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  1. Article ; Online: How stem cells remember their past.

    Royall, Lars N / Jessberger, Sebastian

    Current opinion in cell biology

    2021  Volume 69, Page(s) 17–22

    Abstract: Somatic stem cells are required for tissue development, homeostasis, and repair. Recent data suggested that previous biographical experiences of individual stem cells influence their behavior in the context of tissue formation and govern stem cell ... ...

    Abstract Somatic stem cells are required for tissue development, homeostasis, and repair. Recent data suggested that previous biographical experiences of individual stem cells influence their behavior in the context of tissue formation and govern stem cell responses to external stimuli. Here we provide a concise review how a cell's biography, for example, previous rounds of cell divisions or the age-dependent accumulation of cellular damage, is remembered in stem cells and how previous experiences affect the segregation of cellular components, thus guiding cellular behavior in vertebrate stem cells. Further, we suggest future directions of research that may help to unravel the molecular underpinnings of how past experiences guide future cellular behavior.
    MeSH term(s) Cell Division ; Homeostasis ; Stem Cells
    Language English
    Publishing date 2021-01-08
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't ; Review
    ZDB-ID 1026381-0
    ISSN 1879-0410 ; 0955-0674
    ISSN (online) 1879-0410
    ISSN 0955-0674
    DOI 10.1016/j.ceb.2020.12.008
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  2. Article ; Online: Asymmetric inheritance of centrosomes maintains stem cell properties in human neural progenitor cells.

    Royall, Lars N / Machado, Diana / Jessberger, Sebastian / Denoth-Lippuner, Annina

    eLife

    2023  Volume 12

    Abstract: During human forebrain development, neural progenitor cells (NPCs) in the ventricular zone (VZ) undergo asymmetric cell divisions to produce a self-renewed progenitor cell, maintaining the potential to go through additional rounds of cell divisions, and ... ...

    Abstract During human forebrain development, neural progenitor cells (NPCs) in the ventricular zone (VZ) undergo asymmetric cell divisions to produce a self-renewed progenitor cell, maintaining the potential to go through additional rounds of cell divisions, and differentiating daughter cells, populating the developing cortex. Previous work in the embryonic rodent brain suggested that the preferential inheritance of the pre-existing (older) centrosome to the self-renewed progenitor cell is required to maintain stem cell properties, ensuring proper neurogenesis. If asymmetric segregation of centrosomes occurs in NPCs of the developing human brain, which depends on unique molecular regulators and species-specific cellular composition, remains unknown. Using a novel, recombination-induced tag exchange-based genetic tool to birthdate and track the segregation of centrosomes over multiple cell divisions in human embryonic stem cell-derived regionalised forebrain organoids, we show the preferential inheritance of the older mother centrosome towards self-renewed NPCs. Aberration of asymmetric segregation of centrosomes by genetic manipulation of the centrosomal, microtubule-associated protein Ninein alters fate decisions of NPCs and their maintenance in the VZ of human cortical organoids. Thus, the data described here use a novel genetic approach to birthdate centrosomes in human cells and identify asymmetric inheritance of centrosomes as a mechanism to maintain self-renewal properties and to ensure proper neurogenesis in human NPCs.
    MeSH term(s) Humans ; Neural Stem Cells ; Centrosome/metabolism ; Cell Division ; Brain/metabolism ; Neurogenesis
    Language English
    Publishing date 2023-10-26
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 2687154-3
    ISSN 2050-084X ; 2050-084X
    ISSN (online) 2050-084X
    ISSN 2050-084X
    DOI 10.7554/eLife.83157
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  3. Article ; Online: Injection and electroporation of plasmid DNA into human cortical organoids.

    Denoth-Lippuner, Annina / Royall, Lars N / Gonzalez-Bohorquez, Daniel / Machado, Diana / Jessberger, Sebastian

    STAR protocols

    2022  Volume 3, Issue 1, Page(s) 101129

    Abstract: Pluripotent stem cell-derived human cortical organoids allow for the analysis of stem cell behavior and neurogenesis in neural tissues. Delivery of plasmid DNA into organoids permits visualization of individual cells, characterization of cellular ... ...

