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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

Published online by Cambridge University Press:  28 November 2013

N. Smolinska ,
A. Nitkiewicz ,
A. Maleszka ,
M. Kiezun ,
K. Dobrzyn ,
J. Czerwinska ,
K. Chojnowska  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
A. Nitkiewicz
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
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
J. Czerwinska
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. Chojnowska
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: tkam@uwm.edu.pl
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Abstract

Hypothalamic peptides orexin A (OXA) and orexin B (OXB) are derived from the proteolytic cleavage of a common precursor molecule, prepro-orexin (PPO). They act via two orexin receptors (OX1R and OX2R), which belong to the G-protein coupled receptor superfamily. Orexins are implicated in the regulation of arousal states, energy homeostasis and reproductive neuroendocrine function. The objective of this study was to investigate the presence and changes in orexin expression in the porcine pituitary during the estrous cycle. Adenohypophysis (AP) and neurohypophysis (NP) tissue samples were harvested on days 2 to 3, 10 to 12, 14 to 16, and 17 to 19 of the estrous cycle. The expression of the PPO gene increased in AP and NP during the estrous cycle. The highest PPO protein concentrations in AP were reported on days 2 to 3 (P<0.05), and in NP – on days 10 to 12 and 17 to 19 (P<0.05). The expression of PPO mRNA was lower in AP than in NP, but PPO protein levels were higher in AP. In AP, OXA immunoreactivity was higher (P<0.05) on days 10 to 12 and 14 to 16. In NP, the highest (P<0.05) content of the analyzed protein was observed on days 10 to 12 and the lowest (P<0.05) – on days 14 to 16 and 17 to 19. OXB immunoreactivity in AP reached the highest level (P<0.05) on days 2 to 3, and the lowest level (P<0.05) was determined on days 10 to 12 and 17 to 19. OXB protein concentrations in NP peaked (P<0.05) on days 10 to 12 of the cycle. Our study was the first experiment to demonstrate the expression of the orexin gene and orexin proteins in the porcine pituitary and the correlations between expression levels and the phase of the estrous cycle.

Keywords

prepro-orexinorexin A and Bpituitaryestrous cyclepig
Type
Full Paper
Information
animal , Volume 8 , Issue 2 , February 2014 , pp. 300 - 307
Copyright
Copyright © The Animal Consortium 2013 

