PROSPECTS FOR USING STEM AND PROGENITOR CELLS IN THE THERAPY OF CONSEQUENCES OF NEONATAL HYPOXIC-ISCHEMIC ENCEPHALOPATHY


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Abstract

Objective. To carry out a systems analysis of investigations using cell technologies to treat the sequels of neonatal hypoxic-ischemic encephalopathy. Material and methods. The review includes the data of foreign and Russian articles published on this topic in the past 10 years in the Pubmed database of medical and biological publications and the ClinicalTrials.gov base of clinical trials. Results. Different aspects of cell therapy, from the type of stem cells and the sources of their acquisition to the presumed mechanisms of therapeutic action, were analyzed. The components determining the positive effect, as applied to therapy for neonatal cerebral disorders, including in clinical trials, were considered. Conclusion. Cell technologies have shown their high therapeutic effectiveness and promise for use in neonatology. Nevertheless, it is necessary to conduct further investigations aimed at comprehensively characterizing the type of cells and their origin, doses, and optimal time and route of their administration for the most effective use of cell therapy.

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About the authors

Gennady Tikhonovich Sukhikh

Research Center of Obstetrics, Gynecology, and Perinatology

Email: g_sukhikh@oparina4.ru
PhD, Professor, Academician of RAS, Director Moscow 117997, Ac. Oparina str. 4, Russia

Denis Nikolaevich Silachev

M.V. Lomonosov Moscow State University

Email: silachevdn@genebee.msu.ru
PhD, Senior Researcher, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Irina Borisovna Pevzner

M.V. Lomonosov Moscow State University

Email: irinapevzner@mail.ru
PhD, Senior Researcher, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Ljubava Dmitrievna Zorova

M.V. Lomonosov Moscow State University

Email: lju_2003@list.ru
PhD, Scientific Researcher, International Laser Research Center 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Valentina Andreevna Babenko

M.V. Lomonosov Moscow State University

Email: nucleus-90@yandex.ru
PhD student, Junior Researcher, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Vasiliy Andreevich Popkov

M.V. Lomonosov Moscow State University

Email: popkov@genebee.msu.ru
PhD student, Junior Researcher, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Stanislovas Stasisovich Jankauskas

M.V. Lomonosov Moscow State University

Email: stanislovas@mail.ru
PhD, Researcher, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Viktor Vasilievich Zubkov

Research Center of Obstetrics, Gynecology, and Perinatology

Email: v_zubkov@oparina4.ru
PhD, Professor, Head of Department Moscow 117997, Ac. Oparina str. 4, Russia

Dmitry Borisovich Zorov

M.V. Lomonosov Moscow State University

Email: zorov@genebee.msu.ru
PhD, Professor, Head of Department, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

Egor Yurievich Plotnikov

M.V. Lomonosov Moscow State University

Email: plotnikov@mail.genebee.msu.ru
PhD, Professor, Principal Scientific Researcher, A.N. Belozersky Research Institute of Physicochemical Biology 119992, Russia, Moscow, Leninskye gory 1, bld. 40

