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F-actin-based extensions of the head cyst cell adhere to the maturing spermatids to maintain them in a tight bundle and prevent their premature release in Drosophila testis.

Desai BS, Shirolikar S, Ray K - BMC Biol. (2009)

Bottom Line: Disruption of these F-actin based processes was associated with spermatid bundle disassembly and premature sperm release inside the testis.This is likely to regulate mature sperm release into the seminal vesicle.Overall, this process bears resemblance to mammalian spermiation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai, India. bela@tifr.res.in

ABSTRACT

Background: In Drosophila, all the 64 clonally derived spermatocytes differentiate in syncytium inside two somatic-origin cyst cells. They elongate to form slender spermatids, which are individualized and then released into the seminal vesicle. During individualization, differentiating spermatids are organized in a tight bundle inside the cyst, which is expected to play an important role in sperm selection. However, actual significance of this process and its underlying mechanism are unclear.

Results: We show that dynamic F-actin-based processes extend from the head cyst cell at the start of individualization, filling the interstitial space at the rostral ends of the maturing spermatid bundle. In addition to actin, these structures contained lamin, beta-catenin, dynamin, myosin VI and several other filopodial components. Further, pharmacological and genetic analyses showed that cytoskeletal stability and dynamin function are essential for their maintenance. Disruption of these F-actin based processes was associated with spermatid bundle disassembly and premature sperm release inside the testis.

Conclusion: Altogether, our data suggests that the head cyst cell adheres to the maturing spermatid heads through F-actin-based extensions, thus maintaining them in a tight bundle. This is likely to regulate mature sperm release into the seminal vesicle. Overall, this process bears resemblance to mammalian spermiation.

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Anatomical organization and molecular compositions of actin cap structures around the sperm head assembly inside head cyst cell. (A) Summary of the observations and indication of the positions of (a) the individualization stage, (b) coiled-up stage and (c) empty cysts inside a testis (gray out line). The positions of germ line stem cell (GSC) at the apex and the head and tail cyst cells are marked with distinct colors as indicated in the figure. The axoneme of maturing spermatids (black), the cell nuclei (blue) and major F-actin based structures (red) are highlighted to illustrate the basic observation of this study. The rostral ends of the sperm nuclei moved very slowly towards seminal vesicle during individualization until the mature sperm penetrate the head cyst cell to enter the seminal vesicle. (B) Cross-section view of the relative organizations of actin caps inside head cyst cell and sperm heads during individualization. It is partly adapted from a previous description [1] and updated to summarize the data presented in this report. Only four spermatids are drawn for simplicity in illustrating the organization. The compositions of the different regions are indicated by color coding as shown in the adjacent panel.
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Figure 9: Anatomical organization and molecular compositions of actin cap structures around the sperm head assembly inside head cyst cell. (A) Summary of the observations and indication of the positions of (a) the individualization stage, (b) coiled-up stage and (c) empty cysts inside a testis (gray out line). The positions of germ line stem cell (GSC) at the apex and the head and tail cyst cells are marked with distinct colors as indicated in the figure. The axoneme of maturing spermatids (black), the cell nuclei (blue) and major F-actin based structures (red) are highlighted to illustrate the basic observation of this study. The rostral ends of the sperm nuclei moved very slowly towards seminal vesicle during individualization until the mature sperm penetrate the head cyst cell to enter the seminal vesicle. (B) Cross-section view of the relative organizations of actin caps inside head cyst cell and sperm heads during individualization. It is partly adapted from a previous description [1] and updated to summarize the data presented in this report. Only four spermatids are drawn for simplicity in illustrating the organization. The compositions of the different regions are indicated by color coding as shown in the adjacent panel.

Mentions: In summary, our results highlight the cellular and molecular mechanism of the sperm bundling process in Drosophila . Previous anatomical studies in Drosophila [4] as well as in several other insects [51,52] established that spermatids are tightly bundled towards the end of differentiation and before their release into the SV. This process is predicted to single out abnormal sperm after individualization and thus acts as a quality control step in spermiogenesis [1,4]. However, the cellular and molecular mechanism underlying this process was unknown. The sperm heads are embedded into the somatic-origin head cyst cell at the start of individualization. We have shown that they are held by the head cyst cell through F-actin-based extensions (Figure 9A), Immunohistochemical characterizations combined with pharmacological interventions showed that these are filopodia-like extensions adherent to the maturing sperm heads (Figure 9B). Finally, molecular genetic analysis suggested that shibire/dynamin function is essential in the head cyst cells to maintain the sperm heads in a bundle and prevent their premature release inside the testis. These observations have several interesting parallels with the spermiation process in the mammalian system as discussed in the following sections.


