Publications

Ehle C, Iyer-Bierhoff A, Wu Y, Xing S, Kiehntopf M, Mosig AS, Godmann M, Heinzel T (2024) Downregulation of HNF4A enables transcriptomic reprogramming during the hepatic acute-phase response. Comms Bio, doi:10.1038/s42003-024-06288-1.

Zahel P, Bruggink V, Hülsmann J, Steiniger F, Hofstetter, RK, Heinzel T, Beekmann U, Werz O, Kralisch D (2024) Exploring Microemulsion Systems for the Incorporation of Glucocorticoids into Bacterial Cellulose: A Novel Approach for Anti-Inflammatory Wound Dressings. Pharmaceutics 16, 504; doi: 10.3390/pharmaceutics16040504.

Iyer-Bierhoff A, Wieczorek M, Peter SM, Ward D, Bens M, Vettorazzi S, Guehrs KH, Tuckermann JP, Heinzel T (2024) Acetylation-induced proteasomal degradation of the activated glucocorticoid receptor limits hormonal signaling. iScience 27, 108943; doi: 10.1016/j.isci.2024.108943.
Also see here: https://www.uni-jena.de/en/all-news/acetylation-a-time-keeper-of-glucocorticoid-sensitivity

Hülsmann J, Lindemann H, Wegener J, Kühne M, Godmann M, Koschella A, Coldewey SM, Heinze T, Heinzel T (2023) Dually Modified Cellulose as a Non-Viral Vector for the Delivery and Uptake of HDAC3 siRNA. Pharmaceutics 15, 2659.
https://doi.org/10.3390/pharmaceutics15122659External link

Rao Z, Brunner E, Giszas B, Iyer-Bierhoff A, Gerstmeier J, Börner F, Jordan PM, Pace S, Meyer KPL, Hofstetter RK, Merk D, Paulenz C, Heinzel T, Grunert PC, Stallmach A, Serhan CN, Werner M, Werz O (2023) Glucocorticoids regulate lipid mediator networks by reciprocal modulation of 15-lipoxygenase isoforms affecting inflammation resolution. Proc. Natl. Acad. Sci. USA, 120 (35) e2302070120.
https://doi.org/10.1073/pnas.2302070120External link
Also see here: https://www.uni-jena.de/en/all-news/timing-is-key

Wu Y, He Y, Liu C, Ehle C, Iyer-Bierhoff A, Liu B, Heinzel T, Xing S (2023) Histone deacetylase inhibitor (SAHA) reduces mortality in septic mice by suppressing glycolysis. Int. J. Mol. Sci., 24, 12448.
https://doi.org/10.3390/ijms241512448External link

Kühne M, Hofmann S, Lindemann H, Cseresnyes Z, Dzierza A, Schröder D, Godmann M, Koschella A, Eggeling C, Fischer D, Figge MT, Heinze T, Heinzel T (2023) Analysis of HDACi-Coupled Nanoparticles: Opportunities and Challenges. Methods in Molecular Biology 2589, 129-144.

Lindemann H, Kühne M, Koschella A, Godmann M, Heinzel T, Heinze T (2023) HDACi Delivery Systems Based on Cellulose Valproate Nanoparticles. Methods in Molecular Biology 2589, 195-205.

Marx C, Sonnemann J, Maddocks ODK, Marx-Blümel L, Beyer M, Hoelzer D, Thierbach R, Maletzki C, Linnebacher M, Heinzel T, Krämer OH (2022) Global metabolic alterations in colorectal cancer cells during irinotecan-induced DNA replication stress. Cancer Metab. 10, DOI: 10.1186/s40170-022-00286-9.

Marx C, Sonnemann J, Maddocks ODK, Lilla S, Beyer M, Hauzenberger I, Piée-Staffa A, Siniuk K, Nunna S, Marx-Blümel L, Westermann M, Wagner T, Hoelzer D, Thierbach R, Mullins CS, Kdimati S, Linnebacher M, Neri F, Heinzel T, Wang ZQ, Krämer OH (2021) Mechanistic insights into a p53-regulated cytotoxicity of entinostat and irinotecan against colorectal cancer cells. Mol. Oncol. 15, 3404-3429.

