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Apoptosis in Carcinogenesis and Chemotherapy pp 25–50Cite as

Anti-Cancer Strategy of Transitional Cell Carcinoma of Bladder Based on Induction of Different Types of Programmed Cell Deaths

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Abstract

Current treatment for advanced malignancy of the bladder cancer relies on combination chemotherapeutic agent regimens. In these patients chemotherapeutic resistance emerges in the form of an aggressive subpopulation of tumor cells even if there has been a good initial response. The majority of chemotherapeutic agents target mitotic cancer cells by inducing DNA damage pathways or altering cell cycle regulation. Drug resistance often arises from the remaining post-mitotic cancer cells, which can be further targeted by triggering the intrinsic apoptotic, autophagic, or necrotic pathways. If the death pathway could be activated extrinsically, there would be the potential for a synergistic toxic effect on tumor cells. In addition, if the death pathway was identified as being nonfunctional for any of the reasons outlined, the restoration of function could reactivate the immune system anti-tumor response. Current strategy is to decipher the complexities of death pathways in order to identify key effector molecules and their function. As their mechanisms have been elucidated, so has the knowledge that aberrations can occur at many points along the pathway, interfering with normal function. This has fueled exciting new research attempts to engineer novel therapeutic options.

Keywords

  • Apoptosis
  • Autophagy
  • Bladder Cancer
  • Necrosis

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References

  • Abedin MJ, Wang D, McDonnell MA, Lehmann U, Kelekar A (2007) Autophagy delays apoptotic death in breast cancer cells following DNA damage. Cell Death Differ 14:500–510

    PubMed  CAS  Google Scholar 

  • Adida C, Crotty PL, McGrath J, Berrebi D, Diebold J, Altieri DC (1998) Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation. Am J Pathol 152:43–49

    PubMed  CAS  Google Scholar 

  • Aggarwal BB (2004) Nuclear factor-kappaB: the enemy within. Cancer Cell 6:203–208

    PubMed  CAS  Google Scholar 

  • Aita VM, Liang XH, Murty VV, Pincus DL, Yu W, Cayanis E, Kalachikov S, Gilliam TC, Levine B (1999) Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59:59–65.

    PubMed  CAS  Google Scholar 

  • Akhtar M, Gallagher L, Rohan S (2006) Survivin: role in diagnosis, prognosis, and treatment of bladder cancer. Adv Anat Pathol 13:122–126

    PubMed  CAS  Google Scholar 

  • Altieri DC (2003) Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 22:8581–8589

    PubMed  CAS  Google Scholar 

  • Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB (2007) Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117:326–336

    PubMed  CAS  Google Scholar 

  • Ambrosini G, Adida C, Altieri DC (1997) A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3:917–921

    PubMed  CAS  Google Scholar 

  • Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961–973.

    PubMed  CAS  Google Scholar 

  • Arai M, Sasaki A, Saito N, Nakazato Y (2005) Immunohistochemical analysis of cleaved caspase-3 detects high level of apoptosis frequently in diffuse large B-cell lymphomas of the central nervous system. Pathol Inter 55:122–129

    CAS  Google Scholar 

  • Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104:155–162

    PubMed  CAS  Google Scholar 

  • Bano D, Young KW, Guerin CJ, Lefeuvre R, Rothwell NJ, Naldini L, Rizzuto R, Carafoli E, Nicotera P (2005) Cleavage of the plasma membrane Na$+$/Ca$2+$ exchanger in excitotoxicity. Cell 120:275–285

    PubMed  CAS  Google Scholar 

  • Boone E, Vanden Berghe T, Van Loo G, De Wilde G, De Wael N, Vercammen D, Fiers W, Haegeman G, Vandenabeele P (2000) Structure/function analysis of p55 tumor necrosis factor receptor and fas-associated death domain. Effect on necrosis in L929sA cells. J Biol Chem 275:37596–37603.

    PubMed  CAS  Google Scholar 

  • Botti J, Djavaheri-Mergny M, Pilatte Y, Codogno P (2006) Autophagy signaling and the cogwheels of cancer. Autophagy 2:67–73

    PubMed  CAS  Google Scholar 

  • Brooks AD, Sayers TJ (2005) Reduction of the antiapoptotic protein cFLIP enhances the susceptibility of human renal cancer cells to TRAIL apoptosis. Cancer Immunol Immunother 54:499–505

    PubMed  CAS  Google Scholar 

  • Bursch W, Ellinger A, Kienzl H, Török L, Pandey S, Sikorska M, Walker R, Hermann RS (1996) Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 17:1595–1607

    PubMed  CAS  Google Scholar 

  • Burton PB, Anderson CJ, Corbishly CM (2000) Caspase 3 and p27 as predictors of invasive bladder cancer. N Engl J Med 343:1418–1420

