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Pharmacological, Biochemical and Molecular Study of Adenosine Receptors

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Role of Xenobiotics".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 45997

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Prof. Dr. Katia Varani

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Department of Translational Medicine, University of Ferrara, Ferrara, Italy
Interests: purinergic receptors; cell signaling transduction; chronic inflammatory diseases; neurodegenerative disorders; drug discovery
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Dear Colleagues,

The endogenous purine nucleoside adenosine is involved in the regulation of different functions in every organ and tissue, through interaction with four G protein coupled receptors; A₁, A_2A, A_2B and A₃ adenosine receptors (ARs). Several physiopathological effects, primarily regulating central nervous and peripheral systems, are probably due to the wide distribution of ARs throughout the body. As a consequence, ARs and their modulation could potentially represent an attractive target for drug development in some of the most widespread disorders, such as inflammation, neurodegenerative disorders, ischemia, pain, cancer and fibrosis. In particular, adenosine signaling is involved in neurotransmission, secretion and neuromodulation, and in long term effects including proliferation, differentiation, migration, cell death and regeneration. The potential application of novel compounds, as both pharmacological tools and therapeutic agents, could be very interesting to better highlight the translation of basic adenosine research in the cure of human diseases.

We look forward to your contributions,

Prof. Dr. Katia Varani
Guest Editor

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Keywords

adenosine receptors
drug discovery
cell signalling transduction
neurodegenerative disorders
chronic inflammatory pathologies
heart diseases
cancer
pain
ischemia
clinical biophysics

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Published Papers (11 papers)

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Research

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13 pages, 2576 KiB

Open AccessArticle

Non-Invasive Assessment of Locally Overexpressed Human Adenosine 2A Receptors in the Heart of Transgenic Mice

by Daniel Gündel, Thu Hang Lai, Sladjana Dukic-Stefanovic, Rodrigo Teodoro, Winnie Deuther-Conrad, Magali Toussaint, Klaus Kopka, Rareş-Petru Moldovan, Peter Boknik, Britt Hofmann, Ulrich Gergs, Joachim Neumann and Peter Brust

Int. J. Mol. Sci. 2022, 23(3), 1025; https://doi.org/10.3390/ijms23031025 - 18 Jan 2022

Cited by 2 | Viewed by 2276

Abstract

A_2A adenosine receptors (A_2A-AR) have a cardio-protective function upon ischemia and reperfusion, but on the other hand, their stimulation could lead to arrhythmias. Our aim was to investigate the potential use of the PET radiotracer [¹⁸F]FLUDA to non-invasively determine the A_2A-AR availability for diagnosis of the A_2AR status. Therefore, we compared mice with cardiomyocyte-specific overexpression of the human A_2A-AR (A_2A-AR TG) with the respective wild type (WT). We determined: (1) the functional impact of the selective A_2AR ligand FLUDA on the contractile function of atrial mouse samples, (2) the binding parameters (B_{max and} K_D) of [¹⁸F]FLUDA on mouse and human atrial tissue samples by autoradiographic studies, and (3) investigated the in vivo uptake of the radiotracer by dynamic PET imaging in A_2A-AR TG and WT. After A_2A-AR stimulation by the A_2A-AR agonist CGS 21680 in isolated atrial preparations, antagonistic effects of FLUDA were found in A_2A-AR-TG animals but not in WT. Radiolabelled [¹⁸F]FLUDA exhibited a K_D of 5.9 ± 1.6 nM and a B_max of 455 ± 78 fmol/mg protein in cardiac samples of A_2A-AR TG, whereas in WT, as well as in human atrial preparations, only low specific binding was found. Dynamic PET studies revealed a significantly higher initial uptake of [¹⁸F]FLUDA into the myocardium of A_2A-AR TG compared to WT. The hA_2A-AR-specific binding of [¹⁸F]FLUDA in vivo was verified by pre-administration of the highly affine A_2AAR-specific antagonist istradefylline. Conclusion: [¹⁸F]FLUDA is a promising PET probe for the non-invasive assessment of the A_2A-AR as a marker for pathologies linked to an increased A_2A-AR density in the heart, as shown in patients with heart failure. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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14 pages, 1858 KiB

Open AccessArticle

Istradefylline Mitigates Age-Related Hearing Loss in C57BL/6J Mice

by Min Shin, Madhavi Pandya, Kristan Espinosa, Ravindra Telang, Jordi Boix, Peter R. Thorne and Srdjan M. Vlajkovic

