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Bällchen participates in proliferation control and prevents the differentiation of Drosophila melanogaster neuronal stem cells.

Yakulov T, Günesdogan U, Jäckle H, Herzig A - Biol Open (2014)

Bottom Line: Our results show that the brains of ball mutant larvae are severely reduced in size, which is caused by a reduced proliferation rate of the neuroblasts.Moreover, ball mutant neuroblasts gradually lose the expression of the neuroblast determinants Miranda and aPKC, suggesting their premature differentiation.Our results indicate that BALL represents a novel cell intrinsic factor with a dual function regulating the proliferative capacity and the differentiation status of neuronal stem cells during development.

View Article: PubMed Central - PubMed

Affiliation: Present address: Renal Division, University Hospital Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germany.

No MeSH data available.


Related in: MedlinePlus

ball2 mutant thoracic pNBs proliferate at a reduced rate.(A–A″) Control wild type cell lineage labeled by tub-GAL4 dependent β-Galactosidase (β-Gal) expression through the MARCM system. (A) 3D reconstruction from confocal image sections. Also shown are tilted views of the reconstruction (A′) and a single focal plane (A″) of which the position is indicated by a red dashed line in (A). An individual cell lineage is marked by a white dashed outline. (B) Counterstaining for DNA and the neuronal marker Elav (ELAV). Asterisks indicate the position of the pNBs, arrowheads point at GMCs, which lack ELAV expression. (C–C″) ball2 mutant cell lineages stained, analyzed and displayed the same way as control wild type lineages (A–A″). (D) Counterstaining as in (B). (E) Quantification of neuronal cell numbers in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH. The Number of ELAV expressing cells per cell lineage is displayed on the y-axis (neurons). Mean values and the total number of cell lineages analyzed (n) are given above the bars. (F) Quantification of mitotic pNBs in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The fraction of pNBs that were in mitosis, based on H3S10ph positive staining, is indicated on the y-axis. Mean values and the total number of marked pNBs (n) are given above the bars. (G) Quantification of GMCs lacking ELAV expression in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The number of ELAV negative cells below pNB size per marked cell lineage is indicated on the y-axis. Mean values and the total number of cell lineages (n) are given above the bars. Significance levels from Student's t-tests: p <0.005 (**), p <0.0005 (***). Scale bar in A–D, 10 µm.
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f03: ball2 mutant thoracic pNBs proliferate at a reduced rate.(A–A″) Control wild type cell lineage labeled by tub-GAL4 dependent β-Galactosidase (β-Gal) expression through the MARCM system. (A) 3D reconstruction from confocal image sections. Also shown are tilted views of the reconstruction (A′) and a single focal plane (A″) of which the position is indicated by a red dashed line in (A). An individual cell lineage is marked by a white dashed outline. (B) Counterstaining for DNA and the neuronal marker Elav (ELAV). Asterisks indicate the position of the pNBs, arrowheads point at GMCs, which lack ELAV expression. (C–C″) ball2 mutant cell lineages stained, analyzed and displayed the same way as control wild type lineages (A–A″). (D) Counterstaining as in (B). (E) Quantification of neuronal cell numbers in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH. The Number of ELAV expressing cells per cell lineage is displayed on the y-axis (neurons). Mean values and the total number of cell lineages analyzed (n) are given above the bars. (F) Quantification of mitotic pNBs in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The fraction of pNBs that were in mitosis, based on H3S10ph positive staining, is indicated on the y-axis. Mean values and the total number of marked pNBs (n) are given above the bars. (G) Quantification of GMCs lacking ELAV expression in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The number of ELAV negative cells below pNB size per marked cell lineage is indicated on the y-axis. Mean values and the total number of cell lineages (n) are given above the bars. Significance levels from Student's t-tests: p <0.005 (**), p <0.0005 (***). Scale bar in A–D, 10 µm.

Mentions: Thoracic pNBs resume proliferation at about 36 h after larval hatching (ALH) (Maurange and Gould, 2005). To visualize entire cell lineages that derived from wild type and ball2 mutant NBs, we induced MARCM clones at 24 h ALH, dissected the brains at 96 h ALH and stained them with antibodies against β-Gal and the neuronal marker protein ELAV. Both wild type and ball2 mutant lineages contained multiple ELAV positive neurons, small ELAV negative GMCs and one large ELAV negative pNB (Fig. 3), which was confirmed by antibody staining to visualize additional NB markers such as MIRA and aPKC (see below). The observation that ball2 mutant pNBs were able to generate cell lineages including differentiating neurons demonstrates that BALL is dispensable for the differentiation of both GMCs and neurons.


Bällchen participates in proliferation control and prevents the differentiation of Drosophila melanogaster neuronal stem cells.

