The increase of cerebral microvessels vasodilation in anesthetized rats during acute normobaric hypoxia under the action of interleukin-1 beta
DOI:
https://doi.org/10.33910/2687-1270-2021-2-3-307-317Keywords:
acute normobaric hypoxia, cerebral microvessels, cytokine, interleukin-1 beta, NO-synthaseAbstract
With the administration of the pro-inflammatory cytokine interleukin- 1β (IL-1β), the features of the reactions of cerebral microvessels in anesthetized rats to progressively increasing acute normobaric hypoxia were studied. To confirm the hypothesis that the vasodilatory effects under deep hypoxia with an increase in the level of IL-1β may be associated with NO-dependent mechanisms, a non-selective inhibitor of NO-synthase L-NAME was additionally introduced. The study was carried out on 3 groups of anesthetized Wistar rat with intravenous injection: saline (control, 1 ml), IL-1β (500 ng) and the combined administration of non-selective inhibitor of NO-synthase L-NAME (10 mg/kg) and the same dose IL-1β. A progressive increase in hypoxia from normoxia up to apnea was carried out by using the “rebreathing” technique. Changes in the diameter of the arterial pial microvessels with an initial diameter of up to 50 μm were measured using vital microscopy. An increase in the vasodilation effect of hypoxia in rats under the influence of IL-1β was shown at an oxygen content in the respiratory mixture of 15% and the maximum effect—at a critical state of the body at an oxygen content of 6%. Preliminary inhibition of NO-synthase activity under the action of IL-1β prevented the vasodilation effect of hypoxia with a decrease in oxygen to 10% in the respiratory mixture and made it less expressed at an oxygen content of 4–6%. The results of this study confirm the increased vasodilation of cerebral microvessels with progressively increasing hypoxia under the influence of IL-1β and the participation of NO-dependent mechanisms in the application of this effect.
References
ЛИТЕРАТУРА
Донина, Ж. А., Баранова, Е. В., Александрова, Н. П. (2015) Сопряженные реакции дыхания и гемодинамики наркотизированных крыс на прогрессирующую острую нормобарическую гипоксию. Российский физиологический журнал им. И. М. Сеченова, т. 101, № 10, с. 1169–1180.
Донина, Ж. А., Баранова, Е. В., Александрова, Н. П. (2019) Ингибирование гиперпродукции оксида азота в условиях прогрессивно нарастающей гипоксии на фоне действия ИЛ-1β снижает выживаемость крыс после острой гипоксии. Российский физиологический журнал им. И. М. Сеченова, т. 105, № 12, с. 1514–1525. https://www.doi.org/10.1134/S0869813919120033
Донина, Ж. А., Баранова, Е. В., Александрова, Н. П. (2020) Влияние ингибирования циклооксигеназных путей на резистентность к нарастающей гипоксии у крыс с повышенным уровнем интерлейкина-1 бета. Российский физиологический журнал им. И. М. Сеченова, т. 106, № 11, с. 1400–1411. https://www.doi.org/10.31857/S0869813920110047
Ильина, А. Е., Станислав, М. Л., Денисов, Л. Н., Насонов, Е. Н. (2011) Интерлейкин-1 как медиатор воспаления и терапевтическая мишень. Научно-практическая ревматология, т. 49, № 5, с. 62–71.
Манухина, Е. Б., Малышев, И. Ю. (2003) Роль оксида азота в развитии и предупреждении дисфункции эндотелия. Вестник Витебского государственного медицинского университета, т. 2, № 2, с. 5–17.
