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Telomeric impact of conventional chemotherapy |
Yiming Lu1, Waiian Leong1, Olivier Guérin2,3, Eric Gilson2,4, Jing Ye1() |
1. Ruijin Hospital Af?liated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China; 2. Institut for Research on Cancer ??and Aging, Nice (IRCAN), Nice University, CNRS UMR7284/INSERM U1081, Faculty of Medicine, Nice, France; 3. Geriatric Unit, Cimiez ?Hospital, CHU of Nice, France; 4. Department of Medical Genetics, Archet 2 Hospital, CHU of Nice, France |
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Abstract The increased level of chromosome instability in cancer cells, leading to aneuploidy and gross chromosomal rearrangements, is not only a driving force for oncogenesis but also can be the Achille’s heel of the disease since many chemotherapies (CT) kill cells by inducing a non-tolerable rate of DNA damage. A wealth of published evidence showed that telomere stability can be more affected than the bulk of the genome by several conventional antineoplasic drugs. These results raise the interesting possibility that CT with genotoxic drugs preferentially target telomeres. In agreement with this view, accelerated shortening of telomere length has been described in blood lineage cells following high-dose CT (stem cell transplantation) or non-myeloablative CT. However, almost nothing is known on the consequences of this shortening in terms of telomere stability, senescence and on the development of second cancers or post-treatment aging-like syndromes in cancer survivors (cognitive defect, fertility impairment, etc.). In this article, we propose: (1) telomeres of cancer cells are preferential genomic targets of chemotherapies altering chromosome maintenance; (2) telomere functional parameters can be a surrogate marker of chemotherapy sensitivity and toxicity; (3) the use of anti-telomere molecule could greatly enhance the sensitivity to standards chemotherapies.
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Keywords
telomere
antineoplasic drugs
conventional chemotherapies
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Corresponding Author(s):
Ye Jing,Email:yj11254@rjh.com.cn
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Issue Date: 05 December 2013
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1 |
Xue W, Zender L, Mithing C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007; 445(7128): 656-660 doi: 10.1038/nature05529 pmid:17251933
|
2 |
Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005; 436(7054): 1186-1190 doi: 10.1038/nature03884 pmid:15995699
|
3 |
Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011; 8(3): 151-160 doi: 10.1038/nrclinonc.2010.223 pmid:21364688
|
4 |
Leonetti C, Scarsella M, Riggio G, Rizzo A, Salvati E, D’Incalci M, Staszewsky L, Frapolli R, Stevens MF, Stoppacciaro A, Mottolese M, Antoniani B, Gilson E, Zupi G, Biroccio A. G-quadruplex ligand RHPS4 potentiates the antitumor activity of camptothecins in preclinical models of solid tumors. Clin Cancer Res 2008; 14(22): 7284-7291 doi: 10.1158/1078-0432.CCR-08-0941 pmid:19010844
|
5 |
Biroccio A, Porru M, Rizzo A, Salvati E, D’Angelo C, Orlandi A, Passeri D, Franceschin M, Stevens MF, Gilson E, Beretta G, Zupi G, Pisano C, Zunino F, Leonetti C. DNA damage persistence as determinant of tumor sensitivity to the combination of Topo I inhibitors and telomere-targeting agents. Clin Cancer Res 2011; 17(8): 2227-2236 doi: 10.1158/1078-0432.CCR-10-3033 pmid:21355072