Int. J. Mol. Sci. 2021, 22(15), 8000; https://doi.org/10.3390/ijms22158000 - 27 Jul 2021

Cited by 13 | Viewed by 3075

Abstract

Age-related hearing loss (ARHL) is the most common sensory disorder among older people, and yet, the treatment options are limited to medical devices such as hearing aids and cochlear implants. The high prevalence of ARHL mandates the development of treatment strategies that can prevent or rescue age-related cochlear degeneration. In this study, we investigated a novel pharmacological strategy based on inhibition of the adenosine A_2A receptor (A_2AR) in middle aged C57BL/6 mice prone to early onset ARHL. C57BL/6J mice were treated with weekly istradefylline (A_2AR antagonist; 1 mg/kg) injections from 6 to 12 months of age. Auditory function was assessed using auditory brainstem responses (ABR) to tone pips (4–32 kHz). ABR thresholds and suprathreshold responses (wave I amplitudes and latencies) were evaluated at 6, 9, and 12 months of age. Functional outcomes were correlated with quantitative histological assessments of sensory hair cells. Cognitive function was assessed using the Morris water maze and the novel object recognition test, and the zero maze test was used to assess anxiety-like behaviour. Weekly injections of istradefylline attenuated ABR threshold shifts by approximately 20 dB at mid to high frequencies (16–32 kHz) but did not improve ABR suprathreshold responses. Istradefylline treatment improved hair cell survival in a turn-dependent manner, whilst the cognitive function was unaffected by istradefylline treatment. This study presents the first evidence for the rescue potential of istradefylline in ARHL and highlights the role of A_2AR in development of age-related cochlear degeneration. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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12 pages, 2971 KiB

Open AccessArticle

Adenosine A_2A Receptors Are Upregulated in Peripheral Blood Mononuclear Cells from Atrial Fibrillation Patients

by Héctor Godoy-Marín, Romain Duroux, Kenneth A. Jacobson, Concepció Soler, Hildegard Colino-Lage, Veronica Jiménez-Sábado, José Montiel, Leif Hove-Madsen and Francisco Ciruela

Int. J. Mol. Sci. 2021, 22(7), 3467; https://doi.org/10.3390/ijms22073467 - 27 Mar 2021

Cited by 12 | Viewed by 2715

Abstract

Atrial fibrillation (AF) is the most common form of cardiac arrhythmia seen in clinical practice. While some clinical parameters may predict the transition from paroxysmal to persistent AF, the molecular mechanisms behind the AF perpetuation are poorly understood. Thus, oxidative stress, calcium overload and inflammation, among others, are believed to be involved in AF-induced atrial remodelling. Interestingly, adenosine and its receptors have also been related to AF development and perpetuation. Here, we investigated the expression of adenosine A2A receptor (A2AR) both in right atrium biopsies and peripheral blood mononuclear cells (PBMCs) from non-dilated sinus rhythm (ndSR), dilated sinus rhythm (dSR) and AF patients. In addition, plasma adenosine content and adenosine deaminase (ADA) activity in these subjects were also determined. Our results revealed increased A2AR expression in the right atrium from AF patients, as previously described. Interestingly, increased levels of adenosine content and reduced ADA activity in plasma from AF patients were detected. An increase was observed when A2AR expression was assessed in PBMCs from AF subjects. Importantly, a positive correlation (p = 0.001) between A2AR expression in the right atrium and PBMCs was observed. Overall, these results highlight the importance of the A2AR in AF and suggest that the evaluation of this receptor in PBMCs may be potentially be useful in monitoring disease severity and the efficacy of pharmacological treatments in AF patients. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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25 pages, 6929 KiB

Open AccessArticle

Development of ¹⁸F-Labeled Radiotracers for PET Imaging of the Adenosine A_2A Receptor: Synthesis, Radiolabeling and Preliminary Biological Evaluation

by Thu Hang Lai, Susann Schröder, Magali Toussaint, Sladjana Dukić-Stefanović, Mathias Kranz, Friedrich-Alexander Ludwig, Steffen Fischer, Jörg Steinbach, Winnie Deuther-Conrad, Peter Brust and Rareş-Petru Moldovan

Int. J. Mol. Sci. 2021, 22(5), 2285; https://doi.org/10.3390/ijms22052285 - 25 Feb 2021

