Українська English

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. 2017; 63(6): 118-135

IMMUNOBIOLOGICAL PROPERTIES OF NEUROGENIC CELLS OF THE FETAL BRAIN. І. EXPRESSION OF MOLECULES WITH IMMUNE PROPERTIES

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/fz63.06.118


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. Section I summarizes data on NSC / NPC during the prenatal development. Discussion issues regarding the expression of histocompatibility antigens by NSC / NPC and mature nerve tissue cells in a comparative aspect, as well as the hierarchy of the antigen presenting potential of cells of the central nervous system are considered. Attention is drawn to the role of molecules of the main histocompatibility complex in the development of pre- and postnatal brain. Data on the expression of NSC / NPC immunoactive costimulatory molecules are given, which can determine their immunomodulating effect on cells of the immune system during contact interaction. The data on the expression and production of NSC / NPC immunoregulatory cytokines and growth factors are summarized; they are evidence of the mechanism of the regenerative action of these cells in neurotransplantation, the so-called. “bystander” effect, which justifies the concept of “functional or therapeutic plasticity”.

Keywords: Neurogenic stem cells, neurogenic progenitor cells, molecules of the main histocompatibility complex of I and II class, costimulatory molecules, cytokines, growth factors

Full text: (PDF, in Ukrainian)

References

  1. Vishwakarma SK, Bardia A, Tiwari SK, Paspala SA, Khan AA. Current concept in neural regeneration research: NSCs isolation, characterization and transplantation in various neurodegenerative diseases and stroke: A review. J Adv Res. 2014 ;5(3):277-94. CrossRef PubMed PubMedCentral
    2.  
  2. Harris L, Zalucki O, Piper M, Heng JI. Insights into the Biology and Therapeutic Applications of Neural Stem Cells. Stem Cells Int [serial on the Internet]. 2016 ;2016:9745315 [18 p.].
    3.  
  3. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science. 1992;255(5052):1707-10. CrossRef PubMed
    4.  
  4. 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;91(4):1281-304. CrossRef PubMed PubMedCentral
    5.  
  5. Custo Greig LF, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD. Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci. 2013 Nov;14(11):755-69. CrossRef PubMed PubMedCentral
    6.  
  6. Florio M, Huttner WB. Neural progenitors, neurogenesis and the evolution of the neocortex Development. 2014 Jun;141(11):2182-94. CrossRef PubMed
    7.  
  7. Pilz GA, Shitamukai A, Reillo I, Pacary E, Schwausch J, Stahl R, Ninkovic J, Snippert HJ, Clevers H, Godinho L, Guillemot F, Borrell V, Matsuzaki F, Götz M. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat Commun . 2013 Jul;4:2125 [11 p.]. CrossRef PubMed PubMedCentral
    8.  
  8. Hansen DV, Lui JH, Flandin P, Yoshikawa K, Rubenstein JL, Alvarez-Buylla A, Kriegstein AR.Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat Neurosci. 2013 Nov;16(11):1576-87. CrossRef PubMed PubMedCentral
    9.  
  9. 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. CrossRef PubMed PubMedCentral
    10.  
  10. 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):2681-2688. CrossRef PubMed
    11.  
  11. de Miranda AS, Zhang CJ, Katsumoto A, Teixeira AL. Hippocampal adult neurogenesis: Does the immune system matter? J Neurol Sci. 2017 Jan 15;372:482-495. CrossRef PubMed
    12.  
  12. 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) [serial on the Internet]. 2017 Jan 5 [cited 2017 Sep 15];4(1):e1256856 [4 p.].
    13.  
  13. Zhang J, Jiao J. Molecular Biomarkers for Embryonic and Adult Neural Stem Cell and Neurogenesis. Biomed Res Int [serial on the Internet]. 2015 [cited 2017 Sep 18];2015:727542 [14 p.].
    14.  
  14. Bonnamain V, Neveu I, Naveilhan P.Neural stem/progenitor cells as promising candidates for regenerative therapy of the central nervous system. Front Cell Neurosci [serial on the Internet]. 2012 Apr [cited 2017 Sep 4]; 6: 17 [8 pages.
    15.  
  15. Abbott A. Fetal-cell revival for Parkinson's. Nature. 2014 Jun 12;510(7504):195-6. CrossRef PubMed
    16.  
  16. Gao M, Yao H, Dong Q, Zhang H, Yang Z, Yang Y, Zhu J, Xu M, Xu R. Tumourigenicity and Immunogenicity of Induced Neural Stem Cell Grafts Versus Induced Pluripotent Stem Cell Grafts in Syngeneic Mouse Brain. Sci Rep [serial on the Internet]. 2016 Jul 15 [cited 2017 Sep 8];6:29955 [13 p.].
