Cisplatin-resistant triple-negative breast cancer subtypes: multiple mechanisms of resistance.


Journal

BMC cancer
ISSN: 1471-2407
Titre abrégé: BMC Cancer
Pays: England
ID NLM: 100967800

Informations de publication

Date de publication:
04 Nov 2019
Historique:
received: 24 01 2019
accepted: 21 10 2019
entrez: 6 11 2019
pubmed: 7 11 2019
medline: 4 4 2020
Statut: epublish

Résumé

Understanding mechanisms underlying specific chemotherapeutic responses in subtypes of cancer may improve identification of treatment strategies most likely to benefit particular patients. For example, triple-negative breast cancer (TNBC) patients have variable response to the chemotherapeutic agent cisplatin. Understanding the basis of treatment response in cancer subtypes will lead to more informed decisions about selection of treatment strategies. In this study we used an integrative functional genomics approach to investigate the molecular mechanisms underlying known cisplatin-response differences among subtypes of TNBC. To identify changes in gene expression that could explain mechanisms of resistance, we examined 102 evolutionarily conserved cisplatin-associated genes, evaluating their differential expression in the cisplatin-sensitive, basal-like 1 (BL1) and basal-like 2 (BL2) subtypes, and the two cisplatin-resistant, luminal androgen receptor (LAR) and mesenchymal (M) subtypes of TNBC. We found 20 genes that were differentially expressed in at least one subtype. Fifteen of the 20 genes are associated with cell death and are distributed among all TNBC subtypes. The less cisplatin-responsive LAR and M TNBC subtypes show different regulation of 13 genes compared to the more sensitive BL1 and BL2 subtypes. These 13 genes identify a variety of cisplatin-resistance mechanisms including increased transport and detoxification of cisplatin, and mis-regulation of the epithelial to mesenchymal transition. We identified gene signatures in resistant TNBC subtypes indicative of mechanisms of cisplatin. Our results indicate that response to cisplatin in TNBC has a complex foundation based on impact of treatment on distinct cellular pathways. We find that examination of expression data in the context of heterogeneous data such as drug-gene interactions leads to a better understanding of mechanisms at work in cancer therapy response.

Sections du résumé

BACKGROUND BACKGROUND
Understanding mechanisms underlying specific chemotherapeutic responses in subtypes of cancer may improve identification of treatment strategies most likely to benefit particular patients. For example, triple-negative breast cancer (TNBC) patients have variable response to the chemotherapeutic agent cisplatin. Understanding the basis of treatment response in cancer subtypes will lead to more informed decisions about selection of treatment strategies.
METHODS METHODS
In this study we used an integrative functional genomics approach to investigate the molecular mechanisms underlying known cisplatin-response differences among subtypes of TNBC. To identify changes in gene expression that could explain mechanisms of resistance, we examined 102 evolutionarily conserved cisplatin-associated genes, evaluating their differential expression in the cisplatin-sensitive, basal-like 1 (BL1) and basal-like 2 (BL2) subtypes, and the two cisplatin-resistant, luminal androgen receptor (LAR) and mesenchymal (M) subtypes of TNBC.
RESULTS RESULTS
We found 20 genes that were differentially expressed in at least one subtype. Fifteen of the 20 genes are associated with cell death and are distributed among all TNBC subtypes. The less cisplatin-responsive LAR and M TNBC subtypes show different regulation of 13 genes compared to the more sensitive BL1 and BL2 subtypes. These 13 genes identify a variety of cisplatin-resistance mechanisms including increased transport and detoxification of cisplatin, and mis-regulation of the epithelial to mesenchymal transition.
CONCLUSIONS CONCLUSIONS
We identified gene signatures in resistant TNBC subtypes indicative of mechanisms of cisplatin. Our results indicate that response to cisplatin in TNBC has a complex foundation based on impact of treatment on distinct cellular pathways. We find that examination of expression data in the context of heterogeneous data such as drug-gene interactions leads to a better understanding of mechanisms at work in cancer therapy response.