Schalk F, Fricke J, Um S, Conlon BH, Maus H, Jäger N, Heinzel T, Schirmeister T, Poulsen M, Beemelmanns C (2021) GNPS-guided discovery of xylacremolide C and D, evaluation of their putative biosynthetic origin and bioactivity studies of xylacremolide A and B. RSC Adv. 11, 18748-18756, DOI: 10.1039/d1ra00997d.

Göder A, Ginter T, Heinzel T, Stroh, S, Fahrer, J, Henke A, Krämer OH (2021) STAT1 N-terminal domain discriminatively controls type I and type II IFN signaling. Cytokine, 144, 155552, DOI:10.1016/j.cyto.2021.155552.

Kühne M, Kretzer C, Lindemann H, Godmann M, Heinze T, Werz O, Heinzel T (2021) Biocompatible valproic acid-coupled nanoparticles attenuate lipopolysaccharide-induced inflammation. Int. J. Pharmaceutics, 601:120567. DOI: 10.1016/j.ijpharm.2021.120567. Online ahead of print. PMID: 33812975.

Kühne M, Lindemann H, Grune C, Schröder D, Cseresnyés Z, Godmann M, Koschella A,  Figge MT, Eggeling C, Fischer D, Heinze T, Heinzel T (2021) Biocompatible sulfated valproic acid-coupled polysaccharide-based nanocarriers with HDAC inhibitory activity. J. Controlled Release 329, 717-730, DOI: 10.1016/j.jconrel.2020.10.006.

Liu X, Schneble-Löhnert N, Kristofova M, Qing X, Labisch J, Hofmann S, Ehrenberg S, Sannai M, Jörß T, Ori A, Godmann M, Wang ZQ. (2021) The N-terminal BRCT domain determines MCPH1 function in brain development and fertility. Cell Death Dis. 2021 Feb 1; 12(2):143. doi: 10.1038/s41419-021-03406-3. PMID: 33542216

Lindemann H, Kühne M, Grune C, Warncke P, Hofmann S, Koschella A, Godmann M, Fischer D, Heinzel T, Heinze T (2020) Polysaccharide Nanoparticles Bearing HDAC Inhibitor as Nontoxic Nanocarrier for Drug Delivery. Macromol. Biosci. 20, 2000039

Balakrishnan P, Liebe T, Amro E, Dhaka L, Heinzel T, Heller R (2019) Metabolic stress – signaling and metabolic adaptation. The Science of Hormesis in Health and Longevity, pp. 139-148.

Fischer, J., Müller, S.Y., Netzker, T., Jäger, N., Gacek-Matthews, A., Scherlach, K., Stroe, M.C., García-Altares, M., Pezzini, F., Schoeler, H., et al. (2018). Chromatin mapping identifies BasR, a key regulator of bacteria-triggered production of fungal secondary metabolites. Elife 7. DOI: 10.7554/eLife.40969External link

Göder, A., Emmerich, C., Nikolova, T., Kiweler, N., Schreiber, M., Kühl, T., Imhof, D., Christmann, M., Heinzel, T., Schneider, G., et al. (2018). HDAC1 and HDAC2 integrate checkpoint kinase phosphorylation and cell fate through the phosphatase-2A subunit PR130. Nat Commun 9, 764.

Kosan, C., Heidel, F.H., Godmann, M., and Bierhoff, H. (2018). Epigenetic Erosion in Adult Stem Cells: Drivers and Passengers of Aging. Cells 7.

Kiweler, N., Brill, B., Wirth, M., Breuksch, I., Laguna, T., Dietrich, C., Strand, S., Schneider, G., Groner, B., Butter, F., et al. (2018). The histone deacetylases HDAC1 and HDAC2 are required for the growth and survival of renal carcinoma cells. Arch. Toxicol. 92, 22272243.

