Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

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

Betaine Modulating MIF-Mediated Oxidative Stress, Inflammation and Fibrogenesis in Thioacetamide-Induced Nephrotoxicity

Author(s): Bojan Jorgačević, Sanja Stanković, Jelena Filipović, Janko Samardžić, Danijela Vučević and Tatjana Radosavljević*

Volume 29, Issue 31, 2022

Published on: 23 May, 2022

Page: [5254 - 5267] Pages: 14

DOI: 10.2174/0929867329666220408102856

Price: $65

Abstract

Background: Macrophage migration inhibitory factor (MIF) is a proinflammatory cytokine with chemokine properties released by various immune and non-immune cells. It contributes to the pathogenesis of many inflammatory, autoimmune diseases and malignant tumors.

Objective: Our study aimed to investigate the role of betaine in the modulation of MIF-mediated oxidative stress, inflammation, and fibrogenesis during toxic kidney damage induced by thioacetamide (TAA).

Methods: The experiment is performed on wild-type and knockout MIF-/- C57BL/6 mice. They are randomly divided into groups: Control; Bet-group, received betaine (2% wt/v dissolved in drinking water); MIF-/- mice group; MIF-/- + Bet; TAA-group, treated with TAA (200 mg/kg b.w.), intraperitoneally, 3x/week/8 weeks); TAA+Bet; MIF-/-+TAA, and MIF-/- + TAA+Bet group. After eight weeks of treatment, animals are sacrificed and kidney samples are taken to determine oxidative stress parameters, proinflammatory cytokines, profibrogenic factors, and histopathology of renal tissue.

Results: In MIF-/-mice, TAA decreases malondialdehyde (MDA) concentration, IL-6, tumor necrosis factor-alpha (TNF-α), transforming growth factor-beta 1 (TGF-β1) and platelet-derived growth factor-BB (PDGF-BB) and increases superoxide dismutases (SOD) and catalase (CAT) activities, as well as glutathione (GSH) content in kidneys, compared to TAA group. Betaine alleviates the mechanism of MIF-mediated effects in TAA-induced nephrotoxicity, reducing MDA, IL-6, TNF-α, TGF-β1, and PDGF-BB, and increasing SOD and CAT activity, as well as GSH levels.

Conclusion: MIF mediates TAA-induced nephrotoxicity by increasing oxidative stress, inflammation, and profibrogenic mediators. MIF-targeted therapy could potentially alleviate oxidative stress and inflammation in the kidney, as well as pathohistological changes in renal tissue, but the exact mechanism of its action is not completely clear. Betaine alleviates MIF nephrotoxic effects by increasing the antioxidative capacity of kidney cells, and decreasing lipid peroxidation and cytokine production in the renal tissue. It suggests that betaine can be used for the prevention of kidney damage.

Keywords: Thioacetamide, macrophage migration inhibitory factor, kidney damage, oxidative stress, inflammation, fibrosis, betaine mice.

