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Ceriani, Federico (2014) Quantitative estimate of biochemical and electrical intercellular coupling in the developing cochlea of wild type and DFNB1 mouse models. [Tesi di dottorato]

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Abstract (inglese)

Hearing loss is the most common form of sensory impairment, with approximately one infant/1000 born with profound congenital deafness. Nonsyndromic hearing loss and deafness (DFNB1) is an inherited condition with a mild to severe deafness phenotype caused by mutations in GJB2 (which encodes the protein connexin26) and GJB6 (which encodes connexin30). Gap junction channels formed primarily by these two connexin protein subunits couple non-sensory cells (supporting and epithelial cells) of the mammalian cochlea, forming vast functional syncytia. Previous work has shown that electrical and metabolic coupling mediated by gap junction channels is fundamental for the development and maintenance of hearing. However, precise estimates of the degree of coupling and its alterations under DFNB1 conditions are lacking, notwithstanding the vast body of studies conducted in recombinant expression systems.
In this thesis work, we combined large scale optical recordings, single cell electrophysiology and computer simulations to elucidate the mechanisms that underlie intercellular communication in cochlear supporting cells from juvenile mice (first postnatal week). First, we developed a novel technique based on voltage imaging to map the extent and the degree of electrical coupling in non-sensory cell networks of the developing mouse cochlea. We also quantified precisely the reduction of electrical coupling in cochlear organotypic cultures from transgenic mice with hearing defects due to absence or mutation of connexin30 compared to wild type animals. By comparing our experimental results with numerical simulations, we estimated that cochlear supporting cells in the mouse are already well coupled in the first postnatal week by as many as ∼ 1500 channels per cell pair. In age-matched cultures from connexin30(T5M/T5M) and connexin30(−/−) mice, junctional conductance was reduced respectively by 14% and 91%, and these data account for the increased hearing thresholds exhibited by these animals in the adult stage.
Besides electrical coupling, inner ear gap junction channels and hemichannels have been shown to participate in ATP- and IP3 - dependent intercellular Ca2+ signaling, and alterations of these signaling mechanisms in the postnatal cochlea have been linked to impairment of hearing acquisition. We thus performed Ca2+ imaging experiments aimed at elucidating the mechanisms underlying the generation and intercellular propagation of ATP-mediated Ca2+ signals in cochlear non-sensory cells. We determined that ATP- and IP3 - dependent Ca2+ oscillations in cochlear non-sensory cells can occur at constant intracellular IP3 concentration. We then combined the information gathered from the two types of experimental approaches in a mathematical model that (i) correctly reproduces the range and propagation speed of intercellular Ca2+ waves and (ii) indicates that inception and culmination of selfsustained Ca2+ oscillations are marked by supercritical Hopf bifurcations at ATP concentrations of ∼ 100 nM and ∼1 μM, respectively.
Finally, we investigated the relationship between spontaneous Ca2+ transients in non-sensory cells and spontaneous Ca2+ action potentials in sensory inner hair cells. Our preliminary results suggest that Ca2+ signaling in non-sensory cells may have a modulating effect on spontaneous electrical activity, which is intrinsically generated in inner hair cells.

Abstract (italiano)

La perdita dell’udito è la forma più comune di disabilità sensoriale: circa un bambino su 1000, infatti, è affetto alla nascita da sordità congenita profonda. La sordità non sindromica (DFNB1) è una malattia ereditaria con un fenotipo di sordità che va da lieve a grave, causata da mutazioni nei geni GJB2 (che codifica la proteina connessina26) e GJB6 (che codifica la connessina30). Canali giunzionali formati prevalentemente da queste due proteine accoppiano le cellule non sensoriali (cellule di sostegno e cellule epiteliali) della coclea dei mammiferi, le quali formano vasti sincizi funzionali. Studi precedenti hanno dimostrato che l’accoppiamento elettrico e metabolico mediato da canali giunzionali è fondamentale per lo sviluppo e il mantenimento dell’udito. Tuttavia, nonostante il gran numero di studi condotti in sistemi di espressione, mancano stime precise del grado di accoppiamento e delle sue alterazioni in condizioni DFNB1.

