EXC 115:  Macromolecular Complexes

• Subject Area: Basic Research in Biology and Medicine
• Term: from 2006 to 2019
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 24286296

• Final Report Year: 2020

Final Report Abstract

The Cluster of Excellence Frankfurt “Macromolecular Complexes” (CEF) was established in 2006 by Goethe University together with the Max Planck Institutes of Biophysics and Brain Research. CEF grew out of the long-standing collaborative research on membrane proteins and RNA molecules. CEF strengthened research efforts in these fields by recruiting further excellent scientists to Frankfurt. Following a successful proposal to the Wissenschaftsrat for a new research building, CEF founded the Buchmann Institute for Molecular Life Sciences (BMLS), a state-of-theart research facility which houses research groups from four faculties of the University. CEF enhanced the technological infrastructure in Frankfurt by purchasing new instrumentation. The Frankfurt Center for Advanced Light Microscopy and the Frankfurt Center for Electron Microscopy are both located in the BMLS and were established by scientists recruited by CEF. The Cluster promoted scientific exchange through a range of programmes as well as through workshops, international conferences, lecture series and faculty dinners. CEF scientists published more than 2600 original research publications (incl. 479 research papers in journals with an impact factor of ≥10) during the Cluster’s lifetime. Important structures of macromolecular complexes have been determined in CEF. Examples for important membrane complexes include the atomic structures of complex I and the ATP synthase of the mitochondrial respiratory chain and of the antigen translocation complex TAP. Research on RNA structure and function led to the definition of regulatory principles of temperature sensing riboswitches, the structure-function relationship of RNA polymerase I, the functions of microRNAs and the mechanisms of rRNA maturation and downstream processes during ribosome biogenesis and recycling. For instance, CEF scientists identified the receptors of ubiquitin chains on the proteasome, deciphered the role of linear ubiquitin chains and described macromolecules regulating mitophagy, xenophagy and ER-phagy. They delineated the role of sumoylation in ribosome quality control and characterized the process of genetic quality control in oocytes. The efforts in these three research areas were accompanied by approaches to design or reprogram macromolecular complexes and new methods developed to expand the already strong expertise. CEF scientists established and advanced the principles of optogenetics as well as biochemical methods for light regulation. They also developed biophysical techniques for the structural and functional characterization of macromolecules. Example include light-switchable molecules designed for in-cell applications and time-resolved techniques to study RNA folding. Light sheet microscopy for the observation of development and LILBID mass spectrometry for the analysis of membrane complexes was improved. PELDOR-EPR was developed to a resolution that allows in-cell measurements.

Link to the final report

https://dx.doi.org/10.2314/GBV:1696608775

Publications

• (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639
  Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A, Deisseroth K
  (See online at https://doi.org/10.1038/nature05744)
• (2007) Native protein nanolithography that can write, read and erase. Nat Nanotechnol 2: 220-225
  Tinazli A, Piehler J, Beuttler M, Guckenberger R, Tampé R
  (See online at https://doi.org/10.1038/nnano.2007.63)
• (2008) 4-Chloro-α-cyanocinnamic acid is an advanced, rationally designed MALDI matrix. P Natl Acad Sci USA 105: 12200-12205
  Jaskolla TW, Lehmann WD, Karas M
