scholarly journals Sub-cellular patterns of SPE-6 localization reveal unexpected complexities in C. elegans sperm activation and sperm function

Author(s):  
Jackson J Peterson ◽  
Claire E Tocheny ◽  
Gaurav Prajapati ◽  
Craig W LaMunyon ◽  
Diane C Shakes

Abstract To acquire and maintain directed cell motility, Caenorhabditis elegans sperm must undergo extensive, regulated cellular remodeling, in the absence of new transcription or translation. To regulate sperm function, nematode sperm employ large numbers of protein kinases and phosphatases, including SPE-6, a member of C. elegans’ highly expanded casein kinase 1 superfamily. SPE-6 functions during multiple steps of spermatogenesis, including functioning as a “brake” to prevent premature sperm activation in the absence of normal extracellular signals. Here we describe the sub-cellular localization patterns of SPE-6 during wildtype C. elegans sperm development and in various sperm activation mutants. While other members of the sperm activation pathway associate with the plasma membrane or localize to the sperm’s membranous organelles, SPE-6 surrounds the chromatin mass of unactivated sperm. During sperm activation by either of two semiautonomous signaling pathways, SPE-6 redistributes to the front, central region of the sperm’s pseudopod. When disrupted by reduction-of-function alleles, SPE-6 protein is either diminished in a temperature-sensitive manner (hc187) or is mis-localized in a stage-specific manner (hc163). During the multistep process of sperm activation, SPE-6 is released from its perinuclear location after the spike stage in a process that does not require fusion of membranous organelles with the plasma membrane. After activation, spermatozoa exhibit variable proportions of perinuclear and pseudopod-localized SPE-6, depending on their location within the female reproductive tract. These findings provide new insights regarding SPE-6’s role in sperm activation and suggest that extracellular signals during sperm migration may further modulate SPE-6 localization and function.

1984 ◽  
Vol 31 (5) ◽  
pp. 888-894 ◽  
Author(s):  
John E. Gould ◽  
James W. Overstreet ◽  
Fredrick W. Hanson

Reproduction ◽  
2019 ◽  
Vol 157 (6) ◽  
pp. R243-R256 ◽  
Author(s):  
T Leahy ◽  
J P Rickard ◽  
N C Bernecic ◽  
X Druart ◽  
S P de Graaf

Ejaculation results in the confluence of epididymal spermatozoa with secretions of the accessory sex glands. This interaction is not a prerequisite for fertilisation success, but seminal factors do play a crucial role in prolonging the survival of spermatozoa bothin vitroandin vivoby affording protection from handling induced stress and some selective mechanisms of the female reproductive tract. Reproductive biologists have long sought to identify specific factors in seminal plasma that influence sperm function and fertility in these contexts. Many seminal plasma proteins have been identified as diagnostic predictors of sperm function and have been isolated and appliedin vitroto prevent sperm damage associated with the application of artificial reproductive technologies. Proteomic assessment of the spermatozoon, and its surroundings, has provided considerable advances towards these goals and allowed for greater understanding of their physiological function. In this review, the importance of seminal plasma will be examined through a proteomic lens to provide comprehensive analysis of the ram seminal proteome and detail the use of proteomic studies that correlate seminal plasma proteins with ram sperm function and preservation ability.


2020 ◽  
Vol 76 (09) ◽  
pp. 6445-2020
Author(s):  
ALEKSANDRA KRAWCZYK ◽  
JADWIGA JAWORSKA-ADAMU

The formation of a new diploidal organism is preceded by a series of mutual interactions of haploidal gametes. This process is very complicated and requires the prior activation of reproductive cells. Male gametes eventually mature in the female reproductive tract, acquiring mobility and fertilization. This process takes place in two stages. Sperms are first capacitated. This phenomenon is reversible and leads to structural, cytophysiological and biochemical changes in the sperm plasma membrane as well as to the sperm hyperactivation. Then, due to the contact with the zona pellucida of the oocyte, the irreversible acrosome reaction occurs. This process involves the fusion of the sperm plasma membrane with the outer membrane of the acrosome, the release of enzymes and exposure of the inner acrosome membrane. This enables sperm to penetrate towards the perivitelline space and oolemma. Contact with the oocyte initiates a series of interactions leading to egg activation and the fusion of gametes. Each of these stages involves many different factors that result in the recognition, attraction and adhesion of reproductive cells. Knowledge about the activation mechanisms can improve the effectiveness of supported and controlled reproduction techniques.


Zygote ◽  
2019 ◽  
Vol 27 (1) ◽  
pp. 5-16 ◽  
Author(s):  
Gabriela Hernández-Silva ◽  
Mayel Chirinos

SummarySpermatogenesis is a dynamic process that culminates in the production of mature spermatozoa in the seminiferous tubules of sexually mature animals. Although sperm leaving the testis are fully differentiated, they must further undergo two additional maturation steps before acquiring the capability to fertilize the egg. Such processes take place during the epididymal residency and transport in the seminal fluid during ejaculation and, after delivery into the female reproductive tract, during the journey aiming the encountering the egg in the oviduct. Throughout this trip, spermatozoa are exposed to different reproductive fluids whose molecular compositions regulate the progress towards obtaining a fertilized competent cell. This review summarizes the evidence obtained so far supporting the participation of male and female reproductive tract-derived proteins in the modulation of sperm fertilizing ability and discusses the mechanisms by which such regulation may be accomplished.


