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Facci, Laura (2013) Role of microglia and astrocytes in inflammatory processes involving neurological diseases, chronic pain, and psychiatric disorders, with emphasis on the purinergic P2X7 receptor. [Tesi di dottorato]

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Abstract (inglese)

Under pathological conditions microglia (resident central nervous system (CNS) immune cells) become activated, and produce reactive oxygen and nitrogen species and pro-inflammatory cytokines: molecules that can contribute to disorders including stroke, traumatic brain injury, progressive neurodegenerative disorders such as Alzheimer’s disease, Parkinson’s disease, amyotrophic lateral sclerosis, multiple sclerosis, and several retinal diseases. Given that ATP is frequently released from CNS neurons during tissue damage and inflammation, its actions on microglia-mediated toxicity are especially pertinent. For example, the ATP-gated P2X7 purinergic receptor (P2X7R) cation channel is up-regulated around amyloid beta-peptide plaques in transgenic mouse models of Alzheimer's disease and co-localizes to microglia and astrocytes. Upregulation of P2X7R on microglia occurs also following spinal cord injury and after brain ischemia. ATP, via activation of P2X7R, is one of the most powerful stimuli for secretion of the key pro-inflammatory cytokine interleukin-1β (IL-1β) in its mature form. This project investigates the pharmacological and biochemical behaviors of P2X7R on microglia and astrocytes cultured from rat cerebral cortex, spinal cord and cerebellum, and the relationship between these two glial cell types.
ATP is an efficient stimulus for IL-1β secretion only after the cells have undergone a short 'priming' with endotoxin (lipopolysaccharide (LPS)). Indeed LPS, but not ATP caused release of IL-1β from cortical microglia. However, it is known that the greater part of the IL-1β thus released is the precursor (biologically inactive) form. Purified (>99%) cortical microglia and enriched (>95%) astrocytes were primed for 2 hours with LPS, followed by addition of ATP for 1 hour. Culture medium was then collected and the content of IL-1β quantified by ELISA. The effects of LPS and ATP were concentration-dependent; although LPS alone (but not ATP) modestly stimulated IL-1β release, levels of cytokine release were much higher from primed cells incubated with ATP. The ATP-dependent component was fully blocked by selective P2X7R antagonists, and followed their known rank order of target potency. The P2X7R priming response was also seen with spinal cord and cerebellar microglia, a finding not described in the literature until now.
To rule out a contribution by the minor population of microglia in our astrocyte cultures, the latter were treated with the lysosomotropic agent L-leucyl-L-leucine methyl ester (L-LME) which selectively eliminates cells with cytotoxic potential (e.g. macrophages, microglia). Immunocytochemical and molecular biological evaluation showed L-LME-treated cortical and spinal cord astrocytes to be fully depleted of microglia. These purified astrocytes failed to respond to LPS, and did not show the ATP priming behavior. Responsiveness was recovered upon addition of microglia to the L-LME-treated astrocytes and, moreover, a far more robust release of IL-1β occurred than that achieved with the same numbers of microglia alone. This astrocyte-microglia interaction was also observed for LPS-stimulated release of nitric oxide and IL-6, and was not mediated by astrocyte-derived soluble factors.
Lastly, the LPS/ATP priming behavior was studied by examining the ability of other agents, linked to neuropathology, to replace either LPS or ATP. Neither ethanol (ethanol intoxication; in place of LPS) nor amyloid beta-peptides (Alzheimer disease; in place of ATP) were able to provoke IL-1β release from microglia. However, both zymosan and poly(I:C), agonists of Toll-like receptors -2 and -3, respectively, were capable of substituting LPS (a Toll-like receptor 4 agonist) in the P2X7R priming response. Release of IL-1β in all these cases was antagonized by inhibitors of p38 mitogen-activated protein kinase (a stress response kinase).
