Publications of the laboratory cardiac infection biology and immunology

Böhnke, Janik, Pinkert, Sandra, Schmidt, Maria, Binder, Hans, Bilz, Nicole Christin, Jung, Matthias, Reibetanz, Uta, Beling, Antje, Rujescu, Dan, Claus, Claudia
Coxsackievirus B3 Infection of Human iPSC Lines and Derived Primary Germ-Layer Cells Regarding Receptor Expression.
Int J Mol Sci. 2021 Jan 27;22(3):1220.doi: 10.3390/ijms22031220

Pinkert, Sandra, Kespohl, Meike, Kelm, Nicolas, Kaya, Ziya, Heuser, Arnd, Klingel, Karin, Beling, Antje
Exploration of Analgesia with Tramadol in the Coxsackievirus B3 Myocarditis Mouse Model.
Viruses. 2021 Jun 24;13(7):1222.doi: 10.3390/v13071222.

Hazini, Ahmet, Dieringer, Babette, Pryshliak, Markian, Knoch, Klaus-Peter, Heimann, Lisanne, Tolksdorf, Beatrice, Pappritz, Kathleen, El-Shafeey, Muhammad, Solimena, Michele, Beling, Antje, Kurreck, Jens, Klingel, Karin, Fechner, Henry
miR-375- and miR-1-Regulated Coxsackievirus B3 Has No Pancreas and Heart Toxicity But Strong Antitumor Efficiency in Colorectal Carcinomas.
Hum Gene Ther. 2021 Feb;32(3-4):216-230.doi: 10.1089/hum.2020.228. Epub 2021 Jan 22.

Goetzke, Carl Christoph, Althof, Nadine, Neumaier, Hannah Louise, Heuser, Arndt, Kaya, Ziya, Kespohl, Meike, Klingel, Karin, Beling, Antje
Mitigated viral myocarditis in A/J mice by the immunoproteasome inhibitor ONX 0914 depends on inhibition of systemic inflammatory responses in CoxsackievirusB3 infection.
Basic Res Cardiol. 2021 Feb 1;116(1):7.doi: 10.1007/s00395-021-00848-w.

Voss M, Braun V, Bredow C, Kloetzel PM, Beling Antje
Coxsackievirus B3 Exploits the Ubiquitin-Proteasome System to Facilitate Viral Replication.
Viruses 2021;13(7):1360. doi: 10.3390/v13071360. PMID: 34372566

Munnur D, Teo Q, Eggermont D, Lee HHY, Thery F, Ho J, van Leur SW, Ng WWS, Siu LYL, Beling A, Ploegh H, Pinto-Fernandez A, Damianou A, Kessler B, Impens F, Mok CKP, Sanyal S.
Altered ISGylation drives aberrant macrophage-dependent immune responses during SARS-CoV-2 infection.
Nature Immunology 2021;22(11):1416-1427. doi: 10.1038/s41590-021-01035-8 PMID: 34663977

Thery F, Martina L, Asselman C, Zhang Y, Vessely M, Repo H, Sedeyn K, Moschonas GD, Bredow C, Teo QW, Zhang J, Leandro K, Eggermont D, De Sutter D, Boucher K, Hochepied T, Festjens N, Callewaert N, Saelens X, Dermaut B, Knobeloch KP, Beling A, Sanyal S, Radoshevich L, Eyckerman S, Impens F.
Ring finger protein 213 assembles into a sensor for ISGylated proteins with antimicrobial activity.
Nature Communications 2021;12(1):5772. doi: 10.1038/s41467-021-26061-w. PMID: 34599178

Neumaier HL, Harel S, Klingel K, Kaya Z, Heuser A, Kespohl M, Beling:
ONX 0914 Lacks Selectivity for the Cardiac Immunoproteasome in CoxsackievirusB3 Myocarditis of NMRI Mice and Promotes Virus-Mediated Tissue Damage.
Cells. 2020 Apr 28;9(5):E1093. doi: 10.3390/cells9051093

Bockstahler M, Fischer A, Goetzke CC, Neumaier HL, Sauter M, Kespohl M, Müller AM, Meckes C, Salbach C, Schenk M, Heuser A, Landmesser U, Weiner J, Meder B, Lehmann L, Kratzer A, Klingel K, Katus HA, Kaya Z, Beling A:
Heart-specific immune responses in an animal model of autoimmune-related myocarditis mitigated by an immunoproteasome inhibitor and genetic ablation.
Circulation 2020. doi: 10.1161/CIRCULATIONAHA.119.043171.

