Safety and activity of the first-in-class locked nucleic acid (LNA) miR-221 selective inhibitor in refractory advanced cancer patients: a first-in-human, phase 1, open-label, dose-escalation study.

Advanced Cancer Clinical trial First-in-class First-in-human LNA-i-miR-221 Non-coding RNA therapeutics Phase 1 RNA therapeutics Refractory miR-221 miRNA miRNA therapeutics microRNA

Journal

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

Informations de publication

Date de publication:
26 06 2023
Historique:
received: 25 12 2022
accepted: 16 06 2023
medline: 28 6 2023
pubmed: 27 6 2023
entrez: 26 6 2023
Statut: epublish

Résumé

We developed a 13-mer locked nucleic acid (LNA) inhibitor of miR-221 (LNA-i-miR-221) with a full phosphorothioate (PS)-modified backbone. This agent downregulated miR-221, demonstrated anti-tumor activity against human xenografts in mice, and favorable toxicokinetics in rats and monkeys. Allometric interspecies scaling allowed us to define the first-in-class LNA-i-miR-221 safe starting dose for the clinical translation. In this first-in-human, open-label, dose-escalation phase 1 trial, we enrolled progressive cancer patients (aged ≥ 18 years) with ECOG 0-2 into 5 cohorts. The treatment cycle was based on a 30-min IV infusion of LNA-i-miR-221 on 4 consecutive days. Three patients within the first cohort were treated with 2 cycles (8 infusions), while 14 patients were treated with a single course (4 infusions); all patients were evaluated for phase 1 primary endpoint. The study was approved by the Ethics Committee and Regulatory Authorities (EudraCT 2017-002615-33). Seventeen patients received the investigational treatment, and 16 were evaluable for response. LNA-i-miR-221 was well tolerated, with no grade 3-4 toxicity, and the MTD was not reached. We recorded stable disease (SD) in 8 (50.0%) patients and partial response (PR) in 1 (6.3%) colorectal cancer case (total SD + PR: 56.3%). Pharmacokinetics indicated non-linear drug concentration increase across the dose range. Pharmacodynamics demonstrated concentration-dependent downregulation of miR-221 and upregulation of its CDKN1B/p27 and PTEN canonical targets. Five mg/kg was defined as the recommended phase II dose. The excellent safety profile, the promising bio-modulator, and the anti-tumor activity offer the rationale for further clinical investigation of LNA-i-miR-221 (ClinTrials.Gov: NCT04811898).

Sections du résumé

BACKGROUND
We developed a 13-mer locked nucleic acid (LNA) inhibitor of miR-221 (LNA-i-miR-221) with a full phosphorothioate (PS)-modified backbone. This agent downregulated miR-221, demonstrated anti-tumor activity against human xenografts in mice, and favorable toxicokinetics in rats and monkeys. Allometric interspecies scaling allowed us to define the first-in-class LNA-i-miR-221 safe starting dose for the clinical translation.
METHODS
In this first-in-human, open-label, dose-escalation phase 1 trial, we enrolled progressive cancer patients (aged ≥ 18 years) with ECOG 0-2 into 5 cohorts. The treatment cycle was based on a 30-min IV infusion of LNA-i-miR-221 on 4 consecutive days. Three patients within the first cohort were treated with 2 cycles (8 infusions), while 14 patients were treated with a single course (4 infusions); all patients were evaluated for phase 1 primary endpoint. The study was approved by the Ethics Committee and Regulatory Authorities (EudraCT 2017-002615-33).
RESULTS
Seventeen patients received the investigational treatment, and 16 were evaluable for response. LNA-i-miR-221 was well tolerated, with no grade 3-4 toxicity, and the MTD was not reached. We recorded stable disease (SD) in 8 (50.0%) patients and partial response (PR) in 1 (6.3%) colorectal cancer case (total SD + PR: 56.3%). Pharmacokinetics indicated non-linear drug concentration increase across the dose range. Pharmacodynamics demonstrated concentration-dependent downregulation of miR-221 and upregulation of its CDKN1B/p27 and PTEN canonical targets. Five mg/kg was defined as the recommended phase II dose.
CONCLUSIONS
The excellent safety profile, the promising bio-modulator, and the anti-tumor activity offer the rationale for further clinical investigation of LNA-i-miR-221 (ClinTrials.Gov: NCT04811898).

Identifiants

pubmed: 37365583
doi: 10.1186/s13045-023-01468-8
pii: 10.1186/s13045-023-01468-8
pmc: PMC10294514
doi:

Substances chimiques

locked nucleic acid 0
MicroRNAs 0
MIRN221 microRNA, human 0
MIRN221 microRNA, rat 0
Oligonucleotides 0

Banques de données

ClinicalTrials.gov
['NCT04811898']
EudraCT
['2017-002615-33']

Types de publication

Clinical Trial, Phase I Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

68

Informations de copyright

© 2023. The Author(s).

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Auteurs

Pierfrancesco Tassone (P)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy. tassone@unicz.it.
Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy. tassone@unicz.it.

Maria Teresa Di Martino (MT)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.
Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Mariamena Arbitrio (M)

Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Institute of Research and Biomedical Innovation (IRIB), Italian National Council (CNR), Catanzaro, Italy.

Lucia Fiorillo (L)

Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Nicoletta Staropoli (N)

Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Domenico Ciliberto (D)

Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Alessia Cordua (A)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.

Francesca Scionti (F)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.

Bernardo Bertucci (B)

Radiology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Angela Salvino (A)

Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Mariangela Lopreiato (M)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.

Fredrik Thunarf (F)

Biometrics Department, LINK Medical Research AB, Uppsala, Sweden.

Onofrio Cuomo (O)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.

Maria Cristina Zito (MC)

Pharmacy Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Maria Rosanna De Fina (MR)

Pharmacy Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Amelia Brescia (A)

Pharmacy Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Simona Gualtieri (S)

Phase 1 and Translational Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Caterina Riillo (C)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.

Francesco Manti (F)

Radiology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Daniele Caracciolo (D)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.

Vito Barbieri (V)

Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Eugenio Donato Di Paola (ED)

Pharmacology Unit, Department of Science of Health, Magna Graecia University, Catanzaro, Italy.

Adele Emanuela Di Francesco (AE)

Pharmacy Unit, AOU Renato Dulbecco, Catanzaro, Italy.

Pierosandro Tagliaferri (P)

Department of Experimental and Clinical Medicine (DMSC), Magna Graecia University, Catanzaro, Italy.
Medical Oncology Unit, AOU Renato Dulbecco, Catanzaro, Italy.

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