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Мезенхимные стволовые клетки: свойства и клиническое применение

https://doi.org/10.18699/SSMJ20230204

Аннотация

Мезенхимные стволовые клетки (МСК) – это мультипотентные стромальные клетки, способные дифференцироваться в различные типы клеток, включая адипоциты, остеоциты, хондроциты и др. МСК могут быть выделены из различных тканей организма человека и животных. МСК характеризуются высокой пролиферативной способностью, дифференцировкой в соединительнотканном направлении, паракринной и трофической активностью (продуцируют широкий спектр биологически активных молекул), способны мигрировать в зону повреждения органов и тканей, оказывают иммуносупрессивное действие. Между МСК человека и млекопитающих имеются сходства и различия по фенотипу, функциональной активности. На экспериментальных моделях и в клинических испытаниях показан их терапевтический потенциал, что позволяет рассматривать МСК-ориентированные клеточные технологии как альтернативу традиционным способам лечения. В статье представлен обзор и анализ данных литературы, посвященной изучению свойств МСК, сигнальных путей, вовлеченных в регуляцию активности клеток, перспектив использования МСК в лечении воспалительно-дегенеративных заболеваний. В ходе подготовки обзора из баз данных eLibrary и Национального центра биотехнологической информации (NCBI) взяты полнотекстовые, свободного доступа статьи за период с 2006 по 2022 г.

Об авторе

А. П. Лыков
Новосибирский НИИ туберкулеза Минздрава России
Россия

 Лыков Александр Петрович, к.м.н. 

630040, г. Новосибирск, ул. Охотская, 81а



Список литературы

1. Мезен Н.И., Квачева З.Б., Сычик Л.М. Стволовые клетки: учебно-методическое пособие. Минск: БГМУ, 2014. 62 с.

2. Dominici M., le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defning multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–317. doi:10.1080/14653240600855905

3. Kalinina N.I., Sysoeva V.Yu., Ribina K.A.,Parfenova E.V., Tkachuk V.A. Mesenchymal stem cells in tissue growth and repair. Acta Natura. 2011;3(4):30–37.

4. Anam K., Davis T.A. Comparative analysis of gene transcripts for cell signaling receptors in bone marrow-derived hematopoietic stem/progenitor cell and mesenchymal stromal cell populations. Stem Cell Res. Ther. 2013;4(5):112. doi: 10.1186/scrt323

5. Noort W.A., Oerlemans M.I., Rozemuller H., Feyen D., Jaksani S., Stecher D., Naaijkens B., Martens A.C., Bühring H.J., Doevendans P.A., Sluijter J.P. Human versus porcine mesenchymal stromal cells: phenotype, differentiation potential, immunomodulation and cardiac improvement after transplantation. J. Cell. Mol. Med. 2012;16(8):1827–1839. doi: 10.1111/j.1582-4934.2011.01455.x

6. Lee T.C., Lee T.H., Huang Y.H., Chang N.K., Lin Y.J., Chien P.W., Yang W.H., Lin M.H. Comparison of surface markers between human and rabbit mesenchymal stem cells. PLoS One. 2014;9(11):e111390. doi:10.1371/journal.pone.0111390

7. Ghaneialvar H., Soltani L., Rahmani H.R., Lotf A.S., Soleimani M. Characterization and classifcation of mesenchymal stem cells in several species using surface markers for cell therapy purposes. Indian J. Clin. Biochem. 2018;33(1):46–52. doi: 10.1007/s12291-017-0641-x

8. Lv F.J., Tuan R.S., Cheung K.M., Leung V.Y. Concise review: the surface markers and identity of human mesenchymal stem cells. Stem. Cells. 2014;32(6):1408–1419. doi: 10.1002/stem.1681

9. Jiang W., Xu J. Immune modulation by mesenchymal stem cells. Cell Prolif. 2020;53(1):e12712. doi:10.1111/cpr.12712

10. Purwaningrum M., Jamilah N.S., Purbantoro S.D., Sawangmake C., Nantavisai S. Comparative characteristic study from bone marrow-derived mesenchymal stem cells. J. Vet. Sci. 2021;22(6):e74. doi: 10.4142/jvs.2021.22.e74

11. Liu J., Gao J., Liang Z., Gao C., Niu Q., Wu F., Zhang L. Mesenchymal stem cells and their microenvironment. Stem Cell Res. Ther. 2022;13(1):429. doi: 10.1186/s13287-022-02985-y

12. Borella G., Da Ros A., Borile G., Porcù E., Tregnago C., Benetton M., Marchetti A., Bisio V., Montini B., Michielotto B., … Pigazzi M. Targeting the plasticity of mesenchymal stromal cells to reroute the course of acute myeloid leukemia. Blood.2021;138(7):557–570. doi: 10.1182/blood.2020009845

13. Aqmasheh S., Shamsasanjan K., Akbarzadehlaleh P., Pashoutan Sarvar D., Timari H. Effects of mesenchymal stem cell derivatives on hematopoiesis and hematopoietic stem cells. Adv. Pharm. Bull. 2017;7(2):165–177. doi: 10.15171/apb.2017.021

14. Cao W., Cao K., Cao J., Wang Y., Shi Y. Mesenchymal stem cells and adaptive immune responses.Immunol. Lett. 2015;168(2):147–153. doi: 10.1016/j.imlet.2015.06.003

15. Ma Y., Wang Z., Zhang A., Xu F., Zhao N., Xue J., Zhang H., Luan X. Human placenta-derived mesenchymal stem cells ameliorate GVHD by modulating Th17/Tr1 balance via expression of PD-L2. Life Sci. 2018;214:98–105. doi: 10.1016/j.lfs.2018.10.061