TLRs contribute to CNS immunocompetent cell activation and the resulting pro-inflammatory cascade producing pathological pain. TLR4 recognizes not only LPS, but also ligands called damage associated molecular patterns, released by the injured tissue The involvement of extracellular TLR4 and TLR2, as well as TLR3 in preclinical pain models has been demonstrated. The findings described here further support the notion of astrocyte/microglia interaction, which may improve our understanding in how these cells respond to CNS injury or inflammation, in particular where TLRs are involved

Abstract (italiano)

αLe ricerche svolte hanno riguardato lo studio dei comportamenti della microglia e degli astrociti derivati da corteccia, midollo spinale e cervelletto di ratto in presenza di uno stimolo infiammatorio, in particolare quello associato alla famiglia dei recettori toll-like (TLR) e il recettore purinergico P2X7 (P2X7R). E’ ormai riconosciuto il coinvolgimento della glia nello sviluppo delle malattie neurodegenerative e nel dolore neuropatico, sia nel midollo spinale che nelle aree corticali. In particolare, il rilascio di ATP da cellule danneggiate o morenti (cellule gliali, neuroni e cellule endoteliali) può agire come un segnale di 'pericolo' attraverso un sottotipo di recettori purinergici come il P2X7. I recettori P2X7 possono influenzare la morte cellulare attraverso la capacità di regolare il processo e il rilascio di interluchina-1β (IL-1β), un mediatore chiave nella neurodegenerazione, infiammazione e dolore cronico. L’IL-1β e' rilasciata dai macrofagi e dalla microglia esposta a endotossina batterica (lipopolisaccaride, LPS). Scopo della ricerca svolta è stato quindi la caratterizzazione di queste popolazioni di cellule gliali con metodi immunologici, molecolari, biochimici e farmacologici in presenza o assenza di stimolo infiammatorio (LPS) e l'identificazione del meccanismo del 'priming' (le cellule di microglia trattate per breve tempo con LPS diventano più sensibili all’azione dell’ATP) in termine di rilascio di IL-1β. Fino ad ora la maggior parte degli studi presenti in letteratura hanno esaminato il ruolo della microglia ma non degli astrociti nella neuroinfiammazione.
Il lavoro svolto nel primo anno è consistito principalmente nella caratterizzazione del comportamento della microglia e degli astrociti ottenuti da corteccia, midollo spinale e cervelletto, in termini di risposta ad ATP, in presenza o assenza di uno stimolo infiammatorio come LPS. Per questo scopo è stato utilizzato un modello in vitro di microglia preparata da corteccia cerebrale di ratto di 1-2 giorni d’eta' o da midollo spinale. Dopo 1-2 settimane la popolazione di cellule di microglia vengono separate dagli astrociti e raccolte. Queste colture secondarie di microglia purificate (>99%) e astrociti arricchiti (>95%) (come determinato mediante colorazione immunocitochimica e l'espressione genica (RT-PCR), sono state trattate e il terreno di coltura è stato utilizzato per l’analisi (ELISA) delle citochine (IL-1β, TNF-α, IL-6), rilasciate. Inoltre, nel terreno di coltura si è provveduto a valutare la quantità di ossido d’azoto (NO). La microglia e gli astrociti di controllo e trattati con ATP (fino a 5 mM) non producono una quantità misurabile di IL-1β. Il LPS, alla dose di 100 ng/ml, produce invece un considerevole aumento di NO e IL-1β in funzione del tempo in tutte e due i tipi cellulari.
