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Publications AG Heissmeyer

2021

Hoefig, K.P., Reim, A., Gallus, C., Wong, E.H., Behrens, G., Conrad, C., Xu M. , Kiflinger, L., Ito-Kureha, T., Defourny, K.A.Y., Geerlof, A., Mautner, J., Hauck, S.M., Baumjohann, D., Feederle, R., Mann, M., Wierer, M. Glasmacher, E., Heissmeyer, V. (2021) Defining the RBPome of primary T helper cells to elucidate higher-order Roquin-mediated mRNA regulation. Nat Commun 12, 5208 . https://doi.org/10.1038/s41467-021-25345-5

2020

Li, M., Guo, W., Dong, Y., Wang, X., Dai, D., Liu, X., Wu, Y., Li, M., Zhang, W., Zhou, H., Zhang, Z., Lin, L., Kang, Z., Yu, T., Tian, C., Qin, R., Gui, Y., Jiang, F., Fan, H., Heissmeyer, V., Sarapultsev, A., Wang, L., Luo, S., and Hu, D. (2020). Elevated Exhaustion Levels of NK and CD8(+) T Cells as Indicators for Progression and Prognosis of COVID-19 Disease. Front Immunol 11, 580237.

Weichmann, F., Hett, R., Schepers, A., Ito-Kureha, T., Flatley, A., Slama, K., Hastert, F.D., Angstman, N.B., Cardoso, M.C., Konig, J., Huttelmaier, S., Dieterich, C., Canzar, S., Helm, M., Heissmeyer, V., Feederle, R., and Meister, G. (2020). Validation strategies for antibodies targeting modified ribonucleotides. RNA 26, 1489-1506.

2019

Tavernier, S.J., Athanasopoulos, V., Verloo, P., Behrens, G., Staal, J., Bogaert, D.J., Naesens, L., De Bruyne, M., Van Gassen, S., Parthoens, E., Ellyard, J., Cappello, J., Morris, L.X., Van Gorp, H., Van Isterdael, G., Saeys, Y., Lamkanfi, M., Schelstraete, P., Dehoorne, J., Bordon, V., Van Coster, R., Lambrecht, B.N., Menten, B., Beyaert, R., Vinuesa, C.G., Heissmeyer, V., Dullaers, M., and Haerynck, F. (2019b). A human immune dysregulation syndrome characterized by severe hyperinflammation with a homozygous nonsense Roquin-1 mutation. Nat Commun 10, 4779.

Tavernier, S.J., Athanasopoulos, V., Verloo, P., Behrens, G., Staal, J., Bogaert, D.J., Naesens, L., De Bruyne, M., Van Gassen, S., Parthoens, E., Ellyard, J., Cappello, J., Morris, L.X., Van Gorp, H., Van Isterdael, G., Saeys, Y., Lamkanfi, M., Schelstraete, P., Dehoorne, J., Bordon, V., Van Coster, R., Lambrecht, B.N., Menten, B., Beyaert, R., Vinuesa, C.G., Heissmeyer, V., Dullaers, M., and Haerynck, F. (2019a). Author Correction: A human immune dysregulation syndrome characterized by severe hyperinflammation with a homozygous nonsense Roquin-1 mutation. Nat Commun 10, 5337

von Gamm, M., Schaub, A., Jones, A.N., Wolf, C., Behrens, G., Lichti, J., Essig, K., Macht, A., Pircher, J., Ehrlich, A., Davari, K., Chauhan, D., Busch, B., Wurst, W., Feederle, R., Feuchtinger, A., Tschop, M.H., Friedel, C.C., Hauck, S.M., Sattler, M., Geerlof, A., Hornung, V., Heissmeyer, V., Schulz, C., Heikenwalder, M., and Glasmacher, E. (2019). Immune homeostasis and regulation of the interferon pathway require myeloid-derived Regnase-3. J Exp Med 216, 1700-1723.