16. Ivanova-Todorova E., Bochev I., Dimitrov R., Belemezova K., Mourdjeva M., Kyurkchiev S., Kinov P., Altankova I., Kyurkchiev D. Conditioned medium from adipose tissue-derived mesenchymal stem cells induces CD4+FOXP3+ cells and increases IL-10 secretion. J. Biomed. Biotechnol. 2012;2012:295167.doi: 10.1155/2012/295167

17. Kudlik G., Hegyi B., Czibula Á., Monostori É., Buday L., Uher F. Mesenchymal stem cells promote macrophage polarization toward M2b-like cells.Exp. Cell Res. 2016;348(1):36–45. doi: 10.1016/j.yexcr.2016.08.022

18. Chen C.P., Lee M.Y., Huang J.P., Aplin J.D.,Wu Y.H., Hu C.S., Chen P.C., Li H., Hwang S.M., Liu S.H., Yang Y.C. Trafcking of multipotent mesenchymal stromal cells from maternal circulation through the placenta involves vascular endothelial growth factor receptor-1 and integrins. Stem. Cells. 2008;26(2):550–561. doi: 10.1634/stemcells.2007-0406

19. Wang Y.G., Zhao Y., Li X.M., Tang B., Chu Y.N., Liu Y.L., Zhu H., Zhang Y. Effect of intercellular adhesion molecule-1 on the migration in vitro of murine mesenchymal stem cells and its related mechanism. Zhongguo Shi Yan Xue Ye Xue Za Zhi. 2014;22(2):479–484. doi: 10.7534/j.issn.1009-2137.2014.02.039

20. Balasubramanian S., Venugopal P., Sundarraj S., Zakaria Z., Majumdar A.S., Ta M. Comparison of chemokine and receptor gene expression between Wharton’s jelly and bone marrow-derived mesenchymal stromal cells. Cytotherapy. 2012;14(1):26–33. doi:10.3109/14653249.2011.605119

21. Brooke G., Tong H., Levesque J.P., Atkinson K. Molecular trafcking mechanisms of multipotent mesenchymal stem cells derived from human bone marrow and placenta. Stem. Cells Dev. 2008;17(5):929–940. doi: 10.1089/scd.2007.0156

22. Eleuteri S., Fierabracci A. Insights into the secretome of mesenchymal stem cells and its potential applications. Int. J. Mol. Sci. 2019;20(18):4597. doi:10.3390/ijms20184597

23. Andreeva E., Andrianova I., Rylova J., Gornostaeva A., Bobyleva P., Buravkova L. Proinflammatory interleukins’ production by adipose tissue-derived mesenchymal stromal cells: the impact of cell culture conditions and cell-to-cell interaction. Cell Biochem. Funct. 2015;33(6):386–393. doi: 10.1002/cbf.3125

24. Dabrowski F.A., Burdzinska A., Kulesza A., Sladowska A., Zolocinska A., Gala K., Paczek L., Wielgos M. Comparison of the paracrine activity of mesenchymal stem cells derived from human umbilical cord, amniotic membrane and adipose tissue. J. Obstet. Gynaecol. Res. 2017;43(11):1758–1768. doi: 10.1111/jog.13432

25. Kozlowska U., Krawczenko A., Futoma K., Jurek T., Rorat M., Patrzalek D., Klimczak A. Similarities and differences between mesenchymal stem/progenitor cells derived from various human tissues. World J. Stem. Cells. 2019;11(6):347–374. doi: 10.4252/wjsc.v11.i6.347

26. Ahn S.Y., Maeng Y.S., Kim Y.R., Choe Y.H., Hwang H.S., Hyun Y.M. In vivo monitoring of dynamic interaction between neutrophil and human umbilical cord blood-derived mesenchymal stem cell in mouse liver during sepsis. Stem Cell Res. Ther. 2020;11(1):44. doi: 10.1186/s13287-020-1559-4

27. Chen Y.R., Yan X., Yuan F.Z., Ye J., Xu B.B., Zhou Z.X., Mao Z.M., Guan J., Song Y.F., Sun Z.W.,… Yu J.K. The use of peripheral blood-derived stem cells for cartilage repair and regeneration in vivo: a review. Front. Pharmacol. 2020;11:404. doi: 10.3389/fphar.2020.00404

28. Longhini A.L.F., Salazar T.E., Vieira C., Trinh T., Duan Y., Pay L.M., Li Calzi S., Losh M., Johnston N.A., Xie H., … Grant M.B. Peripheral blood-derived mesenchymal stem cells demonstrate immunomodulatory potential for therapeutic use in horses. PLoS One. 2019;14(3):e0212642. doi: 10.1371/journal.pone.0212642

29. Honczarenko M., Le Y., Swierkowski M., Ghiran I., Glodek A.M., Silberstein L.E. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2006;24(4):1030–1041. doi: 10.1634/stemcells.2005-0319

30. Branly T., Contentin R., Desancé M., Jacquel T., Bertoni L., Jacquet S., Mallein-Gerin F., Denoix J.M., Audigié F., Demoor M., Galéra P. Improvement of the chondrocyte-specifc phenotype upon equine bone marrow mesenchymal stem cell differentiation: influence of culture time, transforming growth factors and type I collagen siRNAs on the differentiation index. Int. J. Mol. Sci. 2018;19(2):435. doi: 10.3390/ijms19020435

31. Jurgens W.J., Oedayrajsingh-Varma M.J., Helder M.N., Zandiehdoulabi B., Schouten T.E., Kuik D.J., Ritt M.J., van Milligen F.J. Effect of tissueharvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell Tissue Res. 2008;332(3):415–426. doi: 10.1007/s00441-007-0555-7

