Research Collection. Nutrition regulates mitochondrial biogenesis in the Drosophila adipose tissue through delg and cyclind/cdk4.

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1 Research Collection Doctoral Thesis Nutrition regulates mitochondrial biogenesis in the Drosophila adipose tissue through delg and cyclind/cdk4 Author(s): Baltzer, Claudia Publication Date: 2010 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library

2 DISS. ETH Nr Nutrition regulates mitochondrial biogenesis in the Drosophila adipose tissue through Delg and CyclinD/Cdk4 A dissertation submitted to ETH ZURICH for the degree of DOCTOR OF SCIENCES presented by Claudia Baltzer Master of Sciences in Biochemistry born on July 6 th 1982 citizen of Zurich, Switzerland Accepted on the recommendation of Prof. Dr. Christian Frei Prof. Dr. Beat Suter Prof. Dr. Linda Partridge Prof. Dr. Wilhelm Krek 2010

3 1 Summary Mitochondria are cellular organelles that perform critical metabolic functions: they generate energy from nutrients and provide metabolites for de novo synthesis of fatty acids and several amino acids. Thus mitochondrial mass and activity must be coordinated with nutrient availability, yet this remains poorly understood. This study demonstrates that Drosophila larvae grown in low yeast food, thus being deprived of nutrients such as amino acids, have strong defects in mitochondrial abundance and respiration activity in the larval fat body. This correlates with reduced expression of nuclear encoded mitochondrial (NEM) proteins, in particular genes involved in oxidative phosphorylation (OXPHOS). Genes involved in glutamine metabolism are also expressed in a nutrient dependent manner, suggesting a coordination of amino acid synthesis with mitochondrial abundance and activity. Moreover, Delg (CG6338), the Drosophila homologue to the alpha subunit of the mammalian transcription factor NRF 2/GABP, was shown to be required for proper expression of most genes encoding mitochondrial proteins. In delg mutants, reduced mitochondrial mass does not translate into reduced OXPHOS activity. The residual mitochondria seem to compensate the lack of mass with higher activity. Our data show that Delg is critical to regulate mitochondrial abundance and expression levels of enzymes required for glutamine metabolism in response to nutrient availability. In agreement with the phenotypes caused by low yeast starvation, knock down of the amino acid antiporter slimfast (slif) was shown to lead to reduced mitochondrial respiration, reduced mitochondrial mass, and reduced expression of NEM proteins. This suggests that the phenotypes observed under low yeast starvation are probably caused by the reduction of amino acids. As Slif has been shown to be an upstream activator of TOR signaling (Colombani et al., 2003), it is very likely that mitochondrial abundance and activity are regulated via the TOR pathway in a nutrient dependent manner. Additionally, the study demonstrates that the nutrient sensitive, growth promoting complex Cyclin D/Cyclin dependent kinase 4 (CycD/Cdk4) requires Delg for its effect on mitochondria. However, whether the CycD/Cdk4 complex is the link 5

4 between TOR signaling, Delg and mitochondrial regulation remains to be elucidated. Towards the end of the larval stages, the larvae stop feeding and start wandering to prepare for pupariation. The wandering stage mimics a kind of starvation status of the larvae. Therefore it was not surprising to observe a reduction of Cytochrome c activity (COX) after control larvae crawled out of the food. In contrast, wandering delg mutants showed significantly increased COX activity. These data support the model that the remaining mitochondria in the delg mutants show higher activity and nutrients indeed down modulate mitochondrial respiratory activity. Taken together, we found that mitochondrial biogenesis is regulated by nutrients, in particular by amino acids probably via the TOR pathway. Furthermore, our data suggests that Delg is critical to regulate or control mitochondrial abundance in respect to CycD/Cdk4, and glutamine metabolism depending on nutrient availability. However, in contrast to nutrients, Delg is not involved in the regulation of mitochondrial activity in the fat body, at least not in the feeding larvae. Our findings are the first genetic evidence that the regulation of mitochondrial mass can be uncoupled from mitochondrial activity. 6