    PubMed  CAS  Google Scholar 

  • Buzzai M, Bauer DE, Jones RG, Deberardinis RJ, Hatzivassiliou G, Elstrom RL, Thompson CB (2005) The glucose dependence of Akt-transformed cells can be reversed by pharmacologic activation of fatty acid $β$-oxidation. Oncogene 24:4165–4173

    PubMed  CAS  Google Scholar 

  • Cairns P, Shaw ME, Knowles MA (1993a) Initiation of bladder cancer may involve deletion of a tumour-suppressor gene on chromosome 9. Oncogene 8:1083–1085

    Google Scholar 

  • Cairns P, Shaw ME, Knowles MA (1993b) Preliminary mapping of the deleted region of chromosome 9 in bladder cancer. Cancer Res 53:1230–1232

    Google Scholar 

  • Cairns P, Tokino K, Eby Y, Sidransky D (1994) Homozygous deletions of 9p21 in primary human bladder tumors detected by comparative multiplex polymerase chain reaction. Cancer Res 54:1422–1424

    PubMed  CAS  Google Scholar 

  • Chai CY, Huang YC, Hung WC, Kang WY, Chen WT (2007) Arsenic salts induced autophagic cell death and hypermethylation of DAPK promoter in SV-40 immortalized human uroepithelial cells. Toxicol Lett 173:48–56.

    PubMed  CAS  Google Scholar 

  • Chan FK, Shisler J, Bixby JG, Felices M, Zheng L, Appel M, Orenstein J, Moss B, Lenardo MJ (2003) A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 278:51613–51621.

    PubMed  CAS  Google Scholar 

  • Chen F, Zhang G, Cao Y, Payne R, See WA (2007) Bacillus Calmette-Guerin inhibits apoptosis in human urothelial carcinoma cell lines in response to cytotoxic injury. J Urol 178:2166–2170

    PubMed  CAS  Google Scholar 

  • Cheng JC, Matsen CB, Gonzales FA, Ye W, Greer S, Marquez VE, Jones PA, Selker EU (2003) Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J Natl Cancer Inst 95:399–409.

    PubMed  CAS  Google Scholar 

  • Corcelle E, Nebout M, Bekri S, Gauthier N, Hofman P, Poujeol P, Fánichel P, Mograbi B (2006) Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res 66:6861–6870

    PubMed  CAS  Google Scholar 

  • Crighton D, Wilkinson S, O’Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM (2006) DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126:121–134

    PubMed  CAS  Google Scholar 

  • Cuervo AM (2004) Autophagy: in sickness and in health. Trends Cell Biol 14:70–77

    PubMed  Google Scholar 

  • Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gálinas C, Fan Y, Nelson DA, Jin S, White E (2006) Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10:51–64

    PubMed  CAS  Google Scholar 

  • Devlin J, Keen AJ, Knowles MA (1994) Homozygous deletion mapping at 9p21 in bladder carcinoma defines a critical region within 2cM of IFNA. Oncogene 9:2757–2760

    PubMed  CAS  Google Scholar 

  • Ding WX, Ni HM, Gao W, Hou YF, Melan MA, Chen X, Stolz DB, Shao ZM, Yin XM (2007) Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem 282:4702–4710

    PubMed  CAS  Google Scholar 

  • Dumitriu IE, Baruah P, Valentinis B, Voll RE, Herrmann M, Nawroth PP, Arnold B, Bianchi ME, Manfredi AA, Rovere-Querini P (2005) Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 174:7506–7515

    PubMed  CAS  Google Scholar 

  • Eguchi Y, Shimizu S, Tsujimoto Y (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57:1835–1840

    PubMed  CAS  Google Scholar 

  • El Mahdani NE, Ameyar M, Cai Z, Colard O, Masliah J, Chouaib S (2000) Resistance to TNF-induced cytotoxicity correlates with an abnormal cleavage of cytosolic phospholipase A2. J Immunol 165:6756–6761

    PubMed  CAS  Google Scholar 

  • Ertmer A, Huber V, Gilch S, Yoshimori T, Erfle V, Duyster J, Elsässer HP, Schätzl HM (2007) The anticancer drug imatinib induces cellular autophagy. Leukemia 21:936–942

    PubMed  CAS  Google Scholar 

  • Eskelinen EL (2005) Maturation of autophagic vacuoles in mammalian cells. Autophagy 1:1–10

    PubMed  CAS  Google Scholar 

  • Eskelinen EL, Prescott AR, Cooper J, Brachmann SM, Wang L, Tang X, Backer JM, Lucocq JM (2002) Inhibition of autophagy in mitotic animal cells. Traffic 3:878–893

    PubMed  CAS  Google Scholar 

  • Fan J, Stanfield J, Guo Y, Karam JA, Frenkel E, Sun X, Hsieh JT (2008) Effect of trans-2,3-dimethoxycinnamoyl azide on enhancing antitumor activity of romidepsin on human bladder cancer. Clin Cancer Res 14:1200–1207

