Ionic regulation of sea urchin sperm motility, metabolism and fertilizing capacity.

J Physiol. 1986 October; 379: 347–365.

PMCID: PMC1182901

R Christen, R W Schackmann, and B M Shapiro

Abstract

In order to pursue the significance of the ionic regulation of sea urchin sperm behaviour, alterations in the cation composition of sea water were tested for their effects on sperm fertilizing capacity. Nearly all changes which resulted in lowered sperm intracellular pH, including lowered sea-water pH, inclusion of the divalent ion chelator EGTA, addition of dithiothreitol, or removal of sea-water Na+, enhanced sperm viability for periods of up to a week. These conditions caused decreased cell motility and elevated ATP concentrations, and prevented the acrosome reaction. Conversely, changes which increased the intracellular pH, decreased sperm ATP concentrations, or induced the acrosome reaction, reduced sperm viability. A single medium, high sea-water K+ concentrations (greater than 100 mM), provided an exception to these general trends. At elevated K+ concentrations sperm were quiescent but became completely infertile. These data show that sperm fertilizing capacity is generally extended by maintenance of the sperm in an inactive state, and the results suggest that decreased cellular energy levels contribute to decreased fertility.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

Ackerman, JJ; Grove, TH; Wong, GG; Gadian, DG; Radda, GK. Mapping of metabolites in whole animals by 31P NMR using surface coils. Nature. 1980 Jan 10;283(5743):167–170. [PubMed]
Barak, LS; Nothnagel, EA; DeMarco, EF; Webb, WW. Differential staining of actin in metaphase spindles with 7-nitrobenz-2-oxa-1,3-diazole-phallacidin and fluorescent DNase: is actin involved in chromosomal movement? Proc Natl Acad Sci U S A. 1981 May;78(5):3034–3038. [PubMed]
Chance, B; Eleff, S; Leigh, JS, Jr; Sokolow, D; Sapega, A. Mitochondrial regulation of phosphocreatine/inorganic phosphate ratios in exercising human muscle: a gated 31P NMR study. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6714–6718. [PubMed]
CHANCE, B; WILLIAMS, GR. Respiratory enzymes in oxidative phosphorylation. IV. The respiratory chain. J Biol Chem. 1955 Nov;217(1):429–438. [PubMed]
CHANCE, B; WILLIAMS, GR. The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Subj Biochem. 1956;17:65–134. [PubMed]
Christen, R; Sardet, C. Changes in permeability of sea urchin egg membrane to urea after fertilization or activation. J Physiol. 1980 Aug;305:1–11. [PubMed]
Christen, R; Schackmann, RW; Shapiro, BM. Elevation of the intracellular pH activates respiration and motility of sperm of the sea urchin, Strongylocentrotus purpuratus. J Biol Chem. 1982 Dec 25;257(24):14881–14890. [PubMed]
Christen, R; Schackmann, RW; Shapiro, BM. Metabolism of sea urchin sperm. Interrelationships between intracellular pH, ATPase activity, and mitochondrial respiration. J Biol Chem. 1983 May 10;258(9):5392–5399. [PubMed]
Christen, R; Schackmann, RW; Dahlquist, FW; Shapiro, BM. 31P-NMR analysis of sea urchin sperm activation. Reversible formation of high energy phosphate compounds by changes in intracellular pH. Exp Cell Res. 1983 Nov;149(1):289–294. [PubMed]
Christen, R; Schackmann, RW; Shapiro, BM. Interactions between sperm and sea urchin egg jelly. Dev Biol. 1983 Jul;98(1):1–14. [PubMed]
Clapper, DL; Brown, GG. Sperm motility in the horseshoe crab, Limulus polyphemus L. II. Partial characterization of a motility initiating factor from eggs and the effects of inorganic cations on motility initiation. Dev Biol. 1980 May;76(2):350–357. [PubMed]
Collins, F; Epel, D. The role of calcium ions in the acrosome reaction of sea urchin sperm: regulation of exocytosis. Exp Cell Res. 1977 Apr;106(1):211–222. [PubMed]
Dawson, MJ; Gadian, DG; Wilkie, DR. Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature. 1978 Aug 31;274(5674):861–866. [PubMed]
Decker, GL; Joseph, DB; Lennarz, WJ. A study of factors involved in induction of the acrosomal reaction in sperm of the sea urchin, Arbacia punctulata. Dev Biol. 1976 Oct 1;53(1):115–125. [PubMed]
Fossel, ET; Morgan, HE; Ingwall, JS. Measurement of changes in high-energy phosphates in the cardiac cycle using gated 31P nuclear magnetic renonance. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3654–3658. [PubMed]
Gatti, JL; Christen, R. Regulation of internal pH of sea urchin sperm. A role for the Na/K pump. J Biol Chem. 1985 Jun 25;260(12):7599–7602. [PubMed]
Gibbons, BH; Gibbons, IR. Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100. J Cell Biol. 1972 Jul;54(1):75–97. [PubMed]
Gibbons, BH; Gibbons, IR. The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm. J Cell Sci. 1973 Sep;13(2):337–357. [PubMed]
Hassinen, IE; Hiltunen, K. Respiratory control in isolated perfused rat heart. Role of the equilibrium relations between the mitochondrial electron carriers and the adenylate system. Biochim Biophys Acta. 1975 Dec 11;408(3):319–330. [PubMed]
Hiltunen, JK; Hassinen, IE. Energy-linked regulation of glucose and pyruvate oxidation in isolated perfused rat heart. Role of pyruvate dehydrogenase. Biochim Biophys Acta. 1976 Aug 13;440(2):377–390. [PubMed]
Illingworth, JA; Ford, WC; Kobayashi, K; Williamson, JR. Regulation of myocardial energy metabolism. Recent Adv Stud Cardiac Struct Metab. 1975;8:271–290. [PubMed]
Johnson, CH; Epel, D. Heavy metal chelators prolong motility and viability of sea urchin sperm by inhibiting spontaneous acrosome reactions. J Exp Zool. 1983 Jun;226(3):431–440. [PubMed]
Johnson, JD; Epel, D. Intracellular pH and activation of sea urchin eggs after fertilisation. Nature. 1976 Aug 19;262(5570):661–664. [PubMed]
Kinsey, WH; SeGall, GK; Lennarz, WJ. The effect of the acrosome reaction on the respiratory activity and fertilizing capacity of echinoid sperm. Dev Biol. 1979 Jul;71(1):49–59. [PubMed]
Lee, HC. A membrane potential-sensitive Na+-H+ exchange system in flagella isolated from sea urchin spermatozoa. J Biol Chem. 1984 Dec 25;259(24):15315–15319. [PubMed]
Lee, HC; Johnson, C; Epel, D. Changes in internal pH associated with initiation of motility and acrosome reaction of sea urchin sperm. Dev Biol. 1983 Jan;95(1):31–45. [PubMed]
LORENZ, FW; TYLER, A. Extension of motile life span of spermatozoa of the domestic fowl by amino acids and proteins. Proc Soc Exp Biol Med. 1951 Oct;78(1):57–62. [PubMed]
Matthews, PM; Bland, JL; Gadian, DG; Radda, GK. The steady-state rate of ATP synthesis in the perfused rat heart measured by 31P NMR saturation transfer. Biochem Biophys Res Commun. 1981 Dec 15;103(3):1052–1059. [PubMed]
Neely, JR; Whitmer, JT; Rovetto, MJ. Effect of coronary blood flow on glycolytic flux and intracellular pH in isolated rat hearts. Circ Res. 1975 Dec;37(6):733–741. [PubMed]
Nishiki, K; Erecińska, M; Wilson, DF. Energy relationships between cytosolic metabolism and mitochondrial respiration in rat heart. Am J Physiol. 1978 Mar;234(3):C73–C81. [PubMed]
Ohtake, H. Respiratory behaviour of sea-urchin spermatozoa. I. Effect of pH and egg water on the respiratory rate. J Exp Zool. 1976 Dec;198(3):303–311. [PubMed]
Opie, LH; Mansford, KR; Owen, P. Effects of increased heart work on glycolysis and adenine nucleotides in the perfused heart of normal and diabetic rats. Biochem J. 1971 Sep;124(3):475–490. [PubMed]
Ridgway, EB; Gilkey, JC; Jaffe, LF. Free calcium increases explosively in activating medaka eggs. Proc Natl Acad Sci U S A. 1977 Feb;74(2):623–627. [PubMed]
Robillard, GT; Konings, WN. Physical mechanism for regulation of phosphoenolpyruvate-dependent glucose transport activity in Escherichia coli. Biochemistry. 1981 Aug 18;20(17):5025–5032. [PubMed]
Schackmann, RW; Christen, R; Shapiro, BM. Membrane potential depolarization and increased intracellular pH accompany the acrosome reaction of sea urchin sperm. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6066–6070. [PubMed]
Schackmann, RW; Eddy, EM; Shapiro, BM. The acrosome reaction of Strongylocentrotus purpuratus sperm. Ion requirements and movements. Dev Biol. 1978 Aug;65(2):483–495. [PubMed]
Schackmann, RW; Shapiro, BM. A partial sequence of ionic changes associated with the acrosome reaction of Strongylocentrotus purpuratus. Dev Biol. 1981 Jan 15;81(1):145–154. [PubMed]
Shen, SS; Steinhardt, RA. Intracellular pH and the sodium requirement at fertilisation. Nature. 1979 Nov 1;282(5734):87–89. [PubMed]
Steinhardt, R; Zucker, R; Schatten, G. Intracellular calcium release at fertilization in the sea urchin egg. Dev Biol. 1977 Jul 1;58(1):185–196. [PubMed]
Tilney, LG; Kiehart, DP; Sardet, C; Tilney, M. Polymerization of actin. IV. Role of Ca++ and H+ in the assembly of actin and in membrane fusion in the acrosomal reaction of echinoderm sperm. J Cell Biol. 1978 May;77(2):536–550. [PubMed]
Timourian, H; Watchmaker, G. Determination of spermatozoan motility. Dev Biol. 1970 Feb;21(1):62–72. [PubMed]
Tombes, RM; Shapiro, BM. Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondrion and tail. Cell. 1985 May;41(1):325–334. [PubMed]
Vincent, A; Blair, JM. The coupling of the adenylate kinase and creatine kinase equilibria. Calculation of substrate and feedback signal levels in muscle. FEBS Lett. 1970 Apr 16;7(3):239–244. [PubMed]
Williamson, JR. Mitochondrial function in the heart. Annu Rev Physiol. 1979;41:485–506. [PubMed]
Yoshioka, T; Inoue, H. High potassium effect on the mobility of sea urchin sperm. Nagoya J Med Sci. 1980 Mar;42(3-4):82–84. [PubMed]