Identifiants

pubmed: 31684899
doi: 10.1186/s12885-019-6278-9
pii: 10.1186/s12885-019-6278-9
pmc: PMC6829976
doi:

Substances chimiques

Antineoplastic Agents 0
Receptors, Androgen 0
Cisplatin Q20Q21Q62J

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1039

Subventions

Organisme : NHGRI NIH HHS
ID : R25 HG007053
Pays : United States
Organisme : NIH HHS
ID : AA018776
Pays : United States
Organisme : NCI NIH HHS
ID : P30CA034196
Pays : United States
Organisme : NHGRI NIH HHS
ID : U41 HG000330
Pays : United States
Organisme : NIAAA NIH HHS
ID : R01 AA018776
Pays : United States

Références

Oncotarget. 2016 Mar 22;7(12):14659-72
pubmed: 26894974
Cancer Lett. 2004 Jul 28;211(1):69-78
pubmed: 15194218
Oncogene. 2003 Oct 20;22(47):7265-79
pubmed: 14576837
Int J Mol Sci. 2016 Aug 31;17(9):
pubmed: 27589736
Breast Cancer Res Treat. 2016 Dec;160(3):425-437
pubmed: 27770282
Sci Rep. 2018 Mar 9;8(1):4306
pubmed: 29523854
Int J Mol Sci. 2014 Feb 27;15(3):3560-79
pubmed: 24583847
Breast Cancer Res. 2010;12 Suppl 2:S3
pubmed: 21050424
Lab Invest. 2018 Jan;98(1):63-78
pubmed: 29106395
Toxicol Lett. 2013 Aug 29;221(3):165-75
pubmed: 23831944
BMC Cancer. 2012 Mar 19;12:91
pubmed: 22429801
Cell Death Dis. 2012 Dec 20;3:e449
pubmed: 23254292
Cancer Chemother Pharmacol. 2009 Jun;64(1):133-42
pubmed: 18998134
Cancer Res. 2007 Jul 1;67(13):6325-32
pubmed: 17616691
Nucleic Acids Res. 2016 Jan 4;44(D1):D1214-9
pubmed: 26467479
Met Based Drugs. 2010;2010:null
pubmed: 20885916
Mamm Genome. 2015 Oct;26(9-10):584-9
pubmed: 26093607
Nucleic Acids Res. 2016 Jan 4;44(D1):D555-9
pubmed: 26656951
Cell Death Dis. 2014 May 29;5:e1257
pubmed: 24874729
J Biol Chem. 2009 May 22;284(21):14029-39
pubmed: 19286655
Gynecol Oncol. 2005 Feb;96(2):287-95
pubmed: 15661210
Cancer Manag Res. 2018 Jan 15;10:91-103
pubmed: 29391830
PLoS One. 2016 Jun 16;11(6):e0157368
pubmed: 27310713
Clin Cancer Res. 2015 Apr 1;21(7):1688-98
pubmed: 25208879
Nature. 2000 Aug 17;406(6797):747-52
pubmed: 10963602
Cell Physiol Biochem. 2014;33(4):1162-75
pubmed: 24751980
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Cancer Biol Ther. 2010 Aug 1;10(3):223-31
pubmed: 20523116
Proc Natl Acad Sci U S A. 2016 Apr 26;113(17):E2373-82
pubmed: 27071093
Cancer Biol Med. 2015 Jun;12(2):106-16
pubmed: 26175926
Clin Cancer Res. 2017 Dec 15;23(24):7521-7530
pubmed: 29246904
ESMO Open. 2017 Sep 14;2(4):e000208
pubmed: 29018573
J Neurochem. 2018 Jan;144(1):93-104
pubmed: 29105080
Nat Cell Biol. 2016 May;18(5):572-8
pubmed: 27088857
Nucleic Acids Res. 2019 Jan 8;47(D1):D948-D954
pubmed: 30247620
Mol Oncol. 2017 Jul;11(7):878-891
pubmed: 28544151
Clin Cancer Res. 2007 Aug 1;13(15 Pt 1):4429-34
pubmed: 17671126
Nucleic Acids Res. 2017 Jan 4;45(D1):D619-D625
pubmed: 27799471
Cancer Res. 2000 Aug 15;60(16):4386-90
pubmed: 10969782
