scholarly journals Energy Metabolism and Hyperactivation of Spermatozoa from Three Mouse Species under Capacitating Conditions

Cells ◽  
2022 ◽  
Vol 11 (2) ◽  
pp. 220
Author(s):  
Ester Sansegundo ◽  
Maximiliano Tourmente ◽  
Eduardo R. S. Roldan
Keyword(s):  
Sperm Competition ◽  
Temporal Dynamics ◽  
Cellular Processes ◽  
Head Displacement ◽  
Mammalian Sperm ◽  
General Terms ◽  
Atp Levels ◽  
Swimming Pattern ◽  
Mouse Species ◽  
Mammalian Fertilization

Mammalian sperm differ widely in sperm morphology, and several explanations have been presented to account for this diversity. Less is known about variation in sperm physiology and cellular processes that can give sperm cells an advantage when competing to fertilize oocytes. Capacitation of spermatozoa, a process essential for mammalian fertilization, correlates with changes in motility that result in a characteristic swimming pattern known as hyperactivation. Previous studies revealed that sperm motility and velocity depend on the amount of ATP available and, therefore, changes in sperm movement occurring during capacitation and hyperactivation may involve changes in sperm bioenergetics. Here, we examine differences in ATP levels of sperm from three mouse species (genus Mus), differing in sperm competition levels, incubated under non-capacitating and capacitating conditions, to analyse relationships between energetics, capacitation, and swimming patterns. We found that, in general terms, the amount of sperm ATP decreased more rapidly under capacitating conditions. This descent was related to the development of a hyperactivated pattern of movement in two species (M. musculus and M. spicilegus) but not in the other (M. spretus), suggesting that, in the latter, temporal dynamics and energetic demands of capacitation and hyperactivation may be decoupled or that the hyperactivation pattern differs. The decrease in ATP levels during capacitation was steeper in species with higher levels of sperm competition than in those with lower levels. Our results suggest that, during capacitation, sperm consume more ATP than under non-capacitating conditions. This higher ATP consumption may be linked to higher velocity and lateral head displacement, which are associated with hyperactivated motility.

scholarly journals Cellular ATP Levels Determine the Stability of a Nucleotide Kinase

2021 ◽  
Vol 8 ◽  
Author(s):  
Oliver Brylski ◽  
Puja Shrestha ◽  
Patricia Gnutt ◽  
David Gnutt ◽  
Jonathan Wolf Mueller ◽  
...  
Keyword(s):  
Protein Stability ◽  
Bound States ◽  
Atp Depletion ◽  
Aps Kinase ◽  
Cellular Processes ◽  
Atp Levels ◽  
Stability Change ◽  
Cell Stability ◽  
The Stability ◽  
Nucleotide Kinase

The energy currency of the cell ATP, is used by kinases to drive key cellular processes. However, the connection of cellular ATP abundance and protein stability is still under investigation. Using Fast Relaxation Imaging paired with alanine scanning and ATP depletion experiments, we study the nucleotide kinase (APSK) domain of 3′-phosphoadenosine-5′-phosphosulfate (PAPS) synthase, a marginally stable protein. Here, we show that the in-cell stability of the APSK is determined by ligand binding and directly connected to cellular ATP levels. The observed protein stability change for different ligand-bound states or under ATP-depleted conditions ranges from ΔGf0 = -10.7 to +13.8 kJ/mol, which is remarkable since it exceeds changes measured previously, for example upon osmotic pressure, cellular stress or differentiation. The results have implications for protein stability during the catalytic cycle of APS kinase and suggest that the cellular ATP level functions as a global regulator of kinase activity.

scholarly journals Discrete Dynamic Model of the Mammalian Sperm Acrosome Reaction: The Influence of Acrosomal pH and Physiological Heterogeneity

2021 ◽  
Vol 12 ◽  
Author(s):  
Andrés Aldana ◽  
Jorge Carneiro ◽  
Gustavo Martínez-Mekler ◽  
Alberto Darszon
Keyword(s):  
Acrosome Reaction ◽  
Human Sperm ◽  
Extracellular Medium ◽  
Mammalian Sperm ◽  
Discrete Dynamic Model ◽  
Acrosomal Exocytosis ◽  
Mammalian Fertilization ◽  
Main Components ◽  
Discrete Mathematical Model ◽  
Physiological Heterogeneity

