GRK 1384:  Enzymes and Multienzyme Complexes Acting on Nucleic Acids

• Subject Area: Basic Research in Biology and Medicine
• Term: from 2006 to 2015
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 19985993

• Final Report Year: 2016

Final Report Abstract

The International Research Training Group (IRTG) was formed by scientists from the Justus‐Liebig‐Universität Giessen, the Philipps‐Universität Marburg, the Lomonosov Moscow State University and the Russian Academy of Sciences. In addition, scientists from the Institute of Biotechnology (Vilnius) and the International Institute of Molecular and Cell Biology (Warsaw) were associated. All participants were selected based on the strength of their expertise in enzymology, molecular and cellular biology, bioinformatics, structural biology, bioorganic and biophysical chemistry. The IRTG focussed on the training of doctoral researchers in the biochemistry of enzymes and multienzyme complexes acting on nucleic acids. These enzymes are crucial for copying, maintenance, repair, and expression of genetic information. Malfunction of several of these enzymes is causally related to human diseases, and understanding their mechanism of action may eventually lead to new therapeutic concepts. Our study and research programme did not only consider proteins as individual structures, but also as components of macromolecular machines or larger networks. Using an array of interdisciplinary expertise present among the partners, we made substantial progress in understanding the structure and function of these enzymes and enzyme complexes, as well as in uncovering functional implications of the cooperation of subunits in multienzyme complexes. Our network based on three main pillars: classical and cutting‐edge methodologies to investigate chromatin/DNA‐ and RNA‐associated processes, modern global genome/transcriptome‐wide experimental approaches, and bioinformatic expertise and capacities. The doctoral researchers analysed in detail the molecular mechanisms of how enzymes acting on nucleic acids function at the single‐molecule level and used this knowledge to develop cutting‐edge tools e.g. for precision genome surgery. Moreover, we used novel chemical and biochemical approaches to investigate large, complex and dynamic complexes both in vitro for high‐resolution structural analysis as well in vivo on a global scale. During the course of the IRTG the emerging role of small non‐coding RNA in cellular function was investigated, and tools for high‐precision genome engineering were developed. High‐throughput approaches, including RNA (RNA‐Seq) deep sequencing, or ChIP‐based techniques, such as ChIP‐Chip or ChIP‐Seq combined with bioinformatic analyses opened up global and integrated views of the dynamics of expression and the processing of genetic information. We attracted dedicated doctoral researchers who learnt and applied contemporary interdisciplinary approaches to address important and timely questions about a subject of central importance in biochemistry and molecular biology, namely the enzymology of enzymes acting on nucleic acids. Our network offered unique opportunities to pursue research projects in an environment of research excellence provided by partners who have similar interests and complementary expertise.

Publications

• (2003). An exosome-like complex in Sulfolobus solfataricus. EMBO Rep 4, 889-93
  Evguenieva-Hackenberg, E., Walter, P., Hochleitner, E., Lottspeich, F. & Klug, G.
  
• (2005). RNA polyadenylation in Archaea: not observed in Haloferax while the exosome polynucleotidylates RNA in Sulfolobus. EMBO Rep 6, 1188-93
  Portnoy, V., Evguenieva-Hackenberg, E., Klein, F., Walter, P., Lorentzen, E., Klug, G. & Schuster, G.
  
• (2005). The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 12, 575-81
  Lorentzen, E., Walter, P., Fribourg, S., Evguenieva-Hackenberg, E., Klug, G. & Conti, E.
  
• (2006). Characterization of native and reconstituted exosome complexes from the hyperthermophilic archaeon Sulfolobus solfataricus. Mol Microbiol 62, 1076-89
  Walter, P., Klein, F., Lorentzen, E., Ilchmann, A., Klug, G. & Evguenieva- Hackenberg, E.
  
• (2006). Sm core variation in spliceosomal small nuclear ribonucleoproteins from Trypanosoma brucei. EMBO J 25, 4513-23
  Wang, P., Palfi, Z., Preusser, C., Lucke, S., Lane, W. S., Kambach, C. & Bindereif, A.
  