    PubMed  CAS  Google Scholar 

  • Feng Z, Zhang H, Levine AJ, Jin S (2005) The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 102:8204–8209

    PubMed  CAS  Google Scholar 

  • Festjens N, Vanden Berghe T, Vandenabeele P (2006) Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757:1371–1387

    PubMed  CAS  Google Scholar 

  • Fontana D, Bellina M, Galietti F, Scoffone C, Cagnazzi E, Guercio S, Cappia S, Pozzi E (1999) Intravesical bacillus calmette-guerin (BCG) as inducer of tumor-suppressing proteins p53 and p21 Waf1-Cip1 during treatment of superficial bladder cancer. J Urol 162:225–230

    PubMed  CAS  Google Scholar 

  • Fuessel S, Kueppers B, Ning S, Kotzsch M, Kraemer K, Schmidt U, Meye A, Wirth MP (2004) Systematic in vitro evaluation of survivin directed antisense oligodeoxynucleotides in bladder cancer cells. J Urol 171:2471–2476

    PubMed  CAS  Google Scholar 

  • Furuya N, Yu J, Byfield M, Pattingre S, Levine B (2005) The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy 1:46–52

    CAS  Google Scholar 

  • Gao X, Zhang Y, Arrazola P, Hino O, Kobayashi T, Yeung RS, Ru B, Pan D (2002) Tsc tumour suppressor proteins antagonize amino-acid–TOR signaling. Nat Cell Biol 4:699–704.

    PubMed  CAS  Google Scholar 

  • Garami A, Zwartkruis FJ, Nobukuni T, Joaquin M, Roccio M, Stocker H, Kozma SC, Hafen E, Bos JL, Thomas G (2003) Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol Cell 11:1457–1466

    Google Scholar 

  • Giannopoulou I, Nakopoulou L, Zervas A, Lazaris AC, Stravodimos C, Giannopoulos A, Davaris PS (2002) Immunohistochemical study of pro-apoptotic factors Bax, Fas and CPP32 in urinary bladder cancer: prognostic implications. Urological research 30:342–345

    PubMed  CAS  Google Scholar 

  • Goffin J, Eisenhauer E (2002) DNA methyltransferase inhibitors-state of the art. Ann Oncol 13:1699–1716.

    PubMed  CAS  Google Scholar 

  • Golstein P, Kroemer G (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32:37–43

    PubMed  CAS  Google Scholar 

  • Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquére S, Eskelinen EL, Pierron G, Saftig P, Kroemer G (2005) The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci 118:3091–3102

    PubMed  CAS  Google Scholar 

  • Goossens V, Grooten J, De Vos K, Fiers W (1995) Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci USA 92:8115–8119

    PubMed  CAS  Google Scholar 

  • Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23:2891–2906

    PubMed  CAS  Google Scholar 

  • Gu Y, Wang C, Cohen A (2004) Effect of IGF-1 on the balance between autophagy of dysfunctional mitochondria and apoptosis. FEBS Lett 577:357–360

    PubMed  CAS  Google Scholar 

  • Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753–766

    PubMed  CAS  Google Scholar 

  • Hall MC, Chang SS, Dalbagni G, Pruthi RS, Seigne JD, Skinner EC, Wolf JS Jr, Schellhammer PF (2007) Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol 178:2314–2330

    PubMed  Google Scholar 

  • Harriman JF, Waters-Williams S, Chu DL, Powers JC, Schnellmann RG (2000) Efficacy of novel calpain inhibitors in preventing renal cell death. J Pharmacol Exp Ther 294:1083–1087

    PubMed  CAS  Google Scholar 

  • Hayakawa M, Ishida N, Takeuchi K, Shibamoto S, Hori T, Oku N, Ito F, Tsujimoto M (1993) Arachidonic acid-selective cytosolic phospholipase A2 is crucial in the cytotoxic action of tumor necrosis factor. J Biol Chem 268:11290–11295

    PubMed  CAS  Google Scholar 

  • Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349:2042–2054

    PubMed  CAS  Google Scholar 

  • Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1:489–495

    PubMed  CAS  Google Scholar 

  • Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, Jäättelä M (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-β, and Bcl-2. Mol Cell 25:193–205

    PubMed  Google Scholar 

  • Inbal B, Bialik S, Sabanay I, Shani G, Kimchi A (2002) DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J Cell Biol 157:455–468

    PubMed  CAS  Google Scholar 

  • Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–590

    PubMed  CAS  Google Scholar 

  • Iwata J, Ezaki J, Komatsu M, Yokota S, Ueno T, Tanida I, Chiba T, Tanaka K, Kominami E (2006) Excess peroxisomes are degraded by autophagic machinery in mammals. J Biol Chem 281:4035–4041

    PubMed  CAS  Google Scholar 

  • Jha AN, Noditi M, Nilsson R, Natarajan AT (1992) Genotoxic effects of sodium arsenite on human cells. Mut Res 284:215–221.

