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Magrini, Elena (2009) Role of neurotransmitters in immune cell function:
serotonin-mediated modulation of CD4+ T-cell chemotaxis.
[Tesi di dottorato]

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Abstract (inglese)

It is becoming increasingly evident that there exist an intimate bidirectional communication between the immune and the nervous system. Growing evidence supports the idea that neurotransmitters are involved in the transmission of information between not only neuronal cells but also immune cells, and that they may play a key role in connecting the two systems. Indeed, both primary and secondary lymphoid organs are innervated with nerve fibres, as is skin.
Among the various neurotransmitters, serotonin (5-HT) is likely involved in several important biological processes outside the central nervous system (CNS). Indeed, this neurotransmitter is produced for the most part (about 90%) by the enterochromaffin cells (ECs) of the gut and it is transported throughout the body by platelets that, under proper conditions, are able to release it. Further, immune cells express serotonin receptors. Thus, serotonin may encounter and eventually affect immune cell activities in more sites of the body and in several contexts of health and disease.
Receptors for 5-HT have been divided into seven major classes, 5-HT1-5-HT7. Previous studies have suggested a role for 5-HT1, 5-HT2 and 5-HT7 receptors in T cell activation. Here, we propose to analyze whether 5-HT, through its action on a particular serotonin receptor, the 5-HT3, may modulates T cell migration. The 5-HT3 receptor is a pentameric channel and belongs to the family of ligand gated ion channels (LGICs), whereas all other serotonin receptors are members of the large family of G protein coupled receptors (GPCRs). To date, five different 5-HT3 receptor subunits have been identified (5-HT3A-HT3E) which can compose the channel.
We observed that both resting and activated T cells express the 5-HT3A subunits, even though the expression is up-regulated upon activation. We could not detect other receptor subunits, indicating that in T cells 5-HT3 is a homopentameric channel. Interestingly, among the different subtypes, expression of the 5-HT3A subunit is essential and sufficient for the formation of a functional receptor.
Then, we confirmed the 5-HT3A expression, and its up-regulation upon activation, at protein level. Moreover, with patch clamp experiments, we demonstrated that the homomeric 5-HT3 channel expressed in human CD4+ T cells is functional. We also found that both resting and activated human CD4+ T cells are able to produce and release 5-HT.
Next, we investigated on the role of the serotonergic system in T lymphocyte migration. We found that the presence of exogenous 5-HT or specific 5-HT3 agonists significantly reduced the CXCL12-induced chemotaxis. Moreover, 5-HT3 antagonists enhanced T cells migration in the absence of exogenous serotonin. Further, the effects on migration were paralleled by those on CXCL12-induced calcium influx, indicating that 5-HT3 receptors control early events of chemokine receptor signaling.
Clearly, the main question is in which physiological context serotonin may influence T cell migration. The tryptophan hydroxilase (TPH) enzyme activity represents the limiting step of 5-HT synthesis. Hypoxia decreases the activity of TPH and thus reduces 5-HT synthesis in rat brain and, in general, a decrease in oxigen concentration is paralleled by a reduction in 5-HT synthesis rate. We demonstrated that even human CD4+ T cells, under hypoxic conditions, reduce the production of 5-HT, both in presence and absence of CXCL12.
During their migration into tissues, T cells are exposed to hypoxic gradients. Indeed, while in the blood the oxigen tension is 5-13 kPa, in tissues it drops to 0.5-2.5 kPa. In addition, low oxigen tension is a key feature of inflammation. Considering that human CD4+ T cells produce and release 5-HT constitutively and that autocrine 5-HT, by the stimulation of 5-HT3 receptors, inhibits T cell migration, we envisaged that hypoxia inhibits T cell migration through a serotonin-dependent mechanism. Our data support this hypothesis and suggest that serotonin may exert a rheostatic control of T cell migration in hypoxia.

Abstract (italiano)

