Motility of fish spermatozoa: from external signaling to flagella response

doi:10.1016/j.repbio.2013.12.005

Reproductive Biology

Volume 14, Issue 3, September 2014, Pages 165-175

https://doi.org/10.1016/j.repbio.2013.12.005 Get rights and content

Abstract

For successful fertilization, spermatozoa must access, bind, and penetrate an egg, processes for which activation of spermatozoa motility is a prerequisite. Fish spermatozoa are stored in seminal plasma where they are immotile during transit through the genital tract of most externally fertilizing teleosts and chondrosteans. Under natural conditions, motility is induced immediately following release of spermatozoa from the male genital tract into the aqueous environment. The nature of an external trigger for the initiation of motility is highly dependent on the aquatic environment (fresh or salt water) and the species’ reproductive behavior. Triggering signals include osmotic pressure, ionic and gaseous components of external media and, in some cases, egg-derived substances. Extensive study of environmental factors influencing fish spermatozoa motility has led to the proposal of several mechanisms of activation in freshwater and marine fish. However, the signal transduction pathways initiated by these mechanisms remain clear. This review presents the current knowledge with respect to (1) membrane reception of the activation signal and its transduction through the spermatozoa plasma membrane via the external membrane components, ion channels, and aquaporins; (2) cytoplasmic trafficking of the activation signal; (3) final steps of the signaling, including signal transduction to the axonemal machinery, and activation of axonemal dyneins and regulation of their activity; and (4) pathways supplying energy for flagellar motility.

Introduction

Sperm quality is a measure of the ability of spermatozoa to successfully fertilize an egg [1]. Spermatozoa motility must be activated to allow them to reach, bind, and penetrate the egg. As a general rule, in fish with external fertilization, spermatozoa are immotile in testis and in seminal fluid [2], and initiation of motility is dependent on the fertilization environment [3], [4], [5], [6], [7]. Several factors are known to regulate spermatozoa motility. In salmonid fishes, motility is initiated by a decrease in potassium ion (K⁺) concentration surrounding the spawned spermatozoa when they are released into fresh water [4]. The main factor in initiation of spermatozoa motility in cyprinid fishes is a decrease in osmolality upon spawning into fresh water [5]. Conversely, hypertonicity of the surrounding medium triggers the motility of spermatozoa of marine teleosts [7]. The motility of spermatozoa in the euryhaline fish, medaka, Oryzias latipes, is not so strictly dependent on environmental osmolality, and may be initiated by values ranging from 25 to 686 mOsm/kg [6]. The fore-mentioned examples suggest the existence of a variety of specific signaling pathways for spermatozoa activation. The species-specific differences in sperm sensitivity to environmental osmotic pressure and ion composition, membrane polarization/depolarization processes, involvement of signaling molecules (e.g., cAMP), and phosphorylation of flagella proteins [2], [3], [8], [9] are of special interest. The primary goal of this review is to summarize current knowledge on signaling pathways involved in the process of spermatozoa activation from the reception of the external signal at the level of the plasma membrane to the activation of axonemal dyneins.

Section snippets

Duration of spermatozoa motility

Motility activation of fish spermatozoa is a process lasting fractions of a second, making studies of the biochemical processes underlying the activity of axonemal structures technically difficult [2], [8], [10]. Estimations of time required for flagellar activity initiation have been described in few fish species. In turbot, Psetta maxima, activation of the flagellum after ceasing CO₂ application occurred within 100 ms [11]. In pipefish, Syngnathus abaster, whose females deposit eggs into a

Membrane reception of the activation signals and their transduction through the membrane

Under natural conditions, external signals triggering spermatozoa motility act at the level of the plasma membrane, inducing changes, among others, in hyperpolarization/depolarization of membranes, ion channels, and aquaporin activity.

From membrane to axoneme: the cytoplasmic trafficking of signals

Internal space of a spermatozoon is limited, but a thin layer of cytoplasm links areas of the cell and contains mediators allowing the cell to decode the signals received and to deliver them to the appropriate sites. For example, an increase in intracellular ion concentration may lead to the activation of adenylyl cyclase (AC), which, in turn, regulates the initiation of motility by a cAMP-dependent mechanism [48]. In mammals, tyrosine phosphorylation of several proteins is up-regulated by

cAMP signaling in spermatozoa motility regulation and its spatial organization

Regulation of spermatozoa motility is linked to the AC/cAMP signaling pathway in mammals, fishes, and sea urchins [60], [61], [62]. The contribution of cAMP-dependent protein kinase A (PKA) as a regulator of motility is well known in some animals [63], [64]. In mammals, two types of adenylyl cyclases have been characterized: a transmembrane AC (tmAC) and a soluble AC [65]. Soluble AC is responsible for cAMP synthesis, whereas the role of tmACs in sperm is not well understood. Cyclic AMP is also

