Effect of melatonin from slow-release implants on aquaporins (AQP1 and AQP4) in the ovine choroid plexus

https://doi.org/10.17221/6/2017-CJASCitation:Szczepkowska A., Skowroński M.T., Kowalewska M., Milewski S., Skipor J. (2018): Effect of melatonin from slow-release implants on aquaporins (AQP1 and AQP4) in the ovine choroid plexus. Czech J. Anim. Sci., 63: 32-42.
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Aquaporins (AQPs) play important role in the cerebrospinal fluid (CSF) secretion and AQP1 and AQP4 are localized in the choroid plexus (CP), which is the main place of CSF production. In ewes, seasonally breeding animals, the turnover rate (TOR) of CSF is photoperiodically modulated and melatonin, a biochemical signal about changing photoperiod, is used to advance the onset of the breeding season by mimicking the stimulatory effect of short days (SD). This study evaluates the effect of melatonin implantation during long days (LD) on AQPs expression in the ovine CP. Studies were performed on ovariectomized, estradiol implanted ewes treated with placebo (n = 6) or with melatonin (n = 6) during LD. Ewes were sacrificed 40 days after melatonin/placebo implantation and CPs from the lateral/third brain ventricles were collected for Real-time and Western blot analyses. Additionally, for immunohistochemical analysis, CP samples were collected from ewes (n = 3) sacrificed during LD. We demonstrated an apical membrane localization of AQP1 and a diffused distribution of AQP4 in the epithelial cells of CP. The mRNA expression of AQP1 was 20 times higher than the expression of all AQP4 isoforms, and among them AQP4 isoforms containing exon 2 constituted approximately 38%. The melatonin implantation significantly (P < 0.05) increased the mRNA expression of AQP1 and AQP4 and the protein level of AQP4 isoforms (33 and 28 kDa). For AQP1 we observed a significant (P < 0.05) decrease of glycosylated (33 kDa) and a significant (P < 0.05) increase of unglycosylated (23 kDa) predominant protein form. Therefore it can be suggested that at least AQP1, which is involved in CSF production and has been demonstrated to be modulated by melatonin implantation, is linked with the photoperiodic modulation of the CSF production in ewes.
Adam Clare L., Findlay Patricia A., Miller David W. (2006): Blood-Brain Leptin Transport and Appetite and Reproductive Neuroendocrine Responses to Intracerebroventricular Leptin Injection in Sheep: Influence of Photoperiod. Endocrinology, 147, 4589-4598 https://doi.org/10.1210/en.2006-0576
Agre Peter, King Landon S., Yasui Masato, Guggino Wm B., Ottersen Ole Petter, Fujiyoshi Yoshinori, Engel Andreas, Nielsen Søren (2002): Aquaporin water channels - from atomic structure to clinical medicine. The Journal of Physiology, 542, 3-16 https://doi.org/10.1113/jphysiol.2002.020818
Chemineau P., Malpaux B., Delgadillo J.A., Guérin Y., Ravault J.P., Thimonier J., Pelletier J. (1992): Control of sheep and goat reproduction: Use of light and melatonin. Animal Reproduction Science, 30, 157-184 https://doi.org/10.1016/0378-4320(92)90010-B
Cogé F, Guenin SP, Fery I, Migaud M, Devavry S, Slugocki C, Legros C, Ouvry C, Cohen W, Renault N, Nosjean O, Malpaux B, Delagrange P, Boutin JA (2009): The end of a myth: cloning and characterization of the ovine melatonin MT2 receptor. British Journal of Pharmacology, 158, 1248-1262 https://doi.org/10.1111/j.1476-5381.2009.00453.x
Fraser S., Cowen P., Franklin M., Francy C., Arendt J. (1983): Direct radioimmunoassay for plasma melatonin. Clinical Chemistry, 29, 386–397.