Borland, K., Diesend, J., Ito-Kureha, T., Heissmeyer, V., Hammann, C., Buck, A.H., Michalakis, S., and Kellner, S. (2019). Production and Application of Stable Isotope-Labeled Internal Standards for RNA Modification Analysis. Genes (Basel) 10.

2018

Rehage, N., Davydova, E., Conrad, C., Behrens, G., Maiser, A., Stehklein, J.E., Brenner, S., Klein, J., Jeridi, A., Hoffmann, A., Lee, E., Dianzani, U., Willemsen, R., Feederle, R., Reiche, K., Hackermuller, J., Leonhardt, H., Sharma, S., Niessing, D., and Heissmeyer, V. (2018). Binding of NUFIP2 to Roquin promotes recognition and regulation of ICOS mRNA. Nat Commun 9, 299.

Essig, K., Kronbeck, N., Guimaraes, J.C., Lohs, C., Schlundt, A., Hoffmann, A., Behrens, G., Brenner, S., Kowalska, J., Lopez-Rodriguez, C., Jemielity, J., Holtmann, H., Reiche, K., Hackermuller, J., Sattler, M., Zavolan, M., and Heissmeyer, V. (2018). Roquin targets mRNAs in a 3'-UTR-specific manner by different modes of regulation. Nat Commun 9, 3810.

Hoefig, K.P., and Heissmeyer, V. (2018). Posttranscriptional regulation of T helper cell fate decisions. J Cell Biol 217, 2615-2631.

Baumjohann, D., and Heissmeyer, V. (2018). Posttranscriptional Gene Regulation of T Follicular Helper Cells by RNA-Binding Proteins and microRNAs. Front Immunol 9, 1794.

Behrens, G., Winzen, R., Rehage, N., Dorrie, A., Barsch, M., Hoffmann, A., Hackermuller, J., Tiedje, C., Heissmeyer, V., and Holtmann, H. (2018). A translational silencing function of MCPIP1/Regnase-1 specified by the target site context. Nucleic Acids Res 46, 4256-4270.

2017

Essig, K., Hu, D., Guimaraes, J.C., Alterauge, D., Edelmann, S., Raj, T., Kranich, J., Behrens, G., Heiseke, A., Floess, S., Klein, J., Maiser, A., Marschall, S., Hrabe de Angelis, M., Leonhardt, H., Calkhoven, C.F., Noessner, E., Brocker, T., Huehn, J., Krug, A.B., Zavolan, M., Baumjohann, D., and Heissmeyer, V. (2017). Roquin Suppresses the PI3K-mTOR Signaling Pathway to Inhibit T Helper Cell Differentiation and Conversion of Treg to Tfr Cells. Immunity 47, 1067-1082 e1012.

2016

Halle, S., Keyser, K.A., Stahl, F.R., Busche, A., Marquardt, A., Zheng, X., Galla, M., Heissmeyer, V., Heller, K., Boelter, J., Wagner, K., Bischoff, Y., Martens, R., Braun, A., Werth, K., Uvarovskii, A., Kempf, H., Meyer-Hermann, M., Arens, R., Kremer, M., Sutter, G., Messerle, M., and Forster, R. (2016). In Vivo Killing Capacity of Cytotoxic T Cells Is Limited and Involves Dynamic Interactions and T Cell Cooperativity. Immunity 44, 233-245.

Elhai, M., Avouac, J., Hoffmann-Vold, A.M., Ruzehaji, N., Amiar, O., Ruiz, B., Brahiti, H., Ponsoye, M., Frechet, M., Burgevin, A., Pezet, S., Sadoine, J., Guilbert, T., Nicco, C., Akiba, H., Heissmeyer, V., Subramaniam, A., Resnick, R., Molberg, O., Kahan, A., Chiocchia, G., and Allanore, Y. (2016). OX40L blockade protects against inflammation-driven fibrosis. Proc Natl Acad Sci U S A 113, E3901-3910.

Janowski, R., Heinz, G.A., Schlundt, A., Wommelsdorf, N., Brenner, S., Gruber, A.R., Blank, M., Buch, T., Buhmann, R., Zavolan, M., Niessing, D., Heissmeyer, V., and Sattler, M. (2016). Roquin recognizes a non-canonical hexaloop structure in the 3'-UTR of Ox40. Nat Commun 7, 11032.

Jeltsch, K.M., and Heissmeyer, V. (2016). Regulation of T cell signaling and autoimmunity by RNA-binding proteins. Curr Opin Immunol 39, 127-135.

Schlundt, A., Niessing, D., Heissmeyer, V., and Sattler, M. (2016). RNA recognition by Roquin in posttranscriptional gene regulation. Wiley Interdiscip Rev RNA 7, 455-469.

Meininger, I., Griesbach, R.A., Hu, D., Gehring, T., Seeholzer, T., Bertossi, A., Kranich, J., Oeckinghaus, A., Eitelhuber, A.C., Greczmiel, U., Gewies, A., Schmidt-Supprian, M., Ruland, J., Brocker, T., Heissmeyer, V., Heyd, F., and Krappmann, D. (2016). Alternative splicing of MALT1 controls signalling and activation of CD4(+) T cells. Nat Commun 7, 11292.

Tagawa, T., Albanese, M., Bouvet, M., Moosmann, A., Mautner, J., Heissmeyer, V., Zielinski, C., Lutter, D., Hoser, J., Hastreiter, M., Hayes, M., Sugden, B., and Hammerschmidt, W. (2016). Epstein-Barr viral miRNAs inhibit antiviral CD4+ T cell responses targeting IL-12 and peptide processing. J Exp Med 213, 2065-2080.

2015

Martinez, G.J., Pereira, R.M., Aijo, T., Kim, E.Y., Marangoni, F., Pipkin, M.E., Togher, S., Heissmeyer, V., Zhang, Y.C., Crotty, S., Lamperti, E.D., Ansel, K.M., Mempel, T.R., Lahdesmaki, H., Hogan, P.G., and Rao, A. (2015). The transcription factor NFAT promotes exhaustion of activated CD8(+) T cells. Immunity 42, 265-278.

Srivastava, M., Duan, G., Kershaw, N.J., Athanasopoulos, V., Yeo, J.H., Ose, T., Hu, D., Brown, S.H., Jergic, S., Patel, H.R., Pratama, A., Richards, S., Verma, A., Jones, E.Y., Heissmeyer, V., Preiss, T., Dixon, N.E., Chong, M.M., Babon, J.J., and Vinuesa, C.G. (2015). Roquin binds microRNA-146a and Argonaute2 to regulate microRNA homeostasis. Nat Commun 6, 6253.

Warth, S.C., Hoefig, K.P., Hiekel, A., Schallenberg, S., Jovanovic, K., Klein, L., Kretschmer, K., Ansel, K.M., and Heissmeyer, V. (2015). Induced miR-99a expression represses Mtor cooperatively with miR-150 to promote regulatory T-cell differentiation. EMBO J 34, 1195-1213.

2014

Schlundt, A., Heinz, G.A., Janowski, R., Geerlof, A., Stehle, R., Heissmeyer, V., Niessing, D., and Sattler, M. (2014). Structural basis for RNA recognition in roquin-mediated post-transcriptional gene regulation. Nat Struct Mol Biol 21, 671-678.

Gewies, A., Gorka, O., Bergmann, H., Pechloff, K., Petermann, F., Jeltsch, K.M., Rudelius, M., Kriegsmann, M., Weichert, W., Horsch, M., Beckers, J., Wurst, W., Heikenwalder, M., Korn, T., Heissmeyer, V., and Ruland, J. (2014). Uncoupling Malt1 threshold function from paracaspase activity results in destructive autoimmune inflammation. Cell Rep 9, 1292-1305.

