Мезенхимальные стволовые клетки в терапии ишемического инсульта
Автор: Наместникова Д.Д., Коваленко Д.Б., Покусаева И.А., Чудакова Д.А., Губский И.Л., Ярыгин К.Н., Баклаушев В.П.
Журнал: Клиническая практика @clinpractice
Рубрика: Обзоры
Статья в выпуске: 4 т.14, 2023 года.
Бесплатный доступ
В последние два десятилетия накоплены данные о том, что трансплантация мезенхимальных стволовых клеток оказывает значимое положительное действие при экспериментальном инфаркте головного мозга у животных. Обнадёживающие результаты доклинических исследований сделали возможным проведение клинических испытаний по трансплантации мезенхимальных стволовых клеток пациентам с ишемическим инсультом. В настоящем обзоре приведены и проанализированы результаты завершённых клинических исследований, посвящённых клеточной терапии ишемического инсульта с помощью мезенхимальных стволовых клеток. На основании проведённого анализа можно заключить, что трансплантация мезенхимальных стволовых клеток является безопасной и целесообразной с патогенетической точки зрения процедурой. Для дальнейшего внедрения данной перспективной технологии терапии в клиническую практику необходимы продолжение рандомизированных плацебоконтролируемых многоцентровых клинических испытаний на большой выборке пациентов и оптимизация протоколов клеточной трансплантации и критериев включения пациентов в исследование. В настоящей работе обсуждаются также возможные стратегии для усиления клеточной терапии с использованием мезенхимальных стволовых клеток.
Клеточная терапия, мезенхимальные стволовые клетки, ишемический инсульт, клинические исследования
Короткий адрес: https://sciup.org/143182384
IDR: 143182384 | DOI: 10.17816/clinpract624157
Список литературы Мезенхимальные стволовые клетки в терапии ишемического инсульта
- Kim J, Thayabaranathan T, Donnan GA, et al. Global Stroke Statistics 2019. Int J Stroke. 2020;15(8):819–838. doi: 10.1177/1747493020909545
- Pu L, Wang L, Zhang R, et al. Projected global trends in ischemic stroke incidence, deaths and disability-adjusted life years from 2020 to 2030. Stroke. 2023;54(5):1330–1339. doi: 10.1161/STROKEAHA.122.040073
- Гудкова В.В., Кимельфельд Е.И., Белов С.Е. Отек головного мозга: от истоков описания к современному пониманию процесса // Consil Med. 2021. Т. 23, № 2. С. 131–135. [Gudkova VV, Kimelfeld EI, Belov SE. Brain oedema: From the origins of description to the modern understanding of the process. Consil Med. 2021;23(2):131–135. (In Russ).] doi: 10.26442/20751753.2021.2.200604
- Игнатьева В.И., Вознюк И.А., Шамалов Н.А., и др. Социально-экономическое бремя инсульта в Российской Федерации // Журнал неврологии и психиатрии им. С.С. Корсакова. 2023. Т. 123, № 8. С. 5. [Ignatyeva VI, Voznyuk IA, Shamalov NA, et al. Social and economic burden of stroke in Russian Federation. J Neurol Psychiatry named after S.S. Korsakov. 2023;123(8):5. (In Russ).] doi: 10.17116/jnevro20231230825
- Feigin VL, Stark BA, Johnson CO, et al. Global, regional, and national burden of stroke and its risk factors, 1990–2019: A systematic analysis for the Global Burden of Disease Study 2019. Lancet Neurol. 2021;20(10):795–820. doi: 10.1016/S1474-4422(21)00252-0
- The top 10 causes of death [Electronic resource]. Режим доступа: https://www.who.int/en/news-room/fact-sheets/detail/the-top-10-causes-of-death. Дата обращения: 09.05.2022.
- Число умерших по основным классам причин смерти. Демография. Федеральная служба государственной статистики [Electronic resource]. Режим доступа: https://rosstat.gov.ru/folder/12781#. Дата обращения: 08.11.2023.
