Gossypol inhibits cullin neddylation by targeting SAG-CUL5 and RBX1-CUL1 complexes.


Journal

Neoplasia (New York, N.Y.)
ISSN: 1476-5586
Titre abrégé: Neoplasia
Pays: United States
ID NLM: 100886622

Informations de publication

Date de publication:
04 2020
Historique:
received: 03 10 2019
revised: 09 02 2020
accepted: 10 02 2020
pubmed: 8 3 2020
medline: 18 11 2020
entrez: 8 3 2020
Statut: ppublish

Résumé

Cullin-RING E3 ligase (CRL) is the largest family of E3 ubiquitin ligase, responsible for ubiquitylation of ∼20% of cellular proteins. CRL plays an important role in many biological processes, particularly in cancers due to abnormal activation. CRL activation requires neddylation, an enzymatic cascade transferring small ubiquitin-like protein NEDD8 to a conserved lysine residue on cullin proteins. Recent studies have validated that neddylation is an attractive anticancer target. In this study, we report the establishment of an Alpha-Screen-based high throughput screen (HTS) assay for in vitro CUL5 neddylation, and screened a library of 17,000 compounds including FDA approved drugs, natural products and synthetic drug-like small-molecule compounds. Gossypol, a natural compound derived from cotton seed, was identified as an inhibitor of cullin neddylation. Biochemical studies showed that gossypol blocked neddylation of both CUL5 and CUL1 through direct binding to SAG-CUL5 or RBX1-CUL1 complex, and CUL5-H572 plays a key role for gossypol binding. On cellular level, gossypol inhibited cullin neddylation in a variety of cancer cell lines and selectively caused accumulation of NOXA and MCL1, the substrates of CUL5 and CUL1, respectively, in multiple cancer cell lines. Combination of gossypol with specific MCL1 inhibitor synergistically suppress growth of human cancer cells. Our study revealed a previously unknown anti-cancer mechanism of gossypol with potential to develop a new class of neddylation inhibitors.

Identifiants

pubmed: 32145688
pii: S1476-5586(19)30393-8
doi: 10.1016/j.neo.2020.02.003
pmc: PMC7076571
pii:
doi:

Substances chimiques

CUL5 protein, human 0
Calcium-Binding Proteins 0
Carrier Proteins 0
Contraceptive Agents, Male 0
Cullin 1 0
Cullin Proteins 0
DMBT1 protein, human 0
DNA-Binding Proteins 0
Multiprotein Complexes 0
RBX1 protein, human 0
Tumor Suppressor Proteins 0
Gossypol KAV15B369O

