Blocking LBH expression causes replication stress and sensitizes triple-negative breast cancer cells to ATR inhibitor treatment.


Journal

Oncogene
ISSN: 1476-5594
Titre abrégé: Oncogene
Pays: England
ID NLM: 8711562

Informations de publication

Date de publication:
Mar 2024
Historique:
received: 30 08 2023
accepted: 18 01 2024
revised: 16 01 2024
medline: 18 3 2024
pubmed: 1 2 2024
entrez: 31 1 2024
Statut: ppublish

Résumé

Triple-negative (ER

Identifiants

pubmed: 38297083
doi: 10.1038/s41388-024-02951-3
pii: 10.1038/s41388-024-02951-3
doi:

Substances chimiques

Cell Cycle Proteins 0
Protein Kinase Inhibitors 0
LBH protein, human 0
Transcription Factors 0
ATR protein, human EC 2.7.11.1
Ataxia Telangiectasia Mutated Proteins EC 2.7.11.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

851-865

Subventions

Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R01GM113256
Organisme : U.S. Department of Defense (United States Department of Defense)
ID : W81XWH-19-1-0255

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med. 2010;363:1938–48.
pubmed: 21067385 doi: 10.1056/NEJMra1001389
Isakoff SJ. Triple-negative breast cancer: role of specific chemotherapy agents. Cancer J. 2010;16:53–61.
pubmed: 20164691 pmcid: 2882502 doi: 10.1097/PPO.0b013e3181d24ff7
Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13:4429–34.
pubmed: 17671126 doi: 10.1158/1078-0432.CCR-06-3045
Nofech-Mozes S, Trudeau M, Kahn HK, Dent R, Rawlinson E, Sun P, et al. Patterns of recurrence in the basal and non-basal subtypes of triple-negative breast cancers. Breast Cancer Res Treat. 2009;118:131–7.
pubmed: 19189211 doi: 10.1007/s10549-008-0295-8
Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61–70.
doi: 10.1038/nature11412
Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012;486:346–52.
pubmed: 22522925 pmcid: 3440846 doi: 10.1038/nature10983
Staaf J, Glodzik D, Bosch A, Vallon-Christersson J, Reutersward C, Hakkinen J, et al. Whole-genome sequencing of triple-negative breast cancers in a population-based clinical study. Nat Med. 2019;25:1526–33.
pubmed: 31570822 pmcid: 6859071 doi: 10.1038/s41591-019-0582-4
Duijf PHG, Nanayakkara D, Nones K, Srihari S, Kalimutho M, Khanna KK. Mechanisms of genomic instability in breast cancer. Trends Mol Med. 2019;25:595–611.
pubmed: 31078431 doi: 10.1016/j.molmed.2019.04.004
Derakhshan F, Reis-Filho JS. Pathogenesis of triple-negative breast cancer. Annu Rev Pathol. 2022;17:181–204.
pubmed: 35073169 pmcid: 9231507 doi: 10.1146/annurev-pathol-042420-093238
Briegel KJ, Joyner AL. Identification and characterization of Lbh, a novel conserved nuclear protein expressed during early limb and heart development. Dev Biol. 2001;233:291–304.
pubmed: 11336496 doi: 10.1006/dbio.2001.0225
Al-Ali H, Rieger ME, Seldeen KL, Harris TK, Farooq A, Briegel KJ. Biophysical characterization reveals structural disorder in the developmental transcriptional regulator LBH. Biochem Biophys Res Commun. 2010;391:1104–9.
pubmed: 20005203 doi: 10.1016/j.bbrc.2009.12.032
Rieger ME, Sims AH, Coats ER, Clarke RB, Briegel KJ. The embryonic transcription cofactor LBH is a direct target of the Wnt signaling pathway in epithelial development and in aggressive basal subtype breast cancers. Mol Cell Biol. 2010;30:4267–79.
pubmed: 20606007 pmcid: 2937547 doi: 10.1128/MCB.01418-09
Lindley LE, Curtis KM, Sanchez-Mejias A, Rieger ME, Robbins DJ, Briegel KJ. The WNT-controlled transcriptional regulator LBH is required for mammary stem cell expansion and maintenance of the basal lineage. Development. 2015;142:893–904.
pubmed: 25655704 pmcid: 4352974
Briegel KJ, Baldwin HS, Epstein JA, Joyner AL. Congenital heart disease reminiscent of partial trisomy 2p syndrome in mice transgenic for the transcription factor Lbh. Development. 2005;132:3305–16.
pubmed: 15958514 doi: 10.1242/dev.01887
Conen KL, Nishimori S, Provot S, Kronenberg HM. The transcriptional cofactor Lbh regulates angiogenesis and endochondral bone formation during fetal bone development. Dev Biol. 2009;333:348–58.
pubmed: 19607824 pmcid: 2760734 doi: 10.1016/j.ydbio.2009.07.003
