Abstract
In many marine fish species, the spermatozoa are immotile in the testis and seminal plasma, and motility is induced when they are released in the aqueous environment. It is well known that the extracellular factors (hyperosmolality or sperm-activating peptides), controlling sperm motility in marine fish, act on the axonemal apparatus through signal transduction across the plasma membrane. To better understand the molecular mechanism regulating axoneme activation in marine fish, the present review examines the existing literature, with particular emphasis on protein phosphorylation/dephosphorylation process.
The present review suggests that: (1) there is no single model that can explain the molecular activation and regulation of sperm motility of the marine fish; (2) only in some species (puffer fish, tilapia, gilthead sea bream, and striped sea bream) protein phosphorylation/dephosphorylation has been shown to be involved in flagellar motility regulation; (3) only a few proteins were identified, which show a change in their state of phosphorylation following sperm activation.
A model of molecular mechanism controlling the activation of sperm motility in gilthead sea bream is being proposed here, which could be a useful model to clarify the sperm motility activation process in other species.
Similar content being viewed by others
Review
In fish with external fertilization, spermatozoa are usually immotile in the seminal tract (Stoss [1983]). The seminal plasma, whose osmolality and composition depends on the species, protects and immobilizes spermatozoa until they are ejaculated and their motility is initiated (Morisawa [1985]). Many environmental stimuli control sperm activation by triggering the different transduction pathways. In salmonids (Baynes et al. [1981]; Billard [1983]; Morisawa et al. [1983a]; Stoss [1983]; Morisawa [1985]) and sturgeons (Gallis et al. [1991]; Toth et al. [1997]; Alavi et al. [2004]), the reduction of the external K+ concentration, upon dilution of semen, initiates sperm motility. Hypotonic exposure after dilution into freshwater is the trigger signal in non-salmonid freshwater fish (Morisawa and Suzuki [1980]; Morisawa et al. [1983b]; Stoss [1983]; Morita et al. [2003]; Krasznai et al. [2003b]), while hypertonic exposure initiates sperm motility in many marine fishes (Morisawa and Suzuki [1980]; Oda and Morisawa [1993]; Detweiler and Thomas [1998]; Krasznai et al. [2003a]). It has been also reported that an egg-associated molecule triggers sperm activation in herring (Yanagimachi and Kanoh [1953]; Yanagimachi [1957a, 1957b]; Yanagimachi et al. [1992]; Oda et al. [1998]).
All these factors lead to the activation of the axoneme through signal transduction across the plasma membrane. Second messengers, such as cAMP and Ca2+, play key roles in the initiation of sperm motility in fish (Morisawa and Okuno [1982]; Krasznai et al. [2000]; Morita et al. [2003]; Zilli et al. [2008a]), as well as mammals (Lindemann [1978]; Tash and Means [1982]; Okamura et al. [1985]), sea urchin (Cook et al. [1994]), mussel (Stephens and Prior [1992]), and tunicate (Opresko and Brokaw [1983]). The second messengers may trigger the dynein-mediated sliding of the axonemal outer-doublet microtubules through different mechanisms such as protein phosphorylation/dephosphorylation (Hayashi et al. [1987]; Lindemann and Kanous [1989]; Inaba et al. [1999]; Nomura et al. [2000] Itoh et al. [2001]; Zilli et al. [2008]a), ADP—binding to dyneine (Lesich et al. [2008]; Hayashi and Shingyoji [2009]) or ionic strength (Cosson et al. [2008a]). This review is focused on the molecular mechanisms that enable environmental stimuli to determine the activation of the axoneme, with emphasis on the role of proteins with phosphorylation/dephosphorylation activity.
Sperm motility activation is mediated by an increase in intracellular calcium
In marine teleosts with external fertilization, three different mechanisms for motility initiation are known. (1) In flatfish species (Inaba et al. [2003]), although osmolarity is the primary factor that regulates the initiation of sperm motility, the intracellular HCO3− concentration plays a key role in this process (higher levels of bicarbonate inhibits motility). The intracellular level of bicarbonate is controlled by a cytosolic carbonic anhydrase that convert intracellular HCO3− into CO2 which lead to decrease in concentration of bicarbonate (CO2 diffuses outside the spermatozoa); (2) in herring, Clupea pallasii spermatozoa motility is initiated by the presence of a sperm motility initiation factor (SMIF), a 105-kDa basic glycoprotein that is localized to the micropylar region of the herring egg (Yanagimachi and Kanoh [1953]; Yanagimachi [1957a, 1957b]; Yanagimachi et al. [1992]; Pillai et al. [1993]); (3) in several marine species (including sea bass Dicentrarchus labrax, tuna Thunnus thynnus, gilthead sea bream Sparus aurata, striped sea bream Lithognathus mormyrus, puffer fish Tetraodontidae, flounder Paralichthys orbignyanus, Atlantic croacker Micropogonias undulatus, hake Merluccius merluccius, and cod Gadus morhua) hyperosmolality regulates sperm activation (Morisawa and Suzuki [1980]; Oda and Morisawa [1993]; Detweiler and Thomas [1998]; Krasznai et al. [2003a]; Zilli et al. [2008]a; Cosson et al. [2008a, 2008b]). Moreover, it has been shown that calcium ions also play a key role in the initiation of sperm motility. Three different mechanisms of action have been proposed for physiological roles of Ca2+: (a) Ca2+ acts directly on the axonemal structures (sea bass and tuna, Cosson et al. [2008a, 2008b]); (b) Ca2+ regulates Ca2+/calmodulin-dependent protein phosphorylation that in turn activates the axoneme (for example in puffer fish or seawater-acclimated euryhaline tilapia Oreochromis mossambicus) (Krasznai et al. [2003a]; Morita et al. [2004]); (c) Ca2+ leads to a cAMP-dependent protein phosphorylation that activates axoneme in gilthead sea bream and striped sea bream (Zilli et al. [2008]a). In all suggested mechanisms, the hyperosmolality signal firstly increases intracellular Ca2+ concentration (Oda and Morisawa [1993]), which is similar to what happens in freshwater fish (Cosson et al. [1989]; Krasznai et al. [2000]) and tunicates (Izumi et al. [1999]). This increase could be due to a calcium influx across the plasma membrane, or to a calcium release from intracellular store, or to a cytosol concentration following massive water efflux by aquaporins.
