Beclin 1 and UVRAG confer protection from radiation-induced DNA damage and maintain centrosome stability in colorectal cancer cells

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Park, Jae Myung ^a   Tougeron, David ^a   Huang, Shengbing ^a   Okamoto, Koichi ^a   Sinicrope, Frank A ^a  

^a MAYO CLINIC CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; AUTOPHAGY PROTEIN 5; BECLIN 1; CASPASE 3; HISTONE H2AX; RAD51 PROTEIN; SMALL INTERFERING RNA; APOPTOSIS REGULATORY PROTEIN; ATG5 PROTEIN, HUMAN; BECN1 PROTEIN, HUMAN; FLUOROURACIL; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BINDING; RAD51 PROTEIN, HUMAN; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN; UVRAG PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; ATG5 GENE; AUTOPHAGY; BECLIN 1 GENE; CELL COUNT; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CENTROSOME; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; GENE; GENE EXPRESSION; GENE INTERACTION; GENE REPRESSION; GENE SILENCING; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IONIZING RADIATION; LC3 GENE; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RADIOSENSITIVITY; REGULATORY MECHANISM; RNA SEQUENCE; USP10 GENE; UVRAG GENE; CELL NUCLEUS; COLORECTAL TUMOR; DNA DAMAGE; DRUG EFFECTS; GAMMA RADIATION; METABOLISM; PATHOLOGY; RADIATION RESPONSE; TUMOR CELL LINE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE, TUMOR; CELL NUCLEUS; CENTROSOME; COLORECTAL NEOPLASMS; CYTOPROTECTION; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; FLUOROURACIL; GAMMA RAYS; GENE KNOCKDOWN TECHNIQUES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PROTEIN BINDING; RAD51 RECOMBINASE; TUMOR SUPPRESSOR PROTEINS;

EID: 84903529027     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100819     Document Type: Article

References (40)

1. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721. (Pubitemid 32004796)
2. Sinha S, Levine B (2008) The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 27 Suppl 1: S137-148.
3. Itakura E, Kishi C, Inoue K, Mizushima N (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19: 5360-5372.
4. Liang C, Feng P, Ku B, Dotan I, Canaani D, et al. (2006) Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nature cell biology 8: 688-699.
5. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, et al. (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-1820. (Pubitemid 38063704)
6. Aita VM, Liang XH, Murty VV, Pincus DL, Yu W, et al. (1999) Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59: 59-65. (Pubitemid 29339873)
7. Ionov Y, Nowak N, Perucho M, Markowitz S, Cowell JK (2004) Manipulation of nonsense mediated decay identifies gene mutations in colon cancer Cells with microsatellite instability. Oncogene 23: 639-645. (Pubitemid 38241265)
8. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, et al. (2007) Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 21: 1621-1635. (Pubitemid 47026367)
9. Yang ZJ, Chee CE, Huang S, Sinicrope FA (2011) The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 10: 1533-1541.
10. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, et al. (2007) Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117: 326-336. (Pubitemid 46203961)
11. Kuwahara Y, Oikawa T, Ochiai Y, Roudkenar MH, Fukumoto M, et al. (2011) Enhancement of autophagy is a potential modality for tumors refractory to radiotherapy. Cell Death Dis 2: e177.
12. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, et al. (2007) Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 21: 1367-1381. (Pubitemid 46871040)
13. Zhao Z, Oh S, Li D, Ni D, Pirooz SD, et al. (2012) A dual role for UVRAG in maintaining chromosomal stability independent of autophagy. Developmental cell 22: 1001-1016.
14. Mao Z, Bozzella M, Seluanov A, Gorbunova V (2008) DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells. Cell Cycle 7: 2902-2906.
15. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, et al. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Current biology: CB 10: 886-895.
16. Ganem NJ, Godinho SA, Pellman D (2009) A mechanism linking extra centrosomes to chromosomal instability. Nature 460: 278-282.
17. Fukasawa K (2007) Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7: 911-924.
18. D'Assoro AB, Lingle WL, Salisbury JL (2002) Centrosome amplification and the development of cancer. Oncogene 21: 6146-6153.
19. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, et al. (2007) Autophagy suppresses tumor progression by limiting chromosomal instability. Genes & development 21: 1367-1381. (Pubitemid 46871040)
20. Myung Park J, Huang S, Wu TT, Foster NR, Sinicrope FA (2013) Prognostic impact of Beclin 1, p62/sequestosome 1 and LC3 protein expression in colon carcinomas from patients receiving 5-fluorouracil as adjuvant chemotherapy. Cancer Biol Ther 14: 100-107.
21. Huang S, Sinicrope FA (2010) Celecoxib-induced apoptosis is enhanced by ABT-737 and by inhibition of autophagy in human colorectal cancer cells. Autophagy 6: 256-269.
22. Huang S, Okamoto K, Yu C, Sinicrope FA (2013) p62/sequestosome-1 upregulation promotes ABT-263-induced caspase-8 aggregation/activation on the autophagosome. J Biol Chem 288: 33654-33666.
23. Flatten K, Dai NT, Vroman BT, Loegering D, Erlichman C, et al. (2005) The role of checkpoint kinase 1 in sensitivity to topoisomerase I poisons. J Biol Chem 280: 14349-14355. (Pubitemid 40517339)
24. Huang S, Yang ZJ, Yu C, Sinicrope FA (2011) Inhibition of mTOR kinase by AZD8055 can antagonize chemotherapy-induced cell death through autophagy induction and down-regulation of p62/sequestosome 1. J Biol Chem 286: 40002-40012.
25. Li X, He L, Che KH, Funderburk SF, Pan L, et al. (2012) Imperfect interface of Beclin1 coiled-coil domain regulates homodimer and heterodimer formation with Atg14L and UVRAG. Nature communications 3: 662.
26. Acu ID, Liu T, Suino-Powell K, Mooney SM, D'Assoro AB, et al. (2010) Coordination of centrosome homeostasis and DNA repair is intact in MCF-7 and disrupted in MDA-MB 231 breast cancer cells. Cancer research 70: 3320-3328.
27. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, et al. (2008) GammaH2AX and cancer. Nat Rev Cancer 8: 957-967.
28. Abraham RT (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 15: 2177-2196.
29. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506. (Pubitemid 36168436)
30. 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: 5720-5728.
31. Bothmer A, Robbiani DF, Di Virgilio M, Bunting SF, Klein IA, et al. (2011) Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol Cell 42: 319-329.
32. Suwaki N, Klare K, Tarsounas M (2011) RAD51 paralogs: roles in DNA damage signalling, recombinational repair and tumorigenesis. Seminars in cell & developmental biology 22: 898-905.
33. Liu J, Xia H, Kim M, Xu L, Li Y, et al. (2010) Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 147: 223-234.
34. Zhao Z, Ni D, Ghozalli I, Pirooz SD, Ma B, et al. (2012) UVRAG: at the crossroad of autophagy and genomic stability. Autophagy 8: 1392-1393.
35. Bourke E, Dodson H, Merdes A, Cuffe L, Zachos G, et al. (2007) DNA damage induces Chk1-dependent centrosome amplification. EMBO Rep 8: 603-609. (Pubitemid 47214716)
36. Sato N, Mizumoto K, Nakamura M, Ueno H, Minamishima YA, et al. (2000) A possible role for centrosome overduplication in radiation-induced cell death. Oncogene 19: 5281-5290.
37. Ward IM, Minn K, van Deursen J, Chen J (2003) p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol Cell Biol 23: 2556-2563. (Pubitemid 36351034)
38. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, et al. (2006) Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nature cell biology 8: 1124-1132. (Pubitemid 44473608)
39. Fremont S, Gerard A, Galloux M, Janvier K, Karess RE, et al. (2013) Beclin-1 is required for chromosome congression and proper outer kinetochore assembly. EMBO reports 14: 364-372.
40. Liang XH, Yu J, Brown K, Levine B (2001) Beclin 1 contains a leucine-rich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res 61: 3443-3449. (Pubitemid 32695039)