271/bbb.80556] [PMID: 19202272]
[27]
Elnagar, S.A. Royal jelly counteracts bucks’ “summer infertility”. Anim. Reprod. Sci., 2010, 121(1-2), 174-180.
[http://dx.doi.org/10.1016/j.anireprosci.2010.05.008] [PMID: 20538419]
[28]
Ali, F.; Abo-Youssef, A.; Messiha, B.; Hemeda, R. Protective effects of quercetin and ursodeoxycholic acid on hepatic ischemiareperfusion injury in rats. Clin. Pharmacol. Biopharm., 2015, 4, 2.
[http://dx.doi.org/10.4172/2167-065X.1000128]
[29]
Zaki, A.M.; El-Tanbouly, D.M.; Abdelsalam, R.M.; Zaki, H.F. Plumbagin ameliorates hepatic ischemia-reperfusion injury in rats: Role of high mobility group box 1 in inflammation, oxidative stress and apoptosis. Biomed. Pharmacother., 2018, 106, 785-793.
[http://dx.doi.org/10.1016/j.biopha.2018.07.004] [PMID: 29990872]
[30]
Cemek, M.; Aymelek, F.; Büyükokuroğlu, M.E.; Karaca, T.; Büyükben, A.; Yilmaz, F. Protective potential of Royal Jelly against carbon tetrachloride induced-toxicity and changes in the serum sialic acid levels. Food Chem. Toxicol., 2010, 48(10), 2827-2832.
[http://dx.doi.org/10.1016/j.fct.2010.07.013] [PMID: 20637822]
[31]
Ahmed, W.M.; Khalaf, A.A.; Moselhy, W.A.; Safwat, G.M. Royal jelly attenuates azathioprine induced toxicity in rats. Environ. Toxicol. Pharmacol., 2014, 37(1), 431-437.
[http://dx.doi.org/10.1016/j.etap.2013.12.010] [PMID: 24444696]
[32]
Reitman, S.; Frankel, S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am. J. Clin. Pathol., 1957, 28(1), 56-63.
[http://dx.doi.org/10.1093/ajcp/28.1.56] [PMID: 13458125]
[33]
Belfield, A.; Goldberg, D.M. Normal ranges and diagnostic value of serum 5'nucleotidase and alkaline phosphatase activities in infancy. Arch. Dis. Child., 1971, 46(250), 842-846.
[http://dx.doi.org/10.1136/adc.46.250.842] [PMID: 5129186]
[34]
Decker, T.; Lohmann-Matthes, M.L. A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Methods, 1988, 115(1), 61-69.
[http://dx.doi.org/10.1016/0022-1759(88)90310-9] [PMID: 3192948]
[35]
Van Weemen, B.K.; Schuurs, A.H. Immunoassay using antigen-enzyme conjugates. FEBS Lett., 1971, 15(3), 232-236.
[http://dx.doi.org/10.1016/0014-5793(71)80319-8] [PMID: 11945853]
[36]
Ellman, G.L. Tissue sulfhydryl groups. Arch. Biochem. Biophys., 1959, 82(1), 70-77.
[http://dx.doi.org/10.1016/0003-9861(59)90090-6] [PMID: 13650640]
[37]
Mihara, M.; Uchiyama, M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem., 1978, 86(1), 271-278.
[http://dx.doi.org/10.1016/0003-2697(78)90342-1] [PMID: 655387]
[38]
Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem., 1974, 47(3), 469-474.
[http://dx.doi.org/10.1111/j.1432-1033.1974.tb03714.x] [PMID: 4215654]
[39]
Keen, J.H.; Habig, W.H.; Jakoby, W.B. Mechanism for the several activities of the glutathione S-transferases. J. Biol. Chem., 1976, 251(20), 6183-6188.
[PMID: 977564]
[40]
Ali, F.E.M.; Azouz, A.A.; Bakr, A.G.; Abo-Youssef, A.M.; Hemeida, R.A.M. Hepatoprotective effects of diosmin and/or sildenafil against cholestatic liver cirrhosis: The role of Keap-1/Nrf-2 and P38-MAPK/NF-κB/iNOS signaling pathway. Food Chem. Toxicol., 2018, 120, 294-304.
[http://dx.doi.org/10.1016/j.fct.2018.07.027] [PMID: 30026087]
[41]
Wang, S.; Abouzied, M.; Smith, D. Proteins as potential endpoint temperature indicators for ground beef patties. J. Food Sci., 1996, 61(1), 5-7.
[http://dx.doi.org/10.1111/j.1365-2621.1996.tb14713.x]
[42]
Towbin, H.; Staehelin, T.; Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA, 1979, 76(9), 4350-4354.
[http://dx.doi.org/10.1073/pnas.76.9.4350] [PMID: 388439]
[43]
Cuello, A.C. Immunohistochemistry II; Wiley Chichester: New York, 1993, Vol. 23
[44]
Bakr, A.G.; El-Bahrawy, A.H.; Taha, H.H.; Ali, F.E.M. Diosmin enhances the anti-angiogenic activity of sildenafil and pentoxifylline against hepatopulmonary syndrome via regulation of TNF-α/VEGF, IGF-1/PI3K/AKT, and FGF-1/ANG-2 signaling pathways. Eur. J. Pharmacol., 2020, 873173008
[http://dx.doi.org/10.1016/j.ejphar.2020.173008] [PMID: 32050083]
[45]
Suvarna, K.S.; Layton, C.; Bancroft, J.D. Bancroft’s Theory and Practice of Histological Techniques E-Book; Elsevier Health Sciences, 2012.
