Triple MAPK inhibition salvaged a relapsed post-BCMA CAR-T cell therapy multiple myeloma patient with a BRAF V600E subclonal mutation.


Journal

Journal of hematology & oncology
ISSN: 1756-8722
Titre abrégé: J Hematol Oncol
Pays: England
ID NLM: 101468937

Informations de publication

Date de publication:
17 08 2022
Historique:
received: 14 06 2022
accepted: 05 08 2022
entrez: 17 8 2022
pubmed: 18 8 2022
medline: 20 8 2022
Statut: epublish

Résumé

Multiple Myeloma (MM) is a progressive plasma cell neoplasm characterized by heterogeneous clonal expansion. Despite promising response rates achieved with anti-BCMA CAR-T cell therapy, patients may still relapse and there are currently no clear therapeutic options in post-CAR-T settings. In this report, we present a case of a post-BCMA CAR-T relapsed/refractory (RR) MM patient with skin extramedullary disease (EMD) in which a novel MAPK inhibition combinatorial strategy was implemented based on next-generation sequencing and in vitro experiments. A 61-year-old male with penta-refractory MM penta- (IgA lambda), ISS stage 3 with hyperdiploidy, gain of 1q21 and del13 was treated with anti-BCMA CAR-T cell therapy, achieving a best response of VGPR. He progressed after 6 months and was salvaged for a short period with autologous stem cell transplantation. Eventually, he progressed with extramedullary disease manifested as subcutaneous nodules. Based on whole-exome sequencing, we identified a BRAF (V600E) dominant subclone in both bone marrow and cutaneous plasmacytoma. Following in vitro experiments, and according to our previous studies, we implemented a triple MAPK inhibition strategy under which the patient achieved a very good partial response for 110 days, which allowed to bridge him to subsequent clinical trials and eventually achieve a stringent complete response (sCR). Here, we show the applicability, effectiveness, and tolerability the triple MAPK inhibition strategy in the context of post-BCMA CAR-T failure in specific subset of patients. The triple therapy could bridge our hospice bound RRMM patient with BRAF (V600E) to further therapeutic options where sCR was achieved. We will further evaluate triple MAPK inhibition in patients with BRAF V600E in a precision medicine clinical trial launching soon.

Sections du résumé

BACKGROUND
Multiple Myeloma (MM) is a progressive plasma cell neoplasm characterized by heterogeneous clonal expansion. Despite promising response rates achieved with anti-BCMA CAR-T cell therapy, patients may still relapse and there are currently no clear therapeutic options in post-CAR-T settings. In this report, we present a case of a post-BCMA CAR-T relapsed/refractory (RR) MM patient with skin extramedullary disease (EMD) in which a novel MAPK inhibition combinatorial strategy was implemented based on next-generation sequencing and in vitro experiments.
CASE PRESENTATION
A 61-year-old male with penta-refractory MM penta- (IgA lambda), ISS stage 3 with hyperdiploidy, gain of 1q21 and del13 was treated with anti-BCMA CAR-T cell therapy, achieving a best response of VGPR. He progressed after 6 months and was salvaged for a short period with autologous stem cell transplantation. Eventually, he progressed with extramedullary disease manifested as subcutaneous nodules. Based on whole-exome sequencing, we identified a BRAF (V600E) dominant subclone in both bone marrow and cutaneous plasmacytoma. Following in vitro experiments, and according to our previous studies, we implemented a triple MAPK inhibition strategy under which the patient achieved a very good partial response for 110 days, which allowed to bridge him to subsequent clinical trials and eventually achieve a stringent complete response (sCR).
CONCLUSION
Here, we show the applicability, effectiveness, and tolerability the triple MAPK inhibition strategy in the context of post-BCMA CAR-T failure in specific subset of patients. The triple therapy could bridge our hospice bound RRMM patient with BRAF (V600E) to further therapeutic options where sCR was achieved. We will further evaluate triple MAPK inhibition in patients with BRAF V600E in a precision medicine clinical trial launching soon.

Identifiants

pubmed: 35978321
doi: 10.1186/s13045-022-01330-3
pii: 10.1186/s13045-022-01330-3
pmc: PMC9382834
doi:

Substances chimiques

B-Cell Maturation Antigen 0
Receptors, Chimeric Antigen 0
BRAF protein, human EC 2.7.11.1
Proto-Oncogene Proteins B-raf EC 2.7.11.1

Types de publication

Case Reports Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

109

Subventions

Organisme : NCI NIH HHS
ID : R01 CA240362
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA252222
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA238229
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA244899
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA204314
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2022. The Author(s).

