Emerging strategies to target the dysfunctional cohesin complex in cancer

References

• Bonev B, Cavalli G. Organization and function of the 3D genome. Nat Rev Genet. 2016 Oct 14;17(11):661–678.
   PubMed Web of Science ®Google Scholar
• Haarhuis JH, Elbatsh AM, Rowland BD. Cohesin and its regulation: on the logic of X-shaped chromosomes. Dev Cell. 2014 Oct 13;31(1):7–18.
   PubMed Web of Science ®Google Scholar
• Haering CH, Lowe J, Hochwagen A, et al. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell. 2002 Apr;9(4):773–788.
   PubMed Web of Science ®Google Scholar
• Gruber S, Haering CH, Nasmyth K. Chromosomal cohesin forms a ring. Cell. 2003 Mar 21;112(6):765–777.
   PubMed Web of Science ®Google Scholar
• Losada A. Cohesin in cancer: chromosome segregation and beyond. Nat Rev Cancer. 2014 Jun;14(6):389–393.
   PubMed Web of Science ®Google Scholar
• Canudas S, Smith S. Differential regulation of telomere and centromere cohesion by the Scc3 homologues SA1 and SA2, respectively, in human cells. J Cell Biol. 2009 Oct 19;187(2):165–173.
   PubMed Web of Science ®Google Scholar
• Gruber S, Arumugam P, Katou Y, et al. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell. 2006 Nov 3;127(3):523–537.
   PubMed Web of Science ®Google Scholar
• Chan KL, Roig MB, Hu B, et al. Cohesin‘s DNA exit gate is distinct from its entrance gate and is regulated by acetylation. Cell. 2012 Aug 31;150(5):961–974.
   PubMed Web of Science ®Google Scholar
• Peters JM, Nishiyama T. Sister chromatid cohesion. Cold Spring Harb Perspect Biol. 2012 Nov 1;4(11).
   PubMed Web of Science ®Google Scholar
• Schockel L, Mockel M, Mayer B, et al. Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat Cell Biol. 2011 Jul 10;13(8):966–972.
   PubMed Web of Science ®Google Scholar
• Murayama Y, Uhlmann F. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature. 2014 Jan 16;505(7483):367–371.
   PubMed Web of Science ®Google Scholar
• Tedeschi A, Wutz G, Huet S, et al. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature. 2013 Sep 26;501(7468):564–568.
   PubMed Web of Science ®Google Scholar
• Nishiyama T, Sykora MM, Huis in ‘T Veld PJ, et al. Aurora B and Cdk1 mediate Wapl activation and release of acetylated cohesin from chromosomes by phosphorylating Sororin. Proc Natl Acad Sci U S A. 2013 Aug 13;110(33):13404–13409.
   PubMed Web of Science ®Google Scholar
• Waizenegger IC, Hauf S, Meinke A, et al. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell. 2000 Oct 27;103(3):399–410.
   PubMed Web of Science ®Google Scholar
• Borges V, Lehane C, Lopez-Serra L, et al. Hos1 deacetylates Smc3 to close the cohesin acetylation cycle. Mol Cell. 2010 Sep 10;39(5):677–688.
   PubMed Web of Science ®Google Scholar
• Bharti SK, Khan I, Banerjee T, et al. Molecular functions and cellular roles of the ChlR1 (DDX11) helicase defective in the rare cohesinopathy Warsaw breakage syndrome. Cell Mol Life Sci. 2014 Jul;71(14):2625–2639.
   PubMed Web of Science ®Google Scholar
• Rao SSP, Huang SC, B GSH, et al. Cohesin loss eliminates all loop domains. Cell. 2017 Oct 5;171(2):305–20 e24.
   PubMed Web of Science ®Google Scholar
• Wutz G, Varnai C, Nagasaka K, et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. Embo J. 2017 Dec 15;36(24):3573–3599.
