NEUROPROTECTIVE EFFECT OF ERYTHROPOETIN IN EXPERIMENTAL CEREBRAL ISCHEMIA
Keywords:
Сerebral ischemia, erythropoietin, neurological status, morphology
Abstract
The presence of receptors for erythropoietin (EPO) on neurons and endothelial cells, its involvement in the embryogenesis of the nervous tissue suggests the EPO neuroprotective effect in the ischemic damage of the brain. The aim of the study was to investigate the EPO effect on the neurological status, microcirculation and morphology of the lesion focus in experimental cerebral ischemia (ECI). Materials and Methods. The study was performed on 70 nonlinear rats. ECI was modeled by the diathermocoagulation of the pial vessels in the sagittal suture projection between the fronto-parietal and parieto-occipital sutures. EPO was used at a dose of 5000 IU/kg with the interval of 3, 24 and 48 hours. The Garcia scale was used to assess the animals' neurological status. Microcirculation in the cerebral cortex tissues was determined by laser Doppler fluorimetry. The number of unmodified neurons, neurons with chromatolysis and shadow cells, and the number of small blood vessels were counted on the area unit in the brain sections in the ischemic damage focus. Results. In rats with ECI, the integral index of neurological status estimated by the Garcia scale decreases on days 1–3–7–14–30; the microcirculation index and the number of intact neurons decrease; the number of neurons with chromatolysis and shadow cells increases in the focus of the cerebral cortex lesion on days 7–14–30. The use of EPO in the total dose of 15.000 IU/kg results in partial recovery in 3–7 days, complete recovery of the neurological status in animals in 14–30 days, microcirculation restoration, growth of the number of intact neurons and small blood vessels, and decrease of neurons with chromatolysis and shadow cells in the ischemic focus in 7–14–30 days.References
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30. Осиков, М.В. Влияние эритропоэтина на процессы свободно-радикального окисления и экспрессию гликопротеинов в тромбоцитах при хронической почечной недостаточности / М.В. Осиков // Бюл. эксперимент. биологии и медицины. – 2014. – Т. 157, № 1. – С. 30–33. [Osikov M.V. [Effect of Erythropoietin on the Processes of Free Radical Oxidation and Expression of Glycoproteins in Platelets in Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2014, vol. 157, no. 1, pp. 30–33. (in Russ.) DOI: 10.1007/s10517-014-2483-3]
2. Brines M., Cerami A. The Receptor that Tames the Innate Immune Response. Mol. Med., 2012, vol. 18, pp. 486–496. DOI: 10.2119/molmed.2011.00414
3. Brines M.L., Ghezzi P., Keenan S. Erythropoietin Crosses the Blood-Brain Barrier to Protect Against Experimental Brain Injury. Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 19, pp. 10526–10531. DOI: 10.1073/pnas.97.19.10526
4. Broxmeyer H.E. Erythropoietin: Multiple Targets, Actions, and Modifying Influences for Biological and Clinical Consideration. J. Exp. Med., 2013, vol. 210, no. 2, pp. 205–208. DOI: 10.1084/jem.20122760.
5. Carnot P., DeFlandre C. Sur l’activite Hemopoietique de Serum au Cours de la Regeneration du Sang. C. R. Acad. Sci. (Paris), 1906, vol. 143, pp. 384–386.
6. D’Andrea A.D., Zon L.I. Erythropoietin Receptor. Subunit Structure and Activation. J. Clin. Invest., 1990, vol. 86, no. 3, pp. 681–687.
7. Desai A., Lewis E., Solomon S. Impact of Erythropoiesis-Stimulating Agents on Morbidity and Mortality in Patients with Heart Failure: an Updated, Post-TREAT Meta-Analysis. Eur. J. Heart Fail., 2010, vol. 12, pp. 936–942. DOI: 10.1093/eurjhf/hfq094
8. Fenjves E.S., Ochoa M.S., Cabrera O. Human, Nonhuman Primate, and Rat Pancreatic Islets Express Erythropoietin Receptors. Transplantation, 2003, vol. 75, pp. 1356–1360. DOI: 10.1097/01.TP.0000062862.88375.BD
9. Hand C.C., Brines M. Promises and Pitfalls in Erythopoietin-Mediated Tissue Protection: Are Nonerythropoietic Derivatives a Way Forward? J. Investig. Med., 2011, vol. 59, no. 7, pp. 1073–1082. DOI: 10.2310/JIM.0b013e3181ed30bf.
