MiR-1287-5p inhibits triple negative breast cancer growth by interaction with phosphoinositide 3-kinase CB, thereby sensitizing cells for PI3Kinase inhibitors.


Journal

Breast cancer research : BCR
ISSN: 1465-542X
Titre abrégé: Breast Cancer Res
Pays: England
ID NLM: 100927353

Informations de publication

Date de publication:
01 02 2019
Historique:
received: 20 09 2018
accepted: 18 01 2019
entrez: 3 2 2019
pubmed: 3 2 2019
medline: 23 7 2019
Statut: epublish

Résumé

Non-coding RNAs and especially microRNAs have been discovered to act as master regulators of cancer initiation and progression. The aim of our study was to discover and characterize the function of yet functionally uncharacterized microRNAs in human breast carcinogenesis. In an unbiased approach, we utilized an established model system for breast cancer (BC) stem cell formation ("mammosphere assay") to identify whole miRNome alterations in breast carcinogenesis. Clinical samples of BC patients were used to evaluate the human relevance of the newly identified miRNA candidates. One promising candidate, miR-1287-5p, was further explored on its impact on several hallmarks of cancer. The molecular mode of action was characterized by whole transcriptome analysis, in silico prediction tools, miRNA-interaction assays, pheno-copy assays, and drug sensitivity assays. Among several other microRNAs, miR-1287-5p was significantly downregulated in mammospheres and human BC tissue compared to normal breast tissue (p < 0.0001). Low expression levels were significantly associated with poor prognosis in BC patients. MiR-1287-5p significantly decreased cellular growth, cells in S phase of cell cycle, anchorage-independent growth, and tumor formation in vivo. In addition, we identified PIK3CB as a direct molecular interactor of miR-1287-5p and a novel prognostic factor in BC. Finally, PI3Kinase pathway chemical inhibitors combined with miR-1287-5p mimic increased the pharmacological growth inhibitory potential in triple negative BC cells. Our data identified for the first time the involvement of miR-1287-5p in human BC and suggest a potential for therapeutic interventions in difficult to treat triple negative BC.

Sections du résumé

BACKGROUND
Non-coding RNAs and especially microRNAs have been discovered to act as master regulators of cancer initiation and progression. The aim of our study was to discover and characterize the function of yet functionally uncharacterized microRNAs in human breast carcinogenesis.
METHODS
In an unbiased approach, we utilized an established model system for breast cancer (BC) stem cell formation ("mammosphere assay") to identify whole miRNome alterations in breast carcinogenesis. Clinical samples of BC patients were used to evaluate the human relevance of the newly identified miRNA candidates. One promising candidate, miR-1287-5p, was further explored on its impact on several hallmarks of cancer. The molecular mode of action was characterized by whole transcriptome analysis, in silico prediction tools, miRNA-interaction assays, pheno-copy assays, and drug sensitivity assays.
RESULTS
Among several other microRNAs, miR-1287-5p was significantly downregulated in mammospheres and human BC tissue compared to normal breast tissue (p < 0.0001). Low expression levels were significantly associated with poor prognosis in BC patients. MiR-1287-5p significantly decreased cellular growth, cells in S phase of cell cycle, anchorage-independent growth, and tumor formation in vivo. In addition, we identified PIK3CB as a direct molecular interactor of miR-1287-5p and a novel prognostic factor in BC. Finally, PI3Kinase pathway chemical inhibitors combined with miR-1287-5p mimic increased the pharmacological growth inhibitory potential in triple negative BC cells.
CONCLUSION
Our data identified for the first time the involvement of miR-1287-5p in human BC and suggest a potential for therapeutic interventions in difficult to treat triple negative BC.

Identifiants

pubmed: 30709367
doi: 10.1186/s13058-019-1104-5
pii: 10.1186/s13058-019-1104-5
pmc: PMC6359814
doi:

Substances chimiques

MIRN1287 microRNA, human 0
MicroRNAs 0
Class I Phosphatidylinositol 3-Kinases EC 2.7.1.137
PIK3CB protein, human EC 2.7.1.137

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

20

Subventions

Organisme : NCATS NIH HHS
ID : UH3TR00943-01
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA182905-01
Pays : United States