The acrosome reaction (AR) is an exocytotic process essential for mammalian fertilization. It involves diverse physiological changes (biochemical, biophysical, and morphological) that culminate in the release of the acrosomal content to the extracellular medium as well as a reorganization of the plasma membrane (PM) that allows sperm to interact and fuse with the egg. In spite of many efforts, there are still important pending questions regarding the molecular mechanism regulating the AR. Particularly, the contribution of acrosomal alkalinization to AR triggering physiological conditions is not well understood. Also, the dependence of the proportion of sperm capable of undergoing AR on the physiological heterogeneity within a sperm population has not been studied. Here, we present a discrete mathematical model for the human sperm AR based on the physiological interactions among some of the main components of this complex exocytotic process. We show that this model can qualitatively reproduce diverse experimental results, and that it can be used to analyze how acrosomal pH (pHa) and cell heterogeneity regulate AR. Our results confirm that a pHa increase can on its own trigger AR in a subpopulation of sperm, and furthermore, it indicates that this is a necessary step to trigger acrosomal exocytosis through progesterone, a known natural inducer of AR. Most importantly, we show that the proportion of sperm undergoing AR is directly related to the detailed structure of the population physiological heterogeneity.

scholarly journals The sperm protein SPACA4 is required for efficient fertilization in mice

2021 ◽  
Author(s):  
Sarah Herberg ◽  
Yoshitaka Fujihara ◽  
Andreas Blaha ◽  
Karin Panser ◽  
Kiyonari Kobayashi ◽  
...  
Keyword(s):  
Zona Pellucida ◽  
Knockout Mice ◽  
Mammalian Species ◽  
Wild Type ◽  
Sperm Protein ◽  
Mammalian Sperm ◽  
Fundamental Process ◽  
Mammalian Fertilization

Fertilization is the fundamental process that initiates the development of a new individual in all sexually reproducing species. Despite its importance, our understanding of the molecular players that govern mammalian sperm-egg interaction is incomplete, partly because many of the essential factors found in non-mammalian species do not have obvious mammalian homologs. We have recently identified the Ly6/uPAR protein Bouncer as a new, essential fertilization factor in zebrafish (Herberg et al., 2018). Here, we show that Bouncer's homolog in mammals, SPACA4, is also required for efficient fertilization in mice. In contrast to fish, where Bouncer is expressed specifically in the egg, SPACA4 is expressed exclusively in the testis. Male knockout mice are severely sub-fertile, and sperm lacking SPACA4 fail to fertilize wild-type eggs in vitro. Interestingly, removal of the zona pellucida rescues the fertilization defect of Spaca4-deficient sperm in vitro, indicating that SPACA4 is not required for the interaction of sperm and the oolemma but rather of sperm and zona pellucida. Our work identifies SPACA4 as an important sperm protein necessary for zona pellucida penetration during mammalian fertilization.

scholarly journals ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization.

1996 ◽  
Vol 134 (3) ◽  
pp. 637-645 ◽  
Author(s):  
C Arnoult ◽  
Y Zeng ◽  
H M Florman
Keyword(s):  
Membrane Potential ◽  
Pertussis Toxin ◽  
Zona Pellucida ◽  
Mammalian Sperm ◽  
Transient Rise ◽  
Transduction Mechanisms ◽  
Dependent Signal ◽  
Sperm Membrane ◽  
Mammalian Fertilization

The sperm acrosome reaction is a Ca(2+)-dependent secretory event required for fertilization. Adhesion to the egg's zona pellucida promotes Ca2+ influx through voltage-sensitive channels, thereby initiating secretion. We used potentiometric fluorescent probes to determine the role of sperm membrane potential in regulating Ca2+ entry. ZP3, the glycoprotein agonist of the zona pellucida, depolarizes sperm membranes by activating a pertussis toxin-insensitive mechanism with the characteristics of a poorly selective cation channel. ZP3 also activates a pertussis toxin-sensitive pathway that produces a transient rise in internal pH. The concerted effects of depolarization and alkalinization open voltage-sensitive Ca2+ channels. These observations suggest that mammalian sperm utilize membrane potential-dependent signal transduction mechanisms and that a depolarization pathway is an upstream transducing element coupling adhesion to secretion during fertilization.