10. Ikeda E. Cellular Response to Tissue Hypoxia and Its Involvement in Disease Progression. Pathol. Int., 2005, vol. 55, pp. 603–610. DOI: 10.1111/j.1440-1827.2005.01877.x
11. Kim M.S., Seo Y.K., Park H.J. The Neuroprotective Effect of Recombinant Human Erythropoietinvia an Antiapoptotic Mechanism on Hypoxic-Ischemic Brain Injury in Neonatal Rats. Korean J. Pediatr., 2010, vol. 53, no. 10, pp. 898–908. DOI: 10.3345/kjp.2010.53.10.898
12. Kowalczyk M., Banach M., Mikhailidis D.P. Erythropoietin Update 2011. Med. Sci Monit., 2011, vol. 17, no. 11, pp. 240–247. DOI: 10.12659/MSM.882037
13. Leist M., Ghezzi P., Grasso G. Derivatives of Erythropoietin that are Tissue Protective but not Erythropoietic. Science. 2004, vol. 305(5681), pp. 239–242. DOI: 10.1126/science.1098313
14. Li J., Luo Y., Li Z. Effects of Erythropoietin Pretreatment on Pro-and Anti-Inflammatory Balance in Rats with Severe Acute Pancreatitis. Nan Fang Yi Ke Da Xue Xue Bao., 2012, vol. 32, no. 1, pp. 93–96.
15. Lin F.K., Suggs S., Lin C.H. Cloning and Expression of the Human Erythropoietin Gene. Proc. Natl. Acad. Sci. U.S.A., 1985, vol. 82, pp. 7580–7584. DOI: 10.1073/pnas.82.22.7580
16. Loeliger M.M., Mackintosh A., de Matteo R. Erythropoietin Protects the Developing Retina in an Ovine Model of Endotoxin-Induced Retinal Injury. Invest. Ophthalmol. Vis. Sci., 2011, vol. 52, pp. 2656–2661. DOI: 10.1167/iovs.10-6455
17. Maiese K., Chong Z.Z., Shang Y.C. Erythropoietin: New Directions for the Nervous System. Int. J. Mol. Sci., 2012, vol. 13, no. 9, pp. 11102–11129. DOI: 10.3390/ijms130911102
18. McPherson R.J., Juul S.E. Erythropoietin for Infants with Hypoxic-Ischemic Encephalopathy. Curr. Opin. Pediatr., 2010, vol. 22, no. 2, pp. 139–145. DOI: 10.1097/MOP.0b013e328336eb57
19. Milano M., Collomp R. Erythropoietin and Neuroprotection: a Therapeutic Perspective. J. Oncol. Pharm. Pract., 2005, vol. 11, no. 4, pp. 145-149.DOI: 10.1191/1078155205jp162oa
20. Sautina L., Sautin Y., Beem E. Induction of Nitric Oxide by Erythropoietin is Mediated by the ? Common Receptor and Requires Interaction with VEGF Receptor 2. Blood, 2010, vol. 115, pp. 896–905. DOI: 10.1182/blood-2009-04-216432
21. Su K.H., Shyue S.K., Kou Y.R. ? Common Receptor Integrates the Erythropoietin Signaling in Activation of Endothelial Nitric Oxide Synthase. J. Cell Physiol., 2011, vol. 226, pp. 3330–3339. DOI: 10.1002/jcp.22678
22. Sugawa M., Sakurai Y., Ishikawa-Ieda Y. Effects of Erythropoietin on Glial Cell Development; Oligodendrocyte Maturation and Astrocyte Proliferation. Neurosci. Res., 2002, vol. 44, no. 4, pp. 391–403. DOI: 10.1016/S0168-0102(02)00161-X
23. Toyoda T., Itai T., Arakawa T. Stabilization of Human Recombinant Erythropoietin Through Interactions with the Highly Branched N-glycans. J. Biochem (Tokyo), 2000, vol. 128, pp. 731–737. DOI: 10.1093/oxfordjournals.jbchem.a022809
24. Trincavelli M.L., Da Pozzo E., Ciampi O. Regulation of Erythropoietin Receptor Activity in Endothelial Cells by Different Erythropoietin (EPO) Derivatives: An in Vitro Study. Int. J. Mol. Sci., 2013, vol. 14, no. 2, pp. 2258–2281. DOI: 10.3390/ijms14022258