• (2007). Aufklärung von Struktur und Funktion des archaealen Exosoms durch Charakterisierung nativer und rekonstituierter Proteinkomplexe aus Sulfolobus solfataricus, Justus-Liebig-Universität Gießen
  Walter, P.
  
• (2007). RNase P of the Cyanophora paradoxa cyanelle: a plastid ribozyme. Biochimie 89, 1528-38
  Li, D., Willkomm, D. K., Schon, A. & Hartmann, R. K.
  
• (2008). dCHD3, a novel ATP-dependent chromatin remodeler associated with sites of active transcription. Mol Cell Biol 28, 2745-57
  Murawska, M., Kunert, N., van Vugt, J., Langst, G., Kremmer, E., Logie, C. & Brehm, A.
  
• (2008). Positive selection at the receptor-binding site of haemagglutinin H5 in viral sequences derived from human tissues. J Gen Virol 89, 1805-10
  Kongchanagul, A., Suptawiwat, O., Kanrai, P., Uiprasertkul, M., Puthavathana, P. & Auewarakul, P.
  
• (2008). Rrp4 and Csl4 are needed for efficient degradation but not for polyadenylation of synthetic and natural RNA by the archaeal exosome. Biochemistry 47, 13158-68
  Evguenieva-Hackenberg, E., Roppelt, V., Finsterseifer, P. & Klug, G.
  
• (2009). Codon volatility of hemagglutinin genes of H5N1 avian influenza viruses from different clades. Virus Genes 38, 404-7
  Auewarakul, P., Chatsurachai, S., Kongchanagul, A., Kanrai, P., Upala, S., Suriyaphol, P. & Puthavathana, P.
  
• (2009). dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO J 28, 533-44
  Kunert, N., Wagner, E., Murawska, M., Klinker, H., Kremmer, E. & Brehm, A.
  
• (2009). Entwicklung eines lichtschaltbaren Restriktionsenzyms : Kontrolle der enzymatischen Aktivität mit Licht, Justus-Liebig-Universität Gießen
  Schierling, B.
  
• (2009). Insights into RNase P RNA structure and function by a retro-evolution approach (Hartmann, R., Ed.), Philipps-Universität Marburg
  Li, D.
  
• (2009). Minor changes largely restore catalytic activity of archaeal RNase P RNA from Methanothermobacter thermoautotrophicus. Nucleic Acids Res 37, 231-42
  Li, D., Willkomm, D. K. & Hartmann, R. K.
  
• (2009). Multiple aspects of ATP-dependent nucleosome translocation by RSC and Mi-2 are directed by the underlying DNA sequence. PLoS One 4, e6345
  van Vugt, J. J., de Jager, M., Murawska, M., Brehm, A., van Noort, J. & Logie, C.
  
• (2009). New azobenzene derivatives for directed modification of proteins. Russian Journal of Bioorganic Chemistry 35, 549-555
  Hien, L. T., Schierling, B., Ryazanova, A. Y., Zatsepin, T. S., Volkov, E. M., Kubareva, E. A., Velichko, T. I., Pingoud, A. & Oretskaya, T. S.
  
• (2009). Physical and functional interactions between Escherichia coli MutL and the Vsr repair endonuclease. Nucleic Acids Res 37, 4453-63
  Heinze, R. J., Giron-Monzon, L., Solovyova, A., Elliot, S. L., Geisler, S., Cupples, C. G., Connolly, B. A. & Friedhoff, P.
  
• (2009). SMN-assisted assembly of snRNP- specific Sm cores in trypanosomes. Genes Dev 23, 1650-64
  Palfi, Z., Jae, N., Preusser, C., Kaminska, K. H., Bujnicki, J. M., Lee, J. H., Gunzl, A., Kambach, C., Urlaub, H. & Bindereif, A.
  
• (2009). Special Sm core complex functions in assembly of the U2 small nuclear ribonucleoprotein of Trypanosoma brucei. Eukaryot Cell 8, 1228-34
  Preusser, C., Palfi, Z. & Bindereif, A.
  
