The PARP Enzyme Family and the Hallmarks of Cancer Part 1. Cell Intrinsic Hallmarks
Abstract
Simple Summary
Abstract
1. Introduction
2. PARPs in Hallmark Cancer Traits
2.1. Sustaining Proliferative Signaling and Evading Growth Suppressors
2.2. Resisting Cell Death
2.3. Enabling Replicative Immortality
2.4. Genome Instability and Mutation
PARPs in DNA Repair
- DSBR
- NER
- SSBR and BER
2.5. Reprogramming Energy Metabolism
3. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Amé, J.C.; Spenlehauer, C.; de Murcia, G. The PARP superfamily. Bioessays 2004, 26, 882–893. [Google Scholar] [CrossRef]
- Munnur, D.; Bartlett, E.; Mikolčević, P.; Kirby, I.T.; Rack, J.G.M.; Mikoč, A.; Cohen, M.S.; Ahel, I. Reversible ADP-ribosylation of RNA. Nucleic Acids Res. 2019, 47, 5658–5669. [Google Scholar] [CrossRef] [PubMed]
- Vyas, S.; Matic, I.; Uchima, L.; Rood, J.; Zaja, R.; Hay, R.T.; Ahel, I.; Chang, P. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 2014, 5, 4426. [Google Scholar] [CrossRef] [PubMed]
- Verheugd, P.; Bütepage, M.; Eckei, L.; Lüscher, B. Players in ADP-ribosylation: Readers and Erasers. Curr. Protein. Pept. Sci. 2016, 17, 654–667. [Google Scholar] [CrossRef] [PubMed]
- Gupte, R.; Liu, Z.; Kraus, W.L. PARPs and ADP-ribosylation: Recent advances linking molecular functions to biological outcomes. Genes Dev. 2017, 31, 101–126. [Google Scholar] [CrossRef]
- Hottiger, M.O.; Hassa, P.O.; Lüscher, B.; Schüler, H.; Koch-Nolte, F. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 2010, 35, 208–219. [Google Scholar] [CrossRef] [PubMed]
- O’Sullivan, J.; Tedim Ferreira, M.; Gagné, J.P.; Sharma, A.K.; Hendzel, M.J.; Masson, J.Y.; Poirier, G.G. Emerging roles of eraser enzymes in the dynamic control of protein ADP-ribosylation. Nat. Commun. 2019, 10, 1182. [Google Scholar] [CrossRef]
- Alemasova, E.E.; Lavrik, O.I. Poly(ADP-ribosyl)ation by PARP1: Reaction mechanism and regulatory proteins. Nucleic Acids Res. 2019, 47, 3811–3827. [Google Scholar] [CrossRef] [PubMed]
- Hegedűs, C.; Virág, L. Inputs and outputs of poly(ADP-ribosyl)ation: Relevance to oxidative stress. Redox Biol. 2014, 2, 978–982. [Google Scholar] [CrossRef] [PubMed]
- Yap, T.A.; Plummer, R.; Azad, N.S.; Helleday, T. The DNA Damaging Revolution: PARP Inhibitors and Beyond. Am. Soc. Clin. Oncol. Educ. Book 2019, 39, 185–195. [Google Scholar] [CrossRef]
- Farmer, H.; McCabe, N.; Lord, C.J.; Tutt, A.N.; Johnson, D.A.; Richardson, T.B.; Santarosa, M.; Dillon, K.J.; Hickson, I.; Knights, C.; et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434, 917–921. [Google Scholar] [CrossRef]
- Lord, C.J.; Ashworth, A. PARP inhibitors: Synthetic lethality in the clinic. Science 2017, 355, 1152–1158. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell 2000, 100, 57–70. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed]
- Boveri, T. Zur Frage der Entstehung Maligner Tumoren; Gustav Fischer: Jena, Germany, 1914; Volume 4. [Google Scholar]
- Vogelstein, B.; Fearon, E.R.; Hamilton, S.R.; Kern, S.E.; Preisinger, A.C.; Leppert, M.; Nakamura, Y.; White, R.; Smits, A.M.; Bos, J.L. Genetic alterations during colorectal-tumor development. N. Engl. J. Med. 1988, 319, 525–532. [Google Scholar] [CrossRef] [PubMed]
- Bell, C.C.; Gilan, O. Principles and mechanisms of non-genetic resistance in cancer. Br. J. Cancer 2020, 122, 465–472. [Google Scholar] [CrossRef]
- Demény, M.A.; Virág, L. The PARP enzyme family and the hallmarks of cancer Part 2. Hallmarks related to cancer host interactions. Cancers. (accepted).
- Curtin, N. PARP inhibitors for anticancer therapy. Biochem. Soc. Trans. 2014, 42, 82–88. [Google Scholar] [CrossRef]
- Wahlberg, E.; Karlberg, T.; Kouznetsova, E.; Markova, N.; Macchiarulo, A.; Thorsell, A.G.; Pol, E.; Frostell, Å.; Ekblad, T.; Öncü, D.; et al. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat. Biotechnol. 2012, 30, 283–288. [Google Scholar] [CrossRef]
- Simbulan-Rosenthal, C.M.; Rosenthal, D.S.; Boulares, A.H.; Hickey, R.J.; Malkas, L.H.; Coll, J.M.; Smulson, M.E. Regulation of the expression or recruitment of components of the DNA synthesome by poly(ADP-ribose) polymerase. Biochemistry 1998, 37, 9363–9370. [Google Scholar] [CrossRef]
- Smulson, M.E.; Simbulan-Rosenthal, C.M.; Boulares, A.H.; Yakovlev, A.; Stoica, B.; Iyer, S.; Luo, R.; Haddad, B.; Wang, Z.Q.; Pang, T.; et al. Roles of poly(ADP-ribosyl)ation and PARP in apoptosis, DNA repair, genomic stability and functions of p53 and E2F-1. Adv. Enzym. Regul. 2000, 40, 183–215. [Google Scholar] [CrossRef]
- Augustin, A.; Spenlehauer, C.; Dumond, H.; Ménissier-De Murcia, J.; Piel, M.; Schmit, A.C.; Apiou, F.; Vonesch, J.L.; Kock, M.; Bornens, M.; et al. PARP-3 localizes preferentially to the daughter centriole and interfeRes. with the G1/S cell cycle progression. J. Cell Sci. 2003, 116, 1551–1562. [Google Scholar] [CrossRef]
- Smith, S.; de Lange, T. Cell cycle dependent localization of the telomeric PARP, tankyrase, to nuclear pore complexes and centrosomes. J. Cell Sci. 1999, 112 Pt 21, 3649–3656. [Google Scholar]
- Kanai, M.; Uchida, M.; Hanai, S.; Uematsu, N.; Uchida, K.; Miwa, M. Poly(ADP-ribose) polymerase localizes to the centrosomes and chromosomes. Biochem. Biophys Res. Commun. 2000, 278, 385–389. [Google Scholar] [CrossRef] [PubMed]
- Kanai, M.; Tong, W.M.; Sugihara, E.; Wang, Z.Q.; Fukasawa, K.; Miwa, M. Involvement of poly(ADP-Ribose) polymerase 1 and poly(ADP-Ribosyl)ation in regulation of centrosome function. Mol. Cell Biol. 2003, 23, 2451–2462. [Google Scholar] [CrossRef] [PubMed]
- Feng, H.; Hu, B.; Liu, K.W.; Li, Y.; Lu, X.; Cheng, T.; Yiin, J.J.; Lu, S.; Keezer, S.; Fenton, T.; et al. Activation of Rac1 by Src-dependent phosphorylation of Dock180(Y1811) mediates PDGFRα-stimulated glioma tumorigenesis in mice and humans. J. Clin. Investig. 2011, 121, 4670–4684. [Google Scholar] [CrossRef] [PubMed]
- Son, D.I.; Hong, S.; Shin, K.S.; Kang, S.J. PARP-1 regulates mouse embryonic neural stem cell proliferation by regulating PDGFRα expression. Biochem. Biophys Res. Commun. 2020, 526, 986–992. [Google Scholar] [CrossRef]
- Gui, B.; Gui, F.; Takai, T.; Feng, C.; Bai, X.; Fazli, L.; Dong, X.; Liu, S.; Zhang, X.; Zhang, W.; et al. Selective targeting of PARP-2 inhibits androgen receptor signaling and prostate cancer growth through disruption of FOXA1 function. Proc. Natl. Acad. Sci. USA 2019, 116, 14573–14582. [Google Scholar] [CrossRef] [PubMed]
- Carroll, J.S.; Liu, X.S.; Brodsky, A.S.; Li, W.; Meyer, C.A.; Szary, A.J.; Eeckhoute, J.; Shao, W.; Hestermann, E.V.; Geistlinger, T.R.; et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 2005, 122, 33–43. [Google Scholar] [CrossRef] [PubMed]
- Krueckl, S.L.; Sikes, R.A.; Edlund, N.M.; Bell, R.H.; Hurtado-Coll, A.; Fazli, L.; Gleave, M.E.; Cox, M.E. Increased insulin-like growth factor I receptor expression and signaling are components of androgen-independent progression in a lineage-derived prostate cancer progression model. Cancer Res. 2004, 64, 8620–8629. [Google Scholar] [CrossRef]
- Cohen-Armon, M. PARP-1 activation in the ERK signaling pathway. Trends Pharmacol. Sci. 2007, 28, 556–560. [Google Scholar] [CrossRef]
- Reed, S.M.; Quelle, D.E. p53 Acetylation: Regulation and Consequences. Cancers 2014, 7, 30–69. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Tavana, O.; Gu, W. p53 modifications: Exquisite decorations of the powerful guardian. J. Mol. Cell Biol. 2019, 11, 564–577. [Google Scholar] [CrossRef]
- Dai, C.; Gu, W. p53 post-translational modification: Deregulated in tumorigenesis. Trends Mol. Med. 2010, 16, 528–536. [Google Scholar] [CrossRef] [PubMed]