[46]
Nakazato, P.C.G.; Victorino, J.P.; Fina, C.F.; Mendes, K.D.S.; Gomes, M.C.J.; Evora, P.R.B.; D’Albuquerque, L.A.C.; Castro-E-Silva, O. Liver ischemia and reperfusion injury. Pathophysiology and new horizons in preconditioning and therapy. Acta Cir. Bras., 2018, 33(8), 723-735.
[http://dx.doi.org/10.1590/s0102-865020180080000008] [PMID: 30208134]
[47]
Saidi, R.F.; Kenari, S.K. Liver ischemia/reperfusion injury: an overview. J. Invest. Surg., 2014, 27(6), 366-379.
[http://dx.doi.org/10.3109/08941939.2014.932473] [PMID: 25058854]
[48]
Pourmoradian, S.; Mahdavi, R.; Mobasseri, M.; Faramarzi, E.; Mobasseri, M. Effects of royal jelly supplementation on body weight and dietary intake in type 2 diabetic females. Health Promot. Perspect., 2012, 2(2), 231-235.
[http://dx.doi.org/10.5681/hpp.2012.028] [PMID: 24688939]
[49]
Yoneshiro, T.; Kaede, R.; Nagaya, K.; Aoyama, J.; Saito, M.; Okamatsu-Ogura, Y.; Kimura, K.; Terao, A. Royal jelly ameliorates diet-induced obesity and glucose intolerance by promoting brown adipose tissue thermogenesis in mice. Obes. Res. Clin. Pract., 2018, 12(Suppl. 2), 127-137.
[http://dx.doi.org/10.1016/j.orcp.2016.12.006] [PMID: 28089395]
[50]
Mahmoud, M.E.; Elsoadaa, S.S. Protective effect of ascorbic acid, biopropolis and royal jelly against aluminum toxicity in rats. Journal of Natural Sciences Research, 2013, 3(1), 102-112.
[51]
El-Nekeety, A.A.; El-Kholy, W.; Abbas, N.F.; Ebaid, A.; Amra, H.A.; Abdel-Wahhab, M.A. Efficacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon, 2007, 50(2), 256-269.
[http://dx.doi.org/10.1016/j.toxicon.2007.03.017] [PMID: 17490698]
[52]
Giannini, E.G.; Testa, R.; Savarino, V. Liver enzyme alteration: a guide for clinicians. CMAJ, 2005, 172(3), 367-379.
[http://dx.doi.org/10.1503/cmaj.1040752] [PMID: 15684121]
[53]
Ghanbari, E.; Khazaei, M.R.; Khazaei, M.; Nejati, V. Royal Jelly Promotes Ovarian Follicles Growth and Increases Steroid Hormones in Immature Rats. Int. J. Fertil. Steril., 2018, 11(4), 263-269.
[http://dx.doi.org/10.22074/ijfs.2018.5156] [PMID: 29043701]
[54]
Konishi, T.; Lentsch, A.B. Hepatic Ischemia/Reperfusion: Mechanisms of Tissue Injury, Repair, and Regeneration. Gene Expr., 2017, 17(4), 277-287.
[http://dx.doi.org/10.3727/105221617X15042750874156] [PMID: 28893351]
[55]
Gasbarrini, A.; Borle, A.B.; Farghali, H.; Bender, C.; Francavilla, A.; Van Thiel, D. Effect of anoxia on intracellular ATP, Na+i, Ca2+i, Mg2+i, and cytotoxicity in rat hepatocytes. J. Biol. Chem., 1992, 267(10), 6654-6663.
[PMID: 1637381]
[56]
Guan, L.Y.; Fu, P.Y.; Li, P.D.; Li, Z.N.; Liu, H.Y.; Xin, M.G.; Li, W. Mechanisms of hepatic ischemia-reperfusion injury and protective effects of nitric oxide. World J. Gastrointest. Surg., 2014, 6(7), 122-128.
[http://dx.doi.org/10.4240/wjgs.v6.i7.122] [PMID: 25068009]
[57]
Xu, D.; Xu, M.; Jeong, S.; Qian, Y.; Wu, H.; Xia, Q.; Kong, X. The Role of Nrf2 in Liver Disease: Novel Molecular Mechanisms and Therapeutic Approaches. Front. Pharmacol., 2019, 9, 1428.
[http://dx.doi.org/10.3389/fphar.2018.01428] [PMID: 30670963]
[58]
Kaspar, J.W.; Niture, S.K.; Jaiswal, A.K. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic. Biol. Med., 2009, 47(9), 1304-1309.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.07.035] [PMID: 19666107]
[59]
Abdel-Gaber, S.A.; Geddawy, A.; Moussa, R.A. The hepatoprotective effect of sitagliptin against hepatic ischemia reperfusion-induced injury in rats involves Nrf-2/HO-1 pathway. Pharmacol. Rep., 2019, 71(6), 1044-1049.
