Publications

Tavernier SJ, Athanasopoulos V, Verloo P, Behrens G, Staal J, Bogaert DJ, Naesens L, De Bruyne M, Van Gassen S, Parthoens E, Ellyard J, Cappello J, Morris LX, Van Gorp H, Van Isterdael G, Saeys Y, Lamkanfi M, Schelstraete P, Dehoorne J, Bordon V, Van Coster R, Lambrecht BN, Menten B, Beyaert R, Vinuesa CG, Heissmeyer V, Dullaers M, Haerynck F. A human immune dysregulation syndrome characterized by severe hyperinflammation with a homozygous nonsense Roquin-1 mutation. Nat Commun. 2019 Oct 21;10(1):4779. doi: 10.1038/s41467-019-12704-6.

von Gamm M, Schaub A, Jones AN, 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, Tschöp MH, Friedel CC, Hauck SM, Sattler M, Geerlof A, Hornung V, Heissmeyer V, Schulz C, Heikenwalder M, Glasmacher E. Immune homeostasis and regulation of the interferon pathway require myeloid-derived Regnase-3. J Exp Med. 2019 May 24. pii: jem.20181762. doi: 10.1084/jem.20181762. 

Borland K, Diesend J, Ito-Kureha T, Heissmeyer V, Hammann C, Buck AH, Michalakis S, Kellner S.
Genes (Basel). Production and Application of Stable Isotope-Labeled Internal Standards for RNA Modification Analysis. 2019 Jan 5;10(1). pii: E26. doi: 10.3390/genes10010026. 

•Essig K, Kronbeck N, Guimaraes JC, Lohs C, Schlundt A, Hoffmann A, Behrens G, Brenner S, Kowalska J, Lopez-Rodriguez C, Jemielity J, Holtmann H, Reiche K, Hackermüller J, Sattler M, Zavolan M, Heissmeyer V. Roquin targets mRNAs in a 3'-UTR-specific manner by different modes of regulation. Nat Commun. 2018 Sep 19;9(1):3810. doi: 10.1038/s41467-018-06184-3.

•Baumjohann D, Heissmeyer V. Posttranscriptional Gene Regulation of T Follicular Helper Cells by RNA-Binding Proteins and microRNAs. Front Immunol. 2018 Jul 31;9:1794. doi: 10.3389/fimmu.2018.01794. 

•Behrens G, Winzen R, Rehage N, Dörrie A, Barsch M, Hoffmann A, Hackermüller J, Tiedje C, Heissmeyer V, Holtmann H. A translational silencing function of MCPIP1/Regnase-1 specified by the target site context. Nucleic Acids Res. 2018 May 4;46(8):4256-4270. doi: 10.1093/nar/gky106. 

• Hoefig KP, Heissmeyer V. Posttranscriptional regulation of T helper cell fate decisions. J Cell Biol. 2018 Apr 23. doi: 10.1083/jcb.201708075. 

• Rehage N, Davydova E, Conrad C, Behrens G, Maiser A, Stehklein JE, Brenner S, Klein J, Jeridi A, Hoffmann A, Lee E, Dianzani U, Willemsen R, Feederle R, Reiche K, Hackermüller J, Leonhardt H, Sharma S, Niessing D, Heissmeyer V. Binding of NUFIP2 to Roquin promotes recognition and regulation of ICOS mRNA. Nat Commun. 2018 Jan 19;9(1):299. doi: 10.1038/s41467-017-02582-1. 

