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Investigation of the effect of C-MYC transcription factoron transcriptional regulation of ATP13A2 gene Skip to content Tez Künye Durumu Investigation of the effect of C-MYC transcription factoron transcriptional regulation of ATP13A2 gene / ATP13A2 geninin transkripsiyonel regülasyonunda C-MYCtranskripsiyon faktörünün etkisinin incelenmesi Yazar:ASLI BERİL TİRYAKİLER Danışman: PROF. DR. ARZU KARABAY KORKMAZ Yer Bilgisi: İstanbul Teknik Üniversitesi / Lisansüstü Eğitim Enstitüsü / Moleküler Biyoloji-Genetik ve Biyoteknoloji Ana Bilim Dalı / Moleküler Biyoloji-Genetik ve Biyoteknoloji Bilim Dalı Konu:Biyoloji = Biology ; Genetik = Genetics ; Moleküler Tıp = Molecular Medicine Dizin: Onaylandı Yüksek Lisans İngilizce 2023 89 s. Parkinson hastalığının (PH) atipik erken başlangıçlı formu olarak da bilinen Kufor- Rakeb Sendromu (KRS) olarak teşhis edilen nadir bir nörodejeneratif hastalık olan KRS, PH’nın semptomları yanı sıra spastisite, demans ve supranükleer bakış felci semptomları ile karakterizedir. KRS’nin, ATP13A2 (PARK9) olarak bilinen transmembran proteininde meydana gelen genetik bir mutasyonun sonucu ortaya çıktığı belirlenmiştir. P5 ATPaz taşıyıcı ailesinin bir üyesi olan ATP13A2, ağırlıklı olarak lizozomlarda bulunmaktadır. Araştırmaya göre ATP13A2, Fe3+, Mn2+, Zn2+ ve Ca2+ gibi metal katyonlarının hücre içerisindeki homeostazını korumakla birlikte, fazla alfa-sinüklein ve poliaminlerin eliminasyonunu arttırmakta ve aynı zamanda lizozom, endoplasmik retikulum ve mitokondri gibi organellerin işlevini sürdürmelerini sağlamaktadır. ATP13A2 (PARK9) geni, inorganik katyonların hücre zarından taşınmasını sağlayan çok geçişli membran proteini olan ATP13A2’nin kodlanmasını sağlar ve hücre içi inorganik katyonların taşınması görevini yapan ATP13A2 genindeki mutasyonlar, KRS hastalığı ile ilişkilendirilmiştir. Laboratuvarımızda gerçekleştirilen önceki araştırma sırasında, ATP13A2 genindeki ön sonlandırma kodonu (PTC) oluşturan bir çerçeve kayması mutasyonunun, hastaların fibroblastlarında ATP13A2 mRNA’nın anlamsız aracılı mRNA bozulması (NMD) mekanizması yoluyla degredasyona yol açtığı keşfedilmiştir. Bu durum çerçeve kayması, mutasyonuna sahip hasta fibroblastlarında güdük ATP13A2 proteininin ekspresyonunun inhibisyonuna yol açmaktadır. 5-azasitidin olarak bilinen NMD baskılayıcı ilaç bu çerçeve kaymasına sahip olan hasta fibroblastlarına uygulandığında, güdük ATP13A2 proteininin ekspresyonu gözlenmiştir fakat hasta fibroblastlarının yanı sıra, 5-azasitidin ilacı sağlıklı kontrol hücrelerine uygulandığında, hasta fibroblastlarında gözlemlenen ATP13A2 mRNA artışının yanı sıra kontrol fibroblastlarında da ATP13A2 mRNA seviyesinde önemli bir artış gözlemlenmesine yol açmıştır. Bu elde edilen sonuçlar birkaç farklı mekanizma ile açıklanabilir. Önceki bir çalışmanın bulguları, NMD mekanizmasının, c-Myc transkripsiyon faktörü tarafından inhibe edilebilir olduğunu göstermiştir. Ek olarak, c-Myc’nin 5-azasitidin ilacının inhibe edici mekanizmasında etkili bir rolü olduğu düşünülmektedir. Laboratuvarımızda yapılan araştırmalarda, hücrelere 5-azasitidin uygulandığında, c- Myc protein ekspresyon düzeylerinin kontrol grubuna göre arttığı saptanmıştır. Daha önceki araştırmamızda, 5-azasitidin’in yalnızca NMD mekanizmasının hasta fibroblastlarında çalışmasını durdurmakla kalmayıp, aynı zamanda kontrol fibroblastlarında ATP13A2 mRNA miktarını da arttırdığını göstermiştir. Bunun nedeni, c-Myc transkripsiyon faktörü miktarında bir artışa neden olan 5- azasitidin ilacının etkisi olabilir. ATP13A2’nin ekspresyonunu düzenlemek için, c- Myc transkripsiyon faktörü, potansiyel bağlanma partnerleri ile heterodimer oluşturarak ATP13A2 promotorunda bulunan CACGTG (E-Box) bölgelerine doğrudan erişebilir ve ekspresyon seviyesini düzenleyebilir. Max (MYC-Associated Factor X) proteini bu potansiyel bağlanma partnerlerinden birine örnek olarak verilebilir. c-myc (MYC), hem genleri aktive edebilen hem de inhibe edebilen bir transkripsiyon faktörünü kodlar. c-Myc, bu mekanizma aracılığıyla hücre proliferasyonu ve hücre döngüsü ilerlemesi gibi temel hücresel fonksiyonları kontrol eden çok sayıda hedef genin ekspresyonunu düzenleyebilir. c-Myc, DNA replikasyonu için bile gereklidir. C-Myc, gen ekspresyonunu düzenlemek için Max ile heterodimerize olarak DNA’da E-box’lara bağlanır. Max, transkripsiyonu ve c-Myc’yi inhibe