- Transplantation of stem and progenitor cells in the long term for correction of the consequences of hypoxic-ischemic encephalopathy of newborn babies
Transplantation of stem and progenitor cells in the long term for correction of the consequences of hypoxic-ischemic encephalopathy of newborn babies
HEALTH OF WOMAN. 2016.10(116):110–120
Transplantation of stem and progenitor cells in the long term for correction of the consequences of hypoxic-ischemic encephalopathy of newborn babies
Veropotvelyan P. N., Tsehmistrenko I. S., Veropotvelyan N. P., Guzhevskaya I. V., Zhabitska L. A., Zhuravleva C. A.
«Interregional centre of medical genetics and prenatal diagnosis», Krivoy Rog
Perinatal center, Kiev
National medical University named after O. O. Bogomolets, Kyiv
The review included the results of the mechanism of therapeutic action of stem cells in cerebral disorders in newborn babies.
The results of the review of foreign publications to analyze different aspects of cell therapy, from the type of stem cells and sources. Studied the components that determine the positive effect in relation to the treatment of ischemia/hypoxia of the brain.Shown high therapeutic efficiency of cellular technologies and the prospects of their application in neonatology. However, it is necessary to study this problem, aimed at a comprehensive characterization of cell type and dose, the optimal time and method of their conduct for the most effective application of cell therapy.
Key words: stem cells, newborn infants, hypoxic-ischemic encephalopathy, asphyxia.
REFERENCES
1. Ali JM, Bolton EM, Bradley JA, Pettigrew GJ. 2013. Allorecognition pathways in transplant rejection and tolerance. Transplantation 96(8):681-8. https://doi.org/10.1097/TP.0b013e31829853ce; PMid:23715047
2. Antonov AG, Ionov OV, Kirtbaya AR, Balashova EN, Nikitina IV, Ryndin AY, Miroschnik EV, Degtyarev DN. 2014. The methodology of therapeutic hypothermia to children born in a state of asphyxia. Anesthesiology and Intensive Care 59(6):76-7.
3. Ashwal S, Ghosh N, Turenius CI, Dulcich M, Denham CM, Tone B et al. 2014. Reparative effects of neural stem cells in neonatal rats with hypoxic-ischemic injury are not influenced by host sex. Pediatr. Res. 75(5):603-11. https://doi.org/10.1038/pr.2014.7; PMid:24463490 PMCid:PMC4404035
4. Bae SH, Kong TH, Lee HS, Kim KS, Hong KS, Chopp M et al. 2012. Long-lasting paracrine effects of human cord blood cells on damaged neocortex in an animal model of cerebral palsy. Cell Transplant. 21(11):2497-515. https://doi.org/10.3727/096368912X640457; PMid:22524897
5. Bahr L, Batsis I, Moll G, Hagg M, Szakos A, Sundberg В et al. 2012. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells. 30(7):1575-8. https://doi.org/10.1002/stem.1118; PMid:22553154
6. Baranov AA, Albitsky VY, Volgina SY, Mendelevich VD. 2001. Premature babies in childhood and adolescence (medical and psychosocial research). M:184.