References

  1. Антонов А.Г., Ионов О.В., Киртбая А.Р., Балашова Е.Н., Никитина И.В., Рындин А.Ю., Мирошник Е.В., Дегтярев Д.Н. Методика проведения лечебной гипотермии детям, родившимся в состоянии асфиксии. Анестезиология и реаниматология. 2014; 59(6): 76-7
  2. Shea K.L., Palanisamy A. What can you do to protect the newborn brain? Curr. Opin. Anaesthesiol. 2015; 28(3): 261-6.
  3. Perlman J.M. Summary proceedings from the neurology group on hypoxic-ischemic encephalopathy. Pediatrics. 2006; 117(3, Pt 2): S28-33.
  4. Cameron S.H., Alwakeel A.J., Goddard L., Hobbs C.E., Gowing E.K., Barnett E.R. et al. 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. 2015; 68: 56-72.
  5. Wang Q., Yang Q., Wang Z., Tong H., Ma L., Zhang Y. et al. 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. 2016; 12(1): 85-96.
  6. Borlongan C.V., Weiss M.D. Baby STEPS: a giant leap for cell therapy in neonatal brain injury. Pediatr. Res. 2011; 70(1): 3-9.
  7. Northington F.J. Brief update on animal models of hypoxic-ischemic encephalopathy and neonatal stroke. ILAR J. 2006; 47(1): 32-8.
  8. Silachev D.N., Shubina M.I., Iankauskas S.S., Mkrtchian V.P., Manskikh V.N., Guliaev M.V., Zorov D.B. Evaluation of a long-term sensomotor deficit after neonatal rat brain ischemia/hypoxia. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013; 63(3): 405-16.
  9. Flax J.D., Aurora S., Yang C., Simonin C., Wills A.M., Billinghurst L.L. et al. Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nat. Biotechnol. 1998; 16(11): 1033-9.
  10. Svendsen C.N., Caldwell M.A., Ostenfeld T. Human neural stem cells: isolation, expansion and transplantation. Brain Pathol. 1999; 9(3): 499-513.
  11. Poltavtseva R.A., Rzhaninova A.A., Revishchin A.V., Aleksandrova M.A., Korochkin L.I., Repin V.S. et al. In vitro development of neural progenitor cells from human embryos. Bull. Exp. Biol. Med. 2001; 132(3): 861-3.
  12. Palmer T.D., Schwartz P.H., Taupin P., Kaspar B., Stein S.A., Gage F.H. Cell culture. Progenitor cells from human brain after death. Nature. 2001; 411(6833): 42-3.
  13. Hirschi K.K., Li S., Roy K. Induced pluripotent stem cells for regenerative medicine. Annu. Rev. Biomed. Eng. 2014; 16: 277-94.
  14. Poltavtseva R.A., Marey M.V., Aleksandrova M.A., Revishchin A.V., Korochkin L.I., Sukhikh G.T. Evaluation of progenitor cell cultures from human embryos for neurotransplantation. Brain Res. Dev. Brain Res. 2002; 134(1-2): 149-54.
  15. Imitola J., Raddassi K., Park K.I., Mueller F.J., Nieto M., Teng Y.D. et al. 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. 2004; 101(52): 18117-22.
  16. Obenaus A., Dilmac N., Tone B., Tian H.R., Hartman R., Digicaylioglu M. et al. Long-term magnetic resonance imaging of stem cells in neonatal ischemic injury. Ann. Neurol. 2011; 69(2): 282-91.
  17. Santilli G., Lamorte G., Carlessi L., Ferrari D., Rota Nodari L., Binda E. et al. Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One. 2010; 5(1): e8575.
  18. Jansen E.M., Solberg L., Underhill S., Wilson S., Cozzari C., Hartman B.K. et al. Transplantation of fetal neocortex ameliorates sensorimotor and locomotor deficits following neonatal ischemic-hypoxic brain injury in rats. Exp. Neurol. 1997; 147(2): 487-97.
  19. Daadi M.M., Davis A.S., Arac A., Li Z., Maag A.L., Bhatnagar R. et al. Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic-ischemic brain injury. Stroke. 2010; 41(3): 516-23.
  20. Takahashi M., Vattanajun A., Umeda T., Isa K., Isa T. Large-scale reorganization of corticofugal fibers after neonatal hemidecortication for functional restoration of forelimb movements. Eur. J. Neurosci. 2009; 30(10): 1878-87.
  21. Popkov V.A., Plotnikov E.Y., Silachev D.N., Zorova L.D., Pevzner I.B., Jankauskas S.S. et al. Diseases and aging: gender matters. Biochemistry (Mosc). 2015; 80(12): 1560-70.
  22. Johnston M.V., Hagberg H. Sex and the pathogenesis of cerebral palsy. Dev. Med. Child Neurol. 2007; 49(1): 74-8.