    Abstract Pluripotent stem cell-derived human cortical organoids allow for the analysis of stem cell behavior and neurogenesis in neural tissues. Delivery of plasmid DNA into organoids permits visualization of individual cells, characterization of cellular components, and manipulation of gene expression. We describe a protocol to transfect cells inside organoids with plasmid DNA using micro-injection and electroporation, allowing for DNA delivery to cells within cortical units. This protocol was optimized for cortical organoids; however, it may be adapted to other organoid models. For complete details on the use and execution of this protocol, please refer to Denoth-Lippuner et al. (2021).
    MeSH term(s) Cerebral Cortex/metabolism ; DNA/genetics ; Electroporation ; Humans ; Organoids/metabolism ; Plasmids ; Transfection
    Chemical Substances DNA (9007-49-2)
    Language English
    Publishing date 2022-01-20
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ISSN 2666-1667
    ISSN (online) 2666-1667
    DOI 10.1016/j.xpro.2022.101129
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  4. Article ; Online: Human neural progenitors establish a diffusion barrier in the endoplasmic reticulum membrane during cell division.

    Bin Imtiaz, Muhammad Khadeesh / Royall, Lars N / Gonzalez-Bohorquez, Daniel / Jessberger, Sebastian

    Development (Cambridge, England)

    2022  Volume 149, Issue 20

    Abstract: Asymmetric segregation of cellular components regulates the fate and behavior of somatic stem cells. Similar to dividing budding yeast and precursor cells in Caenorhabditis elegans, it has been shown that mouse neural progenitors establish a diffusion ... ...

    Abstract Asymmetric segregation of cellular components regulates the fate and behavior of somatic stem cells. Similar to dividing budding yeast and precursor cells in Caenorhabditis elegans, it has been shown that mouse neural progenitors establish a diffusion barrier in the membrane of the endoplasmic reticulum (ER), which has been associated with asymmetric partitioning of damaged proteins and cellular age. However, the existence of an ER diffusion barrier in human cells remains unknown. Here, we used fluorescence loss in photobleaching (FLIP) imaging to show that human embryonic stem cell (hESC)- and induced pluripotent stem cell (iPSC)-derived neural progenitor cells establish an ER diffusion barrier during cell division. The human ER diffusion barrier is regulated via lamin-dependent mechanisms and is associated with asymmetric segregation of mono- and polyubiquitylated damaged proteins. Further, forebrain regionalized organoids derived from hESCs were used to show the establishment of an ER membrane diffusion barrier in more naturalistic tissues, mimicking early steps of human brain development. Thus, the data provided here show that human neural progenitors establish a diffusion barrier during cell division in the membrane of the ER, which may allow for asymmetric segregation of cellular components, contributing to the fate and behavior of human neural progenitor cells.
    MeSH term(s) Cell Division ; Diffusion ; Endoplasmic Reticulum/metabolism ; Humans ; Neural Stem Cells/metabolism
    Language English
    Publishing date 2022-08-04
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 90607-4
    ISSN 1477-9129 ; 0950-1991
    ISSN (online) 1477-9129
    ISSN 0950-1991
    DOI 10.1242/dev.200613
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  5. Article ; Online: The CUL4B-based E3 ubiquitin ligase regulates mitosis and brain development by recruiting phospho-specific DCAFs.

    Stier, Anna / Gilberto, Samuel / Mohamed, Weaam I / Royall, Lars N / Helenius, Jonne / Mikicic, Ivan / Sajic, Tatjana / Beli, Petra / Müller, Daniel J / Jessberger, Sebastian / Peter, Matthias

    The EMBO journal

    2023  Volume 42, Issue 17, Page(s) e112847

    Abstract: The paralogs CUL4A and CUL4B assemble cullin-RING E3 ubiquitin ligase (CRL) complexes regulating multiple chromatin-associated cellular functions. Although they are structurally similar, we found that the unique N-terminal extension of CUL4B is heavily ... ...

    Abstract The paralogs CUL4A and CUL4B assemble cullin-RING E3 ubiquitin ligase (CRL) complexes regulating multiple chromatin-associated cellular functions. Although they are structurally similar, we found that the unique N-terminal extension of CUL4B is heavily phosphorylated during mitosis, and the phosphorylation pattern is perturbed in the CUL4B-P50L mutation causing X-linked intellectual disability (XLID). Phenotypic characterization and mutational analysis revealed that CUL4B phosphorylation is required for efficient progression through mitosis, controlling spindle positioning and cortical tension. While CUL4B phosphorylation triggers chromatin exclusion, it promotes binding to actin regulators and to two previously unrecognized CUL4B-specific substrate receptors (DCAFs), LIS1 and WDR1. Indeed, co-immunoprecipitation experiments and biochemical analysis revealed that LIS1 and WDR1 interact with DDB1, and their binding is enhanced by the phosphorylated N-terminal domain of CUL4B. Finally, a human forebrain organoid model demonstrated that CUL4B is required to develop stable ventricular structures that correlate with onset of forebrain differentiation. Together, our study uncovers previously unrecognized DCAFs relevant for mitosis and brain development that specifically bind CUL4B, but not the CUL4B-P50L patient mutant, by a phosphorylation-dependent mechanism.
    MeSH term(s) Humans ; Ubiquitin-Protein Ligases/genetics ; Ubiquitin-Protein Ligases/metabolism ; Ubiquitination ; Mitosis ; Chromatin ; Brain/metabolism ; Cullin Proteins/genetics ; Cullin Proteins/metabolism
    Chemical Substances Ubiquitin-Protein Ligases (EC 2.3.2.27) ; Chromatin ; Cullin Proteins ; CUL4A protein, human ; CUL4B protein, human
    Language English
    Publishing date 2023-06-27
    Publishing country England
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 586044-1
    ISSN 1460-2075 ; 0261-4189
    ISSN (online) 1460-2075
    ISSN 0261-4189
    DOI 10.15252/embj.2022112847
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  6. Article ; Online: Visualization of individual cell division history in complex tissues using iCOUNT.