Guesdon Vanessa, Malpaux Benoît, Delagrange Philippe, Spedding Michael, Cornilleau Fabien, Chesneau Didier, Haller József, Chaillou Elodie (2013): Rapid effects of melatonin on hormonal and behavioral stressful responses in ewes. Psychoneuroendocrinology, 38, 1426-1434 https://doi.org/10.1016/j.psyneuen.2012.12.011
Herman AP, Misztal T, Herman A (2010): Expression of Interleukin (IL)-1β and IL-1 Receptors Genes in the Hypothalamus of Anoestrous Ewes after Lipopolysaccharide Treatment. Reproduction in Domestic Animals, 45, e426-e433 https://doi.org/10.1111/j.1439-0531.2010.01595.x
Herman Andrzej P., Krawczyńska Agata, Bochenek Joanna, Antushevich Hanna, Herman Anna, Tomaszewska-Zaremba Dorota (2014): Peripheral Injection of SB203580 Inhibits the Inflammatory-Dependent Synthesis of Proinflammatory Cytokines in the Hypothalamus. BioMed Research International, 2014, 1-10 https://doi.org/10.1155/2014/475152
Kaur C., Sivakumar V., Zhang Y., Ling E. A. (2006): Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia, 54, 826-839 https://doi.org/10.1002/glia.20420
King Landon S., Agre Peter (1996): Pathophysiology of the Aquaporin Water Channels. Annual Review of Physiology, 58, 619-648 https://doi.org/10.1146/annurev.ph.58.030196.003155
Kowalewska M., Szczepkowska A., Herman A.P., Pellicer-Rubio M.T., Jałyński M., Skipor J. (2017): Melatonin from slow-release implants did not influence the gene expression of the lipopolysaccharide receptor complex in the choroid plexus of seasonally anoestrous adult ewes subjected or not to a systemic inflammatory stimulus. Small Ruminant Research, 147, 1-7 https://doi.org/10.1016/j.smallrumres.2016.11.018
Lagaraine Christine, Skipor Janina, Szczepkowska Aleksandra, Dufourny Laurence, Thiery Jean-Claude (2011): Tight junction proteins vary in the choroid plexus of ewes according to photoperiod. Brain Research, 1393, 44-51 https://doi.org/10.1016/j.brainres.2011.04.009
Li X., Kong H., Wu W., Xiao M., Sun X., Hu G. (2009): Aquaporin-4 maintains ependymal integrity in adult mice. Neuroscience, 162, 67-77 https://doi.org/10.1016/j.neuroscience.2009.04.044
Lincoln G. A., Clarke I. J. (1994): Photoperiodically-lnduced Cycles in the Secretion of Prolactin in Hypothalamo-Pituitary Disconnected Rams: Evidence for Translation of the Melatonin Signal in the Pituitary Gland. Journal of Neuroendocrinology, 6, 251-260 https://doi.org/10.1111/j.1365-2826.1994.tb00580.x
Misztal T., Romanowicz K., Barcikowski B. (1996): Effects of melatonin infused into the III ventricle on prolactin, beta-endorphin and luteotropin secretion in ewes during the different stages of the reproductive cycle. Acta Neurobiologiae Experimentalis, 56, 769–778.
Moe Svein Erik, Sorbo Jan Gunnar, Sogaard Rikke, Zeuthen Thomas, Petter Ottersen Ole, Holen Torgeir (2008): New isoforms of rat Aquaporin-4. Genomics, 91, 367-377 https://doi.org/10.1016/j.ygeno.2007.12.003
Nazari Z., Nabiuni M., Nejad Z.S., Delfan B., Irian S. (2015): Expression of aquaporins in the rat choroid plexus. Archives of Neuroscience, 2, e17312.
Neely John D., Christensen Birgitte M., Nielsen Søren, Agre Peter (1999): Heterotetrameric Composition of Aquaporin-4 Water Channels . Biochemistry, 38, 11156-11163 https://doi.org/10.1021/bi990941s
Nesic O., Lee J., Unabia G. C., Johnson K., Ye Z., Vergara L., Hulsebosch C. E., Perez-Polo J. R. (2008): Aquaporin 1 – a novel player in spinal cord injury. Journal of Neurochemistry, 105, 628-640 https://doi.org/10.1111/j.1471-4159.2007.05177.x
Nielsen S., Smith B. L., Christensen E. I., Agre P. (1993): Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia.. Proceedings of the National Academy of Sciences, 90, 7275-7279 https://doi.org/10.1073/pnas.90.15.7275
Oshio K., Watanabe H., Song Y., Verkman A.S., Manley G.T. (2005): Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB Journal, 19, 76–78.