  (See online at https://doi.org/10.1073/pnas.0803056105)
• (2008) Optogenetic analysis of synaptic function. Nat Methods 5: 895 - 902
  Liewald JF, Brauner M, Stephens GJ, Bouhours M, Schultheis C, Zhen M, Gottschalk A
  (See online at https://doi.org/10.1038/nmeth.1252)
• (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453: 481-488
  Husnjak K, Elsasser S, Zhang NX, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I
  (See online at https://doi.org/10.1038/nature06926)
• (2008) Serine phosphorylation of ephrinB2 regulates trafficking of synaptic AMPA receptors. Nat Neurosci 11: 1035-1043
  Essmann CL, Martinez E, Geiger JC, Zimmer M, Traut MH, Stein V, Klein R, Acker-Palmer A
  (See online at https://doi.org/10.1038/nn.2171)
• (2008) Structural basis for the selectivity of the external thioesterase of the surfactin synthetase. Nature 454: 907-911
  Koglin A, Löhr F, Bernhard F, Rogov VV, Frueh DP, Strieter ER, Mofid MR, Güntert P, Wagner G, Walsh CT, Marahiel MA, Dötsch V
  (See online at https://doi.org/10.1038/nature07161)
• (2008) The oxazolidinone antibiotics perturb the ribosomal peptidyl-transferase center and effect tRNA positioning. P Natl Acad Sci USA 105: 13339-13344
  Wilson DN, Schluenzen F, Harms JM, Starosta AL, Connell SR, Fucini P
  (See online at https://doi.org/10.1073/pnas.0804276105)
• (2008) The structure of the neuropeptide bradykinin bound to the human G-protein coupled receptor bradykinin B2 as determined by solid-state NMR spectroscopy. Angew Chem Int Edit 47: 1668-1671
  Lopez JJ, Shukla AK, Reinhart C, Schwalbe H, Michel H, Glaubitz C
  (See online at https://doi.org/10.1002/anie.200704282)
• (2008) Translational regulation via L11: molecular switches on the ribosome turned on and off by thiostrepton and micrococcin. Mol Cell 30: 26-38
  Harms JM, Wilson DN, Schluenzen F, Connell SR, Stachelhaus T, Zaborowska Z, Spahn CMT, Fucini P
  (See online at https://doi.org/10.1016/j.molcel.2008.01.009)
• (2008) Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 453: 548-552
  Schreiner P, Chen X, Husnjak K, Randles L, Zhang NX, Elsasser S, Finley D, Dikic I, Walters KJ, Groll M
  (See online at https://doi.org/10.1038/nature06924)
• (2009) Channelrhodopsin-2 is a leaky proton pump. P Natl Acad Sci USA 106: 12317-12322
  Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E
  (See online at https://doi.org/10.1073/pnas.0905852106)
• (2009) High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol 16: 1068-1073
  Pogoryelov D, Yildiz Ö, Faraldo-Gómez JD, Meier T
  (See online at https://doi.org/10.1038/nsmb.1678)
• (2009) Increasing organismal healthspan by enhancing mitochondrial protein quality control. Nat Cell Biol 11: 852-858
  Luce K, Osiewacz HD
  (See online at https://doi.org/10.1038/ncb1893)
• (2009) Molecular basis of transport and regulation in the Na+/betaine symporter BetP. Nature 458: 47-U1
  Ressl S, van Scheltinga ACT, Vonrhein C, Ott V, Ziegler C
  (See online at https://doi.org/10.1038/nature07819)
• (2009) Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol Cell 36: 583-592
  Bohnsack MT, Martin R, Granneman S, Ruprecht M, Schleiff E, Tollervey D
  (See online at https://doi.org/10.1016/j.molcel.2009.09.039)
• (2009) Specific recognition of linear ubiquitin chains by NEMO is important for NF-κB activation p1098. Cell 136: 1098-1109
  Rahighi S, Ikeda F, Kawasaki M, Akutsu M, Suzuki N, Kato R, Kensche T, Uejima T, Bloor S, Komander D, Randow F, Wakatsuki S, Dikic I
  (See online at https://doi.org/10.1016/j.cell.2009.03.007)
• (2010) Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis. Nature 465: 487-491
  Sawamiphak S, Seidel S, Essmann CL, Wilkinson GA, Pitulescu ME, Acker T, Acker-Palmer A
  (See online at https://doi.org/10.1038/nature08995)
• (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329: 448-451
  Hunte C, Zickermann V, Brandt U
