Center for Molecular Medicine Cologne

Büttner, Reinhard | Anokhina, Maria | Odenthal, Margarete - A 01

Epigenetic impact on reprogramming of alternative splicing in cancer

Introduction

Alterations in alternative splicing (AS) profiles are crucial for cancer initiation, progression and metastasis as well as immune defense. RNA splicing and transcription is a coupled process, subjected to epigenetic modifications.

Histone modifying complexes impact the outcome of splicing by regulating the histone marks that play a role in splice site recognition and exon definition, affecting the recruitment of the splicing machinery.

The lysine-specific demethylase 1 is a histone modifier that is overexpressed in a wide variety of cancer types. In this study, we propose to address the mechanistic linkage of the lysine-specific demethylase 1 to cancer associated alternative splicing.

Our Aims

In the present project, we study the mechanistic links of histone modification to oncogenic alternative splic-ing on liver and non-small cell lung cancer, using representative cell systems and transgenic mouse models, both carrying cancer relevant, tumor driving mutations. In addition, we investigate the clinical impact of epigenetically regulated alternative splicing on human liver and lung cancer samples.

  1. In order to examine the impact of the H3K4/K9 methylation signature on alternative splicing, the lysine-specific demethylase 1 will be in¬hibited either pharmacologically or by means of mutations in the catalytic or protein interactive domains, and the alternative spliced transcriptome will be analysed.
  2. Notably, the oncogenic splicing signature of tumor driving key factors will be further examined by minigene reporter construction, by splice site blockade using morpholinos, and additionally by in vivo studies using established transgenic mouse models as well as human lung and liver cancer specimens.

Previous Work

Alternative splicing is a major source of protein diversity involved in many cellular processes. Constitutive splicing is carried out to remove introns by usage of conserved canonical splice sites, whereas alternative splicing (AS) is controlled by additional cis-regulatory elements within the pre-mRNA.

The exonic and intronic splicing enhancer (ESE, ISE) and silencer (ESS, ISS) elements are critical for correct exon recognition and splicing outcome. They define the strength of the splice site by recruitment of the trans-acting splicing factors, mainly including serine/arginine-rich splicing factors (SRSFs) and heterogeneous nuclear ribonucleoproteins (hnRNPs). In response to oncogenic stress, aberrant splicing is observed, strongly promoting cancer progression. Our current findings indicate that epi­genetic dysregulation contributes to a cancer associated, oncogenic alternative splicing pattern.

Chromatin modifying complexes are suggested to be involved in regulating both transcription and splicing by modifying the DNA and histone proteins. Post-translational modifications on the histone tails  are assumed to affect alternative splicing by their influence on the transcription rate, which in turn affects the establishment of the splicing complexes, or by their influence on the recruitment of the splicing machinery, itself. The lysine-specific demethylase 1 is known to be crucial for chromatin remodeling by demethylation of histone 3, namely mono- and di-methylated lysine 4 (H3K4) and lysine 9 (H3K9), resulting in transcriptional gene repression or activation, respectively.

Lysine-specific demethylase 1 is highly overexpressed in a wide variety of cancer types (1-3). Its expression is known to correlate with tumor grade and is associated with malignancy (3) (Figure 1).  Our recent studies reveal that cancer associated overexpression of the lysine-specific demethylase 1 leads to transcriptional control of mediators controlling cell cycle progression (5-6). Moreover, our novel findings provide evidence that expression of the splicing trans-acting machinery is epigenetically controlled by the H3K4 und H3K9 methylation marks.

