Proteomic analysis of the mouse sperm acrosome - towards an understanding of an organelle with diverse functionality

Otčenášková, Tereza; Macíčková, Eliška; Vondráková, Jana; Frolikova, Michaela; Komrsková, Kateřina; Stopková, Romana; Stopka, Pavel

doi:10.1016/j.ejcb.2023.151296

Cited by 5 publications

(7 citation statements)

References 83 publications

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“…Cytoskeletal proteins together with lipocalin sMUP17 were highly abundant in short apical hooks. Although significance of sMUP7 and other detected lipocalins for male reproduction needs to be addressed, these findings are supportive of our recent study (Otčenášková et al, 2023). Enrichment of proteins involved in sperm-oocyte interactions including zona pellucidabinding, protein degradation and gluconeogenesis indicates that sperm with longer hooks are of better fertilisation competency and produce more energy as already postulated by (Varea-Sánchez et al, 2016).…”

Section: Discussionsupporting

confidence: 88%

“…Spermatozoa underwent capacitation and acrosome reaction following the procedure in (Otčenášková et al, 2023). In brief, isolated spermatozoa were collected and transferred to a total of eight Petri dishes with new pre-tempered M2 medium droplets (100 µL, three droplets per dish) at a concentration of 5 ×10 6 sperm per one mL.…”

Section: Sperm Capacitation and Acrosome Reactionmentioning

confidence: 99%

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The longer the better: longer acrosomes contain more proteins involved in sperm-egg interactions

Otčenášková¹,

Stopková²,

Stopka³

2023

Preprint

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Speciation and sperm competition have been shown to be the major driving forces for sperm morphology variation, swimming velocity and metabolism. We used light microscopy to measure sperm traits and nLC-MS/MS to detect proteomic variation in three species of rodents: promiscuous Apodemus flavicollis, less promiscuous Microtus arvalis, and the least promiscuous Mus musculus musculus. We show that the length of sperm apical hook containing the acrosome is the most variable trait and that this variation is reflected by proteomes on interspecific and intraspecific levels. Thus, we provide potential markers of selection such as Ldhc (in Mus and Apodemus) for long acrosomes which is a gene coding L-lactate dehydrogenase that is involved in sperm motility and Spaca1, which is important in sperm-oocyte fusion), and e.g. Mup17 for short acrosomes, a gene coding a Major urinary protein that likely chelates lipophilic compounds after spermiogenesis. In short, longer acrosomes are characteristic of proteins involved in fertilisation and gluconeogenesis, while shorter acrosomes contain more cytoskeletal proteins important for spermiogenesis. For the first time, we demonstrate that there is an innate and evolvable variability in sperm morphology and corresponding proteomes within species that can be driven by sperm competition to species-specific reproductive optima.

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Section: Discussionsupporting

confidence: 88%

Section: Sperm Capacitation and Acrosome Reactionmentioning

confidence: 99%

The longer the better: longer acrosomes contain more proteins involved in sperm-egg interactions

Otčenášková¹,

Stopková²,

Stopka³

2023

Preprint

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“…Interestingly, mammalian acrosomes also contain mitochondrial and proteasomal proteins (Guyonnet et al 2012, Otčenášková et al 2023), presumably because redundant mitochondria are removed from the cytosol after midpiece formation, and the resulting proteins are ubiquitinated and deposited in acrosomes. Here, we provide new evidence that this could be also true for avian species.…”

Section: Resultsmentioning

confidence: 99%

“…This is because some mammalian species (e.g. muroid rodents) have variable apical hooks containing proteins involved in fertility and acrosome reaction (Breed 2004, Immler et al 2007, Johnson et al 2007, Clift et al 2009, Sandera et al 2013, Hook et al 2021) and, for example, resulting proteomes of mouse spermatozoa and acrosomes contain proteins enriched in energetic metabolism (Vicens et al 2017, Otčenášková et al 2023). In this study, the fertilisation process was not detected by GO analysis.…”

Section: Functional Divergence Of Proteomesmentioning

confidence: 99%

Comparative sperm proteomics in selected passerine birds reflects sperm morphology and mitochondrial metabolism

Otčenášková,

Stopková,

Zemanová

et al. 2023

Journal of Vertebrate Biology

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“…In addition to the acrosome’s similarities to lysosomes and secretory granules, recent studies point to mitochondrial engagement in acrosome formation. Condensed mitochondria were found to act as donors to the AV, and several mitochondrial enzymes were shown to localize to the acrosome ( Ren et al, 2019 ; 2022 ; Otčenášková et al, 2023 ). Altogether, this shows that there is a substantial gap in knowledge regarding the acrosomal origin and the molecular mechanism of its biogenesis.…”

Section: Introductionmentioning

confidence: 99%

Inceptor facilitates acrosomal vesicle formation in spermatids and is required for male fertility

Bilekova,

Garcia-Colomer,

Cebrian-Serrano

et al. 2023

Front. Cell Dev. Biol.

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Spermatogenesis is a crucial biological process that enables the production of functional sperm, allowing for successful reproduction. Proper germ cell differentiation and maturation require tight regulation of hormonal signals, cellular signaling pathways, and cell biological processes. The acrosome is a lysosome-related organelle at the anterior of the sperm head that contains enzymes and receptors essential for egg-sperm recognition and fusion. Even though several factors crucial for acrosome biogenesis have been discovered, the precise molecular mechanism of pro-acrosomal vesicle formation and fusion is not yet known. In this study, we investigated the role of the insulin inhibitory receptor (inceptor) in acrosome formation. Inceptor is a single-pass transmembrane protein with similarities to mannose-6-phosphate receptors (M6PR). Inceptor knockout male mice are infertile due to malformations in the acrosome and defects in the nuclear shape of spermatozoa. We show that inceptor is expressed in early spermatids and mainly localizes to vesicles between the Golgi apparatus and acrosome. Here we show that inceptor is an essential factor in the intracellular transport of trans-Golgi network-derived vesicles which deliver acrosomal cargo in maturing spermatids. The absence of inceptor results in vesicle-fusion defects, acrosomal malformation, and male infertility. These findings support our hypothesis of inceptor as a universal lysosomal or lysosome-related organelle sorting receptor expressed in several secretory tissues.

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Proteomic analysis of the mouse sperm acrosome - towards an understanding of an organelle with diverse functionality

Cited by 5 publications

References 83 publications

The longer the better: longer acrosomes contain more proteins involved in sperm-egg interactions

The longer the better: longer acrosomes contain more proteins involved in sperm-egg interactions

Comparative sperm proteomics in selected passerine birds reflects sperm morphology and mitochondrial metabolism

Inceptor facilitates acrosomal vesicle formation in spermatids and is required for male fertility

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