• (2010). Analysis of bacterial RNase P RNA and protein interaction by a magnetic biosensor technique. Biochimie 92, 772-8
  Li, D., Meyer, M. H., Willkomm, D. K., Keusgen, M. & Hartmann, R. K.
  
• (2010). Controlling the enzymatic activity of a restriction enzyme by light. Proc Natl Acad Sci USA 107, 1361-6
  Schierling, B., Noel, A. J., Wende, W., Hien le, T., Volkov, E., Kubareva, E., Oretskaya, T., Kokkinidis, M., Rompp, A., Spengler, B. & Pingoud, A.
  
• (2010). Functional analysis of crosstalk in DNA mismatch repair, Justus- Liebig-Universität Gießen
  Heinze, R. J.
  
• (2010). NS reassortment of an H7-type highly pathogenic avian influenza virus affects its propagation by altering the regulation of viral RNA production and antiviral host response. J Virol 84, 11323-35
  Wang, Z., Robb, N. C., Lenz, E., Wolff, T., Fodor, E. & Pleschka, S.
  
• (2010). NS reassortment of an H7-type highly pathogenic avian influenza virus affects its propagation by1 altering the regulation of viral RNA production and anti-viral host response, Justus-Liebig-Universität Gießen
  Wang, Z.
  
• (2010). Regulation of translation initiation at the Poliovirus IRES, Justus-Liebig-Universität Gießen
  Hirnet, J.
  
• (2010). Sm core variation and biogenesis of spliceosomal small nuclear ribonucleoproteins in Trypanosoma brucei, Justus-Liebig-Universität Gießen
  Preußer, C.
  
• (2010). The NS segment of an H5N1 highly pathogenic avian influenza virus (HPAIV) is sufficient to alter replication efficiency, cell tropism, and host range of an H7N1 HPAIV. J Virol 84, 2122-33
  Ma, W., Brenner, D., Wang, Z., Dauber, B., Ehrhardt, C., Hogner, K., Herold, S., Ludwig, S., Wolff, T., Yu, K., Richt, J. A., Planz, O. & Pleschka, S.
  
• (2011). Archaeal-bacterial chimeric RNase P RNAs: towards understanding RNA's architecture, function and evolution. Chembiochem 12, 1536-43
  Li, D., Gossringer, M. & Hartmann, R. K.
  
• (2011). CHD chromatin remodelers and the transcription cycle. Transcription 2, 244-53
  Murawska, M. & Brehm, A.
  
• (2011). Chemical trapping of the dynamic MutS-MutL complex formed in DNA mismatch repair in Escherichia coli. J Biol Chem 286, 17326-37
  Winkler, I., Marx, A. D., Lariviere, D., Heinze, R. J., Cristovao, M., Reumer, A., Curth, U., Sixma, T. K. & Friedhoff, P.
  
• (2011). Functional characterization of ATP-dependent chromatin remodelers of the CHD family of Drosophila, Philipps-Universität Marburg
  Murawska, M.
  (See online at https://dx.doi.org/10.17192/z2011.0570)
• (2011). Generation of DNA nanocircles containing mismatched bases. Biotechniques 51, 259-62, 264-5
  Xiao, Y., Jung, C., Marx, A. D., Winkler, I., Wyman, C., Lebbink, J. H., Friedhoff, P. & Cristovao, M.
  
• (2011). In vivo and in vitro analysis of 6S RNA-templated short transcripts in Bacillus subtilis. RNA Biol 8, 839-49
  Beckmann, B. M., Burenina, O. Y., Hoch, P. G., Kubareva, E. A., Sharma, C. M. & Hartmann, R. K.
  
• (2011). Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12, 124
  Lechner, M., Findeiss, S., Steiner, L., Marz, M., Stadler, P. F. & Prohaska, S. J.
  
• (2011). Restriction endonuclease SsoII with photoregulated activity--a "molecular gate" approach. Bioconjug Chem 22, 1366-73
  Hien le, T., Zatsepin, T. S., Schierling, B., Volkov, E. M., Wende, W., Pingoud, A., Kubareva, E. A. & Oretskaya, T. S.
  