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  • Dominguez-Valentin, M., E.J. Crosbie, C. Engel, S. Aretz, F. Macrae, I. Winship, G. Capella, H. Thomas, S. Nakken, E. Hovig, M. Nielsen, R.H. Sijmons, L. Bertario, B. Bonanni, M.G. Tibiletti, G.M. Cavestro, M. Mints, N. Gluck, L. Katz, K. Heinimann, C.A. Vaccaro, K. Green, F. Lalloo, J. Hill, W. Schmiegel, D. Vangala, C. Perne, H.G. Strauss, J. Tecklenburg, E. Holinski-Feder, V. Steinke-Lange, J.P. Mecklin, J.P. Plazzer, M. Pineda, M. Navarro, J.B. Vidal, R. Kariv, G. Rosner, T.A. Pinero, M.L. Gonzalez, P. Kalfayan, N. Ryan, S.W. Ten Broeke, M.A. Jenkins, L. Sunde, I. Bernstein, J. Burn, M. Greenblatt, W.H. de Vos Tot Nederveen Cappel, A. Della Valle, F. Lopez-Koestner, K. Alvarez, R. Buttner, H. Gorgens, M. Morak, S. Holzapfel, R. Huneburg, M. von Knebel Doeberitz, M. Loeffler, N. Rahner, J. Weitz, K. Pylvanainen, L. Renkonen-Sinisalo, A. Lepisto, A. Auranen, J.L. Hopper, A.K. Win, R.W. Haile, N.M. Lindor, S. Gallinger, L. Le Marchand, P.A. Newcomb, J.C. Figueiredo, S.N. Thibodeau, C. Therkildsen, H. Okkels, Z. Ketabi, O.G. Denton, E.A. Rodland, H. Vasen, F. Neffa, P. Esperon, D. Tjandra, G. Moslein, J.R. Sampson, D.G. Evans, T.T. Seppala, and P. Moller, Risk-reducing hysterectomy and bilateral salpingo-oophorectomy in female heterozygotes of pathogenic mismatch repair variants: a Prospective Lynch Syndrome Database report.Genet Med, 2021. 23(4): p. 705-712.
  • Quaas, A., J. Rehkaemper, J. Rueschoff, A. Pamuk, T. Zander, A. Hillmer, J. Siemanowski, J. Wittig, R. Buettner, P. Plum, F. Popp, F. Gebauer, C.J. Bruns, H. Loeser, H. Alakus, and B. Schoemig-Markiefka, Occurrence of High Microsatellite-Instability/Mismatch Repair Deficiency in Nearly 2,000 Human Adenocarcinomas of the Gastrointestinal Tract, Pancreas, and Bile Ducts: A Study From a Large German Comprehensive Cancer Center.Front Oncol, 2021. 11: p. 569475.
  • Quaas, A., A. Pamuk, S. Klein, J. Quantius, J. Rehkaemper, A.G. Barutcu, J. Rueschoff, T. Zander, F. Gebauer, A. Hillmer, R. Buettner, W. Schroeder, C.J. Bruns, H. Loser, B. Schoemig-Markiefka, and H. Alakus, Sex-specific prognostic effect of CD66b-positive tumor-infiltrating neutrophils (TANs) in gastric and esophageal adenocarcinoma.Gastric Cancer, 2021. 24(6): p. 1213-1226.
  • Goertzen, N., R. Pappesch, J. Fassunke, T. Bruning, Y.D. Ko, J. Schmidt, F. Grosserueschkamp, R. Buettner, and K. Gerwert, Quantum Cascade Laser-Based Infrared Imaging as a Label-Free and Automated Approach to Determine Mutations in Lung Adenocarcinoma.Am J Pathol, 2021. 191(7): p. 1269-1280.
  • Schoemig-Markiefka, B., J. Eschbach, A.H. Scheel, A. Pamuk, J. Rueschoff, T. Zander, R. Buettner, W. Schroeder, C.J. Bruns, H. Loeser, H. Alakus, and A. Quaas, Optimized PD-L1 scoring of gastric cancer.Gastric Cancer, 2021. 24(5): p. 1115-1122.
  • Kron, A., M. Scheffler, C. Heydt, L. Ruge, C. Schaepers, A.K. Eisert, S. Merkelbach-Bruse, R. Riedel, L. Nogova, R.N. Fischer, S. Michels, D.S.Y. Abdulla, S. Koleczko, J. Fassunke, A.M. Schultheis, F. Kron, F. Ueckeroth, G. Wessling, J. Sueptitz, F. Beckers, J. Braess, J. Panse, C. Grohe, M. Hamm, H.J. Kabitz, K. Kambartel, B. Kaminsky, S. Krueger, C. Schulte, J. Lorenz, J. Lorenzen, W. Meister, A. Meyer, J. Kappes, N. Reinmuth, B. Schaaf, W. Schulte, M. Serke, R. Buettner, and J. Wolf, Genetic Heterogeneity of MET-Aberrant NSCLC and Its Impact on the Outcome of Immunotherapy.J Thorac Oncol, 2021. 16(4): p. 572-582.
  • Weglage, J., F. Wolters, L. Hehr, J. Lichtenberger, C. Wulz, F. Hempel, A. Baier, T. Quack, K. Kohler, T. Longerich, G. Schramm, K. Irungbam, H. Mueller, V. von Buelow, A. Tschuschner, M. Odenthal, U. Drebber, M.E. Arousy, L.N.Z. Ramalho, K. Bankov, P. Wild, J. Pons-Kuhnemann, J. Tschammer, C.G. Grevelding, E. Roeb, and M. Roderfeld, Schistosoma mansoni eggs induce Wnt/beta-catenin signaling and activate the protooncogene c-Jun in human and hamster colon. Sci Rep, 2020. 10(1): p. 22373.