  (See online at https://doi.org/10.1126/science.1191046)
• (2010) High-resolution studies of uniformly 13C,15N- labeled RNA by solid-state NMR spectroscopy. Angew Chem Int Edit 49: 4747-4750
  Cherepanov AV, Glaubitz C, Schwalbe H
  (See online at https://doi.org/10.1002/anie.200906885)
• (2010) Microscopic rotary mechanism of ion translocation in the F0 complex of ATP synthases. Nat Chem Biol 6: 891-899
  Pogoryelov D, Krah A, Langer JD, Yildiz Ö, Faraldo-Gómez JD, Meier T
  (See online at https://doi.org/10.1038/nchembio.457)
• (2010) Regulation of translesion synthesis DNA polymerase η by monoubiquitination. Mol Cell 37: 396-407
  Bienko M, Green CM, Sabbioneda S, Crosetto N, Matic I, Hibbert RG, Begovic T, Niimi A, Mann M, Lehmann AR, Dikic I
  (See online at https://doi.org/10.1016/j.molcel.2009.12.039)
• (2010) Structural basis of Na+-independent and cooperative substrate/product antiport in CaiT. Nature 467: 233-U129
  Schulze S, Koster S, Geldmacher U, van Scheltinga ACT, Kühlbrandt W
  (See online at https://doi.org/10.1038/nature09310)
• (2010) The structure of cbb3 cytochrome oxidase provides insights into proton pumping. Science 329: 327-329
  Buschmann S, Warkentin E, Xie H, Langer JD, Ermler U, Michel H
  (See online at https://doi.org/10.1126/science.1187303)
• (2011) A gene-fusion strategy for stoichiometric and co-localized expression of light-gated membrane proteins. Nat Methods 8: 1083-1088
  Kleinlogel S, Terpitz U, Legrum B, Gokbuget D, Boyden ES, Bamann C, Wood PG, Bamberg E
  (See online at https://doi.org/10.1038/nmeth.1766)
• (2011) Chloroplast Omp85 proteins change orientation during evolution. P Natl Acad Sci USA 108: 13841-13846
  Sommer MS, Daum B, Gross LE, Weis BLM, Mirus O, Abram L, Maier UG, Kühlbrandt W, Schleiff E
  (See online at https://doi.org/10.1073/pnas.1108626108)
• (2011) Determination of the conformation of the 2 ' OH Group in RNA by NMR spectroscopy and DFT calculations. Angew Chem Int Edit 50: 5397-5400
  Nozinovic S, Gupta P, Fürtig B, Richter C, Tullmann S, Duchardt-Ferner E, Holthausen MC, Schwalbe H
  (See online at https://doi.org/10.1002/anie.201007844)
• (2011) DNA damage in oocytes induces a switch of the quality control factor TAp63a from dimer to tetramer. Cell 144: 566-576
  Deutsch GB, Zielonka EM, Coutandin D, Weber TA, Schäfer B, Hannewald J, Luh LM, Durst FG, Ibrahim M, Hoffmann J, Niesen FH, Sentürk A, Kunkel H, Brutschy B, Schleiff E, Knapp S, Acker- Palmer A, Grez M, McKeon F, Dötsch V
  (See online at https://doi.org/10.1016/j.cell.2011.01.013)
• (2011) Ephrin Bs are essential components of the Reelin pathway to regulate neuronal migration. Nature 472: 356-360, 478:274
  Sentürk A, Pfennig S, Weiss A, Burk K, Acker-Palmer A
  (See online at https://doi.org/10.1038/nature09874)
• (2011) Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei. P Natl Acad Sci USA 108: 16992-16997
  Scheffer MP, Eltsov M, Frangakis AS
  (See online at https://doi.org/10.1073/pnas.1108268108)
• (2011) Long-range distance measurements on nucleic acids in cells by pulsed EPR spectroscopy. Angew Chem Int Edit 50: 5070-5074
  Krstić I, Hänsel R, Romainczyk O, Engels JW, Dötsch V, Prisner TF
  (See online at https://doi.org/10.1002/anie.201100886)
• (2011) Macromolecular organization of ATP synthase and complex I in whole mitochondria. P Natl Acad Sci USA 108: 14121-14126
  Davies KM, Strauss M, Daum B, Kief JH, Osiewacz HD, Rycovska A, Zickermann V, Kühlbrandt W
  (See online at https://doi.org/10.1073/pnas.1103621108)
• (2011) Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333: 228-233
  Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C, Dötsch V, Bumann D, Dikic I
  (See online at https://doi.org/10.1126/science.1205405)
• (2011) Realtime multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat Methods 8: 153-U78
