Drosophila neuroblasts retain the daughter centrosome

Januschke, Jens; Llamazares, Salud; Reina, José; González, Cayetano

doi:10.1038/ncomms1245

Cited by 180 publications

(216 citation statements)

References 60 publications

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“…In the case of ACD, there is controversy over the pattern of centrosome inheritance because different results were reported among various model systems: the mother centrosome remained in the daughter cells with self-renewal potential in Drosophila male germ line stem cells (23) and in developing mouse brain neocortex cells (40), whereas the mother centrosome migrated into the daughter cells with differentiation potential in Drosophila neuroblasts (24,25). Because NuMA (Mud: NuMA ortholog in Drosophila) is known to bind to apical polar proteins to ensure the apical-basal orientation of the mitotic spindle in Drosophila neuroblasts and mouse dermal epidermis cells (14,18,19), our findings suggest that the pattern of centrosome migration in neuroblastoma was consistent with that of centrosome migration reported in Drosophila neuroblasts.…”

Section: Discussionmentioning

confidence: 99%

“…In the case of Drosophila melanogaster male germ line stem cells, the mother centrosome stays at a stem cell that is anchored to the niche, whereas the daughter centrosome migrates to the cells at the opposite side with differentiation potential (23). However, in the case of Drosophila melanogaster neuroblasts, the mother centrosome does not stay at the daughter cell with selfrenewal capacity, but migrates to the daughter cell with differentiation potential (24,25). To address this issue, we conducted immunostaining studies of the cells with (TGW) or without (NB69, SK-N-SH, SH-SY5Y, and SK-N-FI) MYCN amplification using an antibody for the mother centrosome marker, ODF2/ cenexin (26).…”

Section: Acd Preferentially Occurs In Human Neuroblastoma Cells With Amentioning

confidence: 99%

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Evidence of asymmetric cell division and centrosome inheritance in human neuroblastoma cells

Izumi

Kaneko

2012

Proc. Natl. Acad. Sci. U.S.A.

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Asymmetric cell division (ACD) is believed to be a physiological event that occurs during development and tissue homeostasis in a large variety of organisms. ACD produces two unequal daughter cells, one of which resembles a multipotent stem and/or progenitor cell, whereas the other has potential for differentiation. Although recent studies have shown that the balance between self-renewal and differentiation potentials is precisely controlled and that alterations in the balance may lead to tumorigenesis in Drosophila neuroblasts, it is largely unknown whether human cancer cells directly show ACD in an evolutionarily conserved manner. Here, we show that the conserved polarity/spindle protein NuMA is preferentially localized to one side of the cell cortex during cell division, generating unequal inheritance of fate-altering molecules in human neuroblastoma cell lines. We also show that the cells with a single copy of MYCN showed significantly higher percentages of ACD than those with MYCN amplification. Moreover, suppression of MYCN in MYCN-amplified cells caused ACD, whereas expression of MYCN in MYCN-nonamplified cells enhanced symmetric cell division. Furthermore, we demonstrate that centrosome inheritance follows a definite rule in ACD: The daughter centrosome with younger mother centriole is inherited to the daughter cell with NuMA preferentially localized to the cell cortex, whereas the mother centrosome with the older mother centriole migrates to the other daughter cell. Thus, the mechanisms of cell division of ACD or symmetric cell division and centrosome inheritance are recapitulated in human cancer cells, and these findings may facilitate studies on cancer stem cells.

