Limits...
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.

Show MeSH

Related in: MedlinePlus

Transmission electron microscopy images of transverse sections of mature sperm heads inside a cyst at the base of a wild-type testis (magnification 28,000×). (A) Cross-section view of mature and individualized sperm nuclei (arrows) inside the head cyst cell (HC, arrowheads). The stage is determined according to an earlier description [4]. Inset shows enlarged view of the nuclei (N) tightly invested with plasma membrane (white arrowhead). The nuclei are embedded in an electron dense material (fine arrows) and membranous projections filled the interstitial space (marked with *). (B) Nuclei (arrows) of post-individualized spermatids inside the head cyst cell are tightly packed with electron dense material around them (fine arrows). They were also placed at one side of the HC. Inset shows 10× enlarged view of part of the bundle. The interstitial space (*) is packed with electron dense material.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2683793&req=5

Figure 2: Transmission electron microscopy images of transverse sections of mature sperm heads inside a cyst at the base of a wild-type testis (magnification 28,000×). (A) Cross-section view of mature and individualized sperm nuclei (arrows) inside the head cyst cell (HC, arrowheads). The stage is determined according to an earlier description [4]. Inset shows enlarged view of the nuclei (N) tightly invested with plasma membrane (white arrowhead). The nuclei are embedded in an electron dense material (fine arrows) and membranous projections filled the interstitial space (marked with *). (B) Nuclei (arrows) of post-individualized spermatids inside the head cyst cell are tightly packed with electron dense material around them (fine arrows). They were also placed at one side of the HC. Inset shows 10× enlarged view of part of the bundle. The interstitial space (*) is packed with electron dense material.

Mentions: Transmission electron microscopy (TEM) studies further showed that the nuclei of the 'individualized' spermatids were tightly invested with plasma membrane (arrows, Figure 2A) and contained very little cytoplasm. They were embedded into the head cyst cell (HC, Figure 2A) with electron dense material around (fine arrows, Figure 2A; see also the inset). An earlier study reported that membrane bound projections containing microfilaments are extended from the head cyst cell and interspersed between the sperm heads after individualization [4]. We also found some tightly packed NBs (arrows, Figure 2B) with dense material around them near the head cyst cell perimeter (fine arrows, Figure 2B; see also the inset). Together with the previous results this suggested that the actin caps are likely to form inside the head cyst cells and therefore, unlikely to be a part of the spermatids.


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)

Transmission electron microscopy images of transverse sections of mature sperm heads inside a cyst at the base of a wild-type testis (magnification 28,000×). (A) Cross-section view of mature and individualized sperm nuclei (arrows) inside the head cyst cell (HC, arrowheads). The stage is determined according to an earlier description [4]. Inset shows enlarged view of the nuclei (N) tightly invested with plasma membrane (white arrowhead). The nuclei are embedded in an electron dense material (fine arrows) and membranous projections filled the interstitial space (marked with *). (B) Nuclei (arrows) of post-individualized spermatids inside the head cyst cell are tightly packed with electron dense material around them (fine arrows). They were also placed at one side of the HC. Inset shows 10× enlarged view of part of the bundle. The interstitial space (*) is packed with electron dense material.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Transmission electron microscopy images of transverse sections of mature sperm heads inside a cyst at the base of a wild-type testis (magnification 28,000×). (A) Cross-section view of mature and individualized sperm nuclei (arrows) inside the head cyst cell (HC, arrowheads). The stage is determined according to an earlier description [4]. Inset shows enlarged view of the nuclei (N) tightly invested with plasma membrane (white arrowhead). The nuclei are embedded in an electron dense material (fine arrows) and membranous projections filled the interstitial space (marked with *). (B) Nuclei (arrows) of post-individualized spermatids inside the head cyst cell are tightly packed with electron dense material around them (fine arrows). They were also placed at one side of the HC. Inset shows 10× enlarged view of part of the bundle. The interstitial space (*) is packed with electron dense material.
Mentions: Transmission electron microscopy (TEM) studies further showed that the nuclei of the 'individualized' spermatids were tightly invested with plasma membrane (arrows, Figure 2A) and contained very little cytoplasm. They were embedded into the head cyst cell (HC, Figure 2A) with electron dense material around (fine arrows, Figure 2A; see also the inset). An earlier study reported that membrane bound projections containing microfilaments are extended from the head cyst cell and interspersed between the sperm heads after individualization [4]. We also found some tightly packed NBs (arrows, Figure 2B) with dense material around them near the head cyst cell perimeter (fine arrows, Figure 2B; see also the inset). Together with the previous results this suggested that the actin caps are likely to form inside the head cyst cells and therefore, unlikely to be a part of the spermatids.

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