- Simbulan-Rosenthal, C.M.; Rosenthal, D.S.; Luo, R.B.; Samara, R.; Jung, M.; Dritschilo, A.; Spoonde, A.; Smulson, M.E. Poly(ADP-ribosyl)ation of p53 in vitro and in vivo modulates binding to its DNA consensus sequence. Neoplasia 2001, 3, 179–188. [Google Scholar] [CrossRef] [PubMed]
- Valenzuela, M.T.; Guerrero, R.; Núñez, M.I.; Ruiz De Almodóvar, J.M.; Sarker, M.; de Murcia, G.; Oliver, F.J. PARP-1 modifies the effectiveness of p53-mediated DNA damage response. Oncogene 2002, 21, 1108–1116. [Google Scholar] [CrossRef] [PubMed]
- Wieler, S.; Gagné, J.P.; Vaziri, H.; Poirier, G.G.; Benchimol, S. Poly(ADP-ribose) polymerase-1 is a positive regulator of the p53-mediated G1 arrest response following ionizing radiation. J. Biol. Chem. 2003, 278, 18914–18921. [Google Scholar] [CrossRef] [PubMed]
- Wesierska-Gadek, J.; Ranftler, C.; Schmid, G. Physiological ageing: Role of p53 and PARP-1 tumor suppressors in the regulation of terminal senescence. J. Physiol. Pharmacol. 2005, 56 (Suppl. 2), 77–88. [Google Scholar]
- Kanai, M.; Hanashiro, K.; Kim, S.H.; Hanai, S.; Boulares, A.H.; Miwa, M.; Fukasawa, K. Inhibition of Crm1-p53 interaction and nuclear export of p53 by poly(ADP-ribosyl)ation. Nat. Cell Biol. 2007, 9, 1175–1183. [Google Scholar] [CrossRef] [PubMed]
- Sizemore, S.T.; Mohammad, R.; Sizemore, G.M.; Nowsheen, S.; Yu, H.; Ostrowski, M.C.; Chakravarti, A.; Xia, F. Synthetic Lethality of PARP Inhibition and Ionizing Radiation is p53-dependent. Mol. Cancer Res. 2018, 16, 1092–1102. [Google Scholar] [CrossRef] [PubMed]
- Yamasaki, L. Role of the RB tumor suppressor in cancer. Cancer Treat. Res. 2003, 115, 209–239. [Google Scholar] [CrossRef]
- Simbulan-Rosenthal, C.M.; Rosenthal, D.S.; Luo, R.; Smulson, M.E. Poly(ADP-ribose) polymerase upregulates E2F-1 promoter activity and DNA pol alpha expression during early S phase. Oncogene 1999, 18, 5015–5023. [Google Scholar] [CrossRef] [PubMed]
- Pacini, A.; Quattrone, A.; Denegri, M.; Fiorillo, C.; Nediani, C.; Ramon y Cajal, S.; Nassi, P. Transcriptional down-regulation of poly(ADP-ribose) polymerase gene expression by E1A binding to pRb proteins protects murine keratinocytes from radiation-induced apoptosis. J. Biol. Chem. 1999, 274, 35107–35112. [Google Scholar] [CrossRef]
- Liu, H.; Knabb, J.R.; Spike, B.T.; Macleod, K.F. Elevated poly-(ADP-ribose)-polymerase activity sensitizes retinoblastoma-deficient cells to DNA damage-induced necrosis. Mol. Cancer Res. 2009, 7, 1099–1109. [Google Scholar] [CrossRef] [PubMed]
- Robaszkiewicz, A.; Wiśnik, E.; Regdon, Z.; Chmielewska, K.; Virág, L. PARP1 facilitates EP300 recruitment to the promoters of the subset of RBL2-dependent genes. Biochim. Biophys Acta Gene Regul. Mech. 2017. [Google Scholar] [CrossRef]
- Terzi, M.Y.; Izmirli, M.; Gogebakan, B. The cell fate: Senescence or quiescence. Mol. Biol. Rep. 2016, 43, 1213–1220. [Google Scholar] [CrossRef]
- Marescal, O.; Cheeseman, I.M. Cellular Mechanisms and Regulation of Quiescence. Dev. Cell 2020, 55, 259–271. [Google Scholar] [CrossRef] [PubMed]
- Efimova, E.V.; Mauceri, H.J.; Golden, D.W.; Labay, E.; Bindokas, V.P.; Darga, T.E.; Chakraborty, C.; Barreto-Andrade, J.C.; Crawley, C.; Sutton, H.G.; et al. Poly(ADP-ribose) polymerase inhibitor induces accelerated senescence in irradiated breast cancer cells and tumors. Cancer Res. 2010, 70, 6277–6282. [Google Scholar] [CrossRef] [PubMed]
- Alotaibi, M.; Sharma, K.; Saleh, T.; Povirk, L.F.; Hendrickson, E.A.; Gewirtz, D.A. Radiosensitization by PARP Inhibition in DNA Repair Proficient and Deficient Tumor Cells: Proliferative Recovery in Senescent Cells. Radiat. Res. 2016, 185, 229–245. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Gao, J.; Zhou, J.; Liu, H.; Xu, C. Olaparib induced senescence under P16 or P53 dependent manner in ovarian cancer. J. Gynecol. Oncol. 2019, 30, e26. [Google Scholar] [CrossRef] [PubMed]
- Fleury, H.; Malaquin, N.; Tu, V.; Gilbert, S.; Martinez, A.; Olivier, M.A.; Sauriol, A.; Communal, L.; Leclerc-Desaulniers, K.; Carmona, E.; et al. Exploiting interconnected synthetic lethal interactions between PARP inhibition and cancer cell reversible senescence. Nat. Commun. 2019, 10, 2556. [Google Scholar] [CrossRef] [PubMed]
- Zaniolo, K.; Rufiange, A.; Leclerc, S.; Desnoyers, S.; Guérin, S.L. Regulation of the poly(ADP-ribose) polymerase-1 gene expression by the transcription factors Sp1 and Sp3 is under the influence of cell density in primary cultured cells. Biochem. J. 2005, 389, 423–433. [Google Scholar] [CrossRef][Green Version]
- Bakondi, E.; Gönczi, M.; Szabó, E.; Bai, P.; Pacher, P.; Gergely, P.; Kovács, L.; Hunyadi, J.; Szabó, C.; Csernoch, L.; et al. Role of intracellular calcium mobilization and cell-density-dependent signaling in oxidative-stress-induced cytotoxicity in HaCaT keratinocytes. J. Investig. Dermatol. 2003, 121, 88–95. [Google Scholar] [CrossRef]
- Hamaoka, T.; Fujiwara, H.; Miura, T. T cell responses in the induction of immune resistance against syngeneic murine myelomas. Nihon Ketsueki Gakkai Zasshi 1978, 41, 1124–1133. [Google Scholar]
- Bakondi, E.; Bai, P.; Szabó, E.E.; Hunyadi, J.; Gergely, P.; Szabó, C.; Virág, L. Detection of poly(ADP-ribose) polymerase activation in oxidatively stressed cells and tissues using biotinylated NAD substrate. J. Histochem. Cytochem. 2002, 50, 91–98. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Zaniolo, K.; Gingras, M.E.; Audette, M.; Guérin, S.L. Expression of the gene encoding poly(ADP-ribose) polymerase-1 is modulated by fibronectin during corneal wound healing. Investig. Ophthalmol. Vis. Sci. 2006, 47, 4199–4210. [Google Scholar] [CrossRef] [PubMed]
- Bryant, H.E.; Schultz, N.; Thomas, H.D.; Parker, K.M.; Flower, D.; Lopez, E.; Kyle, S.; Meuth, M.; Curtin, N.J.; Helleday, T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434, 913–917. [Google Scholar] [CrossRef] [PubMed]
- Calabrese, C.R.; Almassy, R.; Barton, S.; Batey, M.A.; Calvert, A.H.; Canan-Koch, S.; Durkacz, B.W.; Hostomsky, Z.; Kumpf, R.A.; Kyle, S.; et al. Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J. Natl. Cancer Inst. 2004, 96, 56–67. [Google Scholar] [CrossRef] [PubMed]
- Tentori, L.; Leonetti, C.; Scarsella, M.; d’Amati, G.; Portarena, I.; Zupi, G.; Bonmassar, E.; Graziani, G. Combined treatment with temozolomide and poly(ADP-ribose) polymerase inhibitor enhances survival of mice bearing hematologic malignancy at the central nervous system site. Blood 2002, 99, 2241–2244. [Google Scholar] [CrossRef] [PubMed]
- Schlicker, A.; Peschke, P.; Bürkle, A.; Hahn, E.W.; Kim, J.H. 4-Amino-1,8-naphthalimide: A novel inhibitor of poly(ADP-ribose) polymerase and radiation sensitizer. Int. J. Radiat. Biol. 1999, 75, 91–100. [Google Scholar] [CrossRef] [PubMed]
- Soldatenkov, V.A.; Smulson, M. Poly(ADP-ribose) polymerase in DNA damage-response pathway: Implications for radiation oncology. Int. J. Cancer 2000, 90, 59–67. [Google Scholar] [CrossRef]
- Virág, L.; Szabó, C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 2002, 54, 375–429. [Google Scholar] [CrossRef] [PubMed]
- Curtin, N.J.; Szabo, C. Poly(ADP-ribose) polymerase inhibition: Past, present and future. Nat. Rev. Drug Discov. 2020, 19, 711–736. [Google Scholar] [CrossRef] [PubMed]
- Bey, E.A.; Bentle, M.S.; Reinicke, K.E.; Dong, Y.; Yang, C.R.; Girard, L.; Minna, J.D.; Bornmann, W.G.; Gao, J.; Boothman, D.A. An NQO1- and PARP-1-mediated cell death pathway induced in non-small-cell lung cancer cells by beta-lapachone. Proc. Natl. Acad. Sci. USA 2007, 104, 11832–11837. [Google Scholar] [CrossRef] [PubMed]
