Gemcitabine induces poly (ADP-Ribose) polymerase-1 (PARP-1) degradation through autophagy in pancreatic cancer

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Wang, Yufeng ^a   Kuramitsu, Yasuhiro ^a   Tokuda, Kazuhiro ^a   Baron, Byron ^a   Kitagawa, Takao ^a   Akada, Junko ^a   Maehara, Shin Ichiro ^b   Maehara, Yoshihiko ^b   Nakamura, Kazuyuki ^a,c  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c Tokuyama Medical Association Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; AMP ACTIVATED PROTEIN KINASE A1; BECLIN 1; CASPASE; GEMCITABINE; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; CULTURE MEDIUM; DEOXYCYTIDINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CANCER INHIBITION; CELL CYCLE ARREST; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DRUG SENSITIVITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HYPOXIA; PANCREAS CANCER; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STARVATION; ANALOGS AND DERIVATIVES; CULTURE MEDIUM; DRUG EFFECTS; METABOLISM;

ANTIMETABOLITES, ANTINEOPLASTIC; AUTOPHAGY; CULTURE MEDIA, SERUM-FREE; DEOXYCYTIDINE; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; PROTEOLYSIS;

EID: 84907487256     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109076     Document Type: Article

References (41)

1. Heinemann V, Boeck S, Hinke A., Labianca R, Louvet C. (2008) Meta-analysis of randomized trials: evaluation of benefit from gemcitabine-based combination chemotherapy applied in advanced pancreatic cancer. BMC Cancer 8: 82.
2. El-Rayes BF, Philip P.A. (2003) A review of systemic therapy for advanced pancreatic cancer. Clin Adv Hematol Oncol 1: 430-4.
3. Wheatley SP, McNeish I.A. (2005) Survivin: a protein with dual roles in mitosis and apoptosis. Int Rev Cytol 247: 35-88.
4. Moore MJ, Goldstein D, Hamm J., Figer A, Hecht JR, et al. (2007) Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 25: 1960-6.
5. Baker CH, Banzon J, Bollinger J.M., Stubbe J., Samano V, et al. (1991) 29-Deoxy-29-methylenecytidine and 29-deoxy-29,29-difluorocytidine 59-diphosphates: potent mechanism-based inhibitors of ribonucleotide reductase. J Med Chem 34: 1879-84.
6. Huang P, Chubb S, Hertel L.W., Grindey GB, Plunkett W. (1991) Action of 29,29-difluorodeoxycytidine on DNA synthesis. Cancer Res 51: 6110-7.
7. Karnitz LM, Flatten KS, Wagner J.M., Loegering D., Hackbarth JS, et al. (2005) Gemcitabine-induced activation of checkpoint signaling pathways that affect tumor cell survival. Mol Pharmacol 68: 1636-44.
8. Matthews DJ, Yakes FM, Chen J, Tadano M., Bornheim L, et al. (2007) Pharmacological abrogation of S-phase checkpoint enhances the anti-tumor activity of gemcitabine in vivo. Cell Cycle 6: 104-10.
9. Parsels LA, Morgan MA, Tanska D.M., Parsels JD, Palmer BD, et al. (2009) Gemcitabine sensitization by checkpoint kinase 1 inhibition correlates with inhibition of a Rad51 DNA damage response in pancreatic cancer cells. Mol Cancer Ther 8: 45-54.
10. Meijer AJ, Dubbelhuis P.F. (2004) Amino acid signalling and the integration of metabolism. Biochem Biophys Res Commun 313: 397-403.
11. Mizushima N, Levine B, Cuervo A.M., Klionsky D.J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451: 1069-75.
12. Chen S, Rehman SK, Zhang W, Wen A., Yao L, Zhang J. (2010) Autophagy is a therapeutic target in anticancer drug resistance. Biochim Biophys Acta 1806: 220-9.
13. Pardo R, Lo Ré A, Archange C, Ropolo A, Papademetrio DL, et al. (2010) Gemcitabine induces the VMP1-mediated autophagy pathway to promote apoptotic death in human pancreatic cancer cells. Pancreatology 10: 19-26.
14. Kim MY, Zhang T, Kraus W.L. (2005) Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 19: 1951-67.
15. Godon C, Cordelières FP, Biard D., Giocanti N, Mégnin-Chanet F, et al. (2008) PARP inhibition versus PARP-1 silencing: different outcomes in terms of singlestrand break repair and radiation susceptibility. Nucleic Acids Res 36: 4454-64.
16. Schultz N, Lopez E, Saleh-Gohari N, Helleday T. (2003) Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res 31: 4959-64.
17. Wang M, Wu W, Wu W., Rosidi B, Zhang L, et al. (2006) PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 34: 6170-82.
18. Aguilar-Quesada R, Muñoz-Gámez JA, Martín-Oliva D, Peralta A, Valenzuela MT, et al. (2007) Interaction between ATM and PARP-1 in response to DNA damage and sensitization of ATM deficient cells through PARP inhibition. BMC Mol Biol 8: 29.
19. Calabrese CR, Almassy R, Barton S., Batey MA, Calvert AH, et al. (2004) Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J Natl Cancer Inst 96: 56-67.
20. De Soto JA, Deng C.X. (2006) PARP-1 inhibitors: are they the long-sought genetically specific drugs for BRCA1/2-associated breast cancers? Int J Med Sci 3: 117-23.
21. Lee YR, Yu DS, Liang Y.C., Huang KF, Chou SJ, et al. (2013) New approaches of PARP-1 inhibitors in human lung cancer cells and cancer stem-like cells by some selected anthraquinone-derived small molecules. PLoS One 8: e56284.
22. Mori-Iwamoto S, Kuramitsu Y, Ryozawa S., Mikuria K, Fujimoto M, et al. (2007) Proteomics finding heat shock protein 27 as a biomarker for resistance of pancreatic cancer cells to gemcitabine. Int J Oncol 31: 1345-50.
23. Taba K, Kuramitsu Y, Ryozawa S., Yoshida K, Tanaka T, et al. (2010) Heat-shock protein 27 is phosphorylated in gemcitabine-resistant pancreatic cancer cells. Anticancer Res 30: 2539-43.
24. Mori-Iwamoto S, Kuramitsu Y, Ryozawa S., Taba K, Fujimoto M, et al. (2008) A proteomic profiling of gemcitabine resistance in pancreatic cancer cell lines. Mol Med Rep 1: 429-34.
25. Kabeya Y, Mizushima N, Ueno T., Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-8.
26. Mao Z, Hine C, Tian X., Van Meter M, Au M, et al. (2011) SIRT6 promotes DNA repair under stress by activating PARP1. Science 332: 1443-6.
27. Bauer I, Grozio A, Lasigliè D, Basile G, Sturla L, et al. (2012) The NAD+-dependent histone deacetylase SIRT6 promotes cytokine production and migration in pancreatic cancer cells by regulating Ca2+ responses. J Biol Chem 287: 40924-37.
28. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier G.G., Earnshaw W.C. (1994) Cleavage of poly (ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346-7.
29. Mizuno S, Bogaard HJ, Voelkel N.F., Umeda Y., Kadowaki M, et al. (2009) Hypoxia regulates human lung fibroblast proliferation via p53-dependent and -independent pathways. Respir Res 6: 10:17.
30. Vara D, Salazar M, Olea-Herrero N, Guzmán M, Velasco G., Díaz-Laviada I (2011) Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ 18: 1099-111.
31. Robert T, Vanoli F, Chiolo I., Shubassi G, Bernstein KA, et al. (2011) HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 471: 74-9.
32. Botrugno OA, Robert T, Vanoli F., Foiani M, Minucci S. (2012) Molecular pathways: old drugs define new pathways: non-histone acetylation at the crossroads of the DNA damage response and autophagy. Clin Cancer Res 18: 2436-42.
33. Yang YG, Cortes U, Patnaik S., Jasin M, Wang Z.Q. (2004) Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 23: 3872-82.
34. Ewald B, Sampath D, Plunkett W. (2008) ATM and the Mre11-Rad50-Nbs1 complex respond to nucleoside analogue-induced stalled replication forks and contribute to drug resistance. Cancer Res 68: 7947-55.
35. Kaidi A, Weinert BT, Choudhary C, Jackson S.P. (2010) Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329: 1348-53.
36. Patel AG, Sarkaria JN, Kaufmann S.H. (2011) Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc Natl Acad Sci U S A 108: 3406-11.
37. Dai P, Xiong WC, Mei L. (2006) Erbin inhibits RAF activation by disrupting the sur-8-Ras-Raf complex. J Biol Chem 281: 927-33.
38. Shi M, Zhao M, Hu M., Liu D, Cao H, et al. (2012) b2-AR-induced Her2 transactivation mediated by Erbin confers protection from apoptosis in cardiomyocytes. Int J Cardiol [Epub ahead of print].
39. Kimura Y, Kobari M, Yusa T., Sunamura M, Kimura M, et al. (1996) Establishment of an experimental liver metastasis model by intraportal injection of a newly derived human pancreatic cancer cell line (KLM-1). Int J Pancreatol 20: 43-50.
40. Maehara S, Tanaka S, Shimada M., Shirabe K, Saito Y, et al. (2004) Selenoprotein P, as a predictor for evaluating gemcitabine resistance in human pancreatic cancer cells. Int J Cancer 112: 184-9.
41. Iwasaki I, Sugiyama H, Kanazawa S., Hemmi H. (2002) Establishment of cisplatin-resistant variants of human neuroblastoma cell lines, TGW and GOTO, and their drug cross-resistance profiles. Cancer Chemother Pharmacol 49: 438-44.