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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2018; 64(1): 103-117


IMMUNOBIOLOGICAL PROPERTIES OF NEUROGENIC CELLS OF THE FETAL BRAIN. ІI. IMMUNE RESPONSES TO NEUROGENIC STEM CELLS IN VITRO AND IN VIVO

L.D. Liubich, M.I. Lisyany

    SI “Romodanov Neurosurgery Institute, National Academy of Medical Sciences of Ukraine”, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz64.01.103


Abstract

The review presents an analysis of the current state of development of the problem of the brain neurogenic stem and progenitor cells (NSC/NPC) immunobiological properties. In section II the data on immune responses in vitro in cocultivation of NSC/NPC and immune system cells, as well as features of the development of immune responses in vivo after NSC/NPC transplantation are given. The transformation of the notions of the immune response in CNS during NSC/NPC transplantation is considered: from the concept of “absolute immuno-privilege” of the brain to the concept of “functional” or “therapeutic plasticity”, which takes into account various aspects and mechanisms of interaction of cells of the immune system and NSC/NPC. The data on the immune response upon the transplantation of allo- and xenogeneic NSC/NPC and its dependence on the immune status of recipients are summarized. The relevance of studies of the immunobiological properties of neurogenic cells of the fetal brain that facilitate the discovery of mechanisms of action of NSC/NPC and an assessment of the possibility of their practical application for cell therapy of CNS lesions is emphasized.

Keywords: neurogenic stem cells, neurogenic progenitor cells, allotransplantation, xenotransplantation, immune response, immunomodulation.

References

  1. Gonzalez-Perez O, Gutierrez-Fernandez F, Lopez-Virgen V, Collas-Aguilar J, Quinones-Hinojosa A, Garcia-Verdugo JM. Immunological regulation of neurogenic niches in the adult brain. Neuroscience. 2012 Dec 13;226:270-81. doi: 10.1016/j.neuroscience.2012.08.053. CrossRef  
  2. Brombacher TM, Nono JK, De Gouveia KS, Makena N, Darby M, Womersley J, Tamgue O, Brombacher F. IL-13-Mediated Regulation of Learning and Memory. J Immunol. 2017 Apr 1;198(7):2681-8. doi: 10.4049/ jimmunol.1601546.
  3.  
  4. de Miranda AS, Zhang CJ, Katsumoto A, Teixeira AL. Hippocampal adult neurogenesis: Does the immune system matter? J Neurol Sci. 2017 Jan 15;372:482-95. doi: 10.1016/j.jns.2016.10.052. CrossRef  
  5. Song EJ, Jeon SG, Kim KA, Kim JI, Moon M. Restricted CD4+ T cell receptor repertoire impairs cognitive function via alteration of Th2 cytokine levels. Neurogenesis (Austin). 2017 Jan 5;4(1):e1256856 [4 p.]. doi: 10.1080/ 23262133.2016.1256856.
  6.  
  7. Lisyany NI, Rudenko VA, Gnedkova IA, Markova OV, Liubich LD, Belskaya LN, Semenova VM, Oleynik GM, Tsymbalyuk VI, Gorobets OB, Zavalishin IA, Lisyana TA, Nosov AT, Oleksenko NV, Skurtul MI, Vasilieva IG, Stayno LP, Verhoglyadov Yu.P., Grishok SA. Immune system of the brain. Lisyany NI, editor. Kyiv: VIPOL; 1999.
  8.  
  9. Medana I, Martinic MA, Wekerle H, Neumann H. Transection of major histocompatibility complex class I-induced neurites by cytotoxic T-lymphocytes. Am J Pathol. 2001 Sep;159(3):809-15. DOI: 10.1016/S0002- 9440(10)61755-5.
  10.  
