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Current Pharmaceutical Biotechnology

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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

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Research Article

Liuwei Dihuang Decoction Drug-containing Serum Attenuates Transforming Growth Factor-β1-induced Epithelial-mesenchymal Transition in HK-2 Cells by Inhibiting NF-κB/Snail Signaling Pathway

Author(s): Jiajun Pan, Yichen Jiang, Yuanyuan Huang, Haiying Zhang, Xi Wang, Chao Luo, Hui Wang, Miao Tang, Gang Pei and Qun Tang*

Volume 24, Issue 12, 2023

Published on: 20 March, 2023

Page: [1589 - 1602] Pages: 14

DOI: 10.2174/1389201024666230228100718

Price: $65

Abstract

Objectives: The nuclear factor-κB (NF-κB) signaling pathway plays an important role in regulating tubular epithelial-mesenchymal transition (EMT), an indispensable cellular programme for driving organ fibrosis and tumor progression. Liuwei Dihuang Decoction (LWD) is an effective Chinese formula for treating chronic renal failure.

Methods: First, by using morphological examination, immunofluorescence staining assay, RTqPCR, and Western blot analysis, in vitro experiments were designed to analyze NF-κB and EMT markers (including Snail, α-SMA, and E-cadherin) in transforming growth factor-β1 (TGF-β1) induced renal tubular epithelial cells (HK-2) and to detect the expression levels of LWD-CS cotreatment. Then, the recombinant lentiviral vector was overexpressed and knocked down by NF- κB and transfected into HK-2 cells. Cells were treated with TGF-β1 (10 ng/ml) with blank serum or LWD-containing serum, respectively, and the expression of these molecules in the NF-κB/Snail signaling pathway was further evaluated.

Results: Our results confirmed that TGF-β1 could induce EMT, nuclear translocation of NF-κB p65, and activate the NF-κB/Snail signaling pathway in HK-2 cells.

Furthermore, NF-κB knocked-down dramatically increases the TGF-β1-induced mRNA and protein expression level of E-cadherin and reduces the level of Snail and α-SMA; this is reversed by NF-κB overexpression. LWD can decrease the EMT levels through the NF-κB/Snail signaling activation in TGF-β1-induced EMT of HK-2 cells.

Conclusion: The present study provides evidence suggesting a novel mechanism that LWD exerts anti-fibrosis effects through inhibiting activation of the NF-κB/Snail signaling pathway and consequently downregulating the TGF-β1-induced EMT in renal tubular epithelial cells.

Keywords: Tubulointerstitial fibrosis, epithelial mesenchymal transition, NF-κB p65, snail, TGF-β1, Liuwei dihuang decoction drug-containing serum.