« Previous Next »
[1]
Allen, J.H. The wicked problem of chemicals policy: Opportunities for innovation. J. Environ. Stud. Sci., 2013, 3(2), 101-108.
[http://dx.doi.org/10.1007/s13412-013-0117-0]
[2]
Shaikh Omar, A.M.; Shaikh, O. The potential protective influence of flaxseed oil against renal toxicity induced by thioacetamide in rats. Saudi J. Biol. Sci., 2018, 25(8), 1696-1702.
[http://dx.doi.org/10.1016/j.sjbs.2016.09.021] [PMID: 30591787]
[3]
Al-Attar, A.M.; Alrobai, A.A.; Almalki, D.A. Protective effect of olive and juniper leaves extracts on nephrotoxicity induced by thio-acetamide in male mice. Saudi J. Biol. Sci., 2017, 24(1), 15-22.
[http://dx.doi.org/10.1016/j.sjbs.2015.08.013] [PMID: 28053566]
[4]
Keshk, W.A.; Zahran, S.M. Mechanistic role of cAMP and hepatocyte growth factor signaling in thioacetamide-induced nephrotoxicity: Unraveling the role of platelet rich plasma. Biomed. Pharmacother., 2019, 109, 1078-1084.
[http://dx.doi.org/10.1016/j.biopha.2018.10.121] [PMID: 30551358]
[5]
Hong, W.; Zhang, G.; Lu, H.; Guo, Y.; Zheng, S.; Zhu, H.; Xiao, Y.; Papa, A.P.D.; Wu, C.; Sun, L.; Chen, B.; Bai, Y. Epithelial and interstitial Notch1 activity contributes to the myofibroblastic phenotype and fibrosis. Cell Commun. Signal., 2019, 17(1), 145.
[http://dx.doi.org/10.1186/s12964-019-0455-y] [PMID: 31718671]
[6]
Rasmussen, D.G.K.; Boesby, L.; Nielsen, S.H.; Tepel, M.; Birot, S.; Karsdal, M.A.; Kamper, A.L.; Genovese, F. Collagen turnover profiles in chronic kidney disease. Sci. Rep., 2019, 9(1), 16062.
[http://dx.doi.org/10.1038/s41598-019-51905-3] [PMID: 31690732]
[7]
Schyman, P.; Printz, R.L.; Estes, S.K.; Boyd, K.L.; Shiota, M.; Wallqvist, A. Identification of the toxicity pathways associated with thio-acetamide-induced injuries in rat liver and kidney. Front. Pharmacol., 2018, 9, 1272.
[http://dx.doi.org/10.3389/fphar.2018.01272] [PMID: 30459623]
[8]
National Toxicology Program. Thioacetamide. Rep. Carcinog., 2011, 12, 403-404.
[PMID: 21863105]
[9]
Pellegrino, D.; La Russa, D.; Marrone, A. Oxidative imbalance and kidney damage: New study perspectives from animal models to hospitalized patients. Antioxidants, 2019, 8(12), 1-11.
[http://dx.doi.org/10.3390/antiox8120594] [PMID: 31795160]
[10]
Tomsa, A.M.; Alexa, A.L.; Junie, M.L.; Rachisan, A.L.; Ciumarnean, L. Oxidative stress as a potential target in acute kidney injury. PeerJ, 2019, 7, e8046.
[http://dx.doi.org/10.7717/peerj.8046] [PMID: 31741796]
[11]
Ruiz, S.; Pergola, P.E.; Zager, R.A.; Vaziri, N.D. Targeting the transcription factor Nrf2 to ameliorate oxidative stress and inflammation in chronic kidney disease. Kidney Int., 2013, 83(6), 1029-1041.
[http://dx.doi.org/10.1038/ki.2012.439] [PMID: 23325084]
[12]
Lee, Y.H.; Son, J.Y.; Kim, K.S.; Park, Y.J.; Kim, H.R.; Park, J.H.; Kim, K.B.; Lee, K.Y.; Kang, K.W.; Kim, I.S.; Kacew, S.; Lee, B.M.; Kim, H.S. Estrogen deficiency potentiates thioacetamide-induced hepatic fibrosis in sprague-dawley rats. Int. J. Mol. Sci., 2019, 20(15), 1-16.