  Stirman JN, Crane MM, Husson SJ, Wabnig S, Schultheis C, Gottschalk A, Lu H
  (See online at https://doi.org/10.1038/nmeth.1555)
• (2011) SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappa B activity and apoptosis. Nature 471: 637-641
  Ikeda F, Deribe YL, Skånland SS, Stieglitz B, Grabbe C, Franz-Wachtel M, van Wijk SJL, Goswami P, Nagy V, Terzic J, Tokunaga F, Androulidaki A, Nakagawa T, Pasparakis M, Iwai K, Sundberg JP, Schaefer L, Rittinger K, Macek B, Dikic I
  (See online at https://doi.org/10.1038/nature09814)
• (2011) Solution NMR structure of proteorhodopsin. Angew Chem Int Edit 50: 11942-11946
  Reckel S, Gottstein D, Stehle J, Löhr F, Verhoefen MK, Takeda M, Silvers R, Kainosho M, Glaubitz C, Wachtveitl J, Bernhard F, Schwalbe H, Güntert P, Dötsch V
  (See online at https://doi.org/10.1002/anie.201105648)
• (2011) Structural basis for tail-anchored membrane protein biogenesis by the Get3-receptor complex. Science 333: 758-762
  Stefer S, Reitz S, Wang F, Wild K, Pang YY, Schwarz D, Bomke J, Hein C, Löhr F, Bernhard F, Denic V, Dötsch V, Sinning I
  (See online at https://doi.org/10.1126/science.1207125)
• (2011) The threedimensional molecular structure of the desmosomal plaque. P Natl Acad Sci USA 108: 6480-6485
  Al-Amoudi A, Castaño-Diez D, Devos DP, Russell RB, Johnson GT, Frangakis AS
  (See online at https://doi.org/10.1073/pnas.1019469108)
• (2011) Ultra light-sensitive and fast neuronal activation with the Ca(2+)-permeable channelrhodopsin CatCh. Nat Neurosci 14: 513-518
  Kleinlogel S, Feldbauer K, Dempski RE, Fotis H, Wood PG, Bamann C, Bamberg E
  (See online at https://doi.org/10.1038/nn.2776)
• (2012) Complexome profiling identifies TMEM126B as a component of the mitochondrial complex I assembly complex. Cell Metab 16: 538-549
  Heide H, Bleier L, Steger M, Ackermann J, Dröse S, Schwamb B, Zörnig M, Reichert AS, Koch I, Wittig I, Brandt U
  (See online at https://doi.org/10.1016/j.cmet.2012.08.009)
• (2012) Fluorescence-based sensors to monitor localization and functions of linear and K63-linked ubiquitin chains in cells. Mol Cell 47: 797-809
  van Wijk SJL, Fiskin E, Putyrski M, Pampaloni F, Hou J, Wild P, Kensche T, Grecco HE, Bastiaens P, Dikic I
  (See online at https://doi.org/10.1016/j.molcel.2012.06.017)
• (2012) Ultrafast dynamics of a spiropyran in water. J Am Chem Soc 134: 14070-14077
  Kohl-Landgraf J, Braun M, Ozcoban C, Goncalves DPN, Heckel A, Wachtveitl J
  (See online at https://doi.org/10.1021/ja304395k)
• 2012) Transport of drugs by the multidrug transporter AcrB involves an access and a deep binding pocket that are separated by a switch-loop. P Natl Acad Sci USA 109: 5687-5692
  Eicher T, Cha HJ, Seeger MA, Brandstatter L, El-Delik J, Bohnert JA, Kern WV, Verrey F, Grutter MG, Diederichs K, Pos KM
  (See online at https://doi.org/10.1073/pnas.1114944109)
• (2013) MicroRNA-34a regulates cardiac ageing and function. Nature 495: 107-110
  Boon RA, Iekushi K, Lechner S, Seeger T, Fischer A, Heydt S, Kaluza D, Tréguer K, Carmona G, Bonauer A, Horrevoets AJG, Didier N, Girmatsion Z, Biliczki P, Ehrlich JR, Katus HA, Müller OJ, Potente M, Zeiher AM, Hermeking H, Dimmeler S
  (See online at https://doi.org/10.1038/nature11919)
• (2013) Three-state mechanism couples ligand and temperature sensing in riboswitches. Nature 499: 355-U135
  Reining A, Nozinovic S, Schlepckow K, Buhr F, Fürtig B, Schwalbe H
  (See online at https://doi.org/10.1038/nature12378)
• (2015) Accessory NUMM (NDUFS6) subunit harbors a Zn-binding site and is essential for biogenesis of mitochondrial complex I. P Natl Acad Sci USA 112: 5685-5690
  Kmita K, Wirth C, Warnau J, Guerrero-Castillo S, Hunte C, Hummer G, Kaila VRI, Zwicker K, Brandt U, Zickermann V
  (See online at https://doi.org/10.1073/pnas.1424353112)