  11. Drukker M, Katchman H, Katz G, Even-Tov Friedman S, Shezen E, Hornstein E, Mandelboim O, Reisner Y, Benvenisty N. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells Stem Cells. 2006 Feb;24(2):221-9. DOI: 10.1634/stemcells.2005-0188. CrossRef  
  12. Mammolenti M, Gajavelli S, Tsoulfas P, Levy R. Absence of major histocompatibility complex class I on neural stem cells does not permit natural killer cell killing and prevents recognition by alloreactive cytotoxic T lymphocytes in vitro. Stem Cells. 2004;22(6):1101-10. DOI: 10.1634/stemcells.22-6-1101. CrossRef  
  13. Wang L, Shi J, van Ginkel FW, Lan L, Niemeyer G, Martin DR, Snyder EY, Cox NR. Neural stem/progenitor cells modulate immune responses by suppressing T lymphocytes with nitric oxide and prostaglandin E2. Exp Neurol. 2009 Mar;216(1):177-83. doi: 10.1016/j. expneurol.2008.11.017.
  14.  
  15. Drago D, Basso V, Gaude E, Volpe G, Peruzzotti-Jametti L, Bachi A, Musco G, Andolfo A, Frezza C, Mondino A, Pluchino S. Metabolic determinants of the immune modulatory function of neural stem cells. J Neuroinflammation. 2016 Sep 2 [cited 2017 Sep 8];13(1):232 [18 p.]. doi: 10.1186/s12974-016-0667-7. CrossRef  
  16. Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, Snyder EY, Khoury SJ. 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 Dec 28;101(52):18117-22. DOI:10.1073/pnas.0408258102. CrossRef  
  17. Weinger JG, Weist BM, Plaisted WC, Klaus SM, Walsh CM, Lane TE. MHC mismatch results in neural progenitor cell rejection following spinal cord transplantation in a model of viral-induced demyelination. Stem Cells. 2012 Nov;30(11):2584-95. doi: 10.1002/stem.1234. CrossRef  
  18. Hu S, Rotschafer JH, Lokensgard JR, Cheeran MC. Activated CD8+ T lymphocytes inhibit neural stem/ progenitor cell proliferation: role of interferon-gamma. PLoS One. 2014 Aug 18 [cited 2017 Sep 11];9(8):e105219 [11 p.]. doi: 10.1371/journal.pone.0105219. CrossRef  
  19. Odeberg J, Piao JH, Samuelsson EB, Falci S, Akesson E. Low immunogenicity of in vitro-expanded human neural cells despite high MHC expression. J Neuroimmunol. 2005 Apr;161(1-2):1-11. DOI: 10.1016/j. jneuroim.2004.11.016.
  20.  
  21. Zhang H, Shao B, Zhuge Q, Wang P, Zheng C, Huang W, Yang C, Wang B, Su DM, Jin K. Cross-talk between human neural stem/progenitor cells and peripheral blood mononuclear cells in an allogeneic co-culture model. PLoS One. 2015 Feb 6;10(2):e0117432 [15 p.]. doi:10.1371/journal.pone.0117432. CrossRef  
  22. Lee EM, Hurh S, Cho B, Oh KH, Kim SU, Surh CD, Sprent J, Yang J, Kim JY, Ahn C. CD70-CD27 ligation between neural stem cells and CD4+ T cells induces Fas-FasLmediated T-cell death. Stem Cell Res Ther. 2013 May 21 [cited 2017 Sep 11];4(3):56 [10 p.]. doi: 10.1186/scrt206. CrossRef  
  23. Cheeran MC, Jiang Z, Hu S, Ni HT, Palmquist JM, Lokensgard JR. Cytomegalovirus infection and interferongamma modulate major histocompatibility complex class I expression on neural stem cells. J Neurovirol. 2008 Oct;14(5):437-47. doi: 10.1080/13550280802356845. CrossRef  
  24. Laguna Goya R, Busch R, Mathur R, Coles AJ, Barker RA. Human fetal neural precursor cells can up-regulate MHC class I and class II expression and elicit CD4 and CD8 T cell proliferation. Neurobiol Dis. 2011 Feb;41(2):407-14. doi: 10.1016/j.nbd.2010.10.008. CrossRef  
  25. Preynat-Seauve O, de Rham C, Tirefort D, Ferrari- Lacraz S, Krause KH, Villard J. Neural progenitors derived from human embryonic stem cells are targeted by allogeneic T and natural killer cells. J Cell Mol Med. 2009 Sep;13(9B):3556-69. doi: 10.1111/j.1582- 4934.2009.00746.x.
  26.  
