GRK 1273:  Strategies of Human Pathogens to Establish Acute and Chronic Infections

• Subject Area: Microbiology, Virology and Immunology
• Term: from 2006 to 2015
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 969236

• Final Report Year: 2016

Final Report Abstract

Infections by pathogenic bacteria and viruses remain among the most important causes of human mortality and death worldwide. The International Research Training Group IRTG 1273 was jointly established in 2006 by Hannover Medical School (MHH), the Helmholtz Institute for Infection Biology (HZI) and their Swedish partner institution, the Karolinska Institutet, a medical university with world-wide recognition in the field of infection research. The mission of IRTG 1273 was to provide young researchers with the opportunity to perform their Ph.D. thesis in the rapidly moving field of the infection biology of human microbial pathogens in a highly stimulating, competitive, international environment. The core element of the programme was a joint research programme centering on the question how human microbial pathogens achieve acute or persistent infection and how the host organism reacts to persistent infection. Rather than focussing on one selected aspect of infection biology, multiple thematic foci have been selected with the goal of exposing the graduate students to the wide spectrum of modern infectious disease research, and taking advantage of the full breadth of faculty competence available at the three institutions involved in this IRTG. A key element of the IRTG 1273 training strategy was a mobility phase where graduate students spent time in laboratories at the partner institutions. A total of 41 exchange visits took place during the reporting period, amounting to a combined length of 99 months. Since September 1, 2006, when the first seven graduate students started their projects, a total of 44 DFG-funded graduate students plus 18 non-funded graduate students were trained in IRTG 1273. At the time of this report, 30 of the DFG-funded graduate students have obtained a PhD or Dr. rer. nat. degree, the remaining graduate students are expected to complete their doctoral training until the end of 2017. From the start until the completion of this report (end of July 2016), the DFG-funded graduate students of the IRTG have published 150 scientific papers, of which 29 are jointly authored by German and Swedish scientists. These include publications in Blood, Cell Host Microbe, EMBO Mol. Med., Gastroenterology, Gut, J. BacterioL, J. Exp. Med., J. Immunol., J. Infect. Dis., J. Virol., MBio, Nat. Commun., Nat. Immunol., PLoS Pathogens, PNAS, Cell. Microbiol., and many other leading microbiology and immunology journals. The IRTG 1273 graduate students have made important progress in answering questions regarding the strategies that human pathogens use to establish and maintain infections in humans. Due to the breadth of the programme, only few examples can be highlighted in this Summary. Important discoveries included i) the demonstration of the impact of the gastrointestinal microbiota on the diversification of the IgA antibody repertoire in the gut, ii) elucidation of the mechanisms generating genetic diversity during chronic infection with the carcinogenic stomach pathogen, Helicobacter pylori, iii) identification of several novel important mechanisms used by humans to control infection with Hepatitis C virus, iv) role of natural killer cells in different bacterial and viral infections, such as hepatitis C, Streptococcus pneumoniae. Yersinia spp., Listeria monocytogenes, and others. The graduate students benefitted greatly from the complementary skills available in the German and Swedish groups. One particularly successful example were multiple collaborations between groups at the Karolinska Institutet with a focus on human and mouse natural killer cells and groups in Germany with expertise in specific infection systems. The collaboration of these groups and the exchange of graduate students helped to develop a research cluster studying the role of NK cells in diverse human infectious diseases that has been exceptionally productive, resulting in many high-impact publications. Overall, IRTG 1273 has been a major success that achieved all goals that the partner institutions had set forth at the beginning of the project. Many of the collaborations initiated as part of IRTG 1273 will continue past the end of the IRTG 1273 funding period, and many long-lasting scientific friendships have developed, both between graduate students of the three different generations and between faculty members.

Publications

• 2006. Signatures of human regulatory T cells: an encounter with old friends and new players. Genome Biol. 7:R54
  Pfoertner, S., A. Jeron, M. Probst-Kepper, C. A. Guzman, W. Hansen, A. M. Westendorf, T. Toepfer, A. J. Schrader, A. Franzke, J. Buer, R. Geffers
  
• 2007. [Application monitoring of the use of sorafenib in papillary renal cell carcinoma.] Urologe A. 46(9):1291. German
  Schrader, A. J. , A. Hegele, P. Olbert, J. Buer, A. Jeron, R. Hofmann
  
• 2007. A comprehensive proteome map of the lipid-requiring nosocomial pathogen Corynebacterium jeikeium K411. Proteomics. 7:1076-96
  Hansmeier, N., T. C. Chao, S. Daschkey, M. Müsken, J. Kalinowski, A. Pühler, A. Tauch
  
• 2007. A pegylated derivative of alpha-galactosytceramide exhibits improved biological properties. J. Immunol. 179:2065-73
  Ebensen, T., C. Link, P. Riese, K. Schulze, M. Morr, C. A. Guzmán
  
