Carboplatin in BRCA1/2-mutated and triple-negative breast cancer BRCAness subgroups: the TNT Trial
Germline mutations in BRCA1/2 predispose individuals to breast cancer (termed germline-mutated BRCA1/2 breast cancer, gBRCA-BC) by impairing homologous recombination (HR) and causing genomic instability. HR also repairs DNA lesions caused by platinum agents and PARP inhibitors. Triple-negative breas...
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| Published in | Nature medicine Vol. 24; no. 5; pp. 628 - 637 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Nature Publishing Group
01.05.2018
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1078-8956 1546-170X |
| DOI | 10.1038/s41591-018-0009-7 |
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| Abstract | Germline mutations in BRCA1/2 predispose individuals to breast cancer (termed germline-mutated BRCA1/2 breast cancer, gBRCA-BC) by impairing homologous recombination (HR) and causing genomic instability. HR also repairs DNA lesions caused by platinum agents and PARP inhibitors. Triple-negative breast cancers (TNBCs) harbor subpopulations with BRCA1/2 mutations, hypothesized to be especially platinum-sensitive. Cancers in putative 'BRCAness' subgroups-tumors with BRCA1 methylation; low levels of BRCA1 mRNA (BRCA1 mRNA-low); or mutational signatures for HR deficiency and those with basal phenotypes-may also be sensitive to platinum. We assessed the efficacy of carboplatin and another mechanistically distinct therapy, docetaxel, in a phase 3 trial in subjects with unselected advanced TNBC. A prespecified protocol enabled biomarker-treatment interaction analyses in gBRCA-BC and BRCAness subgroups. The primary endpoint was objective response rate (ORR). In the unselected population (376 subjects; 188 carboplatin, 188 docetaxel), carboplatin was not more active than docetaxel (ORR, 31.4% versus 34.0%, respectively; P = 0.66). In contrast, in subjects with gBRCA-BC, carboplatin had double the ORR of docetaxel (68% versus 33%, respectively; biomarker, treatment interaction P = 0.01). Such benefit was not observed for subjects with BRCA1 methylation, BRCA1 mRNA-low tumors or a high score in a Myriad HRD assay. Significant interaction between treatment and the basal-like subtype was driven by high docetaxel response in the nonbasal subgroup. We conclude that patients with advanced TNBC benefit from characterization of BRCA1/2 mutations, but not BRCA1 methylation or Myriad HRD analyses, to inform choices on platinum-based chemotherapy. Additionally, gene expression analysis of basal-like cancers may also influence treatment selection. |
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| AbstractList | Germline mutations in BRCA1/2 predispose individuals to breast cancer (termed germline-mutated BRCA1/2 breast cancer, gBRCA-BC) by impairing homologous recombination (HR) and causing genomic instability. HR also repairs DNA lesions caused by platinum agents and PARP inhibitors. Triple-negative breast cancers (TNBCs) harbor subpopulations with BRCA1/2 mutations, hypothesized to be especially platinum-sensitive. Cancers in putative ‘BRCAness’ subgroups—tumors with BRCA1 methylation; low levels of BRCA1 mRNA (BRCA1 mRNA-low); or mutational signatures for HR deficiency and those with basal phenotypes—may also be sensitive to platinum. We assessed the efficacy of carboplatin and another mechanistically distinct therapy, docetaxel, in a phase 3 trial in subjects with unselected advanced TNBC. A prespecified protocol enabled biomarker–treatment interaction analyses in gBRCA-BC and BRCAness subgroups. The primary endpoint was objective response rate (ORR). In the unselected population (376 subjects; 188 carboplatin, 188 docetaxel), carboplatin was not more active than docetaxel (ORR, 31.4% versus 34.0%, respectively; P = 0.66). In contrast, in subjects with gBRCA-BC, carboplatin had double the ORR of docetaxel (68% versus 33%, respectively; biomarker, treatment interaction P = 0.01). Such benefit was not observed for subjects with BRCA1 methylation, BRCA1 mRNA-low tumors or a high score in a Myriad HRD assay. Significant interaction between treatment and the basal-like subtype was driven by high docetaxel response in the nonbasal subgroup. We conclude that patients with advanced TNBC benefit from characterization of BRCA1/2 mutations, but not BRCA1 methylation or Myriad HRD analyses, to inform choices on platinum-based chemotherapy. Additionally, gene expression analysis of basal-like cancers may also influence treatment selection. Germline mutations in BRCA1/2 predispose individuals to breast cancer (termed germline-mutated BRCA1/2 breast cancer, gBRCA-BC) by impairing homologous recombination (HR) and causing genomic instability. HR also repairs DNA lesions caused by platinum agents and PARP inhibitors. Triple-negative breast cancers (TNBCs) harbor subpopulations with BRCA1/2 mutations, hypothesized to be especially platinum-sensitive. Cancers in putative 'BRCAness' subgroups-tumors with BRCA1 methylation; low levels of BRCA1 mRNA (BRCA1 mRNA-low); or mutational signatures for HR deficiency and those with basal phenotypes-may also be sensitive to platinum. We assessed the efficacy of carboplatin and another mechanistically distinct therapy, docetaxel, in a phase 3 trial in subjects with unselected advanced TNBC. A prespecified protocol enabled biomarker-treatment interaction analyses in gBRCA-BC and BRCAness subgroups. The primary endpoint was objective response rate (ORR). In the unselected population (376 subjects; 188 carboplatin, 188 docetaxel), carboplatin was not more active than docetaxel (ORR, 31.4% versus 34.0%, respectively; P = 0.66). In contrast, in subjects with gBRCA-BC, carboplatin had double the ORR of docetaxel (68% versus 33%, respectively; biomarker, treatment interaction P = 0.01). Such benefit was not observed for subjects with BRCA1 methylation, BRCA1 mRNA-low tumors or a high score in a Myriad HRD assay. Significant interaction between treatment and the basal-like subtype was driven by high docetaxel response in the nonbasal subgroup. We conclude that patients with advanced TNBC benefit from characterization of BRCA1/2 mutations, but not BRCA1 methylation or Myriad HRD analyses, to inform choices on platinum-based chemotherapy. Additionally, gene expression analysis of basal-like cancers may also influence treatment selection. |
| Author | Harper-Wynne, Catherine Timms, Kirsten M Hatton, Matthew Q Lanchbury, Jerry S Barrett-Lee, Peter Fox, Lisa Abraham, Jacinta Chan, Stephen Ellis, Paul Grigoriadis, Anita Smith, Ian E Pinder, Sarah E Gazinska, Patrycja Owen, Julie Hoadley, Katherine A Flanagan, James M Parikh, Jyoti Gillett, Cheryl Ashworth, Alan Wardley, Andrew M Tutt, Andrew Kilburn, Lucy Dowsett, Mitchell Cheang, Maggie Chon U Shaw, Adam Brown, Robert Gutin, Alexander Barrett, Sophie Perou, Charles M Shah, Vandna Bliss, Judith M Roylance, Rebecca Parker, Peter Rahman, Nazneen Harries, Mark Tovey, Holly Kernaghan, Sarah Wilson, Gregory |
| Author_xml | – sequence: 1 givenname: Andrew orcidid: 0000-0001-8715-2901 surname: Tutt fullname: Tutt, Andrew email: andrew.tutt@icr.ac.uk, andrew.tutt@icr.ac.uk organization: Breast Cancer Now Research Unit, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences and Medicine, King's College London, Guy's Hospital, London, UK. andrew.tutt@icr.ac.uk – sequence: 2 givenname: Holly surname: Tovey fullname: Tovey, Holly organization: Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK – sequence: 3 givenname: Maggie Chon U surname: Cheang fullname: Cheang, Maggie Chon U