Мельникова, Н. Н., Баранова, Е. В., Александрова, Н. П. (2018) Реакции церебральных микрососудов на острое гипоксическое воздействие при экзогенном повышении уровня интерлейкина-1β в крови. Российский физиологический журнал им. И. М. Сеченова, т. 104, № 9, с. 1086–1097. https://www.doi.org/10.7868/S0869813918090071
Насонов, Е. Л., Елисеев, М. С. (2016) Роль интерлейкина-1 в развитии заболеваний человека. Научно- практическая ревматология, т. 54, № 1, с. 60–77. https://doi.org/10.14412/1995-4484-2016-60-77
Рюмин, А. М., Отмахова, И. А., Собчак, Д. М. и др. (2018) Определение генетических полиморфизмов и концентрации цитокинов: перспективы использования в клинической практике на примере интерлейкина-1. Цитокины и воспаление, т. 17, № 1-4, с. 20–25.
Серебренникова, С. Н., Семинский, И. Ж., Семенов, Н. В., Гузовская, Е. В. (2012) Интерлейкин-1, интерлейкин-10 в регуляции воспалительного процесса. Сибирский медицинский журнал, т. 115, № 8, с. 5–7.
Симбирцев, А. С. (2001) Интерлейкин-1: от эксперимента в клинику. Медицинская иммунология, т. 3, № 3, с. 431–438.
Токмакова, Т. О., Пермякова, С. Ю., Киселева, А. В. и др. (2012) Мониторинг микроциркуляции в критических состояниях: возможности и ограничения. Общая реаниматология, т. 8, № 2, с. 74–78.
Фрейдлин, И. С., Шейкин, Ю. А. (2001) Эндотелиальные клетки в качестве мишеней и продуцентов цитокинов. Медицинская иммунология, т. 3, № 4, с. 499–514.
Черток, В. М., Коцюба, А. Е. (2012) Эндотелиальный (интимальный) механизм регуляции мозговой гемодинамики: трансформация взглядов. Тихоокеанский медицинский журнал, № 2 (48), с. 17–26.
Шинетова, Л. Е., Омар, А., Елубаева, Л. и др. (2017) Цитокины и артериальная гипертензия. Вестник Казахского Национального медицинского университета, № 1, с. 264–268.
Bohlen, H. G. (2015) Nitric oxide and the cardiovascular system. Comprehensive Physiology, vol. 5, no. 2, pp. 808–823. https://www.doi.org/10.1002/cphy.c140052
Corbett, J. A., Kwon, G., Turk, J., McDaniel, M. L. (1993) IL-1 beta induces the coexpression of both nitric oxide synthase and cyclooxygenase by islets of Langerhans: Activation of cyclooxygenase by nitric oxide. Biochemistry, vol. 32, no. 50, pp. 13767–13770. https://www.doi.org/10.1021/bi00213a002
Coyle, M. G., Oh, W., Stonestreet, B. S. (1993) Effects of indomethacin on brain blood flow and cerebral metabolism in hypoxic newborn piglets. American Journal of Physiology. Heart and Circulatory Physiology, vol. 264, no. 1, pp. H141–H149. https://www.doi.org/10.1152/ajpheart.1993.264.1.H141
Dinarello, C. A. (2009) Immunological and inflammatory functions of the interleukin-1 family. Annual Review of Immunology, vol. 27, pp. 519–550. https://www.doi.org/10.1146/annurev.immunol.021908.132612
Duchemin, S., Boily, M., Sadekova, N., Girouard, H. (2012) The complex contribution of NOS interneurons in the physiology of cerebrovascular regulation. Frontiers in Neural Circuits, vol. 6, article 51. https://www.doi.org/10.3389/fncir.2012.00051
Frangogiannis, N. G. (2015) Interleukin-1 in cardiac injury, repair, and remodeling: Pathophysiologic and translational concepts. Discoveries, vol. 3, no. 1, article e41. https://www.doi.org/10.15190/d.2015.33
Garlanda, C., Dinarello, C. A., Mantovani, A. (2013) The interleukin-1 family: Back to the future. Immunity, vol. 39, no. 6, pp. 1003–1018. https://www.doi.org/10.1016/j.immuni.2013.11.010
