Research Groups

Cellular Biochemistry

The research topic of Liesbeth Veenhoff lab is the nuclear envelope. The development of this membrane-bound structure separating DNA from other cellular components was the crucial evolutionary event that gave rise to eukaryotes. The nuclear envelope protects and organizes the genome. Large protein assemblies, the nuclear pore complexes (NPCs), mediate all traffic across the nuclear envelope. They provide a selective channel for transport of macromolecules between the nuclear and the cytoplasmic compartments, and, between the inner and outer membranes of the nuclear envelope.

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  • Liesbeth Veenhoff Visit

    Group Leader of the Laboratory of Cellular Biochemistry

    Research fields

    Nuclear envelope, nuclear pore complex, membrane protein traffic, yeast ageing

    Research Associates
    Anton Steen
    PhD Students
    Sara Mavrova
    Elizabeth Riquelme Barrientos
    Marije Semmelink
    Annemiek Veldsink
  • The group uses baker’s yeast, Saccharomyces cerevisiae, for their studies. The team investigates how the NPC acts as a selective gate for membrane proteins, and regulates the protein composition and function of the inner nuclear membrane, also as a function of age. Baker’s yeast is an interesting model for studying ageing; indeed many of the molecular players were first identified in yeast. Yeast cells divide asymmetrical and while the mother cell ages, the daughter cell retains replicative potential.

    The group aims for a system wide global characterization of age-related changes, as well as detailed understanding how the NPCs and cognate transport factors play a role in cellular ageing and age-related aggregation pathologies. Microscopy, biochemical and proteomics analysis are the main tools used at the lab.

