Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2021-0063
Animal Reproduction (AR)
REVIEW ARTICLE

The neuroendocrine pathways and mechanisms for the control of the reproduction in female pigs

Shuang Zhao; Zongyi Guo; Wei Xiang; Pingqing Wang

Downloads: 0
Views: 164

Abstract

Within the hypothalamic-pituitary-gonad (HPG) axis, the major hierarchical component is gonadotropin-releasing hormone (GnRH) neurons, which directly or indirectly receive regulatory inputs from a wide array of regulatory signals and pathways, involving numerous circulating hormones, neuropeptides, and neurotransmitters, and which operate as a final output for the brain control of reproduction. In recent years, there has been an increasing interest in neuropeptides that have the potential to stimulate or inhibit GnRH in the hypothalamus of pigs. Among them, Kisspeptin is a key component in the precise regulation of GnRH neuron secretion activity. Besides, other neuropeptides, including neurokinin B (NKB), neuromedin B (NMB), neuromedin S (NMS), α-melanocyte-stimulating hormone (α-MSH), Phoenixin (PNX), show potential for having a stimulating effect on GnRH neurons. On the contrary, RFamide-related peptide-3 (RFRP-3), endogenous opioid peptides (EOP), neuropeptide Y (NPY), and Galanin (GAL) may play an inhibitory role in the regulation of porcine reproductive nerves and may directly or indirectly regulate GnRH neurons. By combining data from suitable model species and pigs, we aim to provide a comprehensive summary of our current understanding of the neuropeptides acting on GnRH neurons, with a particular focus on their central regulatory pathways and underlying molecular basis.

Keywords

pig, reproduction, neuroendocrine, GnRH neuron, RFamide-related peptide-3

References

Amstalden M, Cardoso RC, Alves BRC, Williams GL. Reproduction Symposium: hypothalamic neuropeptides and the nutritional programming of puberty in heifers1,2. J Anim Sci. 2014;92(8):3211-22. http://dx.doi.org/10.2527/jas.2014-7808. PMid:24894003.

Ancel C, Bentsen AH, Sébert M-E, Tena-Sempere M, Mikkelsen JD, Simonneaux V. Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male syrian hamster: the exception proves the rule. Endocrinology. 2012;153(3):1352-63. http://dx.doi.org/10.1210/en.2011-1622. PMid:22275511.

Anderson GM, Relf H-L, Rizwan MZ, Evans JJ. Central and peripheral effects of RFamide-Related Peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology. 2009;150(4):1834-40. http://dx.doi.org/10.1210/en.2008-1359. PMid:19022888.

Arreguin-Arevalo JA, Lents CA, Farmerie TA, Nett TM, Clay CM. KiSS-1 peptide induces release of LH by a direct effect on the hypothalamus of ovariectomized ewes. Anim Reprod Sci. 2007;101(3-4):265-75. http://dx.doi.org/10.1016/j.anireprosci.2006.09.021. PMid:17055196.

Aydin S. Multi-functional peptide hormone NUCB2/nesfatin-1. Endocrine. 2013;44(2):312-25. http://dx.doi.org/10.1007/s12020-013-9923-0. PMid:23526235.

Barb CR, Robertson AS, Barrett JB, Kraeling RR, Houseknecht KL. The role of melanocortin-3 and -4 receptor in regulating appetite, energy homeostasis and neuroendocrine function in the pig. J Endocrinol. 2004;181(1):39-52. http://dx.doi.org/10.1677/joe.0.1810039. PMid:15072565.

Barb CR, Kraeling RR, Rampacek GB, Hausman GJ. The role of neuropeptide Y and interaction with leptin in regulating feed intake and luteinizing hormone and growth hormone secretion in the pig. Reproduction. 2006;131(6):1127-35. http://dx.doi.org/10.1530/rep.1.01108. PMid:16735552.

Barb CR, Hausman GJ, Rekaya R, Lents CA, Lkhagvadorj S, Qu L, Cai W, Couture OP, Anderson LL, Dekkers JC, Tuggle CK. Gene expression in hypothalamus, liver, and adipose tissues and food intake response to melanocortin-4 receptor agonist in pigs expressing melanocortin-4 receptor mutations. Physiol Genomics. 2010;41(3):254-68. http://dx.doi.org/10.1152/physiolgenomics.00006.2010. PMid:20215418.

Bentley GE, Tsutsui K, Kriegsfeld LJ. Recent studies of gonadotropin-inhibitory hormone (GnIH) in the mammalian hypothalamus, pituitary and gonads. Brain Res. 2010;1364:62-71. http://dx.doi.org/10.1016/j.brainres.2010.10.001. PMid:20934414.