Hoiland, R. L., Bain, A. R., Rieger, M. G. et al. (2016) Hypoxemia, oxygen content, and the regulation of cerebral blood flow. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 310, no. 5, pp. R398–R413. https://www.doi.org/10.1152/ajpregu.00270.2015
Kellawan, J. M., Peltonen, G. L., Harrell, J. W. et al. (2019) Differential contribution of cyclooxygenase to basal cerebral blood flow and hypoxic cerebral vasodilation. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 318, no. 2, pp. R468–R479. https://www.doi.org/10.1152/ajpregu.00132.2019
Khazim, K., Azulay, E. E., Kristal, B., Cohen, I. (2018) Interleukin 1 gene polymorphism and susceptibility to disease. Immunology Review, vol. 281, pp. 40–56. https://www.doi.org/10.1111/imr.12620
Liu, X., Quan, N. (2018) Microglia and CNS interleukin-1: Beyond immunological concepts. Frontiers in Neurology, vol. 9, article 8. https://www.doi.org/10.3389/fneur.2018.00008
Lopalсo, G., Cantarini, L., Vitale, A. et al. (2015) Interleukin-1 as a common denominator from autoinflammatory to autoimmune disorders: Premises, perils, and perspectives. Mediators of Inflammation, vol. 2015, article 194864. https://www.doi.org/10.1155/2015/194864
Mantovani, A., Dinarello, C. A., Molgora, M., Garlanda, C. (2019) IL-1 and Related cytokines in the regulation of inflammation and immunity. Immunity, vol. 50, no. 4, pp. 778–795. https://www.doi.org/10.1016/j.immuni.2019.03.012
Monroy, M., Kuluz, J. W., He, D. et al. (2001) Role of nitric oxide in the cerebrovascular and thermoregulatory response to interleukin-1β. American Journal of Physiology. Heart and Circulatory Physiology, vol. 280, no. 4, pp. H1448–H1453. https://www.doi.org/10.1152/ajpheart.2001.280.4.H1448
Ridker, P. M., Everett, B. M., Thuren, T. et al. (2017) Antiinflammatory therapy with canakinumab for atherosclerotic disease. The New England Journal of Medicine, vol. 377, no. 12, pp. 1119–1131. https://www.doi.org/10.1056/NEJMoa1707914
Rothwel, N. J., Luheshi, G. N. (2000) Interleukin 1 in the brain: Biology, pathology and therapeutic target. Trends in Neurosciences, vol. 23, no. 12, pp. 618–625. https://www.doi.org/10.1016/s0166-2236(00)01661-1
Shibata, M., Parfenova, H., Zuckerman, S. L. et al. (1996) Interleukin-1 beta peptides induce cerebral pial arteriolar dilation in anesthetized newborn pigs. Regulatory, Integrative and Comparative Physiology, vol. 270, no. 5, pp. R1044–R1050. https://www.doi.org/10.1152/ajpregu.1996.270.5.R1044
Sriram, K., Laughlin, J. G., Rangamani, P., Tartakovsky, D. M. (2016) Shear-induced nitric oxide production by endothelial cells. Biophysical Journal, vol. 111, no. 1, pp. 208–221. https://www.doi.org/10.1016/j.bpj.2016.05.034
Wong, R., Lenart, N., Hill, L. et al. (2019) Interleukin-1 mediates ischaemic brain injury via distinct actions on endothelial cells and cholinergic neurons. Brain, Behavior, and Immunity, vol. 76, pp. 126–138. https://www.doi.org/10.1016/j.bbi.2018.11.012
REFERENCES
Bohlen, H. G. (2015) Nitric oxide and the cardiovascular system. Comprehensive Physiology, vol. 5, no. 2, pp. 808–823. https://www.doi.org/10.1002/cphy.c140052 (In English)
Chertok, V. M., Kotsyuba, A. E. (2012) Endotelial’nyj (intimal’nyj) mekhanizm regulyatsii mozgovoj gemodinamiki: transformatsiya vzglyadov [Endothelial (intimal) mechanism of cerebral hemodynamics regulation: Changing views]. Tikhookeanskij meditsinskij zhurnal — Pacific Medical Journal, no. 2 (48), p. 17–26. (In Russian)