Yakulov T, Günesdogan U, Jäckle H, Herzig A - Biol Open (2014)

ball2 mutant thoracic pNBs proliferate at a reduced rate.(A–A″) Control wild type cell lineage labeled by tub-GAL4 dependent β-Galactosidase (β-Gal) expression through the MARCM system. (A) 3D reconstruction from confocal image sections. Also shown are tilted views of the reconstruction (A′) and a single focal plane (A″) of which the position is indicated by a red dashed line in (A). An individual cell lineage is marked by a white dashed outline. (B) Counterstaining for DNA and the neuronal marker Elav (ELAV). Asterisks indicate the position of the pNBs, arrowheads point at GMCs, which lack ELAV expression. (C–C″) ball2 mutant cell lineages stained, analyzed and displayed the same way as control wild type lineages (A–A″). (D) Counterstaining as in (B). (E) Quantification of neuronal cell numbers in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH. The Number of ELAV expressing cells per cell lineage is displayed on the y-axis (neurons). Mean values and the total number of cell lineages analyzed (n) are given above the bars. (F) Quantification of mitotic pNBs in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The fraction of pNBs that were in mitosis, based on H3S10ph positive staining, is indicated on the y-axis. Mean values and the total number of marked pNBs (n) are given above the bars. (G) Quantification of GMCs lacking ELAV expression in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The number of ELAV negative cells below pNB size per marked cell lineage is indicated on the y-axis. Mean values and the total number of cell lineages (n) are given above the bars. Significance levels from Student's t-tests: p <0.005 (**), p <0.0005 (***). Scale bar in A–D, 10 µm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4197436&req=5

f03: ball2 mutant thoracic pNBs proliferate at a reduced rate.(A–A″) Control wild type cell lineage labeled by tub-GAL4 dependent β-Galactosidase (β-Gal) expression through the MARCM system. (A) 3D reconstruction from confocal image sections. Also shown are tilted views of the reconstruction (A′) and a single focal plane (A″) of which the position is indicated by a red dashed line in (A). An individual cell lineage is marked by a white dashed outline. (B) Counterstaining for DNA and the neuronal marker Elav (ELAV). Asterisks indicate the position of the pNBs, arrowheads point at GMCs, which lack ELAV expression. (C–C″) ball2 mutant cell lineages stained, analyzed and displayed the same way as control wild type lineages (A–A″). (D) Counterstaining as in (B). (E) Quantification of neuronal cell numbers in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH. The Number of ELAV expressing cells per cell lineage is displayed on the y-axis (neurons). Mean values and the total number of cell lineages analyzed (n) are given above the bars. (F) Quantification of mitotic pNBs in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The fraction of pNBs that were in mitosis, based on H3S10ph positive staining, is indicated on the y-axis. Mean values and the total number of marked pNBs (n) are given above the bars. (G) Quantification of GMCs lacking ELAV expression in wild type control (green) and ball2 mutant (red) cell lineages at 96 h and 72 h ALH, respectively. The number of ELAV negative cells below pNB size per marked cell lineage is indicated on the y-axis. Mean values and the total number of cell lineages (n) are given above the bars. Significance levels from Student's t-tests: p <0.005 (**), p <0.0005 (***). Scale bar in A–D, 10 µm.
Mentions: Thoracic pNBs resume proliferation at about 36 h after larval hatching (ALH) (Maurange and Gould, 2005). To visualize entire cell lineages that derived from wild type and ball2 mutant NBs, we induced MARCM clones at 24 h ALH, dissected the brains at 96 h ALH and stained them with antibodies against β-Gal and the neuronal marker protein ELAV. Both wild type and ball2 mutant lineages contained multiple ELAV positive neurons, small ELAV negative GMCs and one large ELAV negative pNB (Fig. 3), which was confirmed by antibody staining to visualize additional NB markers such as MIRA and aPKC (see below). The observation that ball2 mutant pNBs were able to generate cell lineages including differentiating neurons demonstrates that BALL is dispensable for the differentiation of both GMCs and neurons.

Bottom Line: Our results show that the brains of ball mutant larvae are severely reduced in size, which is caused by a reduced proliferation rate of the neuroblasts.Moreover, ball mutant neuroblasts gradually lose the expression of the neuroblast determinants Miranda and aPKC, suggesting their premature differentiation.Our results indicate that BALL represents a novel cell intrinsic factor with a dual function regulating the proliferative capacity and the differentiation status of neuronal stem cells during development.

View Article: PubMed Central - PubMed

Affiliation: Present address: Renal Division, University Hospital Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germany.

No MeSH data available.


Related in: MedlinePlus