RIP kinase-mediated ROS production triggers XAF1 expression through activation of TAp73 in casticin-treated bladder cancer cells

Chung,Yoon  Hee; Kim,Daejin

doi:10.3892/or.2016.4895

RIP kinase-mediated ROS production triggers XAF1 expression through activation of TAp73 in casticin-treated bladder cancer cells

Authors:
- Yoon Hee Chung
- Daejin Kim
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Affiliations: Department of Anatomy, Chung-Ang University College of Medicine, Seoul 06974, Republic of Korea, Department of Anatomy, Inje University College of Medicine, Busan 47392, Republic of Korea
Published online on: June 22, 2016 https://doi.org/10.3892/or.2016.4895
Pages: 1135-1142

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Abstract

The p53 family protein p73 plays an important role in apoptosis induced by chemotherapeutic drugs. Transcriptionally active (TA) p73 (TAp73) substitutes for p53 in the response to stress. XIAP associated factor 1 (XAF1) is a novel predictive and prognostic factor in patients with bladder cancer, but the association between TAp73 and XAF1 expression in bladder cancer cells is poorly understood. Here, we investigated the status of TAp73 and XAF1 in T24 bladder cancer cells to identify molecular mechanisms in casticin‑exposed T24 cells. Casticin induced activation of JNK/p38 MAPK that preceded activation of the caspase cascade and disruption of the mitochondria membrane potential (∆ψm). Expression of XAF1 and TAp73 was also upregulated in casticin-treated T24 cells. Casticin treatment of T24 cells induced receptor-interacting protein (RIP) kinase expression and increased intracellular production of reactive oxygen species (ROS). Casticin-mediated ROS induced an increase in phosphorylated JNK/p38 MAPK, resulting in progressive upregulation of TAp73, which in turn led to XAF1 expression. Our data suggest that the apoptotic activity of casticin in T24 cells is mediated by activation of the TAp73-XAF1 signaling pathway through RIP kinase-mediated ROS production.