- Солдатов М.А., Климов Л.В., Толмачев А.П., и др. Внутривенная тромболитическая терапия ишемического инсульта препаратом Ревелиза в реальной клинической практике: Результаты исследования IVT-AIS-R // Журнал неврологии и психиатрии им. С.С. Корсакова. 2022. Т. 122, № 12. С. 42. [Soldatov MA, Klimov LV, Tolmachev AP, et al. Intravenous thrombolytic therapy of ischemic stroke with the drug Revelisa in real clinical practice: Results of the IVT-AIS-R study. J Neurol Psychiatry named after S.S. Korsakov. 2022;122(12):42. (In Russ).] doi: 10.17116/jnevro202212212242
- Акжигитов Р.Г., Алекян Б.Г., Алферова В.В. Ишемический инсульт и транзиторная ишемическая атака у взрослых. Клинические рекомендации. Москва, 2021. 181 c. [Akzhigitov RG, Alekian BG, Alferova VV. Ischaemic stroke and transient ischaemic attack in adults. Clinical Recommendations. Moscow; 2021. 181 р. (In Russ).]
- Powers WJ, Rabinstein AA, Ackerson T, et al. Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke a guideline for healthcare professionals from the American Heart Association/American Stroke. Stroke. 2019;50(12):E344–E418. doi: 10.1161/STR.0000000000000211
- Nogueira RG, Jadhav AP, Haussen DC, et al. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. New Engl J Med. 2018;378(1):11–21. doi: 10.1056/NEJMoa1706442
- Федин А.И., Бадалян К.Р. Обзор клинических рекомендаций по лечению и профилактике ишемического инсульта // Журнал неврологии и психиатрии им. С.С. Корсакова. 2019. Т. 119, № 8. C. 95–100. [Fedin AI, Badalyan KR. Review of clinical guidelines for the treatment and prevention of ischemic stroke. J Neurol Psychiatry named after S.S. Korsakov. 2019;119(8): 95–100. (In Russ).] doi: 10.17116/jnevro201911908295
- Гусев Е.И., Мартынов М.Ю., Ясаманова А.Н. Тромболитическая терапия ишемического инсульта // Журнал неврологии и психиатрии им. C.C. Корсакова. 2018. Т. 118, № 12-2. C. 4–14. [Gusev EI, Martynov MY, Yasamanova AN. Thrombolytic therapy of ischaemic stroke. J Neurol Psychiatry named after S.S. Korsakov. 2018;118 (12-2):4–14. (In Russ).] doi: 10.17116/jnevro20181181224
- Horwitz EM, Le Blanc K, Dominici M, et al. Clarification of the nomenclature for MSC: The international society for cellular therapy position statement. Cytotherapy. 2005;7(5):393–395. doi: 10.1080/14653240500319234
- Jin QH, Kim HK, Na JY, et al. Anti-inflammatory effects of mesenchymal stem cell-conditioned media inhibited macrophages activation in vitro. Sci Rep. 2022;12(1):4754. doi: 10.1038/s41598-022-08398-4
- Pang QM, Chen SY, Fu SP, et al. Regulatory role of mesenchymal stem cells on secondary inflammation in spinal cord injury. J Inflammat Res. 2022;(15):573–593. doi: 10.2147/JIR.S349572
- Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy. 2006;8(4):315–317. doi: 10.1080/14653240600855905
- Mikael PE, Willard C, Koyee A, et al. Remodeling of glycosaminoglycans during differentiation of adult human bone mesenchymal stromal cells toward hepatocytes. Stem Cells Development. 2019;28(4):278–289. doi: 10.1089/scd.2018.0197
- Gao Q, Guo M, Jiang X, et al. A Cocktail method for promoting cardiomyocyte differentiation from bone marrow-derived mesenchymal stem cells. Stem Cells Int. 2014;2014:1–11. doi: 10.1155/2014/162024