F-actin-based extensions of the head cyst cell adhere to the maturing spermatids to maintain them in a tight bundle and prevent their premature release in Drosophila testis.

Desai BS, Shirolikar S, Ray K - BMC Biol. (2009)

Anatomical organization and molecular compositions of actin cap structures around the sperm head assembly inside head cyst cell. (A) Summary of the observations and indication of the positions of (a) the individualization stage, (b) coiled-up stage and (c) empty cysts inside a testis (gray out line). The positions of germ line stem cell (GSC) at the apex and the head and tail cyst cells are marked with distinct colors as indicated in the figure. The axoneme of maturing spermatids (black), the cell nuclei (blue) and major F-actin based structures (red) are highlighted to illustrate the basic observation of this study. The rostral ends of the sperm nuclei moved very slowly towards seminal vesicle during individualization until the mature sperm penetrate the head cyst cell to enter the seminal vesicle. (B) Cross-section view of the relative organizations of actin caps inside head cyst cell and sperm heads during individualization. It is partly adapted from a previous description [1] and updated to summarize the data presented in this report. Only four spermatids are drawn for simplicity in illustrating the organization. The compositions of the different regions are indicated by color coding as shown in the adjacent panel.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2683793&req=5

Figure 9: Anatomical organization and molecular compositions of actin cap structures around the sperm head assembly inside head cyst cell. (A) Summary of the observations and indication of the positions of (a) the individualization stage, (b) coiled-up stage and (c) empty cysts inside a testis (gray out line). The positions of germ line stem cell (GSC) at the apex and the head and tail cyst cells are marked with distinct colors as indicated in the figure. The axoneme of maturing spermatids (black), the cell nuclei (blue) and major F-actin based structures (red) are highlighted to illustrate the basic observation of this study. The rostral ends of the sperm nuclei moved very slowly towards seminal vesicle during individualization until the mature sperm penetrate the head cyst cell to enter the seminal vesicle. (B) Cross-section view of the relative organizations of actin caps inside head cyst cell and sperm heads during individualization. It is partly adapted from a previous description [1] and updated to summarize the data presented in this report. Only four spermatids are drawn for simplicity in illustrating the organization. The compositions of the different regions are indicated by color coding as shown in the adjacent panel.
Mentions: In summary, our results highlight the cellular and molecular mechanism of the sperm bundling process in Drosophila . Previous anatomical studies in Drosophila [4] as well as in several other insects [51,52] established that spermatids are tightly bundled towards the end of differentiation and before their release into the SV. This process is predicted to single out abnormal sperm after individualization and thus acts as a quality control step in spermiogenesis [1,4]. However, the cellular and molecular mechanism underlying this process was unknown. The sperm heads are embedded into the somatic-origin head cyst cell at the start of individualization. We have shown that they are held by the head cyst cell through F-actin-based extensions (Figure 9A), Immunohistochemical characterizations combined with pharmacological interventions showed that these are filopodia-like extensions adherent to the maturing sperm heads (Figure 9B). Finally, molecular genetic analysis suggested that shibire/dynamin function is essential in the head cyst cells to maintain the sperm heads in a bundle and prevent their premature release inside the testis. These observations have several interesting parallels with the spermiation process in the mammalian system as discussed in the following sections.

Bottom Line: Disruption of these F-actin based processes was associated with spermatid bundle disassembly and premature sperm release inside the testis.This is likely to regulate mature sperm release into the seminal vesicle.Overall, this process bears resemblance to mammalian spermiation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai, India. bela@tifr.res.in

ABSTRACT

Background: In Drosophila, all the 64 clonally derived spermatocytes differentiate in syncytium inside two somatic-origin cyst cells. They elongate to form slender spermatids, which are individualized and then released into the seminal vesicle. During individualization, differentiating spermatids are organized in a tight bundle inside the cyst, which is expected to play an important role in sperm selection. However, actual significance of this process and its underlying mechanism are unclear.

Results: We show that dynamic F-actin-based processes extend from the head cyst cell at the start of individualization, filling the interstitial space at the rostral ends of the maturing spermatid bundle. In addition to actin, these structures contained lamin, beta-catenin, dynamin, myosin VI and several other filopodial components. Further, pharmacological and genetic analyses showed that cytoskeletal stability and dynamin function are essential for their maintenance. Disruption of these F-actin based processes was associated with spermatid bundle disassembly and premature sperm release inside the testis.

Conclusion: Altogether, our data suggests that the head cyst cell adheres to the maturing spermatid heads through F-actin-based extensions, thus maintaining them in a tight bundle. This is likely to regulate mature sperm release into the seminal vesicle. Overall, this process bears resemblance to mammalian spermiation.

Show MeSH
Related in: MedlinePlus