  27. de Rham C, Villard J. Interaction of ES cell derived neural progenitor cells with natural killer cells and cytotoxic Tcells. Methods Mol Biol 2013;1029:65-75. doi: 10.1007/978-1-62703-478-4_5. CrossRef  
  28. Vagaska B, New SE, Alvarez-Gonzalez C, D'Acquisto F, Gomez SG, Bulstrode NW, Madrigal A, Ferretti P. MHC-class-II are expressed in a subpopulation of human neural stem cells in vitro in an IFNγ-independent fashion and during development. 2016 Apr 15; 6:24251 [14 p.]. doi: 10.1038/srep24251. CrossRef  
  29. Liu J, Hjorth E, Zhu M, Calzarossa C, Samuelsson EB, Schultzberg M, Åkesson E. Interplay between human microglia and neural stem/progenitor cells in an allogeneic co-culture model/ J Cell Mol Med. 2013 Nov;17(11):1434-43. doi: 10.1111/jcmm.12123. CrossRef  
  30. Fainstein N, Einstein O, Cohen ME, Brill L, Lavon I, Ben-Hur T. Time limited immunomodulatory functions of transplanted neural precursor cells. Glia. 2013 Feb;61(2):140-9. doi: 10.1002/glia.22420. CrossRef  
  31. Liu J, Götherström C, Forsberg M, Samuelsson EB, Wu J, Calzarossa C, Hovatta O, Sundström E, Åkesson E. Human neural stem/progenitor cells derived from embryonic stem cells and fetal nervous system present differences in immunogenicity and immunomodulatory potentials in vitro. Stem Cell Res. 2013 May;10(3):325-37. doi:10.1016/j.scr.2013.01.001. CrossRef  
  32. Ottoboni L, De Feo D, Merlini A, Martino G. Commonalities in immune modulation between mesenchymal stem cells (MSCs) and neural stem/precursor cells (NPCs). Immunol Lett. 2015 Dec;168(2):228-39. doi: 10.1016/j. imlet.2015.05.005.
  33.  
  34. Martino G, Pluchino S, Bonfanti L, Schwartz M. Brain regeneration in physiology and pathology: the immune signature driving therapeutic plasticity of neural stem cells. Physiol Rev. 2011 Oct;91(4):1281-304. doi:10.1152/physrev.00032.2010. CrossRef  
  35. Knight J, Hackett C, Breton J, Mao-Draayer Y. Cross-talk between CD4+ T-cells and neural stem/progenitor cells. J Neurol Sci. 2011 Jul 15;306(1-2):121-8. doi: 10.1016/j. jns.2011.03.030.
  36.  
  37. Liu Q, Sanai N, Jin WN, La Cava A, Van Kaer L, Shi FD. Neural stem cells sustain natural killer cells that dictate recovery from brain inflammation. Nat Neurosci. 2016 Feb;19(2):243-52. doi: 10.1038/nn.4211. CrossRef  
  38. Medawar PB. Immunity to homologous grafted skin; the fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. Br J Exp Pathol. 1948 Feb;29(1):58-69. PMID:18865105. PubMed PubMedCentral
  39.  
  40. Chen Z, Phillips LK, Gould E, Campisi J, Lee SW, Ormerod BK, Zwierzchoniewska M, Martinez OM, Palmer TD. MHC Mismatch Inhibits Neurogenesis and Neuron Maturation in Stem Cell Allografts. PLoS One. 2011 Mar 30. doi: 10.1371/journal.pone.0014787. CrossRef  
  41. Bonnamain V, Neveu I, Naveilhan P. Neural stem/ progenitor cells as promising candidates for regenerative therapy of the central nervous system. Front Cell Neurosci. 2012 Apr; 6: 17 [8 pages]. doi:10.3389/ fncel.2012.00017.
  42.  
  43. Barker RA, Widner H. Immune problems in central nervous system cell therapy. NeuroRx. 2004 Oct;1(4):472-81. DOI:10.1602/neurorx.1.4.472. CrossRef  
  44. Lepore AC, Neuhuber B, Connors TM, Han SS, Liu Y, Daniels MP, Rao MS, Fischer I. Long-term fate of neural precursor cells following transplantation into developing and adult CNS. Neuroscience. 2006 Sep 29;142(1):287-304. PMID: 17120358. CrossRef PubMed
  45.  