- Park, E.J.; Min, K.J.; Lee, T.J.; Yoo, Y.H.; Kim, Y.S.; Kwon, T.K. β-Lapachone induces programmed necrosis through the RIP1-PARP-AIF-dependent pathway in human hepatocellular carcinoma SK-Hep1 cells. Cell Death Dis. 2014, 5, e1230. [Google Scholar] [CrossRef] [PubMed]
- Virág, L.; Robaszkiewicz, A.; Rodriguez-Vargas, J.M.; Oliver, F.J. Poly(ADP-ribose) signaling in cell death. Mol. Asp. Med. 2013, 34, 1153–1167. [Google Scholar] [CrossRef] [PubMed]
- Bürkle, A.; Virág, L. Poly(ADP-ribose): PARadigms and PARadoxes. Mol. Asp. Med. 2013, 34, 1046–1065. [Google Scholar] [CrossRef]
- Chen, Y.; Chen, S.; Liang, H.; Yang, H.; Liu, L.; Zhou, K.; Xu, L.; Liu, J.; Yun, L.; Lai, B.; et al. Bcl-2 protects TK6 cells against hydroquinone-induced apoptosis through PARP-1 cytoplasm translocation and stabilizing mitochondrial membrane potential. Environ. Mol. Mutagen. 2018, 59, 49–59. [Google Scholar] [CrossRef]
- Xu, F.; Sun, Y.; Yang, S.Z.; Zhou, T.; Jhala, N.; McDonald, J.; Chen, Y. Cytoplasmic PARP-1 promotes pancreatic cancer tumorigenesis and resistance. Int. J. Cancer 2019, 145, 474–483. [Google Scholar] [CrossRef]
- Hassa, P.O.; Hottiger, M.O. A role of poly (ADP-ribose) polymerase in NF-kappaB transcriptional activation. Biol. Chem. 1999, 380, 953–959. [Google Scholar] [CrossRef]
- Oliver, F.J.; Ménissier-de Murcia, J.; Nacci, C.; Decker, P.; Andriantsitohaina, R.; Muller, S.; de la Rubia, G.; Stoclet, J.C.; de Murcia, G. Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J. 1999, 18, 4446–4454. [Google Scholar] [CrossRef] [PubMed]
- Mann, M.; Kumar, S.; Sharma, A.; Chauhan, S.S.; Bhatla, N.; Kumar, S.; Bakhshi, S.; Gupta, R.; Kumar, L. PARP-1 inhibitor modulate β-catenin signaling to enhance cisplatin sensitivity in cancer cervix. Oncotarget 2019, 10, 4262–4275. [Google Scholar] [CrossRef] [PubMed]
- Nakagawa, Y.; Sedukhina, A.S.; Okamoto, N.; Nagasawa, S.; Suzuki, N.; Ohta, T.; Hattori, H.; Roche-Molina, M.; Narváez, A.J.; Jeyasekharan, A.D.; et al. NF-κB signaling mediates acquired resistance after PARP inhibition. Oncotarget 2015, 6, 3825–3839. [Google Scholar] [CrossRef] [PubMed]
- Veres, B.; Gallyas, F., Jr.; Varbiro, G.; Berente, Z.; Osz, E.; Szekeres, G.; Szabo, C.; Sumegi, B. Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly-(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem. Pharmacol. 2003, 65, 1373–1382. [Google Scholar] [CrossRef]
- Tapodi, A.; Debreceni, B.; Hanto, K.; Bognar, Z.; Wittmann, I.; Gallyas, F., Jr.; Varbiro, G.; Sumegi, B. Pivotal role of Akt activation in mitochondrial protection and cell survival by poly(ADP-ribose)polymerase-1 inhibition in oxidative stress. J. Biol. Chem. 2005, 280, 35767–35775. [Google Scholar] [CrossRef]
- Gallyas, F., Jr.; Sumegi, B.; Szabo, C. Role of Akt Activation in PARP Inhibitor Resistance in Cancer. Cancers 2020, 12, 532. [Google Scholar] [CrossRef] [PubMed]
- Szanto, A.; Hellebrand, E.E.; Bognar, Z.; Tucsek, Z.; Szabo, A.; Gallyas, F., Jr.; Sumegi, B.; Varbiro, G. PARP-1 inhibition-induced activation of PI-3-kinase-Akt pathway promotes resistance to taxol. Biochem. Pharmacol. 2009, 77, 1348–1357. [Google Scholar] [CrossRef]
- Kovacs, K.; Vaczy, A.; Fekete, K.; Kovari, P.; Atlasz, T.; Reglodi, D.; Gabriel, R.; Gallyas, F.; Sumegi, B. PARP Inhibitor Protects Against Chronic Hypoxia/Reoxygenation-Induced Retinal Injury by Regulation of MAPKs, HIF1α, Nrf2, and NFκB. Investig. Ophthalmol. Vis. Sci. 2019, 60, 1478–1490. [Google Scholar] [CrossRef] [PubMed]
- Hegedűs, C.; Kovács, K.; Polgár, Z.; Regdon, Z.; Szabó, É.; Robaszkiewicz, A.; Forman, H.J.; Martner, A.; Virág, L. Redox control of cancer cell destruction. Redox Biol. 2018, 16, 59–74. [Google Scholar] [CrossRef] [PubMed]
- Montero, J.; Dutta, C.; van Bodegom, D.; Weinstock, D.; Letai, A. p53 regulates a non-apoptotic death induced by ROS. Cell Death Differ. 2013, 20, 1465–1474. [Google Scholar] [CrossRef] [PubMed]
- Galluzzi, L.; Pietrocola, F.; Bravo-San Pedro, J.M.; Amaravadi, R.K.; Baehrecke, E.H.; Cecconi, F.; Codogno, P.; Debnath, J.; Gewirtz, D.A.; Karantza, V.; et al. Autophagy in malignant transformation and cancer progression. EMBO J. 2015, 34, 856–880. [Google Scholar] [CrossRef]
- Chen, Z.T.; Zhao, W.; Qu, S.; Li, L.; Lu, X.D.; Su, F.; Liang, Z.G.; Guo, S.Y.; Zhu, X.D. PARP-1 promotes autophagy via the AMPK/mTOR pathway in CNE-2 human nasopharyngeal carcinoma cells following ionizing radiation, while inhibition of autophagy contributes to the radiation sensitization of CNE-2 cells. Mol. Med. Rep. 2015, 12, 1868–1876. [Google Scholar] [CrossRef]
- Rodríguez-Vargas, J.M.; Ruiz-Magaña, M.J.; Ruiz-Ruiz, C.; Majuelos-Melguizo, J.; Peralta-Leal, A.; Rodríguez, M.I.; Muñoz-Gámez, J.A.; de Almodóvar, M.R.; Siles, E.; Rivas, A.L.; et al. ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy. Cell Res. 2012, 22, 1181–1198. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Vargas, J.M.; Rodríguez, M.I.; Majuelos-Melguizo, J.; García-Diaz, Á.; González-Flores, A.; López-Rivas, A.; Virág, L.; Illuzzi, G.; Schreiber, V.; Dantzer, F.; et al. Autophagy requiRes. poly(adp-ribosyl)ation-dependent AMPK nuclear export. Cell Death Differ. 2016, 23, 2007–2018. [Google Scholar] [CrossRef]
- Ji, Y.; Wang, Q.; Zhao, Q.; Zhao, S.; Li, L.; Sun, G.; Ye, L. Autophagy suppression enhances DNA damage and cell death upon treatment with PARP inhibitor Niraparib in laryngeal squamous cell carcinoma. Appl. MicroBiol. Biotechnol. 2019, 103, 9557–9568. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.; Hou, Y.; Zhu, L.; Wang, Z.; Chen, G.; Shu, C.; Liu, Y. Veliparib overcomes multidrug resistance in liver cancer cells. Biochem. Biophys. Res. Commun. 2020, 521, 596–602. [Google Scholar] [CrossRef] [PubMed]
- Wesierska-Gadek, J. Major contribution of the multidrug transporter P-glycoprotein to reduced susceptibility of poly(ADP-ribose) polymerase-1 knock-out cells to doxorubicin action. J. Cell Biochem. 2005, 95, 1012–1028. [Google Scholar] [CrossRef]
- Richardson, D.S.; Allen, P.D.; Kelsey, S.M.; Newland, A.C. Effects of PARP inhibition on drug and Fas-induced apoptosis in leukaemic cells. Adv. Exp. Med. Biol. 1999, 457, 267–279. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Klaus, J.A.; Zhang, J.; Xu, Z.; Kibler, K.K.; Andrabi, S.A.; Rao, K.; Yang, Z.J.; Dawson, T.M.; Dawson, V.L.; et al. Contributions of poly(ADP-ribose) polymerase-1 and -2 to nuclear translocation of apoptosis-inducing factor and injury from focal cerebral ischemia. J. NeuroChem. 2010, 113, 1012–1022. [Google Scholar] [CrossRef] [PubMed]
- Bai, P.; Canto, C.; Brunyánszki, A.; Huber, A.; Szántó, M.; Cen, Y.; Yamamoto, H.; Houten, S.M.; Kiss, B.; Oudart, H.; et al. PARP-2 regulates SIRT1 expression and whole-body energy expenditure. Cell Metab. 2011, 13, 450–460. [Google Scholar] [CrossRef] [PubMed]
- Jankó, L.; Sári, Z.; Kovács, T.; Kis, G.; Szántó, M.; Antal, M.; Juhász, G.; Bai, P. Silencing of PARP2 Blocks Autophagic Degradation. Cells 2020, 9, 380. [Google Scholar] [CrossRef] [PubMed]
- Wu, J.; He, G.T.; Zhang, W.J.; Xu, J.; Huang, Q.B. IRE1α Signaling Pathways Involved in Mammalian Cell Fate Determination. Cell Physiol. Biochem. 2016, 38, 847–858. [Google Scholar] [CrossRef] [PubMed]
- Jaud, M.; Philippe, C.; Di Bella, D.; Tang, W.; Pyronnet, S.; Laurell, H.; Mazzolini, L.; Rouault-Pierre, K.; Touriol, C. Translational Regulations in Response to Endoplasmic Reticulum Stress in Cancers. Cells 2020, 9, 540. [Google Scholar] [CrossRef]