organization: Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK – sequence: 4 givenname: Sarah surname: Kernaghan fullname: Kernaghan, Sarah organization: Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK – sequence: 5 givenname: Lucy surname: Kilburn fullname: Kilburn, Lucy organization: Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK – sequence: 6 givenname: Patrycja surname: Gazinska fullname: Gazinska, Patrycja organization: Breast Cancer Now Research Unit, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences and Medicine, King's College London, Guy's Hospital, London, UK – sequence: 7 givenname: Julie surname: Owen fullname: Owen, Julie organization: King's Health Partners Cancer Biobank, King's College London, London, UK – sequence: 8 givenname: Jacinta surname: Abraham fullname: Abraham, Jacinta organization: Velindre Cancer Centre, Cardiff, UK – sequence: 9 givenname: Sophie surname: Barrett fullname: Barrett, Sophie organization: Beatson West of Scotland Cancer Centre, Glasgow, UK – sequence: 10 givenname: Peter surname: Barrett-Lee fullname: Barrett-Lee, Peter organization: Velindre Cancer Centre, Cardiff, UK – sequence: 11 givenname: Robert surname: Brown fullname: Brown, Robert organization: Division of Molecular Pathology, The Institute of Cancer Research, London, UK – sequence: 12 givenname: Stephen surname: Chan fullname: Chan, Stephen organization: Department of Clinical Oncology, Nottingham University Hospitals NHS Trust, Nottingham, UK – sequence: 13 givenname: Mitchell surname: Dowsett fullname: Dowsett, Mitchell organization: Ralph Lauren Centre for Breast Cancer Research, Royal Marsden Hospital, London, UK – sequence: 14 givenname: James M surname: Flanagan fullname: Flanagan, James M organization: Department of Surgery and Cancer, Imperial College London, London, UK – sequence: 15 givenname: Lisa surname: Fox fullname: Fox, Lisa organization: Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK – sequence: 16 givenname: Anita orcidid: 0000-0003-3434-201X surname: Grigoriadis fullname: Grigoriadis, Anita organization: Breast Cancer Now Research Unit, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences and Medicine, King's College London, Guy's Hospital, London, UK – sequence: 17 givenname: Alexander surname: Gutin fullname: Gutin, Alexander organization: Myriad Genetics, Inc., Salt Lake City, UT, USA – sequence: 18 givenname: Catherine surname: Harper-Wynne fullname: Harper-Wynne, Catherine organization: Kent Oncology Centre, Maidstone and Tunbridge Wells NHS Trust, Kent, UK – sequence: 19 givenname: Matthew Q surname: Hatton fullname: Hatton, Matthew Q organization: Department of Clinical Oncology, Weston Park Hospital, Sheffield, UK – sequence: 20 givenname: Katherine A surname: Hoadley fullname: Hoadley, Katherine A organization: Department of Genetics and Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA – sequence: 21 givenname: Jyoti surname: Parikh fullname: Parikh, Jyoti organization: Department of Radiology, Guy's and St Thomas' Hospitals NHS Foundation Trust, London, UK – sequence: 22 givenname: Peter surname: Parker fullname: Parker, Peter organization: Protein Phosphorylation Laboratory, Francis Crick Institute, London, UK – sequence: 23 givenname: Charles M surname: Perou fullname: Perou, Charles M organization: Department of Genetics and Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA – sequence: 24 givenname: Rebecca surname: Roylance fullname: Roylance, Rebecca organization: Department of Oncology, University College London Hospitals NHS Foundation Trust and NIHR University College London Hospitals Biomedical Research Centre, London, UK – sequence: 25 givenname: Vandna surname: Shah fullname: Shah, Vandna organization: Breast Cancer Now Research Unit, School of Cancer and Pharmaceutical Sciences, Faculty of Life Sciences