Références

Int J Mol Sci. 2014 Nov 06;15(11):20266-89
pubmed: 25383673
Nat Methods. 2015 Aug;12(8):697
pubmed: 26226356
Oncotarget. 2016 Dec 20;7(51):84054-84071
pubmed: 27863432
Br J Cancer. 2015 Aug 11;113(4):569-73
pubmed: 26158421
Clin Pharmacokinet. 2016 Jan;55(1):33-45
pubmed: 26242379
Clin Cancer Res. 2017 Jan 1;23(1):26-34
pubmed: 27126994
Cell. 2008 May 2;133(3):403-14
pubmed: 18455982
BMC Med Genomics. 2009 Jun 09;2:35
pubmed: 19508715
N Engl J Med. 2010 Nov 11;363(20):1938-48
pubmed: 21067385
J Clin Invest. 2011 Oct;121(10):3786-8
pubmed: 21965334
Virol J. 2013 Jun 03;10:175
pubmed: 23732000
Haematologica. 2012 Apr;97(4):586-94
pubmed: 22102710
Cancer Genet. 2013 Sep-Oct;206(9-10):340-6
pubmed: 24238754
Curr Opin Genet Dev. 2009 Feb;19(1):44-50
pubmed: 19167210
Nat Rev Cancer. 2006 Nov;6(11):857-66
pubmed: 17060945
Nat Commun. 2017 Oct 16;8(1):947
pubmed: 29038531
Nat Rev Genet. 2006 Aug;7(8):606-19
pubmed: 16847462
Clin Cancer Res. 2017 Sep 1;23(17):5255-5266
pubmed: 28533224
Nat Rev Drug Discov. 2009 Aug;8(8):627-44
pubmed: 19644473
Nature. 2005 Feb 17;433(7027):769-73
pubmed: 15685193
J Natl Cancer Inst. 2015 Feb 06;107(3):
pubmed: 25663689
Lancet Oncol. 2017 Oct;18(10):1293-1294
pubmed: 28800863
Nat Rev Cancer. 2015 Jan;15(1):7-24
pubmed: 25533673
Cancer Res. 2005 Aug 15;65(16):7065-70
pubmed: 16103053
Mol Cancer. 2014 Jun 04;13:142
pubmed: 24897960
Bioinform Biol Insights. 2015 May 12;9:89-101
pubmed: 25983556
Nat Commun. 2016 Apr 04;7:11169
pubmed: 27041221
Clin Cancer Res. 2017 Mar 1;23(5):1323-1333
pubmed: 27601590
Science. 2002 May 31;296(5573):1655-7
pubmed: 12040186
Nature. 2000 Aug 17;406(6797):747-52
pubmed: 10963602
Mol Biol Rep. 2013 Mar;40(3):2175-86
pubmed: 23196705
Stem Cells. 2014 Jun;32(6):1578-90
pubmed: 24375761
Gastroenterology. 2012 Apr;142(4):886-896.e9
pubmed: 22240480
Breast Cancer Res Treat. 2016 Dec;160(3):439-446
pubmed: 27744485
Proc Natl Acad Sci U S A. 2008 Sep 2;105(35):13057-62
pubmed: 18755892
Breast Cancer Res Treat. 2010 Oct;123(3):725-31
pubmed: 20020197
Clin Cancer Res. 2007 Aug 1;13(15 Pt 1):4429-34
pubmed: 17671126
Cancer Res. 2016 Jul 1;76(13):3666-70
pubmed: 27325641
Cell. 2009 Jan 23;136(2):215-33
pubmed: 19167326
J Natl Cancer Inst. 2017 Oct 1;109(10):
pubmed: 28383653
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10869-74
pubmed: 11553815
N Engl J Med. 2017 Aug 10;377(6):523-533
pubmed: 28578601
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
CA Cancer J Clin. 2017 Jan;67(1):7-30
pubmed: 28055103
Genes Dev. 2003 May 15;17(10):1253-70
pubmed: 12756227

Auteurs

Daniela Schwarzenbacher (D)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria.
Research Unit for Non-coding RNAs and Genome Editing, Medical University of Graz (MUG), Graz, Austria.

Christiane Klec (C)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria.
Research Unit for Non-coding RNAs and Genome Editing, Medical University of Graz (MUG), Graz, Austria.

Barbara Pasculli (B)

Fondazione IRCCS Casa Sollievo della Sofferenza Laboratorio di Oncologia, San Giovanni Rotundo, FG, Italy.

Stefanie Cerk (S)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria.
Research Unit for Non-coding RNAs and Genome Editing, Medical University of Graz (MUG), Graz, Austria.

Beate Rinner (B)

Biomedical Research, Medical University of Graz, Graz, Austria.

Michael Karbiener (M)

Department of Phoniatrics, ENT University Hospital, Medical University of Graz, Graz, Austria.

Cristina Ivan (C)

Department of Experimental Therapeutics -- Unit 1950, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
The Center for RNA Interference and Non-coding RNAs, The University of Texas, MD Anderson Cancer Center, Houston, TX, USA.

Raffaela Barbano (R)

Fondazione IRCCS Casa Sollievo della Sofferenza Laboratorio di Oncologia, San Giovanni Rotundo, FG, Italy.

Hui Ling (H)

Department of Experimental Therapeutics -- Unit 1950, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.

Annika Wulf-Goldenberg (A)

Experimental Pharmacology & Oncology GmbH, EPO, Berlin, Germany.

Stefanie Stanzer (S)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria.
Research Unit for Non-coding RNAs and Genome Editing, Medical University of Graz (MUG), Graz, Austria.

Gabriel Rinnerthaler (G)

IIIrd Medical Department with Hematology and Medical Oncology, Hemostaseology, Rheumatology and Infectious Diseases, Oncologic Center, Paracelsus Medical University, Salzburg, Austria.

Herbert Stoeger (H)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria.

Thomas Bauernhofer (T)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria.

Johannes Haybaeck (J)

Institute of Pathology, Medical University of Graz, Graz, Austria.
Department of Pathology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Gerald Hoefler (G)

Institute of Pathology, Medical University of Graz, Graz, Austria.

Stephan Wenzel Jahn (SW)

Institute of Pathology, Medical University of Graz, Graz, Austria.

Paola Parrella (P)

Fondazione IRCCS Casa Sollievo della Sofferenza Laboratorio di Oncologia, San Giovanni Rotundo, FG, Italy.

George Adrian Calin (GA)

Department of Experimental Therapeutics -- Unit 1950, The University of Texas MD Anderson Cancer Center, Houston, TX, USA.
The Center for RNA Interference and Non-coding RNAs, The University of Texas, MD Anderson Cancer Center, Houston, TX, USA.

Martin Pichler (M)

Division of Oncology, Department of Internal Medicine, Medical University of Graz (MUG), Graz, Austria. mart.pichler@gmx.net.
Research Unit for Non-coding RNAs and Genome Editing, Medical University of Graz (MUG), Graz, Austria. mart.pichler@gmx.net.
Department of Experimental Therapeutics -- Unit 1950, The University of Texas MD Anderson Cancer Center, Houston, TX, USA. mart.pichler@gmx.net.

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