Citation: Nguyen, H.O.; Tiberio, L.;
Facchinetti, F.; Ripari, G.; Violi, V.;
Villetti, G.; Salvi, V.; Bosisio, D.
Modulation of Human Dendritic Cell
Functions by Phosphodiesterase-4
Inhibitors: Potential Relevance for
the Treatment of Respiratory
Diseases. Pharmaceutics 2023, 15, 2254.
https://doi.org/10.3390/
pharmaceutics15092254
Academic Editors: Gaia Codolo,
Barbara Frossi and Teresa Zelante
Received: 27 July 2023
Revised: 23 August 2023
Accepted: 29 August 2023
Published: 31 August 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
pharmaceutics
Review
Modulation of Human Dendritic Cell Functions by
Phosphodiesterase-4 Inhibitors: Potential Relevance for the
Treatment of Respiratory Diseases
Hoang Oanh Nguyen
1
, Laura Tiberio
2
, Fabrizio Facchinetti
3
, Giulia Ripari
2
, Valentina Violi
2
, Gino Villetti
3
,
Valentina Salvi
2,
* and Daniela Bosisio
2,
*
1
ImmunoConcEpT, CNRS UMR 5164, University of Bordeaux, 33000 Bordeaux, France;
hnguyen@immuconcept.org
2
Department of Molecular and Translational Medicine, University of Brescia, 25123 Brescia, Italy;
laura.tiberio@unibs.it (L.T.); g.ripari@unibs.it (G.R.); v.violi@studenti.unibs.it (V.V.)
3
Department of Experimental Pharmacology and Translational Science, Corporate Pre-Clinical R&D,
Chiesi Farmaceutici S.p.A., 43122 Parma, Italy; f.facchinetti@chiesi.com (F.F.); g.villetti@chiesi.com (G.V.)
* Correspondence: valentina.salvi@unibs.it (V.S.); daniela.bosisio@unibs.it (D.B.)
Abstract: Inhibitors of phosphodiesterase-4 (PDE4) are small-molecule drugs that, by increasing
the intracellular levels of cAMP in immune cells, elicit a broad spectrum of anti-inflammatory
effects. As such, PDE4 inhibitors are actively studied as therapeutic options in a variety of human
diseases characterized by an underlying inflammatory pathogenesis. Dendritic cells (DCs) are
checkpoints of the inflammatory and immune responses, being responsible for both activation
and dampening depending on their activation status. This review shows evidence that PDE4
inhibitors modulate inflammatory DC activation by decreasing the secretion of inflammatory and
Th1/Th17-polarizing cytokines, although preserving the expression of costimulatory molecules and
the CD4+ T cell-activating potential. In addition, DCs activated in the presence of PDE4 inhibitors
induce a preferential Th2 skewing of effector T cells, retain the secretion of Th2-attracting chemokines
and increase the production of T cell regulatory mediators, such as IDO1, TSP-1, VEGF-A and
Amphiregulin. Finally, PDE4 inhibitors selectively induce the expression of the surface molecule
CD141/Thrombomodulin/BDCA-3. The result of such fine-tuning is immunomodulatory DCs
that are distinct from those induced by classical anti-inflammatory drugs, such as corticosteroids.
The possible implications for the treatment of respiratory disorders (such as COPD, asthma and
COVID-19) by PDE4 inhibitors will be discussed.
Keywords: cDC1; cDC2; pDC; monocyte-derived DC; tolerogenic DCs; CD80; CD86; IL-12;
TNFα; Tanimilast
1. Introduction
cAMP is a key modulator of inflammation whose intracellular levels are regulated
through hydrolysis by various phosphodiesterases (PDEs) [1]. PDE4, in particular, is a fam-
ily of four genes (PDE4A, PDE4B, PDE4C and PDE4D) encoding cAMP-specific enzymes
sharing a highly conserved catalytic domain and prominently expressed in immune cells.
PDE4 inhibitors increase cAMP intracellular levels by inhibiting cAMP hydrolysis,
thus eliciting a broad spectrum of anti-inflammatory effects in virtually all cells of the
immune system [2]. Because of this, the inhibition of PDE4 enzymes has been clinically
investigated as a therapeutic strategy in a variety of pathological settings, including respira-
tory, dermatological and immune diseases, as well as cognitive and affective disorders [3,4].
Dendritic cells (DCs) are a specialized population of antigen-presenting cells, serving
as sentinels of innate immunity and key initiators of adaptive and anti-viral immune
responses. Deregulated DC functions are one major pathogenetic determinant of virtually
Pharmaceutics 2023, 15, 2254. https://doi.org/10.3390/pharmaceutics15092254 https://www.mdpi.com/journal/pharmaceutics