32. Yang Y.M., Dong X.H., Ma W.C., Guan L.H., Wang Y.H., Huang X.H., Chen J.F., Zhao X. Proliferation, differentiation and immunoregulatory capacities of brown and white adipose-derived stem cells from young and aged mice. Int. J. Stem. Cells. 2020;13(2):246–256.doi: 10.15283/ijsc20019

33. Comite P., Cobianchi L., Avanzini M.A., Mantelli M., Achille V., Zonta S., Ferrari C., Alessiani M., de Silvestri A., Gandolfo G.M., … Bernardo M.E. Immunomodulatory properties of porcine, bone marrowderived multipotent mesenchymal stromal cells and comparison with their human counterpart. Cell Mol. Biol. (Noisy-le-grand). 2011;57 Suppl:OL1600-5. 34. Heino T.J., Alm J.J., Moritz N., Aro H.T. Comparison of the osteogenic capacity of minipig and human bone marrow-derived mesenchymal stem cells. J. Orthop. Res. 2012;30(7):1019–1025. doi: 10.1002/jor.22049

34. Nemeth K., Mayer B., Sworder B.J., Kuznetsov S.A., Mezey E. A practical guide to culturing mouse and human bone marrow stromal cells. Curr. Protoc. Immunol. 2013;102:22F.12.1–22F.12.13. doi:10.1002/0471142735.im22f12s102

35. Nahar S., Nakashima Y., Miyagi-Shiohira C., Kinjo T., Kobayashi N., Saitoh I., Watanabe M., Noguchi H., Fujita J. A comparison of proteins expressed between human and mouse adipose-derived mesenchymal stem cells by a proteome analysis through liquid chromatography with tandem mass spectrometry. Int. J. Mol. Sci. 2018;19(11):3497. doi: 10.3390/ijms19113497

36. Beeravolu N., McKee C., Alamri A., Mikhael S., Brown C., Perez-Cruet M., Chaudhry R. Isolation and characterization of mesenchymal stromal cells from human umbilical cord and fetal placenta. J. Vis. Exp.2017;(122):55224. doi: 10.3791/55224

37. Hoffmann A., Floerkemeier T., Melzer C., Hass R. Comparison of in vitro-cultivation of human mesenchymal stroma/stem cells derived from bonemarrow and umbilical cord. J. Tissue Eng. Regen. Med. 2017;11(9):2565–2581. doi: 10.1002/term.2153

38. Zhang K., Li F., Yan B., Xiao D.J., Wang Y.S., Liu H. Comparison of the cytokine profle in mesenchymal stem cells from human adipose, umbilical cord, and placental tissues. Cell Reprogram. 2021;23(6):336–348. doi: 10.1089/cell.2021.0043

39. Mollentze J., Durandt C., Pepper M.S. An in vitro and in vivo comparison of osteogenic differentiation of human mesenchymal stromal/stem cells. Stem Cells Int. 2021;2021:9919361. doi: 10.1155/2021/9919361

40. Jo C.H., Yoon P.W., Kim H., Kang K.S., Yoon K.S. Comparative evaluation of in vivo osteogenic differentiation of fetal and adult mesenchymal stem cell in rat critical-sized femoral defect model. Cell Tissue Res. 2013;353(1):41–52. doi: 10.1007/s00441-013-1619-5

41. Li C., Wang F., Zhang R., Qiao P., Liu H. Comparison of proliferation and osteogenic differentiation potential of rat mandibular and femoral bone marrow mesenchymal stem cells in vitro. Stem Cells Dev. 2020;29(11):728–736. doi: 10.1089/scd.2019.0256

42. Ock S.A., Baregundi Subbarao R., Lee Y.M., Lee J.H., Jeon R.H., Lee S.L., Park J.K., Hwang S.C., Rho G.J. Comparison of immunomodulation properties of porcine mesenchymal stromal/stem cells derived from the bone marrow, adipose tissue, and dermal skin tissue. Stem Cells Int. 2016;2016:9581350. doi:10.1155/2016/9581350

43. Yang H.J., Kim K.J., Kim M.K., Lee S.J., Ryu Y.H., Seo B.F., Oh D.Y., Ahn S.T., Lee H.Y., Rhie J.W. The stem cell potential and multipotency of human adipose tissue-derived stem cells vary by cell donor and are different from those of other types of stem cells. Cells Tissues Organs. 2014;199(5-6):373–383. doi: 10.1159/000369969

44. Babenko V.A., Silachev D.N., Danilina T.I., Goryunov K.V., Pevzner I.B., Zorova L.D., Popkov V.A., Chernikov V.P., Plotnikov E.Y., Sukhikh G.T., Zorov D.B. Age-related changes in bone-marrow mesenchymal stem cells. Cells. 2021;10(6):1273. doi:10.3390/cells10061273

45. Wang Y., Zhang Z., Chi Y., Zhang Q., Xu F., Yang Z., Meng L., Yang S., Yan S., Mao A., … Han Z.C. Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis. 2013;4(12):e950. doi: 10.1038/cddis.2013.480

46. Chen Y., Hu Y., Yang L., Zhou J., Tang Y.Y., Zheng L.L. Effects of different concentrations of glucose on the osteogenic differentiation of orofacial bone mesenchymal stem cells. Sichuan Da Xue Xue Bao Yi Xue Ban. 2016;47(5):679–684.

