Review Article

Splicing DNA Damage Adaptations for the Management of Cancer Cells

Author(s): Arun Kumar Singh, Deepika Yadav and Rishabha Malviya*

Volume 24, Issue 2, 2024

Published on: 13 November, 2023

Page: [135 - 146] Pages: 12

DOI: 10.2174/0115665232258528231018113410

Price: $65

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Abstract

Maintaining a tumour cell's resistance to apoptosis (organized cell death) is essential for cancer to metastasize. Signal molecules play a critical function in the tightly regulated apoptotic process. Apoptosis may be triggered by a wide variety of cellular stresses, including DNA damage, but its ultimate goal is always the same: the removal of damaged cells that might otherwise develop into tumours. Many chemotherapy drugs rely on cancer cells being able to undergo apoptosis as a means of killing them. The mechanisms by which DNA-damaging agents trigger apoptosis, the interplay between pro- and apoptosis-inducing signals, and the potential for alteration of these pathways in cancer are the primary topics of this review.

Keywords: Apoptosis, extrinsic pathway, p38 signaling, cancer, DNA damage, genetic therapy.

Graphical Abstract
[1]
Lam AQ, Humphreys BD. Onco-nephrology. Clin J Am Soc Nephrol 2012; 7(10): 1692-700.
[http://dx.doi.org/10.2215/CJN.03140312] [PMID: 22879433]
[2]
Linxi W, Li T, Yanping W, et al. Exendin-4 protects HUVECs from t-BHP-induced apoptosis via PI3K/Akt-Bcl-2-caspase-3 signaling. Endocr Res 2016; 41(3): 229-35.
[3]
Ahmed A, Thliveris JC, Shaw A, Sowa M, Gilchrist J, Scott JE. Caspase 3 activity in isolated fetal rat lung fibroblasts and rat periodontal ligament fibroblasts: Cigarette smoke induced alterations. Tob Induc Dis 2013; 11(1): 25.
[4]
Man SM, Kanneganti TD. Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat Rev Immunol 2016; 16(1): 7-21.
[5]
Tsuchiya K. Inflammasome-associated cell death: Pyroptosis, apoptosis, and physiological implications. Microbiol Immunol 2020; 64(4): 252-69.
[6]
Devant P, Kagan JC. Molecular mechanisms of gasdermin D pore-forming activity. Nat Immunol 2023; 24: 1064-75.
[7]
D’arcy MS. Cell death: A review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 2019; 43(6): 582-92.
[8]
Eskandari E, Eaves CJ. Paradoxical roles of caspase-3 in regulating cell survival, proliferation, and tumorigenesis. J Cell Biol 2022; 221(6): 02201159.
[9]
Dantonio PM, Klein MO. Exploring major signaling cascades in melanomagenesis: A rationale route for targetted skin cancer therapy. Biosci Rep 2018; 38(5): BSR20180511.
[10]
Trnka J, Elkalaf M, Anděl M. Lipophilic triphenylphosphonium cations inhibit mitochondrial electron transport chain and induce mitochondrial proton leak. PLoS One 2015; 10(4): e0121837.
[http://dx.doi.org/10.1371/journal.pone.0121837] [PMID: 25927600]
[11]
Vandenabeele P, Bultynck G, Savvides SN. Pore-forming proteins as drivers of membrane permeabilization in cell death pathways. Nat Rev Mol Cell Biol 2023; 24(5): 312-33.
[12]
Wei MC, Lindsten T, Mootha VK, et al. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 2000; 14(16): 2060-71.
[http://dx.doi.org/10.1101/gad.14.16.2060] [PMID: 10950869]
[13]
Ola MS, Nawaz M, Ahsan H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol Cell Biochem 2011; 351: 41-58.
[14]
Zou L, Liu D, Elledge SJ. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc Natl Acad Sci 2003; 100(24): 13827-32.
[http://dx.doi.org/10.1073/pnas.2336100100] [PMID: 14605214]
[15]
Rouse J, Jackson SP. Interfaces between the detection, signaling, and repair of DNA damage. Science 2002; 297(5581): 547-51.
[http://dx.doi.org/10.1126/science.1074740] [PMID: 12142523]
[16]
Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421(6922): 499-506.