Kespohl M, Bredow C, Klingel K, Voß M, Paeschke A, Zickler M, Poller W, Kaya Z, Eckstein J, Fechner H, Spranger J, Fähling M, Wirth EK, Radoshevich L, Thery F, Impens F, Berndt N, Knobeloch KP, Beling A:
Protein modification with ISG15 blocks Coxsackievirus pathology by antiviral and metabolic reprogramming.
Science Advances (Sci Adv.) 2020; 6(11):eaay1109. doi: 10.1126/sciadv.aay1109

Pinkert S, Kopp A, Brückner V, Fechner H, Beling A.:
Single point mutations within the Coxsackie B virus receptor-binding site promote resistance against soluble virus receptor traps. Journal of Virology 2020, 94(19):e00952-20. doi: 10.1128/JVI.00952-20

Zhang Y, Thery F, Wu NC, Luhmann EK, Dussurget O, Foecke M, Bredow C, Jiménez-Fernández D, Leandro K, Beling A, Knobeloch KP, Impens F, Cossart P, Radoshevich L:
The in vivo ISGylome links ISG15 to metabolic pathways and autophagy upon Listeria monocytogenes infection.
Nat Commun. 2019 Nov 26;10(1):5383. doi: 10.1038/s41467-019-13393-x.

Pinkert S, Dieringer B, Klopfleisch R, Savvatis K, Van Linthout S, Pryshliak M, Tschöpe C, Klingel K, Kurreck J, Beling A, Fechner H:
Early Treatment of Coxsackievirus B3-Infected Animals With Soluble Coxsackievirus-Adenovirus Receptor Inhibits Development of Chronic Coxsackievirus B3 Cardiomyopathy.
Circ Heart Fail. 2019 Nov;12(11):e005250. doi: 10.1161/CIRCHEARTFAILURE.119.005250. Epub 2019 Nov 13.

Pinkert S, Pryshliak M, Pappritz K, Knoch K, Hazini A, Dieringer B, Schaar K, Dong F, Hinze L, Lin J, Lassner D, Klopfleisch R, Solimena M, Tschöpe C, Kaya Z, Beling A, Kurreck J, van Linthout S, Klingel K, Fechner H:
Development of a New Mouse Model for Coxsackievirus-Induced Myocarditis by Attenuating Coxsackievirus B3 Virulence in the Pancreas.
Cardiovasc Res. 2019 Oct 9. pii: cvz259. doi: 10.1093/cvr/cvz259. [Epub ahead of print]

Napolitano A, van der Veen AG, Bunyan M, Borg A, Frith D, Howell S, Kjaer S, Beling A, Snijders AP, Knobeloch KP, Frickel EM:
Cysteine-Reactive Free ISG15 Generates IL-1β-Producing CD8α+ Dendritic Cells at the Site of Infection.
J Immunol. 2018 Jun 11. pii: ji1701322. doi: 10.4049/jimmunol.1701322. [Epub ahead of print]

Althof N, Goetzke CC, Kespohl M, Voss K, Heuser A, Pinkert S, Kaya Z, Klingel K, Beling A:
The immunoproteasome-specific inhibitor ONX 0914 reverses susceptibility to acute viral myocarditis.
EMBO Mol Med. 2018;10(2):200-218

Loebel M, Holzhauser L, Hartwig JA, Shukla PC, Savvatis K, Jenke A, Gast M, Escher F, Becker SC, Bauer S, Stroux A, Beling A, Kespohl M, Pinkert S, Fechner H, Kuehl U, Lassner D, Poller W, Schultheiss HP, Zeller T, Blankenberg S, Papageorgiou AP, Heymans S, Landmesser U, Scheibenbogen C, Skurk C:
The forkhead transcription factor Foxo3 negatively regulates natural killer cell function and viral clearance in myocarditis.
Eur Heart J. 2018; 39(10):876-887.