Jeltsch, K.M., Hu, D., Brenner, S., Zoller, J., Heinz, G.A., Nagel, D., Vogel, K.U., Rehage, N., Warth, S.C., Edelmann, S.L., Gloury, R., Martin, N., Lohs, C., Lech, M., Stehklein, J.E., Geerlof, A., Kremmer, E., Weber, A., Anders, H.J., Schmitz, I., Schmidt-Supprian, M., Fu, M., Holtmann, H., Krappmann, D., Ruland, J., Kallies, A., Heikenwalder, M., and Heissmeyer, V. (2014). Cleavage of roquin and regnase-1 by the paracaspase MALT1 releases their cooperatively repressed targets to promote T(H)17 differentiation. Nat Immunol 15, 1079-1089.

Edelmann, S.L., and Heissmeyer, V. (2014). Tfh cell differentiation: missing Stat3 uncovers interferons' interference. Immunity 40, 307-309.

Hoefig, K.P., and Heissmeyer, V. (2014). Degradation of oligouridylated histone mRNAs: see UUUUU and goodbye. Wiley Interdiscip Rev RNA 5, 577-589.

2013

Warth, S.C., and Heissmeyer, V. (2013). Adenoviral transduction of naive CD4 T cells to study Treg differentiation. J Vis Exp.

Vogel, K.U., Edelmann, S.L., Jeltsch, K.M., Bertossi, A., Heger, K., Heinz, G.A., Zoller, J., Warth, S.C., Hoefig, K.P., Lohs, C., Neff, F., Kremmer, E., Schick, J., Repsilber, D., Geerlof, A., Blum, H., Wurst, W., Heikenwalder, M., Schmidt-Supprian, M., and Heissmeyer, V. (2013). Roquin paralogs 1 and 2 redundantly repress the Icos and Ox40 costimulator mRNAs and control follicular helper T cell differentiation. Immunity 38, 655-668.

Hoefig, K.P., Rath, N., Heinz, G.A., Wolf, C., Dameris, J., Schepers, A., Kremmer, E., Ansel, K.M., and Heissmeyer, V. (2013). Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nat Struct Mol Biol 20, 73-81.

Pesic, M., Bartholomaus, I., Kyratsous, N.I., Heissmeyer, V., Wekerle, H., and Kawakami, N. (2013). 2-photon imaging of phagocyte-mediated T cell activation in the CNS. J Clin Invest 123, 1192-1201.

Bronevetsky, Y., Villarino, A.V., Eisley, C.J., Barbeau, R., Barczak, A.J., Heinz, G.A., Kremmer, E., Heissmeyer, V., McManus, M.T., Erle, D.J., Rao, A., and Ansel, K.M. (2013). T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J Exp Med 210, 417-432.

Burger, K., Muhl, B., Rohrmoser, M., Coordes, B., Heidemann, M., Kellner, M., Gruber-Eber, A., Heissmeyer, V., Strasser, K., and Eick, D. (2013). Cyclin-dependent kinase 9 links RNA polymerase II transcription to processing of ribosomal RNA. J Biol Chem 288, 21173-21183.

Canis, M., Lechner, A., Mack, B., Zengel, P., Laubender, R.P., Koehler, U., Heissmeyer, V., and Gires, O. (2013). CD133 induces tumour-initiating properties in HEK293 cells. Tumour Biol 34, 437-443.

Heissmeyer, V., and Vogel, K.U. (2013). Molecular control of Tfh-cell differentiation by Roquin family proteins. Immunol Rev 253, 273-289.

2012

Frohn, A., Eberl, H.C., Stohr, J., Glasmacher, E., Rudel, S., Heissmeyer, V., Mann, M., and Meister, G. (2012). Dicer-dependent and -independent Argonaute2 protein interaction networks in mammalian cells. Mol Cell Proteomics 11, 1442-1456.