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[1]
Bikbov, B.; Purcell, C.A.; Levey, A.S.; Smith, M.; Abdoli, A.; Abebe, M.; Adebayo, O.M.; Afarideh, M.; Agarwal, S.K.; Agudelo-Botero, M.; Ahmadian, E.; Al-Aly, Z.; Alipour, V.; Almasi-Hashiani, A.; Al-Raddadi, R.M.; Alvis-Guzman, N.; Amini, S.; Andrei, T.; Andrei, C.L.; Andualem, Z.; Anjomshoa, M.; Arabloo, J.; Ashagre, A.F.; Asmelash, D.; Ataro, Z.; Atout, M.M.W.; Ayanore, M.A.; Badawi, A.; Bakhtiari, A.; Ballew, S.H.; Balouchi, A.; Banach, M.; Barquera, S.; Basu, S.; Bayih, M.T.; Bedi, N.; Bello, A.K.; Bensenor, I.M.; Bijani, A.; Boloor, A.; Borzì, A.M.; Cámera, L.A.; Carrero, J.J.; Carvalho, F.; Castro, F.; Catalá-López, F.; Chang, A.R.; Chin, K.L.; Chung, S-C.; Cirillo, M.; Cousin, E.; Dandona, L.; Dandona, R.; Daryani, A.; Das Gupta, R.; Demeke, F.M.; Demoz, G.T.; Desta, D.M.; Do, H.P.; Duncan, B.B.; Eftekhari, A.; Esteghamati, A.; Fatima, S.S.; Fernandes, J.C.; Fernandes, E.; Fischer, F.; Freitas, M.; Gad, M.M.; Gebremeskel, G.G.; Gebresillassie, B.M.; Geta, B.; Ghafourifard, M.; Ghajar, A.; Ghith, N.; Gill, P.S.; Ginawi, I.A.; Gupta, R.; Hafezi-Nejad, N.; Haj-Mirzaian, A.; Haj-Mirzaian, A.; Hariyani, N.; Hasan, M.; Hasankhani, M.; Hasanzadeh, A.; Hassen, H.Y.; Hay, S.I.; Heidari, B.; Herteliu, C.; Hoang, C.L.; Hosseini, M.; Hostiuc, M.; Irvani, S.S.N.; Islam, S.M.S.; Jafari Balalami, N.; James, S.L.; Jassal, S.K.; Jha, V.; Jonas, J.B.; Joukar, F.; Jozwiak, J.J.; Kabir, A.; Kahsay, A.; Kasaeian, A.; Kassa, T.D.; Kassaye, H.G.; Khader, Y.S.; Khalilov, R.; Khan, E.A.; Khan, M.S.; Khang, Y-H.; Kisa, A.; Kovesdy, C.P.; Kuate Defo, B.; Kumar, G.A; Larsson, A.O; Lim, L-L; Lopez , A.D; Lotufo , P.A; Majeed, A; Malekzadeh, R; März, W; Masaka, A; Meheretu, H.A.A; Miazgowski, T; Mirica, A; Mirrakhimov, E.M; Mithra, P; Moazen, B; Mohammad, D.K; Mohammadpourhodki, R; Mohammed, S; Mokdad, A.H; Morales, L; Moreno Velasquez, I; Mousavi, S.M; Mukhopadhyay, S; Nachega, J.B; Nadkarni, G.N; Nansseu, J.R; Natarajan, G; Nazari, J; Neal, B; Negoi , R.I; Nguyen , C.T; Nikbakhsh, R; Noubiap , J.J; Nowak, C; Olagunju , A.T; Ortiz, A; Owolabi , M.O; Palladino, R; Pathak, M; Poustchi, H; Prakash, S; Prasad, N; Rafiei, A; Raju , S.B; Ramezanzadeh, K; Rawaf, S; Rawaf , D.L; Rawal, L; Reiner, R.C. Jr;; Rezapour, A; Ribeiro , D.C; Roever, L; Rothenbacher, D; Rwegerera , G.M; Saadatagah, S; Safari, S; Sahle , B.W; Salem, H; Sanabria, J; Santos , I.S; Sarveazad, A; Sawhney, M; Schaeffner, E; Schmidt , M.I; Schutte , A.E; Sepanlou , S.G; Shaikh , M.A; Sharafi, Z; Sharif, M; Sharifi, A; Silva D., A.S; Singh , J.A; Singh , N.P; Sisay M., M.M; Soheili, A; Sutradhar, I; Teklehaimanot , B.F; Tesfay, B; Teshome , G.F; Thakur , J.S; Tonelli, M; Tran , K.B; Tran , B.X; Tran Ngoc, C; Ullah, I; Valdez , P.R; Varughese, S; Vos, T; Vu , L.G; Waheed, Y; Werdecker, A; Wolde , H.F; Wondmieneh , A.B; Wulf Hanson, S; Yamada, T; Yeshaw, Y; Yonemoto, N; Yusefzadeh, H; Zaidi, Z; Zaki, L; Zaman , S.B; Zamora, N; Zarghi, A; Zewdie , K.A; Ärnlöv, J; Coresh, J; Perico, N; Remuzzi, G; Murray , C.J.L; Vos, T. Global, regional, and national burden of chronic kidney disease, 1990-2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet, 2020, 395(10225), 709-733.
[http://dx.doi.org/10.1016/S0140-6736(20)30045-3] [PMID: 32061315]
[2]