Corbett, J. A., Kwon, G., Turk, J., McDaniel, M. L. (1993) IL-1 beta induces the coexpression of both nitric oxide synthase and cyclooxygenase by islets of Langerhans: Activation of cyclooxygenase by nitric oxide. Biochemistry, vol. 32, no. 50, pp. 13767–13770. https://www.doi.org/10.1021/bi00213a002 (In English)
Coyle, M. G., Oh, W., Stonestreet, B. S. (1993) Effects of indomethacin on brain blood flow and cerebral metabolism in hypoxic newborn piglets. American Journal of Physiology. Heart and Circulatory Physiology, vol. 264, no. 1, pp. H141–H149. https://www.doi.org/10.1152/ajpheart.1993.264.1.H141 (In English)
Dinarello, C. A. (2009) Immunological and inflammatory functions of the interleukin-1 family. Annual Review of Immunology, vol. 27, pp. 519–550. https://www.doi.org/10.1146/annurev.immunol.021908.132612 (In English)
Donina, Zh. A., Baranova, E. V., Aleksandrova, N. P. (2015) Sopryazhennye reaktsii dykhaniya i gemodinamiki narkotizirovannykh krys na progressiruyushchuyu ostruyu normobaricheskuyu gipoksiyu [Associated respiratory and hemodynamics response to acute normobaric progressive hypoxia in anesthetized rats]. Rossiyskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 101, no. 10, pp. 1169–1180. (In Russian)
Donina, Zh. A., Baranova, E. V., Aleksandrova, N. P. (2019) Ingibirovanie giperproduktsii oksida azota v usloviyakh progressivno narastayushchej gipoksii na fone dejstviya IL-1β snizhayet vyzhivayemost’ krys posle ostroj gipoksii [Inhibition of the hyperproduction of nitric oxide during progressively increasing hypoxia under the action of IL-1β reduces the survival of rats after acute hypoxia]. Rossiyskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 105, no. 12, pp. 1514–1525. https://www.doi.org/10.1134/S0869813919120033 (In Russian)
Donina, Zh. A., Baranova, E. V., Aleksandrova, N. P. (2020) Vliyaniye ingibirovaniya tsiklooksigenaznykh putej na rezistentnost’ k narastayushchej gipoksii u krys s povyshennym urovnem interlejkina-1 beta [Influence of inhibition of cyclooxygenase pathways on hypoxic resistance in rats with increased levels of interleukin-1β]. Rossiyskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 106, no. 11, pp. 1400–1411. https://www.doi.org/10.31857/S0869813920110047 (In Russian)
Duchemin, S., Boily, M., Sadekova, N., Girouard, H. (2012) The complex contribution of NOS interneurons in the physiology of cerebrovascular regulation. Frontiers in Neural Circuits, vol. 6, article 51. https://www.doi.org/10.3389/fncir.2012.00051 (In English)
Frangogiannis, N. G. (2015) Interleukin-1 in cardiac injury, repair, and remodeling: Pathophysiologic and translational concepts. Discoveries, vol. 3, no. 1, article e41. https://www.doi.org/10.15190/d.2015.33 (In English)
Freidlin, I. S., Sheikine, Y. A. (2001) Endotelialnye kletki v kachestve mishenej i produtsentov tsitokinov [Endothelial cells as targets and producers of cytokines]. Meditsinskaya immunologiya — Medical Immunology (Russia), vol. 3, no. 4, pp. 499–514. (In Russian)
Garlanda, C., Dinarello, C. A., Mantovani, A. (2013) The interleukin-1 family: Back to the future. Immunity, vol. 39, no. 6, pp. 1003–1018. https://www.doi.org/10.1016/j.immuni.2013.11.010 (In English)