• 2007. Solitary intestinal lymphoid tissue provides a productive port of entry for Salmonella entetica serovar Typhimurium. Infect. Immun. 75:1577-85
  Halle. S., D. Bumann, H. Herbrand, Y. Willer, S. Dähne, R. Förster, O. Pabst
  
• 2007. The bacterial second messenger cdiGMP exhibits promising activity as a mucosal adjuvant. Clin. Vaccine Immunol. 14:952-8
  Ebensen, T., K. Schulze, P. Riese, M. Morr, C. A. Guzmán
  
• 2007. The bacterial second messenger cyclic diGMP exhibits potent adjuvant properties. Vaccine. 25:1464-1469
  Ebensen, T., K. Schulze, P. Riese, C. Link, M. Morr, C. A. Guzmán
  
• 2008. Developmental switch of intestinal antimicrobial peptide expression. J. Exp. Med. 205:183-93
  Ménard, S., V. Förster, M. Lotz, D. Gütle, C. U. Duerr, R. L. Gallo, B. Henriques-Normark, K. Pütsep, M. Andersson, E. O. Glocker, M. W. Hornef
  
• 2008. Differential molecular and anatomical basis for B cell migration into the peritoneal cavity and omental milky spots. J. Immunol. 180:2196-2203
  Berberich, S., S. Dähne, A. Schippers. T. Peters, W. Müller, E. Kremmer, R. Förster, O. Pabst
  
• 2008. SOCS-1 protects against Chlamydia pneumoniae-induced lethal inflammation but hampers effective bacterial clearance. J. Immunol. 180:4040-9
  Yang, T., P. Stark, K. Janik, H. Wigzell, M. E. Rottenberg
  
• 2009. Adenosine and IFN-alpha synergistically increase IFN-(gamma) production of human NK cells. J. Leukoc. Biol. 85:452-61
  Jeffe, F., K. A. Stegmann, F. Broelsch, M. P. Manns, M. Cornberg, H. Wedemeyer
  
• 2009. Effect of peptide pools on effector functions of antigen-specific CD8+ T cells. J. Immunol. Methods. 342:33-48
  Suneetha, P. V., V. Schlaphoff, C. Wang, K. A. Stegmann, P. Fytili, S. K. Sarin, M. P. Manns, M. Cornberg, H. Wedemeyer
  
• 2009. Frequency and gene expression profile of regulatory T cells in renal cell carcinoma. Tumour Biol. 30:160-70
  Jeron, A., S. Pfoertner, D. Bruder, R. Geffers, P. Hammerer, R. Hofmann, J. Buer, A. J. Schrader
  
• 2009. GARP: a key receptor controlling FOXP3 in human regulatory T cells. J. Cell. Mol. Med. 13(9B):3343-57
  Probst-Kepper, M., R. Geffers, A. Kröger, N. Viegas, C. Erck, H. J. Hecht, H. Lünsdorf, R. Roubin, D. Moharregh-Khiabani, K. Wagner, F. Ocklenburg, A. Jeron, H. Garritsen, T. P. Arstila, E. Kekäläinen, R. Balling, H. Hauser, J. Buer, S. Weiss
  
• 2009. Gene expression signatures of peripheral CD4+ T cells clearly discriminate between patients with acute and chronic hepatitis B infection. Hepatology. 49:781-90
  Trehanpati, N., R. Geffers, Sukriti, S. Hissar, P. Riese, T. Toepfer, J. Buer, M. Kumar, C. A. Guzman, S. K. Sarin
  
• 2009. Genetic determinants of Pseudomonas aeruginosa biofilm establishment. Microbiology. 156(Pt 2):431-41
  Müsken, M., S. Di Fiore, A. Dötsch. R. Fischer, S. Haussler
  
• 2009. Increased susceptibility for superinfection with Streptococcus pneumoniae during influenza virus infection is not caused by TLR7-mediated lymphopenia. PLoS ONE. 4:e4840
  Stegemann, S., S. Dahlberg, A. Kröger, M. Gereke, D. Bruder, B. Henriques-Normark, M. Gunzer
  
• 2009. Internalization-dependent recognition of Mycobacterium avium ssp. paratuberculosis by intestinal epithelial cells. Cell. Microbiol. 11:1802-15
  Pott, J., T. Basler, C. U. Duerr, M. Rohde, R. Goethe, M. W. Hornef
  
• 2009. Intrahepatic long­ term persistence of parvovirus B19 and its role in chronic viral hepatitis. J. Med. Virol. 81:2079-88
  Wang, C., A. Heim, V. Schlaphoff, P. V. Suneetha, K. A. Stegmann, H. Jiang, M. Krueger, P. Fytili, T. Schulz, M. Cornberg, R. Kandolf, M. P. Manns, C. T. Bock, H. Wedemeyer
  