   PubMed Web of Science ®Google Scholar
• Caron P, Aymard F, Iacovoni JS, et al. Cohesin protects genes against gammaH2AX Induced by DNA double-strand breaks. PLoS Genet. 2012 Jan;8(1):e1002460.
   PubMed Web of Science ®Google Scholar
• Beucher A, Birraux J, Tchouandong L, et al. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. Embo J. 2009 Nov 4;28(21):3413–3427.
   PubMed Web of Science ®Google Scholar
• Remeseiro S, Cuadrado A, Carretero M, et al. Cohesin-SA1 deficiency drives aneuploidy and tumourigenesis in mice due to impaired replication of telomeres. Embo J. 2012 May 2;31(9):2076–2089.
   PubMed Web of Science ®Google Scholar
• Misulovin Z, Pherson M, Gause M, et al. Brca2, Pds5 and Wapl differentially control cohesin chromosome association and function. PLoS Genet. 2018 Feb;14(2):e1007225.
   PubMed Web of Science ®Google Scholar
• Krantz ID, McCallum J, DeScipio C, et al. Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet. 2004 Jun;36(6):631–635.
   PubMed Web of Science ®Google Scholar
• Tonkin ET, Wang TJ, Lisgo S, et al. NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet. 2004 Jun;36(6):636–641.
   PubMed Web of Science ®Google Scholar
• Deardorff MA, Wilde JJ, Albrecht M, et al. RAD21 mutations cause a human cohesinopathy. Am J Hum Genet. 2012 Jun 8;90(6):1014–1027.
   PubMed Web of Science ®Google Scholar
• Lehalle D, Mosca-Boidron AL, Begtrup A, et al. STAG1 mutations cause a novel cohesinopathy characterised by unspecific syndromic intellectual disability. J Med Genet. 2017 Jul;54(7):479–488.
   PubMed Web of Science ®Google Scholar
• Deardorff MA, Kaur M, Yaeger D, et al. Mutations in cohesin complex members SMC3 and SMC1A cause a mild variant of cornelia de Lange syndrome with predominant mental retardation. Am J Hum Genet. 2007 Mar;80(3):485–494.
   PubMed Web of Science ®Google Scholar
• Banerji R, Skibbens RV, Iovine MK. How many roads lead to cohesinopathies?. Dev Dyn. 2017 Nov;246(11):881–888.
   PubMed Web of Science ®Google Scholar
• Solomon DA, Kim T, Diaz-Martinez LA, et al. Mutational inactivation of STAG2 causes aneuploidy in human cancer. Science. 2011 Aug 19;333(6045):1039–1043.
   PubMed Web of Science ®Google Scholar
• Balbas-Martinez C, Sagrera A, Carrillo-de-Santa-Pau E, et al. Recurrent inactivation of STAG2 in bladder cancer is not associated with aneuploidy. Nat Genet. 2013 Dec;45(12):1464–1469.
   PubMed Web of Science ®Google Scholar
• Kon A, Shih LY, Minamino M, et al. Recurrent mutations in multiple components of the cohesin complex in myeloid neoplasms. Nat Genet. 2013 Oct;45(10):1232–1237.
   PubMed Web of Science ®Google Scholar
• Solomon DA, Kim JS, Bondaruk J, et al. Frequent truncating mutations of STAG2 in bladder cancer. Nat Genet. 2013 Dec;45(12):1428–1430.
   PubMed Web of Science ®Google Scholar
• Stephens PJ, Tarpey PS, Davies H, et al. The landscape of cancer genes and mutational processes in breast cancer. Nature. 2012 May 16;486(7403):400–404.
   PubMed Web of Science ®Google Scholar
• Liu Y, Xu H, Van der Jeught K, et al. Somatic mutation of the cohesin complex subunit confers therapeutic vulnerabilities in cancer. J Clin Invest. 2018 Jun;128(7):2951-2965.