[http://dx.doi.org/10.1038/nature01368] [PMID: 12556884]
[17]
D’Amours D, Jackson SP. The MRE11 complex: At the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002; 3(5): 317-27.
[http://dx.doi.org/10.1038/nrm805] [PMID: 11988766]
[18]
Petrini J, Stracker TH. The cellular response to DNA double-strand breaks: defining the sensors and mediators. Trends Cell Biol 2003; 13(9): 458-62.
[http://dx.doi.org/10.1016/S0962-8924(03)00170-3] [PMID: 12946624]
[19]
Fernandez-Capetillo O, Chen HT, Celeste A, et al. DNA damage-induced G2–M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 2002; 4(12): 993-7.
[http://dx.doi.org/10.1038/ncb884] [PMID: 12447390]
[20]
Crighton D, Ryan KM. Splicing DNA-damage responses to tumour cell death. Biochimica et Biophysica Acta (BBA)-. Rev Can 2004; 1705(1): 3-15.
[21]
Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 2000; 14(8): 927-39.
[http://dx.doi.org/10.1101/gad.14.8.927] [PMID: 10783165]
[22]
Foray N, Marot D, Gabriel A, et al. A subset of ATM- and ATR-dependent phosphorylation events requires the BRCA1 protein. EMBO J 2003; 22(11): 2860-71.
[http://dx.doi.org/10.1093/emboj/cdg274] [PMID: 12773400]
[23]
Hirao A, Cheung A, Duncan G, et al. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol Cell Biol 2002; 22(18): 6521-32.
[http://dx.doi.org/10.1128/MCB.22.18.6521-6532.2002] [PMID: 12192050]
[24]
Takai H, Naka K, Okada Y, et al. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J 2002; 21(19): 5195-205.
[http://dx.doi.org/10.1093/emboj/cdf506] [PMID: 12356735]
[25]
Tokarz P, Kaarniranta K, Blasiak J. Role of the cell cycle re-initiation in DNA damage response of post-mitotic cells and its implication in the pathogenesis of neurodegenerative diseases. Rejuvenation Res 2016; 19(2): 131-9.
[http://dx.doi.org/10.1089/rej.2015.1717] [PMID: 26214710]
[26]
Yang S, Kuo C, Bisi JE, Kim MK. PML-dependent apoptosis after DNA damage is regulated by the checkpoint kinase hCds1/Chk2. Nat Cell Biol 2002; 4(11): 865-70.
[http://dx.doi.org/10.1038/ncb869] [PMID: 12402044]
[27]
Xie S, Wu H, Wang Q, et al. Genotoxic stress-induced activation of Plk3 is partly mediated by Chk2. Cell Cycle 2002; 1(6): 424-9.
[http://dx.doi.org/10.4161/cc.1.6.271] [PMID: 12548019]
[28]
Majidinia M, Yousefi B. DNA repair and damage pathways in breast cancer development and therapy. DNA Repair 2017; 54(54): 22-9.
[http://dx.doi.org/10.1016/j.dnarep.2017.03.009] [PMID: 28437752]
[29]
Maiani E, Diederich M, Gonfloni S. DNA damage response: The emerging role of c-Abl as a regulatory switch? Biochem Pharmacol 2011; 82(10): 1269-76.
[http://dx.doi.org/10.1016/j.bcp.2011.07.001] [PMID: 21763684]
[30]
Zannini L, Delia D, Buscemi G. CHK2 kinase in the DNA damage response and beyond. J Mol Cell Biol 2014; 6(6): 442-57.
[http://dx.doi.org/10.1093/jmcb/mju045]
[31]
Evans SC, Lozano G. The Li-Fraumeni syndrome: An inherited susceptibility to cancer. Mol Med Today 1997; 3(9): 390-5.
[http://dx.doi.org/10.1016/S1357-4310(97)01105-2] [PMID: 9302689]
[32]
Rufini A, Tucci P, Celardo I, Melino G. Senescence and aging: The critical roles of p53. Oncogene 2013; 32(43): 5129-43.
[http://dx.doi.org/10.1038/onc.2012.640] [PMID: 23416979]
[33]
Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997; 387(6630): 296-9.