  • Meinrath, J., A. Haak, N. Igci, P. Dalvi, C. Arolt, S. Meemboor, U. Siebolts, H. Eischeidt-Scholz, C. Wickenhauser, I. Grunewald, U. Drebber, R. Buttner, A. Quaas, J.P. Klussmann, M. Odenthal, D. Beutner, and M. Meyer, Expression profiling on subclasses of primary parotid gland carcinomas. Oncotarget, 2020. 11(45): p. 4123-4137.
  • Rheinwalt, K.P., U. Drebber, R. Schierwagen, S. Klein, U.P. Neumann, T.F. Ulmer, A. Plamper, A. Kroh, S. Schipper, M. Odenthal, F.E. Uschner, P. Lingohr, J. Trebicka, and M.J. Brol, Baseline Presence of NAFLD Predicts Weight Loss after Gastric Bypass Surgery for Morbid Obesity. J Clin Med, 2020. 9(11).
  • Wu, X., J. Li, A. Gassa, D. Buchner, H. Alakus, Q. Dong, N. Ren, M. Liu, M. Odenthal, D. Stippel, C. Bruns, Y. Zhao, and R. Wahba, Circulating tumor DNA as an emerging liquid biopsy biomarker for early diagnosis and therapeutic monitoring in hepatocellular carcinoma. Int J Biol Sci, 2020. 16(9): p. 1551-1562.
  • Kron, A., M. Scheffler, C. Heydt, L. Ruge, C. Schaepers, A.K. Eisert, S. Merkelbach-Bruse, R. Riedel, L. Nogova, R.N. Fischer, S. Michels, D.S.Y. Abdulla, S. Koleczko, J. Fassunke, A.M. Schultheis, F. Kron, F. Ueckeroth, G. Wessling, J. Sueptitz, F. Beckers, J. Braess, J. Panse, C. Grohe, M. Hamm, H.J. Kabitz, K. Kambartel, B. Kaminsky, S. Krueger, C. Schulte, J. Lorenz, J. Lorenzen, W. Meister, A. Meyer, J. Kappes, N. Reinmuth, B. Schaaf, W. Schulte, M. Serke, R. Buettner, and J. Wolf, Genetic Heterogeneity of MET-Aberrant NSCLC and Its Impact on the Outcome of Immunotherapy. J Thorac Oncol, 2021. 16(4): p. 572-582.
  • Klein, S., A. Quaas, K.W. Noh, M. Cartolano, N. Abedpour, C. Mauch, J. Quantius, H.C. Reinhardt, R. Buettner, M. Peifer, and D. Helbig, Integrative Analysis of Pleomorphic Dermal Sarcomas Reveals Fibroblastic Differentiation and Susceptibility to Immunotherapy. Clin Cancer Res, 2020. 26(21): p. 5638-5645.
  • Loeser, H., C.B. Wolwer, H. Alakus, S.H. Chon, T. Zander, R. Buettner, A.M. Hillmer, C.J. Bruns, W. Schroeder, F. Gebauer, and A. Quaas, Y Chromosome Loss is a Frequent Event in Barrett's Adenocarcinoma and Associated with Poor Outcome. Cancers (Basel), 2020. 12(7).
  • Rehkaemper, J., M. Korenkov, A. Quaas, J. Rueschoff, A. Pamuk, T. Zander, A.M. Hillmer, R. Buettner, A.H. Hoelscher, C.J. Bruns, H. Loeser, H. Alakus, and B. Schoemig-Markiefka, Amplification of KRAS and its heterogeneity in non-Asian gastric adenocarcinomas. BMC Cancer, 2020. 20(1): p. 587.
  • Schallenberg, S., J. Bork, A. Essakly, H. Alakus, R. Buettner, A.M. Hillmer, C. Bruns, W. Schroeder, T. Zander, H. Loeser, F. Gebauer, and A. Quaas, Loss of the SWI/SNF-ATPase subunit members SMARCF1 (ARID1A), SMARCA2 (BRM), SMARCA4 (BRG1) and SMARCB1 (INI1) in oesophageal adenocarcinoma. BMC Cancer, 2020. 20(1): p. 12.
  • Huang, R.S.P., D. Smith, C.H. Le, W.W. Liu, E. Ordinario, C. Manohar, M. Lee, J. Rajamani, H. Truong, J. Li, C. Choi, J. Li, A. Pati, L. Bubendorf, R. Buettner, K.M. Kerr, F. Lopez-Rios, A. Marchetti, I. Marondel, A.G. Nicholson, A.B. Oz, P. Pauwels, F. Penault-Llorca, G. Rossi, E. Thunnissen, A.H. Newell, G. Pate, and I. Menzl, Correlation of ROS1 Immunohistochemistry With ROS1 Fusion Status Determined by Fluorescence In Situ Hybridization. Arch Pathol Lab Med, 2020. 144(6): p. 735-741.
  • Loeser, H., M. Scholz, H. Fuchs, A. Essakly, A.I. Damanakis, T. Zander, R. Buttner, W. Schroder, C. Bruns, A. Quaas, and F. Gebauer, Integrin alpha V (ITGAV) expression in esophageal adenocarcinoma is associated with shortened overall-survival. Sci Rep, 2020. 10(1): p. 18411.
  • Vigliar, E., R. Cepurnaite, E. Alcaraz-Mateos, S.Z. Ali, Z.W. Baloch, C. Bellevicine, M. Bongiovanni, P. Botsun, D. Bruzzese, L. Bubendorf, R. Buttner, S. Canberk, A. Capitanio, C. Casadio, E. Cazacu, B. Cochand-Priollet, A. D'Amuri, C. Eloy, M. Engels, G. Fadda, G. Fontanini, F. Fulciniti, P. Hofman, A. Iaccarino, A. Ieni, X.S. Jiang, K. Kakudo, I. Kern, I. Kholova, C. Liu, A. Lobo, M.D. Lozano, U. Malapelle, Z. Maleki, P. Michelow, J. Musayev, G. Ozgun, M. Oznur, F.M. Peiro Marques, P. Pisapia, D. Poller, M. Pyzlak, B. Robinson, E.D. Rossi, S. Roy-Chowdhuri, M. Saieg, S. Savic Prince, F.C. Schmitt, F. Javier Segui Ivanez, T. Stoos-Veic, O. Sulaieva, B.J. Sweeney, G. Tuccari, M.L. van Velthuysen, P.A. VanderLaan, P. Vielh, P. Viola, R. Voorham, B. Weynand, P. Zeppa, W.C. Faquin, M.B. Pitman, and G. Troncone, Global impact of the COVID-19 pandemic on cytopathology practice: Results from an international survey of laboratories in 23 countries. Cancer Cytopathol, 2020. 128(12): p. 885-894.