- Wright, W.E.; Shay, J.W. The two-stage mechanism controlling cellular senescence and immortalization. Exp. Gerontol. 1992, 27, 383–389. [Google Scholar] [CrossRef]
- d’Adda di Fagagna, F. Living on a break: Cellular senescence as a DNA-damage response. Nat. Rev. Cancer 2008, 8, 512–522. [Google Scholar] [CrossRef]
- de Lange, T. Shelterin-Mediated Telomere Protection. Annu. Rev. Genet. 2018, 52, 223–247. [Google Scholar] [CrossRef] [PubMed]
- Dilley, R.L.; Greenberg, R.A. ALTernative Telomere Maintenance and Cancer. Trends Cancer 2015, 1, 145–156. [Google Scholar] [CrossRef] [PubMed]
- Yuan, X.; Larsson, C.; Xu, D. Mechanisms underlying the activation of TERT transcription and telomerase activity in human cancer: Old actors and new players. Oncogene 2019, 38, 6172–6183. [Google Scholar] [CrossRef] [PubMed]
- Seimiya, H. Crossroads of telomere biology and anticancer drug discovery. Cancer Sci. 2020, 111, 3089–3099. [Google Scholar] [CrossRef]
- Reddel, R.R.; Bryan, T.M.; Colgin, L.M.; Perrem, K.T.; Yeager, T.R. Alternative lengthening of telomeRes. in human cells. Radiat. Res. 2001, 155, 194–200. [Google Scholar] [CrossRef]
- Gomez, M.; Wu, J.; Schreiber, V.; Dunlap, J.; Dantzer, F.; Wang, Y.; Liu, Y. PARP1 Is a TRF2-associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol. Biol. Cell 2006, 17, 1686–1696. [Google Scholar] [CrossRef] [PubMed]
- Doksani, Y. The Response to DNA Damage at Telomeric Repeats and Its Consequences for Telomere Function. Genes 2019, 10, 318. [Google Scholar] [CrossRef] [PubMed]
- Feuerhahn, S.; Chen, L.Y.; Luke, B.; Porro, A. No DDRama at chromosome ends: TRF2 takes centre stage. Trends Biochem. Sci. 2015, 40, 275–285. [Google Scholar] [CrossRef] [PubMed]
- Schmutz, I.; Timashev, L.; Xie, W.; Patel, D.J.; de Lange, T. TRF2 binds branched DNA to safeguard telomere integrity. Nat. Struct. Mol. Biol. 2017, 24, 734–742. [Google Scholar] [CrossRef] [PubMed]
- Nora, G.J.; Buncher, N.A.; Opresko, P.L. Telomeric protein TRF2 protects Holliday junctions with telomeric arms from displacement by the Werner syndrome helicase. Nucleic Acids Res. 2010, 38, 3984–3998. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Dantzer, F.; Giraud-Panis, M.J.; Jaco, I.; Amé, J.C.; Schultz, I.; Blasco, M.; Koering, C.E.; Gilson, E.; Ménissier-de Murcia, J.; de Murcia, G.; et al. Functional interaction between poly(ADP-Ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol. Cell Biol. 2004, 24, 1595–1607. [Google Scholar] [CrossRef] [PubMed]
- Tahara, H.; Shin-Ya, K.; Seimiya, H.; Yamada, H.; Tsuruo, T.; Ide, T. G-Quadruplex stabilization by telomestatin induces TRF2 protein dissociation from telomeRes. and anaphase bridge formation accompanied by loss of the 3′ telomeric overhang in cancer cells. Oncogene 2006, 25, 1955–1966. [Google Scholar] [CrossRef] [PubMed]
- Gomez, D.; Wenner, T.; Brassart, B.; Douarre, C.; O’Donohue, M.F.; El Khoury, V.; Shin-Ya, K.; Morjani, H.; Trentesaux, C.; Riou, J.F. Telomestatin-induced telomere uncapping is modulated by POT1 through G-overhang extension in HT1080 human tumor cells. J. Biol. Chem. 2006, 281, 38721–38729. [Google Scholar] [CrossRef] [PubMed]
- Salvati, E.; Scarsella, M.; Porru, M.; Rizzo, A.; Iachettini, S.; Tentori, L.; Graziani, G.; D’Incalci, M.; Stevens, M.F.; Orlandi, A.; et al. PARP1 is activated at telomeRes. upon G4 stabilization: Possible target for telomere-based therapy. Oncogene 2010, 29, 6280–6293. [Google Scholar] [CrossRef]
- Ménissier de Murcia, J.; Ricoul, M.; Tartier, L.; Niedergang, C.; Huber, A.; Dantzer, F.; Schreiber, V.; Amé, J.C.; Dierich, A.; LeMeur, M.; et al. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 2003, 22, 2255–2263. [Google Scholar] [CrossRef] [PubMed]
- Amé, J.C.; Fouquerel, E.; Gauthier, L.R.; Biard, D.; Boussin, F.D.; Dantzer, F.; de Murcia, G.; Schreiber, V. Radiation-induced mitotic catastrophe in PARG-deficient cells. J. Cell Sci. 2009, 122, 1990–2002. [Google Scholar] [CrossRef]
- Hsieh, M.H.; Chen, Y.T.; Chen, Y.T.; Lee, Y.H.; Lu, J.; Chien, C.L.; Chen, H.F.; Ho, H.N.; Yu, C.J.; Wang, Z.Q.; et al. PARP1 controls KLF4-mediated telomerase expression in stem cells and cancer cells. Nucleic Acids Res. 2017, 45, 10492–10503. [Google Scholar] [CrossRef]
- d’Adda di Fagagna, F.; Hande, M.P.; Tong, W.M.; Lansdorp, P.M.; Wang, Z.Q.; Jackson, S.P. Functions of poly(ADP-ribose) polymerase in controlling telomere length and chromosomal stability. Nat. Genet. 1999, 23, 76–80. [Google Scholar] [CrossRef] [PubMed]
- El Ramy, R.; Magroun, N.; Messadecq, N.; Gauthier, L.R.; Boussin, F.D.; Kolthur-Seetharam, U.; Schreiber, V.; McBurney, M.W.; Sassone-Corsi, P.; Dantzer, F. Functional interplay between Parp-1 and SirT1 in genome integrity and chromatin-based processes. Cell Mol. Life Sci. 2009, 66, 3219–3234. [Google Scholar] [CrossRef] [PubMed]
- Beneke, S.; Cohausz, O.; Malanga, M.; Boukamp, P.; Althaus, F.; Bürkle, A. Rapid regulation of telomere length is mediated by poly(ADP-ribose) polymerase-1. Nucleic Acids Res. 2008, 36, 6309–6317. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, U.; Das, N.; Bhattacharyya, N.P. Inhibition of telomerase activity by reduction of poly(ADP-ribosyl)ation of TERT and TEP1/TP1 expression in HeLa cells with knocked down poly(ADP-ribose) polymerase-1 (PARP-1) gene. Mutat. Res. 2007, 615, 66–74. [Google Scholar] [CrossRef] [PubMed]
- Smith, S.; Giriat, I.; Schmitt, A.; de Lange, T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 1998, 282, 1484–1487. [Google Scholar] [CrossRef]
- Kaminker, P.G.; Kim, S.H.; Taylor, R.D.; Zebarjadian, Y.; Funk, W.D.; Morin, G.B.; Yaswen, P.; Campisi, J. TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J. Biol. Chem. 2001, 276, 35891–35899. [Google Scholar] [CrossRef] [PubMed]
- Hsiao, S.J.; Poitras, M.F.; Cook, B.D.; Liu, Y.; Smith, S. Tankyrase 2 poly(ADP-ribose) polymerase domain-deleted mice exhibit growth defects but have normal telomere length and capping. Mol. Cell Biol. 2006, 26, 2044–2054. [Google Scholar] [CrossRef]
- Cook, B.D.; Dynek, J.N.; Chang, W.; Shostak, G.; Smith, S. Role for the related poly(ADP-Ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell Biol. 2002, 22, 332–342. [Google Scholar] [CrossRef]
- Sbodio, J.I.; Lodish, H.F.; Chi, N.W. Tankyrase-2 oligomerizes with tankyrase-1 and binds to both TRF1 (telomere-repeat-binding factor 1) and IRAP (insulin-responsive aminopeptidase). Biochem. J. 2002, 361, 451–459. [Google Scholar] [CrossRef]
- Chang, W.; Dynek, J.N.; Smith, S. TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres. Genes Dev. 2003, 17, 1328–1333. [Google Scholar] [CrossRef]
- Donigian, J.R.; de Lange, T. The role of the poly(ADP-ribose) polymerase tankyrase1 in telomere length control by the TRF1 component of the shelterin complex. J. Biol. Chem. 2007, 282, 22662–22667. [Google Scholar] [CrossRef] [PubMed]
- Ye, J.Z.; de Lange, T. TIN2 is a tankyrase 1 PARP modulator in the TRF1 telomere length control complex. Nat. Genet. 2004, 36, 618–623. [Google Scholar] [CrossRef]
- Yamada, M.; Tsuji, N.; Nakamura, M.; Moriai, R.; Kobayashi, D.; Yagihashi, A.; Watanabe, N. Down-regulation of TRF1, TRF2 and TIN2 genes is important to maintain telomeric DNA for gastric cancers. Anticancer Res. 2002, 22, 3303–3307. [Google Scholar]
- Liu, Y.; Snow, B.E.; Kickhoefer, V.A.; Erdmann, N.; Zhou, W.; Wakeham, A.; Gomez, M.; Rome, L.H.; Harrington, L. Vault poly(ADP-ribose) polymerase is associated with mammalian telomerase and is dispensable for telomerase function and vault structure in vivo. Mol. Cell Biol. 2004, 24, 5314–5323. [Google Scholar] [CrossRef]