  46. Krystkowiak P, Gaura V, Labalette M, Rialland A, Remy P, Peschanski M, Bachoud-Lévi AC. Alloimmunisation to donor antigens and immune rejection following foetal neural grafts to the brain in patients with Huntington's disease. PLoS One. 2007 Jan 24;2(1):e166 [4 p]. doi:10.1371/journal.pone.0000166. CrossRef  
  47. Engelhardt B. The blood-central nervous system barriers actively control immune cell entry into the central nervous system. Curr Pharm Des. 2008;14(16):1555-65. PMID:18673197. CrossRef PubMed
  48.  
  49. D'Mello C, Le T, Swain MG. Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factor alpha signaling during peripheral organ inflammation. J Neurosci. 2009 Feb 18;29(7):2089-102. doi:10.1523/JNEUROSCI.3567-08.2009. CrossRef  
  50. Graber JJ, Dhib-Jalbut S. Protective autoimmunity in the nervous system. Pharmacol Ther. 2009 Feb;121(2):147-59. doi: 10.1016/j.pharmthera.2008.10.001. CrossRef  
  51. Michel-Monigadon D, Brachet P, Neveu I, Naveilhan P. Immunoregulatory properties of neural stem cells. Immunotherapy. 2011 Apr;3(4 Suppl):39-41. doi: 10.2217/imt.11.49. CrossRef  
  52. Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med. 2015 Jun 29;212(7):991-9. doi: 10.1084/jem.20142290. CrossRef  
  53. Bucchieri F, Farina F, Zummo G, Cappello F. Lymphatic vessels of the dura mater: a new discovery? J Anat. 2015 Nov;227(5):702-3. doi: 10.1111/joa.12381. CrossRef  
  54. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J. Structural and functional features of central nervous system lymphatic vessels. Nature. 2015 Jul 16;523(7560):337-41. doi: 10.1038/nature14432. CrossRef  
  55. Tarasoff-Conway JM, Carare RO, Osorio RS, Glodzik L, Butler T, Fieremans E, Axel L, Rusinek H, Nicholson C, Zlokovic BV, Frangione B, Blennow K, Ménard J, Zetterberg H, Wisniewski T, de Leon MJ. Clearance systems in the brain-implications for Alzheimer disease. Nat Rev Neurol. 2015 Aug;11(8):457-70. doi: 10.1038/nrneurol.2015.119. CrossRef  
  56. Shimada A, Hasegawa-Ishii S. Histological Architecture Underlying Brain-Immune Cell-Cell Interactions and the Cerebral Response to Systemic Inflammation. Front Immunol. 2017 Jan 19;8:17 [12 p.]. doi: 10.3389/ fimmu.2017. 00017.
  57.  
  58. Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, Klinkert WE, Flugel-Koch C, Issekutz TB, Wekerle H, Flugel A. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature. 2009 Nov 5;462(7269):94-8. doi: 10.1038/nature08478. CrossRef  
  59. Pedemonte E, Mancardi G, Giunti D, Corcione A, Benvenuto F, Pistoia V, Uccelli A. Mechanisms of the adaptive immune response inside the central nervous system during inflammatory and autoimmune diseases. Pharmacol Ther. 2006 Sep;111(3):555-66. DOI: 10.1016/j.pharmthera.2005.11.007. CrossRef  
  60. Schwartz M, Shechter R. Protective autoimmunity functions by intracranial immunosurveillance to support the mind: The missing link between health and disease. Mol Psychiatry. 2010 Apr;15(4):342-54. doi: 10.1038/mp.2010.31. CrossRef  
  61. Klassen HJ, Imfeld KL, Kirov II, Tai L, Gage FH, Young MJ, Berman MA. Expression of cytokines by multipotent neural progenitor cells. Cytokine. 2003 May;22(3-4):101-6. PMID:12849709. CrossRef  
  62. Gutierrez-Fernandez F, Pinto-Gonzalez M, Gonzalez-Perez O. Neuro-immune interactions in the postnatal ventricular- subventricular zone. J Stem Cells. 2014;9(1):53-64. doi: jsc.2014.9.1.53.