• (2015) Design of photocaged puromycin for nascent polypeptide release and spatiotemporal monitoring of translation. Angew Chem Int Edit 54: 3717-3721
  Buhr F, Kohl-Landgraf J, Dieck ST, Hanus C, Chatterjee D, Hegelein A, Schuman EM, Wachtveitl J, Schwalbe H
  (See online at https://doi.org/10.1002/anie.201410940)
• (2015) Direct visualization of newly synthesized target proteins in situ. Nat Methods 12: 411-114
  tom Dieck S, Kochen L, Hanus C, Heumüller M, Bartnik I, Nassim-Assir B, Merk K, Mosler T, Garg S, Bunse S, Tirrel DA, Schuman EM
  (See online at https://doi.org/10.1038/NMETH.3319)
• (2015) Enlightening the photoactive site of channelrhodopsin-2 by DNP-enhanced solid-state NMR spectroscopy. P Natl Acad Sci USA 112: 9896-9901
  Becker-Baldus J, Bamann C, Saxena K, Gustmann H, Brown LJ, Brown RCD, Reiter C, Bamberg E, Wachtveitl J, Schwalbe H, Glaubitz C
  (See online at https://doi.org/10.1073/pnas.1507713112)
• (2015) Horizontal membraneintrinsic alpha-helices in the stator a-subunit of an F-type ATP synthase. Nature 521: 237-240
  Allegretti M, Klusch N, Mills DJ, Vonck J, Kühlbrandt W, Davies KM
  (See online at https://doi.org/10.1038/nature14185)
• (2015) Identification and characterization of hypoxia-regulated endothelial circular RNA. Circ Res 117: 884-890
  Boeckel JN, Jae N, Heumüller AW, Chen W, Boon RA, Stellos K, Zeiher AM, John D, Uchida S, Dimmeler S
  (See online at https://doi.org/10.1161/CIRCRESAHA.115.306319)
• (2015) Influence of arrestin on the photodecay of bovine rhodopsin. Angew Chem Int Edit 54: 13555-13560
  Chatterjee D, Eckert CE, Slavov C, Saxena K, Furtig B, Sanders CR, Gurevich VV, Wachtveitl J, Schwalbe H
  (See online at https://doi.org/10.1002/anie.201505798)
• (2015) Involvement of long-lived intermediate states in the complex folding pathway of the human telomeric G-quadruplex. Angew Chem Int Edit 54: 8444-8448
  Bessi I, Jonker HRA, Richter C, Schwalbe H
  (See online at https://doi.org/10.1002/anie.201502286)
• (2015) Live imaging of Tribolium castaneum embryonic development using light-sheet-based fluorescence microscopy. Nat Protoc 10: 1486-1507
  Strobl F, Schmitz A, Stelzer EHK
  (See online at https://doi.org/10.1038/nprot.2015.093)
• (2015) Mechanistic insight from the crystal structure of mitochondrial complex I. Science 347: 44-49
  Zickermann V, Wirth C, Nasiri H, Siegmund K, Schwalbe H, Hunte C, Brandt U
  (See online at https://doi.org/10.1126/science.1259859)
• (2015) Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp. Nat Commun 6: article 8046
  Gao SQ, Nagpal J, Schneider MW, Kozjak-Pavlovic V, Nagel G, Gottschalk A
  (See online at https://doi.org/10.1038/ncomms9046)
• (2015) Quantitative analysis of cytoskeletal reorganization during epithelial tissue sealing by large-volume electron tomography. Nat Cell Biol 17: 605-U159
  Eltsov M, Dube N, Yu Z, Pasakarnis L, Haselmann-Weiss U, Brunner D, Frangakis AS
  (See online at https://doi.org/10.1038/ncb3159)
• (2015) Regulation of endoplasmic reticulum turnover by selective autophagy. Nature 522: 354-358
  Khaminets A, Heinrich T, Mari M, Grumati P, Huebner AK, Akutsu M, Liebmann L, Stolz A, Nietzsche S, Koch N, Mauthe M, Katona I, Qualmann B, Weis J, Reggiori F, Kurth I, Hübner CA, Dikic I
  (See online at https://doi.org/10.1038/nature14498)
• (2015) SLAP: Small labeling pair for single-molecule super-resolution imaging. Angew Chem Int Edit 54: 10216-10219
  Wieneke R, Raulf A, Kollmannsperger A, Heilemann M, Tampé R
  (See online at https://doi.org/10.1002/anie.201503215)
• (2015) TECPR2 cooperates with LC3C to regulate COPII-dependent er export. Mol Cell 60: 89-104
  Stadel D, Millarte V, Tillmann KD, Huber J, Tamin-Yecheskel BC, Akutsu M, Demishtein A, Ben- Zeev B, Anikster Y, Perez F, Dötsch V, Elazar Z, Rogov V, Farhan H, Behrends C
  (See online at https://doi.org/10.1016/j.molcel.2015.09.010)
