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The expression of chemerin and its receptors (CMKLR1, GPR1, CCRL2) in the porcine uterus during the oestrous cycle and early pregnancy and in trophoblasts and conceptuses

Published online by Cambridge University Press:  13 May 2020

M. Gudelska ,
K. Dobrzyn ,
M. Kiezun ,
E. Rytelewska ,
K. Kisielewska ,
B. Kaminska ,
T. Kaminski  and
N. Smolinska Open the ORCID record for N. Smolinska [Opens in a new window]
M. Gudelska
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
K. Dobrzyn
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
M. Kiezun
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
E. Rytelewska
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
K. Kisielewska
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
B. Kaminska
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
T. Kaminski
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
N. Smolinska*
Affiliation:
Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland
*
†E-mail: nina.smolinska@uwm.edu.pl
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Abstract

Recent research has demonstrated that chemerin may take part in the regulation of reproduction. The aim of this study was to determine the expression of chemerin system – chemerin and its receptors, chemokine-like receptor 1 (CMKLR1), G protein-coupled receptor 1 (GPR1) and C-C chemokine receptor-like 2 (CCRL2) – in the porcine uterus during the oestrous cycle and early pregnancy, and in trophoblasts and conceptuses by real-time PCR and western blotting. Chemerin concentrations in uterine luminal flushings (ULF) were determined using ELISA test. In the endometrium, the highest expression of chemerin and GPR1 proteins was observed during the mid-luteal phase; CMKLR1, during the late luteal phase; and CCRL2, during the follicular phase of the cycle. In the myometrium, chemerin protein expression was enhanced during the early luteal phase, and chemerin receptor proteins were highly expressed during the follicular phase. In the endometrium of pregnant pigs, the highest expression of chemerin and CCRL2 protein was observed during implantation; CMKLR1, during placentation; and GPR1, during embryo migration. In the myometrium, chemerin and CCRL2 protein expression increased at the end of implantation, and the expression of CMKLR1 and GPR1 protein was enhanced during implantation. In the conceptuses and trophoblasts, the highest expression of chemerin system proteins was observed during placentation, with the exception of GPR1 protein in the trophoblasts. The highest concentrations of the analysed adipokine were observed in ULF during the luteal phase of the cycle and during maternal recognition of pregnancy. This is the first study to demonstrate that the expression of the chemerin system in the porcine uterus, conceptuses and trophoblasts, and chemerin concentrations in ULF are influenced by the hormonal milieu in different stages of the oestrous cycle and in early pregnancy. The present results also suggest that chemerin is implicated in the regulation of reproductive functions in pigs.

Keywords

adipokineendometriummyometriumembryopig
Type
Research Article
Information
animal , Volume 14 , Issue 10 , October 2020 , pp. 2116 - 2128
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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References