7. Bohlin K. 2016. Cell-based strategies to reconstitute vital functions in preterm infants with organ failure. Best Pract. Res. Clin. Obstet. Gynecol. 31:99-111. https://doi.org/10.1016/j.bpobgyn.2015.08.012; PMid:26527306
8. Borghesi A, Cova C, Gazzolo D, Stronati M. 2013. Stem cell therapy for neonatal diseases associated with preterm birth. J. Clin. Neonatol. 2(1):1-7. https://doi.org/10.4103/2249-4847.109230; PMid:24027735 PMCid:PMC3761956
9. Borlongan CV, Hadman M, Sanberg CD, Sanberg PR. 2004. Central nervous system entry of peripherally infected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke. 35(10):2385-9. https://doi.org/10.1161/01.STR.0000141680.49960.d7; PMid:15345799
10. Cameron SH, Alwakeel AJ, Goddard L, Hobbs CE, Gowing EK, Barnett ER et al. 2015. Delayed post-treatment with bone marrow-derived mesenchymal stem cells is neurorestorative of striatal medium-spiny projection neurons and improves motor function after neonatal rat hypoxia-ischemia. Mol. Cell. Neurosci. 68:56-72. https://doi.org/10.1016/j.mcn.2015.03.019; PMid:25828540
11. Carroll J. 2012. Human cord blood for the hypoxic-ischemic reonate. Pediatric Research. 71:459–463. https://doi.org/10.1038/pr.2011.53; PMid:22278181 PMCid:PMC3640287
12. Chen L, Huang H, Xi H, Xie Z, Liu R, Jiang Z et al. 2010. Intracranial transplant of olfactory ensheathing cells in children and adolescents with cerebral palsy: a randomized controlled clinical trial. Cell Transplant. 19(2):185-91. https://doi.org/10.3727/096368910X492652; PMid:20350360
13. Chua JY, Pendharkar AV, Wang N, Choi R, Andres RH, Gaeta X et al. 2011. Intra-arterial injection of neural stem cells using a microneedle technique does not cause microembolic strokes. J. Cereb. Blood Flow Metab. 31(5):1263-71. https://doi.org/10.1038/jcbfm.2010.213; PMid:21157474 PMCid:PMC3099630
14. Chou RH, Lu CY, Fan JR, Yu YL, Shyu WC. 2014. The potential therapeutic applications of olfactory ensheathing cells in regenerative medicine. Cell Transplant. 23(4-5):567-71. https://doi.org/10.3727/096368914X678508; PMid:24816451
15. Comi AM, Cho E, Mulholland JD, Hooper A, Li Q, Qu Y et al. 2008. Neural stem cells reduce brain injury after unilateral carotid ligation. Pediatr. Neurol. 38(2):86-92. https://doi.org/10.1016/j.pediatrneurol.2007.10.007; PMid:18206788
16. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E et al. 2009. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells. 27(10):2624-35. https://doi.org/10.1002/stem.194; PMid:19676124
17. Cotten CM, Murtha AP, Goldberg RN, Grotegut CA, Smith PB, Goldstein RF et al. 2014. Feasibility of autologous cord blood cells for infants with hypoxic-ischemic encephalopathy. J. Pediatr. 164(5):973-9. e1.
18. Cui LL, Kerkela E, Bakreen A, Nitzsche F, Andrzejewska A, Nowakowski A et al. 2015. The cerebral embolism evoked by intra-arterial delivery of allogeneic bone marrow mesenchymal stem cells in rats is related to cell dose and infusion velocity. Stem Cell Res. Ther. 6:11. https://doi.org/10.1186/scrt544; PMid:25971703 PMCid:PMC4429328
19. Daadi MM, Davis AS, Arac A, Li Z, Maag AL, Bhatnagar R et al. 2010. Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic-ischemic brain injury. Stroke. 41(3):516-23. https://doi.org/10.1161/STROKEAHA.109.573691; PMid:20075340
20. Danielyan L, Schafer R, von Ameln-Mayerhofer A, Buadze M, Geisler J, Klopfer T et al. 2009. Intranasal delivery of cells to the brain. Eur. J. Cell Biol. 88(6):315-24. https://doi.org/10.1016/j.ejcb.2009.02.001; PMid:19324456
21. Davies MW, Swaminathan M, Chuang SL, Betheras FR. 2000. Reference ranges for the linear dimensions of the intracranial ventricles in preterm neonates. Arch. Dis. Child. Fetal Neonatal Ed. 82(3):F218-23. https://doi.org/10.1136/fn.82.3.F218; PMid:10794790 PMCid:PMC1721078
22. Donega V, van Velthoven C, Nijboer C et al. 2013. Intranasal mesenchymal stem cell treatment for neonatal brain damage: long-term cognitive and sensorimotor improvement. PLoS ONE. 8:e51253. https://doi.org/10.1371/journal.pone.0051253; PMid:23300948 PMCid:PMC3536775
