Research Groups

Stem Cell Regulation and Mechanisms of Regeneration

Regeneration is the process of restoring lost or damaged tissues to their original state. While humans and other mammals have only limited regeneration capacity, some other species can regenerate extremely well. For example, flatworms can grow back entire body parts after amputation, and for this reason have been extensively used as model organisms in research on regeneration. The cellular basis for regeneration is provided by coordinated activity of stem cells, which give rise to various specialized cell types required to reconstitute a tissue.

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  • Eugene Berezikov Visit

    Group Leader of the Laboratory of Stem Cell Regulation and Mechanisms of Regeneration

    Research fields

    Stem cells, regeneration, ageing, flatworms, small RNAs

    Research Associates
    Postdoctoral Fellows
    Ekaterina Ovchinnikova
    PhD Students
    Jakub Wudarski
    Margriet Grelling
    Lisa Glazenburg
  • The research group led by Eugene Berezikov is developing the flatworm Macrostomum lignano as a model organism for research on stem cells, regeneration and ageing. Due to its high regeneration capacity, small size, transparency and clear morphology, ease of culture, short generation time and easiness to genetic manipulation, M. lignano provides a unique and powerful system to study.

    • Mouton S, Grudniewska M, Glazenburg L, Guryev V, Berezikov E (2018) Resilience to aging in the regeneration-capable flatworm Macrostomum lignano. Aging Cell.  
    • Grudniewska M, Mouton S, Grelling M, Wolters AHG, Kuipers J, Giepmans BNG, Berezikov E (2018) A novel flatworm-specific gene implicated in reproduction in Macrostomum lignano. Scientific Reports.
    • Ovchinnikova E, Hoes M, Ustyantsev K, Bomer N, de Jong TV, van der Mei H, Berezikov E, van der Meer P (2018) Modeling Human Cardiac Hypertrophy in Stem Cell-Derived Cardiomyocytes. Stem Cell Reports.
    • Lengerer B, Wunderer J, Pjeta R, Carta G, Kao D, Aboobaker A, Beisel C, Berezikov E, Salvenmoser W, Ladurner P. (2018) Organ specific gene expression in the regenerating tail of Macrostomum lignano. Developmental Biology.
    • Wudarski J, Simanov D, Ustyantsev K, de Mulder K, Grelling M, Grudniewska M, Beltman F, Glazenburg L, Demircan T, Wunderer J, Qi W, Vizoso DB, Weissert PM, Olivieri D, Mouton S, Guryev V, Aboobaker A, Schärer L, Ladurner P, Berezikov E.(2017) Efficient transgenesis and annotated genome sequence of the regenerative flatworm model Macrostomum lignano. Nature Communications  
    • Kenny NJ, de Goeij JM, de Bakker DM, Whalen CG, Berezikov E, Riesgo A. (2017) Towards the identification of ancestrally shared regenerative mechanisms across the Metazoa: A Transcriptomic case study in the Demosponge Halisarca caerulea. Marine Genomics