    17.  
  17. 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. CrossRef PubMed
    18.  
  18. 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 TGF-beta in modulating proliferation. Int Immunol. 2007 Sep;19(9):1063-74. CrossRef PubMed
    19.  
  19. Alegre ML, Lakkis FG, Morelli AE. Antigen Presentation in Transplantation. Trends Immunol. 2016 Dec;37(12):831-843. CrossRef PubMed PubMedCentral
    20.  
  20. Boardman DA, Jacob J, Smyth LA, Lombardi G, Lechler RI. What Is Direct Allorecognition? Curr Transplant Rep. 2016;3(4):275-283. CrossRef PubMed PubMedCentral
    21.  
  21. Marino J, Paster J, Benichou G. Allorecognition by T Lymphocytes and Allograft Rejection. Front Immunol [serial on the Internet]. 2016 Dec 14 [cited 2017 Sep 15];7:582 [9 p.].
    22.  
  22. Weissert R. Adaptive Immunity Is the Key to the Understanding of Autoimmune and Paraneoplastic Inflammatory Central Nervous System Disorders. Front Immunol [serial on the Internet]. 2017 Mar 23 [cited 2017 Sep 15];8:336 [10 p.].
    23.  
  23. Barker RA, Widner H. Immune problems in central nervous system cell therapy. NeuroRx. 2004 Oct;1(4):472-81. CrossRef PubMed PubMedCentral
    24.  
  24. Rogers NJ, Lechler RI. Allorecognition. Am J Transplant. 2001 Jul;1(2):97-102. CrossRef PubMed
    25.  
  25. Alekseev LP, Khaitov RM, Dolbin AG, Boldyreva MN, Trofimov DYu, Alekseeva PL, Minin MG. The main complex of human tissue compatibility (HLA) and clinical transplantology. Immunologiya. 2008; (4): 237-44.
    26.  
  26. Garrido F, Cabrera T, Concha A, Glew S, Ruiz-Cabello F, Stern PL. Natural history of HLA expression during tumor development. Immunol Today. 1993 Oct;14(10):491-9. CrossRef  
  27. Imboden M, Murphy KR, Rakhmilevich AL, Neal ZC, Xiang R, Reisfeld RA, Gillies SD, Sondel PM. The level of MHC class I expression on murine adenocarcinoma can change the antitumor effector mechanism of immunocytokine therapy. Cancer Res. 2001 Feb 15;61(4):1500-7. PubMed
    28.  
  28. Malmberg KJ, Sohlberg E, Goodridge JP, Ljunggren HG. Immune selection during tumor checkpoint inhibition therapy paves way for NK-cell "missing self" recognition. Immunogenetics. 2017 Aug;69(8-9):547-556. CrossRef PubMed PubMedCentral
    29.  
  29. Wieczorek M, Abualrous ET, Sticht J, Álvaro-Benito M, Stolzenberg S, Noé F, Freund C. Major Histocompatibility Complex (MHC) Class I and MHC Class II Proteins: Conformational Plasticity in Antigen Presentation. Front Immunol [serial on the Internet]. 2017 Mar 17 [cited 2017 Sep 7]; 8:292: [16 p.].
    30.  
  30. Holdsworth R, Hurley CK, Marsh SG, Lau M, Noreen HJ, Kempenich JH, Setterholm M, Maiers M. The HLA dictionary 2008: a summary of HLA-A, -B, -C, -DRB1/3/4/5, and DQB1 alleles and their assotiation with serologically defined HLA-A, -B, -C, -DR, and –DQ antigens. Tissue Antigens. 2009 Feb;73(2):95-170. CrossRef PubMed
    31.  
  31. Demina TN, Mailian EA, Gulmamedova ID, Gulmamedov VA. Modern views on the immunology of the gestational process. Reproductive health of a woman. 2003; (19130): 43-8.
    32.  
  32. Agrawal S, Pandey MK. The potential role of HLA-G polymorphism in maternal tolerance to the developing fetus. J Hematother Stem Cell Res. 2003 Dec;12(6):749-56. CrossRef PubMed
    33.  
  33. O'Callaghan CA. Natural killer cell surveillance of intracellular antigen processing pathways mediated by recognition of HLA-E and Qa-1b by CD94/NKG2 receptors. Microbes Infect. 2000 Apr;2(4):371-80. CrossRef  
  34. Lafon M, Prehaud C, Megret F, Lafage M, Mouillot G, Roa M, Moreau P, Rouas-Freiss N, Carosella ED. Modulation of HLA-G expression in human neural cells after neurotropic viral infections. J Virol. 2005 Dec;79(24):15226-37. CrossRef PubMed PubMedCentral
    35.  