    CAS  Google Scholar 

  • Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728

    PubMed  CAS  Google Scholar 

  • Kamat AM, Sethi G, Aggarwal BB (2007) Curcumin potentiates the apoptotic effects of chemotherapeutic agents and cytokines through down-regulation of nuclear factor-kappaB and nuclear factor-kappaB-regulated gene products in IFN-alpha-sensitive and IFN-alpha-resistant human bladder cancer cells. Mol Cancer Ther 6:1022–1030

    PubMed  CAS  Google Scholar 

  • Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S (2004) Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 11:448–457

    PubMed  CAS  Google Scholar 

  • Karam JA, Lotan Y, Karakiewicz PI, Ashfaq R, Sagalowsky AI, Roehrborn CG, Shariat SF (2007a) Use of combined apoptosis biomarkers for prediction of bladder cancer recurrence and mortality after radical cystectomy. Lancet Oncol 8:128–136

    Google Scholar 

  • Karam JA, Fan J, Stanfield J, Richer E, Benaim EA, Frenkel E, Antich P, Sagalowsky AI, Mason RP, Hsieh JT (2007b) The use of histone deacetylase inhibitor FK228 and DNA hypomethylation agent 5-azacytidine in human bladder cancer therapy. Int J Cancer 120:1795–1802

    Google Scholar 

  • Kassouf W, Highshaw R, Nelkin GM, Dinney CP, Kamat AM (2006) Vitamins C and K3 sensitize human urothelial tumors to gemcitabine. J Urol 176:1642–1647

    PubMed  CAS  Google Scholar 

  • Katayama M, Kawaguchi T, Berger MS, Pieper RO (2007) DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ 14:548–558

    PubMed  CAS  Google Scholar 

  • Katzenellenbogen RA, Baylin SB, Herman JG (1999) Hypermethylation of the DAP-kinase CpG island is a common alteration in B-cell malignancies. Blood 93:4347–4353

    PubMed  CAS  Google Scholar 

  • Kelly WK, O’Connor OA, Marks PA (2002) Histone deacetylase inhibitors: from target to clinical trials. Expert Opin Investig Drugs 11:1695–1713

    PubMed  CAS  Google Scholar 

  • Kelly JD, Dai J, Eschwege P, Goldberg JS, Duggan BP, Williamson KE, Bander NH, Nanus DM (2004) Downregulation of Bcl-2 sensitises interferon-resistant renal cancer cells to Fas. Br J Cancer 91:164–170

    PubMed  CAS  Google Scholar 

  • Khan N, Afaq F, Saleem M, Ahmad N, Mukhtar H (2006) Targeting multiple signaling pathways by green tea polyphenol (-)-epigallocatechin-3-gallate. Cancer Res 66:2500–2505

    PubMed  CAS  Google Scholar 

  • Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T (2001) Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2:330–335

    PubMed  CAS  Google Scholar 

  • Kim R, Emi M, Tanabe K, Murakami S, Uchida Y, Arihiro K (2006) Regulation and interplay of apoptotic and non-apoptotic cell death. J. Pathol 208:319–326

    PubMed  CAS  Google Scholar 

  • Kissil JL, Feinstein E, Cohen O, Jones PA, Tsai YC, Knowles MA, Eydmann ME, Kimchi A (1997) DAP-kinase loss of expression in various carcinoma and B-cell lymphoma cell lines: possible implications for role as tumor suppressor gene. Oncogene 15:403–407

    PubMed  CAS  Google Scholar 

  • Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132–1136

    PubMed  CAS  Google Scholar 

  • Kong G, Shin KY, Oh YH, Lee JJ, Park HY, Woo YN, Lee JD (1998) Bcl-2 and p53 expressions in invasive bladder cancers. Acta Oncol 37:715–720

    PubMed  CAS  Google Scholar 

  • Kotoulas OB, Kalamidas SA, Kondomerkos DJ (2006) Glycogen autophagy in glucose homeostasis. Pathol Res Pract 202:631–638

    PubMed  CAS  Google Scholar 

  • Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, Vandenabeele P, Zhivotovsky B, Blagosklonny MV, Malorni W, Knight RA, Piacentini M, Nagata S, Melino G (2005) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12:1463–1467

    PubMed  CAS  Google Scholar 

  • Kwiek JJ, Haystead TA, Rudolph J (2004) Kinetic mechanism of quinone oxidoreductase 2 and its inhibition by the antimalarial quinolines. Biochemistry 43:4538–4547

    PubMed  CAS  Google Scholar 

  • Langer SW, Schmidt G, Sorensen M, Sehested M, Jensen PB (1999) Inhibitors of topoisomerase II as pH-dependent modulators of etoposide-mediated cytotoxicity. Clin Cancer Res 5:2899–2907

    PubMed  CAS  Google Scholar 

  • Li M, Jiang X, Liu D, Na Y, Gao GF, Xi Z (2008) Autophagy protects LNCaP cells under androgen deprivation conditions. Autophagy 4:54–60

    PubMed  CAS  Google Scholar 

  • Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672–676

    PubMed  CAS  Google Scholar 

  • Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, Tran JH, Nedospasov SA, Liu ZG (2004) Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 279:10822–10828.