• 2009. Is the Epstein-Barr virus EBNA-1 protein an oncogen? Proc. Natl. Acad. Sci. USA. 106:2091-2
  Schulz, T. F., S. Cordes
  
• 2009. Mesenteric lymph nodes confine dendritic cell-mediated dissemination of Salmonella enterica serovar Typhimurium and limit systemic disease in mice. Infect. Immun. 77:3170-80
  Voedisch, S. C. Koenecke, S. David, H. Herbrand, R. Förster, M. Rhen, O. Pabst
  
• 2009. Nonhematopoietic cells control the outcome of infection with Listeria monocytogenes in a nucleotide oligomerization domain 1-dependent manner. Infect. Immun. 77:2908-18
  Mosa, A., C. Trumstedt, E. Eriksson, O. Soehnlein, F. Heuts, K. Janik, A. Klos, O. Dittrich-Breiholz, M. Kracht, A. Hidmark, H. Wigzell, M. E. Rottenberg
  
• 2009. O-antigen delays lipopolysaccharide recognition and impairs antibacterial host defense in murine intestinal epithelial cells. PLoS Pathog. 5:e1000567
  Duerr, C. U., S. F. Zenk, C. Chassin, J. Pott, D. Gütle, M. Hensel, M. W. Hornef
  
• 2009. Streptococcus pneumoniae evades human dendritic cell surveillance by pneumolysin expression. EMBO Mol. Med. 1:211-22
  Littmann, M., B. Albiger, A. Frentzen, S. Normark, B. Henriques-Normark, L. Plant
  
• 2009. The roles of the nitrate reductase NarGHJI, the nitrite reductase NirBD and the response regulator GInR in nitrate assimilation of Mycobacterium tuberculosis. Microbiology. 155:1332-9
  Malm. S., Y. Tiffert, J. Micklinghoff, S. Schultze, I. Joost, I. Weber, S. Horst, B. Ackermann, M. Schmidt, W. Wohlleben, S. Ehlers, R. Geffers, J. Reuther, F. C. Bange
  
• 2010. A 96-well plate based optical method for the quantitative and qualitative evaluation of Pseudomonas aeruginosa biofilm formation and its application for susceptibility testing. Nat. Protoc. 5:1460-1469
  Müsken, M., S. Di Fiore, U. Römling, S. Häussler
  
• 2010. Actin reorganization induced by Chlamydia trachomatis Serovar D - Evidence for a critical role of the effector protein CT166 targeting Rac. PLoS ONE. 5:e9887
  Thalmann, J., K. Janik, M. May, K. Sommer, J. Ebeling, F. Hofmann, H. Genth, A. Klos
  
• 2010. Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog. 6(7):e1000978
  Bitzegeio, J., D. Bankwitz, K. Hueging, S. Haid, C. Brohm, M.B. Zeisel, E. Hermann, M. Iken, M. Ott, T.F. Baumert, T. Pietschmann
  
• 2010. Control of intestinal Nod2-mediated peptidoglycan recognition by epithelium-associated lymphocytes. Mucosal Immunol. 4(3):325:34
  Duerr, C. U., N. H. Saizman, A. Dupont, A. Szabo, B. H. Normark, S. Normark, R. M. Locksley, P. Mellroth, M. W. Hornef
  
• 2010. Expression patterns of NKG2A, KIR and CD57 define a process of CD56dim NK cell differentiation uncoupled from NK cell education. Blood 116(19):3853-64
  Björkström, N.K., P. Riese, F. Heuts, S. Andersson, C. Fauriat, M. A. Ivarsson, A. T. Björklund, M. Flodström-Tullberg, J. Michaëlsson, M. E. Rottenberg, C. A. Guzmán, H.-G. Ljunggren, K.-J. Malmberg
  
• 2010. Global genotypephenotype correlations in Pseudomonas aeruginosa. PLoS Pathog. 6(8):e1001074
  Pommerenke, C., M. Müsken, T. Becker, A. Dötsch, F. Klawonn, S. Häussler
  
• 2010. Helicobacter pylori affects the cellular deubiquitinase USP7 and ubiquitin-regulated components TRAF6 and the tumour suppressor p53. Int. J. Med. Microbiol. 301 (3):213-24
  Coombs N., R. Sompallae, P. Olbermann, S. Gastaldello, D. Göppel, M.G. Masucci, C. Josenhans
  
• 2010. Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site and protects conserved neutralizing epitopes. J. Virol. 84(11):5751-63
  Bankwitz, D., E. Steinmann, J. Bitzegeio, S. Ciesek, M. Friesland, E. Hermann, M. B. Zeisel, T. F. Baumert, Z. Keck, S. K. H. Foung, E. I. Pécheur, T. Pietschmann
  