Powder KE, Cousin H, McLinden GP, Craig Albertson R. A nonsynonymous mutation in the transcriptional regulator lbh is associated with cichlid craniofacial adaptation and neural crest cell development. Mol Biol Evol. 2014;31:3113–24.
pubmed: 25234704 pmcid: 4245823 doi: 10.1093/molbev/msu267
Weir E, McLinden G, Alfandari D, Cousin H. Trim-Away mediated knock down uncovers a new function for Lbh during gastrulation of Xenopus laevis. Dev Biol. 2021;470:74–83.
pubmed: 33159936 doi: 10.1016/j.ydbio.2020.10.014
Liu Q, Guan X, Lv J, Li X, Wang Y, Li L. Limb-bud and heart (LBH) functions as a tumor suppressor of nasopharyngeal carcinoma by inducing G1/S cell cycle arrest. Sci Rep. 2015;5:7626.
pubmed: 25557837 pmcid: 4283826 doi: 10.1038/srep07626
Ekwall AK, Whitaker JW, Hammaker D, Bugbee WD, Wang W, Firestein GS. The rheumatoid arthritis risk gene LBH regulates growth in fibroblast-like synoviocytes. Arthritis Rheumatol. 2015;67:1193–202.
pubmed: 25707478 pmcid: 4490933 doi: 10.1002/art.39060
Matsuda S, Hammaker D, Topolewski K, Briegel KJ, Boyle DL, Dowdy S, et al. Regulation of the cell cycle and inflammatory arthritis by the transcription cofactor LBH gene. J Immunol. 2017;199:2316–22.
pubmed: 28807995 doi: 10.4049/jimmunol.1700719
Jiang Y, Zhou J, Zou D, Hou D, Zhang H, Zhao J, et al. Overexpression of Limb-Bud and Heart (LBH) promotes angiogenesis in human glioma via VEGFA-mediated ERK signalling under hypoxia. EBioMedicine. 2019;48:36–48.
pubmed: 31631037 pmcid: 6838451 doi: 10.1016/j.ebiom.2019.09.037
Liu H, Giffen KP, Grati M, Morrill SW, Li Y, Liu X, et al. Transcription co-factor LBH is necessary for the survival of cochlear hair cells. J Cell Sci. 2021;134:jcs254458.
pubmed: 33674448 pmcid: 8077238 doi: 10.1242/jcs.254458
Chen J, Huang C, Chen K, Li S, Zhang X, Cheng J, et al. Overexpression of LBH is associated with poor prognosis in human hepatocellular carcinoma. Onco Targets Ther. 2018;11:441–8.
pubmed: 29403288 pmcid: 5783013 doi: 10.2147/OTT.S152953
Deng M, Yu R, Wang S, Zhang Y, Li Z, Song H, et al. Limb-bud and heart attenuates growth and invasion of human lung adenocarcinoma cells and predicts survival outcome. Cell Physiol Biochem. 2018;47:223–34.
pubmed: 29788015 doi: 10.1159/000489801
Yu R, Li Z, Zhang C, Song H, Deng M, Sun L, et al. Elevated limb-bud and heart development (LBH) expression indicates poor prognosis and promotes gastric cancer cell proliferation and invasion via upregulating Integrin/FAK/Akt pathway. PeerJ. 2019;7:e6885.
pubmed: 31119084 pmcid: 6507893 doi: 10.7717/peerj.6885
Young IC, Brabletz T, Lindley LE, Abreu M, Nagathihalli N, Zaika A, et al. Multi-cancer analysis reveals universal association of oncogenic LBH expression with DNA hypomethylation and WNT-Integrin signaling pathways. Cancer Gene Ther. 2023;30:1234–48.
pubmed: 37268816 pmcid: 10501907 doi: 10.1038/s41417-023-00633-y
Ashad-Bishop K, Garikapati K, Lindley LE, Jorda M, Briegel KJ. Loss of Limb-Bud-and-Heart (LBH) attenuates mammary hyperplasia and tumor development in MMTV-Wnt1 transgenic mice. Biochem Biophys Res Commun. 2019;508:536–42.
pubmed: 30509497 doi: 10.1016/j.bbrc.2018.11.155
Liu L, Luo Q, Xu Q, Xiong Y, Deng H. Limb-bud and heart development (LBH) contributes to glioma progression in vitro and in vivo. FEBS Open Bio. 2022;12:211–20.
pubmed: 34739189 doi: 10.1002/2211-5463.13325
Lamb R, Ablett MP, Spence K, Landberg G, Sims AH, Clarke RB. Wnt pathway activity in breast cancer sub-types and stem-like cells. PLoS One. 2013;8:e67811.
pubmed: 23861811 pmcid: 3701602 doi: 10.1371/journal.pone.0067811
Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T, et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med. 2007;356:217–26.
pubmed: 17229949 doi: 10.1056/NEJMoa063994
Honeth G, Bendahl PO, Ringner M, Saal LH, Gruvberger-Saal SK, Lovgren K, et al. The CD44+/CD24- phenotype is enriched in basal-like breast tumors. Breast Cancer Res. 2008;10:R53.
pubmed: 18559090 pmcid: 2481503 doi: 10.1186/bcr2108
Khramtsov AI, Khramtsova GF, Tretiakova M, Huo D, Olopade OI, Goss KH. Wnt/{beta}-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. Am J Pathol. 2010;176:2911–20.
pubmed: 20395444 pmcid: 2877852 doi: 10.2353/ajpath.2010.091125
Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst. 2008;100:672–9.
pubmed: 18445819 doi: 10.1093/jnci/djn123
Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA. 2009;106:13820–5.
pubmed: 19666588 pmcid: 2720409 doi: 10.1073/pnas.0905718106
Frontini M, Kukalev A, Leo E, Ng YM, Cervantes M, Cheng CW, et al. The CDK subunit CKS2 counteracts CKS1 to control cyclin A/CDK2 activity in maintaining replicative fidelity and neurodevelopment. Dev Cell. 2012;23:356–70.
pubmed: 22898779 pmcid: 3898080 doi: 10.1016/j.devcel.2012.06.018
Gu Y, Rosenblatt J, Morgan DO. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 1992;11:3995–4005.
pubmed: 1396589 pmcid: 556910 doi: 10.1002/j.1460-2075.1992.tb05493.x
Mass G, Nethanel T, Kaufmann G. The middle subunit of replication protein A contacts growing RNA-DNA primers in replicating simian virus 40 chromosomes. Mol Cell Biol. 1998;18:6399–407.
pubmed: 9774655 pmcid: 109225 doi: 10.1128/MCB.18.11.6399
Liaw H, Lee D, Myung K. DNA-PK-dependent RPA2 hyperphosphorylation facilitates DNA repair and suppresses sister chromatid exchange. PLoS One. 2011;6:e21424.
pubmed: 21731742 pmcid: 3120867 doi: 10.1371/journal.pone.0021424
Ashley AK, Shrivastav M, Nie J, Amerin C, Troksa K, Glanzer JG, et al. DNA-PK phosphorylation of RPA32 Ser4/Ser8 regulates replication stress checkpoint activation, fork restart, homologous recombination and mitotic catastrophe. DNA Repair (Amst). 2014;21:131–9.
pubmed: 24819595 doi: 10.1016/j.dnarep.2014.04.008
Toledo L, Neelsen KJ, Lukas J. Replication catastrophe: when a checkpoint fails because of exhaustion. Mol Cell. 2017;66:735–49.
pubmed: 28622519 doi: 10.1016/j.molcel.2017.05.001
Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol. 2014;16:2–9.
pubmed: 24366029 pmcid: 4354890 doi: 10.1038/ncb2897
Marechal A, Zou L. DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb Perspect Biol. 2013;5:a012716.
pubmed: 24003211 pmcid: 3753707 doi: 10.1101/cshperspect.a012716
Smith J, Tho LM, Xu N, Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res. 2010;108:73–112.
pubmed: 21034966 doi: 10.1016/B978-0-12-380888-2.00003-0
Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 2003;300:1542–8.
pubmed: 12791985 doi: 10.1126/science.1083430
Lecona E, Fernandez-Capetillo O. Targeting ATR in cancer. Nat Rev Cancer. 2018;18:586–95.
pubmed: 29899559 doi: 10.1038/s41568-018-0034-3
Kwon M, Kim G, Kim R, Kim KT, Kim ST, Smith S, et al. Phase II study of ceralasertib (AZD6738) in combination with durvalumab in patients with advanced gastric cancer. J Immunother Cancer. 2022;10:e005041.
pubmed: 35790315 pmcid: 9258491 doi: 10.1136/jitc-2022-005041
McMullen M, Karakasis K, Loembe B, Dean E, Parr G, Oza AM. DUETTE: a phase II randomized, multicenter study to investigate the efficacy and tolerability of a second maintenance treatment in patients with platinum-sensitive relapsed epithelial ovarian cancer, who have previously received poly(ADP-ribose) polymerase (PARP) inhibitor maintenance treatment. Int J Gynecol Cancer. 2020;30:1824–8.
pubmed: 32878963 pmcid: 7656147 doi: 10.1136/ijgc-2020-001694
Lord CJ, Ashworth A. PARP inhibitors: synthetic lethality in the clinic. Science. 2017;355:1152–8.
pubmed: 28302823 pmcid: 6175050 doi: 10.1126/science.aam7344
Garrido-Castro AC, Lin NU, Polyak K. Insights into molecular classifications of triple-negative breast cancer: improving patient selection for treatment. Cancer Discov. 2019;9:176–98.
pubmed: 30679171 pmcid: 6387871 doi: 10.1158/2159-8290.CD-18-1177
Marine JC, Dawson SJ, Dawson MA. Non-genetic mechanisms of therapeutic resistance in cancer. Nat Rev Cancer. 2020;20:743–56.
pubmed: 33033407 doi: 10.1038/s41568-020-00302-4
Lehmann BD, Jovanovic B, Chen X, Estrada MV, Johnson KN, Shyr Y, et al. Refinement of triple-negative breast cancer molecular subtypes: implications for neoadjuvant chemotherapy selection. PLoS One. 2016;11:e0157368.
pubmed: 27310713 pmcid: 4911051 doi: 10.1371/journal.pone.0157368
Minn AJ, Kang Y, Serganova I, Gupta GP, Giri DD, Doubrovin M, et al. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J Clin Invest. 2005;115:44–55.
pubmed: 15630443 pmcid: 539194 doi: 10.1172/JCI22320