Boughton CK, Patel SA, Thompson EL, Patterson M, Curtis AE, Amin A, Chen K, Ghatei MA, Bloom SR, Murphy KG. Neuromedin B stimulates the hypothalamic–pituitary–gonadal axis in male rats. Regul Pept. 2013;187:6-11. http://dx.doi.org/10.1016/j.regpep.2013.10.002. PMid:24120470.

Burke MC, Letts PA, Krajewski SJ, Rance NE. Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol. 2006;498(5):712-26. http://dx.doi.org/10.1002/cne.21086. PMID: 16917850.

Caraty A, Smith JT, Lomet D, Ben Saïd S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C, Clarke IJ. Kisspeptin Synchronizes Preovulatory Surges in Cyclical Ewes and Causes Ovulation in Seasonally Acyclic Ewes. Endocrinology. 2007;148(11):5258-67. http://dx.doi.org/10.1210/en.2007-0554. PMid:17702853.

Caraty A, Blomenröhr M, Vogel GMT, Lomet D, Briant C, Beltramo M. RF9 powerfully stimulates gonadotrophin secretion in the Ewe: evidence for a seasonal threshold of sensitivity. J Neuroendocrinol. 2012;24(5):725-36. http://dx.doi.org/10.1111/j.1365-2826.2012.02283.x. PMid:22283564.

Cardoso RC, Alves BRC, Sharpton SM, Williams GL, Amstalden M. Nutritional programming of accelerated puberty in heifers: involvement of pro‐opiomelanocortin neurones in the arcuate nucleus. J Neuroendocrinol. 2015;37(8):647-57. http://dx.doi.org/10.1111/jne.12291. PMid:25944025.

Clarke SA, Dhillo WS. Phoenixin and its role in reproductive hormone release. Semin Reprod Med. 2019;27(4):191-6. http://dx.doi.org/10.1055/s-0039-3400964. PMid:31972864.

Constantin S, Wray S. Galanin activates G protein gated inwardly rectifying potassium channels and suppresses Kisspeptin-10 activation of GnRH neurons. Endocrinology. 2016;157(8):3197-212. http://dx.doi.org/10.1210/en.2016-1064. PMid:27359210.

Czujkowska A, Arciszewski MB. Galanin is Co-Expressed with Substance P, Calbindin and Corticotropin-Releasing Factor (CRF) in The Enteric Nervous System of the Wild Boar (Sus scrofa) Small Intestine. Anat Histol Embryol. 2016;45(2):115-23. http://dx.doi.org/10.1111/ahe.12179. PMid:25907507.

de Croft S, Boehm U, Herbison AE. Activates arcuate kisspeptin neurons through multiple tachykinin receptors in the male mouse. Endocrinology. 2013;154(8):2750-60. http://dx.doi.org/10.1210/en.2013-1231. PMid:23744641.

de Roux N, Genin E, Carel J-C, Matsuda F, Chaussain J-L, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA. 2003;100(19):10972-6. http://dx.doi.org/10.1073/pnas.1834399100. PMid:12944565.

Decourt C, Anger K, Robert V, Lomet D, Bartzen-Sprauer J, Caraty A, Dufourny L, Anderson G, Beltramo M. No Evidence That RFamide-Related Peptide 3 Directly Modulates LH Secretion in the Ewe. Endocrinology. 2016;157(4):1566-75. http://dx.doi.org/10.1210/en.2015-1854. PMid:26862995.

Dhillon SS, Gingerich S, Belsham DD. Neuropeptide Y induces gonadotropin-releasing hormone gene expression directly and through conditioned medium from mHypoE-38 NPY neurons. Regul Pept. 2009;156(1-3):96-103. http://dx.doi.org/10.1016/j.regpep.2009.04.005. PMid:19371763.

Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinology. 2009;150(6):2799-804. http://dx.doi.org/10.1210/en.2008-1623. PMid:19131572.

Elsaesser F. Stimulation of porcine pituitary luteinizing hormone release by galanin: putative auto/paracrine regulation. Neuroendocrinology. 2001;74(5):288-99. http://dx.doi.org/10.1159/000054696. PMid:11694761.

Fang MX, Huang YS, Ye J, Zhang W, Li Y, Nie QH. Identification and characterization of RFRP gene in pigs and its association with reproductive traits. Genet Mol Res. 2014;13(1):1661-71. http://dx.doi.org/10.4238/2014.January.14.8. PMid:24446341.

