1,541
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Repression of the SUMO-conjugating enzyme UBC9 is associated with lowered double minutes and reduced tumor progression

, , , , , , , , , , , , , , & ORCID Icon show all
Article: 2323768 | Received 30 Oct 2023, Accepted 22 Feb 2024, Published online: 11 Mar 2024

References

  • Qiu H, Shao ZY, Wen X, Zhang LZ. New insights of extrachromosomal DNA in tumorigenesis and therapeutic resistance of cancer. Am J Cancer Res. 2020;10(12):4056–14.
  • Jia X, Guan R, Cui X, Zhu J, Liu P, Zhang L, Wang D, Zhang Y, Dong K, Wu J, et al. Molecular structure and evolution mechanism of two populations of double minutes in human colorectal cancer cells. J Cell Mol Med. 2020; 24(24):14205–14216. doi:10.1111/jcmm.16035.
  • Paulsen T, Kumar P, Koseoglu MM, Dutta A. Discoveries of extrachromosomal circles of DNA in normal and tumor cells. Trends Genet. 2018;34(4):270–278. doi:10.1016/j.tig.2017.12.010.
  • Burrell RA, McClelland SE, Endesfelder D, Groth P, Weller MC, Shaikh N, Domingo E, Kanu N, Dewhurst SM, Gronroos E, et al. Replication stress links structural and numerical cancer chromosomal instability. Nature. 2013;2013(4947438):492–496. doi:10.1038/nature11935.
  • Storlazzi CT, Lonoce A, Guastadisegni MC, Trombetta D, D’Addabbo P, Daniele G, L’Abbate A, Macchia G, Surace C, Kok K, et al. Gene amplification as double minutes or homogeneously staining regions in solid tumors: origin and structure. Genome Res. 2010; 20(9):1198–206. doi:10.1101/gr.106252.110.
  • Wu S, Turner KM, Nguyen N, Raviram R, Erb M, Santini J, Luebeck J, Rajkumar U, Diao Y, Li B, et al. Circular ecDNA promotes accessible chromatin and high oncogene expression. Nature. 2019;575(7784):699–703. doi:10.1038/s41586-019-1763-5.
  • Liao Z, Jiang W, Ye L, Li T, Yu X, Liu L. Classification of extrachromosomal circular DNA with a focus on the role of extrachromosomal DNA (ecDNA) in tumor heterogeneity and progression. Biochim Biophys Acta Rev Cancer. 1874;2020(1):188392. doi:10.1016/j.bbcan.2020.188392.
  • Wu S, Bafna V, Mischel PS. Extrachromosomal DNA (ecDNA) in cancer pathogenesis. Curr Opin Genet Dev. 2021. 66:78–82. doi:10.1016/j.gde.2021.01.001.
  • Kim H, Nguyen NP, Turner K, Wu S, Gujar AD, Luebeck J, Liu J, Deshpande V, Rajkumar U, Namburi S, et al. Extrachromosomal DNA is associated with oncogene amplification and poor outcome across multiple cancers. Nat Genet. 2020; 52(9):891–897. doi:10.1038/s41588-020-0678-2.
  • Zhu Y, Gujar AD, Wong CH, Tjong H, Ngan CY, Gong L, Chen YA, Kim H, Liu J, Li M, et al. Oncogenic extrachromosomal DNA functions as mobile enhancers to globally amplify chromosomal transcription. Cancer Cell. 2021;39(5):694–707 e7. doi:10.1016/j.ccell.2021.03.006.
  • Verhaak RGW, Bafna V, Mischel PS. Extrachromosomal oncogene amplification in tumour pathogenesis and evolution. Nat Rev Cancer. 2019;19(5):283–288. doi:10.1038/s41568-019-0128-6.
  • Cox D, Yuncken C, Spriggs AI. Minute chromatin bodies in malignant tumours of childhood. Lancet. 1965;1(7402):55–58. doi:10.1016/S0140-6736(65)90131-5.
  • Shoshani O, Brunner SF, Yaeger R, Ly P, Nechemia-Arbely Y, Kim DH, Fang R, Castillon GA, Yu M, Li JSZ, et al. Chromothripsis drives the evolution of gene amplification in cancer. Nature. 2021;591(7848):137–141. doi:10.1038/s41586-020-03064-z.
  • Shimizu N, Misaka N, Utani K. Nonselective DNA damage induced by a replication inhibitor results in the selective elimination of extrachromosomal double minutes from human cancer cells. Genes Chromosomes Cancer. 2007;46(10):865–74. doi:10.1002/gcc.20473.
  • Cai M, Zhang H, Hou L, Gao W, Song Y, Cui X, Li C, Guan R, Ma J, Wang X, et al. Inhibiting homologous recombination decreases extrachromosomal amplification but has no effect on intrachromosomal amplification in methotrexate-resistant colon cancer cells. Int J Cancer. 2019; 144(5):1037–1048. doi:10.1002/ijc.31781.