23. Donega V, Nijboer CH, van Velthoven CT, Youssef SA, de Bruin A, van Bel F et al. 2015. Assessment of long-term safety and efficacy of intranasal mesenchymal stem cell treatment for neonatal brain injury in the mouse. Pediatr. Res. 78(5):520-6. https://doi.org/10.1038/pr.2015.145; PMid:26270577 PMCid:PMC4635434
24. Donega V, van Velthoven CT, Nijboer CH, Kavelaars A, Heijnen CJ. 2013. The endogenous regenerative capacity of the damaged newborn brain: boosting neurogenesis with mesenchymal stem cell treatment. J. Cereb. Blood Flow Metab. 33(5):625-34. https://doi.org/10.1038/jcbfm.2013.3; PMid:23403379 PMCid:PMC3652688
25. Donega V, Nijboer CH, van Tilborg G, Dijkhuizen RM, Kavelaars A, Heijnen CJ. 2014. Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury. Exp. Neurol. 261:53-64. https://doi.org/10.1016/j.expneurol.2014.06.009; PMid:24945601
26. Efimova O. A. Molecular biology for bioinformatics /no10_epigenetika-1.ppt
27. Erices A, Conget P, Minguell JJ. 2000. Mesenchymal progenitor cells in human umbilical cord blood. J. Br. J. Haematol. 109(1):235-42. https://doi.org/10.1046/j.1365-2141.2000.01986.x; PMid:10848804
28. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL et al. 1998. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat. Biotechnol. 16(11):1033-9. https://doi.org/10.1038/3473; PMid:9831031
29. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. 2001. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs. 169(1):12-20. https://doi.org/10.1159/000047856; PMid:11340257
30. Greggio S, de Paula S, Azevedo PN, Venturin GT, Dacosta JC. 2014. Intra-arterial transplantation of human umbilical cord blood mononuclear cells in neonatal hypoxic-ischemic rats. Life Sci. 96(1-2):33-9. https://doi.org/10.1016/j.lfs.2013.10.017; PMid:24177600
31. Guan LX, Guan H, Li HB, Ren CA, Liu L, Chu JJ et al. 2015. Therapeutic efficacy of umbilical cord-derived mesenchymal stem cells in patients with type 2 diabetes. Exp. Ther. Med. 9(5):1623-30. https://doi.org/10.3892/etm.2015.2339
32. Gutierrez-Fernandez M, Rodriguez-Frutos B, Alvarez-Grech J, Vallejo-Cremades MT, Exposito-Alcaide M, Merino J et al. 2011. Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience 175:394-405. https://doi.org/10.1016/j.neuroscience.2010.11.054; PMid:21144885
33. Guzman R, Choi R, Gera A, De Los Angeles A, Andres RH, Steinberg GK. 2008. Intravascular cell replacement therapy for stroke. Neurosurg. Focus. 24(3-4):E15. https://doi.org/10.3171/FOC/2008/24/3-4/E14; PMid:18341391
34. Hass R, Kasper C, Bohm S, Jacobs R. 2011. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun. Signal. 9:12. https://doi.org/10.1186/1478-811X-9-12; PMid:21569606 PMCid:PMC3117820
35. Hirschi KK, Li S, Roy K. 2014. Induced pluripotent stem cells for regenerative medicine. Annu. Rev. Biomed. Eng. 16:277-94. https://doi.org/10.1146/annurev-bioeng-071813-105108; PMid:24905879 PMCid:PMC4287204
36. Hori J, Ng TF, Shatos M, Klassen H, Streilein JW, Young MJ. 2003. Neural progenitor cells lack immunogenicity and resist destruction as allografts. Stem Cells. 21(4):405-16. https://doi.org/10.1634/stemcells.21-4-405; PMid:12832694
37.http://dbyne.moy.su/news/kogda_vyrastjat_iskusstvennuju_pechen_i_pri_chem_tu/2014-06-25-162
38. http://sciencevsaging.org/content/свободный-/-9
39. http://biofile.ru/bio/19658.html
40. Iguchi A, Terashita Y, Sugiyama M, Ohshima J, Sato TZ, Cho Y et al. 2016. Graft-versus-host disease (GVHD) prophylaxis by using methotrexate decreases pre-engraftment syndrome and severe acute GVHD, and accelerates engraftment after cord blood transplantation. Pediatr. Transplant. 20(1):114-9. https://doi.org/10.1111/petr.12621; PMid:26526424
41. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD et al. 2004. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. USA. 101(52):18117-22. https://doi.org/10.1073/pnas.0408258102; PMid:15608062 PMCid:PMC536055