   Web of Science ®Google Scholar
• Hodis E, Watson IR, Kryukov GV, et al. A landscape of driver mutations in melanoma. Cell. 2012 Jul 20;150(2):251–263.
   PubMed Web of Science ®Google Scholar
• Xu H, Yan M, Patra J, et al. Enhanced RAD21 cohesin expression confers poor prognosis and resistance to chemotherapy in high grade luminal, basal and HER2 breast cancers. BCR. 2011 Jan 21;13(1):R9.
   PubMed Web of Science ®Google Scholar
• van ‘T Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002 Jan 31;415(6871):530–536.
   PubMed Web of Science ®Google Scholar
• Yamamoto G, Irie T, Aida T, et al. Correlation of invasion and metastasis of cancer cells, and expression of the RAD21 gene in oral squamous cell carcinoma. Virchows Arch. 2006 Apr;448(4):435–441.
   PubMed Web of Science ®Google Scholar
• Yun J, Song SH, Kim HP, et al. Dynamic cohesin-mediated chromatin architecture controls epithelial-mesenchymal plasticity in cancer. EMBO Rep. 2016 Sep;17(9):1343–1359.
   PubMed Web of Science ®Google Scholar
• Deb S, Xu H, Tuynman J, et al. RAD21 cohesin overexpression is a prognostic and predictive marker exacerbating poor prognosis in KRAS mutant colorectal carcinomas. Br J Cancer. 2014 Mar 18;110(6):1606–1613.
   PubMed Web of Science ®Google Scholar
• Porkka KP, Tammela TL, Vessella RL, et al. RAD21 and KIAA0196 at 8q24 are amplified and overexpressed in prostate cancer. Genes Chromosomes Cancer. 2004 Jan;39(1):1–10.
   PubMed Web of Science ®Google Scholar
• Yun J, Song SH, Kang JY, et al. Reduced cohesin destabilizes high-level gene amplification by disrupting pre-replication complex bindings in human cancers with chromosomal instability. Nucleic Acids Res. 2016 Jan 29;44(2):558–572.
   PubMed Web of Science ®Google Scholar
• Thol F, Bollin R, Gehlhaar M, et al. Mutations in the cohesin complex in acute myeloid leukemia: clinical and prognostic implications. Blood. 2014 Feb 6;123(6):914–920.
   PubMed Web of Science ®Google Scholar
• Papaemmanuil E, Gerstung M, Bullinger L, et al. Genomic classification and prognosis in acute myeloid leukemia. N Engl J Med. 2016 Jun 9;374(23):2209–2221.
   PubMed Web of Science ®Google Scholar
• Thota S, Viny AD, Makishima H, et al. Genetic alterations of the cohesin complex genes in myeloid malignancies. Blood. 2014 Sep 11;124(11):1790–1798.
   PubMed Web of Science ®Google Scholar
• Corces-Zimmerman MR, Hong WJ, Weissman IL, et al. Preleukemic mutations in human acute myeloid leukemia affect epigenetic regulators and persist in remission. Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2548–2553.
   PubMed Web of Science ®Google Scholar
• Mullenders J, Aranda-Orgilles B, Lhoumaud P, et al. Cohesin loss alters adult hematopoietic stem cell homeostasis, leading to myeloproliferative neoplasms. J Exp Med. 2015 Oct 19;212(11):1833–1850.
   PubMed Web of Science ®Google Scholar
• Yoshida K, Toki T, Okuno Y, et al. The landscape of somatic mutations in Down syndrome-related myeloid disorders. Nat Genet. 2013 Nov;45(11):1293–1299.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research N, Ley Tj, Miller C, et al. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med. 2013 May 30;368(22):2059–2074.
   PubMed Web of Science ®Google Scholar
• Weinberg OK, Gibson CJ, Blonquist TM, et al. Association of mutations with morphological dysplasia in de novo acute myeloid leukemia without 2016 WHO Classification-defined cytogenetic abnormalities. Haematologica. 2018 Apr;103(4):626–633.
