Research Collection. S100a4 and adipocyte metabolism. Doctoral Thesis. ETH Library. Author(s): Röder, Eva. Publication Date: 2014
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1 Research Collection Doctoral Thesis S100a4 and adipocyte metabolism Author(s): Röder, Eva Publication Date: 2014 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 S100a4 and adipocyte metabolism A thesis submitted to attain the degree of DOCTOR OF SCIENCES (Dr. sc. ETH Zurich) presented by EVA RÖDER Mag. rer. nat., University of Vienna born on December 2 nd, 1977 Citizen of Austria Accepted on the recommendation of Prof. Dr. Christian Wolfrum Prof. Dr. Jan Krützfeld Prof. Dr. Wolfgang Langhans Prof. Dr. Gottfried Rudofsky 2014
3 2 Abstract Abstract Obesity is defined by the increase in fat mass which consists mainly of adipocytes. Two possibilities exist for increasing fat mass within the body: one is an increase in adipocyte number called adipogenesis, whereas the other one is the enlargement of already existing adipocytes. This enlargement is known to impair the adipocyte s metabolism as the cell is not able anymore to properly react to external stimuli such as insulin. Obesity is a major risk factor for the development of various diseases including type 2 Diabetes, cardiovascular disease, non-alcoholic fatty liver and some types of cancer. In the past decades, it has emerged as a major health issue as the prevalence is increasing due to sedentary lifestyles and increasing energy intake. It is established that weight loss improves obesity-associated risk factors. Therefore, as a side project of this thesis, a database combining changes in transcriptomics from fat tissue and clinical and behavioral parameters from human individuals undergoing a one year weight reduction program was created. The main project was about S100a4, a member of the S100 protein family, known from various cancer studies. In previous, not yet published studies with knockout mice, it was demonstrated that S100a4, is involved in adipogenesis and insulin sensitivity. The aim of this project was to investigate the underlying mechanisms by the identification of novel interaction candidates and involved pathways. Thus, in vitro differentiation and interaction studies in 3T3-L1 cells were performed. Knockdown of S100a4 resulted in changes in gene expression of numerous genes involved in differentiation, proliferation and apoptosis, such as C/ebpß, Pparγ, cyclin E, cyclin A, Bax and Apaf-1. The evaluation of the transcript levels of these genes within 24h after induction of differentiation indicated increased proliferation upon knockdown of S100a4 in 3T3-L1 cells. In general, excessive activation of factors promoting cell cycle progression triggers the intrinsic pathway of apoptosis. In parallel, differentiation seemed to be amplified within 24h adding to the stress the cells were exposed to. In fact, apoptosis was increased demonstrated by increased levels of active caspase 3 upon knockdown of S100a4. As a result, also lipid droplet formation and terminal differentiation were impaired. Potential candidates for S100a4 interactions were identified by immunoprecipitations and mass spectrometry analysis. Amongst these were Pp2a, a phosphatase involved in numerous cellular processes such as G 1 /S transition of the cell cycle, Api5, an inhibitor of
4 Abstract 3 apoptosis, galectin-1, a lectin which is involved in G 1 /S transition, Ppm1a and b, phosphatases involved in Tgf-ß, NF-κB and insulin signaling and coatomer protein complex I, which is suggested to regulate lipolysis. Pp2a regulates retinoblastoma protein activity which is a key regulator of proliferation and cell cycle progression. Upon knockdown of S100a4, Pp2a activity was decreased, which could be the reason for the deregulation of cell cycle and differentiation. Further, Ppm1a and b could be involved in increased apoptosis by NF-κB regulation. The lower differentiation, resulting in hypertrophy, and increased apoptosis, resulting in increased inflammation could be reasons for insulin resistance in S100a4 knockout mice. Further, there is evidence that the activity of LAR, a phosphatase involved in insulin signaling, is changed upon S100a4 knockdown, adding to insulin resistance. Taken together, we identified numerous pathways and S100a4 interactors involved in these signaling cascades in in vitro studies. For future experiments it will be important, to investigate single pathways in more detail also in knockout mice in order to gain knowledge about the mechanisms in vivo.