42. Janowski M, Lyczek A, Engels C, Xu J, Lukomska B, Bulte JW et al. 2013. Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J. Cereb. Blood Flow Metab. 33(6):921-7. https://doi.org/10.1038/jcbfm.2013.32; PMid:23486296 PMCid:PMC3677113
43. Jansen EM, Solberg L, Underhill S, Wilson S, Cozzari C, Hartman BK et al. 1997. Transplantation of fetal neocortex ameliorates sensorimotor and locomotor deficits following neonatal ischemic-hypoxic brain injury in rats. Exp. Neurol. 147(2):487-97. https://doi.org/10.1006/exnr.1997.6596; PMid:9344572
44. Jin K, Sun Y, Xie L, Mao XO, Childs J, Peel A et al. 2005. Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol. Dis. 18(2):366-74. https://doi.org/10.1016/j.nbd.2004.10.010; PMid:15686965
45. Johnston MV, Hagberg H. 2007. Sex and the pathogenesis of cerebral palsy. Dev. Med. Child Neurol. 49(1):74-8. https://doi.org/10.1017/S0012162207000199.x; PMid:17209983
46. Kao CH, Chen SH, Chio CC, Lin MT. 2008. Human umbilical cord blood-derived CD34+ cells may attenuate spinal cord injury by stimulating vascular endothelial and neurotrophic factors. Shock. 29(1):49-55. PMid:17666954
47. Keroll D. 2013. The use of stem cells in hypoxic-ischemic brain damage of newborn pulp. Magazine «cell and organ transplantation» 1(1).
48. Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E et al. 2007. Morphological and molecular characterization of novel population of CXCR4+ SSEA-4+ Oct-4+ very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia. 21(2):297-303. https://doi.org/10.1038/sj.leu.2404470; PMid:17136117
49. Larijani B, Esfahani EN, Amini P, Nikbin B, Alimoghaddam K, Amiri S et al. 2012. Stem cell therapy in treatment of different diseases. Acta Med. Iran. 50(2):79-96. PMid:22359076
50. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I et al. 2008. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet. 371(9624):1579-86. https://doi.org/10.1016/s0140-6736(08)60690-x
51. Li L, Jiang Q, Ding G, Zhang L, Zhang ZG, Li Q et al. 2010. Effects of administration route on migration and distribution of neural progenitor cells transplanted into rats with focal cerebral ischemia, an MRI study. J. Cereb. Blood Flow Metab. 30(3):653-62. https://doi.org/10.1038/jcbfm.2009.238; PMid:19888287 PMCid:PMC2844252
52. Lin RZ, Dreyzin A, Aamodt K, Dudley AC, Melero-Martin JM. 2011. Functional endothelial progenitor cells from cryopreserved umbilical cord blood. Cell Transplant. 20(4):515-22. https://doi.org/10.3727/096368910X532729; PMid:20887663 PMCid:PMC3036780
53. Li M, Hale JS, Rich JN, Ransohoff RM, Lathia JD. 2012. Chemokine CXCL12 in neurodegenerative diseases: an SOS signal for stem cell-based repair. Trends Neurosci. 35(10):619-28. https://doi.org/10.1016/j.tins.2012.06.003; PMid:22784557 PMCid:PMC3461091
54. Luan Z, Yin G, Hu X et al. 2005. Treatment of an infant with severe neonatal hypoxic-ischemic encephalopathy sequelae with transplantation of human neural stem cells into cerebral ventricle. Zhonghua Erke Zazhi. 43:580–583. PMid:16191266
55. Luan Z, Liu W, Qu S et al. 2011. Treatment of newborns with severe injured brain with transplantation of human neural precursor cells. Zhonghua Erke Zazhi. 49:445–449. PMid:21924058
56. Lundberg J, Sodersten E, Sundstrom E, Le Blanc K, Andersson T, Hermanson O et al. 2012. Targeted intra-arterial transplantation of stem cells to the injured CNS is more effective than intravenous administration: engraftment is dependent on cell type and adhesion molecule expression. Cell Transplant. 21(1):333-43. https://doi.org/10.3727/096368911X576036; PMid:21669035
57. Ma L, Zhou Z, Zhang D, Yang S, Wang J, Xue F et al. 2012. Immunosuppressive function of mesenchymal stem cells from human umbilical cord matrix in immune thrombocytopenia patients. Thromb. Haemost. 107(5):937-50. https://doi.org/10.1160/TH11-08-0596; PMid:22398715