etmek için Mad ailesi proteinleri ile heterodimerize olur. Myc’nin küresel genom ifadesinin ana düzenleyicisi olarak işlev gördüğü ve bu kapasitede Myc’nin temel hücresel işlevleri düzenlediği öne sürülmüştür. Myc ekspresyonunun düzensizliği, geniş hedef gen dizisi nedeniyle kanser de dahil olmak üzere birçok ölümcül hastalığın gelişimi ile ilişkilendirilmiştir. Bu nedenle, bu gen ailesinin karmaşık biyolojik işlevlerinin açıklanamayan doğasını anlamak ve yeni tedavi stratejiler geliştirmek için Myc’nin genomik hedeflerinin kapsamlı bir şekilde araştırılması gerekmektedir. Bu nedenlerle bu çalışma sırasında c-Myc transkripsiyon faktörünün ATP13A2 proteini ve mRNA ekspresyonu üzerindeki etkilerinin belirlenmesi amaçlanmıştır. İlk olarak, biyoinformatik araçlar kullanılarak ATP13A2 promotor bölgesinde, c-Myc’nin potansiyel bağlanma bölgeleri tespit edilmiştir. 2000 bp ATP13A2 promotor bölgesindeki c-Myc transkripsiyon bağlanmasını in vivo olarak tespit etmek amacıyla ChIP analizi yapılmıştır. Western blot deneyleri, c-Myc transkripsiyon faktörünün HEK293T hücrelerinde aşırı eksprese edilmesi durumunda ATP13A2 protein ekspresyon miktarının arttığını; ancak lusiferaz raportör tahlili ve qRT-PCR sonuçları, ATP13A2’nin mRNA seviyelerinin c-Myc aşırı ekspresyonundan 48 saat sonra azaldığını ortaya çıkarmıştır. qRT-PCR ve western blot deneyleri zamana bağlı olarak yapıldığında 7. ve 8. saatlerde anlamlı bir artış, 48. saatte ise anlamlı bir düşüş gözlenmiştir. Bu deneyin bulguları, ATP13A2’nin, protein ve mRNA seviyelerindeki ilk olarak 7-8. saatlerde gözlemlenen anlamlı artışın ardından, mRNA ve protein seviyelerini normal seviyesine yaklaştırarak azaltmak amacıyla bir geri bildirim mekanizmasını aktive edebileceğini göstermektedir. c-Myc transkripsiyon faktörünün ATP13A2 mRNA ve protein seviyesinde 8. saatte gerçekleştirdiği ilk artış, 48. saatte anlamlı bir azalışa dönüşmektedir. Ek olarak, bulgularımız c-Myc transkripsiyon faktörünün ATP13A2 protein ekspresyonu seviyeleri üzerinde önemli bir etkiye sahip olduğunu göstermektedir, ancak c-Myc’nin global gen ekspresyonunu etkilemesi nedeniyle ATP13A2 protein ekspresyon seviyelerini dolaylı yoldan etkileyen başka mekanizmalar da kesinlikle var olmalıdır. Bu tür bir transkripsiyon faktörüne bir örnek, ATP13A2 ifadesini arttırdığı bilinen HIF1A transkripsiyon faktörü olabilir. ATP13A2 proteinindeki artıştan HIF1A’nın sorumlu olup olmadığını belirlemek için, c-Myc’e bağlı HIF1A ekspresyon seviyelerindeki değişimin araştırılması hedeflemiştir. Western blot ve qPCR deneyleri, c-Myc aşırı ekspresyonu üzerine HIF1A proteini ve mRNA seviyelerinin kontrol gruplarına kıyasla arttığını göstermektedir. Son olarak, c-Myc transkripsiyon faktörü hasta fibroblastlarında nükleofeksiyon yoluyla aşırı eksprese edildiğinde, hasta fibroblastlarında NMD inhibisyonu gözlenmiş ve bu durum ATP13A2 genindeki çerçeve kayması mutasyonu sonucu oluşan kısa proteinin western blot analizinde yaklaşık 50 kDa’da görülmesini mümkün kılmıştır. A rare neurodegenerative disease diagnosed as Kufor Rakeb Syndrome (KRS) is also known as an atypical early-onset form of Parkinson’s disease (PD). KRS is characterized by symptoms of spasticity, dementia, and supranuclear gaze palsy in addition to other symptoms of PD. KRS has been linked with mutations that occur in ATP13A2 (PARK9) gene. ATP13A2 gene, expresses the ATP13A2 protein which is known to have a role in the transport of inorganic cations through the membrane of the cell. ATP13A2 belongs to the P5 type ATPase transporter protein family and it can predominantly be found in lysosomes. ATP13A2 protects the cellular homeostasis of metal cations such as Fe3+, Zn2+, Mn2+, and Ca2+, and increases the degradation of accumulated alpha-synuclein, and even maintains the function of organelles including lysosome, mitochondria and endoplasmic reticulum. Previous research carried out in our laboratory discovered that a frameshift mutation forming a pre-termination codon (PTC) in the ATP13A2 gene leads to the degradation of ATP13A2 mRNA through the non-sense-mediated decay (NMD) mechanism, which in turn leads to an inhibition of the expression of the ATP13A2 protein in patients’ fibroblasts. During a previous study done in our laboratory, it was found that when the NMD suppressor drug known as 5-azacytidine was administered to patient cells as well as healthy control cells, a significant