scholarly journals Signaling diversity enabled by Rap1-regulated plasma membrane ERK with distinct temporal dynamics

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Jeremiah Keyes ◽  
Ambhighainath Ganesan ◽  
Olivia Molinar-Inglis ◽  
Archer Hamidzadeh ◽  
Jinfan Zhang ◽  
...  
Keyword(s):  
Plasma Membrane ◽  
Temporal Dynamics ◽  
Resonance Energy Transfer ◽  
Resonance Energy ◽  
Signaling Specificity ◽  
Temporal Regulation ◽  
Cellular Processes ◽  
Extracellular Signal ◽  
Transient Activity ◽  
Erk Activity

A variety of different signals induce specific responses through a common, extracellular-signal regulated kinase (ERK)-dependent cascade. It has been suggested that signaling specificity can be achieved through precise temporal regulation of ERK activity. Given the wide distrubtion of ERK susbtrates across different subcellular compartments, it is important to understand how ERK activity is temporally regulated at specific subcellular locations. To address this question, we have expanded the toolbox of Förster Resonance Energy Transfer (FRET)-based ERK biosensors by creating a series of improved biosensors targeted to various subcellular regions via sequence specific motifs to measure spatiotemporal changes in ERK activity. Using these sensors, we showed that EGF induces sustained ERK activity near the plasma membrane in sharp contrast to the transient activity observed in the cytoplasm and nucleus. Furthermore, EGF-induced plasma membrane ERK activity involves Rap1, a noncanonical activator, and controls cell morphology and EGF-induced membrane protrusion dynamics. Our work strongly supports that spatial and temporal regulation of ERK activity is integrated to control signaling specificity from a single extracellular signal to multiple cellular processes.

scholarly journals Variación espacial y temporal de larvas de peces en una bahía hipersalina del Caribe colombiano

2018 ◽  
Vol 47 (1) ◽  
Author(s):  
Juan José Gallego Zerrato ◽  
Alan Giraldo
Keyword(s):  
Temporal Dynamics ◽  
Fish Larvae ◽  
Spatial Scales ◽  
Dry Season ◽  
Biological Information ◽  
Spatial And Temporal Variation ◽  
Local Conditions ◽  
General Terms ◽  
Sampling Campaign ◽  
Rain Season

Spatial distribution patterns and the diversity of organisms are the result of evolution, biogeography and the interaction between the local abiotic and biotic factors that operate at different temporal and spatial scales. This paper describes the spatial and temporal dynamics of the assembly of larval stages of fish in Bahía Portete and evaluates the relationship between spatial and temporal variation in abundance and local oceanographic conditions. Oceanographic and biological information was obtained from two sampling campaigns in July (dry season) and November (rainy season) 2015 to incorporate these contrasting climatic conditions. During each sampling campaign a mesh of 21 stations was performed, distributed in a systematic way in the Bay. 2763 larvae of fish, belonging to 37 families and 66 species were captured. The structure and composition of the assembly of larvae was significantly different between the periods of study, as well as the richness and diversity of species, being higher in November (rain season) in comparison with July(dry season). In general terms, the abundance and richness of fish larvae in Bahía Portete seem to be related to the availability of food (zooplankton biomass) and local conditions of temperature and salinity, being it’s variation probably influenced by the local circulation pattern.

scholarly journals Sexual selection on protamine and transition nuclear protein expression in mouse species

2014 ◽  
Vol 281 (1783) ◽  
pp. 20133359 ◽  
Author(s):  
Lena Lüke ◽  
Polly Campbell ◽  
María Varea Sánchez ◽  
Michael W. Nachman ◽  
Eduardo R. S. Roldan
Keyword(s):  
Sexual Selection ◽  
Sperm Competition ◽  
Nuclear Protein ◽  
Sperm Head ◽  
Nuclear Proteins ◽  
Sperm Chromatin ◽  
Head Shape ◽  
Mouse Species ◽  
The Relationship ◽  
Protamine 2

