Mass spectrometry-based and functional analysis of novel VCP/ p97 cofactor complexes in health and disease

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1 Research Collection Doctoral Thesis Mass spectrometry-based and functional analysis of novel VCP/ p97 cofactor complexes in health and disease Author(s): Ritz, Danilo 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 N Mass spectrometry-based and functional analysis of novel VCP/p97 cofactor complexes in health and disease A dissertation submitted to ETH ZURICH For the degree of Doctor of Sciences Presented by Danilo Ritz Dipl. Biol., University of Basel Born 28-Aug-1980 Citizen of BRIG VS Accepted on the recommendation of Prof. Matthias Peter, examiner Prof. Hemmo Meyer, co-examiner Prof. Ruedi Aebersold, co-examiner 2010

3 Summary Summary VCP/p97 (Cdc48 in yeast), a member of the AAA (ATPases Associated with various cellular Activities) protein family, is an essential ubiquitin-dependent segregase conserved in eukaryotes. p97 participates in a wide variety of cellular pathways, including regulation of mitosis, ER protein quality control, transcription factor activation, signalling and apoptosis. To fulfil its function in these different pathways, p97 forms alternative multiprotein complexes with distinct sets of adaptor proteins and substrate processing cofactors that determine its functional specificity and localization. However, it is unclear how many VCP/p97-cofactor complexes exist and what their exact protein composition and function is. Intriguingly, missense mutations in p97 cause a progressive and degenerative multisystem disorder, called Inclusion Body Myopathy associated with Paget s disease of bone and Frontotemporal Dementia (IBMPFD) also dubbed VCP-disease. The molecular pathogenesis and why only certain cells and processes are affected has remained unclear. In the first part of this thesis, we established and tested an unbiased mass spectrometry-based approach to isolate and identify p97-associated proteins in mammalian tissue culture cells. Using this approach, we identified a total of 302 potential p97 interactors. We verified six representative candidates with diverse cellular functions, thus confirming that the approach is suitable to identify novel p97-governed processes. In addition, MS-based analysis of the newly identified p97 interactors UBXD1, UBXD8 and UBXD9 showed that these proteins specify novel p97 complexes with potentially distinct, interesting new functions. Furthermore, we applied this approach to compare the protein interaction pattern of wild-type p97 with that of the most frequent IBMPFD-associated mutant p97 R155H. We identified two novel binding factors whose interaction with p97 was specifically reduced by the mutation, the adapter UBXD1 and the membrane trafficking factor caveolin-1 (Cav1). While this finding may lead to understanding of the pathogenesis of this disease, it also more generally proved that this MS approach can be applied to detect differences in the interaction pattern of p97 under diverse conditions. Given the significance of this finding, we investigated the two novel p97 interactors UBXD1 and Cav1 in more detail on the biochemical and functional level in the second part of this thesis. We showed that UBXD1 defines a novel p97 complex, which binds Cav1, and confirmed the effect of the p97 R155H mutation biochemically. Additionally, we showed that the interaction between p97 and Cav1 is not only disturbed by IBMPFD mutations in p97, but also by the disease-relevant mutation P132L in Cav1. Moreover, we revealed that p97 targets Cav1 in SDS-resistant higher order assemblies that occur at or close to the plasma membrane, thus speaking against a role in an ER-associated process. Importantly, we show that Cav1 is mono- or multi-monoubiquitinated and that p97 binds this form of Cav1, suggesting that 3

4 Summary Cav1 may be a substrate of p97. Taken together, these results link the p97 UBXD1 complex to membrane trafficking and suggest that compromised trafficking and homeostasis of caveolin may contribute to the pathogenesis in individuals with IBMPFD. 4