• (2011). SAYP: a bridge connecting specific and general transcription regulators. Cell Cycle 10, 2420
  Kreher, J. & Brehm, A.
  
• (2011). snRNA-specific role of SMN in trypanosome snRNP biogenesis in vivo. RNA Biol 8, 90-100
  Jae, N., Preusser, C., Kruger, T., Tkacz, I. D., Engstler, M., Michaeli, S. & Bindereif, A.
  
• (2011). Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet 7, e1002206
  Murawska, M., Hassler, M., Renkawitz-Pohl, R., Ladurner, A. & Brehm, A.
  
• (2011). Two paralogous splicing factors, hnRNP L and L-like, cooperate in multiple-exon regulation of CD45 alternative splicing, Justus-Liebig-Universität Gießen
  Preußner, M.
  
• (2012). 2'-modified oligoribonucleotides containing 1,2-diol and aldehyde groups. Synthesis and properties. Russian Journal of Bioorganic Chemistry 38, 488-499
  Khomyakova, E. A., Zubin, E. M., Pavlova, L. V., Kazanova, E. V., Smirnov, I. P., Pozmogova, G. E., Muller, S., Dolinnaya, N. G., Kubareva, E. A., Hartmann, R. K. & Oretskaya, T. S.
  (See online at https://doi.org/10.1134/S1068162012050068)
• (2012). A novel zinc-finger nuclease platform with a sequence-specific cleavage module. Nucleic Acids Res 40, 2623-38
  Schierling, B., Dannemann, N., Gabsalilow, L., Wende, W., Cathomen, T. & Pingoud, A.
  (See online at https://doi.org/10.1093/nar/gkr1112)
• (2012). A pRNA-induced structural rearrangement triggers 6S-1 RNA release from RNA polymerase in Bacillus subtilis. EMBO J 31, 1727-38
  Beckmann, B. M., Hoch, P. G., Marz, M., Willkomm, D. K., Salas, M. & Hartmann, R. K.
  (See online at https://doi.org/10.1038/emboj.2012.23)
• (2012). Comparative genomics of Rickettsia helvetica strain AS819. International Journal of Medical Microbiology 302, 108-108
  Speck, S., Dilcher, M., Wehner, S., Riege, K., Marz, M., Hufert, F., Essbauer, S. & Dobler, G.
  
• (2012). Controlling the DNA cleavage activity of lightinducible chimeric endonucleases by bidirectional photoactivation. Bioconjug Chem 23, 1105-9
  Schierling, B. & Pingoud, A.
  (See online at https://doi.org/10.1021/bc3001326)
• (2012). Covalently trapping MutS on DNA to study DNA mismatch recognition and signaling. Mol Biosyst 8, 1861-4
  Heinze, R. J., Sekerina, S., Winkler, I., Biertumpfel, C., Oretskaya, T. S., Kubareva, E. & Friedhoff, P.
  (See online at https://doi.org/10.1039/c2mb25086a)
• (2012). Crosslinking studies of the bacterial RNase P holoenzyme and functional characterisation of the novel protein-only RNase P from Arabidopsis thaliana. Philipps-Universität Marburg
  Pavlova, L. V.
  (See online at https://dx.doi.org/10.17192/z2012.0778)
• (2012). Die Methyl-Binde-Domäne-Proteine MBD2 und MBD3 rekrutieren spezifische NuRD Komplexe, Justus-Liebig-Universität Gießen
  Rust, M.
  