Gaigé S, Bonnet MS, Tardivel C, Pinton P, Trouslard J, Jean A, Guzylack L, Troadec JD, Dallaporta M. c-Fos immunoreactivity in the pig brain following deoxynivalenol intoxication: focus on NUCB2/nesfatin-1 expressing neurons. Neurotoxicology. 2013;34:135-49. http://dx.doi.org/10.1016/j.neuro.2012.10.020. PMid:23164930.

Garcia IS, Teixeira SA, Costa KA, Marques DBD, Rodrigues GA, Costa TC, Guimarães JD, Otto PI, Saraiva A, Ibelli AMG, Cantão ME, Oliveira HC, Ledur MC, Peixoto JO, Guimarães SEF. L‐Arginine supplementation of gilts during early gestation modulates energy sensitive pathways in pig conceptuses. Mol Reprod Dev. 2020;87(7):819-34. http://dx.doi.org/10.1002/mrd.23397. PMid:32592179.

Garcia-Galiano D, Navarro VM, Roa J, Ruiz-Pino F, Sanchez-Garrido MA, Pineda R, Castellano JM, Romero M, Aguilar E, Gaytán F, Diéguez C, Pinilla L, Tena-Sempere M. The anorexigenic neuropeptide, Nesfatin-1, Is indispensable for normal puberty onset in the female rat. J Neurosci. 2010;30(23):7783-92. http://dx.doi.org/10.1523/JNEUROSCI.5828-09.2010. PMid:20534827.

Gibson EM, Humber SA, Jain S, Williams WP 3rd, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology. 2008;149(10):4958-69. http://dx.doi.org/10.1210/en.2008-0316. PMid:18566114.

Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CVR, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology. 2007;148(12):5752-60. http://dx.doi.org/10.1210/en.2007-0961. PMid:17823266.

Hashizume T, Saito H, Sawada T, Yaegashi T, Ezzat AA, Sawai K, Yamashita T. Characteristics of stimulation of gonadotropin secretion by kisspeptin-10 in female goats. Anim Reprod Sci. 2010;118(1):37-41. http://dx.doi.org/10.1016/j.anireprosci.2009.05.017. PMid:19574004.

Herbison AE. Control of puberty onset and fertility by gonadotropin-releasing hormone neurons. Nat Rev Endocrinol. 2016;12(8):452-66. http://dx.doi.org/10.1038/nrendo.2016.70. PMid:27199290.

Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, Yano T, Yamamoto T, Kawamata Y, Habata Y, Asada M, Kitada C, Kurokawa T, Onda H, Nishimura O, Tanaka M, Ibata Y, Fujino M. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol. 2000;2(10):703-8. http://dx.doi.org/10.1038/35036326. PMid:11025660.

Ieda N, Uenoyama Y, Tajima Y, Nakata T, Kano M, Naniwa Y, Watanabe Y, Minabe S, Tomikawa J, Inoue N, Matsuda F, Ohkura S, Maeda K, Tsukamura H. KISS1 Gene Expression in the Developing Brain of Female Pigs in Pre- and Peripubertal Periods. J Reprod Dev. 2014;60(4):312-6. http://dx.doi.org/10.1262/jrd.2013-129. PMid:24909600.

Israel DD, Sheffer-Babila S, de Luca C, Jo Y-H, Liu SM, Xia Q, Spergel DJ, Dun SL, Dun NJ, Chua SC Jr. Effects of Leptin and Melanocortin Signaling Interactions on Pubertal Development and Reproduction. Endocrinology. 2012;153(5):2408-19. http://dx.doi.org/10.1210/en.2011-1822. PMid:22408174.

Jensen RT, Battey JF, Spindel ER, Benya RV. International Union of Pharmacology. LXVIII. Mammalian Bombesin Receptors: Nomenclature, Distribution, Pharmacology, Signaling, and Functions in Normal and Disease States. Pharmacol Rev. 2008;60(1):1-42. http://dx.doi.org/10.1124/pr.107.07108. PMid:18055507.

Jin M, Ma Z, Li X, Su J, Lei Z. The effects of neuromedin S on the hypothalamic-pituitary-testicular axis in male pigs in vitro. Gen Comp Endocrinol. 2019;280:73-81. http://dx.doi.org/10.1016/j.ygcen.2019.04.013. PMid:30981702.

Johnson MA, Tsutsui K, Fraley GS. Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav. 2007;51(1):171-80. http://dx.doi.org/10.1016/j.yhbeh.2006.09.009. PMid:17113584.