    • van der Pol A, Gil A, Silljé HHW, Tromp J, Ovchinnikova ES, Vreeswijk-Baudoin I, Hoes M, Domian IJ, van de Sluis B, van Deursen JM, Voors AA, van Veldhuisen DJ, van Gilst WH, Berezikov E, van der Harst P, de Boer RA, Bischoff R, van der Meer P (2017) Accumulation of 5-oxoproline in myocardial dysfunction and the protective effects of OPLAH. Science Translational Medicine.
    • Zadesenets KS, Ershov NI, Berezikov E, Rubtsov NB  (2017) Chromosome Evolution in the Free-Living Flatworms: First Evidence of Intrachromosomal Rearrangements in Karyotype Evolution of Macrostomum lignano (Platyhelminthes, Macrostomida). Genes.
    • Hoffmann RF, Moshkin YM, Mouton S, Grzeschik NA, Kalicharan RD, Kuipers J, Wolters AHG, Nishida K, Romashchenko AV, Postberg J, Lipps H, Berezikov E, Sibon OCM, Giepmans BNG, Lansdorp PM (2017) Guanine quadruplex structures localize to heterochromatin. Nucleid Acids Research.
    • Vegter EL, Ovchinnikova ES, Silljé HHW, Meems LMG, van der Pol A, van der Velde AR, Berezikov E, Voors AA, de Boer RA, van der Meer P (2017) Rodent heart failure models do not reflect the human circulating microRNA signature in heart failure. PLoS One.
    • Vegter EL, Ovchinnikova ES, van Veldhuisen DJ, Jaarsma T, Berezikov E, van der Meer P, Voors AA. (2017) Low circulating microRNA levels in heart failure patients are associated with atherosclerotic disease and cardiovascular-related rehospitalizations. Clin Res Cardiol.
    • Grudniewska M, Mouton S, Simanov D, Beltman F, Grelling M, de Mulder K, Arindrarto W, Weissert PM, van der Elst S, Berezikov E. (2016) Transcriptional signatures of somatic neoblasts and germline cells in Macrostomum lignano. Elife.  
    • Isik M, Blackwell TK, Berezikov E (2016) MicroRNA mir-34 provides robustness to environmental stress response via the DAF-16 network in C. elegans. Scientific Reports.
    • Vegter EL, Schmitter D, Hagemeijer Y, Ovchinnikova ES, van der Harst P, Teerlink JR, O'Connor CM, Metra M, Davison BA, Bloomfield D, Cotter G, Cleland JG, Givertz MM, Ponikowski P, van Veldhuisen DJ, van der Meer P, Berezikov E, Voors AA , Khan MA.(2016) Use of biomarkers to establish potential role and function of circulating microRNAs in acute heart failure. International Journal of Cardiology.  
    • Dueck A, Evers M, Henz, SR , Unger K, Eichner N, Merkl R, Berezikov E, Engelmann JC, Weigel D, Wenzl S, Meister G  (2016) Gene silencing pathways found in the green alga Volvox carteri reveal insights into evolution and origins of small RNA systems in plants. BMC Genomics.  
    • Zadesenets KS, Vizoso DB, Schlatter A, Konopatskaia ID, Berezikov E, Schärer L, Rubtsov NB (2016) Evidence for Karyotype Polymorphism in the Free-Living Flatworm, Macrostomum lignano, a Model Organism for Evolutionary and Developmental Biology. PLoS One.    
    • Rodrigues M, Ostermann T, Kremeser L, Lindner H, Beisel C, Berezikov E, Hobmayer B, Ladurner P (2016) Profiling of adhesive-related genes in the freshwater cnidarian Hydra magnipapillata by transcriptomics and proteomics. Biofouling.  