• (2012). Differential stimulation of hepatitis C virus RNA translation by microRNA-122 in different cell cycle phases. Cell Cycle 11, 277-85
  Fehr, C., Conrad, K. D. & Niepmann, M.
  (See online at https://doi.org/10.4161/cc.11.2.18699)
• (2012). Genetic characterization of Tribec virus and Kemerovo virus, two tick-transmitted human-pathogenic Orbiviruses. Virology 423, 68-76
  Dilcher, M., Hasib, L., Lechner, M., Wieseke, N., Middendorf, M., Marz, M., Koch, A., Spiegel, M., Dobler, G., Hufert, F. T. & Weidmann, M.
  (See online at https://doi.org/10.1016/j.virol.2011.11.020)
• (2012). Glycyl-tRNA synthetase specifically binds to the poliovirus IRES to activate translation initiation. Nucleic Acids Res 40, 5602-14
  Andreev, D. E., Hirnet, J., Terenin, I. M., Dmitriev, S. E., Niepmann, M. & Shatsky, I. N.
  (See online at https://doi.org/10.1093/nar/gks182)
• (2012). Heterogeneous complexes of the RNA exosome in Sulfolobus solfataricus. Biochimie 94, 1578-87
  Witharana, C., Roppelt, V., Lochnit, G., Klug, G. & Evguenieva-Hackenberg, E.
  (See online at https://doi.org/10.1016/j.biochi.2012.03.026)
• (2012). HnRNP L and L-like cooperate in multiple-exon regulation of CD45 alternative splicing. Nucleic Acids Res 40, 5666-78
  Preussner, M., Schreiner, S., Hung, L. H., Porstner, M., Jack, H. M., Benes, V., Ratsch, G. & Bindereif, A.
  (See online at https://doi.org/10.1093/nar/gks221)
• (2012). Immunostaining of Drosophila polytene chromosomes to investigate recruitment of chromatin-binding proteins. Methods Mol Biol 809, 267-77
  Murawska, M. & Brehm, A.
  
• (2012). mRNA splicing in trypanosomes. Int J Med Microbiol 302, 221-4
  Preusser, C., Jae, N. & Bindereif, A.
  
• (2012). Recruitment of the ATP-dependent chromatin remodeler dMi-2 to the transcribed region of active heat shock genes. Nucleic Acids Res 40, 4879-91
  Mathieu, E. L., Finkernagel, F., Murawska, M., Scharfe, M., Jarek, M. & Brehm, A.
  (See online at https://doi.org/10.1093/nar/gks178)
• (2012). Redesigning the single-chain variant of the restriction endonuclease PvuII by circular permutation. FEBS Lett 586, 1736-41
  Schierling, B., Wende, W. & Pingoud, A.
  (See online at https://doi.org/10.1016/j.febslet.2012.05.012)
• (2012). Single-molecule multiparameter fluorescence spectroscopy reveals directional MutS binding to mismatched bases in DNA. Nucleic Acids Res 40, 5448-64
  Cristovao, M., Sisamakis, E., Hingorani, M. M., Marx, A. D., Jung, C. P., Rothwell, P. J., Seidel, C. A. & Friedhoff, P.
  (See online at https://doi.org/10.1093/nar/gks138)
• (2012). The Drosophila MI-2 chromatinremodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet 8, e1002878
  Fasulo, B., Deuring, R., Murawska, M., Gause, M., Dorighi, K. M., Schaaf, C. A., Dorsett, D., Brehm, A. & Tamkun, J. W.
  (See online at https://doi.org/10.1371/journal.pgen.1002878)
• (2012). The ordered processing of intervening sequences in 23S rRNA of Rhodobacter sphaeroides requires RNase J. RNA Biol 9, 343-50
  Rische, T. & Klug, G.
  (See online at https://doi.org/10.4161/rna.19433)
• (2012). The rotation-coupled sliding of EcoRV. Nucleic Acids Res 40, 4064-70
  Dikic, J., Menges, C., Clarke, S., Kokkinidis, M., Pingoud, A., Wende, W. & Desbiolles, P.
  
• (2012). tRNA processing by protein-only versus RNA-based RNase P: kinetic analysis reveals mechanistic differences. Chembiochem 13, 2270-6
  Pavlova, L. V., Gossringer, M., Weber, C., Buzet, A., Rossmanith, W. & Hartmann, R. K.
  (See online at https://doi.org/10.1002/cbic.201200434)
• (2012). Untersuchungen zur Funktion der RNase J in Rhodobacter sphaeroides, Justus-Liebig-Universität Gießen
  Rische, T. K.
  