• 2015) CUL3-KBTBD6/KBTBD7 ubiquitin ligase cooperates with GABARAP proteins to spatially restrict TIAM1-RAC1 signalling. Mol Cell 57: 995-1010
  Genau HM, Huber J, Baschieri F, Akutsu M, Dötsch V, Farhan H, Rogov V, Behrends C
  (See online at https://doi.org/10.1016/j.molcel.2014.12.040)
• (2016) A eukaryotic sensor for membrane lipid saturation. Mol Cell 63: 1-11
  Covino R, Ballweg S, Stordeur C, Michaelis JB, Puth K, Wernig F, Bahrami A, Ernst AM, Hummer G, Ernst R
  (See online at https://doi.org/10.1016/j.molcel.2016.05.015)
• (2016) Adenosine-to-inosine RNA editing controls cathepsin S expression in atherosclerosis by enabling HuR-mediated post-transcriptional regulation. Nat Med 22: 1140–1150
  Stellos K, Gatsiou A, Stamatelopoulos K, Perisic Matic L, John D, Lunella FF, Jae N, Rossbach O, Amrhein C, Sigala F, Boon RA, Furtig B, Manavski Y, You X, Uchida S, Keller T, Boeckel JN, Franco- Cereceda A, Maegdefessel L, Chen W, Schwalbe H, Bindereif A, Eriksson P, Hedin U, Zeiher AM, Dimmeler S
  (See online at https://doi.org/10.1038/nm.4172)
• (2016) Antigenic peptide recognition on the human ABC transporter TAP resolved by DNP-enhanced solid-state NMR spectroscopy. J Am Chem Soc 138: 13967–13974
  Lehnert E, Mao J, Mehdipour AR, Hummer G, Abele R, Glaubitz C, Tampé R
  (See online at https://doi.org/10.1021/jacs.6b07426)
• (2016) Autophagy and modular restructuring of metabolism control germline tumor differentiation and proliferation in C. elegans. Autophagy 12: 529-546
  Gomes LC, Odedra D, Dikic I, Pohl C
  (See online at https://doi.org/10.1080/15548627.2015.1136771)
• (2016) Global analysis of host and bacterial ubiquitinome in response to Salmonella Typhimurium infection. Mol Cell 62: 967-81
  Fiskin E, Bionda T, Dikic I, Behrends C
  (See online at https://doi.org/10.1016/j.molcel.2016.04.015)
• (2016) Live-cell protein labelling with nanometre precision by cell squeezing. Nat Commun 7: 10372
  Kollmannsperger A, Sharei A, Raulf A, Heilemann M, Langer R, Jensen KF, Wieneke R, Tampé R
  (See online at https://doi.org/10.1038/ncomms10372)
• (2016) Molecular basis for inhibition of AcrB multidrug efflux pump by novel and powerful pyranopyridine derivatives. P Natl Acad Sci USA 113: 3509-3514
  Sjuts H, Vargiu AV, Kwasny SM, Nguyen ST, Kim HS, Ding XY, Ornik AR, Ruggerone P, Bowlin TL, Nikaido H, Pos KM, Opperman TJ
  (See online at https://doi.org/10.1073/pnas.1602472113)
• (2016) Nascent proteome remodeling following homeostatic scaling at hippocampal synapses. Neuron 92: 358-371
  Schanzenbacher CT, Sambandan S, Langer JD, Schuman EM
  (See online at https://doi.org/10.1016/j.neuron.2016.09.058)
• (2016) Phosphoribosylation of ubiquitin promotes serine ubiquitination and impairs conventional ubiquitination. Cell 167: 1636-1649.e13
  Bhogaraju S, Kalayil S, Liu Y, Bonn F, Colby T, Matic I, Dikic I
  (See online at https://doi.org/10.1016/j.cell.2016.11.019)
• (2016) Structure of a bd oxidase indicates similar mechanisms for membraneintegrated oxygen reductases. Science 352: 583-586
  Safarian S, Rajendran C, Müller H, Preu J, Langer JD, Ovchinnikov S, Hirose T, Kusumoto T, Sakamoto J, Michel H
  (See online at https://doi.org/10.1126/science.aaf2477)
• (2016) Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology. Mol Cell 63: 445-456
  Hahn A, Parey K, Bublitz M, Mills Deryck J, Zickermann V, Vonck J, Kühlbrandt W, Meier T
  (See online at https://doi.org/10.1016/j.molcel.2016.05.037)
• (2016) Structure of RNA polymerase I transcribing ribosomal DNA genes. Nature 540: 607–610
  Neyer S, Kunz M, Geiss C, Hantsche M, Hodirnau V-V, Seybert A, Engel C, Scheffer MP, Cramer P, Frangakis AS
  (See online at https://doi.org/10.1038/nature20561)
• (2016) SuReSim: simulating localization microscopy experiments from ground truth models. Nat Meth 13: 319-321
  Venkataramani V, Herrmannsdorfer F, Heilemann M, Kuner T
