Abstract
Melatonin, the key messenger of photoperiodic information, is synthesized in the pineal gland by arylalkylamine N-acetyltransferase enzyme (AANAT). It binds to specific receptors MT1 and MT2 located in the hypothalamus and pituitary gland. Melatonin can modulate the reproductive axis affecting the secretion of gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH). The South American plains vizcacha, Lagostomus maximus, shows natural poliovulation of up to 800 oocytes per estrous cycle, a 154-day long pregnancy, and reactivation of the reproductive axis at mid-gestation with pre-ovulatory follicular recruitment, presence of active corpora lutea, and variations of the endocrine status. Here we analyzed the involvement of melatonin in the modulation of the hypothalamic and pituitary gland physiology of vizcacha thorough several approaches, including histological localization of melatoninergic system components, assessment of melatoninergic components expression throughout the reproductive cycle, and evaluation of the effect of melatonin on hypothalamic and pituitary activities during the follicular and luteal phases of the estrous cycle. AANAT and melatonin receptors were localized in the pineal gland and preoptic area of the hypothalamus. Increase in pineal AANAT and serum melatonin expression was observed as pregnancy progressed, with the lowest hypothalamic MT1 and MT2 levels at mid-pregnancy. Pulsatility assays demonstrated that melatonin induces GnRH and LH secretion at luteal phase. The melatoninergic system effects on hypothalamic and pituitary gland hormones secretion during pregnancy pinpoint to melatonin as a potential key factor underlying the reactivation of the reproductive axis activity at mid-gestation.
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Acknowledgements
Authors are especially grateful to the Ministerio de Agroindustria, Dirección de Flora y Fauna of the Buenos Aires Province, Argentina, for enabling animal capture, to the personnel of ECAS for their invaluable help in trapping and handling the animals, to Sergio Ferraris MV and Fernando Lange MV and their veterinarian staff for their essential help on vizcachas handling and anesthetizing, to Ms. María Sol Clausi Schettini for her technical assistance in tissue processing, to Mr. Santiago Cicculli for his technical assistance in confocal microscopy, to Gaston Barbero PhD for his help with Western Blotting and to Mr. Geronimo Perazzo for his assistance in pulsatility assays.
Funding
This work was supported by CONICET [PIP No. 110/14], MINCyT [PICT-1281/2014] and by Fundación Científica Felipe Fiorellino, Universidad Maimónides, Argentina.
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Material preparation, data collection, and analysis were performed by SEC, PIFI, ARS, SAC, SP, MCC, and NPDG. JH, VL-L, ADV, and VBD contributed to the conception and design of the study. The draft of the manuscript was written by SEC and VBD, and all authors commented on the manuscript. All authors read and approved the final version of the manuscript.
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All the experimental procedures used in this study were reviewed and approved by the Institutional Committee on Use and Care of Experimental Animals (CICUAE) from Universidad Maimónides, Argentina (Resolution No. 7/2013) and conducted in accordance with the guidelines published in the National Institutes of Health (NIH) guide for the care and use of laboratory animals (National Research Council-USA, 2011). Capture and transport of animals were approved by the Ministerio de Agroindustria, Dirección de Flora y Fauna of the Buenos Aires Province, Argentina.
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Supplementary file1 (PDF 149 KB) Specific expression of AANAT, MT1 and MT2 in plains vizcacha, Lagostomus maximus. Representative images of AANAT (a), MT1 (b), and MT2 (c) protein expression determined by Western-blot in tissues of a non-pregnant plains vizcacha. CTX: brain cortex, PT: pituitary gland, HT: hypothalamus, OV: ovary, PN: pineal gland. A single band corresponding to the specific protein 23 kDa, 45 kDa, and 40 kDa was determined for AANAT, MT1, and MT2 respectively, in each assay
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Charif, S.E., Inserra, P.I.F., Schmidt, A.R. et al. Melatonin is involved in the modulation of the hypothalamic and pituitary activity in the South American plains vizcacha, Lagostomus maximus. J Comp Physiol B 192, 141–159 (2022). https://doi.org/10.1007/s00360-021-01405-6
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DOI: https://doi.org/10.1007/s00360-021-01405-6