Kadokawa H, Matsui M, Hayashi K, Matsunaga N, Kawashima C, Shimizu T, Kida K, Miyamoto A. Peripheral administration of kisspeptin-10 increases plasma concentrations of GH as well as LH in prepubertal Holstein heifers. J Endocrinol. 2008;196(2):331-4. http://dx.doi.org/10.1677/JOE-07-0504. PMid:18252956.

Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, Yamamoto N. Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) secretion from the pituitary as well as pulsatile LH secretion in bovines. Domest Anim Endocrinol. 2009;36(4):219-24. http://dx.doi.org/10.1016/j.domaniend.2009.02.001. PMid:19328642.

Kalló I, Vida B, Deli L, Molnár CS, Hrabovszky E, Caraty A, Ciofi P, Coen CW, Liposits Z. Co-localisation of kisspeptin with galanin or neurokinin B in afferents to mouse GnRH neurones. J Neuroendocrinol. 2012;24(3):464-76. http://dx.doi.org/10.1111/j.1365-2826.2011.02262.x. PMid:22129075.

Klenke U, Constantin S, Wray S. Directly Inhibits neuronal activity in a subpopulation of gonadotropin-releasing hormone-1 neurons via Y1 receptors. Endocrinology. 2010;151(6):2736-46. http://dx.doi.org/10.1210/en.2009-1198. PMid:20351316.

Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA. 2006;103(7):2410-5. http://dx.doi.org/10.1073/pnas.0511003103. PMid:16467147.

Kriegsfeld LJ. Driving reproduction: RFamide peptides behind the wheel. Horm Behav. 2006;50(5):655-66. http://dx.doi.org/10.1016/j.yhbeh.2006.06.004. PMid:16876801.

Lane RL, Whitaker BD. Melatonin and tannic acid supplementation in vitro improve fertilization and embryonic development in pigs. Anim Reprod. 2018;15(2):118-23. http://dx.doi.org/10.21451/1984-3143-AR2016-937. PMid:34122642.

Legagneux K, Bernard-Franchi G, Poncet F, La Roche A, Colard C, Fellmann D, Pralong F, Risold PY. Distribution and genesis of the RFRP-producing neurons in the rat brain: comparison with melanin-concentrating hormone- and hypocretin-containing neurons. Neuropeptides. 2009;43(1):13-9. http://dx.doi.org/10.1016/j.npep.2008.11.001. PMid:19101033.

Lents CA, Heidorn NL, Barb CR, Ford JJ. Central and peripheral administration of kisspeptin activates gonadotropin but not somatotropin secretion in prepubertal gilts. Reproduction. 2008;135(6):879-87. http://dx.doi.org/10.1530/REP-07-0502. PMid:18339687.

Lents CA, Lindo AN, Hileman SM, Nonneman DJ. Physiological and genomic insight into neuroendocrine regulation of puberty in gilts. Domest Anim Endocrinol. 2020;73:106446. http://dx.doi.org/10.1016/j.domaniend.2020.106446. PMid:32199704.

Lents CA. Review: kisspeptin and reproduction in the pig. Animal. 2019;13(12):2986-99. http://dx.doi.org/10.1017/S1751731119001666. PMid:31317853.

Lepiarczyk E, Bossowska A, Majewska M, Skowrońska A, Kaleczyc J, Majewski M. Distribution and chemical coding of phoenixin-immunoreactive nerve structures in the spinal cord of the pig. Ann Anat. 2020;232:151559. http://dx.doi.org/10.1016/j.aanat.2020.151559. PMid:32569824.

Li X, Su J, Fang R, Zheng L, Lei R, Wang X, Lei Z, Jin M, Jiao Y, Hou Y, Guo T, Ma Z. The effects of RFRP-3, the mammalian ortholog of GnIH, on the female pig reproductive axis in vitro. Mol Cell Endocrinol. 2013;372(1-2):65-72. http://dx.doi.org/10.1016/j.mce.2013.03.015. PMid:23541949.

Lindo A. Characterization of KNDy neuronal activity in gilts: distribution and effect of a progestin [thesis]. Morgantown: West Virginia University; 2018.

Ma Z, Su J, Guo T, Jin M, Li X, Lei Z, Hou Y, Li X, Jia C, Zhang Z, Ahmed E. Neuromedin B and its receptor: gene cloning, tissue distribution and expression levels of the reproductive axis in pigs. PLoS ONE. 2016 Mar 24;11(3):e0151871. https://doi.org/10.1371/journal.pone.0151871.