Auteurs

Koteswararao Garikapati (K)

DeWitt Daugherty Department of Surgery, Molecular Oncology Program, University of Miami Miller School of Medicine, Miami, FL, USA.
Braman Family Breast Cancer Institute at the Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL, USA.

In-Chi Young (IC)

DeWitt Daugherty Department of Surgery, Molecular Oncology Program, University of Miami Miller School of Medicine, Miami, FL, USA.
Braman Family Breast Cancer Institute at the Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL, USA.

Sunhwa Hong (S)

DeWitt Daugherty Department of Surgery, Molecular Oncology Program, University of Miami Miller School of Medicine, Miami, FL, USA.
Braman Family Breast Cancer Institute at the Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL, USA.

Priyamvada Rai (P)

Department of Radiation Oncology and Tumor Biology Program at the Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL, USA.

Chaitanya Jain (C)

Department of Biochemistry and Molecular Biology, University of Miami Miller School of Medicine, Miami, FL, USA.

Karoline J Briegel (KJ)

DeWitt Daugherty Department of Surgery, Molecular Oncology Program, University of Miami Miller School of Medicine, Miami, FL, USA. kbriegel@med.miami.edu.
Braman Family Breast Cancer Institute at the Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL, USA. kbriegel@med.miami.edu.

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Classifications MeSH