• 2010. Interferon-α-induced TRAIL on natural killer cells is associated with control of hepatitis C virus infection. Gastroenterology. 138:1885-1897
  Stegmann, K. A., N. K. Björkström. H. Veber, S. Ciesek, P. Riese, J. Wiegand, J. Hadem, P. V. Suneetha, J. Jaroszewicz, C. Wang, V. Schlaphoff, P. Fytili, M. Cronberg, M. P. Manns, R. Geffers, T. Pietschmann, C. A. Guzmán, H. G. Ljunggren, H. Wedemeyer
  
• 2010. miR-146a mediates protective innate immune tolerance in the neonate intestine. Cell Host Microbe. 8(4):358-88
  Chassin, C., M. Kocur, J. Pott, C. U. Duerr, D. Gütle, M. Lotz, M. W. Hornef
  
• 2010. Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog. 6(4):e100087
  Bruns, S., O. Kniemeyer, M. Hasenberg, V. Aimanianda, S. Nietzsche, A. Thywissen, A. Jeron, J. P. Latgé, A. A. Brakhage, M. Gunzer
  
• 2010. Thiol peroxidase (Tpx) protects Salmonella enterica from hydrogen peroxide stress in vitro and facilitates intracellular growth. J. Bacteriol. 192(11):2929-32
  Horst, S. A., T. Jaeger, L. Denkel, S. F. Rouf, M. Rhen, F. C. Bange
  
• 2011. Comparative analysis of Ebola virus glycoprotein interactions with human and bat cells. J. Infect. Dis. 204 SuppI 3:S840-9
  Kühl, A., M. Hoffmann, M. A. Müller, V. J. Munster, K. Gnirss, M. Kiene, T.S. Tsegaye, G. Behrens, G. Herder, H. Feldmann, C. Drosten, S. Pöhlmann
  
• 2011. Completion of Hepatitis C virus replication cycle in heterokaryons excludes dominant restrictions in human non-liver and mouse liver cell lines. PLoS Pathog. 7(4):e1002029
  Frentzen, A., K. Hüging, J. Bitzegeio, M. Friesland, S. Haid, J. Gentzsch, M. Hoffmann, D. Lindemann, G. Zimmer, F. Zielecki, F. Weber, E. Steinmann, T. Pietschmann
  
• 2011. Deletion of Kaposi's sarcoma herpesvirus FLICE inhibitory protein (vFLIP) from the viral genome compromises the activation of STAT-1 responsive cellular genes and spindle cell formation in endothelial cells. J. Virol. 85(19):10375-88
  Alkharsah, K. R., W. Singh, R. Bosco, S. Santag, A. Grundhoff, A. Konrad, M. StürzI, D. Wirth, O. Dittrich-Breiholz, M. Kracht, TF. Schulz
  
• 2011. Dissemination of persistent intestinal bacteria via the mesenteric lymph nodes causes typhoid relapse. Infect. Immun. 79(4):1479-88
  Griffin, A. J., L. X. Li, S. Voedisch, O. Pabst, S. J. McSorley
  
• 2011. Dual function of the NK cell receptor 2B4 (CD244) in the regulation of HCV-specific CD8+ T cells. PLoS Pathog. 7(5):e1002045
  Schlaphoff, V., S. Lunemann, P.V. Suneetha, J. Jaroszewicz, J. Grabowski, J. Dietz. F. Helfritz, H. Bektas, C. Sarrazin, M.P. Manns, M. Cornberg, H. Wedemeyer
  
• 2011. Gene expression profiles of T cells from hepatitis E virus infected patients in acute and resolving phase. J. Clin. Immunol. 31(3):498-508
  TrehanPati, N., S. Sukriti, R. Geffers, S. Hissar, P. Riese, T. Toepfer, C.A. Guzman, S.K. Sarin
  
• 2011. Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. USA. 108(12):5033-8
  Kennemann, L., X. Didelot, T. Aebischer, S. Kuhn, B. Drescher, M. Droege, R. Reinhardt, P. Correa, T. F. Meyer, C. Josenhans, D. Falush, S. Suerbaum
  
• 2011. IFN-λ determines the intestinal epithelial antiviral host defense. Proc. Natl. Acad. Sci. USA. 108(19):7944-9
  Pott, J., T. Mahlaköiv, M. Mordstein, C.U. Duerr, T. Michiels, S. Stockinger, P. Staeheli, MW Hornef
  
• 2011. Methionine sulfoxide reductases are essential for virulence of Salmonella Typhimurium. PLoS 6(11):e26974
  Denkel, L. A., S. A. Horst, S. F. Rouf, V. Kitowski, O. M. Böhm, M. Rhen, T. Jäger, F.-C. Bange
  