Calcium influx across the plasma membranes has been demonstrated in spermatozoa of seawater-acclimated Tilapia mossambicus,(Linhart et al. [1999]; Morita et al. [2004]), sea bass,and tuna (Cosson et al. [2008a, 2008b]). In vertebrates and invertebrates, an ATP-driven Ca2+ pump and a Na+/Ca2+exchangers (Wennemuth et al. [2003]) together with many types of calcium channels (Wiesner et al. [1998]; Arnoult et al. [1999]; Serrano et al. [1999]; Westenbroek and Babcock [1999]; Krasznai et al. [2000]; Wennemuth et al. [2000]; Jungnickel et al. [2001]; Quill et al. [2001]; Jagannathan et al. [2002]; Nikpoor et al. [2004]) allow the calcium flux throughout the plasma membranes of spermatozoa. Up to date, only one calcium transporter has been identified in the plasma membranes of fish spermatozoa. This is a reverse-Na+/Ca2+exchange that causes an efflux of Na+ and an influx of Ca2+ during ligand-induced motility initiation in herring sperm (Vines et al. [2002]).
The increase of intracellular calcium concentration could be also a consequence of stretch-activated channel (SAC) activation, when changes in the osmotic pressure occur (Krasznai et al. [2003a]; Cosson et al. [2008a, 2008b]). It is known that SAC may modify the activity of certain membrane proteins (Vandorpe et al. [1994]); therefore, they may increase the calcium membrane conductivity by direct influx of this ion (together with K+) or by the activation of calcium channels as observed in carp (Krasznai et al. [2003b]).
The increase of the intracellular (spermatozoa) calcium concentration, following hyper-osmotic signal, could be also due to the release of Ca2+ from intracellular stores that has been demonstrated in puffer fish (Krasznai et al. [2003a]). Although spermatozoa lack endoplasmic reticulum, it seems that the limited set of organelles that could work as intracellular Ca2+ stores (Naaby-Hansen et al. [2001]; Ho and Suarez [2003]; Publicover et al. [2007]). The role of mitochondria in the calcium storage is still unclear. In sea urchin sperm, a Ca2+ ATPase (SPCA) has been localized into the giant mitochondrion in the midpiece, thus suggesting a possible role of this organelle as Ca2+ store (Gunaratne and Vacquier [2006]).
Another membrane protein involved in the sperm motility initiation in marine fish is aquaporin that could determine an increase of intracellular calcium as a consequence of cytosol concentration due to massive water efflux after hyper-osmotic signal (Cosson et al. [1999]; Zilli et al. [2009]). In particular, two kinds of aquaporins have been identified in gilthead sea bream spermatozoa: aquaporin1a (Aqp1a) and S. aurata aquaglyceroporin (Glp); the last one has been recently identified as Aqp10b (Zilli et al. [2009]; Cerda and Finn [2010]). Aqp1a and Aqp10b are localized in the plasma membrane of the head and flagellum of spermatozoa. Immunostaining technique demonstrated that the expression of aquaporins increases after motility activation, which suggests a possible recruitment of aquaporins into the plasma membrane from intracellular vesicles following hyperosmotic signal (Figure 1). Aqp1a and Aqp10b could play different roles during the process of sperm activation in sea bream. It is suggested that the Aqp1a mediates sperm activation, and Aqp10b involves in the maintenance of motility, as suggested for Aqp7 in human spermatozoa (Saito et al. [2004]). The physiological role of aquaglyceroporins during sperm motility in vertebrates, however, is not well understood, although it is known that mammalian spermatozoa are able to use glycerol aerobically (Mann and White [1956]; Aalbers et al. [1961]) and that organic alcohols (including glycerol) induce protein phosphorylation for motility initiation in chum salmon Oncorhynchus keta (Morita et al. [2005]).
Flagellar axoneme activation: final event in the mechanism of sperm motility activation in marine fish
The final event in the mechanism of sperm motility initiation is the activation of the axoneme. This is a microtubule-based, highly organized, and conserved structure composed by more than 250 kinds of proteins. For motility activation, the activity of dynein (the molecular motor) has to be started (and regulated) to produce the coordinated sliding of microtubules in the axoneme (Brokaw [1989]; King [2000]).
In marine fish, the activation of axoneme is achieved by different mechanisms. In sea bass and tuna spermatozoa, the key factor to start the beating of the flagella is the variation of ionic strength (Alavi and Cosson [2006]; Cosson et al. [2008a]). In particular, Cosson et al. ([2008a]) proposed the following model. The water efflux due to the hyperosmotic shock could cause a local membrane distortion that activates SAC. The activation of the SAC could lead to the activation of water channels resulting in rapid release of water from the cells. The result of this process would increase the ionic strength of intracellular fluids leading to the activation of dynein. In flatfish, HCO3− ion appears to act directly on the axonemal machinery itself since it inhibits the movement of demembranated spermatozoa (Inaba et al. [2003]).