Nucleic Acids Res. 2017 Jan 4;45(D1):D353-D361
pubmed: 27899662
Nucleic Acids Res. 2012 Jan;40(Database issue):D1067-76
pubmed: 22080549
Food Chem Toxicol. 2007 Nov;45(11):2155-64
pubmed: 17619073
World J Surg Oncol. 2015 Feb 25;13:80
pubmed: 25884382
Mol Cancer Res. 2010 Dec;8(12):1633-42
pubmed: 21047769
Onco Targets Ther. 2015 Aug 28;8:2319-27
pubmed: 26356142
J Exp Clin Cancer Res. 2010 May 14;29:49
pubmed: 20470393
Oncotarget. 2016 Jul 19;7(29):45876-45888
pubmed: 27322682
Mamm Genome. 2015 Oct;26(9-10):567-73
pubmed: 26047590
Nucleic Acids Res. 2019 Jan 8;47(D1):D607-D613
pubmed: 30476243
Trends Cancer. 2018 Feb;4(2):110-118
pubmed: 29458961
Nucleic Acids Res. 2015 Jan;43(Database issue):D1071-8
pubmed: 25348409
FEBS Lett. 2012 May 7;586(9):1279-86
pubmed: 22465665
BMB Rep. 2015 Jan;48(1):30-5
pubmed: 24755555
Nucleic Acids Res. 2015 Jan;43(Database issue):D1057-63
pubmed: 25378336
Oncotarget. 2014 Dec 15;5(23):11778-91
pubmed: 25473892
Nature. 2013 Aug 22;500(7463):415-21
pubmed: 23945592
Cell Death Dis. 2014 Jun 12;5:e1292
pubmed: 24922076
Cell Biol Int. 2017 Apr;41(4):405-414
pubmed: 28150354
Pharmacogenomics. 2017 Nov;18(17):1595-1609
pubmed: 29095114
DNA Repair (Amst). 2015 Nov;35:126-36
pubmed: 26519826
ESMO Open. 2019 May 13;4(Suppl 2):e000504
pubmed: 31231572
IUBMB Life. 2007 Nov;59(11):696-9
pubmed: 17885832
Oncogene. 2012 Apr 12;31(15):1869-83
pubmed: 21892204
Biochemistry. 1996 Aug 6;35(31):10004-13
pubmed: 8756462
Nucleic Acids Res. 2017 Jan 4;45(D1):D972-D978
pubmed: 27651457
Am J Hum Genet. 2015 Jul 2;97(1):111-24
pubmed: 26119816
BMC Cancer. 2011 Nov 01;11:470
pubmed: 22044796
J Clin Oncol. 2008 Mar 10;26(8):1275-81
pubmed: 18250347
Eur J Pharmacol. 2014 Oct 5;740:364-78
pubmed: 25058905
J Clin Invest. 2011 Jul;121(7):2750-67
pubmed: 21633166
Oncologist. 2013;18(2):123-33
pubmed: 23404817
Am J Transl Res. 2017 Mar 15;9(3):1127-1138
pubmed: 28386339
Cancer Treat Rev. 2007 Feb;33(1):9-23
pubmed: 17084534

Auteurs

David P Hill (DP)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA. david.hill@jax.org.

Akeena Harper (A)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Joan Malcolm (J)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Monica S McAndrews (MS)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Susan M Mockus (SM)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Sara E Patterson (SE)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Timothy Reynolds (T)

Baylor University, Waco, TX, 76798, USA.

Erich J Baker (EJ)

Baylor University, Waco, TX, 76798, USA.

Carol J Bult (CJ)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Elissa J Chesler (EJ)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Judith A Blake (JA)

The Jackson Laboratory, ME 04609 and Farmington, Bar Harbor, CT, 06032, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH