Chemerin Impairs In Vitro Testosterone Production, Sperm Motility, and Fertility in Chicken: Possible Involvement of Its Receptor CMKLR1

Abstract

<jats:p>The chemokine chemerin is a novel adipokine involved in the regulation of energy metabolism but also female reproductive functions in mammals. Its effects on male fertility are less studied. Here, we investigated the involvement of chemerin in chicken male reproduction. Indeed, the improvement of the sperm of roosters is a challenge for the breeders since the sperm quantity and quality have largely decreased for several years. By using specific chicken antibodies, here we show that chemerin and its main receptor CMKLR1 (chemokine-like receptor 1) are expressed within the chicken testis with the lowest expression in adults as compared to the embryo or postnatal stages. Chemerin and CMKLR1 are present in all testicular cells, including Leydig, Sertoli, and germinal cells. Using in vitro testis explants, we observed that recombinant chicken chemerin through CMKLR1 inhibits hCG (human chorionic gonadotropin) stimulated testosterone production and this was associated to lower 3βHSD (3beta-hydroxysteroid dehydrogenase) and StAR (steroidogenic acute regulatory protein) expression and MAPK ERK2 (Mitogen-Activated Protein Kinase Extracellular signal-regulated kinase 2) phosphorylation. Furthermore, we demonstrate that chemerin in seminal plasma is lower than in blood plasma, but it is negatively correlated with the percentage of motility and the spermatozoa concentration in vivo in roosters. In vitro, we show that recombinant chicken chemerin reduces sperm mass and individual motility in roosters, and this effect is abolished when sperm is pre-incubated with an anti-CMKLR1 antibody. Moreover, we demonstrate that fresh chicken sperm treated with chemerin and used for artificial insemination (AI) in hen presented a lower efficiency in terms of eggs fertility for the four first days after AI. Taken together, seminal chemerin levels are negatively associated with the rooster fertility, and chemerin produced locally by the testis or male tract could negatively affect in vivo sperm quality and testosterone production through CMKLR1.</jats:p>

Diabetes and Obesity—Cumulative or Complementary Effects On Adipokines, Inflammation, and Insulin Resistance

“…CMKLR1 is expressed mainly in adipose tissue (higher levels in white compared to brown adipose tissue), bone, lung, brain, heart, and placenta [55,59]. Chemerin binds to orphan CMKLR1 [24,60], activates the three Gαi subtypes, and the two Gαo isoform [56], exercising in this way main biological functions [57,60]. CMKLR1 activation is responsible for intracellular calcium release and a reduction in cAMP (cyclic adenosine monophosphate) accumulation [59].…”

Chemerin is secreted by the chicken oviduct, accumulates in egg albumen and could promote embryo development

“…In chickens, our team demonstrated that plasma chemerin concentrations were negatively associated with egg hatchability, suggesting a potential role of this adipokine on egg and/or embryo development 22 . After in vivo experiments on fresh rooster sperm incubated with recombinant chicken chemerin and used for artificial insemination (AI), we observed a negative effect of chemerin on egg fertility for the first 3 days after AI, suggesting an impact of this hormone on early embryo development (EED) 23 . In addition, in turkeys, we found that chemerin expression in granulosa cells increases in the mature follicle immediately before ovulation, thus, potentially influencing EED 20 .…”

Adipokines in metabolic and reproductive functions in birds: An overview of current knowns and unknowns

“…Like mammals, chemerin and its main receptor CMKLR1 are present in chicken testes with the lowest expression for adult chicken compared to immature animals (Estienne et al, 2020b). Estienne et al have shown that in vitro recombinant chicken chemerin reduced motility of spermatozoa and inhibits testosterone production bythe testes (Estienne et al, 2020b).…”

“…Like mammals, chemerin and its main receptor CMKLR1 are present in chicken testes with the lowest expression for adult chicken compared to immature animals (Estienne et al, 2020b). Estienne et al have shown that in vitro recombinant chicken chemerin reduced motility of spermatozoa and inhibits testosterone production bythe testes (Estienne et al, 2020b). They demonstrated that chemerin seminal plasma concentration but not chemerin blood plasma was negatively correlated with spermatozoa concentration and motility in vivo in chicken sperm.…”