[http://dx.doi.org/10.1038/387296a0] [PMID: 9153395]
[34]
Honda R, Yasuda H. Association of p19ARF with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J 1999; 18(1): 22-7.
[http://dx.doi.org/10.1093/emboj/18.1.22] [PMID: 9878046]
[35]
de Oca Luna RM, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995; 378(6553): 203-6.
[http://dx.doi.org/10.1038/378203a0] [PMID: 7477326]
[36]
Jones SN, Roe AE, Donehower LA, Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 1995; 378(6553): 206-8.
[http://dx.doi.org/10.1038/378206a0] [PMID: 7477327]
[37]
Stommel JM, Wahl GM. Accelerated MDM2 auto-degradation induced by DNA-damage kinases is required for p53 activation. EMBO J 2004; 23(7): 1547-56.
[http://dx.doi.org/10.1038/sj.emboj.7600145] [PMID: 15029243]
[38]
Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci 2001; 98(20): 11598-603.
[http://dx.doi.org/10.1073/pnas.181181198] [PMID: 11504915]
[39]
Zhou BP, Liao Y, Xia W, Zou Y, Spohn B, Hung MC. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat Cell Biol 2001; 3(11): 973-82.
[http://dx.doi.org/10.1038/ncb1101-973] [PMID: 11715018]
[40]
Giaccia AJ, Kastan MB. The complexity of p53 modulation: Emerging patterns from divergent signals. Genes Dev 1998; 12(19): 2973-83.
[http://dx.doi.org/10.1101/gad.12.19.2973] [PMID: 9765199]
[41]
Lakin ND, Jackson SP. Regulation of p53 in response to DNA damage. Oncogene 1999; 18(53): 7644-55.
[http://dx.doi.org/10.1038/sj.onc.1203015] [PMID: 10618704]
[42]
Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 1997; 91(3): 325-34.
[http://dx.doi.org/10.1016/S0092-8674(00)80416-X] [PMID: 9363941]
[43]
Unger T, Juven-Gershon T, Moallem E, et al. Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2. EMBO J 1999; 18(7): 1805-14.
[http://dx.doi.org/10.1093/emboj/18.7.1805] [PMID: 10202144]
[44]
Siliciano JD, Canman CE, Taya Y, Sakaguchi K, Appella E, Kastan MB. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev 1997; 11(24): 3471-81.
[http://dx.doi.org/10.1101/gad.11.24.3471] [PMID: 9407038]
[45]
Tibbetts RS, Brumbaugh KM, Williams JM, et al. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 1999; 13(2): 152-7.
[http://dx.doi.org/10.1101/gad.13.2.152] [PMID: 9925639]
[46]
Ray A, Milum K, Battu A, Wani G, Wani AA. NER initiation factors, DDB2 and XPC, regulate UV radiation response by recruiting ATR and ATM kinases to DNA damage sites. DNA Repair 2013; 12(4): 273-83.
[http://dx.doi.org/10.1016/j.dnarep.2013.01.003] [PMID: 23422745]
[47]
Chehab NH, Malikzay A, Appel M, Halazonetis TD. Chk2/hCds1 functions as a DNA damage checkpoint in G 1 by stabilizing p53. Genes Dev 2000; 14(3): 278-88.
[http://dx.doi.org/10.1101/gad.14.3.278] [PMID: 10673500]
[48]
Ashcroft M, Taya Y, Vousden KH. Stress signals utilize multiple pathways to stabilize p53. Mol Cell Biol 2000; 20(9): 3224-33.
[http://dx.doi.org/10.1128/MCB.20.9.3224-3233.2000] [PMID: 10757806]
[49]
Oda K, Arakawa H, Tanaka T, et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 2000; 102(6): 849-62.
[http://dx.doi.org/10.1016/S0092-8674(00)00073-8] [PMID: 11030628]
[50]
Okamura S, Arakawa H, Tanaka T, et al. p53DINP1, a p53-inducible gene, regulates p53-dependent apoptosis. Mol Cell 2001; 8(1): 85-94.
[http://dx.doi.org/10.1016/S1097-2765(01)00284-2] [PMID: 11511362]
[51]
Gu W, Shi XL, Roeder RG. Synergistic activation of transcription by CBP and p53. Nature 1997; 387(6635): 819-23.