  • Yang, S.R., A.M. Schultheis, H. Yu, D. Mandelker, M. Ladanyi, and R. Buttner, Precision medicine in non-small cell lung cancer: Current applications and future directions. Semin Cancer Biol, 2020.
  • Wuerdemann, N., S.E. Gultekin, K. Putz, C. Wittekindt, C.U. Huebbers, S.J. Sharma, H. Eckel, A.B. Schubotz, S. Gattenlohner, R. Buttner, E.J. Speel, J.P. Klussmann, S. Wagner, and A. Quaas, PD-L1 Expression and a High Tumor Infiltrate of CD8+ Lymphocytes Predict Outcome in Patients with Oropharyngeal Squamous Cells Carcinoma. Int J Mol Sci, 2020. 21(15).
  • Dominguez-Valentin, M., J.R. Sampson, T.T. Seppala, S.W. Ten Broeke, J.P. Plazzer, S. Nakken, C. Engel, S. Aretz, M.A. Jenkins, L. Sunde, I. Bernstein, G. Capella, F. Balaguer, H. Thomas, D.G. Evans, J. Burn, M. Greenblatt, E. Hovig, W.H. de Vos Tot Nederveen Cappel, R.H. Sijmons, L. Bertario, M.G. Tibiletti, G.M. Cavestro, A. Lindblom, A. Della Valle, F. Lopez-Kostner, N. Gluck, L.H. Katz, K. Heinimann, C.A. Vaccaro, R. Buttner, H. Gorgens, E. Holinski-Feder, M. Morak, S. Holzapfel, R. Huneburg, M.V. Knebel Doeberitz, M. Loeffler, N. Rahner, H.K. Schackert, V. Steinke-Lange, W. Schmiegel, D. Vangala, K. Pylvanainen, L. Renkonen-Sinisalo, J.L. Hopper, A.K. Win, R.W. Haile, N.M. Lindor, S. Gallinger, L. Le Marchand, P.A. Newcomb, J.C. Figueiredo, S.N. Thibodeau, K. Wadt, C. Therkildsen, H. Okkels, Z. Ketabi, L. Moreira, A. Sanchez, M. Serra-Burriel, M. Pineda, M. Navarro, I. Blanco, K. Green, F. Lalloo, E.J. Crosbie, J. Hill, O.G. Denton, I.M. Frayling, E.A. Rodland, H. Vasen, M. Mints, F. Neffa, P. Esperon, K. Alvarez, R. Kariv, G. Rosner, T.A. Pinero, M.L. Gonzalez, P. Kalfayan, D. Tjandra, I.M. Winship, F. Macrae, G. Moslein, J.P. Mecklin, M. Nielsen, and P. Moller, Correction: Cancer risks by gene, age, and gender in 6350 carriers of pathogenic mismatch repair variants: findings from the Prospective Lynch Syndrome Database. Genet Med, 2020. 22(9): p. 1569.
  • Westphalen, B.C., C. Bokemeyer, R. Buttner, S. Frohling, V.I. Gaidzik, H. Glimm, U.T. Hacker, V. Heinemann, A.L. Illert, U. Keilholz, T. Kindler, M. Kirschner, B. Schilling, J.T. Siveke, T. Schroeder, V. Tischler, S. Wagner, W. Weichert, D. Zips, S. Loges, D. Working Group Molecular, and Therapy, Conceptual framework for precision cancer medicine in Germany: Consensus statement of the Deutsche Krebshilfe working group 'Molecular Diagnostics and Therapy'. Eur J Cancer, 2020. 135: p. 1-7.
  • Scheffler, M., A. Holzem, A. Kron, L. Nogova, M.A. Ihle, C. von Levetzow, J. Fassunke, C. Wompner, E. Bitter, S. Koleczko, D.S.Y. Abdulla, S. Michels, R. Fischer, R. Riedel, J.P. Weber, T. Westphal, U. Gerigk, J. Kern, B. Kaminsky, W. Randerath, K.O. Kambartel, S. Merkelbach-Bruse, R. Buttner, and J. Wolf, Co-occurrence of targetable mutations in Non-small cell lung cancer (NSCLC) patients harboring MAP2K1 mutations. Lung Cancer, 2020. 144: p. 40-48.
  • Volz, C., S. Breid, C. Selenz, A. Zaplatina, K. Golfmann, L. Meder, F. Dietlein, S. Borchmann, S. Chatterjee, M. Siobal, J. Schottle, A. Florin, M. Koker, M. Nill, L. Ozretic, N. Uhlenbrock, S. Smith, R. Buttner, H. Miao, B. Wang, H.C. Reinhardt, D. Rauh, M. Hallek, A. Acker-Palmer, L.C. Heukamp, and R.T. Ullrich, Inhibition of Tumor VEGFR2 Induces Serine 897 EphA2-Dependent Tumor Cell Invasion and Metastasis in NSCLC. Cell Rep, 2020. 31(4): p. 107568.
  • Kramer, M., P.S. Plum, O. Velazquez Camacho, K. Folz-Donahue, M. Thelen, I. Garcia-Marquez, C. Wolwer, S. Busker, J. Wittig, M. Franitza, J. Altmuller, H. Loser, H. Schlosser, R. Buttner, W. Schroder, C.J. Bruns, H. Alakus, A. Quaas, S.H. Chon, and A.M. Hillmer, Cell type-specific transcriptomics of esophageal adenocarcinoma as a scalable alternative for single cell transcriptomics. Mol Oncol, 2020. 14(6): p. 1170-1184.