Beling A, Kespohl M:
Proteasomal Protein Degradation: Adaptation of Cellular Proteolysis With Impact on Virus-and Cytokine-Mediated Damage of Heart Tissue During Myocarditis.
Frontiers in Immunology 9. DOI: org/10.3389/fimmu.2018.02620

Meyer IS, Goetzke CC, Kespohl M, Sauter M, Heuser A, Eckstein V, Vornlocher H-P, Anderson DG, Haas J, Meder B, Katus HA, Klingel K, Beling A*, Leuschner F*:
Silencing the CSF-1 Axis Using Nanoparticle Encapsulated siRNA Mitigates Viral and Autoimmune Myocarditis.
Frontiers in Immunology 9:2303. DOI: 10.3389/fimmu.2018.02303.9
* equal senior authorship, corresponding author 

Respondek D, Voss M, Kühlewindt I, Klingel K, Krüger E, Beling A. PA28 modulates antigen processing and viral replication during coxsackievirus B3 infection. PLoS One. 2017 Mar 9;12(3):e0173259. doi: 10.1371/journal.pone.0173259. eCollection 2017. PMID: 28278207

Spur EM, Althof N, Respondek D, Klingel K, Heuser A, Overkleeft HS, Voigt A. Inhibition of chymotryptic-like standard proteasome activity exacerbates doxorubicin-induced cytotoxicity in primary cardiomyocytes. Toxicology. 2016 May 4. pii: S0300-483X(16)30040-3. PMID: 27155237.

Gast M, Schroen B, Voigt A, Haas J, Kuehl U, Lassner D, Skurk C, Escher F, Wang X, Kratzer A, Michalik K, Papageorgiou A, Peters T, Loebel M, Wilk S, Althof N, Prasanth KV, Katus H, Meder B, Nakagawa S, Scheibenbogen C, Schultheiss HP, Landmesser U, Dimmeler S, Heymans S, Poller W. Long noncoding RNA MALAT1-derived mascRNA is involved in cardiovascular innate immunity. J Mol Cell Biol. 2016; pii: mjw003. PMID: 26823496.

Spur EM, Althof N, Respondek D, Klingel K, Heuser A, Overkleeft HS, Voigt A. Inhibition of chymotryptic-like standard proteasome activity exacerbates doxorubicin-induced cytotoxicity in primary cardiomyocytes. Toxicology. 2016 May 4. pii: S0300-483X(16)30040-3. PMID: 27155237.

Gast M, Schroen B, Voigt A, Haas J, Kuehl U, Lassner D, Skurk C, Escher F, Wang X, Kratzer A, Michalik K, Papageorgiou A, Peters T, Loebel M, Wilk S, Althof N, Prasanth KV, Katus H, Meder B, Nakagawa S, Scheibenbogen C, Schultheiss HP, Landmesser U, Dimmeler S, Heymans S, Poller W. Long noncoding RNA MALAT1-derived mascRNA is involved in cardiovascular innate immunity. J Mol Cell Biol. 2016; pii: mjw003. PMID: 26823496.

Mishto M, Liepe J, Textoris-Taube K, Keller C, Henklein P, Weberruß M, Dahlmann B, Enenkel C, Voigt A, Kuckelkorn U, Stumpf MP, Kloetzel PM. Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur J Immunol. 2014; 44(12):3508-21. PMID: 25231383.

Rahnefeld A, Klingel K, Schuermann A, Diny NL, Althof N, Lindner A, Bleienheuft P, Savvatis K, Respondek D, Opitz E, Ketscher L, Sauter M, Seifert U, Tschöpe C, Poller W, Knobeloch KP, Voigt A. Ubiquitin-like protein ISG15 in host defense against heart failure in a mouse model of virus-induced cardiomyopathy. Circulation 2014; 130:1589-1600. PMID: 25165091.

Voigt A, Rahnefeld A, Kloetzel PM and Krüger E. Cytokine-induced oxidative stress in cardiac inflammation and heart failure – how the ubiquitin proteasome system targets this vicious cycle. Front Physiol. 2013; 4:42. PMID: 23508734.

Ebstein F*, Voigt A*, Lange N, Warnatsch A, Schröter F, Prozorovski T, Kuckelkorn U, Aktas O, Seifert U, Kloetzel PM, Krüger E. Immunoproteasomes Are Important for Proteostasis in Immune Responses. Cell 2013; 152:935-937. PMID: 23452842. *equal contribution.

Opitz E, Koch A, Klingel K, Schmidt F, Prokop S, Rahnefeld A, Sauter M, Heppner F, Völker U, Kandolf R, Kuckelkorn U, Stangl K, Krüger E, Kloetzel PM, Voigt A. Impairment of immunoproteasome function by beta5i/LMP7 subunit deficiency results in severe enterovirus myocarditis. PLoS Pathog. 2011; 7(9):e1002233. PMID: 21909276.

