Comparative characteristics of vasopressinergic neurons of the supraoptic and paraventricular nuclei of hypothalamus response in the intermittent hypoxic hypoxia
DOI:
https://doi.org/10.14739/2310-1237.2018.3.151862Keywords:
Arg-vasopressin, cFos protein, hypoxiainducible factor, hypothalamus, hypoxiaAbstract
The vasopressinergic system of the hypothalamus occupies an important place in the neuroendocrine mechanisms of maintaining homeostasis, controlling autonomic reactions and the processes of adaptation of the organism to the acute and chronic stressors. The main portion of the magnocellular vasopressin-synthesizing neurons is localized in the supraoptic nucleus (SON) and in the lateral part of the posterior magnocellular subnuclei of the paraventricular nucleus (PVNpml).The aim of study was to establish the features of the vasopressinergic neurons of the hypothalamus magnocellular nuclei functional state under the inflence of prolonged intermittent hypoxic hypoxia and in the post-hypoxic period.
Materials and methods. The research was carried out on 30 male Wistar rats. Intermittent hypoxia was modeled by daily 6 hour stay of rats at the simulated altitude of 6000 m (pO2 = 9.8 %) for 15 days, the post-hypoxic period lasted 10 days. The distribution of [Arg8]-vasopressin (AVP), cFos, HIF-1α, and HIF-3α proteins was investigated by quantitative immunoflorescence methods in serial frontal sections of hypothalamus.
Results. The hypoxic hypoxia action led to SON neurons degeneration, inhibition of AVP synthesis in SON by 40 %, decrease of cFos protein content by 56 %, and the failure of reaction to hypoxia from the HIF-proteins family. In PVNpml neurons, intermittent hypoxia stimulated 6-fold increase in the AVP content along with cFos-protein increase by 80%. The response of PVNpml neurons to hypoxia was accompanied by 3-times increase of the HIF family proteins content. In the post-hypoxic ially restored in SON neurons, but decrease of cFos-protein synthesis indicated inhibition of secretory activity in SON. In the post-hypoxic period the content of the AVP and the HIF-proteins decreased signifiantly in PVNpml neurons, but the level of all proteins remained higher than in the control group. At the same time, the level of cFos secretory activity did not change signifiantly as compared with the hypoxic period. These data indicate the stability of the high level of functional activity of the PVNpml asopressinergic neurons during the 10-day post-hypoxic period.
Conclusions. Intermittent hypoxia stimulates the functional activity of the PVNpml that manifests as an increase of vasopressin, cFos, HIF-1α, and HIF-3α proteins synthesis in magnocellular neurons. In the post-hypoxic period, a slight decrease in the synthesis of vasopressin, HIF-1α and HIF-3α proteins is observed without a decrease in the cFos protein content in PVNpml.
Intermittent hypoxia inhibits the functional activity of SON neurons, which is partially restored in the post-hypoxic period.
References
Bankir, L., Bichet, D. G., & Morgenthaler, N. G. (2017) Vasopressin: physiology, assessment and osmosensation. J Intern Med., 282(4), 284–97. doi: 10.1111/joim.12645.
Shell, B., Faulk, K., & Cunningham, J. T. (2016) Neural control of blood pressure in chronic intermittent hypoxia. Curr Hypertens Rep., 18(3), 19. doi: 10.1007/s11906-016-0627-8.
Szczepanska-Sadowska, E., Czarzasta, K., & Cudnoch-Jedrzejewska, A. (2018) Dysregulation of the renin-angiotensin system and the vasopressinergic system interactions in cardiovascular disorders. Current Hypertension Reports., 20(3), 19. doi: 10.1007/s11906-018-0823-9.
McEwen, B. S. (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev., 87(3), 873–904. doi: 10.1152/physrev.00041.2006.
Nicolaides, N. C., Kyratzi, E., Lamprokostopoulou, A., Chrousos, G. P., & Charmandari, E. (2015) Stress, the stress system and the role of glucocorticoids. Neuroimmunomodulation, 22(1–2), 6–19. doi: 10.1159/000362736.
Volpi, S., Rabadan-Diehl, C., & Aguilera, G. (2004) Vasopressinergic regulation of the hypothalamic pituitary adrenal axis and stress adaptation. Stress., 7(2), 75–83. doi: 10.1080/10253890410001733535.
Sivukhina, E. V., & Jirikowski, G. F. (2016) Magnocellular hypothalamic system and its interaction with the hypothalamo-pituitary-adrenal axis. Steroids, 111, 21–8. doi: 10.1016/j.steroids.2016.01.008.
Silverman, A. J., & Zimmerman, E. A. (1983) Magnocellular neurosecretory system. Annu Rev Neurosci., 6, 357–80. doi: 10.1146/annurev.ne.06.030183.002041.
Swanson, L. W., & Sawchenko, P. E. (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci., 6, 269–324. doi: 10.1146/annurev.ne.06.030183.001413.
Ramirez, J-M., Folkow, L. P., & Blix, A. S. (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol., 69, 113–43. doi: 10.1146/annurev.physiol.69.031905.163111.
Berezovskij, V. A. (2012) Prirodnaya i instrumental'naya oroterapiya [Natural and instrumental orotherapy]. Doneck: Zaslavskij A.Yu. [in Russian].
Karash, Yu. M., Strelkov, R. B., & Chizhov, F. Ya. (1988) Normobaricheskaya gipoksiya v lechenii, profilaktike i reabilitacii [Normobaric hypoxia in the treatment, prevention and rehabilitation]. Moscow : Medicina. [in Russian].