[http://dx.doi.org/10.3390/ijms20153709] [PMID: 31362375]
[13]
Su, L.J.; Zhang, J.H.; Gomez, H.; Murugan, R.; Hong, X.; Xu, D.; Jiang, F.; Peng, Z.Y. Reactive oxygen species-induced lipid peroxi-dation in apoptosis, autophagy and ferroptosis. Oxid. Med. Cell. Longev., 2019, 2019, 5080843.
[http://dx.doi.org/10.1155/2019/5080843] [PMID: 31737171]
[14]
Wynn, T.A.; Vannella, K.M. Macrophages in tissue repair, regeneration, and fibrosis. Immunity, 2016, 44(3), 450-462.
[http://dx.doi.org/10.1016/j.immuni.2016.02.015] [PMID: 26982353]
[15]
Isaka, Y. Targeting TGF-β signaling in kidney fibrosis. Int. J. Mol. Sci., 2018, 19(9), 1-13.
[http://dx.doi.org/10.3390/ijms19092532] [PMID: 30150520]
[16]
Leaf, I.A.; Duffield, J.S. What can target kidney fibrosis? Nephrol. Dial. Transplant., 2017, 32(Suppl. 1), i89-i97.
[http://dx.doi.org/10.1093/ndt/gfw388] [PMID: 28391346]
[17]
Sinitski, D.; Gruner, K.; Brandhofer, M.; Kontos, C.; Winkler, P.; Reinstädler, A.; Bourilhon, P.; Xiao, Z.; Cool, R.; Kapurniotu, A.; Dekker, F.J.; Panstruga, R.; Bernhagen, J. Cross-kingdom mimicry of the receptor signaling and leukocyte recruitment activity of a hu-man cytokine by its plant orthologs. J. Biol. Chem., 2020, 295(3), 850-867.
[http://dx.doi.org/10.1016/S0021-9258(17)49940-6] [PMID: 31811089]
[18]
Grieb, G. Macrophage migration inhibitory factor (MIF) and its receptors – interactions and suitability as biomarkers. Mini Rev. Med. Chem., 2014, 14(14), 1115.
[http://dx.doi.org/10.2174/138955751414150216102436] [PMID: 25692463]
[19]
Boor, P. MIF in kidney diseases: A story of Dr. Jekyll and Mr. Hyde. Pathologe, 2019, 40(S1), 25-30.
[http://dx.doi.org/10.1007/s00292-018-0548-1] [PMID: 30569239]
[20]
Djudjaj, S.; Martin, I.V.; Buhl, E.M.; Nothofer, N.J.; Leng, L.; Piecychna, M.; Floege, J.; Bernhagen, J.; Bucala, R.; Boor, P. Macro-phage migration inhibitory factor limits renal inflammation and fibrosis by counteracting tubular cell cycle arrest. J. Am. Soc. Nephrol., 2017, 28(12), 3590-3604.
[http://dx.doi.org/10.1681/ASN.2017020190] [PMID: 28801314]
[21]
Day, C.R.; Kempson, S.A. Betaine chemistry, roles, and potential use in liver disease. Biochim. Biophys. Acta, 2016, 1860(6), 1098-1106.
[http://dx.doi.org/10.1016/j.bbagen.2016.02.001] [PMID: 26850693]
[22]
Ejaz, A.; Martinez-Guino, L.; Goldfine, A.B.; Ribas-Aulinas, F.; De Nigris, V.; Ribó, S.; Gonzalez-Franquesa, A.; Garcia-Roves, P.M.; Li, E.; Dreyfuss, J.M.; Gall, W.; Kim, J.K.; Bottiglieri, T.; Villarroya, F.; Gerszten, R.E.; Patti, M.E.; Lerin, C. Dietary betaine supple-mentation increases Fgf21 levels to improve glucose homeostasis and reduce hepatic lipid accumulation in mice. Diabetes, 2016, 65(4), 902-912.
[http://dx.doi.org/10.2337/db15-1094] [PMID: 26858359]
[23]