47. Yang Y.K., Ogando C.R., Wang See C., Chang T.Y., Barabino G.A. Changes in phenotype and differentiation potential of human mesenchymal stem cells aging in vitro. Stem Cell Res. Ther. 2018;9(1):131. doi: 10.1186/s13287-018-0876-3

48. Deng X., Jing D., Liang H., Zheng D., Shao Z. H 2O2 damages the stemness of rat bone marrow-derived mesenchymal stem cells: developing a “stemness loss” model. Med. Sci. Monit. 2019;25:5613–5620. doi:10.12659/MSM.914011

49. Jasenc L., Stražar K., Mihelič A., Mihalič R., Trebše R., Haring G., Jeras M., Zupan J. In vitro characterization of the human skeletal stem cell-like properties of primary bone-derived mesenchymal stem/stromal cells in patients with late and early hip osteoarthritis. Life (Basel). 2022;12(6):899. doi: 10.3390/life12060899

50. Kohno Y., Mizuno M., Ozeki N., Katano H., Otabe K., Koga H., Matsumoto M., Kaneko H., Takazawa Y., Sekiya I. Comparison of mesenchymal stem cells obtained by suspended culture of synovium from patients with rheumatoid arthritis and osteoarthritis. BMC Musculoskelet. Disord. 2018;19(1):78. doi:10.1186/s12891-018-1998-6

51. Tang H.N., Xia Y., Yu Y., Wu R.X., Gao L.N., Chen F.M. Stem cells derived from “inflamed” and healthy periodontal ligament tissues and their sheet functionalities: a patient-matched comparison. J.Clin. Periodontol. 2016;43(1):72–84. doi: 10.1111/jcpe.12501

52. Минуллина И.Р., Дмитриева Р.И., Анисимов С.В., Билибина А.А., Тарасова О.В., Пузанов М.В., Козлова С.Н., Сазонова Ю.В., Моторин Д.В., Стругов В.В., … Шляхто Е.В. Функциональные свойства мезенхимных стволовых клеток жировой ткани больных сердечной недостаточностью и коморбидностями. Бюл. ФЦСКЭ. 2012;5:68–76.

53. Redondo-Castro E., Cunningham C., Miller J., Martuscelli L., Aoulad-Ali S., Rothwell N.J., Kielty C.M., Allan S.M., Pinteaux E. Interleukin-1 primes human mesenchymal stem cells towards an anti-inflammatory and pro-trophic phenotype in vitro. Stem Cell Res. Ther. 2017;8(1):79. doi: 10.1186/s13287-017-0531-4

54. Matsumura E., Tsuji K., Komori K., Koga H., Sekiya I., Muneta T. Pretreatment with IL-1β enhances proliferation and chondrogenic potential of synovium-derived mesenchymal stem cells. Cytotherapy. 2017;19(2):181–193. doi: 10.1016/j.jcyt.2016.11.004

55. Межевикина Л.М., Кашапова И.С. Влияние регуляторных белков LIF, FGF и IL-2 на пролиферацию мезенхимных стволовых клеток костного мозга крупного рогатого скота in vitro. Вет., зоотехния и биотехнол. 2017;(5):92–99.

56. Bastidas-Coral A.P., Hogervorst J.M.A., Forouzanfar T., Kleverlaan C.J., Koolwijk P., Klein-Nulend J., Bakker A.D. IL-6 counteracts the inhibitory effect of IL-4 on osteogenic differentiation of human adipose stem cells. J. Cell Physiol. 2019;234(11):20520–20532. doi: 10.1002/jcp.28652

57. Shen L., Zhang S., Zhang X., Zhang Y., Xie L., Jiang Y., Ma Y., Li G. Enhancing the ability of autophagy and proliferation of bone marrow mesenchymal stem cells by interleukin-8 through Akt-STAT3 pathway in hypoxic environment. Sheng Wu Gong Cheng Xue Bao. 2016;32(10):1422–1432. doi: 10.13345/j.cjb.160035

58. Wang S., Wang G., Zhang L., Li F., Liu K., Wang Y., Shi Y., Cao K. Interleukin-17 promotes nitric oxide-dependent expression of PD-L1 in mesenchymal stem cells. Cell Biosci. 2020;10:73. doi: 10.1186/s13578-020-00431-1

59. El-Zayadi A.A., Jones E.A., Churchman S.M., Baboolal T.G., Cuthbert R.J., El-Jawhari J.J., Badawy A.M., Alase A.A., El-Sherbiny Y.M., McGonagle D. Interleukin-22 drives the proliferation, migration and osteogenic differentiation of mesenchymal stem cells: a novel cytokine that could contribute to new bone formation in spondyloarthropathies. Rheumatology (Oxford). 2017;56(3):488–493. doi: 10.1093/rheumatology/kew384

60. Liang Y., Idrees E., Szojka A.R.A., Andrews S.H.J, Kunze M., Mulet-Sierra A., Jomha N.M., Adesida A.B. Chondrogenic differentiation of synovial fluid mesenchymal stem cells on human meniscus-derived decellularized matrix requires exogenous growth factors. Acta Biomater. 2018;80:131–143. doi:10.1016/j.actbio.2018.09.038

61. Wobma H.M., Tamargo M.A., Goeta S., Brown L.M., Duran-Struuck R., Vunjak-Novakovic G. The influence of hypoxia and IFN-γ on the proteome and metabolome of therapeutic mesenchymal stem cells. Biomaterials. 2018;167:226–234. doi: 10.1016/j.biomaterials.2018.03.027

62. Lykov A., Surovtseva M., Bondarenko N., Kim I., Taskaeva I., Bgatova N., Poveshchenko O. Erythropoietin and mesenchymal stem cells properties. Biointerface Research in Applied Chemistry. 2020;10(5):6197–6207. doi: 10.33263/BRIAC105.61976207

63. de Araújo Farias V., Carrillo-Gálvez A.B., Martín F., Anderson P. TGF-β and mesenchymal stromal cells in regenerative medicine, autoimmunity and cancer. Cytokine Growth Factor Rev. 2018;43:25–37. doi: 10.1016/j.cytogfr.2018.06.002

