Neurosensory perception of environmental cues modulates sperm motility critical for fertilization.
Environmental exposures affect gamete function and fertility, but the mechanisms are poorly understood. Here, we show that pheromones sensed by ciliated neurons in the Caenorhabditis elegans nose alter the lipid microenvironment within the oviduct, thereby affecting sperm motility. In favorable environments, pheromone-responsive sensory neurons secrete a transforming growth factor-β ligand called DAF-7, which acts as a neuroendocrine factor that stimulates prostaglandin-endoperoxide synthase [cyclooxygenase (Cox)]-independent prostaglandin synthesis in the ovary. Oocytes secrete F-class prostaglandins that guide sperm toward them. These prostaglandins are also synthesized in Cox knockout mice, raising the possibility that similar mechanisms exist in other animals. Our data indicate that environmental cues perceived by the female nervous system affect sperm function.
Division of Reproductive Endocrinology and Infertility, Department of Obstetrics and Gynecology, University of Alabama at Birmingham, Birmingham, AL 35294, USA.
Katherine
K
McKnight
Department of Cell, Developmental and Integrative Biology, University of Alabama at Birmingham, Birmingham, AL 35294, USA.
Hieu D
HD
Hoang
Department of Pharmacology and Toxicology, University of Alabama at Birmingham, Birmingham, AL 35294, USA.
Jeevan K
JK
Prasain
Department of Pediatrics, Vanderbilt University, Nashville, TN 37232, USA.
Naoko
N
Brown
Department of Cell, Developmental and Integrative Biology, University of Alabama at Birmingham, Birmingham, AL 35294, USA.
Jack
J
Vibbert
Department of Chemistry, Louisiana State University, Baton Rouge, LA 70803, USA.
Kyle A
KA
Hollister
Department of Pharmacology and Toxicology, University of Alabama at Birmingham, Birmingham, AL 35294, USA.
Ray
R
Moore
Department of Chemistry, Louisiana State University, Baton Rouge, LA 70803, USA.
Justin R
JR
Ragains
Department of Pediatrics, Vanderbilt University, Nashville, TN 37232, USA. Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN 37232, USA.
Jeff
J
Reese
Department of Cell, Developmental and Integrative Biology, University of Alabama at Birmingham, Birmingham, AL 35294, USA. mamiller@uab.edu.
Michael A
MA
Miller
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D004781:Environmental Exposure; D005260:Female; D005306:Fertilization; D008297:Male; D009475:Neurons, Afferent / Q000502:physiology*; D009490:Neurosecretory Systems / Q000502:physiology; D009865:Oocytes / Q000378:metabolism / Q000502:physiology; D010063:Ovum / Q000378:metabolism / Q000502:physiology; D010465:Perception; D010675:Pheromones / Q000502:physiology*; D011451:Prostaglandin-Endoperoxide Synthases / Q000378:metabolism; D011453:Prostaglandins / Q000096:biosynthesis; D013081:Sperm Motility; D013094:Spermatozoa / Q000502:physiology*; D016212:Transforming Growth Factor beta / Q000235:genetics / Q000378:metabolism*
D029742:Caenorhabditis elegans Proteins; C102095:DAF-7 protein, C elegans; D010675:Pheromones; D011453:Prostaglandins; D016212:Transforming Growth Factor beta; D011451:Prostaglandin-Endoperoxide Synthases