• (2013). Compact designer TALENs for efficient genome engineering. Nat Commun 4, 1762
  Beurdeley, M., Bietz, F., Li, J., Thomas, S., Stoddard, T., Juillerat, A., Zhang, F., Voytas, D. F., Duchateau, P. & Silva, G. H.
  
• (2013). Conformational changes and complex formation in DNA mismatch repair, Justus-Liebig-Universität Gießen
  Marx, A. D.
  
• (2013). Die Methylbindeproteine MBD2 und MBD3 unterscheiden sich hinsichtlich ihres genomweiten Bindeverhaltens an methylierten CpG-Inseln, Promotoren und Exon-Sequenzen, sowie ihres Einflusses auf die Genexpression, Justus-Liebig-Universität Gießen
  Günther, K.
  
• (2013). Differential roles for MBD2 and MBD3 at methylated CpG islands, active promoters and binding to exon sequences. Nucleic Acids Res 41, 3010-21
  Gunther, K., Rust, M., Leers, J., Boettger, T., Scharfe, M., Jarek, M., Bartkuhn, M. & Renkawitz, R.
  (See online at https://doi.org/10.1093/nar/gkt035)
• (2013). Exo-endo trans splicing: a new way to link. Cell Res 23, 1071-2
  Preusser, C. & Bindereif, A.
  
• (2013). Generierung hochspezifischer Nukleasen für die zielgerichtete Spaltung genomischer DNA-Sequenzen, Justus-Liebig-Universität Gießen
  Yanik, M.
  
• (2013). Improved dual promotordriven reverse genetics system for influenza viruses. J Virol Methods 193, 603-10
  Mostafa, A., Kanrai, P., Ziebuhr, J. & Pleschka, S.
  (See online at https://doi.org/10.1016/j.jviromet.2013.07.021)
• (2013). Integrative "omics"-approach discovers dynamic and regulatory features of bacterial stress responses. PLoS Genet 9, e1003576
  Berghoff, B. A., Konzer, A., Mank, N. N., Looso, M., Rische, T., Forstner, K. U., Kruger, M. & Klug, G.
  (See online at https://doi.org/10.1371/journal.pgen.1003576)
• (2013). Investigation of microRNA-protein complex recruitment to the hepatitis C virus untranslated regions, Justus-Liebig-Universität Gießen
  Conrad, K. D.
  
• (2013). Light dependent activity of restriction endonucleases. Febs Journal 280, 597-597
  Abrosimova, L., Monakhova, M., Schierling, B., Volkov, E., Romanova, E., Wende, W., Pingoud, A., Kubareva, E. & Oretskaya, T.
  
• (2013). MicroRNA-122 dependent binding of Ago2 protein to hepatitis C virus RNA is associated with enhanced RNA stability and translation stimulation. PLoS One 8, e56272
  Conrad, K. D., Giering, F., Erfurth, C., Neumann, A., Fehr, C., Meister, G. & Niepmann, M.
  (See online at https://doi.org/10.1371/journal.pone.0056272)
• (2013). Orthology-based approaches and applications for comparative genomics, Phillips-Universität Marburg
  Lechner, M.
  
• (2013). Reassortment of NS segments modifies highly pathogenic avian influenza virus interaction with avian hosts and host cells. J Virol 87, 5362-71
  Petersen, H., Wang, Z., Lenz, E., Pleschka, S. & Rautenschlein, S.
  (See online at https://doi.org/10.1128/JVI.02969-12)
• (2013). Siteand strand-specific nicking of DNA by fusion proteins derived from MutH and I-SceI or TALE repeats. Nucleic Acids Res 41, e83
  Gabsalilow, L., Schierling, B., Friedhoff, P., Pingoud, A. & Wende, W.
  (See online at https://doi.org/10.1093/nar/gkt080)
• (2013). STED nanoscopy combined with optical tweezers reveals protein dynamics on densely covered DNA. Nat Methods 10, 910-6
  Heller, I., Sitters, G., Broekmans, O. D., Farge, G., Menges, C., Wende, W., Hell, S. W., Peterman, E. J. & Wuite, G. J.
  