25. Wang G., Huang H., Wu H. Erythropoietin Attenuates Cardiopulmonary Bypass-Induced Renal Inflammatory Injury by Inhibiting Nuclear Factor-?B p65 Expression. Eur. J. Pharmacol., 2012, vol. 689, no. 1–3, pp. 154–159. DOI: 10.1016/j.ejphar.2012.05.027
26. Yamaji R., Okada T., Moriya M. Brain Capillary Endothelial Cells Express Two Forms of Erythropoietin Receptor mRNA. Eur. J. Biochem., 1996, vol. 239, no. 2, pp. 494–500. DOI: 10.1111/j.1432-1033.1996.0494u.x
27. Осиков М.В., Ахматов К.В., Кривохижина Л.В. Патофизиологический анализ влияния эритропоэтина на психологический статус у больных хронической почечной недостаточностью, находящихся на гемодиализе. Человек. Спорт. Медицина. 2010. № 19 (195). С. 110–116. [Osikov M.V., Akhmatov K.V., Krivokhizhina L.V. [Pathophysiological Analysis of the Effect of Erythropoietin on Psychological Status in Patients With Chronic Renal Failure Who are on Hemodialysis]. Chelovek. Sport. Meditsina [Human. Sport. Medicine], 2010, no. 19 (195), pp. 110–116. (in Russ.)]
28. Осиков М.В., Телешева Л.Ф., Агеев Ю.И. Антиоксидантный эффект эритропоэтина при экспериментальной хронической почечной недостаточности. Бюл. эксперимент. биологии и медицины. 2015. Т. 160, № 8. С. 162–165. [Osikov M.V., Telesheva L.F., Ageev Yu.I. [Antioxidant Effect of Erythropoietin in Experimental Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2015, vol. 160, no. 8, pp. 162–165. (in Russ.)]
29. Осиков М.В., Телешева Л.Ф., Агеев Ю.И. Влияние эритропоэтина на апоптоз лимфоцитов при экспериментальной хронической почечной недостаточности. Бюл. эксперимент. биологии и медицины. – 2015. – № 3. – С. 326–329. [Osikov M.V., Telesheva L.F., Ageev Yu.I. [Influence of Erythropoietin on Apoptosis of Lymphocytes in Experimental Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2015, no. 3, pp. 326–329. (in Russ.)]
30. Осиков, М.В. Влияние эритропоэтина на процессы свободно-радикального окисления и экспрессию гликопротеинов в тромбоцитах при хронической почечной недостаточности / М.В. Осиков // Бюл. эксперимент. биологии и медицины. – 2014. – Т. 157, № 1. – С. 30–33. [Osikov M.V. [Effect of Erythropoietin on the Processes of Free Radical Oxidation and Expression of Glycoproteins in Platelets in Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2014, vol. 157, no. 1, pp. 30–33. (in Russ.) DOI: 10.1007/s10517-014-2483-3]
2. Brines M., Cerami A. The Receptor that Tames the Innate Immune Response. Mol. Med., 2012, vol. 18, pp. 486–496. DOI: 10.2119/molmed.2011.00414
3. Brines M.L., Ghezzi P., Keenan S. Erythropoietin Crosses the Blood-Brain Barrier to Protect Against Experimental Brain Injury. Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 19, pp. 10526–10531. DOI: 10.1073/pnas.97.19.10526
4. Broxmeyer H.E. Erythropoietin: Multiple Targets, Actions, and Modifying Influences for Biological and Clinical Consideration. J. Exp. Med., 2013, vol. 210, no. 2, pp. 205–208. DOI: 10.1084/jem.20122760.
5. Carnot P., DeFlandre C. Sur l’activite Hemopoietique de Serum au Cours de la Regeneration du Sang. C. R. Acad. Sci. (Paris), 1906, vol. 143, pp. 384–386.
6. D’Andrea A.D., Zon L.I. Erythropoietin Receptor. Subunit Structure and Activation. J. Clin. Invest., 1990, vol. 86, no. 3, pp. 681–687.
