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Dynamic interplay of spectrosome and centrosome organelles in asymmetric stem cell divisions.

Bang C, Cheng J - PLoS ONE (2015)

Bottom Line: Utilizing time-lapse live cell imaging, customized tracking, and image processing programs, we found that most acentrosomal GSCs have the spectrosomes reposition from the basal end (wild type) to the apical end close to hub-GSC interface (acentrosomal GSCs).For acentrosomal GSCs, their mitotic spindles were still highly oriented and divided asymmetrically with longer mitosis duration, resulting in asymmetric divisions.Moreover, when the spectrosome was knocked out, the centrosomes velocity decreased and centrosomes located closer to hub-GSC interface.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioengineering, The University of Illinois at Chicago, Chicago, Illinois, United States of America.

ABSTRACT
Stem cells have remarkable self-renewal ability and differentiation potency, which are critical for tissue repair and tissue homeostasis. Recently it has been found, in many systems (e.g. gut, neurons, and hematopoietic stem cells), that the self-renewal and differentiation balance is maintained when the stem cells divide asymmetrically. Drosophila male germline stem cells (GSCs), one of the best characterized model systems with well-defined stem cell niches, were reported to divide asymmetrically, where centrosome plays an important role. Utilizing time-lapse live cell imaging, customized tracking, and image processing programs, we found that most acentrosomal GSCs have the spectrosomes reposition from the basal end (wild type) to the apical end close to hub-GSC interface (acentrosomal GSCs). In addition, these apically positioned spectrosomes were mostly stationary while the basally positioned spectrosomes were mobile. For acentrosomal GSCs, their mitotic spindles were still highly oriented and divided asymmetrically with longer mitosis duration, resulting in asymmetric divisions. Moreover, when the spectrosome was knocked out, the centrosomes velocity decreased and centrosomes located closer to hub-GSC interface. We propose that in male GSCs, the spectrosome recruited to the apical end plays a complimentary role in ensuring proper spindle orientation when centrosome function is compromised.

No MeSH data available.


Spectrosome material is transferred via ring canal in GSCs.Spectrosome (Short Adducin-GFP) in wild type GSC is located in the basal position (0 min: interphase and 24min: metaphase). At 1hr 12min, spectrosome is co-localized with the ring canal structure. Spectrosome, together with ring canal structure, grows into the stem cell daughter at 6hr 16min, segregates into both daughter cells and form spectrosome-like structure again at 15hr 20 min. At 20hr 40 min, spectrosomes in both GSC and gonialblast further develop, and the gonialblast separates from GSC. Cellular boundaries and mitotic spindle are visualized with α-tub-GFP. Black arrow: spectrosome. White dash-arrow: spectrosome and/or ring canal tail. *: hub cells. Yellow dash-line: GSC or gonialblast boundary. Solid white arrow: mitotic spindle.
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pone.0123294.g003: Spectrosome material is transferred via ring canal in GSCs.Spectrosome (Short Adducin-GFP) in wild type GSC is located in the basal position (0 min: interphase and 24min: metaphase). At 1hr 12min, spectrosome is co-localized with the ring canal structure. Spectrosome, together with ring canal structure, grows into the stem cell daughter at 6hr 16min, segregates into both daughter cells and form spectrosome-like structure again at 15hr 20 min. At 20hr 40 min, spectrosomes in both GSC and gonialblast further develop, and the gonialblast separates from GSC. Cellular boundaries and mitotic spindle are visualized with α-tub-GFP. Black arrow: spectrosome. White dash-arrow: spectrosome and/or ring canal tail. *: hub cells. Yellow dash-line: GSC or gonialblast boundary. Solid white arrow: mitotic spindle.

Mentions: Next, we investigated, during asymmetric GSC division, how the spectrosome is dynamically transferred among the two daughter cells. Prior to completion of cytokinesis, spectrosome can initially be received by either stem cell daughter (i.e., GSC) or the differentiating daughter cell (i.e., gonialblast or GB) depending on the positioning of the spectrosomes (apically or basally) at the onset of mitosis. The dynamic spectrosome material transfer process can be illustrated in a typical example shown in Fig 3. Prior to and during mitosis, spectrosome in wild type GSC generally remained stationary at the basal end of the GSC, as shown in Fig 3 (0 min, prior to mitosis and 24 min, metaphase). At the end of mitosis (1hr 12 mins), the spectrosome moved to and localized at the bridge between two daughter cells, presumably co-localized with the intercellular bridge known as ring canal. On wild type spectrosome live-imaging sessions, the spectrosome, whether received by the GSC or the gonialblast during mitosis, in almost all cases conjoined to the ring canal and formed a complex. Many hours later, smaller tail region of the ring canal and spectrosome complex grew and further extended into the daughter GSC (Fig 3, 6hr 16min). Finally, the ring canal and spectrosome complex structure broke apart and was transferred to both the daughter GSC and the gonialblast when the gonialblast and the GSC detached from each other (Fig 3, 15hr 20 min). Typical counts of spectrosome like structures in the GSC (Fig 3, 15hr 20 min) vary from one to multiple. Based on many observations, the gonialblast appeared to inherit larger portions of the spectrosome. The GSC and its spectrosome size further grew while the gonialblast slightly separated away from the stem cell niche (Fig 3, 20hr 40 min). These results demonstrate that ring canal plays an important role in facilitating the spectrosome transfer between the two daughter cells (GSC and gonialblast) regardless of the initial spectrosome position prior to mitosis.