5 2 Zusammenfassung Mitochondrien sind zelluläre Organellen die kritische metabolische Funktionen haben: sie versorgen die Zellen mit Energie aus Nährstoffen, liefern aber auch Metaboliten für die de novo Synthese von Molekülen wie Fett und Aminosäuren. Deshalb müsste die mitochondrielle Masse und ihre Aktivität mit dem Vorhandensein von Nährstoffen abgestimmt sein. Eine solche koordinierte Regulation ist bis jetzt nur wenig verstanden. Diese Studie zeigt, dass Fettkörper von Drosophila Larven, die auf Futter mit reduziertem Hefegehalt gewachsen sind, also sehr wenig Aminosäuren zu sich genommen haben, starke Defekte in der Menge an Mitochondrien und deren Atmungsaktivität haben. Dies korreliert mit reduzierter Expression von nukleär kodierten mitochondriellen (NEM) Genen, wobei besonders Gene der oxidativen Phosphorylierung betroffen sind. Gene des Glutamin Metabolismus werden unter anderem abhängig von der Nährstoffkonzentration reguliert. Dies lässt darauf schliessen, dass die Aminosäurensynthese mit der Menge an Mitochondrien und deren Aktivität koordiniert wird. Des Weiteren wurde in dieser Studie gezeigt, dass Delg (CG6338), dem Drosophila Homolog zu der alpha Untereinheit des Transktiptionsfaktors NRF 2/GABP von Säugern, für die korrekte Expression von fast allen Genen welche mitochondrielle Proteine kodieren, benötigt wird. Überraschenderweise führt die Reduktion von mitochondrieller Masse in delg Mutanten nicht zu reduzierter OXPHOS Aktivität. Es ist vielmehr so, dass die verbleibenden Mitochondrien versuchen durch höhere Aktivität die geringere Menge zu kompensieren. Delg reguliert die Menge an Mitochondrien und vor allem die Expression von Enzymen des Glutamin Metabolismus, welche abhängig von der Nährstoffverfügbarkeit sind. Beim Herunterregulerien des Aminosäuren Antiporters slimfast (slif) wurden ähnliche Phänotypen beobachtet: weniger mitochondrielle Atmung, weniger mitochondrielle Masse und reduzierte Expression von Genen die mitochondrielle Proteine kodieren. Diese Resultate zeigen, dass die Phänotypen, die durch eine reduzierte Hefe Diät verursacht werden höchst wahrscheinlich durch mangelhafte Aminosäuren Aufnahme verursacht werden. Da gezeigt 7

6 wurde, dass Slif ein Aktivator des TOR Signalweges ist (Colombani et al., 2003) ist es möglich, dass mitochondrielle Menge und Aktivität nährstoffabhängig durch den TOR Pathway reguliert werden. Des Weiteren zeigt diese Studie, dass der nähstroffsensitive, wachstumsfördernde Komplex Cyclin D/ Cyclin dependent kinase 4 (CycD/Cdk4) Delg benötigt, um einen Effekt auf Mitochondrien zu haben. Ob CycD/Cdk4 jedoch die Verbindung zwischen dem TOR Signalweg, Delg und der Regulation von Mitochondrien ist, muss noch untersucht werden. Gegen Ende der larvalen Phase hören die Tiere auf zu fressen, kommen aus dem Futter herraus und beginnen zu wandern um sich für die Verpuppung vorzubereiten. Diese wandernde Phase simuliert also eine Art Hungerkur. Es war deshalb keine Überraschung, dass Kontroll Larven reduzierte Cytochrom C Oxidase (COX) Aktivität gezeigt haben, als diese in die Wanderphase übergiengen. Wandernde delg Mutanten hatten jedoch signifikant höhere COX Aktivität. Diese Daten unterstützen das Model, dass die verbleibenden Mitochondrien in der delg Mutante eine höhere Aktivität aufweisen und dass Nährstoffe in der Tat mitochondrielle Atmung modulieren können. Zusammenfassend haben wir gefunden, dass mitochondrielle Biogenese durch Nährstoffe reguliert wird, vor allem durch Aminosäuren. Unsere Daten weisen darauf hin, dass diese Regulation durch den TOR Sinalweg geschieht. Des Weiteren weisen unsere Daten darauf hin, dass Delg ein kritischer Faktor ist um die mitochondrielle Menge in Bezug auf CycD/Cdk4 abzustimmen. In Folge der Nährstoffverfügbarkeit reguliert Delg den Glutamin Metabolismus. Im Gegenteil zur Nährstoffverfügbarkeit ist Delg jedoch nicht an der Regulation mitochondrieller Aktivität beteiligt, zumindest nicht in Larven, welche noch fressen. Diese Ergebnisse sind die ersten genetischen Belege, dass mitochondrielle Masse von mitochondrieller Aktivität entkoppelt werden kann. 8

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