    Denoth-Lippuner, Annina / Jaeger, Baptiste N / Liang, Tong / Royall, Lars N / Chie, Stefanie E / Buthey, Kilian / Machado, Diana / Korobeynyk, Vladislav I / Kruse, Merit / Munz, Clara M / Gerbaulet, Alexander / Simons, Benjamin D / Jessberger, Sebastian

    Cell stem cell

    2021  Volume 28, Issue 11, Page(s) 2020–2034.e12

    Abstract: The division potential of individual stem cells and the molecular consequences of successive rounds of proliferation remain largely unknown. Here, we developed an inducible cell division counter (iCOUNT) that reports cell division events in human and ... ...

    Abstract The division potential of individual stem cells and the molecular consequences of successive rounds of proliferation remain largely unknown. Here, we developed an inducible cell division counter (iCOUNT) that reports cell division events in human and mouse tissues in vitro and in vivo. Analyzing cell division histories of neural stem/progenitor cells (NSPCs) in the developing and adult brain, we show that iCOUNT can provide novel insights into stem cell behavior. Further, we use single-cell RNA sequencing (scRNA-seq) of iCOUNT-labeled NSPCs and their progenies from the developing mouse cortex and forebrain-regionalized human organoids to identify functionally relevant molecular pathways that are commonly regulated between mouse and human cells, depending on individual cell division histories. Thus, we developed a tool to characterize the molecular consequences of repeated cell divisions of stem cells that allows an analysis of the cellular principles underlying tissue formation, homeostasis, and repair.
    MeSH term(s) Animals ; Brain ; Cell Division ; Cell Proliferation ; Mice ; Neural Stem Cells ; Organoids ; Sequence Analysis, RNA
    Language English
    Publishing date 2021-09-14
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't
    ZDB-ID 2375354-7
    ISSN 1875-9777 ; 1934-5909
    ISSN (online) 1875-9777
    ISSN 1934-5909
    DOI 10.1016/j.stem.2021.08.012
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  7. Article ; Online: A novel culture method reveals unique neural stem/progenitors in mature porcine iris tissues that differentiate into neuronal and rod photoreceptor-like cells.

    Royall, Lars N / Lea, Daniel / Matsushita, Tamami / Takeda, Taka-Aki / Taketani, Shigeru / Araki, Masasuke

    Brain research

    2017  Volume 1675, Page(s) 51–60

    Abstract: Iris neural stem/progenitor cells from mature porcine eyes were investigated using a new protocol for tissue culture, which consists of dispase treatment and Matrigel embedding. We used a number of culture conditions and found an intense differentiation ... ...

    Abstract Iris neural stem/progenitor cells from mature porcine eyes were investigated using a new protocol for tissue culture, which consists of dispase treatment and Matrigel embedding. We used a number of culture conditions and found an intense differentiation of neuronal cells from both the iris pigmented epithelial (IPE) cells and the stroma tissue cells. Rod photoreceptor-like cells were also observed but mostly in a later stage of culture. Neuronal differentiation does not require any additives such as fetal bovine serum or FGF2, although FGF2 and IGF2 appeared to promote neural differentiation in the IPE cultures. Furthermore, the stroma-derived cells were able to be maintained in vitro indefinitely. The evolutionary similarity between humans and domestic pigs highlight the potential for this methodology in the modeling of human diseases and characterizing human ocular stem cells.
    Language English
    Publishing date 2017-11-15
    Publishing country Netherlands
    Document type Journal Article
    ZDB-ID 1200-2
    ISSN 1872-6240 ; 0006-8993
    ISSN (online) 1872-6240
    ISSN 0006-8993
    DOI 10.1016/j.brainres.2017.08.027
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