5 Zusammenfassung Zusammenfassung VCP/p97 (Cdc48 in Hefe), ein Mitglied der AAA (ATPasen Assoziiert mit verschiedenen zellulären Aktivitäten) Proteinfamilie ist eine essenzielle, Ubiquitinabhängige Segregase, welche in Eukaryonten stark konserviert ist. p97 spielt eine Rolle in vielen verschiedenen zellulären Prozessen, darunter die Regulation der Mitose, Qualitätskontrolle von Proteinen im ER, Aktivierung von Transkriptionsfaktoren, Signaltransduktion und Apoptose. Um in diesen verschiedenen Prozessen zu funktionieren formt p97 alternative Multiprotein-Komplexe mit verschiedenen Gruppen von Adaptor- und Substratprozessierungsproteinen, welche die funktionelle Spezifität und Lokalisierung von p97 beeinflussen. Allerdings ist unklar wie viele solcher VCP/p97 Komplexe existieren und was deren Proteinzusammensetzung und Funktion ist. Darüberhinaus lösen Missens-Mutationen in p97 die progressive und degenerative multisystemische Krankheit Inclusion Body Myopathy assoziiert mit Paget s disease of bone und Fronto-temporal Dementia (IBMPFD) oder VCP-Krankheit aus. Die molekulare Pathogenese dieser Krankheit sowie die Selektivität für Muskel-, Hirn- und Knochengewebe sind unbekannt. Im ersten Teil dieser Studie haben wir ein auf Massenspektrometrie basierendes System zur Isolierung und Identifizierung von p97-assoziierten Proteinen in Säugerzellen etabliert und getestet. Wir haben 312 potentielle p97-interaktoren identifiziert und sechs representative Kandidaten verifiziert. Wir haben damit gezeigt, dass unser System geeignet ist für die Identifizierung von neuen p97-abhängigen Prozessen. Zusätzlich hat die massenspektrometrische Analyse der neu identifizierten Komplexe aus p97 und UBXD1, UBXD8 und UBXD9 gezeigt, dass sie Komplexe mit distinkter Zusammensetzung darstellen, die auf verschiedene, interessante Funktionen hinweisen. Darüberhinaus haben wir dieses System verwendet, um das Interaktionsmuster von p97-wildtyp mit dem der IBMPFD Mutante p97 R155H zu vergleichen. Im Zuge dieser Analyse wurden die zwei neuen p97- Interaktoren UBXD1 und Caveolin 1 (Cav1) entdeckt, welche eine stark reduzierte Interaktion mit p97 R155H aufweisen. Diese Beobachtung könnte nicht nur hilfreich für das Verständnis der Pathogenese von IBMPFD sein. Sie zeigt auch, dass unser System Unterschiede im Interaktionsmuster von p97 in verschiedenen Konditionen detektieren kann. Aufgrund der Signifikanz dieser Beobachtung haben wir im zweiten Teil dieser Studie die neuen p97 Interaktoren UBXD1 und Cav1 auf biochemischer und funktioneller Ebene genauer untersucht. Wir zeigten, dass UBXD1 einen neuen p97 Komplex definiert, welcher mit Cav1 interagiert und durch IBMPFD Mutanten gestört wird. Interessanterweise wird dieser Komplex nicht nur durch IBMPFD Mutationen in p97 gestört, sondern auch von der krankheitsrelevanten Mutation P132L in Cav1. Wir zeigten auch, dass p97 Cav1 in SDSresistenten Assemblierungen höherer Ordnung bindet, welche an oder in der Nähe der 5

6 Zusammenfassung Zellmembran auftreten, was gegen eine Verbindung von p97 and Cav1 durch ER-abhängige Prozesse spricht. Darüberhinaus zeigten wir, dass Cav1 mono oder multi-mono-ubiquitiniert wird und dass p97 mit dieser modifizierten Form von Cav1 interagiert, was darauf hinweist dass Cav1 ein Substrat von p97 ist. Zusammenfassend identifizieren unsere Daten eine Funktion des neuen p97 UBXD1 Komplexes im Membrantransport und Regulation von Cav1, die eine wichtige Komponente in der Pathogenese von IBMPFD darstellen könnte. 6

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