64. Lv C., Zhang T., Li K., Gao K. Bone marrow mesenchymal stem cells improve spinal function of spinal cord injury in rats via TGF-β/Smads signaling pathway. Exp. Ther. Med. 2020;19(6):3657–3663. doi:10.3892/etm.2020.8640

65. Yu F., Wu F., Li F., Liao X., Wang Y., Li X., Wang C., Shi Y., Ye L. Wnt7b-induced Sox11 functions enhance self-renewal and osteogenic commitment of bone marrow mesenchymal stem cells. Stem Cells. 2020;38(8):1020–1033. doi: 10.1002/stem.3192

66. Tian L., Xiao H., Li M., Wu X., Xie Y., Zhou J., Zhang X., Wang B. A novel Sprouty4-ERK1/2-Wnt/β-catenin regulatory loop in marrow stromal progenitor cells controls osteogenic and adipogenic differentiation. Metabolism. 2020;105:154189. doi: 10.1016/j.metabol.2020.154189

67. He Y., Zou L. Notch-1 inhibition reduces proliferation and promotes osteogenic differentiation of bone marrow mesenchymal stem cells. Exp. Ther. Med. 2019;18(3):1884–1890. doi: 10.3892/etm.2019.7765

68. Wang T., Yan R.Q., Xu X.Y., Cao L.L., Liu J.Y., Zheng M.R., Li W.D. Effects of leukaemia inhibitory factor receptor on the early stage of osteogenic differentiation of human bone marrow mesenchymal cells. Folia Biol. (Praha). 2018;64(5-6):186–194.

69. Wang T., Yan R., Xu X., Yu H., Wu J., Yang Y., Li W. Effects of leukemia inhibitory factor receptor on the adipogenic differentiation of human bone marrow mesenchymal stem cells. Mol. Med. Rep. 2019;19(6):4719–4726. doi: 10.3892/mmr.2019.10140

70. Lorthongpanich C., Thumanu K., Tangkiettrakul K., Jiamvoraphong N., Laowtammathron C., Damkham N., U-Pratya Y., Issaragrisil S. YAP as a key regulator of adipo-osteogenic differentiation in human MSCs. Stem Cell Res. Ther. 2019;10(1):402. doi:10.1186/s13287-019-1494-4

71. Zhang Q., Guo Y., Yu H., Tang Y., Yuan Y., Jiang Y., Chen H., Gong P., Xiang L. Receptor activity-modifying protein 1 regulates the phenotypic expression of BMSCs via the Hippo/Yap pathway. J. Cell Physiol. 2019;234(8):13969–13976. doi: 10.1002/jcp.28082

72. Al-Azab M., Wang B., Elkhider A., Walana W., Li W., Yuan B., Ye Y., Tang Y., Almoiliqy M., Adlat S., … Li X. Indian Hedgehog regulates senescence in bone marrow-derived mesenchymal stem cell through modulation of ROS/mTOR/4EBP1, p70S6K1/2 pathway. Aging (Albany NY). 2020;12(7):5693–5715. doi:10.18632/aging.102958

73. Krasina M.E., Kosheleva N.V., Lipina T.V., Karganov M.Yu., Medvedeva Yu.S., Lebedeva M.A., Zurina I.M., Saburina I.N. Regenerative potential of suspension and spheroids of multipotent mesenchymal stromal cells from human umbilical cord on the model of myocardial infarction in rats. Bull. Exp. Biol. Med. 2020;169(4):549–557. doi: 10.1007/s10517-020-04928-0

74. Лыков А.П., Кабаков А.В., Повещенко О.В., Бондаренко Н.А., Повещенко А.Ф., Казаков О.В., Никонорова Ю.В., Коненков В.И. Эффективность терапии клеточным продуктом острого инфаркта миокарда у крыс линии Wistar по данным биоэлектрической активности миокарда. Междунар. ж. прикл. и фундам. исслед. 2014;(8-4):78–84.

75. Bobi J., Solanes N., Fernández-Jimé-nez R., Galán-Arriola C., Dantas A.P., Fernández-Friera L., Gálvez-Montón C., Rigol-Monzó E., Agüero J., Ramírez J., … Rigol M. Intracoronary administration of allogeneic adipose tissue-derived mesenchymal stem cells improves myocardial perfusion but not left ventricle function, in a translational model of acute myocardial infarction. J. Am. Heart. Assoc. 2017;6(5):e005771. doi: 10.1161/JAHA.117.005771

76. Pei Z., Zeng J., Song Y., Gao Y., Wu R., Chen Y., Li F., Li W., Zhou H., Yang Y. In vivo imaging to monitor differentiation and therapeutic effects of transplanted mesenchymal stem cells in myocardial infarction. Sci. Rep. 2017;7(1):6296. doi: 10.1038/s41598-017-06571-8

77. Bartolucci J., Verdugo F.J., González P.L., Larrea R.E., Abarzua E., Goset C., Rojo P., Palma I., Lamich R., Pedreros P.A., … Khoury M. Safety and efcacy of the intravenous infusion of umbilical cord mesenchymal stem cells in patients with heart failure: a phase 1/2 randomized controlled trial (RIMECARD trial [Randomized clinical trial of intravenous infusion umbilical cord mesenchymal stem cells on cardiopathy]). Circ. Res. 2017;121(10):1192–1204. doi: 10.1161/CIRCRESAHA.117.310712

78. Lalu M.M., Mazzarello S., Zlepnig J., Dong Y.Y.R., Montroy J., McIntyre L., Devereaux P.J., Stewart D.J., David Mazer C., Barron C.C., McIsaac D.I., Fergusson D.A. Safety and efcacy of adult stem cell therapy for acute myocardial infarction and ischemic heart failure (SafeCell Heart): a systematic review and meta-analysis. Stem Cells Transl. Med. 2018;7(12):857–866. doi: 10.1002/sctm.18-0120

79. Повещенко О.В., Лыков А.П., Бондаренко Н.А., Ким И.И., Янкайте Е.В., Казаков О.В., Суровцева М.А., Бгатова Н.П., Карпенко А.А., Покушалов Е.А., Коненков В.И. Эффективность внутримышечного введения стволовых/прогениторных клеток в эксперименте на модели ишемии нижней конечности. Ангиол. и сосуд. хирургия. 2016;22(4):51–54.