Thomas, M.F., Abdul-Wajid, S., Panduro, M., Babiarz, J.E., Rajaram, M., Woodruff, P., Lanier, L.L., Heissmeyer, V., and Ansel, K.M. (2012). Eri1 regulates microRNA homeostasis and mouse lymphocyte development and antiviral function. Blood 120, 130-142.

Canis, M., Lechner, A., Mack, B., Zengel, P., Laubender, R.P., Koehler, U., Heissmeyer, V., and Gires, O. (2012). CD133 is a predictor of poor survival in head and neck squamous cell carcinomas. Cancer Biomark 12, 97-105.

2011

Eitelhuber, A.C., Warth, S., Schimmack, G., Duwel, M., Hadian, K., Demski, K., Beisker, W., Shinohara, H., Kurosaki, T., Heissmeyer, V., and Krappmann, D. (2011). Dephosphorylation of Carma1 by PP2A negatively regulates T-cell activation. EMBO J 30, 594-605.

2010

Parameswaran, P., Sklan, E., Wilkins, C., Burgon, T., Samuel, M.A., Lu, R., Ansel, K.M., Heissmeyer, V., Einav, S., Jackson, W., Doukas, T., Paranjape, S., Polacek, C., dos Santos, F.B., Jalili, R., Babrzadeh, F., Gharizadeh, B., Grimm, D., Kay, M., Koike, S., Sarnow, P., Ronaghi, M., Ding, S.W., Harris, E., Chow, M., Diamond, M.S., Kirkegaard, K., Glenn, J.S., and Fire, A.Z. (2010). Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog 6, e1000764.

Glasmacher, E., Hoefig, K.P., Vogel, K.U., Rath, N., Du, L., Wolf, C., Kremmer, E., Wang, X., and Heissmeyer, V. (2010). Roquin binds inducible costimulator mRNA and effectors of mRNA decay to induce microRNA-independent post-transcriptional repression. Nat Immunol 11, 725-733.

Hoefig, K.P., and Heissmeyer, V. (2010). Measuring microRNA expression in size-limited FACS-sorted and microdissected samples. Methods Mol Biol 667, 47-63.

2008

Ansel, K.M., Pastor, W.A., Rath, N., Lapan, A.D., Glasmacher, E., Wolf, C., Smith, L.C., Papadopoulou, N., Lamperti, E.D., Tahiliani, M., Ellwart, J.W., Shi, Y., Kremmer, E., Rao, A., and Heissmeyer, V. (2008). Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat Struct Mol Biol 15, 523-530.

Heissmeyer, V., and Rao, A. (2008). Itching to end NF-kappaB. Nat Immunol 9, 227-229.

Hoefig, K.P., and Heissmeyer, V. (2008). MicroRNAs grow up in the immune system. Curr Opin Immunol 20, 281-287.

2007

Holzel, M., Rohrmoser, M., Orban, M., Homig, C., Harasim, T., Malamoussi, A., Gruber-Eber, A., Heissmeyer, V., Bornkamm, G., and Eick, D. (2007). Rapid conditional knock-down-knock-in system for mammalian cells. Nucleic Acids Res 35, e17.

2006

Wegener, E., Oeckinghaus, A., Papadopoulou, N., Lavitas, L., Schmidt-Supprian, M., Ferch, U., Mak, T.W., Ruland, J., Heissmeyer, V., and Krappmann, D. (2006). Essential role for IkappaB kinase beta in remodeling Carma1-Bcl10-Malt1 complexes upon T cell activation. Mol Cell 23, 13-23.

Wu, Y., Borde, M., Heissmeyer, V., Feuerer, M., Lapan, A.D., Stroud, J.C., Bates, D.L., Guo, L., Han, A., Ziegler, S.F., Mathis, D., Benoist, C., Chen, L., and Rao, A. (2006). FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126, 375-387.