  23. Ashwal S., Ghosh N., Turenius C.I., Dulcich M., Denham C.M., Tone B. et al. Reparative effects of neural stem cells in neonatal rats with hypoxic-ischemic injury are not influenced by host sex. Pediatr. Res. 2014; 75(5): 603-11.
  24. Comi A.M., Cho E., Mulholland J.D., Hooper A., Li Q., Qu Y. et al. Neural stem cells reduce brain injury after unilateral carotid ligation. Pediatr. Neurol. 2008; 38(2): 86-92.
  25. Hass R., Kasper C., Bohm S., Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun. Signal. 2011; 9 : 12.
  26. Zhang R., Liu Y., Yan K., Chen L., Chen X.R., Li P. et al. Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J. Neuroinflammation. 2013; 10: 106.
  27. Najar M., Raicevic G., Crompot E., Fayyad-Kazan H., Bron D., Toungouz M. et al. The immunomodulatory potential of mesenchymal stromal cells: a story of a regulatory network. J. Immunother. 2016; 39(2): 45-59.
  28. Reinders M.E., Dreyer G.J., Bank J.R., Roelofs H., Heidt S., Roelen D.L. et al. Safety of allogeneic bone marrow derived mesenchymal stromal cell therapy in renal transplant recipients: the neptune study. J. Transl. Med. 2015; 13: 344.
  29. Guan L.X., Guan H., Li H.B., Ren C.A., Liu L., Chu J.J. et al. Therapeutic efficacy of umbilical cord-derived mesenchymal stem cells in patients with type 2 diabetes. Exp. Ther. Med. 2015; 9(5): 1623-30.
  30. Wang D., Zhang H., Liang J., Li X., Feng X., Wang H. et al. Allogeneic mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus: 4 years of experience. Cell Transplant. 2013; 22(12): 2267-77.
  31. von Bahr L., Batsis I., Moll G., Hagg M., Szakos A., Sundberg B. et al. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells. 2012; 30(7): 1575-8.
  32. Donega V., Nijboer C.H., van Velthoven C.T., Youssef S.A., de Bruin A., van Bel F. et al. Assessment of long-term safety and efficacy of intranasal mesenchymal stem cell treatment for neonatal brain injury in the mouse. Pediatr. Res. 2015; 78(5): 520-6.
  33. Zhang X., Zhang Q., Li W., Nie D., Chen W., Xu C. et al. Therapeutic effect of human umbilical cord mesenchymal stem cells on neonatal rat hypoxic-ischemic encephalopathy. J. Neurosci. Res. 2014; 92(1): 35-45.
  34. Borlongan C.V., Hadman M., Sanberg C.D., Sanberg P.R. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke. 2004; 35(10): 2385-9.
  35. Wang Y., Deng Y., Zhou G.Q. SDF-1alpha/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res. 2008; 1195: 104-12.
  36. Bae S.H., Kong T.H., Lee H.S., Kim K.S., Hong K.S., Chopp M. et al. Long-lasting paracrine effects of human cord blood cells on damaged neocortex in an animal model of cerebral palsy. Cell Transplant. 2012; 21(11): 2497-515.
  37. Donega V., van Velthoven C.T., Nijboer C.H., Kavelaars A., Heijnen C.J. The endogenous regenerative capacity of the damaged newborn brain: boosting neurogenesis with mesenchymal stem cell treatment. J. Cereb. Blood Flow Metab. 2013; 33(5): 625-34.
  38. Titomanlio L., Kavelaars A., Dalous J., Mani S., El Ghouzzi V., Heijnen C. et al. Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann. Neurol. 2011; 70(5): 698-712.
  39. Uccelli A. 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. 2013; 247: 292-5.
  40. Rosenkranz K., Kumbruch S., Lebermann K., Marschner K., Jensen A., Dermietzel R. et al. 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. 2010; 88(6): 1223-33.
  41. Constantin G., Marconi S., Rossi B., Angiari S., Calderan L., Anghileri E. et al. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells. 2009; 27(10): 2624-35.
  42. Nimgaonkar M.T., Roscoe R.A., Persichetti J., Rybka W.B., Winkelstein A., Ball E.D. A unique population of CD34+ cells in cord blood. Stem Cells. 1995; 13(2): 158-66.
  43. Erices A., Conget P., Minguell J.J. Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 2000; 109(1): 235-42.