[http://dx.doi.org/10.1038/42972] [PMID: 9194564]
[52]
Sakaguchi K, Herrera JE, Saito S, et al. DNA damage activates p53 through a phosphorylation–acetylation cascade. Genes Dev 1998; 12(18): 2831-41.
[http://dx.doi.org/10.1101/gad.12.18.2831] [PMID: 9744860]
[53]
Gostissa M, Hengstermann A, Fogal V, et al. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 1999; 18(22): 6462-71.
[http://dx.doi.org/10.1093/emboj/18.22.6462] [PMID: 10562558]
[54]
Bergamaschi D, Samuels Y, O’Neil NJ, et al. iASPP oncoprotein is a key inhibitor of p53 conserved from worm to human. Nat Genet 2003; 33(2): 162-7.
[http://dx.doi.org/10.1038/ng1070] [PMID: 12524540]
[55]
Gorina S, Pavletich NP. Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2. Science 1996; 274(5289): 1001-5.
[http://dx.doi.org/10.1126/science.274.5289.1001] [PMID: 8875926]
[56]
Samuels-Lev Y, O’Connor DJ, Bergamaschi D, et al. ASPP proteins specifically stimulate the apoptotic function of p53. Mol Cell 2001; 8(4): 781-94.
[http://dx.doi.org/10.1016/S1097-2765(01)00367-7] [PMID: 11684014]
[57]
Rowan S, Ludwig RL, Haupt Y, et al. Specific loss of apoptotic but not cell-cycle arrest function in a human tumor derived p53 mutant. EMBO J 1996; 15(4): 827-38.
[http://dx.doi.org/10.1002/j.1460-2075.1996.tb00418.x] [PMID: 8631304]
[58]
Ryan KM, Vousden KH. Characterization of structural p53 mutants which show selective defects in apoptosis but not cell cycle arrest. Mol Cell Biol 1998; 18(7): 3692-8.
[http://dx.doi.org/10.1128/MCB.18.7.3692] [PMID: 9632751]
[59]
Barlow C, Brown KD, Deng CX, Tagle DA, Wynshaw-Boris A. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat Genet 1997; 17(4): 453-6.
[http://dx.doi.org/10.1038/ng1297-453] [PMID: 9398849]
[60]
Schuler M, Green DR. Mechanisms of p53-dependent apoptosis. Biochem Soc Trans 2001; 29(6): 684-8.
[http://dx.doi.org/10.1042/bst0290684] [PMID: 11709054]
[61]
Miyashita T, Krajewski S, Krajewska M, et al. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 1994; 9(6): 1799-805.
[PMID: 8183579]
[62]
Marigo I, Bosio E, Solito S, et al. Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 2010; 32: 790-802.
[http://dx.doi.org/10.1016/j.immuni.2010.05.010.]
[63]
Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001; 7(3): 683-94.
[http://dx.doi.org/10.1016/S1097-2765(01)00214-3] [PMID: 11463392]
[64]
Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001; 7(3): 673-82.
[http://dx.doi.org/10.1016/S1097-2765(01)00213-1] [PMID: 11463391]
[65]
Owen-Schaub LB, Zhang W, Cusack JC, et al. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol Cell Biol 1995; 15(6): 3032-40.
[http://dx.doi.org/10.1128/MCB.15.6.3032] [PMID: 7539102]
[66]
Zhou M, Gu L, Li F, Zhu Y, Woods WG, Findley HW. DNA damage induces a novel p53-survivin signaling pathway regulating cell cycle and apoptosis in acute lymphoblastic leukemia cells. J Pharmacol Exp Ther 2002; 303(1): 124-31.
[http://dx.doi.org/10.1124/jpet.102.037192] [PMID: 12235242]
[67]
Murphy M, Hinman A, Levine AJ. Wild-type p53 negatively regulates the expression of a microtubule-associated protein. Genes Dev 1996; 10(23): 2971-80.
[http://dx.doi.org/10.1101/gad.10.23.2971] [PMID: 8956998]
[68]
Marchenko ND, Zaika A, Moll UM. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 2000; 275(21): 16202-12.
[http://dx.doi.org/10.1074/jbc.275.21.16202] [PMID: 10821866]
[69]
Mihara M, Erster S, Zaika A, et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11(3): 577-90.