increase in the level of ATP13A2 mRNA was observed in control fibroblasts as well as patient fibroblasts. These results could be explained by several different mechanisms. According to the findings of a previous study, the NMD pathway can be inhibited by the c-Myc transcription factor. In addition, c-Myc is thought to have a role in the NMD inhibitory mechanism of 5-azacytidine. When 5-azacytidine was administered to the cells, it was detected that c-Myc protein expression level was increased compared to the control group. Our earlier research showed that 5-azacytidine not only stops NMD from working in patient fibroblasts, but also raises the amount of ATP13A2 mRNA in control fibroblasts. This could be due to 5-azacytidine causing an increase in the amount of c-Myc transcription factor. In order to regulate the expression of ATP13A2, the c-Myc transcription factor can directly access the CACGTG (E-Box) regions that are located in the ATP13A2 promoter by forming a heterodimer with its potential binding partners such as Max (MYC-Associated Factor X) protein. The c-Myc (MYC) gene expresses a transcription factor that can bind to the DNA and it is capable of both activating and inhibiting transcription. c-Myc targets many different genes that are involved with the essential cellular functions. Some examples for this could be cell proliferation division and cell cycle progression. c-Myc is also essential for DNA replication. The c-Myc transcription factor can heterodimerize with Max to regulate gene expression. It has been proposed that c-Myc functions as a master regulator of global genome expression, and in this capacity Myc regulates essential cellular functions. The dysregulation of c-Myc expression has been linked to the development of several fatal diseases, including cancer, due to its wide array of target genes. Therefore, a comprehensive study of the genomic targets of c-Myc is required for understanding the unexplained nature of this gene family’s complex biological functions and to develop novel therapeutic strategies. For these reasons, the effects of the c-Myc transcription factor on ATP13A2 protein and mRNA expression were investigated during this study. Firstly, the binding sites of c-Myc were detected using bioinformatic tools. In order to detect the binding sites of c-Myc on the 2000 bp ATP13A2 promoter site in vivo, ChIP assay was performed. Western blot experiments have shown that when the c-Myc transcription factor is overexpressed in HEK293T cells, the amount of ATP13A2 protein expression increases; however, the luciferase reporter assay and qRT-PCR results revealed that the mRNA levels of ATP13A2 decreased 48 hours after c-Myc overexpression. When qRT-PCR and western blot experiments were done in a time dependent manner, a significant increase was observed at 7th and 8th hours followed by a significant decrease at 48th hour. The findings of this experiment suggest that ATP13A2 may activate a feedback mechanism to reduce mRNA and protein levels closer to their normal level, following the significant increase in protein and mRNA levels first observed 7 and 8 hours after c-Myc overexpression. The initial increase in the ATP13A2 mRNA and protein levels of the c-Myc transcription factor at the 8th hour turns into a significant decrease at the 48th hour. In addition, our findings indicate that the c-Myc transcription factor has an impact on the levels of ATP13A2 protein expression however there are certainly other transcription factors that could also be affecting the overall expression levels of ATP13A2 protein levels due to c-Myc affecting global gene expression. One example to such transcription factor could be HIF1A which is known to upregulate ATP13A2 expression. To determine if HIF1A could be responsible from the increase in ATP13A2 protein, HIF1A expression levels were targeted for further investigation. Western blot and qPCR experiments showed that upon c-Myc overexpression, HIF1A protein and mRNA levels were increased compared to control groups. Finally, when c-Myc transcription factor was overexpressed in patient fibroblasts by nucleofection, NMD inhibition in patient fibroblasts was observed, which made it possible for the truncated protein that is the result of a frameshift mutation in the ATP13A2 gene to be seen at approximately 50 kDa in western blot analysis.
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