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Uetrecht Group

Dynamics of Viral Structures

Dr. Charlotte Uetrecht

Group Leader

+49 040 8998 87585
charlotte.uetrecht@cssb-hamburg.de

Home Institute

University of Siegen
www.uni-siegen.de/

Leibniz Institute for Experimental Virology (HPI)
www.hpi-hamburg.de/

We focus on assembly of norovirus particles and coronaviral replication complexes. The underlying structural dynamics are investigated by applying state-of-the-art structural mass spectrometry. Furthermore, we develop mass spectrometry techniques to improve the structural resolution and to enable single molecule imaging at X-ray free-electron lasers.

Research Projects

PREVIOUS AND CURRENT RESEARCH

Our research is highly interdisciplinary at the interface of biology and physics further developing structural mass spectrometry (MS) to answer virological questions of high relevance to human health. This is also reflected by further affiliation of the head and several group members to DESY and European XFEL.

Being mainly interested in the structure and dynamics of viral protein complexes, the research aim is to elucidate, how these complex machineries function. We focus on the replication/transcription machinery of RNA viruses, namely coronaviruses, which often exist in many different states to mediate a diverse set of functions. Moreover, we are intrigued by viral particle assembly, where the low abundant intermediates are relevant to drug development but intrinsically hard to study. This work largely focusses on noroviruses, an important human pathogen, for which preventive treatments are still lacking. In capsid assembly, single particle-like approaches are best suited to deduce structural information.

Structural MS is becoming ever more popular as it requires low sample amounts and allows for automation, hence nicely opening up opportunities for systematic investigations of structural dynamics. We use and develop MS based techniques to achieve studying coexisting states in a time-resolved manner, following complementary routes: 1) basic structural information from structural MS; 2) solution structural models from native top-down MS; and 3) gas phase high resolution structures from X-ray free-electron lasers (XFEL). In the latter two cases, our MS based systems will allow selection to look at specific transient states and involve use of the different lightsources in Hamburg including PETRA III, FLASH I/II and the European XFEL. In terms of structural MS, we have native and hydrogen/deuterium exchange (HDX) MS established in the group with multiple protocols to tackle various research questions. The two methods are complementary with native MS providing information on the dynamics of quaternary assemblies and HDX MS delivering local structural information.

Research on coronaviruses has just made it back into the spotlight. As mentioned above coronaviral non-structural proteins (nsps) change structure and function dynamically during infection mediated amongst others by post-translational modifications (PTMs). In our native top-down MS approaches, we hope to correlate structure and PTMs, which is not easily possible by other means. We are expressing nsps with the aim to assemble larger complexes. Comparing bacterial to mammalian expression systems and different viral species will provide insights how PTMs alter assembly. In native MS, enzymatic activity can be directly monitored and at the same time reveal how the complexes shuttle between assembly states as has been performed on viral protease processing of regulatory polyprotein stretches.

For noroviruses, we focus on the viral capsids and how their structure is determined and altered throughout the viral lifecycle. We are currently working mainly with virus-like particles expanding on our work on partial capsid proteins, the P dimer. Thereby, we could reveal the distinct behaviour of various isolates in native and HDX MS. Using HDX MS, we can localize structural changes in the particles upon engagement of attachment factors. This way, we hope to decipher how human noroviruses enter cells and why cell culture production is so difficult. Our work on viral capsids will also largely benefit from single particle imaging at European XFEL and the developments in the EU FET OPEN project MS SPIDOC.

A comic-book take on a virus photoshoot

‘Norovirus Superstar’ gives insights into the EU-funded MS SPIDOC project and explains how European XFEL is used in biology.

© 2021 Véro Mischitz | MS SPIDOC, CC BY ND 4.0 doi:10.22003/XFEL.EU-COMIC-2021-001-EN

Download the comic from https://xfel.tind.io/record/2561

FUTURE PROJECTS AND GOALS

In order to gain in depth understanding of the viral lifecycle, we want to expand from in vitro assembly of protein complexes and viral particles to more holistic approaches. Therefore, we will move to intact murine and human noroviruses as well as looking at endogenous coronaviral complexes from infected cells.