Marx, C., Marx-Blümel, L., Lindig, N., Thierbach, R., Hoelzer, D., Becker, S., Wittig, S., Lehmann, R., Slevogt, H., Heinzel, T., et al. (2018). The sirtuin 1/2 inhibitor tenovin-1 induces a nonlinear apoptosis-inducing factor-dependent cell death in a p53 null Ewings sarcoma cell line. Invest New Drugs 36, 396406.

Pons, M., Reichardt, C.M., Hennig, D., Nathan, A., Kiweler, N., Stocking, C., Wichmann, C., Christmann, M., Butter, F., Reichardt, S., et al. (2018). Loss of Wilms tumor 1 protein is a marker for apoptosis in response to replicative stress in leukemic cells. Arch. Toxicol. 92, 21192135.

Rauch, A., Carlstedt, A., Emmerich, C., Mustafa, A.-H.M., Göder, A., Knauer, S.K., Linnebacher, M., Heinzel, T., and Krämer, O.H. (2018). Survivin antagonizes chemotherapy-induced cell death of colorectal cancer cells. Oncotarget 9, 2783527850.

Mahendrarajah, N., Borisova, M.E., Reichardt, S., Godmann, M., Sellmer, A., Mahboobi, S., Haitel, A., Schmid, K., Kenner, L., Heinzel, T., et al. (2017). HSP90 is necessary for the ACK1-dependent phosphorylation of STAT1 and STAT3. Cell. Signal. 39, 917.

Noack, K., Mahendrarajah, N., Hennig, D., Schmidt, L., Grebien, F., Hildebrand, D., Christmann, M., Kaina, B., Sellmer, A., Mahboobi, S., et al. (2017). Analysis of the interplay between all-trans retinoic acid and histone deacetylase inhibitors in leukemic cells. Arch. Toxicol. 91, 21912208.

Schäfer, C., Göder, A., Beyer, M., Kiweler, N., Mahendrarajah, N., Rauch, A., Nikolova, T., Stojanovic, N., Wieczorek, M., Reich, T.R., et al. (2017). Class I histone deacetylases regulate p53/NF-κB crosstalk in cancer cells. Cell. Signal. 29, 218225.

Wagner, T., Godmann, M., and Heinzel, T. (2017). Analysis of Histone Deacetylases Sumoylation by Immunoprecipitation Techniques. Methods Mol. Biol. 1510, 339351.

Wieczorek, M., Gührs, K.-H., and Heinzel, T. (2017). Assessment of HDACi-Induced Acetylation of Nonhistone Proteins by Mass Spectrometry. Methods Mol. Biol. 1510, 313327.

Kosan, C., and Godmann, M. (2016). Genetic and Epigenetic Mechanisms That Maintain Hematopoietic Stem Cell Function. Stem Cells Int 2016, 5178965.

Hennig, D., Müller, S., Wichmann, C., Drube, S., Pietschmann, K., Pelzl, L., Grez, M., Bug, G., Heinzel, T., and Krämer, O.H. (2015). Antagonism between granulocytic maturation and deacetylase inhibitor-induced apoptosis in acute promyelocytic leukaemia cells. Br. J. Cancer 112, 329337.

Wagner, T., Kiweler, N., Wolff, K., Knauer, S.K., Brandl, A., Hemmerich, P., Dannenberg, J.-H., Heinzel, T., Schneider, G., and Krämer, O.H. (2015). Sumoylation of HDAC2 promotes NF-κB-dependent gene expression. Oncotarget 6, 71237135.

Siklenka, K., Erkek, S., Godmann, M., Lambrot, R., McGraw, S., Lafleur, C., Cohen, T., Xia, J., Suderman, M., Hallett, M., et al. (2015). Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350, aab2006.