  35. Chacon MA, Boulanger LM. MHC class I protein is expressed by neurons and neural progenitors in mid-gestation mouse brain. Mol Cell Neurosci. 2013 Jan;52:117-27. CrossRef PubMed
    36.  
  36. Draper JS, Pigott C, Thomson JA, Andrews PW. Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat. 2002 Mar;200(Pt 3):249-58. CrossRef PubMed PubMedCentral
    37.  
  37. Poltavtseva RA, Marey MV, Aleksandrova MA, Revishchin AV, Korochkin LI, Sukhikh GT. Evaluation of progenitor cell cultures from human embryos for neurotransplantation. Brain Res Dev Brain Res. 2002 Mar 31;134(1-2):149-54. CrossRef  
  38. 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. CrossRef PubMed
    39.  
  39. 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. CrossRef  
  40. Hassan-Zahraee M, Ladiwala U, Lavoie PM, McCrea E, Sekaly RP, Owens T, Antel JP. Superantigen presenting capacity of human astrocytes. J Neuroimmunol. 2000 Jan 24;102(2):131-6. PMID: 10636481. CrossRef  
  41. Al Nimer F, Wennersten A, Holmin S, Meijer X, Wahlberg L, Mathiesen T. MHC expression after human neural stem cell transplantation to brain contused rats. Neuroreport. 2004 Aug 26;15(12):1871-5. CrossRef PubMed
    42.  
  42. 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. CrossRef PubMed PubMedCentral
    43.  
  43. 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. CrossRef PubMed
    44.  
  44. 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. CrossRef PubMed
    45.  
  45. 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 IFN?-independent fashion and during development. Sci Rep [serial on the Internet]. 2016 Apr 15 [cited 2017 Sep 11]; 6:24251 [14 p.].
    46.  
  46. Johansson S, Price J, Modo M. Effect of inflammatory cytokines on major histocompatibility complex expression and differentiation of human neural stem/progenitor cells. Stem Cells. 2008 Sep;26(9):2444-54. CrossRef PubMed
    47.  
  47. Yin L, Fu SL, Shi GY, Li Y, Jin JQ, Ma ZW, Lu PH. Expression and regulation of major histocompatibility complex on neural stem cells and their lineages. Stem Cells Dev. 2008 Feb;17(1):53-65. CrossRef PubMed
    48.  
  48. 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. CrossRef  
  49. 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. CrossRef PubMed
    50.  
  50. 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. CrossRef PubMed PubMedCentral
    51.  
  51. 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
    52.  
  52. 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. CrossRef PubMed PubMedCentral
    53.  
  53. 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. CrossRef PubMed PubMedCentral
    54.  
  54. Zhang A, Yu H, He Y, Shen Y, Pan N, Liu J, Fu B, Miao F, Zhang J. The spatio-temporal expression of MHC class I molecules during human hippocampal formation development. Brain Res. 2013 Sep 5;1529:26-38. CrossRef PubMed
    55.  
  55. Zhang A, Yu H, He Y, Shen Y, Zhang Y, Liu J, Fu B, Lv D, Miao F, Zhang J. Developmental expression and localization of MHC class I molecules in the human central nervous system. Exp Brain Res. 2015 Sep;233(9):2733-43. CrossRef PubMed
    56.  
  56. Neumann H, Wekerle H. Neuronal control of the immune response in the central nervous system: linking brain immunity to neurodegeneration. J Neuropathol Exp Neurol. 1998 Jan;57(1):1-9. CrossRef PubMed
    57.  
  57. Medana I, Martinic MA, Wekerle H, Neumann H. Transection of major histocompatibility complex class Iinduced neurites by cytotoxic T-lymphocytes. Am J Pathol. 2001 Sep;159(3):809-15. CrossRef  
  58. Nagai A, Mishima S, Ishida Y, Ishikura H, Harada T, Kobayashi S, Kim SU. Immortalized human microglial cell line: phenotypic expression. J Neurosci Res. 2005 Aug 1;81(3):342-8. PMID:15957187. CrossRef PubMed
    59.  
  59. Schafer DP, Stevens B. Microglia Function in Central Nervous System Development and Plasticity. Cold Spring Harb Perspect Biol [serial on the Internet]. 2015 Jul 17 [cited 2017 Sep 11];7(10):a020545 [18 p.].
    60.  