  (See online at https://doi.org/10.1038/NMETH.3775)
• (2016) The CUE domain of Cue1 aligns growing ubiquitin chains with Ubc7 for rapid elongation. Mol Cell 62: 918–928
  von Delbrück M, Kniss A, Rogov VV, Pluska L, Bagola K, Löhr F, Güntert P, Sommer T, Dötsch V
  (See online at https://doi.org/10.1016/j.molcel.2016.04.031)
• (2016) Transport of lipophilic carboxylates is mediated by transmembrane helix 2 in multidrug transporter AcrB. Nat Commun 7: 10
  Oswald C, Tam HK, Pos KM
  (See online at https://doi.org/10.1038/ncomms13819)
• (2017) Activity-dependent spatially localized miRNA maturation in neuronal dendrites. Science 355: 634-637
  Sambandan S, Akbalik G, Kochen L, Rinne J, Kahlstatt J, Glock C, Tushev G, Alvarez-Castelao B, Heckel A, Schuman EM
  (See online at https://doi.org/10.1126/science.aaf8995)
• (2017) Chromophore distortions in photointermediates of proteorhodopsin visualized by dynamic nuclear polarization-enhanced solid-state NMR. J Am Chem Soc 139: 16143–16153
  Mehler M, Eckert CE, Leeder AJ, Kaur J, Fischer T, Kubatova N, Brown LJ, Brown RCD, Becker- Baldus J, Wachtveitl J, Glaubitz C
  (See online at https://doi.org/10.1021/jacs.7b05061)
• (2017) Cryo-EM structure of the TOM core complex from Neurospora crassa. Cell 170: 693-700.e7
  Bausewein T, Mills DJ, Langer JD, Nitschke B, Nussberger S, Kühlbrandt W
  (See online at https://doi.org/10.1016/j.cell.2017.07.012)
• (2017) Crystal structure and mechanistic basis of a functional homolog of the antigen transporter TAP. P Natl Acad Sci USA 114: E438–E447
  Nöll A, Thomas C, Herbring V, Zollmann T, Barth K, Mehdipour AR, Tomasiak TM, Brüchert S, Joseph B, Abele R, Oliéric V, Wang M, Diederichs K, Hummer G, Stroud RM, Pos KM, Tampé R
  (See online at https://doi.org/10.1073/pnas.1620009114)
• (2017) csiLSFM combines light-sheet fluorescence microscopy and coherent structured illumination for a lateral resolution below 100 nm. P Natl Acad Sci USA 114: 4869-4874
  Chang B-J, Perez Meza VD, Stelzer EHK
  (See online at https://doi.org/10.1073/pnas.1609278114)
• (2017) Solution NMR structure of a ligand/hybrid-2-G-quadruplex complex reveals rearrangements that affect ligand binding. Angew Chem Int Edit 56: 7102–7106
  Wirmer-Bartoschek J, Bendel LE, Jonker HRA, Grün JT, Papi F, Bazzicalupi C, Messori L, Gratteri P, Schwalbe H
  (See online at https://doi.org/10.1002/anie.201702135)
• (2017) Structure of the 40S-ABCE1 post-splitting complex in ribosome recycling and translation initiation. Nat Struct Mol Biol 24: 453–460
  Heuer A, Gerovac M, Schmidt C, Trowitzsch S, Preis A, Kotter P, Berninghausen O, Becker T, Beckmann R, Tampé R
  (See online at https://doi.org/10.1038/nsmb.3396)
• (2017) Structure of the human MHC-I peptide-loading complex. Nature 551: 525–528
  Blees A, Januliene D, Hofmann T, Koller N, Schmidt C, Trowitzsch S, Moeller A, Tampé R
  (See online at https://doi.org/10.1038/nature24627)
• 6. Helmling C, Wacker A, Wolfinger MT, Hofacker IL, Hengesbach M, Fuertig B, Schwalbe H (2017) NMR structural profiling of transcriptional intermediates reveals riboswitch regulation by metastable RNA conformations. J Am Chem Soc 139: 2647–2656
  Helmling C, Wacker A, Wolfinger MT, Hofacker IL, Hengesbach M, Fuertig B, Schwalbe H
  (See online at https://doi.org/10.1021/jacs.6b10429)
• (2018) Chemo-enzymatic synthesis of position-specifically modified RNA for biophysical studies including light control and NMR spectroscopy. Angew Chem Int Ed 57: 12017-12021
  Keyhani S, Goldau T, Blümler A, Heckel A, Schwalbe H
  (See online at https://doi.org/10.1002/anie.201807125)
• (2018) Endothelial Dab1 signalling orchestrates neuro-glia-vessel communication in the central nervous system. Science 361: eaao2861
  Segarra M, Aburto MR, Cop F, Llaó-Cid C, Härtl R, Damm M, Bethani I, Parrilla M, Husainie D, Schänzer A, Schlierbach H, Acker T, Mohr L, Torres-Masjoan L, Ritter M, Acker-Palmer A