Ginter, T., Fahrer, J., Kröhnert, U., Fetz, V., Garrone, A., Stauber, R.H., Reichardt, W., Müller-Newen, G., Kosan, C., Heinzel, T., et al. (2014). Arginine residues within the DNA binding domain of STAT3 promote intracellular shuttling and phosphorylation of STAT3. Cell. Signal. 26, 16981706.

Hennig, D., Schubert, S., Dargatz, H., Kostenis, E., Fahr, A., Schubert, U.S., Heinzel, T., and Imhof, D. (2014). Novel insights into appropriate encapsulation methods for bioactive compounds into polymers: a study with peptides and HDAC inhibitors. Macromol Biosci 14, 6980.

Licht, V., Noack, K., Schlott, B., Förster, M., Schlenker, Y., Licht, A., Krämer, O.H., and Heinzel, T. (2014). Caspase-3 and caspase-6 cleave STAT1 in leukemic cells. Oncotarget 5, 23052317.

Müller, S., Chen, Y., Ginter, T., Schäfer, C., Buchwald, M., Schmitz, L.M., Klitzsch, J., Schütz, A., Haitel, A., Schmid, K., et al. (2014). SIAH2 antagonizes TYK2-STAT3 signaling in lung carcinoma cells. Oncotarget 5, 31843196.

Rauch, A., Hennig, D., Schäfer, C., Wirth, M., Marx, C., Heinzel, T., Schneider, G., and Krämer, O.H. (2014). Survivin and YM155: how faithful is the liaison? Biochim. Biophys. Acta 1845, 202220.

Wagner, T., Brand, P., Heinzel, T., and Krämer, O.H. (2014). Histone deacetylase 2 controls p53 and is a critical factor in tumorigenesis. Biochim. Biophys. Acta 1846, 524538.

Buchwald, M., Pietschmann, K., Brand, P., Günther, A., Mahajan, N.P., Heinzel, T., and Krämer, O.H. (2013). SIAH ubiquitin ligases target the nonreceptor tyrosine kinase ACK1 for ubiquitinylation and proteasomal degradation. Oncogene 32, 49134920.

Ginter, T., Heinzel, T., and Krämer, O.H. (2013). Acetylation of endogenous STAT proteins. Methods Mol. Biol. 967, 167178.

Kosan, C., Ginter, T., Heinzel, T., and Krämer, O.H. (2013). STAT5 acetylation: Mechanisms and consequences for immunological control and leukemogenesis. JAKSTAT 2, e26102.

Brandl, A., Wagner, T., Uhlig, K.M., Knauer, S.K., Stauber, R.H., Melchior, F., Schneider, G., Heinzel, T., and Krämer, O.H. (2012). Dynamically regulated sumoylation of HDAC2 controls p53 deacetylation and restricts apoptosis following genotoxic stress. Journal of Molecular Cell Biology 4, 284293.

Ginter, T., Bier, C., Knauer, S.K., Sughra, K., Hildebrand, D., Münz, T., Liebe, T., Heller, R., Henke, A., Stauber, R.H., et al. (2012). Histone deacetylase inhibitors block IFNγ-induced STAT1 phosphorylation. Cell. Signal. 24, 14531460.

Pietschmann, K., Bolck, H.A., Buchwald, M., Spielberg, S., Polzer, H., Spiekermann, K., Bug, G., Heinzel, T., Böhmer, F.-D., and Krämer, O.H. (2012a). Breakdown of the FLT3-ITD/STAT5 axis and synergistic apoptosis induction by the histone deacetylase inhibitor panobinostat and FLT3-specific inhibitors. Mol. Cancer Ther. 11, 23732383

Pietschmann, K., Buchwald, M., Müller, S., Knauer, S.K., Kögl, M., Heinzel, T., and Krämer, O.H. (2012b). Differential regulation of PML-RARα stability by the ubiquitin ligases SIAH1/SIAH2 and TRIAD1. Int. J. Biochem. Cell Biol. 44, 132138.