Cited by 5 | Viewed by 3549

Abstract

The adenosine A_2A receptor (A_2AR) represents a potential therapeutic target for neurodegenerative diseases. Aiming at the development of a positron emission tomography (PET) radiotracer to monitor changes of receptor density and/or occupancy during the A_2AR-tailored therapy, we designed a library of fluorinated analogs based on a recently published lead compound (PPY). Among those, the highly affine 4-fluorobenzyl derivate (PPY1; K_i(hA_2AR) = 5.3 nM) and the 2-fluorobenzyl derivate (PPY2; K_i(hA_2AR) = 2.1 nM) were chosen for ¹⁸F-labeling via an alcohol-enhanced copper-mediated procedure starting from the corresponding boronic acid pinacol ester precursors. Investigations of the metabolic stability of [¹⁸F]PPY1 and [18F]PPY2 in CD-1 mice by radio-HPLC analysis revealed parent fractions of more than 76% of total activity in the brain. Specific binding of [¹⁸F]PPY2 on mice brain slices was demonstrated by in vitro autoradiography. In vivo PET/magnetic resonance imaging (MRI) studies in CD-1 mice revealed a reasonable high initial brain uptake for both radiotracers, followed by a fast clearance. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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18 pages, 4036 KiB

Open AccessArticle

Synthesis and Biological Evaluation of a Novel ¹⁸F-Labeled Radiotracer for PET Imaging of the Adenosine A_2A Receptor

by Thu Hang Lai, Magali Toussaint, Rodrigo Teodoro, Sladjana Dukić-Stefanović, Mathias Kranz, Winnie Deuther-Conrad, Rareş-Petru Moldovan and Peter Brust

Int. J. Mol. Sci. 2021, 22(3), 1182; https://doi.org/10.3390/ijms22031182 - 25 Jan 2021

Cited by 10 | Viewed by 3404

Abstract

The adenosine A_2A receptor (A_2AR) has emerged as a potential non-dopaminergic target for the treatment of Parkinson’s disease and, thus, the non-invasive imaging with positron emission tomography (PET) is of utmost importance to monitor the receptor expression and occupancy during an A_2AR-tailored therapy. Aiming at the development of a PET radiotracer, we herein report the design of a series of novel fluorinated analogs (TOZ1-TOZ7) based on the structure of the A_2AR antagonist tozadenant, and the preclinical evaluation of [¹⁸F]TOZ1. Autoradiography proved A_2AR-specific in vitro binding of [¹⁸F]TOZ1 to striatum of mouse and pig brain. Investigations of the metabolic stability in mice revealed parent fractions of more than 76% and 92% of total activity in plasma and brain samples, respectively. Dynamic PET/magnetic resonance imaging (MRI) studies in mice revealed a brain uptake but no A_2AR-specific in vivo binding. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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15 pages, 2170 KiB

Open AccessArticle

Guanosine-Mediated Anxiolytic-Like Effect: Interplay with Adenosine A₁ and A_2A Receptors

by Monica Frinchi, Vincenzo Verdi, Fulvio Plescia, Francisco Ciruela, Maria Grillo, Roberta Garozzo, Daniele F. Condorelli, Patrizia Di Iorio, Francesco Caciagli, Renata Ciccarelli, Natale Belluardo, Valentina Di Liberto and Giuseppa Mudò

Int. J. Mol. Sci. 2020, 21(23), 9281; https://doi.org/10.3390/ijms21239281 - 5 Dec 2020

Cited by 15 | Viewed by 2598

Abstract

Acute or chronic administration of guanosine (GUO) induces anxiolytic-like effects, for which the adenosine (ADO) system involvement has been postulated yet without a direct experimental evidence. Thus, we aimed to investigate whether adenosine receptors (ARs) are involved in the GUO-mediated anxiolytic-like effect, evaluated by three anxiety-related paradigms in rats. First, we confirmed that acute treatment with GUO exerts an anxiolytic-like effect. Subsequently, we investigated the effects of pretreatment with ADO or A₁R (CPA, CCPA) or A_2AR (CGS21680) agonists 10 min prior to GUO on a GUO-induced anxiolytic-like effect. All the combined treatments blocked the GUO anxiolytic-like effect, whereas when administered alone, each compound was ineffective as compared to the control group. Interestingly, the pretreatment with nonselective antagonist caffeine or selective A₁R (DPCPX) or A_2AR (ZM241385) antagonists did not modify the GUO-induced anxiolytic-like effect. Finally, binding assay performed in hippocampal membranes showed that [³H]GUO binding became saturable at 100–300 nM, suggesting the existence of a putative GUO binding site. In competition experiments, ADO showed a potency order similar to GUO in displacing [³H]GUO binding, whereas AR selective agonists, CPA and CGS21680, partially displaced [³H]GUO binding, but the sum of the two effects was able to displace [³H]GUO binding to the same extent of ADO alone. Overall, our results strengthen previous data supporting GUO-mediated anxiolytic-like effects, add new evidence that these effects are blocked by A₁R and A_2AR agonists and pave, although they do not elucidate the mechanism of GUO and ADO receptor interaction, for a better characterization of GUO binding sites in ARs. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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Review