7. Desai A., Lewis E., Solomon S. Impact of Erythropoiesis-Stimulating Agents on Morbidity and Mortality in Patients with Heart Failure: an Updated, Post-TREAT Meta-Analysis. Eur. J. Heart Fail., 2010, vol. 12, pp. 936–942. DOI: 10.1093/eurjhf/hfq094
8. Fenjves E.S., Ochoa M.S., Cabrera O. Human, Nonhuman Primate, and Rat Pancreatic Islets Express Erythropoietin Receptors. Transplantation, 2003, vol. 75, pp. 1356–1360. DOI: 10.1097/01.TP.0000062862.88375.BD
9. Hand C.C., Brines M. Promises and Pitfalls in Erythopoietin-Mediated Tissue Protection: Are Nonerythropoietic Derivatives a Way Forward? J. Investig. Med., 2011, vol. 59, no. 7, pp. 1073–1082. DOI: 10.2310/JIM.0b013e3181ed30bf.
10. Ikeda E. Cellular Response to Tissue Hypoxia and Its Involvement in Disease Progression. Pathol. Int., 2005, vol. 55, pp. 603–610. DOI: 10.1111/j.1440-1827.2005.01877.x
11. Kim M.S., Seo Y.K., Park H.J. The Neuroprotective Effect of Recombinant Human Erythropoietinvia an Antiapoptotic Mechanism on Hypoxic-Ischemic Brain Injury in Neonatal Rats. Korean J. Pediatr., 2010, vol. 53, no. 10, pp. 898–908. DOI: 10.3345/kjp.2010.53.10.898
12. Kowalczyk M., Banach M., Mikhailidis D.P. Erythropoietin Update 2011. Med. Sci Monit., 2011, vol. 17, no. 11, pp. 240–247. DOI: 10.12659/MSM.882037
13. Leist M., Ghezzi P., Grasso G. Derivatives of Erythropoietin that are Tissue Protective but not Erythropoietic. Science. 2004, vol. 305(5681), pp. 239–242. DOI: 10.1126/science.1098313
14. Li J., Luo Y., Li Z. Effects of Erythropoietin Pretreatment on Pro-and Anti-Inflammatory Balance in Rats with Severe Acute Pancreatitis. Nan Fang Yi Ke Da Xue Xue Bao., 2012, vol. 32, no. 1, pp. 93–96.
15. Lin F.K., Suggs S., Lin C.H. Cloning and Expression of the Human Erythropoietin Gene. Proc. Natl. Acad. Sci. U.S.A., 1985, vol. 82, pp. 7580–7584. DOI: 10.1073/pnas.82.22.7580
16. Loeliger M.M., Mackintosh A., de Matteo R. Erythropoietin Protects the Developing Retina in an Ovine Model of Endotoxin-Induced Retinal Injury. Invest. Ophthalmol. Vis. Sci., 2011, vol. 52, pp. 2656–2661. DOI: 10.1167/iovs.10-6455
17. Maiese K., Chong Z.Z., Shang Y.C. Erythropoietin: New Directions for the Nervous System. Int. J. Mol. Sci., 2012, vol. 13, no. 9, pp. 11102–11129. DOI: 10.3390/ijms130911102
18. McPherson R.J., Juul S.E. Erythropoietin for Infants with Hypoxic-Ischemic Encephalopathy. Curr. Opin. Pediatr., 2010, vol. 22, no. 2, pp. 139–145. DOI: 10.1097/MOP.0b013e328336eb57
19. Milano M., Collomp R. Erythropoietin and Neuroprotection: a Therapeutic Perspective. J. Oncol. Pharm. Pract., 2005, vol. 11, no. 4, pp. 145-149.DOI: 10.1191/1078155205jp162oa
20. Sautina L., Sautin Y., Beem E. Induction of Nitric Oxide by Erythropoietin is Mediated by the ? Common Receptor and Requires Interaction with VEGF Receptor 2. Blood, 2010, vol. 115, pp. 896–905. DOI: 10.1182/blood-2009-04-216432
21. Su K.H., Shyue S.K., Kou Y.R. ? Common Receptor Integrates the Erythropoietin Signaling in Activation of Endothelial Nitric Oxide Synthase. J. Cell Physiol., 2011, vol. 226, pp. 3330–3339. DOI: 10.1002/jcp.22678
22. Sugawa M., Sakurai Y., Ishikawa-Ieda Y. Effects of Erythropoietin on Glial Cell Development; Oligodendrocyte Maturation and Astrocyte Proliferation. Neurosci. Res., 2002, vol. 44, no. 4, pp. 391–403. DOI: 10.1016/S0168-0102(02)00161-X
23. Toyoda T., Itai T., Arakawa T. Stabilization of Human Recombinant Erythropoietin Through Interactions with the Highly Branched N-glycans. J. Biochem (Tokyo), 2000, vol. 128, pp. 731–737. DOI: 10.1093/oxfordjournals.jbchem.a022809