- Scuteri A, Miloso M, Foudah D, et al. Mesenchymal stem cells neuronal differentiation ability: A real perspective for nervous system repair? Curr Stem Cell Res Therapy. 2011;6(2):82–92. doi: 10.2174/157488811795495486
- Lee BB, Cripps RA, Fitzharris M, et al. The global map for traumatic spinal cord injury epidemiology: Update 2011, global incidence rate. Spinal Cord. 2014;52(2):110–116. doi: 10.1038/sc.2012.158
- Gartner S, Kaplan HS. Long-term culture of human bone marrow cells. Proc Natl Acad Sci USA. 1980;77(8):4756–4759. doi: 10.1073/pnas.77.8.4756
- Kim DW, Staples M, Shinozuka K, et al. Wharton’s jellyderived mesenchymal stem cells: Phenotypic characterization and optimizing their therapeutic potential for clinical applications. Int J Mol Sci. 2013;14(6):11692–11712. doi: 10.3390/ijms140611692
- Fei X, Jiang S, Zhang S, et al. Isolation, culture, and identification of amniotic fluid-derived mesenchymal stem cells. Cell Biochem Biophys. 2013;67(2):689–694. doi: 10.1007/s12013-013-9558-z
- Secunda R, Vennila R, Mohanashankar AM, et al. Isolation, expansion and characterisation of mesenchymal stem cells from human bone marrow, adipose tissue, umbilical cord blood and matrix: A comparative study. Cytotechnology. 2015;67(5): 793–807. doi: 10.1007/s10616-014-9718-z
- Pierdomenico L, Bonsi L, Calvitti M, et al. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation. 2005;80(6):836–842. doi: 10.1097/01.tp.0000173794.72151.88
- Elahi KC, Klein G, Avci-Adali M, et al. Human mesenchymal stromal cells from different sources diverge in their expression of cell surface proteins and display distinct differentiation patterns. Stem Cells Int. 2016;2016:5646384. doi: 10.1155/2016/5646384
- Griffin MD, Ritter T, Mahon BP. Immunological aspects of allogeneic mesenchymal stem cell therapies. Hum Gene Therapy. 2010;21(12):1641–1655. doi: 10.1089/hum.2010.156
- Kenmuir CL, Wechsler LR. Update on cell therapy for stroke. Stroke Vasc Neurol. 2017;2(2):59–64. doi: 10.1136/svn-2017-000070
- Neri S. Genetic stability of mesenchymal stromal cells for regenerative medicine applications: A fundamental biosafety aspect. Int J Mol Sci. 2019;20(10):2406. doi: 10.3390/ijms20102406
- Наместникова Д.Д., Таирова Р.Т., Сухинич К.К., и др. Клеточная терапия ишемического инсульта. Типы стволовых клеток и результаты доклинических испытаний // Журнал неврологии и психиатрии имени С.С. Корсакова. 2018. Т. 118, № 9. С. 69–75. [Namestnikova DD, Tairova RT, Sukhinich KK, et al. Cell therapy for ischemic stroke. Stem cell types and results of preclinical trials. J Neurol Psychiatry named after S.S. Korsakov. 2018;118(9):69–75. (In Russ).] doi: 10.17116/jnevro201811809269
- Rascón-Ramírez FJ, Esteban-García N, Barcia JA, et al. Are we ready for cell therapy to treat stroke? Fron Cell Dev Biol. 2021;(9):621645. doi: 10.3389/fcell.2021.621645
- Cherkashova E, Namestnikova D, Leonov G, et al. Comparative study of the efficacy of intra-arterial and intravenous transplantation of human induced pluripotent stem cellsderived neural progenitor cells in experimental stroke. Peer J. 2023;(11):e16358. doi: 10.7717/peerj.16358