  63.  
  64. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci. 2006 Feb;9(2):268-75. DOI: 10.1038/nn1629. CrossRef  
  65. Wolf SA, Steiner B, Akpinarli A, Kammertoens T, Nassenstein C, Braun A, Blankenstein T, Kempermann G. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J Immunol. 2009 Apr 1;182(7):3979-84. doi: 10.4049/jimmunol.0801218. CrossRef
  66. Ziv Y, Avidan H, Pluchino S, Martino G, Schwartz M. Synergy between immune cells and adult neural stem/ progenitor cells promotes functional recovery from spinal cord injury. Proc Natl Acad Sci USA. 2006 Aug 29;103(35):13174-9. DOI: 10.1073/pnas.0603747103. CrossRef  
  67. Dereck NC, Cardani AN, Yang CH, Quinnies KM, Crihfield A, Lynch KR, Kipnis J. Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med. 2010 May 10;207(5):1067-80. doi: 10.1084/jem.20091419. CrossRef  
  68. Dooley D, Vidal P, Hendrix S. Immunopharmacological intervention for successful neural stem cell therapy: New perspectives in CNS neurogenesis and repair. Pharmacol Ther. 2014 Jan;141(1):21-31. doi: 10.1016/j. pharmthera.2013.08. 001.
  69.  
  70. Kulkarni A, Scully TJ, O'Donnell LA.. The antiviral cytokine interferon-gamma restricts neural stem/progenitor cell proliferation through activation of STAT1 and modulation of retinoblastoma protein phosphorylation. J Neurosci Res. 2017 Aug;95(8):1582-601. doi: 10.1002/jnr.23987. CrossRef  
  71. Vay SU, Blaschke S, Klein R, Fink GR, Schroeter M, Rueger MA.. Minocycline mitigates the gliogenic effects of proinflammatory cytokines on neural stem cells. J Neurosci Res. 2016 Feb;94(2):149-60. doi: 10.1002/jnr.23686. CrossRef  
  72. Bresjanac M. Neurotransplantation-induced plasticity in the recipient CNS: focusing on the recipient response. Pflugers Arch. 2000 Jan;440(Suppl 1):R163-R165. doi:10.1007/s004240000048. CrossRef  
  73. Erlandsson A, Lin CH, Yu F, Morshead CM. Immunosuppression promotes endogenous neural stem and progenitor cell migration and tissue regeneration after ischemic injury. Exp Neurol. 2011 Jul;230(1):48-57. doi:10.1016/j.expneurol.2010.05.018. CrossRef  
  74. Kokaia Z, Martino G, Schwartz M, Lindvall O. Crosstalk between neural stem cells and immune cells: the key to better brain repair? Nat Neurosci. 2012 Jul 26;15(8):1078-87. doi: 10.1038/nn.3163. CrossRef  
  75. Marteyn A, Sarrazin N, Yan J, Bachelin C, Deboux C, Santin MD, Gressens P, Zujovic V, Baron-Van Evercooren A. Modulation of the Innate Immune Response by Human Neural Precursors Prevails over Oligodendrocyte Progenitor Remyelination to Rescue a Severe Model of Pelizaeus-Merzbacher Disease. Stem Cells. 2016 Apr;34(4):984-96. doi: 10.1002/stem.2263. CrossRef  
  76. Kizil C, Kyritsis N, Brand M. Effects of inflammation on stem cells: together they strive? EMBO Rep. 2015 Apr;16(4):416-26. doi: 10.15252/embr.201439702. CrossRef  
  77. Gincberg G, Arien-Zakay H, Lazarovici P, Lelkes PI. Neural stem cells: therapeutic potential for neurodegenerative diseases. Br Med Bull. 2012 Dec,104(1): 7-19. doi.org/10.1093/bmb/lds024 CrossRef  
  78. Bacigaluppi M, Russo GL, Peruzzotti-Jametti L, Rossi S, Sandrone S, Butti E, De Ceglia R, Bergamaschi A, Motta C, Gallizioli M, Studer V, Colombo E, Farina C, Comi G, Politi LS, Muzio L, Villani C, Invernizzi RW, Hermann DM, Centonze D, Martino G. Neural Stem Cell Transplantation Induces Stroke Recovery by Upregulating Glutamate Transporter GLT-1 in Astrocytes. J Neurosci. 2016 Oct 12;36(41):10529-44. DOI: 10.1523/ JNEUROSCI.1643-16.2016.