    PubMed  CAS  Google Scholar 

  • Linnenbach AJ, Pressler LB, Seng BA, Kimmel BS, Tomaszewski JE, Malkowicz SB (1993) Characterization of chromosome 9 deletions in transitional cell carcinoma by microsatellite assay. Hum Mol Genet 2:1407–1411

    PubMed  CAS  Google Scholar 

  • Liu X, Schnellmann RG (2003) Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. J Pharmacol Exp Ther 304:3–70

    Google Scholar 

  • Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J (2005) Rheb binds and regulates the mTOR kinase. Curr Biol 15:702–713

    PubMed  CAS  Google Scholar 

  • Ludwig AT, Moore JM, Luo Y, Chen X, Saltsgaver NA, O’Donnell MA, Griffith TS (2004) Tumor necrosis factor-related apoptosis-inducing ligand a novel mechanism for Bacillus Calmette-Guerin-induced antitumor activity. Cancer Res 64:3386–3390

    PubMed  CAS  Google Scholar 

  • Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237–248

    PubMed  CAS  Google Scholar 

  • McKnight JJ, Gray SB, O’Kane HF, Johnston SR, Williamson KE (2005) Apoptosis and chemotherapy for bladder cancer. J Urol 173:683–690

    PubMed  CAS  Google Scholar 

  • Micheau O, Solary E, Hammann A, Martin F, Dimanche-Boitrel MT (1997) Sensitization of cancer cells treated with cytotoxic drugs to fas-mediated cytotoxicity. J Natl Cancer Inst 89:783–789

    PubMed  CAS  Google Scholar 

  • Miyao N, Tsai YC, Lerner SP, Olumi AF, Spruck CH 3rd, Gonzalez-Zulueta M, Nichols PW, Skinner DG, Jones PA (1993) Role of chromosome 9 in human bladder cancer. Cancer Res 53: 4066–4070

    PubMed  CAS  Google Scholar 

  • Mizushima N (2007) Autophagy: process and function. Gene Dev 21:2861–2873

    PubMed  CAS  Google Scholar 

  • Mizutani Y, Okada Y, Yoshida O, Fukumoto M, Bonavida B (1997) Doxorubicin sensitizes human bladder carcinoma cells to Fas-mediated cytotoxicity, Cancer 79:1180–1189

    PubMed  CAS  Google Scholar 

  • Munz C (2006) Autophagy and antigen presentation, Cell Microbiol 8:891–898

    PubMed  CAS  Google Scholar 

  • Nagata S (1997) Apoptosis by death factor. Cell 88:355–365

    PubMed  CAS  Google Scholar 

  • O’Donnell MA (2007) Advances in the management of superficial bladder cancer. Semin Oncol 34:85–97

    PubMed  Google Scholar 

  • Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220–9231.

    PubMed  CAS  Google Scholar 

  • Ong F, Moonen LM, Gallee MP, ten Bosch C, Zerp SF, Hart AA, Bartelink H, Verheij M (2001) Prognostic factors in transitional cell cancer of the bladder: an emerging role for Bcl-2 and p53. Radiother Oncol 61:169–175

    PubMed  CAS  Google Scholar 

  • Ono Y, Shimada H, Sorimachi H, Richard I, Saido TC, Beckmann JS, Ishiura S, Suzuki K (1998) Functional defects of a muscle-specific calpain, p94, caused by mutations associated with limb-girdle muscular dystrophy type 2A. J Biol Chem 273:17073–17078

    PubMed  CAS  Google Scholar 

  • Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, Domingo D, Yahalom J (2001) A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 61:439–444

    PubMed  CAS  Google Scholar 

  • Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O, Padmanabhan R, Hild M, Berry DL, Garza D, Hubbert CC, Yao TP, Baehrecke EH, Taylor JP (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:860–864

    Google Scholar 

  • Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E (2004) Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 279:7370–7377

    PubMed  CAS  Google Scholar 

  • Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927–939

    PubMed  CAS  Google Scholar 

  • Pelucchi C, Bosetti C, Negri E, Malvezzi M, La Vecchia C (2006) Mechanisms of disease: The epidemiology of bladder cancer. Nat clin Prac Urol 3:327–340

    CAS  Google Scholar 

  • Petiot A, Faure J, Stenmark H, Gruenberg J (2003) PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J Cell Biol 162:971–979

    PubMed  CAS  Google Scholar 

  • Qin J, Xie LP, Zheng XY, Wang YB, Bai Y, Shen HF, Li LC, Dahiya R (2007) A component of green tea, (-)-epigallocatechin-3-gallate, promotes apoptosis in T24 human bladder cancer cells via modulation of the PI3K/Akt pathway and Bcl-2 family proteins. Biochem Biophys Res Commun 354:852–857