In herring sperm, increasing concentration of calcium ions is the main factor that determines the activation of the axoneme. In particular, sperm motility initiation factor (SMIF) induces calcium influx by opening the voltage-gated calcium channels and activating a reverse Na+/Ca2+ exchange (Vines et al. [2002]). SMIF determines approximately fourfold increase in Ca2+ concentration that acts on the axoneme inducing motility (Pillai et al. [1993]; Vines et al. [2002]; Cherr et al. [2008]).
In some fish species, protein phosphorylation/dephosphorylation is involved in flagellar motility regulation. In puffer fish and tilapia sperm, the activity of the flagellar axoneme is regulated by Ca2+/calmodulin-dependent protein phosphorylation, while in gilthead sea bream and striped sea bream by cAMP-dependent protein phosphorylation (Morita et al. [2003]; Krasznai et al. [2003a]; Zilli et al. [2008]a, [2009]). The major targets of protein phosphorylation/dephosphorylation causing the activation of sperm motility are structural components of dynein arms (inner and outer), kinases, and phosphatases anchored in the axoneme and in the radial spoke proteins (Dey and Brokaw [1991]; Hamasaki et al. [1991]; Porter and Sale [2000]; Yang et al. [2001]). Kinases and phosphatases are required for local control of motor activity (Porter and Sale [2000]; Aparicio et al. [2007]), and radial spoke proteins regulate inner arm dynein by phosphorylation/dephosphorylation (Smith and Lefebvre [1997]; Porter and Sale [2000]). However, only few proteins involved in the initiation of motility in marine fish spermatozoa have been identified. Morita et al. ([2004]) have demonstrated, using demembranated tilapia spermatozoa, that calcium not only initiates flagellar motility but also modulates the flagellar waveform. The same researchers identified a Ca2+-binding protein (CaM) with MW of 18 kDa and pI 4.0 that regulates the flagellar motility in a calcium dependent manner by modifying both the sliding velocity and flagellar waveform (Morita et al. [2003, 2004, 2006]). The same researchers also identified in tilapia spermatozoa a Ca2+/CaM-dependent protein kinase IV (CaMKIV), localized along the flagellum and sleeve structure, that is involved in the activation and regulation of sperm flagellar motility through a Ca2+/CaM-dependent phosphorylation of seven axonemal proteins. In gilthead sea bream, three proteins have been identified that change their phosphorylation state after sperm activation and play a role in the initiation of sperm motility (Zilli et al. [2008]a, [2009]):
-
(1)
An A-kinase anchor proteins (AKAP) have the function of binding to the regulatory subunits (RI and RII) of protein kinase A (PKA) and confining the enzyme to discrete locations within the cell. Therefore, cAMP levels temporally regulate PKA, whereas the spatial regulation within the cell occurs through compartmentalization by binding to AKAP, thus assuring specificity of PKA function. The role of AKAP as a key regulator of sperm motility has been already established (Vijayaraghavan et al. [1997]). In addition, a recent study demonstrated that phosphorylation of AKAP in human sperm results in tail recruitment of PKA and increase of sperm motility, providing evidence for a functional role of phosphorylation of AKAP (Luconi et al. [2004]);
-
(2)
The acetyl-CoA synthetase activates acetate to acetyl-CoA, and provides the cell with the two carbon metabolite used in many anabolic and energy generation processes. Therefore, this enzyme could be activated in motile sperm to increase the level of ATP, which is necessary for flagellar movement;
-
(3)
A novel protein similar to phosphatase and actin regulator 3 of Danio rerio that may be a protein phosphatase inhibitor.
In striped sea bream, two proteins involved in the activation of sperm motility have been identified: myotubularin-related protein 1 and dual-specificity tyrosine phosphorylation-regulated kinase 3 (DYRK3) (Zilli et al. [2008]a). The myotubularin-related protein 1 belongs to the protein-tyrosine phosphatase family, and DYRK3 is a protein kinase auto-phosphorylated on tyrosine residues belonging to the dual-specificity tyrosine phosphorylated and regulated kinase family. Many studies have demonstrated that the development and maintenance of motility is regulated by a complex balance between kinase and phosphatase activities (Tash and Bracho [1994]; Porter and Sale [2000], King [2000]; Aparicio et al. [2007]).
From the above report, it clearly emerges that there are different mechanisms of sperm motility initiation in marine fish. They are species-specific, and they reflect the adaptation to species life histories/environment, and only parts of which have been studied in the different species. The identified proteins that play a role in this mechanism in marine fish are summarized in Table 1, where possible homologues in freshwater fish, invertebrate, and mammalian have been also reported.
S. aurata spermatozoa as a model to study the molecular mechanism of sperm motility activation
The molecular mechanism that determines sperm motility activation in gilthead sea bream has many similarities with the mechanisms observed in many animals (sea urchin, salmonids, and mammals). This is not surprising since that internal microtubule-based structures of the axoneme have been well conserved during evolution. For this reason, the identification of proteins that change their phosphorylation state following sperm motility activation and the understanding of signaling pathways among these in gilthead sea bream spermatozoa could be interesting to clarify this process in other species.
In S. aurata, a drastic change of the environmental osmolality is the signal that triggers sperm motility activation. The transduction of this event in axoneme activation requires action of many intracellular mediators. First event is the water efflux that leads to local distortions of the flagellar membrane that, in turn, activates water channels. Recent study (Zilli et al. [2011]) confirms the important role of aquaporins in initiating sperm motility; in fact, when these proteins are inhibited by HgCl2, the phosphorylation of some proteins (174 kDa protein of head; 147, 97, and 33 kDa proteins of flagella), following the hyper-osmotic shock, is also completely or partially inhibited. However, more than one transduction pathways could be activated when sea bream spermatozoa are ejaculated in seawater, since numerous proteins showed an HgCl2 (Aqps)-independent phosphorylation state after sperm activation.
