Solution structure of the potential splicing factor RBMY in complex with an RNA stem-ioop
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1 Doctoral Thesis ETH No Solution structure of the potential splicing factor RBMY in complex with an RNA stem-ioop A dissertation submitted to the Swiss Federal Institute oftechnology Zurich for the degree of Doctor ofnatural Seiences presented by Lenka Skrisovska Diploma in Biochemistry Masaryk University ofbrno, Czech Republic born 22 April 1976 Czech Republic accepted on the recommendation of Prof. Dr. Frederic H. Allain, examiner Prof. Dr. Rudolf Glockshuber, co-examiner 2005
2 Summary Deletion of the human Y chromosome's long arm results in diseases like azoospermia and oligospermia as major causes of male infertility. Active copies of the RBMY (RNA Binding Motif) genes were localized within the AZFb region on the long arm ofthe human Y chromosome. RBMY genes encode germ cell specific nuclear proteins which play an important role during germ cell development (spermatogenesis). The human RBMY protein contains an N-terminal RNA recognition motif (RRM) and ac-terminal protein-protein interaction domain consisting of repeated motifs of 37 amino acids rich in serine, arginine, glycine and tyrosine. Although the biological function ofrbmy is unknown, several findings suggest a role in pre-mrna splicing. The protein possesses an RNA binding domain and is found in subnuclear regions with high concentrations of splicing components. In addition, protein interaction studies show that the RBMY protein interacts with pre-mrna splicing regulators Tra-2ß and SR proteins. Using in vitro SELEX the consensus RNA binding sequence for the RBMY protein was identified. The solution structure ofthe complex between an 8 base pair RNA duplex capped by a CACAA pentaloop and a truncated RBMY protein containing only the RRM domain was determined by NMR spectroscopy. The RRM domain of RBMY has a typical ßaßßaß topology and forms a four-stranded ß-sheet packed against two u-helices. A large part of the protein surface interacts with the RNA. The CACAA pentaloop is contacted by the ß-sheet and several additional residues carboxy-terminal to the ß-sheet in a manner which is common for RRM domains. However, the structure reveals a previously unknown type of interaction. The loop connecting ß-strands 2 and 3 is insertcd into the major groove of the RNA stern. This structure thus
3 constitutes the first example of an RRM domain binding to the major groove of double-stranded RNA.
4 Zusammenfassung Als Hauptursache für männliche Unfruchtbarkeit gelten die Krankheiten Azoospermia und Oligospermia. Diese werden verursacht durch Deletion des langen Armes des menschlichen Y Chromosoms. Auf dem langen Arm des Y Chromosoms befinden sich aktive Kopien der RBMY ("RNA Binding Motif") Gene, die keimzellspezifische Nukleoproteine kodieren, welche eine wichtige Rolle in der Keimzellentwicklung (Spermatogenese) spielen. Das RBMY-Protein des Menschen besteht aus zwei Domänen. Auf eine N-terminale RNA-bindende Domäne ("RNA Recognition Motif", RRM) folgt eine C-terminale Protein-Protein-Wechselwirkungsdomäne, mit einem sich wiederholenden, aus 37 Aminosäuren bestehenden Motif reich an Serin, Arginin, Glycin und Tyrosin. Obwohl die biologische Funktion von RBMY nicht bekannt ist, gibt es mehrere Hinweise auf eine Beteiligung des Proteins am prä-mrna Spleissprozess. RBMY besitzt eine RNA-bindende Domäne und tritt in subnuklearen Regionen mit hohen Konzentration an Spleisskompononten auf. Zudem konnte gezeigt werden, dass RBMY mit Proteinen, die den Spleissprozess regulieren, den SR Proteinen und Tra-2ß, interagiert. Mittels in vivo SELEX wurde die RNA Konsensussequenz für RBMY ermittelt. Die Lösungsstruktur des Komplexes zwischen der RRM-Domäne des RBMY Proteins und einem aus 8 Basenpaaren bestehenden RNA Stamm, der durch eine Schleife aus 5 Basen abgeschlossen wird, wurde mittels NMRspektroskopischen Methoden aufgeklärt. Die RRM-Domäne von RBMY besitzt eine typische ßaßßaß Topologie und bildet ein viersträngiges ß-Faltblatt mit zwei anliegenden a-helices. Ein grosser Bereich der Proteinoberfläche interagiert mit der RNA. Auf für RRM-Domänen typische Weise binden das ß Faltblatt und einige C-terminal zum Faltblatt gelegene Aminosäurereste die
5 RNA Schleife. Es wurde jedoch ebenfalls eme bis anhin unbekannte Bindungsart beobachtet. Die Bindung der Proteinschleife zwischen den ß Strängen 2 und 3 erfolgt in der Hauptfurche der RNA. Die in dieser Dissertation beschriebene Struktur stellt somit das erste Beispiel einer mit der RNA Hauptfurche interagierenden RRM-Domäne dar.
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