Hallan, S.I.; Øvrehus, M.A.; Romundstad, S.; Rifkin, D.; Langhammer, A.; Stevens, P.E.; Ix, J.H. Long-term trends in the prevalence of chronic kidney disease and the influence of cardiovascular risk factors in Norway. Kidney Int., 2016, 90(3), 665-673.
[http://dx.doi.org/10.1016/j.kint.2016.04.012] [PMID: 27344204]
[3]
Szeto, H.H. Pharmacologic approaches to improve mitochondrial function in AKI and CKD. J. Am. Soc. Nephrol., 2017, 28(10), 2856-2865.
[http://dx.doi.org/10.1681/ASN.2017030247] [PMID: 28778860]
[4]
Liu, Y. Cellular and molecular mechanisms of renal fibrosis. Nat. Rev. Nephrol., 2011, 7(12), 684-696.
[http://dx.doi.org/10.1038/nrneph.2011.149] [PMID: 22009250]
[5]
Liu, B.C.; Tang, T.T.; Lv, L.L.; Lan, H.Y. Renal tubule injury: A driving force toward chronic kidney disease. Kidney Int., 2018, 93(3), 568-579.
[http://dx.doi.org/10.1016/j.kint.2017.09.033] [PMID: 29361307]
[6]
Grande, M.T.; Sánchez-Laorden, B.; López-Blau, C.; De Frutos, C.A.; Boutet, A.; Arévalo, M.; Rowe, R.G.; Weiss, S.J.; López-Novoa, J.M.; Nieto, M.A. Snail1-induced partial epithelial-to-mesenchymal transition drives renal fibrosis in mice and can be targeted to reverse established disease. Nat. Med., 2015, 21(9), 989-997.
[http://dx.doi.org/10.1038/nm.3901] [PMID: 26236989]
[7]
Kalluri, R.; Neilson, E.G. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest., 2003, 112(12), 1776-1784.
[http://dx.doi.org/10.1172/JCI200320530] [PMID: 14679171]
[8]
Siar, C.H.; Ng, K.H. Epithelial-to-mesenchymal transition in ameloblastoma: Focus on morphologically evident mesenchymal phenotypic transition. Pathology, 2019, 51(5), 494-501.
[http://dx.doi.org/10.1016/j.pathol.2019.04.004] [PMID: 31262562]
[9]
Boor, P.; Ostendorf, T.; Floege, J. Renal fibrosis: Novel insights into mechanisms and therapeutic targets. Nat. Rev. Nephrol., 2010, 6(11), 643-656.
[http://dx.doi.org/10.1038/nrneph.2010.120] [PMID: 20838416]
[10]
Meng, X.; Nikolic-Paterson, D.J.; Lan, H.Y. TGF-β The master regulator of fibrosis. Nat. Rev. Nephrol., 2016, 12(6), 325-338.
[http://dx.doi.org/10.1038/nrneph.2016.48] [PMID: 27108839]
[11]
Inoue, T.; Takenaka, T.; Hayashi, M.; Monkawa, T.; Yoshino, J.; Shimoda, K.; Neilson, E.G.; Suzuki, H.; Okada, H. Fibroblast expression of an IκB dominant-negative transgene attenuates renal fibrosis. J. Am. Soc. Nephrol., 2010, 21(12), 2047-2052.
[http://dx.doi.org/10.1681/ASN.2010010003] [PMID: 20847140]
[12]
Wu, Y.; Deng, J.; Rychahou, P.G.; Qiu, S.; Evers, B.M.; Zhou, B.P. Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion. Cancer Cell, 2009, 15(5), 416-428.
[http://dx.doi.org/10.1016/j.ccr.2009.03.016] [PMID: 19411070]
[13]
Veerasamy, M.; Nguyen, T.Q.; Motazed, R.; Pearson, A.L.; Goldschmeding, R.; Dockrell, M.E.C. Differential regulation of E-cadherin and α-smooth muscle actin by BMP 7 in human renal proximal tubule epithelial cells and its implication in renal fibrosis. Am. J. Physiol. Renal Physiol., 2009, 297(5), F1238-F1248.
[http://dx.doi.org/10.1152/ajprenal.90539.2008] [PMID: 19741012]
[14]
Xia, J.; He, L.; Su, X. Interventional mechanisms of herbs or herbal extracts on renal interstitial fibrosis. J. Integr. Med., 2016, 14(3), 165-173.
[http://dx.doi.org/10.1016/S2095-4964(16)60256-X] [PMID: 27181123]
[15]
Xiang, L.; Jiang, P.; Zhou, L.; Sun, X.; Bi, J.; Cui, L.; Nie, X.; Luo, R.; Zhao, X.; Liu, Y. Additive effect of Qidan Dihuang Grain, a Traditional Chinese Medicine, and angiotensin receptor blockers on albuminuria levels in patients with diabetic nephropathy: A randomized, parallel-controlled trial. Evid. Based Complement. Alternat. Med., 2016, 2016, 1-8.