[http://dx.doi.org/10.1016/j.pharep.2019.06.006] [PMID: 31600635]
[60]
Zhou, Y.; Zhang, J.; Lei, B.; Liang, W.; Gong, J.; Zhao, C.; Yu, J.; Li, X.; Tang, B.; Yuan, S. DADLE improves hepatic ischemia/reperfusion injury in mice via activation of the Nrf2/HO‑1 pathway. Mol. Med. Rep., 2017, 16(5), 6214-6221.
[http://dx.doi.org/10.3892/mmr.2017.7393] [PMID: 28901476]
[61]
Joe, Y.; Zheng, M.; Kim, H.J.; Uddin, M.J.; Kim, S.K.; Chen, Y.; Park, J.; Cho, G.J.; Ryter, S.W.; Chung, H.T. Cilostazol attenuates murine hepatic ischemia and reperfusion injury via heme oxygenase-dependent activation of mitochondrial biogenesis. Am. J. Physiol. Gastrointest. Liver Physiol., 2015, 309(1), G21-G29.
[http://dx.doi.org/10.1152/ajpgi.00307.2014] [PMID: 25951827]
[62]
Rak, M.; Bénit, P.; Chrétien, D.; Bouchereau, J.; Schiff, M.; El-Khoury, R.; Tzagoloff, A.; Rustin, P. Mitochondrial cytochrome c oxidase deficiency. Clin. Sci. (Lond.), 2016, 130(6), 393-407.
[http://dx.doi.org/10.1042/CS20150707] [PMID: 26846578]
[63]
El-Desoky, A.E.; Delpy, D.T.; Davidson, B.R.; Seifalian, A.M. Assessment of hepatic ischaemia reperfusion injury by measuring intracellular tissue oxygenation using near infrared spectroscopy. Liver, 2001, 21(1), 37-44.
[http://dx.doi.org/10.1034/j.1600-0676.2001.210106.x] [PMID: 11169071]
[64]
Sato, N. Central role of mitochondria in metabolic regulation of liver pathophysiology. J. Gastroenterol. Hepatol., 2007, 22(Suppl. 1), S1-S6.
[http://dx.doi.org/10.1111/j.1440-1746.2007.04963.x] [PMID: 17567455]
[65]
Sheth, H.; Hafez, T.; Glantzounis, G.K.; Seifalian, A.M.; Fuller, B.; Davidson, B.R. Glycine maintains mitochondrial activity and bile composition following warm liver ischemia-reperfusion injury. J. Gastroenterol. Hepatol., 2011, 26(1), 194-200.
[http://dx.doi.org/10.1111/j.1440-1746.2010.06323.x] [PMID: 21175814]
[66]
Kanoria, S.; Glantzounis, G.; Quaglia, A.; Dinesh, S.; Fusai, G.; Davidson, B.R.; Seifalian, A.M. Remote preconditioning improves hepatic oxygenation after ischaemia reperfusion injury. Transpl. Int., 2012, 25(7), 783-791.
[http://dx.doi.org/10.1111/j.1432-2277.2012.01481.x] [PMID: 22533545]
[67]
Schmidt, M.; Gerlach, F.; Avivi, A.; Laufs, T.; Wystub, S.; Simpson, J.C.; Nevo, E.; Saaler-Reinhardt, S.; Reuss, S.; Hankeln, T.; Burmester, T. Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia. J. Biol. Chem., 2004, 279(9), 8063-8069.
[http://dx.doi.org/10.1074/jbc.M310540200] [PMID: 14660570]
[68]
Zhang, J; Pei, Y; Yang, W; Yang, W; Chen, B; Zhao, X; Long, S Cytoglobin ameliorates the stemness of hepatocellular carcinoma via coupling oxidative-nitrosative stress signals., 2019, 58(3), 334-343..
[http://dx.doi.org/10.1002/mc.22931]
[69]
Thuy, T.T.; Van Thuy, T.T.; Matsumoto, Y.; Hai, H.; Ikura, Y.; Yoshizato, K.; Kawada, N. Absence of cytoglobin promotes multiple organ abnormalities in aged mice. Sci. Rep., 2016, 6, 24990.
[http://dx.doi.org/10.1038/srep24990] [PMID: 27146058]
[70]
Walsh, K.B.; Toledo, A.H.; Rivera-Chavez, F.A.; Lopez-Neblina, F.; Toledo-Pereyra, L.H. Inflammatory mediators of liver ischemia-reperfusion injury. Exp. Clin. Transplant., 2009, 7(2), 78-93.
[PMID: 19715511]
[71]
Chen, Y-F; Wang, K; Zhang, Y-Z; Zheng, Y-F; Hu, F-L In vitro anti-inflammatory effects of three fatty acids from royal jelly. Mediators of inflammation, 2016, 2016

Rights & Permissions Print Cite
Article Metrics
29
© 2024 Bentham Science Publishers | Privacy Policy