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References

Akins, EL and Morrissette, MC 1968. Gross ovarian changes during oestrous cycle of swine. American Journal of Veterinary Research 29, 1953–1957.Google Scholar
Barb, CR and Matteri, RL 2005. Orexin-B modulates luteinizing hormone and growth hormone secretion from porcine pituitary cells in culture. Domestic Animal Endocrinology 28, 331–337.CrossRefGoogle ScholarPubMed
Blanco, M, Gallego, R, Garcia-Caballero, T, Dieguez, C and Beiras, A 2003. Cellular localization of orexins in human anterior pituitary. Histochemistry and Cell Biology 120, 259–264.Google ScholarPubMed
Blanco, M, Lopez, M, Garcia-Caballero, T, Gallego, R, Vazquez-Boquete, A, Morel, G, Senaris, R, Casanueva, F, Dieguez, C and Beiras, A 2001. Cellular localization of orexin receptors in human pituitary. Journal of Clinical Endocrinology and Metabolism 86, 1616–1619.CrossRefGoogle ScholarPubMed
Campbell, RE, Grove, KL and Smith, MS 2003. Gonadotropin-releasing hormone neurons coexpress orexin 1 receptor immunoreactivity and receive direct contacts by orexin fibers. Endocrinology 144, 1542–1548.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Ciereszko, RE, Petroff, BK, Ottobre, AC, Guan, Z, Stokes, BT and Ottobre, JS 1998. Assessment of the mechanism by which prolactin stimulates progesterone production by early corpora lutea of pigs. Journal of Endocrinology 159, 201–209.CrossRefGoogle ScholarPubMed
Date, Y, Mondal, MS, Matsukura, S, Ueta, Y, Yamashita, H, Kaiya, H, Kangawa, K and Nakazato, M 2000. Distribution of orexin/hypocretin in the rat median eminence and pituitary. Molecular Brain Research 6, 1–6.CrossRefGoogle Scholar
De Lecea, L, Kilduff, TS, Peyron, C, Gao, X-B, Foye, PE, Danielson, PE, Fukuhara, C, Battenberg, ELF, Gautvik, VT, Bartlett, FS II, 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.CrossRefGoogle ScholarPubMed
Henricks, DM, Guthrie, HD and Handlin, DL 1972. Plasma estrogen, progesterone and luteinizing hormone levels during the oestrous cycle in pigs. Biology of Reproduction 6, 210–218.CrossRefGoogle Scholar
Jöhren, O, Neidert, SJ, Kummer, M and Dominiak, P 2002. Sexually dimorphic expression of prepro-orexin mRNA in the rat hypothalamus. Peptides 23, 1177–1180.CrossRefGoogle ScholarPubMed
Jöhren, O, Bruggemann, N, Dendorfer, A and Dominiak, P 2003. Gonadal steroids differentially regulate the messenger ribonucleic acid expression of pituitary orexin type 1 receptors and adrenal orexin type 2 receptors. Endocrinology 144, 1219–1225.CrossRefGoogle ScholarPubMed
Jöhren, O, Neidert, SJ, Kummer, M, Dendorfer, A and Dominiak, P 2001. Prepro-orexin and orexin receptor mRNAs are differentially expressed in peripheral tissues of male and female rats. Endocrinology 142, 3324–3331.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
Livak, KJ and Schmittgen, T 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25, 402–408.CrossRefGoogle Scholar
Martynska, L, Wolinska-Witort, E, Chmielowska, M, Bik, W and Baranowska, B 2011. Evaluation of orexin A activity on LH and FSH release from primary culture pituitary cells in immature and mature female rats. Neuroendocrinology Letters 32, 769–773.Google ScholarPubMed
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.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
Pu, S, Jain, MR, Kalra, PS and Kalra, SP 1998. Orexins, a novel family of hypothalamic neuropeptides, modulate pituitary luteinizing hormone secretion in an ovarian steroid-dependent manner. Regulatory Peptides 78, 133–136.Google Scholar
Russell, SH, Small, CJ, Kennedy, AR, Stanley, SA, Seth, A, Murphy, KG, Taheri, S, Ghatei, MA and Bloom, SR 2001. Orexin A interactions in the hypothalamo–pituitary–gonadal axis. Endocrinology 142, 5294–5302.CrossRefGoogle ScholarPubMed
Russell, SH, Kim, MS, Small, CJ, Abbott, CR, Morgan, DG, Taheri, S, Murphy, KG, Todd, JF, Ghatei, MA and Bloom, SR 2000. Central administration of orexin A suppresses basal and domperidone stimulated plasma prolactin. Journal of Neuroendocrinology 12, 1213–1218.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Samson, WK and Taylor, MM 2001. Hypocretin/orexin suppresses corticotroph responsiveness in vitro . American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 281, R1140–R1145.CrossRefGoogle ScholarPubMed
Sasson, R, Dearh, RK, White, RS, Chappell, PE and Mellon, PL 2006. Orexin A induces GnRH gene expression and secretion from GT1-7 hypothalamic GnRH neurons. Neuroendocrinology 84, 353–363.CrossRefGoogle ScholarPubMed
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. American Journal of Physiology – Endocrinology and Metabolism 293, E977–E985.CrossRefGoogle ScholarPubMed
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. American Journal of Physiology – Endocrinology and Metabolism 292, E820–E828.CrossRefGoogle ScholarPubMed
Small, CJ, Goubillon, M-L, Murray, JF, Siddiqui, A, Grimshaw, SE, Young, H, Sivanesan, V, Kalamatianos, T, Kennedy, AR, Coen, CW, Bloom, SR and Wilson, CA 2003. Central orexin A has site-specific effects on luteinizing hormone release in female rats. Endocrinology 144, 3225–3236.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Spinazzi, R, Andreis, PG, Rossi, GP and Nussdorfer, GG 2006. Orexins in the regulation of the hypothalamic–pituitary–adrenal axis. Pharmacological Reviews 58, 46–57.CrossRefGoogle ScholarPubMed
Su, J, Lei, Z, Zhang, W, Ning, H and Ping, J 2008. Distribution of orexin B and its relationship with GnRH in the pig hypothalamus. Research in Veterinary Science 85, 315–323.CrossRefGoogle ScholarPubMed
Taheri, S, Mahmoodi, M, Opacka-Juffry, J, Ghatei, MA and Bloom, SR 1999. Distribution and quantification of immunoreactive orexin A in rat tissues. FEBS Letters 457, 157–161.CrossRefGoogle ScholarPubMed
Voisin, T, Rouet-Benzineb, P, Reuter, N and Laburthe, M 2003. Orexins and their receptors: structural aspects and role in peripheral tissues. Cellular and Molecular Life Sciences 60, 72–87.CrossRefGoogle ScholarPubMed
Wang, JB, Murata, T, Narita, K, Honda, K and Higuchi, T 2003. Variation in the expression of orexin and orexin receptors in the rat hypothalamus during the estrous cycle, pregnancy, parturition, and lactation. Endocrine 22, 127–134.CrossRefGoogle ScholarPubMed
Zhang, S, Blache, D, Vercoe, PE, Adam, CL, Blackberry, MA, Findlay, PA, Eidne, KA and Martin, GB 2005. Expression of orexin receptors in the brain and peripheral tissues of the male sheep. Regulatory Peptides 124, 81–87.CrossRefGoogle ScholarPubMed
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