24. Trincavelli M.L., Da Pozzo E., Ciampi O. Regulation of Erythropoietin Receptor Activity in Endothelial Cells by Different Erythropoietin (EPO) Derivatives: An in Vitro Study. Int. J. Mol. Sci., 2013, vol. 14, no. 2, pp. 2258–2281. DOI: 10.3390/ijms14022258
25. Wang G., Huang H., Wu H. Erythropoietin Attenuates Cardiopulmonary Bypass-Induced Renal Inflammatory Injury by Inhibiting Nuclear Factor-?B p65 Expression. Eur. J. Pharmacol., 2012, vol. 689, no. 1–3, pp. 154–159. DOI: 10.1016/j.ejphar.2012.05.027
26. Yamaji R., Okada T., Moriya M. Brain Capillary Endothelial Cells Express Two Forms of Erythropoietin Receptor mRNA. Eur. J. Biochem., 1996, vol. 239, no. 2, pp. 494–500. DOI: 10.1111/j.1432-1033.1996.0494u.x
27. Осиков М.В., Ахматов К.В., Кривохижина Л.В. Патофизиологический анализ влияния эритропоэтина на психологический статус у больных хронической почечной недостаточностью, находящихся на гемодиализе. Человек. Спорт. Медицина. 2010. № 19 (195). С. 110–116. [Osikov M.V., Akhmatov K.V., Krivokhizhina L.V. [Pathophysiological Analysis of the Effect of Erythropoietin on Psychological Status in Patients With Chronic Renal Failure Who are on Hemodialysis]. Chelovek. Sport. Meditsina [Human. Sport. Medicine], 2010, no. 19 (195), pp. 110–116. (in Russ.)]
28. Осиков М.В., Телешева Л.Ф., Агеев Ю.И. Антиоксидантный эффект эритропоэтина при экспериментальной хронической почечной недостаточности. Бюл. эксперимент. биологии и медицины. 2015. Т. 160, № 8. С. 162–165. [Osikov M.V., Telesheva L.F., Ageev Yu.I. [Antioxidant Effect of Erythropoietin in Experimental Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2015, vol. 160, no. 8, pp. 162–165. (in Russ.)]
29. Осиков М.В., Телешева Л.Ф., Агеев Ю.И. Влияние эритропоэтина на апоптоз лимфоцитов при экспериментальной хронической почечной недостаточности. Бюл. эксперимент. биологии и медицины. – 2015. – № 3. – С. 326–329. [Osikov M.V., Telesheva L.F., Ageev Yu.I. [Influence of Erythropoietin on Apoptosis of Lymphocytes in Experimental Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2015, no. 3, pp. 326–329. (in Russ.)]
30. Осиков, М.В. Влияние эритропоэтина на процессы свободно-радикального окисления и экспрессию гликопротеинов в тромбоцитах при хронической почечной недостаточности / М.В. Осиков // Бюл. эксперимент. биологии и медицины. – 2014. – Т. 157, № 1. – С. 30–33. [Osikov M.V. [Effect of Erythropoietin on the Processes of Free Radical Oxidation and Expression of Glycoproteins in Platelets in Chronic Renal Failure]. Byulleten' eksperimental'noy biologii i meditsiny [Bulletin of Experimental Biology and Medicine], 2014, vol. 157, no. 1, pp. 30–33. (in Russ.) DOI: 10.1007/s10517-014-2483-3]
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26. Yamaji R., Okada T., Moriya M. Brain Capillary Endothelial Cells Express Two Forms of Erythropoietin Receptor mRNA. Eur. J. Biochem., 1996, vol. 239, no. 2, pp. 494–500. DOI: 10.1111/j.1432-1033.1996.0494u.x
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Published
2017-12-01
How to Cite
Osikov, M., Giniatullin, R., Kuzmin, A., & Markelova, E. (2017). NEUROPROTECTIVE EFFECT OF ERYTHROPOETIN IN EXPERIMENTAL CEREBRAL ISCHEMIA. Human. Sport. Medicine, 17(4), 41-49. https://doi.org/10.14529/hsm170405
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Clinical and Experimental Medicine
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