- Plummer, R.; Dua, D.; Cresti, N.; Drew, Y.; Stephens, P.; Foegh, M.; Knudsen, S.; Sachdev, P.; Mistry, B.M.; Dixit, V.; et al. First-in-human study of the PARP/tankyrase inhibitor E7449 in patients with advanced solid tumours and evaluation of a novel drug-response predictor. Br. J. Cancer 2020, 123, 525–533. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Yang, M.H.; Zhao, J.J.; Chen, L.; Yu, S.T.; Tang, X.D.; Fang, D.C.; Yang, S.M. Inhibition of tankyrase 1 in human gastric cancer cells enhances telomere shortening by telomerase inhibitors. Oncol. Rep. 2010, 24, 1059–1065. [Google Scholar] [CrossRef][Green Version]
- Seimiya, H.; Muramatsu, Y.; Ohishi, T.; Tsuruo, T. Tankyrase 1 as a target for telomere-directed molecular cancer therapeutics. Cancer Cell 2005, 7, 25–37. [Google Scholar] [CrossRef]
- Fernández-Marcelo, T.; Frías, C.; Pascua, I.; de Juan, C.; Head, J.; Gómez, A.; Hernando, F.; Jarabo, J.R.; Díaz-Rubio, E.; Torres, A.J.; et al. Poly (ADP-ribose) polymerase 3 (PARP3), a potential repressor of telomerase activity. J. Exp. Clin. Cancer Res. 2014, 33, 19. [Google Scholar] [CrossRef] [PubMed]
- Frías, C.; García-Aranda, C.; De Juan, C.; Morán, A.; Ortega, P.; Gómez, A.; Hernando, F.; López-Asenjo, J.A.; Torres, A.J.; Benito, M.; et al. Telomere shortening is associated with poor prognosis and telomerase activity correlates with DNA repair impairment in non-small cell lung cancer. Lung Cancer 2008, 60, 416–425. [Google Scholar] [CrossRef] [PubMed]
- Boehler, C.; Dantzer, F. PARP-3, a DNA-dependent PARP with emerging roles in double-strand break repair and mitotic progression. Cell Cycle 2011, 10, 1023–1024. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Fernández-Marcelo, T.; Gómez, A.; Pascua, I.; de Juan, C.; Head, J.; Hernando, F.; Jarabo, J.R.; Calatayud, J.; Torres-García, A.J.; Iniesta, P. Telomere length and telomerase activity in non-small cell lung cancer prognosis: Clinical usefulness of a specific telomere status. J. Exp. Clin. Cancer Res. 2015, 34, 78. [Google Scholar] [CrossRef] [PubMed]
- Loeb, L.A. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 1991, 51, 3075–3079. [Google Scholar] [PubMed]
- Loeb, L.A.; Springgate, C.F.; Battula, N. Errors in DNA replication as a basis of malignant changes. Cancer Res. 1974, 34, 2311–2321. [Google Scholar] [PubMed]
- Nowell, P.C. The clonal evolution of tumor cell populations. Science 1976, 194, 23–28. [Google Scholar] [CrossRef] [PubMed]
- Kinzler, K.W.; Vogelstein, B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 1997, 386, 761, 763. [Google Scholar] [CrossRef] [PubMed]
- Langelier, M.F.; Riccio, A.A.; Pascal, J.M. PARP-2 and PARP-3 are selectively activated by 5′ phosphorylated DNA breaks through an allosteric regulatory mechanism shared with PARP-1. Nucleic Acids Res. 2014, 42, 7762–7775. [Google Scholar] [CrossRef]
- Aleksandrov, R.; Dotchev, A.; Poser, I.; Krastev, D.; Georgiev, G.; Panova, G.; Babukov, Y.; Danovski, G.; Dyankova, T.; Hubatsch, L.; et al. Protein Dynamics in Complex DNA Lesions. Mol. Cell 2018, 69, 1046–1061.e1045. [Google Scholar] [CrossRef]
- Caron, M.C.; Sharma, A.K.; O’Sullivan, J.; Myler, L.R.; Ferreira, M.T.; Rodrigue, A.; Coulombe, Y.; Ethier, C.; Gagné, J.P.; Langelier, M.F.; et al. Poly(ADP-ribose) polymerase-1 antagonizes DNA resection at double-strand breaks. Nat. Commun. 2019, 10, 2954. [Google Scholar] [CrossRef] [PubMed]
- Yang, G.; Liu, C.; Chen, S.H.; Kassab, M.A.; Hoff, J.D.; Walter, N.G.; Yu, X. Super-resolution imaging identifies PARP1 and the Ku complex acting as DNA double-strand break sensors. Nucleic Acids Res. 2018, 46, 3446–3457. [Google Scholar] [CrossRef] [PubMed]
- Hochegger, H.; Dejsuphong, D.; Fukushima, T.; Morrison, C.; Sonoda, E.; Schreiber, V.; Zhao, G.Y.; Saberi, A.; Masutani, M.; Adachi, N.; et al. Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J. 2006, 25, 1305–1314. [Google Scholar] [CrossRef] [PubMed]
- Haince, J.F.; McDonald, D.; Rodrigue, A.; Déry, U.; Masson, J.Y.; Hendzel, M.J.; Poirier, G.G. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem. 2008, 283, 1197–1208. [Google Scholar] [CrossRef]
- Krietsch, J.; Caron, M.C.; Gagné, J.P.; Ethier, C.; Vignard, J.; Vincent, M.; Rouleau, M.; Hendzel, M.J.; Poirier, G.G.; Masson, J.Y. PARP activation regulates the RNA-binding protein NONO in the DNA damage response to DNA double-strand breaks. Nucleic Acids Res. 2012, 40, 10287–10301. [Google Scholar] [CrossRef] [PubMed]
- Caron, P.; Polo, S.E. Reshaping Chromatin Architecture around DNA Breaks. Trends Biochem. Sci. 2020, 45, 177–179. [Google Scholar] [CrossRef] [PubMed]
- Coleman, K.A.; Greenberg, R.A. The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J. Biol. Chem. 2011, 286, 13669–13680. [Google Scholar] [CrossRef] [PubMed]
- Hu, Y.; Petit, S.A.; Ficarro, S.B.; Toomire, K.J.; Xie, A.; Lim, E.; Cao, S.A.; Park, E.; Eck, M.J.; Scully, R.; et al. PARP1-driven poly-ADP-ribosylation regulates BRCA1 function in homologous recombination-mediated DNA repair. Cancer Discov. 2014, 4, 1430–1447. [Google Scholar] [CrossRef] [PubMed]
- Boehler, C.; Gauthier, L.R.; Mortusewicz, O.; Biard, D.S.; Saliou, J.M.; Bresson, A.; Sanglier-Cianferani, S.; Smith, S.; Schreiber, V.; Boussin, F.; et al. Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc. Natl. Acad. Sci. USA 2011, 108, 2783–2788. [Google Scholar] [CrossRef] [PubMed]
- Rulten, S.L.; Fisher, A.E.; Robert, I.; Zuma, M.C.; Rouleau, M.; Ju, L.; Poirier, G.; Reina-San-Martin, B.; Caldecott, K.W. PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell 2011, 41, 33–45. [Google Scholar] [CrossRef] [PubMed]
- Fouquin, A.; Guirouilh-Barbat, J.; Lopez, B.; Hall, J.; Amor-Guéret, M.; Pennaneach, V. PARP2 controls double-strand break repair pathway choice by limiting 53BP1 accumulation at DNA damage sites and promoting end-resection. Nucleic Acids Res. 2017, 45, 12325–12339. [Google Scholar] [CrossRef]
- Nagy, Z.; Kalousi, A.; Furst, A.; Koch, M.; Fischer, B.; Soutoglou, E. Tankyrases Promote Homologous Recombination and Check Point Activation in Response to DSBs. PLoS Genet. 2016, 12, e1005791. [Google Scholar] [CrossRef] [PubMed]
- Vodenicharov, M.D.; Ghodgaonkar, M.M.; Halappanavar, S.S.; Shah, R.G.; Shah, G.M. Mechanism of early biphasic activation of poly(ADP-ribose) polymerase-1 in response to ultraviolet B radiation. J. Cell Sci. 2005, 118, 589–599. [Google Scholar] [CrossRef] [PubMed]
- Robu, M.; Shah, R.G.; Petitclerc, N.; Brind’Amour, J.; Kandan-Kulangara, F.; Shah, G.M. Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc. Natl. Acad. Sci. USA 2013, 110, 1658–1663. [Google Scholar] [CrossRef]
- Robu, M.; Shah, R.G.; Purohit, N.K.; Zhou, P.; Naegeli, H.; Shah, G.M. Poly(ADP-ribose) polymerase 1 escorts XPC to UV-induced DNA lesions during nucleotide excision repair. Proc. Natl. Acad. Sci. USA 2017, 114, E6847–E6856. [Google Scholar] [CrossRef]
- King, B.S.; Cooper, K.L.; Liu, K.J.; Hudson, L.G. Poly(ADP-ribose) contributes to an association between poly(ADP-ribose) polymerase-1 and xeroderma pigmentosum complementation group A in nucleotide excision repair. J. Biol. Chem. 2012, 287, 39824–39833. [Google Scholar] [CrossRef] [PubMed]
- Fischer, J.M.; Popp, O.; Gebhard, D.; Veith, S.; Fischbach, A.; Beneke, S.; Leitenstorfer, A.; Bergemann, J.; Scheffner, M.; Ferrando-May, E.; et al. Poly(ADP-ribose)-mediated interplay of XPA and PARP1 leads to reciprocal regulation of protein function. FEBS J. 2014, 281, 3625–3641. [Google Scholar] [CrossRef] [PubMed]