  60. Gobin SJ, Montagne L, Van Zutphen M, Van Der Valk P, Van Den Elsen PJ, De Groot CJ. Upregulation of transcription factors controlling MHC expression in multiple sclerosis lesions. Glia. 2001 Oct;36(1):68-77. PMID: 11571785. CrossRef PubMed
    61.  
  61. Czlonkowska A, Kurkowska-Jastrzebska I, Czlonkowski A, Peter D, Stefano GB. Immune processes in the pathogenesis of Parkinson's disease – a potential role for microglia and nitric oxide. Med Sci Monit. 2002 Aug;8(8):RA165-77. PubMed
    62.  
  62. Van der Maesen K, Hinojoza JR, Sobel RA. Endothelial cell class II major histocompatibility complex molecule expression in stereotactic brain biopsies of patients with acute inflammatory/demyelinaying conditions. J Neuropathol Exp Neurol. 1999 Apr;58(4):346-58. CrossRef PubMed
    63.  
  63. Prat A, Biernacki K, Becher B, Antel JP. B7 expression and antigen presentation by human endothelial cells: requirement for proinflammatory cytokines. J Neuropathol Exp Neurol. 2000 Feb;59(2):129-36. CrossRef PubMed
    64.  
  64. Farmer JR, Altschaefl KM, O'Shea KS, Miller DJ. Activation of the type I interferon pathway is enhanced in response to human neuronal differentiation. PLoS One. [serial on the Internet]. 2013 Mar [cited 2017 Sep 11];8(3):e58813 [14 p.].
    65.  
  65. Lampson LA. Biological significance of HLA-A,B,C expression in neuroblastoma and related cell lines. Prog Clin Biol Res. 1988;271:409-20. PubMed
    66.  
  66. Lehky TJ, Jacobson S. Induction of HLA class II in HTLV-I infected neuronal cell lines. J Neurovirol. 1995 Jun;1(2):145-56. CrossRef PubMed
    67.  
  67. Hollister RD, Xia M, McNamara MJ, Hyman BT. Neuronal expression of class II major histocompatibility complex (HLA-DR) in 2 cases of Pick disease. Arch Neurol. 1997 Mar;54(3):243-8. CrossRef PubMed
    68.  
  68. Goddard CA, Butts DA, Shatz CJ. Regulation of CNS synapses by neuronal MHC class I. Proc Natl Acad Sci USA. 2007 Apr 17;104(16):6828-33. CrossRef PubMed PubMedCentral
    69.  
  69. Tetruashvily MM, Melson JW, Park JJ, Peng X, Boulanger LM. Expression and alternative splicing of classical and nonclassical MHCI genes in the hippocampus and neuromuscular junction. Mol Cell Neurosci. 2016 Apr;72:34-45. CrossRef PubMed PubMedCentral
    70.  
  70. Lee H, Brott BK, Kirkby LA, Adelson JD, Cheng S, Feller MB, Datwani A, Shatz CJ. Synapse elimination and learning rules co-regulated by MHC class I H2-Db. Nature. 2014 May 8;509(7499):195-200. CrossRef PubMed PubMedCentral
    71.  
  71. Cebrián C, Zucca FA, Mauri P, Steinbeck JA, Studer L, Scherzer CR, Kanter E, Budhu S, Mandelbaum J, Vonsattel JP, Zecca L, Loike JD, Sulzer D. MHC-I expression renders catecholaminergic neurons susceptible to T-cell-mediated degeneration. Nat Commun [serial on the Internet]. 2014 Apr 16 [cited 2017 Sep 11];5:3633 [33 p.].
    72.  
  72. Sun C, Zhang H, Li J, Huang H, Cheng H, Wang Y, Li P, An Y. Modulation of the major histocompatibility complex by neural stem cell-derived neurotrophic factors used for regenerative therapy in a rat model of stroke. J Transl Med [serial on the Internet]. 2010 Aug 20 [cited 2017 Sep 11];8:77 [10 p.].
    73.  
  73. Le Blanc K. Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy. 2003;5(6):485-9. CrossRef PubMed
    74.  
  74. Klassen H, Schwartz MR, Bailey AH, Young MJ. Surface markers expressed by multipotent human and mouse neural progenitor cells include tetraspanins and non-protein epitopes. Neurosci Lett. 2001 Oct 26;312(3):180-2. CrossRef  
  75. 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-FasL-mediated T-cell death. Stem Cell Res Ther [serial on the Internet]. 2013 May 21 [cited 2017 Sep 11];4(3):56 [10 p.].
    76.  
  76. Ennas MG, Cocchia D, Silvetti E, Sogos V, Riva A, Torelli S, Gremo F. Immunocompetent cell markers in human fetal astrocytes and neurons in culture. J Neurosci Res. 1992 Jul;32(3):424-36. CrossRef PubMed
    77.  