Successivamente abbiamo analizzato la risposta della microglia e degli astrociti esposti per tempi brevi prima a LPS e poi ad ATP per stimolare il rilascio di una quantità maggiore di IL-1β matura ('priming'). Sia la microglia che gli astrociti, stimolati con LPS e ATP, rilasciano IL-1β . La parte della risposta data dall’ATP e non dall’LPS viene bloccata dagli antagonisti del P2X7R. L’ SB-202190, un inibitore selettivo della miogeno-activated-protein (MAP) chinasi p38, riduce il rilascio di IL-1β indotto da LPS nel 'priming', ma lo aumenta (da 6 a 10 volte) se incubato con LPS in presenza di siero per 24 ore. L’ SB-202190 inoltre, inibisce il rilascio di NO in cellule trattate con LPS per 24 ore. L’SP600125, un inibitore del c-Jun N-terminale chinasi (JNK), aumenta il rilascio di IL-1β indotto da LPS (24 ore) in microglia. In contrasto, nel priming l’SP600125 riduce il rilascio di IL-1β. I due meccanismi di rilascio di IL-1β sono quindi presumibilmente diversi, ma legati alla cascata del segnale della MAP chinasi. La risposta 'priming' è stata anche dimostrata in microglia ottenuta da cervelletto di ratto. Questi resultati rappresentano la prima descrizione della risposta 'priming' nelle cellule gliali del midollo spinale e del cervelletto collegato al P2X7R.
Il lavoro svolto nel secondo anno è consistito principalmente nel caratterizzare dal punto di vista molecolare e farmacologico il rapporto tra microglia e astrociti in queste culture. Siccome le colture arricchite in astrociti contengono una piccola percentuale di microglia (<5%), abbiamo voluto verificare se il rilascio di citochine in seguito a uno stimolo infiammatorio dipende da una azione diretta sugli astrociti o una azione indiretta tramite la presenza della microglia. Per eliminare la microglia residua le colture arricchite in astrociti (corticali o spinali), sono state trattate per un ora con l’agente lisosomotropico L-leucine methyl ester (L-LME) (50 mM), che è tossico per i macrofagi. Dopo un ora di incubazione la soluzione di L-LME è stata sostituita da terreno di coltura per 24 ore, al termine delle quali sono stati iniziati i trattamenti con lo stimolo infiammatorio. Da ora in poi definiamo tali colture come ‘astrociti purificati’. L’RNA messaggero (mRNA) per l’ Iba1, proteina espressa solo nella microglia, non è stato rilevato tramite la tecnica RT-PCR negli astrociti purificati, mentre il segnale è presente nelle cellule prima del trattamento con L-LME. Il trattamento con L-LME elimina anche la risposta LPS/ATP (priming) negli astrociti corticali e spinali purificati. L’aggiunta di una quantità nota di microglia agli astrociti purificati, ripristina la risposta degli astrociti al priming. Tuttavia, lo stesso numero di microglia, da sola, senza la presenza degli astrociti, è insufficiente a produrre il segnale. Lo studio dell’interazione tra microglia e astrociti purificati, è stato esteso anche alla produzione dell’NO e mRNA per iNOS (NO sintasi inducibile). E’stato dimostrato che l’aumento della produzione di NO in seguito a stimolazione con LPS, è stata abolita negli astrociti purificati. L’aggiunta di una quantità nota di microglia alle cellule di astrociti purificati, ripristina la risposta degli astrociti al LPS e di conseguenza un aumento di iNOS e NO. Inoltre, il terreno di coltura dagli astrociti trattati con LPS non è grado a stimolare il rilascio di NO da microglia. Un comportamento simile è stato osservato per IL-6 mRNA e proteine. Questi dati mostrano chiaramente che la microglia, ma non gli astrociti rispondono al LPS, e che il comportamento degli astrociti dipende dalla presenza di microglia.
L'obiettivo ultimo era quello di esaminare, oltre al LPS o ATP, la capacità di altri agenti potenzialmente patologici, ad esempio il peptide beta-amiloide (Aβ), l’etanolo, e agonisti del recettore TLR2 e TLR3 nella risposta 'priming' della microglia. Aβ, il principale costituente delle placche che si trovano nel cervello dei pazienti affetti dalla malattia Alzheimer (AD), può attivare la microglia. E’ stato pubblicato che la proteina Aβ (25-35) aumenta la secrezione di IL-1β nella microglia esposta a LPS. Siccome nel cervello dei pazienti affetti da AD si accumula la forma (1-42) della Aβ e non la (25-35), tutte e due le forme sono state testate per vedere se sono in grado di sostituire l’ATP nella microglia pretrattata con LPS. Nessuno dei due peptidi però si sono dimostrati efficaci.