Yang, W.; Huang, L.; Gao, J.; Wen, S.; Tai, Y.; Chen, M.; Huang, Z.; Liu, R.; Tang, C.; Li, J. Betaine attenuates chronic alco-hol induced fatty liver by broadly regulating hepatic lipid metabolism. Mol. Med. Rep., 2017, 16(4), 5225-5234.
[http://dx.doi.org/10.3892/mmr.2017.7295] [PMID: 28849079]
[24]
Du, J.; Shen, L.; Tan, Z.; Zhang, P.; Zhao, X.; Xu, Y.; Gan, M.; Yang, Q.; Ma, J.; Jiang, A.; Tang, G.; Jiang, Y.; Jin, L.; Li, M.; Bai, L.; Li, X.; Wang, J.; Zhang, S.; Zhu, L. Betaine supplementation enhances lipid metabolism and improves insulin resistance in mice fed a high-fat diet. Nutrients, 2018, 10(2), 131-145.
[http://dx.doi.org/10.3390/nu10020131] [PMID: 29373534]
[25]
Lowry, O.H.; Rosebrough, N.J.; Farr, A.L.; Randall, R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193(1), 265-275.
[http://dx.doi.org/10.1016/S0021-9258(19)52451-6] [PMID: 14907713]
[26]
Girotti, M.J.; Khan, N.; McLellan, B.A. Early measurement of systemic lipid peroxidation products in the plasma of major blunt trauma patients. J. Trauma, 1991, 31(1), 32-35.
[http://dx.doi.org/10.1097/00005373-199101000-00007] [PMID: 1846013]
[27]
Sun, M.; Zigman, S. An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation. Anal. Biochem., 1978, 90(1), 81-89.
[http://dx.doi.org/10.1016/0003-2697(78)90010-6] [PMID: 727489]
[28]
Beers, R.F., Jr; Sizer, I.W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem., 1952, 195(1), 133-140.
[http://dx.doi.org/10.1016/S0021-9258(19)50881-X] [PMID: 14938361]
[29]
Anderson, M.E. Tissue glutathione. In: The DTNB-GSSG reductase recycling assay for total glutathione (GSH+1/2GSSG); Greenwald, R.A., Ed.; CRC Press: Boca Raton, FL, 1986, pp. 317-323.
[30]
Ghosh, S.; Sarkar, A.; Bhattacharyya, S.; Sil, P.C. Silymarin protects mouse liver and kidney from thioacetamide induced toxicity by scavenging reactive oxygen species and activating PI3K-Akt pathway. Front. Pharmacol., 2016, 7, 481.
[http://dx.doi.org/10.3389/fphar.2016.00481] [PMID: 28018219]
[31]
Zargar, S.; Alonazi, M.; Rizwana, H.; Wani, T.A. Resveratrol reverses thioacetamide-induced renal assault with respect to oxidative stress, renal function, DNA damage, and cytokine release in Wistar rats. Oxid. Med. Cell. Longev., 2019, 2019, 1702959.
[http://dx.doi.org/10.1155/2019/1702959] [PMID: 31583036]
[32]
Yogalakshmi, B.; Viswanathan, P.; Anuradha, C.V. Investigation of antioxidant, anti-inflammatory and DNA-protective properties of eugenol in thioacetamide-induced liver injury in rats. Toxicology, 2010, 268(3), 204-212.
[http://dx.doi.org/10.1016/j.tox.2009.12.018] [PMID: 20036707]
[33]
Begum, Q.; Noori, S.; Mahboob, T. Antioxidant effect of sodium selenite on thioacetamide-induced renal toxicity. Pakistan J. Biochem. Mol. Biol., 2011, 44, 21-26.
[34]
Iacobini, C.; Menini, S.; Ricci, C.; Scipioni, A.; Sansoni, V.; Cordone, S.; Taurino, M.; Serino, M.; Marano, G.; Federici, M.; Pricci, F.; Pugliese, G. Accelerated lipid-induced atherogenesis in galectin-3-deficient mice: Role of lipoxidation via receptor-mediated mechanisms. Arterioscler. Thromb. Vasc. Biol., 2009, 29(6), 831-836.