Ma Z, Zhao Y, Yao Y, Lei Z, Jin M, Li X, Jia C, Zhang Z, Li X, Su J. Postnatal developmental of Neuromedin S and its receptor in the male Xiaomeishan pig reproductive axis. Anim Reprod Sci. 2017;181:115-24. http://dx.doi.org/10.1016/j.anireprosci.2017.03.023. PMid:28389048.

Ma Z, Zhang Y, Su J, Yang S, Qiao W, Li X, Lei Z, Cheng L, An N, Wang W, Feng Y, Zhang J. Effects of neuromedin B on steroidogenesis, cell proliferation and apoptosis in porcine Leydig cells. J Mol Endocrinol. 2018;61(1):13-23. http://dx.doi.org/10.1530/JME-17-0242. PMid:29632025.

Magee C, Foradori CD, Bruemmer JE, Arreguin-Arevalo JA, McCue PM, Handa RJ, Squires EL, Clay CM. Biological and anatomical evidence for kisspeptin regulation of the hypothalamic-pituitary-gonadal axis of estrous horse mares. Endocrinology. 2009;150(6):2813-21. http://dx.doi.org/10.1210/en.2008-1698. PMid:19228887.

Marín-García PJ, Llobat L. How does protein nutrition affect the epigenetic changes in pig? A review. Animals (Basel). 2021;11(2):544. http://dx.doi.org/10.3390/ani11020544. PMid:33669864.

Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA. 2005;102(5):1761-6. http://dx.doi.org/10.1073/pnas.0409330102. PMid:15665093.

Millar RP. GnRHs and GnRH receptors. Anim Reprod Sci. 2005;88(1–2):5-28. http://dx.doi.org/10.1016/j.anireprosci.2005.05.032. PMid:16140177.

Mori K, Miyazato M, Ida T, Murakami N, Serino R, Ueta Y, Kojima M, Kangawa K. Identification of neuromedin S and its possible role in the mammalian circadian oscillator system. EMBO J. 2005;24(2):325-35. http://dx.doi.org/10.1038/sj.emboj.7600526. PMid:15635449.

Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol. 2008;199(1):105-12. http://dx.doi.org/10.1677/JOE-08-0197. PMid:18653621.

Muro BBD, Leal DF, Carnevale RF, Torres MA, Mendonça MV, Nakasone DH, Martinez CHG, Ravagnani GM, Monteiro MS, Poor AP, Martins SMMK, Viau P, Oliveira CA, Castro RVG, Bessi BW, Bressan FF, Pulz LH, Strefezzi RF, Almond GW, Andrade AFC. Altrenogest during early pregnancy modulates uterine glandular epithelium and endometrial growth factor expression at the time implantation in pigs. Anim Reprod. 2021;18(1):e20200431. http://dx.doi.org/10.1590/1984-3143-ar2020-0431. PMid:34122654.

Navarro VM, Castellano JM, McConkey SM, Pineda R, Ruiz-Pino F, Pinilla L, Clifton DK, Tena-Sempere M, Steiner RA. Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab. 2011;300(1):E202-10. http://dx.doi.org/10.1152/ajpendo.00517.2010. PMid:21045176.

Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of Gonadotropin-Releasing Hormone Secretion by Kisspeptin/Dynorphin/Neurokinin B Neurons in the Arcuate Nucleus of the Mouse. J Neurosci. 2009;29(38):11859-66. http://dx.doi.org/10.1523/JNEUROSCI.1569-09.2009. PMid:19776272.

Nguyen XP, Nakamura T, Osuka S, Bayasula B, Nakanishi N, Kasahara Y, Muraoka A, Hayashi S, Nagai T, Murase T, Goto M, Iwase A, Kikkawa F. Effect of the neuropeptide phoenixin and its receptor GPR173 during folliculogenesis. Reproduction. 2019;158(1):25-34. http://dx.doi.org/10.1530/REP-19-0025. PMid:30933929.

Ohki-Hamazaki H, Iwabuchi M, Maekawa F. Development and function of bombesin-like peptides and their receptors. Int J Dev Biol. 2005;49(2-3):293-300. http://dx.doi.org/10.1387/ijdb.041954ho. PMid:15906244.

Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature. 2001;411(6837):613-7. http://dx.doi.org/10.1038/35079135. PMid:11385580.

Óvilo C, Fernández A, Fernández AI, Folch JM, Varona L, Benítez R, Nuñez Y, Rodríguez C, Silió L. Hypothalamic expression of porcine leptin receptor (LEPR), neuropeptide Y (NPY), and cocaine- and amphetamine-regulated transcript (CART) genes is influenced by LEPR genotype. Mamm Genome. 2010;21(11–12):583-91. http://dx.doi.org/10.1007/s00335-010-9307-1. PMid:21128076.