  44. Lin R.Z., Dreyzin A., Aamodt K., Dudley A.C., Melero-Martin J.M. Functional endothelial progenitor cells from cryopreserved umbilical cord blood. Cell Transplant. 2011; 20(4): 515-22.
  45. Kucia M., Halasa M., Wysoczynski M., Baskiewicz-Masiuk M., Moldenhawer S., Zuba-Surma E. et al. 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. 2007; 21(2): 297-303.
  46. Naujock M., Stanslowsky N., Reinhardt P., Sterneckert J., Haase A., Martin U. et al. Molecular and functional analyses of motor neurons generated from human cord-blood-derived induced pluripotent stem cells. Stem Cells Dev. 2014; 23(24): 3011-20.
  47. Rocha V., Wagner J.E. Jr., Sobocinski K.A., Klein J.P., Zhang M.J., Horowitz M.M. et al. Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLA-identical sibling. Eurocord and International Bone Marrow Transplant Registry Working Committee on Alternative Donor and Stem Cell Sources. N. Engl. J. Med. 2000; 342(25): 1846-54.
  48. Greggio S., de Paula S., Azevedo P.N., Venturin G.T., Dacosta J.C. Intra-arterial transplantation of human umbilical cord blood mononuclear cells in neonatal hypoxic-ischemic rats. Life Sci. 2014; 96(1-2): 33-9.
  49. de Paula S., Greggio S., Marinowic D.R., Machado D.C., DaCosta J.C. The dose-response effect of acute intravenous transplantation of human umbilical cord blood cells on brain damage and spatial memory deficits in neonatal hypoxiaischemia. Neuroscience. 2012; 210: 431-41.
  50. Verina T., Fatemi A., Johnston M.V., Comi A.M. Pluripotent possibilities: human umbilical cord blood cell treatment after neonatal brain injury. Pediatr. Neurol. 2013; 48(5): 346-54.
  51. Kao C.H., Chen S.H., Chio C.C., Lin M.T. Human umbilical cord blood-derived CD34+ cells may attenuate spinal cord injury by stimulating vascular endothelial and neurotrophic factors. Shock. 2008; 29(1): 49-55.
  52. Wang X., Zhao Y., Wang X. Umbilical cord blood cells regulate the differentiation of endogenous neural stem cells in hypoxic ischemic neonatal rats via the hedgehog signaling pathway. Brain Res. 2014; 1560: 18-26.
  53. Taguchi A., Soma T., Tanaka H., Kanda T., Nishimura H., Yoshikawa H. et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest. 2004; 114(3): 330-8.
  54. Ma L., Zhou Z, Zhang D., Yang S., Wang J., Xue F. et al. Immunosuppressive function of mesenchymal stem cells from human umbilical cord matrix in immune thrombocytopenia patients. Thromb. Haemost. 2012; 107(5): 937-50.
  55. Ali J.M., Bolton E.M., Bradley J.A., Pettigrew G.J. Allorecognition pathways in transplant rejection and tolerance. Transplantation. 2013; 96(8): 681-8.
  56. Schu S., Nosov M., O’Flynn L., Shaw G., Treacy O., Barry F. et al. Immunogenicity of allogeneic mesenchymal stem cells. J. Cell. Mol. Med. 2012; 16(9): 2094-103.
  57. Hori J., Ng T.F., Shatos M., Klassen H., Streilein J.W., Young M.J. Neural progenitor cells lack immunogenicity and resist destruction as allografts. Stem Cells. 2003; 21(4): 405-16.
  58. Iguchi A., Terashita Y., Sugiyama M., Ohshima J., Sato T.Z., Cho Y. et al. Graft-versus-host disease (GVHD) prophylaxis by using methotrexate decreases preengraftment syndrome and severe acute GVHD, and accelerates engraftment after cord blood transplantation. Pediatr. Transplant. 2016; 20(1): 114-9.
  59. Newell L.F., Flowers M.E., Gooley T.A., Milano F., Carpenter P.A., Martin P.J. et al. Characteristics of chronic GVHD after cord blood transplantation. Bone Marrow Transplant. 2013; 48(10): 1285-90.
  60. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I. et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet. 2008; 371(9624): 1579-86.
  61. Shipounova I.N., Petinati N.A., Bigildeev A.E., Zezina E.A., Drize N.I., Kuzmina L.A. et al. 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). 2014; 79(12): 1363-70.
  62. Ma S., Xie N., Li W., Yuan B., Shi Y., Wang Y. Immunobiology of mesenchymal stem cells. Cell Death Differ. 2014; 21(2): 216-25.