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1	Csupor-Löffler B, Hajdú Z, Zupkó I, Réthy B, Falkay G, Forgo P and Hohmann J: Antiproliferative effect of flavonoids and sesquiterpenoids from Achillea millefolium s.1. on cultured human tumour cell lines. Phytother Res. 23:672–676. 2009. View Article : Google Scholar
2	Shen JK, Du HP, Yang M, Wang YG and Jin J: Casticin induces leukemic cell death through apoptosis and mitotic catastrophe. Ann Hematol. 88:743–752. 2009. View Article : Google Scholar : PubMed/NCBI
3	Tang SY, Zhong MZ, Yuan GJ, Hou SP, Yin LL, Jiang H and Yu ZY: Casticin, a flavonoid, potentiates TRAIL-induced apoptosis through modulation of anti-apoptotic proteins and death receptor 5 in colon cancer cells. Oncol Rep. 29:474–480. 2013.
4	Haïdara K, Zamir L, Shi QW and Batist G: The flavonoid Casticin has multiple mechanisms of tumor cytotoxicity action. Cancer Lett. 242:180–190. 2006. View Article : Google Scholar : PubMed/NCBI
5	Pirollo KF, Bouker KB and Chang EH: Does p53 status influence tumor response to anticancer therapies? Anticancer Drugs. 11:419–432. 2000. View Article : Google Scholar : PubMed/NCBI
6	Chen D, Cao J, Tian L, Liu F and Sheng X: Induction of apoptosis by casticin in cervical cancer cells through reactive oxygen species-mediated mitochondrial signaling pathways. Oncol Rep. 26:1287–1294. 2011.PubMed/NCBI
7	Deyoung MP and Ellisen LW: p63 and p73 in human cancer: Defining the network. Oncogene. 26:5169–5183. 2007. View Article : Google Scholar : PubMed/NCBI
8	Yang A, Walker N, Bronson R, Kaghad M, Oosterwegel M, Bonnin J, Vagner C, Bonnet H, Dikkes P, Sharpe A, et al: p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature. 404:99–103. 2000. View Article : Google Scholar : PubMed/NCBI
9	Melino G, De Laurenzi V and Vousden KH: p73: Friend or foe in tumorigenesis. Nat Rev Cancer. 2:605–615. 2002. View Article : Google Scholar : PubMed/NCBI
10	Dötsch V, Bernassola F, Coutandin D, Candi E and Melino G: p63 and p73, the ancestors of p53. Cold Spring Harb Perspect Biol. 2:a0048872010. View Article : Google Scholar : PubMed/NCBI
11	Jost CA, Marin MC and Kaelin WG Jr: p73 is a simian [correction of human] p53-related protein that can induce apoptosis. Nature. 389:191–194. 1997. View Article : Google Scholar : PubMed/NCBI
12	Zou B, Chim CS, Pang R, Zeng H, Dai Y, Zhang R, Lam CS, Tan VP, Hung IF, Lan HY, et al: XIAP-associated factor 1 (XAF1), a novel target of p53, enhances p53-mediated apoptosis via post-translational modification. Mol Carcinog. 51:422–432. 2012. View Article : Google Scholar
13	Liston P, Fong WG, Kelly NL, Toji S, Miyazaki T, Conte D, Tamai K, Craig CG, McBurney MW and Korneluk RG: Identification of XAF1 as an antagonist of XIAP anti-Caspase activity. Nat Cell Biol. 3:128–133. 2001. View Article : Google Scholar : PubMed/NCBI
14	Lee MG, Huh JS, Chung SK, Lee JH, Byun DS, Ryu BK, Kang MJ, Chae KS, Lee SJ, Lee CH, et al: Promoter CpG hyper-methylation and downregulation of XAF1 expression in human urogenital malignancies: Implication for attenuated p53 response to apoptotic stresses. Oncogene. 25:5807–5822. 2006. View Article : Google Scholar : PubMed/NCBI
15	Park GB, Kim YS, Kim D, Kim S, Lee HK, Cho DH, Lee WJ and Hur DY: Melphalan-induced apoptosis of EBV-transformed B cells through upregulation of TAp73 and XAF1 and nuclear import of XPA. J Immunol. 191:6281–6291. 2013. View Article : Google Scholar : PubMed/NCBI
16	Declercq W, Vanden Berghe T and Vandenabeele P: RIP kinases at the crossroads of cell death and survival. Cell. 138:229–232. 2009. View Article : Google Scholar : PubMed/NCBI
17	Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M and Chan FK: Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 137:1112–1123. 2009. View Article : Google Scholar : PubMed/NCBI
18	Wang P, Yu W, Hu Z, Jia L, Iyer VR, Sanders BG and Kline K: Involvement of JNK/p73/NOXA in vitamin E analog-induced apoptosis of human breast cancer cells. Mol Carcinog. 47:436–445. 2008. View Article : Google Scholar
19	Sanchez-Prieto R, Sanchez-Arevalo VJ, Servitja JM and Gutkind JS: Regulation of p73 by c-Abl through the p38 MAP kinase pathway. Oncogene. 21:974–979. 2002. View Article : Google Scholar : PubMed/NCBI