80. Kinnaird T., Stabile E., Burnett M.S., Shou M., Lee C.W., Barr S., Fuchs S., Epstein S.E. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation. 2004;109(12):1543–1549. doi: 10.1161/01.CIR.0000124062.31102.57

81. Капутин М.Ю., Бурнос С.Н. Применение стволовых клеток для лечения больных с критической ишемией нижних конечностей. Вестн. хирургии. 2015;174(1):103–108.

82. Lu D., Jiang Y., Deng W., Zhang Y., Liang Z., Wu Q., Jiang X., Zhang L., Gao F., Cao Y., Chen B., Xue Y. Long-term outcomes of BMMSC compared with BMMNC for treatment of critical limb ischemia and foot ulcer in patients with diabetes. Cell Transplant. 2019;28(5):645–652. doi: 10.1177/0963689719835177

83. Miyamoto T., Muneta T., Tabuchi T., Matsumoto K., Saito H., Tsuji K., Sekiya I. Intradiscal transplantation of synovial mesenchymal stem cells prevents intervertebral disc degeneration through su ppression of matrix metalloproteinase-related genes in nucleus pulposus cells in rabbits. Arthritis Res. Ther.2010;12(6):R206. doi: 10.1186/ar3182

84. Lykov A.P., Bondarenko N.A., Poveshchenko O.V., Kim I.I., Surovtseva M.A., Sadykova Zh.B., Semin G.A., Zavyalov E.L., Krivoshapkin A.L., Konenkov V.I. Treatment of degenerative process in intervertebral disc in Wistar rats with mesenchymal stem cells. Bull. Exp. Biol. Med. 2020;168(4):578–582. doi:10.1007/s10517-020-04756-2

85. Blanco J.F., Villarón E.M., Pescador D., da Casa C., Gómez V., Redondo A.M., López-Villar O., López-Parra M., Muntión S., Sánchez-Guijo F. Autologous mesenchymal stromal cells embedded in tricalcium phosphate for posterolateral spinal fusion: results of a prospective phase I/II clinical trial with long-term follow-up. Stem Cell Res. Ther. 2019;10(1):63. doi:10.1186/s13287-019-1166-4

86. García de Frutos A., González-Tartière P., Coll Bonet R., Ubierna Garcés M.T., Del Arco Churruca A., Rivas García A., Matamalas Adrover A., Saló Bru G., Velazquez J.J., Vila-Canet G., … Càceres Palou E. Randomized clinical trial: expanded autologous bone marrow mesenchymal cells combined with allogeneic bone tissue, compared with autologous iliac crest graft in lumbar fusion surgery. Spine J. 2020;20(12):1899–1910. doi: 10.1016/j.spinee.2020.07.014

87. Lykov A.P., Bondarenko N.A., Poveshchenko O.V., Miller T.V., Poveshchenko A.F., Surovtseva M.A., Bgatova N.P., Konenkov V.I. Prospect of using cell product for the therapy of skin defects in diabetes mellitus. Bull. Exp. Biol. Med. 2017;164(2):266–268.doi: 10.1007/s10517-017-3970-0

88. Imam R.A., Rizk A.A. Efcacy of erythropoietin-pretreated mesenchymal stem cells in murine burn wound healing: possible in vivo transdifferentiation into keratinocytes. Folia Morphol. (Warsz).2019;78(4):798–808. doi: 10.5603/FM.a2019.0038

89. Caliari-Oliveira C., Yaochite J.N., Ramalho L.N., Palma P.V., Carlos D., Cunha Fde Q., de Souza D.A., Frade M.A., Covas D.T., Malmegrim K.C., Oliveira M.C., Voltarelli J.C. Xenogeneic mesenchymal stromal cells improve wound healing and modulate the immune response in an extensive burn model. Cell Transplant. 2016;25(2):201–215. doi:10.3727/096368915X688128

90. Lopes L., Setia O., Aurshina A., Liu S., Hu H., Isaji T., Liu H., Wang T., Ono S., Guo X., Yatsula B., Guo J., Gu Y., Navarro T., Dardik A. Stem cell therapy for diabetic foot ulcers: a review of preclinical and clinical research. Stem Cell Res. Ther. 2018;9(1):188. doi:10.1186/s13287-018-0938-6

91. Fouad H., Sabry D., Elsetohy K., Fathy N. Therapeutic efcacy of amniotic membrane stem cells and adipose tissue stem cells in rats with chemically induced ovarian failure. J. Adv. Res. 2016;7(2):233–241.doi: 10.1016/j.jare.2015.05.002

92. Wang L.L., Yu Y., Guan H.B., Qiao C. Effect of human umbilical cord mesenchymal stem cell transplantation in a rat model of preeclampsia. Reprod. Sci. 2016;23(8):1058–1070. doi: 10.1177/1933719116630417

93. Lykov A.P., Poveshchenko O.V., Surovtseva M.A., Kim I.I., Bgatova N.P. Therapeutic potential of biomedical cell product in DSS-induced inflammation in the small intestine of C57Bl/6 mice. Bull. Exp.Biol. Med. 2018;165(4):576–580. doi: 10.1007/s10517-018-4216-5

94. Miyamoto S., Ohnishi S., Onishi R., Tsuchiya I., Hosono H., Katsurada T., Yamahara K., Takeda H., Sakamoto N. Therapeutic effects of human amnion-derived mesenchymal stem cell transplantation and conditioned medium enema in rats with trinitrobenzene sulfonic acid-induced colitis. Am. J. Transl. Res. 2017;9(3):940–952.