|
6 |
Ye J, Lenain C, Bauwens S, Rizzo A, Saint-Léger A, Poulet A, Benarroch D, Magdinier F, Morere J, Amiard S, Verhoeyen E, Britton S, Calsou P, Salles B, Bizard A, Nadal M, Salvati E, Sabatier L, Wu Y, Biroccio A, Londo?o-Vallejo A, Giraud-Panis MJ, Gilson E. TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell 2010; 142(2): 230-242 doi: 10.1016/j.cell.2010.05.032 pmid:20655466
|
7 |
Ourliac-Garnier I, Poulet A, Charif R, Amiard S, Magdinier F, Reza? K, Gilson E, Giraud-Panis MJ, Bombard S. Platination of telomeric DNA by cisplatin disrupts recognition by TRF2 and TRF1. J Biol Inorg Chem 2010; 15(5): 641-654 doi: 10.1007/s00775-010-0631-4 pmid:20191372
|
8 |
Lee KH, Rudolph KL, Ju YJ, Greenberg RA, Cannizzaro L, Chin L, Weiler SR, DePinho RA. Telomere dysfunction alters the chemotherapeutic profile of transformed cells. Proc Natl Acad Sci USA 2001; 98(6): 3381-3386 doi: 10.1073/pnas.051629198 pmid:11248087
|
9 |
Snyder AR, Zhou J, Deng Z, Lieberman PM. Therapeutic doses of hydroxyurea cause telomere dysfunction and reduce TRF2 binding to telomeres. Cancer Biol Ther 2009; 8(12): 1136-1145 doi: 10.4161/cbt.8.12.8446 pmid:19363303
|
10 |
Hayashi MT, Cesare AJ, Fitzpatrick JA, Lazzerini-Denchi E, Karlseder J. A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat Struct Mol Biol 2012; 19(4): 387-394 doi: 10.1038/nsmb.2245 pmid:22407014
|
11 |
de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 2005; 19(18): 2100-2110 doi: 10.1101/gad.1346005 pmid:16166375
|
12 |
Xin H, Liu D, Songyang Z. The telosome/shelterin complex and its functions. Genome Biol 2008; 9(9): 232 doi: 10.1186/gb-2008-9-9-232 pmid:18828880
|
13 |
Blasco MA. The epigenetic regulation of mammalian telomeres. Nat Rev Genet 2007; 8(4): 299-309 doi: 10.1038/nrg2047 pmid:17363977
|
14 |
Baur JA, Zou Y, Shay JW, Wright WE. Telomere position effect in human cells. Science 2001; 292(5524): 2075-2077 doi: 10.1126/science.1062329 pmid:11408657
|
15 |
Koering CE, Pollice A, Zibella MP, Bauwens S, Puisieux A, Brunori M, Brun C, Martins L, Sabatier L, Pulitzer JF, Gilson E. Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep 2002; 3(11): 1055-1061 doi: 10.1093/embo-reports/kvf215 pmid:12393752
|
16 |
Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007; 318(5851): 798-801 doi: 10.1126/science.1147182 pmid:17916692
|
17 |
Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 2008; 10(2): 228-236 doi: 10.1038/ncb1685 pmid:18157120
|
18 |
Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, Giulotto E, Azzalin CM. CpG-island promoters drive transcription of human telomeres. RNA 2009; 15(12): 2186-2194 doi: 10.1261/rna.1748309 pmid:19850908
|
19 |
Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T. Mammalian telomeres end in a large duplex loop (see comments). Cell 1999; 97(4): 503-514 doi: 10.1016/S0092-8674(00)80760-6 pmid:10338214
|
20 |
Amiard S, Doudeau M, Pinte S, Poulet A, Lenain C, Faivre-Moskalenko C, Angelov D, Hug N, Vindigni A, Bouvet P, Paoletti J, Gilson E, Giraud-Panis MJ. A topological mechanism for TRF2-enhanced strand invasion. Nat Struct Mol Biol 2007; 14(2): 147-154 doi: 10.1038/nsmb1192 pmid:17220898
|
21 |
Park JI, Venteicher AS, Hong JY, Choi J, Jun S, Shkreli M, Chang W, Meng Z, Cheung P, Ji H, McLaughlin M, Veenstra TD, Nusse R, McCrea PD, Artandi SE. Telomerase modulates Wnt signalling by association with target gene chromatin. Nature 2009; 460(7251): 66-72 doi: 10.1038/nature08137 pmid:19571879