Coldren, K. M., Li, D. P., Kline, D. D., Hasser, E. M., & Heesch, C. M. (2017) Acute hypoxia activates neuroendocrine, but not presympathetic, neurons in the paraventricular nucleus of the hypothalamus: differential role of nitric oxide. Am J Physiol Regul Integr Comp Physiol., 312(6), R982–95. doi: 10.1152/ajpregu.00543.2016.
Abramov, A. V. (1998) Vliyanie interval'nykh gipoksicheskikh trenirovok na funkcional'noye sostoyanie peptidergicheskikh nejronov paraventrikulyarnogo yadra gipotalamusa i nejronov stvola mozga krys [The effect of interval hypoxic training on the functional state of the peptidergic neurons of the paraventricular nucleus of the hypothalamus and rat brainstem neurons]. Rossijskij fiziologicheskij zhurnal im. I.M. Sechenova, 84(3), 173–81. [in Russian].
Kolesnik, Yu. M., Orestenko, Yu. N., & Abramov, A. V. (1993) Sostoyanie vazopressin-, oksitocin- i kortikoliberinsinteziruyushchikh struktur gipotalamusa u krys s sakharnym diabetom pri gipoksicheskikh vozdejstviyakh [The state of vasopressin-, oxytocin- and corticoliberin-synthesizing structures of the hypothalamus in diabetic rats with hypoxic effects]. Rossijskij fiziologicheskij zhurnal im. I.M. Sechenova, 79(9), 34–42. [in Russian].
Ramirez, G., Hammond, M., Agosti, S. J., Bittle, P. A., Dietz, J. R., & Colice, G. L. (1992) Effects of hypoxemia at sea level and high altitude on sodium excretion and hormonal levels. Aviat Space Environ Med., 63(10), 891–8.
Robach, P., Lafforgue, E., Olsen, N. V., De´chaux, M., Fouqueray, B., Westerterp-Plantenga, M., et al. (2002) Recovery of plasma volume after 1 week of exposure at 4,350 m. Pflugers Arch., 444(6), 821–8. doi: 10.1007/s00424-002-0894-x.
Rostrup, M. (1998) Catecholamines, hypoxia and high altitude. Acta Physiol Scand, 162(3), 389–399. doi: 10.1046/j.1365-201X.1998.00335.x.
Myers, D. A., & Ducsay, C. A. (2014) Altitude, attitude and adaptation. Advances in Experimental Medicine and Biology, 814, 147–57. doi: 10.1007/978-1-4939-1031-1_13.
Ostergaard, L., Rudiger, A., Wellmann, S., Gammella, E., BeckSchimmer, B., Struck, J., et al. (2014) Argininevasopressin marker copeptin is a sensitive plasma surrogate of hypoxic exposure. Hypoxia., 2, 143–51. doi: 10.2147/HP.S57894.
Summanen, M., Bäck, S., Voipio, J., & Kaila, K. (2018) Surge of peripheral arginine vasopressin in a rat model of birth asphyxia. Front Cell Neurosci., 12, 2. doi: 10.3389/fncel.2018.00002.
Pirs, E. (1962) Gistokhimiya [Histochemistry]. Moscow : Izd-vo in. lit. [in Russian].
Gajdyshev, I. P. (2004) Reshenie nauchnykh i inzhenernykh zadach sredstvami Excel, VBA i C/C++ [Solving scientific and engineering problems with Excel, VBA and C / C ++]. SPb. : BKHV–Peterburg. [in Russian].
Bonfiglio, J. J., Inda, C., Refojo, D., Holsboer, F., Arzt, E., & Silberstein, S. (2011) The corticotropin-releasing hormone network and the hypothalamic-pituitary-adrenal axis: molecular and cellular mechanisms involved. Neuroendocrinology, 94(1), 12–20. doi: 10.1159/000328226.
Keller-Wood, M. (2015) Hypothalamic-pituitary-adrenal axis–feedback control. Compr Physiol., 5(3), 1161–82. doi: 10.1002/cphy.c140065.
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) Glucocorticoid actions on synapses, circuits, and behavior: Implications for the energetics of stress. Frontiers in Neuroendocrinolog, 35(2), 180–96. doi: 10.1016/j.yfrne.2013.12.003.
Sivukhina, E. V., & Jirikowski, G. F. (2014) Adrenal steroids in the brain: Role of the intrinsic expression of corticosteroid-binding globulin (CBG) in the stress response. Steroids., 81, 70–3. doi: 10.1016/j.steroids.2013.11.001.
Han, F., Ozawa, H., Matsuda, K., Nishi, M., & Kawata, M. (2005) Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus. Neuroscience Research., 51(4), 371–81. doi: 10.1016/j.neures.2004.12.013.
Aguilera, G., & Rabadan-Diehl, C. (2000) Vasopressinergic regulation of the hypothalamic–pituitary–adrenal axis: implications for stress adaptation. Regulatory Peptides., 96(1–2), 23–9. doi: 10.1016/S0167-0115(00)00196-8.
Rotondo, F., Butz, H., Syro, L., Yousef, G., Di Ieva, A. D., Restrepo, L. M., et al. (2016) Arginine vasopressin (AVP): a review of its historical perspectives, current research and multifunctional role in the hypothalamo-hypophysial system. Pituitary., 19(4), 345–55. doi: 10.1007/s11102-015-0703-0.
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