[http://dx.doi.org/10.1016/S1097-2765(03)00050-9] [PMID: 12667443]
[70]
Hsieh JK, Yap D, O’Connor DJ, et al. Novel function of the cyclin A binding site of E2F in regulating p53-induced apoptosis in response to DNA damage. Mol Cell Biol 2002; 22(1): 78-93.
[http://dx.doi.org/10.1128/MCB.22.1.78-93.2002] [PMID: 11739724]
[71]
Furukawa Y, Nishimura N, Furukawa Y, et al. Apaf-1 is a mediator of E2F-1-induced apoptosis. J Biol Chem 2002; 277(42): 39760-8.
[http://dx.doi.org/10.1074/jbc.M200805200] [PMID: 12149244]
[72]
Moroni MC, Hickman ES, Denchi EL, et al. Apaf-1 is a transcriptional target for E2F and p53. Nat Cell Biol 2001; 3(6): 552-8.
[http://dx.doi.org/10.1038/35078527] [PMID: 11389439]
[73]
Blattner C, Sparks A, Lane D. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol Cell Biol 1999; 19(5): 3704-13.
[http://dx.doi.org/10.1128/MCB.19.5.3704] [PMID: 10207094]
[74]
Lin WC, Lin FT, Nevins JR. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev 2001; 15(14): 1833-44.
[PMID: 11459832]
[75]
O’Connor DJ, Lu X. Stress signals induce transcriptionally inactive E2F-1 independently of p53 and Rb. Oncogene 2000; 19(20): 2369-76.
[http://dx.doi.org/10.1038/sj.onc.1203540] [PMID: 10828878]
[76]
Kharbanda S, Yuan ZM, Weichselbaum R, Kufe D. Determination of cell fate by c-Abl activation in the response to DNA damage. Oncogene 1998; 17(25): 3309-18.
[http://dx.doi.org/10.1038/sj.onc.1202571] [PMID: 9916993]
[77]
Bar-Shira A, Rashi-Elkeles S, Zlochover L, et al. ATM-dependent activation of the gene encoding MAP kinase phosphatase 5 by radiomimetic DNA damage. Oncogene 2002; 21(5): 849-55.
[http://dx.doi.org/10.1038/sj.onc.1205127] [PMID: 11850813]
[78]
Zhang Y, Ma WY, Kaji A, Bode AM, Dong Z. Requirement of ATM in UVA-induced signaling and apoptosis. J Biol Chem 2002; 277(5): 3124-31.
[http://dx.doi.org/10.1074/jbc.M110245200] [PMID: 11723137]
[79]
Schlesinger TK, Bonvin C, Jarpe MB, et al. Apoptosis stimulated by the 91-kDa caspase cleavage MEKK1 fragment requires translocation to soluble cellular compartments. J Biol Chem 2002; 277(12): 10283-91.
[http://dx.doi.org/10.1074/jbc.M106885200] [PMID: 11782455]
[80]
Juretic N, Santibáñez JF, Hurtado C, Martínez J. ERK 1,2 and p38 pathways are involved in the proliferative stimuli mediated by urokinase in osteoblastic SaOS-2 cell line. J Cell Biochem 2001; 83(1): 92-8.
[http://dx.doi.org/10.1002/jcb.1211] [PMID: 11500957]
[81]
Liu WL, Guo X, Chen QQ, Guo ZG. Opposing effect of p38 CCDPK and p44/42 CCDPK signaling on TNF-alpha-induced apoptosis in bovine aortic endothelial cells. Acta Pharmacol Sin 2001; 22(5): 405-10.
[PMID: 11743886]
[82]
Yosimichi G, Nakanishi T, Nishida T, Hattori T, Takano-Yamamoto T, Takigawa M. CTGF/Hcs24 induces chondrocyte differentiation through a p38 mitogen-activated protein kinase (p38MAPK), and proliferation through a p44/42 MAPK/extracellular-signal regulated kinase (ERK). Eur J Biochem 2001; 268(23): 6058-65.
[http://dx.doi.org/10.1046/j.0014-2956.2001.02553.x] [PMID: 11732999]
[83]
Sarkar D, Su Z, Lebedeva IV, et al. mda-7 (IL-24): Signaling and functional roles. Biotechniques 2002; 33(S4): S30-9.