5 4 Zusammenfassung Zusammenfassung Fettleibigkeit wird durch die Zunahme an Fettmasse, die hauptsächlich aus Fettzellen besteht, definiert. Es gibt zwei Möglichkeiten für die Zunahme der Fettmasse im Körper: einerseits die Erhöhung der Anzahl an Fettzellen, auch Adipogenese genannt, andererseits die Vergrößerung der schon existierenden Fettzellen. Man weiß, dass diese Vergrößerung den Stoffwechsel der Fettzellen beeinträchtigt, da die Zelle nicht mehr fähig ist, auf externe Reize wie Insulin zu reagieren. Fettleibigkeit oder Adipositas ist ein Hauptrisikofaktor für die Entwicklung einer Vielzahl an Erkrankungen wie Typ 2 Diabetes, kardiovaskuläre Erkrankungen, nicht-alkoholisch bedingte Fettleber und manche Krebsarten. Fettleibigkeit entwickelte sich in den vergangenen Jahrzehnten zu einem großen gesundheitlichen Problem, da die Prävalenz durch Bewegungsmangel und erhöhte Energiezufuhr zunimmt. Es ist erwiesen, dass Gewichtsreduktion die gesundheitlichen Risikofaktoren, die mit Fettleibigkeit assoziiert werden, reduziert. Daher wurde als Nebenprojekt dieser Dissertation eine Datenbank kreiert, die Transkriptom-weite Analysen und klinische und Verhaltensparameter von Personen kombiniert, die ein Jahr lang an einem Gewichtsreduktionsprogramm teilgenommen haben. Das Hauptprojekt befasst sich mit S100a4, einem Mitglied der S100 Proteine, welches aus zahlreichen Krebsstudien bekannt ist. Vorangegangene, noch nicht publizierte Studien mit Knockout-Mäusen zeigten, dass S100a4 eine Rolle in Adipogenese und Insulinsensitivität spielt. Das Ziel dieses Projektes war es, die zugrundeliegenden Mechanismen durch die Identifizierung von neuen Interaktionspartnern und den involvierten Signalwegen zu untersuchen. Daher wurden in vitro Differenzierungs- und Interaktionsstudien in 3T3-L1 Zellen durchgeführt. S100a4 Knockdown führte zur Veränderung der Gen-Expression zahlreicher Gene, die an Differenzierung, Proliferation und Apoptose beteiligt sind, darunter C/ebpß, Pparγ, Cyclin E, Cyclin A, Bax und Apaf-1. Die Auswertung der Transkriptionsniveaus dieser Gene innerhalb 24 Stunden nach Induktion der Differenzierung deutete auf erhöhte Proliferation durch den Knockdown hin. Im Allgemeinen löst eine übermässige Aktivierung von Faktoren, die den Zellzyklus vorantreiben, den intrinsischen Weg der Apoptose aus. Gleichzeitig schien die Differenzierung innerhalb der 24 Stunden verstärkt zu sein, was zusätzlich zu dem Stress betrug, dem die Zellen ausgesetzt waren. Tatsächlich war das
6 Zusammenfassung 5 Ausmass an Apoptose durch S100a4-Knockdown erhöht, was durch einen Anstieg an aktiver Caspase-3 gezeigt wurde. Folglich waren auch die Lipidtröpfchenbildung und die terminale Differenzierung beeinträchtigt. Mögliche Kandidaten für Interaktionen mit S100a4 wurden durch Immunopräzipitation und Massenspektrometer-Analysen identifiziert. Unter diesen waren Pp2a, eine Phosphatase, die in zahlreichen zellulären Prozessen involviert ist, unter anderem am Übergang von der G 1 in die S-Phase des Zellzyklus, Api5, ein Apoptose-Inhibitor, Galectin-1, ein Lektin, das am Übergang von der G 1 in die S-Phase des Zellzyklus beteiligt ist, Ppm1a und b, zwei Phosphatasen, die eine Rolle in Tgf-ß, NF-κB und Insulin Signalwegen spielen und CopI, das an der Lipolyse beteiligt sein soll. Pp2a reguliert die Aktivität des Retinoblastoma Proteins, das ein wichtiger Regulator der Proliferation und des Zellzyklus ist. S100a4 Knockdown führte zu einer Aktivitätsabnahme von Pp2a, was der Grund für die Deregulierung des Zellzyklus und der Differenzierung sein könnte. Ferner könnten Ppm1a und b an der Zunahme der Apoptose beteiligt sein durch die Regulierung von NF-κB. Die verringerte Differenzierung, resultierend in Hypertrophie, und die verstärkte Apoptose, resultierend in verstärkter Entzündung, könnten Gründe für die Insulinresistenz in S100a4- Knockout-Mäusen sein. Ferner gibt es Anzeichen dafür, dass die Aktivität von LAR, einer Phosphatase, die in Insulinsignalwegen eine Rolle spielt, durch S100a4-Knockdown verändert ist, was zur Insulinresistenz beitragen kann. Zusammenfassend beschreibt diese Arbeit in in vitro Studien zahlreiche Signalkaskaden und S100a4-Interaktoren, die in diesen Signalkaskaden involviert sind. Für die Zukunft ist es wichtig, detailliert einzelne Signalkaskaden auch in Knockout-Mäusen zu untersuchen, um mehr Kenntnisse über die Vorgänge in vivo zu erhalten.
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