|
22 |
Martinez P, Thanasoula M, Carlos AR, Gómez-López G, Tejera AM, Schoeftner S, Dominguez O, Pisano DG, Tarsounas M, Blasco MA. Mammalian Rap1 controls telomere function and gene expression through binding to telomeric and extratelomeric sites. Nat Cell Biol 2010; 12(8): 768-780 doi: 10.1038/ncb2081 pmid:20622869
|
23 |
Simonet T, Zaragosi LE, Philippe C, Lebrigand K, Schouteden C, Augereau A, Bauwens S, Ye J, Santagostino M, Giulotto E, Magdinier F, Horard B, Barbry P, Waldmann R, Gilson E. The human TTAGGG repeat factors 1 and 2 bind to a subset of interstitial telomeric sequences and satellite repeats. Cell Res 2011; 21(7): 1028-1038 doi: 10.1038/cr.2011.40 pmid:21423270
|
24 |
Yang D, Xiong Y, Kim H, He Q, Li Y, Chen R, Songyang Z. Human telomeric proteins occupy selective interstitial sites. Cell Res 2011; 21(7): 1013-1027 doi: 10.1038/cr.2011.39 pmid:21423278
|
25 |
Brunori M, Luciano P, Gilson E, Géli V. The telomerase cycle: normal and pathological aspects. J Mol Med (Berl) 2005; 83(4): 244-257 doi: 10.1007/s00109-004-0616-2 pmid:15630594
|
26 |
Rudolph KL, Millard M, Bosenberg MW, DePinho RA. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat Genet 2001; 28(2): 155-159 doi: 10.1038/88871 pmid:11381263
|
27 |
Klapper W, Krams M, Qian W, Janssen D, Parwaresch R. Telomerase activity in B-cell non-Hodgkin lymphomas is regulated by hTERT transcription and correlated with telomere-binding protein expression but uncoupled from proliferation. Br J Cancer 2003; 89(4): 713-719 doi: 10.1038/sj.bjc.6601112 pmid:12915884
|
28 |
Nakanishi K, Kawai T, Kumaki F, Hiroi S, Mukai M, Ikeda E, Koering CE, Gilson E. Expression of mRNAs for telomeric repeat binding factor (TRF)-1 and TRF2 in atypical adenomatous hyperplasia and adenocarcinoma of the lung. Clin Cancer Res 2003; 9(3): 1105-1111 pmid:12631614
|
29 |
Bellon M, Datta A, Brown M, Pouliquen JF, Couppie P, Kazanji M, Nicot C. Increased expression of telomere length regulating factors TRF1, TRF2 and TIN2 in patients with adult T-cell leukemia. Int J Cancer 2006; 119(9): 2090-2097 doi: 10.1002/ijc.22026 pmid:16786598
|
30 |
Biroccio A, Rizzo A, Elli R, Koering CE, Belleville A, Benassi B, Leonetti C, Stevens MF, D’Incalci M, Zupi G, Gilson E. TRF2 inhibition triggers apoptosis and reduces tumourigenicity of human melanoma cells. Eur J Cancer 2006; 42(12): 1881-1888 pmid:16750909
|
31 |
Blanco R, Mu?oz P, Flores JM, Klatt P, Blasco MA. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev 2007; 21(2): 206-220 doi: 10.1101/gad.406207 pmid:17234886
|
32 |
Biroccio A, Cherfils-Vicini J, Augereau A, Pinte S, Bauwens S, Ye J, Simonet T, Horard B, Jamet K, Cervera L, Mendez-Bermudez A, Poncet D, Grataroli R, de Rodenbeeke CT, Salvati E, Rizzo A, Zizza P, Ricoul M, Cognet C, Kuilman T, Duret H, Lépinasse F, Marvel J, Verhoeyen E, Cosset FL, Peeper D, Smyth MJ, Londo?o-Vallejo A, Sabatier L, Picco V, Pages G, Scoazec JY, Stoppacciaro A, Leonetti C, Vivier E, Gilson E. TRF2 inhibits a cell-extrinsic pathway through which natural killer cells eliminate cancer cells. Nat Cell Biol 2013; 15(7): 818-828 doi: 10.1038/ncb2774 pmid:23792691
|
33 |