Rahnefeld A, Ebstein F, Albrecht N, Opitz E, Kuckelkorn U, Stangl K, Rehm A, Kloetzel PM, Voigt A. Antigen Presentation Capacity of Dendritic Cells is Impaired in Ongoing Enterovirus-Myocarditis. Eur J Immunol. 2011; 41(9):2774-81. PMID: 21630249.

Voigt A, Elgeti T, Durmus T, Idiz ME, Butler C, Beling M, Schilling R, Klingel K, Kandolf R, Stangl K, Taupitz M, Kivelitz D, Wagner M. Cardiac Magnetic Resonance in Dilated Cardiomyopathy in Adults – Towards Identification of Myocardial Inflammation. Eur Radiol. 2011; 21(5):925-35. PMID: 20963443.

Seifert U, Bialy LP, Ebstein F, Bech-Otschir D, Voigt A, Schröter F, Prozorovski T, Lange L, Steffen J, Rieger M, Kuckelkorn U, Aktas O, Kloetzel PM, Krüger E. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell. 2010; 142(4):613-24.

Voigt A, Trimpert C, Bartel K, Egerer K, Feist E, Gericke C, Kandolf R, Klingel K, Kuckelkorn U, Stangl K, Felix SB, Baumann G, Kloetzel PM, Staudt A. Lack of Evidence for a Pathogenic Role of Proteasome-Directed Autoimmunity in Dilated Cardiomyopathy. Basic Res Cardiol. 2010; 105(4):557-67. PMID: 20336303.

Voigt A, Jaekel S, Textoris-Taube K, Keller C, Drung I, Szalay G, Klingel K, Henklein P, Stangl K, Kloetzel PM, Kuckelkorn U. Generation of in silico predicted Coxsackievirus B3-derived MHC class I epitopes by proteasomes. Amino Acids. 2010; 39(1):243-55. PMID: 19997756.

Voigt A, Bartel K, Egerer K, Trimpert C, Feist E, Gericke C, Kandolf R, Klingel K, Kuckelkorn U, Stangl K, Felix SB, Baumann G, Kloetzel PM, Staudt A. Humoral anti-proteasomal autoimmunity in dilated cardiomyopathy. Basic Res Cardiol. 2010; 105(1):9-18. PMID: 19760349.

Wagner W, Butler C, Rief M, Voigt A, Beling M, Durmus T, Huppertz A, Baumann G, Hamm B, Lembcke A, Vogtmann T. Comparison of Non gated versus ECG-gated 64-Detector Row Computed Tomography for Integrated Electroanatomic Mapping in Patients Undergoing Pulmonary Vein Isolation. Europace 2010; 12:1090-1097.

2009

Jäkel S, Kuckelkorn U, Szalay G, Plötz M, Textoris-Taube K, Opitz E, Klingel K, Stevanovic S, Kandolf R, Kotsch K, Stangl K, Kloetzel PM, Voigt A. Differential interferon responses enhance viral epitope generation by myocardial immunoproteasomes in murine enterovirus myocarditis. Am J Pathol. 2009; 175(2):510-8. PMID: 19590042.

2008

Strehl B, Textoris-Taube K, Jäkel S, Voigt A, Henklein P, Steinhoff U, Kloetzel PM, Kuckelkorn U. Antitopes define preferential proteasomal cleavage site usage. J Biol Chem. 2008; 283(26):17891-7. PMID: 18424434.

2007

Voigt A, Salzmann U, Seifert U, Dathe M, Soza A, Kloetzel PM, Kuckelkorn U. 20S proteasome-dependent generation of an IEpp89 murine cytomegalovirus-derived H-2L(d) epitope from a recombinant protein. Biochem Biophys Res Commun. 2007; 355(2):549-54. PMID: 17303071.

2006

Szalay G*, Meiners S*, Voigt A*, Lauber J, Spieth C, Speer N, Sauter M, Kuckelkorn U, Zell A, Klingel K, Stangl K, Kandolf R. Ongoing coxsackievirus myocarditis is associated with increased formation and activity of myocardial immunoproteasomes. Am J Pathol. 2006; 168(5):1542-52. PMID: 16651621. * equal contribution.

2005

Wang Q, Sanad W, Miller LM, Voigt A, Klingel K, Kandolf R, Stangl K and Baumann G. Infrared imaging of compositional changes in inflammatory cardiomyopathy. Vibrational Spectroscopy, Volume 38, Issues 1–2, 2005, 217-222.