In questo lavoro di tesi, sono state combinate registrazioni ottiche su larga scala , registrazioni elettrofisiologiche su singola cellula e simulazioni al computer per chiarire i meccanismi che sono alla base della comunicazione intercellulare nelle cellule cocleari non sensoriali in topi giovani (prima settimana post-natale) . In primo luogo, abbiamo sviluppato una nuova tecnica basata sull’imaging del potenziale di membrana cellulare per mappare l’estensione e il grado di accoppiamento elettrico nelle reti cellulari non sensoriali della coclea in via di sviluppo . Abbiamo anche quantificato con precisione la riduzione dell’accoppiamento elettrico in colture organotipiche cocleari da topi transgenici con difetti uditivi causati dall’assenza o da mutazioni della connessina30 rispetto ad animali wild type. Confrontando i nostri risultati sperimentali con simulazioni numeriche , abbiamo stimato che le cellule non sensoriali della coclea nel topo sono già ben accoppiate nella prima settimana post-natale da ben ∼ 1500 canali per ogni coppia di cellule. Nelle colture di pari età provenienti da topi connexin30(T5M/T5M) e connexin30(−/−), la conduttanza giunzionale è ridotta rispettivamente del 14% e del 91% , e questi dati sono in accordo con l’aumento delle soglie uditive mostrato da questi animali nella fase adulta . Oltre a fornire l’accoppiamento elettrico , é stato dimostrato che i canali giunzionali dell’orecchio interno partecipano alla segnalazione Ca2+ intracellulare dipendente dall’ATP e dall’IP3, e l’alterazione di questi meccanismi di segnalazione nella coclea postnatale é stata collegata alla compromissione dell’acquisizione dell’udito. Abbiamo quindi eseguito esperimenti di imaging dello ione Ca2+ volti a chiarire i meccanismi alla base della generazione e propagazione intercellulare dei segnali Ca2+ mediati da ATP nelle cellule non sensoriali della coclea. Abbiamo determinato che le oscillazioni Ca2+ dipendenti dall’ATP e dall’IP3 nelle cellule non sensoriali cocleari possono verificarsi in presenza di una concentrazione intracellulare di IP3 costante. Abbiamo poi combinato le informazioni raccolte attraverso i due diversi approcci sperimentali in un modello matematico che (i) riproduce correttamente la velocità e il range di propagazione delle onde Ca2+ intercellulari e (ii) indica che l’inizio e il culmine delle oscillazioni Ca2+ sono contrassegnati da biforcazioni di Hopf supercritiche a concentrazioni di ATP di ∼ 100 nM e ∼ 1 μM, rispettivamente . Infine , abbiamo studiato la relazione tra transienti Ca2+ spontanei delle cellule non sensoriali e i potenziali d’azione spontanei delle cellule ciliate interne. I nostri risultati preliminari suggeriscono che i transienti Ca2+ delle cellule non sensoriali potrebbero avere un effetto modulatorio sull’attività elettrica spontanea , che è intrinsecamente generata nelle cellule ciliate interne.

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Tipo di EPrint:Tesi di dottorato
Relatore:Mammano, Fabio
Dottorato (corsi e scuole):Ciclo 26 > Scuole 26 > BIOSCIENZE E BIOTECNOLOGIE > NEUROBIOLOGIA
Data di deposito della tesi:30 Gennaio 2014
Anno di Pubblicazione:30 Gennaio 2014
Parole chiave (italiano / inglese):cochlea, connexin, genetic deafness, DFNB1, voltage imaging, calcium imaging, patch clamp, spontaneous activity, development, connexins, electrical coupling, Digital phase−sensitive detector, dye coupling, mathematical modeling
Settori scientifico-disciplinari MIUR:Area 02 - Scienze fisiche > FIS/07 Fisica applicata (a beni culturali, ambientali, biologia e medicina)
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:6706
Depositato il:06 Nov 2014 13:34
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