Hoiland, R. L., Bain, A. R., Rieger, M. G. et al. (2016) Hypoxemia, oxygen content, and the regulation of cerebral blood flow. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 310, no. 5, pp. R398–R413. https://www.doi.org/10.1152/ajpregu.00270.2015 (In English)
Ilyina, A. E., Stanislav, M. L., Denisov, L. N., Nasonov, E. L. (2011) Interleykin-1 kak mediator vospaleniya i terapevticheskaya mishen’ [Interleukin-1 as an inflammation mediator and a therapeutic target]. Nauchno-prakticheskaya revmatologiya — Rheumatology Science and Practice, vol. 49, no. 5, pp. 62–71. (In Russian)
Kellawan, J. M., Peltonen, G. L., Harrell, J. W. et al. (2019) Differential contribution of cyclooxygenase to basal cerebral blood flow and hypoxic cerebral vasodilation. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 318, no. 2, pp. R468–R479. https://www.doi.org/10.1152/ajpregu.00132.2019 (In English)
Khazim, K., Azulay, E. E., Kristal, B., Cohen, I. (2018) Interleukin 1 gene polymorphism and susceptibility to disease. Immunology Review, vol. 281, pp. 40–56. https://www.doi.org/10.1111/imr.12620 (In English)
Liu, X., Quan, N. (2018) Microglia and CNS interleukin-1: Beyond immunological concepts. Frontiers in Neurology, vol. 9, article 8. https://www.doi.org/10.3389/fneur.2018.00008 (In English)
Lopalko, G., Cantarini, L., Vitale, A. et al. (2015) Interleukin-1 as a common denominator from autoinflammatory to autoimmune disorders: Premises, perils, and perspectives. Mediators of Inflammation, vol. 2015, article 194864. https://www.doi.org/10.1155/2015/194864 (In English)
Mantovani, A., Dinarello, C. A., Molgora, M., Garlanda, C. (2019) IL-1 and Related cytokines in the regulation of inflammation and immunity. Immunity, vol. 50, no. 4, pp. 778–795. https://www.doi.org/10.1016/j.immuni.2019.03.012 (In English)
Manukhina, E. B., Malyshev, I. Yu. (2003) Rol’ oksida azota v razvitii i preduprezhdenii disfunktsii endoteliya [The role of nitric oxide in the development and prevention of endothelial dysfunction]. Vestnik Vitebskogo gosudarstvennogo meditsinskogo universiteta — Vestnik of Vitebsk State Medical University, vol. 2, no. 2, pp. 5–17. (In Russian)
Melnikova, N. N., Baranova, E. V., Aleksandrova, N. P. (2018) Reaktsii tserebral’nykh mikrososudov na ostroe gipoksicheskoe vozdejstvie pri ekzogennom povyshenii urovnya interlejkina-1β v krovi [Reactions of cerebral microwaves on acute hypoxic impact in exogenous improvement of interleykin-1β level in blood]. Rossiyskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 104, no. 9, pp. 1086–1097. https://www.doi.org/10.7868/S0869813918090071 (In Russian)
Monroy, M., Kuluz, J. W., He, D. et al. (2001) Role of nitric oxide in the cerebrovascular and thermoregulatory response to interleukin-1β. American Journal of Physiology. Heart and Circulatory Physiology, vol. 280, no. 4, pp. H1448–H1453. https://www.doi.org/10.1152/ajpheart.2001.280.4.H1448 (In English)
Nasonov, E. L., Eliseev, M. S. (2016) Rol’ interlejkina-1 v razvitii zabolevanij cheloveka [Role of interleukin-1 in the development of human diseases]. Nauchno-prakticheskaya revmatologiya — Rheumatology Science and Practice, vol. 54, no. 1, pp. 60–77. https://doi.org/10.14412/1995-4484-2016-60-77 (In Russian)