• 2012. A new role of the complement system, C3 provides protection in a mouse model of lung infection with intracellular Chlamydia psittaci. PLoS One. 7(11):e50327
  Bode, J., P. Dutow, K. Sommer, K. Janik, S. Glage, B. Tümmler, A. Munder, R. Laudeley, K. Sachse, A. Klos
  (See online at https://doi.org/10.1371/journal.pone.0050327)
• 2012. A plant-derived flavonoid inhibits entry of all HCV genotypes into human hepatocytes. Gastroenterology. 143:213-222 e215
  Haid, S., A. Novodomska, J. Gentzsch, C. Grethe, S. Geuenich, D. Bankwitz, P. Chhatwal, B. Jannack. T. Hennebelle. F. BailleuI, O. T. Keppler, M. Poenisch, R. Bartenschlager, C. Hernandez, M. Lemasson, A. R. Rosenberg, F. Wong-Staal, E. Davioud-Charvet, T. Pietschmann
  (See online at https://doi.org/10.1053/j.gastro.2012.03.036)
• 2012. Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility. PLoS Pathog. 8(5):e1002670
  Pott, J., S. Stockinger, N. Torow, A. Smoczek, C. Lindner, G. Mclnemey, F. Bäckhed, U. Baumann, O. Pabst, A. Bleich, M. W. Hornef
  (See online at https://doi.org/10.1371/journal.ppat.1002670)
• 2012. An orphan sensor kinase controls quinolone signal production via MexT in Pseudomonas aeruginosa. Mol. Microbiol. 83(3):536-47
  Zaoui, C., J. Overhage, D. Löns, A. Zimmermann, M. Müsken, P. Bielecki, C. Pustelny, T. Becker, M. Nimtz, S. Häussler
  (See online at https://doi.org/10.1111/j.1365-2958.2011.07947.x)
• 2012. Bile acids specifically increase hepatitis C virus RNA-replication. PLoS One. 7(4):e36029
  Chhatwal, P., D. Bankwitz, J. Gentzsch, A. Frentzen, P. Schult, V. Lohmann, T. Pietschmann
  (See online at https://doi.org/10.1371/journal.pone.0036029)
• 2012. ChIP-on-chip analysis identifies IL-22 as direct target gene of ectopically expressed FOXP3 transcription factor in human T cells. BMC Genomics. 13:705
  Jeron, A., W. Hansen, F. Ewert, J. Buer, R. Geffers, D. Bruder
  (See online at https://doi.org/10.1186/1471-2164-13-705)
• 2012. Combined muta- and semisynthesis: a powerful synthetic hybrid approach to access target specific antitumor agents based on ansamitocin P3. Chemistry. 18(3):880-6
  Taft, F., K. Harmrolfs, I. Nickeleit, A. Heutling, M. Kiene, N. Malek, F. Sasse, A. Kirschning
  (See online at https://doi.org/10.1002/chem.201101640)
• 2012. Escape from a dominant HLA-B*15-restricted CD8+ T cell response against hepatitis C virus requires compensatory mutations outside the epitope. J. Virol. 86:991-1000
  Ruhl, M., P. Chhatwal, H. Strathmann, T. Kuntzen, D. Bankwitz, K. Skibbe, A. Walker, F. M. Heinemann, P. A. Horn, T. M. Allen, D. Hoffmann, T. Pietschmann, J. Timm
  (See online at https://doi.org/10.1128/JVI.05603-11)
• 2012. First insight into the kinome of human regulatory T cells. PLoS One. 7(7):e40896
  König, S., M. Probst-Kepper, T. Reinl, A. Jeron, J. Huehn, B. Schraven, L. Jänsch
  (See online at https://doi.org/10.1371/journal.pone.0040896)
• 2012. Genome sequence of Helicobacter pylori hpEurope Strain N6. J. Bacteriol. 194(14):3725-6
  Behrens, W., T. Bönig, S. Suerbaum, C. Josenhans
  (See online at https://doi.org/10.1128/JB.00386-12)
• 2012. Hepatocytes that express variants of cyclophilin A are resistant to HCV infection and replication. Gastroenterology. 143(2):439-47
  von Hahn. T., C. Schiene-Fischer, N.D. Van, S. Pfaender, B. Karavul, E. Steinmann, A. Potthoff, C. Strassburg, N. Hamdi, A. I. Abdelaziz, C. Sarrazin, T. Müller, T. Berg, E. Trépo, H. Wedemeyer, M.P. Manns, T. Pietschmann, S. Ciesek
  (See online at https://doi.org/10.1053/j.gastro.2012.04.053)
• 2012. In vivo sequence variation in HopZ, a phase variable outer membrane protein of Helicobacter pylori. Infect. Immun. 80(12):4364-73
  Kennemann, L., B. Brenneke, S. Andres, L. Engstrand, T. F. Meyer, T. Aebischer, C. Josenhans, S. Suerbaum
  