[http://dx.doi.org/10.1161/ATVBAHA.109.186791] [PMID: 19359660]
[35]
Ozbek, E. Induction of oxidative stress in kidney. Int. J. Nephrol., 2012, 2012, 465897.
[http://dx.doi.org/10.1155/2012/465897] [PMID: 22577546]
[36]
Ganesan, B.; Anandan, R.; Lakshmanan, P.T. Studies on the protective effects of betaine against oxidative damage during experimentally induced restraint stress in Wistar albino rats. Cell Stress Chaperones, 2011, 16(6), 641-652.
[http://dx.doi.org/10.1007/s12192-011-0276-4] [PMID: 21717086]
[37]
Zhang, M.; Zhang, H.; Li, H.; Lai, F.; Li, X.; Tang, Y.; Min, T.; Wu, H. Antioxidant mechanism of betaine without free radical scaveng-ing ability. J. Agric. Food Chem., 2016, 64(42), 7921-7930.
[http://dx.doi.org/10.1021/acs.jafc.6b03592] [PMID: 27677203]
[38]
Bashandy, S.A.E.; Ebaid, H.; Abdelmottaleb Moussa, S.A.; Alhazza, I.M.; Hassan, I.; Alaamer, A.; Al Tamimi, J. Potential effects of the combination of nicotinamide, vitamin B2 and vitamin C on oxidative-mediated hepatotoxicity induced by thioacetamide. Lipids Health Dis., 2018, 17(1), 29.
[http://dx.doi.org/10.1186/s12944-018-0674-z] [PMID: 29444683]
[39]
Hajovsky, H.; Hu, G.; Koen, Y.; Sarma, D.; Cui, W.; Moore, D.S.; Staudinger, J.L.; Hanzlik, R.P. Metabolism and toxicity of thio-acetamide and thioacetamide S-oxide in rat hepatocytes. Chem. Res. Toxicol., 2012, 25(9), 1955-1963.
[http://dx.doi.org/10.1021/tx3002719] [PMID: 22867114]
[40]
Rolo, A.P.; Teodoro, J.S.; Palmeira, C.M. Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic. Biol. Med., 2012, 52(1), 59-69.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.10.003] [PMID: 22064361]
[41]
Kanbak, G.; Akyüz, F.; Inal, M. Preventive effect of betaine on ethanol-induced membrane lipid composition and membrane ATPases. Arch. Toxicol., 2001, 75(1), 59-61.
[http://dx.doi.org/10.1007/s002040000179] [PMID: 11357522]
[42]
Jung, Y.S.; Kim, S.J.; Kwon, D.Y.; Ahn, C.W.; Kim, Y.S.; Choi, D.W.; Kim, Y.C. Alleviation of alcoholic liver injury by betaine in-volves an enhancement of antioxidant defense via regulation of sulfur amino acid metabolism. Food Chem. Toxicol., 2013, 62, 292-298.
[http://dx.doi.org/10.1016/j.fct.2013.08.049] [PMID: 23994088]
[43]
Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.D.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological func-tions and human disease. Int. J. Biochem. Cell Biol., 2007, 39(1), 44-84.
[http://dx.doi.org/10.1016/j.biocel.2006.07.001] [PMID: 16978905]
[44]
Ruze, A.; Chen, B.D.; Liu, F.; Chen, X.C.; Gai, M.T.; Li, X.M.; Ma, Y.T.; Du, X.J.; Yang, Y.N.; Gao, X.M. Macrophage migration inhibitory factor plays an essential role in ischemic preconditioning-mediated cardioprotection. Clin. Sci. (Lond.), 2019, 133(5), 665-680.
[http://dx.doi.org/10.1042/CS20181013] [PMID: 30804219]
[45]
