YB-1 Knockdown Inhibits the Proliferation of Mesothelioma Cells through Multiple Mechanisms.

G2/M checkpoint MDM2 RNA-seq STAT3 Y-box protein-1 apoptosis cell cycle mitosis p21 p53

Journal

Cancers
ISSN: 2072-6694
Titre abrégé: Cancers (Basel)
Pays: Switzerland
ID NLM: 101526829

Informations de publication

Date de publication:
14 Aug 2020
Historique:
received: 16 07 2020
revised: 07 08 2020
accepted: 12 08 2020
entrez: 23 8 2020
pubmed: 23 8 2020
medline: 23 8 2020
Statut: epublish

Résumé

Y-box binding protein-1 (YB-1) is a multifunctional oncoprotein that has been shown to regulate proliferation, invasion and metastasis in a variety of cancer types. We previously demonstrated that YB-1 is overexpressed in mesothelioma cells and its knockdown significantly reduces tumour cell proliferation, migration, and invasion. However, the mechanisms driving these effects are unclear. Here, we utilised an unbiased RNA-seq approach to characterise the changes to gene expression caused by loss of YB-1 knockdown in three mesothelioma cell lines (MSTO-211H, VMC23 and REN cells). Bioinformatic analysis showed that YB-1 knockdown regulated 150 common genes that were enriched for regulators of mitosis, integrins and extracellular matrix organisation. However, each cell line also displayed unique gene expression signatures, that were differentially enriched for cell death or cell cycle control. Interestingly, deregulation of STAT3 and p53-pathways were a key differential between each cell line. Using flow cytometry, apoptosis assays and single-cell time-lapse imaging, we confirmed that MSTO-211H, VMC23 and REN cells underwent either increased cell death, G1 arrest or aberrant mitotic division, respectively. In conclusion, this data indicates that YB-1 knockdown affects a core set of genes in mesothelioma cells. Loss of YB-1 causes a cascade of events that leads to reduced mesothelioma proliferation, dependent on the underlying functionality of the STAT3/p53-pathways and the genetic landscape of the cell.

Identifiants

pubmed: 32823952
pii: cancers12082285
doi: 10.3390/cancers12082285
pmc: PMC7464182
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : National Breast Cancer Foundation
ID : IIRS-18-103
Organisme : Austrian Science Fund
ID : T 1062 Firnberg Program

