Three dimensional structure and interaction with a-amylase from Tenebrio molitor
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- Irmela Becker
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1 Diss. ETH Nr The bifunctional a-amylase/trypsin inhibitor from Ragi: Three dimensional structure and interaction with a-amylase from Tenebrio molitor A dissertation submitted to the Swiss Federal Institute of Technology Zurich for the degree of Doctor of Natural Science presented by Stefan Strobl Dipl. Biol. (Universitat Regensburg, Germany) born on March 30, 1966 Federal Republic of Germany accepted on the recommendation of: Prof. Dr. Rudi Glockshuber, examiner Prof. Dr. Kurt Wuthrich, co-examiner 1997
2 Abstract The structural characterization of the interactions between the bifunctional a-amylase/trypsin inhibitor from Ragi (Eleusine coracana Gaertneri) (RBI) and its target enzymes was the topic of this work. RBI represents the prototype of a relatively new class of plant a-amylase and trypsin inhibitors. The monomeric inhibitor consists of 122 amino acids and is stabilized by 5 intramolecular disulfide bonds. RBI is the only known member of the cereal inhibitor family with both inhibitory functions. In the first part of the thesis, the three-dimensional structure of recombinant RBI was determined with NMR-spectroscopy. RBI possesses an hitherto unknown fold of serine protease inhibitors. It contains four a-helices with "up-and-down" topology and a two-stranded antiparallel (3-sheet, inserted between the third and the fourth a-helix. The conformation of the trypsin binding loop in RBI is identical to the canonical conformation observed for most serine proteinase inhibitors with known three-dimensional structure. However, neither the sequence comparison with related a-amylase inhibitors, nor the known structures of RBI and eukaryotic and bacterial a-amylases allowed an unambiguous identification of the binding site for a-amylase. For a further structural characterization of the interaction between RBI and a-amylases, a RBI/a-amylase complex had to be crystallized. The a-amylase of choice proved to be the enzyme from the larvae of Tenebrio molitor (TMA), the yellow meal worm. A five-step protocol was established to purify the enzyme to homogeneity from a crude larval extract. After enzymatic removal of the N-terminal 5-oxo-proline, the following 17 residues were determined by Edman degradation, which allowed the cloning of the complete cdna of the enzyme. TMA is a monomer of 471 amino acids, contains 4 disulfide bonds and has a calculated isoelectric point of 4.3. TMA was both crystallized as free enzyme and in complex with RBI. The X-ray structure of free TMA was solved to 1.64 A resolution by molecular replacement using the coordinates of porcine pancreatic a-amylase. TMA consists of three domains and has specific binding sites for a chloride and a calcium ion. The A domain (residues 1-97 and ) contains a (p7a)8-barrel-fold and carries the catalytic residues (Asp185, Glu222, and Asp287), as well as the residues involved in chloride binding. The anion presumably serves as allosteric activator of catalysis. Domain B (residues ) consists of several extended secondary structure elements and a short
3 a-helix. It provides the residues involved in calcium binding. The cation is of fundamental importance for the structural integrity of the enzyme. Domain C (residues ) has a p-sandwich structure with greek-key topology. Its strong interactions with the A domain may be important for the thermodynamic stability of the enzyme. The substrate binding site lies in a V-shaped groove at the interface between domain A and B. Residues from both domains form six subsites which bind the oligosaccharide substrate. Cleavage of the a-1,4-glycosyl bond is performed between the third and the fourth bound pyranose ring. The X-ray structure of the complex between RBI and TMA was solved by molecular replacement to 2.5 A resolution using the coordinates of free TMA and RBI. The structure reveals a completely new inhibition mode of a-amylases by proteinaceous inhibitors. The complex is stabilized by extensive interactions between the two proteins within a contact area of 1240 A2. Residues 1 to 11 and 52 to 55 of RBI comprise an arrowheadshaped segment which occupies the active site cleft of TMA. All functional groups of the N-terminal serine residue of RBI are involved in direct or watermediated hydrogen bonds with the three catalytic residues of TMA. Apart from the interactions in the active-site groove of TMA, the complex is further stabilized by numerous hydrogen bonds and hydrophobic interactions between RBI and the B domain of TMA. The binding sites for a-amylase and trypsin are located on opposite sides of RBI and are completely independent. This was confirmed by modelling of the ternary trypsin/rbi/tma complex. Since RBI simultaneously inhibits two important digestive enzymes of animals, it constitutes an efficient plant defense protein. Therefore, the elucidated three-dimensional structures of RBI, TMA and the RBI/TMA complex are of potential interest for phytopharmacy. In particular, they should allow the rational design of specific inhibitors against insect a-amylases.