- Maltseva, E.A.; Krasikova, Y.S.; Sukhanova, M.V.; Rechkunova, N.I.; Lavrik, O.I. Replication protein A as a modulator of the poly(ADP-ribose)polymerase 1 activity. DNA Repair (Amst.) 2018, 72, 28–38. [Google Scholar] [CrossRef] [PubMed]
- Epstein, J.H.; Cleaver, J.E. 3-Aminobenzamide can act as a cocarcinogen for ultraviolet light-induced carcinogenesis in mouse skin. Cancer Res. 1992, 52, 4053–4054. [Google Scholar]
- Caldecott, K.W. Mammalian DNA base excision repair: Dancing in the moonlight. DNA Repair (Amst.) 2020, 93, 102921. [Google Scholar] [CrossRef] [PubMed]
- Das, B.B.; Huang, S.Y.; Murai, J.; Rehman, I.; Amé, J.C.; Sengupta, S.; Das, S.K.; Majumdar, P.; Zhang, H.; Biard, D.; et al. PARP1-TDP1 coupling for the repair of topoisomerase I-induced DNA damage. Nucleic Acids Res. 2014, 42, 4435–4449. [Google Scholar] [CrossRef]
- Fisher, A.E.; Hochegger, H.; Takeda, S.; Caldecott, K.W. Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol. Cell Biol. 2007, 27, 5597–5605. [Google Scholar] [CrossRef] [PubMed]
- Dantzer, F.; de La Rubia, G.; Ménissier-De Murcia, J.; Hostomsky, Z.; de Murcia, G.; Schreiber, V. Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry 2000, 39, 7559–7569. [Google Scholar] [CrossRef] [PubMed]
- Lavrik, O.I.; Prasad, R.; Sobol, R.W.; Horton, J.K.; Ackerman, E.J.; Wilson, S.H. Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair. J. Biol. Chem. 2001, 276, 25541–25548. [Google Scholar] [CrossRef] [PubMed]
- Prasad, R.; Lavrik, O.I.; Kim, S.J.; Kedar, P.; Yang, X.P.; Vande Berg, B.J.; Wilson, S.H. DNA polymerase beta-mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis. J. Biol. Chem. 2001, 276, 32411–32414. [Google Scholar] [CrossRef] [PubMed]
- Lavrik, O.I. PARPs’ impact on base excision DNA repair. DNA Repair (Amst.) 2020, 93, 102911. [Google Scholar] [CrossRef] [PubMed]
- Schreiber, V.; Amé, J.C.; Dollé, P.; Schultz, I.; Rinaldi, B.; Fraulob, V.; Ménissier-de Murcia, J.; de Murcia, G. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem. 2002, 277, 23028–23036. [Google Scholar] [CrossRef] [PubMed]
- Ali, R.; Alabdullah, M.; Alblihy, A.; Miligy, I.; Mesquita, K.A.; Chan, S.Y.; Moseley, P.; Rakha, E.A.; Madhusudan, S. PARP1 blockade is synthetically lethal in XRCC1 deficient sporadic epithelial ovarian cancers. Cancer Lett. 2020, 469, 124–133. [Google Scholar] [CrossRef] [PubMed]
- Ali, R.; Al-Kawaz, A.; Toss, M.S.; Green, A.R.; Miligy, I.M.; Mesquita, K.A.; Seedhouse, C.; Mirza, S.; Band, V.; Rakha, E.A.; et al. Targeting PARP1 in XRCC1-Deficient Sporadic Invasive Breast Cancer or Preinvasive Ductal Carcinoma In Situ Induces Synthetic Lethality and Chemoprevention. Cancer Res. 2018, 78, 6818–6827. [Google Scholar] [CrossRef] [PubMed]
- Ronson, G.E.; Piberger, A.L.; Higgs, M.R.; Olsen, A.L.; Stewart, G.S.; McHugh, P.J.; Petermann, E.; Lakin, N.D. PARP1 and PARP2 stabilise replication forks at base excision repair intermediates through Fbh1-dependent Rad51 regulation. Nat. Commun. 2018, 9, 746. [Google Scholar] [CrossRef]
- Yang, L.; Sun, L.; Teng, Y.; Chen, H.; Gao, Y.; Levine, A.S.; Nakajima, S.; Lan, L. Tankyrase1-mediated poly(ADP-ribosyl)ation of TRF1 maintains cell survival after telomeric DNA damage. Nucleic Acids Res. 2017, 45, 3906–3921. [Google Scholar] [CrossRef]
- Berti, M.; Ray Chaudhuri, A.; Thangavel, S.; Gomathinayagam, S.; Kenig, S.; Vujanovic, M.; Odreman, F.; Glatter, T.; Graziano, S.; Mendoza-Maldonado, R.; et al. Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nat. Struct. Mol. Biol. 2013, 20, 347–354. [Google Scholar] [CrossRef]
- Bhat, K.P.; Cortez, D. RPA and RAD51: Fork reversal, fork protection, and genome stability. Nat. Struct. Mol. Biol. 2018, 25, 446–453. [Google Scholar] [CrossRef]
- Ying, S.; Hamdy, F.C.; Helleday, T. Mre11-dependent degradation of stalled DNA replication forks is prevented by BRCA2 and PARP1. Cancer Res. 2012, 72, 2814–2821. [Google Scholar] [CrossRef]
- Bryant, H.E.; Petermann, E.; Schultz, N.; Jemth, A.S.; Loseva, O.; Issaeva, N.; Johansson, F.; Fernandez, S.; McGlynn, P.; Helleday, T. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. Embo J. 2009, 28, 2601–2615. [Google Scholar] [CrossRef] [PubMed]
- Lemaçon, D.; Jackson, J.; Quinet, A.; Brickner, J.R.; Li, S.; Yazinski, S.; You, Z.; Ira, G.; Zou, L.; Mosammaparast, N.; et al. MRE11 and EXO1 nucleases degrade reversed forks and elicit MUS81-dependent fork rescue in BRCA2-deficient cells. Nat. Commun. 2017, 8, 860. [Google Scholar] [CrossRef]
- Li, M.; Bian, C.; Yu, X. Poly(ADP-ribosyl)ation is recognized by ECT2 during mitosis. Cell Cycle 2014, 13, 2944–2951. [Google Scholar] [CrossRef][Green Version]
- Saxena, A.; Wong, L.H.; Kalitsis, P.; Earle, E.; Shaffer, L.G.; Choo, K.H. Poly(ADP-ribose) polymerase 2 localizes to mammalian active centromeRes. and interacts with PARP-1, Cenpa, Cenpb and Bub3, but not Cenpc. Hum. Mol. Genet. 2002, 11, 2319–2329. [Google Scholar] [CrossRef] [PubMed]
- Saxena, A.; Saffery, R.; Wong, L.H.; Kalitsis, P.; Choo, K.H. Centromere proteins Cenpa, Cenpb, and Bub3 interact with poly(ADP-ribose) polymerase-1 protein and are poly(ADP-ribosyl)ated. J. Biol. Chem. 2002, 277, 26921–26926. [Google Scholar] [CrossRef]
- Pavlova, N.N.; Thompson, C.B. The Emerging Hallmarks of Cancer Metabolism. Cell Metab. 2016, 23, 27–47. [Google Scholar] [CrossRef] [PubMed]
- Pezzuto, A.; Carico, E. Role of HIF-1 in Cancer Progression: Novel Insights. A Review. Curr. Mol. Med. 2018, 18, 343–351. [Google Scholar] [CrossRef]
- Iyer, N.V.; Kotch, L.E.; Agani, F.; Leung, S.W.; Laughner, E.; Wenger, R.H.; Gassmann, M.; Gearhart, J.D.; Lawler, A.M.; Yu, A.Y.; et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 1998, 12, 149–162. [Google Scholar] [CrossRef]
- Kim, J.W.; Tchernyshyov, I.; Semenza, G.L.; Dang, C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: A metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3, 177–185. [Google Scholar] [CrossRef] [PubMed]
- Papandreou, I.; Cairns, R.A.; Fontana, L.; Lim, A.L.; Denko, N.C. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 2006, 3, 187–197. [Google Scholar] [CrossRef]
- Du, L.; Zhang, X.; Han, Y.Y.; Burke, N.A.; Kochanek, P.M.; Watkins, S.C.; Graham, S.H.; Carcillo, J.A.; Szabó, C.; Clark, R.S. Intra-mitochondrial poly(ADP-ribosylation) contributes to NAD+ depletion and cell death induced by oxidative stress. J. Biol. Chem. 2003, 278, 18426–18433. [Google Scholar] [CrossRef] [PubMed]
- Elser, M.; Borsig, L.; Hassa, P.O.; Erener, S.; Messner, S.; Valovka, T.; Keller, S.; Gassmann, M.; Hottiger, M.O. Poly(ADP-ribose) polymerase 1 promotes tumor cell survival by coactivating hypoxia-inducible factor-1-dependent gene expression. Mol. Cancer Res. 2008, 6, 282–290. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez-Flores, A.; Aguilar-Quesada, R.; Siles, E.; Pozo, S.; Rodríguez-Lara, M.I.; López-Jiménez, L.; López-Rodríguez, M.; Peralta-Leal, A.; Villar, D.; Martín-Oliva, D.; et al. Interaction between PARP-1 and HIF-2α in the hypoxic response. Oncogene 2014, 33, 891–898. [Google Scholar] [CrossRef]
- Feijs, K.L.; Kleine, H.; Braczynski, A.; Forst, A.H.; Herzog, N.; Verheugd, P.; Linzen, U.; Kremmer, E.; Lüscher, B. ARTD10 substrate identification on protein microarrays: Regulation of GSK3β by mono-ADP-ribosylation. Cell Commun. Signal. 2013, 11, 5. [Google Scholar] [CrossRef] [PubMed]
- Larsen, S.C.; Hendriks, I.A.; Lyon, D.; Jensen, L.J.; Nielsen, M.L. Systems-wide Analysis of Serine ADP-Ribosylation Reveals Widespread Occurrence and Site-Specific Overlap with Phosphorylation. Cell Rep. 2018, 24, 2493–2505.e2494. [Google Scholar] [CrossRef]