Zhao, G.; He, F.; Wu, C.; Li, P.; Li, N.; Deng, J.; Zhu, G.; Ren, W.; Peng, Y. Betaine in inflammation: Mechanistic aspects and applica-tions. Front. Immunol., 2018, 9, 1070.
[http://dx.doi.org/10.3389/fimmu.2018.01070] [PMID: 29881379]
[46]
Kim, S.K.; Kim, Y.C. Effects of betaine supplementation on hepatic metabolism of sulfur-containing amino acids in mice. J. Hepatol., 2005, 42(6), 907-913.
[http://dx.doi.org/10.1016/j.jhep.2005.01.017] [PMID: 15885362]
[47]
Okada, T.; Kawakami, S.; Nakamura, Y.; Han, K.H.; Ohba, K.; Aritsuka, T.; Uchino, H.; Shimada, K.; Sekikawa, M.; Ishii, H.; Fuku-shima, M. Amelioration of D-galactosamine-induced acute liver injury in rats by dietary supplementation with betaine derived from sugar beet molasses. Biosci. Biotechnol. Biochem., 2011, 75(7), 1335-1341.
[http://dx.doi.org/10.1271/bbb.110105] [PMID: 21737928]
[48]
Yeung, J.H.K.; Or, P.M. Effects of polysaccharide peptides from COV-1 strain of Coriolus versicolor on glutathione and glutathione-related enzymes in the mouse. Food Chem. Toxicol., 2007, 45(6), 953-961.
[http://dx.doi.org/10.1016/j.fct.2006.12.005] [PMID: 17240508]
[49]
Go, E.K.; Jung, K.J.; Kim, J.M.; Lim, H.; Lim, H.K.; Yu, B.P.; Chung, H.Y. Betaine modulates age-related NF-kappaB by thiol-enhancing action. Biol. Pharm. Bull., 2007, 30(12), 2244-2249.
[http://dx.doi.org/10.1248/bpb.30.2244] [PMID: 18057706]
[50]
Zeisel, S. Choline, other methyl-donors and epigenetics. Nutrients, 2017, 9(5), 1-10.
[http://dx.doi.org/10.3390/nu9050445] [PMID: 28468239]
[51]
Thiele, M.; Bernhagen, J. Link between macrophage migration inhibitory factor and cellular redox regulation. Antioxid. Redox Signal., 2005, 7(9-10), 1234-1248.
[http://dx.doi.org/10.1089/ars.2005.7.1234] [PMID: 16115028]
[52]
Li, J.; Tang, Y.; Tang, P.M.K.; Lv, J.; Huang, X.R.; Carlsson-Skwirut, C.; Da Costa, L.; Aspesi, A.; Fröhlich, S. Szczęśniak, P.; Lach-er, P.; Klug, J.; Meinhardt, A.; Fingerle-Rowson, G.; Gong, R.; Zheng, Z.; Xu, A.; Lan, H.Y. Blocking macrophage migration inhibitory factor protects against cisplatin-induced acute kidney injury in mice. Mol. Ther., 2018, 26(10), 2523-2532.
[http://dx.doi.org/10.1016/j.ymthe.2018.07.014] [PMID: 30077612]
[53]
Hong, M.Y.; Tseng, C.C.; Chuang, C.C.; Chen, C.L.; Lin, S.H.; Lin, C.F. Urinary macrophage migration inhibitory factor serves as a potential biomarker for acute kidney injury in patients with acute pyelonephritis. Mediators Inflamm., 2012, 2012, 381358.
[http://dx.doi.org/10.1155/2012/381358] [PMID: 23319831]
[54]
Chen, L.; Zhou, X.; Fan, L.X.; Yao, Y.; Swenson-Fields, K.I.; Gadjeva, M.; Wallace, D.P.; Peters, D.J.M.; Yu, A.; Grantham, J.J.; Li, X. Macrophage migration inhibitory factor promotes cyst growth in polycystic kidney disease. J. Clin. Invest., 2015, 125(6), 2399-2412.
[http://dx.doi.org/10.1172/JCI80467] [PMID: 25961459]
[55]
