SGO1 is Involved in the DNA Damage Response in MYCN-amplified Neuroblastoma Cells

Overview

Journal Sci Rep

Specialty Science

Date 2016 Aug 20

PMID 27539729

Citations 11

Authors

Yuko Murakami-Tonami

Haruna Ikeda

Ryota Yamagishi

Mao Inayoshi

Shiho Inagaki

Satoshi Kishida

Yosuke Komata

Jan Koster

Ichiro Takeuchi

Yutaka Kondo

Tohru Maeda

Yoshitaka Sekido

Hiroshi Murakami

Kenji Kadomatsu

Affiliations

Soon will be listed here.

Abstract

Shugoshin 1 (SGO1) is required for accurate chromosome segregation during mitosis and meiosis; however, its other functions, especially at interphase, are not clearly understood. Here, we found that downregulation of SGO1 caused a synergistic phenotype in cells overexpressing MYCN. Downregulation of SGO1 impaired proliferation and induced DNA damage followed by a senescence-like phenotype only in MYCN-overexpressing neuroblastoma cells. In these cells, SGO1 knockdown induced DNA damage, even during interphase, and this effect was independent of cohesin. Furthermore, MYCN-promoted SGO1 transcription and SGO1 expression tended to be higher in MYCN- or MYC-overexpressing cancers. Together, these findings indicate that SGO1 plays a role in the DNA damage response in interphase. Therefore, we propose that SGO1 represents a potential molecular target for treatment of MYCN-amplified neuroblastoma.

Citing Articles

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References

Tanno Y, Kitajima T, Honda T, Ando Y, Ishiguro K, Watanabe Y . Phosphorylation of mammalian Sgo2 by Aurora B recruits PP2A and MCAK to centromeres. Genes Dev. 2010; 24(19):2169-79. PMC: 2947769. DOI: 10.1101/gad.1945310. View

Hoglund A, Stromvall K, Li Y, Forshell L, Nilsson J . Chk2 deficiency in Myc overexpressing lymphoma cells elicits a synergistic lethal response in combination with PARP inhibition. Cell Cycle. 2011; 10(20):3598-607. PMC: 3266184. DOI: 10.4161/cc.10.20.17887. View

Giunta S, Belotserkovskaya R, Jackson S . DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol. 2010; 190(2):197-207. PMC: 2930281. DOI: 10.1083/jcb.200911156. View

Li Z, Van Calcar S, Qu C, Cavenee W, Zhang M, Ren B . A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc Natl Acad Sci U S A. 2003; 100(14):8164-9. PMC: 166200. DOI: 10.1073/pnas.1332764100. View

Yang J, Ikezoe T, Nishioka C, Yokoyama A . A novel treatment strategy targeting shugoshin 1 in hematological malignancies. Leuk Res. 2012; 37(1):76-82. DOI: 10.1016/j.leukres.2012.10.002. View

Verzijlbergen K, Nerusheva O, Kelly D, Kerr A, Clift D, de Lima Alves F . Shugoshin biases chromosomes for biorientation through condensin recruitment to the pericentromere. Elife. 2014; 3:e01374. PMC: 3910079. DOI: 10.7554/eLife.01374. View

Murga M, Campaner S, Lopez-Contreras A, Toledo L, Soria R, Montana M . Exploiting oncogene-induced replicative stress for the selective killing of Myc-driven tumors. Nat Struct Mol Biol. 2011; 18(12):1331-1335. PMC: 4894468. DOI: 10.1038/nsmb.2189. View

Rottmann S, Wang Y, Nasoff M, Deveraux Q, Quon K . A TRAIL receptor-dependent synthetic lethal relationship between MYC activation and GSK3beta/FBW7 loss of function. Proc Natl Acad Sci U S A. 2005; 102(42):15195-200. PMC: 1257707. DOI: 10.1073/pnas.0505114102. View

Kessler J, Kahle K, Sun T, Meerbrey K, Schlabach M, Schmitt E . A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis. Science. 2011; 335(6066):348-53. PMC: 4059214. DOI: 10.1126/science.1212728. View

10.

Guillou E, Ibarra A, Coulon V, Casado-Vela J, Rico D, Casal I . Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 2010; 24(24):2812-22. PMC: 3003199. DOI: 10.1101/gad.608210. View

11.

Matsuura S, Kahyo T, Shinmura K, Iwaizumi M, Yamada H, Funai K . SGOL1 variant B induces abnormal mitosis and resistance to taxane in non-small cell lung cancers. Sci Rep. 2013; 3:3012. PMC: 3804856. DOI: 10.1038/srep03012. View

12.

Meyer N, Penn L . Reflecting on 25 years with MYC. Nat Rev Cancer. 2008; 8(12):976-90. DOI: 10.1038/nrc2231. View

13.

Chetaille P, Preuss C, Burkhard S, Cote J, Houde C, Castilloux J . Mutations in SGOL1 cause a novel cohesinopathy affecting heart and gut rhythm. Nat Genet. 2014; 46(11):1245-9. DOI: 10.1038/ng.3113. View

14.

Beierle E, Trujillo A, Nagaram A, Kurenova E, Finch R, Ma X . N-MYC regulates focal adhesion kinase expression in human neuroblastoma. J Biol Chem. 2007; 282(17):12503-16. DOI: 10.1074/jbc.M701450200. View

15.

Losada A . Cohesin in cancer: chromosome segregation and beyond. Nat Rev Cancer. 2014; 14(6):389-93. DOI: 10.1038/nrc3743. View

16.

Menssen A, Hermeking H . Characterization of the c-MYC-regulated transcriptome by SAGE: identification and analysis of c-MYC target genes. Proc Natl Acad Sci U S A. 2002; 99(9):6274-9. PMC: 122939. DOI: 10.1073/pnas.082005599. View

17.

Kim J, Krasieva T, LaMorte V, Taylor A, Yokomori K . Specific recruitment of human cohesin to laser-induced DNA damage. J Biol Chem. 2002; 277(47):45149-53. DOI: 10.1074/jbc.M209123200. View

18.

Wang Y, Engels I, Knee D, Nasoff M, Deveraux Q, Quon K . Synthetic lethal targeting of MYC by activation of the DR5 death receptor pathway. Cancer Cell. 2004; 5(5):501-12. DOI: 10.1016/s1535-6108(04)00113-8. View

19.

Zanconato F, Forcato M, Battilana G, Azzolin L, Quaranta E, Bodega B . Genome-wide association between YAP/TAZ/TEAD and AP-1 at enhancers drives oncogenic growth. Nat Cell Biol. 2015; 17(9):1218-27. PMC: 6186417. DOI: 10.1038/ncb3216. View

20.

Chiang Y, Teng S, Su Y, Hsieh F, Wu K . c-Myc directly regulates the transcription of the NBS1 gene involved in DNA double-strand break repair. J Biol Chem. 2003; 278(21):19286-91. DOI: 10.1074/jbc.M212043200. View