Wieczorek, M., Ginter, T., Brand, P., Heinzel, T., and Krämer, O.H. (2012). Acetylation modulates the STAT signaling code. Cytokine Growth Factor Rev. 23, 293305.

Buchwald, M., Pietschmann, K., Müller, J.P., Böhmer, F.D., Heinzel, T., and Krämer, O.H. (2010). Ubiquitin conjugase UBCH8 targets active FMS-like tyrosine kinase 3 for proteasomal degradation. Leukemia 24, 14121421.

Schneider G, Krämer OH, Fritsche P, Schüler S, Schmid RM, Saur D. (2010) Targeting histone deacetylase in pancreatic ductal adenocarcinoma. J Cell Mol Med 14, 1255-1263.

Müller S, Krämer OH. (2010) Inhibitors of HDACs - effective drugs against cancer? Curr Cancer Drug Targets 10, 210-228.

Schneider G, Henrich A, Greiner G, Wolf V, Lovas A, Wieczorek M, Wagner T, Reichardt S, von Werder A, Schmid RM, Weih F, Heinzel T, Saur D, Krämer OH. (2010) Cross talk between NF-kappaB and the tumor supressor p53. Oncogene 29, 2795-2806.

Krämer OH. (2010) HDAC2: a critical factor in health and disease. Trends Pharmacol Sci 30, 647-655.

Krämer OH, Heinzel T. (2010) Phosphorylation-acetylation switch in the regulation of STAT1 signaling. Mol Cell Endocrinol 315, 40-48.

Buchwald M, Krämer OH, Heinzel T. (2009) HDACi - tragets beyond chromatin. Cancer Letters 280, 160-167.

Godmann, M., Gashaw, I., Katz, J.P., Nagy, A., Kaestner, K.H., and Behr, R. (2009a). Krüppel-like factor 4, a pluripotency transcription factor highly expressed in male postmeiotic germ cells, is dispensable for spermatogenesis in the mouse. Mech. Dev. 126, 650664.

Godmann, M., Lambrot, R., and Kimmins, S. (2009b). The dynamic epigenetic program in male germ cells: Its role in spermatogenesis, testis cancer, and its response to the environment. Microsc. Res. Tech. 72, 603619.

Brandl A, Heinzel T, and Krämer OH. (2009) Histone deacetylases - salesmen and customers in the posttranslational modification market. Biology of the Cell 101, 193-205.

Krämer OH, Knauer SK, Greiner G, Jandt E, Reichardt S, Gührs KH, Stauber RH, Böhmer FD, and Heinzel T. (2009) A phosphorylation-acetylation switch regulates STAT1 signaling. Genes & Development 23, 223-235.

Spange S, Wagner T, Heinzel T, and Krämer OH. (2009) Acetylation of non-histone proteins modulates cellular signalling at multiple levels. The International Journal of Biochemistry & Cell Biology 41, 185-198.

Makki MS, Heinzel T, and Englert C. (2008) TSA downregulates Wilms tumor gene 1 (Wt1) expression at multiple levels. Nucleic Acids Research 36, 4067-4078.

Godmann, M., Katz, J.P., Guillou, F., Simoni, M., Kaestner, K.H., and Behr, R. (2008). Krüppel-like factor 4 is involved in functional differentiation of testicular Sertoli cells. Dev. Biol. 315, 552566.

Krämer OH, Müller S, Buchwald M, Reichardt S, and Heinzel T. (2008) Mechanism for ubiquitylation of the leukemia fusion proteins AML1-ETO and PML-RARa. FASEB J 22, 1369-1379.

Krämer OH, Knauer SK, Zimmermann D, Stauber RH, and Heinzel T (2008) Histone deacetylase inhibitors and hydroxyurea modulate the cell cycle and cooperatively induce apoptosis. Oncogene 27, 732-740.

Seneda, M.M., Godmann, M., Murphy, B.D., Kimmins, S., and Bordignon, V. (2008). Developmental regulation of histone H3 methylation at lysine 4 in the porcine ovary. Reproduction 135, 829838.