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

179-191

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Références

Cell Death Dis. 2017 Jun 1;8(6):e2834
pubmed: 28569775
Br J Haematol. 2015 May;169(4):534-43
pubmed: 25733005
Nature. 2009 Apr 9;458(7239):732-6
pubmed: 19360080
Annu Rev Biochem. 2009;78:399-434
pubmed: 19489725
JCI Insight. 2019 Feb 21;4(4):
pubmed: 30668548
Bioorg Med Chem. 2016 Feb 1;24(3):474-83
pubmed: 26337022
Clin Cancer Res. 2016 Aug 15;22(16):4145-57
pubmed: 26983464
J Med Chem. 2010 Aug 12;53(15):5502-10
pubmed: 20684596
J Biomol Screen. 1999;4(2):67-73
pubmed: 10838414
Clin Genitourin Cancer. 2016 Feb;14(1):22-7
pubmed: 26476589
Nat Rev Drug Discov. 2011 Jan;10(1):29-46
pubmed: 21151032
J Med Chem. 2019 Mar 14;62(5):2772-2797
pubmed: 30803229
Cell. 2000 Aug 18;102(4):533-9
pubmed: 10966114
Nature. 2016 Oct 27;538(7626):477-482
pubmed: 27760111
J Med Chem. 2019 Jun 13;62(11):5382-5403
pubmed: 31157974
Mol Oncol. 2015 Aug;9(7):1406-20
pubmed: 25933687
J Med Chem. 2018 Mar 8;61(5):1934-1950
pubmed: 29438612
Cell. 2011 Nov 23;147(5):1024-39
pubmed: 22118460
Science. 2011 Nov 4;334(6056):674-8
pubmed: 21940857
Mol Cell. 2009 Feb 27;33(4):483-95
pubmed: 19250909
Genes Dev. 2005 Jun 1;19(11):1294-305
pubmed: 15901672
J Comp Pathol. 1995 May;112(4):361-71
pubmed: 7593758
Protein Cell. 2019 Oct;10(10):726-744
pubmed: 30850948
Clin Cancer Res. 2010 Feb 1;16(3):814-24
pubmed: 20103673
Eur J Drug Metab Pharmacokinet. 2003 Jul-Sep;28(3):237-43
pubmed: 14527098
Carbohydr Res. 2011 Oct 18;346(14):2070-4
pubmed: 21788013
Cancer Res. 2009 Jun 15;69(12):4974-82
pubmed: 19509229
Cancer Res. 2006 Oct 1;66(19):9437-44
pubmed: 17018598
Nat Commun. 2014 May 13;5:3733
pubmed: 24821572
Nat Protoc. 2014 Sep;9(9):2100-22
pubmed: 25101824
Proc Natl Acad Sci U S A. 2016 Apr 5;113(14):E2011-8
pubmed: 27001857
Clin Cancer Res. 2016 Jan 1;22(1):34-43
pubmed: 26561559
J Thorac Oncol. 2011 Oct;6(10):1757-60
pubmed: 21918390
Invest New Drugs. 2016 Aug;34(4):439-49
pubmed: 27056178
Cell Signal. 2018 Apr;44:92-102
pubmed: 29331584
Neuro Oncol. 2015 Oct;17(10):1333-43
pubmed: 25904638
Annu Rev Biochem. 2001;70:503-33
pubmed: 11395416
Cell. 2014 Jun 19;157(7):1671-84
pubmed: 24949976
Science. 2013 Jul 5;341(6141):84-7
pubmed: 23828940
J Natl Cancer Inst. 2014 May 22;106(6):dju083
pubmed: 24853380
Adv Enzyme Regul. 1984;22:27-55
pubmed: 6382953
Proc Natl Acad Sci U S A. 2016 May 24;113(21):E2935-44
pubmed: 27162365
Cell Death Differ. 2013 Feb;20(2):281-92
pubmed: 22976837
Curr Med Chem. 2019;26(10):1849-1873
pubmed: 28545375
Nat Commun. 2017 Oct 27;8(1):1150
pubmed: 29074978
Future Med Chem. 2017 Jul;9(11):1243-1275
pubmed: 28722469
Clin Cancer Res. 2009 May 1;15(9):3172-6
pubmed: 19366825
EMBO J. 1998 Apr 15;17(8):2208-14
pubmed: 9545234
Cell. 2005 Jul 1;121(7):1085-95
pubmed: 15989957
Invest New Drugs. 2019 Aug;37(4):755-762
pubmed: 31172443
Nature. 2002 Apr 18;416(6882):703-9
pubmed: 11961546
Oncotarget. 2011 Mar;2(3):239-44
pubmed: 21608150
Breast Cancer Res Treat. 2001 Apr;66(3):239-48
pubmed: 11510695
J Biol Chem. 1999 Apr 23;274(17):12036-42
pubmed: 10207026
Breast Cancer Res. 2017 Mar 9;19(1):27
pubmed: 28274247
Clin Cancer Res. 2016 Feb 15;22(4):847-57
pubmed: 26423795
Clin Cancer Res. 2017 Feb 15;23(4):1104-1116
pubmed: 27591266
Mol Cell Biol. 2007 Jun;27(11):4006-17
pubmed: 17387146
J Thorac Oncol. 2010 Oct;5(10):1637-43
pubmed: 20808253
Nat Rev Mol Cell Biol. 2005 Jan;6(1):9-20
pubmed: 15688063
Toxicology. 2012 Dec 16;302(2-3):101-5
pubmed: 23041711
Ann Oncol. 2012 Jul;23(7):1803-8
pubmed: 22112969
J Biol Chem. 1998 Dec 25;273(52):34983-91
pubmed: 9857030
Cell. 2008 Sep 19;134(6):995-1006
pubmed: 18805092
Expert Opin Ther Targets. 2017 Aug;21(8):767-779
pubmed: 28670929
Methods Mol Biol. 2016;1449:453-67
pubmed: 27613056
Annu Rev Biochem. 1998;67:425-79
pubmed: 9759494
Nat Chem Biol. 2017 Aug;13(8):850-857
pubmed: 28581483

Auteurs

Qing Yu (Q)

Cancer Institute of the 2nd Affiliated Hospital and Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.

Zhiguo Hu (Z)

State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 201210, China.

Yanwen Shen (Y)

Cancer Institute of the 2nd Affiliated Hospital and Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.

Yihan Jiang (Y)

Cancer Institute of the 2nd Affiliated Hospital and Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.

Peichen Pan (P)

College of Pharmaceutical Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China.

Tingjun Hou (T)

College of Pharmaceutical Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, China; Institute of Functional Nano and Soft Materials (FUNSOM), Soochow University, Suzhou, Jiangsu 215123, China.

Zhen-Qiang Pan (ZQ)

Department of Oncological Sciences, The Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY 10029-6574, USA.

Jing Huang (J)

Shanghai Institute of Precision Medicine, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China.

Yi Sun (Y)

Cancer Institute of the 2nd Affiliated Hospital and Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China; Division of Radiation and Cancer Biology, Department of Radiation Oncology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: sunyi@umich.edu.

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