As reported in Figure 2 in gilthead sea bream spermatozoa, the rapid water efflux across AQPs determines a reduction in cell volume with the increase in intracellular ionic concentration. It is known that adenylyl cyclase is activated by different mechanisms, such as membrane hyperpolarization (Beltran et al. [1996]; Izumi et al. [1999]) and/or increase in Ca2+ and HCO3− concentration (Visconti and Kopf [1998]). The cAMP signaling pathway starts the activation of sperm motility by phosphorylation of some proteins. This post-transductional modification in sperm motility activation was recently (Zilli et al. [2011]) confirmed by observation that a higher number of protein bands underwent a change of their phosphorylation state at flagella level with respect to the head level in gilthead sea bream. However, it must be underlined that the proposed model fits well to the gilthead sea bream sperm activation but cannot generalize to other marine fish species. A cAMP-dependent protein phosphorylation, involved in sperm motility activation, has been also demonstrated in chum salmon (Itoh et al. [2001]) and trout (Hayashi et al. [1987]). In many species, some proteins phosphorylated in PKA-dependent manner have been identified as the light (from 8 to 30 kDa) or heavy (approximately 500 kDa) chains of the outer arm dynein of sperm flagellum, such as the 21 kDa protein of chum salmon (Inaba et al. [1999]), the 32 and the 500 kDa proteins in sea urchin spermatozoa (Bracho et al. [1998]), the 21 and the 26 kDa proteins in ascidian spermatozoa (Nomura et al. [2000]), the 27 and the 20 kDa proteins of mussel spermatozoa (Stephens and Prior [1992]), and the 18 to 20 kDa protein in C. intestinalis sperm (Dey and Brokaw [1991]). In addition, in salmonid fish, a 48 kDa protein, phosphorylated in a cAMP-dependent manner, was identified as regulatory subunit of PKA (Itoh et al. [2003]). In S. aurata, an AKAP protein that anchors the regulatory subunit of PKA for tethering of protein kinases in close proximity to their target proteins has been identified. Different types of AKAP have been found in spermatozoa, localized into the fibrous sheath of the principal piece (Moss and Gerton [2001]). In mammals, it has been demonstrated that, among the proteins phosphorylated during epididymal maturation, there are several mitochondrial proteins (Aitken et al. [2007]) and a protein phospahatase PP1γ2 (Chakrabarti et al. [2007]). This is in agreement with a previous finding regarding proteins phosphorylated after motility initiation in gilthead sea bream spermatozoa that are precisely one mitochondrial protein (acetyl-CoA synthetase) and one protein that may be a protein phosphatase inhibitor; in addition in striped sea bream, two proteins were identified, a phospatase and a kinase, that are involved in sperm motility activation (Zilli et al. [2008]a). The activation of proteins of sperm mitochondria could be important to provide the energy for sperm motility; in fact, fish sperm quality is correlated with ATP content (Christen et al. [1987]; Zilli et al. [2004]). Mature spermatozoa are highly specialized cells, transcriptionally inactive and unable to synthesize new proteins; for this reason, protein phosphorylation/dephosphorylation has to rely on regulation of many processes that is greater than in many other types of cell (Urner and Sakkas [2003]).
Conclusions
From this review emerges plainly that a complex universal mechanism for sperm motility initiation in marine fish does not exist, but there are different mechanisms that are species-specific, only parts of which have been studied in the different species. In particular, in some of these species (puffer fish, tilapia, gilthead sea bream, and striped sea bream), protein phosphorylation/dephosphorylation has been shown to be involved in flagellar motility regulation and present many similarities with the mechanisms of axoneme activation of marine invertebrate and mammal spermatozoa.
References
Aalbers JC, Mann T, Polge C: Metabolism of boar semen in relation to sperm motility. J Reprod Fert 1961, 2: 42–53. 10.1530/jrf.0.0020042
Aitken RJ, Nixon B, Lin M, Koppers AJ, Lee YH, Baker MA: Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 2007, 9: 554–564. 10.1111/j.1745-7262.2007.00280.x
Alavi SMH, Cosson J: Sperm motility in fishes: (II) Effects of ions and osmotic pressure: a review. Cell Biol Int 2006, 30: 1–14. 10.1016/j.cellbi.2005.06.004
Alavi SMH, Cosson J, Karami M, Amiri BM, Akhoundzadeh MA: Spermatozoa motility in the Persian sturgeon, Acipenser persicus: effects of pH, dilution ratio, ions and osmolality. Reproduction 2004, 128: 819–828. 10.1530/rep.1.00244
Aparicio IM, Bragado MJ, Gil MC, Garcia-Herreros M, Gonzalez Fernandez L, Tapia JA, Garcia-Marin LJ: Porcine sperm motility is regulated by serine phosphorylation of the glycogen synthase kinase-3alpha. Reproduction 2007, 134: 435–444. 10.1530/REP-06-0388
Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M, Florman HM: Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc Natl Acad Sci USA 1999, 96: 6757–6762. 10.1073/pnas.96.12.6757
Baynes SM, Scott AP, Dawson AP: Rainbow trout, Salmo gairdnerii Richardson, spermatozoa: effects of cations and pH on motility. J Fish Biol 1981, 19: 259–267. 10.1111/j.1095-8649.1981.tb05830.x
Becker W, Weber Y, Wetzel K, Eirmbter K, Tejedor F, Joost H-G: Sequence characteristics, subcellular localization and substrate specificity of dyrk-related kinases, a novel family of dual specificity protein kinases. J Biol Chem 1998, 273: 25893–25902. 10.1074/jbc.273.40.25893
Beltran C, Zapata O, Darszon A: Membrane potential regulates sea urchin sperm adenylyl cyclase. Biochemistry 1996, 35: 7591–7598. 10.1021/bi952806v
Billard R: Effects of ceolomic and seminal fluids and various saline diluents on the fertilizing ability of spermatozoa in the rainbow trout, Salmo gairdnerii. J Reprod Fertil 1983, 68: 77–84. 10.1530/jrf.0.0680077
Bracho GE, Fritch JJ, Tash JS: Identification of flagellar proteins that initiate the activation of sperm motility in vivo. Biochem Biophys Res Commun 1998, 242: 231–23. 10.1006/bbrc.1997.7937
Brokaw CJ: Operation and regulation of the flagellar oscillator. In Movement C. Edited by: Warner F, Satir P, Gibbons R. The Dynein ATPases, vol. 1. AR Liss, New York; 1989:267–279.