Heinzel T, and Krämer OH. (2007) Pharmacodynamic markers for histone deacetylase inhibitor development. Drug Discovery Today: Disease Mechanisms 4, 277-283.

Godmann, M., Auger, V., Ferraroni-Aguiar, V., Di Sauro, A., Sette, C., Behr, R., and Kimmins, S. (2007). Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis. Biol. Reprod. 77, 754764.

Atmaca A, Al-Batran SE, Maurer A, Neumann A, Heinzel T, Hentsch B, Schwarz SE, Hövelmann S, Göttlicher M, Knuth A and Jäger E (2007) Valproic Acid (VPA) in Patients with Refractory Advanced Cancer- A Dose Escalating Phase I Clinical Trial. Br. J. Cancer 97, 177-182.

Gromoll, J., Lahrmann, L., Godmann, M., Müller, T., Michel, C., Stamm, S., and Simoni, M. (2007). Genomic checkpoints for exon 10 usage in the luteinizing hormone receptor type 1 and type 2. Mol. Endocrinol. 21, 19841996.

Knauer SK, Krämer OH, Knösel T, Engels K, Rödel F, Walendzik H, Kovács AF, Habtemichael N, Brieger J, Mann W, Heinzel T and Stauber RH (2007) Nuclear export is essential for the biological activity of survivin - Novel aspects to target the survivin pathway in cancer. FASEB J. 21, 207-216.

Novac N, Baus D, Dostert A and Heinzel T (2006) Antagonism between GR and NF-kB for control of the human FasL transcription. FASEB J. 20, 1074-1081.

Krämer OH, Baus D, Knauer S, Stein S, Jäger E, Stauber R, Grez M, Pfitzner E and Heinzel T (2006) Acetylation of Stat1 modulates NF-kB signaling. Genes & Development 20, 473-485.

Tiefenbach J, Novac N, Ducasse M, Eck M, Melchior F and Heinzel T (2006) SUMOylation of the co-repressor N-CoR modulates its capacity to repress transcription. Mol Biol Cell. 17, 1643-1651.

Godmann, M., Kromberg, I., Mayer, J., and Behr, R. (2005). The mouse Krüppel-like Factor 4 (Klf4) gene: four functional polyadenylation sites which are used in a cell-specific manner as revealed by testicular transcript analysis and multiple processed pseudogenes. Gene 361, 149156.

Krämer OH, Zhu P, Ostendorff HP, Golebiewski M, Tiefenbach J, Peters MA, Brill B, Groner B, Bach I, Heinzel T, and Göttlicher M (2003) The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J. 22, 3411-3420. 

Gromoll, J., Wistuba, J., Terwort, N., Godmann, M., Müller, T., and Simoni, M. (2003). A new subclass of the luteinizing hormone/chorionic gonadotropin receptor lacking exon 10 messenger RNA in the New World monkey (Platyrrhini) lineage. Biol. Reprod. 69, 7580.

Göttlicher M, Minucci S, Zhu P, Krämer OH, Schimpf A, Giavara S, Sleeman JP, LoCoco F, Nervi C, Pelicci PG, and Heinzel T (2001) Valproic acid defines a novel class of histone deacetylase inhibitors inducing differentiation of transformed and tumorigenic cells. EMBO J. 20, 6969-6978.

Krämer OH, Göttlicher M, and Heinzel T (2001) Histone deacetylase as a therapeutic target. Trends in Endocrinology and Metabolism 12, 294-300.

Hildebrand D, Tiefenbach J, Heinzel T, Grez M and Maurer AB (2001) Multiple regions of ETO cooperate in transcriptional repression. Biol. Chem. 276, 9889-9895.

Polly P, Herdick M, Moehren U, Baniahmad A, Heinzel T and Carlberg C (2000) VDR-Alien: a novel, DNA-selective vitamin D₃ receptor-corepressor partnership. FASEB J. 14, 1455-1463.