[http://dx.doi.org/10.1155/2016/1064924] [PMID: 27375762]
[16]
Gao, X.; Shang, J.; Liu, H.; Yu, B. A meta-analysis of the clinical efficacy of TCM decoctions made from formulas in the Liuwei Dihuang Wan categorized formulas in treating diabetic nephropathy proteinuria. Evid. Based Complement. Alternat. Med., 2018, 2018, 1-10.
[http://dx.doi.org/10.1155/2018/2427301] [PMID: 30356440]
[17]
Liu, Y.; Zhao, H.; Zhang, J.; Zhang, P.; Li, M.; Qi, F.; Wang, Y.; Kou, S.; Zheng, Q.; Wang, L. The regulatory effect of Liuwei Dihuang pills on cytokines in mice with experimental autoimmune encephalomyelitis. Am. J. Chin. Med., 2012, 40(2), 295-308.
[http://dx.doi.org/10.1142/S0192415X12500231] [PMID: 22419424]
[18]
Zhuang, S.; Jian, Y.M.; Sun, Y.N. Inhibition of N-methyl-N-nitrosourea-induced gastric tumorigenesis by Liuwei Dihuang Pill in db/db mice. World J. Gastroenterol., 2017, 23(23), 4233-4242.
[http://dx.doi.org/10.3748/wjg.v23.i23.4233] [PMID: 28694663]
[19]
Perry, B.; Zhang, J.; Saleh, T.; Wang, Y. Liuwei Dihuang, a traditional Chinese herbal formula, suppresses chronic inflammation and oxidative stress in obese rats. J. Integr. Med., 2014, 12(5), 447-454.
[http://dx.doi.org/10.1016/S2095-4964(14)60044-3] [PMID: 25292344]
[20]
Tang, Q.; Wu, H.; Zhang, X.; Liu, C.Y.; Dong, X.; Wang, X. Effects of Liuwei dihuang decoction on expressions of ZO-1, N-cadherin and vimentin in renal tissue of rats with chronic renal failure. Chinese J. Inform. TCM., 2020, 27(12), 32-37.
[21]
Yan, G.L.; Sun, H.; Zhang, A.H.; Han, Y.; Wang, P.; Wu, X.H.; Meng, X.C.; Wang, X.J. Progress of serum pharmacochemistry of traditional Chinese medicine and further development of its theory and method. Zhongguo Zhongyao Zazhi, 2015, 40(17), 3406-3412.
[PMID: 26978981]
[22]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[23]
Prunotto, M.; Budd, D.C.; Gabbiani, G.; Meier, M.; Formentini, I.; Hartmann, G.; Pomposiello, S.; Moll, S. Epithelial-mesenchymal crosstalk alteration in kidney fibrosis. J. Pathol., 2012, 228(2), 131-147.
[http://dx.doi.org/10.1002/path.4049] [PMID: 22570261]
[24]
Zeisberg, M.; Kalluri, R. Cellular mechanisms of tissue fibrosis. 1. Common and organ-specific mechanisms associated with tissue fibrosis. Am. J. Physiol. Cell Physiol., 2013, 304(3), C216-C225.
[http://dx.doi.org/10.1152/ajpcell.00328.2012] [PMID: 23255577]
[25]
Wang, H.W.; Shi, L.; Xu, Y.P.; Qin, X.Y.; Wang, Q.Z. Hesperetin alleviates renal interstitial fibrosis by inhibiting tubular epithelial-mesenchymal transition in vivo and in vitro. Exp. Ther. Med., 2017, 14(4), 3713-3719.
[http://dx.doi.org/10.3892/etm.2017.4968] [PMID: 29042968]
[26]
Yamaguchi, Y.; Iwano, M.; Suzuki, D.; Nakatani, K.; Kimura, K.; Harada, K.; Kubo, A.; Akai, Y.; Toyoda, M.; Kanauchi, M.; Neilson, E.G.; Saito, Y. Epithelial-mesenchymal transition as a potential explanation for podocyte depletion in diabetic nephropathy. Am. J. Kidney Dis., 2009, 54(4), 653-664.
[http://dx.doi.org/10.1053/j.ajkd.2009.05.009] [PMID: 19615802]
[27]
Farris, A.B.; Colvin, R.B. Renal interstitial fibrosis. Curr. Opin. Nephrol. Hypertens., 2012, 21(3), 289-300.
[http://dx.doi.org/10.1097/MNH.0b013e3283521cfa] [PMID: 22449945]
[28]
Lamouille, S.; Xu, J.; Derynck, R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol., 2014, 15(3), 178-196.