  63. Yoo S.W., Chang D.Y., Lee H.S., Kim G.H., Park J.S., Ryu B.Y. et al. Immune following suppression mesenchymal stem cell transplantation in the ischemic brain is mediated by TGF-beta. Neurobiol. Dis. 2013; 58: 249-57.
  64. Borlongan C.V., Hadman M., Sanberg C.D., Sanberg P.R. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke. 2004; 35(10): 2385-9.
  65. Silachev D.N., Plotnikov E.Y., Babenko V.A., Danilina T.I., Zorov L.D., Pevzner I.B. et al. Intra-arterial administration of multipotent mesenchymal stromal cells promotes functional recovery of the brain after traumatic brain injury. Bull. Exp. Biol. Med. 2015; 159(4): 528-33.
  66. Comi A.M., Cho E., Mulholland J.D., Hooper A., Li Q., Qu Y. et al. Neural stem cells reduce brain injury after unilateral carotid ligation. Pediatr. Neurol. 2008; 38(2): 86-92.
  67. Cameron S.H., Alwakeel A.J., Goddard L., Hobbs C.E., Gowing E.K., Barnett E.R. et al. 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. 2015; 68: 56-72.
  68. Ashwal S., Ghosh N., Turenius C.I., Dulcich M., Denham C.M., Tone B. et al. Reparative effects of neural stem cells in neonatal rats with hypoxic-ischemic injury are not influenced by host sex. Pediatr. Res. 2014; 75(5): 603-11.
  69. Yasuhara T., Matsukawa N., Yu G., Xu L., Mays R.W., Kovach J. et al. Behavioral and histological characterization of intrahippocampal grafts of human bone marrow-derived multipotent progenitor cells in neonatal rats with hypoxic-ischemic injury. Cell Transplant. 2006; 15(3): 231-8.
  70. Jin K., Sun Y., Xie L., Mao X.O., Childs J., Peel A. et al. Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intra ventricular, or intravenous transplantation in the rat. Neurobiol. Dis. 2005; 18(2): 366-74.
  71. Willing A.E., Lixian J., Milliken M., Poulos S., Zigova T., Song S. et al. Intravenous versus intrastriatal cord blood administration in a rodent model of stroke. J. Neurosci. Res. 2003; 73(3): 296-307.
  72. Guzman R., Choi R., Gera A., De Los Angeles A., Andres R.H., Steinberg G.K. Intravascular cell replacement therapy for stroke. Neurosurg. Focus. 2008; 24(3-4): E15.
  73. Gao J., Dennis J.E., Muzic R.F., Lundberg M., Caplan A.I. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs. 2001; 169(1): 12-20.
  74. Rosado-de-Castro P.H., Schmidt Fda R., Battistella V., Lopes de Souza S.A., Gutfilen B., Goldenberg R.C. et al. Biodistribution of bone marrow mononuclear cells after intra-arterial or intravenous transplantation in subacute stroke patients. Regen. Med. 2013; 8(2): 145-55.
  75. Misra V., Lai A., El Khoury R., Chen P.R., Savitz S.I. Intra-arterial delivery of cell therapies for stroke. Stem Cells Dev. 2012; 21(7): 1007-15.
  76. Gutierrez-Fernandez M., Rodriguez-Frutos B., Alvarez-Grech J., Vallejo-Cremades M.T., Exposito-Alcaide M., Merino J. et al. Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience. 2011; 175: 394-405.
  77. Kamiya N., Ueda M., Igarashi H., Nishiyama Y., Suda S., Inaba T. et al. Intraarterial transplantation of bone marrow mononuclear cells immediately after reperfusion decreases brain injury after focal ischemia in rats. Life Sci. 2008; 83(11-12): 433-7.
  78. Pendharkar A.V., Chua J.Y., Andres R.H., Wang N., Gaeta X., Wang H. et al. Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke. 2010; 41(9): 2064-70.
  79. Lundberg J., Sodersten E., Sundstrom E., Le Blanc K., Andersson T., Hermanson O. et al. 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. 2012; 21(1): 333-43.
  80. Robin A.M., Zhang Z.G., Wang L., Zhang R.L., Katakowski M., Zhang L. et al. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2006; 26(1): 125-34.
  81. Li M., Hale J.S., Rich J.N., Ransohoff R.M., Lathia J.D. Chemokine CXCL12 in neurodegenerative diseases: an SOS signal for stem cell-based repair. Trends Neurosci. 2012; 35(10): 619-28.
  82. Cui L.L., Kerkela E., Bakreen A., Nitzsche F., Andrzejewska A., Nowakowski A. et al. 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. 2015; 6: 11.