Carr DW, Hanlon Newell AE: The role of A-kinase anchoring proteins (AKAPs) in regulating sperm function. Soc Reprod Fertil Suppl 2007, 63: 135–142.
Cerda J, Finn RN: Piscine aquaporins: an overview of recent advances. J Exp Zool A: Ecol Genet Physiol 2010, 313A: 623–650. 10.1002/jez.634
Chakrabarti R, Cheng L, Puri P, Soler D, Vijayaraghavan S: Protein phosphatase PP1 gamma 2 in sperm morphogenesis and epididymal initiation of sperm motility. Asian J Androl 2007, 9: 445–452. 10.1111/j.1745-7262.2007.00307.x
Chen Q, Peng H, Lei L, Zhang Y, Kuang H, Cao Y, Shi QX, Ma T, Duan E: Aquaporin 3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration. Cell Res 2011, 21: 922–933. 10.1038/cr.2010.169
Cherr GN, Morisama M, Vines CA, Yoshida K, Smith EH, Matsubara T, Pillai MC, Griffin FJ, Yanagimachi R: Two egg-derived molecules in motility initiation and fertilization in Pacific herring (Clupea pallasi). Int J Dev Biol 2008, 52: 743–752. 10.1387/ijdb.072566gc
Christen F, Gatti J-L, Billard R: Trout sperm motility. The transient movement of trout sperm is related to changes in the concentration of ATP following the activation of flagellar movement. Eur J Biochem 1987, 166: 667–671. 10.1111/j.1432-1033.1987.tb13565.x
Cook SP, Brokaw CJ, Muller CH, Babcock DF: Sperm chemotaxis: egg peptides control cytosolic calcium to regulate flagellar responses. Dev Biol 1994, 165: 10–19. 10.1006/dbio.1994.1229
Cosson MP, Billard R, Letellier L: Rise of internal Ca2+ accompanies the initiation of trout sperm motility. Cell Motil Cytoskel 1989, 14: 424–434. 10.1002/cm.970140312
Cosson J, Billard R, Cibert C, Dreanno C, Suquet M: Ionic factors regulating the motility of fish sperm. In The male gamete: from basic to clinical applications. Edited by: Gagnon C. Cache Rive Press, Vienna, Illinois; 1999:161–186.
Cosson J, Groison A-L, Suquet M, Fauvel C, Dreanno C, Billard R: Studying sperm motility in marine fish: an overview on the state of the art. J Appl Ichthyol 2008, 24: 460–486. 10.1111/j.1439-0426.2008.01151.x
Cosson J, Groison A-L, Suquet M, Fauvel C, Dreanno C, Billard R: Marine fish spermatozoa: racing ephemeral swimmers. Reproduction 2008, 136: 277–294. 10.1530/REP-07-0522
Detweiler C, Thomas P: Role of ions and ion channels in the regulation of Atlantic croaker sperm motility. J Exp Biol 1998, 281: 139–148.
Dey CS, Brokaw CJ: Activation of Ciona sperm motility: phosphorylation of dynein polypeptides and effects of a tyrosine kinase inhibitor. J Cell Sci 1991, 100: 815–824.
Gallis JL, Fedrigo E, Jatteau P, Bonpunt E, Billard R: Siberian sturgeon, Acipenser baeri, spermatozoa. In Acipenser effects of dilution, pH, osmotic pressure, sodium and potassium ions on motility. Edited by: Williot P. Cemagref Publ, France, Bordeaux; 1991:143–151.
Gunaratne HJ, Vacquier VD: Evidence for a secretory pathway Ca2+-ATPase in sea urchin spermatozoa. FEBS Letters 2006, 580: 3900–3904. 10.1016/j.febslet.2006.06.019
Hamasaki T, Barkalow K, Richmond J, Satir P: cAMP-stimulated phosphorylation of an axonemal polypeptide that copurifies with the 22 S dynein arm regulates microtubule translocation velocity and swimming speed in paramecium. Proc Natl Acad Sci USA 1991, 88: 7918–7922. 10.1073/pnas.88.18.7918
Hayashi S, Shingyoji C: Bending-induced switching of dynein activity in elastase-treated axonemes of sea urchin sperm-roles of Ca2+ and ADP. Cell Motil Cytoskel 2009, 66: 292–301. 10.1002/cm.20360
Hayashi H, Yamamoto K, Yonekawa H, Morisawa M: Involvement of tyrosine protein kinase in the initiation of flagellar movement in rainbow trout spermatozoa. J Biol Chem 1987, 262: 16692–16698.
Ho H-C, Suarez SS: Characterization of the intracellular calcium store at the base of the sperm flagellum that regulate hyperactivated motility. Biol Reprod 2003, 68: 1590–1596.