[http://dx.doi.org/10.1038/nrm3758] [PMID: 24556840]
[29]
Lovisa, S.; LeBleu, V.S.; Tampe, B.; Sugimoto, H.; Vadnagara, K.; Carstens, J.L.; Wu, C.C.; Hagos, Y.; Burckhardt, B.C.; Pentcheva-Hoang, T.; Nischal, H.; Allison, J.P.; Zeisberg, M.; Kalluri, R. Epithelial-to-mesenchymal transition induces cell cycle arrest and parenchymal damage in renal fibrosis. Nat. Med., 2015, 21(9), 998-1009.
[http://dx.doi.org/10.1038/nm.3902] [PMID: 26236991]
[30]
Jin, H.; Wang, Y.; Wang, D.; Zhang, L. Effects of qingshen granules on the oxidative stress-NF/kB signal pathway in unilateral ureteral obstruction rats. Evid. Based Complement. Alternat. Med., 2018, 2018, 1-9.
[http://dx.doi.org/10.1155/2018/4761925] [PMID: 29576795]
[31]
Liu, Y. Epithelial to mesenchymal transition in renal fibrogenesis: Pathologic significance, molecular mechanism, and therapeutic intervention. J. Am. Soc. Nephrol., 2004, 15(1), 1-12.
[http://dx.doi.org/10.1097/01.ASN.0000106015.29070.E7] [PMID: 14694152]
[32]
Oba, S.; Kumano, S.; Suzuki, E.; Nishimatsu, H.; Takahashi, M.; Takamori, H.; Kasuya, M.; Ogawa, Y.; Sato, K.; Kimura, K.; Homma, Y.; Hirata, Y.; Fujita, T. miR-200b precursor can ameliorate renal tubulointerstitial fibrosis. PLoS One, 2010, 5(10)e13614
[http://dx.doi.org/10.1371/journal.pone.0013614] [PMID: 21049046]
[33]
Hu, H.H.; Chen, D.Q.; Wang, Y.N.; Feng, Y.L.; Cao, G.; Vaziri, N.D.; Zhao, Y.Y. New insights into TGF-β/Smad signaling in tissue fibrosis. Chem. Biol. Interact., 2018, 292, 76-83.
[http://dx.doi.org/10.1016/j.cbi.2018.07.008] [PMID: 30017632]
[34]
Huang, S.; Susztak, K. Epithelial plasticity versus EMT in kidney fibrosis. Trends Mol. Med., 2016, 22(1), 4-6.
[http://dx.doi.org/10.1016/j.molmed.2015.11.009] [PMID: 26700490]
[35]
Sutariya, B.; Jhonsa, D.; Saraf, M.N. TGF-β The connecting link between nephropathy and fibrosis. Immunopharmacol. Immunotoxicol., 2016, 38(1), 39-49.
[http://dx.doi.org/10.3109/08923973.2015.1127382] [PMID: 26849902]
[36]
Julien, S.; Puig, I.; Caretti, E.; Bonaventure, J.; Nelles, L.; van Roy, F.; Dargemont, C.; de Herreros, A.G.; Bellacosa, A.; Larue, L. Activation of NF-κB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene, 2007, 26(53), 7445-7456.
[http://dx.doi.org/10.1038/sj.onc.1210546] [PMID: 17563753]
[37]
Barberà, M.J.; Puig, I.; Domínguez, D.; Julien-Grille, S.; Guaita-Esteruelas, S.; Peiró, S.; Baulida, J.; Francí, C.; Dedhar, S.; Larue, L.; García de Herreros, A. Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells. Oncogene, 2004, 23(44), 7345-7354.
[http://dx.doi.org/10.1038/sj.onc.1207990] [PMID: 15286702]
[38]
Huber, M.A. Azoitei, N.; Baumann, B.; Grünert, S.; Sommer, A.; Pehamberger, H.; Kraut, N.; Beug, H.; Wirth, T. NF-κB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J. Clin. Invest., 2004, 114(4), 569-581.
[http://dx.doi.org/10.1172/JCI200421358] [PMID: 15314694]
[39]
Yang, H.; Liao, D.; Tong, L.; Zhong, L.; Wu, K. MiR-373 exacerbates renal injury and fibrosis via NF-κB/Matrix metalloproteinase-9 signaling by targeting Sirtuin1. Genomics, 2019, 111(4), 786-792.
[http://dx.doi.org/10.1016/j.ygeno.2018.04.017] [PMID: 29723660]
[40]
Salminen, A.; Kaarniranta, K. NF-kappaB signaling in the aging process. J. Clin. Immunol., 2009, 29(4), 397-405.
[http://dx.doi.org/10.1007/s10875-009-9296-6] [PMID: 19408108]
[41]
