Sperm Head-Tail Linkage Requires Restriction of Pericentriolar Material to the Proximal Centriole End

Galletta, Brian J.; Ortega, Jacob M.; Smith, Samantha L.; Fagerstrom, Carey J.; Fear, Justin M.; Mahadevaraju, Sharvani; Oliver, Brian; Rusan, Nasser M.

doi:10.1016/j.devcel.2020.02.006

Cited by 18 publications

(45 citation statements)

References 89 publications

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“…The signals leading to the local interruption of the dense complex as the centriole approaches are still unclear. It has been recently shown that the docking of the basal body to the nucleus in Drosophila requires a mechanism that relies on the restriction of Pericentrin-like protein (Plp) and the pericentriolar material (PCM) to the proximal end of the centriole [ 53 ]. MTs that nucleate from the pericentriolar material interact with the endoplasmic reticulum and might trigger the local modification of the dense complex.…”

Section: Discussionmentioning

confidence: 99%

The Microtubule Cytoskeleton during the Early Drosophila Spermiogenesis

Riparbelli

Persico

Callaini

2020

Cells

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Sperm elongation and nuclear shaping in Drosophila largely depends on the microtubule cytoskeleton that in early spermatids has centrosomal and non-centrosomal origins. We report here an additional γ-tubulin focus localized on the anterior pole of the nucleus in correspondence of the apical end of the perinuclear microtubules that run within the dense complex. The perinuclear microtubules are nucleated by the pericentriolar material, or centriole adjunct, that surrounds the basal body and are retained to play a major role in nuclear shaping. However, we found that both the perinuclear microtubules and the dense complex are present in spermatids lacking centrioles. Therefore, the basal body or the centriole adjunct seem to be dispensable for the organization and assembly of these structures. These observations shed light on a novel localization of γ-tubulin and open a new scenario on the distribution of the microtubules and the organization of the dense complex during early Drosophila spermiogenesis.

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Section: Discussionmentioning

confidence: 99%

The Microtubule Cytoskeleton during the Early Drosophila Spermiogenesis

Riparbelli

Persico

Callaini

2020

Cells

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“…These findings raised the question of whether the lack of t-Grip84 or t-Grip91 resulted in a general disintegration of the centriole adjunct and basal body. We tested the localization of three basal body proteins, the centriole/pericentriolar material protein PACT, the centriole component Ana1 and Asterless in t-Grip84 ms and t-Grip91 ms mutants to assess the impact of the lack of t-γ-TuRC proteins ( Martinez-Campos et al, 2004 ; Fu et al, 2016 ; Galletta et al, 2020 ). GFP-PACT, Ana1 and Asterless were found on the basal body of t-Grip84 ms and t-Grip91 ms mutant spermatids.…”

Section: Resultsmentioning

confidence: 99%

Microtubule Organizing Centers Contain Testis-Specific γ-TuRC Proteins in Spermatids of Drosophila

Alzyoud

Vedelek

Réthi‐Nagy

et al. 2021

Front. Cell Dev. Biol.

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Microtubule nucleation in eukaryotes is primarily promoted by γ-tubulin and the evolutionary conserved protein complex, γ-Tubulin Ring Complex (γ-TuRC). γ-TuRC is part of the centrosome and basal body, which are the best-known microtubule-organizing centers. Centrosomes undergo intensive and dynamic changes during spermatogenesis, as they turn into basal bodies, a prerequisite for axoneme formation during spermatogenesis. Here we describe the existence of a novel, tissue-specific γ-TuRC in Drosophila. We characterize three genes encoding testis-specific components of γ-TuRC (t-γ-TuRC) and find that presence of t-γ-TuRC is essential to male fertility. We show the diverse subcellular distribution of the t-γ-TuRC proteins during post-meiotic development, at first at the centriole adjunct and then also on the anterior tip of the nucleus, and finally, they appear in the tail region, close to the mitochondria. We also prove the physical interactions between the t-γ-TuRC members, γ-tubulin and Mozart1. Our results further indicate heterogeneity in γ-TuRC composition during spermatogenesis and suggest that the different post-meiotic microtubule organizing centers are orchestrated by testis-specific gene products, including t-γ-TuRC.