• 2012. Influenza A virus does not encode a tetherin antagonist with Vpu-like activity and induces IFN-dependent expression in infected cells. PLoS One. 7(8):e43337
  Winkler, M., S. Bertram, K. Gnirß, I. Nehlmeier, A. Gawanbacht, F. Kirchhoff, C. Ehrhardt, S. Ludwig, M. Kiene, A S. Moldenhauer, U. Goedecke, C.B. Karsten, A. Kühl, S. Pöhlmann
  (See online at https://doi.org/10.1371/journal.pone.0043337)
• 2012. Interferon α-stimulated natural killer cells from patients with acute Hepatitis C Virus (HCV) infection recognize HCV-infected and uninfected hepatoma cells via DNAX accessory molecule-1. J. Infect. Dis. 205(9): 1351-62
  Stegmann, K. A., N. K. Björkström, S. Ciesek, S. Lunemann, J. Jaroszewicz, J. Wiegand, P. Malinski, L. B. Dustin, C. M. Rice, M. P. Manns, T. Pietschmann, M. Cornberg, H.G. Ljunggren, H. Wedemeyer
  (See online at https://doi.org/10.1093/infdis/jis210)
• 2012. Kinome analysis of receptor-induced phosphorylation in human natural killer cells. PLoS One. 7(1):e29672
  König, S., M. Nimtz, M. Scheiter, H.G. Ljunggren, Y.T. Bryceson, L. Jänsch
  (See online at https://doi.org/10.1371/journal.pone.0029672)
• 2012. MAP-kinase regulated cytosolic phospholipase A2 activity is essential for production of infectious Hepatitis C virus particles. PLoS Pathog. 8(7):e1002829
  Menzel, N., W. Fischl, K. Hueging, D. Bankwitz, A. Frentzen, S. Raid, J. Gentzsch, L. Kaderali, R. Bartenschlager, T. Pietschmann
  (See online at https://doi.org/10.1371/journal.ppat.1002829)
• 2012. NK cells in hepatitis C: role in disease susceptibility and therapy. Dig. Dis. 30 Suppl 1:48-54
  Lunemann, S., V. Schlaphoff, M. Cornberg, H. Wedemeyer
  
• 2012. Recruitment of the tumour suppressor protein p73 by Kaposi's Sarkoma Herpesvirus latent nuclear antigen contributes to the survival of primary effusion lymphoma cells. Oncogene. 32(32):3676-85
  Santag, S., W. Jäger, C.B. Karsten, S. Kati, M. Pietrek, D. Steinemann, G. Sarek, P.M. Ojala, T.F. Schulz
  (See online at https://doi.org/10.1038/onc.2012.385)
• 2012. Rhadinoviruses: KSHV and associated malignancies. In: Cancer associated viruses. Robertson E.S. (Ed.). Springer Science + Business Media. New York, pp. 215-249
  Santag, S., T.F. Schulz
  