Liu, J.H.; He, L.; Zou, Z.M.; Ding, Z.C.; Zhang, X.; Wang, H.; Zhou, P.; Xie, L.; Xing, S.; Yi, C.Z. A novel inhibitor of homodimerization targeting MyD88 ameliorates renal interstitial fibrosis by counteracting TGF-β1-induced EMT in vivo and in vitro. Kidney Blood Press. Res., 2018, 43(5), 1677-1687.
[http://dx.doi.org/10.1159/000494745] [PMID: 30380557]
[42]
Tang, R.; Xiao, X.; Lu, Y.; Li, H.; Zhou, Q.; Kwadwo Nuro-Gyina, P.; Li, X. Interleukin-22 attenuates renal tubular cells inflammation and fibrosis induced by TGF-β1 through Notch1 signaling pathway. Ren. Fail., 2020, 42(1), 381-390.
[http://dx.doi.org/10.1080/0886022X.2020.1753538] [PMID: 32338120]
[43]
Song, Y.; Lv, S.; Wang, F.; Liu, X.; Cheng, J.; Liu, S.; Wang, X.; Chen, W.; Guan, G.; Liu, G.; Peng, C. Overexpression of BMP-7 reverses TGF β1 induced epithelial mesenchymal transition by attenuating the Wnt3/β catenin and TGF-β1/Smad2/3 signaling pathways in HK-2 cells. Mol. Med. Rep., 2020, 21(2), 833-841.
[PMID: 31974602]
[44]
Huang, L.; Zhang, F.; Tang, Y.; Qin, J.; Peng, Y.; Wu, L.; Wang, F.; Yuan, Q.; Peng, Z.; Liu, J.; Meng, J.; Tao, L. Fluorofenidone attenuates inflammation by inhibiting the NF-кB pathway. Am. J. Med. Sci., 2014, 348(1), 75-80.
[http://dx.doi.org/10.1097/MAJ.0000000000000187] [PMID: 24534785]
[45]
Gambhir, S.; Vyas, D.; Hollis, M.; Aekka, A.; Vyas, A. Nuclear factor kappa B role in inflammation associated gastrointestinal malignancies. World J. Gastroenterol., 2015, 21(11), 3174-3183.
[http://dx.doi.org/10.3748/wjg.v21.i11.3174] [PMID: 25805923]
[46]
Chung, K.W.; Jeong, H.O.; Lee, B.; Park, D.; Kim, D.H.; Choi, Y.J.; Lee, E.K.; Kim, K.M.; Park, J.W.; Yu, B.P.; Chung, H.Y. Involvement of NF-κBIZ and related cytokines in age-associated renal fibrosis. Oncotarget, 2017, 8(5), 7315-7327.
[http://dx.doi.org/10.18632/oncotarget.14614] [PMID: 28099916]
[47]
Zhang, M.; Guo, Y.; Fu, H.; Hu, S.; Pan, J.; Wang, Y.; Cheng, J.; Song, J.; Yu, Q.; Zhang, S.; Xu, J-F.; Pei, G.; Xiang, X.; Yang, P.; Wang, C-Y. Chop deficiency prevents UUO-induced renal fibrosis by attenuating fibrotic signals originated from Hmgb1/TLR4/NFκB/IL-1β signaling. Cell Death Dis., 2015, 6(8)e1847
[http://dx.doi.org/10.1038/cddis.2015.206] [PMID: 26247732]
[48]
Cichon, M.A.; Radisky, D.C. ROS-induced epithelial-mesenchymal transition in mammary epithelial cells is mediated by NF-κB-dependent activation of Snail. Oncotarget, 2014, 5(9), 2827-2838.
[http://dx.doi.org/10.18632/oncotarget.1940] [PMID: 24811539]
[49]
Bloom, M.J.; Saksena, S.D.; Swain, G.P.; Behar, M.S.; Yankeelov, T.E.; Sorace, A.G. The effects of IKK-beta inhibition on early NF-kappa-B activation and transcription of downstream genes. Cell. Signal., 2019, 55, 17-25.
[http://dx.doi.org/10.1016/j.cellsig.2018.12.004] [PMID: 30543861]
[50]
Zhu, L.F.; Hu, Y.; Yang, C.C.; Xu, X.H.; Ning, T.Y.; Wang, Z.L.; Ye, J.H.; Liu, L.K. Snail overexpression induces an epithelial to mesenchymal transition and cancer stem cell-like properties in SCC9 cells. Lab. Invest., 2012, 92(5), 744-752.
[http://dx.doi.org/10.1038/labinvest.2012.8] [PMID: 22349639]
[51]
Herranz, N.; Pasini, D.; Díaz, V.M.; Francí, C.; Gutierrez, A.; Dave, N.; Escrivà, M.; Hernandez-Muñoz, I.; Di Croce, L.; Helin, K.; García de Herreros, A.; Peiró, S. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol. Cell. Biol., 2008, 28(15), 4772-4781.
[http://dx.doi.org/10.1128/MCB.00323-08] [PMID: 18519590]