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“…During spermiogenesis, the distal centriole orients towards the cell membrane to exclusively form the flagellum ( Avidor-Reiss et al, 2020 ). The end of the proximal centriole emanates microtubules to dock to the nuclear membrane, pulling the centrosome to the nucleus, and then a stable connection between the centrosome and nucleus is formed ( Wu et al, 2016 ; Galletta et al, 2020 ). Previous studies demonstrated that LINC complexes are required for the attachment of the centrosome to the nucleus.…”

Section: Resultsmentioning

confidence: 99%

“…The N-terminus of Nesprin3 could interact with plectin, MACF and BPAG1 and thereby contact IFs and microtubules to regulate centrosome ( Wiche, 1998 ; Ketema et al, 2007 ; Cartwright and Karakesisoglou, 2014 ). The centrosome, constituting the microtubule organizing center (MOCT) of cells ( Azimzadeh, 2020 ), is the center of attachment between the sperm head and tail during the formation of flagella ( Galletta et al, 2020 ). During spermiogenesis, the proximal centriole, associated with the nucleus, inserts into the implantation fossa, which is opposite to the acrosome, and the segmented columns and the capitulum together form a connecting piece in the region, while the distal centriole sets the template for the flagellum ( Fawcett and Phillips, 1969 ; Fawcett, 1975 ).…”

Section: Discussionmentioning

confidence: 99%

“…The head-tail coupling apparatus (HTCA) (also called the connecting piece or neck), which is a centrosome-based structure, mediates the tight junction of the sperm head and flagellum. HTCA develops from the centrosome and is composed of proximal centrioles, distal centrioles and pericentriolar materials, including segmented columns and capitulum ( Galletta et al, 2020 ; Wu et al, 2020 ). The HTCA attaching to the nuclear membrane is a prerequisite for the tight connection between the sperm head and tail, causing decapitation of sperm and infertility when faulty ( Galletta et al, 2020 ; Wu et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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SUN5 Interacting With Nesprin3 Plays an Essential Role in Sperm Head-to-Tail Linkage: Research on Sun5 Gene Knockout Mice

Zhang

Yang

Huang

et al. 2021

Front. Cell Dev. Biol.

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Acephalic spermatozoa syndrome is a rare genetic and reproductive disease. Recent studies have shown that approximately 33–47% of patients with acephalic spermatozoa syndrome have SUN5 mutations, but the molecular mechanism underlying this phenomenon has not been elucidated. In this study, we generated Sun5 knockout mice and found that the head-to-tail linkage was broken in Sun5–/– mice, which was similar to human acephalic spermatozoa syndrome. Furthermore, ultrastructural imaging revealed that the head-tail coupling apparatus (HTCA) and the centrosome were distant from the nucleus at steps 9–10 during spermatid elongation. With the manchette disappearing at steps 13–14, the head and the tail segregated. To explore the molecular mechanism underlying this process, bioinformatic analysis was performed and showed that Sun5 may interact with Nesprin3. Further coimmunoprecipitation (Co-IP) and immunofluorescence assays confirmed that Sun5 and Nesprin3 were indeed bona fide interaction partners that formed the linker of the nucleoskeleton and cytoskeleton (LINC) complex participating in the connection of the head and tail of spermatozoa. Nesprin3 was located posterior and anterior to the nucleus during spermiogenesis in wild-type mice, whereas it lost its localization at the implantation fossa of the posterior region in Sun5–/– mice. Without correct localization of Nesprin3 at the nuclear membrane, the centrosome, which is the originator of the flagellum, was distant from the nucleus, which led to the separation of the head and tail. In addition, isobaric tag for relative and absolute quantitation results showed that 47 proteins were upregulated, and 56 proteins were downregulated, in the testis in Sun5–/– mice, and the downregulation of spermatogenesis-related proteins (Odf1 and Odf2) may also contribute to the damage to the spermatozoa head-to-tail linkage. Our findings suggested that Sun5 is essential for the localization of Nesprin3 at the posterior nuclear membrane, which plays an essential role in the sperm head-tail connection.

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Sperm Head-Tail Linkage Requires Restriction of Pericentriolar Material to the Proximal Centriole End

Cited by 18 publications

References 89 publications

The Microtubule Cytoskeleton during the Early Drosophila Spermiogenesis

The Microtubule Cytoskeleton during the Early Drosophila Spermiogenesis

Microtubule Organizing Centers Contain Testis-Specific γ-TuRC Proteins in Spermatids of Drosophila

SUN5 Interacting With Nesprin3 Plays an Essential Role in Sperm Head-to-Tail Linkage: Research on Sun5 Gene Knockout Mice

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