Li, J.H.; Tang, Y.; Lv, J.; Wang, X.H.; Yang, H.; Tang, P.M.K.; Huang, X.R.; He, Z.J.; Zhou, Z.J.; Huang, Q.Y.; Klug, J.; Meinhardt, A.; Fingerle-Rowson, G.; Xu, A.P.; Zheng, Z.H.; Lan, H.Y. Macrophage migration inhibitory factor promotes renal injury induced by ischemic reperfusion. J. Cell. Mol. Med., 2019, 23(6), 3867-3877.
[http://dx.doi.org/10.1111/jcmm.14234] [PMID: 30968541]
[56]
Stefaniak, J.; Schiefer, J.; Miller, E.J.; Krenn, C.G.; Baron, D.M.; Faybik, P. Macrophage migration inhibitory factor as a potential pre-dictor for requirement of renal replacement therapy after orthotopic liver transplantation. Liver Transpl., 2015, 21(5), 662-669.
[http://dx.doi.org/10.1002/lt.24103] [PMID: 25762421]
[57]
Pohl, J.; Papathanasiou, M.; Heisler, M.; Stock, P.; Kelm, M.; Hendgen-Cotta, U.B.; Rassaf, T.; Luedike, P. Renal replacement therapy neutralizes elevated MIF levels in septic shock. J. Intensive Care, 2016, 4(1), 39.
[http://dx.doi.org/10.1186/s40560-016-0163-2] [PMID: 27313864]
[58]
Wang, Z.; Wei, M.; Wang, M.; Chen, L.; Liu, H.; Ren, Y.; Shi, K.; Jiang, H. Inhibition of macrophage migration inhibitory factor reduc-es diabetic nephropathy in type II diabetes mice. Inflammation, 2014, 37(6), 2020-2029.
[http://dx.doi.org/10.1007/s10753-014-9934-x] [PMID: 24958012]
[59]
Merk, M.; Baugh, J.; Zierow, S.; Leng, L.; Pal, U.; Lee, S.J.; Ebert, A.D.; Mizue, Y.; Trent, J.O.; Mitchell, R.; Nickel, W.; Kavathas, P.B.; Bernhagen, J.; Bucala, R. The Golgi-associated protein p115 mediates the secretion of macrophage migration inhibitory factor. J. Immunol., 2009, 182(11), 6896-6906.
[http://dx.doi.org/10.4049/jimmunol.0803710] [PMID: 19454686]
[60]
Ping, Z.; Peng, Y.; Lang, H.; Xinyong, C.; Zhiyi, Z.; Xiaocheng, W.; Hong, Z.; Liang, S. Oxidative stress in radiation-induced cardio-toxicity. Oxid. Med. Cell. Longev., 2020, 2020, 3579143.
[http://dx.doi.org/10.1155/2020/3579143] [PMID: 32190171]
[61]
Djudjaj, S.; Lue, H.; Rong, S.; Papasotiriou, M.; Klinkhammer, B.M.; Zok, S.; Klaener, O.; Braun, G.S.; Lindenmeyer, M.T.; Cohen, C.D.; Bucala, R.; Tittel, A.P.; Kurts, C.; Moeller, M.J.; Floege, J.; Ostendorf, T.; Bernhagen, J.; Boor, P. Macrophage migration inhibi-tory factor mediates proliferative GN via CD74. J. Am. Soc. Nephrol., 2016, 27(6), 1650-1664.
[http://dx.doi.org/10.1681/ASN.2015020149] [PMID: 26453615]
[62]
Go, E.K.; Jung, K.J.; Kim, J.Y.; Yu, B.P.; Chung, H.Y. Betaine suppresses proinflammatory signaling during aging: The involvement of nuclear factor-kappaB via nuclear factor-inducing kinase/IkappaB kinase and mitogen-activated protein kinases. J. Gerontol. A Biol. Sci. Med. Sci., 2005, 60(10), 1252-1264.
[http://dx.doi.org/10.1093/gerona/60.10.1252] [PMID: 16282556]
[63]
Lee, E.K.; Jang, E.J.; Jung, K.J.; Kim, D.H.; Yu, B.P.; Chung, H.Y. Betaine attenuates lysophosphatidylcholine-mediated adhesion mol-ecules in aged rat aorta: Modulation of the nuclear factor-κB pathway. Exp. Gerontol., 2013, 48(5), 517-524.