  • Shostak, K., Z. Jiang, B. Charloteaux, A. Mayer, Y. Habraken, L. Tharun, S. Klein, X. Xu, H.Q. Duong, A. Vislovukh, P. Close, A. Florin, F. Rambow, J.C. Marine, R. Buttner, and A. Chariot, The X-linked trichothiodystrophy-causing gene RNF113A links the spliceosome to cell survival upon DNA damage. Nat Commun, 2020. 11(1): p. 1270.
  • Schiffmann, L.M., H. Loeser, A.S. Jacob, M. Maus, H. Fuchs, Y. Zhao, L. Tharun, A. Essakly, A. Iannos Damanakis, T. Zander, R. Buttner, W. Schroder, C. Bruns, A. Quaas, and F. Gebauer, Dickkopf-2 (DKK2) as Context Dependent Factor in Patients with Esophageal Adenocarcinoma. Cancers (Basel), 2020. 12(2).
  • Sommer, J., C. Dorn, E. Gabele, F. Bataille, K. Freese, T. Seitz, W.E. Thasler, R. Buttner, R. Weiskirchen, A. Bosserhoff, and C. Hellerbrand, Four-And-A-Half LIM-Domain Protein 2 (FHL2) Deficiency Aggravates Cholestatic Liver Injury. Cells, 2020. 9(1).
  • Engel, C., A. Ahadova, T.T. Seppala, S. Aretz, M. Bigirwamungu-Bargeman, H. Blaker, K. Bucksch, R. Buttner, W.T. de Vos Tot Nederveen Cappel, V. Endris, E. Holinski-Feder, S. Holzapfel, R. Huneburg, M. Jacobs, J.J. Koornstra, A.M. Langers, A. Lepisto, M. Morak, G. Moslein, P. Peltomaki, K. Pylvanainen, N. Rahner, L. Renkonen-Sinisalo, K. Schulmann, V. Steinke-Lange, A. Stenzinger, C.P. Strassburg, P.C. van de Meeberg, M. van Kouwen, M. van Leerdam, D.B. Vangala, J. Vecht, M.L. Verhulst, M. von Knebel Doeberitz, J. Weitz, S. Zachariae, M. Loeffler, J.P. Mecklin, M. Kloor, H.F. Vasen, t.D.L.S.C.G. German Hnpcc Consortium, and R. Finnish Lynch Syndrome, Associations of Pathogenic Variants in MLH1, MSH2, and MSH6 With Risk of Colorectal Adenomas and Tumors and With Somatic Mutations in Patients With Lynch Syndrome. Gastroenterology, 2020. 158(5): p. 1326-1333.
  • Riabinska, A., D. Lehrmann, R.D. Jachimowicz, G. Knittel, C. Fritz, A. Schmitt, A. Geyer, C. Heneweer, M. Wittersheim, L.P. Frenzel, A. Torgovnick, J.L. Wiederstein, C.M. Wunderlich, M. Ortmann, A. Paillard, W. Wossmann, A. Borkhardt, S. Burdach, M.L. Hansmann, A. Rosenwald, S. Perner, G. Mall, W. Klapper, A. Merseburg, M. Kruger, H. Grull, T. Persigehl, F.T. Wunderlich, M. Peifer, O. Utermohlen, R. Buttner, F. Beleggia, and H.C. Reinhardt, ATM activity in T cells is critical for immune surveillance of lymphoma in vivo. Leukemia, 2020. 34(3): p. 771-786.
  • Dominguez-Valentin, M., J.R. Sampson, T.T. Seppala, S.W. Ten Broeke, J.P. Plazzer, S. Nakken, C. Engel, S. Aretz, M.A. Jenkins, L. Sunde, I. Bernstein, G. Capella, F. Balaguer, H. Thomas, D.G. Evans, J. Burn, M. Greenblatt, E. Hovig, W.H. de Vos Tot Nederveen Cappel, R.H. Sijmons, L. Bertario, M.G. Tibiletti, G.M. Cavestro, A. Lindblom, A. Della Valle, F. Lopez-Kostner, N. Gluck, L.H. Katz, K. Heinimann, C.A. Vaccaro, R. Buttner, H. Gorgens, E. Holinski-Feder, M. Morak, S. Holzapfel, R. Huneburg, M.V. Knebel Doeberitz, M. Loeffler, N. Rahner, H.K. Schackert, V. Steinke-Lange, W. Schmiegel, D. Vangala, K. Pylvanainen, L. Renkonen-Sinisalo, J.L. Hopper, A.K. Win, R.W. Haile, N.M. Lindor, S. Gallinger, L. Le Marchand, P.A. Newcomb, J.C. Figueiredo, S.N. Thibodeau, K. Wadt, C. Therkildsen, H. Okkels, Z. Ketabi, L. Moreira, A. Sanchez, M. Serra-Burriel, M. Pineda, M. Navarro, I. Blanco, K. Green, F. Lalloo, E.J. Crosbie, J. Hill, O.G. Denton, I.M. Frayling, E.A. Rodland, H. Vasen, M. Mints, F. Neffa, P. Esperon, K. Alvarez, R. Kariv, G. Rosner, T.A. Pinero, M.L. Gonzalez, P. Kalfayan, D. Tjandra, I.M. Winship, F. Macrae, G. Moslein, J.P. Mecklin, M. Nielsen, and P. Moller, Cancer risks by gene, age, and gender in 6350 carriers of pathogenic mismatch repair variants: findings from the Prospective Lynch Syndrome Database. Genet Med, 2020. 22(1): p. 15-25.
  • Wagener-Ryczek S, Schoemmel M, Kraemer M, Bruns C, Schroeder W, Zander T, Gebauer F, Alakus H, Merkelbach-Bruse S, Buettner R, Loeser H, Thelen M, Schlosser HA, and Quaas A (2020). Immune profile and immunosurveillance in treatment-naive and neoadjuvantly treated esophageal adenocarcinoma. Cancer Immunol Immunother 69, 523-33.
     