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18 pages, 613 KiB

Open AccessReview

Adenosine Receptors in Neuropsychiatric Disorders: Fine Regulators of Neurotransmission and Potential Therapeutic Targets

by Silvia Pasquini, Chiara Contri, Stefania Merighi, Stefania Gessi, Pier Andrea Borea, Katia Varani and Fabrizio Vincenzi

Int. J. Mol. Sci. 2022, 23(3), 1219; https://doi.org/10.3390/ijms23031219 - 22 Jan 2022

Cited by 30 | Viewed by 5689

Abstract

Adenosine exerts an important role in the modulation of central nervous system (CNS) activity. Through the interaction with four G-protein coupled receptor (GPCR) subtypes, adenosine subtly regulates neurotransmission, interfering with the dopaminergic, glutamatergic, noradrenergic, serotoninergic, and endocannabinoid systems. The inhibitory and facilitating actions of adenosine on neurotransmission are mainly mediated by A₁ and A_2A adenosine receptors (ARs), respectively. Given their role in the CNS, ARs are promising therapeutic targets for neuropsychiatric disorders where altered neurotransmission represents the most likely etiological hypothesis. Activating or blocking ARs with specific pharmacological agents could therefore restore the balance of altered neurotransmitter systems, providing the rationale for the potential treatment of these highly debilitating conditions. In this review, we summarize and discuss the most relevant studies concerning AR modulation in psychotic and mood disorders such as schizophrenia, bipolar disorders, depression, and anxiety, as well as neurodevelopment disorders such as autism spectrum disorder (ASD), fragile X syndrome (FXS), attention-deficit hyperactivity disorder (ADHD), and neuropsychiatric aspects of neurodegenerative disorders. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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31 pages, 2248 KiB

Open AccessReview

Current Adenosinergic Therapies: What Do Cancer Cells Stand to Gain and Lose?

by Jana Kotulová, Marián Hajdúch and Petr Džubák

Int. J. Mol. Sci. 2021, 22(22), 12569; https://doi.org/10.3390/ijms222212569 - 22 Nov 2021

Cited by 12 | Viewed by 3539

Abstract

A key objective in immuno-oncology is to reactivate the dormant immune system and increase tumour immunogenicity. Adenosine is an omnipresent purine that is formed in response to stress stimuli in order to restore physiological balance, mainly via anti-inflammatory, tissue-protective, and anti-nociceptive mechanisms. Adenosine overproduction occurs in all stages of tumorigenesis, from the initial inflammation/local tissue damage to the precancerous niche and the developed tumour, making the adenosinergic pathway an attractive but challenging therapeutic target. Many current efforts in immuno-oncology are focused on restoring immunosurveillance, largely by blocking adenosine-producing enzymes in the tumour microenvironment (TME) and adenosine receptors on immune cells either alone or combined with chemotherapy and/or immunotherapy. However, the effects of adenosinergic immunotherapy are not restricted to immune cells; other cells in the TME including cancer and stromal cells are also affected. Here we summarise recent advancements in the understanding of the tumour adenosinergic system and highlight the impact of current and prospective immunomodulatory therapies on other cell types within the TME, focusing on adenosine receptors in tumour cells. In addition, we evaluate the structure- and context-related limitations of targeting this pathway and highlight avenues that could possibly be exploited in future adenosinergic therapies. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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13 pages, 1457 KiB

Open AccessReview

Uncovering the Mechanisms of Adenosine Receptor-Mediated Pain Control: Focus on the A₃ Receptor Subtype

by Elisabetta Coppi, Federica Cherchi, Elena Lucarini, Carla Ghelardini, Felicita Pedata, Kenneth A. Jacobson, Lorenzo Di Cesare Mannelli, Anna Maria Pugliese and Daniela Salvemini

Int. J. Mol. Sci. 2021, 22(15), 7952; https://doi.org/10.3390/ijms22157952 - 26 Jul 2021

