Sperm Chemotaxis: The First Authentication Events Between Conspecific Gametes Before Fertilization

Chemoattractant molecules for sperm in plants are low molecular weight organic compounds such as the bimalate ions in the bracken fern (Brokaw 1957, 1958) and unsaturated cyclic or linear hydrocarbons, such as ectocarpene, in the brown algae (Maier and Müller 1986). In the aquatic fungus A. macrogynus, the female gametes release a sesquiterpene “sirenin” as a attractant for male gametes (Machlis 1973), and interestingly, a different compound called “parisin” released by the male gametes is able to attract flagellated female gametes of the same species (Pommerville and Olson 1987).

In animals, sperm chemoattractants have been identified in several species, and most of these chemoattractant molecules are proteins or peptides. Chemoattractants such as “resact ” in sea urchins (Ward et al. 1985; Guerrero et al. 2010), “sepsap ” in cuttlefish (Zatylny et al. 2002), and “asterosap ” in starfish (Böhmer et al. 2005) are peptides. A 21-kDa protein named “allurin ” in the amphibian Xenopus laevis (Olson et al. 2001) and tryptophan in abalone (Riffell et al. 2002) act as sperm chemoattractants. In the hydrozoan Hippopodius hippopus, the attractant has not yet been identified but has been characterized as a small and thermoresistant protein with a molecular mass of 25 kDa and an isoelectric point of 3.5 (Cosson et al. 1986). Recently, a Coomassie Blue-affinity glycoprotein, “Micropyler Sperm Attractant” (MSA), around the opening and inside of the micropyle of herring and flounder eggs has been identified that guides (“attract”) the spermatozoa into the micropyle (Yanagimachi et al. 2013).

On the other hand, nonproteinaceous chemoattractants have been identified in coral and ascidians: the chemoattractant of the coral Montipora digitata is an unsaturated fatty alcohol (Coll et al. 1994), and those of the ascidians Ciona intestinalis and Ascidia sydneiensis (Yoshida et al. 2002; Matsumori et al. 2013) are sulfated hydroxysterols. Mammalian spermatozoa also show chemotactic behavior, and many candidate chemoattractants for spermatozoa have been proposed (Eisenbach and Giojalas 2006). Recently, progesterone released from the cumulus oophorus was considered as a candidate of sperm attractant for human sperm (Guidobaldi et al. 2008). On the other hand, odorants such as bourgeonal (Spehr et al. 2003) and lyral (Fukuda et al. 2004), which are aromatic aldehydes used in perfumes, could also act as chemoattractants in human and mouse sperm, respectively.

Where are the sperm chemoattractants released? Fern sperms show a chemotactic response to secretions from the female reproductive structures (Pfeffer 1884). Sperm attractants of sea urchins and sea stars (starfish) are derived from the egg jelly (Ward et al. 1985; Nishigaki et al. 1996), and the source of sperm attractant of the hydrozoan, the siphonophore, is a cupule, the extracellular structure of the egg (Carré and Sardet 1981). Therefore, sperm attractants are released from the egg accessory organs or female gametes in these species. In contrast, in ascidians, sperm-attracting activity does not originate from the overall egg coat as a layer of jelly surrounding the eggs, but originates from the egg (Yoshida et al. 1993), indicating that the eggs themselves release the chemoattractant for the sperm.

In all examples of well-characterized chemotaxis, the intracellular Ca²⁺ concentration ([Ca²⁺] _i ) appears to be a common element of absolute necessity in the attraction mechanism (Kaupp et al. 2008; Yoshida and Yoshida 2011). Ca²⁺ plays a key role in the regulation of flagellar beating, and in the case of sea urchin spermatozoa, the sperm attractant triggers [Ca²⁺] _i fluctuations (Böhmer et al. 2005; Wood et al. 2005) that appear to correlate with the asymmetrical beating of sperm flagella (Brokaw et al. 1974; Brokaw 1979). In the hydrozoan siphonophore s, the diameters of the sperm trajectories decrease on approach of the sperm to the cupule (a sperm-attracting accessory organ of the egg), but the sperm trajectories are unchanged in the absence of Ca²⁺ (Cosson et al. 1984). A similar role for extracellular Ca²⁺ in mediating flagellar asymmetry of the spermatozoon during chemotactic behavior has been reported in hydrozoa (Miller and Brokaw 1970; Cosson et al. 1984). In ascidians, the spermatozoa normally exhibit circular movements, as just described, and maintain [Ca²⁺] _i at very low levels (Shiba et al. 2008). During chemotactic behavior the spermatozoa produce frequent and transient increases of [Ca²⁺] _i in the flagella (Ca²⁺ bursts) (Shiba et al. 2008). Interestingly, the Ca²⁺ bursts are consistently evoked at points at which the spermatozoon is around a temporally minimal value for a given sperm-activating and sperm-attracting factor (SAAF) concentration (Shiba et al. 2008) and to trigger a sequence of “turn-and-straight” movements. These data suggest that sperm attractants induce Ca²⁺ entry from extracellular spaces into the sperm cell, and the resultant increase in [Ca²⁺] _i mediates the beating of sperm flagella, resulting in chemotactic “turn-and-straight” movements.

As described here, the molecular structures of sperm chemoattractants are different in different species, and factors from one species cannot attract the sperm of another species. This specificity ensures species-specific fertilization by preventing crossbreeding. Species or genus specificity in sperm chemotaxis has been observed in hydrozoa (Miller 1979) and in echinoderms, other than sea urchins (Miller 1985a, 1997). However, no chemotactic cross-reactivity exists in siphonophore species examined, and contact with seawater without attractants is enough to activate sperm motility, although the presence of Ca²⁺ ions in seawater is involved in the chemo-attraction process (Cosson 1990). Mammalian species also seem to share a common sperm attractant molecule (Sun et al. 2003; Guidobaldi et al. 2008; Teves et al. 2006), suggesting the lack of species specificity. In Mollusca, even though the abalone species seem to show species specificity in sperm chemotaxis (Riffell et al. 2004), there is a lack of species specificity of sperm chemotaxis among chitons (Miller 1977).