Akins, EL and Morrissette, MC 1968. Gross ovarian changes during estrous cycle of swine. American Journal of Veterinary Research 29, 1953–1957.Google ScholarPubMed
Anderson, LL 1978. Growth, protein content and distribution of early pig embryos. Anatomical Record 190, 143–153.CrossRefGoogle ScholarPubMed
Anderson, LL 2009. Reproductive biology of pigs. Animal Industry Report AS 655, ASL R2443.CrossRefGoogle Scholar
Brunetti, L, Orlando, G, Ferrante, C, Recinella, L, Leone, S, Chiavaroli, A, Di Nisio, C, Shohreh, R, Manippa, F, Ricciuti, A and Vacca, M 2014. Peripheral chemerin administration modulates hypothalamic control of feeding. Peptides 51, 115–121.CrossRefGoogle ScholarPubMed
Carlino, C, Trotta, E, Stabile, H, Morrone, S, Bulla, R, Soriani, A, Iannitto, ML, Agostinis, C, Mocci, C, Minozzi, M, Aragona, C, Perniola, G, Tedesco, F, Sozzani, S, Santoni, A and Gismondi, A 2012. Chemerin regulates NK cell accumulation and endothelial cell morphogenesis in the decidua during early pregnancy. Journal of Clinical Endocrinology & Metabolism 97, 3603–3612.CrossRefGoogle ScholarPubMed
Carson, DD, Bagchi, I, Dey, SK, Enders, AC, Fazleabas, AT, Lessey, BA and Yoshinaga, K 2000. Embryo implantation. Developmental Biology 223, 217–237.CrossRefGoogle ScholarPubMed
De Henau, O, Degroot, GN, Imbault, V, Robert, V, De Poorter, C, Mcheik, S, Galés, C, Parmentier, M and Springael, JY 2016. Signaling properties of chemerin receptors CMKLR1, GPR1 and CCRL2. PLoS ONE 11, e0164179.CrossRefGoogle ScholarPubMed
Dobrzyn, K, Smolinska, N, Szeszko, K, Kiezun, M, Maleszka, A, Rytelewska, E and Kaminski, T 2017. Effect of progesterone on adiponectin system in the porcine uterus during early pregnancy. Journal of Animal Science 95, 338–352.Google ScholarPubMed
Du, XY, Zabel, BA, Myles, T, Allen, SJ, Handel, TM, Lee, PP, Butcher, EC and Leung, LL 2009. Regulation of chemerin bioactivity by plasma carboxypeptidase N, carboxypeptidase B (activated thrombin-activable fibrinolysis inhibitor), and platelets. Journal of Biological Chemistry 284, 751–758.CrossRefGoogle Scholar
Dunon, D, Piali, L and Imhof, BA 1996. To stick or not to stick: the new leukocyte homing paradigm. Current Opinion in Cell Biology 8, 714–723.CrossRefGoogle ScholarPubMed
Fazleabas, AT, Geisert, RD, Bazer, FW and Roberts, RM 1983. Relationship between release of plasminogen activator and estrogen by blastocysts and secretion of plasmin inhibitor by uterine endometrium in the pregnant pig. Biology of Reproduction 29, 225–238.CrossRefGoogle ScholarPubMed
Garces, MF, Sanchez, E, Acosta, BJ, Angel, E, Ruiz, AI, Rubio-Romero, JA, Dieguez, C, Nogueiras, R and Caminos, JE 2012. Expression and regulation of chemerin during rat pregnancy. Placenta 33, 373–378.CrossRefGoogle ScholarPubMed
Garces, MF, Sanchez, E, Ruíz-Parra, AI, Rubio-Romero, JA, Angel-Müller, E, Suarez, MA, Bohórquez, LF, Bravo, SB, Nogueiras, R, Diéguez, C and Caminos, JE 2013. Serum chemerin levels during normal human pregnancy. Peptides 42, 138–43.CrossRefGoogle ScholarPubMed
Geisert, RD, Brookbank, JW, Roberts, RM and Bazer, FW 1982. Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocyst during elongation on day 12 of pregnancy. Biology of Reproduction 27, 941–955.CrossRefGoogle ScholarPubMed
Geisert, RD, Zavy, MT, Moffatt, RJ, Blair, RM and Yellin, T 1990. Embryonic steroids and the establishment of pregnancy in pigs. Journal of Reproduction and Fertility - Supplement 40, 293–305.Google ScholarPubMed
Geisert, RD, Thatcher, WW and Renegar, RH 1981. Relationship between porcine blastocyst development and uterine secretions. Biology of Reproduction 24(suppl. 1), 122A.Google Scholar
Goralski, KB, McCarthy, TC, Hanniman, EA, Zabel, BA, Butcher, EC, Parlee, SD, Muruganandan, S and Sinal, CJ 2007. Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. Journal of Biological Chemistry 282, 28175–28188.CrossRefGoogle ScholarPubMed
Gry, M, Rimini, R, Strömberg, S, Asplund, A, Pontén, F, Uhlén, M and Nilsson, P 2009. Correlations between RNA and protein expression profiles in 23 human cell lines. BMC Genomics 10, 365.CrossRefGoogle ScholarPubMed
Gygi, SP, Rochon, Y, Franza, BR and Aebersold, R 1999. Correlation between protein and mRNA abundance in yeast. Molecular and Cellular Biology 19, 1720–1730.CrossRefGoogle ScholarPubMed
Jin, CH, Yi, KW, Ha, YR, Shin, JH, Park, HT, Kim, T and Hur, JY 2015. Chemerin expression in the peritoneal fluid, serum, and ovarian endometrioma of women with endometriosis. American Journal of Reproductive Immunology 74, 379–386.CrossRefGoogle ScholarPubMed