  79.  
  80. Reekmans K, Praet J, Daans J, Reumers V, Pauwels P, Van der Linden A, Berneman ZN, Ponsaerts P. Current challenges for the advancement of neural stem cell biology and transplantation research. Stem Cell Rev. 2012 Mar;8(1):262-78. doi: 10.1007/s12015-011-9266-2. CrossRef  
  81. Praet J, Santermans E, Daans J, Le Blon D, Hoornaert C, Goossens H, Hens N, Van der Linden A, Berneman Z, Ponsaerts P. Early Inflammatory Responses Following Cell Grafting in the CNS Trigger Activation of the Subventricular Zone: A Proposed Model of Sequential Cellular Events. Cell Transplant. 2015; 24(8):1481-92. doi: 10.3727/096368914X682800. CrossRef  
  82. Le Blon D, Hoornaert C, Detrez JR, Bevers S, Daans J, Goossens H, De Vos WH, Berneman Z, Ponsaerts P. Immune remodelling of stromal cell grafts in the central nervous system: therapeutic inflammation or (harmless) side-effect? J Tissue Eng Regen Med.. 2016 Jun 20; [7 p.]. doi: 10.1002/term.2188. CrossRef  
  83. Capetian P, Döbrössy M, Winkler C, Prinz M, Nikkhah G. To be or not to be accepted: the role of immunogenicity of neural stem cells following transplantation into the brain in animal and human studies. Semin Immunopathol. 2011 Nov;33(6):619-26. doi: 10.1007/s00281-011-0272-x. CrossRef  
  84. Phillips LK, Gould EA, Babu H, Krams SM, Palmer TD, Martinez OM. Natural killer cell-activating receptor NKG2D mediates innate immune targeting of allogeneic neural progenitor cell grafts. Stem Cells. 2013 Sep;31(9):1829-39. doi: 10.1002/stem.1422. CrossRef  
  85. Chen Z, Palmer TD. Cellular repair of CNS disorders: an immunological perspective. Hum Mol Genet. 2008 Apr 15;17(R1):R84-92. doi: 10.1093/hmg/ddn104. CrossRef  
  86. Hori J, Ng TF, Shatos M, Klassen H, Streilein JW, Young MJ. Neural progenitor cells lack immunogenicity and resist destruction as allografts. Stem Cells. 2003;21(4):405-16. PMID: 12832694. CrossRef PubMed
  87.  
  88. Akesson E, Wolmer-Solberg N, Cederarv M, Falci S, Odeberg J. Human neural stem cells and astrocytes, but not neurons, suppress an allogeneic lymphocyte response. Stem Cell Res. 2009 Jan;2(1):56-67. doi: 10.1016/j.scr.2008.06.002. CrossRef  
  89. Ideguchi M, Shinoyama M, Gomi M, Hayashi H, Hashimoto N, Takahashi J. Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cell-derived neural precursor cells. J Neurosci Res. 2008 Jul;86(9):1936-43. doi: 10.1002/jnr.21652. CrossRef  
  90. Kim DE, Tsuji K, Kim YR, Mueller FJ, Eom HS, Snyder EY, Lo EH, Weissleder R, Schellingerhout D. Neural stem cell transplant survival in brains of mice: assessing the effect of immunity and ischemia by using real-time bioluminescent imaging. Radiology. 2006 Dec;241(3):822-30. doi:10.1148/radiol.2413050466. CrossRef  
  91. Wang XJ, Liu WG, Zhang YH, Lu GQ, Chen SD. Effect of transplantation of c17.2 cells transfected with interleukin- 10 gene on intracerebral immune response in rat model of Parkinson's disease. Neurosci Lett. 2007 Aug 16;423(2):95-9. doi:10.1016/j.neulet.2007.06.029. CrossRef  
  92. Ben-Hur T. Immunomodulation by neural stem cells. J Neurol Sci. 2008 Feb 15;265(1-2):102-4. doi:10.1016/j. jns.2007.05.007.