[http://dx.doi.org/10.1016/j.exger.2013.02.024] [PMID: 23466300]
[64]
Poulsen, K.L.; McMullen, M.R.; Huang, E.; Kibler, C.D.; Sheehan, M.M.; Leng, L.; Bucala, R.; Nagy, L.E. Novel role of macrophage migration inhibitory factor in upstream control of the unfolded protein response after ethanol feeding in mice. Alcohol. Clin. Exp. Res., 2019, 43(7), 1439-1451.
[http://dx.doi.org/10.1111/acer.14065] [PMID: 31009094]
[65]
Poulsen, K.L.; Mcmullen, M.; Sheehan, M.; Leng, L.; Bucala, R.; Nagy, L. Protection from Gao-Binge induced liver injury in MIF-/- mice is associated with decreased ER stress. J. Hepatol., 2018, 68, S47-S48.
[http://dx.doi.org/10.1016/S0168-8278(18)30313-1]
[66]
Kim, M.J.; Kim, W.S.; Kim, D.O.; Byun, J.E.; Huy, H.; Lee, S.Y.; Song, H.Y.; Park, Y.J.; Kim, T.D.; Yoon, S.R.; Choi, E.J.; Ha, H.; Jung, H.; Choi, I. Macrophage migration inhibitory factor interacts with thioredoxin-interacting protein and induces NF-κB activity. Cell. Signal., 2017, 34, 110-120.
[http://dx.doi.org/10.1016/j.cellsig.2017.03.007] [PMID: 28323005]
[67]
Shin, M.S.; Kang, Y.; Wahl, E.R.; Park, H.J.; Lazova, R.; Leng, L.; Mamula, M.; Krishnaswamy, S.; Bucala, R.; Kang, I. Macrophage migration inhibitory factor regulates U1 small nuclear RNP immune complex-mediated activation of the NLRP3 inflammasome. Arthritis Rheumatol., 2019, 71(1), 109-120.
[http://dx.doi.org/10.1002/art.40672] [PMID: 30009530]
[68]
Günther, S.; Bordenave, J.; Hua-Huy, T.; Nicco, C.; Cumont, A.; Thuillet, R.; Tu, L.; Quatremarre, T.; Guilbert, T.; Jalce, G.; Batteux, F.; Humbert, M.; Savale, L.; Guignabert, C.; Dinh-Xuan, A.T. Macrophage migration inhibitory factor (MIF) inhibition in a murine model of bleomycin-induced pulmonary fibrosis. Int. J. Mol. Sci., 2018, 19(12), 4105.
[http://dx.doi.org/10.3390/ijms19124105] [PMID: 30567353]
[69]
Marin, V.; Poulsen, K.; Odena, G.; McMullen, M.R.; Altamirano, J.; Sancho-Bru, P.; Tiribelli, C.; Caballeria, J.; Rosso, N.; Bataller, R.; Nagy, L.E. Hepatocyte-derived macrophage migration inhibitory factor mediates alcohol-induced liver injury in mice and patients. J. Hepatol., 2017, 67(5), 1018-1025.
[http://dx.doi.org/10.1016/j.jhep.2017.06.014] [PMID: 28647568]
[70]
Tsai, M.T.; Chen, C.Y.; Pan, Y.H.; Wang, S.H.; Mersmann, H.J.; Ding, S.T. Alleviation of carbon-tetrachloride-induced liver injury and fibrosis by betaine supplementation in chickens. Evid. Based Complement. Alternat. Med., 2015, 2015, 725379.
[http://dx.doi.org/10.1155/2015/725379]
[71]
Bingül, İ.; Aydın, A.F.; Başaran-Küçükgergin, C.; Doğan-Ekici, I.; Çoban, J.; Doğru-Abbasoğlu, S.; Uysal, M. Highfat diet plus carbon tetrachloride-induced liver fibrosis is alleviated by betaine treatment in rats.. Int. Immunopharmacol., 2016, 39, 199-207.
[http://dx.doi.org/10.1016/j.intimp.2016.07.028] [PMID: 27494683]

Rights & Permissions Print Cite
Article Metrics
32
1
© 2024 Bentham Science Publishers | Privacy Policy