• Essig K, Hu D, Guimaraes JC, Alterauge D, Edelmann S, Raj T, Kranich J, Behrens G, Heiseke A, Floess S, Klein J, Maiser A, Marschall S, Hrabĕ de Angelis M, Leonhardt H, Calkhoven CF, Noessner E, Brocker T, Huehn J, Krug AB, Zavolan M, Baumjohann D, Heissmeyer V. Roquin Suppresses the PI3K-mTOR Signaling Pathway to Inhibit T Helper Cell Differentiation and Conversion of Treg to Tfr Cells. Immunity 2017, Volume 47, Issue 6, p1067-1082.e12. DOI: http://dx.doi.org/10.1016/j.immuni.2017.11.008

• Tagawa, T.*, Albanese, M.*, Bouvet, M., Moosmann, A., Mautner, J., Heissmeyer, V., Zielinski, C., Lutter, D., Hoser, J., Hastreiter, M., Hayes, M., Sugden, B., & Hammerschmidt, W. (2016). Epstein-Barr viral miRNAs inhibit antiviral CD4+ T cell responses targeting IL- 12 and peptide processing. J Exp Med, 213(10), 2065-2080. doi:10.1084/jem.20160248 (*equal author contribution).

• Janowski R, Heinz GA, Schlundt A, Wommelsdorf N, Brenner S, Gruber AR, Blank M, Buch T, Buhmann R, Zavolan M, Niessind D, Heissmeyer V, Sattler M. (2016) Roquin recognizes a non-canonial hexaloop structure in the 3-UTR of Ox40. Nat Commun 7, 11032.

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

• Meininger, I, Griesbach RA, Hu D, Gehring, T, Bertossi, A, Kranich, J, Oeckinghaus, A, Eitelhuber, AC, Greczmiel, U, Gewies, A, Schmidt-Supprian, M, Ruland, J, Brocker, T, Heissmeyer, V, Heyd, F, Krappmann, D. (2016) Alternative splicing of MALT1 controls signaling and activation of CD4+ T cells. Nat Commun. 2016 Apr 12;7:11929.

• Halle S, Keyser KA, Stahl FR, Busche A, Marquardt A, Zheng X, Galla M, Heissmeyer V, Heller K, Boelter J, Wagner K, Bischoff Y, Martens R, Braun A, Werth K, Uvarovski A, Kempf H, Meyer-Herrmann M, Arens R, Kremer M, Sutter G, Messerle M, Förster R. (2016) In Vivo Killing Capacity of Cytotoxic T Cells Is Limited and Involves Dynamic Interactions and T Cell Cooperativity. Immunity. 2016 Feb 16;44(2):233-45.

• Schlundt A, Niessing D, Heissmeyer V, Sattler M. (2016) RNA recognition by Roquin in posttranscriptional gene regulation. Wiley Interdiscip Rev RNA, 2016 Feb 4.

• Warth SC, Hoefig KP, Hiekel A, Schallenberg S, Jovanovic K, Klein L, Kretschmer K, Ansel KM, Heissmeyer V. 2015. Induced miR-99a expression represses Mtor cooperatively with miR-150 to promote regulatory T-cell differentiation. EMBO J 34: 1195-213

• Srivastava M, Duan G, Kershaw NJ, Athanasopoulos V, Yeo JH, Ose T, Hu D, Brown SH, Jergic S, Patel HR, Pratama A, Richards S, Verma A, Jones EY, Heissmeyer V, Preiss T, Dixon NE, Chong MM, Babon JJ, Vinuesa CG. 2015. Roquin binds microRNA-146a and Argonaute2 to regulate microRNA homeostasis. Nat Commun 6: 6253

• Martinez GJ, Pereira RM, Aijo T, Kim EY, Marangoni F, Pipkin ME, Togher S, Heissmeyer V, Zhang YC, Crotty S, Lamperti ED, Ansel KM, Mempel TR, Lahdesmaki H, Hogan PG, Rao A. 2015. The transcription factor NFAT promotes exhaustion of activated CD8(+) T cells. Immunity 42: 265-78

• Schlundt A, Heinz GA, Janowski R, Geerlof A, Stehle R, Heissmeyer V, Niessing D, Sattler M. 2014. Structural basis for RNA recognition in roquin-mediated post-transcriptional gene regulation. Nat Struct Mol Biol 21: 671-8

• Jeltsch KM, Hu D, Brenner S, Zoller J, Heinz GA, Nagel D, Vogel KU, Rehage N, Warth SC, Edelmann SL, Gloury R, Martin N, Lohs C, Lech M, Stehklein JE, Geerlof A, Kremmer E, Weber A, Anders HJ, Schmitz I, Schmidt-Supprian M, Fu M, Holtmann H, Krappmann D, Ruland J, Kallies A, Heikenwalder M, 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: 1079-89