- Namestnikova DD, Gubskiy IL, Revkova VA, et al. Intra-arterial stem cell transplantation in experimental stroke in rats: Realtime MR visualization of transplanted cells starting with their first pass through the brain with regard to the therapeutic action. Front Neurosci. 2021;15:641970. doi: 10.3389/fnins.2021.641970
- Sukhinich KK, Namestnikova DD, Gubskii IL, et al. Distribution and migration of human placental mesenchymal stromal cells in the brain of healthy rats after stereotaxic or intra-arterial transplantation. Bulletin Exp Biol Med. 2020;168(4):542–551. doi: 10.1007/s10517-020-04750-8
- Cherkashova EA, Burunova VV, Bukharova TB, et al. Comparative analysis of the effects of intravenous administration of placental mesenchymal stromal cells and neural progenitor cells derived from induced pluripotent cells on the course of acute ischemic stroke in rats. Bulletin Exp Biol Med. 2019;166(4):558–566. doi: 10.1007/s10517-019-04392-5
- Cherkashova EA, Namestnikova DD, Gubskiy IL, et al. Dose-dependent effects of intravenous mesenchymal stem cell transplantation in rats with acute focal cerebral ischemia. Bulletin Exp Biol Med. 2022;173(4):514–518. doi: 10.1007/S10517-022-05573-5
- Cherkashova EA, Namestnikova DD, Gubskiy IL, et al. Dynamic MRI of the mesenchymal stem cells distribution during intravenous transplantation in a rat model of ischemic stroke. Life. 2023;13(2):288. doi: 10.3390/life13020288
- Namestnikova DD, Gubskiy IL, Cherkashova EA, et al. Therapeutic efficacy and migration of mesenchymal stem cells after intracerebral transplantation in rats with experimental ischemic stroke. Bulletin Exp Biol Med. 2023;175(1):116–125. doi: 10.1007/s10517-023-05822-1
- Zhang XL, Zhang XG, Huang YR, et al. Stem cell-based therapy for experimental ischemic stroke: A preclinical systematic review. Front Cell Neurosci. 2021;(15):628908. doi: 10.3389/fncel.2021.628908
- Barbash IM, Chouraqui P, Baron J, et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation. 2003;108(7):863–868. doi: 10.1161/01.CIR.0000084828.50310.6A
- Boltze J, Arnold A, Walczak P, et al. The dark side of the force: Constraints and complications of cell therapies for stroke. Front Neurol. 2015;(6):155. doi: 10.3389/fneur.2015.00155
- Vasconcelos-dos-Santos A, Rosado-de-Castro PH, Lopes de Souza SA, et al. Intravenous and intra-arterial administration of bone marrow mononuclear cells after focal cerebral ischemia: Is there a difference in biodistribution and efficacy? Stem Cell Res. 2012;9(1):1–8. doi: 10.1016/j.scr.2012.02.002
- Guzman R, Janowski M, Walczak P. Intra-arterial delivery of cell therapies for stroke. Stroke. 2018;49(5):1075–1082. doi: 10.1161/STROKEAHA.117.018288
- Toyoshima A, Yasuhara T, Kameda M, et al. Intra-Arterial transplantation of allogeneic mesenchymal stem cells mounts neuroprotective effects in a transient ischemic stroke model in rats: Analyses of therapeutic time window and its mechanisms. PLoS One. 2015;10(6):e0127302. doi: 10.1371/journal.pone.0127302
- Li W, Shi L, Hu B, et al. Mesenchymal stem cell-based therapy for stroke: Current understanding and challenges. Front Cell Neurosci. 2021;(15):628940. doi: 10.3389/fncel.2021.628940
- Zhou L, Zhu H, Bai X, et al. Potential mechanisms and therapeutic targets of mesenchymal stem cell transplantation for ischemic stroke. Stem Cell Res Ther. 2022;13(1):195. doi: 10.1186/S13287-022-02876-2
- Zhuang WZ, Lin YH, Su LJ, et al. Mesenchymal stem/ stromal cell-based therapy: Mechanism, systemic safety and biodistribution for precision clinical applications. J Biomed Sci. 2021;28(1):28. doi: 10.1186/s12929-021-00725-7
- Yong KW, Choi JR, Mohammadi M, et al. Mesenchymal stem cell therapy for ischemic tissues. Stem Cells Int. 2018;2018:8179075. doi: 10.1155/2018/8179075
- Bang OY, Lee JS, Lee PH, et al. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol. 2005;57(6):874–882. doi: 10.1002/ana.20501
- Lee JS, Hong JM, Moon GJ, et al. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells. 2010;28(6): 1099–1106. doi: 10.1002/stem.430
- Honmou O, Houkin K, Matsunaga T, et al. Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain. 2011;134(6): 1790–1807. doi: 10.1093/brain/awr063
- Bhasin A, Srivastava MV, Kumaran SS, et al. Autologous mesenchymal stem cells in chronic stroke. Cerebrovasc Dis Extra. 2011;1(1):93–104. doi: 10.1159/000333381
- Bhasin A, Srivastava MV, Mohanty S, et al. Stem cell therapy: A clinical trial of stroke. Clin Neurol Neurosur. 2013;115(7): 1003–1008. doi: 10.1016/j.clineuro.2012.10.015
- Fang J, Guo Y, Tan S, et al. Autologous endothelial progenitor cells transplantation for acute ischemic stroke: A 4-Year follow-up study. Stem Cells Translat Med. 2019;8(1):14–21. doi: 10.1002/sctm.18-0012
- Hess DC, Wechsler LR, Clark M, et al. Safety and efficacy of multipotent adult progenitor cells in acute ischaemic stroke (MASTERS): A randomised, double-blind, placebocontrolled, phase 2 trial. Lancet Neurol. 2017;16(5):360–368. doi: 10.1016/S1474-4422(17)30046-7
- Levy ML, Crawford JR, Dib N, et al. Phase I/II study of safety and preliminary efficacy of intravenous allogeneic mesenchymal stem cells in chronic stroke. Stroke. 2019;50(10):2835–2841. doi: 10.1161/STROKEAHA.119.026318
- Steinberg GK, Kondziolka D, Wechsler LR, et al. Clinical outcomes of transplanted modified bone marrow-derived mesenchymal stem cells in stroke: A phase 1/2a study. Stroke. 2016;47(7):1817–1824. doi: 10.1161/STROKEAHA.116.012995
- Qiao LY, Huang FJ, Zhao M, et al. A two-year follow-up study of cotransplantation with neural stem/progenitor cells and mesenchymal stromal cells in ischemic stroke patients. Cell Transplant. 2014;23(1 Suppl):65–72. doi: 10.3727/096368914x684961
- Lee J, Chang WH, Chung W, et al. Efficacy of intravenous mesenchymal stem cells for motor recovery after ischemic stroke: A neuroimaging study. Stroke. 2022;53(1):20–28. doi: 10.1161/STROKEAHA.121.034505
- Jaillard A, Hommel M, Moisan A, et al. Autologous mesenchymal stem cells improve motor recovery in subacute ischemic stroke: A randomized clinical trial. Translat Stroke Res. 2020;11(5): 910–923. doi: 10.1007/s12975-020-00787-z
- De Celis-Ruiz E, Fuentes B, Moniche F, et al. Allogeneic adipose tissue-derived mesenchymal stem cells in ischaemic stroke (AMASCIS-02): A phase IIb, multicentre, double-blind, placebocontrolled clinical trial protocol. BMJ Open. 2021;11(8):e051790. doi: 10.1136/bmjopen-2021-051790
- Bang OY, Kim EH, Cho YH, et al. Circulating extracellular vesicles in stroke patients treated with mesenchymal stem cells: A biomarker analysis of a randomized trial. Stroke. 2022;53(7):2276–2286. doi: 10.1161/STROKEAHA.121.036545