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Section: Discussionmentioning

confidence: 99%

Section: Acd Preferentially Occurs In Human Neuroblastoma Cells With Amentioning

confidence: 99%

Evidence of asymmetric cell division and centrosome inheritance in human neuroblastoma cells

Izumi

Kaneko

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Mother and daughter centrosomes could be traced either by photoconvertible PACT and the daughter centriole marker Cnb (centrobin) (Januschke et al 2011) or distinguished by the different fluorescence intensity of PACT . Early in the cell cycle, the daughter centrosome organizes an aster that remains by the apical cortex, whereas the mother loses PCM and microtubule-organizing activity and moves extensively throughout the cell .…”

Section: Asymmetry Of Centrioles Centrosomes and Fate Decisionsmentioning

confidence: 99%

The Centrosome and Its Duplication Cycle

Hagan

Glover

2015

Cold Spring Harb Perspect Biol

206

194

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“…Indeed, the centrosomes at the poles of the bipolar spindle and inherited separately by the two resulting daughter cells have different ages (15). Although the relevance of this asymmetry is unclear, the inheritance of the old and young centrosomes correlates with specific cell fates in many stem cells (16)(17)(18). We investigated whether the partition of the plasmid clusters correlated with centrosome age.…”

Section: Significancementioning

confidence: 99%

Asymmetric partitioning of transfected DNA during mammalian cell division

Wang

Denoth-Lippuner

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Foreign DNA molecules and chromosomal fragments are generally eliminated from proliferating cells, but we know little about how mammalian cells prevent their propagation. Here, we show that dividing human and canine cells partition transfected plasmid DNA asymmetrically, preferentially into the daughter cell harboring the young centrosome. Independently of how they entered the cell, most plasmids clustered in the cytoplasm. Unlike polystyrene beads of similar size, these clusters remained relatively immobile and physically associated to endoplasmic reticulum-derived membranes, as revealed by live cell and electron microscopy imaging. At entry of mitosis, most clusters localized near the centrosomes. As the two centrosomes split to assemble the bipolar spindle, predominantly the old centrosome migrated away, biasing the partition of the plasmid cluster toward the young centrosome. Down-regulation of the centrosomal proteins Ninein and adenomatous polyposis coli abolished this bias. Thus, we suggest that DNA clustering, cluster immobilization through association to the endoplasmic reticulum membrane, initial proximity between the cluster and centrosomes, and subsequent differential behavior of the two centrosomes together bias the partition of plasmid DNA during mitosis. This process leads to their progressive elimination from the proliferating population and might apply to any kind of foreign DNA molecule in mammalian cells. Furthermore, the functional difference of the centrosomes might also promote the asymmetric partitioning of other cellular components in other mammalian and possibly stem cells.foreign DNA | asymmetric cell division | centrosome | endoplasmic reticulum | Ninein G enerally, noncentromeric DNA molecules are mitotically instable in eukaryotes. This results in their apparent disappearance from an ever-increasing proportion of the progeny of an affected cell (e.g., 1-3). Endogenous sources of such DNA are recombination byproducts [double minutes, extrachromosomal ribosomal (r)DNA circles (ERCs) and other DNA circles (3-6)] or mitotic defects generating noncentromeric chromosomal fragments and cytoplasmic micronuclei (1, 7). Exogenous sources are DNA of pathogens or DNA, typically plasmids, artificially introduced into cells. For the latter, decades of work established that plasmid-born protein expression is transient, persisting only for a few cell cycles (8). This finding is consistent with plasmid DNA being somehow eliminated through divisions. Thus, some mechanisms seem to prevent the propagation of foreign DNA and extrachromosomal DNA in proliferating eukaryotic cells. However, how this is achieved is unclear.In animal cells, DNA sensors mediate the early detection of exogenous DNA, such as DNA of invading pathogens and artificially introduced DNA (9-11). Both in leukocytes and nonprofessional immune cells, these can trigger innate immune responses, such as cytokine production, autophagy, and apoptosis (9). However, what happens to the DNA molecules themselves over time is unclear. When microi...

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Drosophila neuroblasts retain the daughter centrosome

Cited by 180 publications

References 60 publications

Evidence of asymmetric cell division and centrosome inheritance in human neuroblastoma cells

Evidence of asymmetric cell division and centrosome inheritance in human neuroblastoma cells

The Centrosome and Its Duplication Cycle

Asymmetric partitioning of transfected DNA during mammalian cell division

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