Salvati E, Leonetti C, Rizzo A, Scarsella M, Mottolese M, Galati R, Sperduti I, Stevens MF, D’Incalci M, Blasco M, Chiorino G, Bauwens S, Horard B, Gilson E, Stoppacciaro A, Zupi G, Biroccio A. Telomere damage induced by the G-quadruplex ligand RHPS4 has an antitumor effect. J Clin Invest 2007; 117(11): 3236-3247 doi: 10.1172/JCI32461 pmid:17932567
|
34 |
Gilson E, Géli V. How telomeres are replicated. Nat Rev Mol Cell Biol 2007; 8(10): 825-838 doi: 10.1038/nrm2259 pmid:17885666
|
35 |
Bao K, Cohen SN. Reverse transcriptase activity innate to DNA polymerase I and DNA topoisomerase I proteins of Streptomyces telomere complex. Proc Natl Acad Sci USA 2004; 101(40): 14361-14366 doi: 10.1073/pnas.0404386101 pmid:15353591
|
36 |
Bankhead T, Kobryn K, Chaconas G. Unexpected twist: harnessing the energy in positive supercoils to control telomere resolution. Mol Microbiol 2006; 62(3): 895-905 doi: 10.1111/j.1365-2958.2006.05423.x pmid:16999829
|
37 |
Germe T, Miller K, Cooper JP. A non-canonical function of topoisomerase II in disentangling dysfunctional telomeres. EMBO J 2009; 28(18): 2803-2811 doi: 10.1038/emboj.2009.223 pmid:19680223
|
38 |
Klapper W, Qian W, Schulte C, Parwaresch R. DNA damage transiently increases TRF2 mRNA expression and telomerase activity. Leukemia 2003; 17(10): 2007-2015 doi: 10.1038/sj.leu.2403086 pmid:14513051
|
39 |
Zhang YW, Zhang ZX, Miao ZH, Ding J. The telomeric protein TRF2 is critical for the protection of A549 cells from both telomere erosion and DNA double-strand breaks driven by salvicine. Mol Pharmacol 2008; 73(3): 824-832 doi: 10.1124/mol.107.039081 pmid:18025071
|
40 |
Su CH, Chu WC, Lan KH, Li CP, Chao Y, Lin HC, Lee SD, Tsai YC, Lee WP. Gemcitabine causes telomere attrition by stabilizing TRF2. Eur J Cancer 2012; 48(18): 3465-3474 doi: 10.1016/j.ejca.2012.04.015 pmid:22704123
|
41 |
Fumagalli M, Rossiello F, Clerici M, Barozzi S, Cittaro D, Kaplunov JM, Bucci G, Dobreva M, Matti V, Beausejour CM, Herbig U, Longhese MP, d’Adda di Fagagna F. Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat Cell Biol 2012; 14(4): 355-365 doi: 10.1038/ncb2466 pmid:22426077
|
42 |
Schr?der CP, Wisman GB, de Jong S, van der Graaf WT, Ruiters MH, Mulder NH, de Leij LF, van der Zee AG, de Vries EG. Telomere length in breast cancer patients before and after chemotherapy with or without stem cell transplantation. Br J Cancer 2001; 84(10): 1348-1353 doi: 10.1054/bjoc.2001.1803 pmid:11355946
|
43 |
Rufer N, Brümmendorf TH, Chapuis B, Helg C, Lansdorp PM, Roosnek E. Accelerated telomere shortening in hematological lineages is limited to the first year following stem cell transplantation. Blood 2001; 97(2): 575-577 doi: 10.1182/blood.V97.2.575 pmid:11154240
|
44 |
Rocci A, Ricca I, Dellacasa C, Longoni P, Compagno M, Francese R, Lobetti Bodoni C, Manzini P, Caracciolo D, Boccadoro M, Ferrero D, Ladetto M, Carlo-Stella C, Tarella C. Long-term lymphoma survivors following high-dose chemotherapy and autograft: evidence of permanent telomere shortening in myeloid cells, associated with marked reduction of bone marrow hematopoietic stem cell reservoir. Exp Hematol 2007; 35(4): 673-681 doi: 10.1016/j.exphem.2006.12.006 pmid:17379077
|
45 |
Yoon SY, Sung HJ, Park KH, Choi IK, Kim SJ, Oh SC, Seo JH, Choi CW, Kim BS, Shin SW, Kim YH, Kim JS. Telomere length shortening of peripheral blood mononuclear cells in solid-cancer patients undergoing standard-dose chemotherapy might be correlated with good treatment response and neutropenia severity. Acta Haematol 2007; 118(1): 30-37 doi: 10.1159/000101558 pmid:17429195