- Gagné, J.P.; Isabelle, M.; Lo, K.S.; Bourassa, S.; Hendzel, M.J.; Dawson, V.L.; Dawson, T.M.; Poirier, G.G. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 2008, 36, 6959–6976. [Google Scholar] [CrossRef]
- Gagné, J.P.; Pic, E.; Isabelle, M.; Krietsch, J.; Ethier, C.; Paquet, E.; Kelly, I.; Boutin, M.; Moon, K.M.; Foster, L.J.; et al. Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res. 2012, 40, 7788–7805. [Google Scholar] [CrossRef]
- Carter-O’Connell, I.; Jin, H.; Morgan, R.K.; Zaja, R.; David, L.L.; Ahel, I.; Cohen, M.S. Identifying Family-Member-Specific Targets of Mono-ARTDs by Using a Chemical Genetics Approach. Cell Rep. 2016, 14, 621–631. [Google Scholar] [CrossRef]
- Mayo, E.F.G.; Salvatore Scarpa, E.; Stilla, A.; Dani, N.; Chiacchiera, F.; Kleine, H.; Attanasio, F.; Lüscher, B.; Di Girolamo, M. ARTD10/PARP10 Induces ADP-Ribosylation of GAPDH and Recruits GAPDH into Cytosolic Membrane-Free Cell Bodies When Overexpressed in Mammalian Cells. Challenges 2018, 9, 22. [Google Scholar] [CrossRef]
- Yang, W.; Zheng, Y.; Xia, Y.; Ji, H.; Chen, X.; Guo, F.; Lyssiotis, C.A.; Aldape, K.; Cantley, L.C.; Lu, Z. ERK1/2-dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat. Cell Biol. 2012, 14, 1295–1304. [Google Scholar] [CrossRef]
- Iansante, V.; Choy, P.M.; Fung, S.W.; Liu, Y.; Chai, J.G.; Dyson, J.; Del Rio, A.; D’Santos, C.; Williams, R.; Chokshi, S.; et al. PARP14 promotes the Warburg effect in hepatocellular carcinoma by inhibiting JNK1-dependent PKM2 phosphorylation and activation. Nat. Commun. 2015, 6, 7882. [Google Scholar] [CrossRef] [PubMed]
- Fouquerel, E.; Goellner, E.M.; Yu, Z.; Gagné, J.P.; Barbi de Moura, M.; Feinstein, T.; Wheeler, D.; Redpath, P.; Li, J.; Romero, G.; et al. ARTD1/PARP1 negatively regulates glycolysis by inhibiting hexokinase 1 independent of NAD+ depletion. Cell Rep. 2014, 8, 1819–1831. [Google Scholar] [CrossRef] [PubMed]
- Robey, R.B.; Hay, N. Is Akt the “Warburg kinase”?—Akt-energy metabolism interactions and oncogenesis. Semin. Cancer Biol. 2009, 19, 25–31. [Google Scholar] [CrossRef] [PubMed]
- Sundaresan, N.R.; Pillai, V.B.; Wolfgeher, D.; Samant, S.; Vasudevan, P.; Parekh, V.; Raghuraman, H.; Cunningham, J.M.; Gupta, M.; Gupta, M.P. The deacetylase SIRT1 promotes membrane localization and activation of Akt and PDK1 during tumorigenesis and cardiac hypertrophy. Sci. Signal. 2011, 4, ra46. [Google Scholar] [CrossRef] [PubMed]
- Pinton, G.; Manente, A.G.; Murer, B.; De Marino, E.; Mutti, L.; Moro, L. PARP1 inhibition affects pleural mesothelioma cell viability and uncouples AKT/mTOR axis via SIRT1. J. Cell Mol. Med. 2013, 17, 233–241. [Google Scholar] [CrossRef]
- Ethier, C.; Tardif, M.; Arul, L.; Poirier, G.G. PARP-1 modulation of mTOR signaling in response to a DNA alkylating agent. PLoS ONE 2012, 7, e47978. [Google Scholar] [CrossRef] [PubMed]
- Li, N.; Zhang, Y.; Han, X.; Liang, K.; Wang, J.; Feng, L.; Wang, W.; Songyang, Z.; Lin, C.; Yang, L.; et al. Poly-ADP ribosylation of PTEN by tankyrases promotes PTEN degradation and tumor growth. Genes Dev. 2015, 29, 157–170. [Google Scholar] [CrossRef] [PubMed]
- Smolková, K.; Mikó, E.; Kovács, T.; Leguina-Ruzzi, A.; Sipos, A.; Bai, P. Nuclear Factor Erythroid 2-Related Factor 2 in Regulating Cancer Metabolism. Antioxid. Redox Signal. 2020, 33, 966–997. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.J.; Sun, Z.; Villeneuve, N.F.; Zhang, S.; Zhao, F.; Li, Y.; Chen, W.; Yi, X.; Zheng, W.; Wondrak, G.T.; et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008, 29, 1235–1243. [Google Scholar] [CrossRef]
- Singh, A.; Bodas, M.; Wakabayashi, N.; Bunz, F.; Biswal, S. Gain of Nrf2 function in non-small-cell lung cancer cells confers radioresistance. Antioxid. Redox Signal. 2010, 13, 1627–1637. [Google Scholar] [CrossRef] [PubMed]
- Rojo de la Vega, M.; Chapman, E.; Zhang, D.D. NRF2 and the Hallmarks of Cancer. Cancer Cell 2018, 34, 21–43. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Liu, X.; Long, M.; Huang, Y.; Zhang, L.; Zhang, R.; Zheng, Y.; Liao, X.; Wang, Y.; Liao, Q.; et al. NRF2 activation by antioxidant antidiabetic agents accelerates tumor metastasis. Sci. Transl. Med. 2016, 8, 334ra351. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.; Misra, V.; Thimmulappa, R.K.; Lee, H.; Ames, S.; Hoque, M.O.; Herman, J.G.; Baylin, S.B.; Sidransky, D.; Gabrielson, E.; et al. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med. 2006, 3, e420. [Google Scholar] [CrossRef]
- Shibata, T.; Kokubu, A.; Gotoh, M.; Ojima, H.; Ohta, T.; Yamamoto, M.; Hirohashi, S. Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology 2008, 135, 1358–1368.e4. [Google Scholar] [CrossRef]
- Taguchi, K.; Yamamoto, M. The KEAP1-NRF2 System as a Molecular Target of Cancer Treatment. Cancers 2020, 13, 46. [Google Scholar] [CrossRef] [PubMed]
- Mitsuishi, Y.; Taguchi, K.; Kawatani, Y.; Shibata, T.; Nukiwa, T.; Aburatani, H.; Yamamoto, M.; Motohashi, H. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 2012, 22, 66–79. [Google Scholar] [CrossRef] [PubMed]
- Wu, T.; Wang, X.J.; Tian, W.; Jaramillo, M.C.; Lau, A.; Zhang, D.D. Poly(ADP-ribose) polymerase-1 modulates Nrf2-dependent transcription. Free Radic. Biol. Med. 2014, 67, 69–80. [Google Scholar] [CrossRef]
- Chinopoulos, C.; Seyfried, T.N. Mitochondrial Substrate-Level Phosphorylation as Energy Source for Glioblastoma: Review and Hypothesis. ASN Neuro 2018, 10, 1759091418818261. [Google Scholar] [CrossRef] [PubMed]
- Formentini, L.; Macchiarulo, A.; Cipriani, G.; Camaioni, E.; Rapizzi, E.; Pellicciari, R.; Moroni, F.; Chiarugi, A. Poly(ADP-ribose) catabolism triggers AMP-dependent mitochondrial energy failure. J. Biol. Chem. 2009, 284, 17668–17676. [Google Scholar] [CrossRef] [PubMed]
- Ancey, P.B.; Contat, C.; Meylan, E. Glucose transporters in cancer-from tumor cells to the tumor microenvironment. FEBS J. 2018, 285, 2926–2943. [Google Scholar] [CrossRef]
- Zhao, M.; Zhang, Z. Glucose Transporter Regulation in Cancer: A Profile and the Loops. Crit. Rev. Eukaryot. Gene Expr. 2016, 26, 223–238. [Google Scholar] [CrossRef] [PubMed]
- Courtnay, R.; Ngo, D.C.; Malik, N.; Ververis, K.; Tortorella, S.M.; Karagiannis, T.C. Cancer metabolism and the Warburg effect: The role of HIF-1 and PI3K. Mol. Biol. Rep. 2015, 42, 841–851. [Google Scholar] [CrossRef] [PubMed]
- Brown, R.S.; Wahl, R.L. Overexpression of Glut-1 glucose transporter in human breast cancer. An immunohistochemical study. Cancer 1993, 72, 2979–2985. [Google Scholar] [CrossRef]
- Yamamoto, T.; Seino, Y.; Fukumoto, H.; Koh, G.; Yano, H.; Inagaki, N.; Yamada, Y.; Inoue, K.; Manabe, T.; Imura, H. Over-expression of facilitative glucose transporter genes in human cancer. Biochem. Biophys Res. Commun. 1990, 170, 223–230. [Google Scholar] [CrossRef]
- Younes, M.; Brown, R.W.; Stephenson, M.; Gondo, M.; Cagle, P.T. Overexpression of Glut1 and Glut3 in stage I nonsmall cell lung carcinoma is associated with poor survival. Cancer 1997, 80, 1046–1051. [Google Scholar] [CrossRef]
- Mellanen, P.; Minn, H.; Grénman, R.; Härkönen, P. Expression of glucose transporters in head-and-neck tumors. Int. J. Cancer 1994, 56, 622–629. [Google Scholar] [CrossRef]
- Barthel, A.; Okino, S.T.; Liao, J.; Nakatani, K.; Li, J.; Whitlock, J.P., Jr.; Roth, R.A. Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1. J. Biol. Chem. 1999, 274, 20281–20286. [Google Scholar] [CrossRef] [PubMed]
- Wieman, H.L.; Wofford, J.A.; Rathmell, J.C. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol. Biol. Cell 2007, 18, 1437–1446. [Google Scholar] [CrossRef] [PubMed]