Research Team

17

Group Leader

Dr. Charlotte Uetrecht
Phone:+49 40 8998 87585

E-Mail

PhD Student

Lara Flacht
Phone:+49 40 8998 87558

E-Mail

PhD Student

Alice Grün

Masters Student

Tobias Lichtenberg

Postdoctoral Scientist

Dr. Alan Kádek

Postdoctoral Scientist

Dr. Thomas Kierspel

Staff Scientist

Dr. Knut Kölbel

PhD Student

Janine-Denise Kopicki

Postdoctoral Scientist

Dr. Boris Krichel

Research Technician

Jürgen Müller-Guhl

Masters Student

Sarah Nentwich

PhD Student

Ronja Pogan

PhD Student

Sänger, Lennart

PhD Student

Kira Schamoni-Kast

PhD Student

Lars Thiede

Masters Student

Sibel Toker

EU Project Coordinator

Silvia Wissel

Publications

2021

Yan H, Lockhauserbäumer J, Szekeres GP, Mallagaray A, Creutznacher R, Taube S, Peters T, Pagel K, Uetrecht C (2021) Protein Secondary Structure Affects Glycan Clustering in Native Mass Spectrometry. Life (Basel). 11(6). doi: 10.3390/life11060554.

Günther S, Reinke PYA, Fernández-García Y, Lieske J, Lane TJ, Ginn HM, Koua FHM, Ehrt C, Ewert W, Oberthuer D, Yefanov O, Meier S, Lorenzen K, Krichel B, Kopicki JD, Gelisio L, Brehm W, Dunkel I, Seychell B, Gieseler H, Norton-Baker B, Escudero-Pérez B, Domaracky M, Saouane S, Tolstikova A, White TA, Hänle A, Groessler M, Fleckenstein H, Trost F, Galchenkova M, Gevorkov Y, Li C, Awel S, Peck A, Barthelmess M, Schlünzen F, Lourdu Xavier P, Werner N, Andaleeb H, Ullah N, Falke S, Srinivasan V, França BA, Schwinzer M, Brognaro H, Rogers C, Melo D, Zaitseva-Doyle JJ, Knoska J, Peña-Murillo GE, Mashhour AR, Hennicke V, Fischer P, Hakanpää J, Meyer J, Gribbon P, Ellinger B, Kuzikov M, Wolf M, Beccari AR, Bourenkov G, von Stetten D, Pompidor G, Bento I, Panneerselvam S, Karpics I, Schneider TR, Garcia-Alai MM, Niebling S, Günther C, Schmidt C, Schubert R, Han H, Boger J, Monteiro DCF, Zhang L, Sun X, Pletzer-Zelgert J, Wollenhaupt J, Feiler CG, Weiss MS, Schulz EC, Mehrabi P, Karničar K, Usenik A, Loboda J, Tidow H, Chari A, Hilgenfeld R, Uetrecht C, Cox R, Zaliani A, Beck T, Rarey M, Günther S, Turk D, Hinrichs W, Chapman HN, Pearson AR, Betzel C, Meents A (2021) X-ray screening identifies active site and allosteric inhibitors of SARS-CoV-2 main protease. Science. 372(6542):642-646. doi: 10.1126/science.abf7945.

Simanjuntak Y, Schamoni-Kast K, Grün A, Uetrecht C, Scaturro P (2021) Top-Down and Bottom-Up Proteomics Methods to Study RNA Virus Biology. Viruses.13(4). doi: 10.3390/v13040668.

Dülfer J, Yan H, Brodmerkel MN, Creutznacher R, Mallagaray A, Peters T, Caleman C, Marklund EG, Uetrecht C (2021) Glycan-Induced Protein Dynamics in Human Norovirus P Dimers Depend on Virus Strain and Deamidation Status. Molecules. 26(8). doi: 10.3390/molecules26082125.

