MiR-146b-5p regulates IL-23 receptor complex expression in chronic lymphocytic leukemia cells.


Journal

Blood advances
ISSN: 2473-9537
Titre abrégé: Blood Adv
Pays: United States
ID NLM: 101698425

Informations de publication

Date de publication:
25 10 2022
Historique:
accepted: 30 06 2022
received: 09 07 2021
pubmed: 13 7 2022
medline: 18 10 2022
entrez: 12 7 2022
Statut: ppublish

Résumé

Chronic lymphocytic leukemia (CLL) cells express the interleukin-23 receptor (IL-23R) chain, but the expression of the complementary IL-12Rβ1 chain requires cell stimulation via surface CD40 molecules (and not via the B-cell receptor [BCR]). This stimulation induces the expression of a heterodimeric functional IL-23R complex and the secretion of IL-23, initiating an autocrine loop that drives leukemic cell expansion. Based on the observation in 224 untreated Binet stage A patients that the cases with the lowest miR-146b-5p concentrations had the shortest time to first treatment (TTFT), we hypothesized that miR-146b-5p could negatively regulate IL-12Rβ1 side chain expression and clonal expansion. Indeed, miR-146b-5p significantly bound to the 3'-UTR region of the IL-12Rβ1 mRNA in an in vitro luciferase assay. Downregulation of miR-146b-5p with specific miRNA inhibitors in vitro led to the upregulation of the IL-12Rβ1 side chain and expression of a functional IL-23R complex similar to that observed after stimulation of the CLL cell through the surface CD40 molecules. Expression of miR-146b-5p with miRNA mimics in vitro inhibited the expression of the IL-23R complex after stimulation with CD40L. Administration of a miR-146b-5p mimic to NSG mice, successfully engrafted with CLL cells, caused tumor shrinkage, with a reduction of leukemic nodules and of IL-12Rβ1-positive CLL cells in the spleen. Our findings indicate that IL-12Rβ1 expression, a crucial checkpoint for the functioning of the IL-23 and IL-23R complex loop, is under the control of miR-146b-5p, which may represent a potential target for therapy since it contributes to the CLL pathogenesis. This trial is registered at www.clinicaltrials.gov as NCT00917540.

Identifiants

pubmed: 35819446
pii: 485867
doi: 10.1182/bloodadvances.2021005726
pmc: PMC9647700
doi:

Substances chimiques

Interleukin-23 0
MicroRNAs 0
RNA, Messenger 0
Receptors, Antigen, B-Cell 0
CD40 Ligand 147205-72-9

Banques de données

ClinicalTrials.gov
['NCT00917540']

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

5593-5612

Informations de copyright

© 2022 by The American Society of Hematology. Licensed under Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0), permitting only noncommercial, nonderivative use with attribution. All other rights reserved.

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Auteurs

Serena Matis (S)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Anna Grazia Recchia (A)

Hematology Unit AO of Cosenza, Cosenza, Italy.
Biothecnology Research Unit, AO, Cosenza, Italy.

Monica Colombo (M)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Martina Cardillo (M)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
Department of Experimental Medicine, University of Genoa, Genoa, Italy.

Marina Fabbi (M)

Biotherapy Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Katia Todoerti (K)

Hematology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.

Sabrina Bossio (S)

Hematology Unit AO of Cosenza, Cosenza, Italy.
Biothecnology Research Unit, AO, Cosenza, Italy.

Sonia Fabris (S)

Hematology Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.

Valeria Cancila (V)

Tumor Immunology Unit, Department of Health Sciences, University of Palermo School of Medicine, Palermo, Italy.

Rosanna Massara (R)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Daniele Reverberi (D)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Laura Emionite (L)

Animal Facility, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Michele Cilli (M)

Animal Facility, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Giannamaria Cerruti (G)

Molecular Diagnostic Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Sandra Salvi (S)

Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Paola Bet (P)

Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Simona Pigozzi (S)

Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
Department of Surgical and Diagnostic Sciences (DISC), University of Genoa, Genoa, Italy.

Roberto Fiocca (R)

Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
Department of Surgical and Diagnostic Sciences (DISC), University of Genoa, Genoa, Italy.

Adalberto Ibatici (A)

Hematology Unit and Transplant Center, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Emanuele Angelucci (E)

Hematology Unit and Transplant Center, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Massimo Gentile (M)

Hematology Unit AO of Cosenza, Cosenza, Italy.
Biothecnology Research Unit, AO, Cosenza, Italy.

Paola Monti (P)

Mutagenesis and Cancer Prevention Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Paola Menichini (P)

Mutagenesis and Cancer Prevention Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Gilberto Fronza (G)

Mutagenesis and Cancer Prevention Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Federica Torricelli (F)

Laboratory of Translational Research, Azienda USL IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Alessia Ciarrocchi (A)

Laboratory of Translational Research, Azienda USL IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Antonino Neri (A)

Scientific Directorate, Azienda USL IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Franco Fais (F)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.
Department of Experimental Medicine, University of Genoa, Genoa, Italy.

Claudio Tripodo (C)

Tumor Immunology Unit, Department of Health Sciences, University of Palermo School of Medicine, Palermo, Italy.

Fortunato Morabito (F)

Biothecnology Research Unit, AO, Cosenza, Italy.
Hematology and Bone Marrow Transplant Unit, Hemato-Oncology Department, Augusta Victoria Hospital, East Jerusalem, Israel.

Manlio Ferrarini (M)

Department of Experimental Medicine, University of Genoa, Genoa, Italy.

Giovanna Cutrona (G)

Molecular Pathology Unit, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

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