- Wang Y, Huang J, Gong L, et al. The plasticity of mesenchymal stem cells in regulating surface HLA-I. iScience. 2019;(15): 66–78. doi: 10.1016/j.isci.2019.04.011
- Lee HJ, Kang KS, Kang SY, et al. Immunologic properties of differentiated and undifferentiated mesenchymal stem cells derived from umbilical cord blood. J Veterinary Sci. 2016;17(3):289–297. doi: 10.4142/jvs.2016.17.3.289
- Le Blanc K, Tammik C, Rosendahl K, et al. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31(10):890–896. doi: 10.1016/S0301-472X(03)00110-3
- Yousufuddin M, Young N. Aging and ischemic stroke. Aging. 2019;11(9):2542–2544. doi: 10.18632/aging.101931
- Yamaguchi S, Horie N, Satoh K, et al. Age of donor of human mesenchymal stem cells affects structural and functional recovery after cell therapy following ischaemic stroke. J Cerebral Blood Flow Metabol. 2018;38(7):1199–1212. doi: 10.1177/0271678X17731964
- Boozer S, Lehman N, Lakshmipathy U, et al. Global characterization and genomic stability of human multistem, a multipotent adult progenitor cell. Stem Cell Res Adv. 2011; 4(1):119–134. PMID: 20498688
- Dao MA, Tate CC, Aizman I, et al. Comparing the immunosuppressive potency of naïve marrow stromal cells and Notch-transfected marrow stromal cells. J Neuroinflammat. 2011;8(1):133. doi: 10.1186/1742-2094-8-133
- Dao M, Tate CC, McGrogan M, et al. Comparing the angiogenic potency of naïve marrow stromal cells and Notchtransfected marrow stromal cells. J Translat Med. 2013;11(1):81. doi: 10.1186/1479-5876-11-81
- Tate CC, Fonck C, McGrogan M, et al. Human mesenchymal stromal cells and their derivative, SB623 cells, rescue neural cells via trophic support following in vitro ischemia. Cell Transplant. 2010;19(8):973–984. doi: 10.3727/096368910X494885
- Aizman I, Tate CC, McGrogan M, et al. Extracellular matrix produced by bone marrow stromal cells and by their derivative, SB623 cells, supports neural cell growth. J Neurosci Res. 2009;87(14):3198–3206. doi: 10.1002/jnr.22146
- Yasuhara T, Matsukawa N, Hara K, et al. Notch-Induced rat and human bone marrow stromal cell grafts reduce ischemic cell loss and ameliorate behavioral deficits in chronic stroke animals. Stem Cells Development. 2009;18(10):1501–1514. doi: 10.1089/scd.2009.0011
- Steinberg GK, Kondziolka D, Wechsler LR, et al. Two-year safety and clinical outcomes in chronic ischemic stroke patients after implantation of modified bone marrow–derived mesenchymal stem cells (SB623): A phase 1/2a study. J Neurosur. 2019; 131(5):1462–1472. doi: 10.3171/2018.5.JNS173147
- Namestnikova DD, Cherkashova EA, Sukhinich KK, et al. Combined cell therapy in the treatment of neurological disorders. Biomed. 2020;8(12):613. doi: 10.3390/biomedicines8120613
- Hosseini SM, Farahmandnia M, Razi Z, et al. Combination cell therapy with mesenchymal stem cells and neural stem cells for brain stroke in rats. Int J Stem Cells. 2015;8(1):99–105. doi: 10.15283/ijsc.2015.8.1.99
- Sun K, Zhou Z, Ju X, et al. Combined transplantation of mesenchymal stem cells and endothelial progenitor cells for tissue engineering: A systematic review and meta-analysis. Stem Cell Res Ther. 2016;7(1):151. doi: 10.1186/s13287-016-0390-4