Krichel B, Bylapudi G, Schmidt C, Blanchet C, Schubert R, Brings L, Koehler M, Zenobi R, Svergun D, Lorenzen K, Madhugiri R, Ziebuhr J, Uetrecht C (2021) Hallmarks of Alpha- and Betacoronavirus non-structural protein 7+8 complexes. Sci Adv. 7(10). doi: 10.1126/sciadv.abf1004.

Han H, Round E, Schubert R, Gül Y, Makroczyová J, Meza D, Heuser P, Aepfelbacher M, Barák I, Betzel C, Fromme P, Kursula I, Nissen P, Tereschenko E, Schulz J, Uetrecht C, Ulicný J, Wilmanns M, Hajdu J, Lamzin VS, Lorenzen K (2021) The XBI BioLab for life science experiments at the European XFEL. J Appl Crystallogr. 54(Pt 1):7-21. doi: 10.1107/S1600576720013989.

2020

Schulz EC, Henderson SR, Illarionov B, Crosskey T, Southall SM, Krichel B, Uetrecht C, Fischer M, Wilmanns M (2020) The crystal structure of mycobacterial epoxide hydrolase A. Sci Rep. 2020 Oct 6;10(1):16539. doi: 10.1038/s41598-020-73452-y.

Sobolev E, Zolotarev S, Giewekemeyer K, Bielecki J, Okamoto K, Reddy H, Andreasson J, Ayyer K, Barak I, Bari S, Barty A, Bean R, Bobkov S, Chapman H, Chojnowski G, Daurer B, Dörner K, Ekeberg T, Flückiger L, Galzitskaya O, Gelisio L, Hauf S, Hogue B, Horke D, Hosseinizadeh A, Ilyin V, Jung C, Kim C, Kim Y, Kirian R, Kirkwood H, Kulyk O, Küpper J, Letrun R, Loh N, Lorenzen K, Messerschmidt M, Mühlig K, Ourmazd A, Raab N, Rode A, Rose M, Round A, Sato T, Schubert R, Schwander P, Sellberg J, Sikorski M, Silenzi A, Song C, Spence J, Stern S, Sztuk-Dambietz J, Teslyuk A, Timneanu N, Trebbin M, Uetrecht C, Weinhausen B, Williams G, Xavier P, Xu C, Vartanyants I, Lamzin V, Mancuso A, Maia F (2020) Megahertz single-particle imaging at the European XFEL. Communications Physics. 3(1): doi: 10.1038/s42005-020-0362-y.

Günther S, Reinke P, Oberthuer D, Yefanov O, Ginn H, Meier S, Lane T, Lorenzen K, Gelisio L, Brehm W, Dunkel I, Domaracky M, Saouane S, Lieske J, Ehrt C, Koua F, Tolstikova A, White T, Groessler M, Fleckenstein H, Trost F, Galchenkova M, Gevorkov Y, Li C, Awel S, Peck A, Xavier P, Barthelmess M, Schlünzen F, Werner N, Andaleeb H, Ullah N, Falke S, Franca B, Schwinzer M, Brognaro H, Seychell B, Gieseler H, Melo D, Zaitsev-Doyle J, Norton-Baker B, Knoska J, Esperanza G, Mashhour A, Guicking F, Hennicke V, Fischer P, Rogers C, Monteiro D, Hakanpää J, Meyer J, Noei H, Gribbon P, Ellinger B, Kuzikov M, Wolf M, Zhang L, Sun X, Pletzer-Zelgert J, Wollenhaupt J, Feiler C, Weiss M, Schulz E, Mehrabi P, Schmidt C, Schubert R, Han H, Krichel B, Fernández-García Y, Escudero-Pérez B, Günther S, Turk D, Uetrecht C, Beck T, Tidow H, Chari A, Zaliani A, Rarey M, Cox R, Hilgenfeld R, Chapman H, Pearson A, Betzel C, Meents A (2020) Catalytic cleavage of HEAT and subsequent covalent binding of the tetralone moiety by the SARS-CoV-2 main protease. bioRxiv. doi: 10.1101/2020.05.02.043554.

