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Franchi, Nicola (2011) Individuazione e caratterizzazione di geni per metallotioneine e altre proteine detossificanti in ascidie. [Tesi di dottorato]

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Abstract (inglese)

In order to study the evolution of metallothioneins (MTs) in deuterostomes I have analysed these proteins in Tunicates, which are invertebrate chordates, sister-group of vertebrates. I have isolated the complete cDNA sequences of Ciona intestinalis, Molgula manhattensis and Ascidiella aspersa MTs. Their deduced amino acid sequences are similar in length (39 to 41 amino acids) and each protein has about 30% of cysteine residues which are organised in the typical clusters of vertebrate MTs.
Afterword, my investigation was mainly focused on C. intestinalis, a model tunicate of which the whole genome is available. Nevertheless, no MTs had been previously annotated. After the identification of MT, the research has followed two pathways. The first one was aimed at identifying the tissues involved in the transcription and the gene expression profiles in response to heavy metals such as Zn, Cd and Cu. As regards this last point, in addition to MT, I also considered genes for phytochelatin synthase (PCS), Cu/Zn superoxide dismutase (Cu/Zn SOD), glutamate-cysteine ligase (GCLC) catalytic subunit, glutathione synthetase (GS), glutathione peroxidase 7 (GPX7) and proliferating cell nuclear antigen (PCNA), looking for relationships between them. In order to define their possible evolution, the second approach involved bioinformatic analyses, aimed at understanding the organisation of the gene structure, promoter regions and sequence identity of MTs and of all the other considered proteins.
The deduced protein sequence of C. intestinalis MT (CiMT-1) is quite different from the other deuterostome MTs: it is the shortest MT so far identified in this group, with only 39 amino acids in comparison with 61-68 amino acids of the other taxa. In addition, the KKS motif, that links the two domains (α and β) of the vertebrate MTs, is completely missing. The identity between CiMT-1 and other deuterostome MTs is quite low, ranging from 18.8 and 38.3%.
Vertebrate MT genes show a tripartite structure, with three exons and two introns. Introns differ in length, but their relative position is conserved: the first intron interrupts the sequence at amino acid 9, while the second intron at amino acid 31 or 32, at the junction of the α and β domains. CIMT-1 shows the same tripartite structure, with the first intron in the typical vertebrate position, while the second intron is located in the 3’UTR, as in echinoderm MTs.
The promoter region of CIMT-1 shows features present in both vertebrates and in echinoderms: it contains three half-AREs (antioxidant responsive element) as in echinoderms, and one typical vertebrate ARE. Four MREs (metal responsive elements) are also present.
Cd exposure increases the transcription of CIMT-1 in a non linear way: an initial increase, at 6 h, is followed by a decrease to the control levels at 24 h, then another increase is present after 96 h. Treatments with Zn and Cu, however, induce the gene transcription progressively up to the end of treatment (120 h) when the messenger levels are fourfold the control values.
CiMT-1 mRNA is present only in haemocytes, specifically in granulocytes. These cells, after 24 h of treatment with Cd, are present in tunic and their amount is twice that of controls. Therefore, the decrease of transcript at 24 h may be a result of this cell migration. The subsequent increase is presumably due to specific cellular proliferation of granulocytes in the blood lacunae. This scenario is confirmed by the high rate of cell death in tunic, where haemocytes accumulate, and also by the massive transcription of PCNA in treated samples. Indeed, both CiMT-1 and PCNA show a peak of expression at 96 h. The results obtained with phytochelatin synthase fit with this hypothesis.
In C. intestinalis, PCS is expressed in granulocytes and the mRNA levels remain comparable to those of controls up to 72 h, but then they rise up to 96 h. From literature data it is known that this gene is not inducible, but it is activated in presence of divalent metal ions. Again, it is very likely that the observed messenger peak is not a consequence of an induction phenomenon, but of a strong proliferation of granulocytes.
This is the first data on the transcription of this gene, on the location at granulocyte level and on its involvement in metal detoxification processes in deuterostomes.
The study of the behaviour of the genes involved in detoxification suggests that the enzymes (SOD, GPX) may have a marginal role, whereas the cystein-rich molecules (PCS, GS, GCL) play an important role in presence of Cd, Cu and Zn. Moreover, the localisation of these transcripts, by in situ hybridisation, suggests that circulating haemocytes are the cells mostly involved in detoxification processes.

Abstract (italiano)