58. Ma S, Xie N, Li W, Yuan B, Shi Y, Wang Y. 2014. Immunobiology of mesenchymal stem cells. Cell Death Differ. 21(2):216-25. https://doi.org/10.1038/cdd.2013.158; PMid:24185619 PMCid:PMC3890955
59. Mancias-Guerra C, Marroquin-Escamilla AR, Gonzalez-Llano O, Villarreal-Martinez L, Jaime-Perez JC, Garcia-Rodriguez F et al. 2014. Safety and tolerability of intrathecal delivery of autologous bone marrow nucleated cells in children with cerebral palsy: an open-label phase I trial. Cytotherapy. 16(6):810-20. https://doi.org/10.1016/j.jcyt.2014.01.008; PMid:24642016
60. Meier C, Middelanis J, Wasielewski B et al. 2006. Spastic paresis after perinatal brain damage in rats is reduced by human cord blood mononuclear cells. Pediatric Research. 59:244-249. https://doi.org/10.1203/01.pdr.0000197309.08852.f5; PMid:16439586
61. Misra V, Lal A, El Khoury R, Chen PR, Savitz SI. 2012. Intra-arterial delivery of cell therapies for stroke. Stem Cells Dev. 21(7):1007-15. https://doi.org/10.1089/scd.2011.0612; PMid:22181047 PMCid:PMC3328761
62. Mitsialis SA, Kourembanas S. 2016. Stem cell-based therapies for the newborn lung and brain: Possibilities and challenges. Semin. Perinatol. 40(3):138-51. https://doi.org/10.1053/j.semperi.2015.12.002; PMid:26778234 PMCid:PMC4808378
63. Murase S, Horwitz AF. 2002. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J. Neurosci. 22(9):3568-79. PMid:11978833
64. Narogan MV, Vorona LD, Petraki VL, Prityko AG, Simernitsky BP, Romanova RI, Sidorenko EE, Malyutina LV, Petrova A. 2013. Experience of extremely premature infants with intraventricular hemorrhage complicated by progressive hydrocephalus. Russian Vestnik Perinatology and pediatrics 58(3):25-9.
65. Najar M, Raicevic G, Crompot E, Fayyad-Kazan H, Bron D, Toungouz M et al. 2016. The immunomodulatory potential of mesenchymal stromal cells: a story of a regulatory network. J. Immunother. 39(2):45-59. https://doi.org/10.1097/CJI.0000000000000108; PMid:26849074
66. Naujock M, Stanslowsky N, Reinhardt P, Sterneckert J, Haase A, Martin U et al. 2014. Molecular and functional analyses of motor neurons generated from human cord-blood-derived induced pluripotent stem cells. Stem Cells Dev. 23(24):3011-20. https://doi.org/10.1089/scd.2014.0180; PMid:25007389
67. Newell LF, Flowers ME, Gooley TA, Milano F, Carpenter PA, Martin PJ et al. 2013. Characteristics of chronic GVHD after cord blood transplantation. Bone Marrow Transplant. 48(10):1285-90. https://doi.org/10.1038/bmt.2013.48; PMid:23584444 PMCid:PMC3795867
68. Nimgaonkar MT, Roscoe R, Persichetti J, Rybka WB, Winkelstein A, Ball ED. 1995. A unique population of CD34+ cells in cord blood. Stem Cells. 13(2):158-66. https://doi.org/10.1002/stem.5530130207; PMid:7540469
69. Northington FJ. 2006. Brief update on animal models of hypoxic-ischemic encephalopathy and neonatal stroke. ILAR. J. 47(1):32-8. https://doi.org/10.1093/ilar.47.1.32; PMid:16391429
70. Obenaus A, Dilmac N, Tone B, Tian HR, Hartman R, Digicayliog M et al. 2011. Long-term magnetic resonance imaging of stem cells in neonatal ischemic injury. Ann. Neurol. 69(2):282-91. https://doi.org/10.1002/ana.22168; PMid:21387373 PMCid:PMC3069664
71. Palmer TD, Schwartz PH, Taupin P, Kaspar B, Stein SA, Gage FH. 2001. Cell culture. Progenitor cells from human brain after death. Nature 411(6833):42-3. https://doi.org/10.1038/35075141; PMid:11333968
72. Paula S, Greggio S, Marinowic DR, Machado DC, DaCosta JC. 2012. The dose-response effect of acute intravenous transplantation of human umbilical cord blood cells on brain damage and spatial memory deficits in neonatal hypoxia-ischemia. Neuroscience 210:431-41. https://doi.org/10.1016/j.neuroscience.2012.03.009; PMid:22441035
73. Pendharkar AV, Chua JY, Andres RH, Wang N, Gaeta X, Wang H et al. 2010. Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke. 41(9):2064-70. https://doi.org/10.1161/STROKEAHA.109.575993; PMid:20616329 PMCid:PMC4831577
74. Perlman JM. 2006. Summary proceedings from the neurology group on hypoxic-ischemic encephalopathy. Pediatrics. 117(3;2):28-33.