Horstmann JA, Lunelli M, Cazzola H, Heidemann J, Kühne C, Steffen P, Szefs S, Rossi C, Lokareddy RK, Wang C, Lemaire L, Hughes KT, Uetrecht C, Schlüter H, Grassl GA, Stradal TEB, Rossez Y, Kolbe M, Erhardt M (2020) Methylation of Salmonella Typhimurium flagella promotes bacterial adhesion and host cell invasion. Nat Commun. 11(1):2013. doi: 10.1038/s41467-020-15738-3.

Krichel B, Falke S, Hilgenfeld R, Redecke L, Uetrecht C (2020) Processing of the SARS-CoV pp1a/ab nsp7-10 region. Biochem J. 477(5):1009-1019. doi: 10.1042/BCJ20200029.

Anjanappa R, Garcia-Alai M, Kopicki JD, Lockhauserbäumer J, Aboelmagd M, Hinrichs J, Nemtanu IM, Uetrecht C, Zacharias M, Springer S, Meijers R (2020) Structures of peptide-free and partially loaded MHC class I molecules reveal mechanisms of peptide selection. Nat Commun. 11(1):1314. doi: 10.1038/s41467-020-14862-4.

Heidemann J, Kölbel K, Konijnenberg A, Van Dyck J, Garcia-Alai M, Meijers R, Sobott F, Uetrecht C (2020) Further insights from structural mass spectrometry into endocytosis adaptor protein assemblies. International Journal of Mass Spectrometry. 447:116240-. doi: 10.1016/j.ijms.2019.116240.

2019

Bernal I, Römermann J, Flacht L, Lunelli M, Uetrecht C, Kolbe M (2019) Structural analysis of ligand-bound states of the Salmonella type III secretion system ATPase InvC. Protein Sci. 28(10):1888-1901. doi: 10.1002/pro.3704.

Bernal I, Börnicke J, Heidemann J, Svergun D, Horstmann JA, Erhardt M, Tuukkanen A, Uetrecht C, Kolbe M (2019) Molecular Organization of Soluble Type III Secretion System Sorting Platform Complexes. J Mol Biol. 431(19):3787-3803. doi: 10.1016/j.jmb.2019.07.004.

Weiss VU, Pogan R, Zoratto S, Bond KM, Boulanger P, Jarrold MF, Lyktey N, Pahl D, Puffler N, Schelhaas M, Selivanovitch E, Uetrecht C, Allmaier G (2019) Virus-like particle size and molecular weight/mass determination applying gas-phase electrophoresis (native nES GEMMA). Anal Bioanal Chem. 411(23):5951-5962. doi: 10.1007/s00216-019-01998-6.

Dülfer J, Kadek A, Kopicki JD, Krichel B, Uetrecht C (2019) Structural mass spectrometry goes viral. Adv Virus Res. 105:189-238. doi: 10.1016/bs.aivir.2019.07.003.

Kesgin-Schaefer S, Heidemann J, Puchert A, Koelbel K, Yorke BA, Huse N, Pearson AR, Uetrecht C, Tidow H (2019) Crystal structure of a domain-swapped photoactivatable sfGFP variant provides evidence for GFP folding pathway. FEBS J. 286(12):2329-2340. doi: 10.1111/febs.14797

Uetrecht C, Lorenzen K, Kitel M, Heidemann J, Robinson Spencer JH, Schlüter H, Schulz J (2019) Native mass spectrometry provides sufficient ion flux for XFEL single-particle imaging. J Synchrotron Radiat. 26(Pt 3):653-659. doi: 10.1107/S1600577519002686.

Mallagaray A, Creutznacher R, Dülfer J, Mayer PHO, Grimm LL, Orduña JM, Trabjerg E, Stehle T, Rand KD, Blaum BS, Uetrecht C, Peters T (2019) A post-translational modification of human Norovirus capsid protein attenuates glycan binding. Nat Commun. 10(1):1320. doi: 10.1038/s41467-019-09251-5.

Zaitsev-Doyle J, Puchert A, Pfeifer Y, Yan H, Yorke B, Müller-Werkmeister H, Uetrecht C, Rehbein J, Huse N, Pearson A, Sans M (2019) Synthesis and characterisation of α-carboxynitrobenzyl photocaged l -aspartates for applications in time-resolved structural biology. RSC Advances. 9(15):8695-8699. doi: 10.1039/C9RA00968J.