    • Rempel IL, Steen A, Veenhoff LM. (2020) Poor old pores-The challenge of making and maintaining nuclear pore complexes in aging. FEBS J.  
    • Novarina D, Janssens GE, Bokern K, Schut T, van Oerle NC, Kazemier HG, Veenhoff LM, Chang M. (2019) A genome-wide screen identifies genes that suppress the accumulation of spontaneous mutations in young and aged yeast cells. Aging Cell.  
    • Rempel IL, Popken P, Ghavami A, Mishra A, Hapsari RA, Wolters AHG, VeldsinkAC, Klaassens M, Meinema AC, Poolman B, Giepmans BNG, Onck PR, Steen A, Veenhoff LM. (2019) Flexible and Extended Linker Domains Support Efficient Targeting of Heh2 to the Inner Nuclear Membrane. Structure.
    • Rempel IL, Crane MM, Thaller DJ, Mishra A, Jansen DP, Janssens G, Popken P, Akşit A, Kaeberlein M, van der Giessen E, Steen A, Onck PR, Lusk CP, Veenhoff LM. (2019) Age-dependent deterioration of nuclear pore assembly in mitotic cells decreases transport dynamics. Elife.  
    • Cabrera M, Novarina D, Rempel IL, Veenhoff LM, and Chang M. (2017) A simple microfluidic platform to study age-dependent protein abundance and localization changes in Saccharomyces cerevisiae. Microbial Cell.
    • Novarina D, Mavrova SN, Janssens GE, Rempel IL, Veenhoff LM, Chang M. (2017) Increased genome instability is not accompanied by sensitivity to DNA damaging agents in aged yeast cells. DNA Repair.  
    • Janssens GE, Veenhoff LM. (2016) The Natural Variation in Lifespans of Single YeastCells Is Related to Variation in Cell Size, Ribosomal Protein, and Division Time. PLoS One.
    • Janssens GE, Veenhoff LM. (2016) Evidence for the hallmarks of human aging inreplicatively aging yeast. Microb Cell.
    • Janssens GE, Meinema AC, González J, Wolters JC, Schmidt A, Guryev V, Bischoff R, Wit EC, Veenhoff LM, Heinemann M. (2015) Protein biogenesis machinery is a driver of replicative aging in yeast. ELife.
    • Laba JK, Steen A, Popken P, Chernova A, Poolman B, Veenhoff LM. (2015) Active Nuclear Import of Membrane Proteins Revisited. Cells.
    • Kralt A, Jagalur NB, van den Boom V, Lokareddy RK, Steen A, Cingolani G, Fornerod M, Veenhoff LM. (2015) Conservation of inner nuclear membrane targeting sequences in mammalian Pom121 and yeast Heh2 membrane proteins. Molecular Biology of the Cell.
    • Lokareddy RK, Hapsari RA, van Rheenen M, Pumroy RA, Bhardwaj A, Steen A, Veenhoff LM, Cingolani G. (2015) Distinctive Properties of the Nuclear Localization Signals of Inner Nuclear Membrane Proteins Heh1 and Heh2. Structure.
    • Kralt A, Carretta M, Mari M, Reggiori F, Steen A, Poolman B, Veenhoff LM. (2015) Intrinsically disordered linker and plasma membrane-binding motif sort Ist2 andSsy1 to junctions. Traffic.  
    • Popken P, Ghavami A, Onck PR, Poolman B, Veenhoff LM. (2015) Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex. Molecular Biology of the Cell.
    • Ghavami A, Veenhoff LM, van der Giessen E, Onck PR. (2015) Probing the disordered domain of the nuclear pore complex through coarse-grained molecular dynamics simulations. Biophysical Journal.
    • Laba JK, Steen A, Veenhoff LM. (2014) Traffic to the inner membrane of the nuclear envelope. Current Opinion in Cell Biology.
    • Meinema AC, Poolman B, Veenhoff LM. (2013) Quantitative analysis of membrane protein transport across the nuclear pore complex. Traffic.
    • Meinema AC, Poolman B, Veenhoff LM. (2012) The transport of integral membrane proteins across the nuclear pore complex. Nucleus.
    • Meinema AC, Laba JK, Hapsari RA, Otten R, Mulder FA, Kralt A, van den Bogaart G, Lusk CP, Poolman B, Veenhoff LM. (2011) Long unfolded linkers facilitate membrane protein import through the nuclear pore complex. Science.
    • Kooistra SM, van den Boom V, Thummer RP, Johannes F, Wardenaar R, Tesson BM,Veenhoff LM, Fusetti F, O'Neill LP, Turner BM, de Haan G, Eggen BJ. (2010) Undifferentiated embryonic cell transcription factor 1 regulates ESC chromatin organization and gene expression. Stem Cells.
    • Mika JT, van den Bogaart G, Veenhoff L, Krasnikov V, Poolman B. (2010) Molecular sieving properties of the cytoplasm of Escherichia coli and consequences of osmotic stress. Molecular Microbiology.
    • Veenhoff LM, Meinema AC, Poolman B. (2010) A karyopherin acts in localized protein synthesis. Cell Cycle.
    • Wiederhold E, Veenhoff LM, Poolman B, Slotboom DJ. (2009) Proteomics of Saccharomyces cerevisiae Organelles. Molecular & Cellular proteomics.
    • Gauci S, Veenhoff LM, Heck AJ, Krijgsveld J. (2009) Orthogonal separation techniques for the characterization of the yeast nuclear proteome. Journal of proteome research.
    • van den Bogaart G, Meinema AC, Krasnikov V, Veenhoff LM, Poolman B. (2009) Nuclear transport factor directs localization of protein synthesis during mitosis. Nature Cell Biology.
    • Krügel U, Veenhoff LM, Langbein J, Wiederhold E, Liesche J, Friedrich T, Grimm B, Martinoia E, Poolman B, Kühn C. (2008) Transport and sorting of the solanum tuberosum sucrose transporter SUT1 is affected by posttranslational modification. The Plant Cell.
    • Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Rout MP, Sali A. (2007) Determining the architectures of macromolecular assemblies. Nature.
    • Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Sali A, Rout MP. (2007) The molecular architecture of the nuclear pore complex. Nature.
    • van Montfort BA, Doeven MK, Canas B, Veenhoff LM, Poolman B, Robillard GT. (2002) Combined in-gel tryptic digestion and CNBr cleavage for the generation of peptide maps of an integral membrane protein with MALDI-TOF mass spectrometry. Biochimica Biophysica Acta.
    • Dokudovskaya S, Veenhoff LM, Rout MP. (2002) Cleave to leave: structural insights into the dynamic organization of the nuclear pore complex. Molecular Cell.
    • Veenhoff LM, Heuberger EH, Poolman B. (2002) Quaternary structure and function of transport proteins. Trends in Biochemical sciences.
    • Heuberger EH, Veenhoff LM, Duurkens RH, Friesen RH, Poolman B. (2002) Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation. Journal of molecular biology.
    • Veenhoff LM, Heuberger EH, Poolman B. (2001) The lactose transport protein is a cooperative dimer with two sugar translocation pathways. The EMBO Journal.
    • Veenhoff LM, Geertsma ER, Knol J, Poolman B. (2000) Close approximation of putative alpha -helices II, IV, VII, X, and XI in the translocation pathway of the lactose transport protein of Streptococcus thermophilus. The Journal of Biological Chemistry.
    • Veenhoff LM, Poolman B. (1999) Substrate recognition at the cytoplasmic and extracellular binding site of the lactose transport protein of Streptococcus thermophilus. The Journal of Biological Chemistry.
    • Spooner PJ, Veenhoff LM, Watts A, Poolman B. (1999) Structural information on a membrane transport protein from nuclear magnetic resonance spectroscopy using sequence-selective nitroxide labeling. Biochemistry.
    • Knol J, Veenhoff LM, Liang WJ, Henderson PJ, Leblanc G, Poolman B. (1996) Unidirectional reconstitution into detergent-destabilized liposomes of the purified lactose transport system of Streptococcus thermophilus. The Journal of Biological Chemistry.
  • PhD students trained in the lab of Liesbeth Veenhoff:

    2012 Anne Meinema
    Postdoctoral Fellow ETH Zurich, Switserland

    2015 Annemarie Kralt
    Postdoctoral Fellow, ETH Zurich, Switserland

    2015 Petra Popken
    PRA Health Sciences, the Netherlands

    2016 Justyna Laba
    PRA Health Sciences, the Netherlands

    2016 R. Astri Hapsari
    Postdoctoral Fellow, Institut Teknologi Bandung (ITB), Indonesia

    2016 Georges Janssens
    Postdoctoral Fellow, Karolinska Institute, Stockholm, Sweden

    2019 Irina Rempel

    Biozentrum, University of Basel, Switzerland




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