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A Tale of Two Cells: Endocannabinoid-Signaling Regulates Functions of Neurons and Sperm¹

Division of Anatomy & Cell Biology,³ Department of Pathology & Anatomical Sciences Department of Gynecology & Obstetrics,⁴ School of Medicine & Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York 14214

Sea urchin and human sperm contain receptors for neurotransmitters and psychoactive drugs, including cannabinoid receptors (CNRs). Anandamide, arachidonoylethanolamide (AEA), is a lipid-signal molecule that is an endogenous agonist for CNRs. AEA is enyzmatically released from membrane phospholipids when neurons are stimulated. Retrograde AEA signals from depolarized postsynaptic neurons inhibit neurotransmitter release at synapses in mammalian brain. Analogous processes regulate sperm functions during fertilization in sea urchins. AEA and (–)9tetrahydrocannabinol [(–)9THC], the major psychoactive constituent of marijuana, inhibit fertilization by blocking acrosomal exocytosis/acrosome reactions (AR) stimulated by egg jelly. The acrosome is a Golgi-derived secretory granule in sperm analogous to synaptic vesicles in neurons. AEA and (–)9THC do not block ionophore-induced AR, suggesting that they inhibit AR by modulating signal transduction event(s) before opening of ion channels. Unfertilized sea urchin eggs have enzymes required to release AEA from membrane phospholipids. These results indicate that sea urchin eggs may release AEA after activation by the fertilizing sperm. Released AEA may then react with CNRs in nearby sperm to block AR, thereby helping to prevent polyspermy. AEA is present in human seminal plasma, midcycle oviductal fluid, and follicular fluid. Sperm are sequentially exposed to these fluids as they move from the vagina to the site of fertilization in the oviduct. R-methanandamide (AM-356), a metabolically stable AEA analog, and (–)9THC modulate capacitation and fertilizing potential of human sperm in vitro. These findings suggest that AEA signaling directly affects sperm functions required for fertilization and provide additional evidence for common signaling processes in neurons and sperm.

acrosome reaction, anandamide, cannabinoid receptors, capacitation, fertilization, hyperactivated motility, neurotransmitters, signal transduction, sperm, synaptic vesicles

² Correspondence: Herbert Schuel, Division of Anatomy and Cell Biology, Department of Pathology and Anatomical Sciences, School of Medicine and Biomedical Sciences, 206 Farber Hall, University at Buffalo, SUNY, Buffalo, NY 14214. FAX: 716 829 2911; schuel{at}acsu.buffalo.edu

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