Borde, M., Barrington, R.A., Heissmeyer, V., Carroll, M.C., and Rao, A. (2006). Transcriptional basis of lymphocyte tolerance. Immunol Rev 210, 105-119.2005

2005

Oberdoerffer, P., Kanellopoulou, C., Heissmeyer, V., Paeper, C., Borowski, C., Aifantis, I., Rao, A., and Rajewsky, K. (2005). Efficiency of RNA interference in the mouse hematopoietic system varies between cell types and developmental stages. Mol Cell Biol 25, 3896-3905.

Heissmeyer, V., Macian, F., Varma, R., Im, S.H., Garcia-Cozar, F., Horton, H.F., Byrne, M.C., Feske, S., Venuprasad, K., Gu, H., Liu, Y.C., Dustin, M.L., and Rao, A. (2005b). A molecular dissection of lymphocyte unresponsiveness induced by sustained calcium signalling. Novartis Found Symp 267, 165-174; discussion 174-169.

Heissmeyer, V., Ansel, K.M., and Rao, A. (2005a). A plague of autoantibodies. Nat Immunol 6, 642-644.

2004

Heissmeyer, V., Macian, F., Im, S.H., Varma, R., Feske, S., Venuprasad, K., Gu, H., Liu, Y.C., Dustin, M.L., and Rao, A. (2004). Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat Immunol 5, 255-265.

Kobori, M., Yang, Z., Gong, D., Heissmeyer, V., Zhu, H., Jung, Y.K., Gakidis, M.A., Rao, A., Sekine, T., Ikegami, F., Yuan, C., and Yuan, J. (2004). Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK complex. Cell Death Differ 11, 123-130.

Heissmeyer, V., and Rao, A. (2004). E3 ligases in T cell anergy--turning immune responses into tolerance. Sci STKE 2004, pe29.

Scharschmidt, E., Wegener, E., Heissmeyer, V., Rao, A., and Krappmann, D. (2004). Degradation of Bcl10 induced by T-cell activation negatively regulates NF-kappa B signaling. Mol Cell Biol 24, 3860-3873.

2001

Muller, D.N., Heissmeyer, V., Dechend, R., Hampich, F., Park, J.K., Fiebeler, A., Shagdarsuren, E., Theuer, J., Elger, M., Pilz, B., Breu, V., Schroer, K., Ganten, D., Dietz, R., Haller, H., Scheidereit, C., and Luft, F.C. (2001). Aspirin inhibits NF-kappaB and protects from angiotensin II-induced organ damage. FASEB J 15, 1822-1824.

Heissmeyer, V., Krappmann, D., Hatada, E.N., and Scheidereit, C. (2001). Shared pathways of IkappaB kinase-induced SCF(betaTrCP)-mediated ubiquitination and degradation for the NF-kappaB precursor p105 and IkappaBalpha. Mol Cell Biol 21, 1024-1035.

Krappmann, D., Patke, A., Heissmeyer, V., and Scheidereit, C. (2001). B-cell receptor- and phorbol ester-induced NF-kappaB and c-Jun N-terminal kinase activation in B cells requires novel protein kinase C's. Mol Cell Biol 21, 6640-6650.

2000

Kordes, U., Krappmann, D., Heissmeyer, V., Ludwig, W.D., and Scheidereit, C. (2000). Transcription factor NF-kappaB is constitutively activated in acute lymphoblastic leukemia cells. Leukemia 14, 399-402.

1999

Heissmeyer, V., Krappmann, D., Wulczyn, F.G., and Scheidereit, C. (1999). NF-kappaB p105 is a target of IkappaB kinases and controls signal induction of Bcl-3-p50 complexes. EMBO J 18, 4766-4778.

Dechend, R., Hirano, F., Lehmann, K., Heissmeyer, V., Ansieau, S., Wulczyn, F.G., Scheidereit, C., and Leutz, A. (1999). The Bcl-3 oncoprotein acts as a bridging factor between NF-kappaB/Rel and nuclear co-regulators. Oncogene 18, 3316-3323.