4 Kurzfassung Gegenstand der vorliegenden Arbeit war es, den bifunktionalen a-amylase/trypsininhibitor aus Ragi (Eleusine coracana Gaertneri) (RBI) in Hinblick auf die strukturellen Wechselwirkungen mit seinen Zielenzymen zu charakterisieren. RBI stellt den Prototyp einer relativ neuen Klasse von pflanzlichen a-amylase- und Trypsininhibitoren dar. Der monomere Inhibitor besteht aus 122 Aminosauren und wird durch funf intramolekulare Disulfidbrucken stabilisiert. RBI ist das einzig bekannte Mitglied der Ceralien-lnhibitorfamilie mit beiden inhibitorischen Eigenschaften. Im ersten Teil der Doktorarbeit wurde die dreidimensionale Struktur von rekombinantem RBI mittels NMR-Spektroskopie bestimmt. RBI besitzt ein bis dahin fur Serinproteaseinhibitoren unbekanntes Faltungsmotif. Es besteht aus vier a-helices mit "auf-ab"-topologie und einem zweistrangigen antiparallelen P-Faltblatt, das zwischen der dritten und der vierten Helix liegt. Die Konformation des Trypsinbindungsloops in RBI entspricht Konformation, die fur die meisten Trypsininhibitoren dreidimensionaler Struktur beobachtet wird. der kanonischen mit bekannter Die a-amylasebindungsstelle konnte weder durch Sequenzvergleich mit verwandten a-amylaseinhibitoren, noch durch die bekannten Strukturen von RBI und eukaryotischen und bakteriellen a-amylasen eindeutig identifiziert werden. Die strukturelle Charakterisierung der Wechselwirkungen zwischen RBI und a-amylasen erforderte die Kristallisation eines RBI/a-Amylase- Komplexes. Die a-amylase aus der Larve von Tenebrio molitor (TMA), dem gelben Mehlwurm, erwies sich hierfur als Enzym der Wahl. Es wurde aus den Larven durch ein funfstufiges Verfahren gereinigt. Nach enzymatischer Abspaltung des N-terminalen 5-oxo-Prolins wurden die folgenden 17 Reste durch Edman-Abbau bestimmt, wodurch die Klonierung der gesamten cdna des Enzyms moglich wurde. TMA ist ein monomeres Enzym und besteht aus 471 Aminosauren, besitzt vier Disulfidbrucken und hat einen berechneten isoelektrischen Punkt von 4,3. TMA wurde sowohl in freier Form, als auch im Komplex mit RBI kristallisiert. Gelost wurde die Rontgenstruktur der freien TMA mit einer Auflosung von 1,64 A durch molekularen Ersatz mit den Koordinaten der pankreatischen Schweine-a-Amylase. TMA besteht aus drei Domanen und hat spezifische Bindungsstellen fur je ein Chlorid- und Calciumion. Domane A (Reste 1-97 und ) besitzt das Faltungsmotiv eines ((3/a)s-
5 Fasses. In Domane A liegen sowohl die katalytischen Reste (Asp185, Glu222 und Asp287), als auch die Reste, die an der Chloridbindung beteiligt sind. Das Anion dient wahrscheinlich als allosterischer Aktivator der Katalyse. Domane B (Reste ) besteht aus mehreren langgestreckten Sekundarstrukturelementen und einer kurzen a-helix. In Domane B liegen die Reste, die das Calciumion binden. Das Kation ist fur die strukturelle Integritat des Enzyms von fundamentaler Bedeutung. Domane C (Reste ) hat eine p-sandwichstruktur mit "greek-key" Topologie. Wechselwirkungen Die starken der Domane C mit der A-Domane sind wahrscheinlich wichtig fur die thermodynamische Stabilitat des Enzyms. Die Substratbindungsstelle liegt in einer V-formigen Vertiefung an der Kontaktflache zwischen den Domanen A und B. Reste beider Domanen bilden sechs Subbindungsstellen, die das Oligosaccharidsubstrat binden. Die Spaltung der a-1,4-glycosidischen Bindung erfolgt zwischen dem dritten dem vierten gebundenen Pyranosering. und Der Komplex zwischen RBI und TMA wurde durch molekularen Ersatz mit den Koordinaten der freien TMA und von RBI mit 2,5 A Auflosung gelost. Die Struktur zeigt einen vollstandig neuen Inhibitionsmechanismus fur a-amylasen durch Proteininhibitoren. Der Komplex wird durch extensive Wechselwirkungen zwischen beiden Proteinen stabilisiert. Die Kontaktflache umfasst 1240 A2. Reste 1 bis 11 und 52 bis 55 bilden ein pfeilspitzenformiges Segment, das die Rinne mit dem aktiven Zentrum der TMA besetzt. Alle funktionellen Gruppen des N-terminalen Serinrests von RBI sind an direkten oder durch Wasser vermittelten Wasserstoffbrucken mit den drei katalytisch aktiven Resten der TMA beteiligt. Abgesehen von den Wechselwirkungen in der Substratbindungsrinne wird der Komplex stoffbrucken und hydrophoben Wechselwirkungen B-Domane von TMA stabilisiert. durch eine Vielzahl von Wasser zwischen RBI und der Die Bindungsstellen fur a-amylase und Trypsin befinden sich an gegenubertiegenden Stellen in RBI und sind vollstandig voneinander unabhangig. Dies wurde durch das Modellieren des temaren Trypsin/RBI/TMA Komplexes bestatigt. Da RBI zwei wichtige tierische Verdauungsenzyme hemmt, stellt es ein effizientes pflanzliches Verteidigungsprotein dar. Deshalb konnten die aufgeklarten Strukturen von RBI, TMA und des RBI/TMA- Komplexes von Interesse fur den Pflanzenschutz sein. sie die Moglichkeit eroffnen, rational spezifische Inhibitoren gegen Insektena-Amylasen zu entwickeln. Insbesondere sollten
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