[http://dx.doi.org/10.2144/Oct0204] [PMID: 12395925]
[84]
Porras A, Zuluaga S, Black E, et al. P38 alpha mitogen-activated protein kinase sensitizes cells to apoptosis induced by different stimuli. Mol Biol Cell 2004; 15(2): 922-33.
[http://dx.doi.org/10.1091/mbc.e03-08-0592] [PMID: 14617800]
[85]
Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature 2001; 411(6835): 342-8.
[http://dx.doi.org/10.1038/35077213] [PMID: 11357141]
[86]
Momand J, Jung D, Wilczynski S, Niland J. The MDM2 gene amplification database. Nucleic Acids Res 1998; 26(15): 3453-9.
[http://dx.doi.org/10.1093/nar/26.15.3453] [PMID: 9671804]
[87]
Vousden KH. Human papillomaviruses and cervical carcinoma. Cancer Cells 1989; 1(2): 43-50.
[PMID: 2561870]
[88]
Strasser A, Huang DC, Vaux DL. The role of the bcl-2/ced-9 gene family in cancer and general implications of defects in cell death control for tumourigenesis and resistance to chemotherapy. Biochim Biophys Acta 1997; 1333(2): F151-78.
[PMID: 9395285]
[89]
Bruckheimer EM, Cho S, Brisbay S, et al. The impact of bcl-2 expression and bax deficiency on prostate homeostasis in vivo. Oncogene 2000; 19(20): 2404-12.
[http://dx.doi.org/10.1038/sj.onc.1203571] [PMID: 10828882]
[90]
Naik P, Karrim J, Hanahan D. The rise and fall of apoptosis during multistage tumorigenesis: Down-modulation contributes to tumor progression from angiogenic progenitors. Genes Dev 1996; 10(17): 2105-16.
[http://dx.doi.org/10.1101/gad.10.17.2105] [PMID: 8804306]
[91]
Rampino N, Yamamoto H, Ionov Y, et al. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 1997; 275(5302): 967-9.
[http://dx.doi.org/10.1126/science.275.5302.967] [PMID: 9020077]
[92]
Soengas MS, Capodieci P, Polsky D, et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 2001; 409(6817): 207-11.
[http://dx.doi.org/10.1038/35051606] [PMID: 11196646]
[93]
Zörnig M, Grzeschiczek A, Kowalski MB, Hartmann KU, Möröy T. Loss of Fas/Apo-1 receptor accelerates lymphomagenesis in E mu L-MYC transgenic mice but not in animals infected with MoMuLV. Oncogene 1995; 10(12): 2397-401.
[PMID: 7784089]
[94]
Grønbæk K, Straten P, Ralfkiaer E, et al. Somatic Fas mutations in non-Hodgkin’s lymphoma: Association with extranodal disease and autoimmunity. Blood 1998; 92(9): 3018-24.
[http://dx.doi.org/10.1182/blood.V92.9.3018] [PMID: 9787134]
[95]
Pitti RM, Marsters SA, Lawrence DA, et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature 1998; 396(6712): 699-703.
[http://dx.doi.org/10.1038/25387] [PMID: 9872321]
[96]
Djerbi M, Screpanti V, Catrina AI, Bogen B, Biberfeld P, Grandien A. The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J Exp Med 1999; 190(7): 1025-32.
[http://dx.doi.org/10.1084/jem.190.7.1025] [PMID: 10510092]
[97]
Dzreyan V, Eid M, Rodkin S, Pitinova M, Demyanenko S. E2F1 expression and apoptosis initiation in crayfish and rat peripheral neurons and glial cells after axonal injury. Int J Mol Sci 2022; 23(8): 4451.
[http://dx.doi.org/10.3390/ijms23084451] [PMID: 35457270]
[98]
Teitz T, Wei T, Valentine MB, et al. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat Med 2000; 6(5): 529-35.
[http://dx.doi.org/10.1038/75007] [PMID: 10802708]
[99]
Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 1997; 3(8): 917-21.
[http://dx.doi.org/10.1038/nm0897-917] [PMID: 9256286]
[100]
Adida C, Haioun C, Gaulard P, et al. Prognostic significance of survivin expression in diffuse large B-cell lymphomas. Blood 2000; 96(5): 1921-5.
