Phospholipid methylation in starfish spermatozoa is linked to sperm chemoattraction.

Abstract

The mechanism whereby ovarian peptides cause sperm attraction was studied in the starfish. Phospholipid methylation and protein-O-carboxyl methylation, reactions linked to chemotactic responses in a variety of systems, were studied in starfish sperm. When sperm were preincubated with [methyl-3H]methionine and then exposed to the attractant, a rapid drop in radioactivity occurred in the phospholipid fraction. Methylated phospholipids decreased by 90% in the first 2 sec; however, no change was observed in endogenous methylation of protein carboxyl groups. The effect on phospholipid methylation was dose dependent, with a 40% reduction in radioactive phospholipids in sperm occurring with the minimal amount of attractant necessary to obtain a positive response in a sperm attraction bioassay. Attractants from species of starfish with little or no cross-reactivity in the bioassay had a limited effect on phospholipid methylation. The transmethylase inhibitor, homocysteine, caused a marked decrease in the accumulation of methylated phospholipids under basal conditions, which was correlated with as much as a 50-fold increase in sperm sensitivity to the attractant. The addition of chemoattractant resulted in a reduction in the amount of all individual methylated phospholipids, but the amount of phosphatidylmono[3H]methylethanolamine relative to the other methylated phospholipid decreased by a factor of 4 after stimulation. Homocysteine had the same effect. The reduction in methylated phospholipids by attractants suggests that phospholipid methylation is linked to the mechanism of action of these peptides. Methylation of phospholipids may play a role in the rapid desensitization of sperm cells to the attractant, which would be required for the orientation of the spermatozoa in the gradient of ovarian peptide.Sperm chemotaxis has been demonstrated in Asteroidea, a major class ofechinoderms (1). The substance responsible for the attraction is produced by the ovaries and is of low molecular weight, highly polar, sensitive to proteases, and stable to heat and acid (T. Punnett and R.L.M., unpublished data). The affected spermatozoa swim up a gradient of the chemoattractant, which is specific at least at the family level in starfish. This response leads to more efficient and appropriate sperm-egg interaction in the open sea, where fertilization normally takes place in these animals. However, the mechanism by which these attractants exert their effect on sperm is not known.Transmethylase reactions are involved in a variety of chemotactic responses (for review, see ref.2). In bacteria, membrane-associated proteins are methylated by a proteincarboxyl methyltransferase as a requirement for chemotaxis (3,4). Many cells such as cellular slime molds (5), guinea pig macrophages (6), and rabbit neutrophils (2) exhibit changes in the phospholipid composition of the plasma membrane consistent with the activation of phospholipid methyltransferases after exposure to specific attractants. Because of the well-known involvement of transm...

Regulation of sperm flagellar motility by calcium and cAMP‐dependent phosphorylation

“…Exposure of spermatozoa to the chemoattractant peptides caused a large decrease in phospholipid methylation, leading to suggestions that phospholipid methylation may be important in the response to temporal changes in receptor occupancy [54]. …”

Metabolism of unusual membrane phospholipids in the marine sponge Microciona prolifera

“…Although the major pathways of phospholipid biosynthesis are well established in both prokaryotes and eukaryotes (Vance & Vance, 1985; Hawthorne & Ansell, 1982; Mudd, 1980), extensive efforts are still being directed to the study of phospholipid class interconversion. for instance the methylation of PE to PC.1 0006-2960/91 /0430-372S02.50/0 © 1991 American Chemical Society Investigations have been carried out on a variety of cells and organisms, including Escherichia coli (Jackson et al, 1986), yeast (Carman, 1989), a slime mold (Alemany et al, 1980), crustaceans (Chapelle, 1986, starfish spermatozoa (Tezon et al, 1986), mammalian erythrocytes (Hirata & Axelrod, 1978a,b), leukocytes (Hirata et al, 1979;Pike et al, 1979), and hepatocytes (Ridgway et al, 1989;Sundler & Akesson, 1975) . The general perception is that phospholipid methylation and turnover, next to de novo biosynthesis, are highly regulated processes vital to the adjustment of membrane fluidity, biosignaling, and chemotaxis.…”