Il fatto che esista una comunicazione bidirezionale tra il sistema immunitario e quello nervoso sta diventando sempre più evidente. Molti sono i dati a favore dell’idea che i neurotrasmettitori non sono solo coinvolti nello scambio di informazioni tra cellule neuronali, ma anche tra quelle del sistema immunitario. Non solo, si pensa che questi possano giocare un ruolo chiave anche nella comunicazione tra i due sistemi. Non a caso, sia gli organi linfoidi primari che secondari sono innervati da fibre nervose, così come lo è la pelle.
Tra i diversi tipi di neurotrasmettitori, la serotonina (5-HT) sembra essere coinvolta in diversi importanti processi biologici che avvengono anche al di fuori del sistema nervoso centrale (CNS). Infatti, questo neurotrasmettitore è prodotto principalmente (circa per il 90%) dalle cellule enterocromaffiniche (ECs) dell’intestino ed è trasportato nell’organismo dalle piastrine che, in appropriate condizioni, lo rilasciano. Inoltre, le cellule del sistema immunitario esprimono recettori per la serotonina. Pertanto, la serotonina può entrare in contatto ed eventualmente modificare le attività del sistema immunitario in più siti dell’organismo e in diversi contesti fisiologici e patologici.
I recettori della serotonina possono essere divisi in sette maggiori classi, 5-HT1-5-HT7.
Studi precedenti hanno mostrato che alcuni di essi, in particolare modo i recettori 5-HT1, 5-HT2 e 5-HT7, hanno un ruolo nell’attivazione delle cellule T. Nei nostri studi ci siamo concentrati su un eventuale ruolo della serotonina nella migrazione dei linfociti T, attraverso l’interazione con un suo particolare recettore, il 5-HT3. Il recettore 5-HT3 è un canale pentamerico che appartiene alla famiglia dei canali ionici attivati da ligando (LGICs), mentre tutti gli altri recettori serotonergici appartengono alla famiglia dei recettori accoppiati a proteine G (GPCRs). Ad oggi, sono state identificate cinque differenti subunità che possono costituire il recettore 5-HT3.
Dapprima, abbiamo dunque dimostrato che le cellule T CD4+ umane, sia resting che attivate, esprimono solo la subunità 5-HT3A e che la sua espressione aumenta dopo attivazione. Le altre subunità non sono espresse, dunque il recettore HT3A nelle cellule T è un canale omopentamerico. È interessante considerare il fatto che, tra le diverse subunità esistenti, l’espressione della subunità 5-HT3A è condizione essenziale e sufficiente per la formazione del canale.
In seguito, abbiamo confermato, a livello proteico, l’espressione della suddetta subunità e la sua aumentata espressione dopo attivazione. Inoltre, abbiamo dimostrato che il recettore è funzionale con esperimenti di patch clamp. Abbiamo poi dimostrato che linfociti T, sia resting che attivati, sono capaci di produrre e rilasciare serotonina.
In seguito, siamo passati allo studio del possibile ruolo del sistema serotonergico nella chemotassi dei lifociti T. Abbiamo osservato che la presenza di serotonina esogena, o di agonisti specifici del canale 5-HT3, riducono significativamente la chemotassi in risposta a CXCL12. Inoltre, l’inibizione del canale mediante antagonisti specifici induce un aumento della migrazione, in assenza di serotonina esogena. Gli effetti osservati in migrazione sono risultati confrontabili con quelli ottenuti in esperimenti di flussi di calcio in risposta a CXCL12, indicando che il recettore 5-HT3 controlla i primi eventi della trasduzione del segnale indotta da chemochina.
Ci siamo poi chiesti in quale contesto la serotonina potesse influenzare la migrazione dei linfociti. L’attività dell’enzima triptofano idrossilasi (TPH) rappresenta il passaggio limitante nella sintesi della serotonina. È stato dimostrato, in cervelli di ratto, che l’ipossia riduce l’attività di questo enzima e, in generale, una diminuzione nella concentrazione di ossigeno causa una riduzione nella velocità di sintesi della serotonina da parte di questo enzima. Abbiamo dimostrato che anche in cellule T CD4+ umane, in condizioni ipossiche, la produzione di serotonina è ridotta, sia in presenza che in assenza di CXCL12.
Nella migrazione verso i tessuti, le cellule T sono esposte ad un gradiente d’ossigeno. Infatti, mentre nel sangue la tensione d’ossigeno è di 5-13 kPa, nei tessuti questa si riduce a 0.5-2.5 kPa. Non solo, una ridotta tensione d’ossigeno è una delle principali caratteristiche delle condizioni infiammatorie. Considerando che le cellule T umane producono e rilasciano serotonina costitutivamente e che la stimolazione autocrina del canale 5-HT3 inibisce la migrazione delle cellule T, abbiamo ipotizzato che l’ipossia potesse ridurre la migrazione cellulare, attraverso una modulazione della produzione di serotonina endogena. I nostri dati hanno confermato tale ipotesi, suggerendo che la serotonina in grado di effettuare un controllo reostatico della migrazione delle cellule T in ipossia.

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Tipo di EPrint:Tesi di dottorato
Relatore:Viola, Antonella
Dottorato (corsi e scuole):Ciclo 21 > Scuole per il 21simo ciclo > BIOSCIENZE > BIOLOGIA CELLULARE
Data di deposito della tesi:28 Gennaio 2009
Anno di Pubblicazione:2009
Parole chiave (italiano / inglese):T cell chemotaxis serotonin
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/11 Biologia molecolare
Struttura di riferimento:Dipartimenti > pre 2012 - Dipartimento di Scienze Biomediche Sperimentali
Codice ID:1536
Depositato il:28 Gen 2009
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