[PMID: 10961895]
[101]
Islam A, Kageyama H, Takada N, et al. High expression of Survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 2000; 19(5): 617-23.
[http://dx.doi.org/10.1038/sj.onc.1203358] [PMID: 10698506]
[102]
Campbell KJ, Rocha S, Perkins ND. Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B. Mol Cell 2004; 13(6): 853-65.
[http://dx.doi.org/10.1016/S1097-2765(04)00131-5] [PMID: 15053878]
[103]
Tang D, Kidd VJ. Cleavage of DFF-45/ICAD by multiple caspases is essential for its function during apoptosis. J Biol Chem 1998; 273(44): 28549-52.
[http://dx.doi.org/10.1074/jbc.273.44.28549] [PMID: 9786842]
[104]
Scaffidi C, Schmitz I, Krammer PH, Peter ME. The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 1999; 274(3): 1541-8.
[http://dx.doi.org/10.1074/jbc.274.3.1541] [PMID: 9880531]
[105]
Ashkenazi A, Dixit VM. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 1999; 11(2): 255-60.
[http://dx.doi.org/10.1016/S0955-0674(99)80034-9] [PMID: 10209153]
[106]
Kubbutat MHG, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997; 387(6630): 299-303.
[http://dx.doi.org/10.1038/387299a0] [PMID: 9153396]
[107]
Ashcroft M, Kubbutat MHG, Vousden KH. Regulation of p53 function and stability by phosphorylation. Mol Cell Biol 1999; 19(3): 1751-8.
[http://dx.doi.org/10.1128/MCB.19.3.1751] [PMID: 10022862]
[108]
El-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75(4): 817-25.
[http://dx.doi.org/10.1016/0092-8674(93)90500-P] [PMID: 8242752]
[109]
Hermeking H, Lengauer C, Polyak K, et al. 14-3-3sigma is a p53-regulated inhibitor of G2/M progression. Mol Cell 1997; 1(1): 3-11.
[http://dx.doi.org/10.1016/S1097-2765(00)80002-7] [PMID: 9659898]
[110]
Liu G, Parant JM, Lang G, et al. Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice. Nat Genet 2004; 36(1): 63-8.
[http://dx.doi.org/10.1038/ng1282] [PMID: 14702042]
[111]
Oda E, Ohki R, Murasawa H, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000; 288(5468): 1053-8.
[http://dx.doi.org/10.1126/science.288.5468.1053] [PMID: 10807576]
[112]
Chipuk JE, Kuwana T, Bouchier-Hayes L, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004; 303(5660): 1010-4.
[http://dx.doi.org/10.1126/science.1092734] [PMID: 14963330]
[113]
Chipuk JE, Maurer U, Green DR, Schuler M. Pharmacologic activation of p53 elicits Bax-dependent apoptosis in the absence of transcription. Cancer Cell 2003; 4(5): 371-81.
[http://dx.doi.org/10.1016/S1535-6108(03)00272-1] [PMID: 14667504]
[114]
Bell LA, Ryan KM. Life and death decisions by E2F-1. Cell Death Differ 2004; 11(2): 137-42.
[http://dx.doi.org/10.1038/sj.cdd.4401324] [PMID: 14526389]
[115]
Kulbay M, Paimboeuf A, Ozdemir D, Bernier J. Review of cancer cell resistance mechanisms to apoptosis and actual targeted therapies. J Cell Biochem 2022; 123(11): 1736-61.
[http://dx.doi.org/10.1002/jcb.30173] [PMID: 34791699]
[116]
Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-κB in p53-mediated programmed cell death. Nature 2000; 404(6780): 892-7.
[http://dx.doi.org/10.1038/35009130] [PMID: 10786798]
[117]
Croxton R, Ma Y, Song L, Haura EB, Cress WD. Direct repression of the Mcl-1 promoter by E2F1. Oncogene 2002; 21(9): 1359-69.
[http://dx.doi.org/10.1038/sj.onc.1205157] [PMID: 11857079]
[118]
Han X, Sun Y. PROTACs: A novel strategy for cancer drug discovery and development. MedComm 2023; 4(3): e290.
[http://dx.doi.org/10.1002/mco2.290]

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