  93.  
  94. Gao L, Lu Q, Huang LJ, Ruan LH, Yang JJ, Huang WL, ZhuGe WS, Zhang YL, Fu B, Jin KL, ZhuGe QC. Transplanted neural stem cells modulate regulatory T, γδ T cells and corresponding cytokines after intracerebral hemorrhage in rats. Int J Mol Sci. 2014 Mar 13;15(3):4431-41. doi: 10.3390/ijms15034431. CrossRef  
  95. Alić I, Kosi N, Kapuralin K, Gorup D, Gajović S, Pochet R, Mitrečić D. Neural stem cells from mouse strain Thy1 YFP-16 are a valuable tool to monitor and evaluate neuronal differentiation and morphology. Neurosci Lett. 2016 Nov 10;634:32-41. doi: 10.1016/j.neulet.2016.10.001. CrossRef  
  96. Sukhinich KK, Kosykh AV, Aleksandrova MA. Differentiation and Cell-Cell Interactions of Neural Progenitor Cells Transplanted into Intact Adult Brain. Bull Exp Biol Med. 2015 Nov;160(1):115-22. doi: 10.1007/s10517-015-3111-6. CrossRef  
  97. Modo M, Mellodew K, Rezaie P. In vitro expression of major histocompatibility class I and class II antigens by conditionally immortalized murine neural stem cells. Neurosci Lett. 2003 Feb 6;337(2):85-8. PMID: 12527394. CrossRef  
  98. McLaren FH, Svendsen CN, Van der Meide P, Joly E. Analysis of neural stem cells by flow cytometry: cellular differentiation modifies patterns of MHC expression. J Neuroimmunol. 2001 Jan 1;112(1-2):35-46. PMID: 11108931. CrossRef  
  99. Borlongan CV, Stahl CE, Cameron DF, Saporta S, Freeman TB, Cahill DW, Sanberg PR. CNS immunological modulation of neural graft rejection and survival. Neurol Res. 1996 Aug;18(4):297-304. PMID:8875445 CrossRef PubMed
  100.  
  101. Ubiali F, Nava S, Nessi V, Frigerio S, Parati E, Bernasconi P, Mantegazza R, Baggi F. Allorecognition of human neural stem cells by peripheral blood lymphocytes despite low expression of MHC molecules: role of TGFbeta in modulating proliferation. Int Immunol. 2007 Sep;19(9):1063-74. doi:10.1093/intimm/dxm079. CrossRef  
  102. Walczak P, Chen N, Eve D, Hudson J, Zigova T, Sanchez-Ramos J, Sanberg PR, Sanberg CD, Willing AE. Long-term cultured human umbilical cord neural-like cells transplanted into the striatum of NOD SCID mice. Brain Res Bull. 2007 Sep 14;74(1-3):155-63. doi: 10.1016/j.brainresbull.2007.06.015. CrossRef  
  103. Molcanyi M, Riess P, Bentz K, Maegele M, Hescheler J, Schäfke B, Trapp T, Neugebauer E, Klug N, Schäfer U. Trauma-associated inflammatory response impairs embryonic stem cell survival and integration after implantation into injured rat brain. J Neurotrauma. 2007 Apr;24(4):625-37. doi: 10.1089/neu.2006.0180. CrossRef  
  104. Armstrong RJ, Harrower TP, Hurelbrink CB, McLaughin M, Ratcliffe EL, Tyers P, Richards A, Dunnett SB, Rosser AE, Barker RA. Porcine neural xenografts in the immunocompetent rat: immune response following grafting of expanded neural precursor cells. Neuroscience. 2001;106(1):201-16. PMID:11564430. CrossRef  
  105. Mattis VB, Wakeman DR, Tom C, Dodiya HB, Yeung SY, Tran AH, Bernau K, Ornelas L, Sahabian A, Reidling J, Sareen D, Thompson LM, Kordower JH, Svendsen CN. Neonatal immune-tolerance in mice does not prevent xenograft rejection. Exp Neurol. 2014 Apr;254:90-8. doi:10.1016/j.expneurol.2014.01.007. CrossRef

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