   PubMed Web of Science ®Google Scholar
• Tsai CH, Hou HA, Tang JL, et al. Prognostic impacts and dynamic changes of cohesin complex gene mutations in de novo acute myeloid leukemia. Blood Cancer J. 2017 Dec 29;7(12):663.
   PubMedGoogle Scholar
• Eisfeld AK, Kohlschmidt J, Mrozek K, et al. Mutation patterns identify adult patients with de novo acute myeloid leukemia aged 60 years or older who respond favorably to standard chemotherapy: an analysis of Alliance studies. Leukemia. 2018 Jun;32(6):1338–1348.
   PubMed Web of Science ®Google Scholar
• Lindsley RC, Mar BG, Mazzola E, et al. Acute myeloid leukemia ontogeny is defined by distinct somatic mutations. Blood. 2015 Feb 26;125(9):1367–1376.
   PubMed Web of Science ®Google Scholar
• Duployez N, Marceau-Renaut A, Boissel N, et al. Comprehensive mutational profiling of core binding factor acute myeloid leukemia. Blood. 2016 May 19;127(20):2451–2459.
   PubMed Web of Science ®Google Scholar
• Galeev R, Baudet A, Kumar P, et al. Genome-wide RNAi screen identifies cohesin genes as modifiers of renewal and differentiation in human HSCs. Cell Rep. 2016 Mar 29;14(12):2988–3000.
   PubMed Web of Science ®Google Scholar
• Viny AD, Ott CJ, Spitzer B, et al. Dose-dependent role of the cohesin complex in normal and malignant hematopoiesis. J Exp Med. 2015 Oct 19;212(11):1819–1832.
   PubMed Web of Science ®Google Scholar
• Xu H, Balakrishnan K, Malaterre J, et al. Rad21-cohesin haploinsufficiency impedes DNA repair and enhances gastrointestinal radiosensitivity in mice. PloS one. 2010 Aug 12;5(8):e12112.
   PubMed Web of Science ®Google Scholar
• National Cancer Institute. Cancer stat facts. 2018. [Cited 2019 Jan]. Available from: https://seer.cancer.gov/statfacts/
   Google Scholar
• Chen HS, De Leo A, Wang Z, et al. BET-inhibitors disrupt Rad21-dependent conformational control of KSHV latency. PLoS Pathog. 2017 Jan;13(1):e1006100.
   PubMed Web of Science ®Google Scholar
• Filippakopoulos P, Qi J, Picaud S, et al. Selective inhibition of BET bromodomains. Nature. 2010 Dec 23;468(7327):1067–1073.
   PubMed Web of Science ®Google Scholar
• Park S, Willingham MC, Qi J, et al. Metformin and JQ1 synergistically inhibit obesity-activated thyroid cancer. Endocr Relat Cancer. 2018 Oct;25(10):865–877.
   PubMed Web of Science ®Google Scholar
• Carra G, Panuzzo C, Morena D, et al. BET Inhibitors in Chronic Lymphocytic Leukemia. Blood. 2017;130(Suppl 1):2542.
   Google Scholar
• Baltz NJ, Colorado NC, Yan Y, et al. JQ1, a potential therapeutic molecule for myeloid leukemia with PTEN deficiency. Blood. 2016;128(22):5899.
   Web of Science ®Google Scholar
• Atienza JM, Roth RB, Rosette C, et al. Suppression of RAD21 gene expression decreases cell growth and enhances cytotoxicity of etoposide and bleomycin in human breast cancer cells. Mol Cancer Ther. 2005 Mar;4(3):361–368.
   PubMed Web of Science ®Google Scholar
• Qi W, Liu X, Cooke LS, et al. AT9283, a novel aurora kinase inhibitor, suppresses tumor growth in aggressive B-cell lymphomas. Int J Cancer. 2012 Jun 15;130(12):2997–3005.