- Chen TS, Lai RC, Lee MM, et al. Mesenchymal stem cell secretes microparticles enriched in pre-microRNAs. Nucleic Acids Res. 2009;38(1):215–224. doi: 10.1093/nar/gkp857
- Zhang Y, Dong N, Hong H, et al. Mesenchymal stem cells: Therapeutic mechanisms for stroke. Int J Mol Sci. 2022;23(5):2550. doi: 10.3390/ijms23052550
- Ullah M, Liu DD, Thakor AS. Mesenchymal stromal cell homing: Mechanisms and strategies for improvement. iScience. 2019;(15):421–438. doi: 10.1016/j.isci.2019.05.004
- Harrell C, Fellabaum C, Jovicic N, et al. Molecular mechanisms responsible for therapeutic potential of mesenchymal stem cell-derived secretome. Cells. 2019;8(5):467. doi: 10.3390/cells8050467
- Dörnen J, Dittmar T. The role of MSCs and cell fusion in tissue regeneration. Int J Mol Sci. 2021;22(20):10980. doi: 10.3390/ijms222010980
- Babenko VA, Silachev DN, Popkov VA, et al. Miro1 enhances mitochondria transfer from multipotent mesenchymal stem cells (MMSC) to neural cells and improves the efficacy of cell recovery. Molecules. 2018;23(3):687. doi: 10.3390/molecules23030687
- Chen J, Li Y, Katakowski M, et al. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res. 2003;73(6):778–786. doi: 10.1002/jnr.10691
- Esneault E, Pacary E, Eddi D, et al. Combined therapeutic strategy using erythropoietin and mesenchymal stem cells potentiates neurogenesis after transient focal cerebral ischemia in rats. J Cerebral Blood Flow Metabol. 2008;28(9):1552–1563. doi: 10.1038/jcbfm.2008.40
- Maltman DJ, Hardy SA, Przyborski SA. Role of mesenchymal stem cells in neurogenesis and nervous system repair. Neurochem Int. 2011;59(3):347 356. doi: 10.1016/j.neuint.2011.06.008
- Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem. 2006;98(5):1076–1084. doi: 10.1002/jcb.20886
- Lee RH, Pulin AA, Seo MJ, et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell. 2009;5(1):54–63. doi: 10.1016/j.stem.2009.05.003
- Kubo H, Shimizu M, Taya Y, et al. Identification of mesenchymal stem cell (MSC)‐transcription factors by microarray and knockdown analyses, and signature molecule‐marked MSC in bone marrow by immunohistochemistry. Genes Cells. 2009;14(3):407–424. doi: 10.1111/j.1365-2443.2009.01281.x
- Wilkins A, Kemp K, Ginty M, et al. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. 2009;3(1):63–70. doi: 10.1016/j.scr.2009.02.006
- Wakabayashi K, Nagai A, Sheikh AM, et al. Transplantation of human mesenchymal stem cells promotes functional improvement and increased expression of neurotrophic factors in a rat focal cerebral ischemia model. J Neurosci Res. 2009;88(5):1017–1025. doi: 10.1002/jnr.22279
- Sterner RC, Sterner RM. Immune response following traumatic spinal cord injury: Pathophysiology and therapies. Front Immunol. 2022;(13):1084101. doi: 10.3389/fimmu.2022.1084101
- Pricola KL, Kuhn NZ, Haleem‐Smith H, et al. Interleukin‐6 maintains bone marrow‐derived mesenchymal stem cell stemness by an ERK1/2‐dependent mechanism. J Cell Biochem. 2009;108(3):577–588. doi: 10.1002/jcb.22289
- Leibinger M, Müller A, Gobrecht P, et al. Interleukin-6 contributes to CNS axon regeneration upon inflammatory stimulation. Cell Death Dis. 2013;4(4):e609–e609. doi: 10.1038/cddis.2013.126
- Gene Ontology Resource [Electronic resource]. Режим доступа: https://geneontology.org/. Дата обращения: 12.11.2023.
