MicroRNA-34a promotes DNA damage and mitotic catastrophe

Cell Cycle

Volumn 12, Issue 22, 2013, Pages 3500-3511

  Kofman, Alexander V ^a,b   Kim, Jungeun ^a   Park, So Yeon ^a   Dupart, Evan ^a   Letson, Christopher ^a   Bao, Yongde ^a   Ding, Kai ^c   Chen, Quan ^c   Schiff, David ^d   Larner, James ^c   Abounader, Roger ^a,d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b Medical Center LDS 2   (Russian Federation)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

53BP1; Brain tumors; DNA damage; MicroRNA 34a; Mitosis; Mitotic catastrophe

Indexed keywords

DOUBLE STRANDED DNA; LENTIVIRUS VECTOR; MICRORNA 34A; PROTEIN P53;

ANAPHASE; ARTICLE; CANCER CELL CULTURE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL POPULATION; CHROMOSOME BREAKAGE; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; GLIOBLASTOMA; GLIOMA CELL; MALIGNANT NEOPLASTIC DISEASE; METAPHASE; MITOSIS; OXIDATIVE STRESS; RADIOSENSITIVITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STABLE EXPRESSION; TUMOR SUPPRESSOR GENE; X IRRADIATION;

53BP1; BRAIN TUMORS; DNA DAMAGE; MICRORNA-34A; MITOSIS; MITOTIC CATASTROPHE;

APOPTOSIS; CELL LINE, TUMOR; DNA DAMAGE; DOWN-REGULATION; HUMANS; MICRORNAS; MITOSIS; MUTATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84890335663     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.26459     Document Type: Article

References (53)