2018

Holm T, Kopicki JD, Busch C, Olschewski S, Rosenthal M, Uetrecht C, Günther S, Reindl S (2018) Biochemical and structural studies reveal differences and commonalities among cap-snatching endonucleases from segmented negative-strand RNA viruses. J Biol Chem. 293(51):19686-19698. doi: 10.1074/jbc.RA118.004373.

Nitsche J, Josts I, Heidemann J, Mertens HD, Maric S, Moulin M, Haertlein M, Busch S, Forsyth VT, Svergun DI, Uetrecht C, Tidow H (2018) Structural basis for activation of plasma-membrane Ca2+-ATPase by calmodulin. Commun Biol. 1:206. doi: 10.1038/s42003-018-0203-7.

Bücher KS, Yan H, Creutznacher R, Ruoff K, Mallagaray A, Grafmüller A, Dirks JS, Kilic T, Weickert S, Rubailo A, Drescher M, Schmidt S, Hansman G, Peters T, Uetrecht C, Hartmann L (2018) Fucose-Functionalized Precision Glycomacromolecules Targeting Human Norovirus Capsid Protein. Biomacromolecules. 19(9):3714-3724. doi: 10.1021/acs.biomac.8b00829.

Pogan R, Dülfer J, Uetrecht C (2018) Norovirus assembly and stability. Curr Opin Virol. 31:59-65. doi: 10.1016/j.coviro.2018.05.003.

Shin HC, Deterra D, Park J, Kim H, Nishikiori M, Uetrecht C, Ahlquist PG, Arbulu M, Blick RH (2018) Ultra-high mass multimer analysis of protein-1a capping domains by a silicon nanomembrane detector. J Proteomics. 175:5-11. doi: 10.1016/j.jprot.2017.11.024.

Pogan R, Schneider C, Reimer R, Hansman G, Uetrecht C (2018) Norovirus-like VP1 particles exhibit isolate dependent stability profiles. J Phys Condens Matter. 30(6):064006. doi: 10.1088/1361-648X/aaa43b.

Garcia-Alai MM, Heidemann J, Skruzny M, Gieras A, Mertens HDT, Svergun DI, Kaksonen M, Uetrecht C, Meijers R (2018) Epsin and Sla2 form assemblies through phospholipid interfaces. Nat Commun. 9(1):328. doi: 10.1038/s41467-017-02443-x

2017

Wegener H, Mallagaray Á, Schöne T, Peters T, Lockhauserbäumer J, Yan H, Uetrecht C, Hansman GS, Taube S (2017) Human norovirus GII.4(MI001) P dimer binds fucosylated and sialylated carbohydrates. Glycobiology. 27(11):1027-1037. doi: 10.1093/glycob/cwx078

2016

Szameit K, Berg K, Kruspe S, Valentini E, Magbanua E, Kwiatkowski M, Chauvot de Beauchêne I, Krichel B, Schamoni K, Uetrecht C, Svergun DI, Schlüter H, Zacharias M, Hahn U (2016) Structure and target interaction of a G-quadruplex RNA-aptamer. RNA Biol. 13(10):973-987. doi: 10.1080/15476286.2016.1212151.

Snijder J, Kononova O, Barbu IM, Uetrecht C, Rurup WF, Burnley RJ, Koay MS, Cornelissen JJ, Roos WH, Barsegov V, Wuite GJ, Heck AJ (2016) Assembly and Mechanical Properties of the Cargo-Free and Cargo-Loaded Bacterial Nanocompartment Encapsulin. Biomacromolecules. 17(8):2522-9. doi: 10.1021/acs.biomac.6b00469.

Hantke MF, Hasse D, Ekeberg T, John K, Svenda M, Loh D, Martin AV, Timneanu N, Larsson DS, van der Schot G, Carlsson GH, Ingelman M, Andreasson J, Westphal D, Iwan B, Uetrecht C, Bielecki J, Liang M, Stellato F, DePonte DP, Bari S, Hartmann R, Kimmel N, Kirian RA, Seibert MM, Mühlig K, Schorb S, Ferguson K, Bostedt C, Carron S, Bozek JD, Rolles D, Rudenko A, Foucar L, Epp SW, Chapman HN, Barty A, Andersson I, Hajdu J, Maia FR (2016) A data set from flash X-ray imaging of carboxysomes. Sci Data. 3:160061. doi: 10.1038/sdata.2016.61.

Dunne M, Leicht S, Krichel B, Mertens HD, Thompson A, Krijgsveld J, Svergun DI, Gómez-Torres N, Garde S, Uetrecht C, Narbad A, Mayer MJ, Meijers R (2016) Crystal Structure of the CTP1L Endolysin Reveals How Its Activity Is Regulated by a Secondary Translation Product. J Biol Chem. 291(10):4882-93. doi: 10.1074/jbc.M115.671172.

2015

Mallagaray A, Lockhauserbäumer J, Hansman G, Uetrecht C, Peters T (2015) Attachment of norovirus to histo blood group antigens: a cooperative multistep process. Angew Chem Int Ed Engl. 54(41):12014-9. doi: 10.1002/anie.201505672.

von der Heyde A, Lockhauserbäumer J, Uetrecht C, Elleuche S (2015) A hydrolase-based reporter system to uncover the protein splicing performance of an archaeal intein. Appl Microbiol Biotechnol. 99(18):7613-24. doi: 10.1007/s00253-015-6689-8.

Skruzny M, Desfosses A, Prinz S, Dodonova SO, Gieras A, Uetrecht C, Jakobi AJ, Abella M, Hagen WJ, Schulz J, Meijers R, Rybin V, Briggs JA, Sachse C, Kaksonen M (2015) An organized co-assembly of clathrin adaptors is essential for endocytosis. Dev Cell. 33(2):150-62. doi: 10.1016/j.devcel.2015.02.023.

2013

Tseng YH, Uetrecht C, Yang SC, Barendregt A, Heck AJ, Peng WP (2013) Game-theory-based search engine to automate the mass assignment in complex native electrospray mass spectra. Anal Chem. 85(23):11275-83. doi: 10.1021/ac401940e.

Snijder J, Uetrecht C, Rose RJ, Sanchez-Eugenia R, Marti GA, Agirre J, Guérin DM, Wuite GJ, Heck AJ, Roos WH (2013) Probing the biophysical interplay between a viral genome and its capsid. Nat Chem. 5(6):502-9. doi: 10.1038/nchem.1627.

Broeker NK, Gohlke U, Müller JJ, Uetrecht C, Heinemann U, Seckler R, Barbirz S (2013) Single amino acid exchange in bacteriophage HK620 tailspike protein results in thousand-fold increase of its oligosaccharide affinity. Glycobiology. 23(1):59-68. doi: 10.1093/glycob/cws126.

Schulz J, Bari S, Buck J, Uetrecht C (2013) Sample refreshment schemes for high repetition rate FEL experiments. In: Tschentscher T, Tiedtke K, editors. SPIE Optics + Optoelectronics

2012

Zaccheus MV, Broeker NK, Lundborg M, Uetrecht C, Barbirz S, Widmalm G (2012) Structural studies of the O-antigen polysaccharide from Escherichia coli TD2158 having O18 serogroup specificity and aspects of its interaction with the tailspike endoglycosidase of the infecting bacteriophage HK620. Carbohydr Res. 357:118-25. doi: 10.1016/j.carres.2012.05.022.

2011

Baclayon M, Shoemaker GK, Uetrecht C, Crawford SE, Estes MK, Prasad BV, Heck AJ, Wuite GJ, Roos WH (2011) Prestress strengthens the shell of Norwalk virus nanoparticles. Nano Lett. 11(11):4865-9. doi: 10.1021/nl202699r.