    PubMed  CAS  Google Scholar 

  • Raisuddin S, Jha AN (2004) Relative sensitivity of fish and mammalian cells to sodium arsenate and arsenite as determined by alkaline single-cell gel electrophoresis and cytokinesis-block micronucleus assay. Environ Mol Mutagen 44:83–89

    PubMed  CAS  Google Scholar 

  • Reed JC (1999) Dysregulation of apoptosis in cancer. J Clin Oncol 17:2941–2953

    PubMed  CAS  Google Scholar 

  • Reggiori F, Klionsky DJ (2005) Autophagosomes: biogenesis from scratch? Curr Opin Cell Biol 17:415–422

    PubMed  CAS  Google Scholar 

  • Rez G, Csak J, Fellinger E, Làszlò L, Kovàcs AL, Oliva O, Kovàcs J (1996) Time course of vinblastine-induced autophagocytosis and changes in the endoplasmic reticulum in murine pancreatic acinar cells: a morphometric and biochemical study. Eur J Cell Biol 71:341–350

    PubMed  CAS  Google Scholar 

  • Richard I, Broux O, Allamand V, Fougerousse F, Chiannilkulchai N, Bourg N, Brenguier L, Devaud C, Pasturaud P, Roudaut C, Hillaire D, Passosbueno MR, Zatz M, Tischfield JA, Fardeau M, Jackson CE, Cohen D, Beckmann JS (1995) Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81:27–40

    PubMed  CAS  Google Scholar 

  • Richon VM, Webb Y, Merger R, Sheppard T, Jursic B, Ngo L, Civoli F, Breslow R, Rifkind RA, Marks PA (1996) Second generation hybrid polar compounds are potent inducers of transformed cell differentiation. Proc Natl Acad Sci USA 93:5705–5708

    PubMed  CAS  Google Scholar 

  • Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F (2006) Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol Cell 98:53–67

    PubMed  CAS  Google Scholar 

  • Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, Giazzon M, Dumitriu IE, Müller S, Iannacone M, Traversari C, Bianchi ME, Manfredi AA (2004) HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 5:825–830

    PubMed  CAS  Google Scholar 

  • Salz W, Eisenberg D, Plescia J, Garlick DS, Weiss RM, Wu XR, Sun TT, Altieri DC (2005) A survivin gene signature predicts aggressive tumor behavior. Cancer Res 65:3531–3534

    PubMed  CAS  Google Scholar 

  • Saucedo LJ, Gao X, Chiarelli DA, Li L, Pan D, Edgar BA (2003) Rheb promotes cell growth as a component of the insulin/TOR signalling network, Nat Cell Biol 5:566–571.

    PubMed  CAS  Google Scholar 

  • Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195

    PubMed  CAS  Google Scholar 

  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26:1749–1760

    PubMed  CAS  Google Scholar 

  • Schimmer AD (2004) Inhibitor of apoptosis proteins translating basic knowledge into clinical practice. Cancer Res 64:7183–7190

    PubMed  CAS  Google Scholar 

  • Schneider JG, Finck BN, Ren J, Standley KN, Takagi M, Maclean KH, Bernal-Mizrachi C, Muslin AJ, Kastan MB, Semenkovich CF (2006) ATM-dependent suppression of stress signaling reduces vascular disease in metabolic syndrome. Cell Metabol 4:377–389

    CAS  Google Scholar 

  • Schultz IJ, Kiemeney LA, Karthaus HF, Witjes JA, Willems JL, Swinkels DW, Gunnewiek JM, de Kok JB (2004) Survivin mRNA copy number in bladder washings predicts tumor recurrence in patients with superficial urothelial cell carcinomas. Clin Chem 50:1425–1428

    PubMed  CAS  Google Scholar 

  • Schumacher PA, Eubanks JH, Fehlings MG (1999) Increased calpain I-mediated proteolysis, and preferential loss of dephosphorylated NF200, following traumatic spinal cord injury. Neuroscience 91:733–744

    PubMed  CAS  Google Scholar 

  • Shankar S, Singh TR, Srivastava RK (2004) Ionizing radiation enhances the therapeutic potential of TRAIL in prostate cancer in vitro and in vivo intracellular mechanisms. Prostate 61:35–49

    PubMed  CAS  Google Scholar 

  • Shao Y, Gao Z, Marks PA, Jiang X (2004) Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc Natl Acad. Sci USA 101:18030–18035

    PubMed  CAS  Google Scholar 

  • Shariat SF, Kim J, Raptidis G, Ayala GE, Lerner SP (2003) Association of p53 and p21 expression with clinical outcome in patients with carcinoma in situ of the urinary bladder. Urology 61:1140–1145

    PubMed  Google Scholar 

  • Shariat SF, Tokunaga H, Zhou J, Kim J, Ayala GE, Benedict WF, Lerner SP (2004a) p53, p21, pRB, and p16 expression predict clinical outcome in cystectomy with bladder cancer. J Clin Oncol 22:1014–1024