Cited by 22 | Viewed by 5934

Abstract

Agonists of the G_i protein-coupled A₃ adenosine receptor (A₃AR) have shown important pain-relieving properties in preclinical settings of several pain models. Active as a monotherapy against chronic pain, A₃AR agonists can also be used in combination with classic opioid analgesics. Their safe pharmacological profile, as shown by clinical trials for other pathologies, i.e., rheumatoid arthritis, psoriasis and fatty liver diseases, confers a realistic translational potential, thus encouraging research studies on the molecular mechanisms underpinning their antinociceptive actions. A number of pathways, involving central and peripheral mechanisms, have been proposed. Recent evidence showed that the prototypical A₃AR agonist Cl-IB-MECA and the new, highly selective, A₃AR agonist MRS5980 inhibit neuronal (N-type) voltage-dependent Ca²⁺ currents in dorsal root ganglia, a known pain-related mechanism. Other proposed pathways involve reduced cytokine production, immune cell-mediated responses, as well as reduced microglia and astrocyte activation in the spinal cord. The aim of this review is to summarize up-to-date information on A₃AR in the context of pain, including cellular and molecular mechanisms underlying this effect. Based on their safety profile shown in clinical trials for other pathologies, A₃AR agonists are proposed as novel, promising non-narcotic agents for pain control. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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24 pages, 1109 KiB

Open AccessReview

Adenosine and Inflammation: Here, There and Everywhere

by Silvia Pasquini, Chiara Contri, Pier Andrea Borea, Fabrizio Vincenzi and Katia Varani

Int. J. Mol. Sci. 2021, 22(14), 7685; https://doi.org/10.3390/ijms22147685 - 19 Jul 2021

Cited by 89 | Viewed by 9278

Abstract

Adenosine is a ubiquitous endogenous modulator with the main function of maintaining cellular and tissue homeostasis in pathological and stress conditions. It exerts its effect through the interaction with four G protein-coupled receptor (GPCR) subtypes referred as A₁, A_2A, A_2B, and A₃ adenosine receptors (ARs), each of which has a unique pharmacological profile and tissue distribution. Adenosine is a potent modulator of inflammation, and for this reason the adenosinergic system represents an excellent pharmacological target for the myriad of diseases in which inflammation represents a cause, a pathogenetic mechanism, a consequence, a manifestation, or a protective factor. The omnipresence of ARs in every cell of the immune system as well as in almost all cells in the body represents both an opportunity and an obstacle to the clinical use of AR ligands. This review offers an overview of the cardinal role of adenosine in the modulation of inflammation, showing how the stimulation or blocking of its receptors or agents capable of regulating its extracellular concentration can represent promising therapeutic strategies for the treatment of chronic inflammatory pathologies, neurodegenerative diseases, and cancer. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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13 pages, 11738 KiB

Open AccessReview

Adenosine Receptor Reserve and Long-Term Potentiation: Unconventional Adaptive Mechanisms in Cardiovascular Diseases?

by Régis Guieu, Michele Brignole, Jean Claude Deharo, Pierre Deharo, Giovanna Mottola, Antonella Groppelli, Franck Paganelli and Jean Ruf

Int. J. Mol. Sci. 2021, 22(14), 7584; https://doi.org/10.3390/ijms22147584 - 15 Jul 2021

Cited by 5 | Viewed by 2807

Abstract

While the concept of a receptor reserve (spare receptors) is old, their presence on human cells as an adaptive mechanism in cardiovascular disease is a new suggestion. The presence of spare receptors is suspected when the activation of a weak fraction of receptors leads to maximal biological effects, in other words, when the half-maximal effective concentration (EC₅₀) for a biological effect (cAMP production, for example) is lower than the affinity (K_D) of the ligand for a receptor. Adenosine is an ATP derivative that strongly impacts the cardiovascular system via its four membrane receptors, named A₁R, A_2AR, A_2BR, and A₃R, with the A₁R being more particularly involved in heart rhythm, while the A_2AR controls vasodilation. After a general description of the tools necessary to explore the presence of spare receptors, this review focuses on the consequences of the presence of spare adenosine receptors in cardiovascular physiopathology. Finally, the role of the adenosinergic system in the long-term potentiation and its possible consequences on the physiopathology are also mentioned. Full article

(This article belongs to the Special Issue Pharmacological, Biochemical and Molecular Study of Adenosine Receptors)

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