   PubMed Web of Science ®Google Scholar
• Shah M, Gallipoli P, Lyons J, et al. Effects of the novel aurora kinase/JAK inhibitor, AT9283 and imatinib on Philadelphia positive cells in vitro. Blood Cells Mol Dis. 2012 Mar 15;48(3):199–201.
   PubMed Web of Science ®Google Scholar
• Hay AE, Murugesan A, DiPasquale AM, et al. A phase II study of AT9283, an aurora kinase inhibitor, in patients with relapsed or refractory multiple myeloma: NCIC clinical trials group IND.191. Leuk Lymphoma. 2016;57(6):1463–1466.
   PubMed Web of Science ®Google Scholar
• Okabe S, Tauchi T, Ohyashiki JH, et al. Mechanism of MK-0457 efficacy against BCR-ABL positive leukemia cells. Biochem Biophys Res Commun. 2009 Mar 20;380(4):775–779.
   PubMed Web of Science ®Google Scholar
• Lin YG, Immaneni A, Merritt WM, et al. Targeting aurora kinase with MK-0457 inhibits ovarian cancer growth. Clin Cancer Res off J Am Assoc Cancer Res. 2008 Sep 1;14(17):5437–5446.
   PubMed Web of Science ®Google Scholar
• Giles FJ, Swords RT, Nagler A, et al. MK-0457, an Aurora kinase and BCR-ABL inhibitor, is active in patients with BCR-ABL T315I leukemia. Leukemia. 2013 Jan;27(1):113–117.
   PubMed Web of Science ®Google Scholar
• Seymour JF, Kim DW, Rubin E, et al. A phase 2 study of MK-0457 in patients with BCR-ABL T315I mutant chronic myelogenous leukemia and philadelphia chromosome-positive acute lymphoblastic leukemia. Blood Cancer J. 2014 Aug 15;4:e238.
   PubMed Web of Science ®Google Scholar
• Rathos MJ, Khanwalkar H, Joshi K, et al. Potentiation of in vitro and in vivo antitumor efficacy of doxorubicin by cyclin-dependent kinase inhibitor P276-00 in human non-small cell lung cancer cells. BMC Cancer. 2013 Jan 23;13:29.
   PubMed Web of Science ®Google Scholar
• Shirsath NP, Manohar SM, Joshi KS. P276-00, a cyclin-dependent kinase inhibitor, modulates cell cycle and induces apoptosis in vitro and in vivo in mantle cell lymphoma cell lines. Mol Cancer. 2012 Oct 18;11:77.
   PubMed Web of Science ®Google Scholar
• Cheng CY, Liu CJ, Huang YC, et al. BI2536 induces mitotic catastrophe and radiosensitization in human oral cancer cells. Oncotarget. 2018 Apr 20;9(30):21231–21243.
   PubMedGoogle Scholar
• Lian G, Li L, Shi Y, et al. BI2536, a potent and selective inhibitor of polo-like kinase 1, in combination with cisplatin exerts synergistic effects on gastric cancer cells. Int J Oncol. 2018 Mar;52(3):804–814.
   PubMed Web of Science ®Google Scholar
• Dohner H, Lubbert M, Fiedler W, et al. Randomized, phase 2 trial of low-dose cytarabine with or without volasertib in AML patients not suitable for induction therapy. Blood. 2014 Aug 28;124(9):1426–1433.
   PubMed Web of Science ®Google Scholar
• H SA D, Sanz MA, Deeren D, et al. Phase III randomized trial of volasertib plus low-dose cytarabine (ldac) versus placebo plus ldac in patients aged >65 years with previously untreated aml, ineligible for intensive therapy. In: Cools J, editors. 21st Congress Of The European Hematology Association Copenhagen; June 9–12, 2016; Denmark. Haematologica: 2016. p.185–186.
   Google Scholar
• Zhang N, Scorsone K, Ge G, et al. Identification and characterization of separase inhibitors (Sepins) for cancer therapy. J Biomol Screen. 2014 Jul;19(6):878–889.
