Chemerin Abundance in Egg White and Its Expression with Receptors in Extra-embryonic Annexes of Pekin Ducks: Implications for Embryo Development

Overview

Journal Poult Sci

Publisher Elsevier

Specialty Veterinary Medicine

Date 2024 Jul 13

PMID 39002372

Authors

Bernardi Ophelie

Rame Christelle

Reverchon Maxime

Rouger Romuald

Dupont Joelle

Affiliations

Soon will be listed here.

Abstract

Embryonic mortality is a significant problem in the commercial duck industry worldwide. Therefore, identification of new biomarkers for duck embryo development is necessary. In the chicken (order Galliformes), we previously showed that chemerin is a hormone locally produced by the reproductive tract in hens, particularly in the magnum area, leading to its accumulation in the egg white and within the embryo annexes during embryonic development. We therefore hypothesized that the chemerin concentration in egg white could be a biomarker of egg performance and reproductive parameters in Pekin ducks (order Anseriformes). Thus, we collected eggs from Pekin ducks over a 5-d period at three stages of the laying period (before the laying peak, after the laying peak, and at the end of the laying period) to measure the chemerin concentrations in egg white by enzyme-linked immunosorbent assay. The chemerin concentration in egg white decreased during the laying period and was not associated with reproductive parameters. We found negative correlations between the chemerin level in egg white and the albumen weight. Reverse-transcriptase quantitative polymerase chain reaction showed that chemerin and its three receptors CMKLR1, GPR1, and CCRL2 were expressed in the reproductive tract and within allantoic and amniotic annexes during embryo development. Chemerin concentrations strongly increased in amniotic fluid on embryonic day 16 (ED16) when the egg white was transferred into the amniotic sac. Finally, chemerin inhibition in egg white by in ovo injections of anti-chemerin antibodies (0.01, 0.1, and 1 µg) increased the embryo mortality rate. These data demonstrate the important role of the chemerin system during egg formation and embryo development in Pekin ducks, suggesting their potential use as biomarkers for determining the quality of poultry eggs and embryo development.

References

Mann K . The chicken egg white proteome. Proteomics. 2007; 7(19):3558-68. DOI: 10.1002/pmic.200700397. View

Mellouk N, Rame C, Delaveau J, Rat C, Marchand M, Mercerand F . Food restriction but not fish oil increases fertility in hens: role of RARRES2?. Reproduction. 2018; 155(4):321-331. DOI: 10.1530/REP-17-0678. View

Estienne A, Brossaud A, Reverchon M, Rame C, Froment P, Dupont J . Adipokines Expression and Effects in Oocyte Maturation, Fertilization and Early Embryo Development: Lessons from Mammals and Birds. Int J Mol Sci. 2020; 21(10). PMC: 7279299. DOI: 10.3390/ijms21103581. View

Bernardi O, Freville M, Rame C, Reverchon M, Dupont J . Chemerin concentration in egg white in layer and broiler hens during the laying period for 2 successive generations. Poult Sci. 2023; 103(2):103342. PMC: 10784314. DOI: 10.1016/j.psj.2023.103342. View

Legros J, Jan S, Bonnassie S, Gautier M, Croguennec T, Pezennec S . The Role of Ovotransferrin in Egg-White Antimicrobial Activity: A Review. Foods. 2021; 10(4). PMC: 8070150. DOI: 10.3390/foods10040823. View

De Henau O, Degroot G, Imbault V, Robert V, De Poorter C, Mcheik S . Signaling Properties of Chemerin Receptors CMKLR1, GPR1 and CCRL2. PLoS One. 2016; 11(10):e0164179. PMC: 5055294. DOI: 10.1371/journal.pone.0164179. View

Bernardi O, Estienne A, Reverchon M, Bigot Y, Froment P, Dupont J . Adipokines in metabolic and reproductive functions in birds: An overview of current knowns and unknowns. Mol Cell Endocrinol. 2021; 534:111370. DOI: 10.1016/j.mce.2021.111370. View

WYBURN G, Johnston H, DRAPER M, Davidson M . The fine structure of the infundibulum and magnum of the oviduct of Gallus domesticus. Q J Exp Physiol Cogn Med Sci. 1970; 55(3):213-32. DOI: 10.1113/expphysiol.1970.sp002071. View

Estienne A, Brossaud A, Rame C, Bernardi O, Reverchon M, Rat C . Chemerin is secreted by the chicken oviduct, accumulates in egg albumen and could promote embryo development. Sci Rep. 2022; 12(1):8989. PMC: 9148909. DOI: 10.1038/s41598-022-12961-4. View

10.

Zhang X, Wu M, Wang S, Zhang H, Du Z, Li Y . Genetic selection on abdominal fat content alters the reproductive performance of broilers. Animal. 2017; 12(6):1232-1241. DOI: 10.1017/S1751731117002658. View

11.

Bernardi O, Rame C, Reverchon M, Dupont J . Expression of chemerin and its receptors in extra-embryonic annexes and role of chemerin and its GPR1 receptor in embryo development in layer and broiler hens. Poult Sci. 2023; 103(2):103339. PMC: 10753086. DOI: 10.1016/j.psj.2023.103339. View

12.

Mellouk N, Rame C, Barbe A, Grandhaye J, Froment P, Dupont J . Chicken Is a Useful Model to Investigate the Role of Adipokines in Metabolic and Reproductive Diseases. Int J Endocrinol. 2018; 2018:4579734. PMC: 6029501. DOI: 10.1155/2018/4579734. View

13.

Estienne A, Rame C, Ganier P, Chahnamian M, Barbe A, Grandhaye J . Chemerin impairs food intake and body weight in chicken: Focus on hypothalamic neuropeptides gene expression and AMPK signaling pathway. Gen Comp Endocrinol. 2021; 304:113721. DOI: 10.1016/j.ygcen.2021.113721. View

14.

Mattern A, Zellmann T, Beck-Sickinger A . Processing, signaling, and physiological function of chemerin. IUBMB Life. 2014; 66(1):19-26. DOI: 10.1002/iub.1242. View

15.

Richards M, Proszkowiec-Weglarz M . Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult Sci. 2007; 86(7):1478-90. DOI: 10.1093/ps/86.7.1478. View

16.

Wang J, Liang Y, Omana D, Kav N, Wu J . Proteomics analysis of egg white proteins from different egg varieties. J Agric Food Chem. 2011; 60(1):272-82. DOI: 10.1021/jf2033973. View

17.

Bernardi O, Reverchon M, Estienne A, Baumard Y, Rame C, Brossaud A . Chicken white egg chemerin as a tool for genetic selection for egg weight and hen fertility. Front Physiol. 2022; 13:1012212. PMC: 9513417. DOI: 10.3389/fphys.2022.1012212. View

18.

Yoshizaki N, Ito Y, Hori H, Saito H, Iwasawa A . Absorption, transportation and digestion of egg white in quail embryos. Dev Growth Differ. 2002; 44(1):11-22. DOI: 10.1046/j.1440-169x.2002.00620.x. View

19.

Jeong W, Lim W, Kim J, Ahn S, Lee H, Jeong J . Cell-specific and temporal aspects of gene expression in the chicken oviduct at different stages of the laying cycle. Biol Reprod. 2012; 86(6):172. DOI: 10.1095/biolreprod.111.098186. View

20.

Estienne A, Bernardi O, Rame C, Reverchon M, Tricoire S, Froment P . The influence of selection in wild pheasant (Phasianus colchicus) breeding on reproduction and the involvement of the chemerin system. Poult Sci. 2022; 102(1):102248. PMC: 9692031. DOI: 10.1016/j.psj.2022.102248. View