• Hoefig KP, Heissmeyer V. 2014. Degradation of oligouridylated histone mRNAs: see UUUUU and goodbye. Wiley Interdiscip Rev RNA 5: 577-89

• Gewies A, Gorka O, Bergmann H, Pechloff K, Petermann F, Jeltsch KM, Rudelius M, Kriegsmann M, Weichert W, Horsch M, Beckers J, Wurst W, Heikenwalder M, Korn T, Heissmeyer V, Ruland J. 2014. Uncoupling Malt1 threshold function from paracaspase activity results in destructive autoimmune inflammation. Cell Rep 9: 1292-305

• Edelmann SL, Heissmeyer V. 2014. Tfh cell differentiation: missing Stat3 uncovers interferons' interference. Immunity 40: 307-9

• Warth SC, Heissmeyer V. 2013. Adenoviral transduction of naive CD4 T cells to study Treg differentiation. J Vis Exp

• Vogel KU, Edelmann SL, Jeltsch KM, Bertossi A, Heger K, Heinz GA, Zoller J, Warth SC, Hoefig KP, Lohs C, Neff F, Kremmer E, Schick J, Repsilber D, Geerlof A, Blum H, Wurst W, Heikenwalder M, Schmidt-Supprian M, 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: 655-68

• Pesic M, Bartholomaus I, Kyratsous NI, Heissmeyer V, Wekerle H, Kawakami N. 2013. 2-photon imaging of phagocyte-mediated T cell activation in the CNS. J Clin Invest 123: 1192-201

• Hoefig KP, Rath N, Heinz GA, Wolf C, Dameris J, Schepers A, Kremmer E, Ansel KM, Heissmeyer V. 2013. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nat Struct Mol Biol 20: 73-81

• Heissmeyer V, Vogel KU. 2013. Molecular control of Tfh-cell differentiation by Roquin family proteins. Immunol Rev 253: 273-89

• Canis M, Lechner A, Mack B, Zengel P, Laubender RP, Koehler U, Heissmeyer V, Gires O. 2013. CD133 induces tumour-initiating properties in HEK293 cells. Tumour Biol 34: 437-43

• Burger K, Muhl B, Rohrmoser M, Coordes B, Heidemann M, Kellner M, Gruber-Eber A, Heissmeyer V, Strasser K, Eick D. 2013. Cyclin-dependent kinase 9 links RNA polymerase II transcription to processing of ribosomal RNA. J Biol Chem 288: 21173-83

• Bronevetsky Y, Villarino AV, Eisley CJ, Barbeau R, Barczak AJ, Heinz GA, Kremmer E, Heissmeyer V, McManus MT, Erle DJ, Rao A, Ansel KM. 2013. T cell activation induces proteasomal degradation of Argonaute and rapid remodeling of the microRNA repertoire. J Exp Med 210: 417-32

• Thomas MF, Abdul-Wajid S, Panduro M, Babiarz JE, Rajaram M, Woodruff P, Lanier LL, Heissmeyer V, Ansel KM. 2012. Eri1 regulates microRNA homeostasis and mouse lymphocyte development and antiviral function. Blood 120: 130-42

• Frohn A, Eberl HC, Stohr J, Glasmacher E, Rudel S, Heissmeyer V, Mann M, Meister G. 2012. Dicer-dependent and -independent Argonaute2 protein interaction networks in mammalian cells. Mol Cell Proteomics 11: 1442-56

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

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

• Parameswaran P, Sklan E, Wilkins C, Burgon T, Samuel MA, Lu R, Ansel KM, Heissmeyer V, Einav S, Jackson W, Doukas T, Paranjape S, Polacek C, dos Santos FB, Jalili R, Babrzadeh F, Gharizadeh B, Grimm D, Kay M, Koike S, Sarnow P, Ronaghi M, Ding SW, Harris E, Chow M, Diamond MS, Kirkegaard K, Glenn JS, Fire AZ. 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