75. Poltavtseva RA, Rzhaninova AA, Revishchin AV, Aleksandrova MA, Korochkin LI, Repin VS et al. 2001. In vitro development of neural progenitor cells from human embryos. Bull. Exp. Biol. Med. 132(3):861-3. https://doi.org/10.1023/A:1013170701936; PMid:11740578
76. Poltavtseva RA, Marey MV, Aleksandrova MA, Revishchin AV, Korochkin LI, Sukhikh GT. 2002. Evaluation of progenitor cell cultures from human embryos for neurotransplantation. Brain Res. Dev. Brain Res. 134(1-2):149-54. https://doi.org/10.1016/S0165-3806(02)00274-2
77. Popkov VA, Plotnikov EY, Silachev DN, Zorova LD, Pevzner IB, Jankauskas SS et al. 2015. Diseases and aging: gender matters. Biochemistry (Mosc). 80(12):1560-70. https://doi.org/10.1134/S0006297915120032; PMid:26638680
78. Reinders ME, Dreyer GJ, Bank JR, Roelofs H, Heidt S, Roelen DL et al. 2015. Safety of allogeneic bone marrow derived mesenchymal stromal cell therapy in renal transplant recipients: the neptune study. J. Transl. Med. 13:344. https://doi.org/10.1186/s12967-015-0700-0; PMid:26537851 PMCid:PMC4632480
79. Rice J, Vannucci R, Brierly J. 1981. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol. 9:131–141. https://doi.org/10.1002/ana.410090206; PMid:7235629
80. Rocha V, Wagner JEJr, Sobocinski KA, Klein JP, Zhang MJ, Horowitz MM et al. 2000. Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLA-identical sibling. Eurocard and International Bone Marrow Transplant Registry Working Committee on Alternative Donor and Stem Cell Sources. N. Engl. J. Med. 342(25):1846-54. https://doi.org/10.1056/NEJM200006223422501; PMid:10861319
81. Rosado-de-Castro PH, Fda R. Schmidt, Battistella V, Lopes de Souza SA, Gutfilen B, Goldenberg RC et al. 2013. Biodistribution of bone marrow mononuclear cells after intra-arterial or intravenous transplantation in subacute stroke patients. Regen. Med. 8(2):145-55. https://doi.org/10.2217/rme.13.2; PMid:23477395
82. Rosenkranz K, Kumbruch S, Lebermann K, Marschner K, Jensen A, Dermietzel R et al. 2010. The chemokine SDF-1/CXCL12 contributes to the ‘homing’ of umbilical cord blood cells to a hypoxic-ischemic lesion in the rat brain. J. Neurosci. Res. 88(6):1223-33. PMid:19937807
83. Santilli G, Lamorte G, Carlessi L, Ferrari D, Rota Nodari L, Binda E et al. 2010. Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One. 5(1):e8575. https://doi.org/10.1371/journal.pone.0008575; PMid:20052410 PMCid:PMC2797394
84. Silachev DN, Shubina MI, Iankauskas SS, Mkrtchian VP, Manskikh VN, Guliaev MV, Zorov DB. 2013. Evaluation of a long-term sensomotor deficit after neonatal rat brain ischemia/hypoxia. Vyssh Nerv Deiat Im I P Pavlova. 63(3):405-16.
85. Silachev DN, Khailova LS, Babenko VA, Gulyaev MV, Kovalchuk SI, Zorova LD et al. 2014. Neuroprotective effect of glutamate-substituted analog of gramicidin A is mediated by the uncoupling of mitochondria. Biochim. Biophys. Acta. 1840(12):3434-42.
