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Expression of the orexin system in the porcine uterus, conceptus and trophoblast during early pregnancy

Published online by Cambridge University Press:  02 July 2015

N. Smolinska ,
M. Kiezun ,
K. Dobrzyn ,
K. Szeszko ,
A. Maleszka  and
T. Kaminski
N. Smolinska*
Affiliation:
Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn-Kortowo, Poland
M. Kiezun
Affiliation:
Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn-Kortowo, Poland
K. Dobrzyn
Affiliation:
Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn-Kortowo, Poland
K. Szeszko
Affiliation:
Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn-Kortowo, Poland
A. Maleszka
Affiliation:
Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn-Kortowo, Poland
T. Kaminski
Affiliation:
Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn-Kortowo, Poland
*
†E-mail: [email protected]
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Abstract

Orexin A and B are hypothalamic peptides derived from the prepro-orexin (PPO) precursor. Orexins stimulate food intake and arousal. Those peptides bind and activate two G protein-coupled receptors: orexin receptor 1 (OX1R) and orexin receptor 2 (OX2R). Numerous authors have suggested that orexins play an important role in the regulation of the reproductive functions. The objective of the present study was to analyse the presence of and changes in the gene and protein expression pattern of the orexin system in the porcine uterus, conceptus and trophoblast (chorioallantois) during early pregnancy. In the endometrium, the highest PPO and OX1R gene expression was detected on days 15 to 16 of gestation. The OX2R mRNA content in the endometrium was higher on days 10 to 11 and 15 to 16 than on days 12 to 13 and 27 to 28. In the trophoblasts, PPO gene expression was higher on days 30 to 32 than on days 27 to 28. The highest PPO protein content in the endometrium was noted on days 12 to 13. The highest OX1R protein content in the endometrium was detected on days 10 to 11, whereas OX2R protein on days 15 to 16. In the trophoblasts, PPO and OX1R protein levels were more pronounced on days 27 to 28 than on days 30 to 32, but OX2R expression was higher on days 30 to 32. The expression of PPO, OX1R and OX2R was different in the conceptuses and trophoblasts during early pregnancy. Local orexin production and the presence of the specific orexin receptors suggest that the orexin system may participate in the control of porcine reproductive functions by exerting endocrine and auto/paracrine effects on the uterus, conceptuses and trophoblasts during early pregnancy. This study provides the first evidence for the presence of orexins and their receptors in the uteri, conceptuses and trophoblasts in pigs during early pregnancy. The local orexin system is dependent on the stage of pregnancy.

Keywords

orexin A and Borexin receptors 1 and 2uteruspregnancypig
Type
Research Article
Information
animal , Volume 9 , Supplement 11 , November 2015 , pp. 1820 - 1831
Copyright
© The Animal Consortium 2015 