    Google Scholar 

  • Shariat SF, Casella R, Khoddami SM, Hernandez G, Sulser T, Gasser TC, Lerner SP (2004b) Urine detection of survivin is a sensitive marker for the noninvasive diagnosis of bladder cancer. J Urol 171:626–630

    Google Scholar 

  • Shariat SF, Ashfaq R, Karakiewicz PI, Saeedi O, Sagalowsky AI, Lotan Y (2007) Survivin expression is associated with bladder cancer presence, stage, progression, and mortality. Cancer 109:1106–1113

    PubMed  CAS  Google Scholar 

  • Shen HM, Lin Y, Choksi S, Tran J, Jin T, Chang L, Karin M, Zhang J, Liu ZG (2004) Essential roles of receptor-interacting protein and TRAF2 in oxidative stress-induced cell death. Mol Cell Biol 24:5914–5922.

    PubMed  CAS  Google Scholar 

  • Singh S, Aggarwal BB (1995) Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane). J Biol Chem 270:24995–25000

    PubMed  CAS  Google Scholar 

  • Singh RP, Gu M, Agarwal R (2008) Silibinin inhibits colorectal cancer growth by inhibiting tumor cell proliferation and angiogenesis. Cancer Res 68:2043–2050

    PubMed  CAS  Google Scholar 

  • Smith SD, Wheeler MA, Plescia J, Colberg JW, Weiss RM, Altieri DC (2001) Urine detection of survivin and diagnosis of bladder cancer. JAMA 285:324–328

    PubMed  CAS  Google Scholar 

  • Srivastava RK, Chen Q, Siddiqui I, Sarva K, Shankar S (2007) Linkage of curcumin-induced cell cycle arrest and apoptosis by cyclin-dependent kinase inhibitor p21(/WAF1/CIP1). Cell Cycle 6:2953–2961

    PubMed  CAS  Google Scholar 

  • Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, Daram P, Breuer S, Thomas G, Hafen E (2003) Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat Cell Biol 5:559–565.

    PubMed  CAS  Google Scholar 

  • Sudarshan S, Holman DH, Hyer ML, Voelkel-Johnson C, Dong JY, Norris JS (2005) In vitro efficacy of Fas ligand gene therapy for the treatment of bladder cancer. Cancer Gene Ther 12:12–18

    PubMed  CAS  Google Scholar 

  • Svatek RS, Herman MP, Lotan Y, Casella R, Hsieh JT, Sagalowsky AI, Shariat SF (2006) Soluble Fas-A promising novel urinary marker for the detection of recurrent superficial bladder cancer. Cancer 106:1701–1707

    PubMed  CAS  Google Scholar 

  • Syntichaki P, Xu K, Driscoll M, Tavernarakis N (2002) Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419:939–944

    PubMed  CAS  Google Scholar 

  • Takeuchi H, Kanzawa T, Kondo Y, Kondo S (2004) Inhibition of platelet-derived growth factor signalling induces autophagy in malignant glioma cells. Br J Cancer 90:1069–1075

    PubMed  CAS  Google Scholar 

  • Tanida I, Tanida-Miyake E, Komatsu M, Ueno T, Kominami E (2002) Human Apg3p/Aut1p homologue is an authentic E2 enzyme for multiple substrates, GATE-16, GABARAP, and MAP–LC3, and facilitates the conjugation of hApg12p to hApg5p. J Biol Chem 277:13739–13744

    PubMed  CAS  Google Scholar 

  • Tanida I, Tanida-Miyake E, Ueno T, Kominami E (2001) The human homolog of Saccharomyces cerevisiae Apg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP–LC3. J Biol Chem 276:1701–1706

    PubMed  CAS  Google Scholar 

  • Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK (2001) The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105:345–355

    PubMed  CAS  Google Scholar 

  • Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J (2003) Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 13:1259–1268.

    PubMed  CAS  Google Scholar 

  • Temkin V, Huang Q, Liu H, Osada H, Pope RM (2006) Inhibition of ADP/ATP exchange in receptor-interacting protein-mediated necrosis. Mol Cell Biol 26:2215–2225

    PubMed  CAS  Google Scholar 

  • Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8:487–496

    PubMed  CAS  Google Scholar 

  • Tice RR, Yager JW, Andrews P, Crecelius E (1997) Effect of hepatic methyl donor status on urinary excretion and DNA damage in B6C3F1 mice treated with sodium arsenite. Mutat Res 386:315–334

    PubMed  CAS  Google Scholar 

  • Tyagi A, Singh RP, Agarwal C, Agarwal R (2006) Silibinin activates p53-caspase 2 pathway and causes caspase-mediated cleavage of Cip1/p21 in apoptosis induction in bladder transitional-cell papilloma RT4 cells: evidence for a regulatory loop between p53 and caspase 2. Carcinogenesis 27:2269–2280