Lo scopo di questa ricerca è quello di analizzare le metallotioneine (MT) nei Tunicati, taxon il sister-group dei Vertebrati, allo scopo di studiare l’evoluzione delle metallotioneine nei deuterostomi invertebrati. Ho quindi isolato sequenze complete di cDNA per MT nei Tunicati Ciona intestinalis, Molgula manhattensis e Ascidiella aspersa. In questi organismi le MT presentano sequenze aminoacidiche dedotte simili, di lunghezza compresa tra 39 e 41 aminoacidi e con circa il 30% di residui cisteinici organizzati nei tipici cluster conservati delle MT dei Vertebrati.
La mia indagine si è quindi concentrata su C. intestinalis, organismo modello dei Tunicati per il quale è disponibile la sequenza dell’intero genoma. Nonostante questo, nessuna MT era stata annotata. Dopo aver identificato la MT, la ricerca si è orientata su due percorsi. Il primo percorso era volto a comprendere quali fossero i tessuti coinvolti nella trascrizione di questo gene e quali ne fossero i profili di espressione in risposta a metalli pesanti quali Zn, Cd e Cu. In quest’ambito ho anche considerato la fitochelatino sitetasi (PCS), la Cu/Zn superossido dismutasi (Cu-Zn SOD), la glutammato cistein-ligasi (GCLC) subunità catalitica, la glutatione sintetasi (GS), la glutatione perossidasi 7 (GPX7) e l’antigene nucleare di proliferazione cellulare (PCNA), al fine di valutarne le relazioni. Il secondo approccio, di tipo bioinformatico, era volto a chiarire l’organizzazione genica, la struttura delle regioni promotrici e le identità di sequenza delle metallotioneine e delle altre proteine studiate, al fine di far luce sulla possibile evoluzione delle sequenze prese in esame.
Le sequenza proteica dedotta da C. intestinalis (CiMT-1) è decisamente diversa dalle MT degli altri deuterostomi: essa risulta essere la più corta MT fino ad ora individuata in questo gruppo, presentando 39 aminoacidi contro 61-68 degli altri taxa. Inoltre, manca completamente il motivo KKS che connette i due domini (alpha e beta) delle MT dei vertebrati. Si evidenziano quindi bassi livelli di identità aminoacidica, tra 18,8% e 38,3%, con le MT degli altri deuterostomi.
Tutte le MT dei vertebrati hanno struttura genica tripartita, con tre esoni e due introni. Gli introni differiscono in lunghezza, ma la loro posizione relativa è conservata: il primo introne interrompe la sequenza all’aminoacido 9, mentre il secondo introne interrompe la sequenza all’aminoacido 31 o 32, alla giunzione dei domini alpha e beta. CiMT-1 mostra la stessa struttura tripartita, con il primo introne nella posizione tipica dei vertebrati, mentre il secondo introne è posto nella regione 3‘UTR, come nelle MT degli echinodermi.
Anche la regione promotrice di CiMT-1mostra caratteristiche presenti sia negli echinodermi che nei vertebrati: possiede tre half-ARE (antioxidant responsive element) come negli echinodermi ed una sequenza ARE tipica dei vertebrati. Esso presenta inoltre quattro MRE (metal responsive elements) ben distanziati.
Il trattamento con Cd induce aumenti del trascritto di CiMT-1 con andamento irregolare: un primo aumento è presente a 6 h, seguito da una diminuzione fino a quasi i livelli di controllo a 24 h per poi ricrescere fino ad un picco massimo dopo 96 h. I trattamenti con Zn e Cu, invece, inducono valori di trascrizione quattro volte superiori rispetto ai livelli dei controlli solo a fine trattamento (120 h) con un andamento di crescita pressoché lineare nel tempo. Il trascritto per CiMT-1 è presente a livello dei soli granulociti. Tali cellule a 24 h di trattamento con Cd si accumulano nella tunica in numero circa doppio rispetto ai controlli. Pertanto la diminuzione di trascritto riscontrato a 24 h può essere conseguenza di questa migrazione cellulare, mentre il successivo aumento è presumibilmente da imputare a proliferazione cellulare specifica dei granulociti in circolo. Questo scenario è confermato dall’alto tasso di morte cellulare nella tunica, dove gli emociti si accumulano, ed inoltre dalla massiccia trascrizione di PCNA nei campioni trattati. Infatti sia CiMT-1 che PCNA presentano un picco di espressione a 96 h.. A confermare tale ipotesi sono i risultati relativi alla fitochelatino-sintetasi. In C. intestinalis il gene viene espresso dai granulociti ed i livelli di trascritto rimangono simili a quelli dicontrollo fino a 72 h, per poi crescere a 96 h. Da dati di letteratura è noto che questo gene non è inducibile, ma viene attivato in presenza di ioni metallici bivalenti. E’ molto probabile quindi, che questo picco non sia una conseguenza di un fenomeno di induzione, ma della forte proliferazione cellulare dei granulociti. E’ da notare che questo è il primo dato che dimostra la trascrizione di questo gene in organismi deuterostomi, la sua localizzazione esclusiva a livello dei granulociti e il suo coinvolgimento in processi di detossificazione da metalli.
Lo studio degli andamenti degli altri geni coinvolti nella detossificazione suggerisce che la componente enzimatica (SOD, GPX) possa avere un ruolo marginale, mentre la componente tiolica (PCS, GS, GCL) svolga un ruolo primario in presenza sia di Cd, che di Cu e Zn. Inoltre la localizzazione tramite ibridazione in situ di questi trascritti evidenzia che gli emociti circolanti sono le cellule maggiormente coinvolte nei processi di detossificazione.

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Tipo di EPrint:Tesi di dottorato
Relatore:Piccinni, Ester
Correlatore:Ballarin, Loriano
Dottorato (corsi e scuole):Ciclo 23 > Scuole per il 23simo ciclo > BIOSCIENZE > BIOLOGIA EVOLUZIONISTICA
Data di deposito della tesi:NON SPECIFICATO
Anno di Pubblicazione:28 Gennaio 2011
Parole chiave (italiano / inglese):ascidie, metallothioneine, detossificazione, ROS, metalli
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/05 Zoologia
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:3706
Depositato il:20 Lug 2011 13:04
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