Références

Xu J, et al. Molecular signaling in multiple myeloma: association of RAS/RAF mutations and MEK/ERK pathway activation. Oncogenesis. 2017;6(5): e337.
doi: 10.1038/oncsis.2017.36 pubmed: 28504689 pmcid: 5523069
Subbiah V, Baik C, Kirkwood JM. Clinical development of BRAF plus MEK inhibitor combinations. Trends Cancer. 2020;6(9):797–810.
doi: 10.1016/j.trecan.2020.05.009 pubmed: 32540454
Lito P, et al. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell. 2012;22(5):668–82.
doi: 10.1016/j.ccr.2012.10.009 pubmed: 23153539 pmcid: 3713778
Corcoran RB, et al. EGFR-mediated reactivation of MAPK signaling contributes to insensitivity of BRAF-mutant colorectal cancers to RAF inhibition with vemurafenib. Cancer Discov. 2012;2(3):227–35.
doi: 10.1158/2159-8290.CD-11-0341 pubmed: 22448344 pmcid: 3308191
Adamopoulos C, et al. Exploiting allosteric properties of RAF and MEK inhibitors to target therapy-resistant tumors driven by oncogenic BRAF signaling. Cancer Discov. 2021;11(7):1716–35.
doi: 10.1158/2159-8290.CD-20-1351 pubmed: 33568355 pmcid: 8295204
Stockslager MA, et al. Functional drug susceptibility testing using single-cell mass predicts treatment outcome in patient-derived cancer neurosphere models. Cell Rep. 2021;37(1): 109788.
doi: 10.1016/j.celrep.2021.109788 pubmed: 34610309
Chandarlapaty S. Negative feedback and adaptive resistance to the targeted therapy of cancer. Cancer Discov. 2012;2(4):311–9.
doi: 10.1158/2159-8290.CD-12-0018 pubmed: 22576208 pmcid: 3351275
Samatar AA, Poulikakos PI. Targeting RAS-ERK signalling in cancer: promises and challenges. Nat Rev Drug Discov. 2014;13(12):928–42.
doi: 10.1038/nrd4281 pubmed: 25435214
Karoulia Z, Gavathiotis E, Poulikakos PI. New perspectives for targeting RAF kinase in human cancer. Nat Rev Cancer. 2017;17(11):676–91.
doi: 10.1038/nrc.2017.79 pubmed: 28984291 pmcid: 6000833
Mincu RI, et al. Cardiovascular Adverse events associated with BRAF and MEK inhibitors: a systematic review and meta-analysis. JAMA Netw Open. 2019;2(8): e198890.
doi: 10.1001/jamanetworkopen.2019.8890 pubmed: 31397860 pmcid: 6692687
Banks M, et al. Cardiovascular effects of the MEK inhibitor, trametinib: a case report, literature review, and consideration of mechanism. Cardiovasc Toxicol. 2017;17(4):487–93.
doi: 10.1007/s12012-017-9425-z pubmed: 28861837 pmcid: 6319910
Okabe S, et al. Copanlisib, a novel phosphoinositide 3-kinase inhibitor, combined with carfilzomib inhibits multiple myeloma cell proliferation. Ann Hematol. 2019;98(3):723–33.
doi: 10.1007/s00277-018-3547-7 pubmed: 30430191
Larson SM, et al. Inhibition of PI3K Alpha and PI3K delta with copanlisib shows preclinical activity as a single agent and in combination in multiple myeloma. Blood. 2017;130(Supplement 1):3084–3084.
Chen S, et al. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–90.
doi: 10.1093/bioinformatics/bty560 pubmed: 30423086 pmcid: 6129281
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60.
doi: 10.1093/bioinformatics/btp324 pubmed: 19451168 pmcid: 2705234
McKenna A, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–303.
doi: 10.1101/gr.107524.110 pubmed: 20644199 pmcid: 2928508
Shen R, Seshan VE. FACETS: allele-specific copy number and clonal heterogeneity analysis tool for high-throughput DNA sequencing. Nucleic Acids Res. 2016;44(16): e131.
doi: 10.1093/nar/gkw520 pubmed: 27270079 pmcid: 5027494
Khanna, A., et al., Bam-readcount -- rapid generation of basepair-resolution sequence metrics. ArXiv, 2021.
Narzisi G, et al. Genome-wide somatic variant calling using localized colored de Bruijn graphs. Commun Biol. 2018;1:20.
doi: 10.1038/s42003-018-0023-9 pubmed: 30271907 pmcid: 6123722
Kim S, et al. Strelka2: fast and accurate calling of germline and somatic variants. Nat Methods. 2018;15(8):591–4.
doi: 10.1038/s41592-018-0051-x pubmed: 30013048
Gillis S, Roth A. PyClone-VI: scalable inference of clonal population structures using whole genome data. BMC Bioinform. 2020;21(1):571.
doi: 10.1186/s12859-020-03919-2
Caravagna G, et al. Detecting repeated cancer evolution from multi-region tumor sequencing data. Nat Methods. 2018;15(9):707–14.
doi: 10.1038/s41592-018-0108-x pubmed: 30171232 pmcid: 6380470
Dobin A, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21.
doi: 10.1093/bioinformatics/bts635 pubmed: 23104886
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30.
doi: 10.1093/bioinformatics/btt656 pubmed: 24227677
Leek JT, et al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics. 2012;28(6):882–3.
doi: 10.1093/bioinformatics/bts034 pubmed: 22257669 pmcid: 3307112
Hanzelmann S, Castelo R, Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinform. 2013;14:7.
doi: 10.1186/1471-2105-14-7
Ramakrishnan V, Kumar S. PI3K/AKT/mTOR pathway in multiple myeloma: from basic biology to clinical promise. Leuk Lymphoma. 2018;59(11):2524–34.
doi: 10.1080/10428194.2017.1421760 pubmed: 29322846
Pratilas CA, et al. (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc Natl Acad Sci U S A. 2009;106(11):4519–24.
doi: 10.1073/pnas.0900780106 pubmed: 19251651 pmcid: 2649208

Auteurs

Muhammad Elnaggar (M)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Sarita Agte (S)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Paula Restrepo (P)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Meghana Ram (M)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

David Melnekoff (D)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Christos Adamopoulos (C)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Mark M Stevens (MM)

, Travera, Medford, MA, USA.

Katerina Kappes (K)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Violetta Leshchenko (V)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Daniel Verina (D)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Sundar Jagannath (S)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Poulikos I Poulikakos (PI)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Samir Parekh (S)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Alessandro Laganà (A)

Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA. alessandro.lagana@mssm.edu.
Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA. alessandro.lagana@mssm.edu.
Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA. alessandro.lagana@mssm.edu.

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