- Alonso-Alonso ML, García-Posadas L, Diebold Y. Extracellular vesicles from human adipose-derived mesenchymal stem cells: A review of common cargos. Stem Cell Rev Rep. 2022;18(3): 854–901. doi: 10.1007/s12015-021-10155-5
- Ferguson SW, Wang J, Lee CJ, et al. The microRNA regulatory landscape of MSC-derived exosomes: A systems view. Sci Rep. 2018;8(1):1419. doi: 10.1038/s41598-018-19581-x
- Kong X, Gao J. Macrophage polarization: A key event in the secondary phase of acute spinal cord injury. J Cell Mol Med. 2017;21(5):941–954. doi: 10.1111/jcmm.13034
- An N, Yang J, Wang H, et al. Mechanism of mesenchymal stem cells in spinal cord injury repair through macrophage polarization. Cell Biosci. 2021;11(1):41. doi: 10.1186/s13578-021-00554-z
- Shao M, Jin M, Xu S, et al. Exosomes from long noncoding RNA-Gm37494-ADSCs repair spinal cord injury via shifting microglial M1/M2 polarization. Inflammat. 2020;43(4): 1536–1547. doi: 10.1007/s10753-020-01230-z
- Chen QH, WF, Liu L, et al. Mesenchymal stem cells regulate the Th17/Treg cell balance partly through hepatocyte growth factor in vitro. Stem Cell Res Ther. 2020;11(1):91. doi: 10.1186/s13287-020-01612-y
- Liu J, Liu Q, Chen X. The immunomodulatory effects of mesenchymal stem cells on regulatory B cells. Front Immunol. 2020;(11):1843. doi: 10.3389/fimmu.2020.01843
- Zeng X, Ma Y, Chen Y, et al. Autocrine fibronectin from differentiating mesenchymal stem cells induces the neurite elongation in vitro and promotes nerve fiber regeneration in transected spinal cord injury. J Biomed Materials Res A. 2016; 104(8):1902–1911. doi: 10.1002/jbm.a.35720
- Nazari-Shafti TZ, Neuber S, Garcia Duran A, et al. Human mesenchymal stromal cells and derived extracellular vesicles: Translational strategies to increase their proangiogenic potential for the treatment of cardiovascular disease. Stem Cells Translat Med. 2020;9(12):1558–1569. doi: 10.1002/sctm.19-0432
- Gong M, Yu B, Wang J, et al. Mesenchymal stem cells release exosomes that transfer miRNAs to endothelial cells and promote angiogenesis. Oncotarget. 2017;8(28):45200–45212. doi: 10.18632/oncotarget.16778
- Colliander R, Alleman K, Diaz M, et al. Stem cell implants: Emerging innovation for stroke recovery. J Neuro Oncol Res. 2023;3(1):3102.
- Buga M, Di Napoli M, Popa-Wagner A. Preclinical models of stroke in aged animals with or without comorbidities: Role of neuroinflammation. Biogerontol. 2013;14(6):651–662. doi: 10.1007/s10522-013-9465-0
- Sommer CJ. Ischemic stroke: Experimental models and reality. Acta Neuropathol. 2017;133(2):245–261. doi: 10.1007/s00401-017-1667-0
- Ahlfors JE, Azimi A, El-Ayoubi R, et al. Examining the fundamental biology of a novel population of directly reprogrammed human neural precursor cells. Stem Cell Res Ther. 2019;10(1):166. doi: 10.1186/s13287-019-1255-4
- Popp A, Jaenisch N, Witte OW, et al. Identification of ischemic regions in a rat model of stroke. PLoS One. 2009;4(3):e4764. doi: 10.1371/journal.pone.0004764
- Weber RZ, Bernardoni D, Rentsch NH, et al. Visualization and estimation of stroke infarct volumes in rodents. bioRxiv. 2023;2023:547245. doi: 10.1101/2023.07.14.547245
- Saunders DE, Clifton AG, Brown MM. Measurement of infarct size using MRI predicts prognosis in middle cerebral artery infarction. Stroke. 1995;26(12):2272–2276. doi: 10.1161/01.STR.26.12.2272
- González RG. Clinical MRI of acute ischemic stroke. J Magnetic Resonance Imaging. 2012;36(2):259–271. doi: 10.1002/jmri.23595
- Milidonis X, Marshall I, Macleod MR, et al. Magnetic resonance imaging in experimental stroke and comparison with histology: Systematic review and meta-analysis. Stroke. 2015;46(3): 843–851. doi: 10.1161/STROKEAHA.114.007560
- Qiao J, Cai X, Xiao Q, et al. Data on MRI brain lesion segmentation using K-means and gaussian mixture modelexpectation maximization. Data Brief. 2019;27:104628. doi: 10.1016/j.dib.2019.104628
- Valverde JM, Shatillo A, De Feo R, et al. Automatic cerebral hemisphere segmentation in rat MRI with ischemic lesions via attention-based convolutional neural networks. Neuroinformat. 2023;21(1):57–70. doi: 10.1007/s12021-022-09607-1
- Kevin Zhou S, Fichtinger G, Rueckert D. Handbook of medical image computing and computer assisted intervention. Elsevier; 2019. 1043 p. doi: 10.1016/C2017-0-04608-6