20	Yang J, Yang Y, Tian L, Sheng XF, Liu F and Cao JG: Casticin-induced apoptosis involves death receptor 5 upregulation in hepatocellular carcinoma cells. World J Gastroenterol. 17:4298–4307. 2011. View Article : Google Scholar : PubMed/NCBI
21	Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, Tran JH, Nedospasov SA and Liu ZG: Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem. 279:10822–10828. 2004. View Article : Google Scholar : PubMed/NCBI
22	Kaiser WJ and Offermann MK: Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J Immunol. 174:4942–4952. 2005. View Article : Google Scholar : PubMed/NCBI
23	Müller M, Schilling T, Sayan AE, Kairat A, Lorenz K, Schulze-Bergkamen H, Oren M, Koch A, Tannapfel A, Stremmel W, et al: TAp73/Delta Np73 influences apoptotic response, chemosensitivity and prognosis in hepatocellular carcinoma. Cell Death Differ. 12:1564–1577. 2005. View Article : Google Scholar : PubMed/NCBI
24	Liston P, Roy N, Tamai K, Lefebvre C, Baird S, Cherton-Horvat G, Farahani R, McLean M, Ikeda JE, MacKenzie A, et al: Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature. 379:349–353. 1996. View Article : Google Scholar : PubMed/NCBI
25	Arora V, Cheung HH, Plenchette S, Micali OC, Liston P and Korneluk RG: Degradation of survivin by the X-linked inhibitor of apoptosis (XIAP)-XAF1 complex. J Biol Chem. 282:26202–26209. 2007. View Article : Google Scholar : PubMed/NCBI
26	Fong WG, Liston P, Rajcan-Separovic E, St Jean M, Craig C and Korneluk RG: Expression and genetic analysis of XIAP-associated factor 1 (XAF1) in cancer cell lines. Genomics. 70:113–122. 2000. View Article : Google Scholar : PubMed/NCBI
27	Ju WC, Huang GB, Luo XY, Ren WH, Zheng DQ, Chen PJ, Lou YF and Li B: X-linked inhibitor of apoptosis-associated factor l (XAFl) enhances the sensitivity of colorectal cancer cells to cisplatin. Med Oncol. 31:2732014. View Article : Google Scholar : PubMed/NCBI
28	Straszewski-Chavez SL, Visintin IP, Karassina N, Los G, Liston P, Halaban R, Fadiel A and Mor G: XAF1 mediates tumor necrosis factor-alpha-induced apoptosis and X-linked inhibitor of apoptosis cleavage by acting through the mitochondrial pathway. J Biol Chem. 282:13059–13072. 2007. View Article : Google Scholar : PubMed/NCBI
29	Wang X, Wu G, Cao G, Yang L, Xu H, Huang J and Hou J: Zoledronic acid inhibits the pentose phosphate pathway through attenuating the Ras-TAp73-G6PD axis in bladder cancer cells. Mol Med Rep. 12:4620–4625. 2015.PubMed/NCBI
30	Zhang Y, Yan W, Jung YS and Chen X: Mammary epithelial cell polarity is regulated differentially by p73 isoforms via epithelial-to-mesenchymal transition. J Biol Chem. 287:17746–17753. 2012. View Article : Google Scholar : PubMed/NCBI
31	Sayan AE, D'Angelo B, Sayan BS, Tucci P, Cimini A, Cerù MP, Knight RA and Melino G: p73 and p63 regulate the expression of fibroblast growth factor receptor 3. Biochem Biophys Res Commun. 394:824–828. 2010. View Article : Google Scholar : PubMed/NCBI
32	Zhang D, Lin J and Han J: Receptor-interacting protein (RIP) kinase family. Cell Mol Immunol. 7:243–249. 2010. View Article : Google Scholar : PubMed/NCBI
33	Stanger BZ, Leder P, Lee TH, Kim E and Seed B: RIP: A novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell. 81:513–523. 1995. View Article : Google Scholar : PubMed/NCBI
34	Chaudhary PM, Eby M, Jasmin A, Bookwalter A, Murray J and Hood L: Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-kappaB pathway. Immunity. 7:821–830. 1997. View Article : Google Scholar
35	Festjens N, Vanden Berghe T, Cornelis S and Vandenabeele P: RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ. 14:400–410. 2007. View Article : Google Scholar : PubMed/NCBI
36	Lin Y, Devin A, Cook A, Keane MM, Kelliher M, Lipkowitz S and Liu ZG: The death domain kinase RIP is essential for TRAIL (Apo2L)-induced activation of IkappaB kinase and c-Jun N-terminal kinase. Mol Cell Biol. 20:6638–6645. 2000. View Article : Google Scholar : PubMed/NCBI
37	Siegel R, Naishadham D and Jemal A: Cancer statistics, 2013. CA Cancer J Clin. 63:11–30. 2013. View Article : Google Scholar : PubMed/NCBI