Author(s):  
Miguel Ricardo Leung ◽  
Ravi Teja Ravi ◽  
Bart M. Gadella ◽  
Tzviya Zeev-Ben-Mordehai

To become fertilization-competent, mammalian sperm must undergo a complex series of biochemical and morphological changes in the female reproductive tract. These changes, collectively called capacitation, culminate in the exocytosis of the acrosome, a large vesicle overlying the nucleus. Acrosomal exocytosis is not an all-or-nothing event but rather a regulated process in which vesicle cargo disperses gradually. However, the structural mechanisms underlying this controlled release remain undefined. In addition, unlike other exocytotic events, fusing membranes are shed as vesicles; the cell thus loses the entire anterior two-thirds of its plasma membrane and yet remains intact, while the remaining nonvesiculated plasma membrane becomes fusogenic. Precisely how cell integrity is maintained throughout this drastic vesiculation process is unclear, as is how it ultimately leads to the acquisition of fusion competence. Here, we use cryoelectron tomography to visualize these processes in unfixed, unstained, fully hydrated sperm. We show that paracrystalline structures within the acrosome disassemble during capacitation and acrosomal exocytosis, representing a plausible mechanism for gradual dispersal of the acrosomal matrix. We find that the architecture of the sperm head supports an atypical membrane fission–fusion pathway that maintains cell integrity. Finally, we detail how the acrosome reaction transforms both the micron-scale topography and the nanoscale protein landscape of the sperm surface, thus priming the sperm for fertilization.


2021 ◽  
Vol 22 (21) ◽  
pp. 11809
Author(s):  
Veronika Merc ◽  
Michaela Frolikova ◽  
Katerina Komrskova

In mammals, integrins are heterodimeric transmembrane glycoproteins that represent a large group of cell adhesion receptors involved in cell–cell, cell–extracellular matrix, and cell–pathogen interactions. Integrin receptors are an important part of signalization pathways and have an ability to transmit signals into and out of cells and participate in cell activation. In addition to somatic cells, integrins have also been detected on germ cells and are known to play a crucial role in complex gamete-specific physiological events, resulting in sperm-oocyte fusion. The main aim of this review is to summarize the current knowledge on integrins in reproduction and deliver novel perspectives and graphical interpretations presenting integrin subunits localization and their dynamic relocation during sperm maturation in comparison to the oocyte. A significant part of this review is devoted to discussing the existing view of the role of integrins during sperm migration through the female reproductive tract; oviductal reservoir formation; sperm maturation processes ensuing capacitation and the acrosome reaction, and their direct and indirect involvement in gamete membrane adhesion and fusion leading to fertilization.


2015 ◽  
Vol 27 (1) ◽  
pp. 118
Author(s):  
M. Ahmad ◽  
N. Ahmad ◽  
M. Anzar

The extent of changes in sperm structure and function affect the success of fertilization ultimately during the pathway to ovum in the female reproductive tract. The success of AI with frozen-thawed semen varies in dairy and beef breeds of bovine because of differed alterations in sperm during transport in female tract after insemination. To our knowledge, no report is available comparing the changes in dairy and beef sperm leading to death in female tract. Therefore, this study was aimed to investigate the changes in motility, generation of reactive oxygen species (superoxide and hydrogen peroxide), and their relation to sperm death [asymmetry (apoptosis) and rupture of plasma membrane] of dairy and beef frozen-thawed semen during incubation at 37°C for 24 h. This incubation was aimed to mimic the environment of female reproductive tract. Frozen dairy semen (n = 4 bulls) was procured from a Canadian breeding station, whereas beef semen was collected from breeding beef bulls (n = 3; 5 replicates), diluted with Tris-based extender (composition was same as used in dairy semen), cooled to +4°C over 90 min, and cryopreserved by programmable freezer using standard rate as used in dairy semen. Two straws per replicate were thawed at 37°C from both types of semen, pooled separately, and incubated at 37°C for 24 h in capped tubes. Each pooled semen sample was evaluated for motility with CASA, superoxide (O2–, and hydrogen peroxide (H2O2) radical using HE/YoPRO and H2DCFDA/PI assay, respectively, and asymmetry of plasma membrane using YoPRO/PI assay through flow cytometric analysis at 0, 2, 4, 6, 12, and 24 h of incubation. The MIXED procedure of SAS (SAS Institute Inc., Cary, NC, USA) was used to analyse the data as 2 × 6 factorial model for 2 types of semen (dairy and beef) and 6 time points using time as repeated measure. A threshold limit of 30% was considered for motility and live sperm to get optimum fertility. Sperm motility remained higher (P < 0.05) than threshold limit till 6 h in dairy (50.95 ± 2.62%) and 2 h in beef semen (30.28 ± 6.95%). Dairy semen possessed more (P < 0.05) nonapoptotic sperm without O2– (HE–/YoPRO–) till 6 h of incubation than beef semen. The increase in apoptotic sperm containing superoxide radical (HE+/YoPRO+) over time was more (P < 0.05) in beef semen till 6 h of incubation. The rise in dead sperm containing H2O2 (H2DCFDA+/PI+) was recorded more in beef than in dairy semen until 6 h of incubation. Live sperm without apoptosis (YoPRO–/PI–) were higher until 24 h in dairy (49.36 ± 4.56%) compared with beef semen (24.89 ± 3.85%), whereas viable sperm with apoptosis (YoPRO+/PI–) were found similar in both types of semen over time. In conclusion, dairy frozen-thawed semen possessed more live sperm without reactive oxygen species (superoxide and hydrogen peroxide) until 6 h of incubation than did beef semen. The decrease in superoxide radical was more in dairy than in beef semen. Dead and apoptotic sperm increased more in beef frozen-thawed semen over time during incubation. This inference suggests performing the insemination late near ovulation with beef frozen-thawed semen because of less viable life than dairy semen.


