Cited by 243Multiple Myeloma Research and TreatmentsChronic Lymphocytic Leukemia ResearchProstate Cancer Treatment and Research

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Identification of resistance pathways and therapeutic targets in relapsed multiple myeloma patients through single-cell sequencing

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Cohen, Yael C., Zada, Mor, Wang, Shuang-Yin, Bornstein, Chamutal, David, Eyal, Moshe, Adi, Li, Baoguo, Shlomi-Loubaton, Shir, Gatt, Moshe E., Gur, Chamutal, Lavi, Noa, Ganzel, Chezi, Luttwak, Efrat, Chubar, Evgeni, Rouvio, Ory, Vaxman, Iuliana, Pasvolsky, Oren, Ballan, Mouna, Tadmor, Tamar, Nemets, Anatoly, Jarchowcky-Dolberg, Osnat, Shvetz, Olga, Laiba, Meirav, Shpilberg, Ofer, Dally, Najib, Avivi, Irit, Weiner, Assaf, Amit, Ido·2021·Nature Medicine

DOI 10.1038/s41591-021-01232-wPMC PMC7612793

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Abstract

Multiple myeloma (MM) is a neoplastic plasma-cell disorder characterized by clonal proliferation of malignant plasma cells. Despite extensive research, disease heterogeneity within and between treatment-resistant patients is poorly characterized. In the present study, we conduct a prospective, multicenter, single-arm clinical trial (NCT04065789), combined with longitudinal single-cell RNA-sequencing (scRNA-seq) to study the molecular dynamics of MM resistance mechanisms. Newly diagnosed MM patients (41), who either failed to respond or experienced early relapse after a bortezomib-containing induction regimen, were enrolled to evaluate the safety and efficacy of a daratumumab, carfilzomib, lenalidomide and dexamethasone combination. The primary clinical endpoint was safety and tolerability. Secondary endpoints included overall response rate, progression-free survival and overall survival. Treatment was safe and well tolerated; deep and durable responses were achieved. In prespecified exploratory analyses, comparison of 41 primary refractory and early relapsed patients, with 11 healthy subjects and 15 newly diagnosed MM patients, revealed new MM molecular pathways of resistance, including hypoxia tolerance, protein folding and mitochondria respiration, which generalized to larger clinical cohorts (CoMMpass). We found peptidylprolyl isomerase A (PPIA), a central enzyme in the protein-folding response pathway, as a potential new target for resistant MM. CRISPR-Cas9 deletion of PPIA or inhibition of PPIA with a small molecule inhibitor (ciclosporin) significantly sensitizes MM tumor cells to proteasome inhibitors. Together, our study defines a roadmap for integrating scRNA-seq in clinical trials, identifies a signature of highly resistant MM patients and discovers PPIA as a potent therapeutic target for these tumors.

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RETRACTED ARTICLE: A novel necroptosis signature for predicting survival in lung adenocarcinoma
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Additional file 2 of Dynamic single-cell RNA-seq analysis reveals distinct tumor program associated with microenvironmental remodeling and drug sensitivity in multiple myeloma
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Additional file 11 of Malignant clonal evolution drives multiple myeloma cellular ecological diversity and microenvironment reprogramming
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Authors: Cohen, Y. C., Zada, M., Wang, S.-Y., Bornstein, C., David, E., Moshe, A., Li, B., Shlomi-Loubaton, S., Gatt, M. E., Gur, C., Lavi, N., Ganzel, C., Luttwak, E., Chubar, E., Rouvio, O., Vaxman, I., Pasvolsky, O., Ballan, M., Tadmor, T., Nemets, A., Jarchowcky-Dolberg, O., Shvetz, O., Laiba, M., Shpilberg, O., Dally, N., Avivi, I., Weiner, A., & Amit, I.
Affiliations: Tel Aviv University (IL)
Weizmann Institute of Science (IL)
Hebrew University of Jerusalem (IL)
Rambam Health Care Campus (IL)
Shaare Zedek Medical Center (IL)
Emek Medical Center (IL)
Soroka Medical Center (IL)
Carmel Medical Center (IL)
Bnai Zion Medical Center (IL)
Barzilai Medical Center (IL)
Meir Medical Center (IL)
Kaplan Medical Center (IL)
Assuta Medical Center (IL)
Rebecca Sieff Hospital (IL)
Corresponding author: Weiner, Assaf
Amit, Ido
ORCID: Cohen, Yael C.
Zada, Mor
Wang, Shuang-Yin
Bornstein, Chamutal
David, Eyal
Li, Baoguo
Gatt, Moshe E.
Gur, Chamutal
Lavi, Noa
Ganzel, Chezi
Luttwak, Efrat
Rouvio, Ory
Vaxman, Iuliana
Pasvolsky, Oren
Tadmor, Tamar
Shpilberg, Ofer
Avivi, Irit
Weiner, Assaf
Amit, Ido
Venue: Nature Medicine
Publisher: Springer Science and Business Media LLC
Published: 2021-02-22
Volume: 27
Issue: 3
Pages: 491-503
ISSN: 1078-8956 (ISSN-L)
1546-170X
DOI: 10.1038/s41591-021-01232-w
PMC: PMC7612793
OpenAlex: W3133251387
Cited by: 235
References: 55
Citations by year: 2026: 30 · 2025: 33 · 2024: 51 · 2023: 58 · 2022: 48 · 2021: 15
FWCI: 29.33
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Medicine (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Amgen
European Molecular Biology Organization (ALTF 263‐2018)
Topics: Health Sciences › Medicine › Hematology › Multiple Myeloma Research and Treatments
Health Sciences › Medicine › Hematology › Chronic Lymphocytic Leukemia Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Prostate Cancer Treatment and Research
Keywords: relapsed multiple myeloma, treatment resistance, resistance mechanisms, single-cell RNA sequencing, daratumumab, carfilzomib, lenalidomide, dexamethasone, bortezomib, proteasome inhibitors, PPIA, hypoxia tolerance, mitochondrial respiration, therapeutic target, CRISPR/Cas9 gene deletion, cyclosporine
MeSH terms: Lenalidomide, Adult, Aged, Aged, 80 and over, Antibodies, Monoclonal, Antineoplastic Combined Chemotherapy Protocols, Dexamethasone, Female, Humans, Male, Middle Aged, Multiple Myeloma, Neoplasm Recurrence, Local, Oligopeptides, Case-Control Studies, Treatment Outcome, Drug Resistance, Neoplasm, Single-Cell Analysis

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Identification of resistance pathways and therapeutic targets in relapsed multiple myeloma patients through single-cell sequencing

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