Ridker, P. M., Everett, B. M., Thuren, T. et al. (2017) Antiinflammatory therapy with canakinumab for atherosclerotic disease. The New England Journal of Medicine, vol. 377, no. 12, pp. 1119–1131. https://www.doi.org/10.1056/NEJMoa1707914 (In English)
Rothwel, N. J., Luheshi, G. N. (2000) Interleukin 1 in the brain: Biology, pathology and therapeutic target. Trends in Neurosciences, vol. 23, no. 12, pp. 618–625. https://www.doi.org/10.1016/s0166-2236(00)01661-1 (In English)
Ryumin, A. M., Otmakhova, I. A., Sobchak, D. M. et al. (2018) Opredelenie geneticheskikh polimorfizmov i kontsentratsii tsitokinov: perspektivy ispol’zovaniya v klinicheskoj praktike na primere interlejkina 1 [Determination of genetic polymorphisms and cytokine concentrations: Prospects for use in clinical practice by the example of interleukin 1]. Tsitokiny i vospalenie — Cytokines and Inflammation, vol. 17, no. 1-4, pp. 20–25. (In Russian)
Serebrennikova, S. N., Seminsky, I. G., Semenov, N. V., Guzovskaya, E. V. (2012) Interlejkin-1, interlejkin-10 v regulyatsii vospalitel’nogo protsessa [Interleukin-1, interleukin-10 in regulation of inflammatory process]. Sibirskij meditsinskij zhurnal — Siberian Medical Journal (Irkutsk), vol. 115, no. 8, pp. 5–7. (In Russian)
Shibata, M., Parfenova, H., Zuckerman, S. L. et al. (1996) Interleukin-1 beta peptides induce cerebral pial arteriolar dilation in anesthetized newborn pigs. Regulatory, Integrative and Comparative Physiology, vol. 270, no. 5, pp. R1044–R1050. https://www.doi.org/10.1152/ajpregu.1996.270.5.R1044 (In English)
Shinetova, L. E., Omar, A., Elubaeva, L. et al. (2017) Tsitokiny i arterial’naya gipertenziya [Cytokines and hypertension]. Vestnik Kazakhskogo Natsional’nogo meditsinskogo universiteta — Vestnik of Kazakh National Medical University, no. 1, pp. 264–268. (In Russian)
Simbirtsev, A. S. (2001) Interlejkin-1: ot eksperimenta v kliniku [Eukin-1: From experiment to clinic]. Meditsinskaya immunologiya — Medical Immunology (Russia), vol. 3, no. 3, pp. 431–438. (In Russian)
Sriram, K., Laughlin, J. G., Rangamani, P., Tartakovsky, D. M. (2016) Shear-induced nitric oxide production by endothelial cells. Biophysical Journal, vol. 111, no. 1, pp. 208–221. https://www.doi.org/10.1016/j.bpj.2016.05.034 (In English)
Tokmakova, T. O., Permyakova, S. Yu., Kiseleva, A. V. et al. (2012) Monitoring mikrotsirkulyatsii v kriticheskikh sostoyaniyakh: vozmozhnosti i ogranicheniya [Monitoring the microcirculation in critical conditions: Possibilities and limitations]. Obshchaya reanimatologiya — General Reanimatology, vol. 8, no. 2, pp. 74–78. (In Russian)
Wong, R., Lenart, N., Hill, L. et al. (2019) Interleukin-1 mediates ischaemic brain injury via distinct actions on endothelial cells and cholinergic neurons. Brain, Behavior, and Immunity, vol. 76, pp. 126–138. https://www.doi.org/10.1016/j.bbi.2018.11.012 (In English)
Downloads
Published
Issue
Section
License
Copyright (c) 2021 Nadezhda N. Melnikova
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The work is provided under the terms of the Public Offer and of Creative Commons public license Attribution-NonCommercial 4.0 International (CC BY-NC 4.0). This license allows an unlimited number of persons to reproduce and share the Licensed Material in all media and formats. Any use of the Licensed Material shall contain an identification of its Creator(s) and must be for non-commercial purposes only.
