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Cendron, F (2020) Are the heterogeneous nuclear ribonucleoproteins SQUID and Hrb87F involved in the regulation of circadian rhythmicity in Drosophila melanogaster? [Ph.D. thesis]

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Abstract (italian or english)

The search for new genes involved in circadian rhythmicity in Drosophila melanogaster led to the identification of the RNA binding proteins Hrb87F and SQUID, as partners of Cryptochrome, the photoreceptor responsible for light-synchronization of the circadian clock. In the clock machinery, different post-transcriptional mechanisms have evolved to adjust and consolidate the oscillation of clock genes and proteins in interlocked negative feedback loops. The aim of my PhD project was to study the possible involvement of Hrb87F and SQUID in the post-transcriptional control of the circadian clock in Drosophila.
These preliminary data were confirmed by Co-Immunoprecipitation and western-blot experiments using transgenic flies expressing a tagged version of Cry (HACRY) under the control of the driver timGAL4, for SQUID, while for Hrb87F the interaction was validated by yeast two-hybrid assay, in which dCRY was challenged to Hrb87F as prey.
To achieve more information about a possible role of the clock in the expression of Squid and Hrb87F in Drosophila head, the analysis of the expression profile of the two hnRNPs (mRNAs and proteins) was performed during the 24 hours in wild type (wt) and clock mutant per0 flies. As for Hrb87F, mRNA levels showed an oscillatory trend in LD (Light-Dark) and DD (Dark-Dark) either in wt and per0 flies; the protein levels oscillate in LD and DD in wt flies, but not in per0, suggesting a potential role for the circadian clock in the translational/posttranslational control of the protein. As for Squid, neither the mRNA nor the protein showed rhythmic expression in LD and DD.
Subsequently, the involvement of SQUID and Hrb87F in the generation of the circadian rhythmicity was studied analyzing the locomotor activity pattern of flies’ mutant for each of the two genes. Mutants for both genes showed an impairment of the daily rhythmicity, with a loss of the morning anticipation in LD and low levels of rhythmicity in DD at 29°C, 23°C, 18°C and 15°C, suggesting that Squid and Hrb87F could play a role either in the generation and in the light-synchronization of the circadian behaviour. However, the analysis of locomotor activity in constant light, performed in order to further dissect the possible role of Squid in the light synchronization of the clock, revealed that the light-synchronization of the clock is not impaired in these flies.
The expression of period and timeless and the alternative splicing variants in relation to the temperature were also analyzed in wt and Squid mutant brains by using multiplex real time PCR. The results suggest that the expression of period and timeless mRNA is altered in Squid mutant compared to wt both in LD and DD at each temperature. Moreover, the quantities of per unspliced at high temperature and tim unspliced at low temperature are lower both in LD and DD in the
mutant. This suggests an increase of the splicing events and thus an involvement of SQUID in the post-transcriptional control of clock genes.
In collaboration with Dr Milena Damulewicz (Jagiellonian University of Krakow - Poland), the expression of PERIOD was analyzed in the clock neurons by immunocytochemistry in flies reared at both 18°C and 23°C in LD and DD. At 23°C and 18°C the oscillation of PER in l-LNvs clock neurons is lost, while, in s-LNvs, the accumulation of protein is delayed by 3 hours with a broader peak that reflects a low kinetic of degradation. The analysis of PDF projections from clock neurons shows a profound disorganization of PDF release, suggesting that it can, at least partially, account for the locomotor activity defect observed in the Squid mutant.
Taken together, these results highlight the possible involvement of the hnRNPs Hrb87F and SQUID in the generation and maintenance of circadian rhythmicity in Drosophila melanogaster.