Peltoniemi O, Björkman S, Oropeza-Moe M, Oliviero C. Developments of reproductive management and biotechnology in the pig. Anim Reprod. 2019;16(3):524-38. http://dx.doi.org/10.21451/1984-3143-AR2019-0055. PMid:32435295.

Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenröhr M, Pinilla L, van Noort PI, Tena-Sempere M. Characterization of the inhibitory roles of RFRP3, the mammalian ortholog of GnIH, in the control of gonadotropin secretion in the rat: in vivo and in vitro studies. Am J Physiol Endocrinol Metab. 2010;299(1):E39-46. http://dx.doi.org/10.1152/ajpendo.00108.2010. PMid:20424142.

Qi Y, Oldfield BJ, Clarke IJ. Projections of RFamide-related peptide-3 neurones in the ovine hypothalamus, with special reference to regions regulating energy balance and reproduction. J Neuroendocrinol. 2009;21(8):690-7. http://dx.doi.org/10.1111/j.1365-2826.2009.01886.x. PMid:19500220.

Ralph C, Kirkwood R, Tilbrook A. A single intravenous injection of Kisspeptin evokes an increase in luteinising hormone in 15- and 18- week-old gilts. Anim Reprod Sci. 2017;57(12):2469. http://dx.doi.org/10.1071/ANv57n12Ab067.

Ramaswamy S, Seminara SB, Plant TM. Evidence from the agonadal juvenile male rhesus monkey (Macaca mulatta) for the view that the action of neurokinin B to Trigger Gonadotropin-Releasing Hormone Release Is Upstream from the Kisspeptin Receptor. Neuroendocrinology. 2011;94(3):237-45. http://dx.doi.org/10.1159/000329045. PMid:21832818.

Redmond JS, Baez-Sandoval GM, Spell KM, Spencer TE, Lents CA, Williams GL, Amstalden M. Developmental Changes in Hypothalamic Kiss1 Expression during Activation of the Pulsatile Release of Luteinising Hormone in Maturing Ewe Lambs. J Neuroendocrinol. 2011;23(9):815-22. http://dx.doi.org/10.1111/j.1365-2826.2011.02177.x. PMid:21679258.

Rizwan MZ, Porteous R, Herbison AE, Anderson GM. Cells expressing RFamide-related peptide-1/3, the mammalian gonadotropin-inhibitory hormone orthologs, are not hypophysiotropic neuroendocrine neurons in the rat. Endocrinology. 2009;150(3):1413-20. http://dx.doi.org/10.1210/en.2008-1287. PMid:19008316.

Roa J, Herbison AE. Direct regulation of gnrh neuron excitability by arcuate nucleus POMC and NPY neuron neuropeptides in female mice. Endocrinology. 2012;153(11):5587-99. http://dx.doi.org/10.1210/en.2012-1470. PMid:22948210.

Roesler R, Kent P, Schröder N, Schwartsmann G, Merali Z. Bombesin receptor regulation of emotional memory. Rev Neurosci. 2012;23(5–6):571-86. PMid:23096238.

Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O’Rahilly S, Carlton MBL, Crowley WF Jr, Aparicio SAJR, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349(17):1614-27. http://dx.doi.org/10.1056/NEJMoa035322. PMid:14573733.

Semple RK, Achermann JC, Ellery J, Farooqi IS, Karet FE, Stanhope RG, O’rahilly S, Aparicio SA. Two novel missense mutations in G protein-coupled receptor 54 in a patient with hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2005;90(3):1849-55. http://dx.doi.org/10.1210/jc.2004-1418. PMid:15598687.

Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA. 2005;102(6):2129-34. http://dx.doi.org/10.1073/pnas.0409822102. PMid:15684075.

Siawrys G, Buchowski H. Modulation of anterior pituitary cell luteinizing hormone secretory activity by neuropeptide Y in early pregnant pigs. J Physiol Pharmacol. 2018;69(5):719-26. https://doi.org/10.26402/jpp.2018.5.06.

Silva PCP, Brasil OO, Souto PLG, Moreira NH, Silva JP, Silva BDM, Ramos AF. Fixed-time artificial insemination protocols on brazilian locally adapted breed gilts on ovulatory response and embryo production. Anim Reprod. 2021;18(1):e20200776. http://dx.doi.org/10.1590/1984-3143-ar2020-0776. PMid:34122655.

Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN. Variation in Kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology. 2008a;149(11):5770-82. http://dx.doi.org/10.1210/en.2008-0581. PMid:18617612.

Smith JT, Rao A, Pereira A, Caraty A, Millar RP, Clarke IJ. Kisspeptin is present in ovine hypophysial portal blood but does not increase during the preovulatory luteinizing hormone surge: evidence that gonadotropes are not direct targets of kisspeptin in vivo. Endocrinology. 2008b;149(4):1951-9. http://dx.doi.org/10.1210/en.2007-1425. PMid:18162520.

Smith JT, Li Q, Yap KS, Shahab M, Roseweir AK, Millar RP, Clarke IJ. Kisspeptin is essential for the full preovulatory LH surge and stimulates GnRH release from the isolated ovine median eminence. Endocrinology. 2011;152(3):1001-12. http://dx.doi.org/10.1210/en.2010-1225. PMid:21239443.

Smith JT, Young IR, Veldhuis JD, Clarke IJ. Gonadotropin-inhibitory hormone (GnIH) secretion into the ovine hypophyseal portal system. Endocrinology. 2012;153(7):3368-75. http://dx.doi.org/10.1210/en.2012-1088. PMid:22549225.

Sonstegard T, Fahrenkrug S, Carlson D. Precision animal breeding to make genetically castrated animals for improved animal welfare and alternative breeding applications. J Anim Sci. 2017;95(suppl 2):149-50. http://dx.doi.org/10.2527/asasmw.2017.307.

Spergel DJ. Neuropeptidergic modulation of GnRH neuronal activity and GnRH secretion controlling reproduction: insights from recent mouse studies. Cell Tissue Res. 2019;375(1):179-91. http://dx.doi.org/10.1007/s00441-018-2893-z. PMid:30078104.

Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol. 2004;16(10):850-8. http://dx.doi.org/10.1111/j.1365-2826.2004.01240.x. PMid:15500545.

Thorson JF, Desaulniers AT, Lee C, White BR, Ford JJ, Lents CA. The role of RFamide-related peptide 3 (RFRP3) in regulation of the neuroendocrine reproductive and growth axes of the boar. Anim Reprod Sci. 2015;159:60-5. http://dx.doi.org/10.1016/j.anireprosci.2015.05.013. PMid:26051609.

Thorson JF, Heidorn NL, Ryu V, Czaja K, Nonneman DJ, Barb CR, Hausman GJ, Rohrer GA, Prezotto LD, McCosh RB, Wright EC, White BR, Freking BA, Oliver WT, Hileman SM, Lents CA. Relationship of neuropeptide FF receptors with pubertal maturation of gilts. Biol Reprod. 2017;96(3):617-34. http://dx.doi.org/10.1095/biolreprod.116.144998. PMid:28339619.

Thorson JF, Prezotto LD, Adams H, Petersen SL, Clapper JA, Wright EC, Oliver WT, Freking BA, Foote AP, Berry ED, Nonneman DJ, Lents CA. Energy balance affects pulsatile secretion of luteinizing hormone from the adenohypophesis and expression of neurokinin B in the hypothalamus of ovariectomized gilts†. Biol Reprod. 2018;99(2):433-45. http://dx.doi.org/10.1093/biolre/ioy069. PMid:30101293.

Thorson JF, Prezotto LD, Cardoso RC, Sharpton SM, Edwards JF, Welsh TH Jr, Riggs AC, Amstalden M, Gary GL. Hypothalamic distribution, adenohypophyseal receptor expression, and ligand functionality of rfamide-related peptide 3 in the mare during the breeding and nonbreeding seasons. Biol Reprod [serial on the Internet]. 2014 Feb 1 [cited 2021 Feb 27];90(2):1-9. Available from: https://academic.oup.com/biolreprod/article-lookup/doi/10.1095/biolreprod.113.112185

Tomikawa J, Homma T, Tajima S, Shibata T, Inamoto Y, Takase K, Inoue N, Ohkura S, Uenoyama Y, Maeda K, Tsukamura H. Molecular characterization and estrogen regulation of hypothalamic KISS1 gene in the pig. Biol Reprod. 2010;82(2):313-9. http://dx.doi.org/10.1095/biolreprod.109.079863. PMid:19828777.

Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O’Rahilly S, Semple RK. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet. 2009;41(3):354-8. http://dx.doi.org/10.1038/ng.306. PMid:19079066.