and Medicine, King's College London, Guy's Hospital, London, UK – sequence: 26 givenname: Adam surname: Shaw fullname: Shaw, Adam organization: Department of Medical and Molecular Genetics, Guy's and St Thomas' NHS Foundation Trust, London, UK – sequence: 27 givenname: Ian E surname: Smith fullname: Smith, Ian E organization: Breast Unit, The Royal Marsden NHS Foundation Trust, London, UK – sequence: 28 givenname: Kirsten M surname: Timms fullname: Timms, Kirsten M organization: Myriad Genetics, Inc., Salt Lake City, UT, USA – sequence: 29 givenname: Andrew M orcidid: 0000-0002-9639-0888 surname: Wardley fullname: Wardley, Andrew M organization: NIHR Manchester Clinical Research Facility at The Christie and Division of Cancer Sciences and University of Manchester, Manchester Academic Health Science Centre, Manchester, UK – sequence: 30 givenname: Gregory surname: Wilson fullname: Wilson, Gregory organization: The Christie NHS Foundation Trust, Manchester, UK – sequence: 31 givenname: Cheryl surname: Gillett fullname: Gillett, Cheryl organization: Research Oncology, Division of Cancer Studies, King's College London, Guy's Hospital, London, UK – sequence: 32 givenname: Jerry S surname: Lanchbury fullname: Lanchbury, Jerry S organization: Myriad Genetics, Inc., Salt Lake City, UT, USA – sequence: 33 givenname: Alan surname: Ashworth fullname: Ashworth, Alan organization: UCSF Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, USA – sequence: 34 givenname: Nazneen surname: Rahman fullname: Rahman, Nazneen organization: Cancer Genetics Unit, The Royal Marsden NHS Foundation Trust, London, UK – sequence: 35 givenname: Mark surname: Harries fullname: Harries, Mark organization: Department of Medical Oncology, Guy's and St Thomas Foundation Trust, London, UK – sequence: 36 givenname: Paul surname: Ellis fullname: Ellis, Paul organization: Department of Medical Oncology, Guy's and St Thomas Foundation Trust, London, UK – sequence: 37 givenname: Sarah E orcidid: 0000-0003-4167-8910 surname: Pinder fullname: Pinder, Sarah E organization: Research Oncology, Division of Cancer Studies, King's College London, Guy's Hospital, London, UK – sequence: 38 givenname: Judith M surname: Bliss fullname: Bliss, Judith M organization: Clinical Trials and Statistics Unit, The Institute of Cancer Research, London, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29713086$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright Nature Publishing Group May 2018 |
| Copyright_xml | – notice: Copyright Nature Publishing Group May 2018 |
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| References | 30976601 - Stem Cell Investig. 2019 Feb 22;6:4. doi: 10.21037/sci.2019.02.01. 29736021 - Nat Med. 2018 May;24(5):535-537. doi: 10.1038/s41591-018-0033-7. |
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| Snippet | Germline mutations in BRCA1/2 predispose individuals to breast cancer (termed germline-mutated BRCA1/2 breast cancer, gBRCA-BC) by impairing homologous... |
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| SubjectTerms | Biomarkers BRCA1 protein BRCA1 Protein - genetics BRCA2 Protein - genetics Breast cancer Cancer Cancer therapies Carboplatin Carboplatin - therapeutic use Chemotherapy Deoxyribonucleic acid DNA Female Gene expression Genomic instability Homologous recombination Homologous Recombination - genetics Homology Humans Lesions Maintenance Methylation Mutation Mutation - genetics Platinum Poly(ADP-ribose) polymerase Progression-Free Survival Stability Subgroups Subpopulations Treatment Outcome Triple Negative Breast Neoplasms - drug therapy Triple Negative Breast Neoplasms - genetics Tumors |
| Title | Carboplatin in BRCA1/2-mutated and triple-negative breast cancer BRCAness subgroups: the TNT Trial |
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