86. Silachev DN, Plotnikov EY, Babenko VA, Danilina TI, Zorov LD, Pevzner IB et al. 2015. Intra-arterial administration of multipotent mesenchymal stromal cells promotes functional recovery of the brain after traumatic brain injury. Bull. Exp. Biol. Med. 159(4):528-33. https://doi.org/10.1007/s10517-015-3009-3; PMid:26388566
87. Schu S, Nosov M, O’Flynn L, Shaw G, Treacy O, Barry F et al. 2012. Immunogenicity of allogeneic mesenchymal stem cells. J. Cell. Mol. Med. 16(9):2094-103. https://doi.org/10.1111/j.1582-4934.2011.01509.x; PMid:22151542 PMCid:PMC3822979
88. Shea KL, Palanisamy A. 2015. What can you do to protect the newborn brain? Curr. Opin. Anaesthesiol. 28(3):261-6. https://doi.org/10.1097/ACO.0000000000000184; PMid:25827279
89. Shipounova IN, Petinati NA, Bigildeev AE, Zezina EA, Drize NI, Kuzmina LA et al. 2014. Analysis of results of acute graft-versus-host disease prophylaxis with donor multipotent mesenchymal stromal cells in patients with hemoblastoses after allogeneic bone marrow transplantation. Biochemistry (Mosc). 79(12):1363-70. https://doi.org/10.1134/S0006297914120104; PMid:25716730
90. Sukhikh GT, Silachyov DN, Pevzner IB, Zorova LD, Babenko VA, Popkov VA, Yankausjkas SS, Zubkov VV, Zorov DB, Plotnikov EYu. 2015. Prospects for using stem and progenitor cells in the therapy of consequences of neonatal hypoxic-ischemic encephalopathy. Obstetrics and gynecology 5:55-66.
91. Sun J, Allison J, McLaughlin C, Sledge L, Waters-Pick B, Wease S et al. 2010. Differences in quality between privately and publicly banked umbilical cord blood units: a pilot study of autologous cord blood infusion in children with acquired neurologic disorders. Transfusion. 50(9):1980-7. https://doi.org/10.1111/j.1537-2995.2010.02720.x; PMid:20546200 PMCid:PMC3816574
92. Svendsen CN, Caldwell MA, Ostenfeld T. 1999. Human neural stem cells: isolation, expansion and transplantation. Brain Pathol. 9(3):499-513. https://doi.org/10.1111/j.1750-3639.1999.tb00538.x; PMid:10416990
93. Takahashi M, Vattanajun A, Umeda T, Isa K, Isa T. 2009. Large-scale reorganization of corticofugal fibers after neonatal hemidecortication for functional restoration of forelimb movements. Eur. J. Neurosci. 30(10):1878-87. https://doi.org/10.1111/j.1460-9568.2009.06989.x; PMid:19895560
94. Takahashi K, Yamanaka S. 2013. Induced pluripotent stem cells in medicine and biology. Development. 140:2257–2267. https://doi.org/10.1242/dev.092551; PMid:23715538
95. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H et al. 2004. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest. 114(3):330-8. https://doi.org/10.1172/JCI200420622; PMid:15286799 PMCid:PMC484977
96. Thorne RG, Frey WH. 2001. Delivery of neurotrophic factors to the central nervous system: pharmacokinetic considerations. 2nd. Clin. Pharmacokinet. 40(12):907-46. https://doi.org/10.2165/00003088-200140120-00003; PMid:11735609
97. Titomanlio L, Kavelaars A, Dalous J, Mani S, Ghouzzi V, Heijnen C et al. 2011. Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann. Neurol. 70(5):698-712. https://doi.org/10.1002/ana.22518
98. Uccelli A. 2013. Mesenchymal stem cells exert a remarkable regenerative effect requiring minimal CNS integration: commentary on: «Mesenchymal stem cells protect CNS neurons against glutamate excitotoxicity by inhibiting glutamate receptor expression and function» by Voulgari-Kokota et al. Exp. Neurol. 247:292-5. https://doi.org/10.1016/j.expneurol.2013.01.028; PMid:23384664
99. Van Velthoven C, Kavelaars A, van Bel F, Heijnen C. 2010. Nasal administration of stem cells: a promising novel route for ischemic brain damage. Pediatric Research 68:419–422. https://doi.org/10.1203/pdr.0b013e3181f1c289