• 2012. Structural basis for intrinsic thermosensing by the master virulence regulator RovA of Yersinia. J. Biol. Chem. 287(43):35796-803
  Quade, N., C. Mendonca, K. Herbst, A. K. Heroven, C. Ritter, D. W. Heinz, P. Dersch
  (See online at https://doi.org/10.1074/jbc.M112.379156)
• 2012. The mammalian intestinal epithelium as integral player in the establishment and maintenance of host-microbial homeostasis. Semin. Immunol. 24(1):25-35
  Duerr, C. U., M. W. Hornef
  (See online at https://doi.org/10.1016/j.smim.2011.11.002)
• 2012. The nucleotide excision repair (NER) system of Helicobacter pylori: Role in mutation prevention and chromosomal import patterns after natural transformation. BMC Microbiol. 12(1):67
  Moccia, C., J. Krebes, S. Kulick, X. Didelot, C. Kraft, C. Bahlawane, S. Suerbaum
  (See online at https://doi.org/10.1186/1471-2180-12-67)
• 2012. The role of the alternative coreceptor GPR15 in SIV tropism for human cells. Virology. 433(1 ):73-84
  Kiene, M., A. Marzi, A. Urbanczyk, S. Bertram, T. Fisch, I. Nehlmeier, K. Gnirß, C.B. Karsten. D. Palesch, J. Münch, F. Chiodi, S. Pöhlmann, I. Steffen
  (See online at https://doi.org/10.1016/j.virol.2012.07.012)
• 2012. The ubiquitin-specific protease USP7 modulates the replication of Kaposi's Sarcoma Herpesvirus latent episomal DNA. J. Virol. 86(12):6745-57
  Jäger, W., S. Santag, M. Weidner-Glunde, E. Gellermann, S. Kati, M. Pietrek, A. Viejo-Borbolla, T. F. Schulz
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• 2012. The YfiBNR signal transduction mechanism reveals novel targets for the evolution of persistent Pseudomonas aeruginosa in cystic fibrosis airways. PLoS Pathog. 8(6): e1002760
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• 2012. Two methods of heterokaryon formation to discover HCV restriction factors. J. Vis. Exp. (65):e4029
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• 2013. Biotin sulfoxide reductase contributes to oxidative stress tolerance and virulence in Salmonella enterica serovar Typhimurium. Microbiology. 159(Pt 7):1447-58
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• 2013. Bromo- and extraterminal domain chromatin regulators serve as cofactors for murine leukemia virus integration. J. Virol. 87(23): 12721-36
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• 2013. Cell entry, efficient RNA replication, and production of infectious hepatitis C virus progeny in mouse liver-derived cells. Hepatology. 59(1):78-88
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• 2013. Characterization of hepatitis C virus intra- and inter-genotypic chimeras reveals a role of the glycoproteins in virus envelopment. J. Virol. 87:13297-13306
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• 2013. Characterization of rough and smooth morphotypes of Mycobacterium abscessus isolated from clinical specimens. J. Clin. Microbiol. 52(1):244-50
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• 2013. Characterization of the inhibition of hepatitis C virus entry by in vitro-generated and patient-derived oxidized low-density lipoprotein. Hepatology. 57:1716-1724
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• 2013. Compromised function of natural killer cells in acute and chronic viral hepatitis. J. Infect. Dis. 209(9):1362-73
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• 2013. Hepatitis c Virus p7 is critical for capsid assembly and envelopment. PLoS Pathog. 9(5): e1003355
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• 2013. Identification of the alternative sigma factor SigX regulon and its implications for Pseudomonas aeruginosa pathogenicity. J. Bacteriol. 196(2):345-56
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• 2013. Inactivation of hepatitis C virus infectivity by human breast milk. J. Infect. Dis. 208(12):1943-52
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• 2013. Platelet activation suppresses HIV-1 spread in adjacent T cells. Retrovirology. 10(1):48
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• 2013. Protein kinase inhibitors CK59 and CID755673 alter primary human NK cell effector functions. Front. Immunol. 4:66
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• 2013. Role of energy sensor TlpD of Helicobacter pylori in gerbil colonization and genome analyses after adaptation in the gerbil. Infect. Immun. 81 (10):3534-51
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• 2013. Severity of allergic airway disease to house dust mite allergen is not increased after clinical recovery of lung infection with Chlamydia pneumoniae in mice. Infect. Immun. 81{9):3366-74
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• 2013. The complement C3a receptor is critical in defense against Chlamydia psittaci in mouse lung infection and required for antibody and optimal T cell response. J. Infect. Dis. 209(8): 1269-78
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• 2013. The complex methylome of the human gastric pathogen Helicobacter pylori. Nucleic Acids Res. 42(4):2415-32
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• 2013. The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella typhimurium. Mol. Microbiol. 90(6):1216-32
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• 2013. The inflammatory kinase MAP4K4 promotes reactivation promotes reactivation of Kaposi's Sarcoma Herpesvirus and enhances the invasiveness of infected endothelial cells. PLoS Pathog. 9(11):e1003737
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• 2013. Thermostability of seven hepatitis C virus genotypes in vitro and in vivo. J. Viral Hepat. 20(7):478-85
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• 2013. TLR7 contributes to the rapid progression but not to the overall fatal outcome of secondary pneumococcal disease following influenza A virus infection. J. Innate Immun. 5{1):84-96
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• 2013. Turmeric curcumin inhibits entry of all hepatitis C virus genotypes into human liver cells. Gut. 63(7):1137-49
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• 2014. Age-dependent enterocyte invasion and microcolony formation by salmonella. PLoS Pathog. 10(9):e1004385
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• 2014. Analysis of essential viral gene functions after highly efficient adenofection of cells with cloned human cytomegalovirus genomes. Viruses. 6(1):354-70
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• 2014. Apolipoprotein E co-determines tissue-tropism of hepatitis C virus and it Is crucial for viral cell-to cell transmission by contributing to a post-envelopment step of assembly. J. Virol. 88:1433-1446
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• 2014. Bidirectional genomic exchange between Helicobacter pylori strains from a family in Coventry, United Kingdom. Int. J. Med. Microbiol. 304(8): 1135-46
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• 2014. Caspase-8 controls the gut response to microbial challenges by Tnf-α-dependent and independent pathways. Gut. 64(4):601-10
