17-DMAG dually inhibits Hsp90 and histone lysine demethylases in alveolar rhabdomyosarcoma.

Cancer Molecular Biology Omics

Journal

iScience
ISSN: 2589-0042
Titre abrégé: iScience
Pays: United States
ID NLM: 101724038

Informations de publication

Date de publication:
22 Jan 2021
Historique:
received: 09 04 2020
revised: 09 06 2020
accepted: 23 12 2020
entrez: 25 1 2021
pubmed: 26 1 2021
medline: 26 1 2021
Statut: epublish

Résumé

Histone lysine demethylases (KDMs) play critical roles in oncogenesis and therefore may be effective targets for anticancer therapy. Using a time-resolved fluorescence resonance energy transfer demethylation screen assay, in combination with multiple orthogonal validation approaches, we identified geldanamycin and its analog 17-DMAG as KDM inhibitors. In addition, we found that these Hsp90 inhibitors increase degradation of the alveolar rhabdomyosarcoma (aRMS) driver oncoprotein PAX3-FOXO1 and induce the repressive epigenetic mark H3K9me3 and H3K36me3 at genomic loci of PAX3-FOXO1 targets. We found that as monotherapy 17-DMAG significantly inhibits expression of PAX3-FOXO1 target genes and multiple oncogenic pathways, induces a muscle differentiation signature, delays tumor growth and extends survival in aRMS xenograft mouse models. The combination of 17-DMAG with conventional chemotherapy significantly enhances therapeutic efficacy, indicating that targeting KDM in combination with chemotherapy may serve as a therapeutic approach to PAX3-FOXO1-positive aRMS.

Identifiants

pubmed: 33490904
doi: 10.1016/j.isci.2020.101996
pii: S2589-0042(20)31193-7
pmc: PMC7811140
doi:

Types de publication

Journal Article

Langues

eng

Pagination

101996

Subventions

Organisme : NCI NIH HHS
ID : R01 CA229739
Pays : United States
Organisme : NCI NIH HHS
ID : R03 CA212802
Pays : United States

Informations de copyright

© 2020 The Author(s).

Déclaration de conflit d'intérêts

The authors declare no competing interests.