1. Thompson LH. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutat Res 2012; 751:158-246; PMID:22743550; http://dx.doi.org/10. 1016/j. mrrev.2012.06.002
2. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359:492-507; PMID:18669428; http://dx.doi.org/10.1056/NEJMra0708126
3. Iwabuchi K, Bartel PL, Li B, Marraccino R, Fields S. Two cellular proteins that bind to wild-type but not mutant p53. Proc Natl Acad Sci U S A 1994; 91:6098-102; PMID:8016121; http://dx.doi.org/10.1073/pnas.91.13.6098 (Pubitemid 24188290)
4. Kobayashi J, Iwabuchi K, Miyagawa K, Sonoda E, Suzuki K, Takata M, Tauchi H. Current topics in DNA double-strand break repair. J Radiat Res 2008; 49:93-103; PMID:18285658; http://dx.doi.org/10.1269/jrr.07130 (Pubitemid 351468636)
5. Zimmermann M, Lottersberger F, Buonomo SB, Sfeir A, de Lange T. 53BP1 regulates DSB repair using Rif1 to control 5? end resection. Science 2013; 339:700-4; PMID:23306437; http://dx.doi.org/10.1126/science.1231573
6. Dimitrova N, Chen YC, Spector DL, de Lange T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 2008; 456:524-8; PMID:18931659; http://dx.doi.org/10.1038/nature07433 (Pubitemid 50304845)
7. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N, et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 2002; 4:993-7; PMID:12447390; http://dx.doi.org/10.1038/ncb884 (Pubitemid 35469431)
8. Wang B, Matsuoka S, Carpenter PB, Elledge SJ. 53BP1, a mediator of the DNA damage checkpoint. Science 2002; 298:1435-8; PMID:12364621; http://dx.doi.org/10.1126/science.1076182 (Pubitemid 35346146)
9. Stewart GS, Stankovic T, Byrd PJ, Wechsler T, Miller ES, Huissoon A, Drayson MT, West SC, Elledge SJ, Taylor AM. RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling. Proc Natl Acad Sci U S A 2007; 104:16910-5; PMID:17940005; http://dx.doi.org/10.1073/pnas.0708408104 (Pubitemid 350210964)
10. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, Grfte M, Chan KL, Hickson ID, Bartek J, et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 2011; 13:243-53; PMID:21317883; http://dx.doi.org/10.1038/ ncb2201
11. Hermeking H. p53 enters the microRNA world. Cancer Cell 2007; 12:414-8; PMID:17996645; http://dx.doi.org/10.1016/j.ccr.2007.10.028 (Pubitemid 350046413)
12. Cha YH, Kim NH, Park C, Lee I, Kim HS, Yook JI. MiRNA-34 intrinsically links p53 tumor suppressor and Wnt signaling. Cell Cycle 2012; 11:1273-81; PMID:22421157; http://dx.doi.org/10.4161/cc.19618
13. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D, Purow B, Abounader R. microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 2010; 9:1031-6; PMID:20190569; http://dx.doi.org/10.4161/cc.9. 6.10987
14. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E, Marcinkiewicz L, Jiang J, Yang Y, Schmittgen TD, et al. microRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009; 69:7569-76; PMID:19773441; http://dx.doi.org/10.1158/0008-5472.CAN-09-0529
15. Siemens H, Jackstadt R, Kaller M, Hermeking H. Repression of c-Kit by p53 is mediated by miR-34 and is associated with reduced chemoresistance, migration and stemness. Oncotarget 2013; PMID:24009080
16. Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U, Hermeking H. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 2011; 10:4256-71; PMID:22134354; http://dx.doi.org/10.4161/cc.10.24.18552
17. Akao Y, Noguchi S, Iio A, Kojima K, Takagi T, Naoe T. Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Lett 2011; 300:197-204; PMID:21067862; http://dx.doi.org/10. 1016/j. canlet.2010.10.006
18. Kojima K, Fujita Y, Nozawa Y, Deguchi T, Ito M. MiR-34a attenuates paclitaxel-resistance of hormonerefractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate 2010; 70:1501-12; PMID:20687223; http://dx.doi.org/10.1002/pros.21185
19. Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, Mendell JT, Jiang J, Schmittgen TD, Patel T. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 2006; 130:2113-29; PMID:16762633; http://dx.doi.org/10.1053/j. gastro.2006.02.057 (Pubitemid 43816961)
20. Nakatani F, Ferracin M, Manara MC, Ventura S, Del Monaco V, Ferrari S, et al. miR-34a predicts survival of Ewing's sarcoma patients and directly influences cell chemosensitivity and malignancy. J Pathol 2011
21. Vinall RL, Ripoll AZ, Wang S, Pan CX, deVere White RW. MiR-34a chemosensitizes bladder cancer cells to cisplatin treatment regardless of p53-Rb pathway status. Int J Cancer 2012; 130:2526-38; PMID:21702042
22. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 26:745-52; PMID:17540599; http://dx.doi.org/10.1016/j. molcel.2007.05.010 (Pubitemid 46856245)
23. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, Oren M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007; 26:731-43; PMID:17540598; http://dx.doi.org/10.1016/j. molcel.2007.05.017 (Pubitemid 46856247)
24. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447:1130-4; PMID:17554337; http://dx.doi.org/10.1038/ nature05939 (Pubitemid 47014436)
25. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, Venere M, Ditullio RA Jr., Kastrinakis NG, Levy B, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434:907-13; PMID:15829965; http://dx.doi.org/10.1038/ nature03485 (Pubitemid 40559004)
26. Nakamura AJ, Redon CE, Bonner WM, Sedelnikova OA. Telomere-dependent and telomere-independent origins of endogenous DNA damage in tumor cells. Aging (Albany NY) 2009; 1:212-8; PMID:20157510
27. Rodier F, Muñoz DP, Teachenor R, Chu V, Le O, Bhaumik D, Coppé JP, Campeau E, Beauséjour CM, Kim SH, et al. DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci 2011; 124:68-81; PMID:21118958; http://dx.doi.org/10.1242/jcs.071340
28. Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR, Fraser P, Jackson SP. Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 2011; 193:97-108; PMID:21444690; http://dx.doi.org/10.1083/jcb.201011083
29. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003; 426:194-8; PMID:14608368; http://dx.doi.org/10.1038/nature02118 (Pubitemid 37442589)
30. Takai H, Smogorzewska A, de Lange T. DNA damage foci at dysfunctional telomeres. Curr Biol 2003; 13:1549-56; PMID:12956959; http://dx.doi.org/10.1016/ S0960-9822(03)00542-6 (Pubitemid 37078413)
31. Walters DK, Wu X, Tschumper RC, Arendt BK, Huddleston PM, Henderson KJ, et al. Evidence for ongoing DNA damage in multiple myeloma cells as revealed by constitutive phosphorylation of H2AX. Leukemia: official journal of the Leukemia Society of America. Leukemia Research Fund, UK 2011; 25:1344-53; http://dx.doi.org/10.1038/leu.2011.94
32. Quinlan GJ, Gutteridge JM. Hydroxyl radical generation by the tetracycline antibiotics with free radical damage to DNA, lipids and carbohydrate in the presence of iron and copper salts. Free Radic Biol Med 1988; 5:341-8; PMID:2855734; http://dx.doi.org/10.1016/0891-5849(88)90106-2 (Pubitemid 19024284)
33. Quinlan GJ, Gutteridge JM. DNA base damage by beta-lactam, tetracycline, bacitracin and rifamycin antibacterial antibiotics. Biochem Pharmacol 1991; 42:1595-9; PMID:1930286; http://dx.doi.org/10.1016/0006-2952(91)90429-9
34. Ganem NJ, Pellman D. Linking abnormal mitosis to the acquisition of DNA damage. J Cell Biol 2012; 199:871-81; PMID:23229895; http://dx.doi.org/10.1083/ jcb.201210040
35. Giunta S, Belotserkovskaya R, Jackson SP. DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 2010; 190:197-207; PMID:20660628; http://dx.doi.org/10.1083/jcb.200911156
36. Nelson G, Buhmann M, von Zglinicki T. DNA damage foci in mitosis are devoid of 53BP1. Cell Cycle 2009; 8:3379-83; PMID:19806024; http://dx.doi.org/ 10.4161/cc.8.20.9857
37. Hayashi MT, Karlseder J. DNA damage associated with mitosis and cytokinesis failure. Oncogene 2013; PMID:23318447; http://dx.doi.org/10.1038/ onc.2012.615
38. Zhang W, Peng G, Lin SY, Zhang P. DNA damage response is suppressed by the high cyclin-dependent kinase 1 activity in mitotic mammalian cells. J Biol Chem 2011; 286:35899-905; PMID:21878640; http://dx.doi.org/10.1074/jbc.M111. 267690
39. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008; 15:1153-62; PMID:18404154; http://dx.doi.org/10.1038/cdd.2008.47 (Pubitemid 351850968)
40. Jullien D, Vagnarelli P, Earnshaw WC, Adachi Y. Kinetochore localisation of the DNA damage response component 53BP1 during mitosis. J Cell Sci 2002; 115:71-9; PMID:11801725 (Pubitemid 34105530)
41. Akhter S, Richie CT, Deng JM, Brey E, Zhang X, Patrick C Jr., Behringer RR, Legerski RJ. Deficiency in SNM1 abolishes an early mitotic checkpoint induced by spindle stress. Mol Cell Biol 2004; 24:10448-55; PMID:15542852; http://dx.doi.org/10.1128/MCB.24.23.10448-10455.2004 (Pubitemid 39507881)
42. Xia Z, Morales JC, Dunphy WG, Carpenter PB. Negative cell cycle regulation and DNA damageinducible phosphorylation of the BRCT protein 53BP1. J Biol Chem 2001; 276:2708-18; PMID:11042216; http://dx.doi.org/10.1074/jbc. M007665200
43. Perfettini JL, Nardacci R, Séror C, Raza SQ, Sepe S, Saïdi H, Brottes F, Amendola A, Subra F, Del Nonno F, et al. 53BP1 represses mitotic catastrophe in syncytia elicited by the HIV-1 envelope. Cell Death Differ 2010; 17:811-20; PMID:19876065; http://dx.doi.org/10.1038/cdd.2009.159
44. Duan W, Xu Y, Dong Y, Cao L, Tong J, Zhou X. Ectopic expression of miR-34a enhances radiosensitivity of non-small cell lung cancer cells, partly by suppressing the LyGDI signaling pathway. J Radiat Res 2013; 54:611-9; PMID:23349340; http://dx.doi.org/10.1093/jrr/rrs136
45. Liu C, Zhou C, Gao F, Cai S, Zhang C, Zhao L, Zhao F, Cao F, Lin J, Yang Y, et al. MiR-34a in age and tissue related radio-sensitivity and serum miR-34a as a novel indicator of radiation injury. Int J Biol Sci 2011; 7:221-33; PMID:21448283; http://dx.doi.org/10.7150/ijbs.7.221
46. Ghawanmeh T, Thunberg U, Castro J, Murray F, Laytragoon-Lewin N. miR-34a expression, cell cycle arrest and cell death of malignant mesothelioma cells upon treatment with radiation, docetaxel or combination treatment. Oncology 2011; 81:330-5; PMID:22237142; http://dx.doi.org/10.1159/000334237
47. Wang B, Li D, Kovalchuk O. p53 Ser15 phosphorylation and histone modifications contribute to IR-induced miR-34a transcription in mammary epithelial cells. Cell Cycle 2013; 12:2073-83; PMID:23759592; http://dx.doi.org/10.4161/cc.25135
48. Wong MY, Yu Y, Walsh WR, Yang JL. microRNA-34 family and treatment of cancers with mutant or wildtype p53 (Review). Int J Oncol 2011; 38:1189-95; PMID:21399872
49. Kato M, Paranjape T, Müller RU, Nallur S, Gillespie E, Keane K, Esquela-Kerscher A, Weidhaas JB, Slack FJ. The mir-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells. Oncogene 2009; 28:2419-24; PMID:19421141; http://dx.doi.org/10. 1038/onc.2009.106
50. Deckbar D, Birraux J, Krempler A, Tchouandong L, Beucher A, Walker S, Stiff T, Jeggo P, Löbrich M. Chromosome breakage after G2 checkpoint release. J Cell Biol 2007; 176:749-55; PMID:17353355; http://dx.doi.org/10.1083/ jcb.200612047 (Pubitemid 46425534)
51. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA doublestrand breaks. J Cell Biol 2000; 151:1381-90; PMID:11134068; http://dx.doi.org/10.1083/ jcb.151.7.1381 (Pubitemid 32047588)
52. Fang Z, Rajewsky N. The impact of miRNA target sites in coding sequences and in 3'UTRs. PLoS One 2011; 6:e18067; PMID:21445367; http://dx.doi.org/10. 1371/journal.pone.0018067
53. Vitale I, Galluzzi L, Castedo M, Kroemer G. Mitotic catastrophe: a mechanism for avoiding genomic instability. Nat Rev Mol Cell Biol 2011; 12:385-92; PMID:21527953; http://dx.doi.org/10.1038/nrm3115