|
46 |
Buttiglieri S, Ruella M, Risso A, Spatola T, Silengo L, Avvedimento EV, Tarella C. The aging effect of chemotherapy on cultured human mesenchymal stem cells. Exp Hematol 2011; 39(12): 1171-1181 doi: 10.1016/j.exphem.2011.08.009 pmid:21864489
|
47 |
González-Suárez E, Samper E, Flores JM, Blasco MA. Telomerase-deficient mice with short telomeres are resistant to skin tumorigenesis. Nat Genet 2000; 26(1): 114-117 doi: 10.1038/79089 pmid:10973262
|
48 |
Feldser DM, Greider CW. Short telomeres limit tumor progression in vivo by inducing senescence. Cancer Cell 2007; 11(5): 461-469 doi: 10.1016/j.ccr.2007.02.026 pmid:17433785
|
49 |
Mauch PM, Kalish LA, Marcus KC, Coleman CN, Shulman LN, Krill E, Come S, Silver B, Canellos GP, Tarbell NJ. Second malignancies after treatment for laparotomy staged IA-IIIB Hodgkin’s disease: long-term analysis of risk factors and outcome. Blood 1996; 87(9): 3625-3632 pmid:8611686
|
50 |
M’kacher R, Bennaceur-Griscelli A, Girinsky T, Koscielny S, Delhommeau F, Dossou J, Violot D, Leclercq E, Courtier MH, Béron-Gaillard N, Assaf E, Ribrag V, Bourhis J, Feneux D, Bernheim A, Parmentier C, Carde P. Telomere shortening and associated chromosomal instability in peripheral blood lymphocytes of patients with Hodgkin’s lymphoma prior to any treatment are predictive of second cancers. Int J Radiat Oncol Biol Phys 2007; 68(2): 465-471 doi: 10.1016/j.ijrobp.2007.01.050 pmid:17418962
|
51 |
Smith RE. Risk for the development of treatment-related acute myelocytic leukemia and myelodysplastic syndrome among patients with breast cancer: review of the literature and the National Surgical Adjuvant Breast and Bowel Project experience. Clin Breast Cancer 2003; 4(4): 273-279
|
52 |
Soleimani R, Heytens E, Darzynkiewicz Z, Oktay K. Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging (Albany NY) 2011; 3(8): 782-793 pmid:21869459
|
53 |
Deprez S, Amant F, Smeets A, Peeters R, Leemans A, Van Hecke W, Verhoeven JS, Christiaens MR, Vandenberghe J, Vandenbulcke M, Sunaert S. Longitudinal assessment of chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning. J Clin Oncol 2012; 30(3): 274-281 doi: 10.1200/JCO.2011.36.8571 pmid:22184379
|
54 |
Quesnel C, Savard J, Ivers H. Cognitive impairments associated with breast cancer treatments: results from a longitudinal study. Breast Cancer Res Treat 2009; 116(1): 113-123 doi: 10.1007/s10549-008-0114-2 pmid:18629633
|
55 |
Zhang P, Pazin MJ, Schwartz CM, Becker KG, Wersto RP, Dilley CM, Mattson MP. Nontelomeric TRF2-REST interaction modulates neuronal gene silencing and fate of tumor and stem cells. Curr Biol 2008; 18(19): 1489-1494 doi: 10.1016/j.cub.2008.08.048 pmid:18818083
|
56 |
Poncet D, Belleville A, t’kint de Roodenbeke C, Roborel de Climens A, Ben Simon E, Merle-Beral H, Callet-Bauchu E, Salles G, Sabatier L, Delic J, Gilson E. Changes in the expression of telomere maintenance genes suggest global telomere dysfunction in B-chronic lymphocytic leukemia. Blood 2008; 111(4): 2388-2391 doi: 10.1182/blood-2007-09-111245 pmid:18077792
|
57 |
Augereau A, T’kint de Roodenbeke C, Simonet T, Bauwens S, Horard B, Callanan M, Leroux D, Jallades L, Salles G, Gilson E, Poncet D. Telomeric damage in early stage of chronic lymphocytic leukemia correlates with shelterin dysregulation. Blood 2011; 118(5): 1316-1322 doi: 10.1182/blood-2010-07-295774 pmid:21355086
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