NMR studies of the structure and function of PrP C, using recombinant prion protein
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1 Diss. ETH Nr NMR studies of the structure and function of PrP C, using recombinant prion protein A dissertation submitted to the Swiss Federal Institute of Technology Zürich for the degree of Doctor of Natural Science presented by Dominikus Amadeus Lysek Master of Chemistry (The University of Edinburgh, Scotland, UK) Born on August 06, 1974 Federal Republic of Germany accepted on the recommendation of: Prof. Dr. Kurt Wüthrich, examiner Prof. Dr. Rudi Glockshuber, co-examiner 2003
2 Abstract Abstract Transmissible spongiform encephalopathies (TSE) are a group of infectious neuronal disorders, such as scrapie in sheep, bovine spongiform encephalopathy (BSE), chronic wasting disease (CWD) in cervids, and Creutzfeldt-Jakob disease (CJD) in man. The only major component identified from samples enriched in TSE infectivity so far, is a host-encoded protein, termed prion protein (PrP). The observation led to the proposition of the so-called protein-only-hypothesis. It states that the infectious agent of all TSEs consists mainly, if not entirely, of PrP Sc, an abnormal aggregated isoform of the normal cellular prion protein (PrP C ). However, it is still unclear how this conversion process correlates with the development of TSE symptoms, as even the physiological function of PrP C is still controversial. In this thesis two aspects of PrP C are investigated. One is the identification of structural features of PrP C that are important for the observed species barrier in the transmission of TSEs among various mammals. The other is the search for physiological functions, and possible protein interaction-partners of PrP C. All investigations were performed on recombinant prion protein produced in E. coli. The recombinant PrP is considered to be structurally similar, if not identical, to PrP C. In the first section, the 3-dimensional structures of the C-terminal domain with residues * of a human variant of PrP and of PrPs from several other species were solved: hprp(s170n), PrP from dog (cprp), cat (fprp), elk (eprp), and chicken (chprp). The first four structures address the question of the widely different susceptibility towards TSE among mammals. In addition, the structure of chprp( ) enabled the search for 3-dimensional epitopes that were conserved along different evolutionary lines. The above PrP-structures all possess, as expected, the same global architecture as the previously determined wild-type bovine, human, murine, and Syrian hamster prion proteins. New insights were gained from the identification of two localised conformational markers in the mammalian PrPs. These are the length and quality of the definition of helix α3, and the NMR-observability of the residues in the loop * If not otherwise indicated, the numbering of the human prion protein is used throughout the thesis
3 Abstract comprising residues Poor definition of the C-terminal part of helix 3 is characteristic for murine PrP and has now been observed also for cprp, and fprp. The NMR observability of the complete loop has so far been unique for Syrian hamster PrP, and is now also documented for hprp(s170n) and especially for eprp, which is the only prion protein structure that shows no NMR line broadening for this polypeptide segment. Furthermore, the solution structure of the C-terminal domain of chprp, and supplementary data on the turtle prion protein (tprp), permitted the identification of a three-dimensional epitope, which shows high similarity to the laminin α2 chain. This suggests that PrP C and the laminins might compete for the same receptor. This common receptor is possibly the laminin receptor. Characterisation of the full-length mature chicken prion protein (chprp(25 241)) showed that the N-terminal flexible tail does not form a folded domain. However, less flexibility was observed when compared with the mammalian PrPs. Furthermore, it was demonstrated that chprp(25 241) has the ability to form a PrP Sc -like isoform. A protocol used previously to form recombinant mammalian amyloid prion protein (PrP ram ) proved successful also with chprp. The PrP-aggregates that were obtained show similar biophysical, and biochemical characteristics as mammalian PrP Sc. In a final project the binding of mprp(90 231) to one SH3 domain of the growth factor receptor bound protein 2 (Grb2) was studied. The interaction of the C-terminal SH3 domain of Grb2 (Grb2_cSH3) with the prion protein had previously been identified through a yeast-two-hybrid screen. Here, the interaction was quantified using various spectroscopic methods. The binding site on the murine prion protein fragment was mapped to a highly conserved region consisting of residues (human numbering). The tight binding constant of K D = 5.5 µm between the two proteins can be explained by both the occurrence of prolines at positions 102 and 105, and the complementary charge distribution on the two protein surfaces. Furthermore, it was found that the mprp(90 231)-Grb2_cSH3 interaction is severely hindered if either of the two Gerstmann-Sträussler-Scheinker related mutations P102L or P105L are present. Therefore these two mutations of the prion protein could directly contribute to some of the symptoms characteristic for Gerstmann-Sträussler-Scheinker syndrome, such as ataxia, hyperphosphorylated tau deposition, and cognitive decline