95. Wang R., Yuan W., Zhao Q., Song P., Yue J., Lin S.D., Zhao T.B. An experimental study of preventing and treating acute radioactive enteritis with human umbilical cord mesenchymal stem cells. Asian Pac. J. Trop. Med. 2013;6(12):968–971. doi: 10.1016/S1995-7645(13)60173-X

96. Sherman A.B., Gilger B.C., Berglund A.K., Schnabel L.V. Effect of bone marrow-derived mesenchymal stem cells and stem cell supernatant on equine corneal wound healing in vitro. Stem Cell Res. Ther. 2017;8(1):120. doi: 10.1186/s13287-017-0577-3

97. Carter K., Lee H.J., Na K.S., Fernandes-Cunha G.M., Blanco I.J., Djalilian A., Myung D. Characterizing the impact of 2D and 3D culture conditions on the therapeutic effects of human mesenchymal stemcell secretome on corneal wound healing in vitro and ex vivo. Acta Biomater. 2019;99:247–257. doi: 10.1016/j.actbio.2019.09.022

98. Limoli P.G., Vingolo E.M., Limoli C., Nebbioso M. Antioxidant and biological properties of mesenchymal cells used for therapy in retinitis pigmentosa. Antioxidants (Basel). 2020;9(10):983. doi: 10.3390/antiox9100983

99. Oliva J. Therapeutic properties of mesenchymal stem cell on organ ischemia-reperfusion injury. Int. J. Mol. Sci. 2019;20(21):5511. doi: 10.3390/ijms20215511

100. Archambault J., Moreira A., McDaniel D., Winter L., Sun L., Hornsby P. Therapeutic potential of mesenchymal stromal cells for hypoxic ischemic encephalopathy: A systematic review and meta-analysis of preclinical studies. PLoS One. 2017;12(12):e0189895.doi: 10.1371/journal.pone.0189895

101. Jafarzadeh Bejargafshe M., Hedayati M., Zahabiasli S., Tahmasbpour E., Rahmanzadeh S., NejadMoghaddam A. Safety and efcacy of stem cell therapy for treatment of neural damage in patients with multiple sclerosis. Stem. Cell Investig. 2019;6:44. doi: 10.21037/sci.2019.10.06

102. Gutiérrez-Fernández M., Rodríguez-Frutos B., Ramos-Cejudo J., Teresa Vallejo-Cremades M., Fuentes B., Cerdán S., Díez-Tejedor E. Effects of intravenous administration of allogenic bone marrow- and adipose tissue-derived mesenchymal stem cells on functional recovery and brain repair markers in experimental ischemic stroke. Stem Cell Res. Ther. 2013;4(1):11. doi:10.1186/scrt159

103. Рудаков В.С., Деев Р.В., Губарев К.К., Астрелина Т.А., Еремин И.И., Жгутов Ю.А., Онницев Е.И., Мавликеев М.О., Титова А.А., Восканян С.Э. Влияние трансплантации аллогенных мультипотентных мезенхимальных стромальных клеток костного мозга на регенерацию печени после обширной резекции в эксперименте. Гены и клетки. 2018;13(2):83–88. doi: 10.23868/201808025

104. Yang X., Meng Y., Han Z., Ye F., Wei L., Zong C. Mesenchymal stem cell therapy for liver disease: full of chances and challenges. Cell Biosci. 2020;10:123. doi: 10.1186/s13578-020-00480-6

105. Cao Z., Zhang G., Wang F., Liu H., Liu L., Han Y., Zhang J., Yuan J. Protective effects of mesenchymal stem cells with CXCR4 up-regulation in a rat renal transplantation model. PLoS One. 2013;8(12):e82949. doi: 10.1371/journal.pone.0082949

106. Hostettler K.E., Gazdhar A., Khan P., Savic S., Tamo L., Lardinois D., Roth M., Tamm M., Geiser T. Multipotent mesenchymal stem cells in lung fbrosis. PLoS One. 2017;12(8):e0181946. doi: 10.1371/journal.pone.0181946

107. Tsai P.J., Wang H.S., Shyr Y.M., Weng Z.C., Tai L.C., Shyu J.F., Chen T.H. Transplantation of insulin-producing cells from umbilical cord mesenchymal stem cells for the treatment of streptozotocin-induced diabetic rats. J. Biomed. Sci. 2012;19(1):47. doi:10.1186/1423-0127-19-47

108. Pochon C., Notarantonio A.B., Laroye C., Reppel L., Bensoussan D., Bertrand A., Rubio M.T., d’Aveni M. Wharton’s jelly-derived stromal cells and their cell therapy applications in allogeneic haematopoietic stem cell transplantation. J. Cell. Mol. Med. 2022;26(5):1339–1350. doi: 10.1111/jcmm.17105

109. Nachmias B., Zimran E., Avni B. Mesenchymal stroma/stem cells: Haematologists’ friend or foe? Br. J. Haematol. 2022;199(2):175–189. doi: 10.1111/bjh.18292

110. Zhao L., Chen S., Yang P., Cao H., Li L. The role of mesenchymal stem cells in hematopoietic stem cell transplantation: prevention and treatment of graft-versus-host disease. Stem Cell Res. Ther.2019;10(1):182. doi: 10.1186/s13287-019-1287-9