  • Wu F, Fan J, Fang J, Dalvi PS, Odenthal M, Fang N.: Single Cell Sequencing: A New Dimension in Cancer Diagnosis and Treatment. Adv Exp Med Biol. 2020;1255:109-121. doi: 10.1007/978-981-15-4494-1_9. PMID: 32949394 Review.
  • Kuiper-Makris C, Zanetti D, Vohlen C, Fahle L, Muller M, Odenthal M, Felderhoff-Muser U, Dotsch J, and Alejandre Alcazar MA (2020). Mendelian randomization and experimental IUGR reveal the adverse effect of low birth weight on lung structure and function. Sci Rep 10, 22395.
  • Weglage J, Wolters F, Hehr L, Lichtenberger J, Wulz C, Hempel F, Baier A, Quack T, Kohler K, Longerich T, Schramm G, Irungbam K, Mueller H, von Buelow V, Tschuschner A, Odenthal M, Drebber U, Arousy ME, Ramalho LNZ, Bankov K, Wild P, Pons-Kuhnemann J, Tschammer J, Grevelding CG, Roeb E, and Roderfeld M (2020). Schistosoma mansoni eggs induce Wnt/beta-catenin signaling and activate the protooncogene c-Jun in human and hamster colon. Sci Rep 10, 22373.
Prof. Dr. Reinhard Büttner CMMC Cologne
Prof. Dr. Reinhard Büttner