Abstract (a different language)

La ricerca di nuovi geni coinvolti nel controllo della ritmicità circadiana in Drosophila melanogaster ha permesso di identificare una possibile interazione delle due ribonucleoproteine SQUID e HRB87F con CRYPTOCROME. Nella regolazione molecolare dell’orologio circadiano, si sono evoluti diversi eventi di regolazione post trascrizionale che aggiustano e consolidano l’espressione ritmica dei geni orologio e delle corrispettive proteine, secondo un meccanismo a feedback negativo. Per tale motivo lo scopo di questo lavoro è stato studiare e analizzare il possibile coinvolgimento delle hnRNPs nel controllo post-trascrizionale dell’orologio circadiano in Drosophila.
In una fase iniziale, per confermare i risultati ottenuti in precedenza, sono stati condotti esperimenti di Co-Immunoprecipitazione e western-blot in mosche transgeniche in grado di esprimere una versione di CRY associata all’epitopo HA (HACRY) sotto il controllo del driver timGal4. L’anticorpo anti-SQUID ha identificato una proteina nel campione co-immunoprecipitato, confermando l’interazione, mentre il legame con HRB87F è stato osservato mediante l’utilizzo del sistema del doppio ibrido di lievito.
In seguito è stato valutato il possibile coinvolgimento dell’orologio circadiano nell’espressione delle hnRNPs nell’intera testa del moscerino. I livelli di espressione del mRNA di Hrb87F mostrano un trend oscillatorio in LD (luce-buio) e DD (buio costante), sia nel wt che nel mutante per0, mentre la proteina oscilla in LD e DD nelle mosche wt, ma non nelle per0, suggerendo un possibile ruolo dell’orologio circadiano nel controllo traduzionale o post-traduzionale della proteina. L’analisi dell’espressione del gene Squid ha dimostrato, invece, che né mRNA né proteina vengono espressi in maniera ritmica, né in LD né DD.
Successivamente, è stato studiato l’intervento delle due ribonucleoproteine nella generazione della ritmicità circadiana, analizzando l’attività locomotoria di mosche mutanti per entrambi i geni.
Tutti i mutanti hanno riportato un’alterazione della ritmicità circadiana, con una perdita dell’anticipazione dell’attività mattutina in LD e bassi livelli di ritmicità in DD a 29°C, 23°C, 18°C e 15°C. I risultati ottenuti suggeriscono che Squid e Hrb87F possano partecipare alla generazione di un fenotipo ritmico nell’attività locomotoria. Questa analisi è stata completata studiando, inoltre, l’attività locomotoria del mutante squid in condizione di luce costante (LL), poiché esibiva un fenotipo associabile a quello in cui è presente un’alterazione del meccanismo di sincronizzazione della luce; si è visto che, le mosche mutanti presentano un risposta in LL paragonabile al wt, sottolineando un corretto funzionamento del meccanismo di sincronizzazione della luce.

Abbiamo analizzato i profili di espressione dei geni period e timeless e delle rispettive varianti dovute a splicing alternativo legato alla temperatura. I risultati ottenuti mostrano che l’espressione è alterata nel mutante Squid, rispetto al controllo wt, sia in LD sia in DD ad ogni temperatura considerata, evidenziando che è presente un elevata attività di splicing.
In fine, in collaborazione con la Dott. Milena Damulewicz (Università di Jagiellonian di Kracovia - Polonia), è stata condotta un’analisi dell’espressione di PERIOD nei neuroni orologio in mosche mutanti Squid e wt, mediante immunocitochimica a 18°C e 23°C in LD e DD. Si è visto che sia a 23°C sia a 18°C, l’oscillazione di PER nei neuroni orologio l-LNv, viene persa sia in LD sia in DD, mentre nei neuroni s-LNv sia a 23°C sia a 18°C si assiste a un ritardo nell’accumulo della proteina seguito da una cinetica di degradazione più lenta rispetto ai controlli. L’analisi delle proiezioni del neuropeptide PDF ha evidenziato una profonda disorganizzate nel mutante squid.
Nel complesso, tutti questi risultati suggeriscono un coinvolgimento di HRB87F e SQUID nella generazione e nel mantenimento della ritmicità circadiana in Drosophila melanogaster.

EPrint type:Ph.D. thesis
Tutor:Costa, Rodolfo
Ph.D. course:Ciclo 30 > Corsi 30 > BIOSCIENZE
Data di deposito della tesi:25 June 2018
Anno di Pubblicazione:23 March 2020
Key Words:HRB87F, SQUID, HnRNPs, Drosophila melanogaster, circadian clock,
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/11 Biologia molecolare
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:11262
Depositato il:13 Nov 2019 12:45
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