Inaba K, Kagami O, Ogawa K: Tctex2-related outer arm dynein light chain is phosphorylated at activation of sperm motility. Biochem Biophys Res Commun 1999, 256: 177–183. 10.1006/bbrc.1999.0309
Inaba K, Dréanno C, Cosson J: Control of flatfish sperm motility by CO2 and carbonic anhydrase. Cell Motil Cytoskel 2003, 55: 174–187. 10.1002/cm.10119
Itoh A, Inaba K, Fujinoki M, Morisawa M: Motility-associated and cyclic AMP-dependent protein phosphorylation in the sperm of the chum salmon, Oncorhynchus keta. Biomed Res 2001, 22: 241–248.
Itoh A, Inaba K, Ohtake H, Fujinoki M, Morisawa M: Characterization of a cAMP-dependent protein kinase catalytic subunit from rainbow trout spermatozoa. Biochem Biophys Res Com 2003, 305: 855–861. 10.1016/S0006-291X(03)00840-4
Izumi H, Marian T, Inaba K, Oka Y, Morisawa M: Membrane hyperpolarization by sperm-activating and -attracting factor increases cAMP level and activates sperm motility in the ascidian Ciona intestinalis. Dev Biol 1999, 213: 246–25. 10.1006/dbio.1999.9367
Jagannathan S, Punt EL, Gu Y, Arnoult C, Sakkas D, Barratt CL, Publicover SJ: Identification and localisation of T-type voltage-operated calcium channel subunits in human male germ cells. Expression of multiple isoforms. J Biol Chem 2002, 8: 8449–8456.
Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM: Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 2001, 3: 499–502. 10.1038/35074570
King SM: The dynein microtubule motor. Biochim Biophys Acta 2000, 1496: 60–75. 10.1016/S0167-4889(00)00009-4
Krasznai Z, Marian T, Izumi H, Damjanovich S, Balkay L, Tron L, Morisawa M: Membrane hyperpolarization removes inactivation of Ca2+ channels leading to Ca2+ influx and initiation of sperm motility in the common carp. Biophysics 2000, 97: 2052–2067.
Krasznai Z, Morisawa M, Krasznai ZT, Morisawa S, Inaba K, Bazsane ZK, Rubovszky B, Bodnár B, Borsos A, Márián T: Gadolinium, a mechano-sensitive channel blocker, inhibits osmosis initiated motility of sea- and freshwater fish sperm, but does not affect human or ascidian sperm motility. Cell Motil Cytoskel 2003, 55: 232–243. 10.1002/cm.10125
Krasznai Z, Morisawa M, Morisawa S, Krasznai ZT, Tron L, Marian T: Role of ion channels and membrane potential in the initiation of carp sperm motility. Aquat Living Resour 2003, 16: 445–449. 10.1016/S0990-7440(03)00054-8
Lesich KA, Pelle DW, Lindemann CB: Insights into the mechanism of ADP action on flagellar motility derived from studies on bull sperm. Biophys J 2008, 95: 472–482. 10.1529/biophysj.107.127951
Lindemann CB: A cAMP-induced increase in the motility of demembranated bull sperm models. Cell 1978, 13: 9–18. 10.1016/0092-8674(78)90133-2
Lindemann CB, Kanous KS: Regulation of mammalian sperm motility. Arch Androl 1989, 23: 1–22. 10.3109/01485018908986783
Linhart O, Walford J, Silvaloganathan B, Lam TJ: Effect of osmolality and ions on the motility of stripped and testicular sperm of freshwater- and seawater-acclimated tilapia, Oreochromis mossambicus. J Fish Biol 1999, 55: 1344–1358.
Luconi M, Carloni V, Marra F, Ferruzzi P, Forti G, Baldi E: Increased phosphorylation of AKAP by inhibition of phosphatidylinositol 3-kinase enhances human sperm motility through tail recruitment of protein kinase A. J Cell Sci 2004, 117: 1235–1246. 10.1242/jcs.00931
Luconi M, Cantini G, Baldi E, Forti G: Role of a-kinase anchoring proteins (AKAPs) in reproduction. Front Biosci 2011, 16: 1315–1330. 10.2741/3791
Ma TH, Liu JF, Zhao RF, Jiang H, Dai LS, Zhao YM, Zhao ZH, Zhang JB: Association analysis of aquaporin 7 (AQP7) gene variants with semen quality and fertility in bulls. Turk J Vet Anim Sci 2011, 35: 63–66.
Mann T, White LG: Metabolism of glycerol, sorbitol and related compounds by spermatozoa. Nature, Lond 1956, 178: 142–143.
Marín-Briggiler CI, Jha KN, Chertihin O, Buffone MG, Herr JC, Vazquez-Levin MH, Visconti PE: Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation. J Cell Sci 2005, 118: 2013–2022. 10.1242/jcs.02326
Morisawa M: Initiation mechanism of sperm motility at spawning in teleost. Zool Sci 1985, 2: 605–615.
Morisawa M, Okuno M: Cyclic AMP induces maturation of trout sperm axoneme to initiate motility. Nature 1982, 295: 703–704. 10.1038/295703a0
Morisawa M, Suzuki K: Osmolality and potassium ions: Their roles in initiation of sperm motility in teleosts. Science 1980, 210: 1145–1147. 10.1126/science.7444445
Morisawa M, Suzuki K, Morisawa S: Effects of potassium and osmolality on spermatozoan motility of salmonid fishes. J Exp Biol 1983, 107: 105–113.
Morisawa M, Suzuki K, Shimizu H, Morisawa S, Yasuda K: Effects of osmolality and potassium on motility of spermatozoa from freshwater cyprinid fishes. J Exp Biol 1983, 107: 95–103.