• (2013). Systematic analysis and evolution of 5S ribosomal DNA in metazoans. Heredity 111, 410-421
  Vierna, J., Wehner, S., Siederdissen, C. H. Z., Martinez-Lage, A. & Marz, M.
  (See online at https://doi.org/10.1038/hdy.2013.63)
• (2013). TALE-PvuII fusion proteins--novel tools for gene targeting. PLoS One 8, e82539
  Yanik, M., Alzubi, J., Lahaye, T., Cathomen, T., Pingoud, A. & Wende, W.
  (See online at https://doi.org/10.1371/journal.pone.0082539)
• (2013). The correlation of genome size and DNA methylation rate in metazoans. Theory Biosci 132, 47-60
  Lechner, M., Marz, M., Ihling, C., Sinz, A., Stadler, P. F. & Krauss, V.
  (See online at https://doi.org/10.1007/s12064-012-0167-y)
• (2013). The heterogeneity of the RNA degradation exosome in Sulfolobus solfataricus, Justus-Liebig-Universität Gießen
  Witharana, C.
  
• (2013). Tropism of avian influenza A (H5N1) virus to mesenchymal stem cells and CD34+ hematopoietic stem cells. PLoS One 8, e81805
  Thanunchai, M., Kanrai, P., Wiboon-Ut, S., Puthavathana, P., Hongeng, S. & Thitithanyanont, A.
  
• (2014). A functional insulator screen identifies NURF and dREAM components to be required for enhancerblocking. PLoS One 9, e107765
  Bohla, D., Herold, M., Panzer, I., Buxa, M. K., Ali, T., Demmers, J., Kruger, M., Scharfe, M., Jarek, M., Bartkuhn, M. & Renkawitz, R.
  (See online at https://doi.org/10.1007/s11225-014-9562-3)
• (2014). Circulation of classical swine influenza virus in Europe between the wars? Arch Virol 159, 1467-73
  Lange, J., Groth, M., Kanrai, P., Pleschka, S., Scholtissek, C., Durrwald, R., Platzer, M., Sauerbrei, A. & Zell, R.
  (See online at https://doi.org/10.1007/s00705-013-1950-x)
• (2014). CTCF induces histone variant incorporation, erases the H3K27me3 histone mark and opens chromatin. Nucleic Acids Res 42, 11941-51
  Weth, O., Paprotka, C., Gunther, K., Schulte, A., Baierl, M., Leers, J., Galjart, N. & Renkawitz, R.
  (See online at https://doi.org/10.1093/nar/gku937)
• (2014). Deletion of the Synechocystis sp. PCC 6803 kaiAB1C1 gene cluster causes impaired cell growth under lightdark conditions. Microbiology 160, 2538-50
  Dorrich, A. K., Mitschke, J., Siadat, O. & Wilde, A.
  (See online at https://doi.org/10.1099/mic.0.081695-0)
• (2014). Detection of very long antisense transcripts by whole transcriptome RNA-Seq analysis of Listeria monocytogenes by semiconductor sequencing technology. PLoS One 9, e108639
  Wehner, S., Mannala, G. K., Qing, X., Madhugiri, R., Chakraborty, T., Mraheil, M. A., Hain, T. & Marz, M.
  (See online at https://doi.org/10.1371/journal.pone.0108639)
• (2014). Dissemination of 6S RNA among bacteria. RNA Biol 11, 1467-78
  Wehner, S., Damm, K., Hartmann, R. K. & Marz, M.
  (See online at https://doi.org/10.4161/rna.29894)
• (2014). Ectopically tethered CP190 induces large-scale chromatin decondensation. Sci Rep 4, 3917
  Ahanger, S. H., Gunther, K., Weth, O., Bartkuhn, M., Bhonde, R. R., Shouche, Y. S. & Renkawitz, R.
  (See online at https://doi.org/10.1038/srep03917)
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