Références

Nat Rev Cancer. 2014 Nov;14(11):736-46
pubmed: 25342631
J Thorac Oncol. 2018 Sep;13(9):1269-1283
pubmed: 29966799
PLoS One. 2013 Sep 03;8(9):e74297
pubmed: 24019961
Neoplasma. 2014;61(4):379-91
pubmed: 25027739
J Thorac Oncol. 2011 Oct;6(10):1753-6
pubmed: 21918389
Cell Death Dis. 2018 May 22;9(6):603
pubmed: 29789534
Hum Mutat. 2016 Sep;37(9):865-76
pubmed: 27328919
Lung Cancer. 2005 Jul;49 Suppl 1:S95-8
pubmed: 15950811
J Cell Physiol. 2018 Nov;233(11):8952-8961
pubmed: 29904909
Mol Genet Metab. 2000 Jun;70(2):85-98
pubmed: 10873390
Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12384-9
pubmed: 14530393
Nat Genet. 2003 Mar;33(3):357-65
pubmed: 12567188
Front Cell Dev Biol. 2019 Oct 01;7:221
pubmed: 31632972
Lancet. 2016 Apr 2;387(10026):1405-1414
pubmed: 26719230
Eur J Cancer. 2010 Mar;46(5):954-65
pubmed: 20079629
J Biol Chem. 2000 Jun 23;275(25):18794-800
pubmed: 10764767
J Cell Physiol. 2020 Jan 22;:
pubmed: 31967332
Br J Cancer. 2015 Mar 3;112(5):783-92
pubmed: 25633038
Front Oncol. 2020 Feb 21;10:187
pubmed: 32154179
MethodsX. 2019 Oct 18;6:2468-2475
pubmed: 31720237
Cancer Res. 1999 Jan 15;59(2):342-6
pubmed: 9927044
Biochem J. 2013 Jan 1;449(1):11-23
pubmed: 23216250
Oncotarget. 2015 Sep 29;6(29):26583-98
pubmed: 26378048
Stem Cells Int. 2017;2017:6193106
pubmed: 28928774
Genome Biol. 2014;15(12):550
pubmed: 25516281
J Thorac Oncol. 2018 Feb;13(2):258-272
pubmed: 29113949
Nat Struct Mol Biol. 2010 Nov;17(11):1358-66
pubmed: 20972445
Acta Naturae. 2017 Apr-Jun;9(2):4-16
pubmed: 28740723
Biochim Biophys Acta. 2016 Dec;1864(12):1631-1640
pubmed: 27544639
Int J Cancer. 2016 Jul 15;139(2):433-45
pubmed: 26939718
Future Oncol. 2009 Mar;5(2):153-6
pubmed: 19284373
J Biol Chem. 2003 Sep 12;278(37):35516-23
pubmed: 12835324
J Clin Oncol. 2003 Jul 15;21(14):2636-44
pubmed: 12860938
RNA Biol. 2020 Apr;17(4):487-499
pubmed: 31944153
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Br J Cancer. 2004 Jul 19;91(2):355-8
pubmed: 15188009
Oncotarget. 2016 Dec 13;7(50):82139-82157
pubmed: 27384875
Cells. 2019 Sep 05;8(9):
pubmed: 31492019
Oncogene. 2000 Dec 14;19(54):6194-202
pubmed: 11175333
Oncogene. 2011 Aug 25;30(34):3649-60
pubmed: 21423216
Nucleic Acids Res. 2004 Jan 12;32(1):316-27
pubmed: 14718551
Oncogene. 2005 Dec 15;24(56):8314-25
pubmed: 16158057
Breast Cancer Res. 2007;9(5):R61
pubmed: 17875215
Cancer Discov. 2012 May;2(5):401-4
pubmed: 22588877
Genome Biol. 2010;11(10):R106
pubmed: 20979621
Mol Cancer Res. 2015 Feb;13(2):250-62
pubmed: 25256710
Mol Cell Biol. 2005 Sep;25(17):7432-40
pubmed: 16107692
Mol Cell Biol. 2006 Jan;26(1):277-92
pubmed: 16354698
Leukemia. 2013 Feb;27(2):441-50
pubmed: 22772059
Sci Rep. 2015 Mar 05;5:8768
pubmed: 25740062
Nat Rev Mol Cell Biol. 2016 Aug;17(8):496-510
pubmed: 27301673
Nat Genet. 2006 Oct;38(10):1133-41
pubmed: 16964264
Genes Cells. 2014 Jun;19(6):504-16
pubmed: 24774443
Cancer Lett. 2019 Jun 28;452:119-131
pubmed: 30905819
Drug Des Devel Ther. 2019 Jan 14;13:317-326
pubmed: 30679904
Cancer Sci. 2018 Sep;109(9):2717-2733
pubmed: 30047193
Cell. 2019 Oct 17;179(3):802-802.e1
pubmed: 31626778
J Natl Cancer Inst. 2012 Jan 18;104(2):133-46
pubmed: 22205655
Biomolecules. 2020 Apr 11;10(4):
pubmed: 32290447
P T. 2017 Aug;42(8):514-521
pubmed: 28781505
Cancer Immunol Immunother. 2013 Mar;62(3):517-27
pubmed: 23052245
Tumour Biol. 2013 Apr;34(2):847-51
pubmed: 23242608
Nat Commun. 2018 Apr 30;9(1):1734
pubmed: 29712925
Oncol Rep. 2019 May;41(5):2889-2896
pubmed: 30864697

Auteurs

Thomas G Johnson (TG)

The Asbestos Diseases Research Institute (ADRI), Concord Hospital, Concord, Sydney 2139, Australia.
The ANZAC Research Institute, Concord Repatriation General Hospital, Sydney 2139, Australia.
Faculty of Medicine and Health, The University of Sydney Concord Clinical School, Sydney 2139, Australia.
Sydney Catalyst Translational Research Centre, Sydney 2050, Australia.

Karin Schelch (K)

Institute of Cancer Research, Department of Medicine I, Medical University of Vienna, 1090 Vienna, Austria.

Kaitao Lai (K)

The ANZAC Research Institute, Concord Repatriation General Hospital, Sydney 2139, Australia.
Faculty of Medicine and Health, The University of Sydney Concord Clinical School, Sydney 2139, Australia.

Kamila A Marzec (KA)

The ANZAC Research Institute, Concord Repatriation General Hospital, Sydney 2139, Australia.

Marina Kennerson (M)

The ANZAC Research Institute, Concord Repatriation General Hospital, Sydney 2139, Australia.
Faculty of Medicine and Health, The University of Sydney Concord Clinical School, Sydney 2139, Australia.
Molecular Medicine Laboratory, Concord Repatriation General Hospital, Sydney 2139, Australia.

Michael Grusch (M)

Institute of Cancer Research, Department of Medicine I, Medical University of Vienna, 1090 Vienna, Austria.

Glen Reid (G)

Department of Pathology, The University of Otago, Dunedin 9054, New Zealand.
The Maurice Wilkins Centre, University of Otago, Dunedin 9054, New Zealand.

Andrew Burgess (A)

The ANZAC Research Institute, Concord Repatriation General Hospital, Sydney 2139, Australia.
Faculty of Medicine and Health, The University of Sydney Concord Clinical School, Sydney 2139, Australia.

Classifications MeSH