  83. Li L., Jiang Q., Ding G., Zhang L., Zhang Z.G., Li Q. et al. 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. 2010; 30(3): 653-62.
  84. Chua J.Y., Pendharkar A.V., Wang N., Choi R., Andres R.H., Gaeta X. et al. Intra-arterial injection of neural stem cells using a microneedle technique does not cause microembolic strokes. J. Cereb. Blood Flow Metab. 2011; 31(5): 1263-71.
  85. Janowski M., Lyczek A., Engels C., Xu J., Lukomska B., Bulte J.W. et al. Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J. Cereb. Blood Flow Metab. 2013; 33(6): 921-7.
  86. Thorne R.G., Frey W.H. 2nd. Delivery of neurotrophic factors to the central nervous system: pharmacokinetic considerations. Clin. Pharmacokinet. 2001; 40(12): 907-46.
  87. Silachev D.N., Khailova L.S., Babenko V.A., Gulyaev M.V., Kovalchuk S.I., Zorova L.D. et al. Neuroprotective effect of glutamate-substituted analog of gramicidin A is mediated by the uncoupling of mitochondria. Biochim. Biophys. Acta. 2014; 1840(12): 3434-42.
  88. Donega V., Nijboer C.H., van Tilborg G., Dijkhuizen R.M., Kavelaars A., Heijnen C.J. Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury. Exp. Neurol. 2014; 261: 53-64.
  89. Donega V., Nijboer C.H., van Velthoven C.T., Youssef S.A., de Bruin A., van Bel F. et al. Assessment of long-term safety and efficacy of intranasal mesenchymal stem cell treatment for neonatal brain injury in the mouse. Pediatr. Res. 2015; 78(5): 520-6.
  90. Murase S., Horwitz A.F. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J. Neurosci. 2002; 22(9): 3568-79.
  91. Danielyan L., Schafer R., von Ameln-Mayerhofer A., Buadze M., Geister J., Klopfer T. et al. Intranasal delivery of cells to the brain. Eur. J. Cell Biol. 2009; 88(6): 315-24.
  92. Zwijnenburg P.J., van der Poll T., Florquin S., van Deventer S.J., Roord J.J., van Furth A.M. Experimental pneumococcal meningitis in mice: a model of intranasal infection. J. Infect. Dis. 2001; 183(7): 1143-6.
  93. Cotten C.M., Murtha A.P., Goldberg R.N., Grotegut C.A., Smith P.B., Goldstein R.F et al. Feasibility of autologous cord blood cells for infants with hypoxic-ischemic encephalopathy. J. Pediatr. 2014; 164(5): 973-9. e1.
  94. Sun J., Allison J., McLaughlin C., Sledge L., Waters-Pick B., Wease S. et al. 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. 2010; 50(9): 1980-7.
  95. Mancias-Guerra C., Marroquin-Escamilla A.R., Gonzalez-Llano O., Villarreal-Martinez L., Jaime-Perez J.C., Garcia-Rodriguez F. et al. Safety and toler ability of intrathecal delivery of autologous bone marrow nucleated cells in children with cerebral palsy: an open-label phase I trial. Cytotherapy. 2014; 16(6): 810-20.
  96. Chen L., Huang H., Xi H., Xie Z., Liu R., Jiang Z. et al. Intracranial transplant of olfactory ensheathing cells in children and adolescents with cerebral palsy: a randomized controlled clinical trial. Cell Transplant. 2010; 19(2): 185-91
  97. Chou R.H., Lu C.Y., Fan J.R., Yu Y.L., Shyu W.C. The potential therapeutic applications of olfactory ensheathing cells in regenerative medicine. Cell Transplant. 2014; 23(4-5): 567-71.
  98. Bohlin K. Cell-based strategies to reconstitute vital functions in preterm infants with organ failure. Best Pract. Res. Clin. Obstet. Gynaecol. 2016; 31: 99-111.
  99. Mitsialis S.A., Kourembanas S. Stem cell-based therapies for the newborn lung and brain: Possibilities and challenges. Semin. Perinatol. 2016; 40(3):138-51.
  100. Borghesi A., Cova C., Gazzolo D., Stronati M. Stem cell therapy for neonatal diseases associated with preterm birth. J. Clin. Neonatol. 2013; 2(1): 1-7.
  101. Larijani B., Esfahani E.N., Amini P., Nikbin B., Alimoghaddam K., Amiri S. et al. Stem cell therapy in treatment of different diseases. Acta Med. Iran. 2012; 50(2): 79-96.

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