Owler B.K., Pitham T., Wang D. (2010): Aquaporins: relevance to cerebrospinal fluid physiology and therapeutic potential in hydrocephalus. Cerebrospinal Fluid Research, 7, 15.
Ron N.P., Kazianis J.A., Padbury J.F., Brown C.M., McGonnigal B.G., Sysyn G.D., Sadowska G.B., Stonestreet B.S. (2005): Ontogeny and the effects of corticosteroid pretreatment on aquaporin water channels in the ovine cerebral cortex. Reproduction, Fertility and Development, 17, 535–542.https://doi.org/10.1071/RD03044
Skipor J., Thiery J.C. (2008): The choroid plexus–cerebrospinal fluid system: undervaluated pathway of neuroendocrine signaling into the brain. Acta Neurobiologiae Experimentalis, 68, 414–428.
Skowronski M. T., Lebeck J., Rojek A., Praetorius J., Fuchtbauer E.-M., Frokiaer J., Nielsen S. (2006): AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. AJP: Renal Physiology, 292, F956-F965 https://doi.org/10.1152/ajprenal.00314.2006
Speake Tracey, Freeman Lyle J., Brown Peter D. (2003): Expression of aquaporin 1 and aquaporin 4 water channels in rat choroid plexus. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1609, 80-86 https://doi.org/10.1016/S0005-2736(02)00658-2
Szczepkowska Aleksandra, Wąsowska Barbara, Gilun Przemysław D., Lagaraine Christine, Robert Vincent, Dufourny Laurence, Thiéry Jean-Claude, Skipor Janina (2012): Pattern of expression of vascular endothelial growth factor and its receptors in the ovine choroid plexus during long and short photoperiods. Cell and Tissue Research, 350, 157-166 https://doi.org/10.1007/s00441-012-1431-7
Thiery J. C., Robel P., Canepa S., Delaleu B., Gayrard V., Picard-Hagen N., Malpaux B. (2003): Passage of progesterone into the brain changes with photoperiod in the ewe. European Journal of Neuroscience, 18, 895-901 https://doi.org/10.1046/j.1460-9568.2003.02796.x
Thiery Jean-Claude, Lomet Didier, Schumacher Michael, Liere Philippe, Tricoire Helene, Locatelli Alain, Delagrange Philippe, Malpaux Benoit (2006): Concentrations of estradiol in ewe cerebrospinal fluid are modulated by photoperiod through pineal-dependent mechanisms. Journal of Pineal Research, 41, 306-312 https://doi.org/10.1111/j.1600-079X.2006.00370.x
Thiery Jean-Claude, Lomet Didier, Bougoin Sylvain, Malpaux Benoit (2009): Turnover rate of cerebrospinal fluid in female sheep: changes related to different light-dark cycles. Cerebrospinal Fluid Research, 6, 9- https://doi.org/10.1186/1743-8454-6-9
Venero J.L., Vizuete M.L., Ilundáin A.A., Machado A., Echevarria M., Cano J. (1999): Detailed localization of aquaporin-4 messenger RNA in the CNS: preferential expression in periventricular organs. Neuroscience, 94, 239-250 https://doi.org/10.1016/S0306-4522(99)00182-7
Venero José L., Vizuete Marı́a L., Machado Alberto, Cano Josefina (2001): Aquaporins in the central nervous system. Progress in Neurobiology, 63, 321-336 https://doi.org/10.1016/S0301-0082(00)00035-6
Zhao Sheng, Fernald Russell D. (2005): Comprehensive Algorithm for Quantitative Real-Time Polymerase Chain Reaction. Journal of Computational Biology, 12, 1047-1064 https://doi.org/10.1089/cmb.2005.12.1047
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