  (See online at https://doi.org/10.1126/science.aao2861)
• (2018) Food sensation modulates locomotion by dopamine and neuropeptide signalling in a distributed neuronal network. Neuron 100: 1414-1428.e10
  Oranth A, Schultheis C, Tolstenkov O, Erbguth K, Nagpal J, Hain D, Brauner M, Wabnig S, Steuer Costa W, McWhirter RD, Zels S, Palumbos S, Miller Iii DM, Beets I, Gottschalk A
  (See online at https://doi.org/10.1016/j.neuron.2018.10.024)
• (2018) Insights into catalysis and function of phosphoribosyl-linked serine ubiquitination. Nature 557: 734-738
  Kalayil S, Bhogaraju S, Bonn F, Shin D, Liu Y, Gan N, Basquin J, Grumati P, Luo Z-Q, Dikic I
  (See online at https://doi.org/10.1038/s41586-018-0145-8)
• (2018) Locking loop movement in the ubiquinone pocket of complex I disengages the proton pumps. Nat Commun 9: 4500
  Cabrera-Orefice A, Yoga EG, Wirth C, Siegmund K, Zwicker K, Guerrero-Castillo S, Zickermann V, Hunte C, Brandt U
  (See online at https://doi.org/10.1038/s41467-018-06955-y)
• (2018) Plant-specific ribosome biogenesis factors in Arabidopsis thaliana with essential function in rRNA processing. Nucleic Acids Res 47: 1880–1895
  Palm D, Streit D, Shanmugam T, Weis BL, Ruprecht M, Simm S, Schleiff E
  (See online at https://doi.org/10.1093/nar/gky1261)
• (2018) Tris -N-nitrilotriacetic acid fluorophore as a self-healing dye for single-molecule fluorescence imaging. J Am Chem Soc 140: 11006-11012
  Glembockyte V, Wieneke R, Gatterdam K, Gidi Y, Tampé R, Cosa G
  (See online at https://doi.org/10.1021/jacs.8b04681)
• (2018) Unexplored nucleotide binding modes for the ABC exporter MsbA. J Am Chem Soc 140: 14112–14125
  Kaur H, Abreu B, Akhmetzyanov D, Lakatos-Karoly A, Soares CM, Prisner T, Glaubitz C
  (See online at https://doi.org/10.1021/jacs.8b06739)
• (2019) Active site rearrangement and structural divergence in prokaryotic respiratory oxidases. Science 366: 100-104
  Safarian S, Hahn A, Mills DJ, Radloff M, Eisinger ML, Nikolaev A, Meier-Credo J, Melin F, Miyoshi H, Gennis RB, Sakamoto J, Langer JD, Hellwig P, Kühlbrandt W, Michel H
  (See online at https://doi.org/10.1126/science.aay0967)
• (2019) Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows. Proc Natl Acad Sci USA 116: 4250-4255
  Blum TB, Hahn A, Meier T, Davies KM, Kühlbrandt W
  (See online at https://doi.org/10.1073/pnas.1816556116)
• (2019) Rhodopsin-based voltage imaging tools for use in muscles and neurons of Caenorhabditis elegans. Proc Natl Acad Sci USA 116: 17051-17060
  Azimi Hashemi N, Bergs ACF, Schüler C, Scheiwe AR, Steuer Costa W, Bach M, Liewald JF, Gottschalk A
  (See online at https://doi.org/10.1073/pnas.1902443116)
• (2019) Rotary substates of mitochondrial ATP synthase reveal the basis of flexible F1-Fo coupling. Science 364: eaaw9128
  Murphy BJ, Klusch N, Langer J, Mills DJ, Yildiz O, Kühlbrandt W
  (See online at https://doi.org/10.1126/science.aaw9128)
• (2019) Structural basis for functional interactions in dimers of SLC26 transporters. Nat Commun 10: 2032
  Chang YN, Jaumann EA, Reichel K, Hartmann J, Oliver D, Hummer G, Joseph B, Geertsma ER
  (See online at https://doi.org/10.1038/s41467-019-10001-w)
• 2019) Conformation space of a heterodimeric ABC exporter under turnover conditions. Nature 571: 580–583
  Hofmann S, Januliene D, Mehdipour AR, Thomas C, Stefan E, Brüchert S, Kuhn BT, Geertsma ER, Hummer G, Tampé R, Moeller A
  (See online at https://doi.org/10.1038/s41586-019-1391-0)
• (2020) SRSF7 maintains its homeostasis through the expression of Split-ORFs and nuclear body assembly. Nat Struct Mol Biol 27 260–273
  Königs V, Machado CdOF, Arnold BL, Blümel N, Solovyeva A, Löbbert S, Schafranek M, Mozos IRDL, Wittig I, McNicoll F, Schulz MH, Müller-McNicoll M
  (See online at https://doi.org/10.1038/s41594-020-0385-9)