Institute for General Pathology and Pathological Anatomy

CMMC - PI - A 01

Executive Board Member

+49 221 478 6320

+49 221 478 6360

Institute for General Pathology and Pathological Anatomy

Kerpener Str. 62

50937 Cologne

https://pathologie.uk-koeln.de/institut/

CMMC Profile Page

Curriculum Vitae (CV)

Publications on PubMed

Publications - Reinhard Büttner

Link to PubMed

Dr. Maria Anokhina CMMC Cologne
Dr. Maria Anokhina

Institute for General Pathology and Pathological Anatomy

CMMC - Co-PI - A 01

 

Publications - Maria Anokhina

Link to PubMed

Prof. Dr. Margarete Odenthal CMMC Cologne
Prof. Dr. Margarete Odenthal

Institute for General Pathology and Pathological Anatomy

CMMC - Co-PI -  A 01

CMMC - Co-PI - A 02

+49 221 478 6367

+49 221 478 6360

Institute for General Pathology and Pathological Anatomy

Kerpener Str. 62

50937 Cologne

https://pathologie.uk-koeln.de/forschung/translationale-molekularpathologie-ag-odenthal/

CMMC Profile Page

Curriculum Vitae (CV)

Publications on PubMed

Publications - Margarete Odenthal

Link to PubMed

Figure 1
Figure 2
Group Members

Hannah Eischeid-Scholz, BTA
Ulrike Koitzsch, BTA
Dr. Sonja Meemboor, Scientific Coordinator
Dr. Maria Anokhina, Post-Doc
Dr. Priya Dalvi, Post-Doc
Dr. Xiaojie Yu, Post-Doc
Lingyu Wang, PhD student
Marcel Schmiel, Medical student
Alice Sferruzza, Medical student
Miriam Weiß, Medical Student