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
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
851-865Subventions
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