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References

Bazer, FW and Johnson, GA 2014. Pig blastocyst-uterine interactions. Differentiation 87, 52–65.Google Scholar
Chemelli, RM, Willie, JT, Sinton, CM, Elmquist, JK, Scammell, T, Lee, C, Richardson, JA, Williams, SC, Xiong, Y, Kisanuki, Y, Fitch, TE, Nakazato, M, Hammer, RE, Saper, CB and Yanagisawa, M 1999. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98, 437–451.Google Scholar
Dall'Aglio, C, Pascucci, L, Mercati, F, Polisca, A, Ceccarelli, P and Boiti, C 2012. Immunohistochemical detection of the orexin system in the placenta of cats. Research in Veterinary Science 92, 362–365.Google Scholar
De Lecea, L, Kilduff, TS, Peyron, C, Gao, X-B, Foye, PE, Danielson, PE, Fukuhara, C, Battenberg, ELF, Gautvik, VT, Bartlett II, FS, Franlel, WN, Van den Pol, AN, Bloom, FE, Gautvik, KM and Sutcliffe, JG 1998. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proceedings of the National Academy of Sciences of the United States of America 95, 322–327.Google Scholar
Dehan, P, Canon, C, Trooskens, G, Rehli, M, Munaut, C, Van Criekinge, W and Delvenne, P 2013. Expression of type 2 orexin receptor in human endometrium and its epigenetic silencing in endometrial cancer. Journal of Clinical Endocrinology & Metabolism 98, 1549–1557.Google Scholar
Godden, KE, Landry, JP, Slepneva, N, Migues, PV and Pompeiano, M 2014. Early expression of hypocretin/orexin in the chick embryo brain. PLoS One 9, e106977.Google Scholar
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
Harney, JP and Bazer, FW 1989. Effect of porcine conceptus secretory proteins on interestrous interval and uterine secretion of prostaglandins. Biology of Reproduction 41, 277–284.Google Scholar
Ka, H, Jaeger, LA, Johnson, GA, Spencer, TE and Bazer, FW 2001. Keratinocyte growth factor expression is up-regulated by estrogen in porcine uterine endometrium and it functions in trophectodermal cell proliferation and differentiation. Endocrinology 142, 2303–2310.CrossRefGoogle ScholarPubMed
Kaminski, T, Smolinska, N, Nitkiewicz, A and Przala, J 2010a. Expression of orexin receptors 1 (OX1R) and 2 (OX2R) in the porcine pituitary during the oestrous cycle. Animal Reproduction Science 117, 111–118.CrossRefGoogle ScholarPubMed
Kaminski, T, Smolinska, N, Nitkiewicz, A and Przala, J 2010b. Expression of orexin receptors 1 (OX1R) and 2 (OX2R) in the porcine hypothalamus during the oestrous cycle. Journal of Physiology and Pharmacology 64, 363–371.Google Scholar
Maleszka, A, Smolinska, N, Nitkiewicz, A, Kiezun, M, Chojnowska, K, Dobrzyn, K, Jazowska, J and Kaminski, T 2013. Expression of orexin A and B in the porcine hypothalamus during the oestrous cycle. Journal of Physiology and Pharmacology 64, 55–63.Google Scholar
Nakabayashi, M, Suzuki, T, Takahashi, K, Totsune, K, Muramatsu, Y, Kaneko, C, Date, F, Takeyama, J, Darnel, AD, Moriya, T and Sasano, H 2003. Orexin-A expression in human peripheral tissues. Molecular and Cellular Endocrinology 205, 43–50.Google Scholar
Nitkiewicz, A, Smolinska, N, Przala, J and Kaminski, T 2010. Expression of orexin receptors 1 (OX1R) and 2 (OX2R) in the porcine ovary during the oestrous cycle. Regulatory Peptides 165, 186–190.Google Scholar
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
Nitkiewicz, A, Smolinska, N, Maleszka, A, Chojnowska, K and Kaminski, T 2014. Expression of orexins and their precursor in the porcine ovary and the influence of orexins on ovarian steroidogenesis in pigs. Animal Reproduction Science 148, 53–62.Google Scholar
Ross, JW, Ashworth, MD, Hurst, AG, Malayer, JR and Geisert, RD 2003. Analysis and characterization of differential gene expression during rapid trophoblastic elongation in the pig using suppression subtractive hybridization. Reproductive Biology and Endocrinology 1, 23.Google Scholar
Sakurai, T, Amemiya, A, Ishii, M, Matsuzaki, I, Chemelli, RM, Tanaka, H, Williams, SC, Richardson, JA, Kozlowski, GP, Wilson, S, Arch, JR, Buckingham, RE, Haynes, AC, Carr, SA, Annan, RS, McNulty, DE, Liu, WS, Terret, JA, Elshourbagy, NA, Bergsma, DJ and Yanagisawa, M 1998. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573–585.Google Scholar
Silveyra, P, Lux-Lantos, V and Libertun, C 2007a. Both orexin receptors are expressed in rat ovaries and fluctuate with the estrous cycle: effects of orexin receptor antagonists on gonadotropins and ovulation. The American Journal of Physiology – Endocrinology and Metabolism 293, E977–E985.Google Scholar
Silveyra, P, Catalano, PN, Lux-Lantos, V and Libertun, C 2007b. Impact of proestrous milieu on expression of orexin receptors and prepro-orexin in rat hypothalamus and hypophysis: actions of Cetrorelix and Nembutal. The American Journal of Physiology – Endocrinology and Metabolism 292, E820–E828.Google Scholar
Smolinska, N, Kaminski, T, Siawrys, G and Przala, J 2007. Long form of leptin receptor gene and protein expression in the porcine ovary during the estrous cycle and early pregnancy. Reproductive Biology 7, 17–39.Google Scholar
Smolinska, N, Dobrzyn, K, Maleszka, A, Kiezun, M, Szeszko, K and Kaminski, T 2014a. Expression of adiponectin and adiponectin receptors 1 (AdipoR1) and 2 (AdipoR2) in the porcine uterus during the oestrous cycle. Animal Reproduction Science 146, 42–54.CrossRefGoogle ScholarPubMed
Smolinska, N, Nitkiewicz, A, Maleszka, A, Kiezun, M, Dobrzyn, K, Czerwinska, J, Chojnowska, K and Kaminski, T 2014b. The effect of the estrous cycle on the expression of prepro-orexin gene and protein and the levels of orexin A and B in the porcine pituitary. Animal 8, 300–307.Google Scholar
Steininger, TL, Kilduff, TS, Behan, M, Benca, RM and Landry, CF 2004. Comparison of hypocretin/orexin and melanin-concentrating hormone neurons and axonal projections in the embryonic and postnatal rat brain. Journal of Chemical Neuroanatomy 27, 165–181.Google Scholar
Urbanska, A, Sokolowska, P, Woldan-Tambor, A, Bieganska, K, Brix, B, Jöhren, O, Namiecinska, M and Zawilska, JB 2012. Orexins/Hypocretins acting at Gi protein-coupled OX2 receptors inhibit cyclic AMP synthesis in the primary neuronal cultures. Journal of Molecular Neuroscience 46, 10–17.Google Scholar
Vogel, C and Marcotte, EM 2012. Insight into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews Genetics 13, 227–232.Google Scholar
Waclawik, A, Blitek, A and Ziecik, AJ 2010. Oxytocin and tumor necrosis factor alpha stimulate expression of prostaglandin E2 synthase and secretion of prostaglandin E2 by luminal epithelial cells of the porcine endometrium during early pregnancy. Reproduction 140, 613–622.CrossRefGoogle ScholarPubMed
Waclawik, A, Jabbour, HN, Blitek, A and Ziecik, AJ 2009. Estradiol-17beta, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. Endocrinology 150, 3823–3832.Google Scholar
White, FJ, Kimball, EM, Wyman, G, Stein, DR, Ross, JW, Ashworth, MD and Geisert, RD 2009. Estrogen and interleukin-1beta regulation of trophinin, osteopontin, cyclooxygenase-1, cyclooxygenase-2, and interleukin-1beta system in the porcine uterus. The Society for Reproduction and Fertility 66 (suppl. 1), 203–204.Google Scholar
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