Morita M, Takemura A, Okuno M: Requirement of Ca2+ on activation of sperm motility in euryhaline tilapia (Oreochromis mossambicus). J Exp Biol 2003, 206: 913–921. 10.1242/jeb.00153
Morita M, Takemura A, Okuno M: Acclimation of sperm motility apparatus in seawater-acclimated euryhaline tilapia, Oreochromis mossambicus. J Exp Biol 2004, 207: 337–34. 10.1242/jeb.00748
Morita M, Fujinoki M, Okuno M: K+-independent initiation of motility in chum salmon sperm treated with an organic alcohol, glycerol. J Exp Biol 2005, 208: 4549–4556. 10.1242/jeb.01921
Morita M, Takemura A, Nakajima A, Okuno M: Microtubule sliding movement in tilapia sperm flagella axoneme is regulated by Ca2+/calmodulin-dependent protein phosphorylation. Cell Motil Cytoskel 2006, 63: 459–470. 10.1002/cm.20137
Morita M, Nishikawa A, Nakajima A, Iguchi A, Sakai K, Takemura A, Okuno M: Eggs regulate sperm flagellar motility initiation, chemotaxis and inhibition in the coral Acropora digitifera. A gemmifera and A tenuis. J Exp Biol 2009, 209: 4574–4579.
Moss SB, Gerton GL: A-kinase anchor proteins in endocrine systems and reproduction. Trends Endocrinol Metabol 2001, 12: 434–440. 10.1016/S1043-2760(01)00493-3
Moss SB, Turner RM, Burkert KL, VanScoy BH, Gerton GL: Conservation and function of a bovine sperm A-kinase anchor protein homologous to mouse AKAP82. Biol Reprod 1999, 61: 335–342. 10.1095/biolreprod61.2.335
Naaby-Hansen S, Wolkowicz MJ, Klotz K, Bush LA, Westbrook VA, Shibahara H, Shetty J, Coonrod SA, Reddi PP, Shannon J, Kinter M, Sherman NE, Fox J, Flickinger CJ, Herr JC: Co-localization of the inositol 1,4,5-trisphosphate receptor and calreticulin in the equatorial segment and in membrane bounded vesicles in the cytoplasmic droplet of human spermatozoa. Mol Hum Reprod 2001, 7: 923–933. 10.1093/molehr/7.10.923
Nikpoor P, Mowla SJ, Movahedin M, Ziaee SA, Tiraihi T: CatSper gene expression in postnatal development of mouse testes and in subfertile men with deficient sperm motility. Hum Reprod 2004, 19: 124–12. 10.1093/humrep/deh043
Nomura M, Inaba K, Morisawa M: Cyclic AMP- and calmodulin/dependent phosphorylation of 21- and 26-kDa proteins in axoneme is a prerequisite for SAAF-induced motile activation in ascidian spermatozoa. Dev Growth Differ 2000, 42: 129–138. 10.1046/j.1440-169x.2000.00489.x
Nomura M, Inaba K, Morisawa M: Calmodulin/calmodulin-dependent protein kinase II mediates SAAF-induced motility activation of ascidian sperm. Cell Motil Cytoskeleton 2004, 59: 28–37. 10.1002/cm.20020
Oda S, Morisawa M: Rises of intracellular Ca2+ and pH mediate the initiation of sperm motility by hyperosmolality in marine teleosts. Cell Mot Cytoskel 1993, 25: 171–178. 10.1002/cm.970250206
Oda S, Igarashi Y, Manaka K-I, Koibuchi N, Sakai-Sawada M, Sakai K, Morisawa M, Ohtake H, Shimuzu N: Sperm-activating proteins obtained from the Herring eggs are homologous to trypsin inhibitors and synthesized in follicle cells. Develop Biol 1998, 204: 55–63. 10.1006/dbio.1998.9056
Okamura N, Tajima Y, Soejima A, Masuda H, Sugita Y: Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. J Biol Chem 1985, 260: 9699–9705.
Opresko L, Brokaw CJ: cAMP-dependent phosphorylation associated with activation of motility of Ciona sperm flagella. Gamete Res 1983, 8: 201–218. 10.1002/mrd.1120080302
Pillai MC, Shields TS, Yanagimachi R, Cherr GN: Isolation and partial purification of the sperm motility initiation factor from eggs of the Pacific Herring, Clupea pallasi. J Exp Zool 1993, 265: 336–342. 10.1002/jez.1402650316
Porter ME, Sale WS: The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol 2000, 151: F37-F42. 10.1083/jcb.151.5.F37
Publicover S, Harper CV, Barratt C: [Ca2+]i signalling in sperm-making the most of what you've got. Nat Cell Biol 2007, 9: 235–242. 10.1038/ncb0307-235
Quill TA, Ren D, Clapham DE, Garbers DL: A voltage-gated ion channel expressed specifically in spermatozoa. Proc Natl Acad Sci USA 2001, 98: 12527–12531. 10.1073/pnas.221454998
Saito K, Kageyama Y, Okada Y, Kawakami S, Kihara K, Ishibashi K, Sasaki S: Localization of aquaporin-7 in human testis and ejaculated sperm: possible involvement in maintenance of sperm quality. J Urol 2004, 172: 2073–2076. 10.1097/01.ju.0000141499.08650.ab
Serrano CJ, Trevino CL, Felix R, Darszon A: Voltage dependent Ca2+ channel subunit expression and immunolocalization in mouse spermatogenic cells and sperm. FEBS Lett 1999, 462: 171–176. 10.1016/S0014-5793(99)01518-5
Shayu D, Kesava CC, Soundarajan R, Rao AJ: Effects of ICI 182780 on estrogen receptor expression, fluid absorption and sperm motility in the epididymis of the bonnet monkey. Reprod Biol Endocrinol 2005, 3: 10. 10.1186/1477-7827-3-10
Smith EF, Lefebvre PA: The role of central apparatus components in flagellar motility and microtubule assembly. Cell Motil Cytoskel 1997, 38: 1–8. 10.1002/(SICI)1097-0169(1997)38:1<1::AID-CM1>3.0.CO;2-C
Stephens RE, Prior G: Dynein from serotonin-activated cilia and flagella: extraction characteristics and distinct sites for cAMP-dependent protein phosphorylation. J Cell Sci 1992, 103: 999–1012.