   PubMedGoogle Scholar
• Xu W, Ying Y, Shan L, et al. Enhanced expression of cohesin loading factor NIPBL confers poor prognosis and chemotherapy resistance in non-small cell lung cancer. J Transl Med. 2015 May;12(13):153.
   Google Scholar
• Zheng L, Zhou H, Guo L, et al. Inhibition of NIPBL enhances the chemosensitivity of non-small-cell lung cancer cells via the DNA damage response and autophagy pathway. Onco Targets Ther. 2018;11:1941–1948.
   PubMed Web of Science ®Google Scholar
• Zhou H, Zheng L, Lu K, et al. Downregulation of cohesin loading factor Nipped-B-Like Protein (NIPBL) induces cell cycle arrest, apoptosis, and autophagy of breast cancer cell lines. Med Sci Monit. 2017 Oct;7(23):4817–4825.
   Google Scholar
• Li J, Feng W, Chen L, et al. Downregulation of SMC1A inhibits growth and increases apoptosis and chemosensitivity of colorectal cancer cells. J Int Med Res. 2016 Feb;44(1):67–74.
   PubMed Web of Science ®Google Scholar
• Yang Y, Zhang Z, Wang R, et al. siRNA-mediated knockdown of SMC1A expression suppresses the proliferation of glioblastoma cells. Mol Cell Biochem. 2013 Sep;381(1–2):209–215.
   PubMed Web of Science ®Google Scholar
• McLornan DP, List A, Mufti GJ. Applying synthetic lethality for the selective targeting of cancer. N Engl J Med. 2014 Oct 30;371(18):1725–1735.
   PubMed Web of Science ®Google Scholar
• van der Lelij P, Lieb S, Jude J, et al. Synthetic lethality between the cohesin subunits STAG1 and STAG2 in diverse cancer contexts. eLife. 2017 Jul 10;6.
   PubMed Web of Science ®Google Scholar
• Benedetti L, Cereda M, Monteverde L, et al. Synthetic lethal interaction between the tumour suppressor STAG2 and its paralog STAG1. Oncotarget. 2017 Jun 6;8(23):37619–37632.
   PubMedGoogle Scholar
• Jyotsana N, Sharma A, Chaturvedi A, et al. RNA interference efficiently targets human leukemia driven by a fusion oncogene in vivo. Leukemia. 2018 Jan;32(1):224–226.
   PubMed Web of Science ®Google Scholar
• Herceg Z, Wang ZQ. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat Res. 2001 Jun 2;477(1–2):97–110.
   PubMed Web of Science ®Google Scholar
• O‘Shaughnessy J, Osborne C, Pippen JE, et al. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N Engl J Med. 2011 Jan 20;364(3):205–214.
   PubMed Web of Science ®Google Scholar
• Bailey ML, O‘Neil NJ, van Pel DM, et al. Glioblastoma cells containing mutations in the cohesin component STAG2 are sensitive to PARP inhibition. Mol Cancer Ther. 2014 Mar;13(3):724–732.
   PubMed Web of Science ®Google Scholar
• Yadav S, Sehrawat A, Eroglu Z, et al. Role of SMC1 in overcoming drug resistance in triple negative breast cancer. PloS one. 2013;8(5):e64338.
   PubMed Web of Science ®Google Scholar
• McLellan JL, O‘Neil NJ, Barrett I, et al. Synthetic lethality of cohesins with PARPs and replication fork mediators. PLoS Genet. 2012;8(3):e1002574.
   PubMed Web of Science ®Google Scholar
• Zuin J, Casa V, Pozojevic J, et al. Regulation of the cohesin-loading factor NIPBL: role of the lncRNA NIPBL-AS1 and identification of a distal enhancer element. PLoS Genet. 2017 Dec;13(12):e1007137.