Post-copulatory sexual selection in the form of sperm competition is known to influence the evolution of male reproductive proteins in mammals. The relationship between sperm competition and regulatory evolution, however, remains to be explored. Protamines and transition nuclear proteins are involved in the condensation of sperm chromatin and are expected to affect the shape of the sperm head. A hydrodynamically efficient head allows for fast swimming velocity and, therefore, more competitive sperm. Previous comparative studies in rodents have documented a significant association between the level of sperm competition (as measured by relative testes mass) and DNA sequence evolution in both the coding and promoter sequences of protamine 2. Here, we investigate the influence of sexual selection on protamine and transition nuclear protein mRNA expression in the testes of eight mouse species that differ widely in levels of sperm competition. We also examined the relationship between relative gene expression levels and sperm head shape, assessed using geometric morphometrics. We found that species with higher levels of sperm competition express less protamine 2 in relation to protamine 1 and transition nuclear proteins. Moreover, there was a significant association between relative protamine 2 expression and sperm head shape. Reduction in the relative abundance of protamine 2 may increase the competitive ability of sperm in mice, possibly by affecting sperm head shape. Changes in gene regulatory sequences thus seem to be the basis of the evolutionary response to sexual selection in these proteins.

scholarly journals Phosphatidylserine on viable sperm and phagocytic machinery in oocytes regulate mammalian fertilization

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Claudia M. Rival ◽  
Wenhao Xu ◽  
Laura S. Shankman ◽  
Sho Morioka ◽  
Sanja Arandjelovic ◽  
...  
Keyword(s):  
Motile Sperm ◽  
Head Region ◽  
Skeletal Myoblasts ◽  
Mammalian Sperm ◽  
Species Survival ◽  
Key Players ◽  
Sperm Entry ◽  
Viable Sperm ◽  
Mammalian Fertilization ◽  
Initial Interaction

Abstract Fertilization is essential for species survival. Although Izumo1 and Juno are critical for initial interaction between gametes, additional molecules necessary for sperm:egg fusion on both the sperm and the oocyte remain to be defined. Here, we show that phosphatidylserine (PtdSer) is exposed on the head region of viable and motile sperm, with PtdSer exposure progressively increasing during sperm transit through the epididymis. Functionally, masking phosphatidylserine on sperm via three different approaches inhibits fertilization. On the oocyte, phosphatidylserine recognition receptors BAI1, CD36, Tim-4, and Mer-TK contribute to fertilization. Further, oocytes lacking the cytoplasmic ELMO1, or functional disruption of RAC1 (both of which signal downstream of BAI1/BAI3), also affect sperm entry into oocytes. Intriguingly, mammalian sperm could fuse with skeletal myoblasts, requiring PtdSer on sperm and BAI1/3, ELMO2, RAC1 in myoblasts. Collectively, these data identify phosphatidylserine on viable sperm and PtdSer recognition receptors on oocytes as key players in sperm:egg fusion.

scholarly journals Of mice and women: advances in mammalian sperm competition with a focus on the female perspective

2020 ◽  
Vol 375 (1813) ◽  
pp. 20200082
Author(s):  
Renée C. Firman
Keyword(s):  
Sperm Competition ◽  
Reproductive Tract ◽  
Female Reproductive Tract ◽  
Selective Force ◽  
Mammal Species ◽  
Female Reproductive Success ◽  
Positive Effects ◽  
Mammalian Sperm ◽  
Made In ◽  
Female Perspective

Although initially lagging behind discoveries being made in other taxa, mammalian sperm competition is now a productive and advancing field of research. Sperm competition in mammals is not merely a ‘sprint-race’ between the gametes of rival males, but rather a race over hurdles; those hurdles being the anatomical and physiological barriers provided by the female reproductive tract, as well as the egg and its vestments. With this in mind, in this review, I discuss progress in the field while focusing on the female perspective. I highlight ways by which sperm competition can have positive effects on female reproductive success and discuss how competitive outcomes are not only owing to dynamics between the ejaculates of rival males, but also attributable to mechanisms by which female mammals bias paternity toward favourable sires. Drawing on examples across different species—from mice to humans—I provide an overview of the accumulated evidence which firmly establishes that sperm competition is a key selective force in the evolution of male traits and detail how females can respond to increased sperm competitiveness with increased egg resistance to fertilization. I also discuss evidence for facultative responses to the sperm competition environment observed within mammal species. Overall, this review identifies shortcomings in our understanding of the specific mechanisms by which female mammals ‘select’ sperm. More generally, this review demonstrates how, moving forward, mammals will continue to be effective animal models for studying both evolutionary and facultative responses to sperm competition. This article is part of the theme issue ‘Fifty years of sperm competition’.

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