• Hoefig KP, Heissmeyer V. 2010. Measuring microRNA expression in size-limited FACS-sorted and microdissected samples. Methods Mol Biol 667: 47-63

• Glasmacher E, Hoefig KP, Vogel KU, Rath N, Du L, Wolf C, Kremmer E, Wang X, Heissmeyer V. 2010. Roquin binds inducible costimulator mRNA and effectors of mRNA decay to induce microRNA-independent post-transcriptional repression. Nat Immunol 11: 725-33

• Hoefig KP, Heissmeyer V. 2008. MicroRNAs grow up in the immune system. Curr Opin Immunol 20: 281-7

• Heissmeyer V, Rao A. 2008. Itching to end NF-kappaB. Nat Immunol 9: 227-9

• Ansel KM, Pastor WA, Rath N, Lapan AD, Glasmacher E, Wolf C, Smith LC, Papadopoulou N, Lamperti ED, Tahiliani M, Ellwart JW, Shi Y, Kremmer E, Rao A, Heissmeyer V. 2008. Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat Struct Mol Biol 15: 523-30

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

• Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L, Rao A. 2006. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126: 375-87

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

• Borde M, Barrington RA, Heissmeyer V, Carroll MC, Rao A. 2006. Transcriptional basis of lymphocyte tolerance. Immunol Rev 210: 105-19

• Oberdoerffer P, Kanellopoulou C, Heissmeyer V, Paeper C, Borowski C, Aifantis I, Rao A, Rajewsky K. 2005. Efficiency of RNA interference in the mouse hematopoietic system varies between cell types and developmental stages. Mol Cell Biol 25: 3896-905

• Heissmeyer V, Macian F, Varma R, Im SH, Garcia-Cozar F, Horton HF, Byrne MC, Feske S, Venuprasad K, Gu H, Liu YC, Dustin ML, Rao A. 2005. A molecular dissection of lymphocyte unresponsiveness induced by sustained calcium signalling. Novartis Found Symp 267: 165-74; discussion 74-9

• Heissmeyer V, Ansel KM, Rao A. 2005. A plague of autoantibodies. Nat Immunol 6: 642-4

• Scharschmidt E, Wegener E, Heissmeyer V, Rao A, Krappmann D. 2004. Degradation of Bcl10 induced by T-cell activation negatively regulates NF-kappa B signaling. Mol Cell Biol 24: 3860-73

• Kobori M, Yang Z, Gong D, Heissmeyer V, Zhu H, Jung YK, Gakidis MA, Rao A, Sekine T, Ikegami F, Yuan C, Yuan J. 2004. Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK complex. Cell Death Differ 11: 123-30

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

• Heissmeyer V, Macian F, Im SH, Varma R, Feske S, Venuprasad K, Gu H, Liu YC, Dustin ML, Rao A. 2004. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat Immunol 5: 255-65

• Muller DN, Heissmeyer V, Dechend R, Hampich F, Park JK, Fiebeler A, Shagdarsuren E, Theuer J, Elger M, Pilz B, Breu V, Schroer K, Ganten D, Dietz R, Haller H, Scheidereit C, Luft FC. 2001. Aspirin inhibits NF-kappaB and protects from angiotensin II-induced organ damage. FASEB J 15: 1822-4

• Krappmann D, Patke A, Heissmeyer V, 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: 6640-50

• Heissmeyer V, Krappmann D, Hatada EN, 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: 1024-35

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

• Heissmeyer V, Krappmann D, Wulczyn FG, Scheidereit C. 1999. NF-kappaB p105 is a target of IkappaB kinases and controls signal induction of Bcl-3-p50 complexes. EMBO J 18: 4766-78

• Dechend R, Hirano F, Lehmann K, Heissmeyer V, Ansieau S, Wulczyn FG, Scheidereit C, Leutz A. 1999. The Bcl-3 oncoprotein acts as a bridging factor between NF-kappaB/Rel and nuclear co-regulators. Oncogene 18: 3316-23