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• 2014. Chlamydia psittaci: New insights into genomic diversity, clinical pathology, host-pathogen interaction and anti-bacterial immunity. Int. J. Med. Microbiol. 304(7):877-93
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• 2014. Complement factor C5 but not C3 contributes significantly to hydrosalpinx development in mice infected with Chlamydia muridanim. Infect. Immun. 82(8):3154-63
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• 2014. Concomitant TLR/RLH signaling of radioresistant and radiosensitive cells is essential for protection against vesicular stomatitis virus infection. J. Immunol. 193(6):3045-54
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• 2014. Contribution of Veillonella parvula to Pseudomonas aeruginosa mediated pathogenicity in a murine tumor model system. Infect. Immun. 83(1):417-29
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• 2014. Dendritic cells coordinate innate immunity via MyD88 signaling to control Listeria monocytogenes infection. Cell Rep. 6(4):698-708
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• 2014. Dynamics of Lewis b binding and sequence variation of the babA adhesin gene during chronic Helicobacter pylori infection in humans. MBio. 5(6). pii: e02281-14
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• 2014. Effects of HDV infection and pegylated interferon α treatment on the natural killer cell compartment in chronically infected individuals. Gut. 64(3);469-82
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• 2014. Efficient virus assembly, but not infectivity, determines the magnitude of hepatitis C virus induced interferon-α responses of plasmacytoid dendritic cells. J. Virol. 89(6):3200-8
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• 2014. Expression of the human cytomegalovirus UL11 glycoprotein in viral infection and evaluation of its effect on virus-specific CD8 T cells. J. Virol. 88(24): 14326-39
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• 2014. Few Foxp3+ regulatory T cells are sufficient to protect adult mice from lethal autoimmunity. Eur. J. Immunol. 44(10):2990-3002
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• 2014. GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol. Microbiol. 93(3):439-52
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• 2014. Independent bottlenecks characterize colonization of systemic compartments and gut lymphoid tissue by salmonella. PLoS Pathog. 10(7):e1004270
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• 2014. Influence of PhoP and intra-species variations on virulence of Yersinia pseudotuberculosis during the natural oral infection route. PLoS One. 9(7):e103541
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• 2014. Interleukin-13-mediated paneth cell degranulation and antimicrobial peptide release. J. Innate Immun. 6(4);530-41
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• 2014. Intranasal formulations: promising strategy to deliver vaccines. Expert. Opin. Drug Deliv. 11(10):1619-34
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• 2014. ln situ characterization of intrahepatic non-parenchymal cells in PSC reveals phenotypic patterns associated with disease severity. PLoS One. 9(8):e105375
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• 2014. Mechanisms of methods for hepatitis c virus inactivation. Appl. Environ. Microbiol. 81(5):1616-21
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• 2014. MyD88 signalling in myeloid cells is sufficient to prevent chronic mycobacterial infection. Eur. J. Immunol. 44(5): 1399-409
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• 2014. Natural reservoirs for homologs of hepatitis C virus. Emerg Microbes Infect. 3(3):e21
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• 2014. PEG-IFN alpha but not Ribavirin alters NK cell phenotype and function in patients with chronic Hepatitis C. PLoS One. 9(4):e94512
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• 2014. Rapid rebound of the Treg compartment in DEREG mice limits the impact of Treg depletion on mycobacterial burden, but prevents autoimmunity. PLoS One. 9(7):e102804
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• 2014. Role of capsule and suilysin in mucosal infection of complement-deficient mice with Streptococcus suis. Infect. Immun. 82(6):2460-71
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• 2014. Role of hypervariable region 1 for the interplay of hepatitis C virus with entry factors and lipoproteins. J. Virol. 88:12644-12655
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• 2014. Selective and efficient generation of functional Batf3- dependent CD103+ dendritic cells from mouse bone marrow. Blood. 124(20):3081-91
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• 2014. Successful anti-scavenger receptor class B type I (SR-BI) monoclonal antibody therapy in humanized mice after challenge with HCV variants with in vitro resistance to SR-BI-targeting agents. Hepatology 60:1508-1518
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• 2014. Toll-like receptor 3 signalling up-regulates expression of the HIV co-receptor G-protein coupled receptor 15 on human CD4+ T cells. PLoS One. 9(2):e88195
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• 2014. TRIF signaling drives homeostatic intestinal epithelial antimicrobial peptide expression. J. Immunol. 193(8):4223-34
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• 2015. Acetate dissimilation and assimilation in Mycobacterium tuberculosis depend on carbon availability. J. Bacteriol. 197(19):3182-90
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• 2015. Activated NKT cells imprint NK-cell differentiation, functionality and education. Eur. J. Immunol. 45(6): 1794-807
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• 2015. Active suppression of intestinal CD4(+)TCRαβ(+) T-lymphocyte maturation during the postnatal period. Nat. Commun. 6:7725
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• 2015. An optimized, fast-to-perform mouse lung infection model with the human pathogen Chlamydia trachomatis for in vivo screening of antibiotics, vaccine candidates and modified host-pathogen interactions. Pathog. Dis. 74(2). pii: ftv120
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• 2015. Assessment of cross-species transmission of hepatitis C-related non­ primate hepacivirus in a population of humans at high risk of exposure. J. Gen. Virol. 96(9):2636-42
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• 2015. Clinical course of infection and viral tissue tropism of hepatitis C virus-like nonprimate hepaciviruses in horses. Hepatology. 61(2):448-59
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• 2015. Constitutive production of c-di-GMP is associated with mutations in a variant of Pseudomonas aeruginosa with altered membrane composition. Sci. Signal. 8(372):ra36
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