  • Meng X, Qi X, Guo H, Cai M, Li C, Zhu J, Chen F, Guo H, Li J, Zhao Y, et al. Novel role for non-homologous end joining in the formation of double minutes in methotrexate-resistant colon cancer cells. J Med Genet. 2015; 52(2):135–44. doi:10.1136/jmedgenet-2014-102703.
  • Yu L, Zhao Y, Quan C, Ji W, Zhu J, Huang Y, Guan R, Sun D, Jin Y, Meng X, et al. Gemcitabine eliminates double minute chromosomes from human ovarian cancer cells. PloS One. 2013; 8(8):e71988. doi:10.1371/journal.pone.0071988.
  • Canute GW, Longo SL, Longo JA, Shetler MM, Coyle TE, Winfield JA, Hahn PJ. The hydroxyurea-induced loss of double-minute chromosomes containing amplified epidermal growth factor receptor genes reduces the tumorigenicity and growth of human glioblastoma multiforme. Neurosurgery. 1998;1998(33):609–616. doi:10.1097/00006123-199803000-00031.
  • Flotho A, Melchior F. Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem. 2013;82(1):357–85. doi:10.1146/annurev-biochem-061909-093311.
  • Bergink S, Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature. 2009;458(7237):461–7. doi:10.1038/nature07963.
  • Chang HM, Yeh ETH. SUMO: from bench to bedside. Physiol Rev. 2020;100(4):1599–1619. doi:10.1152/physrev.00025.2019.
  • Zhu S, Sachdeva M, Wu F, Lu Z, Mo YY. Ubc9 promotes breast cell invasion and metastasis in a sumoylation-independent manner. Oncogene. 2010;2010(2912):1763–1772. doi:10.1038/onc.2009.459.
  • Lopez I, Chalatsi E, Ellenbroek SIJ, Andrieux A, Roux PF, Cerapio JP, Jouvion G, van Rheenen J, Seeler JS, Dejean A. An unanticipated tumor-suppressive role of the SUMO pathway in the intestine unveiled by Ubc9 haploinsufficiency. Oncogene. 2020;39(43):6692–6703. doi:10.1038/s41388-020-01457-y.
  • Sarangi P, Zhao X. SUMO-mediated regulation of DNA damage repair and responses. Trends Biochem Sci. 2015;40(4):233–42. doi:10.1016/j.tibs.2015.02.006.
  • Cancer genome atlas research, N. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;5137517:202–209. 10.1038/nature13480.
  • Seeler JS, Dejean A. SUMO and the robustness of cancer. Nat Rev Cancer. 2017;17(3):184–197. doi:10.1038/nrc.2016.143.
  • Mo YY, Yu Y, Theodosiou E, Ee PL, Beck WT. A role for Ubc9 in tumorigenesis. Oncogene. 2005;2005(2416):2677–2683. doi:10.1038/sj.onc.1208210.
  • Fang S, Qiu J, Wu Z, Bai T, Guo W. Down-regulation of UBC9 increases the sensitivity of hepatocellular carcinoma to doxorubicin. Oncotarget. 2017;8(30):49783–49795. doi:10.18632/oncotarget.17939.
  • Moschos SJ, Mo YY. Role of SUMO/Ubc9 in DNA damage repair and tumorigenesis. J Mol Histol. 2006;37(5–7):309–319. doi:10.1007/s10735-006-9030-0.
  • Li Y, Jiang X, Zhang Y, Gao Z, Liu Y, Hu J, Hu X, Li L, Shi J, Gao N. Nuclear accumulation of UBC9 contributes to SUMOylation of lamin A/C and nucleophagy in response to DNA damage. J Exp Clin Cancer Res. 2019;38(1):67. doi:10.1186/s13046-019-1048-8.
  • Mo YY, Moschos SJ. Targeting Ubc9 for cancer therapy. Expert Opin Ther Targets. 2005;9(6):1203–16. doi:10.1517/14728222.9.6.1203.
  • Mo YY, Yu Y, Ee PL, Beck WT. Overexpression of a dominant-negative mutant Ubc9 is associated with increased sensitivity to anticancer drugs. Cancer Res. 2004;64(8):2793–8. doi:10.1158/0008-5472.CAN-03-2410.
  • Kim YS, Keyser SG, Schneekloth JS Jr. Synthesis of 2‘,3’,4’-trihydroxyflavone (2-D08), an inhibitor of protein sumoylation. Bioorg Med Chem Lett. 2014;24(4):1094–1097. doi:10.1016/j.bmcl.2014.01.010.
  • Zhou P, Chen X, Li M, Tan J, Zhang Y, Yuan W, Zhou J, Wang G. 2-D08 as a SUMOylation inhibitor induced ROS accumulation mediates apoptosis of acute myeloid leukemia cells possibly through the deSumoylation of NOX2. Biochem Biophys Res Commun. 2019;513(4):1063–1069. doi:10.1016/j.bbrc.2019.04.079.