4 Zusammenfassung Zusammenfassung Übertragbare spongiforme Enzephalopathien (TSEs, vom Englischen: transmissible spongiform encephalopathies) stellen eine Gruppe von infektiösen neuronalen Erkrankungen dar, zu denen Scrapie beim Schaf, die Bovine spongiforme Enzephalopathie (BSE), Chronic Wasting Disease bei Cerviden und die Creutzfeldt-Jakob Krankheit beim Menschen gehören. Die einzige bisher identifizierte Hauptkomponente des angereicherten infektiösen Materials ist das Wirt-kodierte Prionprotein (PrP). Diese Tatsache führte zum Vorschlag der sogenannten Protein-only -Hypothese. Diese besagt, dass das infektiöse Agens der TSEs hauptsächlich, wenn nicht gänzlich, aus einer abnormalen aggregierten Isoform (PrP Sc ) des normalen, zellulären Prionproteins (PrP C ) besteht. Da selbst die physiologische Funktion von PrP C immer noch unklar ist, ist es nicht bekannt, wie dieser Konversionsprozess mit den Symptomen des Verlaufs von TSEs zusammenhängt. In der vorliegenden Doktorarbeit werden zwei Aspekte von PrP C behandelt: Zum einen die Identifikation von strukturellen Aspekten des PrP C, welche für die beobachtete Spezienbarriere in der Übertragung von TSEs unter Säugern wichtig sind, zum anderen die Suche nach den physiologischen Funktionen, und möglichen Protein Bindungspartnern von PrP C. Alle Untersuchungen wurden an rekombinanten, in E. coli hergestellten Prionproteinen durchgeführt. Rekombinantes PrP wird in struktureller Hinsicht als äquivalent der zellulären Form des Prionproteins (PrP C ) erachtet. Im ersten Teil wurde die drei-dimensionale Struktur der C-terminalen Domäne der PrPs, bestehend aus den Aminosäureresten *, von verschiedenen Spezien und einer Variante des humanen PrP gelöst: humane Variante S170N (hprp(s170n)), PrP vom Hund (cprp), Katze (fprp), Hirsch (eprp) und Huhn (chprp). Mit den ersten vier Strukturen wurde versucht, Einblicke in die unterschiedliche Suszeptibilität dieser Säuger gegenüber TSE zu erlangen. Die Struktur von chprp( ) ergab die Möglichkeit zur Suche nach 3-dimensionalen Epitopen, welche während der Evolution des Prionproteins in verschiedenen Spezien konserviert wurden. * Falls nicht anders angegeben, wurde die Nummerierung für das humane Prionprotein verwendet
5 Zusammenfassung Die hier präsentierten PrP-Strukturen bestehen alle aus dem selben Aufbau, wie die zuvor gelösten Prionproteine von Mensch, Rind, Maus und syrischem Hamster. Neue Einblicke wurden durch die Identifikation von zwei Konformations-Markern in Säuger PrPs ermöglicht. Diese sind die Länge und Qualität der Helix α3, und die NMR- Beobachtbarkeit von Aminosäuere-Resten der Schlaufe bestehend aus Resten Der für das Maus-PrP charakteristische, schlecht defininierte C-terminus der Helix 3 wurde nun auch für cprp und fprp beobachtet. Die bisher nur für das Prionprotein des syrischen Hamsters beschriebene NMR-Beobachtbarkeit der kompletten Schlaufe wurde jetzt auch für hprp(s170n), und für eprp beobachtet. Letzteres ist das einzige bisher gelöste Prionprotein ist, welches für diese Region keine Linienverbreiterung in den NMR-Spektren aufweisst. Des weiteren wurde durch die Struktur der C-terminalen Domäne des chprp, in Kombination mit Daten des Schildkröten Prionproteins, ein 3-dimensionaler Epitope indentifiziert. Dieser zeigt grosse Ähnlichkeit mit der Laminin α2 Kette. Dies könnte bedeuten, dass PrP C ein kompetitiver Bindingspartner zu den Laminins sein könnte. Ein mögliches gemeinsames Zielprotein wäre der Laminin-Rezeptor. Die Charakterisierung des vollständigen Huhn Prionproteins (chprp(25 241)) zeigte, dass der N-terminale flexible Schwanz keine eigenständige globulär gefaltete Domäne darstellt. Trotzdem zeigt er weniger Flexibilität im Vergleich mit dem N- terminalen Schwanz von Säuger Prionproteinen. Weiterhin wurde gezeigt, dass chprp(25 241) die Möglichkeit besitzt, eine PrP Sc -ähnliche Form einzunehmen. Das Protokoll für die Herstellung von recombinantem amyloiden Prionprotein (PrP ram ) wurde erfolgreich angewandt. Die dabei hergestellten PrP-Aggregate wiesen biophysikalische und biochemische Ähnlichkeiten zu PrP Sc auf. In dem abschliessenden Projekt wurde die Bindung vom murinen PrP fragment mprp(90 231) zur C-terminalen SH3 domäne des Growth Factor Receptor Bound Protein 2 (Grb2_cSH3) untersucht. Ursprünglich wurde die Wechselwirkung zwischen der Grb2 und dem Prionprotein durch ein Yeast-two-Hybrid System beobachtet. Hier wurde nun diese Wechselwirkung mit verschiedenen Spektroskopiearten quantifiziert. Es wurde festgestellt, dass die Bindungsstelle für die SH3 Domäne auf dem Prionprotein aus den Resten besteht und in verschiedenen Prionproteinen konserviert ist. Die starke Bindungskonstante von K D = 5,5 µm zwischen den Bindungspartnern kann durch die beiden Proline in Position - 8 -
6 Zusammenfassung 102 und 105 und die entgegengesetzten Ladungen auf den Proteinoberflächen erklärt werden. Dazu kommt, dass die Wechselwirkung zwischen den zwei Proteinfragmenten durch die Einführung von zwei Mutationen (P102L oder P105L), welche mit Gerstmann-Sträussler-Scheinker-Syndrom (GSS) in Verbindung gebracht werden, stark behindert wird. Dies wirft die Vermutung auf, dass diese zwei Mutationen des Prionproteingens (Prnp) der Ursprung für einige der charakteristischen GSS Sympthome wie Ataxia, hyperphosphorilierte Tau- Ablagerungen, oder Gedächtnisschwund sind
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