[52]
Wu, Y.; Zhou, B.P. TNF-α/NF-κB/Snail pathway in cancer cell migration and invasion. Br. J. Cancer, 2010, 102(4), 639-644.
[http://dx.doi.org/10.1038/sj.bjc.6605530] [PMID: 20087353]
[53]
Brzozowa, M.; Michalski, M.; Wyrobiec, G.; Piecuch, A.; Dittfeld, A.; Harabin-Słowińska, M.; Boroń, D.; Wojnicz, R. The role of Snail1 transcription factor in colorectal cancer progression and metastasis. Contemp. Oncol., 2015, 4(4), 265-270.
[http://dx.doi.org/10.5114/wo.2014.42173] [PMID: 26557772]
[54]
Hu, Z.; Liu, X.; Tang, Z.; Zhou, Y.; Qiao, L. Possible regulatory role of Snail in NF-κB-mediated changes in E-cadherin in gastric cancer. Oncol. Rep., 2013, 29(3), 993-1000.
[http://dx.doi.org/10.3892/or.2012.2200] [PMID: 23254865]
[55]
El-Dawla, N.M.Q.; Sallam, A.A.M.; El-Hefnawy, M.H.; El-Mesallamy, H.O. E-cadherin and periostin in early detection and progression of diabetic nephropathy: Epithelial-to-mesenchymal transition. Clin. Exp. Nephrol., 2019, 23(8), 1050-1057.
[http://dx.doi.org/10.1007/s10157-019-01744-3] [PMID: 31104272]
[56]
Wang, S.; Yan, Y.; Cheng, Z.; Hu, Y.; Liu, T. Sotetsuflavone suppresses invasion and metastasis in non-small-cell lung cancer A549 cells by reversing EMT via the TNF-α/NF-κB and PI3K/AKT signaling pathway. Cell Death Discov., 2018, 4(1), 26.
[http://dx.doi.org/10.1038/s41420-018-0026-9] [PMID: 29531823]
[57]
Zhuang, W.; Li, Z.; Dong, X.; Zhao, N.; Liu, Y.; Wang, C.; Chen, J. Schisandrin B inhibits TGF-β1-induced epithelial-mesenchymal transition in human A549 cells through epigenetic silencing of ZEB1. Exp. Lung Res., 2019, 45(5-6), 157-166.
[http://dx.doi.org/10.1080/01902148.2019.1631906] [PMID: 31268360]
[58]
Song, S.; Qiu, D.; Luo, F.; Wei, J.; Wu, M.; Wu, H.; Du, C.; Du, Y.; Ren, Y.; Chen, N.; Duan, H.; Shi, Y. Knockdown of NLRP3 alleviates high glucose or TGFB1-induced EMT in human renal tubular cells. J. Mol. Endocrinol., 2018, 61(3), 101-113.
[http://dx.doi.org/10.1530/JME-18-0069] [PMID: 30307163]
[59]
Lee, Y.J.; Park, J.H.; Oh, S.M. Activation of NF-κB by TOPK upregulates Snail/Slug expression in TGF-β1 signaling to induce epithelial-mesenchymal transition and invasion of breast cancer cells. Biochem. Biophys. Res. Commun., 2020, 530(1), 122-129.
[http://dx.doi.org/10.1016/j.bbrc.2020.07.015] [PMID: 32828273]
[60]
Feng, H.; Lu, J.J.; Wang, Y.; Pei, L.; Chen, X. Osthole inhibited TGF β-induced epithelial-mesenchymal transition (EMT) by suppressing NF-κB mediated Snail activation in lung cancer A549 cells. Cell Adhes. Migr., 2017, 11(5-6), 464-475.
[http://dx.doi.org/10.1080/19336918.2016.1259058] [PMID: 28146373]
[61]
Tong, J.; Shen, Y.; Zhang, Z.; Hu, Y.; Zhang, X.; Han, L. Apigenin inhibits epithelial-mesenchymal transition of human colon cancer cells through NF-κB/Snail signaling pathway. Biosci. Rep., 2019, 39(5)BSR20190452
[http://dx.doi.org/10.1042/BSR20190452] [PMID: 30967496]
[62]
Feng, M.; Feng, J.; Chen, W.; Wang, W.; Wu, X.; Zhang, J.; Xu, F.; Lai, M. Lipocalin2 suppresses metastasis of colorectal cancer by attenuating NF-κB-dependent activation of snail and epithelial mesenchymal transition. Mol. Cancer, 2016, 15(1), 77.
[http://dx.doi.org/10.1186/s12943-016-0564-9] [PMID: 27912767]
[63]
Zhang, G.D.; Li, Y.; Liao, G.J.; Qiu, H.W. LncRNA NKILA inhibits invasion and migration of osteosarcoma cells via NF-κB/Snail signaling pathway. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(10), 4118-4125.