Dynamic interplay of spectrosome and centrosome organelles in asymmetric stem cell divisions.

Bang C, Cheng J - PLoS ONE (2015)

Spectrosome material is transferred via ring canal in GSCs.Spectrosome (Short Adducin-GFP) in wild type GSC is located in the basal position (0 min: interphase and 24min: metaphase). At 1hr 12min, spectrosome is co-localized with the ring canal structure. Spectrosome, together with ring canal structure, grows into the stem cell daughter at 6hr 16min, segregates into both daughter cells and form spectrosome-like structure again at 15hr 20 min. At 20hr 40 min, spectrosomes in both GSC and gonialblast further develop, and the gonialblast separates from GSC. Cellular boundaries and mitotic spindle are visualized with α-tub-GFP. Black arrow: spectrosome. White dash-arrow: spectrosome and/or ring canal tail. *: hub cells. Yellow dash-line: GSC or gonialblast boundary. Solid white arrow: mitotic spindle.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4388834&req=5

pone.0123294.g003: Spectrosome material is transferred via ring canal in GSCs.Spectrosome (Short Adducin-GFP) in wild type GSC is located in the basal position (0 min: interphase and 24min: metaphase). At 1hr 12min, spectrosome is co-localized with the ring canal structure. Spectrosome, together with ring canal structure, grows into the stem cell daughter at 6hr 16min, segregates into both daughter cells and form spectrosome-like structure again at 15hr 20 min. At 20hr 40 min, spectrosomes in both GSC and gonialblast further develop, and the gonialblast separates from GSC. Cellular boundaries and mitotic spindle are visualized with α-tub-GFP. Black arrow: spectrosome. White dash-arrow: spectrosome and/or ring canal tail. *: hub cells. Yellow dash-line: GSC or gonialblast boundary. Solid white arrow: mitotic spindle.
Mentions: Next, we investigated, during asymmetric GSC division, how the spectrosome is dynamically transferred among the two daughter cells. Prior to completion of cytokinesis, spectrosome can initially be received by either stem cell daughter (i.e., GSC) or the differentiating daughter cell (i.e., gonialblast or GB) depending on the positioning of the spectrosomes (apically or basally) at the onset of mitosis. The dynamic spectrosome material transfer process can be illustrated in a typical example shown in Fig 3. Prior to and during mitosis, spectrosome in wild type GSC generally remained stationary at the basal end of the GSC, as shown in Fig 3 (0 min, prior to mitosis and 24 min, metaphase). At the end of mitosis (1hr 12 mins), the spectrosome moved to and localized at the bridge between two daughter cells, presumably co-localized with the intercellular bridge known as ring canal. On wild type spectrosome live-imaging sessions, the spectrosome, whether received by the GSC or the gonialblast during mitosis, in almost all cases conjoined to the ring canal and formed a complex. Many hours later, smaller tail region of the ring canal and spectrosome complex grew and further extended into the daughter GSC (Fig 3, 6hr 16min). Finally, the ring canal and spectrosome complex structure broke apart and was transferred to both the daughter GSC and the gonialblast when the gonialblast and the GSC detached from each other (Fig 3, 15hr 20 min). Typical counts of spectrosome like structures in the GSC (Fig 3, 15hr 20 min) vary from one to multiple. Based on many observations, the gonialblast appeared to inherit larger portions of the spectrosome. The GSC and its spectrosome size further grew while the gonialblast slightly separated away from the stem cell niche (Fig 3, 20hr 40 min). These results demonstrate that ring canal plays an important role in facilitating the spectrosome transfer between the two daughter cells (GSC and gonialblast) regardless of the initial spectrosome position prior to mitosis.

Bottom Line: Utilizing time-lapse live cell imaging, customized tracking, and image processing programs, we found that most acentrosomal GSCs have the spectrosomes reposition from the basal end (wild type) to the apical end close to hub-GSC interface (acentrosomal GSCs).For acentrosomal GSCs, their mitotic spindles were still highly oriented and divided asymmetrically with longer mitosis duration, resulting in asymmetric divisions.Moreover, when the spectrosome was knocked out, the centrosomes velocity decreased and centrosomes located closer to hub-GSC interface.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioengineering, The University of Illinois at Chicago, Chicago, Illinois, United States of America.

ABSTRACT
Stem cells have remarkable self-renewal ability and differentiation potency, which are critical for tissue repair and tissue homeostasis. Recently it has been found, in many systems (e.g. gut, neurons, and hematopoietic stem cells), that the self-renewal and differentiation balance is maintained when the stem cells divide asymmetrically. Drosophila male germline stem cells (GSCs), one of the best characterized model systems with well-defined stem cell niches, were reported to divide asymmetrically, where centrosome plays an important role. Utilizing time-lapse live cell imaging, customized tracking, and image processing programs, we found that most acentrosomal GSCs have the spectrosomes reposition from the basal end (wild type) to the apical end close to hub-GSC interface (acentrosomal GSCs). In addition, these apically positioned spectrosomes were mostly stationary while the basally positioned spectrosomes were mobile. For acentrosomal GSCs, their mitotic spindles were still highly oriented and divided asymmetrically with longer mitosis duration, resulting in asymmetric divisions. Moreover, when the spectrosome was knocked out, the centrosomes velocity decreased and centrosomes located closer to hub-GSC interface. We propose that in male GSCs, the spectrosome recruited to the apical end plays a complimentary role in ensuring proper spindle orientation when centrosome function is compromised.

No MeSH data available.