111. Ringdén O., Moll G., Gustafsson B., Sadeghi B. Mesenchymal stromal cells for enhancing hematopoietic engraftment and treatment of graft-versushost disease, hemorrhages and acute respiratory distress syndrome. Front. Immunol. 2022;13:839844. doi: 10.3389/fmmu.2022.839844

112. Nagoba B., Gavkare A., Rayate A., Mumbre S.Positive aspects, negative aspects and challenges associated with stem cell therapy for COVID-19: a mini-review. Curr. Stem Cell Res. Ther. 2022;17(8):720–726. doi: 10.2174/1574888X16666211102092039

113. Kavianpour M., Saleh M., Verdi J. The role of mesenchymal stromal cells in immune modulation of COVID-19: focus on cytokine storm. Stem Cell Res. Ther. 2020;11(1):404. doi: 10.1186/s13287-020-01849-7

114. Wang Q. Li T., Wu W., Ding G. Interplay between mesenchymal stem cell and tumor and potential application. Hum. Cell. 2020;33(3):444–458. doi:10.1007/s13577-020-00369-z

115. Zhao M., Sachs P.C., Wang X., Dumur C.I., Idowu M.O., Robila V., Francis M.P., Ware J., Beckman M., Rizki A., Holt S.E., Elmore L.W. Mesenchymal stem cells in mammary adipose tissue stimulate progression of breast cancer resembling the basal-type. Cancer Biol. Ther. 2012;13(9):782–792. doi: 10.4161/cbt.20561

116. Shahab-Osterloh S., Witte F., Hoffmann A., Winkel A., Laggies S., Neumann B., Seiffart V., Lindenmaier W., Gruber A.D., Ringe J., … Gross G. Mesenchymal stem cell-dependent formation of heterotopic tendon-bone insertions (osteotendinous junctions). Stem Cells. 2010;28(9):1590–1601. doi: 10.1002/stem.487

117. Petrou P., Kassis I., Levin N., Paul F., Backner Y., Benoliel T., Oertel F.C., Scheel M., Hallimi M., Yaghmour N., … Karussis D. Benefcial effects of autologous mesenchymal stem cell transplantation in active progressive multiple sclerosis. Brain. 2020;143(12):3574–3588. doi: 10.1093/brain/awaa333

118. Shoukrie S.I., Venugopal S., Dhanoa R.K., Selvaraj R., Selvamani T.Y., Zahra A., Malla J., Hamouda R.K., Hamid P.F. Safety and efcacy of injecting mesenchymal stem cells into a human knee joint to treat osteoarthritis: a systematic review. Cureus. 2022;14(5):e24823. doi: 10.7759/cureus.24823

119. Shu P., Sun D.L., Shu Z.X., Tian S., Pan Q., Wen C.., Xi J.Y., Ye S.N. Therapeutic applications of genes and gene-engineered mesenchymal stem cells for femoral head necrosis. Hum. Gene Ther. 2020;31(5-6):286–296. doi: 10.1089/hum.2019.306

120. Hu C., Li L. Preconditioning influences mesenchymal stem cell properties in vitro and in vivo. J. Cell Mol. Med. 2018;22(3):1428–1442. doi: 10.1111/jcmm.13492

121. Rafat A., Mohammadi Roushandeh A., Alizadeh A., Hashemi-Firouzi N., Golipoor Z. Comparison of the melatonin preconditioning efcacy between bone marrow and adipose-derived mesenchymal stem cells. Cell J. 201;20(4):450–458. doi: 10.22074/cellj.2019.5507

122. Entrena A., Varas A., Vázquez M., Melen G.J., Fernández-Sevilla L.M., García-Castro J., Ramírez M.,Zapata A.G., Vicente Á. Mesenchymal stem cells derived from low risk acute lymphoblastic leukemia patients promote NK cell antitumor activity. Cancer Lett. 201;363(2):156–165. doi: 10.1016/j.canlet.2015.04.012

123. Vatsa P., Negi R., Ansari U.A., Khanna V.K., Pant A.B. Insights of extracellular vesicles of mesenchymal stem cells: a prospective cell-free regenerative medicine for neurodegenerative disorders. Mol. Neurobiol. 2022;59(1):459–474. doi: 10.1007/s12035-021-02603-7

124. Tang H., Luo H., Zhang Z., Yang D. Mesenchymal Stem Cell-Derived Apoptotic Bodies: Biological Functions and Therapeutic Potential. Cells. 2022;11(23):3879. doi: 10.3390/cells11233879

125. Batsali A.K. Georgopoulou A., Mavroudi I., Matheakakis A., Pontikoglou C.G., Papadaki H.A. The role of bone marrow mesenchymal stem cell derived extracellular vesicles (MSC-EVs) in normal and abnormal hematopoiesis and their therapeutic potential. J. Clin. Med. 2020;9(3):856. doi: 10.3390/jcm9030856

126. Mendt M., Rezvani K., Shpall E. Mesenchymal stem cell-derived exosomes for clinical use. Bone Marrow Transplant. 201954(Suppl 2):789–792. doi:10.1038/s41409-019-0616-z

127. Hu C., Zhao L., Zhang L. Bao Q., Li L. Mesenchymal stem cell-based cell-free strategies: safe and effective treatments for liver injury. Stem Cell Res. Ther. 2020;11(1):377. doi: 10.1186/s13287-020-01895-1


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Лыков А.П. Мезенхимные стволовые клетки: свойства и клиническое применение. Сибирский научный медицинский журнал. 2023;43(2):40-53. https://doi.org/10.18699/SSMJ20230204

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Lykov A.P. Mesenchymal stem cells: properties and clinical application. Сибирский научный медицинский журнал. 2023;43(2):40-53. (In Russ.) https://doi.org/10.18699/SSMJ20230204

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