  • Zhou L, Zheng L, Hu K, Wang X, Zhang R, Zou Y, Zhong L, Wang S, Wu Y, Kang T. Sumoylation stabilizes hSSB1 and enhances the recruitment of NBS1 to DNA damage sites. Signal Transduct Target Ther. 2020;5(1):80. doi:10.1038/s41392-020-0172-4.
  • Xie M, Yu J, Ge S, Huang J, Fan X. SUMOylation homeostasis in tumorigenesis. Cancer Lett. 2020. 469:301–309. doi:10.1016/j.canlet.2019.11.004.
  • West SC. Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol. 2003;4(6):435–45. doi:10.1038/nrm1127.
  • Zou Y, Liu Y, Wu X, Shell SM. Functions of human replication protein a (RPA): from DNA replication to DNA damage and stress responses. J Cell Physiol. 2006;208(2):267–73. doi:10.1002/jcp.20622.
  • Bohm S, Bernstein KA. The role of post-translational modifications in fine-tuning BLM helicase function during DNA repair. DNA Repair (Amst). 2014. 22:123–32. doi:10.1016/j.dnarep.2014.07.007.
  • Morris JR. SUMO in the mammalian response to DNA damage. Biochem Soc Trans. 2010;38(Pt 1):92–97. doi:10.1042/BST0380092.
  • Zhang M, Jiang D, Xie X, He Y, Lv M, Jiang X. miR-129-3p inhibits NHEJ pathway by targeting SAE1 and represses gastric cancer progression. Int J Clin Exp Pathol. 2019;12(5):1539–1547.
  • Baba D, Maita N, Jee JG, Uchimura Y, Saitoh H, Sugasawa K, Hanaoka F, Tochio H, Hiroaki H, Shirakawa M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature. 2005;2005(4357044):979–982. doi:10.1038/nature03634.
  • Wei L, Zhao X. Roles of SUMO in replication initiation, progression, and termination. Adv Exp Med Biol. 1042;2017:371–393. doi:10.1007/978-981-10-6955-0_17.
  • Bachant J, Alcasabas A, Blat Y, Kleckner N, Elledge SJ. The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol Cell. 2002;9(6):1169–82. doi:10.1016/S1097-2765(02)00543-9.
  • Potts PR, Yu H. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nature Structural & Molecular Biology. 2007;14(7):581–90. doi:10.1038/nsmb1259.
  • Hendriks IA, Lyon D, Young C, Jensen LJ, Vertegaal AC, Nielsen ML. Site-specific mapping of the human SUMO proteome reveals co-modification with phosphorylation. Nature Structural & Molecular Biology. 2017;24(3):325–336. doi:10.1038/nsmb.3366.
  • Hendriks IA, Vertegaal AC. A comprehensive compilation of SUMO proteomics. Nat Rev Mol Cell Biol. 2016;17(9):581–95. doi:10.1038/nrm.2016.81.
  • Li YJ, Stark JM, Chen DJ, Ann DK, Chen Y. Role of SUMO: SIM-mediated protein–protein interaction in non-homologous end joining. Oncogene. 2010;2010(2924):3509–3518. doi:10.1038/onc.2010.108.
  • Guzzo CM, Berndsen CE, Zhu J, Gupta V, Datta A, Greenberg RA, Wolberger C, Matunis MJ. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci Signal. 2012;5(253):ra88. doi:10.1126/scisignal.2003485.
  • Zhu J, Yu Y, Meng X, Fan Y, Zhang Y, Zhou C, Yue Z, Jin Y, Zhang C, Yu L, et al. De novo-generated Small palindromes are characteristic of amplicon boundary junction of double minutes. Int J Cancer. 2013; 133(4):797–806. doi:10.1002/ijc.28084.
  • Sun W, Quan C, Huang Y, Ji W, Yu L, Li X, Zhang Y, Zheng Z, Zou H, Li Q, et al. Constitutive ERK1/2 activation contributes to production of double minute chromosomes in tumour cells. J Pathol. 2015; 235(1):14–24. doi:10.1002/path.4439.
  • Sanborn JZ, Salama SR, Grifford M, Brennan CW, Mikkelsen T, Jhanwar S, Katzman S, Chin L, Haussler D. Double minute chromosomes in glioblastoma multiforme are revealed by precise reconstruction of oncogenic amplicons. Cancer Res. 2013;73(19):6036–45. doi:10.1158/0008-5472.CAN-13-0186.
  • Nikolaev S, Santoni F, Garieri M, Makrythanasis P, Falconnet E, Guipponi M, Vannier A, Radovanovic I, Bena F, Forestier F, et al. Extrachromosomal driver mutations in glioblastoma and low-grade glioma. Nat Commun. 2014; 5(1):5690. doi:10.1038/ncomms6690.