Uetrecht C, Heck AJ (2011) Modern biomolecular mass spectrometry and its role in studying virus structure, dynamics, and assembly. Angew Chem Int Ed Engl. 50(36):8248-62. doi: 10.1002/anie.201008120.

Brasch M, de la Escosura A, Ma Y, Uetrecht C, Heck AJ, Torres T, Cornelissen JJ (2011) Encapsulation of phthalocyanine supramolecular stacks into virus-like particles. J Am Chem Soc. 133(18):6878-81. doi: 10.1021/ja110752u.

Tseng YH, Uetrecht C, Heck AJ, Peng WP (2011) Interpreting the charge state assignment in electrospray mass spectra of bioparticles. Anal Chem. 83(6):1960-8. doi: 10.1021/ac102676z.

Uetrecht C, Barbu IM, Shoemaker GK, van Duijn E, Heck AJ (2011) Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat Chem. 3(2):126-32. doi: 10.1038/nchem.947.

Karagöz GE, Duarte AM, Ippel H, Uetrecht C, Sinnige T, van Rosmalen M, Hausmann J, Heck AJ, Boelens R, Rüdiger SG (2011) N-terminal domain of human Hsp90 triggers binding to the cochaperone p23. Proc Natl Acad Sci U S A. 108(2):580-5. doi: 10.1073/pnas.1011867108.

2010

Uetrecht C, Watts NR, Stahl SJ, Wingfield PT, Steven AC, Heck AJ (2010) Subunit exchange rates in Hepatitis B virus capsids are geometry- and temperature-dependent. Phys Chem Chem Phys12(41):13368-71. doi: 10.1039/c0cp00692k.

Roos WH, Gibbons MM, Arkhipov A, Uetrecht C, Watts NR, Wingfield PT, Steven AC, Heck AJ, Schulten K, Klug WS, Wuite GJ (2010) Squeezing protein shells: how continuum elastic models, molecular dynamics simulations, and experiments coalesce at the nanoscale. Biophys J. 99(4):1175-81. doi: 10.1016/j.bpj.2010.05.033.

Fu CY, Uetrecht C, Kang S, Morais MC, Heck AJ, Walter MR, Prevelige PE Jr (2010) A docking model based on mass spectrometric and biochemical data describes phage packaging motor incorporation. Mol Cell Proteomics. 1764-73. doi: 10.1074/mcp.M900625-MCP200.

Shoemaker GK, van Duijn E, Crawford SE, Uetrecht C, Baclayon M, Roos WH, Wuite GJ, Estes MK, Prasad BV, Heck AJ (2010) Norwalk virus assembly and stability monitored by mass spectrometry. Mol Cell Proteomics. 1742-51. doi: 10.1074/mcp.M900620-MCP200.

Uetrecht C, Rose RJ, van Duijn E, Lorenzen K, Heck AJ (2010) Ion mobility mass spectrometry of proteins and protein assemblies. Chem Soc Rev. 39(5):1633-55. doi: 10.1039/b914002f.

2008

Uetrecht C, Versluis C, Watts NR, Roos WH, Wuite GJ, Wingfield PT, Steven AC, Heck AJ (2008) High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids. Proc Natl Acad Sci U S A. 105(27):9216-20. doi: 10.1073/pnas.0800406105.  

Barbirz S, Müller JJ, Uetrecht C, Clark AJ, Heinemann U, Seckler R (2008) Crystal structure of Escherichia coli phage HK620 tailspike: podoviral tailspike endoglycosidase modules are evolutionarily related. Mol Microbiol. 69(2):303-16. doi: 10.1111/j.1365-2958.2008.06311.x.

Lorenzen K, Olia AS, Uetrecht C, Cingolani G, Heck AJ (2008) Determination of stoichiometry and conformational changes in the first step of the P22 tail assembly. J Mol Biol. 379(2):385-96. doi: 10.1016/j.jmb.2008.02.017.

Uetrecht C, Versluis C, Watts NR, Wingfield PT, Steven AC, Heck AJ (2008) Stability and shape of hepatitis B virus capsids in vacuo. Angew Chem Int Ed Engl. 47(33):6247-51. doi: 10.1002/anie.200802410.