   PubMed Web of Science ®Google Scholar
• Mazumdar C, Shen Y, Xavy S, et al. Leukemia-associated cohesin mutants dominantly enforce stem cell programs and impair human hematopoietic progenitor differentiation. Cell Stem Cell. 2015 Dec 3;17(6):675–688.
   PubMed Web of Science ®Google Scholar
• Itzykson R, Kosmider O, Cluzeau T, et al. Impact of TET2 mutations on response rate to azacitidine in myelodysplastic syndromes and low blast count acute myeloid leukemias. Leukemia. 2011 Jul;25(7):1147–1152.
   PubMed Web of Science ®Google Scholar
• Sekeres MA, Othus M, List AF, et al. Randomized phase II study of azacitidine alone or in combination with lenalidomide or with vorinostat in higher-risk myelodysplastic syndromes and chronic myelomonocytic leukemia: north american intergroup study SWOG S1117. J Clin Oncol. 2017 Aug 20;35(24):2745–2753.
   PubMed Web of Science ®Google Scholar
• Ioannidou A, Zachaki S, Karakosta M, et al. Cohesin RAD21 gene promoter methylation in patients with chronic lymphocytic leukemia. Cytogenet Genome Res. 2018;154(3):126–131.
   PubMed Web of Science ®Google Scholar
• Zuin J, Dixon JR, van der Reijden MI, et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc Natl Acad Sci U S A. 2014 Jan 21;111(3):996–1001.
   PubMed Web of Science ®Google Scholar
• Jung KY, Wang H, Teriete P, et al. Perturbation of the c-Myc-Max protein-protein interaction via synthetic alpha-helix mimetics. J Med Chem. 2015 Apr 9;58(7):3002–3024.
   PubMed Web of Science ®Google Scholar
• Huang Z, Zhang M, Burton SD, et al. Targeting the Tcf4 G13ANDE17 binding site to selectively disrupt beta-catenin/T-cell factor protein-protein interactions. ACS Chem Biol. 2014 Jan 17;9(1):193–201.
   PubMed Web of Science ®Google Scholar
• Zhang N, Ge G, Meyer R, et al. Overexpression of Separase induces aneuploidy and mammary tumorigenesis. Proc Natl Acad Sci U S A. 2008 Sep 2;105(35):13033–13038.
   PubMed Web of Science ®Google Scholar
• Adams D, Gonzalez-Duarte A, O‘Riordan WD, et al. Patisiran, an RNAi therapeutic, for hereditary transthyretin amyloidosis. N Engl J Med. 2018 Jul 5;379(1):11–21.
   PubMed Web of Science ®Google Scholar
• Singh NN, Howell MD, Androphy EJ, et al. How the discovery of ISS-N1 led to the first medical therapy for spinal muscular atrophy. Gene Ther. 2017 Sep;24(9):520–526.
   PubMed Web of Science ®Google Scholar
• Coelho T, Adams D, Silva A, et al. Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N Engl J Med. 2013 Aug 29;369(9):819–829.
   PubMed Web of Science ®Google Scholar
• Fitzgerald K, White S, Borodovsky A, et al. A highly durable RNAi therapeutic inhibitor of PCSK9. N Engl J Med. 2017 Jan 5;376(1):41–51.
   PubMed Web of Science ®Google Scholar
• Mohell N, Alfredsson J, Fransson A, et al. APR-246 overcomes resistance to cisplatin and doxorubicin in ovarian cancer cells. Cell Death Dis. 2015 Jun 18;6:e1794.
   PubMed Web of Science ®Google Scholar
• Gligoris T, Lowe J. Structural insights into ring formation of cohesin and related Smc complexes. Trends Cell Biol. 2016 Sep;26(9):680–693.
   PubMed Web of Science ®Google Scholar
• Hara K, Zheng G, Qu Q, et al. Structure of cohesin subcomplex pinpoints direct shugoshin-Wapl antagonism in centromeric cohesion. Nat Struct Mol Biol. 2014 Oct;21(10):864–870.
   PubMed Web of Science ®Google Scholar