L’ intossicazione da etanolo cronica e acuta promuove i processi infiammatori nel cervello e nelle cellule gliali agendo sul TLR4. L’etanolo, dunque, potrebbe attivare la microglia e sostituire LPS nella risposta 'priming' per l’ATP. Per dimostrare questa teoria, la microglia corticale e da midollo spinale è stata incubata con 100 mM etanolo o 1 microg/ml LPS per due ore, seguita da incubazione con 5 mM ATP per un' ora. Successivamente è stato misurato il rilascio di IL-β nel mezzo di coltura che ha dimostrato l’effetto dell’ATP, ma non dell’etanolo, sulle cellule pretrattate con LPS.
La microglia oltre al TLR4 esprime anche TLR2 e TLR3 funzionali che, quando attivati, partecipano al dolore neuropatico causato da lesioni nervose. Finora non sono stati fatti studi che dimostrano il coinvolgimento degli agonisti TLR2 e TLR3 sulla microglia ‘primed’ e il rilascio di citochina IL-1β. L’agonista TLR2 (Zymosan) e TLR3 (Poly(I:C)), sono stati dunque testati nella microglia al posto del LPS e si sono dimostrati capaci di attivare la microglia, corticale, spinale e cerebellare. In presenza di ATP sono stati in grado, come il LPS, di essere efficaci come ‘priming’ in termini di rilascio di IL-1β. Un inibitore selettivo della MAP chinasi p38 (SB-202190) riduce il rilascio di IL-1β indotto da Zymosan o Poly(I:C) nel 'priming', ma lo aumenta (circa 4 volte) se incubato per 24 ore, in presenza di siero.
Questo studio costituisce un contributo originale alla ricerca nel campo della neuroinfiammazione a livello cellulare e in particolare il rapporto tra astrociti e microglia. Dato che gli astrociti sono molto più numerosi della microglia nel sistema nervoso centrale, questi dati suggeriscono che una simile interazione tra astrociti e microglia in vivo può essere un elemento importante per l'evoluzione di una patologia infiammatoria. Inoltre, questo lavoro dimostra per la prima volta che l'attivazione del P2X7R si verifica in microglia da midollo spinale e da cervelletto, che può verificarsi con agonisti TL2 e TLR3 oltre che con TLR4. Questo amplia notevolmente le possibilità di partecipazione del recettore P2X7 nella neuroinfiammazione

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Tipo di EPrint:Tesi di dottorato
Relatore:Giusti, Pietro
Dottorato (corsi e scuole):Ciclo 25 > Scuole 25 > SCIENZE FARMACOLOGICHE > FARMACOLOGIA MOLECOLARE E CELLULARE
Data di deposito della tesi:24 Gennaio 2013
Anno di Pubblicazione:24 Gennaio 2013
Parole chiave (italiano / inglese):Microglia, Astrociti, Corteccia, Midollo spinale, Cervelletto, Recettore purinergicoP2X7, Adenosina trifosfato, Lipopolisaccaride, Recettori Toll-like, Interleuchina-1β Ossido di azoto, Neuroinfiammazione Microglia, Astrocytes, Cortex, Spinal cord, Cerebellum, Purinergic receptor P2X7, Adenosine triphosphate, Lipopolysaccharide, Toll-like receptors, Interleukin-1β, Nitric oxide, Neuroinflammation
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/14 Farmacologia
Struttura di riferimento:Dipartimenti > Dipartimento di Scienze del Farmaco
Codice ID:5462
Depositato il:15 Ott 2013 09:07
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