Bioenergetics of flagellar motility

A prerequisite of spermatozoa motility is that the hydrolysis of ATP be catalyzed by dynein ATPase, which liberates chemical energy and is coupled to the mechanical sliding of adjacent microtubules. Energy-supplying pathways for spermatozoa may differ according to fish species and may include glycolysis, phospholipid catabolism and triglyceride metabolism, the Krebs cycle, and oxidative phosphorylation [86], [87], [88]. The latter provides energy insufficient to compensate for ATP utilization

Conclusions

In fish spermatozoa, motility initiation is well described biochemically but not phenomenologically. It is a brief event, with the described events lasting milliseconds, difficult to capture by microscopic imagery, and may represent a challenge to the observer. Spermatozoa activation is a complex and highly organized process. In general, the reception of external activating stimuli is followed by signaling conducted by second messengers (cAMP, cGMP, Ca²⁺, ROS, NO) (Fig. 1), and, finally,

Conflict of interest

We declare no actual or potential conflict of interest regarding the submitting manuscript. Viktoriya Dzyuba and Jacky Cosson.

Acknowledgements

The authors acknowledge financial support from projects: GACR P502/11/0090 and P502/12/1973, CENAKVA CZ.1.05/2.1.00/01.0024. Special thanks to Borys Dzyuba for his valuable comments and discussion. The Lucidus Consultancy, UK, is gratefully acknowledged for the English correction and suggestions.

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Copyright © 2014 Society for Biology of Reproduction & the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn. Published by Elsevier Urban & Partner Sp. z o.o. All rights reserved.

Review ArticleMotility of fish spermatozoa: from external signaling to flagella response

Abstract

Introduction

Section snippets

Duration of spermatozoa motility

Membrane reception of the activation signals and their transduction through the membrane

From membrane to axoneme: the cytoplasmic trafficking of signals

cAMP signaling in spermatozoa motility regulation and its spatial organization

Bioenergetics of flagellar motility

Conclusions

Conflict of interest

Acknowledgements

Aquaculture

Cell Biol Int

Theriogenology

Comp Biochem Physiol C

Aquaculture

Anim Reprod Sci

Theriogenology

Comp Biochem Physiol A

Steroids

Gen Comp Endocrinol

Gen Comp Endocrinol

Theriogenology

J Biol Chem

Aquat Living Resour

Anim Reprod Sci

J Biol Chem

Biochem Biophys Res Commun

J Biol Chem

Biochem Biophys Res Commun

Biochem Biophys Res Commun

J Theor Biol

Biophys J

J Biol Chem

Comp Biochem Physiol B

Biophys J

Adv Dev Biol

Theriogenology

Frenetic activation of fish spermatozoa flagella entails short-term motility, portending their precocious decadence

J Fish Biol

Effects of potassium and osmolality on spermatozoan motility in salmonid fishes

J Exp Biol

Effects of osmolality and potassium on motility of spermatozoa from freshwater cyprinid fishes

J Exp Biol

Marine fish spermatozoa: racing ephemeral swimmers

Reproduction

The ionic and osmotic factors controlling motility of fish spermatozoa

Aquacult Int

Adaptation and strategy for fertilization in the sperm of teleost fish

J Appl Ichthyol

Control of flatfish sperm motility by CO2 and carbonic anhydrase

Cell Motil Cytoskeleton

Variable sperm size and motility activation in the pipefish, Syngnathus abaster; adaptations to paternal care or environmental plasticity?

Reprod Fertil Dev

Spermatozoa motility of trout (Oncorhynchus mykiss) and carp (Cyprinus carpio)

J Appl Ichthyol

Fertilization in fishes and the problem of polyspermy

Unusual motility characteristics of sperm of the spotted wolffish

J Fish Biol

Long lasting sticklebacks sperm; is ovarian fluid a key to success in freshwater?

J Fish Biol

Sperm storage and motility in the ovary of the marine sculpin Alcichthys alcicornis (Teleostei:Scorpaeniformes), with internal gametic association

J Exp Zool

Sperm attractant in the micropyle region of fish and insect eggs

Biol Reprod

Effects of extracellular environment on the osmotic signal transduction involved in activation of motility of carp spermatozoa

J Reprod Fertil

Characterization and partial purification of sperm-activating substances from eggs of herring, Clupea palasii

J Exp Zool

Factors controlling sperm entry into the micropyle of salmonid and herring eggs

Dev Growth Differ

A high molecular weight glycoprotein in seminal plasma is a sperm immobilizing factor in the teleost Nile tilapia, Oreochromis niloticus

Dev Growth Differ

Effects of osmolality on sperm morphology, motility and flagellar wave parameters in Northern pike (Esox lucius L.)

Theriogenology

Semen characteristics in Acipenser persicus in relation to sequential stripping

J Appl Ichthyol

Sperm features in turbot (Scophthalmus maximus): a comparison with other fresh water and marine fish species

Aquat Living Resour

Review Article
Motility of fish spermatozoa: from external signaling to flagella response

Control of flatfish sperm motility by CO₂ and carbonic anhydrase