    • Chereji RV, Kan TW, Grudniewska MK, Romashchenko AV, Berezikov E, Zhimulev IF, Guryev V, Morozov AV, Moshkin YM (2016) Genome-wide profiling of nucleosome sensitivity and chromatin accessibility in Drosophila melanogaster. Nucleic Acids Research.  
    • Bruno N, ter Maaten JM, Ovchinnikova ES, Vegter EL, Valente MA van der Meer P de Boer RA, van der Harst P, Schmitter D, Metra M, O'Connor CM, Ponikowski P, Teerlink JR, Cotter G, Davison B, Cleland JG, Givertz MM, Bloomfield DM, Dittrich HC, Pinto YM, van Veldhuisen DJ, Hillege HL, Berezikov E, Voors AA (2016) MicroRNAs relate to early worsening of renal function in patients with acute heart failure. International Journal of Cardiology.
    • Wu CC, Kruse F, Vasudevarao MD, Junker JP, Zebrowski DC, Fischer K, Noël ES, Grün D, Berezikov E, Engel FB, van Oudenaarden A, Weidinger G, Bakkers J (2016) Spatially Resolved Genome-wide Transcriptional Profiling Identifies BMP Signaling as Essential Regulator of Zebrafish Cardiomyocyte Regeneration. Developmental Cell.
    • Hoffmann RF, Moshkin YM, Mouton S, Grzeschik NA, Kalicharan RD, Kuipers J, Wolters AH, Nishida K, Romashchenko AV, Postberg J, Lipps H, Berezikov E, Sibon OC, Giepmans BN, Lansdorp PM (2016) Guanine quadruplex structures localize to heterochromatin. Nucleic Acids Research.  
    • Desvignes T, Batzel P, Berezikov E, Eilbeck K, Eppig JT, McAndrews MS, Singer A, Postlethwait JH (2015) miRNA Nomenclature: A View Incorporating Genetic Origins, Biosynthetic Pathways, and Sequence Variants. Trends Genetics.
    • Ovchinnikova ES, Schmitter D, Vegter EL, ter Maaten JM, Valente MAE, Liu LCY, van der Harst P, Pinto YM, de Boer RA, Meyer S, Teerlink JR, O’Connor CM, Metra M, Davison BA, Bloomfield DM, Cotter G, Cleland JG, Mebazaa A, Laribi S, Givertz MM, Ponikowski P, van der Meer P, van Veldhuisen DJ, Voors AA*, Eugene Berezikov. (2015) Signature of circulating microRNAs in patients with acute heart failure. European Journal of Heart Failure.  
    • Ikeda K, Horie-Inoue K, Ueno T, Suzuki T, Sato W, Shigekawa T, Osaki A, Saeki T, Berezikov E, Mano H, Inoue S (2015) miR-378a-3p modulates tamoxifen sensitivity in breast cancer MCF-7 cells through targeting GOLT1A. Scientific Reports.
    • Arbore R, Sekii K, Beisel C, Ladurner P, Berezikov E, Schärer L (2015) Positional RNA-Seq identifies candidate genes for phenotypic engineering of sexual traits. Frontiers in Zoology.
    • Junker JP, Noe ES, Guryev V, Peterson KA, Shah G, Huisken J,  McMahon AP, Berezikov E, Bakkers J, van Oudenaarden A. (2014) Genome-wide RNA Tomography. Cell.
    • Babae N, Bourajjaj M, Liu Y, Van Beijnum JR, Cerisoli F, Scaria PV, Verheul M, Van Berkel MP, Pieters EHE, Van Haastert R, Yousefi A, Mastrobattista E, Storm G, Berezikov E, Cuppen E, Woodle M, Schaapveld RQJ, Prevost GP, Griffioen AW, Van Noort PI , Schiffelers RM (2014) Systemic miRNA-7 delivery inhibits tumor angiogenesis and growth in murine xenograft glioblastoma. Oncotarget.

    • Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, et all. (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature.
    • Lengerer B, Pjeta R, Wunderer J, Rodrigues M, Arbore R, Schärer L, Berezikov E, Hess MW, Pfaller K, Egger B, Obwegeser S, Salvenmoser W, Ladurner P. (2014) Biological adhesion of the flatworm Macrostomum lignano relies on a duo-gland system and is mediated by a cell type-specific intermediate filament protein. Frontiers in Zoology.
    • Moreno-Mateos MA, Barragán V, Torres B, Rodríguez-Mateo C, Méndez-Vidal C, Berezikov E, Mudduluru G, Allgayer H, Pintor-Toro JA. (2013) Novel small RNA expression libraries uncover hsa-miR-30b and hsa-miR-30c as important factors in anoikis resistance. RNA.
    • Isik M, Berezikov E. (2013) Biolistic transformation of Caenorhabditis elegans. Methods Molecular Biology.
    • Janicke T, Marie-Orleach L, De Mulder K, Berezikov E, Ladurner P, Vizoso DB, Schärer L. (2013) Sex allocation adjustment to mating group size in a simultaneous hermaphrodite. Evolution.
    • Demircan T, Berezikov E. (2013) The Hippo pathway regulates stem cells during homeostasis and regeneration of the flatworm Macrostomum lignano. Stem Cells and Development.
    • Leptidis S, El Azzouzi H, Lok SI, de Weger R, Olieslagers S, Kisters N, Silva GJ, Heymans S, Cuppen E, Berezikov E, De Windt LJ, da Costa Martins P. (2013) A deep sequencing approach to uncover the miRNOME in the human heart. PloS One.
    • Chiodin M, Børve A, Berezikov E, Ladurner P, Martinez P, Hejnol A. (2013) Mesodermal gene expression in the acoel Isodiametra pulchra indicates a low number of mesodermal cell types and the endomesodermal origin of the gonads. PloS One.
    • Kaaij LJ, Hoogstrate SW, Berezikov E, Ketting RF. (2013) piRNA dynamics in divergent zebrafish strains reveal long-lasting maternal influence on zygotic piRNA profiles. RNA.
    • Simanov D, Mellaart-Straver I, Sormacheva I, Berezikov E. (2012) The Flatworm Macrostomum lignano Is a Powerful Model Organism for Ion Channel and Stem Cell Research. Stem cells international.
    • Isik M, Berezikov E . (2012) Expression pattern analysis of microRNAs in Caenorhabditis elegans. Methods Molecular Biology.
    • Berezikov E. (2011) Evolution of microRNA diversity and regulation in animals. Nature Reviews Genetics.
    • Ryazansky SS, Gvozdev VA, Berezikov E. (2011) Evidence for post-transcriptional regulation of clustered microRNAs in Drosophila. BMC Genomics.
    • modENCODE Consortium. (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science.
    • Berezikov E, Robine N, Samsonova A, Westholm JO, Naqvi A, Hung JH, Okamura K, Dai Q, Bortolamiol-Becet D, Martin R, Zhao Y, Zamore PD, Hannon GJ, Marra MA, Weng Z, Perrimon N, Lai EC. (2010) Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Research.
    • Isik m, Korswagen H, Berezikov E. (2010) Expression patterns of intronic microRNAs in Caenorhabditis elegans. Silenc.
    • Berezikov E, Liu N, Flynt AS, Hodges E, Rooks M, Hannon GJ, Lai EC. (2010) Evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Nat. Genet.
    • van Wolfswinkel JC, Claycomb JM, Batista PJ, Mello CC, Berezikov E, Ketting RF. (2009) CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell.
    • de Wit E, Linsen SE, Cuppen E, Berezikov E. (2009) Repertoire and evolution of miRNA genes in four divergent nematode species. Genome Res.
    • Vreugdenhil E, Berezikov E. (2009) Fine-tuning the brain: MicroRNAs. Frontiers in Neuroendocrinology.
    • van Rij RP, Berezikov E. (2009) Small RNAs and the control of transposons and viruses in Drosophila. Trends in microbiology.
    • Schwamborn JC, Berezikov E, Knoblich JA. (2009) The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell.
    • Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. (2007) Mammalian mirtron genes. Molecular cell.
    • Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, Draper BW, Ketting RF. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell.
    • Berezikov E, Thuemmler F, van Laake LW, Kondova I, Bontrop R, Cuppen E, Plasterk RH. (2006) Diversity of microRNAs in human and chimpanzee brain. Nature Genetics.
    • Berezikov E, van Tetering G, Verheul M, van de Belt J, van Laake L, Vos J, Verloop R, van de Wetering M, Guryev V, Takada S, van Zonneveld AJ, Mano H, Plasterk R, Cuppen E. (2006) Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysis. Genome Research.
    • Berezikov E, Cuppen E, Plasterk RH. (2006) Approaches to microRNA discovery. Nature Genetics.
    • Berezikov E, Plasterk RH. (2005) Camels and zebrafish, viruses and cancer: a microRNA update. Human Molecular Genetics.
    • Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RH.. (2005) MicroRNA expression in zebrafish embryonic development. Science.v
    • Berezikov E, Guryev V, Cuppen E. (2005) CONREAL web server: identification and visualization of conserved transcription factor binding sites. Nucleic Acids Research.
    • Berezikov E, Guryev V, van de Belt J, Wienholds E, Plasterk RH, Cuppen E. (2005) Phylogenetic shadowing and computational identification of human microRNA genes. Cell.
    • Berezikov E, Guryev V, Plasterk RH, Cuppen E. (2003) CONREAL: conserved regulatory elements anchored alignment algorithm for identification of transcription factor binding sites by phylogenetic footprinting. Genome Research.
    • Berezikov E, Plasterk RH, Cuppen E. (2002) GENOTRACE: cDNA-based local GENOme assembly from TRACE archives. Bioinformatics.
    • Berezikov E, Bucheton A, Busseau I. (2000) A search for reverse transcriptase-coding sequences reveals new non-LTR retrotransposons in the genome of Drosophila melanogaster. Genome Biology.
    • Berezikov E, Blinov AG, Scherbik S, Cox CK, Case ST. (1998) Structure and polymorphism of the Chironomus thummi gene encoding special lobe-specific silk protein, ssp160. Gene.
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