BMC Zoology ◽  
2020 ◽  
Vol 5 (1) ◽  
Author(s):  
Yu-Chia Chang ◽  
Jane-Fang Yu ◽  
Tse-En Wang ◽  
Shih-Chien Chin ◽  
Yu-Syuan Wei ◽  
...  

Abstract Background Formosan Pangolin (Manis pentadactyla pentadactyla) is one of the three subspecies of Chinese pangolins, it is also an isolated sub-species naturally habitat in Taiwan. Despite earlier report on successful breeding of Sunda (Manis javanica) pangolin, breeding of Formosan pangolins in zoo captive populations is still challenging due to unknown reproductive characterizations of this species in both male and female populations. Results We characterized for the first time, reproductive tract of male Formosan pangolin. We showed pangolin epididymis was a collagen-enriched organ with apparent segmented sub-regions similar to other mammals. However, unlike most mammals exhibited two V-ATPase subunits, Formosan pangolin exhibited only V-ATPase subunit 2. This specific V-ATPase subunit extended its cellular localization throughout the cytoplasm of epididymal clear cells, suggesting pH regulation of luminal microenvironment might be different from other mammals. Electron micrographs showed rod-shaped pangolin sperm cells with multi-lamellar membrane structure at the sperm head. Similar to well-defined capacitation and acrosome reaction membrane changes in other mammals, we reported three distinct patterns (homogenous, punctuated and faded) of pangolin sperm head membrane changes. The concurrent increase in phosphotyrosine protein expression detected at the sperm mid-piece/tail and the emergence of punctuated membrane aggregates likely representing three sperm activation stages, namely inactivated, capacitated and acrosome reacted status of pangolin sperm. Conclusion By revealing unique epididymal V-ATPase distribution and sperm membrane dynamics in Formosan pangolin, we would understand better the fundamental aspects of reproduction parameters of Formosan pangolin.


Reproduction ◽  
2018 ◽  
Vol 156 (2) ◽  
pp. 163-172 ◽  
Author(s):  
Lucía Saucedo ◽  
Cristian Sobarzo ◽  
Nicolás G Brukman ◽  
Héctor A Guidobaldi ◽  
Livia Lustig ◽  
...  

Fibroblast growth factor 2 (FGF2) and its receptors (FGFRs) have been described in several tissues, where they regulate cellular proliferation, differentiation, motility and apoptosis. Although FGF2/FGFRs expression in the male reproductive tract has been reported, there is scarce evidence on their presence in the female reproductive tract and their involvement in the modulation of sperm function. Therefore, the objective of this study was to determine the expression of FGF2 in the female reproductive tract and to assess the role of the FGF2/FGFRs system in the regulation of sperm physiology using the murine model. FGF2 was detected in uterus and oviduct protein extracts, and it was immunolocalized in epithelial cells of the uterus,isthmusandampulla, as well as in thecumulus oophorus-oocyte complex. The receptors FGFR1, FGFR2, FGFR3 and FGFR4 were immunodetected in the flagellum and acrosomal region of sperm recovered from thecaudaepididymis. Analysis of testis sections showed the expression of FGFRs in germ cells at different stages of the spermatogenesis, suggesting the testicular origin of the sperm FGFRs. Sperm incubation with recombinant FGF2 (rFGF2) led to increased sperm motility and velocity and to enhanced intracellular Ca2+levels and acrosomal loss compared to the control. In conclusion, this study shows that FGF2 is expressed in tissues of the female reproductive tract. Also, the fact that functional FGFRs are present in mouse sperm and that rFGF2 affects sperm motility and acrosomal exocytosis, suggests the involvement of this system in thein vivoregulation of sperm function.


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