    PubMed  CAS  Google Scholar 

  • Tyagi A, Raina K, Singh RP, Gu M, Agarwal C, Harrison G, Glode LM, Agarwal R (2007) Chemopreventive effects of silymarin and silibinin on N-butyl-N-(4-hydroxybutyl) nitrosamine induced urinary bladder carcinogenesis in male ICR mice. Mol Cancer Ther 6:3248–3255

    PubMed  CAS  Google Scholar 

  • Vakkila J, Lotze MT (2004) Inflammation and necrosis promote tumour growth. Nat Rev Immunol 4:641–648

    PubMed  CAS  Google Scholar 

  • Vercammen D, Beyaert R, Denecker G, Goossens V, Van Loo G, Declercq W, Grooten J, Fiers W, Vandenabeele P (1998) Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 187:1477–1485

    PubMed  CAS  Google Scholar 

  • Wang JP, Qi L, Moore MR, Ng JC (2002) A review of animal models for the study of arsenic carcinogenesis. Toxicol Lett 133:17–31

    PubMed  CAS  Google Scholar 

  • Waters SL, Sarang SS, Wang KKW, Schnellmann RG (1997) Calpains mediate calcium and chloride influx during the late phase of cell injury. J Pharmacol Exp Ther 283:1177–1184

    PubMed  CAS  Google Scholar 

  • Wu X, Obata T, Khan Q, Highshaw RA, De Vere White R, Sweeney C (2004) The phosphatidylinositol-3 kinase pathway regulates bladder cancer cell invasion. BJU Int 93:143–150

    PubMed  CAS  Google Scholar 

  • Xu Y, Huang S, Liu ZG, Han J (2006) Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J Biol Chem 281:7788–8795.

    Google Scholar 

  • Xu K, Tavernarakis N, Driscoll M (2001) Necrotic cell death in C. elegans requires the function of calreticulin and regulators of Ca(2+) release from the endoplasmic reticulum. Neuron 31:957–971

    PubMed  CAS  Google Scholar 

  • Yagita H, Takeda K, Hayakawa Y, Smyth MJ, Okumura K (2004) TRAIL and its receptors as targets for cancer therapy. Cancer Sci 95:777–783

    PubMed  CAS  Google Scholar 

  • Yamana K, Bilim V, Hara N, Kasahara T, Itoi T, Maruyama R, Nishiyama T, Takahashi K, Tomita Y (2005) Prognostic impact of FAS/CD95/APO-1 in urothelial cancers: decreased expression of Fas is associated with disease progression. Br J Cancer 93:544–551

    PubMed  CAS  Google Scholar 

  • Yamashima T, Tonchev AB, Tsukada T, Saido TC, Imajoh-Ohmi S, Momoi T, Kominami E (2003) Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus 13:791–800

    PubMed  CAS  Google Scholar 

  • Yamashima T, Kohda Y, Tsuchiya K, Ueno T, Yamashita J, Yoshioka T, Kominami E (1998) Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on ‘calpain-cathepsin hypothesis’. Eur J Neurosci 10:1723–1733

    PubMed  CAS  Google Scholar 

  • Yao KC, Komata T, Kondo Y, Kanzawa T, Kondo S, Germano IM (2003) Molecular response of human glioblastoma multiforme cells to ionizing radiation: cell cycle arrest, modulation of the expression of cyclin-dependent kinase inhibitors, and autophagy. J Neurosurg 98:378–384

    PubMed  CAS  Google Scholar 

  • Yu L, Alva A, Su H, Dutt P, Freundt E, Welsh S, Baehrecke EH, Lenardo MJ (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304:1500–1502

    PubMed  CAS  Google Scholar 

  • Zeh HJ III, Lotze MT (2005) Addicted to death: invasive cancer and the immune response to unscheduled cell death. J Immunother 28:1–9

    PubMed  Google Scholar 

  • Zhang Y, Gao X, Saucedo LJ, Ru B, Edgar BA, Pan D (2003) Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins. Nat Cell Biol 5:578–581

    PubMed  CAS  Google Scholar 

  • Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, Hagberg H, Blomgren K (2005) The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 12:162–176

    PubMed  CAS  Google Scholar 

  • Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB (2004) Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 18:1272–1282

    PubMed  CAS  Google Scholar 

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  1. Department of Urology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA

    Jer-Tsong Hsieh

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  1. Jose A. Karam
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  1. Department of Surgery Shatin, Chinese University of Hong Kong Prince of Wales Hospital, Shatin, New Territories, Hong Kong/PR China

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Karam, J.A., Hsieh, JT. (2009). Anti-Cancer Strategy of Transitional Cell Carcinoma of Bladder Based on Induction of Different Types of Programmed Cell Deaths. In: Chen, G.G., Lai, P.B. (eds) Apoptosis in Carcinogenesis and Chemotherapy. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9597-9_2

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