Ka, H, Seo, H, Choi, Y, Yoo, I and Han, J 2018. Endometrial response to conceptus-derived estrogen and interleukin-1β at the time of implantation in pigs. Journal of Animal Science and Biotechnology 6, 9–44.Google Scholar
Kaeoket, K, Persson, E and Dalin, AM 2001. The sow endometrium at different stages of the oestrous cycle: studies on morphological changes and infiltration by cells of the immune system. Animal Reproduction Science 65, 95–114.CrossRefGoogle ScholarPubMed
Li, JJ, Bickel, PJ and Biggin, MD 2014. System wide analyses have underestimated protein abundances and the importance of transcription in mammals. PeerJ 2014, 1–26.Google Scholar
Lord, E, Ledoux, S, Murphy, BD, Beaudry, D and Palin, MF 2005. Expression of adiponectin and its receptors in swine. Journal of Animal Science 83, 565–578.CrossRefGoogle ScholarPubMed
Mattern, A, Zellmann, T and Beck-Sickinger, AG 2014. Processing, signaling, and physiological function of chemerin. International Union of Biochemistry and Molecular Biology Life 66, 19–26.CrossRefGoogle ScholarPubMed
Meder, W, Wendland, M, Busmann, A, Kutzleb, C, Spodsberg, N, John, H, Richter, R, Schleuder, D, Meyer, M and Forssman, WG 2003. Characterization of human circulating TIG2 as a ligand for the orphan receptor ChemR23. FEBS Letters 555, 495–499.CrossRefGoogle ScholarPubMed
Nitkiewicz, A, Smolinska, N, Maleszka, A, Kiezun, M and Kaminski, T 2012. Localization of orexin A and orexin B in the porcine uterus. Reproductive Biology 12, 135–155.CrossRefGoogle ScholarPubMed
Reverchon, M, Cornuau, M, Ramé, C, Guerif, F, Royère, D and Dupont, J 2012. Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells. Human Reproduction 27, 1790–1800.CrossRefGoogle ScholarPubMed
Reverchon, M, Ramé, C, Bertoldo, M and Dupont, J 2014. Adipokines and the female reproductive tract. International Journal of Endocrinology 2014, 232454.CrossRefGoogle ScholarPubMed
Rourke, JL, Dranse, HJ and Sinal, CJ 2015. CMKLR1 and GPR1 mediate chemerin signaling through the RhoA/ROCK pathway. Molecular and Cellular Endocrinology 417, 36–51.CrossRefGoogle ScholarPubMed
Salmi, M and Jalkanen, S 1997. How do lymphocytes know where to go: current concepts and enigmas of lymphocyte homing. Advances in Immunology 64, 139–217.CrossRefGoogle ScholarPubMed
Smolinska, N, Dobrzyn, K, Kiezun, M, Szeszko, K, Maleszka, A and Kaminski, T 2016. Effect of adiponectin on the steroidogenic acute regulatory protein, P450 side chain cleavage enzyme and 3β-hydroxysteroid dehydrogenase genes expression, progesterone and androstenedione production by the porcine uterus during early pregnancy. Journal of Physiology and Pharmacology 67, 443–456.Google ScholarPubMed
Smolinska, N, Kiezun, M, Dobrzyn, K, Rytelewska, E, Kisielewska, K, Gudelska, M, Zaobidna, E, Bogus-Nowakowska, K, Wyrebek, J, Bors, K, Kopij, G, Kaminska, B and Kaminski, T 2019. Expression of chemerin and its receptors in the porcine hypothalamus and plasma chemerin levels during the oestrous cycle and early pregnancy. International Journal of Molecular Sciences 9, E3887.CrossRefGoogle Scholar
Smolinska, N, Maleszka, A, Dobrzyn, K, Kiezun, M, Szeszko, K and Kaminski, T 2014. Expression of adiponectin and adiponectin receptors 1 and 2 in the porcine uterus, conceptus, and trophoblast during early pregnancy. Theriogenology 82, 951–965.CrossRefGoogle ScholarPubMed
Spagnuolo-Weaver, M, Fuerst, R, Campbell, ST, Meehan, BM, McNeilly, F, Adair, B and Allan, G 1999. A fluorimeter-based RT-PCR method for the detection and quantitation of porcine cytokines. Journal of Immunological Methods 230, 19–27.CrossRefGoogle ScholarPubMed
Wittamer, V, Franssen, JD, Vulcano, M, Mirjolet, JF, Le Poul, E, Migeotte, I, Brezillonn, S, Tyldesley, R, Blanpain, C, Detheux, M, Mantovani, A, Sozzani, S, Vassart, G, Parmentier, M and Communi, D 2003. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluid. Journal of Experimental Medicine 198, 977–985.CrossRefGoogle Scholar
Yang, YL, Ren, LR and Sun, LF 2016. The role of GPR1 signaling in mice corpus luteum. Journal of Endocrinology 230, 55–65.CrossRefGoogle ScholarPubMed
Zabel, BA, Allen, SJ, Kulig, P, Allen, JA, Cichy, J, Handel, TM and Butcher, EC 2005. Chemerin activation by serine proteases of the coagulation, fibrinolytic, and inflammatory cascades. Journal of Biological Chemistry 280, 34661–34666.CrossRefGoogle ScholarPubMed
Ziecik, AJ, Waclawik, A, Kaczmarek, MM, Blitek, A, Jalali, BM and Andronowska, A 2011. Mechanisms for the establishment of pregnancy in the pig. Reproduction in Domestic Animals 46, 31–41.CrossRefGoogle ScholarPubMed
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