Treen AK, Luo V, Belsham DD. Phoenixin activates immortalized GnRH and kisspeptin neurons through the novel receptor GPR173. Mol Endocrinol. 2016;30(8):872-88. http://dx.doi.org/10.1210/me.2016-1039. PMid:27268078.

Tsutsumi R, Webster NJG. GnRH pulsatility, the pituitary response and reproductive dysfunction. Endocr J. 2009;56(6):729-37. http://dx.doi.org/10.1507/endocrj.K09E-185. PMid:19609045.

Weems PW, Lehman MN, Coolen LM, Goodman RL. The roles of neurokinins and endogenous opioid peptides in control of pulsatile LH secretion. In: Litwack G, editor. Vitamins and hormones [Internet]. USA: Elsevier; 2018 [cited 2021 Feb 27]. p. 89-135. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0083672918300116

Wójcik-Gładysz A, Polkowska J. Neuropeptide Y--a neuromodulatory link between nutrition and reproduction at the central nervous system level. Reprod Biol. 2006;6(Suppl. 2):21-8. PMid:17220938.

Wu M, Dumalska I, Morozova E, Van Den Pol AN, Alreja M. Gonadotropin inhibitory hormone inhibits basal forebrain vGluT2-gonadotropin-releasing hormone neurons via a direct postsynaptic mechanism. J Physiol. 2009;587(Pt 7):1401-11. http://dx.doi.org/10.1113/jphysiol.2008.166447. PMid:19204051.

Wylot B, Tworus K, Okrasa S. the effects of mu-, delta- and kappa-opioid receptor activation on luteinizing and follicle-stimulating hormone secretion from porcine pituitary cells. J Physiol Pharmacol. 2013;64(4):505-11. PMid:24101398.

Xu G, Li J, Zhang D, Su T, Li X, Cui S. HSP70 inhibits pig pituitary gonadotrophin synthesis and secretion by regulating the corticotropin-releasing hormone signaling pathway and targeting SMAD3. Domest Anim Endocrinol. 2021;74:106533. http://dx.doi.org/10.1016/j.domaniend.2020.106533. PMid:32992141.

Yang G, Su J, Yao Y, Lei Z, Zhang G, Li X. The regulatory mechanism of neuromedin S on luteinizing hormone in pigs. Anim Reprod Sci. 2010;122(3–4):367-74. http://dx.doi.org/10.1016/j.anireprosci.2010.10.011. PMid:21071159.

Yang G, Su J, Yao Y, Lei Z, Zhang G, Liu Y, Liu J, Li X. Distribution of neuromedin S and its receptor NMU2R in pigs. Res Vet Sci. 2012;92(2):180-6. http://dx.doi.org/10.1016/j.rvsc.2010.11.013. PMid:21185043.

Yano T, Iijima N, Kakihara K, Hinuma S, Tanaka M, Ibata Y. Localization and neuronal response of RFamide related peptides in the rat central nervous system. Brain Res. 2003;982(2):156-67. http://dx.doi.org/10.1016/S0006-8993(03)02877-4. PMid:12915251.

Yoshida H, Habata Y, Hosoya M, Kawamata Y, Kitada C, Hinuma S. Molecular properties of endogenous RFamide-related peptide-3 and its interaction with receptors. Biochim Biophys Acta. 2003;1593(2-3):151-7. PMid:12581859.

Yosten GLC, Lyu R-M, Hsueh AJW, Avsian-Kretchmer O, Chang J-K, Tullock CW, Dun SL, Dun N, Samson WK. A novel reproductive peptide, phoenixin. J Neuroendocrinol. 2013;25(2):206-15. http://dx.doi.org/10.1111/j.1365-2826.2012.02381.x. PMid:22963497.

Zhou D, Zhuo Y, Che L, Lin Y, Fang Z, Wu D. Nutrient restriction induces failure of reproductive function and molecular changes in hypothalamus–pituitary–gonadal axis in postpubertal gilts. Mol Biol Rep. 2014;41(7):4733-42. http://dx.doi.org/10.1007/s11033-014-3344-x. PMid:24728609.

Zmijewska A, Czelejewska W, Dziekonski M, Gajewska A, Franczak A, Okrasa S. Effect of kisspeptin and RFamide-related peptide-3 on the synthesis and secretion of LH by pituitary cells of pigs during the estrous cycle. Anim Reprod Sci. 2020;214:106275. http://dx.doi.org/10.1016/j.anireprosci.2020.106275. PMid:32087907.
 


Submitted date:
07/19/2021

Accepted date:
11/10/2021

61b0e34ca95395171d3d9d13 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections