Autophagy inhibition switches low-dose camptothecin-induced premature senescence to apoptosis in human colorectal cancer cells

Biochemical Pharmacology

Volumn 90, Issue 3, 2014, Pages 265-275

  Zhang, Jian Wei ^a   Zhang, Shan Shan ^a   Song, Jian Rui ^a,b   Sun, Kai ^a,c   Zong, Chen ^a   Zhao, Qiu Dong ^a   Liu, Wen Ting ^a   Li, Rong ^a   Wu, Meng Chao ^a   Wei, Li Xin ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; Autophagy; DNA damage response; Human colorectal cancer cells; Low dose chemotherapy; Senescence

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; ATM PROTEIN; AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 6; AUTOPHAGY PROTEIN 7; BECLIN 1; CAMPTOTHECIN; CASPASE 3; CHOLECYSTOKININ OCTAPEPTIDE; GREEN FLUORESCENT PROTEIN; HISTONE H2AX; MICROTUBULE ASSOCIATED PROTEIN 1; PROTEIN; PROTEIN P21; PROTEIN P53; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER CELL; CANCER CHEMOTHERAPY; CELL STRUCTURE; COLORECTAL CANCER; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; HCT116 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION;

APOPTOSIS; AUTOPHAGY; DNA DAMAGE RESPONSE; HUMAN COLORECTAL CANCER CELLS; LOW-DOSE CHEMOTHERAPY; SENESCENCE;

ADENINE; AMP-ACTIVATED PROTEIN KINASES; ANTINEOPLASTIC AGENTS; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; AUTOPHAGY; CAMPTOTHECIN; CELL AGING; CELL LINE, TUMOR; CHLOROQUINE; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; HUMANS; LYSOSOMES; NEOPLASM PROTEINS; OSMOLAR CONCENTRATION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84903879581     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.05.009     Document Type: Article

References (43)

1. G. Klement, S. Baruchel, J. Rak, S. Man, K. Clark, and D.J. Hicklin et al. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity J Clin Invest 105 2000 R15 R24
2. G. Gasparini Metronomic scheduling: the future of chemotherapy Lancet Oncol 2 2001 733 740
3. D. Loven, E. Hasnis, F. Bertolini, and Y. Shaked Low-dose metronomic chemotherapy: from past experience to new paradigms in the treatment of cancer Drug Discov Today 18 2013 193 201
4. A. Litwiniec, L. Gackowska, A. Helmin-Basa, A. Zuryń, and A. Grzanka Low-dose etoposide-treatment induces endoreplication and cell death accompanied by cytoskeletal alterations in A549 cells: does the response involve senescence? The possible role of vimentin Cancer Cell Int 13 2013 9
5. M.A. Sliwinska, G. Mosieniak, K. Wolanin, A. Babik, K. Piwocka, and A. Magalska et al. Induction of senescence with doxorubicin leads to increased genomic instability of HCT116 cells Mech Ageing Dev 130 2009 24 32
6. I.B. Roninson Tumor cell senescence in cancer treatment Cancer Res 63 2003 2705 2715 (Pubitemid 36667137)
7. D.A. Gewirtz, S.E. Holt, and L.W. Elmore Accelerated senescence: an emerging role in tumor cell response to chemotherapy and radiation Biochem Pharmacol 76 2008 947 957
8. P. Kahlem, B. Dorken, and C.A. Schmitt Cellular senescence in cancer treatment: friend or foe J Clin Invest 113 2004 169 174 (Pubitemid 38544199)
9. J-P. Coppé, C.K. Patil, F. Rodier, Y. Sun, D.P. Muñoz, and J. Goldstein et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor PLoS Biol 6 2008 2853 2868
10. L.W. Elmore, X. Di, C. Dumur, S.E. Holt, and D.A. Gewirtz Evasion of a single-step, chemotherapy-induced senescence in breast cancer cells: implications for treatment response Clin Cancer Res 11 2005 2637 2643 (Pubitemid 40569464)
11. R.S. Roberson, S.J. Kussick, E. Vallieres, S-Y.J. Chen, and D.Y. Wu Escape from therapy-induced accelerated cellular senescence in p53-null lung cancer cells and in human lung cancers Cancer Res 65 2005 2795 2803 (Pubitemid 40490082)
12. A. Seluanov, V. Gorbunova, A. Falcovitz, A. Sigal, M. Milyavsky, and I. Zurer et al. Change of the death pathway in senescent human fibroblasts in response to DNA damage is caused by an inability to stabilize p53 Mol Cell Biol 21 2001 1552 1564 (Pubitemid 32156375)
13. D. Glick, S. Barth, and K.F. Macleod Autophagy: cellular and molecular mechanisms J Pathol 221 2010 3 12
14. A.T. Vessoni, E.C. Filippi-Chiela, C.F. Menck, and G. Lenz Autophagy and genomic integrity Cell Death Differ 20 2013 1444 1454
15. L-M. Gerland, S. Peyrol, C. Lallemand, R. Branche, J-P. Magaud, and M. Ffrench Association of increased autophagic inclusions labeled for beta-galactosidase with fibroblastic aging Exp Gerontol 38 2003 887 895 (Pubitemid 36952670)
16. A.R.J. Young, M. Narita, M. Ferreira, K. Kirschner, M. Sadaie, and J.F.J. Darot et al. Autophagy mediates the mitotic senescence transition Genes Dev 23 2009 798 803
17. X-L. Guo, D. Li, F. Hu, J-R. Song, S-S. Zhang, and W-J. Deng et al. Targeting autophagy potentiates chemotherapy-induced apoptosis and proliferation inhibition in hepatocarcinoma cells Cancer Lett 320 2012 171 179
18. J. Li, N. Hou, A. Faried, S. Tsutsumi, and H. Kuwano Inhibition of autophagy augments 5-fluorouracil chemotherapy in human colon cancer in vitro and in vivo model Eur J Cancer 46 2010 1900 1909
19. G. Xi, X. Hu, B. Wu, H. Jiang, C.Y.F. Young, and Y. Pang et al. Autophagy inhibition promotes paclitaxel-induced apoptosis in cancer cells Cancer Lett 307 2011 141 148
20. Y. Pommier Topoisomerase I inhibitors: camptothecins and beyond Nat Rev Cancer 6 2006 789 802 (Pubitemid 44450467)
21. S. Pankiv, T.H. Clausen, T. Lamark, A. Brech, J-A. Bruun, and H. Outzen et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy J Biol Chem 282 2007 24131 24145 (Pubitemid 47328003)
22. R.H. te Poele, A.L. Okorokov, L. Jardine, J. Cummings, and S.P. Joel DNA damage is able to induce senescence in tumor cells in vitro and in vivo Cancer Res 62 2002 1876 1883 (Pubitemid 34408516)