Stoss J: Fish gamete preservation and spermatozoa physiology. In Fish Physiology. Edited by: Hoar WS, Randall DJIII, Donaldson EM. Academic, New York; 1983:305–350.
Tash JS, Bracho GE: Regulation of sperm motility: emerging evidence for a major role for protein phosphatases. J Androl 1994, 15: 505–509.
Tash JS, Means AR: Regulation of protein phosphorylation and motility of sperm by cyclic adenosine monophosphate and calcium. Biol Reprod 1982, 26: 745–763. 10.1095/biolreprod26.4.745
Toth GP, Ciereszko A, Christ SA, Dabrowski K: Objective analysis of sperm motility in the lake sturgeon (Acipenser fulvescens): activation and inhibition conditions. Aquaculture 1997, 154: 337–348. 10.1016/S0044-8486(97)00066-5
Urner F, Sakkas D: Protein phosphorylation in mammalian spermatozoa. Reproduction 2003, 125: 17–26. 10.1530/rep.0.1250017
Vandorpe DH, Small DL, Dabrowski AR, Morris CE: FMRFamide and membrane stretch as activators of the Aplysa. Biophys J 1994, 66: 46–58. 10.1016/S0006-3495(94)80749-0
Vijayaraghavan S, Goueli SA, Davey MP, Carr DW: Protein kinase anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 1997, 21: 4747–4752.
Vines CA, Yoshida K, Griffin FJ, Pillai MC, Morisawa M, Yanagimachi R, Cherr GN: Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange. PNAS 2002, 99: 2026–2031. 10.1073/pnas.042700899
Visconti PE, Kopf GS: Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 1998, 59: 1–6. 10.1095/biolreprod59.1.1
Wennemuth G, Westenbroek RE, Xu T, Hille B, Babcock DF: CaV2.2 and CaV2.3 (N- and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm. J Biol Chem 2000, 275: 21210–21217. 10.1074/jbc.M002068200
Wennemuth G, Carlson AE, Harper AJ, Babcock DF: Bicarbonate actions on flagellar and calcium channel responses: initial events in sperm activation. Development 2003, 130: 1317–1326. 10.1242/dev.00353
Westenbroek RE, Babcock DF: Discrete regional distributions suggest diverse functional roles of calcium channel α1 subunits in sperm. Dev Biol 1999, 207: 457–46. 10.1006/dbio.1998.9172
Wiesner B, Weiner J, Middendorff R, Hagen V, Kaupp UB, Weyand I: Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm. J Cell Biol 1998, 42: 473–48.
Yanagimachi R: Some properties of the sperm activating factor in the micropyle area of the herring egg. Annot Zool Jap 1957, 30: 114–119.
Yanagimachi R: Studies of fertilization of Clupea pallasi. III Manner of sperm entrance in to the egg . Zool Mag (Japan) 1957, 66: 222–225.
Yanagimachi R, Kanoh Y: Manner of sperm entry in herring egg, with special reference to the role of calcium ions in fertilization. J Fac Sci Hokkaido 1953, 11: 487–494.
Yanagimachi R, Cherr G, Pillai M, Baldwin J: Evidence suggesting the presence of a sperm-attracting substance around the micropyles of salmonid and herring eggs. Growth Develop Differ 1992, 34: 447–461. 10.1111/j.1440-169X.1992.00447.x
Yang P, Diener DR, Rosenbaum JL, Sale WS: Localization of calmodulin and dynein light chain LC8 in flagellar radial spokes. J Cell Biol 2001, 153: 1315–1326. 10.1083/jcb.153.6.1315
Zilli L, Schiavone R, Zonno V, Storelli C, Vilella S: ATP concentration and β-D-glucuronidase activity as indicators of sea bass semen quality. Biol Reprod 2004, 70: 1679–1684. 10.1095/biolreprod.103.027177
Zilli L, Schiavone R, Storelli C, Vilella S: Molecular mechanisms determining sperm motility initiation in two sparids (Sparus aurata and Lithognathus mormyrus). Biol Reprod 2008, 79: 356–366. 10.1095/biolreprod.108.068296
Zilli L, Schiavone R, Chauvigné F, Cerdà J, Storelli C, Vilella S: Evidence for the involvement of aquaporins in sperm motility activation of the teleost gilthead sea bream (Sparus aurata). Biol Reprod 2009, 81: 880–888. 10.1095/biolreprod.109.077933
Zilli L, Beirão J, Schiavone R, Herraez MP, Cabrita E, Storelli C, Vilella S: Aquaporin inhibition changes protein phosphorylation pattern following sperm motility activation in fish. Theriogenology 2011, 76: 737–744. 10.1016/j.theriogenology.2011.04.006
Author information
Authors and Affiliations
Corresponding author
Additional information
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
ZL has made substantial contributions to conception and design. SR and SC have been involved in drafting the manuscript. VS has been involved in revising the manuscript critically for important intellectual content. All authors read and approved the final manuscript.
Authors’ original submitted files for images
Below are the links to the authors’ original submitted files for images.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Zilli, L., Schiavone, R., Storelli, C. et al. Molecular mechanism regulating axoneme activation in marine fish: a review. Int Aquat Res 4, 2 (2012). https://doi.org/10.1186/2008-6970-4-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/2008-6970-4-2