Références

Nat Commun. 2014 Apr 08;5:3630
pubmed: 24710217
Cold Spring Harb Perspect Med. 2014 Nov 03;4(11):a025650
pubmed: 25368019
Bioorg Med Chem Lett. 2001 Apr 9;11(7):909-13
pubmed: 11294389
J Biol Chem. 2011 Dec 2;286(48):41616-25
pubmed: 21914792
Nature. 2003 Sep 25;425(6956):407-10
pubmed: 14508491
Mod Pathol. 2004 Jun;17(6):660-9
pubmed: 15098008
Cancer Res. 2010 Aug 15;70(16):6497-508
pubmed: 20663909
Nucleic Acids Res. 2019 Dec 16;47(22):11623-11636
pubmed: 31647098
Cell. 2007 Feb 23;128(4):693-705
pubmed: 17320507
J Biomol Screen. 1999;4(2):67-73
pubmed: 10838414
Cancer Res. 2010 Aug 15;70(16):6456-66
pubmed: 20682797
Int J Mol Sci. 2018 Jan 13;19(1):
pubmed: 29342868
J Biol Chem. 2013 Jul 19;288(29):21376-88
pubmed: 23744078
Nat Med. 2019 Nov;25(11):1721-1727
pubmed: 31700186
Cancer Lett. 2008 Oct 18;270(1):10-8
pubmed: 18457914
J Natl Cancer Inst. 2015 Apr 29;107(6):djv080
pubmed: 25925418
Nat Rev Genet. 2012 Apr 03;13(5):343-57
pubmed: 22473383
J Natl Cancer Inst. 2006 Sep 6;98(17):1193-203
pubmed: 16954472
Cancer Res. 2017 Sep 1;77(17):4626-4638
pubmed: 28684529
Chem Biol. 2003 Apr;10(4):361-8
pubmed: 12725864
J Med Chem. 2014 Jul 24;57(14):5975-85
pubmed: 24971742
Cell Rep. 2017 Jun 13;19(11):2304-2318
pubmed: 28614716
Proc Natl Acad Sci U S A. 2014 Apr 8;111(14):5195-200
pubmed: 24706829
Cell. 2004 Dec 29;119(7):941-53
pubmed: 15620353
Cell Chem Biol. 2017 Mar 16;24(3):371-380
pubmed: 28262558
Oncogene. 2001 Sep 10;20(40):5736-46
pubmed: 11607823
Cancer Biol Ther. 2002 Mar-Apr;1(2):97-104
pubmed: 12170781
Mol Oncol. 2014 Mar;8(2):323-36
pubmed: 24388362
Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8324-8
pubmed: 8078881
Pediatr Blood Cancer. 2013 Jul;60(7):E42-5
pubmed: 23303741
Cancer Discov. 2017 Aug;7(8):884-899
pubmed: 28446439
BMC Evol Biol. 2008 Oct 24;8:294
pubmed: 18950507
Proc Natl Acad Sci U S A. 2006 May 16;103(20):7625-30
pubmed: 16684877
ACS Med Chem Lett. 2017 Jul 27;8(8):869-874
pubmed: 28835804
N Engl J Med. 2008 Mar 13;358(11):1148-59
pubmed: 18337604
Clin Cancer Res. 2012 Feb 1;18(3):796-807
pubmed: 22065083
J Med Chem. 1999 Jan 28;42(2):260-6
pubmed: 9925731
EMBO J. 1998 Aug 17;17(16):4829-36
pubmed: 9707442
Mol Cancer Res. 2017 Dec;15(12):1777-1791
pubmed: 28923841
Nature. 2012 Aug 16;488(7411):404-8
pubmed: 22842901
Nat Genet. 2013 Jan;45(1):34-42
pubmed: 23202127
PLoS One. 2010 Nov 23;5(11):e15535
pubmed: 21124847
J Hematol Oncol. 2019 Dec 4;12(1):129
pubmed: 31801559
Pediatr Blood Cancer. 2008 Jul;51(1):34-41
pubmed: 18260120
J Med Oncol Ther. 2016;1(2):34-40
pubmed: 28149961
Mol Cancer Ther. 2018 Sep;17(9):1902-1916
pubmed: 29997151
Cancer Chemother Pharmacol. 1998;42(4):273-9
pubmed: 9744771
Nat Med. 2011 Mar;17(3):330-9
pubmed: 21386836
Nat Cell Biol. 2019 Feb;21(2):226-237
pubmed: 30692625
Blood. 2007 Jul 15;110(2):678-85
pubmed: 17395781
Mol Cell. 2014 Jan 9;53(1):32-48
pubmed: 24361252
Nat Rev Mol Cell Biol. 2012 Apr 04;13(5):297-311
pubmed: 22473470
Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):4105-10
pubmed: 21368131
Sci Transl Med. 2018 May 16;10(441):
pubmed: 29769286
Nat Rev Genet. 2007 Nov;8(11):829-33
pubmed: 17909537
J Clin Oncol. 2002 Jun 1;20(11):2672-9
pubmed: 12039929
Clin Cancer Res. 2002 May;8(5):962-6
pubmed: 12006507
Cell Stem Cell. 2012 Jul 6;11(1):50-61
pubmed: 22770241
Nat Rev Drug Discov. 2013 Dec;12(12):917-30
pubmed: 24232376
Methods. 2013 Mar;59(3):301-15
pubmed: 23270813
J Exp Med. 2018 Nov 5;215(11):2833-2849
pubmed: 30266800
Free Radic Biol Med. 2010 Jun 1;48(11):1559-63
pubmed: 20211249
Mol Cell. 2007 Jan 12;25(1):1-14
pubmed: 17218267
Nat Med. 2015 Jul;21(7):827
pubmed: 26151328
Cancer Res. 2017 Nov 1;77(21):5900-5912
pubmed: 28883001
Nature. 2013 Oct 17;502(7471):333-339
pubmed: 24132290
Ann N Y Acad Sci. 2009 Oct;1177:185-97
pubmed: 19845621
PLoS One. 2011 Mar 18;6(3):e17830
pubmed: 21445275
Nucleic Acids Res. 2013 Apr;41(8):4433-46
pubmed: 23435229
Chem Biol. 2015 Sep 17;22(9):1185-96
pubmed: 26364928
Cell. 2018 Nov 29;175(6):1716
pubmed: 30500540
PLoS One. 2011;6(8):e23354
pubmed: 21853114
Cell. 1997 Apr 18;89(2):239-50
pubmed: 9108479
Cancer Cell. 2016 Jan 11;29(1):32-48
pubmed: 26766589
Genes (Basel). 2019 Feb 12;10(2):
pubmed: 30759871
Nat Rev Cancer. 2010 Jul;10(7):457-69
pubmed: 20574448
Mol Cancer Res. 2015 Nov;13(11):1445-51
pubmed: 26219697
Pediatr Blood Cancer. 2012 Jul 15;59(1):185-8
pubmed: 21538821
Proc Natl Acad Sci U S A. 2018 Jun 12;115(24):E5566-E5575
pubmed: 29844188
Nat Rev Mol Cell Biol. 2005 Nov;6(11):838-49
pubmed: 16261189
Pediatr Blood Cancer. 2013 Sep;60(9):1411-7
pubmed: 23526739

Auteurs

Shivendra Singh (S)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Ahmed Abu-Zaid (A)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Wenwei Lin (W)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Jonathan Low (J)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Alireza Abdolvahabi (A)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Hongjian Jin (H)

Center for Applied Bioinformatics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Qiong Wu (Q)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Bailey Cooke (B)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Jie Fang (J)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

John Bowling (J)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Sivaraja Vaithiyalingam (S)

Protein Technologies Center, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.
Department of Structural Biology, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Duane Currier (D)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Mi-Kyung Yun (MK)

Department of Structural Biology, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Dinesh M Fernando (DM)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Julie Maier (J)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Heather Tillman (H)

Department of Pathology, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Purva Bulsara (P)

Department of Biostatistics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Zhaohua Lu (Z)

Department of Biostatistics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Sourav Das (S)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Anang Shelat (A)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Zhenmei Li (Z)

Department of Structural Biology, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Brandon Young (B)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Richard Lee (R)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Zoran Rankovic (Z)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Andrew J Murphy (AJ)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Stephen W White (SW)

Department of Structural Biology, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.
Graduate School of Biomedical Sciences, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Andrew M Davidoff (AM)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Taosheng Chen (T)

Department of Chemical Biology and Therapeutics, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis, TN 38105, USA.

Jun Yang (J)

Department of Surgery, St Jude Children's Research Hospital, 262 Danny Thomas Place, Memphis TN 38105, USA.

Classifications MeSH