- McBrayer, S.K.; Cheng, J.C.; Singhal, S.; Krett, N.L.; Rosen, S.T.; Shanmugam, M. Multiple myeloma exhibits novel dependence on GLUT4, GLUT8, and GLUT11: Implications for glucose transporter-directed therapy. Blood 2012, 119, 4686–4697. [Google Scholar] [CrossRef] [PubMed]
- Garrido, P.; Osorio, F.G.; Morán, J.; Cabello, E.; Alonso, A.; Freije, J.M.; González, C. Loss of GLUT4 induces metabolic reprogramming and impairs viability of breast cancer cells. J. Cell Physiol. 2015, 230, 191–198. [Google Scholar] [CrossRef] [PubMed]
- Yeh, T.Y.; Sbodio, J.I.; Tsun, Z.Y.; Luo, B.; Chi, N.W. Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochem. J. 2007, 402, 279–290. [Google Scholar] [CrossRef]
- Su, Z.; Deshpande, V.; James, D.E.; Stöckli, J. Tankyrase modulates insulin sensitivity in skeletal muscle cells by regulating the stability of GLUT4 vesicle proteins. J. Biol. Chem. 2018, 293, 8578–8587. [Google Scholar] [CrossRef]
- Bai, P.; Cantó, C.; Oudart, H.; Brunyánszki, A.; Cen, Y.; Thomas, C.; Yamamoto, H.; Huber, A.; Kiss, B.; Houtkooper, R.H.; et al. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 2011, 13, 461–468. [Google Scholar] [CrossRef] [PubMed]
- Módis, K.; Gero, D.; Erdélyi, K.; Szoleczky, P.; DeWitt, D.; Szabo, C. Cellular bioenergetics is regulated by PARP1 under resting conditions and during oxidative stress. Biochem. Pharmacol. 2012, 83, 633–643. [Google Scholar] [CrossRef]
- Scovassi, A.I. Mitochondrial poly(ADP-ribosylation): From old data to new perspectives. FASEB J. 2004, 18, 1487–1488. [Google Scholar] [CrossRef]
- Bai, P.; Nagy, L.; Fodor, T.; Liaudet, L.; Pacher, P. Poly(ADP-ribose) polymerases as modulators of mitochondrial activity. Trends Endocrinol. Metab. 2015, 26, 75–83. [Google Scholar] [CrossRef] [PubMed]
- Brunyanszki, A.; Szczesny, B.; Virág, L.; Szabo, C. Mitochondrial poly(ADP-ribose) polymerase: The Wizard of Oz at work. Free Radic. Biol. Med. 2016, 100, 257–270. [Google Scholar] [CrossRef]
- Rossi, M.N.; Carbone, M.; Mostocotto, C.; Mancone, C.; Tripodi, M.; Maione, R.; Amati, P. Mitochondrial localization of PARP-1 requiRes. interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J. Biol. Chem. 2009, 284, 31616–31624. [Google Scholar] [CrossRef]
- Márton, J.; Fodor, T.; Nagy, L.; Vida, A.; Kis, G.; Brunyánszki, A.; Antal, M.; Lüscher, B.; Bai, P. PARP10 (ARTD10) modulates mitochondrial function. PLoS ONE 2018, 13, e0187789. [Google Scholar] [CrossRef]
- Bensaad, K.; Favaro, E.; Lewis, C.A.; Peck, B.; Lord, S.; Collins, J.M.; Pinnick, K.E.; Wigfield, S.; Buffa, F.M.; Li, J.L.; et al. Fatty acid uptake and lipid storage induced by HIF-1α contribute to cell growth and survival after hypoxia-reoxygenation. Cell Rep. 2014, 9, 349–365. [Google Scholar] [CrossRef]
- Ma, Y.; Temkin, S.M.; Hawkridge, A.M.; Guo, C.; Wang, W.; Wang, X.Y.; Fang, X. Fatty acid oxidation: An emerging facet of metabolic transformation in cancer. Cancer Lett. 2018, 435, 92–100. [Google Scholar] [CrossRef] [PubMed]
- Huang, K.; Du, M.; Tan, X.; Yang, L.; Li, X.; Jiang, Y.; Wang, C.; Zhang, F.; Zhu, F.; Cheng, M.; et al. PARP1-mediated PPARα poly(ADP-ribosyl)ation suppresses fatty acid oxidation in non-alcoholic fatty liver disease. J. Hepatol. 2017, 66, 962–977. [Google Scholar] [CrossRef] [PubMed]
- Gariani, K.; Ryu, D.; Menzies, K.J.; Yi, H.S.; Stein, S.; Zhang, H.; Perino, A.; Lemos, V.; Katsyuba, E.; Jha, P.; et al. Inhibiting poly ADP-ribosylation increases fatty acid oxidation and protects against fatty liver disease. J. Hepatol. 2017, 66, 132–141. [Google Scholar] [CrossRef] [PubMed]
- Fhu, C.W.; Ali, A. Fatty Acid Synthase: An Emerging Target in Cancer. Molecules 2020, 25, 3935. [Google Scholar] [CrossRef]
- Wu, X.; Dong, Z.; Wang, C.J.; Barlow, L.J.; Fako, V.; Serrano, M.A.; Zou, Y.; Liu, J.Y.; Zhang, J.T. FASN regulates cellular response to genotoxic treatments by increasing PARP-1 expression and DNA repair activity via NF-κB and SP1. Proc. Natl. Acad. Sci. USA 2016, 113, E6965–E6973. [Google Scholar] [CrossRef] [PubMed]
- Murata, M.M.; Kong, X.; Moncada, E.; Chen, Y.; Imamura, H.; Wang, P.; Berns, M.W.; Yokomori, K.; Digman, M.A. NAD+ consumption by PARP1 in response to DNA damage triggers metabolic shift critical for damaged cell survival. Mol. Biol. Cell 2019, 30, 2584–2597. [Google Scholar] [CrossRef]
- Sun, C.; Fang, Y.; Labrie, M.; Li, X.; Mills, G.B. Systems approach to rational combination therapy: PARP inhibitors. Biochem. Soc. Trans. 2020, 48, 1101–1108. [Google Scholar] [CrossRef]
- Dréan, A.; Lord, C.J.; Ashworth, A. PARP inhibitor combination therapy. Crit. Rev. Oncol. Hematol. 2016, 108, 73–85. [Google Scholar] [CrossRef]
- Fang, Y.; McGrail, D.J.; Sun, C.; Labrie, M.; Chen, X.; Zhang, D.; Ju, Z.; Vellano, C.P.; Lu, Y.; Li, Y.; et al. Sequential Therapy with PARP and WEE1 Inhibitors Minimizes Toxicity while Maintaining Efficacy. Cancer Cell 2019, 35, 851–867.e857. [Google Scholar] [CrossRef] [PubMed]
- Minchom, A.; Aversa, C.; Lopez, J. Dancing with the DNA damage response: Next-generation anti-cancer therapeutic strategies. Ther. Adv. Med. Oncol. 2018, 10, 1758835918786658. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.D.; Kong, F.E.; Qi, L.; Lin, J.X.; Yan, Q.; Loong, J.H.C.; Xi, S.Y.; Zhao, Y.; Zhang, Y.; Yuan, Y.F.; et al. PARP inhibitor Olaparib overcomes Sorafenib resistance through reshaping the pluripotent transcriptome in hepatocellular carcinoma. Mol. Cancer 2021, 20, 20. [Google Scholar] [CrossRef]
- Yang, L.; Zhang, Y.; Shan, W.; Hu, Z.; Yuan, J.; Pi, J.; Wang, Y.; Fan, L.; Tang, Z.; Li, C.; et al. Repression of BET activity sensitizes homologous recombination-proficient cancers to PARP inhibition. Sci. Transl. Med. 2017, 9. [Google Scholar] [CrossRef] [PubMed]
- Song, D.; He, H.; Sinha, I.; Hases, L.; Yan, F.; Archer, A.; Haldosen, L.A.; Zhao, C.; Williams, C. Blocking Fra-1 sensitizes triple-negative breast cancer to PARP inhibitor. Cancer Lett. 2021, 506, 23–34. [Google Scholar] [CrossRef] [PubMed]
- Erdélyi, K.; Bai, P.; Kovács, I.; Szabó, E.; Mocsár, G.; Kakuk, A.; Szabó, C.; Gergely, P.; Virág, L. Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J. 2009, 23, 3553–3563. [Google Scholar] [CrossRef] [PubMed]
- Kovács, K.; Erdélyi, K.; Hegedűs, C.; Lakatos, P.; Regdon, Z.; Bai, P.; Haskó, G.; Szabó, E.; Virág, L. Poly(ADP-ribosyl)ation is a survival mechanism in cigarette smoke-induced and hydrogen peroxide-mediated cell death. Free Radic. Biol. Med. 2012, 53, 1680–1688. [Google Scholar] [CrossRef] [PubMed]
- Kiss, A.; Ráduly, A.P.; Regdon, Z.; Polgár, Z.; Tarapcsák, S.; Sturniolo, I.; El-Hamoly, T.; Virág, L.; Hegedűs, C. Targeting Nuclear NAD(+) Synthesis Inhibits DNA Repair, Impairs Metabolic Adaptation and Increases Chemosensitivity of U-2OS Osteosarcoma Cells. Cancers 2020, 12, 1180. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Demény, M.A.; Virág, L. The PARP Enzyme Family and the Hallmarks of Cancer Part 1. Cell Intrinsic Hallmarks. Cancers 2021, 13, 2042. https://doi.org/10.3390/cancers13092042
Demény MA, Virág L. The PARP Enzyme Family and the Hallmarks of Cancer Part 1. Cell Intrinsic Hallmarks. Cancers. 2021; 13(9):2042. https://doi.org/10.3390/cancers13092042
Chicago/Turabian StyleDemény, Máté A., and László Virág. 2021. "The PARP Enzyme Family and the Hallmarks of Cancer Part 1. Cell Intrinsic Hallmarks" Cancers 13, no. 9: 2042. https://doi.org/10.3390/cancers13092042
APA StyleDemény, M. A., & Virág, L. (2021). The PARP Enzyme Family and the Hallmarks of Cancer Part 1. Cell Intrinsic Hallmarks. Cancers, 13(9), 2042. https://doi.org/10.3390/cancers13092042