[PMID: 31173281]
[64]
Yuan, Y.; Li, S.L.; Cao, Y.L.; Li, J.J.; Wang, Q.P. LKB1 suppresses glioma cell invasion via NF-κB/Snail signaling repression. OncoTargets Ther., 2019, 12, 2451-2463.
[http://dx.doi.org/10.2147/OTT.S193736] [PMID: 31040689]
[65]
Zhang, X.L.; Chen, M.L.; Zhou, S.L. Fentanyl increases colorectal carcinoma cell apoptosis by inhibition of NF-κB in a Sirt1-dependent manner. APJCP, 2014, 15(22), 10015-10020.
[PMID: 25520062]
[66]
Basak, S.; Behar, M.; Hoffmann, A. Lessons from mathematically modeling the NF-κB pathway. Immunol. Rev., 2012, 246(1), 221-238.
[http://dx.doi.org/10.1111/j.1600-065X.2011.01092.x] [PMID: 22435558]
[67]
Hai, L.; Liu, P.; Yu, S.; Yi, L.; Tao, Z.; Zhang, C. Jagged1 is clinically prognostic and promotes invasion of glioma-initiating cells by activating NF-κB(p65) signaling. Cell. Physiol. Biochem., 2018, 51(6), 2925-2937.
[68]
Wang, S.; Yang, Z.; Xiong, F.; Chen, C.; Chao, X.; Huang, J.; Huang, H. Betulinic acid ameliorates experimental diabetic-induced renal inflammation and fibrosis via inhibiting the activation of NF-κB signaling pathway. Mol. Cell. Endocrinol., 2016, 434, 135-143.
[http://dx.doi.org/10.1016/j.mce.2016.06.019] [PMID: 27364889]
[69]
Xie, X.; Peng, J.; Chang, X.; Huang, K.; Huang, J.; Wang, S.; Shen, X.; Liu, P.; Huang, H. Activation of RhoA/ROCK regulates NF-κB signaling pathway in experimental diabetic nephropathy. Mol. Cell. Endocrinol., 2013, 369(1-2), 86-97.
[http://dx.doi.org/10.1016/j.mce.2013.01.007] [PMID: 23376009]
[70]
Du, C.; Yi, X.; Liu, W.; Han, T.; Liu, Z.; Ding, Z.; Zheng, Z.; Piao, Y.; Yuan, J.; Han, Y.; Xie, M.; Xie, X. MTDH mediates trastuzumab resistance in HER2 positive breast cancer by decreasing PTEN expression through an NFκB-dependent pathway. BMC Cancer, 2014, 14(1), 869.
[http://dx.doi.org/10.1186/1471-2407-14-869] [PMID: 25417825]
[71]
Shen, Y.L.; Wang, S.J.; Rahman, K.; Zhang, L.J.; Zhang, H. Chinese herbal formulas and renal fibrosis: An overview. Curr. Pharm. Des., 2018, 24(24), 2774-2781.
[http://dx.doi.org/10.2174/1381612824666180829103355] [PMID: 30156149]
[72]
Sun, X.; Liu, Y.; Li, C.; Wang, X.; Zhu, R.; Liu, C.; Liu, H.; Wang, L.; Ma, R.; Fu, M.; Zhang, D.; Li, Y. Recent advances of curcumin in the prevention and treatment of renal fibrosis. BioMed Res. Int., 2017, 2017, 1-9.
[http://dx.doi.org/10.1155/2017/2418671] [PMID: 28546962]
[73]
Jiang, M.; Yang, J.; Zhang, C.; Liu, B.; Chan, K.; Cao, H.; Lu, A. Clinical studies with traditional Chinese medicine in the past decade and future research and development. Planta Med., 2010, 76(17), 2048-2064.
[http://dx.doi.org/10.1055/s-0030-1250456] [PMID: 20979016]
[74]
Wang, J.; Yao, K.; Yang, X.; Liu, W.; Feng, B.; Ma, J. Chinese patent medicine liu wei di huang wan combined with antihypertensive drugs, a new integrative medicine therapy, for the treatment of essential hypertension: A systematic review of randomized controlled trials. Evid Based Complement Alternat Med., 2012, 2012, 714805.
[75]
Xu, Z.J.; Shu, S.; Li, Z.J.; Liu, Y.M.; Zhang, R.Y.; Zhang, Y. Liuwei Dihuang pill treats diabetic nephropathy in rats by inhibiting of TGF-β/SMADS, MAPK, and NF-kB and upregulating expression of cytoglobin in renal tissues. Medicine, 2017, 96(3)e5879
[http://dx.doi.org/10.1097/MD.0000000000005879] [PMID: 28099346]

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