100. Van Velthoven C, Kavelaars A, Heijnen C. 2012. Mesenchymal stem cells as a treatment for neonatal ischemia. Pediatric Research. 71:474–481. https://doi.org/10.1038/pr.2011.64; PMid:22430383
101. Verina T, Fatemi A, Johnston MV, Comi AM. 2013. Pluripotent possibilities: human umbilical cord blood cell treatment after neonatal brain injury. Pediatr. Neurol. 48(5):346-54. https://doi.org/10.1016/j.pediatrneurol.2012.10.010
102. Wang Y, Deng Y, Zhou GQ. 2008. SDF-1alpha/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res. 1195:104-12. https://doi.org/10.1016/j.brainres.2007.11.068; PMid:18206136
103. Wang D, Zhang H, Liang J, Li X, Feng X, Wang H et al. 2013. Allogeneic mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus: 4 years of experience. Cell Transplant. 22(12):2267-77. PMid:24388428
104. Wang Q, Yang Q, Wang Z, Tong H, Ma L, Zhang Y et al. 2016. Comparative analysis of human mesenchymal stem cells from fetal-bone marrow, adipose tissue, and Warton’s jelly as sources of cell immunomodulatory therapy. Hum. Vaccin. Immunother. 12(1):85-96. https://doi.org/10.1080/21645515.2015.1030549; PMid:26186552 PMCid:PMC4962749
105. Wang X, Zhao Y, Wang X. 2014. Umbilical cord blood cells regulate the differentiation of endogenous neural stem cells in hypoxic ischemic neonatal rats via the hedgehog signaling pathway. Brain Res. 1560:18-26. https://doi.org/10.1016/j.brainres.2014.02.019; PMid:24565927
106. Wasielewski B, Jensen A, Roth-Harer A et al. 2012. Neuroglial activation and CX43 expression are reduced upon transplantation of human umbilical cord blood cells after perinatal hypoxic-ischemic injury. Brain Research 1487:39–53. https://doi.org/10.1016/j.brainres.2012.05.066; PMid:22796290
107. Willing AE, Lixian J, Milliken M, Poulos S, Zigova T, Song S et al. 2003. Intravenous versus intrastriatal cord blood administration in a rodent model of stroke. J. Neurosci. Res. 73(3):296-307. https://doi.org/10.1002/jnr.10659; PMid:12868063
108. Yasuhara T, Matsukawa N, Yu G, Xu L, Mays RW, Kovach J et al. 2006. Behavioral and histological characterization of intrahippocampal grafts of human bone marrow-derived multipotent progenitor cells in neonatal rats with hypoxic-ischemic injury. Cell Transplant. 15(3):231-8. https://doi.org/10.3727/000000006783982034; PMid:16719058
109. Yoo SW, Chang DY, Lee HS, Kim GH, Park JS, Ryu BY et al. 2013. Immune following suppression mesenchymal stem cell transplantation in the ischemic brain is mediated by TGF-beta. Neurobiol. Dis. 58:249-57. https://doi.org/10.1016/j.nbd.2013.06.001; PMid:23759293
110. Zhang X, Zhang Q, Li W, Nie D, Chen W, Xu C et al. 2014. Therapeutic effect of human umbilical cord mesenchymal stem cells on neonatal rat hypoxic-ischemic encephalopathy. J. Neurosci. Res. 92(1):35-45. https://doi.org/10.1002/jnr.23304; PMid:24265136
111. Zhang R, Liu Y, Yan K, Chen L, Chen XR, Li P et al. 2013. Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J. Neuroinflammation. 10:106. https://doi.org/10.1186/1742-2094-10-106; PMid:23971414 PMCid:PMC3765323
112. Zhao L, Duan W, Reyes M et al. 2002. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Experimental Neurology 174:11–20. https://doi.org/10.1006/exnr.2001.7853; PMid:11869029
113. Zwijnenburg PJ, van der Poll T, Florquin S, van Deventer SJ, Roord JJ, van Furth AM. 2001. Experimental pneumococcal meningitis in mice: a model of intranasal infection. J. Infect. Dis. 183(7):1143-6. https://doi.org/10.1086/319271; PMid:11237845