  77. Sergent-Tanguy S, Véziers J, Bonnamain V, Boudin H, Neveu I, Naveilhan P. Cell surface antigens on rat neural progenitors and characterization of the CD3 (+)/CD3 (-) cell populations. Differentiation. 2006 Dec;74(9-10):530-41. CrossRef PubMed
    78.  
  78. 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 U S A. 2004 Dec 28;101(52):18117-22. CrossRef PubMed PubMedCentral
    79.  
  79. Panchision DM, Chen HL, Pistollato F, Papini D, Ni HT, Hawley TS. Optimized flow cytometric analysis of central nervous system tissue reveals novel functional relationships among cells expressing CD133, CD15, and CD24. Stem Cells. 2007 Jun;25(6):1560-70. CrossRef PubMed
    80.  
  80. Allport JR, Shinde Patil VR, Weissleder R. Murine neuronal progenitor cells are preferentially recruited to tumor vasculature via alpha4-integrin and SDF- 1alpha-dependent mechanisms. Cancer Biol Ther. 2004 Sep;3(9):838-44. CrossRef PubMed
    81.  
  81. Gonzalez R, Hamblin MH, Lee JP. Neural Stem Cell Transplantation and CNS Diseases. CNS Neurol Disord Drug Targets. 2016;15(8):881-6. CrossRef PubMed
    82.  
  82. 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 [serial on the Internet]. 2015 Feb 6 [cited 2017 Sep 8];10(2):e0117432 [15 p.].
    83.  
  83. 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. CrossRef  
  84. Hu S, Rotschafer JH, Lokensgard JR, Cheeran MC. Activated CD8+ T lymphocytes inhibit neural stem/progenitor cell proliferation: role of interferon-gamma.PLoS One [serial on the Internet]. 2014 Aug 18 [cited 2017 Sep 11];9(8):e105219 [11 p.].
    85.  
  85. Choe Y, Huynh T, Pleasure SJ. Migration of oligodendrocyte progenitor cells is controlled by transforming growth factor ß family proteins during corticogenesis. J Neurosci. 2014 Nov 5;34(45):14973-83. CrossRef PubMed PubMedCentral
    86.  
  86. Kandasamy M, Lehner B, Kraus S, Sander PR, Marschallinger J, Rivera FJ, Trümbach D, Ueberham U, Reitsamer HA, Strauss O, Bogdahn U, Couillard-Despres S, Aigner L. TGF-beta signalling in the adult neurogenic niche promotes stem cell quiescence as well as generation of new neurons. J Cell Mol Med. 2014 Jul;18(7):1444-59. CrossRef PubMed PubMedCentral
    87.  
  87. Khanghahi AM, Zeynali B, Akhlaghpoor A, Tafreshi AP, Krieglstein K. Activation of TGFß1 signaling enhances early dopaminergic differentiation in unrestricted somatic stem cells. Neurosci Lett. 2014 Nov 7;583:60-4. CrossRef PubMed
    88.  
  88. Li W, Wei W, Ding S. TGF-ß Signalling in Stem Cell Regulation. Methods Mol Biol. 2016;1344:137-45. CrossRef PubMed
    89.  
  89. Wang T, Yuan W, Liu Y, Zhang Y, Wang Z, Zhou X, Ning G, Zhang L, Yao L, Feng S, Kong X. The role of the JAKSTAT pathway in neural stem cells, neural progenitor cells and reactive astrocytes after spinal cord injury. Biomed Rep. 2015 Mar;3(2):141-6. CrossRef PubMed PubMedCentral
    90.  
  90. Seo JH, Maki T, Maeda M, Miyamoto N, Liang AC, Hayakawa K, Pham LD, Suwa F, Taguchi A, Matsuyama T, Ihara M, Kim KW, Lo EH, Arai K. Oligodendrocyte precursor cells support blood-brain barrier integrity via TGF-ß signaling. PLoS One [serial on the Internet]. 2014 Jul 31 [cited 2017 Sep 12];9(7):e103174 [11 p.].
    91.  
  91. Pringproa K, Rungsiwiwut R, Tantilertcharoen R, Praphet R, Pruksananonda K, Baumgärtner W, Thanawongnuwech R. Tropism and Induction of Cytokines in Human Embryonic-Stem Cells-Derived Neural Progenitors upon Inoculation with Highly-Pathogenic Avian H5N1 Influenza Virus. PLoS One [serial on the Internet]. 2015 Aug 14 [cited 2017 Sep 12];10(8):e0135850 [14 p.]..
    92.  
  92. 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. CrossRef PubMed PubMedCentral
© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2025.