23. E. Crescenzi, G. Palumbo, J. de Boer, and H.J.M. Brady Ataxia telangiectasia mutated and p21CIP1 modulate cell survival of drug-induced senescent tumor cells: implications for chemotherapy Clin Cancer Res 14 2008 1877 1887 (Pubitemid 351469475)
24. Y. Shiloh The ATM-mediated DNA-damage response: taking shape Trends Biochem Sci 31 2006 402 410 (Pubitemid 44038916)
25. S. Bekker-Jensen, and N. Mailand Assembly and function of DNA double-strand break repair foci in mammalian cells DNA Repair (Amst) 9 2010 1219 1228
26. L.C. Riches, A.M. Lynch, and N.J. Gooderham Early events in the mammalian response to DNA double-strand breaks Mutagenesis 23 2008 331 339
27. D.M. Gwinn, D.B. Shackelford, D.F. Egan, M.M. Mihaylova, A. Mery, and D.S. Vasquez et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint Mol Cell 30 2008 214 226 (Pubitemid 351626684)
28. N. Hay, and N. Sonenberg Upstream and downstream of mTOR Genes Dev 18 2004 1926 1945 (Pubitemid 39071573)
29. R.W. Goehe, X. Di, K. Sharma, M.L. Bristol, S.C. Henderson, and K. Valerie et al. The autophagy-senescence connection in chemotherapy: must tumor cells (self) eat before they sleep J Pharmacol Exp Ther 343 2012 763 778
30. A. Petiot, E. Ogier-Denis, E.F. Blommaart, A.J. Meijer, and P. Codogno Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells J Biol Chem 275 2000 992 998 (Pubitemid 30051145)
31. A.U. Lüthi, and S.J. Martin The CASBAH: a searchable database of caspase substrates Cell Death Differ 14 2007 641 650 (Pubitemid 46444502)
32. J. Liu, H. Xia, M. Kim, L. Xu, Y. Li, and L. Zhang et al. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13 Cell 147 2011 223 234
33. Z. Han, W. Wei, S. Dunaway, J.W. Darnowski, P. Calabresi, and J. Sedivy et al. Role of p21 in apoptosis and senescence of human colon cancer cells treated with camptothecin J Biol Chem 277 2002 17154 17160 (Pubitemid 34967748)
34. D. Hanahan, G. Bergers, and E. Bergsland Less is more, regularly: metronomic dosing of cytotoxic drugs can target tumor angiogenesis in mice J Clin Invest 105 2000 1045 1047 (Pubitemid 30217688)
35. T. Browder, C.E. Butterfield, B.M. Kraling, B. Shi, B. Marshall, and M.S. O'Reilly et al. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer Cancer Res 60 2000 1878 1886 (Pubitemid 30207647)
36. J.J. O'Leary, R.L. Shapiro, C.J. Ren, N. Chuang, H.W. Cohen, and M. Potmesil Antiangiogenic effects of camptothecin analogues 9-amino-20(S)- camptothecin, topotecan, and CPT-11 studied in the mouse cornea model Clin Cancer Res 5 1999 181 187 (Pubitemid 29045192)
37. F. d'Adda di Fagagna, P.M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, and T. Von Zglinicki et al. A DNA damage checkpoint response in telomere-initiated senescence Nature 426 2003 194 198 (Pubitemid 37442589)
38. O.A. Sedelnikova, I. Horikawa, D.B. Zimonjic, N.C. Popescu, W.M. Bonner, and J.C. Barrett Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks Nat Cell Biol 6 2004 168 170 (Pubitemid 38425717)
39. M.G. Hollomon, N. Gordon, J.M. Santiago-O'Farrill, and E.S. Kleinerman Knockdown of autophagy-related protein 5, ATG5, decreases oxidative stress and has an opposing effect on camptothecin-induced cytotoxicity in osteosarcoma cells BMC Cancer 13 2013 500
40. B. Levine, and J. Abrams p53: the Janus of autophagy Nat Cell Biol 10 2008 637 639
41. E. Tasdemir, M.C. Maiuri, L. Galluzzi, I. Vitale, M. Djavaheri-Mergny, and M. D'Amelio et al. Regulation of autophagy by cytoplasmic p53 Nat Cell Biol 10 2008 676 687 (Pubitemid 351772933)
42. M. Olivier, R. Eeles, M. Hollstein, M.A. Khan, C.C. Harris, and P. Hainaut The IARC TP53 database: new online mutation analysis and recommendations to users Hum Mutat 19 2002 607 614 (Pubitemid 34556481)
43. L.W. Elmore, C.W. Rehder, X. Di, P.A. McChesney, C.K. Jackson-Cook, and D.A. Gewirtz et al. Adriamycin-induced senescence in breast tumor cells involves functional p53 and telomere dysfunction J Biol Chem 277 2002 35509 35515